Biodiversity, Ecosystem Functioning, and Human Wellbeing

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Biodiversity,
Ecosystem
Functioning, and
Human Wellbeing
An Ecological and Economic
Perspective
EDITED BY

Shahid Naeem,
Daniel E. Bunker,
Andy Hector,
Michel Loreau,
and
Charles Perrings

1
3
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Contents

List of contributors viii

Preface xi
Shahid Naeem, Daniel E. Bunker, Andy Hector, Michel Loreau,
and Charles Perrings

Acknowledgments xiv

Part 1: Introduction, background, and meta-analyses 1

1 Introduction: the ecological and social implications of changing

biodiversity. An overview of a decade of biodiversity and
ecosystem functioning research 3
Shahid Naeem, Daniel E. Bunker, Andy Hector, Michel Loreau,
and Charles Perrings

2 Consequences of species loss for ecosystem functioning:

meta-analyses of data from biodiversity experiments 14
Bernhard Schmid, Patricia Balvanera, Bradley J. Cardinale, Jasmin Godbold,
Andrea B. Pfisterer, David Raffaelli, Martin Solan, and Diane S. Srivastava

3 Biodiversity-ecosystem function research and biodiversity futures:

early bird catches the worm or a day late and a dollar short? 30
Martin Solan, Jasmin A. Godbold, Amy Symstad, Dan F. B. Flynn,
and Daniel E. Bunker

Part 2: Natural science foundations 47

4 A functional guide to functional diversity measures 49

Owen L. Petchey, Eoin J. O’Gorman, and Dan F. B. Flynn

5 Forecasting decline in ecosystem services under realistic

scenarios of extinction 60
J. Emmett Duffy, Diane S. Srivastava, Jennie McLaren, Mahesh Sankaran,
Martin Solan, John Griffin, Mark Emmerson, and Kate E. Jones

6 Biodiversity and the stability of ecosystem functioning 78

John N. Griffin, Eoin J. O’Gorman, Mark C. Emmerson, Stuart R. Jenkins,
Alexandra-Maria Klein, Michel Loreau, and Amy Symstad

v
vi CONTENTS

7 The analysis of biodiversity experiments: from pattern

toward mechanism 94
Andy Hector, Thomas Bell, John Connolly, John Finn, Jeremy Fox,
Laura Kirwan, Michel Loreau, Jennie McLaren, Bernhard Schmid,
and Alexandra Weigelt

8 Towards a food web perspective on biodiversity and

ecosystem functioning 105
Bradley Cardinale, Emmett Duffy, Diane Srivastava, Michel Loreau,
Matt Thomas, and Mark Emmerson

9 Microbial biodiversity and ecosystem functioning under

controlled conditions and in the wild 121
Thomas Bell, Mark O. Gessner, Robert I. Griffiths, Jennie McLaren,
Peter J. Morin, Marcel van der Heijden, and Wim van der Putten

10 Biodiversity as spatial insurance: the effects of habitat

fragmentation and dispersal on ecosystem functioning 134
Andrew Gonzalez, Nicolas Mouquet, and Michel Loreau

Part 3: Ecosystem services and human wellbeing 147

11 Incorporating biodiversity in climate change mitigation initiatives 149

Sandra Dı́az, David A. Wardle, and Andy Hector

12 Restoring biodiversity and ecosystem function: will an integrated

approach improve results? 167
Justin Wright, Amy Symstad, James M. Bullock, Katharina Engelhardt,
Louise Jackson, and Emily Bernhardt

13 Managed ecosystems: biodiversity and ecosystem functions in

landscapes modified by human use 178
Louise Jackson, Todd Rosenstock, Matthew Thomas, Justin Wright,
and Amy Symstad

14 Understanding the role of species richness for crop pollination services 195
Alexandra-Maria Klein, Christine Müller, Patrick Hoehn, and Claire Kremen

15 Biodiversity and ecosystem function: perspectives on disease 209

Richard S. Ostfeld, Matthew Thomas, and Felicia Keesing

16 Opening communities to colonization – the impacts of invaders on

biodiversity and ecosystem functioning 217
Katharina Engelhardt, Amy Symstad, Anne-Helene Prieur-Richard,
Matthew Thomas, and Daniel E. Bunker
 CONTENTS vii

17 The economics of biodiversity and ecosystem services 230

Charles Perrings, Stefan Baumgärtner, William A. Brock, Kanchan Chopra, Marc Conte,
Christopher Costello, Anantha Duraiappah, Ann P. Kinzig, Unai Pascual, Stephen Polasky,
John Tschirhart, and Anastasios Xepapadeas

18 The valuation of ecosystem services 248

Edward B. Barbier, Stefan Baumgärtner, Kanchan Chopra, Christopher Costello, Anantha
Duraiappah, Rashid Hassan, Ann P. Kinzig, Markus Lehman, Unai Pascual, Stephen Polasky,
and Charles Perrings

19 Modelling biodiversity and ecosystem services in coupled

ecological–economic systems 263
William A. Brock, David Finnoff, Ann P. Kinzig, Unai Pascual, Charles Perrings,
John Tschirhart, and Anastasios Xepapadeas

Part 4: Summary and synthesis 279

20 TraitNet: furthering biodiversity research through the curation,

discovery, and sharing of species trait data 281
Shahid Naeem and Daniel E. Bunker

21 Can we predict the effects of global change on biodiversity loss

and ecosystem functioning? 290
Shahid Naeem, Daniel E. Bunker, Andy Hector, Michel Loreau,
and Charles Perrings

References 299
Index 357
 Contributors

Patricia Balvanera, Centro de Investigaciones en Ecosis- Sandra Dı́az, Instituto Multidisciplinario de Biologı́a
temas, Universidad Nacional Autónoma de México, Vegetal (CONICET-UNC) and FCEFyN, Universidad
Apdo. Postal 27-3, Sta. Ma. de Guido, Morelia, Nacional de Córdoba, Casilla de Correo 495, 5000
Michoacán, México 58090; [email protected] Córdoba, Argentina; [email protected]
Edward B. Barbier, University of Wyoming, Department J. Emmett Duffy, Virginia Institute of Marine Science,
of Economics and Finance, Department 3985, Ross Hall The College of William and Mary, Gloucester Point, VA
123, Laramie, WY 82071, USA; [email protected] 23062-1346, USA; [email protected]
Stefan Baumgärtner, Leuphana Universität Lüneburg Anantha Duraiappah, Ecosystem Services Economics
Centre for Sustainability ManagementPostfach 2440 D- Unit, Division of Environmental Policy Implementa-
21314 Lüneburg, Germany; [email protected] tion, United Nations Environment Programme
Thomas Bell, Department of Zoology, University of (UNEP),United Nations Avenue, Gigiri, PO Box 30552,
Oxford, South Parks Road, Oxford OX1 3PS, UK; 00100Nairobi, Kenya;[email protected]
[email protected] Mark C. Emmerson, Environmental Research Institute,
Emily Bernhardt, Department of Biology, Box 90388, University College Cork, Lee Road, Cork, Ireland, and
Duke University, Durham, NC 27708, USA; ebern- Department of Zoology, Ecology and Plant Science
[email protected] Distillery Fields, North Mall, University College Cork,
William A. Brock, University of Wisconsin, Madison – Ireland; [email protected]
Department of Economics, 1180 Observatory Drive, Katharina Engelhardt, University of Maryland Center for
Madison, WI 53706, USA; [email protected] Environmental Science, Appalachian Laboratory, 301
Daniel E. Bunker, Department of Biological Sciences, Braddock Road, Frostburg, MD 21532, USA; engel-
New Jersey Institute of Technology, 433 Colton Hall, [email protected]
University Heights, Newark, NJ 07102-1982, USA; John Finn, Teagasc, Environment Research Centre, Johns-
[email protected] town Castle, Wexford Ireland; john.fi[email protected]
Bradley J. Cardinale, Department of Ecology, Evolution David Finnoff, University of Wyoming, Department of
and Marine Biology, University of California at Santa Economics and Finance, Department 3985, Ross Hall
Barbara, Santa Barbara, California 93106, USA; cardi- 123, Laramie, WY 82071, USA; [email protected]
[email protected] Dan F. B. Flynn, Department of Ecology, Evolution and
Kanchan Chopra, Institute of Economic Growth, Delhi Environmental Biology (E3B), Columbia University,
University Enclave, Delhi – 110 007, India; kan- Schermerhorn Extension, 10th Floor, Mail Code 5557,
[email protected] 1200 Amsterdam Avenue, New York, NY 10027, USA;
John Connolly, Environmental and Ecological Modelling [email protected]
Group, UCD School of Mathematical Sciences, Dublin, Jeremy Fox, Department of Biological Sciences, University
Ireland; [email protected] of Calgary, 2500 University Drive NW, Calgary, Alberta
Marc Conte, Environmental Science & Management, Uni- T2N 1N4 Canada; [email protected]
versity of California Santa Barbara, 4410 Bren Hall,Santa Mark O. Gessner, Department of Aquatic Ecology, Eawag:
Barbara, CA 93106-5131, USA; [email protected] Swiss Federal Institute of Aquatic Science & Technology,
Christopher Costello, Donald Bren School of Environ- 8600 Dübendorf, Switzerland and Institute of Integrative
mental Science & Management, University of California Biology (IBZ), ETH Zurich, 8600 Dübendorf, Switzerland
Santa Barbara, 4410 Bren Hall,Santa Barbara, CA 93106- Jasmin A. Godbold, Oceanlab, University of Aberdeen,
5131, USA; [email protected] Main Street, Newburgh, Aberdeenshire, AB41 6AA,
UK; [email protected]

viii
 CONTRIBUTORS ix

Andrew Gonzalez, Department of Biology, McGill Jennie R. McLaren, Department of Botany, University of
University, 1205 Dr., Penfield Avenue, Montreal, H3A British Columbia, #3529-6270 University Boulevard,
1B1, Canada; [email protected] Vancouver, BC, V6T 1Z4, Canada; jmclaren@
John N. Griffin, Marine Biological Association of the interchange.ubc.ca.
United Kingdom, The Laboratory, Citadel Hill, Ply- Peter J. Morin, Department of Ecology, Evolution, and
mouth PL1 2PB, UK and Marine Biology and Ecology Natural Resources, Rutgers Cook College, 148 ENRS
Research Centre, School of Biological Sciences, Uni- Building, Cook Campus, 14 College Farm Road, New
versity of Plymouth, Plymouth PL4 8AA, UK Brunswick, New Jersey, USA
Robert I. Griffiths, Molecular Microbial Ecology Section, Nicolas Mouquet, ISEM-UMR 5554, University of
Centre for Ecology and Hydrology (Oxford), Mansfield Montpellier II, Place Eugene Bataillon, CC065, 34095
Road, Oxford OX1 3SR, UK Montpellier Cedex 05, France
Rashid Hassan, Dept of Agricultural Economics Exten- Christine Müller, Institute of Environmental Sciences,
sion and Rural Development, University of Pretoria, University of Zürich, Winterthurerstrasse 190, CH-8057
PRETORIA 0002, South Africa;[email protected] Zürich, Switzerland
Andy Hector, Institute of Environmental Sciences, Shahid Naeem, Department of Ecology, Evolution, and
University of Zurich, CH-8057, Zurich, Switzerland; Environmental Biology, Columbia University, 1200
[email protected] Amsterdam Ave, MC 5557, New York, NY 10025, USA;
Patrick Hoehn, Department of Crop Science, Agroecology, [email protected]
University of Göttingen, Waldweg 26, 37073 Göttingen, Eoin J. O’Gorman, Environmental Research Institute, Lee
Germany Road Cork, Ireland, and Department of Zoology, Ecology
Louise Jackson, Department of Land, Air and Water and Plant Science, Distillery Fields, North Mall,
Resources, University of California, Davis, CA 95616, University College Cork, Ireland; [email protected]
USA; [email protected] Richard S. Ostfeld, Cary Institute of Ecosystem Studies,
Stuart R. Jenkins, School of Ocean Sciences, University PO Box AB, Millbrook, NY 12545, USA
Bangor Menai Bridge, Anglesey LL59 5AB, UK Unai Pascual, Department of Land Economy, University
Kate E. Jones, Institute of Zoology, Zoological Society of of Cambridge, 19 Silver Street, Cambridge, CB3 9EP,
London and Cambridge University, Regent’s Park, UK; [email protected]
London NW1 4RY, UK Charles Perrings, ecoSERVICES Group, School of Life
Felicia Keesing, Biology Program, Bard College, Annan- Sciences, Arizona State University, Box 874501, Tempe,
dale-on-Hudson, NY 12504, USA AZ 85287-4501, USA; [email protected]
Ann P. Kinzig, ecoSERVICES Group, School of Life Sci- Owen L. Petchey, Department of Animal and Plant
ences, Arizona State University, Box 874501, Tempe, AZ Sciences, Alfred Denny Building, University of Shef-
85287-4501, USA; [email protected] field, Western Bank, Sheffield S10 2TN, UK; o.petchey@
Laura Kirwan, Teagasc, Environment Research Centre, sheffield.ac.uk
Johnstown Castle, Wexford Ireland; Laura.Kirwan@ Andrea B. Pfisterer, Institute of Environmental Sciences,
teagasc.ie Universität Zürich, Winterthurerstrasse 190, CH-8057
Alexandra-Maria Klein, Department of Environmental Zürich, Switzerland; pfi[email protected]
Science, Policy and Management, 137 Mulford Hall, Stephen Polasky, Department of Applied Economics,
University of California at Berkeley, California 94720- University of Minnesota, 1994 Buford Avenue, St Paul,
3114, USA and Department of Crop Science, Agro- MN 55108, USA; [email protected]
ecology, University of Göttingen, Waldweg 26, 37073 Anne-Helene Prieur-Richard, DIVERSITAS, Muséum
Göttingen, Germany National d’Histoire Naturelle (MNHN), 57 Rue Cuvier –
Claire Kremen, Department of Environmental Science, CP 41, 75231 Paris Cedex 05, France; anne-helene@
Policy and Management, 137 Mulford Hall, University diversitas-international.org
of California at Berkeley, California 94720-3114, USA David Raffaelli, Environment Department, University of
Markus Lehmann, Secretariat of the Convention on Bio- York, York, UK; [email protected]
logical Diversity, 413, Saint Jacques Street, suite 800 Todd Rosenstock, Department of Plant Sciences,
Montreal QC, H2Y 1N9, Canada; markus.leh- University of California, Davis, CA 95616, USA;
[email protected] [email protected]
Michel Loreau, Department of Biology, McGill University, Mahesh Sankaran, Institute of Integrative and Compar-
1205 ave Docteur Penfield, Montreal, Québec H3A 1B1, ative Biology, Faculty of Biological Sciences, University
Canada; [email protected] of Leeds, Leeds LS2 9JT, UK
x CONTRIBUTORS

Bernhard Schmid, Institute of Environmental Sciences, Marcel van der Heijden, Ecological Farming systems
Universität Zürich, Winterthurerstrasse 190, CH-8057 Research Station ART, Agroscope Reckenholz Tanikon,
Zürich, Switzerland; bernhard.schmid@ uwinst.uzh.ch Reckenholzstrasse 191, 8046 Zurich, Switzerland and Vrije
Martin Solan, Oceanlab, University of Aberdeen, Main Universiteit Amsterdam, Faculty of Earth and Life Sci-
Street, Newburgh, Aberdeenshire, Scotland AB41 6AA, ences, Institute of Ecological Science, Department of
UK; [email protected] Animal Ecology, De Boelelaan 1085, 1081 HVAmsterdam,
Diane S. Srivastava, Department of Zoology, University The Netherlands
of British Columbia, Vancouver, British Columbia V6T Wim H. van der Putten, Netherlands Institute for Ecology
1Z4, Canada; [email protected] (NIOO-KNAW), Centre for Terrestrial Ecology, P.O. Box 40,
Amy Symstad, U.S. Geological Survey, Northern Prairie 6666 ZG Heteren, The Netherlands and Laboratory of
Wildlife Research Center, 306 East Saint Joseph Street, Nematology, Wageningen University and Research Centre,
Suite 210, Rapid City, SD 57701, USA and U.S. PO Box 8123, 6700 ES Wageningen, The Netherlands
Geological Survey, Northern Prairie Wildlife Research David A. Wardle, Department of Forest Ecology
Center, 26611 U.S. Highway 385, Hot Springs, SD 57747, and Management, Swedish University of Agricultural
USA; [email protected] Sciences, SE901-83 Umeå, Sweden
Matthew Thomas, Center for Infectious Disease Dynamics Alexandra Weigelt, Institute of Ecology, University
and Department of Entomology, 1 Chemical Ecology Lab, of Jena, Dornburgerstr. 159, 07743 Jena, Germany;
Penn State, University Park 16802, PA, USA; mbt13@psu. alexandra. [email protected].
edu and Matthew Thomas, CSIRO Entomology, GPO Box Justin Wright, Department of Biology, Box 90338, Duke
1700, Canberra, ACT 2601, Australia; matthew.tho- University, Durham, NC 27708, USA; [email protected]
[email protected] Anastasios Xepapadeas, University of Economics and
John Tschirhart, University of Wyoming, Department of Business Department of International and European
Economics and Finance, Department 3985, Ross Hall Economic Studies 76 Patission Street, 104 34 Athens,
123, Laramie, WY 82071, USA; [email protected] Greece; [email protected]
 Preface

This volume serves as an introduction, reference, and functioning. Sixth, the research was largely experi-
survey both of the profound transformation experi- mental, complex, abstract, and confirmatory in
enced in the last decade by ecology’s fast-growing nature (i.e. simply confirming that changes in biodi-
field of biodiversity and ecosystem functioning and versity did indeed change ecosystem functioning).
of the economics of ecosystem services. Motivated in Finally, work on biodiversity and ecosystem func-
the early 1990s by environmental concerns over tioning was colored by a tremendous debate over
worldwide declines in biodiversity, the biodiversity interpretation of its findings.
and ecosystem functioning research area originated Over the last few years, however, biodiversity
as a synthesis of the relatively disparate fields of and ecosystem functioning research has evolved
community and ecosystem ecology. Neither disci- dramatically. This volume provides a thorough
pline by itself could adequately describe the wide review of the new face presented by the second
array of possible ecological consequences of biodi- generation of biodiversity and ecosystem function-
versity loss (Loreau et al. 2001, Naeem et al. 2002, ing research. Its 21 chapters are written by more than
Hooper et al. 2005). The first generation of research on 60 authors who have been at the forefront of this
biodiversity and ecosystem functioning rapidly grew transition. Virtually everything that characterized
into a discipline that can be characterized by several the first generation of biodiversity and ecosystem
features (Loreau et al. 2002). First, species or func- functioning research has changed. First, rather than
tional group richness was the primary way of oper- species or functional group richness, the new focus is
ationally defining and manipulating biodiversity. on trait-based, functional biodiversity, as well as on
Second, many studies often worked within a single community composition. Second, biodiversity and
trophic level (usually plants), though microcosm and ecosystem functioning studies are increasingly
mesocosm studies using microbes and invertebrates multi-trophic and span both terrestrial and marine
proved exceptions. Third, research efforts considered ecosystems in comparison to the dominance of ter-
only biogeochemical processes, especially primary restrial plant studies that typified earlier biodiversity
productivity, as ecosystem functions. Fourth, the and ecosystem functioning work. Third, trait-based
prevailing mechanisms were limited to niche com- mechanisms of ecosystem functioning have become a
plementarity (i.e. niche differences lead to greater major thrust for contemporary biodiversity and
exploitation of available resources that lead to greater ecosystem functioning research, while niche com-
levels of ecosystem functioning) and selection effects plementarity and selection effects are considered to
(i.e. higher diversity communities invariably contain be co-occurring (not conflicting) mechanisms.
one or a few dominant species with disproportionate Fourth, rather than assuming random local extinc-
influences over ecosystem function) that were often tions, much new work on biodiversity and ecosystem
viewed as opposing hypotheses vying for suprem- functioning employs trait-based extinction probabil-
acy. Fifth, local extinction or biodiversity loss was ities or increasingly uses empirical extinction sce-
largely considered a random process and experi- narios to establish its biodiversity gradients. Fifth,
ments focused on producing as many randomly compared to the more abstract deliberations of the
constructed species combinations as possible to first generation of biodiversity and ecosystem func-
explore how biodiversity loss influenced ecosystem tioning research, there is now much more attention to

xi
xii PREFACE

the role of biodiversity and ecosystem functioning in ecological stocks and flows that underpin the
restoration ecology, agriculture, invasions, disease, production of many ecosystem services. This
pollination, climate change, and other ecosystem- volume explains and expands upon the ways in
service-related environmental issues. Finally, con- which the new face of biodiversity and ecosystem
sensus has been achieved (Loreau et al. 2001, Hooper functioning research is interfacing with research
et al. 2005) and the debate that once clouded the into the decisions that people make about how to
interpretation of biodiversity and ecosystem func- use the resources of the environment.
tioning findings has largely abated.
There are also entirely new features of the
The contents of this volume
second generation of biodiversity and ecosystem
functioning research as well. Enough studies have In 2000, the National Science Foundation (NSF) fun-
now accumulated to allow meta-analyses, which ded a Research Coordinating Network (RCN) enti-
obviate the sometimes subjective interpretation of tled ‘Biotic Mechanisms of Ecosystem Regulation in
trends in biodiversity and ecosystem functioning the Global Environment’ (BioMERGE) to foster col-
experiments expressed during the earlier conten- laboration and usher biodiversity and ecosystem
tious period. Second, in silico, trait-based simula- functioning research through its maturation phase
tion modeling of biodiversity and ecosystem (Naeem et al. 2007). The relationship between biodi-
functioning relationships at larger scales has aug- versity and ecosystem functioning is also the central
mented the complex and costly combinatorial theme of the ecoSERVICES core project of DIVER-
experimental approach and represents an entirely SITAS (http://www.diversitas-international.org/),
new and promising method for large-scale biodi- an international programme that promotes biodi-
versity and ecosystem functioning research. Third, versity science and aims to bridge the science and
metacommunity theory applied to biodiversity and policy interface. This volume is the final product of a
ecosystem functioning provides additional under- five-year collaboration between BioMERGE and
standing of ecosystem complexity and stability. DIVERSITAS.
Beyond the basic science of biodiversity and The volume is divided into four sections. The
ecosystem functioning, this volume also explores first section, Introduction, Background, and Meta-
the current state of the economics of biodiversity Analyses, provides the background for the volume.
and ecosystem services. With antecedents in both The editors provide the background, historical
natural resource and ecological economics, this context, and an overview of the volume’s content
field of economics incorporates insights from in Chapter 1, followed by a meta-analysis by
ecology to build an understanding of the ways in Schmid et al. (Chapter 2) that quantitatively tests
which biodiversity and ecosystem functioning several biodiversity and ecosystem functioning
contribute to human wellbeing. The field received hypotheses using the enormous body of published
a major stimulus from the Millennium Ecosystem experimental studies. The last chapter in this sec-
Assessment’s (2005b) focus on ecosystem services – tion is an historical and quantitative analysis of the
the benefits that people derive from the processes impact of biodiversity and ecosystem functioning
and functioning of both ‘natural’ and ‘managed’ research by Solan et al. (Chapter 3) that quantita-
ecosystems. By conceptualizing ecosystem pro- tively tests several biodiversity and ecosystem
cesses and functioning as factors in the production functioning hypotheses using the enormous body
of ecosystem services that directly or indirectly of published experimental studies.
benefit people, the Millennium Ecosystem Assess- The second section, Natural Science Foundations,
ment has brought many ecological questions consists of seven chapters. In Chapter 4, Petchey et al.
within the realm of economics. For example, it has describe one of the major contributions of biodiver-
made it natural to analyze the trade-offs (in terms sity and ecosystem functioning research to ecology:
of ecosystem services) of alternative ecological an increasing emphasis on functional diversity.
configurations. At the same time it has com- Petchey et al. illustrate both the advantages and
pelled economists to pay serious attention to the challenges of focusing on functional diversity by
 PREFACE xiii

reviewing how authors have attempted to quantify third of Earth’s terrestrial surfaces, and focus on
functional diversity. Duffy et al. (Chapter 5), biological control as a case study. Klein et al.
consider how functional diversity has transformed (Chapter 14) discuss the critical ecosystem service of
biodiversity and ecosystem functioning research pollination, which is equally important for many
from a largely confirmatory science to one that is crops as well as unmanaged or restored systems.
increasingly predictive. The mitigation of disease (Chapter 15 by Ostfeld et
The remaining chapters of the second section al.) and biological invasions (Chapter 16 by Engel-
address universal challenges for all of ecology, in hardt et al.) are two other biotic ecosystem services
the context of biodiversity and ecosystem func- that are strongly influenced by biodiversity.
tioning. These are stability and complexity (Chap- What truly makes this volume unique are the
ter 6 by Griffin et al.), identifying the mechanisms chapters of Section 3, which consider the eco-
generating ecological relationships (Chapter 7 by nomic perspective. Perrings et al. (Chapter 17)
Hector et al.), the importance of trophic structure provide a synthesis of the economics of ecosystem
(Chapter 8 by Cardinale et al.), microbial ecology services and biodiversity, and the options open to
(Chapter 9 by Bell et al.), and the importance of the policy-makers to address the failure of markets
spatial dimension and metacommunities in deter- to account for the loss of ecosystem services.
mining the effects of diversity on ecosystem func- Barbier et al. (Chapter 18) examine the challenges
tioning (Chapter 10 by Gonzalez et al.). of valuing ecosystem services and, hence, to
The third section takes research on biodiversity understanding the human consequences of deci-
and ecosystem functioning further than it has ever sions that neglect these services. Brock et al.
gone into the human dimension. The first six (Chapter 19) examine the ways in which econo-
chapters cover the most pressing environmental mists are currently incorporating biodiversity and
challenges humanity faces. Notably, these chapters ecosystem functioning research into decision
also highlight a new emphasis on ecosystem ser- models for the conservation and management of
vices that go beyond the historic focus on primary biodiversity.
productivity. Dı́az et al. consider the effects of bio- The fourth and final section consists of two
diversity on the carbon cycle (Chapter 11) as a way chapters, one describing the new, ambitious
to shed light on anthropogenic climate change that direction of biodiversity and ecosystem function-
has been largely devoid of considerations of biodi- ing research to become a global science (Chapter
versity. Wright et al. consider the role that diversity 20) and a synthesis of this volume (Chapter 21) by
may play in fostering the restoration of degraded or the editors that describes the nature of the progress
abandoned habitats (Chapter 12). Jackson et al. made thus far and the future directions and chal-
(Chapter 13) consider the importance of biodiversity lenges that have been covered by the many authors
in the agricultural ecosystems that now cover one of this volume.
 Acknowledgments

This volume is the summation of five years of coop- Borneo (2005) and Switzerland (2006) with the help
eration among biodiversity and ecosystem function- of Chris Philipson, Glen Reynolds, Philipppe Saner,
ing researchers and environmental economists and Maja Weilenmann. Two ecoSERVICES work-
fostered through joint meetings between BioMERGE shops in Paris, coordinated by John Tschirhardt
and BESTNet (NSF-funded Research Coordination (2005) and Charles Perrings (2007), laid the
Networks) and the ecoSERVICES project of DIVER- groundwork for the economic chapters included in
SITAS. This collaboration was founded on the prin- the volume.
ciples of inclusiveness (i.e. including participants The bulk of the funding for BioMERGE came
irrespective of their position on the issues), attention from NSF grants # 0130289 and 0435178 with addi-
to balance across the various stages in scientific tional support from the University of Washington,
careers (i.e. include graduate students, postdoctoral Seattle, and Columbia University. Funding for
researchers, junior and senior faculty), and gender BESTNet came from NSF grant # 0639252. DIVER-
balance. SITAS contributed both financial and logistical sup-
Justin Wright, the first associate director of port to a number of the preparatory workshops, and
BioMERGE, coordinated meetings in Seattle (2002) in particular supported the participation of non-US
and the Missouri Botanical Garden (2003). Daniel participants. This volume and its contents serves as a
Bunker, the second associate director of BioMERGE, testament to the value of supporting international
and Andy Hector, the then co-chair of DIVERSITAS’ cooperation, integration, and synthesis among social
ecoSERVICES core project, coordinated meetings in and natural scientists in basic and applied research.

xiv
PART 1
Introduction, background,
and meta-analyses
This page intentionally left blank
 CHAPTER 1

Introduction: the ecological and social

implications of changing biodiversity.
An overview of a decade of
biodiversity and ecosystem
functioning research
Shahid Naeem, Daniel E. Bunker, Andy Hector, Michel Loreau,
and Charles Perrings

1.1 Biodiversity, ecosystem functioning,

value of biodiversity dominates. These topics,
and human wellbeing: An unconventional
however, are often tacked on as final chapters that
perspective
are poorly integrated with the earlier ‘pure’ ecol-
Conventional approaches to ecology often lack the ogy. This approach obscures the inextricable links
necessary integration to make a compelling case for between biodiversity, ecosystems, and human
the critical importance of biodiversity to ecosystem wellbeing.
functioning and human wellbeing. Traditional ecol- This linear march through the biological hierarchy,
ogy textbooks (e.g. Ricklefs and Miller 1999, Krebs loosely coupled with its significance to human well-
2001, Smith and Smith 2005, Begon et al. 2006), for being, while of some pedagogical merit, does not
example, often begin with species adaptations to prepare one for understanding and applying ecology
local environmental conditions and then proceed in the context of the modern world. In today’s world,
through topics such as the population biology of almost everything, especially biodiversity, has been
single species, the dynamics of interacting popula- impacted by human activities (Millennium Ecosystem
tions (e.g. competitors, predator–prey, host–parasite, Assessment 2005c, Kareiva et al. 2007). A different,
mutualisms, food webs), the relationship between rather unconventional approach is needed for
stability and complexity, biogeography, and biomes, understanding ecology and environmental biology,
with little mention of ecosystem ecology. Ecosystem one that asks the question that is rarely asked by
ecology is included, but treated separately. Topics ecology texts – What is the significance of biodiversity to
such as C, N, P, and S biogeochemistry, primary and human wellbeing?
secondary production, decomposition, trophic pyra- Rather than the conventional perspective, which
mids, and energy flow make sparse reference to sees biodiversity as a culmination of population and
population or community ecology. Today, most community ecological processes with ecosystem
ecology texts also include treatment of environ- processes being separate, ecologists at a conference
mental issues such as pollution, the ozone hole, in 1992 in Bayreuth, Germany, considered an alter-
climate change, collapsing fisheries, disappearing native perspective, one that added biotic feedback
forests, the adverse consequences of unbounded from biodiversity to ecosystem processes (Schulze
human population growth, emerging diseases, and and Mooney 1993). Although this concept of biotic
conservation biology; this last topic being where the feedback was unconventional and controversial,

3
4 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

it actually dates back to Darwin. In the Origin,

Darwin (1859) hypothesizes, based on his principle of

Ecological function
divergence, that as diversity evolves and fills niche
space it will lead to an increase in productivity and
other ecosystem processes due to the ecological
‘division of labour’ (Hector and Hooper 2002). There
are also a few later echoes of this idea before it
was fully reborn at the 1992 Bayreuth conference.
Carlander (1952) found a positive relationship
between the diversity of freshwater fishes and their
overall secondary productivity, which he interpreted 0 Biodiversity loss Natural
as coming about due to more complete filling of level
niche space. Similarly, in two papers that are under- Biodiversity
appreciated in the biodiversity and ecosystem
functioning literature, Bell (1990, 1991) found Figure 1.1 A plethora of trajectories of ecosystem function in response
to changes in biodiversity. Historically, initial discussions of the relation-
that complementary differences amongst species
ship between biodiversity and ecosystem functioning were facilitated by
of Chlamydomonas led to increased productivity the heuristic device of plotting hypothetical responses of ecosystem
and greater temporal stability of production. Nev- functions, such as primary production or nutrient cycling rates, against a
ertheless, it was only following the 1992 Bayreuth gradient in biodiversity that was considered to embody taxonomic,
conference that investigation of the effects of biodi- functional, phylogenetic, and even the spatial and temporal dimensions of
biological diversity. ‘Natural’ indicates the maximum level of diversity
versity on ecosystem functioning coalesced as a
typical for an ecosystem, whereas positions to the right of ‘natural’
focused research area. indicate the addition of exotic or domestic species that lead to higher
The first generation of research on the relation- levels of diversity. The solid line reflects the hypothesis that many species
ship between biodiversity and ecosystem function- were redundant, which would lead to a ceiling in gains per species added.
ing consisted largely of experimental confirmations The dotted, hump-shaped line reflects a linear increase in which species
contributed similarly to functioning, followed by a decline when exotic
that the two were indeed linked with one another –
species were added. The small-dash, linear line indicates improvements in
changes in biodiversity had predictable effects on ecosystem functioning with every species added, suggesting no redun-
ecosystem functioning (Loreau et al. 2002). Both dancy. The dashed, concave up curve indicates a dramatic decline in
the design of the experiments and interpretation function as soon as diversity drops below natural levels due to the loss of
of the results, however, were surrounded by keystone species. The long-dashed line indicates an idiosyncratic or
unpredictable response of functioning to biodiversity loss. Over fifty dif-
much debate (e.g. Guterman 2000, Kaiser 2000,
ferent hypothetical trajectories have been described.
Naeem 2000, Tilman 2000, Wardle et al. 2000b).
Solan et al. (Chapter 3) review the history and
impacts of biodiversity and ecosystem functioning
research, providing an in depth analysis of what to interpret. Furthermore, biodiversity does not
began as a rather unconventional approach to eco- exist in nature outside of ecosystems; nor does an
logical research, but which has since grown into a ecosystem exist without biodiversity – plotting one
major paradigm in ecology. orthogonal to the other as dependent and inde-
The simple heuristic of plotting a trajectory of pendent variables is a strange thing to do. The
ecosystem functioning against a gradient in biodi- bivariate plot, various biodiversity and ecosystem
versity in a bivariate plot (Fig. 1.1), an approach functioning trajectories, and their interpretation are
begun by Vitousek and Hooper (1993), and asking reviewed elsewhere (e.g. Schläpfer and Schmid
what the shape of the trajectory might be, provoked 1999, Naeem 2001b, Naeem et al. 2002), thus we will
much research and discussion, but such simple not dwell on them here. Research on the relation-
plots belie the underlying complexity of the prob- ship between biodiversity and ecosystem function-
lem. Biodiversity and ecosystem function are both ing has moved well beyond this early framework.
difficult to define and quantify; thus trajectories Today, the complexities underlying the relation-
in such a poorly defined bivariate space are difficult ships between biodiversity and ecosystem
 INTRODUCTION 5

functioning consume contemporary research. The nitrogen-fixing or sulfur-reducing) environmental

thought experiment that follows will serve to factors such as soil moisture, salinity, and nutrient
illustrate these complexities. availability (e.g. Lavorel and Garnier 2002). The
species we introduce will be related to one another
by their functional traits, ranging from being
1.2 Sterilizing Earth: a thought
nearly redundant (having the full set of traits in
experiment in three parts
common) or nearly singular (possessing largely
As an introduction to this topic and to provide the unique traits) (e.g. Naeem 1998). Third, species
context for this volume, let us perform the follow- will also possess homologous characters that
ing thought experiment in three parts. First, con- reflect their shared evolutionary history or phy-
sider a space anywhere on Earth’s surface at any logeny and will be either closely or distantly
scale – a park, city, farm, lake, river, wetland, sea, related (e.g. Ackerly 2004, Edwards et al. 2007).
biome, or the biosphere – and then sterilize it. Every Fourth, species will either consume, be consumed
plant, animal, and microorganism that occupies this by, compete with, parasitize, or facilitate other
space is destroyed, leaving nothing behind but species in a web of interactions that vary in
rocks, sand, water, dead organic matter, and a strength (inset in Fig. 1.2) (e.g. McCann et al. 1998,
variety of atmospheric gasses. Second, humans are Thébault and Loreau 2006). Fifth, the abundance of
spared but now find themselves in the barren species, in terms of either density or mass, will
space, their wellbeing entirely dependent on how vary depending on each species’ growth rates,
one restores the ecosystem. Third, we erect a barrier body size, metabolism and life history (e.g. Brown
to all living organisms and we use this barrier to et al. 2004), resource availability (e.g. Tilman 1982),
control the functional, phylogenetic, and biogeo- stoichiometry (Elser and Sterner 2002), interactions
graphic identity of the species we allow to enter. with other species, top down and bottom up con-
We also allow for the direct importation of species, trols within the food web (Pimm 1982, De Ruiter
be they native, exotic, domestic, or genetically et al. 2005, McCann et al. 2005), and spatial factors
engineered. We also use the barrier to control the (e.g. Tilman and Kareiva 1997, Loreau et al. 2003).
timing and order of entry, the abundance, and Sixth, species are assembled by biogeographic
spatial distribution of the species that enter. In other processes (e.g. MacArthur and Wilson 1967,
words, we, the human occupants of the space, fully MacArthur 1972, Hubbell 2001, Lomolino and
control every aspect of the biodiversity of organ- Heaney 2004). Seventh, the timing, order of entry,
isms that will re-populate the sterile space. The and other factors affecting assembly also influence
importance of biodiversity, ecosystem functioning, biodiversity (e.g. Weiher and Keddy 1999, Fukami
and the wellbeing of the humans occupying the and Morin 2003, Larsen et al. 2005). Collectively,
space would begin to be revealed as biodiversity is these many factors determine the biodiversity one
reestablished. If the experiment sounds a little finds in a community, all of them influencing flows
bizarre, recall that the ill-fated Biosphere II had of nutrients into and out of the inorganic pool, the
much the same aims. use and return of water, and the flow of energy
Once we have fixed this image in our mind, we sequestered by primary producers and lost
can immediately see that there is a near infinite through respiration (De Angelis 1992, Loreau 1994,
number of ways to go about reestablishing biodi- Loreau 1995, Grover and Loreau 1996, De
versity in a sterile space and if human wellbeing is Mazancourt et al. 1998, Hulot et al. 2000, Norberg
at stake, the decisions we make take on enormous et al. 2001).
importance. Figure 1.2 illustrates this thought The preceding long list of factors is meant to
experiment and summarizes the key elements of emphasize the overwhelming complexity of what is
biodiversity that we have to consider. First, each embodied in the structure and function of biodi-
species we introduce possesses functional traits versity in ecosystems and the dilemma we face if
which reflect their tolerances and responses to (e.g. we have to construct an ecosystem from the ground
drought or salt tolerance) and impacts on (e.g. up. There are three approaches we could take in
6 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Primary production Respiration

Figure 1.2 Graphic model of the relationship between
Functional trait biodiversity, ecosystem function, and human wellbeing. This
clustering figure reflects the thought experiment described in the text in
which humans are dependent on the services derived from
the functioning ecosystem within which they reside. In the
central box, species are portrayed as different shapes and
Biogeographic Interaction colors and their abundance is indicated by the number of
grouping web each shape. The upper dendrogram reflects species clustering
Abundance

by similarity in functional traits. The lower dendrogram

reflects species relations by phylogeny. The ovals below the
box represent the inorganic nutrient pool and water
resources. All compartments can potentially have inputs and
outputs (immigration and emigration in the case of biodi-
versity and humans). Curved, parallel lines indicate conduits
between compartments. The inset represents a web of biotic
interactions (arrows linking species) of different strengths
(width of arrows). The figure motivates the thought
Emigration
immigration exercise of imagining how biodiversity is related to ecosystem
Phylogenetic functioning and human wellbeing by considering how
clustering such relationships are affected by the species selected to
reside in the ecosystem, and the resulting mix of traits,
phylogenetic relationships, biotic interactions, and other
factors. The main purpose of the figure is to illustrate the
Inorganic nutrient Water complexity of what underlies otherwise simple relationships
pool resources typically plotted in biodiversity and ecosystem function
bivariate space (Fig. 1.1).

repopulating a sterile space, all of which reflect the This thought experiment demonstrates that every
rapidly evolving field of biodiversity and ecosys- species contributes to ecosystem functioning and
tem functioning. We could simply restore bio- human wellbeing in complex ways, though obvi-
diversity to what it was at the time of sterilization, ously at different levels (from negligible to enor-
under the assumption that that was the best bio- mous) and with different impacts on humans (from
diversity for the people who lived there. We could, beneficial to harmful). We know that each species
alternatively, avoid making the assumption that we admit into the space will change its ecosystem
resident biodiversity is the best for humanity and functions (e.g. primary productivity, nutrient
employ ecological principles to engineer the con- cycling, decomposition), its biotic functions (e.g. its
struction of a biota that would maximize the well- susceptibility to invasion, the likelihood that an
being of its human residents. Finally, we could emerging disease might spread, or the dynamic
explore numerous combinations of species at dif- stability of its populations), and the wellbeing of its
ferent relative densities and monitor ecosystem human occupants (e.g. the prevalence of poverty,
function and human wellbeing until we obtained hunger, and economic prosperity). (Note that we
the biodiversity that optimizes human wellbeing. distinguish between ecosystem and biotic functions,
We will refer to these three approaches as restor- the former referring to biogeochemical functions and
ative, eco-engineered, and explorative, respectively. the latter referring to the influences of species on one
 INTRODUCTION 7

another. Some researchers, however, use ecosystem for different communities differing in biodiversity,
function to refer to both biogeochemical and biotic is a plot like Fig. 1.1. The exercise, however, illus-
functions.) Obviously some species additions will trates how difficult it is to obtain such plots, how
have little effect while others will have dramatic complex the underlying processes are, and how
impacts. Further, because all species interact with difficult interpretation of such plots might be.
one another directly or indirectly, with strengths of
interaction that vary in sign and magnitude (inset in
1.3 The evolution of biodiversity
Fig. 1.2), the impact of each species will be within the
and ecosystem functioning research
context of the community present.
Of the three approaches to restore our sterilized Our thought experiment makes transparent how
space, restorative, eco-engineered, and explorative, any attempt to experimentally explore the rela-
the most neutral approach, or one that requires the tionship between biodiversity and ecosystem func-
least commitment to any particular ecological tioning requires the researcher to make several
framework, is the explorative approach that con- decisions that ultimately determine what can and
ducts hundreds (if not thousands or millions) of cannot be inferred from the results. What should be
experiments in which each experiment randomly manipulated, for example? Should species richness,
creates a different community, sometimes rich in functional diversity, genetic diversity, relative
biodiversity, other times poor or intermediate. abundance, or some combination of these or other
With each species selection, one imports a set of factors be manipulated? Should species be selected
traits, modifies the functional and phylogenetic based on biogeography (e.g. only species known to
clustering of the community, modifies the com- coexist in nature), or could one use any species that
munity web, and, depending on the density and is likely to survive in the experiment (e.g. a series of
mass of individuals initially imported, alters the exotic species or domestic species)? How extensive
relative abundance of species. In short, every biotic should the biodiversity gradient of the experiment
function is modified in some way. Immediately be? Should the lowest level of diversity in the
upon introduction, every entering species will also experimental biodiversity gradient be a sterile plot,
affect the flow of nutrients, energy, and water a single species, or a complete food web with only
through the system in some way, again in ways one species per trophic level? Should the highest
ranging from small to large. level of biodiversity gradient be all species that co-
If during an explorative biodiversity and eco- occur in nature, a subset, or more than what is
system functioning approach to repopulating a typically found in nature, and should several
sterile habitat we simultaneously plot some metric trophic levels be used with as many species per
of the diversity of the species we include (e.g. trophic level as possible?
functional diversity, see Chapter 4) against some Most decisions in biodiversity and ecosystem
metric of ecosystem functioning (e.g. net primary functioning experiments concern two things; the
production) or against some metric of a biotic rationale for species selection and the extent of the
function (e.g. resistance to the spread of an biodiversity gradient to be used in re-populating
emerging disease) or against some measure of the replicates. One of the first biodiversity and
human wellbeing, what would that plot look like? ecosystem functioning experiments (Naeem et al.
Would the values for biodiversity, ecosystem 1994, Naeem et al. 1995), for example, was a
function, biotic function, or human wellbeing complex, multi-trophic terrestrial mesocosm built
show any correlations? Would the maximum for in a system of growth chambers known as the
human wellbeing coincide with maximum Ecotron (Lawton et al. 1993, Lawton 1996).
biodiversity? Biodiversity and ecosystem func- Researchers selected species known to co-occur in
tioning research attempts to shed light on these the field, and were likely to survive in the growth
and many other questions. chambers; they paid little attention to whether the
Note that the end product of such an exercise, species were exotic or not. The researchers also
repeatedly plotting ecosystem function measured decided to use a biodiversity gradient of just three
8 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

levels of species richness, but to retain multiple findings to real-world problems associated with
trophic levels throughout. Experiments that fol- biodiversity loss. Key features of this new research
lowed took similar approaches – they began with a include greater precision in its metrics as well as
pool of species that were known to co-occur in increasing integration of the many processes and
nature, were not overly concerned with whether factors known to impact biodiversity. Greater pre-
they were exotic or not, and established replicate cision in metrics, for example, involved the evolu-
systems (microcosms, artificial ponds, flower pots, tion of better, more appropriate and applicable
and grassland plots) cleansed of the species they measures of biodiversity. In this regard, functional
wanted to manipulate. The experimenters then diversity has emerged as the frontrunner for the
repopulated their cleansed replicates with species. most relevant component of biodiversity with
Each experiment, however, took slightly different respect to ecosystem functioning (Díaz and Cabido
approaches. For example, the experiments of 2001, Naeem 2002a, Petchey and Gaston 2002a).
Cedar Creek, Minnesota, focused exclusively on How one defines, quantifies, and uses functional
plants (Tilman et al. 1996, Reich et al. 2001) as did diversity to interpret how changes in biodiversity
the European BIODEPTH experiments (Hector et can impact ecosystem functioning has become a
al. 1999), though one BIODEPTH site manipulated dominant part of biodiversity and ecosystem func-
insect abundance (Mulder et al. 1999). Hooper tioning research (see Petchey et al., Chapter 4).
manipulated only plants in Californian serpentine Biodiversity and ecosystem functioning research
grasslands, but focused on functional groups has also expanded to include important elements
rather than species (Hooper and Vitousek 1997). In of ecological systems previously understudied.
fact, most grassland experiments did a combina- Among them, trophic complexity has become a
tion of both functional group and species manip- major theme in contemporary biodiversity and
ulations (Tilman et al. 1997b, Naeem et al. 1999, ecosystem functioning research. Rather than work-
Wardle et al. 2000a, Reich et al. 2004). ing within a single trophic level like many early
Early theory and experiments were confirmatory; plant-only experiments, trophic complexity has
they primarily sought to examine the possibility become an important part of biodiversity and eco-
that diversity could indeed affect ecosystem func- system functioning experiments and theory (see
tioning. As biodiversity and ecosystem functioning Cardinale et al., Chapter 8). Additionally, rather
research shifted out of its early confirmatory phase, than black-boxing the microbial world or using
however, it increased the scope of organisms and them for microcosm tests of theory, biodiversity
systems it investigated and became more explor- and ecosystem functioning is expanding to uncover
atory in scope. Hundreds of experiments explored the role of microbes in more complex and natural
freshwater, stream, wetland, microbial, coral reefs, systems (see Bell et al., Chapter 9).
marine ecosystems, and grassland ecosystems, Research on the relationship between biodiversity
many of which are discussed directly in this and stability has also gone beyond the initial attempt
volume or indirectly as parts of meta-analyses. to simply confirm if there was or was not a relation-
Although each experiment is unique, common to all ship between the two to recognizing multiple rela-
of them was the need to decide rationally which tionships (mostly positive, some neutral, and a few
species to select for inclusion or exclusion and what negative) and multiple mechanisms (see Griffin et al.,
would constitute the gradient in biodiversity. Chapter 6). Theory has also gone well beyond
The expansion in extent, scope, and complexity of resource-based or Lotka–Volterra type models to
biodiversity and ecosystem functioning experi- explore multitrophic systems, metacommunities, and
ments led the field to become more predictive other theoretical advances (see e.g. Gonzalez et al.,
rather than confirmatory and exploratory, with an Chapter 10).
increased emphasis, first, on developing theory With advances in experiments, observational
with which to interpret these experimental results studies, precision in metrics, tools, and theory,
(Hector et al. Chapter 7, Loreau and Hector 2001, knowledge on biodiversity and ecosystem func-
Fox and Harpole 2008), and later on applying these tioning is now sufficiently developed that the first
 INTRODUCTION 9

projections of the ecosystem consequences of bio- (Dasgupta 2001). Running down natural capital does
diversity loss have begun. Developing means for not only mean the depletion of non-renewable
biodiversity and ecosystem functioning projections resources like oil, minerals, fossil water, it also means
was the goal of the National Science Foundation the loss of biodiversity (Sala et al. 2000, Millennium
research coordinating network known as Biotic Ecosystem Assessment 2005b) and ecosystem ser-
Mechanisms of Ecosystem Regulation in the Global vices (Millennium Ecosystem Assessment 2005a,
Environment (BioMERGE) (Naeem and Wright Kareiva et al. 2007). In some cases, this has left people
2003, Naeem et al. 2007). This is an ambitious and little better off than they were before. Many of the two
important trend in biodiversity and ecosystem billion people in poverty, or the one billion in hunger,
functioning research. It is ambitious because it are dependent on common-pool environmental
incorporates many factors that impact biodiversity resources for their livelihoods. In other cases, the
(see the long list we provided above) into simula- costs associated with the loss of natural capital are
tions to project future states of ecosystem func- simply not taken into account by those whose actions
tioning. It is important because these projections are have caused it. Indeed, there is a widespread view
meant to be realistic and large-scale and useful to that our systematic neglect of the human costs of the
researchers, managers, and policymakers alike. erosion of natural capital stocks has to change (World
Currently, studies that have used this approach are Commission on Environment and Development
limited, but show promise. Duffy et al. (Chapter 5) 1987, United Nations Environmental Program 2007,
review this emerging field in biodiversity and eco- Holdren 2008). For change to be well-informed, we
system functioning research. need to better understand the consequences of erod-
ing the natural capital base.
The replacement of naturally occurring animals
1.4 Biodiversity and humanity: strains
and plants with domesticated species began in ter-
in a productive partnership
restrial systems over ten thousand years ago and is
The minute humanity began to manipulate nature now increasing in aquatic and marine systems as
beyond what is common for ecosystem engineers well (Duarte et al. 2007). When human populations
like beavers or termites (Jones et al. 1994), or what were small, such substitutions of naturally diverse
might be expected from niche construction (Laland systems with smaller numbers of more manageable,
and Sterelny 2006), humans began a path that would higher-yielding species, was not likely to have
lead to extraordinary success, but at an extraordi- major impacts on ecosystem functioning at large
nary price. Success can be seen in terms of humans scales. As the scale of human activity has increased,
becoming the dominant geomorphic (Wilkinson however, so has its ecological impact.
2005), biogeochemical (Vitousek et al. 1997), and The initial conditions of the thought experiment,
consumer species (Imhoff et al. 2004). In the last that of complete human domination of ecosystems,
two centuries, aided by access to fossil fuel and are admittedly extreme, but they represent an
fossil water, humanity has appropriated an ever- important endpoint in a continuum that structures
increasing proportion of terrestrial surfaces (Foley the conceptual framework of biodiversity and eco-
et al. 2005, Worm et al. 2005), net primary productivity system functioning research. At one end, all of
(Haberl et al. 2007), fresh water (Vörösmarty et al. humanity’s needs are met by managing ecosystems
2000, Oki and Kanae 2006), and marine resources using only the species necessary to maximize
(Worm et al. 2006). In so doing, levels of output and human wellbeing. At the other end of the contin-
consumption have grown everywhere – albeit at very uum is a state in which every need of humanity is
uneven rates. Success has meant a process of eco- met by nature – a state that probably last existed six
nomic development that has built up stocks of ‘pro- million years ago when our primate ancestors
duced’ and ‘human’ capital (infrastructure, buildings, started down the evolutionary pathway that would
equipment, and financial assets on the one side, lead to the origination of the human species.
technology, skills, education, and learning on the Where in the gradient, from complete human
other), whilst running down stocks of ‘natural’ capital domination of ecosystems to being no different
10 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

from other species in their impacts, is human Furthermore, monocultures or combinations of just
wellbeing optimized? The right balance remains two or three species could often out-produce com-
unknown, but it is clear that humanity is shifting munities that were much more species-rich. In terms
to the end where all of humanity’s needs are met of production, it seemed one could get by with far
by heavily managed ecosystems. In the case of fewer species in an ecosystem than was typically
agro-ecosystems, Jackson et al. (Chapter 13) note found in nature.
such systems now comprise 65 per cent of terres- Lost production due to simplification in natural
trial ecosystems, with 10 per cent in high-input systems (which was counter to the production-
agriculture, 15 per cent in low-input agriculture, simplification tradeoff in managed systems where
and 40 per cent in mixed use. By 2050 an additional production appears to improve under simplifica-
109 hectares of wildlands are likely to be converted tion) was only one part of the picture; stability
to managed lands to feed our growing population. could also be affected by biodiversity loss. Proof
Managed ecosystems reflect a production- that stability and diversity were positively related,
simplification tradeoff in which the production of however, was much more difficult to demonstrate
utilitarian biomass (i.e. edible plants and animals, (McCann 2000, Cottingham et al. 2001). Biodiver-
biofuel, lumber) is increased at the expense of sity was seen as a means of enhancing system
native biodiversity that may appear at first glance reliability (Naeem and Li 1997, Naeem 1998,
to have less utility, though its full utility has yet to Naeem 2003) and a means of improving and sta-
be understood or inventoried. The transformation bilizing long-term gains in ecosystem function (e.g.
of complex landscapes that typically housed hun- Doak et al. 1998, Tilman et al. 1998, Yachi and
dreds of species of plants and vertebrates, thou- Loreau 1999).
sands of species of invertebrates, and untold An important point that many researchers have
numbers of species of microorganisms, to managed made, but which is seldom demonstrated, was that
systems always lowers local (e.g. species per square production was not the only function that was
meter) taxonomic richness to a tenth or hundredth affected by biodiversity loss. There is increasing
of its original value. More importantly, biodiversity evidence that the maintenance of multiple ecosystem
loss associated with simplification often brings with processes requires many more species than does the
it concomitant reductions in trait diversity and maintenance of a single process (Eviner and Chapin
reductions in the number, type, strengths, and 2003, Hector and Bagchi 2007, Gamfeldt et al. 2008).
arrangement of biotic interactions among species in An important example of a multiple function is the
the community web. Simplification refers more role of biomass production as both a provisioning
specifically to such reductions in functional diver- ecosystem service (i.e. timber and non-timber forest
sity and complexity than it does to taxonomic loss. products) as well as regulatory service in terms of
Initially, biodiversity and ecosystem functioning carbon storage (Díaz et al., Chapter 11).
research focused on the single function of produc- While understanding the true costs of the pro-
tion which would prove to be neither a persuasive duction-simplification tradeoff in terms of changes in
argument for conserving biodiversity nor an accu- the magnitude, reliability, and stability of multiple
rate reflection of the true costs of ecological sim- biogeochemical functions is a major thrust in biodi-
plification. Biodiversity and ecosystem functioning versity and ecosystem functioning research, of equal
studies generally found a positive, asymptotic rela- importance are the impacts of simplification on
tionship between biodiversity and production, sug- biotic functions. Jackson et al. (Chapter 13) note that
gesting that biodiversity loss meant loss in biocontrol and pollination (see Klein et al., Chapter
production and implying that human wellbeing 14), both biotic functions, have received attention in
would decline in the face of such declining produc- the biodiversity and ecosystem functioning literature
tion. The demonstrated relationships, however, typi- and are frequently cited as examples of ecosystem
cally described strong gains in production with just a services relevant to agro-ecosystems (Balvanera et al.
few species and vanishingly small gains in produc- 2005, Tscharntke et al. 2005, Philpott and Armbrecht
tion with each species added (Schmid, Chapter 2). 2006, Kremen et al. 2007, Priess et al. 2007). Two
 INTRODUCTION 11

other examples of biotic functions include the for granted that if the left-hand side of the construct
influences of biodiversity over invasive species (see was demonstrated, then the right-hand part of the
Engelhardt et al., Chapter 16) and diseases (see construct, the link between ecosystem services and
Ostfeld et al., Chapter 15). human wellbeing, would follow. And if it did not
The question of restoration, especially restoration follow automatically, then it was up to economists
targets, takes on new meaning in light of the pro- to separately pursue the right-hand side of the
duction-simplification tradeoff and the relationship construct.
between biodiversity and ecosystem functioning. In principle, the logic of working on individual
Most habitats designated for restoration have lost parts of the construct was sound and in keeping
biodiversity either due to simplification (e.g. for with the tradition of ecologists and economists
agriculture) or degradation by pollution or unsus- working separately. In practice, however, the result
tainable extraction, such as clear cutting lumber was that the natural science of biodiversity and
or over harvesting fish. Restoring simplified or ecosystem functioning, though published in high-
degraded habitats to some version of their former profile scientific journals, failed to carry through to
self requires thinking about restoring not only lost management and policy (Solan et al., Chapter 3).
diversity, but lost functioning and services as well The apparent simplification–biodiversity tradeoff,
(Wright et al., Chapter 12). which was the hallmark of human development,
was pitted against scientific cautions about hidden
costs. The value of land, water, farms, lumber,
1.5 The emergence of a unified
fisheries, and other natural resources are, however,
natural–social biodiversity and
far greater than the potential gains suggested by
ecosystem functioning framework
biodiversity and ecosystem functioning research.
Biodiversity and ecosystem functioning research Vanishingly small gains in production in abstract
can and should supply managers, conservation experimental systems or arguments about
biologists, policy makers, and other interested improved stability were not translated into eco-
parties, with the information they need to make the system services (i.e. the right-hand side of the
best decisions they can regarding their effects on construct). Indeed, in spite of the adoption of the
biodiversity. Although it has so far done poorly at biodiversity ! ecosystem functioning ! ecosystem
informing management and policy (Solan et al., services ! human wellbeing framework by the
Chapter 3), it is founded on a central construct that Millennium Assessment and over a decade of bio-
clearly indicates that it can do so. This construct is diversity and ecosystem functioning research, only
written simply as, a handful of case studies were available to support
the Assessment’s conclusions that greater biodi-
Biodiversity ! Ecosystem Functioning !
versity provides more ecosystem services. A case
Ecosystem Services ! Human Wellbeing,
study approach was similarly used by Balmford
where each arrow represents a causal relationship et al. (2002). Early attempts to estimate the economic
and ecosystem services are ecosystem functions that value of the ecosystem services supported by bio-
benefit humans. This framework, in fact, became diversity received considerable attention (e.g.
the central framework for the Millennium Assess- Costanza et al. 1997, Costanza and Folke 1997,
ment (2003). Pimentel et al. 1997), but because they rested on
Typically, biodiversity and ecosystem function- questionable methodology were dismissed by most
ing researchers assumed that if they demonstrated economists. Nevertheless, they did serve to
that biodiversity was important to the magnitude emphasize that non-marketed ecosystem services
and stability of any ecosystem function, then it were more important than previously believed.
would automatically follow that biodiversity is At the same time, there is little evidence from
important to the magnitude and stability of eco- over a decade and a half of research – comprising
system services and, by extension, to the magnitude hundreds of biodiversity and ecosystem function-
and stability of human wellbeing. That is, they took ing and economic analyses and the adoption of the
12 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

principles by the Millennium Assessment – that biological resources that support not only provi-
biodiversity conservation as a route to improve sioning services (e.g. the production of foods,
human wellbeing has become a strong part of the fuels and fibres) and cultural services (e.g. the non-
private or public consciousness. consumptive enjoyment of landscapes for recrea-
While each link in the biodiversity ! ecosystem tional, educational, scientific, spiritual, or cultural
functioning ! ecosystem services ! human reasons), but also regulating services. In the last
wellbeing framework is important in its own right, case, the economic theory of portfolio choice pro-
these links do need to be developed in unison, as vides a natural way to investigate the implications
neither the natural science underlying the influ- of biodiversity for risk management.
ence of biodiversity on ecosystem functioning nor A third thrust addresses the incorporation of
the social science underlying the link between ecosystem components into economic decision
ecosystem services and human wellbeing can carry models. Brock et al. (Chapter 19) review the ways in
the day on their own. Economists’ perspectives on which economists model decision problems in
the importance of biodiversity have contributed coupled ecological–economic systems that are sub-
significantly to understanding the social implica- ject to varying levels of anthropogenic impact. They
tions of biodiversity loss (Barbier et al. 1994, Per- also discuss the consequences of the different
rings 1995, Perrings et al. 1995, Swanson 1995, objectives that motivate people, ranging from the
Folke et al. 1996, Chichilisky and Heal 1998, Hol- preservation of naturalness to the management of
lowell 2001); thus the foundation for a unified food production systems.
framework exists. Central to this unification, as both Perrings et al.
The economic literature on biodiversity and eco- (Chapter 17) and Brock et al. (Chapter 19) note, is an
system services is rapidly growing (Heal 2005, understanding of (a) the mechanisms that connect
Carson 2008). There are three major thrusts to this biodiversity and ecosystem functioning to the pro-
literature, which are reflected in the chapters duction of valued ecosystem services, and (b) the
included in this volume. One thrust addresses the set of incentives that lead individuals to behave in
reasons why markets fail to allocate biological ways that are more or less closely aligned with the
resources efficiently, and identifies corrective meas- social interest. All too frequently, decisions made
ures. Perrings et al. (Chapter 17) identify the exter- by private resource users neglect costs that are
nality and public good problems that lie at the heart displaced onto others.
of biodiversity loss, and survey the range of cor- There is a complex array of social and natural
rective mechanisms discussed in the literature. feedbacks that the simple biodiversity ! ecosystem
These include the development of markets for ser- functioning ! ecosystem services ! human well-
vices such as ecotourism or bioprospecting. But being construct does not capture. Incorporating these
they also include a number of instruments designed feedbacks will be necessary if effective economic
to encourage resource users to take the biodiversity instruments based on biodiversity and ecosystem
consequences of their actions into account, such as services are to be designed to ensure that private
taxes, access charges, user fees, payment for eco- decisions are compatible with the social interest. The
system services, direct compensation payment, and chapters on economics make it clear that the emerg-
transferable development rights. ing natural–social unified approach can occur if
A second thrust addresses the valuation of eco- ecologists and economists work together.
system services and, through this, of the biodiver-
sity and ecosystem functioning that underpins the
Summary
production of services. Barbier et al. (Chapter 18)
review the economics of ecosystem service valua- In this introduction, we have reviewed the basic
tion, and illustrate the way in which the demand ideas that have structured the revolution in the
for basic ecosystem components may be derived natural and social sciences that inextricably links
from the demand for ecosystem services. They biodiversity with human wellbeing. Our emphasis
show how the approach can be used to value the is on the scientific basis for biodiversity’s influence
 INTRODUCTION 13

over ecosystem functioning and its concomitant exploratory phase at the beginning of this century,
effects on human wellbeing. Although the contem- and is now in the throes of building a new, joint,
porary field of biodiversity and ecosystem func- natural–social model for humanity. The authors of
tioning emerged only in 1992 (the year of the Earth these chapters are those who have spearheaded this
Summit in Rio and the establishment of the United change and are driving its leading edge. What fol-
Nations Convention on Biological Diversity and the lows are descriptions of those achievements,
United Nations Framework Convention on Climate advances, and future directions. The reader will
Change), the field of biodiversity and ecosystem find what unfolds to be as scientifically fascinating
functioning has evolved rapidly through three as it is relevant to solving our most pressing envi-
stages. It first survived the contentious confirma- ronmental problems.
tory years of the late 1990s, moved through an
 CHAPTER 2

Consequences of species loss for

ecosystem functioning: meta-analyses
of data from biodiversity experiments
Bernhard Schmid, Patricia Balvanera, Bradley J. Cardinale,
Jasmin Godbold, Andrea B. Pfisterer, David Raffaelli, Martin Solan,
and Diane S. Srivastava

2.1 Introduction and a representative response at the ecosystem,

community, or population level, were significantly
2.1.1 Two meta-analyses of biodiversity
influenced by several factors; the specifics of exper-
studies published in 2006
imental designs, the type of system studied, and the
The study of patterns in the distribution and category of response measured. For example, biodi-
abundance of species in relation to environmental versity effects were particularly strong when
variables in nature (e.g. Whittaker 1975), and to the experimental designs included high-diversity
species interactions (Krebs 1972), has had a long mixtures (>20 species) and in well-controlled sys-
tradition in ecology. With increasing concern tems (i.e. laboratory mesocosm facilities).
about the consequences of environmental change A second meta-analysis was conducted by
for species extinctions, researchers started to assess Cardinale et al. (2006a) which focused on experi-
the potential of a reversed causation: does a ments, published from 1985–2005, where species
change in species diversity affect environmental richness was manipulated at a focal trophic level
factors and species interactions, such as soil fer- and either standing stock (abundance or biomass)
tility or species invasion? Manipulative experi- at that same trophic level, or resource depletion
ments that explicitly tested the new paradigm (nutrients or biomass) at the level ‘below’ the focal
started in the early 1990s and since then the level was measured. Cardinale et al. (2006a) used
number of such studies has been increasing expo- log ratios of responses to characterize biodiversity
nentially (Balvanera et al. 2006, Chapter 3). effects. Their analyses showed that species-rich
In 2006, two meta-analysis papers were pub- communities achieved higher stocks and depleted
lished which together provided the most compre- resources more fully than species-poor communi-
hensive quantitative assessment of the overall ties, but that diverse communities did not neces-
trends observed in manipulative biodiversity sarily capture more resources or achieve more
experiments to date. Both studies showed that, on biomass than the most productive species in
average, random reductions in diversity resulted monoculture. Cardinale et al. (2006a) also fitted data
in reductions of ecosystem functions, but differed in from experiments to a variety of functional rela-
the covariates examined. First, Balvanera et al. tionships, and found that experiments were usually
(2006) analyzed studies published from 1974–2004. best approximated by a saturating function. The
This meta-analysis showed that biodiversity effects, results from both meta-analyses were remarkably
measured as correlation coefficients between some consistent across different trophic levels and
measure of biodiversity (usually species richness) between terrestrial and aquatic ecosystems. In this

14
 CONSEQUENCES OF SPECIES LOSS FOR ECOSYSTEM FUNCTIONING 15

chapter we present further analyses of the two low to high, in most cases a biodiversity effect can be
meta-data sets, in parallel, and attempt a joint more specifically defined as a positive or negative
interpretation. relationship between variations in biodiversity as the
explanatory variable and a function as response
variable. Thus, a positive diversity effect occurs when
2.1.2 The two meta-data sets used
a relationship is positive and a negative biodiversity
in this chapter
effect occurs when a relationship is negative.
The two meta-data sets assembled by Balvanera
et al. (2006) and Cardinale et al. (2006a) are hereafter
2.1.3 Hypotheses
referred to as B and C, respectively. Together, the
two databases contain more than 900 published The goal of meta-analyses of biodiversity–ecosystem
effects of biodiversity on ecosystem functioning functioning experiments is to assess to what extent
(Schmid et al. 2009, Cardinale et al. 2009). In B, these biodiversity effects reported in single studies can be
effects were extracted directly from the publications generalized across different design variables, sys-
and therefore rely on the analysis (assumed to be tem types, and response categories. Ideally,
correctly executed) carried out by the original hypotheses about variation between studies should
authors. In more than half of the cases, the extrac- be derived, a priori, from underlying mathematical
ted biodiversity effects were correlation coefficients theory about mechanisms responsible for biodiver-
(Balvanera et al. 2006). For these, and for additional sity effects. In practice, however, it is often only
cases, significance, direction, and shape of the possible to look for patterns in variation of biodi-
relationship between biodiversity and each versity effects and then develop explanatory
response variable could be extracted. In C, the hypotheses in retrospect. This is primarily due to
mean values of response variables were available the fact that the majority of biodiversity experi-
for each level of species richness. This allowed the ments included in our meta-databases focused on
authors to decide whether a linear, log-linear, or demonstrating biodiversity effects rather than
saturating curve (Michaelis–Menten) was the best attempting to test specific mechanistic hypotheses
fitting relationship (see Cardinale et al. 2006a). (for an exception, see e.g. Dimitrakopoulos and
For ease of comparison with B, the correlation Schmid 2004). The hypotheses presented in this
coefficients obtained using the log-linear fit in C chapter are derived from patterns found in the pre-
are used for this chapter. These were very closely vious meta-analyses of B and C. To avoid repetition
correlated with the correlation coefficients on the of results reported in Balvanera et al. (2006), we omit
Michaelis–Menten scale (r ¼ 0.99, n ¼ 105). The hypotheses relating to the influence of specific
significance was not assessed in C because the experimental designs. Instead, we consider several
relationships were calculated from means. new hypotheses (see below). We also consider the
If the same response variable was measured shape of the relationship between biodiversity and
repeatedly in an experiment, it was only entered specific response variables.
once in each of the two meta-databases: B focused on Our first hypothesis is that biodiversity effects
the first date on which measurements were taken in differ among ecosystem types (Hooper et al. 2005).
a study (excluding establishment phases of experi- Differences in biodiversity effects among ecosys-
ments) while C selected the last date of published tems could arise, for example, from variation in the
measurements. Although about half of the mea- ratios of producer/consumer stocks, or the size,
surements contained in C are also in B, the two data generation times, or growth rates of dominant
sets were kept separate for our new analyses organisms. For example, Giller et al. (2004) sug-
because of the different ways in which biodiversity gested that biodiversity–ecosystem functioning
effects were initially extracted or calculated. relationships differ between aquatic and terrestrial
We speak of a ‘biodiversity effect’ if a function ecosystems because of more rapid turnover of
varies among different levels of biodiversity. Because material and individuals in aquatic systems. How-
different levels of biodiversity can be ordered from ever, despite the often expressed concern that
16 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

extrapolation from one ecosystem type to another is ness manipulations than rates (or depletion of
unwarranted (Hooper et al. 2005, Balvanera et al. resources). However, as with differences between
2006), we were unable to find specific predictions ecosystem types, it is difficult to predict the direc-
about the direction of differences in biodiversity tion of the differences. Using the argument made
effects between ecosystem types. above that, for example, community size (as a
We distinguish between population-level func- measure of standing stock) may have upper limits
tions, recorded for individual target species, such due to the total availability of resources in the
as density, cover or biomass; community-level environment, whereas rates of change in commu-
functions, recorded for multi-species assemblages, nity size should not be restricted in this way, it
such as density, biomass, consumption, diversity; follows that rates should be affected more strongly
and ecosystem-level functions, which could not be than stocks. This argument is used by researchers
assigned to population- or community-level and who claim that plant species richness may well
included abiotic components such as nutrients, increase plant productivity but not carbon storage
water or CO2/O2. Our second hypothesis then is (see e.g. Körner 2004). On the other hand, the the-
that species richness enhances community (and ory developed by Michel Loreau (personal com-
ecosystem) responses but affects population munication) predicts that stocks should be more
responses negatively (Balvanera et al. 2006). responsive than rates.
This follows from basic Lotka–Volterra dynamics Whereas the above hypotheses can already be
(see e.g. Kokkoris et al. 1999, Loreau 2004), and the applied to biodiversity studies focusing on a single
assumption of a maximum community response trophic level, our fourth hypothesis specifically
given by the total availability of resources in the concerns biodiversity effects observed in multi-
environment. Consider for example a system with trophic studies. We consider the effect of changing
s species, where the population growth rate (ri) of biodiversity at one trophic level on functions carried
species i, with carrying capacity Ki in monoculture, out by a different (mostly adjacent) trophic level. If
will be reduced by its own population size (Ni) as the latter is above the manipulated level, we speak of
well as the populations of s–1 competing species bottom-up biodiversity effects; if it is below the
(N1 . . . Ns): manipulated level, we speak of top-down biodiver-
sity effects. Despite some similarities between sys-
ri ¼ ri;max
ðKi  Ni  a1;i
N1  a2;i
N2  : : : tems with one versus two trophic levels (Ives et al.
 as;i
Ns Þ/Ki 2005), biodiversity effects may be more difficult to
generalize and predict in multi-trophic systems
Every addition to a community with species i of a because of the many possibilities for positive and
species j with an inter-specific competition coefficient negative feedback (see e.g. Petermann et al. 2008), as
aj,i > 0 will reduce the growth rate ri and thus nega- well as differences between generalist and specialist
tively affect the population size of species i. However, interactions (Petchey et al. 2004a, Thébault and
if aj,i < 1 > ai,j, the sum of the two species i and j can Loreau 2006, Petchey et al. 2008). Theory and some
produce a larger community size Ni þ Nj than each empirical results suggest that bottom-up effects of
species by itself. That is, if inter-specific competition biodiversity should usually be negative because
coefficients are generally smaller than 1, the com- higher diversity increases resistance to disease and
munity size can increase with increasing species predation (Koricheva et al. 2000, Loreau 2001, Fox
richness according to Lotka–Volterra dynamics. 2004a, Petchey et al. 2004a, Keesing et al. 2006, Duffy
Hypothetically, with increasing species richness, total et al. 2007). However, some empirical results suggest
community responses can be summed over more opposite trends (e.g. Koricheva et al. 2000, Pfisterer
populations, but individual populations will each be et al. 2003, Gamfeldt et al. 2005). Top-down biodi-
under increasing pressure (McGrady-Steed and versity effects should also be negative because a
Morin 2000, Brown et al. 2001, Bunker et al. 2005). more diverse community at trophic level t should be
Our third hypothesis predicts that standing able to deplete the community at trophic level t – 1
stocks should respond differently to species rich- more completely, thus reducing functions such as
 CONSEQUENCES OF SPECIES LOSS FOR ECOSYSTEM FUNCTIONING 17

standing stock at the this lower trophic level (Fox biodiversity and response functions. Using a survey,
2004b, Petchey et al. 2004a, Fox 2005a, Duffy et al. Schläpfer et al. (1999) canvassed expert opinions as
2007). This leaves positive effects of biodiversity for to whether the relationship was either constant (i.e.
within-trophic level (a large number of studies sur- no relationship), idiosyncratic, linear, non-linear
veyed in the two meta-analyses) and for symbiont (logistic, optimum), log-linear, or asymptotic.
relationships. However, these patterns may differ The simplest hypothesis about the shape of
between green (living plant-based) and brown biodiversity–ecosystem functioning relationships
(detrital-based) food webs. A recent meta-analysis of is that of a constant response for all species rich-
top-down and bottom-up effects in detrital food ness levels, either including or excluding a species
webs (Srivastava et al., 2009) showed that detrital richness level of zero. However, including zero
processing (top-down effects) was increased by high species provides a stricter hypothesis that has
detritivore diversity, but showed variable responses almost never been tested empirically (in most
to detrital diversity (bottom-up effects). experiments the zero-richness level was not
Finally, positive effects may also be expected if included) and will therefore not be discussed fur-
the trophic distance between the level at which ther. A problem with the hypothesis of constant
biodiversity is varied and the level at which the response is that it cannot be tested for statistical
response is measured is two or a multiple of two significance.
(e.g. top-down from secondary consumers at level The experts in Schläpfer et al. (1999) predicted
t to primary producers at level t – 2, or, conversely, log-linear or saturating shapes for relationships
from trophic levels t to t þ 2), because two nega- between biodiversity and primary production,
tive interactions can together lead to a positive nutrient cycling, or water cycling. Such shapes are
one. Such effects are implicit in the Hairston– also predicted by niche theory, which assumes
Smith–Slobodkin (1960) hypothesis and can be seen complementarity in resource use among species,
in some of the output from simulation models but increasing niche overlap with increasing species
(Petchey et al. 2004a). In the previous meta-analysis richness (Tilman 1997, Loreau 1998a, Schmid et al.
of Balvanera et al. (2006), however, we observed 2002b). Linear, logistic, or even exponential rela-
that biodiversity effects tend to get weaker the tionships may be expected between biodiversity
greater the trophic distance is between the level at and bioregulation (e.g. biocontrol or resistance to
which diversity is manipulated and the level at the spread of disease), if interactions among species
which a function is measured. are highly specialized (Stephan et al. 2000, cf. gene-
Our fifth and final hypothesis considers the for-gene interactions in host–parasite systems).
premise that if increasing species richness of a com- Indeed, about half of the experts in the survey of
munity increases total resource and space use, then Schläpfer et al. (1999) predicted an exponential or
less of the resource or space should be available to logistic shape for relationships between biodiversity
potential invaders unless they are competitive domi- and bioregulation.
nants that displace the existing native species. That is, In the last part of our analyses, we ask, if a
if the number of species that can fit in the community function asymptotes at high diversity, how many
depends on the ‘niche dimensionality’ of the envi- species are required for a 50 per cent of the maxi-
ronment (Harpole and Tilman 2007), then the more mum function. If the biodiversity–function rela-
species that are already there in a community, the tionship is log-linear, we ask how much a 50 per
more difficult it will be for further species to success- cent or 75 per cent reduction in species richness
fully colonize (Fargione et al. 2003, Mwangi et al. 2007). changes the function.

2.1.4 Shape of the biodiversity–ecosystem 2.1.5 Methods of analysis

functioning relationship
Our new analyses of the influence of explanatory
In the second part of the analyses, we focus on terms on both the variation and shape of biodi-
the expected shape of the relationship between versity effects were based on the data descriptions
18 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

and methods presented in B and C. For B, we Study site and publication were used as random
added data on the significance, direction, and shape terms. Latitude and longitude were tested against
of biodiversity effects to the correlation coefficients site as an error term. Explanatory terms which
used in the original analysis. We distinguished varied within sites (but not within publications)
the following shapes of biodiversity effects in B: were tested against publication as an error term (as
negative, negative linear, negative log-linear, in B and C). To avoid problems of confounding and
no relationship, positive, positive linear, positive correlated responses, all explanatory terms were
log-linear, positive but not linear, and none of fitted both individually and in a combined analysis.
these conditions. For C, we calculated correlation Only if a fixed term was significant in both cases
coefficients after fitting log-linear relationships, (comparing the likelihood of a model with and
excluding studies with only two species richness without the term) was it retained for further anal-
levels (where correlation coefficients can only be 1 ysis. With these stringent rules, we tried to ensure
or –1). Furthermore, we used log-linear fits because that hypothesis tests were robust across an entire
these were often also used in the original papers. To data set and not due to influences of correlated
assess the shape of biodiversity effects in C, we fitted variation in other factors. Interactions between
linear, log-linear, and saturating (Michaelis–Menten) explanatory terms were also tested, but were sel-
curves. dom retained in the model under the stringent rules
In B, we used three different measures of the rela- mentioned above.
tionship between biodiversity and response Logistic mixed models were used to analyze dif-
to analyze differences in biodiversity effects: (1) cor- ferences in significances (probability of observing
relation coefficients (r) standardized to Zr values, (2) significant biodiversity effects) and signs (probability
significances (0 for relationships with P  0.05, 1 for of observing a significant positive biodiversity effect
relationships with P < 0.05), and (3) signs (–/þ, only among the significant effects) in relationships
significant relationships). In C, we used only corre- between biodiversity and response in B. Significance
lation coefficients standardized to Zr values in the corresponds to the finding that a standardized cor-
analysis. Correlation coefficients were converted into relation coefficient is significantly different from
Zr values to improve normality (correlation coeffi- zero. Even if information about the correlation
cients are bound between –1 and 1 and thus not coefficient was not available, the direction of the
normally distributed). The formula for the conversion effect could be extracted from the original publica-
is (Rosenberg et al. 2000): tions, and therefore positive versus negative signifi-
cance could be distinguished. To avoid overrating


Zr ¼ 0:5 ln ð 1 þ rÞ=ð 1  rÞ : studies with small sample sizes in the logistic mod-
els, the number of experimental units per study
The number of plots, N, used for the determination divided by the mean number of experimental units
of each single biodiversity effect in the original across all studies was used as a weighting variable
publications, corrected by the degree of freedom, for each data point. To test the five hypotheses,
was used as weighting variable in B (note that n, as we used ratios of mean deviances as approximate
opposed to N, will be used later to refer to the F-values (McCullagh and Nelder 1989). This
number of effects rather than the number of allowed us to use publication as the appropriate
plots used to calculate a single effect). Because the error term for corresponding fixed terms that did
correlation coefficients in C were calculated from the not vary within publications.
means at each level of species richness, Zr values All presented means of Zr values, percentages of
were weighted by the number of species richness significant biodiversity effects or percentages of
levels used in fitting the relationship. In both B and positive directions among significant biodiversity
C, analyses with unweighted Zr values yielded effects, are weighted means using the weighting
similar results and are therefore not presented. variables mentioned above. Values and significance
We used linear mixed-model analyses to test the levels that are not presented in figures or tables are
influence of explanatory terms on the Zr values. given in the text.
 CONSEQUENCES OF SPECIES LOSS FOR ECOSYSTEM FUNCTIONING 19

2.2 Hypotheses to explain variation explanatory terms than the larger meta-data set B,
in biodiversity effects only one fixed term was retained in the model. In B,
terms for finer categories of responses were fitted to
Before the detailed presentation of the results, an
reduce the amount of unexplained variance
overview of the analyses, including all the explan-
(residual).
atory terms discussed below, is provided (Table
2.1). This table first lists the fixed terms in
the different models (generally in descending order 2.2.1 Distribution of studies
of F-values) followed by the random terms. In the The reported biodiversity effects came from more
analysis of meta-data set C, which contained more than 100 independent experiments, mainly carried
homogeneous data and thus fewer candidate out in North America and Europe (Fig. 2.1).

Table 2.1 Multivariate mixed-model analyses for (a) data in B (cf. Balvanera et al. 2006) and (b) data in C (cf. Cardinale et al. 2006a).

Source of variation Degree of freedom % var. explained F-ratio P

(a)
Proportion of significant effects
Responses of communities 6¼ ecosystems 6¼ populations (see 2.2.3) 2 5.4 31.5 < 0.001
Responses vary among ecosystem types (see 2.2.2) 7 8.5 6.4 < 0.001
Responses of residents > invaders (see 2.2.6) 1 0.5 6.0 0.015
Responses vary among response groups 27 4.7 2.0 0.002
Responses vary among study sites (random term) 92 22.4 1.3 0.189
Responses vary among publications (random term) 41 7.4 2.2 < 0.001
Residual 595 51.1
Proportion of positive within significant effects
Responses of residents > invaders (see 2.2.6) 1 11.0 145.7 < 0.001
Responses of stocks 6¼ rates (see 2.2.4) 1 5.3 70.6 < 0.001
Responses of communities 6¼ ecosystems 6¼ populations (see 2.2.3) 2 5.9 39.1 < 0.001
Top-down and bottom-up responses 6¼ others (see 2.2.5) 5 4.7 12.3 < 0.001
Responses vary among ecosystem types (see 2.2.2) 7 12.1 5.3 < 0.001
Responses vary among response groups 24 8.5 4.7 < 0.001
Responses vary among study sites (random term) 81 17.7 0.7 0.936
Responses vary among publications (random term) 40 12.9 4.3 < 0.001
Residual 291 21.9
Zr-values
Responses of communities 6¼ ecosystems 6¼ populations (see 2.2.3) 2 18.6 88.9 < 0.001
Responses of residents > invaders (see 2.2.6) 1 4.2 40.4 < 0.001
Responses decrease with cos(latitude) 1 2.5 11.6 0.001
Responses of stocks 6¼ rates (see 2.2.4) 2 3.3 15.8 < 0.001
Responses vary among ecosystem types (see 2.2.2) 7 12.9 6.6 < 0.001
Top-down and bottom-up responses 6¼ others (see 2.2.5) 5 1.2 2.3 0.042
Responses vary among response groups 24 4.1 1.7 0.031
Responses vary among study sites (random term) 63 13.3 0.8 0.834
Responses vary among publications (random term) 30 8.4 2.7 < 0.001
Residual 302 31.5
(b)
Zr-values
Responses of stocks 6¼ resource depletion (see 2.2.4) 1 4.2 9.5 0.003
Responses vary among publications (random term) 43 67.8 3.6 < 0.001
Residual 63 28.0
20 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

(a)

⫺2.8 – ⫺1.5
⫺1.5 – 0
0 – 1.5
1.5 – 2.4

(b)

⫺2 – ⫺11
⫺1 – 0
0–1
1–2
2–4
4–6
6–8

Figure 2.1 Geographical distribution of studies in B from which standardized correlation coefficients (Zr) between biodiversity and response variables could be
extracted (see Balvanera et al. 2006). The size of the symbols is proportional to Zr.
symbols indicate positive, · symbols negative biodiversity effects.
(b) Geographical distribution of studies in C from which log-ratios of responses at highest species richness and responses of average monocultures could be extracted
(measure ‘LLR1’ in Cardinale et al. 2006). The size of the symbols is proportional to LLR1.
symbols indicate positive, · symbols negative biodiversity effects.

Interestingly, Zr values declined significantly with more contrasting conditions. To what extent the
increasing cosine of latitude in the larger data set B difference in Zr values between European and
(Table 2.1(a)). However, this trend was largely North American studies may be confounded by
explained by higher values in Europe (n ¼ 187, researcher preferences remains unknown.
mean Zr ¼ 0.26) relative to those from North A larger number of biodiversity effects are docu-
America (n ¼ 234, mean Zr ¼ –0.6), with the latter mented for terrestrial studies than are documented
representing lower latitudes (higher cosines). Bio- for aquatic studies (Table 2.2(a)). Of the terrestrial
diversity effects did not vary across altitudes of fraction, a large number of the biodiversity effects
study sites, but most of these were located < 500 m reported are from studies carried out in grassland
above sea level. The geographical distribution of ecosystems (60 per cent in B and 45 per cent in C). It
studies indicates a strong bias towards locations is therefore not surprising that a large number of
where the major funding is, rather than where the biodiversity effects are reported from studies
science is most warranted (see Chapter 3). Experi- manipulating plant diversity, with detritivores plus
ments undertaken in the tropics (e.g. Potvin and mycorrhizae coming second, herbivores third, and
Gotelli 2008) and at high latitudes are urgently carnivores fourth (Table 2.2(a)). In B, 154 of all bio-
needed to further test biodiversity effects under diversity effects could be classified as an ecosystem
 CONSEQUENCES OF SPECIES LOSS FOR ECOSYSTEM FUNCTIONING 21

Table 2.2 (a) Number of studies in which different trophic groups have been manipulated in aquatic and terrestrial ecosystems and (b) number of studies in
which different trophic groups have been manipulated and stocks or rates/depletion of resources have been measured.

Consumers Detritivores Herbivores Plants Multitrophic Total

or mycorrhizae manipulations

(a)
Database B (cf. Balvanera et al. 2006)
Aquatic 3 12 41 54 40 150
Terrestrial 4 87 5 510 15 621
Total 7 99 46 564 55 771
Database C (cf. Cardinale et al. 2006)
Aquatic 17 22 21 13 73
Terrestrial 8 12 3 51 74
Total 25 34 24 64 147
(b)
Database B (cf. Balvanera et al. 2006)
Stocks 4 67 32 415 33 551
Rates 3 32 14 147 22 218
Unclassified 0 0 0 2 0 2
Total 7 99 46 564 55 771
Database C (cf. Cardinale et al. 2006)
Stocks 19 28 10 14 76
Depletion of resources 6 6 14 50 71
Total 25 34 24 64 147

response, 434 as a community response and 183 as a larly across both stocks (n ¼ 99, 11, 66, 321, 40, 14,
population response. Ecosystem service groups respectively) and rates (n ¼ 86, 6, 30, 83, 5, 8,
covered in B included 251 biodiversity effects on respectively). However, there were only a few rela-
primary production (including abundance and tions that could be classified as top-down biodiver-
standing biomass), 254 on bioregulation, 195 on soil sity effects (category ‘below’, n ¼ 17). Among
fertility, 46 on nutrient and water cycling, and 10 on the bottom-up biodiversity effects (category ‘above’,
climate regulation. n ¼ 185), about a third were cases where detrital
The majority of biodiversity effects concerned diversity of primary producers was manipulated
responses of standing stock, but a considerable and decomposer functions were measured (n ¼ 65).
number was also related to rates (in B) or resource
depletion (in C; Table 2.2(b)). Resource depletion in
C was measured as (1) instantaneous rate (n ¼ 5) or 2.2.2 Biodiversity effects vary among
as a reduction in resource compared with (2) control ecosystem types (hypothesis 1, Table 2.3)
without species (n ¼ 44, or n ¼ 28 for experiments In both B and C biodiversity effects came mainly
that lasted less than one generation time) or (3) the from four broadly defined ecosystem types:
beginning of the experiment (n ¼ 21, or n ¼ 13 for grassland, fresh-water, marine, and forest. Note
experiments that lasted less than one generation that the breadth of definition is narrower for those
time); one value was not classified. In B, relation- ecosystem types in which a larger number of
ships between the trophic level at which species studies have been carried out (grassland) than in
richness was manipulated and the one at which a those with fewer studies (aquatic marine).
response was measured (above, below, ecosystem, The remaining biodiversity effects were repre-
same, symbiont, within [multitrophic diversity sented by approximately the same number of
manipulations]) were distributed more or less regu- other ecosystem types (bacterial microcosm, crop/
22 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Table 2.3 Tests of hypotheses about variation in biodiversity effects (see Sections 2.1.3 and 2.1.5). ‘Cardinale’ and ‘Balvanera’ refer to data in C
(cf. Cardinale et al. 2006a) and in B (cf. Balvanera et al. 2006), respectively.

Number Hypothesis Cardinale Balvanera Balvanera Balvanera

Zr (n ¼ 108) Zr (n  449) P (sign.)(n  766) P (pos. sign.)(n  766)

1 Biodiversity effects vary among ecosystem types no (P > 0.1) yes (P < 0.001) yes (P < 0.001) yes (P < 0.001)
2 Biodiversity effects differ between – yes (P < 0.001) yes (P < 0.001) yes (P < 0.001)
ecosystem, community and
population level
3 Biodiversity effects differ between yes (P ¼ 0.003) yes (P < 0.001) yes (P < 0.001) yes (P < 0.001)
stocks and rates or depletion of resources
4 Biodiversity effects depend on trophic – yes (P < 0.001) yes (P < 0.001) yes (P ¼ 0.035)
relationships (confounded
with above)
5 Biodiversity affects residents and – yes (P < 0.001) yes (P ¼ 0.004) yes (P < 0.001)
invaders differently

successional, ruderal/salt marsh, soil community). the biodiversity effects on community-level responses
Zr values varied significantly between ecosystem (Fig. 2.2(a)). This suggests a more direct mechanistic
types in B, but not in C (Table 2.3). When tested, link in the latter case. In the meta-analysis of B, the
the significance remained when ecosystem service difference among ecosystem-, community-, and pop-
groups (refer to previous paragraph) or finer cat- ulation-level responses was identified as the strongest
egories of responses (see Table 2.1(a)) were fit explanatory factor for variation in biodiversity effects.
before ecosystem type in the analyses. However, In the new analysis presented here, this is true for both
because the significant variation in B was, at Zr values and significances (Table 2.3, Fig. 2.2(a)). The
least partly, due to stronger biodiversity effects result remained highly significant (F2,209 ¼ 82.5, P <
in the ecosystem types with lower values of n 0.001; mixed model with site and publication as ran-
(see B), it is too early to draw any general con- dom terms) even if only significant Zr values were
clusions. More importantly, there was no overall analyzed (n ¼ 307).
tendency in any of the analyses for biodiversity
effects to be more (or less) frequently positive
2.2.4 Biodiversity effects differ between
(or more or less often significant) in terrestrial
stocks and rates (or depletion of resources)
systems than it was for aquatic ecosystems.
(hypothesis 3, Table 2.3)
This supports the view that similar mechanistic
processes underpin the biodiversity–ecosystem In B, biodiversity effects on stocks and rates were
functioning relationship under terrestrial and distinguished: stocks referred to levels of an eco-
aquatic conditions. system property (e.g. standing biomass) whilst
rates referred to changes in such levels over time. In
C, biodiversity effects on stocks and depletion of
2.2.3 Biodiversity effects differ among
resources were distinguished: stocks referred to
ecosystem, community, and population levels
levels of an ecosystem property only at a focal
(hypothesis 2, Table 2.3)
trophic group (see Table 2.2(b)) whilst depletion
Our results strongly suggest that while increasing referred to direct rates of resource depletion, or to
species richness often enhances the performance of differences between the consumed and uncon-
entire communities, it also often reduces the average sumed resource levels at a trophic group below the
contributions of individual species. Biodiversity focal one (see Section 2.2.1). In the following test of
effects on ecosystem-level (abiotic) responses also our third hypothesis, we treat resource depletion as
tend to be positive, but not as much and not as often as equivalent to rates.
 CONSEQUENCES OF SPECIES LOSS FOR ECOSYSTEM FUNCTIONING 23

(a) (b)
1.0 0.6

235
0.4

Zr values (mean ± 1 S.E.)

0.8
434 320
64 551
183 0.2
Probability

0.6
218
128 0
0.4 154 150
–0.2

0.2 –0.4

0.0 –0.6
Community Ecosystem Population Stock Rate
responses responses responses responses responses

(c) (d)
1.0 0.6
9 12
163 0.4

Zr values (mean ± 1 S.E.)

0.8 22
404 314
44 237 37 27
17 0.2
Probability

0.6 112
302
185 45
220 0
10
98
0.4
–0.2

0.2 –0.4

0.0 –0.6
Bottom- Top- Eco- Within- Sym- Resp. to 0-link 1-link 2-link
up down system trophic biont multi- resp. resp. resp
resp. resp. resp. level resp. trophic
resp. manip.

Figure 2.2 Probability (left y-axis) of observing significant responses to biodiversity (height of shaded plus unshaded column) and proportion of
positive responses among them (height of shaded column relative to height of shaded plus unshaded column). If the shaded bar is shorter than the
unshaded bar, then significant biodiversity effects have a greater probability to be negative than positive. The average Zr value (± 1 standard error) is
also shown for each category (axis on the right). The number of measured responses in each group is listed. Response categories for test of (a)
hypothesis 2 (Section 2.2.3), (b) hypothesis 3 (Section 2.2.4), (c) hypothesis 4 (Section 2.2.5) and (d) a corollary to hypothesis 4. Data from meta-data set
B (Balvanera et al. 2006).

In B, we found more significant and more pos- A similar result was found in C, where Zr values
itive effects of species richness on stocks than we for stocks (mean Zr ¼ 1.53) were significantly (F1,63
did on rates (Table 2.3, Fig. 2.2(b)). Overall, 55 per ¼ 9.52, P < 0.01; mixed model with publication as
cent of the significant biodiversity effects on rates random term) larger than Zr values for depletion
were negative, as were the average Zr values for of resources (mean Zr ¼ 1.01). If those depletion
those rates. For example, resource extraction from measures which were taken after a time interval of
primary producers (disease severity, consumed a generation or more were excluded (see Section
biomass) usually declined with increasing plant 2.2.1), then the difference between Zr values for
species richness. These results were robust to stocks and depletion of resources (mean Zr ¼ 0.82)
changes in fitting sequence of other hypotheses. became even larger (F1,49 ¼ 13.48, P < 0.001; mixed
24 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

model with publication as random term). The Zr and F2,293 ¼ 44.9/P < 0.001 for differences in Zr
values were higher in C than in B. This was values). This result is consistent with our hypoth-
probably due to two differences between the esis that two negative effects between adjacent
analyses: in B, Zr values were averaged over a trophic groups should, on balance, multiply to
more heterogeneous set of responses, whilst in C, a positive effect between groups at a trophic dis-
Zr values were calculated from means at each tance of two.
species richness level, thereby excluding variation
around means. When compared to stocks, the
2.2.6 Biodiversity affects residents and
significantly lower Zr values for depletion of
invaders differently (hypothesis 5, Table 2.3)
resources in C may in part be due to a difference in
trophic distance: stocks in C were measured at the In B, 93 of the 771 biodiversity effects concerned
trophic level where diversity was manipulated and the response of invaders to the species richness of
there was depletion of resources at the trophic the residents in a community. Of these, 76 per cent
level below (see hypothesis 4). were significant biodiversity effects. The vast
majority (89 per cent) of the significant biodiver-
sity effects were negative, as were the average
2.2.5 Biodiversity effects depend on trophic
Zr values. That is, invader functions were reduced
relationships (hypothesis 4, Table 2.3)
at higher biodiversity of residents, corresponding
Our findings support the predictions that top-down to an increased invasion resistance of more
biodiversity effects should be negative (i.e. increased diverse resident communities. This contrasts with
diversity at one trophic level reduces the function 59 per cent significant biodiversity effects on
performed by the trophic level below) and biodi- responses of residents, of which only 31 per cent
versity effects within trophic levels, and for symbi- were negative (Fig. 2d). These results demonstrate
ont relationships, should be positive (Table 2.3; Fig. that one of the most general effects of high biodi-
2.2(c)). Bottom-up biodiversity effects (i.e. increased versity is increased invasion resistance (Knops
diversity at one trophic level changes the function et al. 1999, Hector et al. 2001, van Ruijven et al.
performed by the trophic level above) were on 2003, Fargione and Tilman 2005, Spehn et al. 2005,
average close to zero, although we had expected Mwangi et al. 2007), thereby corroborating our
them to be negative. This was due to the fact that fifth hypothesis.
bottom-up biodiversity effects on functions mea-
sured for detritivores were generally positive (28 out
of 36 significant effects), whereas other bottom-up 2.3 Hypotheses about the shape of
biodiversity effects were more often negative (37 out the relationship between biodiversity
of 58 significant effects) than positive. Analysis of a and responses (Table 2.4)
larger dataset found equal numbers of positive and The first five hypotheses in Table 2.4 specify alter-
negative bottom-up biodiversity effects of detrital native shapes of biodiversity effects found in the
diversity on functions measured for detritivores previous meta-analyses and expected by experts
(Srivastava et al. 2009). (Schläpfer et al. 1999).
When we analyzed differences among responses
at increasing trophic distance (t ± 0 < t ± 1 < t ± 2)
to the level whose biodiversity was manipulated, 2.3.1 Alternative shapes of biodiversity effects
we found that effects within trophic levels and at a Four out of 23 experts predicted that the general
trophic distance of two were positive (higher shape of biodiversity effects would be a horizontal
function values at higher biodiversity levels), in line in Schläpfer et al. (1999). Out of the 771 biodi-
contrast to those at a distance of one (Fig. 2.2(d); versity effects assembled in B, 286 (37 per cent) could
F2,504 ¼ 13.4/P < 0.001 for differences in frequency not be assigned a specific shape and were therefore
of significant effects, F2,271 ¼ 63.7/P < 0.001 considered as horizontal. Although none of the
for differences in frequency of positive effects, experts predicted the linear relationship as a general
 CONSEQUENCES OF SPECIES LOSS FOR ECOSYSTEM FUNCTIONING 25

Table 2.4 Tests of hypotheses and questions about the shape of biodiversity effects. ‘Schläpfer’, ‘Cardinale’, and ‘Balvanera’ refer to data in Schläpfer et al.
(1999), in C (cf. Cardinale et al. 2006a), and in B (cf. Balvanera et al. 2006), respectively.

Number Hypothesis or question Schläpfer experts (n < 38) Cardinale (n  108) Balvanera (n  771)

1 Biodiversity effects have no 4 of 23 experts – 286 of 771 cases

discernible shape
2 Biodiversity effects are linear 0 of 23 experts 34 of 108 cases 164 of 771 cases
3 Biodiversity effects have a discernible 18 of 23 experts 74 of 108 cases 321 of 771 cases
shape but are not linear
4 Biodiversity effects are log-linear 25 of 108 cases 101 of 771 cases
15 of 22 experts
5 Biodiversity effects saturate 49 of 108 cases –
6 Shape of biodiversity effects on 17 log-lin./sat., 8 no rel., 17 saturating, 90 no/idios., 81 other,
primary production (incl. biomass, 3 lin., 3 logist., 1 optimum 15 log-linear, 46 log-linear, 34 linear
abundance) 11 linear
7 Shape of biodiversity effects on 16 log-lin./sat., 8 no rel., – 18 other, 15 no/idios.,
nutrient and water cycling 4 logist., 2 lin., 1 optimum 11 linear, 2 log-linear
8 Shape of biodiversity effects on responses 15 logist./expon., – 83 linear, 72 no/idios.,
related to bioregulation 10 log-lin./sat., 4 lin. 60 other, 39 log-linear
9 Number of species required for 5–6 1.2 –
50% response (positive,
saturating relationship)
10 Reduction in response with ca. 30% 10.90% –
reduction from 16 ! 8 species
(positive, log-linear relationship)

shape for biodiversity effects, the linear function rating curve was the best fitting in 49 studies
actually did fit best in 34 out of 108 cases (32 per (Table 2.4). However, the log-linear was the worst-
cent) in C; and it was observed in 164 out of 771 fitting relationship in only seven cases, compared
cases (21 per cent) in B (Table 2.4). Where the with 66 for the linear and 35 for the saturating
highest species richness was < 10, linear relation- relationship. Thus the log-linear relationship has
ships were observed in 27 per cent and 40 per cent an intermediate position: it crudely fits a large
of the studies in B and C, respectively. Among number of biodiversity effects. This may reflect a
studies in which the highest species richness was  mixture of operating mechanisms, including com-
10, 19 per cent in B and 28 per cent in C were linear. plementarity and selection effects (Schmid et al.
The majority of biodiversity effects that were 2002b). Nevertheless, most theoretical models (see
assigned a shape, however, were not linear, e.g. Tilman et al. 1997c, Loreau 1998a, Cardinale
reflecting the predictions of the majority (78 per et al. 2004) show that biodiversity effects should
cent) of experts and consistent with theoretical saturate, at least at high levels of species
expectations (Section 2.1.4; see also Chapter 8). richness, which are seldom ascertained in experi-
Experts and authors of the publications used in B mental studies. It should be noted that R2 values
did not distinguish between non-linear curves that and vote counting are very crude measures for
do (Michaelis–Menten) or do not saturate (log- distinguishing between functions of different
linear). In C, however, this distinction could shape.
be made and showed that the average R2 value
was 0.690 and 0.682 for the saturating Michaelis–
2.3.2 Shapes of biodiversity effects differ
Menten and log-linear relationship, respectively.
between major response categories
Furthermore, if the linear relationship was
included in the comparison, the log-linear was the Whilst the previous section focused on the general
best fitting in only 25 studies, whereas the satu- shape of all analyzed biodiversity effects, the
26 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

following section will investigate differences in the response for the species richness level of zero, which
shapes of biodiversity effects between studies. In is not always appropriate, as for example in the case
particular, we want to test the hypothesis that of evapotranspiration of an ecosystem. We think a
biodiversity effects on primary production and more interesting question is how many species does
nutrient and water cycling are log-linear (or satu- one need relative to a one-species monoculture to
rating), whereas those on bioregulation are more obtain some percentage of maximal function.
often linear or logistic. The data in B and C pro- When experts were asked to predict the con-
vide some support for these hypotheses (6–8 in sequences of a 50 per cent species loss from 16 to 8
Table 2.4). A large number of observed effects of species, they overestimated the reduction in the
plant diversity on primary production, or respon- response by a factor of three under the assumption of
ses related to it, including all types of abundance a positive, log-linear relationship (Table 2.4). The
measures, were log-linear or saturating, whereas empirical log-linear results from C suggest that, with
the few examples for responses related to nutrient each halving of species richness, the response would
and water cycling did not reveal any clear pattern be reduced by about 11 per cent of the 16-species
(Table 2.4). Responses related to bioregulation in B richness level. Reduction in the number of species
showed the lowest proportion of log-linear rela- from 16 to 1 species would involve four halving
tionships and the highest proportion of linear events, corresponding to a reduction by about 44 per
ones. This is broadly consistent with the hypoth- cent. Similarly, if we assume a saturating Michaelis–
esis and the expectation of the experts (Schläpfer Menten relationship the average reduction in C
et al. 1999), who predicted the smallest amount of from 16 to 8 species would be 5.2 per cent and from 16
log-linear biodiversity effects or, in other words, to 1 species would be 38.8 per cent. Comparing
redundancy for these responses. Despite the large the expert predictions for the reduction from 16 to 8
body of literature on biocontrol there is, to our (30 per cent) and from 16 to 4 (40 per cent; see
knowledge, no general theory about how the Schläpfer et al. 1999) suggests that the experts
diversity of hosts should be related to diversity of assumed a linear relationship between species rich-
enemies. This is the case even though empirical ness and response, even though they selected a
work on quantitative interaction webs across weaker relationship more often (see Section 2.3.1).
varying diversity levels has been done (e.g.
Albrecht et al. 2007) and the importance of distin-
2.4 What have we learned from
guishing between interactions with generalists
biodiversity manipulation experiments?
versus specialists has been demonstrated in models
of multitrophic diversity manipulations (Petchey The joint interpretation of results from of the new
et al. 2004a, Thébault and Loreau 2005). analyses of the two meta-data sets of B and C
demonstrates that, despite the large heterogeneity of
data, biodiversity effects are a general feature of most
2.3.3 Consequences of observed shapes biological systems. Recent discussions have focused
of biodiversity effects on the details of experimental design and analyses, as
Under the assumption of a positive, saturating rela- well as the mechanisms underpinning biodiversity
tionship, the experts in Schläpfer et al. (1999) greatly effects (see e.g. Cardinale et al. 2007). It is gratifying to
overestimated the number of species required to see that these issues could not mask the influence and
reach 50 per cent of the maximum response. importance of major biological factors in explaining
The average estimate was between 5–6 species the variation in biodiversity effects.
(Schläpfer et al. 1999), whereas analysis of the data in
C suggested that an average of only 1.2 species are 2.4.1 Hypotheses to explain variation
needed (Table 2.4). This result suggests that the in biodiversity effects
presence of a single species results in almost half of
the response. However, one limitation of fitting The major biological factors used in the analyses
Michaelis–Menten curves is that they assume a zero presented in Table 2.1 involve multilevel factors
 CONSEQUENCES OF SPECIES LOSS FOR ECOSYSTEM FUNCTIONING 27

such as different ecosystem types or types of Our third hypothesis was that biodiversity
response variables (i.e. response groups), where we effects on stocks might differ from biodiversity
could only state the existence of significant varia- effects on rates, but we could not predict the
tion, and factors, with few well-interpretable levels direction of the difference (Section 2.2.4). Never-
and contrasts between these levels. We tested five theless, we clearly showed that there were differ-
hypotheses regarding the influence of these bio- ences between stocks and rates and that, in fact,
logical factors on the strength and direction of biodiversity influenced stocks more strongly and
biodiversity effects (see Table 2.3). The first more positively than rates (or depletions of
hypothesis that biodiversity effects vary between resources). This result was consistent in both
ecosystem types and therefore restrict the potential analyses of the B and C meta-data sets, despite
for generalizations from one ecosystem to another, some differences between the two. In C, stocks
was confirmed (Section 2.2.2). However, the sur- were measured directly in the diversity-manipu-
prising (cf. Giller et al. 2004) similarity of responses lated group, whereas depletions of resources were
between terrestrial and aquatic ecosystems (and measured at the trophic level below. In B, stocks
among the ecosystem types studied most often) and rates were measured at the same or at differ-
shows that there are very likely to be common ent trophic levels above or below the one manip-
processes and patterns operating among different ulated. Our results are still difficult to understand,
ecosystems. but we can at least conclude that the assumption
The second hypothesis, that an increasing that rates or depletion of resources should be more
diversity of species positively affects responses at responsive to biodiversity than stocks is wrong.
the community (and ecosystem) level and nega- This becomes relevant, for example, in the context
tively affects responses at the population level, of rates and stocks in ecosystem carbon cycling
was also confirmed (Section 2.2.3). This supports (Körner 2003, Körner 2004). According to our
predictions from basic Lotka–Volterra theory and results, there is no longer a reason to believe that
arguments about density compensation high biodiversity will simply increase turnover
(McGrady-Steed and Morin 2000). If total resource rates rather than storage.
or energy inputs from the environment fix the The fourth hypothesis predicted that increased
response at community or ecosystem level (see e.g. biodiversity at one trophic level reduces functions
Bunker et al. 2005), and if these inputs are dis- at other trophic levels (negative bottom-up and
tributed among several species, the average top-down biodiversity effects), whereas it increa-
response of species at population level must go ses functions at the same trophic level or for
down as diversity goes up. The evidence for this symbionts (Section 2.2.5). Indeed, these predictions
effect in the current analysis was very strong and were met, with the exception that bottom-up bio-
robust across the large range of biodiversity effects diversity effects (mainly detrital diversity of pri-
in the meta-dataset of B. It would be interesting to mary producers) on detritivore functions were
explore whether a theoretical relationship can be mostly positive. In a new meta-analysis using a
found between positive/negative effects of biodi- larger number of such studies, Srivastava et al.
versity on community/population-level responses, (2009) found equal numbers of positive and neg-
as found here, and the better-known positive/ ative effects of detrital diversity on detritivore
negative effects of biodiversity on temporal var- functions. Although other bottom-up biodiversity
iation in community/population-level responses effects and top-down biodiversity effects were
(May 1974, Tilman 1996, Flynn et al. 2008). mostly negative in the present analysis, this was
The comparatively weak influence of biodiversity not the case when two trophic levels separated the
on ecosystem-level responses may reflect an indi- manipulated and the measured groups. This indi-
rect relationship between biotic components, cates that two negative biodiversity effects
whose biodiversity was manipulated, and abiotic between adjacent trophic levels can multiply to a
components of which functional responses were positive effect between more distant levels. It is
measured. gratifying to see that even for multi-trophic
28 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

biodiversity studies predictions made on theore- resource uptake and conversion are consistent with
tical grounds (e.g. Loreau 2001, Fox 2004a, Fox increasing overlap of resource niches that are
2004b, Fox 2005a, Petchey et al. 2004a, Keesing expected with increasing diversity (Tilman 1997,
et al. 2006, Duffy et al. 2007) are broadly supported Loreau 1998a). Such limitations may not affect
by data, although it is still too early to derive relationships between biodiversity and bioregula-
further generalizations. tion. However, it should be noted that studies of
Our fifth hypothesis, that increasing biodiversity bioregulation tend to manipulate just a few species
should affect the responses of residents positively and across minimal levels of species richness and this
the responses of invaders negatively, was strongly may provide an alternative explanation for the
supported by the data in B and was highly robust differences.
across the span of measurements and ecosystems With the detailed metadata contained in C, it is
(Section 2.2.6). Nevertheless, there has been some possible to calculate how severe reductions of
debate whether this is a general trend or a specific species richness might be in comparison to esti-
feature of experiments (Levine and D’Antonio 1999, mates provided by the experts 10 years ago. When
Fridley et al. 2007). The problem here is that in non- doing so, we were surprised to find that experts
experimental situations it is hard to distinguish assumed that a much larger number of species (5–6)
invaders from residents unless the invasion process is would be needed to maintain responses at half-
directly observed; also, conditions that favour diver- saturation level than the empirical investigations
sity in general cannot be dissected from those that estimate. The empirical estimates suggest that the
promote invaders in particular (Espinosa-García et al. average monoculture should already reach the half-
2004). Nevertheless, niche theory predicts a lowered saturation level. Similarly, in comparison to
availability of free niche space with increased species empirical findings, experts overestimated the con-
richness (Fargione et al. 2003, Harpole and Tilman sequences of halving species richness by a factor of
2007, Mwangi et al. 2007), as well as the results from three. This suggests that experts often do not think
the experiments presented here, both of which are about the difference between systems with no
consistent with positive biodiversity effects on inva- species and a system with a single species, perhaps
sion resistance. because experts do not consider it meaningful to
measure ecosystem properties at a species richness
level of zero.
2.4.2 Alternative shapes of biodiversity effects
At this juncture, one fundamentally important
Although a large number of biodiversity effects caveat should be considered. As Hector and Bagchi
have the shape of a log-linear or a saturating curve, (2007) have shown, it is likely that more than one
these shapes are by no means the only ones (e.g. species will be needed to maintain multiple
Chapter 1) – especially if responses related to responses at half-level. Thus it could well turn out
bioregulation are considered (both beneficial and that as the number of responses considered are
detrimental interactions between species whose increased, the number of species needed to main-
diversity was manipulated and those species whose tain multi-response half-levels is also likely to
responses were measured). For the latter, biodi- increase to (or above) an expert-estimated satura-
versity effects often did not diminish or saturate tion of around 5–6 species.
over the range of species richness levels tested. In
contrast, responses related to primary production
2.4.3 Recommendations for the
and nutrient or water cycling did show evidence of
next-generation biodiversity experiments
deceleration or reaching saturation (Section 2.3.2).
This difference between biodiversity effects on It was only possible to review biodiversity effects
bioregulation and biodiversity effects on water or reported until summer 2005. In the meantime, the
element cycling was expected on theoretical number of studies has increased further and new
grounds as well as being predicted by experts meta-analyses could be started. We hope that
(Schläpfer et al. 1999). Saturating relationships for some of the new and future studies will look
 CONSEQUENCES OF SPECIES LOSS FOR ECOSYSTEM FUNCTIONING 29

Table 2.5 Some variables that should be included in publications and more specifically at mechanisms generating bio-
meta-data bases of biodiversity experiments.
diversity effects. If so, future meta-analyses can
Number Variable go beyond the testing of rather phenomenologi-
cal hypotheses and begin to understand mecha-
1 Reference (author and date) nistic processes.
2 Experiment/study identification
We suggest that the old and new data should
3 Locality (logitude, latitude)
be combined in an open-access data table that
4 Level of control (enclosed, field)
would allow continuous monitoring of overall
5 Ecosystem type
6 Cause of diversity gradient
trends and further analysis. Comparing the
7 The species diversity measure used variables used in the two existing databases
8 Type of experiment (substitutive vs. additive) showed that a similar reduced set was indepen-
9 Trophic group for diversity gradient dently derived by the two groups of authors
10 Lowest species richness from a multitude of candidate variables
11 Highest species richness (Table 2.5). Values for this set of variables should
12 Number of species richness levels be reported, if possible, by every new study on
13 Total number of species in pool biodiversity–ecosystem functioning relation-
14 Total number of different species compositions
ships. The latter will require a change in ethos
15 Total number of experimental units (N)
and a willingness to share data both nationally
16 Response measured
and internationally (a trend which is increasing
17 Trophic level of response
18 Mean response
across many disciplines, such as molecular biol-
19 Mean response at lowest richness ogy), but would significantly bolster crosscutting
20 Standard error of mean response at lowest richness analyses aimed at identifying the generalities of
21 Mean response at highest richness biodiversity effects.
22 Standard error of mean response at highest richness
23 Significance level
24 Direction of effect
Acknowledgements
25 Correlation coefficient We thank Michel Loreau, Peter Morin, Shahid
26 Type of correlation coefficient (univariate or multivariate)
Naeem, and an anonymous reviewer for very
27 Shape of functional response to biodiversity
useful comments on the manuscript of this
...
chapter. We thank the Swiss Agency for the
... Further variables indicating additional experimental
treatments
Environment, Forests and Landscape (SAEFL) for
... etc. financial support.
 CHAPTER 3

Biodiversity-ecosystem function
research and biodiversity futures:
early bird catches the worm or a day
late and a dollar short?
Martin Solan, Jasmin A. Godbold, Amy Symstad, Dan F. B. Flynn,
and Daniel E. Bunker

3.1 Introduction Although initial experiments successfully articu-

In the early 1990s, an increasing number of ecolo- lated BEF hypotheses by manipulating biodiversity
gists began to challenge the view that biodiversity under controlled laboratory conditions (for reviews,
was merely an expression of the abiotic conditions see Loreau et al. 2001, Covich et al. 2004, Hooper
of the environment and, instead, started to recog- et al. 2005), critics were quick to assert that labora-
nize that the properties of ecosystems are also tory studies lack realism because they tend to
mediated by the biota (e.g. Lubchenco et al. 1991, include a few ‘non-representative’ taxa, often from
Chapin et al. 1992). Consequently, research foci only one trophic level, and attributes of the system
shifted from elucidating the effects of abiotic con- are measured infrequently and in the absence of the
ditions on biodiversity to investigating biodi- appropriate environmental context. Strong debate
versity’s effects on ecosystem processes (Naeem followed (for summary, see Mooney 2002) over the
et al. 2002). The development of this central tenet applicability of such data to the real world and its
was formalized at a conference held in Bayreuth, capacity to inform policy-relevant issues (Carpenter
Germany in 1991 (Schulze and Mooney 1993) and 1996, Srivastava and Vellend 2005). Further,
led to an extended range of hypotheses (Schläpfer discussion surrounding fundamental differences
and Schmid 1999) that collectively formed a in opinion over experimental methodology (e.g.
framework within which the relationship between Huston 1997, Wardle 1998, Wardle 1999, Doak et al.
biodiversity and ecosystem function (hereafter, 1998) and the emergence of empirical studies
BEF) could be experimentally tested (Schmid et al. that were not consistent with theoretical predictions
2002a, Raffaelli et al. 2003). The emerging BEF ide- (e.g. Wardle et al. 1997a, Gastine et al. 2003) gave
ology received widespread attention and has the impression to the wider ecological community
become one of the central research agendas in that opinion was divided and advice contradictory
contemporary ecology (Loreau et al. 2001, Loreau (Kaiser 2000, Cameron 2002, Schmid 2002); argu-
et al. 2002), spurred by the anticipation that ably what was actually being witnessed was the
anthropogenic global change will dramatically ordinary, albeit rapid, evolution and maturation of
reduce biodiversity in most ecosystems and will a new paradigm (Naeem 2002b). Unlike other eco-
have considerable ecological consequences and logical debates, however, the BEF community
affect human wellbeing within the next century became disproportionately distracted by a minority
(Vitousek et al. 1997, Sala et al. 2000, Diaz et al. 2006, of detractors and went to extraordinary lengths
Fischlin et al. 2007). to defend its position (e.g. Naeem et al. 1999,

30
 BIODIVERSITY-ECOSYSTEM FUNCTION RESEARCH AND BIODIVERSITY FUTURES 31

Srivastava et al. 2004, Bulling et al. 2006, Benton used in the science base almost since its beginning,
et al. 2007), attract and encourage other ecologists the general trend shows a growing appreciation of
(Austin 1999, Emmerson and Huxham 2002, Raffaelli the power of these different approaches to incorpo-
et al. 2003, Prosser et al. 2007), and demonstrate rate more realism. Following Paris, it became clear
reconciliation between opposing camps, most that BEF experiments needed to integrate processes
prominently at a conference entitled ‘Biodiversity that are responsible for the generation, maintenance,
and Ecosystem Functioning: Synthesis and Per- and loss of biodiversity at local and regional scales.
spectives’ held in Paris, France, in 2000 (Hughes The first phase of BEF research had generated the
and Petchey 2001, Loreau et al. 2001, Loreau et al. necessary theory and developed the framework for
2002). This legacy of distrust has been slow to fade laboratory experiments (Phase 1, Fig. 3.1), but it
and continues to reinforce the view that the core lacked sufficient environmental context to remove
BEF literature lacks credibility and is irrelevant to high levels of uncertainty when referencing the
global ecological issues, a dialogue likely to hinder likely consequences of future global change. Con-
the dissemination of information to managers and sequently, the scope of BEF research broadened
policymakers (Benton et al. 2007). (Reality filter, Fig. 3.1). The next phase of BEF
Articulating the appropriate interpretation of BEF research added realism using a range of strategies
research is of fundamental importance if we are to including connection to the real world (e.g. Duffy
provide a tenable solution to the biodiversity crisis. et al. 2003) and the use of real assemblages in the
Achieving this goal is proving difficult despite over- laboratory (e.g. Widdecombe et al. 2000, Emmerson
whelming support for the notion that biological et al. 2001), field experiments using species addition
diversity regulates ecosystem processes (Schläpfer or removal (e.g. Hector et al. 1999, Symstad and
et al. 1999). Syntheses of the first 15 years of research Tilman 2001), in situ manipulation (e.g. O’Connor
provide ample evidence that increasing biodiversity and Crowe 2005), or by increasing system com-
can have positive effects on ecosystem processes plexity through the incorporation of multiple trophic
and that these average effects are best explained by levels (Petchy et al. 1999, France and Duffy 2006a),
the loss of the most productive species from the community complexity (France and Duffy 2006b), or
community (Balvanera et al. 2006, Cardinale et al. multiple ecosystem processes (Hector and Bagchi
2006a). Part of the problem in communicating the 2007). At the same time, theoretical models were
significance of these results is undoubtedly historical extended to include environmental fluctuations (e.g.
(Raffaelli et al. 2005a), but there is also a real difficulty Yachi and Loreau 1999, Ives and Cardinale 2004)
in expressing a consistent position on BEF matters and further validated using empirical data (e.g.
because of the wide variation in how ecosystems Emmerson and Raffaelli 2000, Swan and Palmer
respond to altered species diversity. As more realism 2005, Fox 2006). A move away from the use of
is incorporated into experimental studies, the effects random extinction scenarios to the consideration of
of biodiversity on ecosystem processes tend to be biodiversity futures based on available data (e.g.
weaker because ecosystem processes are a product Solan et al. 2004, Zavaleta and Hulvey 2004, Bunker
of multiple biological and environmental variables et al. 2005, McIntyre et al. 2007, Bracken et al. 2008)
(e.g. Petchey et al. 1999, O’Connor and Crowe 2005, accompanied the innovative use of field observa-
Balvanera et al. 2006, Dyson et al. 2007). tions (Phase 3, Fig. 3.1) (e.g. Wardle et al. 1997a,
In order to capture such complexity a more Troumbis and Memtsas 2000, Cardinale et al. 2005,
holistic approach needs to be adopted (e.g. Naeem Ruesink et al. 2006), including natural and anthro-
and Wright 2003) that collates a portfolio of evi- pogenic gradients (Vitousek et al. 1994, Austin 2002,
dence from several lines of enquiry (e.g. Keer and Fukami and Wardle 2005). This third phase is cur-
Zedler 2002, Muotka and Laasonen 2002). Looking rently in its infancy (see Naeem and Wright 2003,
across the literature, it is clear that BEF science has Naeem 2006b), but its genesis heralds a point in BEF
attempted to achieve this in a series of phases (Fig. research history where the discipline has matured
3.1). Although the timing of publications from each and a full suite of evidence (i.e. theory, method-
phase shows that different approaches have been ology, laboratory and field experiments, field
 Concerns over consequences of biodiversity loss
• Economic • Ethical Schulze and Mooney (1994)
• Scientific • Religious Vitousek et al. (1997)

Hypothesis generation
• Rivet
• Redundancy
• Idiosyncratic

Hypothetical scenario Laboratory experiments Historical data Theoretical

Phase 1: Environmental

generation
variation controlled

For reviews: Emmerson and Tilman et al. (1997b)

• Expert opinion Hooper et al. (2005) Huxham (2002) Cardinale et al. (2004)
Sala et al. (2000) Naeem et al. (2002)
Hughes and Petchey (2001)
Loreau et al. (2001)
Criticism, validation
Limitations
& modification
• Small scale
• Heterogeneity of variance
• Simple communities
• Confounding factors
Aarssen (1997), Huston (1997),
• One trophic level
Ieno et al. (2006) • No species interactions

Reality filter

Connection to real world Real world in Field experiments Combinatorial

laboratory Theoretical
Duffy et al. (2003) Bruno et al. (2005)
Emmerson et al. (2001) Bruno et al. (2006) Yachi and Loreau (1999)
Widdicombe et al. (2000) Cardinale et al. (2000)
Ives and Cardinale (2004)
Gross and Cardinale (2005)
Increasing system complexity In - situ Sp. addition and removal
Phase 2: Inclusion of subset of

• Time (O’Connor and Crowe 2005) Biles et al. (2003) Hector et al. (1999)
environmental variation

• Multi-trophism (France and Duffy 2006a) Swan and Palmer (2004) Symstad and Tilman(2001)
• Community complexity (France and Duffy 2006b) O’Connor and Crowe (2005) Diaz et al. (2003)
• Multi-functionality (Hector and Bagchi 2007)

Biodiversity futures
based on data Model with validation
Naeem and Wright (2003) Emmerson and Raffaelli(2000)
Swan and Palmer (2005)
Fox (2006)
Empirically derived Summaries and
scenario generation meta-analyses
Controversy Covich et al. (2004) Relevance
Solan et al. (2004) Zavaleta and Hulvey (2004) Balvanera et al. (2006)
Bunker et al. (2005) McIntyre et al. (2007) Flint and Kalke (2005) Cardinale et al. (2006)
Bracken et al. (2008) Raffaelli et al. (2005a, b) Worm et al. (2006) Srivastava and Vellend (2005)

Movement to the real world

environmental variation
Phase 3: Incorporating

Natural and anthropogenic gradients of disturbance Field observations Indirect manipulations

Fukami and Wardle (2005) Wardle et al. (1997) • Diseases
Troumbis and Memtsas (2000) • Extractive industry
Cardinale et al. (2005) • Paleological record
Statistical partitioning Natural reduction of Ruesink et al. (2006) • ‘Freak’ disturbance events

e.g. • partial linear regression confounding factors

• variance partitioning Vitousek et al. (1994)
Austin (2002)

Application in the real world

Extension to landscape Connection with Translation Aid management and

and ecosystem scales ecosystem services to policy conservation issues
Diaz et al. (2006) Millennium Assessment (2005) Srivastava and Vellend (2005)

BEF indices
Expert advice Scholes and Briggs (2005)
Rouget et al. (2006)
Loreau et al. (2006) Zhang and Zhang (2007)

Figure 3.1 Summary of the research approaches adopted to address the relationship between biodiversity and ecosystem function in the peer-reviewed
scientific literature. Modified from Godbold (2008). See Plate 1.
 BIODIVERSITY-ECOSYSTEM FUNCTION RESEARCH AND BIODIVERSITY FUTURES 33

observations, and natural and anthropogenic OR “species diversity” OR “species richness”) AND
experiments) has become available in a form that (“ecosystem function” OR “ecosystem proces*”)” in the
can be presented to managers and policymakers. titles and keywords of all document types, in all
At a time when understanding the consequences languages, was performed. Only publications from
of biodiversity loss is of critical value (Pimm et al. 1990–2006 (inclusive) were used, as these span
1995, Chapin et al. 2000c), the large number and records published from immediately before the
broad range of papers contributing to BEF research Bayreuth conference (1991, proceedings published
raise important questions about whether the BEF in Schulze and Mooney 1993) to the most recent
literature is sufficiently visible to effectively inform adaptive synthesis workshop (BioMERGE, Biotic
front-line managers and policymakers. Whilst there Mechanisms of Ecosystem Regulation in the Global
are several authoritative reviews on the present Environment; an NSF funded research coordination
status (Loreau et al. 2001, Covich et al. 2004, Hooper network) held in Switzerland in December, 2006.
et al. 2005, Balvanera et al. 2006, Cardinale et al. The results of this screening are hereafter referred to
2006a) and clear ideas have been articulated as the BEF database. In all subsequent analyses,
regarding future research needs (e.g. Bulling et al. search returns were refined by publication year to
2006, Raffaelli 2006, Naeem 2006b), it remains remove entries published in 2007.
unclear what the large arsenal of scientific papers in As the focus is to determine how BEF research and
the BEF archive has collectively accomplished in ideology propagates through the peer-reviewed lit-
terms of information supply. In this chapter, the core erature, publications in the BEF database were
peer-reviewed BEF literature is identified and examined, using the ISI Web of Science results analysis
described. The sequential flow of information from tool, by publication year, source title, subject cate-
this literature base is then tracked through the sci- gory, country of research origin, or document type.
entific literature to other scientific disciplines. Trends For tracking the relative influence of previously
in funding dedicated to BEF research are examined published sources of information, the annual citation
to gauge government support for the topic, and rate was used as an estimate of scientific importance.
trends in the appearance of biodiversity as a topic in To adjust for differences in publication year, the
popular literature and the legal and legislative are- annual citation rate was calculated by dividing the
nas are quantified to estimate the incorporation of total citation count by the number of years since
research findings into the public arena. Finally, the publication. Self-citations (authors citing themselves)
application of the science by end users tasked with were not excluded (but were differentiated) because it
managing the environment is explored. The notion is recognized that such contributions are important in
that BEF research forms a primarily academic field the dissemination of information across the scientific
that contributes little to environmental concerns is community. To examine the relationship between
critically examined and recommendations are year of publication, impact factor of the journal in
offered that may enhance dialogue among which it is published, and number of authors with
researchers, managers and policy makers. the total number of citations and the annual citation
rate, simple correlations were calculated. In addition,
variation in annual citation rate among publications
3.2 Methodology categorized by their subject matter (discussion, the-
ory, methodology, laboratory experiments, field
3.2.1 The biodiversity-ecosystem function experiments, field observations, or practical applica-
literature base tion in the real world), country affiliation of
To obtain the most representative sample of peer- first author, and ecological habitat type (not habitat-
reviewed publications examining the BEF relation- specific, freshwater, terrestrial, or marine) were
ship, citation data were retrieved from the ISI Web examined graphically. Correlations and graphical
of Knowledge using the Science Citation Index Expanded examinations are preferential to other methods (such
and Social Sciences Citation Index databases. A ‘general as linear regression or analysis of variance) in this
search’ using the search term “(“biodiversity” case, because other factors that may influence why a
34 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

paper is cited cannot be controlled for or incorporated Environment Research Council) are required to
into the analysis. Thus, any observed relationships classify the research against an Environmental and
are indicative and not necessarily causative. Natural Resource Issues (ENRI) classification. The
Not all publications will carry the same weight total expenditure on research within the ENRI cat-
of influence in informing the wider scientific egory of ‘biodiversity’ for 2001–2006 was collated.
community. Publications that have been cited For the USA, the National Science Foundation
more frequently are likely to have a dispropor- (NSF) website (http://www.nsf.org/) was sear-
tionate influence on the dissemination of infor- ched for all awards granted between 1 January 1990
mation and ideology through the literature. The and 31 December 2006, using the search term:
six most cited publications from the BEF database (biodiversity OR “species diversity” OR “species rich-
were used to gain an impression of how heavily ness”) AND ecosystem AND (function OR proces*).
cited publications directly and indirectly influence To investigate how BEF research and ideology
the wider scientific community. Following Benton is used outside the peer-reviewed literature, the
et al. (2007), publications that directly cited each of Lexis-Nexis Butterworth online service (http://www.
these six publications (n ¼ 2546) were assigned to lexisnexis.com/) was searched using the search term
categories (discussion, theory, methodology, labora- “biodiversity OR species diversity OR species richness
tory experiments, field experiments, field observa- OR ecosystem function OR ecosystem process” for the
tions, or practical application in the real world) period 1990–2006. For both the UK and USA, all
that reflect how the information contained occurrences of the search terms in newspaper stories,
within each paper was used in the subsequent legislation (including hearings and enacted laws), and
generation of publications. As these six first- court case documents were determined for each year.
generation publications are themselves cited by Another broad category central to the application
other highly cited publications, it is also possible to of BEF research are planning documents used and
gain an impression of the information flow as it is generated by managers and agencies. The Final
disseminated across multiple generations of pub- Environmental Impact Statement (FEIS) for general
lications. For each generation of publications, the five management plans of three US national parks (USDI-
most highly cited publications citing the previous National Park Service 2006a, b, 2007) and three US
generation were determined and linked, either national forest/grassland complexes (USDA Forest
directly or indirectly (through subsequent genera- Service 1997, 2001a, b) were manually searched for
tions), to the six most highly cited publications from language indicating the acceptance of BEF ideology.
the BEF database. The horizontal extension of such The references cited within five of these documents
linkages was continued until either all of the top five (citations for the sixth were unavailable) were cate-
citing publications were from publications not listed gorized by topic (e.g. taxon natural history and dis-
within the BEF database or until the publications tribution, methodology, planning documents), source
were yet to be cited. The properties of the resulting (journal, book, government agency research report),
network provide an indication of the rate, form and and age (the difference between their publication year
connectivity of information flow within the BEF and the year the FEIS was published). These docu-
community and to multiple disciplines. ments were completed between 1997–2007 and cover
approximately 6.9 million ha of public lands in the
northern Great Plains, Colorado Rocky Mountains,
3.2.2 Biodiversity and BEF science impact
and Sierra Nevada in the USA.
outside the scientific literature
The proportion of funding from national science 3.3 Results
budgets allocated to BEF-related research provides
a measure of how high BEF sits on national scien-
3.3.1 Description of BEF database
tific agendas and whether its status is gaining Between 1990 and 2006, a total of 942 publications
momentum or waning over time. In the UK, in the peer-reviewed literature have either directly
research proposals submitted to NERC (Natural or indirectly considered concepts surrounding the
 BIODIVERSITY-ECOSYSTEM FUNCTION RESEARCH AND BIODIVERSITY FUTURES 35

(a) (b)
200 0.7
Frequency of publications (year–1)
0.6

Proportion of publications
150
0.5

0.4
100
0.3

0.2
50
0.1
0 0.0
1990 1992 1994 1996 1998 2000 2002 2004 2006

Bi esh nv. y

Pl oil ci.
Fo t S i.
re ci.

an l. gy

Phgro aphl.
G L y. Gnomy

M ere gy

M gi ool ies
tid er y
O E Bio stry

en i e y

Enicro dity
Fi Stuol.

.
M odi w. B Sci

S .S .

En Z her .

ic ing
tid C l.

H olo r.

gr
c s

s d
an Sc

A ogr Bio
Fr E log

ul ne og
ul v. io

. & mn og
is on

v. bi
ce vo lo

.A
o
Year

Ec

v.
.&

En
ar
M
Subject category
(c) (d)
0.10 0.6

Proportion of publications
Proportion of publications

0.08 0.5

0.4
0.06
0.3
0.04
0.2
0.02
0.1

0.00 0.0
Ec col os
. y
iv Ec col ett.
A rs. l. A gia
So se .

J. ser ien .
A v. ce

Ec Na ol.

So Aca . Pr ste ce
Fo il B d. og. ms

. M an .

SA
Fr UK
e
us en

G ana a
Sw erm da
N itze ny
ew rl d
a s
ut nl d
A d
A It a
en y

D Spa a
en in

k
Bi . E re

on ag.

C a
r.
at c co ie l.
.

l. iol.

Ec ol. che A
st l. i. U r.
l. on pl
il rv
l

ol M m

ze nd
Sw anc

C rali

ic

n
tin
on Sc Eco
ol og

rg al

ar
N the lan

So Fi lan
h an
og
N . E E sc vo

re io Sc Se
ol tu

Ec Bio S
l. ol sy n
E ik

A ed

hi
Ec

a
pp C p

fr
U
e o o
e L

m
pp B

a
O

e r
o
O

ds
C

en
od

Tr

P. ar

Country or territory
Bi

Source title

Figure 3.2 Summary of the BEF database (n ¼ 942) in terms of (a) the frequency of publications per year and (b)–(d), the ranked proportion of
publications per subject category, source title, or country/territory of research origin. For clarity, subject categories or countries/territories are only illustrated if,

effects of biodiversity on ecosystem function. The sity and conservation (7 per cent) (Fig. 3.2(b)).
majority of these contributions are based on Approximately a quarter (n ¼ 235) of publications
studies in terrestrial systems (60 per cent), but in the BEF database are published in Oikos (8 per
aquatic systems are also well represented (13 per cent), Ecology (6 per cent), Ecology Letters (6 per
cent freshwater, 11 per cent marine). The remain- cent), or Oecologia (4 per cent), with the remaining
ing 17 per cent (n ¼ 158) of contributions in the contributions distributed across an additional 210
database are not specific to a particular habitat source titles (Fig. 3.2(c)). The majority of publica-
and mainly consist of generic discussion (n ¼ 94) tions include authors/co-authors from Europe
or the development of theory (n ¼ 24) and meth- (65 per cent) or the USA (49 per cent), although a
odology (n ¼ 34). The number of publications per total of 59 countries or territories are represented
annum increased from no publications in 1990 to (Fig. 3.2(d)). Closer examination reveals that the
172 in 2006 (Fig. 3.2(a)). Collectively, the BEF majority of BEF research is led by authors in the
database spans 50 ISI subject categories; the USA (43 per cent) and the UK (13 per cent), with
majority of publications fall within ecology (63 per other significant lead authors emanating from
cent), environmental sciences (14 per cent), marine France (6 per cent), Canada (5 per cent) and
and freshwater biology (8 per cent), or biodiver- Sweden (4 per cent). The content of individual
36 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

publications varies, from the discussion of BEF ber of citations to discursive papers is relatively
ideology (31 per cent) to reporting the results low, although some of these papers are cited fre-
from manipulative experiments carried out in the quently. In contrast, laboratory experiments and
laboratory (14 per cent) or in the field (18 per theoretical papers have the highest median citation
cent). Although discussion and reports of manip- rates and papers that attempt to apply BEF ideol-
ulative experiments dominate the literature, it ogy to the real world are rarely cited, possibly
is important to emphasize that these data are reflecting differences in motivation between those
complemented by a substantial number (21 per tasked with academic science and those tasked
cent) of correlative field observations. A smaller with managing or conserving natural resources.
proportion of publications are concerned with the The median citation rate is not greatly affected by
development of theory (5 per cent) and method- habitat type, most likely because the most cited
ology (6 per cent), and fewer still (6 per cent) use publications are predominantly theoretical and a
BEF ideology to underpin management philoso- few discursive publications that are of generic
phy or applications in the real world. value.

3.3.2 What determines citation frequency? 3.3.3 Who is taking notice?

Contributions in the BEF database have collec- The six most cited papers within the BEF database
tively been cited > 22,000 times (¼ 23.9 cites per (hereafter referred to as the BEF-6) consist of a
item) and have an h-index – the number n of general review (Loreau et al. 2001), the develop-
papers that have all received at least n citations ment of methodology (Huston 1997) and key
(Hirsch 2005) – of 72, indicating high quality sci- laboratory (Naeem et al. 1994) or field experiments
ence. Of these, 49 per cent are incidences of self- (Hooper and Vitousek 1997, Tilman et al. 1997b,
citation (¼ 11.7 self-cites per item) suggesting a Hector et al. 1999) based on terrestrial plant com-
rather insular science base. However, although the munities. Collectively, these papers have been
propensity to self-cite has risen dramatically in cited over 2500 times and, individually, their
recent years, the proportion of citations by mean citation rate (424 ± 62.6, x̄ ± 1 s:d:) is greater
researchers outside of the BEF database is than that of major developments in other fields
increasing (inferred from the widening gap published at approximately the same time (e.g. the
between self vs. non-self citations, Fig. 3.3(a)). discovery of the first planet outside our solar
Analyses of the BEF database demonstrate that system, Wolszczan and Frail 1992 [cited 298
times]; or the discovery of the oldest known
several other variables may have an effect on
hominid, White et al. 1994 [cited 220 times]). In
whether a paper is cited more or less frequently.
each case, the percolation of ideas through the
Of the variables examined in this chapter, the total literature has followed a similar path, from dis-
number of times a paper is cited is most strongly cursive contributions through to applications
related to journal impact factor (r ¼ 0.45) and the of ideology in the real world (Fig. 3.4). Interest-
year of publication (r ¼ –0.39); total citation rate is ingly, however, as the BEF discipline has
only weakly, if at all, related to the publication’s matured (particularly post-Paris) there is some
number of authors (r ¼ 0.15). For annual citation indication that the time taken for BEF ideology to
rate, the relative strength of the three variables is influence applications in the real world has
the same, but journal impact factor (r ¼ 0.47; Fig. shortened and that the emphasis of papers has
3.3(c)) is the only one that accounts for a reason- moved away from phase one and towards phase
two and three (in Fig. 3.4, compare pink in panel
able amount of the variance (year of publication,
d, a paper published in 2001, to the earlier
r ¼ –0.12, Fig. 3.3(b); number of authors, r ¼ 0.26,
papers in other panels). Building on previous
Fig. 3.3(d)). There is also an indication that the contributions decreases the time required for
subject matter (r ¼ –0.14, Fig. 3.3(e)) and broad gaining confidence in the relevance and applica-
habitat type (r ¼ –0.13, Fig. 3.3(f)) of the individual bility of research findings (i.e. closing the credi-
study are of lesser importance. The median num- bility gap, sensu Benton et al. 2007), circumventing
 BIODIVERSITY-ECOSYSTEM FUNCTION RESEARCH AND BIODIVERSITY FUTURES 37

(a) 6000 (b)

120
5000

Annual citation rate

100
Citation frequency

4000 80
3000 60

2000 40

1000 20

0
0
1990 1992 1994 1996 1998 2000 2002 2004 2006 1990 1992 1994 1996 1998 2000 2002 2004 2006
Year Year
(c) (d)
120 120

100
Annual citation rate

100

Annual citation rate

80 80

60 60

40 40

20 20

0 0
0 5 10 15 20 25 30 0 10 20 30 40
Impact factor Number of authors
(e) (f)
120 120

100 100
Annual citation rate
Annual citation rate

80 80

60 60

40 40

20 20

0 0
1 2 3 4 5 6 7 1 2 3 4
Subject matter of study Habitat type of study

Figure 3.3 Citations to the BEF database between 1990 and 2006: (a) citation frequency by year including (solid circles) and excluding (open circles) self-
citations, (b)–(f) annual citation rate in relation to (b) the year of publication, (c) impact factor, (d) number of authors, (e) publication subject matter and (f)
habitat type. Subject matter refers to the content of each paper: 1 ¼ discussion, 2 ¼ theory, 3 ¼ methodology, 4 ¼ laboratory experiments, 5 ¼ field
experiments, 6 ¼ field observation, and 7 ¼ practical application in the real world. Habitat type refers to the studied ecosystem, such that 1 ¼ not habitat
specific, 2 ¼ freshwater, 3 ¼ terrestrial and 4 ¼ marine.

the need for an extended period of critique before the pathway from the BEF-6 to the external scien-
conclusions are generally accepted by the wider tific community, however, varies considerably. In
community. the first generation of publications, the most influ-
The BEF-6 influence the next generation of pub- ential papers directly citing the BEF-6 tend to be
lications either directly (solid lines, Fig. 3.5) or from within the BEF database, indicating a rapid
indirectly along the linkages between citation integration and absorption of philosophy by the
nodes (horizontal branches, Fig. 3.5) and via other BEF community but a lack of penetration to other
citations (dotted lines, Fig. 3.5). The length of disciplines. This process is reversed in subsequent
38 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

(a) 1.0 (b) 1.0

Proportion of citations
Proportion of citations
to Naeem et al. (1994)
0.8 0.8

to Huston (1997)
0.6 0.6

0.4 0.4

0.2 0.2

0.0 0.0
1994 1996 1998 2000 2002 2004 2006 1994 1996 1998 2000 2002 2004 2006
Year Year
(c) 1.0 (d) 1.0
Proportion of citations
to Tilman et al. (1997)

Proportion of citations
0.8 0.8

to Loreau et al. (2001)

0.6 0.6

0.4 0.4

0.2 0.2

0.0 0.0
1994 1996 1998 2000 2002 2004 2006 1994 1996 1998 2000 2002 2004 2006
Year Year
1.0 1.0
to Hooper and Vitousek (1997)

(e) (f)
Proportion of citations
Proportion of citations
to Hector et al. (1999)

0.8 0.8

0.6 0.6

0.4 0.4

0.2 0.2

0.0 0.0
1994 1996 1998 2000 2002 2004 2006 1994 1996 1998 2000 2002 2004 2006
Year Year

Figure 3.4 The influence of the six most cited papers from the BEF database since publication to December 2006 for (a) Naeem et al. (1994), (b) Huston
(1997), (c) Tilman et al. (1997), (d) Loreau et al. (2001), (e) Hector et al. (1999) and (f) Hooper and Vitousek (1997). These publications influenced
subsequent publications by contributing to discussion (red), development or reinforcement of theory (orange) or methodology (yellow), or by initiating or
informing laboratory experiments (green), field manipulations (turquoise), or field observations (blue), or they were used to underpin practical applications in
the real world (pink). Expanded from Benton et al. (2007). See Plate 2.

generations such that, by the fourth generation of 3.3.4 Is BEF research being supported?
publications, the most influential publications cit- In the USA, the mean annual sum (±1 s.d.) granted
ing BEF ideology are all outside of the BEF database annually to BEF-related research over the years
(or are yet to be cited). These tend to be contribu- examined (1995–2006) was US$6,563,952 ± 8,727,303
tions relating to invasive species, food web, or or, from 2001–2006 (post-Paris), U$11,817,500 ±
landscape ecology and a significant proportion of 9.965,911 (· 0.5 for approximate conversion to £GBP) ,
these tend to be review articles. but the range of award sizes increased considerably
 BIODIVERSITY-ECOSYSTEM FUNCTION RESEARCH AND BIODIVERSITY FUTURES 39

Hooper and Vitousek 1997 [346]

Hawkins et al. 2003 [186]
Willig et al. 2003 [150]
Mittelbach et al. 2001 [220]
Hector et al. 1999 [383] Leibhold et al. 2004 [150]
Ricklefs et al. 2004 [183]
Tilman et al. 2001 [195] Cardinale et al. 2002 [122]
Schroeter et al. 2005 [44]
Folke et al. 2005 [38]
Worm et al. 2006 [35]
Balvanera et al. 2006 [0]
Lewin et al. 2006 [0]
Hooper et al. 2005 [117] Zobel et al. 2006 [0]
Srivastava & Vellend 2005 [8] Renne et al. 2006 [0]
MacDougall 2005 [3] MacDougall & Turkinton 2006 [0]
MacDougall et al. 2006 [2]
Chan et al. 2006 [0]
Lamb et al. 2005 [31]
Tilman et al. 2002 [103]
Newman 2003 [1007]
Loreau et al. 2001 [403] Dunne et al. 2002a [100]
Dunne et al. 2002b [80] Williams et al. 2002 [60]
Garlaschelli et al. 2003 [58]
Jordano et al. 2003 [57]
Folk et al. 2004 [48]
De Deyn et al 2004 [21]
Ruess et al. 2004 [15]
ISI Web of Knowledge
Yeates 2003 [36] Murder et al. 2003 [19]
(extracted records = 942)
Dufty 2002 [68] Mulder et al. 2005 [14]
Yeates et al. 2003 [11]
Dufty et al. 2003 [50]
Dufty 2003 [40]
Berlow et al. 2004 [39]
Diaz et al. 2004 [54]
Tilman et al. 1996 [544]
Naeem et al. 1994 [527] Tilman et al. 1994 [469]
van der Heijden et al. 1998 [579]
Purvis & Hector 2000 [140]
Huston 1997 [440] Waide et al. 1999 [305] Knapp & Smith 2000 [140]
Zhu et al. 2000 [133]
Foody 2002 [185]
Peterson et al. 2002 [151]
Whitham et al. 2003 [89]
Lavorel & Garnier 2002 [95]
Wardle et al. 2004a [85]
Chapill et al. 2000c [309]
Callaway & Ridenour 2004 [33]
Diaz & Cabido 2001 [108]
Ehrenfeld 2003 [58] Wolfe & Klironomos 2005 [10]
Tilman et al. 1997b [447] Zedler & Kercher 2004 [11]
Allison & Votosek [11]
Petchey & Gaston 2002a [59]
Sala et al. 2000 [423]
Sakai et al. 2001 [360]
Tilman 1999b [323] Gaston 2000 [311]
Loreau 2000 [154] Loreau & Hector 2001 [159] Naeem & Wright 2003 [53]

Figure 3.5 The rate, form, and connectivity of information flow within the BEF community and to multiple disciplines from the six most highly cited papers
(¼BEF-6) within the BEF database. For each generation of publications, the five most highly cited publications citing the previous generation were determined
and linked, either directly (solid lines) or indirectly (dotted lines) to the BEF-6 via other highly cited publications. Line colour indicates the generation
sequence (blue ! red ! green ! orange). Publications not included in the BEF database are presented as a citation. The number of cites (from publication
until December 2006) are indicated in square brackets. References listed are available in the electronic appendix. See Plate 3.

during this period (Fig. 3.6(a)). Interestingly, of BEF research. In the UK, between 2001 and
although the total NSF research budget plateaus 2006, the mean (± 1 s.d.) annual amount of
after 2004, the percentage of grant money to BEF funding for biodiversity-related research was
research projects increased sharply (Fig. 3.6(b)), £12,188,321 ± 1,505,590 (· 2 for approximate con-
indicating a shift in the perceived importance version to US$), or 23.3 ± 3.2 per cent of the total
40 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

(a) 10×106 (b) 4.5×109 0.8

NSF allocation to BEF research

Amount awarded (US$ grant–1)

4.0×109

(% total available budget)

NSF research budget ($)
1×106 0.6

9
3.5×10
100×103 0.4
3.0×109

10×103 0.2
2.5×109

1×103 2.0×109 0.0

1996 1998 2000 2002 2004 2006 1996 1998 2000 2002 2004 2006
Year Year

(c) 16×106 50

NERC allocation to ENRI Biodiversity

research (% total available budget)
14×106
NERC research budget (£)

40
12×106

10×106 30

8×106
20
6×106

4×106 10

2×106
0
2001 2002 2003 2004 2005 2006
Year

Figure 3.6 Funding allocated to BEF-related research by the National Science Foundation in the USA and to all biodiversity related research by the
Natural Environment Research Council in the UK from 1995–2006 (USA) and 2000–2006 (UK). (a) Annual individual award amounts in the USA shown in
boxplots by year, on a log axis; boxes range between the 25th and 75th percentiles, with lines at the median, and whiskers range to the 5th and 95th
percentiles. Points are outliers. (b)–(c) Total funds awarded to all research (solid lines) and percentage of the total funding awarded to BEF-related
research (dashed lines) within each calendar year for the USA (b) and UK (c).

NERC funding awarded. This allocation has ronment and Development, held in Rio de Janeiro,
increased from £10,940,384 in 2001 to £14,540,280 in Brazil in 1992 (Fig. 3.7). Although the signing of
2006 (Fig. 3.6(c)), representing 17.0–23.1 per cent of the treaty had an immediate impact, media cov-
total NERC funding. In contrast to the USA, how- erage was quick to wane. However, biodiversity
ever, the BEF budget in the UK has essentially remained firmly in the news, albeit at low but
remained constant despite the fact that the total slowly increasing frequency over the next 5–7
research budget has been increasing. Clearly, the years. Following a series of major natural disasters
academic interest in BEF research has been trans- around the globe in the late 1990s, the number of
lated effectively and has a major impact on these two newspaper stories concerning the environment
funding agencies. and biodiversity increased dramatically. This
pattern of media interest paralleled the rise in
legislative enactments and court cases related to
3.3.5 Export of BEF ideology
environmental protection (Fig. 3.7), although the
It is clear that news stories relating to biodiversity total number of cases is low. In the USA, the
in both the UK and the USA were initiated by the steady increase in biodiversity-related documents
signing of the Convention on Biological Diversity in court cases appears from a qualitative analysis
during the United Nations Conference on Envi- to be driven by cases involving habitat protection,
 BIODIVERSITY-ECOSYSTEM FUNCTION RESEARCH AND BIODIVERSITY FUTURES 41

(a) 3500 100 (b) 1400 20

3000 80 1200

No. of cases/enactments

No. of cases/enactments
15
No. of news stories

No. of news stories

2500 1000
60
2000 800
40 10
1500 600
20
1000 400
5
500 0 200

0 0 0
1990 1992 1994 1996 1998 2000 2002 2004 2006 1990 1992 1994 1996 1998 2000 2002 2004 2006
Year Year

Figure 3.7 An indication of the export of BEF research and ideology from the peer-reviewed scientific literature to the public domain for (a) the USA and
(b) the UK in media (open circles), legislation (crosses), and court cases (closed circles) for the period 1990–2006.

with several non-governmental organizations (e.g. of future generations. In contrast, the national forests
the Center for Biological Diversity, the Natural and grasslands, administered by the Department of
Resources Defense Council, and the Sierra Club) Agriculture’s Forest Service, were established
appearing frequently. Similarly, habitat protection expressly for multiple uses, and until recently, their
issues appear to compose the bulk of the US leg- emphasis in management has been on extractive
islative documents concerning biodiversity, uses, especially timber harvesting and cattle grazing.
although these terms also appear in hearings on In response to changing scientific and public views,
the Clean Air and Clean Water acts. the Chief of the Forest Service announced in 1992
It seems that the timing of the emergence of BEF that an ecological approach would be adopted so
concepts in the public domain coincided with major that national forests and grasslands would ‘repre-
events or announcements that raise public awareness sent diverse, healthy, productive, and sustainable
of environmental issues, rather than any direct lob- ecosystems’ (USDA Forest Service 1997, p. 3).
bying by the BEF community to increase political Although all the planning documents that were
attention to the consequences of biodiversity loss reviewed used this approach, terms such as ‘process’
(Loreau et al. 2006 provides one exception). Interest- and ‘function’ were generally not equivalent to the
ingly, environmental issues in general received less same terms used in the BEF database (e.g. fire,
attention in the UK during the 2005 electoral cam- flooding, or insect or pathogen outbreaks in the
paigns, rebounding in the following year, suggesting planning documents; primary productivity, nutrient
that issues with direct impacts closer to home may retention, or carbon storage in the BEF database). All
override more indirect global concerns. of the documents also followed their respective
agencies’ policies in emphasizing biodiversity as
something to preserve, protect, and, where neces-
3.3.6 Transfer of concepts to end users
sary, restore, and they often stated that one way to
and stakeholders
do this is to maintain ‘naturally functioning eco-
The evaluation of the transfer of BEF concepts to systems.’ Thus, although management seems to
those making management decisions is decidedly emphasize biodiversity as a function of the envi-
less quantitative than the other portions of this ronment, rather than the reverse, there is scope for
chapter, but it reveals some interesting information. BEF science to influence management.
In the USA, the Department of the Interior’s Interestingly, BEF concepts are more prevalent in
National Park Service oversees all national parks, the Forest Service documents than in the Park Ser-
whose purpose is to conserve, unimpaired, the nat- vice documents. In Park Service plans, the closest
ural and historic resources therein for the enjoyment statement to the BEF assertion that biodiversity
42 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

improves ecosystem function was an aspiration to journals in which BEF research is most often pub-
‘restore native ecological processes by reintrodu- lished (those in Fig. 3.1(c) in decreasing order of
cing native plants and animals and removing non- citations: Conservation Biology, Ecological Applica-
native species where practicable’ (USDI National tions, Ecology, Ecosystems, Bioscience).
Park Service 2006a, p. 100). In Forest Service plans,
the BEF ideology was relatively common. For
3.4 Conclusions and recommendations
example, the decisions made in developing the
management plan for the northern Great Plains The two great sins of innovation are to be either too
units emphasized the need to ‘ . . . sustain ecosys- early or too late with the solution to a problem, an
tems by ensuring their health, diversity, and pro- adage of particular relevance when assembling the
ductivity’ (USDA Forest Service 2001a). More evidence base needed to understand the extent to
explicitly, the FEIS for the Sierra Nevada forest plan which changes in biodiversity are causally linked to
states that ‘an ecosystem that is well supplied with ecosystem processes. A naïve view is that ecologists
native species, has a level of biomass that is not are perfectly placed to answer BEF hypotheses, as
maximizing available nutrients and water, and is human civilizations have long understood the
adapted to disturbance, is typically a resilient one’ importance of biotic interactions and the environ-
(USDA Forest Service 2001b, p. 104), consistent ment (McNeely 1994, Rozzi 2004) and much of the
with the experimental findings of Pfisterer and scientific information required to understand the
Schmid (2002). The planning document was, how- BEF relationship, including experiments that
ever, completed before this publication (loc. cit.), directly manipulate diversity, have been in place
indicating that either the management philosophy since the mid-19th century (Hector and Hooper
in Sierra Nevada was ahead of BEF research or that 2002, Statzner and Moss 2004). Contemporary BEF
it was alluding to untested concepts. studies build on these older perspectives and the
Although BEF concepts do appear in these analyses in this chapter confirm that that these
management plans, those tasked with preparing the syntheses are readily absorbed by the wider scien-
documents are not directly citing the BEF literature. tific community. Since Paris, the discipline has
It is clear that, for most management units, indi- matured and gained scientific credibility. Indeed,
vidual species are still of major concern, since their contrary to criticisms voiced in the late 1990s, a
natural history, distribution, and management suite of evidence is now available based on theory,
comprise major portions of the references cited (Fig. empirical investigations, field observations, and
3.8(a–b)). References to ecological concepts (such as practical application, backed by large-scale (e.g.
BEF) are relatively rare, comprising just 19 of the 19,485 km2, Kennedy et al. 2003) and long-term
227 published ecological references cited across observations in terrestrial plant (19 years, O’Connor
the five plans. These findings are consistent with et al. 2001), soil (10 years, Lindberg et al. 2002) and
the survey undertaken by Pullin et al. (2004) which marine systems (7 years, Paine 2002). Yet in spite of
showed that only 23 per cent of managers ‘always’ this wealth of evidence, the scientific consensus that
or ‘usually’ used scientific publications when com- biodiversity is critical for ecosystem function has
piling management plans. The latest (< 5 years old) only partially been embedded in the policy arena.
research is often not cited (Fig. 3.8c), most likely Indeed, if future generations are presented with the
due to the long time taken to prepare and finalize BEF science base as it now stands, it will be
these documents (> 2 years). Interestingly, period- incomprehensible to them if policy makers have not
ical articles are the most common type of citation fully adopted this consensus and utilized it to
(56 per cent), but books or book chapters (24 per moderate and mitigate global scale problems
cent) are an important source of ecological infor- caused by biodiversity loss.
mation. Symposium proceedings (11 per cent), Although the evidence base is well resourced and
government research reports (5 per cent), and the- available, establishing generality by substantiating
ses or dissertations (4 per cent) comprise the rest. hypotheses with multiple lines of enquiry is limited
Only 16 of the 227 ecological references cited are in in practice (good examples include Keer and Zedler
 BIODIVERSITY-ECOSYSTEM FUNCTION RESEARCH AND BIODIVERSITY FUTURES 43

(a) 70 (b) 100

BNP
GSDNPP
60
SKCNP
80 NGPNFG
% of cited references

% of cited references
50 CRMNFG

40 60

30 40
20
20
10

0 0
y

d gy
nv ip.

t r ry

es n
gm rt

h
gm gy

m tho lan

l.

er
s

s
l.

ua
Ta xon log

a
rc

ct

ct

co
m po

co
gm to

th
ol t pl
ity olo

r
m lo

fe

fe
ea
om Me t p

ol esc

pt
.e
e
M en

e
Ta bio

O
n bio

ef

ef
t/
un d

ce
os
gm

an

p.
.r

on
ot

ec
.i

sp
um
N

C
./
m
ec
te

ve

m
Bi

n
xo

H
Si
b.

om
xo

si
Pu

va
Ta

C
In
C

(c) 100
BNP
GSDNPP
SKCNP
80 NGPNHG
% of cited references

CRMNFG

60

40

20

0
1

10

+
0–

2–

–1

–2

20
5–

10

15

Figure 3.8 The types and age of references cited by five Final Environmental Impact Statements (FEIS) for national park and national forest/grassland
general management plans. In (a), all references are categorized by subject matter: ‘Not Biology’ ¼ physical science, paleontology, economics, and census
information; ‘Taxon Biology’ ¼ natural history, distribution, and conservation status of species or select taxa, and field guides/taxonomic keys; ‘Taxon Mgmt
Plan’ ¼ management plans/guidelines for specific taxa, and reports on anthropogenic impacts on specific taxa; ‘Methodology’ ¼ guidelines on monitoring,
habitat delineation, and range evaluation; ‘Community Desc’ ¼ descriptions of plant communities and vegetation maps; ‘Biol Inventory’ ¼ biological
inventory and survey results, including disease incidences, for a given region; ‘Mgmt Report’ ¼ unpublished site-specific biological evaluations and
management or monitoring reports; ‘Site Mgmt Plan’ ¼ management plans for parks, forests, grasslands, and refuges; and ‘Pub Ecol Research’ ¼ published
ecological research (not including natural history, distribution, etc. in the first category). In (b), references from the ‘Pub Ecol Research’ category are further
categorized as taxon-specific management or ecology, effects of human-caused disturbances (i.e. unintentional management; e.g. vehicle or foot traffic,
climate change, acid deposition) on taxa or communities, invasive species effects, community or ecosystem ecology, conceptual, or other. In panel (c), the
percentages of cited references since publication year of the FEIS are presented.

2002, Muotka and Laasonen 2002). Even when emergence of the BEF paradigm occurred when
achieved, an effective interface between policy- concerns relating to environmental change were
makers and scientists is, at best, underdeveloped – beginning to gain momentum and at a time when
despite some lobbying for the installation of such a there was heightened public awareness of the gen-
mechanism (e.g. Loreau et al. 2006). It seems that eral impacts that human activities have on the
the primary problem for the BEF community is not biosphere (e.g. Halpern et al. 2008). Whilst BEF
the science base, but one of communication. The investigators undoubtedly contributed to and
44 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

shaped opinion, it is evident that BEF science was have focussed on the values of ecosystem services
catapulted into the public domain because it was whilst failing to incorporate the link between bio-
absorbed into general discussions about global diversity and ecosystem service provision at a
change, rather than because of any top down landscape level (Kremen 2005).
coordinated effort by the BEF community to There is some reassurance that BEF science is
directly emphasize BEF concepts. Where opportu- being noticed outside of the BEF community, albeit
nities for high-profile communication have taken that the primary routes of dissemination (discus-
place (e.g. Issues in Ecology publication and the sion of wider issues in the public arena or scholarly
subsequent attempt to revoke; Naeem et al. 1999, reviews of associated fields in the scientific litera-
Wardle et al. 2000b), the ambiguity caused by ture) are incidental rather than directed. Irrespec-
competing scientific views over the relevance and tive of the mechanism of dissemination, the effect
extrapolation potential of controlled experiments (since the mid-1990s) has been a five-fold reduction
(which represent < 6 per cent of the BEF database) in the time taken for the latest research findings to
may have prevented effective communication of the be implemented in real-world conservation efforts.
science to the media and policymakers at a time In some cases the motivation for such rapid adop-
that mattered most. tion of the science has been commercial gain
It is clear that there are also major deficiencies in (Bullock et al. 2001, Skelton and Barrett 2005), but in
communication between those carrying out the most cases three main drivers seem more likely to
fundamental science and those tasked with gener- be responsible. First, longer exposure time of the
ating and implementing management objectives, general topic places the subject area on the agenda
conservation strategy, or policy. Cultural differ- and increases capacity to build on prior knowledge,
ences between the way interdisciplinary fields go short-circuiting the inherent time lag associated
about their science (attendance of different con- with the credibility process that needs to be in
ferences, publication in and readership of different place before action can be taken (Benton et al. 2007).
journals, access to information sources, technical Second, the maturation of the discipline towards
terminology) form a significant barrier (Raffaelli et experimental designs and approaches that incor-
al. 2005a), such that policymakers are often una- porate more realism (Phases 2–3 and beyond, Fig.
ware of developments in BEF science and vice 3.1) makes the science base less nebular and more
versa. Direct appeals from one community to applicable to large-scale real-world environmental
another, although rare, have been made (Minns problems, and therefore more accessible and tract-
et al. 2001 provide a notable example), but tend to able to environmental managers. Increasingly, aca-
remain in a format and/or source that remains demic scientists are teaming up with environmental
inaccessible to the target audience. A recent analy- managers to perform large-scale experiments that
sis of views on biodiversity research in Europe otherwise would not be possible (e.g. Bison–prairie
(Hildén et al. 2006) confirms that these problems are dog–plant impacts on grassland ecosystem pro-
significant, concluding that ‘policy makers do not cesses in the Badlands National Park, USA; Fah-
understand biodiversity, its value or research nestock and Detling 2002). Third, the more
results’ and that ‘relevant policy processes are not widespread adoption of sustainable ecological
researched’ because ‘researchers do not understand concepts (for example, the ecological approach
management needs’ (p. 16). This stalemate appears adopted by the US Forest Service) provides strong
to be a product of subtle differences in opinion over impetus to converge towards a standardized,
what information, if any, should underpin effective practical approach to ecosystem-based manage-
ecosystem management strategies; some ecological ment that fulfils, or at least incorporates, conser-
concepts do not always translate well to conserva- vation principles and strategies required by law
tion measures (Gascon and Lovejoy 1998). Indeed, and desired by the public.
BEF science has tended to concentrate on the con- It is clear that decision making is being informed
sequences of biodiversity loss for specific ecosystem by BEF ideology, but the influence that the scien-
processes, whereas managers and policy makers tific community has on this process appears to
 BIODIVERSITY-ECOSYSTEM FUNCTION RESEARCH AND BIODIVERSITY FUTURES 45

be small relative to the force of social change in likely to bridge this divide, lead to the appropriate
attitudes. If the BEF research community is to exchange of information, and hasten the develop-
effectively inform managers and policymakers in ment of policy based on a portfolio of evidence
time to mitigate impending global problems, the that incorporates levels of uncertainty (Benton
needs of these customers have to be considered et al. 2007). Whether future generations consider
and impediments to communication must be rec- the BEF science as the early bird that caught the
ognized and overcome. Only an extended science– worm, or as a primarily academic field that was a
policy consultation involving the interaction of day late and a dollar short, will depend on whe-
BEF scientists and decision makers (i.e. evidence- ther the next phase of BEF research enhances the
based conservation, sensu Sutherland et al. 2004) is science–policy interface.
This page intentionally left blank
PART 2
Natural science foundations
This page intentionally left blank
 CHAPTER 4

A functional guide to functional

diversity measures
Owen L. Petchey, Eoin J. O’Gorman, and Dan F. B. Flynn

4.1 Introduction
tional traits, both functional diversity and use of the
4.1.1 What is functional diversity and why resource pool will decline in concert. Other changes
is it important? associated with loss of access to that resource pool
Functional diversity is a component of biodiversity might include a reduction in ecosystem processes,
that concerns what organisms do, rather than, for such as net primary production.
example, their taxonomic identity (Tilman 2001, Another illustration of the interactions that are
Naeem and Wright 2003, Hooper et al. 2005, implicitly represented in measures of functional
Petchey and Gaston 2006). What kinds of resources diversity is that the effect on functional diversity of
do organisms exploit, where do they exploit them, losing a particular species (or adding a particular
and when do they exploit them? Each of these species) is context-dependent. The context here is
characteristics, and many others, can be a compo- the other species present in the community. In one
nent of functional diversity. Since ecosystem pro- context, loss of a particular species can have little
cesses ultimately result from the actions of effect on functional diversity. This would be if the
organisms, knowing about these actions and sum- community contains, and continues to contain,
marizing them in a measure of diversity should functionally similar species to the lost species. If
inform about ecosystem processes (Tilman 2001, there are no similar species, however, the loss of the
Hooper et al. 2005). Therefore, functional diversity same species could have a large effect.
has the potential to link morphological, physiolog- Thus functional diversity is a measure of diver-
ical, and phenological variation at the individual sity that implicitly incorporates some mechanisms
level to ecosystem processes and patterns. of ecological interactions between species. In doing
One critical reason that functional diversity so, it provides a general (and yes, assumption-
might link organisms and ecosystems is that it laden) approach for scaling from characteristics of
implicitly contains information about how species individuals to properties of communities and eco-
will compensate for the loss of another. For illus- systems. This makes functional diversity a poten-
tration, consider some species that are functionally tially powerful concept in ecology. At present,
rather similar, and some that are rather dissimilar. much attention is focused on how to measure it,
The similar species each access the same pool of and that is the broad subject of this chapter.
resources. If one of these species is lost, no reduc-
tion in the use of that resource pool results, as the
4.1.2 Why not functional group richness?
other species are present and will accordingly
simply increase their use of that same resource. One method for quantifying functional diversity is
There will also be only a small loss of functional to examine the characteristics of some species, and
diversity, since the lost species was not very unique to somehow assign species to functional groups (or
in its functional characteristics. If, however, the lost guilds) based on these characteristics (Root 1967).
species was quite dissimilar to others in its func- This is a popular method, because of the perceived

49
50 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

ease of assigning species groups, and has been used functional group, and, for example, the effects of
repeatedly in biodiversity-ecosystem function species richness and extinction on functional group
experiments. However, this method has several richness are arbitrary.
major drawbacks, all linked to the central issue of Finally, evidence exists that some real assign-
how to assign species to groups. The details of the ments of species to functional groups are little
assignment is relatively unimportant here, and better than random assignment of species to
methods range from the very subjective to more groups. In particular, correlations between func-
objective (Holmes et al. 1979, Chapin et al. 1996, tional group richness and ecosystem processes in a
Díaz and Cabido 1997). What is critical here is the well-studied grassland plant ecosystem were often
decision about how similar species need to be in higher with random assignment of species groups
order to belong to the same functional group, or than the actual grouping used (Petchey 2004,
rather where the boundaries of the groups should Wright et al. 2006).
be placed. This decision defines the number of
functional groups and the average number of spe-
4.1.3 Non-grouping measures of functional
cies in a functional group. The number of functional
diversity
groups represented by the species in a local
assemblage (functional group richness) is the mea- The recognition that functional group richness is a
sure of functional diversity. problematic measure of functional diversity
The first problem with functional group richness prompted the search for better alternatives. Given
is that any interspecific differences within a group some information about what species do, how can
are ignored. This is less of a problem if species form one transform this into a measure of the diversity of
very distinct groups; that is, if species’ functional what the species do? If we record what species do
characteristics are distributed discontinuously. quantitatively, and call this information their traits,
However, if variation is more continuous, the or functional traits, then the problem is how to
amounts of variation that are ignored by functional measure the diversity of trait values. Thinking of
group richness could be large. Since many impor- the species as points in n-dimensional trait space,
tant functional traits are continuous, this is a large the question becomes how to measure the diversity
problem. Even traits which are often considered of a cloud of points in n-dimensional space.
discontinuous, like N-fixing or not, are in fact con- One of the first solutions was by Walker et al.
tinuous at some scale, with the efficiency of nitro- (1999), followed by Petchey and Gaston’s (2002a)
gen fixation varying under different soil conditions use of a method of measuring phylogenetic
(Vitousek et al. 2002). diversity to solve the problem. Since then, a small
The second problem is that the behaviour of industry has sprung up, with frequent critiques,
functional group richness depends greatly on the suggestions of new measures, and supposed
number of functional groups that are defined improvements to old measures (Mason et al. 2003,
(Petchey & Gaston 2002a, Fonseca and Ganade Heemsbergen et al. 2004, Botta-Dukát 2005, Mason
2001). Defining many functional groups results in et al. 2005, Mouillot et al. 2005a, Pavoine and
few species per functional group, and strong effects Doledec 2005, Ricotta 2005a, b, Cornwell et al.
of species richness (and extinctions) on functional 2006, Lep
s et al. 2006, Podani and Schmera 2006,
diversity, as the number of functional groups Petchey and Gaston 2007, Fox and Harpole 2008,
begins to approximate the number of species. Mouchet et al. 2008, Quintana et al. 2008, Walker et
Defining few functional groups results in many al. 2008). The impression one might come away
species per functional group, and weak effects of with from so much activity in this field is lack of
species richness on functional diversity. consensus about the most appropriate measure of
Third, no objective method exists for deciding functional diversity.
how different species should be in order to belong The aim of this chapter is to provide a functional
to different functional groups. Consequently, the guide to functional diversity measurements by
number of functional groups, number of species per two complementary approaches. First, through
 A FUNCTIONAL GUIDE TO FUNCTIONAL DIVERSITY MEASURES 51

illustrations of the uses that functional diversity deviations of species from the weighted mean of the
can be put to: what types of ecological questions species. It is therefore relatively similar to variance.
can functional diversity help us answer? And The weighting of trait values by species can be by
second, by showing potential users how to abundance, and so gives a measure of functional
choose among six different measures of functional diversity that can account for differences in abun-
diversity. Examples show how several of the dance between species.
metrics work (i.e. what they do), in particular how This metric was designed solely to work with
they respond to changes in species richness and single traits, which considerably restricts its utility,
species composition, highlighting crucial aspects but its authors recognized this limitation and sug-
of the metrics, and how they apply to two simu- gested averaging for multiple traits. The solution
lated datasets. We will also get a sense of where used in the simulations below follows this sug-
the field needs to go through this analytical gesting and averages FDvar values across multiple
review. traits. It is also possible to weight the FDvar values
for each trait by the degree of statistical independ-
ence from other traits, a technique which has
4.2 What metrics are out there?
been proposed by researchers working on related
We will focus on six measures of functional questions in functional ecology, although not pre-
diversity. viously for FDvar. The notion is to discount traits
which are highly correlated with other traits. One

Convex hull volume (CHV) (Cornwell et al. 2006)
formulation of this weighting parameter is

FDvar (Mason et al. 2003)
X T  

Functional attribute diversity (FAD) (Walker et al. r2tl
wt ¼ 2 þ
1
1 , for T traits, considering the
1999)/Mean dissimilarity (MD) (Heemsbergen et al. l¼1
2
2004) relationship between trait t and all other traits l

Rao’s quadratic entropy (Q) (Botta-Dukát 2005) (Kark et al. 2002, Mouillot et al. 2005c).

FD (Petchey and Gaston 2002a)

Podani and Schmera’s modification to FD (here 4.2.2 Distance-based measures
termed FDLD) (Podani and Schmera 2006) (MD/FAD and Q)
These can be divided among three categories: MD (mean dissimilarity) (Heemsbergen et al. 2004)
measures that work on trait values directly (CHV and FAD (Functional Attribute Diversity) (Walker
and FDvar), measures that work on the distance et al. 1999) are both calculated as the mean distance
matrix (FAD/MD and Q), and measures that work between species in multivariate space. Note that
on the functional dendrogram (FD and FDLD). another distance-based measure is now available
(Schmera et al. 2009). This requires a decision about
the distance measure used: for example, Euclidean,
4.2.1 Measures directly using the trait values
Manhattan, or Gower. Hereafter we use MD to
(CHV and FDvar)
include both MD and FAD.
The convex hull volume (CHV) is the smallest Q, representing Rao’s quadratic entropy, was
convex shape (set) that can enclose a set of points in proposed as a measure of functional diversity by
n-dimensional space, where each trait provides a Botta-Dukát (2005). It is the sum, across species
new dimension. It was first employed as a measure pairs, of the product of the distance between the
of the dispersion of species in n-dimensional trait two species in trait space and their two relative
space by Cornwell et al. (2006). In one-dimensional abundances. However, other researchers have
space, convex hull volume is the range of the data implemented a modified version of Q, using arbi-
(maximum value minus the minimum). This mea- trary weighting values rather than using relative
sure has only been used for continuous traits. abundances, which are then modified until the
FDvar (Mason et al. 2003), when used with a sin- maximum explanatory power for the ecosystem
gle trait, can be thought of as the sum of squared function of interest is achieved (Weigelt et al. 2008).
52 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Table 4.1 Number of papers citing Walker et al. (1999)/Heemsbergen et al. (2004) for FAD/MD, Petchey and Gaston (2002a) for FD, Mason et al. (2003)
for FDvar, Botta-Dukát (2005) for Q, Cornwell et al. (2006) for CHV and Podani and Schmera (2006) for FDLD. The greater number of citations for FAD/MD
and FD are a reflection of the age of the papers.

Number of citations

Theme of paper FAD/MD FD FDvar Q CHV FDLD Total*

Unrelated studies 96 21 4 1 7 1 124

Use of discrete groupings or standard diversity indices 46 8 1 1 1 0 55
Methods associated with calculating functional diversity 11 11 3 4 0 3 20
New measure of functional diversity 7 11 1 0 0 1 18
Application to empirical data 3 8 4 3 1 0 16
Benefits of looking at functional diversity 9 11 1 1 0 0 15
Pro’s and con’s of indices 7 7 4 2 0 0 8
Potential use as ecological indicator 1 5 4 0 0 0 6
Total number of times cited 180 82 22 12 9 5 262

*
There is some overlap in papers cited, so ‘Total’ refers to the actual number of papers cited under each heading.

Researchers should thus take care when interpret- 4.3 Applications of functional diversity
ing studies using Q to examine specifically what
implementation was used. We compiled a list of papers that cite seven of the
key functional diversity methods papers: FAD/MD
(Walker et al. 1999, Heemsbergen et al. 2004), FD
4.2.3 Dendrogram-based measures (FD, FDLD) (Petchey and Gaston 2002a), FDvar (Mason et al.
2003), Q (Botta-Dukát 2005), CHV (Cornwell et al.
FD (Petchey and Gaston 2002a) is the branch length 2006) and FDLD (Podani and Schmera 2006) from
across the regional functional dendrogram that is the ISI database. The list of citing papers was
required to join the set of species present in an examined to see how continuous functional diver-
assemblage. The regional functional dendrogram sity measures are being used (see Table 4.1). Each
describes the functional relationships among the citing paper was classified into one of eight cate-
species in a region, and is constructed from the gories according to their main focus. In total, these
traits of species. It is important to note that only one seven methods papers were cited by 262 unique
dendrogram is constructed: the regional dendro- papers (FAD 137, MD 45, FD 82, FDvar 22, Q 12,
gram (regional because it contains all the species of CHV 9, FDLD 5).
interest in the study region). The FD of local One striking pattern in papers citing the
assemblages is the length of branches required to seven methods papers is the low application to
connect across this regional dendrogram the spe- empirical work. Just 16 (out of 262) studies have
cies in a local assemblage. attempted to apply one of the six functional diver-
In FDLD (Podani and Schmera 2006), each local sity indices to empirical data. Heemsbergen et al.
assemblage has its own dendrogram constructed. (2004) manipulated the functional dissimilarity of
This is very different from FD (Petchey and Gaston detritivore communities in soil microcosms (mea-
2002a), in which only one dendrogram, the regional sured using MD). They found that functional dis-
dendrogram, is constructed. This has no effect on similarity, and not species number, led to
what the measures can be used for. For example, community compositional effects on key ecosystem
both FD and FDLD can be used to measure the processes (loss of leaf litter mass and soil respira-
relative functional diversity of local assemblages; tion). MD was also used to assess the functional
both can be used to assess the effect of new species similarity of plants in an Australian rangeland
(invaders) on functional diversity. community (Walker and Langridge 2002). This
 A FUNCTIONAL GUIDE TO FUNCTIONAL DIVERSITY MEASURES 53

study followed on from the methods used in been used to calculate the functional diversity of
Walker et al. (1999); however, this time they found zooplankton in Canadian lakes (Barnett and Beisner
that the most dominant species in the community 2007), applied to long-term avian distribution
were no more dissimilar to each other than to all datasets (Petchey et al. 2007), and used to determine
other species. the functional significance of forest diversity in a long
FD and MD have been compared to species term biodiversity experiment (Scherer-Lorenzen
richness (SR) and functional group richness (FGR) et al. 2007b).
using data from the BIODEPTH experiments Another subset of citing papers consider the pros
(Petchey et al. 2004b). Here, it was found that FD and cons of these functional diversity indices.
and MD had greater explanatory power because Petchey and Gaston (2006) provide a review of the
they use a much greater amount of trait information most popular functional diversity measures in BEF
and can allow for small differences between species (Biodiversity-Ecosystem Functioning) research,
that functional groups ignore. SR, FGR, FD, and some of which are evaluated by Ricotta (2005a).
MD have also been analyzed for roadside data from Podani and Schmera (2006) review dendrogram-
Bibury in the UK (Thompson et al. 2005). FD has based measures of functional diversity. Mason et al.
been used to test if functional diversity of exotic (2003) highlight that FD does not account for spe-
mammalian predators leads to extinction of island cies abundance, and claim incorrectly that it is a
bird species (Blackburn et al. 2005) and if there is a simple surrogate for SR. They acknowledge the
loss in functional diversity of a tropical amphibian shortcomings of FDvar in only accounting for one
community after logging activities (Ernst et al. character at a time. Botta-Dukát (2005) suggests that
2006). De Bello et al. (2006) used a variation of Q to Q is the best alternative as it uses both species
calculate the functional diversity of plots exposed to abundance and pairwise functional differences
various levels of sheep grazing. between species, a view echoed by other authors
Recently (2007–2008), the number of papers (Lep
s et al. 2006). It has been proposed that func-
incorporating these continuous measures of func- tional diversity can be split into functional richness,
tional diversity into empirical studies has notably evenness, and divergence (Mason et al. 2005). Here,
risen. This is perhaps a sign that they are being FD can be considered a measure of functional
increasingly recognized as a useful way to examine richness, while FDvar and Q can be considered
applied questions. Schamp et al. (2008) used CHV measures of functional divergence. A functional
as one of six metrics to estimate the dispersion of diversity framework for BEF research has also been
traits (biomass, height, and seed mass) in their suggested, based around use of response and effect
target plant community. Epps et al. (2007) used Q to traits (Lavorel and Garnier 2002, Naeem and
calculate the chemical diversity of litter and foliar Wright 2003).
mixtures. They then examined the relationship There still appears to be a sizeable portion of
between species richness and chemical diversity studies that make use of functional group richness,
using published data from temperate and tropical despite this method being discouraged in many of
forest systems. Jiang et al. (2007) compared the the continuous functional diversity papers. This is
effects of plant functional diversity (measured using particularly true of older studies (2000–2003) that
FDvar) on community productivity and soil water cite Walker et al. (1999). This is unsurprising given
content in an experiment on artificial plant com- that, at this stage, continuous measures of func-
munities. Mason et al. (2007, 2008) examined the tional diversity were not yet widely recognized. For
functional diversity of French lake communities example, Allen et al. (2003), Anderson et al. (2000),
using FDvar as a measure of functional divergence. Davic (2003), Decocq and Hermy (2003), Hector
Mouillot et al. (2007) used both FD and FDvar to et al. (2000), Lep
s et al. (2001), Lloret and Vila (2003),
determine whether assembly rules in lagoon fish Ni (2003), and Richardson et al. (2002) all used
communities are driven by functional traits and to discrete functional groups or plant functional types
seek relationships between functional diversity of as measures of functional diversity. More recently,
fish and environmental gradients. FD has also trophic groupings have been empirically shown to
54 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

be inappropriate for grassland species (Heisse et al. have escaped notice to date (Poulin 2004).
2007), arable plants (Hawes et al. 2005), lake- Attempts have also been made to encourage phyto-
dwelling shredders (Bjelke and Herrmann 2005), plankton ecologists to make use of the new meth-
and larval anuran predators (Chalcraft and Rese- ods for studying functional diversity in lakes
tarits 2003). (Weithoff 2003). This could be important for BEF
Discrete functional groupings continue to be research given the short generation times associated
employed in studies of functional diversity. For with phytoplankton, allowing true succession to
example, Berg et al. (2004), Bret-Harte et al. (2004), take place in one season. Finally, it has been dem-
Chu et al. (2006), Dimitrakopoulos et al. (2006), onstrated that even for species-rich systems like
Downing (2005), Fischer et al. (2007), Krab et al. coral reefs, a single functionally important family,
(2008), Micheli and Halpern (2005), Moretti (2006), parrotfish, are the only creatures carrying out sig-
and Zavaleta and Hulvey (2007) all used trophic nificant bioerosion, a major reef process (Bellwood
groups, functional groups or grass/forb/legume et al. 2003). Without attempting to quantify the
classifications. In many cases, the use of discrete functional diversity of ecosystems and the con-
functional groupings seems to be a result of the sequences of loss of that diversity in an appropriate
difficulty in applying trait-based functional diver- way, we are in danger of overlooking a crucial
sity measures to real systems. The large amounts aspect of BEF relationships.
of data collection necessary for appropriate Other studies that cite these key functional
trait clustering may prove impractical for many diversity methods papers discuss the use of traits
studies. Additionally, there may be a perception (Cornelissen et al. 2003, Norberg 2004, Poff et al.
that the subjectivity surrounding the choice and 2006, Barnett et al. 2007) and species abundances
number of traits makes continuous measures as (de Bello et al. 2007, Lavorel et al. 2008) in quan-
arbitrary as discrete measures of functional diver- tifying functional diversity. There is also a signif-
sity. This point is further highlighted by the icant body of work that recommends the use of
number of authors that have used variations of functional diversity as an ecological indicator in
the main continuous functional diversity measures environmental impact assessment (Bady et al.
(Roscher et al. 2004, Fukami et al. 2005, Pavoine 2005, Heino 2005, Mouillot et al. 2005b, Dierssen
and Doledec 2005) or proposed additional func- 2006, Henle et al. 2006, Mouillot et al. 2006).
tional diversity indices (Dumay et al. 2004, Ricotta Here, in the presence of increased environmental
2004, Bady et al. 2005, Mouillot et al. 2005a, stress, the range of functional attributes is likely
Thuiller et al. 2006a). to be narrow as only the most adapted species
In spite of this apparent reluctance to embrace survive, with the niche filtering concept suggest-
continuous measures of functional diversity in ing that surviving species will share many bio-
empirical BEF studies, there seems to be an logical characteristics (Franzén 2004, Statzner and
increasing appreciation for the benefits of these Moss 2004).
measures over discrete functional groupings. A
bootstrap analysis on empirical data from the
BIODEPTH experiments shows that FGR has rel- 4.4 Differences between measures.
atively poor power for explaining variation in an Effects of species richness on functional
ecosystem process (Petchey 2004). Naeem and diversity
Wright (2003), Jax (2005), Ricotta (2005a) and
4.4.1 Background
Bulling et al. (2006) have all recommended the use
of functional diversity for advancing the under- Biodiversity can affect ecosystem processes by a
standing of how biodiversity affects ecosystem variety of routes (Tilman 1999b, Chapin et al.
functioning, rather than focusing just on species 2000c). As biodiversity changes, so does composi-
diversity. There has been a call for studies of tion and richness. For example, an invasion adds
parasite biodiversity to look to taxonomic and a novel species with a novel identity, thereby
functional diversity for patterns and processes that changing composition; it also increases species
 A FUNCTIONAL GUIDE TO FUNCTIONAL DIVERSITY MEASURES 55

richness by one. During the late 1990s and into 4.4.2 Methods
the first decade of the twenty-first century an
A collection of local assemblages varying in species
acrimonious debate flared around these effects
composition and richness were simulated. The spe-
(Loreau et al. 2001). Which was more important:
cies richness gradient, from six to 20 species, was
the effects of the identity of a novel species, or
constructed by randomly selecting species from a
the effects of having one more species (Loreau et al.
regional species pool containing 20 species. At each
2001)?
species richness level there were up to five distinct
Experimental and theoretical results suggested
communities, each containing a different random
that both can be important in different situations
composition of species. Obviously, there was only
(Hooper and Vitousek 1997, Huston 1997, Tilman
one composition possible for the 20 species com-
1997). One investigation focused on the effects of
munity, and some random draws within a richness
species richness and composition on functional
level may have contained the same set of species.
diversity (Petchey and Gaston 2002a). When is
Five sets of assemblages that each represented an
functional diversity affected strongly by species
extinction trajectory from 20 to six species were also
richness, and when strongly by species composition?
constructed. These trajectories are useful to know
Since functional diversity should relate with eco-
how loss (or gain) of a species can affect a functional
system processes, the answer to this question
diversity measure.
also informs about the relative importance of species
The functional diversity of each local community
richness and composition for ecosystem processes.
was calculated by the methods described in Section
Since the then-dominant measure of functional
2 (CHV, FDvar, MD, Q, FD, FDLD). Simulations and
diversity, namely functional group richness,
measurements of all measures of functional diver-
was problematic for answering questions about
sity were made in R (R Development Core Team
the importance of species richness, Petchey and
2008). Where required, distances were Euclidean
Gaston (2002a) developed a continuous measure
and the clustering algorithm was UPGMA. Contact
(FD – see above). Results of this and a related
OLP for R script to calculate the measures of func-
study (Petchey and Gaston 2002b) indicated that
tional diversity, including convex hull volume.
the effective dimensionality of trait space deter-
Calculating convex hull volume is complex
mined the relative importance of species richness
(Cornwell et al. 2006). In the R library geometry
and composition. The effects of species richness
(Grasman and Gramacy 2008) the function convhulln
were strongest in high dimensional space; the
interfaces the Qhull library (Barber et al. 1996). For
effects of composition dominated in low dimen-
one dimensional data (one trait) we made CHV the
sional space.
range of the data (maximum value minus the mini-
The effective dimensionality of trait space results
mum value). CHV requires that the number of spe-
from the number of traits used to measure func-
cies is greater than the number of traits, since each
tional diversity and the correlation (or lack thereof)
species is a vertex in the convex hull, hence the
between them. Many uncorrelated traits means
lowest richness in the simulations was six species.
high effective dimensionality, while many corre-
We made two separate sets of simulations. In one,
lated traits or few traits (regardless of correlation)
species differed in only one trait, and in the other
means low effective dimensionality.
they differed in five traits. Trait values were drawn
Thus the nature of the variation among species
from a normal distribution with a mean of zero and
was critically important for understanding patterns
standard deviation of one. When there were five
of functional diversity. Furthermore, Petchey and
traits, there were no correlations between them.
Gaston (2002a) found that this conclusion was
robust to details of how their functional dendro-
gram was constructed. Here, we extend Petchey 4.4.3 Results
and Gaston’s simulations and ask how robust is The effect of trait number (one versus five) was
their conclusion in the face of variation in how consistent across all six diversity measures.
functional diversity is measured. Increasing the number of traits caused a greater
56 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

(a) 1.0 (b) 1.0 (c) 1.0

0.8 0.8 0.8

0.6 0.6 0.6

FDLD
CHV
FD

0.4 0.4 0.4

0.2 0.2 0.2

0.0 0.0 0.0

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20
Species richness Species richness Species richness

(d) 1.0 (e) 1.0 (f) 1.0

0.8 0.8 0.8

0.6 0.6 0.6

FDLD
CHV
FD

0.4 0.4 0.4

0.2 0.2 0.2

0.0 0.0 0.0

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20
Species richness Species richness Species richness

Figure 4.1 Simulated relationships between three measures of functional diversity (FD, CHV, FDLD; see Section 4.4 for explanation) when species in
the regional pool differ in one trait dimension (top row) or five trait dimensions (bottom row). At each richness level there are five different
communities (filled circles), each a random draw of species from the regional pool. There are also five extinction trajectories, from 20 species to six
species, shown by unbroken lines.

effect of species richness on functional diversity and one (FDvar) appeared to show a negative
values, and a weaker effect of species composition. relationship (Fig. 4.2).
The effect was clearest for FD, CHV, and FDLD Effects of species loss differed qualitatively
(Fig. 4.1), and was also present for MD, Q, and between the six measures. Two (FD and CHV)
FDvar (Fig. 4.2). With one trait, values of functional either decreased or remained the same when a
diversity varied greatly within a level of species species was lost (Fig. 4.1). The other four (FDLD,
richness (panels (a), (b), and (c) in Figs. 4.1 and MD, Q, FDvar) decreased, increased, or remained
4.2); there was much reduced variation with five unchanged (Figs. 4.1 and 4.2).
traits (panels (d), (e), and (f) in Figs. 4.1 and 4.2).
Similarly, with one trait, different sequences of
4.4.4 Conclusions
species loss had very different effects on the loss of
functional diversity. With five traits, loss of func- The effect of number of traits on the relative
tional diversity was more similar among different importance of species richness and composition
sequences of species loss. (Petchey and Gaston 2002a), appears robust to dif-
The general relationship between species rich- ferent measures of functional diversity. Therefore,
ness and functional diversity differed greatly to understand the effects of richness and composi-
among the six measures. Three (FD, CHV, and tion, the choice of which traits to include in mea-
FDLD) exhibited an overall positive relationship sures of functional diversity is obviously critical.
with species richness (Fig. 4.1). Two (MD and Q) The choice of which functional diversity measure to
exhibited little relationship with species richness, use with this question is less important. This
 A FUNCTIONAL GUIDE TO FUNCTIONAL DIVERSITY MEASURES 57

(a) 1.0 (b) 1.0 (c) 1.0

0.8 0.8 0.8

0.6 0.6 0.6

FDvar
MD
Q

0.4 0.4 0.4

0.2 0.2 0.2

0.0 0.0 0.0

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20
Species richness Species richness Species richness

(d) 1.0 (e) 1.0 (f) 1.0

0.8 0.8 0.8

0.6 0.6 0.6

FDvar
MD
Q

0.4 0.4 0.4

0.2 0.2 0.2

0.0 0.0 0.0

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20
Species richness Species richness Species richness

Figure 4.2 Simulated relationships between three measures of functional diversity (Q, MD, FDvar; see Section 4.4 for explanation)
when species in the regional pool differ in one trait dimension (top row) or five trait dimensions (bottom row). All other details are the
same as in Fig. 4.1.

reinforces previous findings (e.g. Petchey and is correct (Ricotta 2005a); only FD and CHV meet
Gaston 2002a) that details of the functional diver- this criteria. However, others suggest that mea-
sity measure (such as distance measure and clus- sures of functional diversity should not be closely
tering method) may have little importance relative correlated with species richness, or even that
to choosing appropriate sets of traits. functional diversity should be independent of
The qualitative effect of species richness on species richness (e.g. Mason et al. 2003). It remains
functional diversity does, however, differ between unclear, however, how to reconcile these ideas
diversity measures. For example, FD, CHV, and with the suggestions that increases (or decreases)
FDLD generally increase with increases in species in species richness cannot cause a decrease or
richness, while the others (MD, Q, FDvar) do not. (increase) in functional diversity. Furthermore,
This broad difference results from the fact that loss there may be multiple ‘facets’ to functional diver-
of a species can cause increases in some measures sity that are not included in our analyses. For
of functional diversity (MD, Q, FDvar), but cannot example, how regularly are species distributed in
cause an increase in other measures (FD, CHV). trait space, and the regularity of the distribution of
FDLD can increase, but only rarely and by small species abundances in trait space (Villéger et al.
amounts (Figs. 4.1(c) and (f)). Should a measure of 2008). Indeed, adding species abundances to
functional diversity be able to increase when an measures of functional diversity greatly increases
extinction occurs? Should a measure be able to the complexity of measurement.
decrease when a species is added? Why do some measures behave very differently
Suggestions that the answer to the last two from others? Consider the idea of the species
questions is ‘no’ mean that a positive relationship in an assemblage forming a cloud of data in
58 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

n-dimensional trait space. FD and CHV are intui- of new measures of functional diversity in Table
tively similar, and both measure, in some broad 4.1), and far too little effort thinking about which
sense, the volume of trait space that is represented traits to include. What traits of plants are important
by the data cloud. As they both measure volume (in determinants of biomass production (Díaz and
some sense), adding a species cannot cause a Cabido 1997)? What traits of stream invertebrates
decrease, and removing a species cannot cause an are important determinants of leaf litter breakdown
increase. They do, however, differ in the sense that (Jonsson and Malmqvist 2000)? To stand any
volume is measured. CHV is the minimum (con- chance of measuring functional diversity correctly,
vex) volume that includes all the species (points in these questions (and those about the traits of other
the data cloud). Whether any species, or how many organisms) must be answered. Which traits to
species, occupy the space inside the convex hull has include is a great challenge – ‘great’ in the sense
no effect on CHV. This is clear in Fig. 4.1(b), where that it gives a reason and opportunity to spend time
loss (or addition) of species often has no effect on learning more about what the organisms in eco-
CHV. Furthermore, CHV is influenced perhaps systems do.
more than other measures by the most extreme (i.e. If we are confident that we have the functionally
minimum and maximum) trait values, since these, important traits, only then can we ask ‘which
by definition, determine the volume. In contrast, measure?’ There certainly isn’t one answer to this
FD measures, in a sense, a combination of the size question, but here are some thoughts on how to
of the data cloud, and how filled in is the data decide. First, decide if you (i.e. your ecological
cloud. That is, FD is affected both by the range of question) need a measure of functional diversity
trait values present, and by the different species that includes evenness in relative abundances of
that might occur within the range. (FDLD is in these species (Q and FDvar) (Ricotta 2007). In doing so,
respects similar to FD and CHV.) note that a ‘yes’ answer means that addition of a
MD, Q, and FDvar are also intuitively similar to species can decrease functional diversity and loss
each other. These each represent, in some sense, the of a species can increase it (Figs. 4.1 and 4.2, panels
average distance between species in n-dimensional (d) and (e)). If you need a measure that does
space. Here, adding a species that lies close to not include species’ relative abundances, and does
several other species can decrease the average dis- not allow addition (or loss) of species to decrease
tance, or increase it if the new species is distant (or increase) functional diversity, then FD or
from most others. Conversely, removing a species CHV are appropriate. If you need a measure that
that lies close to other species will likely increase incorporates how much of a range of trait
the average distance. space is filled choose FD; otherwise CHV is likely
sufficient.
If you can’t make up your mind about any of
4.5 Discussion these questions, or are curious, see how the answer
to your particular question depends on the measure
4.5.1 Which measure?
(as in Section 4.4). You may find, as here, that the
First, this question is secondary to that of which choice of measure is less important than which
traits to include (Naeem and Wright 2003, Lep
s et traits are included in the measure.
al. 2006, Petchey and Gaston 2006). Indeed, the
question of what qualifies as a ‘functional trait’ may
4.5.2 Conclusions
be complex and hierarchical (Violle et al. 2007). The
measure can be less important than the traits What is the significance of this enormous activity
included (Figs. 4.1 and 4.2), and this phenomenon is in developing metrics for the quantification of
probably quite general. A consequence is that we functional diversity? Functional diversity is a vital
risk focusing too much effort on the rather ‘easy’ component of research about the functional con-
practice of inventing new measures and modifying sequences of biodiversity (Biodiversity-Ecosystem
old ones (as demonstrated by the high proportion Functioning, or BEF research). Indeed, the
 A FUNCTIONAL GUIDE TO FUNCTIONAL DIVERSITY MEASURES 59

Millennium Ecosystem Assessment concluded that Other important challenges remain. The data
species per se is less important than what the spe- demands of including intraspecific variability in
cies do. Arguably this knowledge was implicit in measures of functional diversity (Cianciaruso et al.
the design of some of the earliest biodiversity 2009). It seems clear, however, that variation
experiments. For example, Naeem et al. (1994) among the individuals in a species could have
chose for the Ecotron experiments a functionally important effects on community and ecosystem
balanced set of plant species. Consequently, the processes (e.g. Pachepsky et al. 2007). Another
ecosystem services that humans rely upon are challenge is how to estimate total functional
more likely related with the functional diversity diversity from a sample. Rarefaction methods can
of organisms, rather than taxonomic or phyloge- be applied to functional diversity measures and
netic diversity. The examples in Section 4.3 pro- have potential (e.g. Walker et al. 2008). Perhaps
vide some empirical evidence for this. The most importantly, we need to carry out experi-
explosion of different measures may represent the ments that test the assumptions and predictions of
recognized importance of creating an accurate and functional diversity. The knowledge from these
predictive measure. It has always been clear that will help us understand the broad ecological
we first need to know which traits are important questions to which functional diversity can make a
for each ecosystem service we might choose to significant contribution.
focus on. Our analyses in Section 4.4 show that
the choice of traits may hold more sway than the
4.6 Acknowledgements
choice of a functional diversity index. The conclu-
sion must therefore be that understanding species’ We thank participants at the BioMERGE-DIVER-
natural histories (traits) and how these interact with SITAS meeting in Ascona, Switzerland, in
their environment is a prerequisite for functional December 2006, including Justin Wright, Martin
diversity to be a concept that can lead to management Solan, Katia Engelhardt, Mahesh Sankaran, and
and conservation of ecosystem services. Dan Bunker.
 CHAPTER 5

Forecasting decline in ecosystem

services under realistic scenarios
of extinction
J. Emmett Duffy, Diane S. Srivastava, Jennie McLaren, Mahesh
Sankaran, Martin Solan, John Griffin, Mark Emmerson,
and Kate E. Jones

5.1 Introduction
concerted research effort arose to identify and
Estimates suggest that Earth is in the midst of the understand the relationships between changing
sixth mass extinction in its history, with rates of biodiversity and functioning of ecosystems (Schulze
species loss 3–4 orders of magnitude above the and Mooney 1994). Using synthesized communities
average over geologic time (Pimm et al. 1995, Dirzo of different species richness under controlled con-
and Raven 2003). Unlike previous mass extinctions ditions in field plots and in the lab, researchers
caused by asteroid impacts, intense volcanism, or focused explicitly on the question of how the
geochemical changes (Vermeij 2004), the current number of species (or functional groups) within a
crisis is driven by an entirely unprecedented phe- community influences aggregate ecosystem prop-
nomenon: human transformation of the global erties such as productivity and resource use (Kinzig
environment (Vitousek et al. 1997, Sala et al. 2000). et al. 2001, Loreau et al. 2001, Loreau et al. 2002,
The principal drivers of this extinction are habitat Hooper et al. 2005, and Chapters 1–3). Theoretical,
loss, over-exploitation, pollution, and impacts of experimental and observational validation studies
invasive species (Purvis et al. 2000c). These drivers of biodiversity-ecosystem functioning linkages have
have not only dramatically increased the back- subsequently developed into a growth industry, as
ground rate of extinction, but they have also gen- the present volume attests.
erally reduced biodiversity at local scales, and Motivated in part by conservation concerns, ini-
altered the species composition of communities. tial studies focused on the likely environmental
Superimposed on global and local declines in consequences of biodiversity loss, but the compli-
diversity, the distributions of many remaining cated experiments and mixed interpretations soon
species are being radically altered as human activ- refocused efforts on nuances of design and statistics
ities transport them, intentionally or otherwise, to (Huston 1997, Allison 1999, Loreau and Hector
new regions and habitats. Establishment of these 2001). One early result was that experiments
non-native species can increase local species rich- examining biodiversity-ecosystem function links
ness, but further alters the composition of commu- converged on a ‘random assembly’ design, which
nities (Sax and Gaines 2003) and ultimately leads to synthesized simple – but often artificial – commu-
homogenization and decline of biodiversity across nities of varying species richness under controlled
the globe. conditions and measured changes in ecosystem
These changes in biodiversity have raised serious properties along the gradient in species richness
concerns about their consequences for human wel- (Schmid et al. 2002a). While this approach is capable
fare. Partly for this reason, in the early 1990s a of rigorously partitioning the effects of species

60
 FORECASTING DECLINE IN ECOSYSTEM SERVICES 61

number and interactions on ecosystem processes a morphological, behavioural, or physiological

(Chapter 7), the factors producing diversity change characteristic of an organism that affects perfor-
were unspecified and, implicitly, regarded as mance. Thus, in this original sense, it is inherently
unimportant. As a consequence, the focus of related to function. We use the term in essentially
experiments became disconnected from the pro- this sense here, emphasizing that a trait is a prop-
blems of applied conservation science (Srivastava erty that can, in principle, be measured on an
2002, Duffy 2003, Srivastava and Vellend 2005). individual organism.
Despite their statistical advantages, it has been rec- Making the connection from environmental
ognized for some time that the random assembly change to altered ecosystem services can be thought
designs common in biodiversity and ecosystem of as a process involving three overlapping stages.
functioning experiments usually do not mimic real- Given a particular driver of environmental change,
world processes of diversity loss (for a counter- we need first to know whether it will cause an
example, see the sensitivity to stress scenario in extinction or decline of species: trait-based models of
Solan et al. 2004), which arise as traits of organisms vulnerability can make testable predictions about
mediate responses to specific drivers of environ- what kinds of species will be lost (and gained). The
mental change (Huston 1997, Grime 1998, Srivastava second stage is structural reorganization: basic prin-
2002, Giller et al. 2004, Lep
s 2004). In essence, ran- ciples of trait-based community interactions and
dom assembly designs trade off realism for precision succession can be used to predict how a community
in interpretation. To assess the implications of reorganizes in response to species loss and gain.
this trade-off, theory (Gross and Cardinale 2005), Third, and finally, is functional reorganization: trait-
simulations (Petchey and Gaston 2002b, Ostfeld based principles of physiology and ecology and
and LoGiudice 2003, Solan et al. 2004, McIntyre et al. insights from biodiversity and ecosystem function-
2007), and experiments (Jonsson et al. 2002, Zavaleta ing research can, in principle, predict consequences
and Hulvey 2004) have begun to explore effects of the changed community structure for biomass
on ecosystem properties of non-random extinction, distributions, and rates of productivity and bio-
simulating explicit loss scenarios based on vulner- geochemical processes.
ability of species with certain traits or mimicking A simple example of application of this trait-based
natural gradients of diversity loss in nature (see framework involves the trophic cascade: (1) the
Fig. 3.1). correlated traits of large body size, carnivory, and
In this chapter we explore the prospects for a associated ‘slow’ life history (low fecundity and
more rigorous linkage of biodiversity and ecosys- population growth rate, long generation time) ren-
tem functioning research to empirically based pro- der species vulnerable to overexploitation and
cesses of extinction. The key to developing a harassment, (2) consequent loss of large predators
general predictive framework for relating environ- causes relatively predictable structural changes in a
mental change, through biodiversity change, to community, typically increasing abundance of their
effects on ecosystem services is a focus on organ- herbivore prey and indirectly reducing plant abun-
ismal traits (Chapin et al. 1997, Hooper et al. 2002, dance, and (3) these structural changes produce
Lavorel and Garnier 2002, Naeem and Wright 2003, functional changes, typically including reduced pri-
McGill et al. 2006), and specifically the correspon- mary productivity. This general phenomenon has
dence, or lack thereof, between (1) response traits been observed in a wide range of ecosystem types in
that influence risk of decline or extinction in response to habitat alteration and hunting (e.g. Pace
response to a driver, (2) traits – involving both et al. 1999), showing that some degree of generali-
response and effect – that mediate community zation is possible in linking realistic impacts of
reorganization after primary extinction(s), and (3) environmental change, through changing biodiver-
effect traits that influence ecosystem functioning. sity to changing ecosystem functioning.
The term ‘trait’ has been used in a variety of ways Although we are a long way from generalizing
and its history is fraught with some confusion such an integrated approach, important advances
(Violle et al. 2007). Darwin used the term to refer to have been made. We can begin such an integration
62 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

by summarizing what is known about how organ- properties of the organisms interacting with their
ismal traits affect risk of extinction under major environments. We focus here primarily on intrinsic
drivers of environmental change, how traits influ- traits of individual organisms.
ence community reorganization following extinc-
tions, how traits affect major ecosystem processes, 5.2.2 Empirical results
and the degree of covariance among these response
and effect traits. To date, efforts to ‘connect the dots’ As a first pass at finding general patterns linking
between these components have focused mainly on response traits to extinction risk, we searched the
plant assemblages (e.g. Díaz and Cabido 1997, literature for data relating intrinsic organismal traits
Lavorel and Garnier 2002, Díaz et al. 2007). Here we to species decline as a basis for developing empir-
begin to extend trait-based approaches linking ically based extinction trajectories and predicting
extinction and ecosystem functioning to multitrophic their ecosystem impacts. We focused on several
ecosystems and we review the few empirical studies drivers of environmental change known, suspected,
that have explicitly addressed how realistic extinc- or anticipated to be important in affecting species
tion scenarios affect ecosystem functioning. abundance and distribution; these included loss or
fragmentation of habitat, nitrogen deposition,
atmospheric CO2 concentration, climate warming,
5.2 Extinction filters: environmental precipitation, and exploitation. Most of the empiri-
change and response traits mediating cal studies we found correlated intrinsic organismal
decline traits with species decline or rarity in response to
these factors (Tables 5.1 and 5.2).
5.2.1 Background
A notable feature of the results is the contrast
Recent years have seen major growth in under- between patterns for plants and animals. The studies
standing how organismal traits predispose species of plant population decline that we found consid-
to endangerment and extinction, across a range of ered nearly the full spectrum of drivers, including
environmental drivers and taxa including plants nitrogen deposition, habitat fragmentation and loss,
(Suding et al. 2005, Wiegmann and Waller 2006), atmospheric CO2 concentration, warming, and pre-
amphibians (Lips et al. 2003, Cooper et al. 2008), cipitation (Table 5.1). The animal studies spanned a
reptiles (Foufopoulos and Ives 1999), birds (Gaston narrower range of drivers, mostly involving habitat
and Blackburn 1995, Davies et al. 2007), mammals loss (including fragmentation and conversion),
(Purvis et al. 2000a, Fisher et al. 2003, Jones et al. which was also a major driver for plant decline, and
2003, Blackburn et al. 2005, Cardillo et al. 2005), and overharvesting (Table 5.2). These different foci may
marine fishes (Jennings et al. 1998, Jennings et al. reflect real differences in processes driving decline of
1999, Dulvy et al. 2004), as well as some synthesis animal versus plant species, but it is also possible
across taxa (Purvis et al. 2000c). The probability that that research effort or perception of which drivers
a species will go extinct depends both on intrinsic are most important may differ among animal and
traits, such as body size and degree of habitat plant ecologists, or among marine and terrestrial
specialization, and on extrinsic factors. There is researchers (Raffaelli et al. 2005b). For example,
abundant evidence that low population density, despite the paucity of studies linking plant extinction
small geographic range, and proximity to human to harvesting, it’s clear that a number of medicinal
populations increase risk of decline and extinction and ornamental plant species have been endangered
across a broad spectrum of plant and animal taxa by harvesting, including the rosy periwinkle (Cath-
(e.g. Laurance 1991, Foufopoulos and Ives 1999, aranthus roseus) of Madagascar and the Pacific yew
Purvis et al. 2000b, Harcourt et al. 2002, Jones et al. (Taxus brevifolia) in the USA. The plant studies also
2003, Blackburn et al. 2004, Cardillo et al. 2004, tended to focus on functional groups (grasses, forbs,
Henle et al. 2004, Hero et al. 2005, Kiessling and trees), life history syndromes (perennial, annual),
Aberhan 2007). Despite their clear importance, and taxonomic groups (dicots, legumes) rather than
these characters are, at least in part, emergent individual species, such that the plant analyses often
 FORECASTING DECLINE IN ECOSYSTEM SERVICES 63

Table 5.1 Plant traits associated with population change in response to environmental change in empirical studies. Response shows the sign of population
change associated with the listed trait.

Driver Trait Response Reference

N-deposition Life history: perennial – 1

Taxonomy: legumes – 1
Pollination: self – 2
Growth form: forbs – 3
Growth form: trees – 4
Growth form: grasses þ 3
Habitat loss and fragmentation Stature: short – 5, 6, 7
Seed longevity: short – 2
Seed size: large – 8
Dispersal: wind – 5
Dispersal: ant – 5
Seed size: small – 6
Taxonomy: legumes – 6
Taxonomy: dicots – 7
Pollination: animal-assisted – 9, 10
Global change (increased CO2) Growth form: C4-grasses – 11, 12
Growth form: C4-grasses 0 13
Growth form: C3-grasses – 13, 14, 15
Growth form: C3-grasses þ 11
Growth form: forbs þ 11, 12, 13, 14, 15
Growth form: C3-trees þ 16, 17
Taxonomy: legumes þ 11, 14
Global change (warming) Growth form: shallow-rooted forbs – 18
Growth form: forbs – 19
Growth form: forbs þ 3
Growth form: grasses 0 3
Growth form: tap-rooted forbs 0/þ 18
Growth form: shrubs þ 19
Global change (increased precipitation) Growth form: grasses 0 3
Growth form: trees þ 4, 20, 21
Growth form: forbs þ 3

1 Suding et al. (2005); 2 Freville et al. (2007); 3 Zavaleta et al. (2003); 4 Davis et al. (1999); 5 Williams et al. (2005); 6 Leach and Givnish
(1996); 7 Duncan and Young (2000); 8 Cramer et al. (2007); 9 Sodhi et al. (2008); 10 Aguilar et al. (2006); 11 Reich et al. (2001); 12 Polley et al.
(2003); 13 Owensby et al. (1999); 14 Teyssonneyre et al. (2002); 15 Potvin and Vasseur (1997); 16 Polley et al. (1997); 17 Bond and Midgley
(2000); 18 Cross and Harte (2007); 19 Harte and Shaw (1995); 20 Kraaij and Ward (2006); 21 Davis et al. (1998).

considered suites of co-occurring traits. Although trait per se. Despite its ambiguous nature, we have
animal studies more commonly addressed single retained trophic level as a ‘trait’ in our analyses,
traits such as body size and habitat specialization, since it is at least partly dictated by individual-level
many also identified one or more components of a traits (body morphology, dentition, digestive physi-
multi-trait ‘slow life history’ syndrome as a risk ology, etc.), and is relatively conserved within
factor. Finally, several animal studies found that clades. We recognize, however, that future research
extinction risk was greater at higher ‘trophic level’, a would benefit from more rigorous identification of
complex concept defined by the organism’s interac- the intrinsic traits that dictate an organism’s trophic
tion with its environment, rather than an organismal level.
Table 5.2 Animal traits associated with population change in response to environmental change in empirical studies. Response shows the sign of population change associated with the listed trait. We follow the
original authors in treating trophic level as a ‘trait’, although this is a proxy for a syndrome of intrinsic traits and interactions with the external environment (see text).

Fish Reptiles Mammals Birds Invertebrates

Driver Trait Response Reference Response Reference Response Reference Response Reference Response Reference

Habitat loss and Body size: large – 1 –––– 2, 3, 4, 5 ––0 6, 7, 8 000 9, 10, 11
fragmentation
Body size: small –0 8, 12
Specialization – 1 ––– 13, 14, 15 –– 2, 16 ––––0 7, 12, 17, 18, 19 –– 20, 21
Life history: ‘slow’ – 1 ––– 16, 22, 23 ––0 18, 24, 12
Trophic level: high – 22 –––––0 9, 10, 25, 26,
27, 11
Climate warming Specialization – 28 – 29
Exploitation Body size: large –––– 30, 31, 32, 33 – 12
Specialization 0 12
Life history: ‘slow’ –– 30, 33 – 34 – 12
Trophic level: high –– 35, 36
Undifferentiated Body size: large 0 37 0 38 ––– 6, 39, 40
Body size: small – 41
Specialization – 37 – 14 ––– 39, 40, 42 –– 43, 44
Life history: ‘slow’ – 41 0 38 – 42
Trophic level: high 0 38 ––– 39, 40, 42

1 Olden et al. (2008); 2 Harcourt et al. (2002); 3 Cardillo et al. (2005); 4 Collen et al. (2006); 5 Johnson et al. (2002); 6 Gaston and Blackburn (1995); 7 Feeley et al. (2007); 8 Foufopoulos and Mayer
(2007); 9 Didham et al. (1998a); 10 Davies et al. (2000); 11 Starzomski and Srivastava (2007); 12 Owens and Bennett (2000); 13 Foufopoulos and Ives (1999); 14 Segura et al. (2007); 15 Watling and
Donnelly (2007); 16 Laurance (1991); 17 Shultz et al. (2005); 18 Jiguet et al. (2007); 19 S ekericioglu et al. (2002); 20 Kotiaho et al. (2005); 21 Charrette et al. (2006); 22 Purvis et al. (2000b);
_
23 Jones et al. (2003); 24 Amano and Yamaura (2007); 25 Didham et al. (1998b); 26 Gilbert et al. (1998); 27 Hoyle (2004); 28 Laidre et al. (2008); 29 S ekericioglu et al. (2008); 30 Jennings et al.
_
(1998); 31 Jennings et al. (1999); 32 Dulvy et al. (2004); 33 Reynolds et al. (2005); 34 Bodmer et al. (1997); 35 Pauly et al. (1998); 36 Hutchings and Baum (2005); 37 Angermeier (1995);
38 Brashares (2005); 39 Gillespie (2001); 40 Boyer (2008); 41 Cooper et al. (2008); 42 Kruger and Radford (2008); 43 Biesmeijer et al. (2006); 44 Gonzalez–Megias et al. (2008)
 FORECASTING DECLINE IN ECOSYSTEM SERVICES 65

Our survey of response traits suggests a few have seldom been considered in this context (Duffy
potential generalizations. For plants, these are more 2003, Thebault and Loreau 2003, Thebault and Lor-
tentative than for animals: there is abundant evi- eau 2006, Duffy et al. 2007). The long and rich history
dence that commonly recognized plant growth of research linking plant traits to environmental
forms respond differently to a variety of environ- gradients is also highly relevant to biodiversity and
mental change drivers. The most consistent such ecosystem functioning research. Although plant
pattern we found is that rising atmospheric CO2 biodiversity and ecosystem functioning research has
tends to increase the abundance of forbs at the historically focused on species and functional
expense of grasses, and possibly favours C3 over groups, a more explicit focus on traits better
C4 plants. There is also some evidence that warm- approaches the mechanistic processes linking envi-
ing and increased precipitation favour shrubs and ronmental change to ecosystem processes (e.g.
trees over grasses. More generally, however, the McGill et al. 2006). Such trait-focused research is
responses of plants to environmental change appear providing important generalizations linking envi-
idiosyncratic. This likely reflects the context- ronmental change through biodiversity change to
dependency of trait associations with response to ecosystem functioning (Lavorel and Garnier 2002,
environmental change (Lavorel and Garnier 2002, Diaz et al. 2004, Díaz et al. 2007, Suding et al. 2008).
Eviner and Chapin 2003, Brook et al. 2008). Some caveats are in order. We, like most previous
For animals, the patterns appear somewhat authors, have considered both drivers of environ-
clearer. The major drivers of decline and extinction mental change and traits singly (with the exception
of animal species are generally recognized to be of trait syndromes such as ‘slow life history’ and
habitat loss (including fragmentation and conver- ‘trophic level’). However, multiple drivers typically
sion) and overexploitation (Purvis et al. 2000c). For operate simultaneously and synergistically (Sala
most animal taxa studied, analyses considered how et al. 2000, Brook et al. 2008), and different traits can
traits correlated with rarity in space or decline also interact to increase risk of extinction above that
through time, assuming that these are functions of expected from individual trait values, as demon-
both habitat loss and exploitation/persecution. For strated for desert fishes (Davies et al. 2004, Olden
marine fishes, there is some confidence that over- et al. 2008). Moreover, the importance of intrinsic
harvesting is indeed a major driver of the patterns biological traits in predicting extinction can be
observed (Dulvy et al. 2005, Olden et al. 2007). sharpened in proximity to dense human popula-
The studies we reviewed suggest that the response tions, as demonstrated for carnivores (Cardillo et al.
traits that render animal species vulnerable to these 2004). Thus, a pressing direction for future work is
drivers, across a disparate range of taxa including study of how synergisms between single and mul-
mammals, birds, fishes, reptiles, and even some tiple drivers of extinction, and among traits, influ-
insects, are surprisingly consistent and include ence community reorganization and, thus,
large body size, high trophic level, and specializa- ecosystem functioning (Sala et al. 2000, Vinebrooke
tion in diet and/or habitat (Table 5.2). A similar et al. 2004, Starzomski and Srivastava 2007).
result also emerges from a very different source: in
experimental microbial food webs exposed to
environmental warming, extinctions occurred dis- 5.3 Structural reorganization: traits
proportionately among top predators and herbi- and community organization
vores (Petchey et al. 1999).
5.3.1 Background

5.2.3 Summary Predicting how a community reorganizes in

response to environmental change encompasses the
The vulnerability of large animals and high trophic whole of community ecology, so generalizing the
levels emphasizes that studies of predator loss and role of organismal traits in this process is accord-
trophic cascades are directly relevant to biodiversity ingly challenging. By analogy with ecosystem
and ecosystem functioning research, though they functioning, community reorganization can be
66 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

considered to involve both response and effect compensation effect decays with further extinctions
traits, although these have received less attention in (Ives and Cardinale 2004). But competition and
community ecology (McGill et al. 2006). In the other interactions also complicate predictions. In a
context of community organization, response traits dynamic theoretical simulation, Ives and Cardinale
are those that mediate an organism’s sensitivity to (2004) confirmed that, in the absence of interactions
influences such as interspecific competition (e.g. among species, extinction order could be perfectly
plant biomass and height, Gaudet and Keddy 1988), predicted from species’ direct tolerances to the
grazing (e.g. plant height and life history, Díaz et al. theoretical stressor. However, extinction order was
2007), and changing resources (e.g. specific leaf less predictable in the presence of strong interspe-
area, Ackerly and Cornwell 2007); effect traits are cific interactions because compensation among
those that mediate an organism’s influence on other remaining species after an initial extinction changed
species, such as predator hunting mode and habitat the interaction pathways in the web. Moreover, the
breadth (Schmitz et al. 2004, Schmitz 2008). In mechanism by which species diversity affects
principle, community organization stems from function is also important here. Specifically, com-
interactions mediated by such response and effect pensation amplifies differences between extinction
traits, and the positive or negative feedbacks from scenarios when diversity–function effects are driven
these changes that influence community structure. by resource partitioning, but has less effect when
One indirect approach to linking traits with they are driven by facilitation or sampling
species interactions is to focus on how distribu- mechanisms (Gross and Cardinale 2005).
tions of traits within communities are influenced
by key community interactions. An example on a
5.3.2 Empirical results: compensation
large scale is the global synthesis of data on how
terrestrial plant assemblages respond to ungulate Several simulation studies have examined the
grazing. Meta-analysis of 197 studies from all over influence of biomass compensation in mediating
the world revealed that grazing favoured annuals the impacts of primary extinctions on ecosystem
over perennials, short plants over tall plants, processes. Solan et al. (2004) showed that the
prostrate over erect plants, and stoloniferous and degree of numerical compensation among marine
rosette architecture over tussock architecture (Díaz benthic invertebrates can have a large impact on
et al. 2007). Such comparative studies provide predicted changes in biogenic mixing depth under
insight on how traits are linked to interactions but different extinction scenarios (Fig. 5.1). Specifi-
do not reveal the dynamic responses of interacting cally, when extinction order was random, com-
species. pensation by remaining species maintained
In the context of biodiversity and ecosystem community-level function (biogenic mixing depth)
functioning research, two aspects of community down to very low levels of species richness;
structural reorganization have received most interestingly, this compensation was much less
attention to date. The first is biomass or numerical effective when extinction proceeded in a more
compensation, i.e. growth or expansion of remaining realistic order by body size (Fig. 5.1). Simulations
species to fill the void left by a species that goes of freshwater fish assemblages similarly found that
extinct. Most studies of community response to the presence or absence of compensation among
extinction, like studies of biodiversity and ecosys- tropical freshwater fishes had a strong effect on the
tem functioning generally, have focused on com- rates of nutrient recycling (McIntyre et al. 2007).
petitive assemblages within a trophic level, so the Thus the degree of compensation can have major
process of primary interest has been compensation consequences for how and whether species loss
by surviving species after loss of competitors. In affects ecosystem functioning.
general, theory shows that compensation tends to Two important questions are: (1) How common
buffer community- and ecosystem-level properties is compensation in nature? and (2), Is there any
from species loss, and that the order of extinctions consistent relationship between organismal traits
is important in determining whether or not this and the strength of compensation? Regarding the
 FORECASTING DECLINE IN ECOSYSTEM SERVICES 67

Non-interactive model Interactive model

(no compensation) (compensatory)
6

4
Extinction
Biogenic mixing depth (cm)

random
2

0 Figure 5.1 Evidence from simulation studies that

6 extinction impacts on ecosystem functioning (biogenic mixing
depth in marine sediments) depend strongly on the order of
marine invertebrate species loss and the interactions among
4 species in the reorganizing community. Simulations based on
Extinction empirical data show that declining diversity has very different
by body size
effects on mixing depth depending on whether extinction
2 order is random (top) versus ordered by loss of largest-bodied
species first (bottom), and whether remaining species show
biomass compensation (right) or not (left). The two clouds of
0 points in each panel represent sequences with and without
0 50 100 150 0 50 100 150
the very large, mobile deposit-feeding brittle star in this
Species richness system. After Solan et al. (2004), used by permission.

first question, Larsen et al. (2005) found no evi- unaware of studies explicitly addressing relation-
dence of compensation in bee and beetle assem- ships of traits to compensation in competitive com-
blages as species were lost along gradients of munities.
human impact in the field; together with a positive
correlation between response (vulnerability) and
5.3.3 Background: cascading extinction
effect (ecosystem process) traits, this led to
decline of function as species were lost from the The second aspect of structural reorganization that
assemblages (Fig. 5.2). It is not clear how common has received attention in biodiversity and ecosys-
such situations are. Moreover, species are not tem functioning research involves the effects of
equal in their ability to compensate (Lyons and species loss on subsequent loss of additional spe-
Schwartz 2001, Smith and Knapp 2003), meaning cies, i.e. ‘cascading (or secondary) extinction’. In
that different extinction scenarios, which leave natural multitrophic ecosystems the general prob-
behind a community with different species, also lem of community reorganization involves not
result in differing potential for compensation. only compensation among competitors but also
For example, among grassland plants, dominant interactions among trophic levels (e.g. Ives and
species compensated for removal of the rarest Cardinale 2004). These interactions clearly depend
species, whereas rare species could not compen- on traits of the species involved, as well as of the
sate for reductions in the density of the dominant abiotic environment, implying that they are con-
species (Smith and Knapp 2003). In answer to the text-dependent. Several studies have addressed
second question, competitive ability has been the effects on multitrophic communities of losing
linked to particular traits, for example, to indi- species by focusing on summary descriptors of
vidual biomass, height, canopy architecture, and these interactions such as trophic level, con-
leaf shape among wetland plants (Gaudet and nectance, and interaction strength. Disruption of
Keddy 1988). And compensation following feeding links or positive interactions, such as pol-
lake acidification is reported to diminish at higher lination, can precipitate secondary extinctions
trophic levels (Vinebrooke et al. 2003). But we are (Pimm 1980), with further implications for
68 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

16 3500
14 3000
Dung burial rate (gh–1)

Pollen deposition
12
2500
10
2000
8
1500
6
4 1000

2 500
0 0
0 2 4 6 8 10 12 14 0 2 4 6 8 10 12
Dung beetle species richness Native bee species richness

Figure 5.2 Rates of ecosystem services increase with species richness in surveys across gradients in human disturbance for two different systems, taxa,
and ecosystem processes. In both cases insect abundance was positively related to species richness, suggesting weak density compensation among
species. After Larsen et al. (2005), used by permission.

ecosystem functioning. Loss of a consumer species Nevertheless, some generalizations appear pos-
can release certain of its prey species from control, sible. One apparently general finding of studies
drive others to extinction as released competitors simulating species loss from empirical food webs
proliferate, and/or deprive specialized higher or interaction networks is that the networks tend
predators of food, fostering their extinction. to be quite robust (in terms of secondary extinc-
tions) to random loss of species, but much more
vulnerable to loss of highly connected species (Solé
5.3.4 Results: cascading extinction
and Montoya 2001, Dunne et al. 2002a, Memmott
Secondary or cascading extinctions that result et al. 2004). Since skewed distribution in the
from loss of a focal species have been the subject of number of links among species appears typical of
considerable attention in theory and simulation empirical food and interaction webs (Berlow et al.
studies (Table 5.3). Recent studies have identified 1999), this result emphasizes the importance of
trophic position (Borrvall et al. 2000, Christianou focusing conservation attention on highly con-
and Ebenman 2005, Eklöf and Ebenman 2006), nected species. A second apparent pattern emerg-
connectivity (Solé and Montoya 2001, Dunne et al. ing is that cascading extinctions seem to be most
2002b, Memmott et al. 2004, Eklöf and Ebenman severe after loss of species at low trophic levels
2006), and the configuration of trophic interactions and to affect most severely those at higher trophic
(Christianou and Ebenman 2005) as important levels (Table 5.3). These patterns, however, are
properties in determining which primary species sensitive to variation in model assumptions and
deletions are most likely to cause secondary clearly preliminary.
extinctions, and which species are most likely to go
extinct secondarily (reviewed by Ebenman and
5.3.5 Summary and conclusions
Jonsson 2005). The theoretical results are difficult
to generalize, in part because of variation among The complexity of interactions within food webs
studies in assumptions, including strength and highlights both conceptual and empirical chal-
nature of competition, redundancy among species lenges to further progress. A key conceptual
within groups, and skew in interaction strengths. challenge is development of an objective, empiri-
Recent studies confirm that such assumptions are cally based framework for defining interaction
important to how loss of a focal species affects traits at the level of individual organisms that
secondary extinction and its ecosystem con- reliably predict trophic level, competitive ability,
sequences (Thebault et al. 2007). and compensation. For example, high trophic level
Table 5.3 Traits influencing community reorganization via secondary extinctions after loss of a focal species.

Trait(s) promoting secondary extinction

Study type Focal species Secondary spp Effect of species richness Reference

Model – Trophic specialization of predators Richness increases secondary extinctions; 1

(after plant or herbivore removal); trophic connectance increases secondary extinctions
generalism of prey (after carnivore removal)
Model Low trophic level (autotrophs) – Richness reduces secondary extinctions 2
Model – High trophic level Richness reduces secondary extinctions 3
(only in absence of stochastic variation)
Model Low trophic level; strong interactions High trophic level; weak interaction – 4
with consumers with resources; strong interaction
with consumers
Model High trophic level – Richness reduces secondary extinctions 5
Model Highly connected; low trophic level High trophic level (consumers generally) Connectance reduces secondary 6
extinctions generally (but increases
loss of top predators)
Model Low trophic level (with High trophic level Richness increases secondary extinctions in 7
intraspecific competition) absence of consumer intraspecific
competition, but decreases extinctions with
consumer competition
Model; simulations of – High trophic level (consumers generally); – 8
empirical food webs trophic uniqueness
Simulations of Highly connected – – 9
empirical food webs
Simulations of Highly connected – No effect of richness; connectance 10
empirical food webs reduces secondary extinctions
Simulations of Highly connected – – 11
empirical food webs
Simulation of empirical Highly connected – – 12
plant-pollinator networks

1 Pimm (1980); 2 Borrvall et al. (2000); 3 Ebenman et al. (2004); 4 Christianou and Ebenman (2005); 5 Borrvall and Ebenman (2006); 6 Eklöf and Ebenman (2006); 7 Thebault et al. (2007); 8 Petchey
et al. (2008); 9 Solé and Montoya (2001); 10 Dunne et al. (2002b); 11 Dunne et al. (2004); 12 Memmott et al. (2004).
70 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

has been identified as a correlate of extinction and community structure, to altered ecosystem
vulnerability in a range of taxa (Table 5.2), but functioning.
trophic level is not a trait per se but an emergent First, the nature of the linkage depends critically
feature of the focal organism’s interaction with on scale. Several studies have shown that basic
other species and its abiotic environment. Can we demographic and size traits of organisms scale
identify traits of individual organisms or species allometrically (e.g. Enquist et al. 1999, Marba et al.
that index trophic level, and if so, how precisely? 2007), and correspond closely to ecosystem pro-
For example, morphological traits are routinely cesses, at global or cross-ecosystem scales. These
used by palaeontologists to identify trophic level include, for example, the allometric scaling of
in fossil assemblages (Dunne et al. 2008), and metabolism with body size in plants (Enquist et al.
defensive chemicals in a plant may indicate its low 2003). Such approaches have recently been extended
vulnerability to grazers and thus low connectance to multitrophic ecosystems to predict the potential
in a food web. Similarly, are there measurable biomass and distribution of marine fishes on a global
traits of individual organisms that index potential scale based on primary production and temperature
for biomass or numerical compensation? And does (Jennings et al. 2008). These are results of central
the degree of compensation differ systematically importance to linking traits mechanistically to eco-
among taxa, by environmental conditions, or as a system functioning, but it is unclear how such
function of measurable individual-level traits? Can global-scale allometric relationships translate to the
we identify traits of species that reliably predict local scales of interest in environmental conservation
their impacts on secondary extinctions, and their and management. The scatter in global, log-log plots
sensitivity to different drivers of extinction? Do of trait versus process likely conceals large variance
species that are especially vulnerable to secondary among species on local scales with narrower ranges
extinction play important functional roles in of trait values and lower diversity. Thus, at local
communities? Even if the effects of traits are con- scales, prediction of ecosystem functioning may
text-dependent, such information could still be require finer resolution of traits.
useful if the trait–context interactions are consis- A second, more serious complication is that many
tent and predictable. Answering these questions ecosystem processes are mediated by multiple
will require a tighter integration between empiri- traits. This poses the challenge of reducing the
cal investigations of species loss and interactions, dimensionality of trait space, ideally by finding
and modelling of food webs. suites of consistently correlated traits. Accordingly,
considerable effort has gone into methods for
defining ‘functional groups’ of species (Hooper et al.
5.4 Effect traits and ecosystem 2002, Naeem 2002a, Naeem and Wright 2003,
function Petchey and Gaston 2006), yet many functional
group classifications turn out to have limited use-
5.4.1 Background
fulness at the level of local communities since
Tremendous effort has been devoted to correlating functional traits can vary independently across
plant traits with population and ecophysiological species (Eviner and Chapin 2003, Wright et al. 2006).
processes (effect traits), and with environmental In at least some contexts, however, there are pre-
gradients and responses to disturbance (response dictable suites of co-occurring traits that can be
traits). For example, plant resource capture, pro- reduced to a small number of trait syndromes or
ductivity, and decomposition have been linked to ‘strategies’ that correlate with functional processes
a variety of morphological, chemical, and demo- (e.g. Craine et al. 2002, Diaz et al. 2004). The exis-
graphic traits (Table 5.4). This literature is exten- tence of consistent suites of functional traits is also
sive and we do not review it comprehensively suggested indirectly by the strong differences
(Hooper et al. 2002, Lavorel and Garnier 2002), but among major clades of plants in, for example,
focus on two themes relevant to linking environ- decomposability of their foliage (Cornwell et al.
mental change, through changes in biodiversity 2008). Again, the power and utility of the
 FORECASTING DECLINE IN ECOSYSTEM SERVICES 71

Table 5.4 A selective summary of plant traits influencing process rates in terrestrial ecosystems. Response shows the sign of the ecosystem response
with increasing value of the trait.

Function Trait Response Reference

Productivity Specific leaf area (SLA) þ 1, 2, 3, 4, 5

N concentration þ 2, 4, 5
Plant size þ 2, 4
Dry matter content þ 1, 5
Rooting depth þ 1, 4
Potential relative growth rate þ 6
Shoot:root ratio þ 2
Decomposition N concentration þ 4, 5, 7, 8, 9
Taxonomy: dicots þ 9, 10, 11
C:N ratio – 4, 12, 13
Lignin content – 4, 11, 14
Taxonomy: monocots – 9, 10
Specific leaf area (SLA) þ 5
Leaf toughness – 12
Leaf dry matter content – 5
Resource capture and utilization Leaf N þ 15, 16
Taxonomy: legumes þ 4, 17
Specific leaf area (SLA) þ 3
Root mass þ 16
Plant mass – 7
N concentration – 7

1 Lavorel and Garnier (2002); 2 Heisse et al. (2007); 3 Díaz and Cabido (1997); 4 Chapin (2003); 5 Garnier et al. (2004); 6 Vile et al. (2006);
7 Wardle et al. (1998); 8 Cortez et al. (2007); 9 Cornelissen and Thompson (1997); 10 Wardle et al. (2002); 11 Cornelissen (1996); 12 Perez-
Harguindeguy et al. (2000); 13 Madritch and Hunter (2004); 14 Aerts (1997); 15 Diaz et al. (2004); 16 Drenovsky et al. (2008); 17 Hooper and
Vitousek (1998)

relationships depend on scale. At regional or global across 640 plant species from three continents
scales, basic ecological processes can be clearly revealed a globally consistent ‘major axis of evo-
related to traits (e.g. Diaz et al. 2004, Díaz et al. 2007, lutionary specialization’ reflecting the evolution-
Enquist et al. 2007). An important direction of ary trade-offs between rapid resource acquisition
research in this area involves the emergence of new on the one hand and conservation and protection
approaches that allow interpretation of ecosystem of tissues on the other (Diaz et al. 2004). Principle
responses within the context of multiple effect and component analysis showed that the first axis,
response traits. interpreted as a predictor of resource capture and
use, was correlated with relative growth rate, leaf
nitrogen content, and litter decomposition rate,
5.4.2 Empirical results
as well as palatability to generalist herbivores
The most successful efforts linking organismal (Fig. 5.3). Similarly, as mentioned in a previous
traits with ecosystem processes have been at section, grazing by vertebrates produces a char-
regional to global scales. Recent syntheses confirm acteristic change in the suite of traits dominating
that certain syndromes of functional traits recur vegetation, although the details vary to some
predictably across different habitats and unrelated degree among regions (Díaz et al. 2007). Among
floras. For example, measurement of a suite of 12 animals, the simple trait of body size proves both
standardized traits, including leaf and canopy general and useful on local scales, for example, the
characteristics, phenology and life history traits, regular scaling of predator and prey body sizes
72 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Argentina England

8
r = –0.38 r = –0.58
6
4

PCA 1
2
0
–2
–4
0 20 40 60 80 100 0 20 40 60 80 100
Decomposition rate (% dw loss)

6
r = –0.52 r = –0.60
4
PCA 1

2
0
–2
–4
0 2 4 6 0 2 4 6
N content (% dw)

10
r = –0.58 r = –0.67
8
6
PCA 1

4
2
0
–2
–4
0 0.1 0.2 0.3 0.4 0 0.1 0.2 0.3 0.4
Relative growth rate

Figure 5.3 Syndromes of plant functional traits are consistent across disparate regions and taxa, and are closely tied to ecosystem processes.
The figure shows similar correlations between Principal Component Axis 1 (defining plants with smaller, thicker, tougher leaves, and lower specific
leaf area and three aspects of ecosystem functioning in two geographically and floristically different regions. After Diaz et al. (2004), used by
permission.

across a wide range of systems (Brose et al. 2006). ated with this variance in risk. We also showed that
Refining such approaches for application at the species differ in their effects on ecosystem function-
scale of local communities would be a valuable ing, and again that certain traits are correlated with
step forward. this variance in function. These imply that the order
in which species are lost from a community, the
secondary extinctions that ensue, and the degree to
5.5 Empirical evidence linking realistic which remaining species compensate in biomass,
biodiversity change to ecosystem will have important consequences for how ecosys-
functioning tem function changes. This brings us back to the
question of whether and how changes in function
5.5.1 Background
predicted by random-loss experiments approximate
The previous sections documented that species differ changes expected under more realistic (trait-based)
in extinction risk and that certain traits are associ- extinction scenarios.
 FORECASTING DECLINE IN ECOSYSTEM SERVICES 73

Studies addressing ecosystem impacts of realistic showed substantially different patterns than those
extinction scenarios have generally used one of two predicted if species were lost in random order.
approaches. Most commonly, they have explored Similar results have been found in three experi-
the plausible hypothesis that a certain trait (e.g. ments. First, grassland ecosystem functioning
body size) predisposes species to extinction under a (resistance to invasibility) was more strongly
given driver, then used species trait data to simu- related to diversity when the plant richness gradi-
late a corresponding extinction order (e.g. Solan ent simulated the observed nested pattern of spe-
et al. 2004, Bunker et al. 2005, McIntyre et al. 2007). cies loss (Zavaleta and Hulvey 2004) than when
A second approach has used empirical information plant assemblages were synthesized with a random
on changes in assemblage composition along nat- loss scenario (Dukes 2001); in this case the invasion
ural or anthropogenic environmental gradients as a resistance provided by higher diversity was
proxy for extinction order, and asked how changes reduced more under the realistic extinction scenario
in trait distribution along the gradient influence (Fig. 5.4). Second, detritus processing by stream
ecosystem properties (Zavaleta and Hulvey 2004, insects was more strongly related to diversity when
Srinivasan et al. 2007). These approaches explicitly insect richness gradients reflected realistic extinc-
recognize that species are likely to go extinct in a tion scenarios than when the gradients were
particular order, as particular traits render a given assembled at random (Jonsson et al. 2002). Finally,
species more or less sensitive to particular extinc- nitrogen uptake by tidepool seaweeds was pos-
tion drivers. Where the effects of environmental itively correlated with seaweed diversity along a
change (e.g. disturbance) are well characterized in natural diversity gradient, but not a random-
time and/or space, position along the gradient assembly gradient (Bracken et al. 2008).
allows reconstruction of the relative severity of These differences in the functional effects of real-
disturbance and the actual sequence of species loss. istic versus random extinction scenarios depend, in
part, on the covariance between the traits that lead to
high extinction risk and the traits related to high
5.5.2 Empirical results
functional importance (Solan et al. 2004). If these two
Several studies have contrasted ecosystem effects of sets of traits are positively correlated, i.e. there is
realistic extinction scenarios and random-loss sce- substantial overlap in the traits that mediate extinc-
narios, and nearly all demonstrate that these have tion vulnerability and effects on ecosystem pro-
very different impacts on ecosystem functioning cesses, then functioning will decrease rapidly with
(Table 5.5). Recent simulation studies took advan- only a few species lost from the community (Lavorel
tage of existing data on the per capita functional and Garnier 2002, Raffaelli et al. 2002). For example,
impact of species to predict effects of extinctions on in a simulation study of neotropical trees (Bunker
function when species with certain traits (e.g. large et al. 2005) in which large trees disappeared first,
body size) or documented sensitivity to disturbance there was a rapid decline in carbon storage because
(e.g. intensive agriculture) were simulated to go the remaining trees, even after increasing in density,
extinct first. These include effects of terrestrial ver- did not have the traits (high wood density, height)
tebrates on Lyme Disease risk (Ostfeld and required to store carbon maximally. At the other
LoGiudice 2003), benthic marine invertebrates on extreme, if the traits associated with extinction risk
bioturbation (Solan et al. 2004), European grassland are negatively correlated with those important for
plants on biomass production (Schläpfer et al. 2005), function, then realistic extinctions will eliminate
beetles on dung burial, and bees on pollination species of low functional importance and have less
rates (Larsen et al. 2005), neotropical trees on carbon effect on ecosystem functioning, at least initially,
storage (Bunker et al. 2005), perturbing lake com- than random extinctions. For example, in the study
munities on secondary extinctions (Srinivasan et al. on productivity in European grasslands (Schläpfer
2007), and freshwater tropical fishes on nutrient et al. 2005), intensive farming led first to loss of the
recycling (McIntyre et al. 2007). In all seven studies, less productive species, and thus extinctions under
many – though not all – extinction scenarios this scenario had less impact on productivity than
Table 5.5 Summary of studies exploring consequences of non-random extinction sequences for ecosystem functioning ‘Rand ¼ random.’

Change with declining diversity

Organism Ecosystem Trait mediating Study type Extinction driver Random Realistic Real – Rand Reference
manipulated process extinction

Grassland plants Primary production Productivity, competitive Experiment, Management – 0,þ Weaker 1
(biomass accumulation) ability simulation (fertilizer and
mowing)
Grassland plants Resistance to exotic Unspecified (from Experiment Disturbance (nested 0 – Stronger 2
invasion nested subset analysis) subset analysis)
Forest trees Carbon storage, Size, growth rate, Simulation Management, 0 0, –, 0 Similar, stron- 3
(biological drought-sensitivity environmental ger,
insurance) change similar
Marine algae Nutrient use Unspecified (natural Experiment Unspecified 0 – Stronger 4
gradient)
Bees Pollination Body size Simulation Habitat loss/ – – Stronger 5
fragmentation
Dung beetles Dung burial (nutrient Body size Simulation Habitat loss/ – – Stronger 5
recycling, fragmentation
seed dispersal)
Mammalian hosts Protection from Lyme Body size, home range Simulation Habitat fragmentation þ – Stronger 6
of Lyme disease disease risk size, trophic level
Stream insects Detritus (leaf) processing Tolerance of acidification Experiment Pollution 0 – Stronger 7
and organic pollution
Tropical FW fishes Nutrient regeneration Body size, trophic level, Simulation Fishing – – Stronger 8
Freshwater organisms Stability (resistance to Unspecified (from nested Simulation Unspecified – 0 Weaker 9
secondary extinctions) subset analysis)
Marine benthic Nutrient regeneration Body size, population size, Simulation Unspecified – – Stronger 10
invertebrates sensitivity to disturbance (body size)/
weaker
(rarity)
Three plant and three Unspecified (response Leaf N content, rooting Simulation N deposition (plants), – – Stronger 11
animal assemblages variable depth harvesting (animals)
was functional diversity) (plants); body size
(animals)

1 Schläpfer et al. (2005); 2 Zavaleta and Hulvey (2004); 3 Bunker et al. (2005); 4 Bracken et al. (2008); 5 Larsen et al. (2005); 6 Ostfeld and LoGiudice (2003); 7 Jonsson et al. (2002); 8 McIntyre et al.
(2007); 9 Srinivasan et al. (2007); 10 Solan et al. (2004); 11 Petchey and Gaston (2002b).
 FORECASTING DECLINE IN ECOSYSTEM SERVICES 75

Extinction order Extinction order

realistic random
440 800

340 600

Invader biomass
Invader biomass
240 400

140 200

40 0
10 12 14 16 18 20 22 0 4 8 12 16
Resident species richness

Figure 5.4 Evidence from field experiments that extinction impacts on ecosystem functioning (invasibility) depend strongly on the order of grassland plant
species loss. Invader performance in experimental plots declined with native richness when the diversity gradient reflected real-world patterns (left, Zavaleta
and Hulvey 2004, used by permission), but was unrelated to native richness when extinction order was determined randomly (right, Dukes 2001, used by
permission). Invasibility is displayed as aboveground biomass of the alien starthistle, Centaurea soltitialis. Left panel shows the regression line and 95%
confidence intervals.

random loss of species. Despite increasing realism in traits can result in major changes in ecosystem-
species loss trajectories, however, the few studies level processes after a loss of a particular species.
performed to date have considered only single This is shown dramatically in extinction simula-
forcing agents. If individual species have multiple tions of marine benthic invertebrates (Solan et al.
traits that each expose them to different extinction 2004) (Fig. 5.1) and tropical freshwater fishes
drivers, it follows that in the presence of multiple (McIntyre et al. 2007), in which biodiversity and
drivers of extinction the ecosystem consequences of ecosystem functioning relationships fall into two
biodiversity loss may be much greater than current distinct domains depending on whether the dom-
evidence suggests (Sala et al. 2000, Brook et al. 2008). inant species is present or not.

5.5.3 Summary 5.6 Discussion

A nearly universal result of both the small number As the examples discussed here illustrate, the cor-
of experiments and the larger but still modest relation between extinction traits and functional
number of simulations that have compared ran- traits depends critically on both the extinction sce-
dom with non-random extinction scenarios (Table nario and the function under consideration, so it is
5.5) is that the order of species loss has profound currently difficult to make global generalizations
consequences for the direction, rate, and magni- about the sign of the correlation (see Lavorel and
tude of change in ecosystem functioning with Garnier 2002). The mechanism also matters: if niche
extinction. Importantly, studies of non-random complementarity drives diversity effects on func-
extinction scenarios suggest that, more often than tion, then the variety of functional traits (‘functional
not, realistic extinction orders have larger effects diversity’) may be more important than any par-
on ecosystem responses than random loss ticular functional trait in determining ecosystem
sequences, and thus that random-loss designs may functioning. Simulations using empirical data from
often underestimate the ecosystem consequences at least six assemblages (tested by Petchey and
of diversity loss (Table 5.5, Duffy 2009). Another Gaston 2002b) suggest that functional diversity is
striking finding is that, even in very species-rich indeed reduced more under realistic than under
assemblages, strong skew in body size or other random extinction scenarios.
76 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

An important limitation of simulation studies scenarios of extinction and invasion, and the reor-
comparing realistic and random species extinctions ganization of food webs that follows this turnover
is that they require assumptions about how the (Schwartz et al. 2000, Srivastava 2002, Srivastava
remaining species in the community would and Vellend 2005). A focus on response and effect
numerically respond to the loss of species. These traits, and the covariance between them, is a
assumptions differ between studies. For example, promising way forward.
Ostfeld and LoGiudice (2003) and Srinivasan et al. Finally, it is worth reiterating explicitly why we
(2007) assumed no numerical compensation are interested in the links between biodiversity and
amongst remaining species, whereas Bunker et al. ecosystem functioning in the first place. There are
(2005) and Dukes (2001) assumed full compensation many arguments for concern over the declining
across all species. These assumptions are critical state of biodiversity – from purely aesthetic and
because, as discussed earlier, compensation mat- moral to nakedly commercial – but probably the
ters. Species interactions also complicate predic- most compelling reason is the role of diverse living
tions about the order of species loss in response to a organisms in creating and maintaining the complex
stressor, because the loss of each species causes a life support system without which humanity would
reorganization of interactions and abundances in literally be doomed. The lack of public urgency
the food web. In the empirically based simulation regarding this problem can be traced in part to the
studies discussed earlier, the order of species loss limitations of classical economics in valuing both
(and thus effects on ecosystem functioning) was the benefits of living organisms and ecosystems
based on species’ direct vulnerability to the stressor that are outside traditional markets, and in esti-
(e.g. Solan et al. 2004), whereas it is clear that mating the costs of degrading natural systems
indirect interactions among species can change the (Chapters 17 and 18). Trait-based approaches can
sensitivity of species to stressors (Ives and Cardi- contribute to these practical challenges in several
nale 2004). The covariance between functional ways. First, they can give us a clearer prediction of
response and effect traits is thus likely to be con- how natural communities are likely to change
text-dependent in food webs of interacting species. under particular scenarios of environmental impact.
Soberingly, dynamic species interactions such as Second, by discovering general links between
compensation and cascading extinctions can result environmental change, community response, and
in a great range of possible outcomes of species ecosystem functioning based on measurable traits,
extinction, with potentially vastly differing con- these approaches can reduce the dependence of
sequences for ecosystem functioning. policy implementation on specific taxonomic
Another limitation of much trait-based research expertise, which is in short supply and declining.
to date is its focus on single guilds or trophic levels Third, defining the role of particular types of
(marine infauna, Solan et al. 2004, forest trees, organisms (defined by traits) in mediating particu-
Bunker et al. 2005, dung beetles, Larsen et al. 2005). lar ecosystem services provides data necessary to
Yet it is clear from observations, experiments, and parameterize economic models underlying policy
simulations that the broader effects of extinction on instruments for sustainability (Chapter 17) gener-
ecosystem structure and functioning are often ally, and is essential to moving from traditional
mediated by trophic interactions (Pace et al. 1999, single-species harvesting models to models that
Dunne et al. 2002b, Petchey et al. 2002b, Rayner et al. take account of the complex interactions typical of
2007). Thus, a critical frontier in conservation ecol- all real ecosystems (Chapter 19).
ogy involves expanding trait-based approaches for
multi-trophic communities (Belgrano et al. 2005,
5.7 Conclusions and future directions
Duffy et al. 2007). Indeed, the extent to which the
last decade’s high-profile research on biodiversity The field of extinction research is currently very
and ecosystem functioning can be applied to real- active, and recent years have produced a rich body
world conservation and management problems will of data on the traits that predispose particular
depend critically on linking that work to realistic taxa to endangerment and extinction, and
 FORECASTING DECLINE IN ECOSYSTEM SERVICES 77

increasingly, their synergisms (Purvis et al. 2000c, that influence the degree of compensation among
Traill et al. 2007, Brook et al. 2008). These data potentially competing species, and more generally,
can inform improved design of studies, experi- the strength of interactions of all kinds
mental and otherwise, that explore the effects of between species (Berlow et al. 2004). Another key
specific environmental change drivers on com- research need is a focus on multiple traits and how
munity organization (including biodiversity) and they interact with multiple drivers of extinction.
its consequences for ecosystem processes. The Early trait-based approaches to linking environ-
importance of such studies is highlighted by mental change with ecosystem impacts have
the marked differences in outcomes of both understandably focused on individual traits.
experiments and simulations as a function of the However, it is clear that traits are often correlated
specific extinction trajectories employed and, in with one another, often respond in concert to dri-
simulations, the assumptions made about how vers of change, and can interact to influence eco-
species interact. system functioning in non-linear ways (Eviner and
One otherwise complimentary reviewer of this Chapin 2003). The same is true of extinction dri-
chapter noted that ‘Most of the generalizations vers (Sala et al. 2000, Brook et al. 2008). Thus, an
that can be made might be guessed by an under- important frontier is developing multivariate
graduate fresh out of a good ecology class.’ It is models of correlated trait change and of trait
true that the vulnerability of species with large effects, and how they ripple out to influence
body sizes, ‘slow’ life histories, specialized habits, functioning of ecosystems (Lavorel and Garnier
small geographic ranges, and low population den- 2002, Craine et al. 2002, Eviner and Chapin 2003,
sities are both well-established and self-evident. Poff et al. 2006.
The bright side of this observation is that these
strong generalizations offer correspondingly clear
Acknowledgments
guidance on how to design tests and predictive
models that better link realistic extinction to eco- We are grateful to Andy Hector for organizing the
system functioning. As one example, the vulner- stimulating BioMERGE workshop in Ascona,
ability of large animals high in the food chain, Switzerland, from which this chapter arose, as well
which also often are strong interactors, argues for a as the other members of the workshop. We also
better marriage of approaches focusing on hori- acknowledge Shahid Naeem and two anonymous
zontal diversity within levels with predator–prey reviewers for comments that improved the MS,
ecology and food-web modelling (Chapter 8; and the National Science Foundation (OCE-
Duffy et al. 2007). A key research need is a better 0623874 to JED) and the Natural Sciences and
characterization, both theoretical and empirical, Engineering Research Council of Canada (DSS) for
of the intrinsic traits and environmental factors support.
 CHAPTER 6

Biodiversity and the stability

of ecosystem functioning
John N. Griffin, Eoin J. O’Gorman, Mark C. Emmerson, Stuart
R. Jenkins, Alexandra-Maria Klein, Michel Loreau, and Amy Symstad

6.1 Introduction the 1990s as attention to extinction’s consequences

for the stability of ecosystem functioning increased
6.1.1 Overview
(Tilman and Downing 1994, Naeem and Li 1997).
Concern that the rapid anthropogenic erosion of This BEF perspective recognized that fluctuating
biodiversity (Wilson 1992) may undermine the abundances of component species may not produce
delivery of ecosystem services (Daily 1997) has instability at the community or ecosystem level
prompted a synthesis of community and ecosystem because compensatory reactions among species
ecology over the last decade. Biodiversity-ecosystem dampen fluctuations of aggregate abundance (Tilman
functioning (BEF) research is central to this emerging 1996). The distinction between population and com-
synthesis, asking how biodiversity is related to the munity-level variability was firmly drawn (Tilman
magnitude and stability of ecosystem processes. Iso- 1996) and attention was focused on the latter through
lating species richness (and diversity) effects from the BEF research agenda.
species composition has been a chief goal of BEF Within the BEF framework, experiments and
research. That species richness generally enhances the theory explicitly relating to the effect of species
mean magnitude of a variety of ecosystem properties richness on community-level aggregate properties
is now well established (Hooper et al. 2005; Balvanera (mainly biomass) have focused on variability
et al. 2006; Cardinale et al. 2006a), but the effect of through time in relation to background environ-
species richness on the stability of ecosystem prop- mental variation (temporal stability) as well as on
erties remains equivocal (Hooper et al. 2005). the impact (resistance) and recovery (resilience) of
Early consensus (Odum 1953, MacArthur 1955, such properties to discrete, and often extreme,
Elton 1958, Pimentel 1961) that diversity enhances perturbations. In this chapter we review recent
various aspects of community and ecosystem sta- empirical studies examining the links between
bility was largely founded on qualitative observa- species richness and these three facets of stability
tions and intuitive reasoning. This view was (see Ives and Carpenter 2007 for a review of other
apparently contradicted by the results from rigorous types of stability). In addition, recognizing that
mathematical treatments (e.g. May 1972) which explicit BEF experiments are limited in their spatial
showed that in a food web context stability was and temporal scope, we adopt a wider perspective
related to system properties, i.e. connectance, species by discussing how changes in biodiversity may
richness, and interaction strength, and importantly, undermine stabilizing properties of food webs and
could be reduced by species richness. Recognition the ability of ecosystems to resist state-changes.
that stability has multiple definitions that can apply Furthermore, using examples we emphasize that
to all levels of ecological organization (Pimm 1984; direct measurement of the stability of ecosystem
see also Loreau et al. 2002) helped pave the way for a services across gradients of human impacts can
new, synthetic perspective that developed during show how stability is influenced by human

78
 BIODIVERSITY AND THE STABILITY OF ECOSYSTEM FUNCTIONING 79

activities – both directly and indirectly via changes under the insurance hypothesis, as species tolerant
in diversity. to a pulse perturbation or directional change in
conditions are more likely to occur in diverse
communities (Walker 1992, Yachi and Loreau 1999).
6.1.2 Theory linking biodiversity and stability
On the other hand, the resilience of aggregate
Theory has established strong links between species community properties (the return rate following an
richness and the temporal variability of commu- equal reduction in the populations of all component
nity-level properties and has provided a variety of species) is not incorporated under the insurance
possible explanatory mechanisms (reviewed by hypothesis, in which species populations are dif-
Cottingham et al. 2001, Loreau et al. 2002; see Box ferentially affected by the environment or pertur-
6.2). Doak et al. (1998) argued that a reduction in bations. The resilience of populations may in fact be
community variability with increased diversity is reduced by high levels of diversity in competitive
an inevitable consequence of ‘statistical averaging’, communities (Loreau and Behera 1999). This theory
i.e. the sum of many randomly and independently does not account for differences between species in
variable items is less variable than the average item. growth rates, however, which may result in a
The strength of this effect depends on how the positive relationship between species richness and
variances of populations scale with their means return rate of community biomass (resilience)
(Tilman et al. 1998), and the evenness of species’ through a sampling effect (Steiner et al. 2005b).
abundances and how their fluctuations are related Theory has yet to explicitly address this possibility,
(Doak et al. 1998, Tilman et al. 1998). however.
The importance of how species fluctuations are
related is also reflected in another proposed stability
6.2 Empirical findings
mechanism that is closely related to the concept of
statistical averaging: the ‘insurance hypothesis’. This Problems with the design and interpretation of
assumes that interspecific niche differentiation causes experimental tests (Givnish 1994, Huston 1997,
species to respond differently to the environment and Fukami et al. 2001) together with a general shortage
that this differential response can produce compen- of such tests, have hampered the attempts of earlier
satory dynamics among species, buffering the impact reviews to assess the effect of diversity on temporal
of environmental changes (McNaughton 1977, stability, resistance and resilience (Cottingham et al.
Walker 1992, Naeem and Li 1997). The insurance 2001, Loreau et al. 2002, Hooper et al. 2005). Sub-
hypothesis depends upon functional redundancy: the sequent vigorous empirical research has recently
concept that species within the same functional group been conducted in this area. This work has been
may replace each other with no consequences for generally less open to alternative interpretation, as
ecosystem function. The stabilizing role of this experimental designs have evolved to limit several
mechanism further depends upon the diversity of confounding factors previously identified (but see
species’ responses within functional groups (func- Wardle and Grime 2003). It has long been recog-
tional response diversity; Lavorel and Garnier 2002, nized that species composition can have strong
Elmquist et al. 2003). Theoretical models of competi- influences on ecosystem properties. Isolating the
tive communities formalized the insurance hypothe- role of species richness per se has been a chief goal
sis and confirmed that species diversity can stabilize of BEF research, and is the focus of empirical
community properties in the face of changing envi- studies reviewed here.
ronmental conditions (Yachi and Loreau 1999, Ives
et al. 1999). This prediction also generally holds for
6.2.1 Temporal stability
simple, theoretical, multi-trophic systems (Ives et al.
2000; Thébault and Loreau 2005) and metacommu- We first examine empirical tests of the general
nities (Loreau et al. 2003). hypothesis that diversity enhances the temporal
The resistance of aggregate community proper- stability of community-level properties such as
ties is also theoretically enhanced by diversity biomass or production, measured as the reciprocal
80 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

of the coefficient of variation (1/CV). CV is an algal species richness on community biomass. This
appropriate, and widely used, measure of varia- effect was, however, context-dependent, in that it
bility because it is standardized to the mean, occurred only under conditions of low nutrient
accounting for the tendency of variability to availability; no diversity effect was detectable under
increase with the mean. Note that in the primary enriched conditions. Petchey et al. (2002) also did not
literature authors report either temporal variability find an effect of species richness on the temporal
(CV) or temporal stability (1/CV). For consistency, stability of community-level biomass, either under
we interpret and discuss diversity effects from all constant or fluctuating temperature conditions. In
studies in terms of temporal stability, such that only a single case did diversity destabilize commu-
positive effects are stabilizing (see Table 6.1). nity biomass (Gonzalez and Descamps-Julien 2004).
Eighteen separate papers published between 1994 The mixed outcomes of these experiments, and
and 2006 include a total of 22 cases in which com- the lack of support for diversity–stability relation-
munity-level temporal stability was measured. ships in some cases, can be explained by a range of
These studies were conducted in a range of systems mechanisms that might obscure diversity effects:
varying in scale from aquatic microcosms to natural
1) A direct destabilizing effect of diversity on popula-
forest stands. Overall, diversity stabilized commu-
tion level (growth rates: Gonzalez and Descamps-
nity-level properties in 13 cases, had no significant
Julien 2004; biomass: Petchey et al. 2002) variances
effect in 8, and reduced stability in a single study.
exists and caused some populations to vary more
We first deal with studies that have examined the
within diverse communities to the extent that they
temporal stability of community-level properties
eclipsed the effect of stabilizing mechanisms.
(principally biomass or its production) within a
2) Synchrony of species responses to environmental
single trophic level in both manipulative and
variability might have limited insurance effects of
observational studies. We then consider studies that
increased species richness.
have manipulated the diversity of communities
3) Low evenness and hence high variance among
across multiple trophic levels and examined how
population biomasses within communities could
such manipulations affect the temporal stability of
weaken the relation between species richness and
biomass and ecosystem process rates.
community-level stability (Ives and Hughes 2002,
Petchey et al. 2002).
6.2.1.1 Temporal stability of biomass within
a single trophic level A key challenge for future studies is to elucidate
Direct tests of the diversity–temporal stability the source of variability among experiments and
hypothesis within a single trophic level have been environmental contexts. Explicit consideration of
mainly conducted within replicated grassland plots the degree of functional response diversity (sensu
and microcosms. Recent grassland experiments in Lavorel and Garnier 2002) represented by species
which diversity was directly manipulated show a within increasingly species-rich communities
stabilizing effect of diversity (Caldeira et al. 2005, would be an important development (see e.g.
Tilman et al. 2006b). These studies reported reduced Walker 1999) that could help explain effects of
stability of constituent populations but greater species richness more completely. Moreover, the
community-level stability with increased species degree of environmental heterogeneity through
richness, which is consistent with theory and pre- time will dictate the extent to which such functional
vious experimental evidence (Tilman 1996). response diversity can be realized (see Tylianakis
Amongst the microcosm examples, only two of five et al. 2008) and should be explicitly considered in
studies supported the diversity–temporal stability future studies.
hypothesis. Steiner et al. (2005a) found that the Natural gradients in diversity are expected to be
aggregate biomass of four zooplankton species in driven by external factors that may obscure the
mixture exhibited greater stability than monocultures effect of diversity on stability and complicate
of the constituent species. Furthermore, Zhang and interpretation (Ives and Carpenter 2007). However,
Zhang (2006a) found an overall stabilizing effect of examining natural patterns of diversity and
Table 6.1 Effect of diversity on the temporal stability of ecosystem properties.

Reference Trophic level Ecosystem Factor Diversity gradienta Ecosystem type Time scale Div levels Type of div effect
function

Caldeira et al. (2005) Primary prod Community biomass Exp. M Grassland 3 yr 1 to 14 Positive
Dang et al. (2005) Decomposer Decomposition Exp. M Stream 28 d 1 to 16 Positive
Dodd et al. (1994) Primary prod Community biomass Nutr. F Grassland 42 yr 8 to 45 Positive
DeClerk et al. (2006) Primary prod Primary productivity Nat. F Forest 64 yr 1 to 4 None
Gonzalez and Primary prod Community biomass Exp. M Aquatic 64 d 1 to 6 Negative
Descamps-Julien (2004)
Morin and McGradySteed Multi Community CO2 flux Exp. M Aquatic 42 d 3 to 9 None
(2004)1
Petchey et al. (2002) Protists and Community biomass Constant temp. Exp. M Aquatic 6w 2 to 8 None
bacteria
Petchey et al. (2002) Protists and Community biomass Fluctuating temp. Exp. M Aquatic 6w 2 to 8 None
bacteria
Romanuk et al. (2006) Multi Community biomass Low nutrient Exp. M (dilution) Aquatic 5w 1 to 8 Positive
Romanuk et al. (2006) Multi Community biomass Med. nutrient Exp. M (dilution) Aquatic 5w 1 to 8 None
Romanuk et al. (2006) Multi Community biomass High nutrient Exp. M (dilution) Aquatic 5w 1 to 8 None
Steiner (2005b) Consumers only Community biomass Nat. F Aquatic 5m 11 to 24 Positive
Steiner et al. (2005a) Consumers only Community biomass Exp. M Aquatic 48 d 1 and 4 Positive
Steiner et al. (2005b) Multi Community biomass Exp. M Aquatic 22 d 1, 2, 4 spp Positive
(X 5 trophic groups)
Timan (1996) Primary prod Community biomass Nutr. F Grassland 8 yr 1 to 26 Positive
Tilman et al. (2006) Primary prod Community biomass Exp. F Grassland 10 yr 1 to 16 Positive
Tylianakis et al. (2006) Multi Parasitism Nat. F Agricultural 16 m 1 to 4 Positive
Valone and Hoffman (2003a,b) Primary prod Community biomass Quadrat scale Nat. F Grassland 11 yr 1 to 16 Positive
Valone and Hoffman (2003a,b) Primary prod Community biomass Plot scale Nat. F Grassland 11 yr 1 to 16 None
Vogt et al. (2006) Multi Community biomass Exp. M (dilution) Aquatic 7w 1 to 8 Positive
Zhang and Zhang (2006a) Primary prod Community biomass High nutrient Exp. M Aquatic 77 d 1,2,4,6 None
Zhang and Zhang (2006a) Primary prod Community biomass Low nutrient Exp. M Aquatic 77 d 1,2,4,6 Positive

a
Exp.: experimentally created diversity gradient; Nat.: naturally occurring diversity gradient; Nutr.: gradient produced by different nutrient levels. F.: field study; M.: mesocosm/microcosm study.
1
Reanalysis of McGrady-Steed et al. (1997)
82 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

stability can reveal inter-relationships between the biodiversity still acts as biological insurance for
environment, stability and diversity. Valone and ecosystem processes (Ives et al. 2000, Thébault and
Hoffman (2003a,b) used an 11-year time series of Loreau 2005). Early empirical studies (Naeem and
grassland plots that varied naturally in species Li 1997, McGrady-Steed et al. 1997) showed a sta-
richness to investigate the relationship between bilizing effect of diversity on community-level
population and community-level temporal stability. properties but were difficult to interpret due to
In this system, population stability increased with confounding factors (Huston 1997, Fukami et al.
diversity, perhaps because the natural, productiv- 2001). Indeed, Morin and McGrady-Steed (2004) re-
ity-driven diversity gradient resulted in larger, analyzed data from their earlier publication (1997)
and thus relatively more stable, populations at and found that the previously reported effect
higher diversity (Valone and Hoffman 2003b). At was due to spatial variability among replicates.
the community level, the authors found a weak Recent BEF experiments, all conducted within
stabilizing effect of diversity at the small quadrat microcosms, have provided a further, less contro-
(0.25 m2) scale but not at the larger plot (0.25 ha) vertible, glimpse at the possible effects of diversity
scale (Valone and Hoffman 2003a). The incongru- on stability in multi-trophic systems. Steiner et al.
ity could be due to the scale of biological interac- (2005b) showed that diversity increased the tem-
tions, or simply due to smaller samples sizes, and poral stability of community biomass, whilst spe-
thus reduced statistical power, at larger scales. cies composition best explained variability in
At an even larger spatio-temporal scale, DeClerck population-level abundance. They invoke the posi-
et al.’s (2006) analysis indicates that there is no tive selection effect, suggesting that dominance of
relationship between a naturally occurring gradi- species with high population stability could
ent of conifer diversity and the temporal stability underlie much of the observed influence of diver-
of annual biomass production in Sierra Nevada sity. It would be interesting to investigate whether
forest stands. This may be explained by a low the populations of species that dominate mixtures
degree of species richness and highly correlated are generally more stable, since if there is a trade-off
responses of species to environmental changes. between resistance and productivity (Lep
s et al.
Diversity–temporal stability relationships are 1982), the opposite may be true.
expected to be highly variable across natural gra- Other mechanisms are proposed in studies based
dients depending on the environmental driver of on a microbial rock pool system. In microcosm
species diversity, the functional response range studies, Vogt et al. (2006) and Romanuk et al. (2006)
among the species, and direct environmental also found a stabilizing effect of diversity on the
influences on stability. aggregate abundance of the community, but here,
greater population stability at higher species richness
6.2.1.2 Temporal stability in multi-trophic summed to produce greater community stability. The
communities mechanism dampening population-level variability
Broadly, studies investigating the effects of diver- is not clear, but Romanuk et al. (2006) postulate that in
sity on temporal stability in multi-trophic systems pools with high levels of unused resources, popula-
fall into one of two categories: 1) Those that tions will tend to fluctuate more, because niche
examine diversity effects on the temporal stability complementarity (at higher diversity) reduces
of community-level (and often population) bio- resource levels, thus stabilizing populations. Their
mass; 2) Those that manipulate the diversity of a finding that population variability was greater in
non-basal species and examine effects on the sta- high nutrient microcosms is consistent with such a
bility of a non-biomass ecosystem process, e.g. mechanism (but contrasts with the findings of single
decomposition. We begin by addressing the former trophic level studies which showed that increased
type of multitrophic level study. productivity led to the loss of a diversity effect
Theory developed in the context of the BEF (Zhang and Zhang 2006b). In an observational study
research field predicts that, despite the complexity Kolasa and Li (2003) found that diversity increased
added when considering multi-trophic interactions, the temporal stability of microbial rock pool
 BIODIVERSITY AND THE STABILITY OF ECOSYSTEM FUNCTIONING 83

populations, but only when increasing specialization,

and therefore variability, of individual species with Box 6.1 From abundance to functioning
increasing diversity was statistically controlled. This
study shows that opposing forces operating in natu- The vast majority of diversity–temporal stability studies have
ral communities may yield no net effect of diversity used community biomass or its production as their measure
on population stability. of ecosystem functioning. Many of the theoretical
Two notable studies have considered how species mechanisms linking stability to diversity may equally apply
richness affects the temporal stability of ecosystem to other community-aggregated properties, but this has
seldom been tested. The stability of process rates represents
functions other than biomass or its production in
an important divergence from recent theory; instead of
multi-trophic systems. Dang et al. (2005) tested the
variation in species’ summed abundances forming the
effect of fungal diversity on both the mean magnitude response variable, the efficiency of species mediating
and temporal stability of decomposition. Whilst ecosystem functioning is also of interest. In this case, the
diversity had no effect on the magnitude, temporal density-mediated component directly linked to theory
stability increased in close correspondence to the null- pertaining to community biomass stability remains, but a
model of statistical averaging. Furthermore, the potentially density-independent ‘efficiency’ component is
outcome was robust to a range of environmental added. Furthermore, the specificity of the process measured
contexts. Tylianakis et al. (2006) examined the effect is likely to impact results. For example, If the ecosystem
of parasitoid diversity on the temporal stability of function is the flux of a particular nutrient (Bracken and
parasitism of wasps and bees. Again, diversity Stachowicz, 2006), there may be less functional redundancy
than for a universal process such as primary production or
enhanced the temporal stability of this ecosystem
decomposition. Since functional redundancy is a central
process, indicating that diversity may play an
tenet of the diversity–stability relationship, this suggests
important role in stabilizing trophic control within that, as functions become more specific, their stability will
complex food webs. Interestingly, the effect of be increasingly associated with the population stability of
diversity reported by both Dang et al. (2005) and the one or a few species mediating the function and
Tylianakis et al. (2006) was non-linear, producing less with the total diversity of the system. Where
the most rapid decrease in variability at relatively species vary in their contributions to multiple functions,
low levels of richness. This is consistent with statis- functional redundancy will be further reduced if such
tical averaging models (Doak et al. 1998; but see Box multiple functions are considered concurrently (Gamfeldt
6.2), but more studies, as well as theory pertaining to et al. 2007).
ecosystem processes other than biomass (Box 6.1), are
needed to determine the generality of these results.
Overall, the very restricted number of studies because these studies did not test mechanisms. Other
limits our ability to assess the effect of diversity on stabilizing mechanisms in food webs could be more
temporal stability in multi-trophic systems. However, prevalent as species richness and food web com-
the possibility that diversity may increase population plexity increases, thus stabilizing populations (Sec-
stability in these systems is intriguing and warrants tion 6.3.1). Direct empirical evidence of such effects,
further exploration, as it is contrary to theory and and how their efficacy and prevalence varies with
experiments conducted within single-trophic level, diversity, has yet to emerge. Detailed analyses of
competitive communities and May’s (1972, 1973) dynamic trophic interactions over a range of tempo-
models. Theory for multi-trophic systems (Thébault ral and spatial scales would be necessary to demon-
and Loreau 2005) predicts that diversity may increase strate such effects in food webs.
population stability under some conditions, for
instance, when consumers are either specialists or
generalists with a trade-off between niche breadth
6.2.2 The effects of discrete perturbations
and attack rate, and their temporal niche differentia- 6.2.2.1 Resistance
tion is low. It is difficult to assess whether these Tests of the insurance hypothesis could be garnered
mechanisms identified by theory explain the results from early studies comparing stress resistance across
of recent experimental and observational studies successional diversity gradients. The findings of
84 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Box 6.2 What causes diversity’s effects on temporal stability?

Despite established theoretical mechanisms linking diversity summed covariances have generally been interpreted as
and temporal stability, there is currently little consensus indicative of compensatory dynamics owing to competitive
regarding the relative importance of mechanisms release and/or differential response to environmental
underpinning effects observed in empirical studies. A number conditions (Tilman 1999; Petchey et al. 2002). But a
of authors have examined components of temporal variability fundamental problem with this statistical approach is that
in order to gain insight into the mechanisms underlying summed variances and summed covariances are strongly
observed effects of diversity. Temporal stability (ST), measured dependent on each other, and do not capture distinct
as 1/CV of community biomass, can be expressed as (Lehman biological mechanisms. Both reduced summed variances and
and Tilman 2000): reduced summed covariances are ultimately driven by the
P same mechanism, i.e. asynchronous species responses to
species biomasses environmental flutuactions (Loreau and de Mazancourt,
ST ¼ pP ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
P ffi
species variances þ species covariances unpublished manuscript).
Of the 18 studies discussed here (Table 6.1), nine included
The numerator in this equation captures the short-term or information on the statistical components of temporal
average effect of diversity on community biomass. All else stability; multiple contexts in two studies yield 13 experiments
being equal, an increase in average community biomass with for consideration. Nine of these experiments reported a
diversity due to overyielding tends to increase community positive effect of diversity on temporal stability, whilst two did
stability simply because average community biomass is used not detect an effect (Table 6.2).
to scale the variances and covariances in the CV. Additional Contrary to Tilman’s (1996) suggestion, the negative
long-term stabilizing effects of diversity can result from covariance effect – the result of increasingly asynchronous
reduced summed variances, reduced summed covariances, or population fluctuations with increasing diversity – is not a
both in the denominator. Reduction in summed variances has common phenomenon. Species richness resulted in
generally been interpreted as indicative of statistical averaging increasingly negative summed covariances in just a single
(Tilman 1999; Cottingham et al. 2001), whilst reduced study (Petchey et al. 2002). Two experiments actually

Table 6.2 Studies reporting the statistical components of temporal stability, their reported effects of diversity on community stability (1/CV),
summed covariances, summed variances, total community biomass, and the mean-variance scaling factor (z).
P P P
Reference Trophic level Stability Covariance Variance Biomass z*

Caldeira et al. (2005) Single Positive Increased Increased Increased >1

Petchey et al. (2002) Single None Reduced N/A Increased >1
Romanuk et al. (2006) Multiple (low nutrient) Positive No effect Increased Increased 1
Romanuk et al. (2006) Multiple (med nutrient) Positive No effect Increased Increased 0.83
Romanuk et al. (2006) Multiple (high nutrient) Positive No effect Increased Increased 0.85
Steiner (2005b) Single Positive No effect Reduced N/A 1.45
Steiner et al. (2005a) Single Positive No effect No effect Increased N/A
Steiner et al. (2005b) Multiple Positive No effect No effect Increased 1.55
Tilman et al. (2006) Single Positive No effect Reduced Increased 1.6
Valone and Hoffman (2003a) Single Positive Increased No effect Increased N/A
Vogt et al. (2006) Multiple Positive No effect Reduced No effect N/A
Zhang and Zhang (2006a) Single (low nutrient) Positive No effect No effect No effect 1.74
Zhang and Zhang (2006a) Single (high nutrient) None No effect No effect No effect 1.79

* z is a parameter in the equation relating CV for community biomass to total community biomass and the number of species in the community. The statistical
averaging stabilizing effect only occurs when z > 1 (Tilman et al. 1998).

continues
 BIODIVERSITY AND THE STABILITY OF ECOSYSTEM FUNCTIONING 85

Box 6.2 (continued) covariances or variances. Statistical averaging due to

revealed increasingly positive covariances with more asynchronous species fluctuations most likely contributed to
diversity. If species are similarly influenced by environmental the temporal stability of aggregate properties in numerous
variability, species abundances will track environmental studies – in fact, all seven studies that measured the scaling
conditions in a correlated manner (Vasseur et al. 2006; relationship between mean and variance reported values
Loreau and de Mazancourt 2008). Species may also respond indicating that, even in the absence of changes in summed
similarly if changes in environmental conditions are extreme covariances, diversity would be expected to enhance stability
relative to the range of tolerances exhibited by the (Doak et al. 1998; Tilman et al. 1998; Table 6.2).
assemblage (see Allison 2004). Positive species covariances Only two studies in multi-trophic systems measured the
do not necessarily preclude positive net diversity effects on statistical components of temporal stability, and they found
stability because any deviation from perfect correlation mixed results: whilst Vogt et al. (2006) invoke reduced
between species environmental responses can in principle population variability with diversity as a driver of community-
stabilize aggregate community properties (Yachi and Loreau level stability, Steiner et al. (2005b) found no such effect,
1999; Ives et al. 1999). instead crediting a form of the selection effect – the low
Greater diversity yielded increased, reduced, and population variability of dominant species with stabilization.
unaffected summed variances in four, three, and five With only two studies, comparisons between these and single-
studies, respectively. These mixed overall findings suggest trophic systems are not possible. Their greater complexity
that summed variances, just as summed covariances, allows for quite different patterns to emerge, however, as we
depend on context-specific factors not universally linked to discuss below in the context of food web ecology.
diversity, such as competitive interactions and how Overall, both theory and empirical data suggest that we
population abundance changes with diversity (see Valone have not yet started to disentangle the biological mechanisms
and Hoffman 2003a), in agreement with recent theory that underlie the stabilizing effects of diversity on ecosystem
(Loreau and de Mazancourt, unpublished manuscript). properties. The statistical partitioning of summed species
The most consistent explanation for a positive diversity– variances and summed species covariances, which was
stability effect is a combination of overyielding and proposed for this purpose, has proved ineffective. New
asynchronous species fluctuations. Of the seven experiments innovative approaches are needed to address mechanisms.
that yielded a stabilizing effect of diversity and reported One promising, but data demanding, alternative would be to
summed biomass with respect to diversity, overyielding test observed patterns of species temporal variations against a
(diversity and biomass were positively related) occurred in five. neutral model of community dynamics under the combined
If overyielding occurs, variance can be smaller relative to the influence of density dependence, environmental forcing and
mean even in the absence of any changes in summed demographic stochasticity (Loreau and de Mazancourt 2008).

such studies have been varied, with several sug- Early empirical findings generally, but not
gesting positive (Hurd and Wolf 1974, Mellinger and completely, supported the supposition that
McNaughton 1975, Lep
s et al. 1982) and others diversity will increase the resistance of commu-
suggesting a negative (Smedes and Hurd 1981, nity-level properties to perturbation (Loreau et al.
Berish and Ewel 1988) relationship between diversity 2002). Diversity increased resistance to drought
and resistance. These studies should, however, be across a gradient of nutrient enrichment in
interpreted with caution, as species composition and experimental grassland plots (Tilman and
life-history traits also vary during succession (Odum Downing 1994), even after the confounding
1969), making the role of diversity per se ambiguous. effect of fertilization was analytically controlled
Thus, a rigorous BEF experimental approach was (Tilman 1996). Several subsequent studies also
developed during the 1990s to more explicitly test revealed a positive diversity–resistance relation-
the hypothesis. Thirteen studies, including 14 ship (Griffiths et al. 2000, Joshi et al. 2000, Mulder
experiments, three of which measured two ecosys- et al. 2001). Wardle et al. (2000a), however,
tem properties each, have used this approach (Table emphasized the importance of composition,
6.3). Five experiments yielded a positive effect of finding no effect of plant functional group rich-
diversity, whilst eight showed no effect and four ness on stability to drought in a greenhouse
showed a destabilizing effect. experiment.
Table 6.3 Effects of diversity on resistance to specific perturbations.

Reference Stability Trophic level Ecosystem Diversity Ecosystem type Perturbation Time scale Div levels Type of
property property measureda gradientb div effect

Allison (2004) Resistance Primary prod Community biomass Rem. F Intertidal Heating 21 m 1 to 3 FG Negative
Caldeira et al. (2005) Resistance Primary prod Community biomass Exp. F Grassland Drought/frost 1 yr 1 to 14 None
DeClerk et al. (2006) Resistance Primary prod Primary Productivity Nat. F Forest Drought 64 yr 1 to 4 None
Griffiths et al. (2000) Resistance Multi Decomposition rate Rem. M Pasture soil Heating 1 yr NA Positive
Joshi et al. (2000) Resistance Primary prod Community biomass Exp. F Grassland Invasion 1 yr 1 to 32 Positive
Kahmen et al. (2005) Resistance Primary prod AG Community biomass Nat. F Grassland Drought 7w 13 to 38 None
Kahmen et al. (2005) Resistance Primary prod BG Community biomass Nat. F Grassland Drought 7w 13 to 38 Positive
Mulder et al. (2001) Resistance Primary prod Community biomass Exp. F Bryophytes Drought 5d 1 to 32 Positive
Pfisterer and Schmid (2002) Resistance Primary prod Community biomass Exp. F Grassland Drought 8w 1 to 32 None
Pfisterer and Schmid (2002)1 Resistance Primary prod Community biomass Exp. F Grassland Drought 8w 1 to 32 Negative
Tilman and Downing (1994)2 Resistance Primary prod Community biomass Nutr. F Grassland Drought 2 yr 1 to 26 Positive
Van Peer et al. (2004) Resistance Primary prod Community biomass Exp. M Grassland Drought and heat 8w 1 to 8 Negative
Wardle et al. (2000) Resistance Multi Plant biomass Exp. M Grassland Drought 14 m 2 to 7 None
Wardle et al. (2000) Resistance Multi Decomposition rate Exp. M Grassland Drought 14 m 2 to 7 None
Zhang and Zhang (2006a) Resistance Primary prod Community biomass Exp. M (HN) Aquatic Cold 6d 1,2,4,7 none
Zhang and Zhang (2006a) Resistance Primary prod Community biomass Exp. M (LN) Aquatic Cold 77 d 1,2,4,8 none
Zhang and Zhang (2006b) Resistance Primary prod Community biomass Exp. M Aquatic Cold 105 d 1 to 5 Negative

a
AG: above-ground; BG: below-ground
b
Exp.: experimentally created diversity gradient; Rem.: gradient produced from selective removal of species; Nat.: naturally occurring diversity gradient; Nutr.: gradient produced by different nutrient levels. F.: field study; M.:
mesocosm/microcosm study. LN: low nutrients. HN: high nutrients
1
Resistance as measured as absolute biomass lost (see text)
2
As reanalysed by Tilman (1996)
 BIODIVERSITY AND THE STABILITY OF ECOSYSTEM FUNCTIONING 87

These earlier studies, as well as theory, did not The positive pre-stress relationship between
consider pre-disturbance effects of diversity on diversity and biomass was diminished as the
resource use and community composition. Incor- demand for water exceeded acquisition in species-
porating these effects yields several possible con- rich communities.
sequences stemming from selection effects and In all of these experiments the positive diversity–
complementarity – the mechanisms that lead to resistance relationship predicted by the insurance
positive relationships between diversity and the hypothesis was absent, implying that diversity may
magnitude of ecosystem functioning. If the positive not simultaneously increase the magnitude and
selection effect is in operation, fast-growing species, resistance of ecosystem functioning. High commu-
which tend to be more vulnerable to stress (Lep
s nity biomass could mean that each individual within
et al. 1982), may dominate diverse mixtures, poten- a diverse community suffers greater resource limita-
tially producing a negative diversity–resistance tion, as a finite resource supply is under greater
relationship. Recent synthesis shows that while the demand; in effect, the disturbance size is greater for
positive selection effect is a common phenomenon in each individual. The shortfall between resource
BEF studies, there are a substantial number of demand and supply may outweigh the effect of the
studies reporting negative selection effects (Cardi- increasing range of species’ tolerances with greater
nale et al. 2007). This raises the possibility that the diversity.
above mechanism may be reversed in these cases, The implication of this hypothesis is that in the
but empirical studies have yet to examine this absence of a positive diversity–biomass relation-
possibility. ship, evidence of the insurance effect will be more
Pfisterer and Schmid (2002) postulate that com- likely. There are insufficient studies to assess this
plementarity indirectly rendered diverse grassland rigorously, but three studies provide tentative
plots at the Swiss BIODEPTH site more vulnerable support for this hypothesis. Across a natural
to experimental drought: the drought reduced the diversity gradient in German grasslands, Kahmen
niche complementarity responsible for greater pro- et al. (2005) found that the resistance of below-
duction in diverse communities. This raises the ground biomass to an experimental drought
possibility that there may be a trade-off between a increased with plant diversity, but no effect on
positive influence of diversity on the magnitude of aboveground biomass was observed. Reference
ecosystem functioning and ecosystem stability. An plots showed no relationship between diversity and
important point is that Pfisterer and Schmid (2002) pre-stress biomass. Mulder et al. (2001) and Hughes
recorded a greater absolute reduction in biomass in and Stachowicz (2004) similarly reported a positive
more diverse plots, whilst there was no difference influence of diversity on stress resistance in systems
when resistance was measured relative to pre- without a pre-disturbance diversity–biomass rela-
drought biomass. Resistance is most meaningfully tionship.
measured as a reduction in an ecosystem process
relative to the pre-perturbation level; indeed, this is 6.2.2.2 Resilience
commonly practiced (Pimm 1984) and is consistent Loreau and Behera (1999) found that diversity and
with measures of temporal stability. resilience may be negatively related within theore-
Other experiments have revealed no effect of tical competitive communities. Based on the very
diversity on this metric of resistance, despite pos- few published empirical tests (Table 6.4), no con-
itive effects of diversity on pre-stress biomass sistent influence of diversity on resilience of com-
(Wardle et al. 2000a, Caldeira et al. 2005, Zhang munity properties is evident. Studies of successional
and Zhang 2006a). Furthermore, both Caldeira et diversity gradients show negative relationships
al. (2005) and Zhang and Zhang (2006a) report that between diversity and resilience (Smedes and Hurd
complementarity and selection effects were not 1981, Lep
s et al. 1982), but species’ life-history traits
modified by environmental stress. Finally, Van probably played a confounding role here. Theore-
Peer et al. (2004) found a negative effect of diver- tical predictions (Loreau and Behera 1999) are sup-
sity on resistance measured in relative terms. ported by just a single BEF experiment (Pfisterer and
Table 6.4 Effects of diversity on resilience of ecosystem properties following a perturbation.

Reference Stability property Trophic level Ecosystem property Diversity Ecosystem Perturbation Time scale Div levelsb Type of
measured gradienta type div effect

Allison (2004) Resilience Primary prod Community biomass Exp. M Intertidal Heating 21 m 1 to 3 FG Positive
DeClerk et al. (2006) Resilience Primary prod Primary Productivity Nat. F Forest Drought 64 yr 1 to 4 Positive
Griffiths et al. (2000) Resilience Multi Decomposition rate Rem. M Pasture soil Heating 1 yr Positive
Pfisterer and Schmid (2002) Resilience Primary prod Community biomass Exp. M Grassland Drought 8w 1 to 32 Negative
Steiner et al. (2006) Resilience Multi Community biomass Exp. M (HN) Aquatic Non-selective 53 d 1 to 4 None
Steiner et al. (2006) Resilience Multi Community biomass Exp. M (LN) Aquatic Non-selective 53 d 1 to 4 Positive
Tilman and Downing (1994)1 Resilience Primary prod Community biomass Nutr. F Grassland Drought 2 yr 1 to 26 None

a
Exp.: experimentally created diversity gradient; Rem.: gradient produced from selective removal of species; Nat.: naturally occurring diversity gradient; Nutr.: gradient produced by different nutrient levels. F.: field study; M.:
mesocosm/microcosm study. LN: low nutrients. HN: high nutrients
b
FG.: Functional groups
1
As reanalysed by Tilman (1996)
 BIODIVERSITY AND THE STABILITY OF ECOSYSTEM FUNCTIONING 89

Schmid 2002), which showed lower resilience in bilizing effect of diversity in the face of extreme
high-diversity grassland plots nine months after perturbations – a trade-off that needs further
drought. Tilman (1996) found no effect of diversity mechanistic exploration. Multi-trophic studies have
on resilience after analytically removing the con- been limited in number and scope, mainly being
founding factors present in an earlier analysis conducted in microbial rock pools or laboratory
(Tilman and Downing 1994). Conversely, resilience microcosms. Nevertheless, the typical result that
increased with functional group richness in inter- populations are actually stabilized by diversity in
tidal seaweed communities (Allison 2004), with these systems is intriguing and represents a major
conifer species richness in the Sierra Nevada distinction from classical theory (e.g. May 1973) and
(DeClerck et al. 2006), and with diversity within five findings from some grassland experiments (Tilman
trophic levels in a microcosm experiment (Steiner 1996, Tilman et al. 2006b).
et al. 2006). DeClerck et al. (2006) invoke comple-
mentarity, suggesting that during community
6.3 A broadening perspective
recovery, resources are abundant, thus resource
partitioning is possible along several niche axes – a Whilst of undoubted value, controlled experiments
postulation that perhaps deserves further theoretical are logistically constrained. Isolating the role of
and empirical consideration. Steiner et al. (2006), on diversity per se from that of species identity
the other hand, credit their result to the sampling has proven a formidable task requiring large
effect, as resilient communities exhibited a reduction numbers of treatments and replicates. This has
in evenness over time. limited experiments to tractable, closed, small-scale
It is difficult to separate resilience from resistance. systems–predominantly grassland plots and labo-
Indeed, most studies have not removed the legacy of ratory microcosms. Hence the degree to which the
resistance from measures of community recovery findings from these experiments are applicable to
(Tilman and Downing 1994, Mulder et al. 2001, larger, landscape scales, different systems, and the
Pfisterer and Schmid 2002, Allison 2004). To achieve delivery of important ecosystem services is ques-
this, a non-selective mortality event must occur or be tionable.
experimentally applied (Steiner et al., 2006). In Building a more complete understanding of the
nature, however, resistance and resilience are inex- role of diversity in stabilizing ecosystem function-
tricably linked, because the community recovers ing in these broader contexts requires approaches
with its post-perturbation composition and abun- that trade replication and control for studies con-
dance. Thus, whilst equally reducing abundances of ducted over larger scales and in complete systems.
populations to isolate resilience per se from the In this section we outline three areas that address
effects of the disturbance is of considerable theore- this link. First, we discuss several recent develop-
tical interest, the relevance to real systems is ques- ments in theory that demonstrate how properties of
tionable. food webs can affect aspects of population and
community stability. Second, we assess possible
effects of diversity on stability in systems with
6.2.3 Summary of empirical progress
multiple stable states, before finally highlighting the
Numerous diversity–stability experiments have possible role of diversity in stabilizing the delivery
been published in the last half-decade, substantially of two key ecosystem services: pollination and yield
improving our understanding of the relationship from fisheries.
between diversity and various facets of stability at
population and community levels. Whilst diversity
6.3.1 Lessons from food webs
was commonly found to enhance community-level
temporal stability, the effect of diversity on resis- Although BEF research has begun to examine the
tance and resilience is more equivocal. There is effect of diversity on the stability of multi-trophic
some empirical evidence to suggest that positive aquatic systems, the tie between food web theory
diversity–productivity effects may preclude a sta- and BEF science is not yet strong. This is
90 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

unfortunate, because recent developments in food changing in species composition, structure, and
web theory illustrate several stabilizing properties dynamics (de Ruiter et al. 2005), yet most theoretical
of food webs that may explain the inconsistency of studies of diversity–stability relationships assume
results in BEF-stability studies so far. Moreover, static patterns of trophic linkage (May 1972, Pimm
how species loss affects these properties can pro- and Lawton 1977, 1978, de Ruiter et al. 1995, Neutel
vide insight on diversity’s effects in systems too et al. 2002). Adaptation is suggested as one mecha-
complex for controlled experimental treatments. It nism from which food web flexibility arises (Kondoh
must be noted that the food web literature provides 2006), with adaptive defences by prey and adaptive
definitions of stability that often vary from those in foraging by predators influencing the strength of
the BEF literature, they generally focus on recovery trophic interactions. The flexibility provided by
times following perturbations to the system, but adaptive foraging should enhance community per-
also encompass measures of temporal variability sistence, as predators capable of a foraging shift can
among component species. Additional aspects of maximize their net energy gain by switching away
stability, not addressed in BEF experiments to date, from a less profitable resource. Indeed, Kondoh
may also have implications for ecosystem func- (2003) demonstrated that the classic negative
tioning, and as such several are outlined here. complexity–stability relationship of many theoretical
It is now widely acknowledged that weak trophic studies is inverted when the effects of adaptive for-
interactions confer stability (population-level resil- aging behaviour are incorporated. There are obvious
ience) in natural food webs, and therefore that food implications of this mechanism for the diversity–
webs with lower mean interaction strength are more stability relationship, although they have yet to be
stable. However, the configuration of interactions is explicitly explored in the context of BEF research. A
also important, as the destabilizing effects of strong reduction of species diversity through the loss of
trophic links can be dampened if those strong links prey species will limit the prey-switching options of
are coupled to weak interactions (McCann 2000). adaptively foraging predators.
Coupled weak and strong interactions can promote Primary species loss can trigger secondary
asynchronous population fluctuations of prey, sta- extinctions, further reducing diversity and its
bilizing aggregate prey biomass as well as resource associated stabilizing effects on ecosystem func-
supply to a switching predator (McCann 2000). This tioning. The tolerance of a food web to species loss
weak interaction effect may have marked implica- is also an important aspect of stability in its own
tions for the temporal stability of community bio- right: robustness (see Loreau et al. 2002). The traits
mass in food webs. Furthermore, it has been shown of the deleted species markedly affect the likelihood
that weak interactions confer local stability to food and extent of secondary extinctions (see also
webs when they occur in omnivorous food web Chapter 5). For example, like keystone species and
loops (Neutel et al. 2002, Emmerson and Yearsley ecosystem engineers, the loss of a highly connected
2004). Simulation studies have shown that an anal- species (species with a high proportion of total
ogous effect can be scaled up to fast and slow possible trophic links realized) has been shown to
‘energy channels’ within food webs generated have disproportionate effects on food web structure
through alternative energy sources (Rooney et al. (Solé and Montoya 2001).
2006). Species loss will alter the number and con- Robustness may also depend on the characteristics
figuration of stabilizing weak interactions, as well as of the entire food web. The amount of connectance is
the mean interaction strength (McArthur 1955, important, as high connectance may delay the onset
McCann 2000), potentially destabilizing populations of an extinction threshold (Dunne et al. 2002b).
and ecosystem functions. Whether connectance and species richness are asso-
In reality, food webs are not static structures fixed ciated in empirical (not theoretical) food webs is
in time; they are dynamic, varying in structure sea- unresolved, however. Whilst Dunne et al. (2002b)
sonally and from year to year. How such dynamic report no relationship, Montoya and Solé (2003)
topologies persist is poorly understood. In this con- found connectance to be lower in species-rich webs.
text, food webs are flexible structures, constantly The distribution of trophic links between species, the
 BIODIVERSITY AND THE STABILITY OF ECOSYSTEM FUNCTIONING 91

degree distribution, also has consequences for Loreau et al. 2002, Hooper 2005), stability has been
robustness. Food webs with skewed degree dis- considered with respect to a single ‘stability
tributions, i.e. numerous poorly linked species and a domain.’ Both theory and observations, however,
few highly linked species, are robust to random have shown that many ecosystems can exhibit non-
species deletion but sensitive to removal of the most linear dynamics, switching between multiple stable
connected species (Solé and Montoya 2001, Dunne et states (Scheffer and Carpenter 2003). It is thus
al. 2002b). This is because randomly deleted species unclear the extent to which findings from the
are likely to be poorly linked, thus having minimal studies discussed here (Table 6.1) can be applied to
knock-on effects on others. Across 12 well-described multiple equilibrium systems. Ecological resilience
food webs, Montoya and Solè (2003) show that the sensu Holling (1973) describes the amount of dis-
degree distribution becomes progressively more turbance a system can absorb whilst still remaining
skewed with increasing species richness. Conse- within the same basin of attraction and can be
quently, species-poor webs are less robust in heuristically viewed as the size of a particular sta-
response to random species loss, since most species bility domain. Changing environmental conditions,
are moderately well linked. Therefore, whether compounded perturbations and/or species loss can
species-rich food webs are likely to be more robust reduce ecological resilience, increasing the proba-
to species loss depends on whether species loss is bility of an abrupt ‘catastrophic shift’ to an alter-
random with respect to species’ connectedness (see native state. The insurance hypothesis has been
also Chapter 5). Other key factors that determine the incorporated into this view of ecosystems (e.g.
effects of diversity on cascading species extinctions Peterson et al. 1998, Gunderson 2000): assuming
and ecosystem functioning include the strength of that biodiversity increases the range of responses to
intraspecific density dependence (Thébault et al. the environment (functional response diversity), a
2007). more diverse system is buffered against impacts of
Although the properties that affect food web sta- perturbations and resultant catastrophic shifts.
bility are critical to understanding the stability of Despite a dearth of experimental studies, the idea
ecosystem functioning in complex (multi-trophic) that biodiversity begets stability in systems with
systems, it must be noted that comparisons across multiple stable states seems to be widely accepted.
food webs may give results that differ from changes Reviews of regime shifts and ecosystem resilience
within a single food web. It is unknown, for example, assume a strong connection between functional
whether the degree distribution of a species-rich web response diversity and resilience (e.g. Gunderson
will become increasingly centralized, mirroring spe- 2000) or loss of diversity and loss of function
cies-poor webs, as diversity is eroded within it. If this (Briske et al. 2006). The diversity–stability concept
happens, food webs losing species will become ever even seems to have influenced environmental
more sensitive to random species deletion, yielding a management in certain systems. For example,
positive feedback that may exacerbate system col- maintaining or increasing landscape diversity in
lapse. Cross-fertilization of ideas between BEF and pastures and rangelands is encouraged or required
food web science will help answer this and other by many land-use agencies and programs (e.g.
unknowns. Investigating how food web properties Mason et al. 2003, Mitchell et al. 2005), often for
vary concurrently with species richness in natural maintaining or increasing biodiversity itself, but
and manipulated food webs will help to better inte- also for increasing resilience in the face of distur-
grate BEF science with food web theory. bance (Pellant et al. 2004, Drever et al. 2006). The
question is whether evidence supporting these
ideas exists in the systems to which they are
6.3.2 Diversity–stability in complex,
applied. Rangelands and coral reefs, two systems
real-world systems
that provide a number of ecosystem services for a
6.3.2.1 Systems with multiple stable states large part of the Earth’s population and exhibit
In all explicit diversity–stability experiments dis- dramatic instability (undergo state changes) serve
cussed here and elsewhere (Cottingham et al. 2001, as examples.
92 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Range and pasture lands occupy approximately most functional groups, presumably making them
20 per cent of the land surface of the globe in less susceptible to such phase-shift-causing per-
areas that are particularly susceptible to drastic turbations (Bellwood et al. 2004). However, taxo-
ecosystem changes such as desertification and nomic richness does not guarantee functional
grass-to-shrubland conversion (Hodgson and Illius resilience. A different single species, which is rel-
1996). Consequently, they have been the focus of atively rare, was responsible for reversing an
many conceptual developments regarding ecologi- experimentally induced coral–algal phase shift
cal thresholds and alternative state theory, which in the same system by high consumption on the
are closely tied to the concept of ecological resil- fleshy algae (Bellwood et al. 2006). The effect of
ience (e.g. Briske et al. 2006). Although there is a this single keystone species in the latter study was
wealth of literature on these topics, and the entire a complete surprise, in that it was previously
basis of rangeland management is now shifting to unknown to consume these algae. The identity of
this paradigm in some parts of the world (USDA- species, rather than richness per se, may thus have
NRCS 1997), there has been little research directly dominant effects on the resilience of coral reefs
testing the role of biodiversity in rangeland resil- (see also Bellwood et al. 2003).
ience, state changes, or other aspects of stability at That this surprise occurred in one of the better-
the scales that are applicable to range and pasture studied systems in the world clearly supports the
managers. precautionary approach in biodiversity conserva-
Two studies that directly address the relation- tion. These results also highlight the fact that high
ship between biodiversity and stability in actual diversity does not guarantee high redundancy and
production systems had contrasting results. In the stability often associated with it. If all the
Australian sheep pastures with a range of plant redundancy is in one functional group, then
species richness caused by various manipulations diversity will not necessarily promote stability. This
(grazing regime, fertilization) and environmental is particularly relevant in light of the perturbations
conditions (climate, soils), variability of herbage that afflict ecosystems today. All ecosystems
production over 3–4 years was either not signifi- evolved with a regime of disturbance, and evolu-
cantly related or slightly negatively related to tionary processes likely led to functional effect
plant diversity or species richness (Kemp et al. redundancy within these systems because of dif-
2003). On the other hand, in dairy cattle pastures ferences in organisms’ responses to this disturbance
planted specifically to compare plant species rich- regime (e.g. Walker et al. 1999). Novel individual
ness effects on herbage production, yield did not perturbations (e.g. new diseases), as well as new
differ significantly among treatments of 2, 3, 6, or 9 combinations of disturbance events, could be tap-
species in years with normal precipitation, but the ping into functional types where that response
two-species pasture did have lower production redundancy does not yet exist.
than the others in a dry year (Sanderson et al.
2005). 6.3.2.2 Diversity and the stability of
The evidence from coral reefs is equally equiv- ecosystem services
ocal. A biogeographical comparison can provide a Several empirical studies have recently emerged
tentative insight into the possible role of species that bridge the gap between controlled experi-
diversity in providing resilience on coral reefs. In ments and real-world applications, demonstrating
the Caribbean, eutrophication from increased how human-impacted ecosystems can be used to
nutrient inputs, disease, and over-harvesting of examine the roles of environmental change and
herbivorous fishes has resulted in a phase shift biodiversity in the stability of ecosystem service
from coral- to fleshy macroalgae-dominated reef provision. Here we discuss two ecosystem ser-
communities (Hughes 1994). Although the suite of vices, first pollination and second fisheries yield,
functional groups is similar between Indo-Pacific as examples. Both of these examples suggest that
reef systems and Caribbean reef systems, the for- species diversity can influence the stability of
mer have much greater taxonomic diversity within ecosystem service provision.
 BIODIVERSITY AND THE STABILITY OF ECOSYSTEM FUNCTIONING 93

Pollination is one key ecosystem service that ther efforts to explore the role of species diversity in
has received attention within agricultural land- mediating various aspects of the stability of eco-
scapes. Kremen et al. (2002, 2004) showed that system service delivery will both inform the man-
intensive farming practices and a reduced pro- agement of such services, and also contribute to our
portion of natural habitats negatively affects general understanding of diversity–stability rela-
the diversity of pollinators and temporal stability tionships in real-world systems. Such studies will
of melon pollination. Sites with high pollinator also help to integrate our understanding of the
species richness provided more stable pollination drivers of species diversity and its ecological
services over time than sites with low species effects.
richness because of asynchronous fluctuations in
the populations of pollinators from one year to
6.4 Conclusions
the next. The role of species richness in spatial
stability of pollination was demonstrated in coffee Recent studies have yielded great progress in
plantations: greater pollinator diversity, which is understanding diversity’s effects on the stability
affected by local (e.g. plant diversity, light avail- of ecosystem functioning in increasingly complex
ability) and regional (e.g. isolation from natural systems. Clearly, however, there is still much
habitat) factors, reduced spatial variation in fruit work to be done to reconcile theory, experimental
set between coffee plants (Klein et al. 2003a, b; results, and observations from natural or human-
Chapter 14). altered systems. A key step towards this goal
Fisheries provide an important source of food for must be elucidating the mechanistic basis of
much of the world’s population, underpinning the diversity effects on aspects of stability in a range
diets and economies of many coastal communities of systems; a challenge that requires greater inte-
in the world’s poorer countries. Collating data from gration of theoretical and empirical work (Box 6.2).
the world’s fisheries, Worm et al. (2006) found that Insights from a growing body of food web analy-
the proportion of collapsed fisheries in a region was ses and simulations may help to explain the find-
negatively related to its fish taxonomic diversity. ings of BEF stability studies in multi-trophic
Furthermore, they discovered that the likelihood of systems.
recovery from fisheries collapse was positively To increase the applicability of diversity–stability
associated with species richness across large marine research the effects of realistic diversity changes on
ecosystems. Causality is difficult to infer from this valuable ecosystem services must be investigated.
correlative approach, but the results support the Studies across gradients of anthropogenic impacts
supposition that diversity increases both resistance have great potential to address this need, as these
to – and recovery from – over-exploitation. Those gradients incorporate both local (habitat) and
harvesting the fish benefit from greater diversity, as landscape factors responsible for shifts in diversity
the reliability and abundance of total catches (Chapter 14). Long-term measures of diversity and
increases with diversity. Humans act as switching, related ecosystem services across these land-use
wide-ranging predators, releasing stocks from gradients, combined with modelling and meso-
predation as they become scarce (McCann 2000) cosm studies based on the communities occurring
and changing to a more abundant species, thus across these gradients, would help to elucidate the
deriving a stable supply from numerous fluctuating effect of biodiversity on the stability of key eco-
resources (Worm et al. 2006). This mechanism may system services and potentially shed light on the
partly explain why diverse fisheries are less likely underlying mechanisms. Recent work in the field
to collapse – it is more profitable to switch targets if of ecological economics shows that stability
more abundant species are available. The well- adds additional economic value to ecosystem ser-
known collapse of the Newfoundland cod fishery vices in the form of insurance (Chapter 17), further
could be attributed to a single target species, underlining the importance of a thorough under-
compared to the diverse portfolio of taxa exploited standing of the effect of biodiversity on ecosystem
in tropical subsistence fisheries, for example. Fur- functioning and associated services.
 CHAPTER 7

The analysis of biodiversity

experiments: from pattern toward
mechanism
Andy Hector, Thomas Bell, John Connolly, John Finn, Jeremy Fox,
Laura Kirwan, Michel Loreau, Jennie McLaren, Bernhard Schmid,
and Alexandra Weigelt

7.1 Introduction review the debate over the mechanisms responsible

for relationships between biodiversity and ecosys-
This chapter reviews the methods developed to
tem functioning.
investigate the mechanisms that generate relation-
ships between diversity and functioning in biodi-
7.1.1 Background
versity experiments. What do we mean by
mechanism? An important recent advance in ecol- Following a landmark conference in 1992, the study
ogy and evolution has been the championing of of the relationship between biodiversity and eco-
mechanistic statistical models (Mangel and Hilbourn system functioning became a focused area of
1997). These statistical models are mechanistic in the research. In the edited book that arose from that
sense that their parameters refer to biological pro- meeting (McNaughton 1993, Schulze and Mooney
cesses that can be quantified, rather than to 1993) quoted the following from Chapter 4 of On
unmeasureable abstract concepts that often prove The Origin of Species: ‘It has been experimentally
useful in purely theoretical models of ideas. Simi- proved that if a plot of ground be sown with one
larly, non-linear regression analysis is often species of grass, and a similar plot be sown with
described as ‘semi-mechanistic’ when parameters several distinct genera of grasses, a greater number
can be at least loosely related to biological processes of plants and a greater weight of dry herbage can
(Pinheiro and Bates 2000). In many areas of science thus be raised’. The quote concisely makes a pre-
there are often multiple layers of mechanism diction – that more diverse plant communities
underlying the phenomena of interest. As we will should be more productive – and indicates the
explain below, some of the models reviewed in this underlying mechanism. Darwin contrasts one spe-
chapter could be termed fully mechanistic in that cies with several distinct genera, implying that it is
they can be built to include parameters that refer the ecological niche differences between species
directly to ecological processes (e.g. predation rates), that underlie this effect. More extensive text from
whereas some of the other methods could be termed Darwin’s Natural Selection (Stauffer 1975) clarifies
semi-mechanistic in the sense that they can indicate that Darwin really was relating biodiversity to
the presence of ecological processes (e.g. ‘comple- ecosystem functioning via what he termed the
mentarity effects’) even if, as explained above, they ‘ecological division of labour’ (Hector and Hooper
cannot quantify the exact biological process that 2002) when he wrote that, ‘A greater absolute
underlies these effects. To understand the motivation amount of life can be supported . . . when life is
for the development of these methods we first developed under many and widely different

94
 THE ANALYSIS OF BIODIVERSITY EXPERIMENTS: FROM PATTERN TOWARD MECHANISM 95

forms . . . the fairest measure of the amount of life existing datasets. Two of the main limitations of
being probably the amount of chemical composi- these methods are that they require measurements
tion and decomposition within a given period.’ of how species affect ecosystem functioning when
Following McNaughton many researchers have grown alone (that is all species must be grown in
reproduced this quote and its popularity reflects the monoculture) and the contributions of individual
tendency of ecologists at this time to focus on these species to the ecosystem functioning of mixtures
ecological niche differentiation mechanisms and the (e.g. the total productivity of a mixed community
species ‘complementarity’ (as introduced by must be broken down into the contributions of
Woodhead 1906) that results from these differences. individual species). For certain organisms and for
However, there is a second class of potential particular functions, these requirements are often
mechanisms that was under-represented in the difficult or impossible to meet. Hence there is the
early literature. The sampling effect hypothesis need for a varied toolbox of methods for the anal-
(Aarssen 1997, Huston 1997, Loreau 1998a, Tilman ysis of mechanism in biodiversity experiments that
et al. 1997c) proposes that in biodiversity experi- can encompass all organisms and all ecosystem
ments randomly assembled diverse communities processes. We think that this suite of tools now
have a higher probability of containing and being exists and the aim of this chapter is to provide a
dominated by the species which is most productive comparative review and users guide to these
when grown alone. The selection effect (Loreau and methods. Given the number of methods and limited
Hector 2001) and dominance effect (Fox 2005b) are space, and the fact that all of the methods have
similar but more general effects that relate the rel- already been described in the literature, we restrict
ative abundance of species in mixtures to their the main text to general descriptions only (with
performance when grown alone (see below). detailed supplementary material provided by the
Species complementarity is sometimes used with authors of each method). The literature has mainly
reference only to resource partitioning. However, focused on productivity as an ecosystem function
both conceptually and in practice, it is often difficult and our discussion does the same even though
to separate resource partitioning from facilitation some of these methods can be applied to other
and other ecological processes such as diversity- ecosystem process.
dependent differences in natural enemy impacts
(Connell 1978, Janzen 1970, Root 1973, Zhu et al.
2000). This set of ‘complementarity effects’ and the 7.2 Analysis of mechanism in
alternative set of ‘sampling’, ‘selection’ or ‘domi- biodiversity experiments
nance effects’ are not mutually exclusive (they often 7.2.1 Transgressive overyielding
can and do occur together) and can produce very
similar patterns. This means that when analyzing One of the simplest analyses that can be performed is
biodiversity experiments, process cannot be inferred a comparison of the functioning of mixtures relative
from pattern alone. Distinguishing the contributions to the best-performing single-species community
of these alternative classes of mechanism has become (monoculture). Mixtures that perform significantly
an important goal in the analysis of biodiversity better than the best monoculture are said to trans-
experiments, since they can indicate what sorts of gressively overyield and transgressive overyielding
ecological processes have generated the observed has often been seen as the acid test for positive effects
pattern and are important considerations in inter- of biodiversity (Cardinale et al. 2006a, Cardinale et al.
preting the results of these experiments. 2007, Hector et al. 2002b, Kirwan et al. 2007).

7.1.2 Limitations and needs 7.2.2 Overyielding: relative yields

Some of the methods available to investigate A second approach is to look for overyielding more
mechanism in biodiversity experiments have lim- generally by comparison to the single-species per-
itations that mean they cannot be applied to many formances of all of the species present in a mixed
96 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

community. The concept of ‘relative yields’ (RYs) yields versus their null expectation values) and is
has been used for this purpose in plant ecology and linearly related to RYT (but scaled to a null value of
agriculture since the mid-twentieth century (De Wit zero rather than 1). Complementarity effect values
and Van den Bergh 1965, Harper 1977, Vandermeer > 0 indicate positive effects of biodiversity on
1989). The relative yield of a plant species is simply overyielding while values < 0 indicate interference
its biomass in mixture expressed as a proportion of competition. The other half of the partition is a
its biomass in monoculture. Summing the relative covariance term that was inspired by the Price
yields for all species in a mixture provides a relative equation from evolutionary genetics (although as
yield total (RYT). Relative Yield Total values greater we explain below the additive partitioning method
than one show that increases in the abundance of and Price equation are different). The selection
some species in mixture have not been exactly effect measures the covariance between a species
compensated by decreases in others (as would be trait (e.g. monoculture biomass) and its perfor-
the case in a zero-sum game (Hubbell 2001)). mance in mixture. Positive selection effect values
Overyielding (as distinct from transgressive over- indicate that species with greater than average
yielding) is often taken to indicate resource parti- monoculture biomass perform better than expected
tioning but can also occur through facilitation and in mixture, while negative values indicate the con-
other mechanisms, such as the reduction of natural verse. While the Loreau–Hector additive partition-
enemy impacts in mixtures (as described above). ing method does not examine biological processes
Loreau (1998b) devised a more general scheme of directly, it has allowed major advances in the
deviations from expected values that are closely debate over the mechanisms underlying the pat-
related to the earlier relative yield-based measures. terns found in biodiversity experiments (e.g. Loreau
Overyielding-based methods usually assume a and Hector 2001, Cardinale et al. 2007).
substitutive experimental design in which total
density is held constant, independent of diversity, 7.2.3.2 Tripartite additive partitioning of
although the method can be adapted for additive biodiversity effects
designs too (where additive means that the total One limitation of the additive partition is that it
density is the summed total of the densities of all of assumes, as do relative yields, that complementar-
the component species). ity is distributed equally across species. This means
that it may over- or underestimate total comple-
mentarity, some of which falls under the selection
7.2.3 Additive partitioning methods
effect (Petchey 2004). The tripartite partition (Fox
7.2.3.1 Two-way additive partitioning 2005b) is a modification of the additive partition of
of biodiversity effects Loreau and Hector (2001) described above. The
The additive partitioning method (Loreau and two versions share the same goal of identifying
Hector 2001) extends the relative yield approach whether, and for what reasons, the functioning of a
described above to define an overall net biodiver- given mixture of species deviates from that expec-
sity effect and to partition this into two additive ted under a simple null hypothesis (see supple-
components: a complementarity effect and a selec- ment). However, the tripartite version partitions
tion effect (see supplementary material). In a sub- the difference between observed and expected
stitutive experiment, the net biodiversity effect (for function into three additive components: the dom-
a community formed from species started at equal inance effect (DE), trait-independent complemen-
densities) is simply the difference between the tarity effect (TICE), and trait-dependent
observed yield of the mixture and the average of complementarity effect (TDCE). The two versions
the monoculture yields. The net biodiversity effect are related as follows. The complementarity effect
equals zero when individual plants grow equally from the two-way additive partition corresponds
well in monoculture and mixture. The comple- exactly to the trait-independent complementarity
mentarity effect is based on changes in relative effect from the tripartite version. However, the
yields (or rather, differences in observed relative tripartite partition can be thought of as taking the
 THE ANALYSIS OF BIODIVERSITY EXPERIMENTS: FROM PATTERN TOWARD MECHANISM 97

original two-way split into complementarity and individual species (Fox 2006). The assumption of a
selection effects from Loreau and Hector (2001) and ‘summed’ ecosystem function covers primary pro-
performing a further split by dividing the selection ductivity and many other functions, but does not
effect into the dominance effect and a trait-depen- cover many others (see Fox and Harpole 2008). The
dent complementarity effect (SE ¼ DE þ TDCE). Price equation partition divides the difference in
Species with particular traits (monoculture yields) total function between two sites, DT, into three
can do better than expected in mixtures either at the additive components. The species richness effect
expense of other species (pure competitive (SRE) is that part of DT attributable to random loss
replacement as quantified by the dominance effect), of species richness, independent of which species
or not at the expense of other species (trait-depen- were lost. The species composition effect (SCE) is
dent complementarity effect). that part of DT attributable to non-random loss of
species making higher- or lower-than-average con-
tributions to total ecosystem function. The context
7.2.4 Applying the Price equation
dependence effect (CDE) is that part of DT attrib-
to biodiversity experiments
utable to between-site differences in the functional
Relative yield-based approaches, and the related contributions of the species present at both sites (i.e.
additive partitioning approaches, have primarily the functional contributions of these species are not
been used to aid the interpretation of substitutive constant, but rather are context-dependent).
experiments with plants or similar organisms. In The Price equation partition takes (and extends)
such experiments, interest centres on whether the the original Price equation developed in evolu-
functioning of a diverse mixture of species deviates tionary biology to classify and partition the causes
from that expected under the null model that intra- of evolutionary change in mean phenotype (Frank
and interspecific interactions are identical. How- 1995, 1997, Price 1970, 1995) and applies it to the
ever, in many circumstances, interest centres on effects of changes in biodiversity on ecosystem
comparing the functioning of different sites directly processes. In evolution, the mean phenotype of an
with one another, rather than on comparing each to offspring population can differ from that of a
a null model. This may be because no appropriate parental population for two reasons: natural selec-
null model exists, because information to parame- tion (covariation between parental fitness and
trize a null model is lacking, or simply because the parental phenotype), and imperfect transmission
investigator wishes to consider all processes that (factors, such as environmental change, that cause
cause ecosystem function to vary among sites the phenotypes of offspring to deviate on average
rather than factoring out the effects of some pro- from those of their parents). In mathematical terms,
cesses by comparison to a null model. For instance, natural selection is analogous to the Species Com-
an investigator might be interested in how the position Effect. For instance, non-random death of
functioning of a site has changed since a historical (selection against) large-bodied individuals will
extinction event, or in explaining variation in reduce mean body size in the next generation,
function along a natural diversity gradient. The assuming body size is heritable and all else being
Price equation partition (Fox 2006, Fox and Harpole equal. Analogously, non-random extinction of high-
2008) was designed for such cases. functioning species will reduce mean function per
The Price equation partition classifies the species, and thus total function, all else being equal.
mechanisms that cause two sites (a ‘pre-loss’ site of Imperfect transmission is precisely analogous to the
higher species richness, and a ‘post-loss’ site of Context Dependence Effect. For instance, if all off-
lower species richness) to differ in ecosystem spring to have larger body sizes than their parents
function (see supplement). The Price equation par- then, all else being equal, mean offspring body size
tition assumes that the species at the post-loss will exceed mean parental body size. Analogously,
site comprise a nested subset of the species at the if all species remaining at the post-loss site
pre-loss site, and that total ecosystem function function at a higher level than they did at the pre-
comprises the sum of the separate contributions of loss site, mean function per species, and thus total
98 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

!
function loss, all else being equal, will be higher at X
s
y ¼ b0 þ bLR xLR þ bNLR xNLR þ bi xi þ bQ xQ
the post-loss site (while functioning is usually i
thought of as declining with species loss it could þ bM xM þ e
also increase).
where b0 is the intercept, bLR is the coefficient
7.2.5 Classical statistical analysis associated with linear richness (richness treated as a
of mechanisms continuous variable), bNLR is the coefficient associ-
ated with species richness treated as a categorical
7.2.5.1 Random partitions design and analysis variable, the bi 0 s are the coefficients associated
Bell et al. (2005b) introduced a direct approach to with the presence/absence of each species, bQ is the
the analysis that avoids calculating derived values coefficient associated with each partitioned species
(e.g. complementarity effects) which must then be pool, bM is the coefficient associated with each
statistically analyzed in a second stage. Their composition, and e is a normally distributed ran-
approach is a direct analysis of the primary data dom variable. One important feature of this method
using normal least squares and general linear of analysis is that, when it is used along with the
models. The Bell et al. approach includes several experiment design described above, the non-linear
notable features of both the design and analysis. richness and species identity terms are orthogonal
The design takes a full species pool, N, and forms (do not share sums-of-squares). Consequently, it is
a diversity gradient by dividing by integer factors possible to parse some of the explained variation
of N. For example, Bell et al. selected a pool of 72 into either variation due to species identity or to
study species (from 103 available species) so variation due to non-linear richness. Another
that their diversity gradient comprised the series 72 unique feature of the design is that the collective
(72/1), 36 (72/2), 24 (72/3), 18 (72/4), 12 (72/6), 9 effects of species interactions can be captured by the
(72/8), 8 (72/9), 6 (72/12), 4 (72/18), 3 (72/24), non-linear richness term (bNLR). This ‘deviation
2 (72/36), 1 (72/72). In other words, the species from linearity’ term provides an ensemble test for
pool was randomly divided in half, randomly all species interactions combined.
divided into thirds and so on. The resulting com-
munities were termed a ‘partition’ of the selected 7.2.5.2 The diversity–interactions statistical
species pool (to avoid confusion note the use the modelling approach
word in a difference sense to the additive parti- The diversity–interactions approach (Kirwan et al.
tioning equations described above). This approach 2007) is also a more direct application of classical
was then repeated using different random selec- statistical methods that has several similarities to
tions to produce different replicate partitions, that the analysis conducted by Bell et al. (2005b) (see
is replicate diversity gradients that divide up the http://www.diversity-model.com/). The approach
species pool in different ways (for example, two is based on a framework of statistical models whose
replicate gradients would divide the species pool coefficients reflect the effects of species identity and
into two different half-pools rather than using the species interactions. The initial community compo-
same selection of species). This approach ensures sitions are described by the abundance of each
that, within each replicate partition, each species is species as a proportion of total initial abundance
present once at every level of diversity (a species is (M). The species proportions (Pi) are either planned
present in one monoculture, in one two-species experimental proportions or the relative abun-
community and so on). dances of species measured early in the experiment.
The method fits a least-squares model to the The regression equations describe the ecosystem
data that includes terms for the species process response variable (y) as follows:
richness, the presence/absence (identity) of
each species, and the composition of the commu- X
s X
s
nity. The level of ecosystem functioning, y, is y¼ bi Pi þ aM þ dij Pi Pj þ e
i¼1 i; j¼1; i<j
modelled as:
 THE ANALYSIS OF BIODIVERSITY EXPERIMENTS: FROM PATTERN TOWARD MECHANISM 99

models can be fitted to data from such a design.

Here, bi (the identity effect of the ith species) is the
However, by including experimental communities
expected monoculture performance of the ith species,
that provide good coverage of the design space, such
a is the effect of overall initial abundance, dij is a
as communities dominated by one or a subset of
measure of the strength of interaction between species
species, we can test for more complex patterns of
i and j, and e is the residual term. The model is fitted
species interaction (Kirwan et al. 2007). Also, pre-
using standard regression techniques. The sign of an
diction of the diversity effect may be reliable over a
interaction coefficient dij indicates whether the inter-
wider range of communities in which all component
action between species i and j has a synergistic or
species are not equally represented.
antagonistic effect on ecosystem function. The total
contribution to ecosystem function of the interaction is
dijPiPj and also depends on the initial relative abun- 7.3 Discussion
dances of the two species. The response in a mixed
7.3.1 Pattern
community expected solely from monoculture per-
Ps
formance is y ¼ bi Pi . The net biodiversity effect in Meta-analysis of the results from the first decade of
i¼1
Ps research in this area clearly shows a positive rela-
model (7.1) is dij Pi Pj , the sum of all pairwise tionship between biodiversity and ecosystem func-
i;j¼1; i<j
tioning; a pattern which is consistent across trophic
interactions among species. This diversity effect
groups (producers, herbivores, detrivores, and
generalizes to a rich class of alternative models
predators) and present in both terrestrial and
based on alternative assumptions about the strength
marine ecosystems (Balvanera et al. 2006, Cardinale
of pairwise species interactions. For example, the
et al. 2006a, Worm et al. 2006). However, in terres-
strength of pairwise interactions may all be the same
trial ecosystems the relationship between biodiver-
(identical values of dij) leading to a diversity effect
Ps sity and ecosystem functioning is generally quickly
d Pi Pj that is related to evenness (Kirwan et al. saturating with increasing diversity (Cardinale et al.
i;j¼1; i<j
2006a) suggesting that the effect of random biodi-
2007). Alternatively, there may be clear patterns
versity loss on ecosystem functioning will be ini-
among the dij that reflect the traits of the species in
tially weak but accelerating (Hector et al. 1999).
the mixture (e.g. a functional group model that has a
common interaction coefficient for all pairwise
interactions between species from different func-
7.3.2 Transgressive overyielding
tional groups). Interactions may also involve more
than two species or more complex functions. Many The low frequency of transgressive overyielding in
of these alternative models are hierarchical to model the meta-analysis performed by Cardinale et al.
(7.1) or to the model with a single interaction coef- (2006a) led them to suggest that the general positive
ficient, which leads to straightforward comparisons relationship between biodiversity and productivity
of models to identify the most appropriate. For in their analysis was most likely due to sampling
example, a pair of nested models with and without effects. The logic is that if complementarity is
species interactions can be compared to test whether present it should increase the performance of the
the ecosystem process response is determined only mixed community above that of even the best sin-
by species identity effects or by identity effects and gle species. However, as we show below, there can
species interactions. The complexity to which we can be widespread complementarity without trans-
describe patterns of interaction, and the sensitivity gressive overyielding. In other words, lack of
to discriminate between alternative patterns, transgressive overyielding does not mean lack of
depend on the range and patterns of relative abun- complementarity. On the contrary, it has been
dances that were selected in the experimental shown using the classical Lotka–Volterra competi-
design. Many diversity–function experiments use tion model that stable coexistence can occur in
communities with varying species richness, but mixed communities via niche complementarity
equal relative abundances. Diversity–interaction without transgressive overyielding (Beckage and
100 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Gross 2006, Loreau 2004). This can be simply tions are often at greater risk of extinction) so that a
illustrated as follows. Consider two species that species which is not highly abundant in the original
differ in their productivities when grown alone so full community may be one of the species which is
that the first is more productive than the second. lost as diversity declines. In this example, it is not
Assume that these two species can stably coexist clear that the species with the highest-yielding
together through some form of resource partition- monoculture should be the benchmark for com-
ing (or equivalent form of niche differentiation). parison since it may not even be present in the later
Complementary resource use will act to increase depauperate community, let alone the dominant
the productivity of the two-species mixtures above species (Hector et al. 2002a). As we discuss below
the level that would be expected if the two species (see: negative selection effects), in biodiversity
were not complementary, that is if resource com- experiments it is often the case that the species that
petition were a zero-sum game. However, this dominate communities are not those that are most
effect will be countered by the reduction in pro- productive when grown alone (indeed they often
ductivity caused simply by the replacement in the have lower-than-average monoculture yields). In
mixture of some of the more productive species by these situations the case for taking the species with
individuals from the less productive species. the most productive monocultures as the bench-
Transgressive overyielding will only occur when mark for comparison is not clear. An alternative
the increase in productivity due to complementarity approach would be to take the monoculture value
is stronger than the reduction in productivity of the species that dominates mixtures instead
caused simply by the ‘dilution’ of the most pro- since, for example, this is the species that would be
ductive species by the introduction into the mixture expected to go extinct last based on population size
of individuals of less productive species. arguments (Hector et al. 2002a).
The comparison of the yields of a variety of
polycultures with particular monocultures selected
7.3.3 Overyielding and the additive
post hoc also raises several statistical issues that
partitioning methods
complicate the test (Schmid et al. 2008). Further-
more, it is not clear how to best define transgressive Additive partitioning methods allowed the first
overyielding in biodiversity experiments. The situ- attempts at identifying the relative importance of
ation in an agricultural setting is clearer: for a the different classes of mechanism underlying the
farmer the question is whether a mixture can patterns reviewed above (see also Schmid et al. this
overyield the most productive monoculture volume). Meta-analysis of plant biodiversity
(although even the agricultural reckoning is com- experiments reveals that almost all studies are
plicated by issues of monoculture and mixture driven by a combination of complementarity and
production and price stability of components over selection effects but that overall complementarity
time with varying climates and biotic challenges). effects are nearly twice as strong as selection effects
However, outside of agriculture the choice is less (Cardinale et al. 2007). However, even though
clear because, in principle, every monoculture pro- complementarity effects have a greater effect than
vides a potential benchmark for comparison (Hec- selection effects they are not strong enough to cause
tor et al. 2002a). The traditional agricultural test for mixtures to do significantly better than the best
overyielding is arguably the most natural test when monocultures in most cases, as discussed above.
the species with the highest monoculture yield Another feature revealed by the additive parti-
dominates the depauperate communities. However, tioning method is the unexpected frequency of
it is easy to imagine cases where traditional agri- negative selection effects (e.g. counter to the pre-
cultural overyielding is not the only natural choice. dictions of the original sampling effect hypothesis).
One example occurs when the species that is high- In the meta-analysis of additive partitioning results
est yielding in monoculture is not highly abundant from experiments with plants 44% of studies
in the mixtures. Abundance is often taken as showed negative selection effects. In other words,
inversely related to extinction risk (small popula- in nearly half of all experiments communities were
 THE ANALYSIS OF BIODIVERSITY EXPERIMENTS: FROM PATTERN TOWARD MECHANISM 101

Selection

Complementarity

200

400

600
Biodiversity effect

Figure 7.1 Box-and-whisker plot summary of the 44 studies with additive partitioning data reviewed in Cardinale et al. (2007). The box and whiskers
show quartiles of the distributions of the selection (above) and complementarity (below) effects. The heavy central bar is the median and the notches on the
boxes indicate an approximate P ¼ 0.05 test for the median values versus zero. Points show two positive outliers for the selection effect values.

not dominated by highly productive species but by trait-dependent complementarity effect, depending
species with a lower-than-average monoculture on whether species with ‘larger’ niches have high or
biomass (Fig. 7.1). By looking only at the outcome low monoculture biomasses.
of competition in mixtures plant ecologists have too The hypothesis that trait-dependent complemen-
often equated high productivity with competitive tarity effects arise from ‘nested niches’, while trait-
dominance. While this is often the case, there are independent complementarity effects arise from
many situations where less productive species are non-overlapping niches, could be tested experimen-
able to become dominant. The mechanisms by tally by manipulating the scope for niche differenti-
which they achieve this remain poorly understood ation. For instance, Dimitrakopoulos and Schmid
and could be addressed by future research. (2004) planted monocultures and mixtures of plants
The key innovation of the tripartite additive in various depths of soil, and found an increasing
partitioning method was the identification of the selection effect with increasing soil depth. The
trait-dependent complementarity effect. Ecolog- complementarity effect (equivalent to the trait-inde-
ically, a non-zero trait-independent complementar- pendent complementarity effect from Fox 2006)
ity effect occurs when the ecological mechanisms increased with soil depth so it is possible that the
that mediate the strength of interspecific interac- increase in the selection effect was due, at least in
tions relative to intraspecific interactions differen- part, to an increasingly strong trait-dependent com-
tially affect high-yielding species, so that plementarity effect in deeper soil. Increasing soil
monoculture biomass covaries with traits that allow depth might be expected to increase the trait-
species to overyield in mixture (Petchey 2004). Fox dependent complementarity effect if some species
(2005b) suggests that such covariation might reflect with low monoculture biomass can produce only
‘nested niches’ (also called ‘included niches’). In this shallow roots, while species with high monoculture
view, species with ‘larger’ niches benefit from being biomass can produce shallow and deep roots. Deep
planted in mixture, because their niches contain soil would allow species with high monoculture
those of species with ‘small’ niches with ‘room to biomass to access a resource pool unavailable to
spare’. However, species with ‘small’ niches expe- shallow-rooted species, allowing deep-rooted species
rience equal niche overlap whether planted in to attain high biomass in mixture, but not at the
monoculture or mixture. Therefore, species with expense of shallow-rooted species.
larger niches grow better in mixture than in To date, there have been few formal comparisons
monoculture, but not at the expense of species with of the bi- and tripartite versions of the additive
small niches. This leads to a positive or negative partitioning method. In other words, there have
102 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

been few formal assessments of the contribution The Price equation partition requires knowledge of
made by the trait-dependent complementarity the functional contributions of individual species,
effect. Our published (Fox 2005b) and unpublished and retains the information about which species
results to date suggest that trait-dependent com- were lost. Indeed, the reason for assuming that the
plementarity often makes a relatively minor con- less diverse site comprises a strict subset of the
tribution. One interpretation of the typically small species in the more diverse site is so that infor-
magnitude of the trait-dependent complementarity mation about which species were lost can be
effect is that niches are not usually ‘nested’. That is, retained in a useful fashion (see Appendix B in Fox
the ecological mechanisms that mediate the and Harpole (2008) and our supplementary mate-
strength of interspecific interactions relative to rial). By retaining this information, the Price
intraspecific interactions typically do not differen- equation partition defines terms (SRE, SCE, and
tially affect high-yielding species. This hypothesis CDE) that have a straightforward mechanistic
could be tested by manipulating factors thought to interpretation independent of the details of study
mediate the ecological differentiation of species. It design. In situations where either the Price equa-
would also be interesting to look for the trait- tion partition or classical statistical approaches can
dependent complementarity effect in circumstances be applied, the investigator should carefully con-
in which it might be expected to be large (e.g. to sider the question of interest in order to select the
examine the functioning of mixtures of generalist most useful approach.
and specialist consumers).
As a general procedure we recommend analysts
7.3.5 The diversity–interaction statistical
compare these related overyielding and partition-
modelling approaches
ing approaches and, all else being equal, select the
simplest one that describes the data well. For One advantage of the application of these classical
example, presenting the tripartite method will be statistical methods to biodiversity experiments is
essential when trait-dependent complementarity that they avoid calculation of derived values (com-
plays an appreciable role but presenting the selec- plementarity effects and so on) that must then be
tion and complementarity effect may otherwise analyzed in a second stage. Furthermore, the meth-
suffice (in the limit, when trait-dependent comple- ods do not require monocultures (as with additive
mentarity effects are zero the dominance and partitioning), nor a full mixture (as in the Price
selection effects are mathematically equivalent). In equation), nor individual species contributions to the
other cases, near equal monoculture biomasses functioning of mixtures. Ideally a simplex design
make the selection effect covariance term trivial and assures that species are grown in different combi-
relative yield totals or deviations from expected nations and at different relative abundances but
values (Loreau 1998b) provide a simpler alternative species may be simply present (100 per cent) or
to additive partitioning (e.g. Vojtech et al. 2008). absent (0 per cent). When species are simply present
or absent the analysis of Bell et al. (2005b) can be
seen as a special case of the approach of Kirwan et al.
7.3.4 The Price equation
(2007). So, while the additive partitioning and Price
The Price equation partition is a natural approach equation approaches have mainly been applied to
when interest centres on the effects of species loss aboveground biomass production in plants these
from an initially diverse community, and the eco- classical statistical approaches should be applicable
system function of interest comprises the summed to any ecosystem function (e.g. Sheehan et al. 2006).
contributions of individual species. The other One advantage of classical statistical approaches is
major approach for comparing observed ecosys- that they do not require knowledge of the functional
tem function among sites is classical statistics (see contributions of individual species, and some clas-
Section 7.2.5). The Price equation partition and sical statistical approaches also omit information
classical statistics can be viewed as trading off about which species are absent from which sites. By
retention of information vs general applicability. omitting this information, classical statistics gains
 THE ANALYSIS OF BIODIVERSITY EXPERIMENTS: FROM PATTERN TOWARD MECHANISM 103

Table 7.1 Overview of when the methods reviewed in this chapter can be applied depending on the information collected (whether or not individual
species contributions to ecosystem processes can or has been measured) and type of experimental design (whether the relative abundance of species in
communities is known or simply their initial presence or absence; and whether species mixtures and monocultures are all nested subsets of a single high-
diversity community.

Information/Design Transgressive Random Diversity Relative yields Price

overyielding partitions interactions and additive equation partition
partitioning

No individual species contributions H H

Species presence/absence
No individual species contributions H H H
Species relative abundance
Individual species contributions H H H H
Individual species contributions Nested communities H H H H H

more general applicability, for instance to ecosystem the underlying mechanisms. Wider application of
functions that do not comprise the summed con- the methods described here should help resolve the
tributions of individual species, and to sites that do debate over mechanism that has continued largely
not comprise nested subsets of species. The general due to the failure of many studies to address the
applicability of classical statistics allows a greater underlying biological processes in an informative
range of cross-study comparisons (Balvanera et al. way (Cardinale 2006a, 2007). We finish with some
2006), although this generality comes with the risk of words of warning and suggestions for future work.
allowing statistically valid comparisons whose sci- Few, if any, of the methods reviewed here have
entific interpretation is obscure (Fox and Harpole been comprehensively explored. By that, we mean
2008). One cost of omitting information is that the their behaviour has not been investigated with
interpretation of the terms of a fitted statistical extensive simulation studies. This is a clear need for
model will necessarily depend on the details of the future work. Furthermore, most studies to date
model and the study design. For instance, effects of have tended to select one method and apply it in
species richness found by studies with different isolation. On the one hand, it is good that analyses
designs will have differing interpretations because of should focus on the most appropriate method at the
the other terms included in the respective statistical design stage. On the other hand, we are at a stage
models. A final limitation of the classical statistical where it would also be interesting to run the dif-
approach is that it cannot identify biological mech- ferent methods on the same dataset and to compare
anism directly, but its ability to identify strong pat- and contrast the results. In this way we can see
terns among species interactions should direct the where the different methods agree or disagree and
focus of more detailed explanatory research. demonstrate the advantages of one method over
another in terms of what they reveal about the
underlying biology. These approaches also need to
7.4 Conclusions and recommendations
be extended, or alternatives invented, that can deal
Our main conclusion is that the range of techniques with mechanism in multitrophic biodiversity
developed for the analysis of mechanisms in biodi- experiments.
versity experiments is now broad enough that we Finally, while our review emphasizes the ways
judge that some investigation of mechanisms should in which analytical methods have tried to move
be possible for all studies published to date that closer to biological mechanisms, none of the
examine effects of diversity within a single trophic methods described here measures the processes
level (plant biodiversity experiments for example; involved. Ideally the analyses described here will
Table 7.1). This should enable a move from purely be supplemented by experimental approaches
phenomenological studies to those that also address that directly quantify the processes involved in
104 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

species interactions and which are not applied resources. Only then will we be able to ask how
post hoc but are specified at the experimental well derived measures, like the biodiversity effects
design stage. These could include direct measures from the additive partitioning analyses and
of natural enemy attack in monocultures and the statistical interactions from classical approa-
mixtures for example, or the use of isotope meth- ches, map onto biological interactions in diverse
ods that can identify stocks and flows of communities.
 CHAPTER 8

Towards a food web perspective on

biodiversity and ecosystem
functioning
Bradley Cardinale, Emmett Duffy, Diane Srivastava, Michel Loreau,
Matt Thomas, and Mark Emmerson

8.1 Introduction
that they exert a disproportionate influence over
One of the most common questions asked by food web dynamics. This idea has fueled much
researchers across a variety of scientific disciplines is debate over the prevalence of omnivory in food
‘How does the number of nodes connected together webs (Polis and Strong 1996, Thompson et al. 2007,
into a network influence the efficiency and reliability Yodzis 1984) and whether the increased number of
of that network?’. While social scientists and epide- feeding links that result from omnivory increases or
miologists might think of ‘nodes’ and ‘connections’ decreases the stability of energy flow through a
as people interacting within a social network, com- food web (McCann et al. 1998, MacArthur 1955).
puter scientists, neurologists, and civil engineers Identifying species that represent influential nodes
would instead think of servers connected together in has also been one of the primary goals in the search
a world-wide web, synapses connecting neurons in for ‘ecosystem engineers’ (Jones et al. 1994), ‘key-
the brain, or hubs connecting to other hubs in a stone species’ (Paine 1966, Power et al. 1996) or
transportation network or telecommunications grid other types of ‘strong interactors’ (Wootton and
(Albert and Barabasi 2002, Newman 2003). Regard- Emmerson 2005) that might have cascading effects
less of the particular study system, all of these on the diversity and biomass of species at a variety
individuals ask similar questions about how the of different trophic levels (Paine 1966, Carpenter
number of nodes and connections among nodes et al. 1987, Elser et al. 1988).
influence the efficiency and reliability by which In the 1990s, ecologists began to pursue a slightly
information, disease, energy, or matter is transmitted different perspective on food webs. This perspec-
throughout that network. tive focused not on the cascading impacts of indi-
Within the field of ecology, one of the oldest and vidual species, but rather on how the number of
most fundamental questions asked by researchers is species that comprise any single trophic level might
‘How does the number of species interacting within control fluxes of energy and matter. Research in this
a food web influence the efficiency and reliability area was generally referred to as Biodiversity effects
by which energy and matter are transmitted on Ecosystem Functioning (BEF for short), and was
through that web?’. Research on this topic can be often justified on grounds that (1) loss of biological
broadly divided into two foci. Historically, much diversity ranks among the most pronounced chan-
attention in ecology has focused on identifying ges to the global environment (Sala et al. 2000,
those taxa that are the most influential nodes in a Pimm et al. 1995), and (2) reductions in diversity,
food web. For many years, it has been thought that and corresponding changes in species composition,
some subset of species might represent ‘hubs’ of may alter fluxes of energy and matter that underlie
interactions and/or exhibit such strong interactions important services that ecosystems provide to

105
106 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

(a) 25 100 (b)

Number species

20 80

% Studies
15 60

10 40

5 20

0 0
1 2 3 4 5 6
Trophic level

Figure 8.1 (a) Summary of the biological complexity of biodiversity-ecosystem functioning (BEF) studies performed to date. On the x-axis is the
number of trophic levels included in different experiments. On the left-hand y-axis (plotted as grey bars) is the mean number of species per trophic
level. On the right hand y-axis (plotted as triangles) is the percentage of studies that have included 1, 2, or more trophic levels. Note that 93 per cent
of BEF experiments have focused on a single trophic level composed of a mean seven species. (b) An example of the complexity of a real, yet still relatively
simple natural food web in a salt marsh (from Lafferety et al. 2007). Note that within this system there are dozens of species (nodes) and hundreds of feeding
links (lines connecting nodes) among plants, herbivores, predators and parasites that span six or more trophic levels. Figure reproduced with permission
from K. Lafferty. See Plate 4.

humanity (e.g. production of food, pest/disease simplifications are justified, or alternatively, whether
control, water purification, etc. Daily 1997, Chapin et they have led ecologists to potentially erroneous
al. 1998). While the value of BEF research for conser- conclusions. However, what is clear is that a large
vation biology and management has been questioned body of research in ecology has shown that interac-
by some (Schwartz et al. 2000, Srivastava and Vellend tions of species across trophic levels can have cas-
2005), there is a more fundamental reason for the cading impacts that influence the diversity and
recent prominence of this topic. BEF is one of the few biomass of organisms at numerous levels in a food
research topics in ecology that examines how bio- web. At the very least, this suggests that the past focus
logical variation per se acts as an independent variable of BEF on diversity within single trophic levels may
to regulate key community and ecosystem-level pro- be insufficient to quantitatively predict, and perhaps
cesses (Naeem 2002b). Understanding the ecological even qualitatively reflect, the ecological consequences
consequences of variation among species has shown of diversity loss.
much potential to complement our historical focus on In this chapter, we continue with the development
the ecological impacts of highly influential species. of an idea that originated with other authors who
Although the BEF paradigm has evolved consid- have argued that, in order to understand how
erably over the past 15–20 years and been increasingly extinction alters the functioning of whole ecosys-
applied to a variety of organisms and ecosystems, tems, ecologists will likely need to merge modern
studies have continued to focus mostly on simplified paradigms of BEF with much more classic ideas in
‘model’ communities. In fact, the typical experiment food web ecology that consider not only the func-
has manipulated an average of just seven species in an tional role of diversity within trophic levels, but the
average of just one trophic group (Fig. 8.1(a)). Such interactions of species across trophic levels (Duffy
minimal levels of complexity are far from the realities et al. 2007, Bruno and Cardinale 2008, Petchey et al.
of natural food webs, where, even for some of the 2004a). Our chapter is organized as follows. In Sec-
simplest communities, species interact within webs tion 8.2 we briefly review five hypotheses about how
composed of hundreds of species spanning many fluxes of energy and matter through a food web
trophic levels (Lafferty et al. 2006, Polis 1991, Martinez might depend on the diversity of species comprising
1992). At present, it is unclear whether such over- a web. Those hypotheses are divided into those that
 TOWARDS A FOOD WEB PERSPECTIVE ON BIODIVERSITY AND ECOSYSTEM FUNCTIONING 107

contrast diversity effects within different trophic impacts on processes that are disproportionate to
levels versus those that focus on diversity effects their abundance or biomass. Duffy’s (2002) paper
across trophic levels. In Section 8.3 we outline the was one of the first to call for a merger of BEF and
empirical support for or against these hypotheses, food-web theory, and the hypotheses put forth in
emphasizing that most are still unresolved and in that paper were useful, in part, because they
need of testing. In the final Section 8.4, we outline represented an alternative to those posed by a
just a few of the areas of research that we believe number of other authors. For example, some have
will be fruitful as ecologists move towards an inte- argued that extinction at higher trophic levels
gration of BEF into food-web ecology. may, in fact, have less impact on ecological pro-
cesses than extinction at lower trophic levels.
These arguments have usually been based on the
8.2 Five early hypotheses about idea that animals are more generalized in their use
multi-trophic biodiversity and ecosystem of resources than historically appreciated, either
function because the extent of omnivory and intra-guild
predation has been underestimated (Rosenheim et
8.2.1 Diversity effects within trophic levels al. 1995, Holt and Polis 1997, Polis and Holt 1992),
8.2.1.1 Top-down effects of diversity grow increasingly or because animals can ‘switch’ among different
strong at higher trophic levels prey species by moving across habitats (Polis et al.
1997, McCann et al. 2005). Resource generalization
has been proposed to dampen the effects of con-
C1 Cn
sumer diversity on prey populations (Finke and
+++ Denno 2005, Snyder and Ives 2003).

H1 Hn 8.2.1.2 Increasing diversity of a resource reduces

the strength of top-down control by consumers
++

P1 Pn
C
+
–
N
R1 Rn

Early hypotheses proposed that species extinction

from higher trophic levels was likely to have greater The majority of BEF studies performed to date have
impacts on the functioning of ecosystems than taken a ‘top-down’ perspective, meaning that they
extinction from lower trophic levels (Table 8.1). have examined how diversity within a given
Duffy (2002) argued that three characteristics trophic level impacts the fraction of resources con-
potentially make ecological processes more sensitive sumed, and production of biomass, by that focal
to extinction by consumers than plants: (1) because trophic level. In contrast, diversity may also have
species at higher trophic levels have lower popula- ‘bottom-up’ effects on the dynamics of food webs,
tion sizes and are under stronger anthropogenic meaning that the diversity of resources may influ-
pressure than most wild plants, higher trophic levels ence how efficiently those resources are consumed
face greater risks of extinction and higher rates of and converted into biomass by higher trophic levels
species loss; (2) consumer assemblages have lower (Table 8.1). At least three hypotheses have been
overall richness and higher degrees of resource proposed to explain how resource diversity might
specialization, leading to less ‘functional redun- influence trophic dynamics: (2.1) the variance in
dancy’ and limited potential for surviving species to edibility hypothesis argues that a more diverse prey
compensate for processes performed by lost coun- assemblage is more likely to contain at least one
terparts; and (3) unlike plants, consumers often have species that is resistant to consumers (Leibold 1989,
Table 8.1 Five early hypotheses about multi-trophic BEF. What do the data say?

Section Hypothesis Key reference(s) Section Balance of evidence Certainty Key references

8.2.1 Diversity effects within trophic levels

8.2.1.1 Top-down effects of diversity grow increasingly Duffy (2002) 8.3.1.1 The balance of evidence is not consistent with this hypothesis. Medium Balvanera et al. (2006),
strong at higher trophic levels. Recent meta-analyses have found no difference in the to high Cardinale et al. (2006a,
direction or magnitude of diversity effects for groups of 2007)
producers, herbivores, detritivores, or predators. In fact,
there tends to be considerable generality such that decreases
in species richness decrease the efficiency of resource
capture and the amount of biomass produced by any given
trophic group.
8.2.1.2 Increasing diversity of resources reduces the Leibold (1989), 8.3.1.2 The balance of evidence is consistent with this hypothesis. Low to Andow (1991), Hillebrand
strength of top-down control by consumers. Duffy (2002), Summaries suggest that consumption of lower by higher medium and Cardinale (2004)
Ostfeld and trophic levels is reduced when a resource base is more
LoGiudice diverse. Note, however, that most of the available data
(2003), Root comes from studies that have not directly manipulated the
(1973) richness of resources. Several controlled experiments have
provided counter-examples, so the generality of this
hypothesis remains unclear.
8.2.2 Diversity effects across trophic levels
8.2.2.1 Top-down effects of consumer diversity oppose Holt & Loreau 8.3.2.2 Recent meta-analyses suggest that the top-down effects of Low Srivastava et al. (2009)
the bottom-up effects of resource diversity. (2002), Thébault consumer diversity are qualitatively different than the
and Loreau bottom-up effects of resource diversity. However, these
(2003, 2005) effects have not been opposing as suggested by this
hypothesis. Note, however, that few studies have
simultaneously manipulated the richness of species at
adjacent trophic levels, so conclusions are tentative.
8.2.2.2 Diversity effects on biomass production and Holt and Loreau 8.3.2.1 The balance of evidence does not support this hypothesis. Of the Low Mulder et al. (1999), Duffy et
resource capture by a given trophic level are (2002), Thébault few experiments that have manipulated species richness in the al. (2005), Wodjak (2005),
reduced in the presence of a higher trophic and Loreau presence vs. absence of a higher trophic level, results are and this chapter
level. (2003) decidedly mixed. Analyses presented in this chapter further
show no evidence that the effects of plant diversity on plant
biomass differ for experiments performed in the presence vs.
absence of herbivores.
8.2.2.3 Trophic cascades are weaker in diverse Strong (1992) 8.3.2.3 Experiments and data summaries to date have been equivocal None Schmitz et al. (2000), Borer et
communities. and contradictory. At present, there is no clear reason to al. (2005), Cardinale et al.
accept or reject this hypothesis. (2003, 2006b), Wilby et al.
(2005), Snyder et al. (2006),
Finke and Denno (2005),
Byrnes et al. (2006)
 TOWARDS A FOOD WEB PERSPECTIVE ON BIODIVERSITY AND ECOSYSTEM FUNCTIONING 109

Duffy 2002); (2.2) the dilution hypothesis (Ostfeld and tially more complex. While predator diversity
LoGiudice 2003), which has also been called the generally decreases prey biomass, prey diversity
resource concentration hypothesis in the agro-ecology can increase or decrease biomass depending on
literature (Root 1973), suggests that specialist con- how different life-history trade-offs influence the
sumers become less efficient at finding and attacking coexistence of prey.
their resource in a diverse prey assemblage; and (2.3)
the balanced diet hypothesis suggests that a more
diverse prey assemblage provides a more complete 8.2.2.2 Diversity effects on biomass production
nutrition and, as a result, leads to higher consumer and resource capture by any focal trophic level
biomass (DeMott 1998). While hypotheses (1) and (2) are reduced in the presence of higher trophic levels
predict that trophic efficiency will decrease as the
diversity of resources increases, (2.3) predicts the
C⬘
opposite.

C1 Cn
8.2.2 Diversity effects across trophic levels
+ (0)
8.2.2.1 Top-down effects of consumer diversity oppose
R
the bottom-up effects of resource diversity

In their recent review, Duffy et al. (2007) used the

C1 Cn
terms ‘horizontal’ and ‘vertical’ diversity to distin-
– + guish between the richness of species within a
trophic level and the richness of trophic levels that
R1 Rn
comprise a food web. They argued that one of the
primary limitations in merging BEF with food-web
An important, but still unresolved issue is whe- theory is knowing how the impacts of divesity
ther the overall impacts of diversity loss at within trophic levels depend on the length of food
adjacent levels are opposing or reinforcing, chains (i.e. how horizontal and vertical diversity
antagonistic or synergistic. Hypotheses (2.1) and interact). The first step in overcoming this limitation
(2.2) suggest that consumer diversity tends to is to ask how the diversity effects of any single
enhance the flux of resources from lower to trophic level are altered by the presence or absence
higher trophic levels, whereas resource diversity of the next highest trophic level. Holt and Loreau
tends to reduce these fluxes. Collectively, these (2002) used simple consumer–resource models to
two hypotheses lead to a third hypothesis: that argue that the effects of plant diversity on nutrient
extinction of species from adjacent trophic levels uptake and plant biomass production are reduced
will have opposing impacts on the flux of energy in the presence of herbivores. This occurs because
and matter through a food web (Table 8.1). This herbivory selects for dominance by poor plant
prediction has received some theoretical support competitors that are also the most tolerant to
from mathematical models showing that simulta- consumption by herbivores. Subsequent models by
neous changes in diversity from consumers and Thébault and Loreau (2003) also suggested that
their resource leads to countervailing effects on addition of higher trophic levels might qualita-
total resource use and biomass production (The- tively alter diversity–production relationships at
bault and Loreau 2003, Thebault and Loreau 2005, lower levels; however, the direction of these
Holt and Loreau 2002). Fox (2004b) provided a impacts depends on both the nature of trade-offs
counter example in which he used Lotka–Volterra between a plant’s competitive ability and ability to
models to show that the joint response of prey resist herbivory, and on the degree of consumer
biomass to prey and predator diversity is poten- specialization.
110 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

8.2.2.3 Trophic cascades are weaker in effects are stronger at higher trophic levels.
diverse communities Balvanera et al. (2006) reviewed 103 studies in
which they could examine 400þ correlation coef-
ficients relating species richness to a variety of
C1⬘ Cn⬘
ecological processes. They found no evidence for
– differential correlations between diversity and any
– of the response variables at various trophic levels.
C1 Cn
Similarly, Cardinale et al. (2006a) collated data
from 111 experiments that have manipulated spe-
cies richness and examined how this aspect of
R
diversity impacts the capture of resources and
production of biomass. Their analyses compared
In his seminal critique of the empirical evidence for four trophic groups: (1) microalgal, macroalgal, or
trophic cascades, Strong (1992) argued that cas- herbaceous plants assimilating nutrients or water,
cades are ‘a relatively unusual sort of food web (2) protozoan or metazoan herbivores consuming
mechanics . . . over the full range of ecological com- live algal or herbaceous plant tissue, (3) protozoan
munities, evidence is that these cascades are or metazoan predators consuming live prey, and
restricted to fairly low-diversity places where great (4) bacterial, fungal or metazoan detritivores con-
influence can issue from one or a few species.’ He suming dead organic matter. They showed that, on
went on to suggest that trophic cascades are ‘all average, experimental reduction of species rich-
wet,’ meaning they occur primarily in aquatic eco- ness decreases the standing stock abundance or
systems where communities are characterized by biomass of the focal trophic group, resulting in less
linear, low-diversity food chains. In contrast, he complete resource use by that group (Fig. 8.2).
argued that terrestrial food webs are more reticu- However, the standing stock of, and resource
late and ‘consumption is so differentiated in spe- depletion by, the most diverse polycultures were
ciose systems that its overall effects are buffered.’ indistinguishable from those of species that per-
The idea that diversity modifies the strength of formed best in monoculture. Importantly, the
trophic cascades can be broken down into at least authors could not detect any statistical difference
two distinct hypotheses: (1) increasing the diversity in the magnitude of diversity effects among the
of species comprising secondary consumers C’ four trophic groups.
tends to decrease the strength of indirect effects on Collectively, these meta-analyses suggest there
a basal resource R, and (2) increasing diversity of is considerable generality in the way that the
primary consumers C tends to decrease the indirect diversity of species impact resource capture and
effects of C’ on R. This latter hypothesis is very biomass production in food webs. The fact that
much an extension of hypotheses (2.1) and (2.2), as Cardinale (2006a) and Balvanera (2006) both found
all of these rely on the assumption that an that the BEF relationships did not change dra-
increasing diversity of resources tends to reduce the matically across trophic levels could imply that, if
top-down impacts of consumers on food-web niche complementarity is the main mechanism
dynamics (Table 8.1). driving these patterns, then the degree of niche
complementarity could be similar across trophic
groups. Identifying whether the mechanisms that
8.3 What do the data say? dictate BEF relationships are the same across dif-
ferent levels of biological organization is a key
8.3.1 Diversity effects within trophic levels
next step in BEF research (a point we return to in
8.3.1.1 Are diversity effects stronger at higher Section 8.4.1). Although studies to date show
trophic levels? (Hypothesis 2.1.1) considerable generality in diversity effects across
Empirical evidence gathered to date does not trophic levels, we should emphasize that there still
appear to support the hypothesis that diversity tend to be fewer absolute numbers of species at
 TOWARDS A FOOD WEB PERSPECTIVE ON BIODIVERSITY AND ECOSYSTEM FUNCTIONING 111

Producers Herbivores Predators Detritivores Producers Herbivores Predators Detritivores

3

2 4
LRmean (SST)

LRmax (SST)
1
2
0
0
–1

–2 35, 15, 3 4, 9, 1 4, 1, 1 3, 3, 0 –2
7, 21, 11 3, 11, 0 3, 0, 3 1, 2, 0
8
4 1
LRmean (RD)

LRmax (RD)
2 0

–1
0
–2
–2
5, 9, 0 0, 7, 1 1, 18, 0 16, 13, 0 1, 10, 1 1, 9, 0 0, 16, 0 3, 18, 0

Figure 8.2 Summary of the results of experiments that have manipulated the richness of species in four trophic groups t (producers, herbivores,
predators, and detritivores), and examined how richness impacts the standing stock abundance or biomass of t (SST – top graphs) or the fraction of
resources depleted by t (RD – bottom graphs). The y-axes in all graphs give the diversity ‘effect size’, measured using two log ratios. LRmean (left graphs)
compares SST and RD in the most diverse polyculture used in a study to the average of all monocultures. LRmax (right graphs) compares SST and RD
from the most diverse polyculture used in a study to the species having the highest values of SST or RD in monoculture. Each data point is the mean effect size
for all replicates in an experiment ± 95 per cent CI. Dashed horizontal grey lines give the 95 per cent CI for all experiments combined based on results
from a mixed model ANOVA. Numbers below each figure are the number of studies that have shown significantly positive effects of diversity, no effect,
or negative effects of diversity. Data are from Cardinale et al. (2006a).

higher trophic levels, and that these species tend to resource in a diverse prey assemblage, best
be disproportionately prone to extinction (a point accounted for the observed patterns. A summary of
we return to in Section 8.4.2). Thus, it is still rea- aquatic studies by Hillebrand and Cardinale (2004)
sonable to hypothesize that food webs can tolerate tallied results from 172 experimental manipulations
fewer extinctions at higher trophic levels before of herbivores and showed that consumption of
ecosystem functioning is altered. algal biomass generally declined with increasing
algal species richness. Although these patterns are
8.3.1.2 Does resource/prey diversity weaken consistent with hypothesis (2.2), some caution is
the strength of top-down control? (Hypothesis 2.1.2) warranted when interpreting these summaries,
Empirical evidence gathered thus far is mostly since the studies reviewed did not manipulate
consistent with the hypothesis that increasing prey species diversity directly, and many potentially
diversity tends to reduce the impacts of consumers confounding factors were not controlled for. This
on prey. Andow (1991) tallied the results of 200þ caveat is particularly important when considering
studies of herbivorous arthropods and found that the mixed results from the limited number of
more than half of the herbivore species had lower experiments that have manipulated resource
population sizes on plant polycultures as opposed diversity directly. Several studies do provide evi-
to monocultures. He argued that the resource con- dence consistent with the variance-in-edibility
centration hypothesis, in which specialist con- hypothesis (Steiner 2001, Duffy et al. 2005), or for the
sumers have a more difficult time finding their dilution hypothesis (Keesing et al. 2006, Wilsey and
112 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Aquatic Terrestrail Figure 8.3 A summary of the impact of plant species richness on the
2 production of plant biomass when herbivores are present or absent in
experimental units. Data were taken from the summaries of Cardinale et al.
Effect of plant species richness

(2006, 2007). The log ratio of plant biomass in the most diverse polyculture
on plant biomass, In(Bp/Bm)

Bp to biomass in the average monoculture Bm was analyzed using a mixed

1
model ANOVA with herbivores (y/n), ecosystem (aquatic vs. terrestrial), and
their two-way interaction included as fixed effects, experiment accounted for
as a random effect, and observations weighted by the inverse of their
0 variance. Analyses indicate that the impacts of plant diversity on plant
production do not differ when herbivores are absent vs. present (F ¼ 0.01, P
90 15 ¼ 0.92), and that this conclusion is consistent among ecosystems (F ¼
9
–1 0.07, P ¼ 0.80 for interaction). These data and analyses should not be
29 taken as conclusive evidence that herbivores do not impact plant
diversity–biomass relationships since the studies summarized here differ in
–2 many ways that cannot be explicitly accounted for. However, these data can
serve as a null hypothesis for experiments that explicitly manipulate plant
Yes No Yes No
diversity in the presence versus absence of higher trophic levels.
Herbivores present?

Polley 2002, Otway et al. 2005) where increasing bottom-up effects of resource (detrital) diversity on
diversity of resources leads to reduced consumption consumption of dead organic matter. Their meta-
by higher trophic levels. Other studies provide analysis indicated that reductions in detritivore
support for the balanced diet hypothesis, showing diversity generally led to reductions in rates of
that mixed diets of primary producers tend to decomposition, but changes in the diversity of
enhance herbivore growth and biomass accumula- detrital resources led to no detectable change in
tion (Pfisterer et al. 2003, DeMott 1998). Thus, decomposition. The implication is that consumer,
although the balance of evidence appears consistent but not resource diversity, impacts consumption
with hypothesis (2.2), these conclusions should be and energy flow in ‘brown’ food webs (detritus-
considered tentative. consumer). However, an important point to keep in
mind is that the resources studied by Srivastava
et al. (2009) are ‘dead,’ meaning they are non-living
8.3.2 Diversity effects across trophic levels
resources that have no potential to show dynamic
8.3.2.1 Do top-down effects of diversity differ coupling to their consumers. A number of mathe-
from bottom-up effects? (Hypothesis 2.2.1) matical models suggest that diversity–function
To date, studies that have simultaneously manipu- relationships could be qualitatively different when
lated the richness of species at adjacent trophic resources are ‘living’, such as in ‘green’ food webs
levels are rare (Fig. 8.1(a)), and it is difficult to draw (i.e. plant-based systems) where populations have
many general conclusions about the direction of the potential to respond to changes in the density of
top-down versus bottom-up effects of diversity in their consumers (Loreau 2001, Ives et al. 2005). The
food webs. However, a recent meta-analysis by potentially important contrast between systems that
Srivastava et al. (2009) suggests that hypothesis (2.1) have dynamic (living) vs. non-dynamic (non-living) is
is not supported in detrital systems. These authors an issue that we return to in Section 8.4.1. For now,
compiled the results of 90 experiments reported in suffice it to say that we do not know whether the
28 studies of detritivores to ask ‘Do changes in results of Srivastava et al. (2009) are specific to detrital
consumer (i.e. detritivore) diversity have the same systems, or whether they hold more generally.
effect on rates of resource consumption as changes
in resource (i.e. detrial) diversity?’. To address this 8.3.2.3 Are diversity effects at one trophic level
question, they compared the top-down effects of altered by higher levels? (Hypothesis 2.2.2.)
consumer (detritivore) diversity on the consump- Only a handful of experiments have manipulated
tion of dead organic matter (decomposition) to the the richness of species in a focal trophic level and
 TOWARDS A FOOD WEB PERSPECTIVE ON BIODIVERSITY AND ECOSYSTEM FUNCTIONING 113

then simultaneously manipulated the presence/ ecosystems found no evidence that variation in the
absence of a higher trophic level. Mulder et al. (1999) strength of cascades was related to the richness of
varied plant diversity in the presence and absence of predators, herbivores, or plants (Borer et al. 2005). In
insect herbivores in a grassland plant assemblage. In contrast, a limited number of experiments have
the absence of herbivores, plant biomass increased manipulated the diversity of predators at top trophic
with plant diversity, whereas when insects were levels and shown that diversity can indirectly alter
present, they fed heavily on species with interme- plant biomass by changing rates of herbivory. Cas-
diate biomass, weakening the impact of plant cading effects of predator diversity have been dem-
diversity and biomass. Conversely, in a seagrass onstrated in agricultural (Cardinale et al. 2003, Wilby
system, effects of herbivore richness on plant pro- et al. 2005, Snyder et al. 2006), salt marsh (Finke and
duction were stronger in the presence of a higher Denno 2005), and kelp forest systems (Byrnes et al.
trophic level (crabs) than in their absence (Duffy et al. 2006), and have been attributed to non-additive
2005), which presumably occurred because of tra- interactions (Cardinale et al. 2003, Cardinale et al.
deoffs between species abilities to compete for 2006b), omnivory (Bruno and O’Connor 2005), intra-
resources versus resist predators. In other experi- guild predation (Finke and Denno 2005), and chan-
ments, addition of a higher trophic level changed not ges in herbivore behavior (Finke and Denno 2005,
only the magnitude but also the sign of the Byrnes et al. 2006). Yet, the magnitude and direction
diversity–function relationship at the prey level (e.g. of predator richness impacts on plant biomass and
Hattenschwiler and Gasser 2005, Wojdak 2005). production have been inconsistent among studies
We have been able to further examine hypothesis (see Bruno and Cardinale 2008 for a review). Thus,
(2.2.2) by collating data from the meta-analyses of although predator richness frequently has cascading
Cardinale et al. (2006a, 2007) for studies that have impacts on food-web properties, it is difficult at this
manipulated the richness of primary producers. We point in time to predict whether these cascading
divided experiments into those that did versus did effects generally increase or decrease plant biomass.
not allow herbivores access to experimental plots Therefore, at present, there is no clear evidence that
or pots, and then compared how plant diversity can be used to accept or reject Strong’s (1992)
influenced plant biomass between the two types of hypothesis that trophic cascades are restricted to
studies. Although plant species richness generally low-diversity linear food chains.
increased the production of plant biomass, we found
no evidence that herbivores alter the magnitude of
plant diversity effects (Figure 8.3). This was true for 8.4 Where do we go from here?
studies performed in both aquatic as well as terrestrial
8.4.1 Detailing mechanisms: niche partitioning
ecosystems. Although these analyses are far from
and life-history tradeoffs
conclusive, when taken with the mixed results of
experiments they suggest that widespread support William Dillard, founder and Chairman of Dillard’s
for hypothesis (2.2.2) is presently lacking. department stores, once said that the three most
important factors for the success of a business are
8.3.2.4 Are trophic cascades weaker in ‘location, location, location.’ Similarly, we believe
diverse communities? (Hypothesis 2.2.3) that the three most important factors that will
Experiments and data summaries that have addres- determine the success of the BEF paradigm will be
sed hypothesis (2.2.3) to date have been equivocal our ability to identify mechanisms, mechanisms,
and contradictory. Schmitz et al. (2000) performed a mechanisms! Understanding the mechanisms that
meta-analysis of 14 terrestrial experiments that underlie diversity effects essentially requires that
manipulated higher predators and found evidence researchers return to several of ecology’s classic
that the cascading effects of predator removal on questions about how niche partitioning and life-
plant damage were weaker in systems that had history tradeoffs allow species to coexist. Chesson
higher herbivore diversity. A more comprehensive (2000) provided what is perhaps the most elegantly
analysis of trophic cascades measured in a variety of organized summary of the mechanisms that allow
114 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

d
SK
B=
1 + a(S – 1)

Frequency of utilization
a=0 w

Community
biomass, B
0<a<1
d

a=1
w
Species richness, S
Resource dimension

Figure 8.4 (a) Solutions to Lotka–Volterra competition equations showing how species richness affects community biomass production for differing
levels of interaction strength. Note there is a positive, but decelerating relationship between B and S for all 0 < a < 1. This is an inevitable consequence of
niche packing (insets) where the addition of species to a system with finite resource forces the average species to occupy a smaller fraction of resource
space. Thus, the more species there are, the less each species contributes to resource capture and biomass production, on average.

coexistence. He showed that, for a wide variety of systems (Loreau 2004, Tilman et al. 1997c, Ives et al.
mathematical models, coexistence is ultimately 2005, Cardinale et al. 2004). The discrete time
determined by the balance of two interacting forces, Lotka–Volterra models of competition serve as an
which he called equalizing and stabilizing. Equalizing example (Cardinale et al. 2004), where the biomass of
forces are those that minimize differences in the fit- any species i in a local community can be described as
ness of species, causing interspecific interactions to
2 0 13
have weaker influence over population dynamics. P
N

6 B bi ðtÞ þ a bj ðtÞC7
Hubbel’s (2001) neutral theory of biodiversity is the
6 B j6¼i C7
extreme case of an equalizing force where demo- bi ðt þ 1Þ ¼ bi ðtÞexp6ri B1  C7 ð8:1Þ
4 @ Ki A5
graphic parameters are assumed to be identical
among species such that interacting with another
species has the same per capita impact as interacting Ki is the equilibrium biomass of i in the absence of
with a congener. Equalizing mechanisms are not competitors, ri is the intrinsic rate of increase in
mathematically stable and cannot allow long-term biomass, and a is the ratio of inter- to intra-specific
coexistence. Rather, equalizing mechanisms only interaction. If species have similar carrying capaci-
serve to slow the inevitable outcome of species ties and symmetric interactions, then all species
interactions. Thus, long-term coexistence requires have the same biomass at equilibrium, b(1), and
some type of stabilizing force that involves niche for any local community
differentiation in space or time. Regardless of whe-
ther niche differentiation occurs through partitioning bð1Þ þ aðS  1ÞbðaÞ ¼ K ð8:2Þ
of limited resources, shared predators, or some other
dimension of a species niche, stabilizing forces all From this, the total biomass of the community is
share the feature that they reduce interspecific rela-
tive to intraspecific interactions, leading to a per SK
capita growth advantage of a species when rare. Bð1Þ ¼ ð8:3Þ
1 þ aðS  1Þ
The literature is ripe with models that examine
how reductions in interspecific relative to intra- For the extreme cases of a ¼ 1 or a ¼ 0, eq. 3
specific interactions regulate the impacts of species reduces to B ¼ K and B ¼ SK, respectively, which
diversity on the production of single trophic-level shows that community biomass is independent of,
 TOWARDS A FOOD WEB PERSPECTIVE ON BIODIVERSITY AND ECOSYSTEM FUNCTIONING 115

or a linear function of richness (Fig. 8.4). For all resist or recover from consumption, this can moderate
other scenarios where 0 < a < 1, community bio- coexistence among prey (Holt et al. 1994) and dictate
mass is a positive but decelerating function of whether prey biomass increases or decreases with
species richness. Importantly, the curvilinearity of diversity (Holt and Loreau 2002, Thebault and Loreau
this function has nothing to do with how ‘unique’ 2003). Similarly, the tradeoff between the degree of
or ‘redundant’ species are. Rather, the decelerating resource specialization and assimilation efficiency of
relationship is an inevitable consequence of pack- consumers has important implications for the BEF
ing more species into a finite niche axis. Even relationship. The diversity of consumers that pay no
when all species are specialists with a unique cost to generalism, i.e. that do not trade off their
niche, the contributions by any single species to ability to consume a wide diversity of resources
resource capture and biomass production must against their efficiency at consuming each of these
decline as a function of richness (i.e. b _ 1/S, Eqn resources, typically has a strong destabilizing effect
8.2), causing each increase in diversity to contrib- on both population- and ecosystem-level fluctuations,
ute smaller increments to resource capture and whereas species diversity has a stabilizing effect on
biomass. ecosystem-level fluctuations when consumers do
Equation (8.3) predicts a rather straightforward set have such tradeoffs (Thebault and Loreau 2005).
of relationships between species diversity and com- So are the consequences of extinction the same in
munity biomass for any trophic group that is sup- single versus multi-trophic systems? Theory pre-
ported by a non-dynamic resource (e.g. plants dicts that the answer entirely depends on the form
assimilating inorganic resources, detritivores feeding of tradeoffs that mediate the coexistence of both
on dead organic matter, etc.). One of the key questions consumers and their resources, and whether or not
as we extend BEF theory to multi-trophic systems is resources exhibit density dependent dynamics and
whether this same set of simple relationships holds overexploitation by consumers. What we need now
true for systems where the resources are themselves are innovative experiments that manipulate the
dynamic. Interestingly, several authors have ana- strength of consumer–resource interactions and/or
lyzed Lotka–Volterra models for both dynamic and the existence of tradeoffs that are presumed to
non-dynamic resources and found that the effects of underlie diversity effects in multi-trophic systems.
species diversity on community biomass are often Although such innovative experiments will no
qualitatively similar between one and two trophic- doubt be challenging, they have the potential to
level systems (Thebault and Loreau 2003, Thebault yield some of the most important new insights into
and Loreau 2006, Ives et al. 2005, Fox 2004b). There the functioning of food webs.
seems to be just two general instances where new
behaviors emerge in a multi-trophic system. The first
8.4.2 Realistic scenarios of extinction
occurs when dynamic resources, which have the
potential to be overexploited in a multi-trophic sys- It is well established that species extinction is a non-
tem, are brought to extinction by their consumers. random process. Throughout both geological and
Overexploitation or extinction of resources by a modern time, certain biological traits such as dis-
diverse group of generalist consumers can yield persal ability, generation time, body size, geo-
humped-shaped diversity–biomass relationships in graphic range, and local density have proven to be
both predators and prey, which is a BEF relationship correlated with extinction risk (McKinney 1997,
that is not found in single trophic-level systems Lawton and May 1995, Purvis et al. 2000a). Trophic
(Thebault and Loreau 2003, Thebault and Loreau position also appears to be correlated with extinc-
2006, Ives et al. 2005). Second, there are certain types of tion risk. In marine systems, extinction of fish spe-
life-history tradeoffs that can alter the shape and cies generally proceeds from the top of food webs
magnitude of a diversity–biomass relationship (The- downward (Pauly et al. 1998), which is partly due
bault and Loreau 2003, Thebault and Loreau 2006). to human preferences for large-bodied fish, and
For example, when resource species exhibit a tradeoff partly because such fish have low resilience due to
between their competitive abilities and their ability to late maturity and slow growth (Myers and Worm
116 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

1025

Size of study system (m2 or L)/mean organism size (g)

Sm
1022 < 1 generation > 1 generation

Cl
1019

1016
Bu
Spatial scale

1013

1010 Un
Tr

107 Mo
Wo
104

101

10–2

10–5
10–3 10–2 10–1 10–0 101 102 103 104 105 106
Time-scale
Duration of experiment (d)/mean generation time (d)

Figure 8.5 The spatial and temporal scale of biodiversity-ecosystem functioning experiments. The experimental duration (in days) and spatial scale
(in m2 or L) of experiments reviewed by Cardinale et al. (2006) were standardized to the mean generation time and body sizes of the focal organisms. Data
were divided into four trophic groups: Plants ¼ green circles, Herbivores ¼ blue triangles, Predators ¼ red squares, Detritivores ¼ brown diamonds.
The scale of each individual study is given by smaller symbols while the medians for each trophic group are shown as larger symbols. The box denoted by the
dashed line gives the 10th and 90th percentiles for the scale of all experiments. For comparative purposes we show the scale of several natural extinctions:
Wo ¼ wolves from Yellowstone National Park, USA; Mo ¼ Moa from New Zealand; Tr ¼ Trout from Lake Superior, USA; Un ¼ Unionid mussels from
the lower Mississippi River, USA; Bu ¼ Various species of butterflies in Europe; Cl ¼ Loss of certain cladoceran zooplankton from Lake Superior, USA;
Sm ¼ Global eradication of the small pox virus. See Plate 5.

2005). In terrestrial systems, studies similarly report random extinctions). Predators may have high
higher extinction probabilities for predators than functional importance in food webs, first because of
their prey (Kruess and Tscharntke 1994, Didham the strength of top-down processes in food webs
et al. 1998b). (Duffy 2003), and second because predators may
Non-random patterns of extinction can affect have traits that are additionally correlated with high
diversity–function relationships in at least two ways: functional impact (e.g. body size – Solan et al. 2004).
via the functional traits lost, and via changes in Following extinction of a species, diversity–function
community interactions. Initially, ecosystem function relationships are additionally influenced by the res-
may be most affected by the functional traits of the ponse of the surviving species to loss of a community
species that preferentially go extinct (Srivastava and member. Gross and Cardinale (2005) showed that
Vellend 2005, Lavorel and Garnier 2002). Positive the effect of species interactions amongst survivors
covariance between extinction risk and the magni- depends critically on the mechanisms that underlie
tude (Gross and Cardinale 2005) or uniqueness diversity–function relationships: niche partitioning,
(Petchey and Gaston 2002b) of a species functional facilitation or the sampling effect each make very
effects can exacerbate the impacts of species loss on different predictions about how biased extinction
ecosystem function (i.e. diversity–function effects scenarios differ from random extinction scenarios.
are initially stronger for realistic extinctions than In food web simulations, Ives and Cardinale (2004)
 TOWARDS A FOOD WEB PERSPECTIVE ON BIODIVERSITY AND ECOSYSTEM FUNCTIONING 117

showed that the coupling of directional extinction persal as a process affecting species coexistence
with species interactions can lead to unexpected becomes particularly prominent at higher trophic
changes in the functional importance of species. levels where organisms are typically more mobile (at
Although it is clear that non-random patterns of least, on the shorter time-scales of most experiments)
extinction can have very different implications than and, therefore, have the ability to integrate informa-
the random extinctions that commonly simulated in tion across a landscape and aggregate in response to
experiments, our ability to predict the functional the density of their prey. This is important because
changes that stem from non-random extinction – dispersal and aggregation across spatially distinct
particularly the top-down effects of species loss on patches or habitat boundaries can translate into
ecosystem function – is still in its infancy. After our various forms of niche partitioning that stabilize
need to characterize interaction strengths and inter- competitive interactions and consumer–resource
specific tradeoffs (Section 8.4.1), our single biggest gap dynamics (Armstrong 1976, McCann et al. 2005). As it
of knowledge stems from a lack of information about modifies coexistence, dispersal across patches or
levels of covariance between extinction risk and spe- habitat boundaries can also qualitatively alter the BEF
cies-specific impacts on rates of ecological processes at relationship (Mouquet et al. 2002).
various trophic levels. Although most of the work that has examined how
dispersal affects BEF relationships has focused on
single trophic level systems, it is useful to quickly
8.4.3 Environmental heterogeneity, patch review here and then consider how these predictions
dynamics, and scale might be extended to systems with dynamic resour-
ces. A wide variety of ecological models have
The typical biodiversity experiment performed to date highlighted the important role that dispersal plays in
has taken place in experimental units slightly larger maintaining the diversity of communities (e.g. Island
than a five-gallon bucket, and has run for less than one Biogeography Theory – MacArthur and Wilson 1967,
generation of the focal organisms (Fig. 8.5). While ‘mass’ effects – Shmida and Wilson 1985, ‘rescue’
there are noteworthy exceptions (Tilman et al. 2001, effects – Brown and Kodricbrown 1977). Historically,
Hector et al. 1999), it seems safe to say that most of our models of dispersal have been phenomenological,
inferences about biodiversity stem from experiments meaning they did not explain the existence of diver-
performed at spatial scales much smaller, and tem- sity based on first principles. Instead, these models
poral scales much shorter than those at which species assumed there was some ‘magical’ pool of species that
extinctions actually matter (also see Naeem 2001a for a coexisted at large scales via some unknown mecha-
more complete review). Overcoming this mismatch in nism(s), and these species generated propagules that
scale is a daunting task, and the difficulties of per- could subsidize local populations. The emergence of
forming large-scale, long-term experiments are why meta-community theory (Leibold et al. 2004) repre-
ecologists use simplified model systems in the first sented a major advance because these models
place (Srivastava et al. 2004). Nevertheless, ecologists acknowledged that everything in a propagule pool
have begun to make progress on these issues by must ultimately come from the collection of patches
incorporating the important ecological factors that or habitats that span a species range. Based on first
co-vary with scale into their experimental designs principles, meta-community models predict both the
(Cardinale and Palmer 2002, Dimitrakopoulos and causes and consequences of diversity at ‘local’
Schmid 2004, Mulder et al. 2001) and accounting for (organisms interacting as communities within pat-
them in meta-analyses of experiments performed at ches) and ‘regional’ scales (patches of communities
different scales (Cardinale et al. 2007). connected by dispersal).
The issue of scale is by no means unique to BEF One common form of meta-community models
research, nor is it specific to multi-trophic systems. assumes that species coexist through tradeoffs in
There are, however, certain characteristics of multi- their abilities to compete in patches that have dif-
trophic systems that make it especially important that fering types or supply rates of resources (i.e. what
we deal more directly with the issue. Namely, dis- Leibold et al. 2004 call ‘species-sorting’ models).
118 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

These models predict that at the scale of any local sively). The general idea of the spatial insurance
community, increasing the number of species in the hypothesis is that while one species may be sufficient
meta-community serves only to ensure that species to maximize production in any local community, the
best adapted to a given patch will colonize and maximization of productivity across all patches in any
dominate that patch. This is the typical ‘selection heterogeneous landscape requires that a diversity of
effect’ of diversity (Loreau and Hector 2001, Huston species exhibit niche differences at a regional scale.
1997), which has been formalized as follows: assume Meta-community models like that used to generate
that species can be ranked by their carrying capaci- the spatial insurance hypothesis are important
ties such that K(m) represents the species having the because they serve as a springboard from which we
highest carrying capacity in any single patch, K(m-1) can address more pressing issues within the field of
is the next highest, and so on. If competition among BEF research. From the perspective of basic theory,
species is strong (a ¼ 1 in Eqn 8.1), only one species we need to extend meta-community models to con-
from the regional pool gamma will be present in a sider how species diversity impacts the production of
patch at equilibrium, and the biomass in a patch will be community biomass when consumers and their
   resources both move across a spatially heterogeneous
Ncol Ncol Ncol landscape. We need to know what happens to BEF
Bð1Þ ¼ KðmÞ þ 1  Kðm1Þ
 g  g g  1 relationships when (1) resources have a spatial refuge
ð8:4Þ
Ncol Ncol Ncol from their consumers, (2) consumers and resources
þ 1 1 Kðm2Þ þ :::
g g1 g2 disperse at similar versus different rates, or (3) species
exhibit spatially mediated tradeoffs, such as in their
Equation (8.4) says that the amount of biomass
dispersal versus competitive abilities, or dispersal
produced in a patch at equilibrium is proportional
versus ability to resist consumption. At the same time,
to the probability, Ncol/g, that the species with the
we need experiments that explicitly mimic the
highest carrying capacity, K(m), will colonize the
assumptions of different meta-community models,
patch. If a patch is not colonized by the most
and then examine how diversity impacts the pro-
productive species, then the probability that the
duction of local and regional biomass for various
second most productive species, K(m–1)
, will 
colo-  mechanisms that allow consumer–resource coexis-
nize and dominate the patch is 1  Ngcol N g1 .
col
tence. These advances are essential if we expect to
Note that as the number of species colonizing a
patch increases, the probability that a patch predict the ecological consequences of extinction
becomes dominated by the most productive spe- from real food webs where the norm is that species
cies in the regional species pool approaches unity. move across habitat boundaries and make choices
However, one key point is that for the selection about where to spend their time in order to maximize
effect to operate in the first place, species diversity fitness.
must first exist in the regional colonist pool (i.e. g
must exist at the scale of a meta-community). But
in order for diversity to be maintained in the 8.4.4 Socio-economic impacts of food web
regional colonist pool, species must exhibit some diversity
form of tradeoff that ensures they use resources in
After several decades of research, it has become
ways that are complementary across patches. This
apparent that loss of diversity from an ecosystem can
suggests that the same mechanisms that ensure
complementary use of resources across patches in have impacts on ecological processes that rival, if not
a region also produce species-specific selection exceed, many other forms of environmental change.
effects at the scale of a local community (Cardinale Ecologists are now in a position to estimate the
et al. 2004). number of species required to maximize the removal
Loreau et al. (2003) similarly showed that coexis- of greenhouses gasses like CO2 from the atmosphere,
tence of species at a regional scale could maximize remove nutrient pollutants from streams and lakes
biological production at a local scale, and called this that serve as drinking water, or to produce crops and
the ‘spatial insurance’ hypothesis of diversity (also see fisheries. Indeed, it is now possible to make reason-
Chapter 10, where Gonzalez treats the issue exten- ably educated estimates of how diversity loss
 TOWARDS A FOOD WEB PERSPECTIVE ON BIODIVERSITY AND ECOSYSTEM FUNCTIONING 119

Box 8.1 Socioeconomic impacts of predator diversity

One of the primary services that ecosystems provide to aphids, the parasitoid wasp became more efficient at
society is the biological control of insect pests. This attacking the pea aphid. As a result, when all three
service is estimated to be worth US$400 billion per year enemies were together they reduced aphid populations to
globally (Costanza et al. 1997). Although it has long been one-half of that achieved by any enemy species alone.
assumed that effective pest management requires a This translated to a 51 per cent increase in the yield of
diversity of predators, parasites, and pathogens (collectively alfalfa. Alfalfa is the fourth most widely grown crop in the
called ‘natural enemies’), experiments designed to USA with an estimated annual value of US$11.7 billion
explicitly test this hypothesis have only recently begun. (source: US Department of Agriculture). In 2003 when
Two case studies highlight the range of results observed this study was performed, alfalfa was selling for $150 per
thus far. acre. The state of Wisconsin dedicates 3.5 million acres to
the production of alfalfa. Assuming the results of this
experiment can be generalized to Wisconsin, the
economic benefit of predator diversity would be roughly US
$525 million during a single harvesting cycle. In a typical
year in the midwestern USA, alfalfa is harvested 3· per
summer.

Case study 2: Predator diversity increases pest

populations

In a second field experiment, Cardinale et al. (2006)

manipulated the diversity of a different group of aphid
predators, this time focusing on three species of
ladybeetles that are all generalist predators. When the
ladybeetles were placed together in field enclosures, they
A parasitoid female Aphidius wasp laying her egg in a pea aphid. tended to compete with each other in a way that
reduced their individual ability to capture prey. As a result,
Case study 1: Predator diversity decreases pest more diverse predator assemblages were roughly 60 per
populations cent less efficient at controlling aphid populations than
expected based on how each ladybeetle performed
In a field experiment performed in Wisconsin, USA, when alone. In this case, the antagonistic interactions
Cardinale et al. (2003) manipulated the richness of three among the predators led to a 17 per cent decrease in
natural enemies of aphids (pea and cowpea) that are alfalfa yield. This result emphasizes that predator species
herbivorous pests of alfalfa. Two of the enemies – a can interact in ways that may have economic costs. A key
ladybeetle and an assassin bug – were generalist predators challenge for ecologists is to determine the frequency of
that fed on both aphid species. The third was a specialist positive and negative interactions among predators that
parasitoid wasp that attacks only pea aphids. They found might help us evaluate the costs versus benefits of
that as generalist predators reduced the density of both biodiversity.

translates into societally meaningful units – whether Invertebrate predators, parasitoids, and pathogens
that be in dollars, health risks, carbon credits, or can be important promoters of top-down control in
otherwise. terrestrial food webs, helping to keep pests below
The socio-economic implications of biodiversity economically damaging levels. This natural bio-
are perhaps most obvious from studies of higher- logical control of pests represents a valuable eco-
trophic levels, including those of pollinators, and system service that is essential to sustainable
of natural enemies that control pest populations. production of food and fibre. Recent economic
120 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

valuation of the services provided by insects sug- (Ricketts et al. 2004). At a more regional level, Losey
gests the value of biological control of native pests and Vaughan (2006) calculate that native pollinators
by natural enemies is $4.49 billion per year in the (mostly bees) may be responsible for > $3 billion of
USA alone (Losey and Vaughan 2006), and > US fruit and vegetables produced in the USA.
$400 billion per year at a global scale (Costanza Although often less direct, changes in biodiver-
et al. 1997). While classical biological control tends sity and associated trophic structure have major
to focus on the contribution of individual species of implications for issues such as disease risk, with
natural enemies, a growing number of studies sug- associated impacts on economics and human well
gest that the efficiency of biocontrol is often a func- being. For example, top predators are often the first
tion of non-additive interactions among multiple species to disappear as habitat is destroyed and
predators, parasitoids, and pathogens (Rosenheim fragmented. As elaborated in Chapter 15, when
2007, Losey and Denno 1998, Snyder and Ives 2003, predators are lost to ecosystems, their prey may
Snyder et al. 2006, Finke and Denno 2005, Cardinale increase in abundance, leading to increased trans-
et al. 2003, Cardinale et al. 2006b). Although it is not mission efficiency of zoonotic diseases such as
yet clear whether these interactions among enemies Lyme disease (Ostfeld and Holt 2004, Dobson et al.
generally increase or decrease prey populations, it is 2006). While quantifying the benefit of biodiversity
clear that the economic impacts of natural enemy in terms of disease regulation and infected cases
diversity can be substantial (Box 8.1). averted is clearly complex, many diseases such as
Crop pollination is another ecosystem service malaria, tick-borne encephalitis, and West Nile
centred on interactions across trophic levels. The fever have been shown to increase as biodiversity
global value of pollination services have been esti- falls (Dobson et al. 2006, and Chapter 15).
mated at US$117 billion per year (Costanza et al.
1997) and in a recent review, Klein et al. (2007)
8.5 Summary
concluded that fruit, vegetable, or seed biodiversity
(i.e. richness, abundance, and distribution of mul- The emerging paradigm of Biodiversity Effects on
tiple species of pollinators) in delivering this eco- Ecosystem Functioning has shown great potential
system service are often poorly quantified. Similar to augment ecology’s historical focus on the causes
to evaluations of classical biocontrol, where the of biodiversity with a much more contemporary
focus is on the action of one or few natural enemies understanding of its ecological consequences. Even
rather than diversity per se, many of the economic so, BEF studies have, thus far, been limited to
valuations of pollination services consider the con- highly simplified ‘model’ communities that are
tribution of honey bees alone. Klein et al. (2007) nowhere near the trophic complexity of real com-
report case studies for nine crops on four continents munities. To overcome this limitation, it is now
implicating a diversity of pollinators and revealing imperative that ecologists begin to merge the BEF
that agricultural intensification jeopardizes wild bee paradigm with more classic ideas in food web
communities and their stabilizing effect on polli- ecology that detail how interactions among trophic
nation services at the landscape scale. At the indi- levels that play out in space and time can constrain
vidual farm level, such natural pollination services fluxes of energy and matter. Most hypotheses about
can contribute significantly to annual income; a the functional role of diversity within and across
study from a coffee plantation in Costa Rica, for trophic levels are in their infancy, and they repre-
example, indicated native bee species account for sent a rich opportunity for new work during the
$62,000, or 7 per cent of the farm’s annual income second generation of BEF experiments.
 CHAPTER 9

Microbial biodiversity and ecosystem

functioning under controlled
conditions and in the wild
Thomas Bell, Mark O. Gessner, Robert I. Griffiths, Jennie R. McLaren,
Peter J. Morin, Marcel van der Heijden, and Wim H. van der Putten

9.1 Introduction microbial populations and communities, so a

familiar refrain is that microcosm experiments with
Microbial communities have been and continue to constructed communities are much too simplified
be used widely to test basic ideas in ecology, and to have a bearing on what occurs in nature. In
studies of the relationship between biodiversity and addition, many environmental microbiologists have
ecosystem functioning are no exception. Although argued that experiments using artificially assem-
microbial microcosm studies have been successful at bled microbial communities are irrelevant at best
shedding light on debates in biodiversity-ecosystem (misleading at worst) because the experiments are
functioning research (Petchey et al. 2002), for many conducted at inappropriate temporal and spatial
community ecologists, their raison d’être is limited to scales. Although the dichotomy we describe
testing hypotheses with a degree of abstraction just between environmental microbiologists and micro-
slightly below that of mathematical models. The cosm microbial ecologists is a caricature, there is
underlying idea is that simple microcosms, like nevertheless a clear need for increased communi-
theoretical models, are surrogates for what might cation between these groups of researchers.
be occurring in more complicated and, it is often Largely due to the development of powerful and
implied, more interesting communities composed accessible molecular techniques, it is increasingly
of larger organisms. In this context, the aim of most possible to ask ecological and evolutionary questions
microbial microcosm studies is to create a highly of natural microbial communities, even though it
simplified system to ensure unequivocal identifi- remains difficult to manipulate microbes in the field
cation of patterns and causal mechanisms. In bio- the way we can manipulate larger organisms. Without
diversity-ecosystem functioning research, this has the ability to manipulate microbes in the field, causal
required experimental assembly of communities mechanisms continue to be difficult to pin down.
that are much less species-rich than the microbial The first purpose of this review is to give a
communities in natural ecosystems. glimpse of the considerable advances in microbial
Apart from the small coterie of ‘microcosmologists’ ecology, and to outline how microbial biodiversity
(Carpenter 1996), there is a separate fraternity of affects the functioning of ecosystems in what is a
environmental microbiologists who typically pub- rapidly expanding field of study. The second pur-
lish in a different suite of journals and attend dif- pose is to contrast the results reported primarily in
ferent conferences than ecologists interested in microbiological journals with those of ecologists who
larger organisms, even though many of the research use microbes as model systems. We concentrate on
questions are similar. The focus of environmental non-pathogenic prokaryotic and eukaryotic micro-
microbiologists is to understand naturally occurring bial communities, leaving discussions of pathogenic

121
122 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

microbial communities to Chapter 15. We do not diversity therefore proceed by taking a number of
discuss viruses in the current review, in part because sub-samples: first by taking only a subset of the
of a lack of biodiversity-ecosystem functioning cells in the community, then a subset of the DNA
studies explicitly using viruses. However, given that from those cells, and then, for example, amplifying
many viruses appear to be host-specific and that a particular locus from the extracted DNA before
they are important in controlling microbial popula- sequencing a subset of the DNA that has been
tions and hence community structure in many eco- amplified (Fig. 9.1). Although it is true that surveys
systems (Suttle 2007), viral diversity is very likely to of non-microbial organisms do not identify all of
have considerable repercussions for ecosystem the individuals in the examined community, such
functioning. ecological surveys of larger organisms generally
record a significant percentage. Surveys of micro-
bial communities, in contrast, typically identify
9.2 Microbial biodiversity and many orders of magnitude fewer individuals than
ecosystem functioning are actually present. Currently, a clone library (i.e. a
collection of clones of chromosomal DNA that can
9.2.1 Microbial biodiversity
be used to quantify microbial diversity; Fig. 9.2)
One of the principal difficulties in analyzing the might comprise a few hundred individuals (per-
relationship between microbial diversity and ecosys- haps hundreds of thousands of individuals in the
tem functioning is that it is notoriously complicated to near future), whereas the community would be
describe the diversity of microbial communities. Most likely to contain at least 105 cells per cubic centi-
microbial groups lack sufficient morphological fea- metre (of soil or water), often several orders of
tures to permit identification to the species level using magnitude more, and the community contains
conventional taxonomy or classical microbiological many thousands of cubic centimetres. Much less
techniques (e.g. staining cell walls or using selective than 1 per cent of a community is therefore recor-
media). In addition, most of the microbial world ded for even the most extensive surveys of micro-
eludes investigation under controlled conditions bial communities. This creates a problem because
because of difficulties in culturing most microbial many richness estimators rely on guessing at the
strains in the laboratory (Rappé and Giovannoni distribution of abundance in the community (i.e.
2002). DNA-based molecular techniques have how many rare species have not been observed in
provided highly resolved descriptions of microbial the survey). Since such a small portion of the
communities (e.g. Venter et al. 2004, Sogin et al. 2006), community is sampled, the distribution of abun-
but even current high-throughput sequencing dance in microbial communities is still unknown.
approaches have not comprehensively surveyed a While it is possible to make educated guesses at a
single ecosystem, and all techniques suffer from both distribution of abundance and extrapolate numbers
sampling error and sampling bias (Fig. 9.1). of species (Curtis and Sloan 2004, Quince et al.
The first difficulty in assessing microbial diver- 2008), such estimates remain speculative. The new
sity is that the number of individuals to identify is generation of sequencing technologies will curtail
too large for any reasonable ecological survey this problem to some extent, but even sequencing
(Hughes et al. 2001), although new sequencing hundreds of thousands of individuals in a microbial
technologies have the potential to provide reason- community will still represent only a minuscule
ably good estimates of diversity in some species- portion of the total community.
poor microbial habitats in the foreseeable future The second difficulty in assessing microbial bio-
(Quince et al. 2008). Even extremely unproductive diversity is that the sample is not a random subset
environments such as drinking water will have of the larger community. In Fig. 9.1, each arrow
thousands of microbial cells per cubic centimetre, represents a situation in which a sub-sample is
and typical communities contain more cells than taken. Each sub-sample is biased (i.e. non-random);
could possibly be identified individually using for example, some sequences amplify more readily
current technology. Techniques to assess microbial than others during a polymerase chain reaction
 MICROBIAL BIODIVERSITY AND ECOSYSTEM FUNCTIONING 123

An ecosystem

Culture dependent
techniques. Cells are
Cells. A sample from the cultured on agar plates
ecosystem containing and characterized by
living microbial cells morphology or using
selective media.

Reassociation kinetics. Double

Metagenomics. Extracted DNA Culture independent stranded DNA is heated until
is sequenced and assembled techniques. DNA is the strands separate. The
into putative genomes. extracted and purified kinetics describing the rate at
The number of genomes is an from the cells. which strands re-associate gives
estimate of species richness. a measure of diversity.

Polymerase chain
reaction. One locus is
amplified.

Total species discovered

Community fingerprints. Amplified DNA is separated

Microarrays. The PCR product is
according to some sequence-specific property.For Clone number
washed over a slide printed with
example, denaturing-gradient gel electrophoresis
oligonucleotides. Complementary
(DGGE) separates DNA sequences according to their Clone libraries. Amplified DNA is
DNA binds to the ologonucleotides
propensity to denature at a particular denaturant sequenced. The rate of accumulation
and produces a fluorescent signal.
concentration. Denatured DNA stops moving through of novel sequences provides an
The number of positive signals
an agarose gel leading to different banding patterns estimate of diversity.
gives an estimate of diversity.
depending on the composition of the communities.

Figure 9.1 Popular methods for estimating microbial diversity. Microbial cells are too abundant and morphologically similar to survey using conventional
ecological techniques. Rather, a series of subsamples are taken, where each arrow in the figure represents a subsample. Difficulties arise in estimating
microbial diversity because the degree to which these are random subsamples is poorly understood.

(PCR) (Muyzer and Smalla 1998), which biases the exist for larger organisms, the degree to which the
final DNA copy number of each species compared sub-samples constitute non-random samples of the
to the original species mixture. Different initial copy community remains largely unknown and an area
numbers in different species can also significantly of active study. It is only after these problems have
affect the final mixture of PCR products (Farrelly been resolved that it will be possible to accurately
et al. 1995). Although the same issues of sample bias assess microbial diversity.
124 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Microcosm Removal Observational Fig 9.2 A schematic interpretation of microbial biodiversity-

experiments experiments studies ecosystem functioning studies. Experiments that construct communi-
Ecosystem functioning

ties from culturable microbes have frequently found positive, satu-

rating relationships between diversity and ecosystem functioning.
These experiments have been conducted with at most 102 species.
Removal experiments, where the diversity of natural communities is
reduced, have shown mixed results, but there is often little effect of
even significant declines in biodiversity on ecosystem functioning. For
example, Wertz et al. (2006) reduced diversity from an estimated 8.3
· 106 bacterial species down to an estimated 8.4 · 102 species but
found little reduction in a variety of ecosystem response measures.
Observational studies of natural bacterial communities have found a
variety of relationships, but there is frequently no clear pattern or a
100 102 104 106 108 negative relationship.
Bacterial species richness

The final difficulty with estimating microbial 2008, van der Heijden et al. 2008). In aquatic
diversity is that there is ongoing controversy in environments, microbes often set the level of pri-
defining what constitutes a microbial species mary production and decomposition. In terrestrial
(Achtman and Wagner 2008). As with larger ecosystems, microbial communities are important
organisms, species identity is relatively clear among drivers of decomposition, thus converting organic
microbial species that reproduce sexually. When matter into forms that are available for uptake
reproduction is asexual, as is generally the case, the by plants. As a result, microorganisms account for
main alternative is to infer whether two individuals a major portion of ecosystem metabolism and
are of the same species if they share an arbitrary biomass, on a global scale, accounting for a repor-
degree of DNA sequence similarity. Often, 97 per ted 50 per cent of the total protoplasm on Earth
cent sequence similarity is taken as the threshold, (Whitman et al. 1998). Microbes contribute to the
although different cut-offs are used for different loci regulation of Earth’s climate by mediating fluxes of
or for different taxonomic groups. In addition, carbon dioxide, nitrous oxide, methane, and other
many microbes frequently transfer DNA directly greenhouse gases (Bardgett et al. 2008). The ability
from an individual of one species to an individual of microbial communities to metabolize even the
of a different species, a process referred to as hori- most recalcitrant molecules is a testament to their
zontal gene transfer. Because the biological species enormous metabolic repertoire.
concept does not extend to the typical reproductive Microbes are also important in an applied con-
systems of most microbes, measures of ‘biodiver- text. For example, they are a key consideration for
sity’ in the microbial literature can have vastly agricultural practices, particularly when agriculture
different interpretations depending on the particu- relies on renewable resources and is employed to
lar species definition that is employed. Although minimize environmental degradation. Microbes
we use the term ‘species’ in the current chapter, it is have been exploited as ‘microbial pesticides’(Qaim
evident that microbial biodiversity-ecosystem and Zilberman 2003), including both naturally
functioning studies will have to be interpreted in occurring and genetically modified pathogens that
light of the species definition used, and conflicting directly or indirectly reduce pest populations. Per-
results might simply result from differences in haps the best-known example is Bacillus thur-
species definitions. ingiensis, which produces a toxin that deteriorates
insect mid-gut epithelial cells, thus halting larval
insect foraging. There is enormous functional var-
9.2.2 Microbial functions
iation even within microbial species. In B. thur-
Microbial communities are pivotal for the func- ingiensis, for example, the variation in pathogenicity
tioning of the world’s ecosystems (Falkowski et al. and host specificity is attributed in part to which
 MICROBIAL BIODIVERSITY AND ECOSYSTEM FUNCTIONING 125

Table 9.1 Putting a price on microbial functions. Global economic ecosystems makes them of particular importance
valuations of some important microbial services. These data were compiled
both for basic ecological investigations and in an
by FAO in 1998 and have not been adjusted to current market value.
applied context. Unlike with larger organisms,
Ecosystem service Value (billion US$ per year) research on microbial diversity is not driven by con-
Soil formation on agricultural land 500 servation worries, but by the enormous benefits (and
Nitrogen fixation for agriculture 90 harm) to humans that could arise once the factors
Pharmaceuticals of microbial origin 42.5 affecting microbial functions are well understood in
Synthesis of industrial enzymes 1.3 terms of harnessing beneficial services and prevent-
ing harmful impacts. For example, even marginal
increases in the ability of a microbial community to
plasmids they carry (Rasko et al. 2005), but plasmid metabolize harmful constituents in sewage might
diversity in the context of microbial biodiversity- have significant economic ramifications (Wagner and
ecosystem functioning studies has been largely Loy 2002); algal communities have promise as bio-
ignored. There is also the possibility that horizontal fuels or as food (Gross 2008); and altering microbial
gene transfer is important in maintaining ecosystem gut functioning might prevent obesity and therefore
functioning, which also is a process that is largely reduce medical costs (Backhed et al. 2004). In many of
absent in larger organisms. these areas, the key is to understand how differences
There are numerous other examples in which in the structure and performance of microbial com-
microbial diversity affects managed ecosystems munities translate into differences in functioning,
and human life, the intimate involvement of which is precisely the question being addressed by
microbes in so many processes making it difficult to ecologists investigating the relationship between
put a monetary value on microbial diversity. biodiversity and ecosystem functioning.
Despite the growing recognition of the importance
of microbial biodiversity, the significance of this
biodiversity component is only beginning to be 9.3 Functioning of microbial
acknowledged in biodiversity policy debates. While communities under controlled
most are not worried about microbial species going conditions
extinct, even small changes in the functioning of
9.3.1 Model systems for biodiversity research
microbial communities have the potential for sig-
nificant impacts on economy, welfare and other Microbial communities have a venerable history as
aspects of human life (Table 9.1). Perhaps as a con- model systems for studying questions in commu-
sequence, all signatories to the World Trade nity ecology (Jessup et al. 2005). Their popularity
Agreement now must adopt and implement patent stems in part from the ease with which it is possible
laws for microorganisms and for biotechnology to conduct experiments over many generations
processes applied to living organisms, based on under controlled laboratory conditions. Such rapid
international tariff and trade rules (FAO 1998). This generation times allow the communities to arrive at
will undoubtedly have implications for the use and the equilibrium conditions upon which many
management of microbial diversity, as it becomes mathematical models are based. In addition, con-
the legal property not only of the patent depositor, trolled laboratory microcosm experiments allow for
but also of the country of origin, regardless of where communities to be experimentally assembled
the organisms were collected. For microbial com- according to a prescribed design by drawing dif-
munities, it might not be imperative to conserve ferent combinations of species from laboratory
specific species or strains, but rather to conserve stocks of pure cultures. In contrast, studies of nat-
specific metabolic pathways, which may be the ural communities lack this opportunity, in part
result of millions of years of evolution and might be because the levels of diversity are too high to be
lost due to chance conditions (Falkowski et al. 2008). tractable for this type of approach. The combination
In summary, the importance of microbial commu- of short generation times and fine control of com-
nities in determining flows of energy and matter in munity membership has resulted in microbial
126 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

microcosms becoming a reasonable ‘halfway house reduced temporal variability in total community
between mathematical models and the full com- biomass, especially in more productive environ-
plexity of the field’ (Lawton 1995). ments. Temporal variability in the biomass of
Critics have argued that microcosm experiments individual populations was not affected by diver-
lack generality, rely on overly simplified commu- sity, nor by productivity. Differences in the species
nities, or are experiments that are conducted at an composition among diversity treatments had no
inappropriate scale (Carpenter 1996, Jessup et al. influence on the variability of community-level
2004). Clearly, if the question under investigation is biomass, while composition did affect the varia-
to understand how a specific ecosystem operates bility of biomass at the level of individual popula-
then there is no substitute for the real thing. But if tions. The effect of diversity, but not the
the purpose is to understand more generally the destabilizing effects of productivity predicted by
processes that are important for how biodiversity the paradox of enrichment, predominated in these
affects ecosystem functioning, there is no intrinsic microcosms.
reason to choose one system over another, and it In a separate experiment, diversity was manipu-
would seem sensible to use systems in which it is lated and community biomass was predicted based
easiest to conduct the necessary experiments. With on allometric relationships between organism size
this line of reasoning, microbial communities and abundance (Long et al. 2006). Microcosms with
appear to be the ideal model system for biodiver- greater diversity tended to yield more total biomass
sity-ecosystem functioning studies. Since much of than systems of lower diversity, and organism size
this research was reviewed previously (Petchey played only a transient role in determining biomass.
et al. 2002), we limit the following sections to sub- This result is consistent with positive effects of
sequent advances in the field. diversity on overyielding noted in other, very dif-
ferent systems (Loreau and Hector 2001, Loreau et al.
2001). Krumins et al. (2006) further explored the
9.3.2 Microcosm biodiversity-functioning
indirect impact of bacterivore diversity on rates of
experiments
bacterially mediated decomposition of wheat seeds,
9.3.2.1 Protistan food webs and they found that bacterivores altered both the
Since the last review of studies of biodiversity and taxonomic composition and overall metabolic activ-
ecosystem functioning in eukaryotic microbes ity of the bacterial community.
(Petchey et al. 2002) there have been a number of Other studies have explored the impacts of var-
new developments. Having established that posi- ious factors, including assembly history, produc-
tive diversity-functioning relationships often exist tivity, and consumers on patterns of diversity.
in these microcosms (Petchey et al. 2002), the field Fukami and Morin (2003) showed that the specific
has begun investigating how this relationship is temporal sequence of species arrival had a pro-
modified by important ecological drivers, for found effect on the form of relationships between
example how systems of different diversity respond microbial diversity and productivity, estimated as
to experimental perturbations, to alterations in the biomass accumulation (Fukami and Morin 2003).
amount of available resources, and to manipulating Hump-shaped, concave, or monotonically increas-
other factors which indirectly manipulate diversity, ing patterns can all result simply from differences
such as predator abundance. in the history of community assembly. Other work
Steiner and colleagues explored patterns of tem- shows that different forms of predation, specifically
poral variability in the presence or absence of per- that imposed by specialist versus generalist con-
turbations in multitrophic food webs of differing sumers, can either promote or eliminate positive
diversity (Steiner 2005a, Steiner et al. 2006). Theo- relations between productivity and protist diversity
retical studies predict that increased productivity (Jiang and Morin 2005).
destabilizes populations (Rosenzweig 1971) but can Finally, a reanalysis of an earlier biodiversity-
stabilize total community biomass. In unperturbed ecosystem functioning study (McGrady-Steed et al.
food webs, greater diversity was correlated with 1997) in response to critiques of the design of
 MICROBIAL BIODIVERSITY AND ECOSYSTEM FUNCTIONING 127

early biodiversity experiments (Fukami et al. 2001, ment. One recent study looked at mixtures of up to
Loreau et al. 2001) confirmed that elevated biodi- eight bacterial strains selected for their ability to
versity can reduce variability in some aspects of grow on cellulose in monoculture (Wohl et al. 2004).
ecosystem functioning (Morin and McGrady-Steed By selecting only species that utilized a particular
2004). The effect is not related to a reduction in the substrate (cellulose), and then offering those species
temporal variation in ecosystem functioning, but only that substrate in spatially homogenous
rather reflects reduced variation among replicate (shaken) microcosms, the study was designed to
communities of similar diversity at any point in time. prevent resource use complementarity from being
This is perhaps best interpreted as reduced spatial important. It was therefore not surprising that the
variation in functioning in more diverse systems. observed influence of diversity was partly attrib-
utable to a selection effect. Interestingly, despite
9.3.2.2 Aquatic bacteria being selected on a single substrate, species richness
Bacteria have provided some important advances appeared to be important in addition to the effects
in understanding biodiversity-ecosystem function- of selection, possibly due to facilitation among
ing relationships because of the relative ease with species. In contrast, facilitation is unlikely to have
which it is possible to assemble communities and been driving the overall pattern of increase in
store strains for prolonged periods. For example, in functioning with increasing biodiversity in the Bell
the most species-rich microbial biodiversity-eco- et al. (2005b) study or else an accelerating biodi-
system functioning experiments to date, Bell et al. versity-ecosystem functioning relationship (i.e.
(2005b) used 72 naturally co-occurring bacterial where the slope of the relationship increases with
species and found a positive relationship between increasing biodiversity) would have been observed,
species richness and community respiration in although such an observation would have been
aquatic microcosms (Bell et al. 2005b). Both diver- hidden if facilitation was rare. This does not
sity and species identity were important in deter- exclude the possibility that facilitation is common
mining functioning in this study. A similar in microbial communities, but it might often be
conclusion was reached when investigating the masked by the increasing degree of redundancy as
relationship between genotype diversity and eco- species are added to the community.
system functioning using a single species of bacte- One of the principle advantages of using bacteria
ria, Pseudomonas fluorescens (Hodgson et al. 2002), in biodiversity-ecosystem functioning experiments
where evidence was found for a significant effect of is that short generation times allow simultaneous
functional (ecotype) and genotypic diversity on investigations of evolutionary and ecological pro-
both productivity and invasion resistance as mea- cesses. For example, a single generalist genotype of
sured by the degree to which mixture yields Pseudomonas fluorescens diverges into a number of
exceeded the maximum monoculture yields of the distinct specialist ecotypes that inhabit the micro-
constituent strains. There is therefore the opportu- cosm sides, air–water interface, and open water
nity for significant diversity effects even within (Buckling et al. 2000). This niche differentiation
species. In contrast, experiments using four bacte- leads to increased levels of functioning (Hodgson
rial species found little evidence that species rich- et al. 2002), so any processes that disrupt the extent
ness affected ecosystem functioning (wheat seed to which diversification occurs (Brockhurst et al.
mass loss) because species that contributed little to 2006, Brockhurst et al. 2007) will also affect the level
seed mass loss tended to become dominant (Jiang of ecosystem functioning. Thus, unlike with larger,
2007). Similar experiments have suggested that a longer-lived organisms, in microbial systems it is
significant relationship between bacterial diversity possible to examine the evolutionary processes
and functioning might only become apparent in the directly and so too make hypotheses about which
context of the larger food web (Naeem and Li 1997, ecological mechanisms will be important in deter-
Naeem et al. 2000). mining functioning (Fukami et al. 2007, Venail et al.
These outcomes might be determined by the 2008). If, as many have suggested, there is wide-
method used to isolate bacteria from the environ- spread functional redundancy in bacterial
128 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

communities, bacterial diversity must be main- logical in nature, so that the mechanisms behind
tained in nature in the absence of niche differences, and circumstances under which fungal diversity
which is contrary to many theories of species effects on litter decomposition emerge in aquatic
coexistence. For the microcosms used by Bell et al. microcosms are currently unknown.
(2005b), there is evidence that the communities There is also evidence that richness of aquatic
were neutrally assembled (Woodcock et al. 2007), hyphomycete communities can indirectly enhance
leading to an independent prediction that any decomposition through a positive effect on resource
positive relationship between diversity and func- quality for invertebrate detritivores (Lecerf et al.
tioning in this system should be a consequence of 2005). Further more ecosystem processes other than
the selection effect. The next generation of microbial litter decomposition (e.g. fungal biomass produc-
experiments in this field is therefore likely to tion) may be enhanced by diverse communities
include studies that simultaneously investigate the (Duarte et al. 2006). Lastly, even when average rates
causes and consequences of biodiversity. of decomposition are independent of species rich-
ness, variability of rates has been found to decline
9.3.2.3 Fungi strongly with increasing fungal richness (Dang et al.
Fungal communities are important drivers of 2005), as predicted from theoretical models (Doak et
litter decomposition with potential for influencing al. 1998) and observed in other types of systems
carbon sequestration in soils and, for aquatic fungi, (Tilman et al. 2006b, Lecerf et al. 2007). All else being
in downstream lakes, reservoirs and oceans. Con- equal, this should lead to higher predictability of
sequently, there is great interest in understanding litter decomposition rates when fungal communi-
the degree to which the diversity and structure of ties in streams are diverse.
fungal communities affect rates of decomposition. In microcosm experiments with culturable
Varying the species richness of leaf-colonizing saprotrophic soil fungi, increased richness resulted
stream fungi (aquatic hyphomycetes) in micro- in faster decomposition rates on grass litter (Deacon
cosms had no effect on average leaf decomposition et al. 2006), forest soil (Wardle et al. 2004a, Tiunov
rates in communities with up to eight fungal spe- and Scheu 2005) and powdered cellulose (Tiunov
cies (Dang et al. 2005, Duarte et al. 2006), which and Scheu 2005). Although species richness in these
implies a high degree of functional redundancy experiments was much lower than the number of
among these fungi. However, in a separate experi- species in the ecosystems from where the fungi
ment, cultures containing two early fungal coloni- were isolated, positive diversity effects on decom-
zers of leaves enhanced decomposition by 73 per position also emerged in an experiment that
cent compared to values expected from decompo- involved a rather high number of fungal species (43
sition rates of single-species cultures (Treton et al. taxa) (Setälä and McLean 2004). Nevertheless,
2004). This outcome, in contrast to results from communities with low species richness (six species)
experiments using communities of several species were as effective as the most diverse community in
(Dang et al. 2005, Duarte et al. 2006), is strong evi- maintaining ecosystem functioning (Setälä and
dence of complementarity resulting in faster litter McLean 2004), indicating that fungal diversity
decomposition. In a similar vein, Bärlocher and effects on decomposition saturate at low levels, as
Corkum (2003) reported a tendency towards faster has been found in many other circumstances.
decomposition with increasing fungal richness (1 to
5 species), although mixed communities never 9.3.2.4 Mutualistic microbe–plant interactions
caused greater mass loss than the most effective Mycorrhizal fungi and nitrogen-fixing bacteria form
species alone (Bärlocher and Corkum 2003). Ravir- symbiotic associations with approximately 80 per
aja et al. (2006) also found that both species richness cent of all terrestrial plants, and therefore constitute
and identities affected leaf mass loss in microcosms, an important pathway by which nutrients (e.g.
although again the most effective fungal species inorganic nitrogen and phosphorus) are taken up
degraded leaves faster than species mixtures. To by primary producers. Several studies have
date, all of these studies have been phenomeno- manipulated mycorrhizal diversity and measured
 MICROBIAL BIODIVERSITY AND ECOSYSTEM FUNCTIONING 129

plant performance. Results indicate that plant bial communities and not only to the subsets that
diversity, productivity and invasion success are can be cultured (Fig. 9.1).
responsive to either mycorrhizal diversity or In general, the difficulty with current culture-
mycorrhizal identity (van der Heijden et al. 1998, independent studies is that any genuine biodi-
Stampe and Daehler 2003, Vogelsang et al. 2006). versity effect tends to be confounded because of
Similarly, manipulation of rhizobia in experimental differences among species in their susceptibility to
dune grassland showed that presence of these elimination during the biodiversity manipulation
nitrogen-fixing bacteria enhanced nitrogen capture procedure. This is evident from the titles of the
(þ85 per cent), plant productivity (þ35 per cent) articles that use this kind of approach, where some
and plant evenness (þ34 per cent) (van der Heijden studies claim to examine the impact of diversity
et al. 2006). The diversity of bacterial symbionts was (Cavigelli and Robertson 2000, Bonkowski et al.
partly responsible for these effects because several 2001, Muller et al. 2003), others investigate the
of the legume species present in the microcosms impact of community structure (Franklin et al.
formed host-specific associations with specific 2001, van der Gast et al. 2003, Griffiths et al. 2004),
rhizobia. There is evidence that some of the effects and others focus on the impact of species compo-
of mycorrhizal diversity depend on the environ- sition (Cavigelli and Robertson 2000). Yet all of
mental context, depending on the species of plant these studies performed precisely the same kind of
that is infected and fertility of the soil (Jonsson et al. manipulation; rare or susceptible species were
2001). Recently, there have been some clues of how eliminated. What these studies can demonstrate is
complementarity among mycorrhizal strains oper- whether either reductions in biodiversity or the
ates. In particular, some mycorrhizal families elimination of particular species are correlated
appear to protect against fungal pathogens, with changes in the magnitude or stability of
while other families enhance phosphorus uptake. functioning, but unambiguous attribution of
As a consequence, plant growth is enhanced when effects to diversity changes is not possible.
both types of family are present (Maherali and
Klironomos 2007).
9.4.2 Field experiments and observations

9.4 Functioning of microbial 9.4.2.1 Soil microbes

communities in the wild Soil microbial communities play a pivotal role in
determining rates of litter decomposition (Wardle
9.4.1 Diversity and functioning in the 2002). One of the major hurdles is that microbial
microbial wilderness diversity in soils is extraordinarily high, with as
Since most microbes cannot be cultured, it is gen- many as tens of thousands of bacterial and fungal
erally impossible to experimentally assemble com- species in a single gram of soil. With so many
munities from a library of constituent species to species apparently competing for a limited set of
reflect the makeup of communities in natural eco- resources, the predominant view is that many soil
systems. The alternative to the culture-dependent microbes are functionally redundant (Chapin et al.
approach is to conduct experiments or perform 1997, Wardle et al. 2004a, Deacon et al. 2006). There
comparative analyses using exclusively culture- are opportunities for, resource partitioning espe-
independent techniques to manipulate or describe cially on the most recalcitrant or exotic substrates.
microbial diversity and simultaneously measure Lignin, for example, is most efficiently degraded by
ecosystem process rates in situ (Cavigelli and some basidiomycetous fungi commonly referred
Robertson 2000) or in artificially created ecosystems to as white-rot fungi. Although there may be pro-
(Bonkowski et al. 2001, Griffiths et al. 2004, Girvan nounced differences in enzymatic capacities
et al. 2005). In both cases, differences in the micro- among microbial species to degrade other plant
bial communities among replicates can be identified polymers, it appears that most have the metabolic
or created, and quantified. The advantage of this machinery to break down the majority of the
approach is that the results apply to whole micro- common substrates they encounter. Hutchinson’s
130 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

‘paradox of the plankton’ (which asks how a large ammonia oxidation, and therefore concluded that
number of species can be maintained in a given there is potential for important effects of nitrifier
community when they appear to be occupying community structure and diversity on nitrification
similar niches) (Hutchinson 1961) remains unre- rates (Cavigelli and Robertson 2000).
solved for soil microbes. While the high levels of Manipulating the diversity of higher trophic
diversity might be explained in part by the intri- levels in soil communities can also influence
cate physical structure of the soil environment decomposition rate indirectly through their effect
(Crawford et al. 2005) as well as the rich set of on bacterial and fungal populations (Cragg and
interactions among substrate availability, abiotic Bardgett 2001, Hättenschwiler et al. 2005). For
conditions (e.g. pH, temperature) and the specific example, there was no increase in decomposition
species that are in the vicinity (Treton et al. 2004, with increasing bactivorous nematode richness,
Wardle et al. 2004a), it is difficult to envision how even though some nematode species suppressed
thousands or, for bacteria, many more species can bacterial activity and diversity (De Mesel et al.
occupy finely differentiated niches. The prediction is 2006). However, species composition appeared to
therefore that many soil species are functionally play a role in controlling decomposition when
redundant. richness had no effect in collembola (Cragg and
There have been several experiments in which Bardgett 2001) or microbivorous nematodes
soil microbial diversity has been reduced through (Mikola and Setälä 1998).
either fumigation or dilution. When a fumigation Overall, artificially reduced levels of diversity
treatment was applied, Griffiths (2000) found have not resulted in a clear effect on soil func-
that ‘general’ soil functions (such as total com- tioning. It is certainly the case that that functioning
munity respiration) were inversely correlated is sometimes decreased when biodiversity is
with biodiversity, while the relationship was reduced, but the reasons why this occurs remains
positive for ‘specific’ functions such as nitrifica- equivocal (see 9.4.1 above). The predominant
tion (Griffiths et al. 2000). In contrast, Degens theme in the soil literature is that it is difficult to
(1998) found that the reductions in diversity draw generalizations about the relationship
caused by fumigation caused a decrease in between soil microbial diversity and processes
decomposition rate of simple organic compounds, (Raffaelli et al. 2002, Hättenschwiler et al. 2005).
although this relationship disappeared at high Relationships often appear to be idiosyncratic
levels of soil moisture. A similar decrease in (Raffaelli et al. 2002, Hättenschwiler et al. 2005)
decomposition rate was found in soil microbial although aspects of redundancy and keystone
communities with reduced diversity achieved by species effects are also evident (Setälä and McLean
dilution, although differences were only found 2004). Clearly, these kinds of experiment remain in
between the highest and lowest dilution levels their infancy, and further investigations are nec-
(Griffiths et al. 2001). Wertz et al. (2006) created essary to construct an image of how the diversity
differences in soil microbial diversity among and composition of soil microbial communities
replicate communities by diluting soil microbial influence soil processes.
suspensions before inoculation, after which they
allowed soil microbial biomass to recover (Wertz 9.4.2.2 Microbe–plant interactions
et al. 2006). Their results suggest considerable Soil microbial communities interact directly
functional redundancy, even for the specific pro- and indirectly with plant roots as pathogens
cesses they measured, such as ammonium trans- and symbionts (direct interactions) and decom-
formation, which are carried out by relatively posers and antagonists (indirect interactions)
limited numbers of taxa (ammonia oxidizers, (Wardle et al. 2004a). In turn, plants manipulate
which carry out the first step of nitrification). the chemical environment surrounding their roots
Comparative studies that used natural differences by secreting chemicals that favour particular
in soil nitrifier communities found that the iden- microbial consortia, thereby altering the composi-
tity of the species in the soil affected rates of tion and diversity of the root-associated microbial
 MICROBIAL BIODIVERSITY AND ECOSYSTEM FUNCTIONING 131

communities (Wardle 2002). The positive and abundance than on diversity (Wardle et al. 2004a,
negative feedbacks between plants and microbial Milcu et al. 2006).
communities form an enormously complex net-
work of interactions that is only beginning to be 9.4.2.2 Aquatic fungi
understood (Lep
s et al. 2001, Scheu 2001, Bezemer The relationship between fungal diversity and
et al. 2005, De Deyn and Van der Putten 2005, ecosystem functioning has also received some
Bezemer et al. 2006). attention in aquatic ecosystems because of the
There is some evidence to suggest that plant importance of fungi in litter decomposition. Results
diversity plays a role in determining microbial from two surveys in streams suggest that the spe-
diversity and ecosystem functioning (Hooper et al. cies-poor fungal communities presumably affected
2005), but the importance of plant diversity com- by forestry practices or water pollution do not
pared with processes within soil microbial food result in altered leaf decomposition rates (Raviraja
webs remains uncertain (Kowalchuk et al. 2002). et al. 1998, Bärlocher and Graça 2002). However, the
Although there are examples of effects of plant general paucity of such field data and the problem
species richness on soil functioning (Zak et al. of drawing inferences about cause and effect from
2003), for the most part the effect of plant diversity correlational data currently impede conclusive
appears to be plant species-specific (Cleland et al. answers about the significance of aquatic fungal
2004, De Deyn et al. 2004, Wardle et al. 2004a, diversity for litter decomposition.
Viketoft et al. 2005), and is often complicated
because plant and microbial communities
9.5 Synthesis
operate at different time-scales (Korthals et al.
2001, Hedlund et al. 2003) and there are complex The experiments to date that have assembled
interactions among soil microbial species (Milcu microbial communities in microcosms point toward
et al. 2006). a positive relationship between diversity and eco-
Influences of soil microbial diversity on plant system functioning in most cases, although this
performance or plant communities have been outcome is by no means universal. While much
rarely examined, mostly owing to the difficulty of more research is required before firm conclusions
manipulating soil microbial diversity. Selectively can be drawn, the positive relationships observed
excluding part of the soil microbial community primarily in microcosm experiments appear to be
requires severe manipulations (e.g. via fumigation, driven by a variety of mechanisms, including
see above) before an effect on ecosystem processes complementary resource use and selection effects.
can be observed (Bonkowski and Roy 2005). There As with studies involving larger organisms, how-
have been some initiatives, such as Bradford et al. ever, the task of identifying causal mechanisms is
(2002), who manipulated size classes of soil only just beginning.
organisms and concluded that effects of While the experiments reviewed above have
soil organisms from different size classes on plant demonstrated that there is potential for positive
productivity and plant community composition biodiversity-ecosystem functioning relationships
are relatively minor and that effects of larger in microbial communities, they have not shown
organisms supersede those of the smaller organ- whether such a relationship is common in species-
isms (Bradford et al. 2002). rich natural communities. In contrast with the
Results from studies that have included soil results of manipulative microcosm experiments,
microbes and soil invertebrates indicate that soil non-manipulative surveys (which compare mea-
microbial effects on plant community performance sures of ecosystem functioning associated with
may be overruled by effects of the invertebrates natural variation in microbial communities) and
(Bonkowski et al. 2001, Bradford et al. 2002, Bezemer experiments (in which natural microbial commu-
et al. 2005, Wurst et al. 2008). Overall, the effects of nities are manipulated) have found inconsistent
the decomposer community appear to depend more effects of diversity on ecosystem functioning.
on community composition and relative species This raises the principal question in microbial
132 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

biodiversity-ecosystem functioning studies of why respiration) scaled with the logarithm of bacterial
apparent discrepancies exist between these two species richness. Consequently, the addition of the
approaches. first 100 species to the community is expected
There are real difficulties in attempting to bring to increase the level of community respiration by
together the two lines of enquiry that assemble 200 per cent, whereas adding an additional 100
species from their constituent species versus species would increase respiration rate by < 10 per
experiments or observations using natural com- cent. Thus, extrapolating curves from microcosm
munities. Currently unculturable bacteria cannot be experiments such as those by Bell et al. (2005b)
directly manipulated, making it impossible in would predict that even very large reductions in the
practice to conduct well-designed manipulative diversity of natural communities have negligible
biodiversity experiments with truly natural micro- effects on ecosystem functioning.
bial communities. Even though the ability to A second possibility is that those species that
describe the diversity of these communities is rap- can be cultured may be poorly representative of
idly increasing as new DNA sequencing technolo- the larger community, in which case we should
gies are becoming widespread, the approach with not expect the results of manipulative experiments
natural communities will remain comparative to apply to microbial communities as a whole even
unless new means are devised to manipulate if their diversity were as low as in the experiments.
microbial species directly without the need for While it is certainly the case that libraries of cul-
culturing. Such comparative studies can give clues tivable microbes are unrepresentative of the larger
to causal mechanisms, but they inevitably suffer community, and also that only an extremely small
from the fundamental problem of relating cause portion of the total microbial diversity has been
and effect in an unambiguous manner. Even if it studied in this manner, biodiversity-ecosystem
were possible to manipulate natural communities functioning experiments have now been con-
directly, attempting to manipulate communities ducted with an array of cultivable organisms. In
with thousands of species poses enormous practical addition, it might be important to bear in mind
challenges because of the exorbitant number of that there is a flip-side to the ‘cultivability’ debate,
possible species combinations. which is that culture-independent techniques
There are a number of possible reasons as to why might be picking up primarily metabolically inac-
discrepancies commonly occur between small-scale tive cells. Depending on how community mem-
manipulations of species-poor cultivable commu- bership is defined, these inactive cells might not be
nities and large-scale observations of natural community members of interest in the context of
microbial communities. Perhaps the most obvious assessing effects on ecosystem functioning. If
possibility is that the two approaches focus on indeed diversity in field experiments is mostly
different parts of the same relationship. Manipula- reduced by affecting species in a resting state, it
tive experiments with assembled communities would not be surprising that even large declines in
consider levels of species richness from 100 to at diversity fail to curtail ecosystem functioning, at
most 102 species, whereas field manipulations least at a gross level and in the short-term scales.
reduce levels of diversity from much greater than Evidently, metabolically inactive cells might play a
102 down to 102 species (Wertz et al. 2006), and key role in fluctuating or shifting environmental
observational studies are comparing communities conditions, but it is unclear to what extent inactive
with > 103 species (Fig. 9.2). Since microbial studies cells become metabolically active. Thus, the ques-
have typically found a saturating relationship tion of how microbial diversity is measured or
between diversity and ecosystem functioning, even defined remains pivotal to discussions about the
large reductions of diversity in species-rich com- effects of microbial biodiversity on ecosystem
munities are expected to have little effect on eco- functioning.
system functioning. For example, Bell et al. (2005b) A third possible reason is that while microcosm
found that a generic measure of ecosystem func- studies favour fast-growing r-strategists, experi-
tioning brought about by bacteria (community mental manipulations of natural microbial
 MICROBIAL BIODIVERSITY AND ECOSYSTEM FUNCTIONING 133

communities are likely to eliminate preferentially phylogenies and taxonomies that remain beyond our
rare species. Even when rare species have the ability to resolve, and exhibit lateral gene transfer
potential to play a significant role they are least that is almost unheard of elsewhere in nature.
likely to contribute notably to ecosystem function- Nevertheless, it appears that many of the patterns of
ing (compared to common species) due simply to diversity in microbial communities are broadly
their rarity. Therefore, to some extent such experi- similar to those of larger organisms (Green et al.
mental manipulations may lead to conservative 2004, Horner-Devine et al. 2004, Bell et al. 2005a,
estimates of microbial diversity effects on ecosys- Fuhrman et al. 2006, Martiny et al. 2006).
tem functioning. Establishing the generality of this conclusion
Advances in molecular techniques have revealed in relation to microbial biodiversity-ecosystem
that there are many similarities in the community functioning research is imperative. There is a
ecology of microbes and larger organisms, suggest- great deal of excitement that findings in microbial
ing that there might also be similarities in the rela- biodiversity-ecosystem functioning research can
tionship between diversity and ecosystem produce both considerable academic advances
functioning. These technological advances have not in understanding how ecosystems operate, and
only increased our ability to do experiments, but practical advances in harnessing microbial com-
also to survey the microbial wilderness the way we munities or preventing microbial disease. How-
have explored wild communities of larger organisms ever, the inconsistencies between the various
for centuries. Currently, several studies have approaches that we highlight in the current review
revealed that prokaryotes have been on Earth bil- underline the real need for a better understanding
lions of years before eukaryotes and multicellular of the causes and consequences of changing
organisms, that microbes constitute enormous bio- microbial biodiversity before the potential of
mass, exhibit unique and extraordinarily varied microbial biodiversity-ecosystem functioning
biochemistry that drives biogeochemistry, have studies can be fully realized.
 CHAPTER 10

Biodiversity as spatial insurance: the

effects of habitat fragmentation and
dispersal on ecosystem functioning
Andrew Gonzalez, Nicolas Mouquet, and Michel Loreau

10.1 Introduction
community processes, such as biomass production
Anthropogenic habitat destruction (e.g. strip min- and nutrient uptake (Cardinale et al. 2007),
ing or clear cutting of forests), conversion to agri- although data from unmanipulated plant commu-
culture (e.g. conversion of grasslands to croplands nities suggest that these effects may be weaker or
or rangelands, or conversion of forests to planta- masked by other covarying factors in the environ-
tions), and fragmentation (e.g. dividing ecosystems ment (Grace et al. 2007, Hector et al. 2007). Overall,
inhabited by native species into parcels that are the beneficial effects of biodiversity in experimental
separated by inhospitable terrain) are generally conditions have been shown to saturate at relatively
considered the dominant drivers of biodiversity low to moderate levels, even when several func-
loss. The loss of inhabitable area is the predominant tions are considered simultaneously (Hector and
cause of population (Hughes et al. 1997) and species Bagchi 2007). The relevance of results from biodi-
extinctions (Pimm et al. 1995). Isolation of fragments versity and ecosystem function experiments, given
of habitat and edge effects associated with such the rapid saturation of biodiversity effects, has
fragmentation can cause further declines in both the questioned their utility as a case for conservation
number of species, changes in their relative abun- biology and has led to calls for a broadening of
dance, and other aspects of biodiversity within empirical and theoretical perspectives within the
remnant habitat patches (e.g. Andrén 1994, Fahrig field (Gonzalez and Chaneton 2002, Srivastava 2003,
2003, Ewers and Didham 2006). Although other Srivastava and Velland 2005, Lawlor et al 2002).
anthropogenic drivers (e.g. climate change, over- Biodiversity effects on ecosystem functioning
exploitation, and the spread of non-indigenous (BEF), though small or sometimes negligible in
species that adversely affect indigenous species) are small-scale studies, may nevertheless be more sig-
growing in importance, it is clear that their impacts nificant at larger spatial and temporal scales (Yachi
will be felt within the context of ongoing habitat and Loreau 1999, Loreau et al. 2003, Cardinale et al.
loss. Indeed, strong synergies between habitat 2004). Typically, experimental BEF studies have
fragmentation and climate change are expected been performed over small spatial and temporal
(Holt 1990, Travis 2003) and will likely compound scales, relative to the size, mean habitat range, and
the loss of biodiversity at local and regional scales. generation times of the organisms involved.
The threat of widespread and rapid loss of bio- Although these limitations are most acutely asso-
diversity across most regions has prompted two ciated with studies of terrestrial plant and tree
decades of research on the impacts of biodiversity communities, experiments with aquatic systems can
loss on ecosystem functioning and services. A also have similar limitations. The results of BEF
number of controlled experiments have established experiments, whether terrestrial or aquatic,
that reduced levels of species diversity can impact although clearly valuable for establishing the effect

134
 BIODIVERSITY AS SPATIAL INSURANCE: THE EFFECTS OF HABITAT FRAGMENTATION 135

of varying local biodiversity, cannot provide a of diversity and ecosystem functioning in remnant
complete understanding of the spatial processes fragments. Second, we will then show how spatial
affecting the relationship between biodiversity and variance in biodiversity can affect estimates
ecosystem functioning at landscape (e.g. more of regional functioning by non-linear averaging
than one ecosystem), regional, or global scales (Benedetti-Cecchi 2005). Finally we will use a
(Gonzalez and Chaneton 2002, Rantalainen et al. 2005, metacommunity framework to formalize the spatial
Srivastava and Velland 2005, Dobson et al. 2006). insurance hypothesis (Loreau et al. 2003). Throughout
The loss of biodiversity in fragmented landscapes we will consider how each of these perspectives
has underscored the importance of viewing com- informs our understanding of the impacts of habitat
munities as ‘open’ structures dependent upon spa- destruction and fragmentation on biodiversity and
tial fluxes from the surrounding communities in the ecosystem functioning and stability. We will con-
region (Kareiva and Wennergren 1995, Leibold et al. clude that our understanding of the relationship
2004). Although the importance of dispersal for the between biodiversity and ecosystem functioning is
maintenance of biodiversity is relatively well substantially altered when we incorporate the spa-
understood (e.g. MacArthur and Wilson 1967, tial processes required to link local and regional
Schmida and Wilson 1985; Loreau and Mouquet scales.
1999, Amarasekare 2004, Holyoak et al. 2005,
Mouquet et al. 2005) its importance to ecosystem
10.2 Fragmentation, species loss
functioning remains relatively unexplored (Kareiva
and functioning debts
and Wennergren 1995). For example, weak flows
of individuals between habitats may have signifi- Habitat destruction is not a uniform process and
cant impacts on population production (Holt and the end result is typically a mosaic of remnant
Loreau 2002, Mouquet et al. 2002, Ives et al. 2004) fragments of habitat containing a subsample of the
and community stability (Huxel and McCann 1998, flora and fauna that occupied the formerly con-
Loreau et al. 2003). From this perspective, a more tinuous habitat (Fahrig 2003, Ewers and Didham
complete understanding of the impacts of biodi- 2006). The loss of habitable area, increased isola-
versity loss on local ecosystem functioning requires tion and increased edge effects associated with
a fuller understanding of dispersal-dependent fragmentation collectively initiate a process of
mechanisms of biodiversity. At the regional, or community disassembly (Diamond 1972), involv-
metacommunity scales, the spatial components of ing declines in both species abundance and
diversity – both spatial variance in diversity among diversity within remnant habitat fragments.
habitats or patches and turnover in composition Community disassembly following habitat frag-
from habitat to habitat or patch to patch – are sig- mentation can be simplified to two processes
nificant determinants of ecosystem functioning at operating at different time-scales: the first a rela-
scales greater than the habitat or patch (Fukami tively rapid sampling of the original diversity as
et al. 2001, Bond and Chase 2002, Gonzalez and habitat is lost and the second a longer-term pro-
Chaneton 2002, Loreau et al. 2003a,b, Cardinale cess of decay or ‘relaxation’ in residual diversity
et al. 2004, Leibold and Norberg 2004). A frame- from the remaining fragments. Ecologists have
work for understanding how spatial processes sought to calculate the extent of future species loss
mediate biodiversity-ecosystem functioning rela- due to habitat destruction and fragmentation, but
tionship is needed to improve our understanding little attention has been paid to estimating the
and ability to predict the ecosystem consequences functional (i.e. biogeochemical or ecosystem pro-
of biodiversity loss at larger scales. cess) effects of community disassembly in frag-
In this chapter we will review several concepts mented landscapes (e.g. Laurence et al. 1997,
that allow us to link local and regional scales of the Larsen et al. 2005, Rantalainen et al. 2005)
biodiversity and ecosystem functioning relation- Most experiments relating ecosystem function
ship. First we will consider how the species–area to changes in species diversity have so far
relationship can link loss of habitat to delayed loss adopted a ‘static’ approach. Ecosystem variables
136 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

are usually measured across gradients of spatially a new equilibrium in species richness within the
interspersed diversity treatments, consisting of landscape, e.g. Brooks et al. 1999). The method
communities assembled at random from a given involves increasing the exponent (z) of the
species pool (e.g. Tilman et al. 1997; Hector et al. species–area relationship to account for the dis-
1999). Although these designs are useful for proportionate loss of species from small areas of
revealing diversity effects independent of species habitat. If the original habitat area Ao, is reduced to
composition, they might not reveal the ecosystem An, we do not simply expect the original number of
changes that accompany diversity loss in frag- species to decline to Sn, but rather to Sn estimated
mented habitats, where extinction is a non-random with a new higher value of z. Here we use this
process dominated by non-equilibrium dynamics. approach to examine how habitat fragmentation
In particular, the identity of species extinctions will affect local ecosystem functioning.
(e.g. rare versus dominant) and the timing of their Figure 10.1 depicts our conceptual model. We
occurrence may be variable and delayed (e.g. the begin with the familiar species–area relationship,
extinction debt described by Tilman et al. 1994, S ¼ cAz, which describes how diversity S scales
Gonzalez 2000, Vellend et al. 2006). The functional with area A raised to the power z, where z ranges
effects of extinction debts in fragmented land- from about 0.15 for continuous tracts of continental
scapes are unobservable in experiments if they use habitat to about 0.25 for habitat islands. Two
spatially structured gradients of fixed diversity species–area curves can be drawn corresponding to
levels as a surrogate for species loss following ‘before’ and ‘after’ fragmentation. These curves can
fragmentation. be used to estimate how many species there are in a
Delayed losses of diversity due to habitat frag- given area before fragmentation by interpolating
mentation should also generate a functioning debt – along the ‘before’ fragmentation curve (z ¼ 0.15).
i.e. a delayed alteration in ecosystem attributes The eventual loss of species from a fragment
driven by the delayed decline and extirpation of because of isolation (i.e. due to relaxation) can be
species persisting in remnant patches (Gonzalez estimated by switching to the lower, but steeper,
and Chaneton 2002). The possibility that extinction species–area curve (z ¼ 0.25). These changes in
debts may be associated with functioning debts has species richness can then be mapped onto the
received little attention to date. This is in part generally saturating function (Cardinale et al. 2006)
because the static and local approach of current describing the relationship between species richness
experimental protocols precludes the study of these and ecosystem functioning (e.g. productivity) to
dynamic aspects of diversity loss. Although recent produce estimates of Df, the delayed change in
studies have addressed the problem of species loss ecosystem functioning in a fragment due to the
as a non-random process through theoretical (Ives delayed species loss. This approach predicts that
and Cardinale 2005) and statistical means (Solan the smaller the fragment, the larger the reduction in
et al. 2004) they have not the addressed the more ecosystem functioning (functioning debt) due to
complex dynamical issues arising from habitat delayed species loss (Fig. 10.1).
fragmentation (Fahrig 2003). Extinction debts are Few data exist to test the validity of this
threshold phenomena (Ovaskainen and Hanski approach for natural landscapes. A good starting
2002) that arise because species persistence depends point would be to use data from experimental
upon the spatial configuration of the landscape; model systems (e.g. Wardle et al. 2003b). Gonzalez
fragmentation affects landscape connectivity that and Chaneton (2002) noted the existence of a
alters local and regional colonization and extinction functioning debt following the delayed loss of
rates. The challenge now is to understand how this species in experimental fragments of a bryophyte-
phenomenon of diversity loss affects ecosystem based microecosystem, but they did not try to
functioning. predict the extent of the functioning debt from the
For a long time the species–area relationship has observed species loss. Although it may take con-
been used to estimate the extent of species loss due siderable time for local extinction to occur, certainly
to destruction and relaxation (the slow approach to experiments could be conducted in a grassland
 BIODIVERSITY AS SPATIAL INSURANCE: THE EFFECTS OF HABITAT FRAGMENTATION 137

Before fragmentation After fragmentation

z = 0.15

Species richness
Frag2 before
z = 0.25
Frag2 after
Frag1 before

Frag1 after

Atotal Afrag2 Afrag1 ∆f1 ∆f2

Area Function

Figure 10.1 Predicting the delayed effects of habitat loss and isolation on local ecosystem functioning. The upper panel shows two fragments of differing
area before and after habitat destruction (habitat is represented in grey). The lower left graph shows the two species–area relationships corresponding to
before (z ¼ 0.15) and after (z ¼ 0.25) fragment isolation. The lower right graph shows a typical relationship between species richness and ecosystem
functioning. The loss of species richness due to isolation is predicted by the increase in the slope of the species–area relation. This change in species richness
due to isolation and community disassembly (frag 1 or 2 before) can be mapped onto the species richness-functioning relation (frag 1 or 2 after) to estimate
the delayed change in function (Df, the functioning debt).

setting to estimate the functional impacts of com- loss due to habitat destruction should involve the
munity isolation from the surrounding landscape top-down collapse of food webs (Holt et al.
(e.g. Robinson et al. 1992). Experiments in tractable 1999). Although the evidence for this is equivocal
systems, such as microbial microcosms, would be (Mikkelson 1994, Holyoak 2000, Gonzalez and
able to evaluate the different effects of fragmenta- Chaneton 2002, Rantalainen et al. 2005), the func-
tion (e.g. isolation, edge effects, loss of area), and tional consequences of such trophic collapse are
directly address how these causes of local extinction likely to be great (e.g. Duffy 2003, Rantalainen et al.
affect ecosystem functioning, although the labora- 2005, Rooney et al. 2006). Habitat destruction and
tory context of microcosms often limits their utility fragmentation are the major causes of species loss
for predicting phenomena in larger, more complex, in terrestrial ecosystems and more work is needed
less environmentally controlled ecosystems like to establish how it affects ecosystem functioning
grasslands or forests. (Kareiva and Wennergren 1995).
Others have recently pointed out the utility of the
species–area relationship to address other impacts
10.3 Spatial variance of biodiversity
of area loss on ecosystem functioning (Tilman
in fragmented landscapes
1999a, Naelsund and Norberg 2006, Dobson et al.
2006), but have not used the approach to estimate We noted that habitat fragmentation creates land-
the functional impacts of extinction debts. Dobson scapes with many remnant fragments of variable
et al. (2006) pointed out that some functional groups size and species richness (Fahrig 2003). In the pre-
(e.g. body size) and higher trophic levels are vious section we raised the problem of estimating
expected to have greater values for the exponent z, the longer-term functional impacts of species loss
and thus differential sensitivity to area loss. An within a given fragment. Here we address the
important consequence of this is that species problem of estimating the mean change in
138 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

functioning across a set of fragments of variable sponds to the low end of Benedetti-Cecchi’s (2005)
size and species richness. range. This is due in part because our use of the
Within fragmented landscapes distributions of species–area relationship constrains the range of
fragment size are often skewed with relatively few variation in species richness across fragments.
large patches distributed within a network of a However, Benedetti-Cecchi (2005) also used a larger
large number of small patches (e.g. Keitt et al. 1997). range of variation (spatial variance) in species
This variation in fragment area translates into spa- richness that may not be entirely realistic at the
tial variation in species diversity that may be scale of local communities (Crawley and Harral
exacerbated by a mix of deterministic and stochastic 2001).
patterns of extinction and colonization across frag- Our example raises empirical issues that merit
ments (Wright et al. 2007). What are the con- further study. We assumed that the form of the BEF
sequences of spatial variance in diversity from function is constant across the region of interest and
fragment to fragment for estimating the change in thus the same function can be used to map diversity
mean ecosystem functioning at the landscape level? to function for any given community. Although this
The answer involves spatial averaging. Benedetti- assumption probably breaks down across larger
Cecchi (2005) recently pointed out that spatial var- regions (e.g. Hector et al. 1999) we know remark-
iation in local diversity could significantly reduce ably little about spatial variation in BEF relation-
estimates of mean ecosystem functioning in a ships at regional scales. We also assumed that the
fragmented landscape if the non-linear relationship species–area relationship could be used as a first
between biodiversity and ecosystem functioning approximation to map the distribution of fragment
was not taken in account. This reasoning is based size to the spatial variance in biodiversity. The
on Jensen’s inequality (Jensen 1906, Ruel and Ayres general nature of non-linear averaging and the
1999), the well known property that the expected potential for large changes in spatial variation in
value of a concave down function typical of biodi- diversity in disturbed landscapes suggest that this
versity-functioning relationships, is lower than the effect is likely to be sufficiently great that future
function of the expected value: E(f (X)) < f (E(X)). studies should estimate it. Finally, we note that
Thus spatial variation in diversity (between com- similar arguments can be made when estimating
munities) would, as a result of non-linear averaging variation in mean ecosystem functioning when
across patches, produce lower than expected levels species diversity varies through time (Ruel and
of ecosystem functioning. Drawing upon data Ayres 1999), as it will in any fragmented landscape
from recent terrestrial plant experiments Benedetti- undergoing relaxation (Brooks et al. 1999, Gonzalez
Cecchi (2005) found that, depending on the level of 2002).
variance he assumed around the mean, Jensen’s
inequality could result in a 5–45% reduction in
10.4 Linking local to regional: the
biomass production when compared to the case
spatial insurance hypothesis
where spatial homogeneity in diversity was
assumed. Although the range of this effect is large, In the previous sections we have ignored dispersal
it has generally been statistically significant. and its role in driving spatial patterns of diversity
Few biodiversity-functioning experiments have and ecosystem process. The loss of biodiversity in
been conducted at the appropriate spatial scale to fragmented landscapes forces a perspective that
verify the importance of community-to-community communities are ‘open’ structures dependent upon
variation in diversity due to non-linear averaging. dispersal from the surrounding communities in the
In Fig. 10.2 we provide an example of how Jensen’s region (Kareiva and Wennergren 1995, Tilman and
inequality may lower the estimate of mean com- Kareiva 1997, Leibold et al. 2004). However, the
munity production in landscapes with different way in which dispersal mediates the effects of
distributions of habitat fragment size. Although we diversity on ecosystem functioning has only
obtain a reduction in mean functioning due to recently been investigated theoretically (Holt and
Jensen’s inequality, the effect is modest and corre- Loreau 2002, Mouquet and Loreau 2002, Loreau
 BIODIVERSITY AS SPATIAL INSURANCE: THE EFFECTS OF HABITAT FRAGMENTATION 139

20

15

Function
10

0
Constant 0 10 20
Species richness

20 18

15 17 0.77% 5%
Function

Biomass
10 16

5
15

0
Normal 14
0 10 20
Constant Normal Exp.
Species richness
20

15
Function

10

Exponential 0
0 10 20
Species richness

(a) Fragmented (b) BDEF function (c) Jensen’s inequality

landscapes

Figure 10.2 Spatial variation in species richness due to variation in fragment area across three different landscapes demonstrates the effect of Jensen’s
inequality. To calculate Jensens’s inequality we assumed a nonlinear biodiversity-functioning relationship (a) of the form aS/(S þ b) where S ¼ species
richness, a ¼ 20, and b ¼ 2. We then generated three types of landscape of 30 fragments each with equal total fragment area. In the first landscape every
fragment has a constant area (A ¼ 5 units), in the second each fragment area was drawn from a normal distribution (l ¼ 5, r ¼ 2), and in the third the
fragment area was drawn from an exponential distribution (l ¼ 5). The fragments drawn here are for illustration only and are not to scale. We used the
species–area relationship (S ¼ cAz, where z ¼ 0.3) to generate species richness for each fragment in the three landscapes. Here we assume that the
extinction debt has been paid and that z is at its equilibrium. (b) Values of species richness were then used to generate values for ecosystem function for each
fragment (black dot for each fragment). We then compared mean biomass production per fragment (± 95% CI generated by Monte Carlo randomization,
1,000 iterations) for each landscape (c). The difference between the three landscapes defines the level of Jensen’s inequality.

et al. 2003a and Loreau et al. 2003b, Mouquet mediates the effects of diversity of ecosystem
and Loreau 2003, Cardinale et al. 2004, Leibold and functioning both directly and indirectly, an
Norberg 2004) and experimentally (Gonzalez and effect we have called the spatial insurance hypothesis
Chaneton 2002, Matthiesen and Hillebrand 2005, (Loreau et al. 2003a).
France and Duffy 2006b, Venail et al. 2008). The spatial insurance hypothesis is based on
We recently formalized the idea that dispersal two mechanisms: (1) compensatory fluctuations
140 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

between species (or functional groups) in the resource) in any given local community at differ-
presence of spatio-temporal environmental het- ent times. All species are assumed to be identical
erogeneity, and (2) dispersal-driven spatial aver- in all other aspects of their ecology (e.g. equal
aging of environmental heterogeneity. Under the death and dispersal rates). Coexistence is not
first mechanism dispersal maintains biodiversity, driven by temporal variation (i.e. resource parti-
which buffers ecosystem functioning against tioning through time) but is dependent on a spatial
environmental fluctuations because functional storage effect (Snyder and Chesson 2004), whereby
compensations among species (or phenotypes) dispersal allows species to persist by tracking
provide enhanced and more predictable aggregate spatio-temporal variation in environmental qual-
ecosystem properties. Under the second mecha- ity. In the absence of dispersal resource competi-
nism dispersal directly buffers growth rates and tion ensures that only a single species will persist
inflates mean biomass production. This effect is with variable abundance in each community. Thus
based on the well-known principle that in the dispersal ensures local coexistence and environ-
presence of dispersal, spatial variability in popu- mental niche partitioning ensures regional coexis-
lation growth averages arithmetically whilst in the tence (Mouquet and Loreau 2002).
absence of dispersal variability in growth averages The equations governing the metacommunity
geometrically (e.g. Ives et al. 2004). In general, the read:
arithmetic mean will be greater than the geometric
mean and this will translate into greater mean
population biomass in the presence of dispersal. dNij ðtÞ
¼ ½eij cij ðtÞRj ðtÞ  mij Nij ðtÞ
The extent to which spatial averaging due to dis- dt
a X M
persal translates into greater mean biomass will þ Nik ðtÞ  aNij ðtÞ
M  1 k6¼j
depend upon the extent of the increase in popu-
lation growth rate and the strength of density dRj ðtÞ X
S
¼ Ij  lj Rj ðtÞ  Rj ðtÞ cij ðtÞNij ðtÞ
dependence (Ives et al. 2004). Previous theoretical dt i
results suggest that the relationship between dis-
persal and mean biomass is unimodal with a peak Nij(t) is the biomass of species i (e.g. a plant) and
at low to intermediate rates of dispersal (Holt Rj(t) is the amount of limiting resource (e.g. a
1993, Holt et al. 2005). nutrient such as nitrogen) in community j at time t.
The metacommunity consists of M communities and
S species in total. Species i consumes the resource at
10.4.1 A source–sink metacommunity model:
a rate cij(t), converts it into new biomass with effi-
‘contemporaneous disequilibrium’
ciency eij, and dies at rate mij in community j. We
We reanalyze the source–sink metacommunity assume that the resource is renewed locally through
model of Loreau et al. (2003) with more species and a constant input flux Ij, and is lost at a rate lj. Species
by varying the input of nutrients within the disperse at a rate a, dispersal is global, and propa-
metacommunity. We begin with a fragmented gules are redistributed uniformly across the land-
(patchy) landscape composed of a number of scape but do not return from the community they
communities each experiencing variation in habi- come from. We further assume that the consump-
tat quality (e.g. fluctuating temperature). We tion rates cij(t) reflect the match between species
assume that each community experiences sinusoi- traits and local environmental conditions as in
dal variation in the environment which varies out- Mouquet et al. (2002). Let the constant trait value of
of-phase across communities. We assume a set of species i be Hi, which may be interpreted as its niche
species competing for a single resource and that optimum along an environmental gradient, and the
species show dissimilar responses to the environ- fluctuating environmental value of community j be
ment. Because they have different environmental Ej(t). We assume that both species traits and envi-
optima each species will be the best competitor ronmental values vary between 0 and 1, and that a
(defined by the rate at which they take up species’ consumption rate is highest when the
 BIODIVERSITY AS SPATIAL INSURANCE: THE EFFECTS OF HABITAT FRAGMENTATION 141

environmental value matches its niche optimum as persal. Temporal mean diversity (local and
measured by its trait value. Specifically, consump- regional) and temporal mean productivity and its
tion rates are given by: coefficient of variation (CV) were calculated over
the last 200,000 iterations.
1:5  jHi  Ej ðtÞj
cij ðtÞ ¼
10
10.4.2 Metacommunity dynamics
Ecosystem productivity at time t is the production The dynamics of the metacommunity are strongly
of new biomass per unit time, average meta- dependent upon the rate of dispersal. Dispersal
community productivity is thus: permits local coexistence. Increasing dispersal, and
resource input increases the level at which diversity
P
S P
M
is maintained both locally and regionally (Figs. 10.3
eij cij ðtÞRj ðtÞNij ðtÞ
i¼1 j¼1 (a) and (b)). Local diversity attains a maximum
UðtÞ ¼ value of seven species for a ¼ 0.07, whilst regional
M
diversity declines to a minimum for a ¼ 0.004 and
Here we study a metacommunity made up of 20 then returns to its maximum for a ¼ 0.1. For values
communities. Because various community proper- of dispersal greater than 0.1, local and regional
ties (e.g. local and regional diversity and stability) diversity declines linearly. Species best adapted to
are known to vary with rate of resource input we the average environmental conditions at the meta-
also examined the effect of varying the rate of community scale now prevail; recall that because
resource input (system fertility) on metacommunity the environment varies out of phase across the
production and stability. In our simulations, metacommunity the average condition is E ¼ 0.5 to
we considered the following parameters: eij ¼ 0.2; which intermediate species are best adapted. Spe-
mij ¼ 0.2; Ij ¼ (110 or 165); ‘j ¼ 10;. Environmental cies adapted to the extremes of environmental
fluctuations follow a sinusoid with period T: variation contribute progressively less to commu-
nity productivity and eventually go extinct locally
   
1 2pt and regionally. Local and regional diversity are
Ej ðtÞ ¼ sin Einitj þ þ1
2 T now at their lowest levels and the metacommunity
has now been reduced to a metapopulation of a
In contrast to our previous analysis (Loreau et al. single species. Overall, increasing dispersal has
2003) we do not force the initial environmental strongly non-linear effects on the diversity of the
conditions in each community so that each species source–sink metacommunity. Although diversity is
is the best competitor in a different community: the causally dependent upon the rate of dispersal in
Einitj were chosen randomly from a uniform dis- this metacommunity it is useful to study the change
tribution between ± 2p resulting in Ej(0) being in local and regional dynamics as a function of
random between 0 and 1. This more realistic variation in species richness and as a function of
assumption results in fewer species having source dispersal rate.
communities, and demonstrates the robustness of
our results to variation in initial conditions. We
10.4.3 Metacommunity productivity
started the simulation with 20 species (H1 ¼ 1 and
Hi ¼ Hi1  1/20 for i ¼ 2 to 20). Simulations at Mean temporal productivity (the rate of biomass
each dispersal value were repeated 50 times with production per unit time averaged over the last
different initial environmental conditions and 200,000 iterations) was affected by dispersal and
results were averaged over the 50 repetitions. Each attained its lowest level when dispersal was absent.
simulation lasted 800,000 iterations (Euler approxi- Increasing dispersal resulted in a unimodal
mation with Dt ¼ 0.08) with the period T chosen to response in mean ecosystem productivity that
be large enough (T ¼ 40,000) so that there was peaked at dispersal rates of 0.01 (Fig. 10.3(c)). The
rapid competitive exclusion in the absence of dis- position of this peak was not affected by the rate of
142 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

(a) 16 (b) 16

Regional diversity
12 12

Local diversity
8 8

4 4

0 0
0.0001 0.001 0.01 0.1 1 0.0001 0.001 0.01 0.1 1

(c) 20 (d) 0.5

CV of mean productivity
16 0.4
Mean productivity

0.3
12
0.2
8
0.1
4 0

0 –0.1
0.0001 0.001 0.01 0.1 1 0.0001 0.001 0.01 0.1 1
Dispersal rate Dispersal rate
(e) 20 (f) 0.5
CV of mean productivity

16 0.4
Mean productivity

0.3
12
0.2
8
0.1
4
0

0 –0.1
0.2 2 20 0.2 2 20
Local diversity Local diversity

Figure 10.3 Mean regional (gamma) diversity (a), mean local (alpha) diversity (b), mean temporal productivity (c), and the mean temporal CV of mean
productivity as a function of dispersal rate averaged over 50 simulations. Mean ecosystem productivity (e) and the mean temporal CV of mean productivity (f)
as a function of dispersal rate. Variation between simulations is shown with standard error (a, b, c) and standard deviation (d). The symbols in each plot
indicate different rates of resource input: filled circles I ¼ 110; empty circles I ¼ 165. All other parameter values are given in the text.

resource input, although average productivity diversity-ecosystem functioning experiments.

increased significantly with increasing resource Increasing resource flow did not greatly alter the
input, both in the presence and absence of dis- form of the richness–productivity relation; for a
persal. When productivity was plotted against local given level of species richness local productivity
species richness (Fig. 10.3(e)) we obtained an was increased roughly two-fold.
increasing log-linear function that resembles the Increasing dispersal also enhances the produc-
concave down relationship observed in many bio- tivity of each species directly through the
 BIODIVERSITY AS SPATIAL INSURANCE: THE EFFECTS OF HABITAT FRAGMENTATION 143

60 Figure 10.4 Example of how spatial averaging produces

species-specific biomass peaks at different dispersal rates.
We have averaged individual species biomasses over the last
50
250,000 time steps within a single community. We give
values for different dispersal rates (each species is repre-
40 sented by a different grey line). Each species has a distinct
Species biomass

mode, indicating the rate of dispersal at which each is most

productive within this particular community. Parameter
30
values are given in the text with I ¼ 140.

20

10

0
0 0.001 0.002 0.004 0.01 0.02 0.04 0.1 0.2 0.4 1
Dispersal rate

phenomenon of spatial averaging. The effect of This insurance effect of diversity is obtained at low
dispersal rate on productivity can be seen for levels of dispersal that maximize diversity. As
all species in Fig. 10.4. The figure shows species- above, spatial averaging also contributes to eco-
specific responses to increasing dispersal whereby system stability by enhancing mean productivity
the level of dispersal that maximizes mean pro- (the denominator in the CV). However, low dis-
ductivity due to spatial averaging differs among persal is not great enough to synchronize biomass
species. growth across the metacommunity and eliminate
compensation. This contrasts with the dynamics at
high levels of dispersal (a ¼ 0.4) where the domi-
10.4.4 Metacommunity stability
nant species is strongly synchronized across the
We summarized the stability of ecosystem pro- community and spatial averaging dampens bio-
ductivity with the coefficient of variation (CV ¼ mass fluctuations.
standard deviation/mean, e.g. Tilman 1999a,
Hughes and Ives 2002). As local species richness 10.4.5 Discussion
increases the CV declines non-linearly (Fig. 10.3(f)).
Increasing resource flow rate enhances this stabi- The results of our metacommunity model reveal the
lizing effect of species richness (Fig. 10.3(f)). The CV importance of dispersal as a key process affecting
shows a very different relation with increasing the structure and function of patchy or fragmented
dispersal rate (Fig. 10.3(d)). Here we see an inverse landscapes. Two types of insurance effect were
unimodal relationship with the minimum CV observed: an increase in the temporal mean of
obtained for intermediate dispersal (a ¼ 0.02–0.1). ecosystem productivity within and between com-
Ecosystem productivity is strongly stabilized by munities, and a decrease in temporal variability.
dispersal and is very stable at intermediate levels of Dispersal rate mediates the strength of these
dispersal. Stability is still greater at high rates of insurance effects and links the diversity and func-
dispersal than at very low rates, and this is again tioning of communities from local to regional
due to spatial averaging. Increasing resource flow scales. Importantly our model allowed us to quan-
further improves stability and reduces the CV tify and compare the indirect and direct roles of
across all levels of dispersal, but especially at the dispersal underlying the spatial insurance hypoth-
lowest rates. esis: (1) dispersal indirectly affects the insurance
Stability arises because of compensatory species effects of diversity by maintaining diversity in
dynamics within local communities (not shown). heterogeneous environments, and this effect is
144 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

complemented by (2) the direct functional effects of to the environment will reduce the insurance effects
dispersal due to spatial averaging. Furthermore, we show here (Ives et al. 1999). Although increasing
increasing the rate of resource flow enhances these interspecific synchrony will decrease the insurance
effects. The relative importance of these two pro- effects evident in our model, it will conversely
cesses in fragmented landscapes will depend upon increase the species diversity necessary to generate
the type of coexistence mechanisms (dispersal- the same level of insurance. Thus in spatially het-
dependent or independent) and the degree of spa- erogeneous landscapes more species will be
tio-temporal heterogeneity and connectivity in required to achieve the same level of buffering as
the metacommunity. The assumptions of our environmental fluctuations become more phase-
source–sink metacommunity model are such that synchronized among communities.
both effects of dispersal are important; we now Compensatory fluctuations in total community
discuss each in turn. biomass also occurred in space across the meta-
community. Total metacommunity biomass was
10.4.5.1 Diversity as insurance thus buffered by the out-of-phase variation in
Biodiversity can buffer ecosystem productivity patch-to-patch community biomass. The propaga-
against strong environmental variation as long as tion of this spatial insurance effect to the meta-
species with an appropriate environmental trait is community level arose because of our assumption
present and able to grow under the prevailing that the environment varied out-of-phase across
environmental state (recently called ‘response local communities. Increasing the spatial autocor-
diversity’ Elmqvist et al. 2003). Environmental relation in the environmental conditions will
niches of this type have been studied before in a diminish phase difference amongst patches. At this
single patch case and are thought to be a common scale phase synchrony will increase the number of
mechanism by which diversity may buffer function patches required to achieve the same level of spatial
over long time-scales (Chesson et al. 2002, Lehman insurance; two patches that fluctuate out-of-phase
and Tilman 2000, Gonzalez and De Feo 2007). are sufficient to strongly buffer productivity,
When associated with dispersal and asynchronous whereas a greater number of patches are required
environmental variation across communities, envi- to generate the same effect as communities become
ronmental niches can provide a robust mechanism increasingly in phase across the metacommunity. In
for long-term species coexistence (e.g. a spatial general spatial autocorrelation decays with distance
storage effect, Chesson 2000). (Koenig 1999). The rate at which spatial autocorre-
The increase in the mean productivity with spe- lation decays with distance will determine the
cies richness in our metacommunity model stem- number of patches and the inter-patch distance
med from the compensatory dynamics between required to maximize phase asynchrony, and ulti-
species through time. Longer-term studies of mately, the scale at which spatial insurance effects
diversity and productivity in grasslands have are most pronounced. Spatially explicit versions of
revealed the importance of compensatory dynamics our model will be needed to address these impor-
for the function and stability of grasslands tant issues.
(McNaughton 1985, Dodd et al. 1994, Bai et al. 2004).
In our model the functional species trait (rate of 10.4.5.2 Dispersal and spatial averaging
nutrient uptake) was linked to the environment Decreasing the rate of dispersal in the meta-
state. Because we assumed that species were evenly community has a significant direct effect on the
separated along the temporal environmental gra- mean and variability of ecosystem productivity and
dient, fluctuations in the environment altered the biomass. This direct effect of dispersal occurs inde-
relative competitive ability of each species, which pendently of diversity and has been shown for single
drove the strong compensatory dynamics we species metapopulation models (Holt 1993, Ives et al.
observed. Any environmental factor (biotic or abi- 2004, Holt et al. 2005, Matthews and Gonzalez 2007).
otic) that imposes a shared source of mortality and From these previous results the expected relation-
disrupts phase synchrony in interspecific responses ship between dispersal rate and mean biomass is
 BIODIVERSITY AS SPATIAL INSURANCE: THE EFFECTS OF HABITAT FRAGMENTATION 145

unimodal with a peak at low to intermediate rates of saturating, concave-down function typical of many
dispersal. We have shown (Fig. 10.4) that this is biodiversity-ecosystem functioning experiments and
indeed the case for most species in the meta- similar to that shown in Fig. 10.3e. No attempt was
community, the exception being the species that made to study the community dynamics in this rela-
dominate the metacommunity at low and high rates tively short-term microcosm experiment.
of dispersal that show a U-shaped relationship Gonzalez and Chaneton (2002) used corridors to
between dispersal rate and mean biomass. Figure sustain dispersal from a large continuous block of
10.4 also reveals differences between species in the habitat to satellites of isolated fragments of moss
level of dispersal that caused a peak in mean inhabited by a diverse community of micro-
abundance; different species tend to contribute to the arthropods. In this experiment secondary produc-
spatial averaging component of the spatial insurance tion of this decomposer community was the
effects as dispersal is increased. Overall, spatial ecosystem function of interest. Local extinction
averaging plays a relatively more important role in occurred in the isolated moss fragments after several
spatial insurance effects as diversity declines at months of delay, but not in those maintained by
higher rates of dispersal (Loreau et al. 2003). dispersal (corridor-sustained rescue effects). Frag-
Although theoretically spatial averaging is well ments unconnected by corridors maintained two-
understood there is relatively little empirical evi- thirds less secondary biomass than those connected
dence. Good evidence for spatial averaging has by corridors. Thus dispersal seemed to buffer the
been found in single-species microcosms (e.g. Ives ecosystem’s capacity for organic matter processing
et al. 2004, Gonzalez and Matthews 2007) and in a in these experimentally fragmented habitats. How-
single multispecies microcosm experiment (Fig. 3 in ever, dispersal rate was not controlled in a manner
Matthiessen and Hillebrand 2006). Clearly, much that could test the range of effects encompassed by
more empirical work is required to establish the the spatial insurance hypothesis.
importance of spatial averaging for the functioning France and Duffy (2006b) created experimental
and stability of fragmented landscapes. seagrass metacommunities in mesocosms and
examined the effect of adding dispersal corridors
10.4.5.3 Empirical tests of the theory on ecosystem functioning and stability. The dis-
Recent years have seen several experiments address persal corridors allowed mobile grazers to move
the effects of dispersal on the relationship between from community to community, and thereby affect
biodiversity and ecosystem functioning (Gonzalez rates of grazing and primary production. Dispersal
and Chaneton 2002, France and Duffy 2006b, Mat- tended to decrease diversity (alpha and beta) and
thiessen and Hillebrand 2006). The results of these increased the temporal variability of local grazer
experiments are broadly consistent with the spatial abundance. Also dispersal tended to reduce spatial
insurance hypothesis although none represents a variability in grazer abundance, and enhanced
precise test of the model we used. grazer impacts on edible algae. Overall, results
Matthiessen and Hillebrand (2006) constructed were considered inconsistent with the spatial
laboratory metacommunities of benthic microalgae. insurance hypothesis, although because the main
They enhanced the rate of dispersal from the experi- outcomes of the model are non-linear the theory
mental ‘regional pool’ (aquaria) into the local com- also predicts destabilizing effects on functioning
munities (open-top, upright plastic tubes in the and stability; unfortunately, dispersal rates were
aquaria) by increasing the frequency at which the not estimated during the experiment and so it is
algae were scraped from the bottom of the aquaria and difficult to assess how they were affected by the
resuspended into the water column. As predicted by presence of corridors. Importantly, there is a clear a
the spatial insurance hypothesis they found unimodal mismatch between the assumptions of the theory
relationships between dispersal rate and local species that is based on dynamics of competition, and the
richness and biovolume (a measure of primary pro- multitrophic experimental system France and
duction). When they used species richness as the Duffy (2006b) used to test it. Further theory
predictor, variable biomass production showed the examining the diversity and functioning of food
146 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

webs in metacommunities (e.g. Holt and Loreau suggest that changes in landscape connectivity and
2002) is required to understand the results from fertility (resource flow) following anthropogenic
this and other ecosystems with trophic complexity. fragmentation may alter both species diversity and
Although these experiments have tested various ecosystem processes at local and regional scales.
aspects of the spatial insurance hypothesis, none Because of the non-linear effects of dispersal, both
provides a complete test. The model assumes strong increasing and decreasing landscape connectivity
spatio-temporal heterogeneity that has highly can either increase or decrease diversity and the
dynamic affects on the outcome of competition. Under temporal and spatial variability of (meta)ecosystem
these assumptions dispersal has a strongly non-linear processes (Loreau et al. 2003b). The impact of
effect on diversity and ecosystem functioning. Future reduced dispersal will depend upon the initial level
tests of the spatial insurance hypothesis will therefore of landscape connectivity and the dispersal ability
require good experimental control of a number of of the organisms considered. Experiments addres-
factors – metacommunity size, dispersal rate, spatio- sing how scales of resource heterogeneity and dis-
temporal heterogeneity – and the direct measurement persal interact to affect ecosystem diversity and
of local and regional diversity and ecosystem func- stability are needed.
tioning over extended periods of time. Recent work has established an important link
between ecological and economic aspects of the
insurance value of biodiversity (e.g. Armsworth
10.5 Conclusions
and Roughgarden 2003, Baumgärtner 2007, and
This chapter has emphasized the spatial dimension Chapter 18). Biodiversity has insurance value in
of the relationship between biodiversity and eco- economic terms because management decisions
system functioning. All the results we have raised that alter biodiversity can affect the mean and
have broad implications for the conservation and variance of returns associated with an ecosystem
management of fragmented landscapes. First, we good in a variable environment. Thus a risk adverse
considered the link between local and regional resource manager should optimize levels of biodi-
processes using simple rules to scale diversity and versity by, for example, adjusting the area and
function with area. Our results suggest that species connectivity of a nature reserve (Armsworth and
loss due to habitat destruction may have delayed Roughgarden 2003), or sustaining pollinator ser-
impacts on local function (a functioning debt). These vices by maintaining pollinator-preferred habitat.
results complement the idea that area loss will have This insurance value of biodiversity exists in addi-
the greatest functional effects as higher trophic tion to the direct and indirect (use and non-use)
levels suffer higher rates of extinction (Dobson et al. benefits normally associated with biodiversity. The
2006). Spatial processes, just like multitrophic theory outlined in this chapter stresses that
interactions, have the potential to generate complex knowledge of spatial processes across ecosystems
non-linear effects on biodiversity and ecosystem will be essential if we are to understand the effects
functioning. Second, we indicated that spatial var- of fragmentation on the ecological and economic
iance in species richness (perhaps caused by habitat impacts of biodiversity loss.
fragmentation) should be taken into account when
scaling the mean relationship between biodiversity
Acknowledgements
and ecosystem functioning from local to regional
scales. A.G. and M.L. are funded by the National Science
We used a source–sink metacommunity model to Engineering and Research Council of Canada, the
examine various aspects of how spatial and tem- Canada Research Chair Program, and a team grant
poral variability in the environment can be buffered funded by Le Fonds Québécois de la Recherche sur
by diversity. The metacommunity framework is a la Nature et les Technologies. NM is funded by the
valuable way to link local and regional scales. The Programme National EC2CO and ANR Jeune Cheu-
model predicts positive relationships between chenr. The comments and suggestions of S. Naeem
diversity, productivity, and stability. These results and two reviewers improved the manuscript.
PART 3
Ecosystem services and human
wellbeing
This page intentionally left blank
 CHAPTER 11

Incorporating biodiversity in climate

change mitigation initiatives
Sandra Díaz, David A. Wardle, and Andy Hector

11.1 Introduction initiatives to be taken by different countries, the Kyoto

Climate change mitigation through the sequestration Protocol explicitly excludes natural ecosystems
of carbon (C), and the protection of biodiversity have already extant in 1990 as C sinks (http://unfccc.int/
captured the attention of scientists, governmental resource/docs/cop6secpart/l11r01.pdf). This is also
agencies, and the public in general in the past few the case with regard to the Clean Development
years. This is justifiable in view of the formidable Mechanisms (CMD, http://unfccc.int/resource/
challenges posed by them to the long-term sustain- docs/2002/sbsta/misc22a04.pdf; see also Article 12
ability of the Earth’s life support systems (Millen- of the Kyoto Protocol) by which developed countries
nium Ecosystem Assessment 2005b, IPCC 2007). that emit C in excess of agreed-upon limits can obtain
Biodiversity and C sequestration in the bio- C offsets by investing in initiatives to sequester C and
sphere have seldom been considered in an inte- foster sustainable development in less developed
grated way, either by international conventions or countries. Here, only afforestation and reforestation
by the scientific community. Biodiversity considera- qualify as eligible land use initiatives during the first
tions have been taken into account only marginally commitment period of 2008–2012 (http://unfccc.int/
in international initiatives and agreements aimed at kyoto_protocol/items/2830.php).
mitigating the ecological impacts of climate change. There is no mention of biodiversity in the main
The most influential of these initiatives is the Kyoto text of the Kyoto Protocol. The documents emerg-
Protocol to the United Nations Framework Con- ing from several meetings between 2001 and 2008
vention on Climate Change (UNFCCC), which is (Conferences of the Parties to the UNFCCC 7-13,
intended to slow down the human contribution to and meetings of the Subsidiary Body for Scientific
increased atmospheric carbon dioxide concentration and Technological Advice, http://unfccc.int/
(http://unfccc.int/resource/docs/convkp/kpeng. meetings/items/2654.php) represent an advance in
pdf). This protocol was entered into force in February the sense that they incorporate biodiversity con-
2005 and has now been signed and ratified by 183 cerns. For example, the Marrakech (CoP-7), Milan
states. The Kyoto Protocol considers net C seques- (CoP-9) and Buenos Aires (CoP-10) accords, and the
tration in the biosphere as one way to stabilize carbon modalities for implementation of the CDM projects
dioxide levels in the atmosphere, and offers countries (CoP-11) explicitly state that LULUCF (land use,
the opportunity to receive ‘carbon credits’ for land use change, and forestry) and CDM initiatives
enhancing sequestration. According to the definitions must contribute to the conservation of biodiversity
of the Marrakech Accord, climate change mitigation and sustainable use of natural resources, as well as
measures based on biological sequestration of C to the promotion of C sequestration. Following the
include afforestation, reforestation, revegetation, and Montreal meeting (CoP 11), a request was issued to
forest, cropland and grazing land management analyze the inclusion of avoided deforestation
(http://unfccc.int/resource/docs/cop7/13a02.pdf). (Reducing Emissions from Deforestation and Deg-
However, when defining eligible C sequestration radation, or REDD) as part of the UNFCC activities

149
150 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

in developing countries, either as part of the CDM include other components, such as the identity and
next commitment period starting in 2012, or as a abundance of species and functional and structural
separate instrument designed specifically for this traits, in our analysis, since recent syntheses (Díaz
purpose. REDD are now an integral part of the et al. 2005, Hooper et al. 2005, Díaz et al. 2006,
‘Bali Road Map’ (http://unfccc.int/resource/docs/ Chapin et al. 2008) highlight the fact that composi-
2007/cop13/eng/06a01.pdf), which resulted from tion is more important in determining ecosystem
CoP 13. As in the case of the CDMs, the fact that functioning than richness.
the REDD initiatives should be compatible with
the preservation of biodiversity is explicitly
11.2 How can biodiversity affect C
mentioned. These represent important steps for-
sequestration?
ward, but biodiversity is still considered as a
rather general ‘side benefit’ of carbon sequestra- The success of C sequestration initiatives depends
tion initiatives. on how much C can be stored in the long term,
Academic publications (e.g. Kremen et al. 2000, which in turn depends on the net balance between
Noss 2001, Niesten et al. 2002, Niles et al. 2002, C gain and C loss over long periods. It also depends
Schulze et al. 2002, Sanz et al. 2004, Balvanera et al. on how important the C-sequestering ecosystem is
2005, Kremen 2005, Balvanera et al. 2006, Fearnside perceived to be by the local stakeholders and the
2006b, Betts et al. 2008, Field et al. 2008) and society at large, which in turn depends on the
assessment reports aimed to inform international extent to which positive ancillary effects (such as
conventions on the best ways to mitigate the effects preserved or enhanced ecosystem services other
of global change (e.g. Gitay et al. 2002, Díaz et al. than C sequestration) can be obtained from it. This
2003, Díaz et al. 2005, Stern 2006, Fischlin et al. 2007, is because when stakeholders value the potential of
Royal Society 2008) have stressed the importance of an ecosystem to provide drinking water, food,
considering biodiversity, and analyzed the eco- aesthetic enjoyment, protection against natural
nomic, social, and environmental costs and benefits disasters, and other services, they are more likely to
of incorporating biodiversity-related criteria into C protect its integrity, and therefore its C sequestra-
sequestration. However, in our opinion the fact that tion capacity, in the long term.
biodiversity not only has intrinsic value but could In this chapter we summarize the theoretical
also enhance or reduce the effectiveness of C bases and some emerging evidence by which bio-
sequestration actions has not been sufficiently diversity as defined above could influence the
explored. overall success of C sequestration initiatives. We
In this chapter we ask whether forest plant bio- focus on path one of Fig. 11.1, and claim that bio-
diversity, through its effects on ecosystem processes diversity should be explicitly considered in the
and especially on long-term C storage, is likely to design of C sequestration initiatives.
have relevant consequences for the effectiveness of It is common in international negotiations to use
C sequestration. We first consider the theoretical the term ‘C sequestration’ in a loose sense, to refer
background by which this could happen. Then we to the enhancement of both C stocks in and influxes
consider the available evidence. Finally, we make into the biosphere through avoided deforestation,
some recommendations based on this background afforestation, reforestation, revegetation, and forest,
and identify knowledge gaps and future research cropland, and grazing land management. In the
needs. ecological sense, however, C sequestration refers to
We refer to biodiversity as the number, abun- the maintenance or enhancement of C stocks in the
dance and identity of genotypes, populations, spe- biosphere. This is because large influxes can
cies, functional groups and traits, and landscape sometimes be accompanied by large effluxes,
units present in a given ecosystem (Millennium resulting in no net C accumulation. Net C seques-
Ecosystem Assessment 2005b, Díaz et al. 2006). In tration occurs when the size and/or residence time
taking this broad approach, we consider species of C stocks increases, due to a long-term positive
richness as just one component of biodiversity, and balance between an ecosystem’s C gains through
 INCORPORATING BIODIVERSITY IN CLIMATE CHANGE MITIGATION INITIATIVES 151

How much? How fast? How reliably?

Size of C stock Sink capacity Pool persistence
over time
Net balance between Sink strength of Likelihood of C release
C gain and loss plant-soil system back to atmosphere
due to natural and
Ecosystem surface
antropogenic causes
area
2
1 1 1

Ancillary benefits
C Sequestration
in biosphere + Ecosystem
services other
than C
sequestration
Figure 11.1 The success of climate change mitigation
initiatives based on the biological sequestration of C depends
on two main components: path (1), the amount and
persistence of C sequestered in the plant–soil system; and
Climate change mitigation options path (2), the ancillary benefits provided by the C stock to
humans. The positive effect of ancillary benefits is twofold.
On the one hand, humans get extra benefits as well as
Highly unsuccessful Highly successful climate change mitigation, such as regulation of water
quality and quantity, soil fertility protection, traditional
Small, short-lived, Large, long-lived, products, or cultural continuity (‘win-win’ options). On the
highly vulnerable highly reliable other hand, the higher these benefits, the more likely the
C pools C pools local communities are to preserve the C stock, thus
Low ancillary High ancillary increasing its long-term reliability.
benefits benefits

net primary productivity and C losses through eration could be an integral part of the design
heterotrophic respiration and non-respiratory and implementation of policy and management
processes such as fire, harvest, and leakages of actions aimed at enhancing the long-term C
particulate, dissolved, or volatile C compounds sequestration capacity as well as the overall eco-
(Catovsky et al. 2002, Schulze et al. 2002, Chapin system-service value of primary, managed, and
et al. 2005, Schulze 2005). If biodiversity has the planted forests.
potential to affect C gain through productivity, or C
loss through respiration and non-respiratory pro-
11.2.1 C sequestration predictions based
cesses, then it follows that it should influence both
on different theoretical approaches
the gross and the net C sequestration capacity of
ecosystems. In this contribution, we use the term C How could biodiversity affect C sequestration in
sequestration (i.e. C storage) in the ecological sense, primary, managed, or planted forests? At present,
as a positive long-term change in, or maintenance there are three main theories leading to different
of, C stocks. We refer to C influxes into the biotic predictions. These theories are the neutral hypoth-
system as C uptake or C capture. esis, the mass ratio hypothesis, and the niche com-
Different theoretical backgrounds and some plementarity hypothesis. We distinguish the neutral
emerging evidence suggest that different compo- hypothesis from the other two because species
nents of biodiversity (species and genotype com- differences play no role in it. Life history tradeoffs
position, number and spatial arrangement) differ between species underlie both the mass ratio and
in their potential to modify the magnitude, rate, niche complementarity hypotheses, but the first
and long-term permanence of the biosphere’s C proposes that species influence ecosystem func-
stocks and fluxes. Therefore, biodiversity consid- tioning according to their traits and in direct
152 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

proportion to their relative abundance whereas should strongly influence C uptake via net primary
the other also takes species interactions into productivity and C loss via decomposition and
account. disturbance. Fast acquisition of C per unit of leaf
biomass or leaf area and long-term conservation of
standing biomass are not expected to be maximized
11.2.2 The neutral hypothesis
at the same time. This is because, across major taxa
The Unified Neutral Theory of Biodiversity and and biomes, there should be a tradeoff between a
Biogeography (Hubbell 2001) predicts that diver- suite of attributes that promote fast C and mineral
sity can be maintained with random, neutral drift nutrient acquisition and fast decomposition, and
in species abundances so long as the evolution of another suite of attributes that promotes conserva-
new species can balance stochastic extinctions. tion of resources within well-protected tissues and
Within the context of the links between biodiver- slow decomposition (Grime 1979, Hobbie 1992,
sity and C sequestration, the neutral hypothesis Cornelissen et al. 1999, Aerts and Chapin 2000, Díaz
acts as a useful ‘nothing happens’ model. The et al. 2004, Wright et al. 2004). The former, acquisi-
neutral hypothesis assumes that individuals of all tive, suite includes attributes such as leaves that are
species have equal per capita probabilities of nutrient-rich, palatable, and short-lived, and often
recruitment and mortality. On the surface the wood of low density. This suite is more common in
theory may seem to predict that all species are light-demanding early-successional plants that act
equal, but that is only the case for the recruitment as pioneers after disturbance (Coley 1983, Pacala et
and mortality rates, and functional traits are not al. 1996, Cornelissen et al. 1999, Ellis et al. 2000, Ter
explicitly considered. An attempt to reconcile Steege and Hammond 2001, Laurance et al. 2006),
neutral theory with niche theory proposes that and leads to shorter C and nutrient residence time
species achieve equal per capita rates of recruitment in the ecosystem because of their short leaf lifespan
and mortality by different resource allocation tra- and fast litter decomposition rates (DeAngelis 1992,
deoffs (Hubbell 2001: Chapter 10). However, the Hobbie 1992, Aerts 1995, Wardle et al. 2004a). The
relative abundance of species is random with latter, conservative, suite of traits includes leaves
respect to their traits. If C storage is determined by that are nutrient-poor, unpalatable, and long-lived,
the traits of species then under a neutral model, and often dense wood. This suite is more common
the sequestration capacity of forests will vary in late-successional plants, which in forests include
randomly over time along with neutral drift in the mostly disturbance-intolerant species (especially
relative abundances of species. during ecosystem retrogression or decline, Walker
et al. 2001, Wardle et al. 2004b); these species can
increase C storage and mineral nutrient residence
11.2.3 The mass ratio hypothesis
time as a result of their long leaf lifespan and slow
According to the mass ratio hypothesis (Grime litter decomposition rates. As a consequence of the
1998), resource dynamics at any given time in an existence of these suites of strongly associated
ecosystem strongly depend on the structural and attributes, there is a tradeoff at the ecosystem level
functional characteristics of the dominant (i.e. most between short-term C assimilation rate and long-
abundant) primary producers, and ecosystem term C storage. Within forest ecosystems, many
functioning should be strongly affected by their life forest types are successional mosaics where early-
history tradeoffs. Therefore the total C stock of an and late-successional patches coexist as a result of
ecosystem, its sink strength (the rate of change of natural die-off events or, more commonly, small
the stock), and its residence time (the time that C (e.g. tree fall) and large (e.g. forest fires) disturbance
will remain sequestered in the system) should events (Denslow 1987, Crews et al. 1995, Pacala et al.
strongly depend on the functional attributes of the 1996, Richardson et al. 2004). Early-successional and
dominant plants, as well as on climate and soil late-successional patches are dominated by acquis-
nutrients (Fig. 11.2). The traits of the dominants itive and conservative species, respectively, leading
 INCORPORATING BIODIVERSITY IN CLIMATE CHANGE MITIGATION INITIATIVES 153

los
s +
n /C e
i nc
ga
C bala
Cold (boreal, high-altitude) climate
– Temperate climate

Tropical climate

Fertile, productive Infertile, unproductive

ecosystems ecosystems

Plants and litter

Fast-growing, short-lived plants Slow-growing, long-lived plants
High allocation of C to growth High C allocation to secondary compounds
High specific leaf area Low specific leaf area
Short leaf lifespan Long leaf lifespan
High N and low phenolics, lignin and Low N and high phenolics, lignin
structural carbohydrates in litter and structural carbohydrates in litter
Fast C turnover, high or low C stocks Slow C turnover, high or low C stocks

Soil webs and processes

Bacterial-based energy channel Fungal-based energy channel
High density earthworms High density enchytraeid worms
Relatively low density microarthropods High density macro- and microarthropods
High bioturbation of soil Low soil mixing
Rapid decomposition and mineralization Slow decomposition and mineralization
High nutrient supply rates Low nutrient supply rates
Low soil C sequestration High soil C sequestration

Figure 11.2 The traits of plants, especially dominant plants, strongly influence C and mineral nutrient cycling and thus C sequestration capacity in different
ecosystems. Plant traits serve as determinants of the quality and quantity of resources that enter the soil and the key ecological processes in the decomposer
subsystem driven by the soil biota. These linkages between belowground and aboveground systems feed back (dotted line) to the plant community positively
in fertile ecosystems (left) and negatively in infertile ecosystems (right). C sequestration is highest in infertile conditions because decomposition is more
impaired than net primary productivity by infertility and in colder conditions because decomposition is impaired more than net primary productivity by low
temperatures (Derived from Wardle et al. 2004a).

to a differentiation in ecosystem processes between of disturbances such as fire, wind-throw, and epi-
patches of different successional age. We should sodic herbivory, that are major avenues of C loss
note here that while the mass ratio hypothesis from ecosystems (Laurance 2000, Knohl et al. 2002,
describes the dominance of these strategies within Lavorel and Garnier 2002, Chapin 2003, Pausas
patches, the landscape scale diversity between et al. 2004, Gough et al. 2008), and have important
patches represents a form of niche complementarity consequences for the long-term success of C
(see below). sequestration initiatives. As well as this indirect
The structural and physiological traits of the effect through C sequestration capacity, the struc-
dominant plants can also influence the probability tural and phenological attributes of vegetation
154 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

cover over large areas can affect climate directly. is not matched by an increase in the amount of C
Functional traits of the dominants, such as leaf stored in the soil (Fontaine et al. 2004), and may
lifespan, growth form, root depth, and stomatal have important, though largely unrealized, con-
conductance affect albedo, roughness, and evapo- sequences for soil C persistence and hence eco-
transpiration. Through these biophysical feedbacks, system C sequestration. Conversely, increasing
the functional and structural composition of land domination of the plant community by plant spe-
patches can influence climate at the local, regional, cies that are unproductive but contain high
and even trans-regional scale, depending on the amounts of recalcitrant lignin and polyphenol
land area covered by each vegetation type (Chapin compounds in their litter (such as can occur during
et al. 2000a, Chapin et al. 2000b, Thompson et al. ecosystem retrogression) can contribute to greater
2004, Chapin et al. 2005, Betts et al. 2008, Chapin retention of C in the soil even when NPP is
et al. 2008). Recently, Körner (2005) has summarized declining (Wardle et al. 2003a) (Fig. 11.2).
the variety of functional traits in temperate and Tree species (or forest vegetation types) can differ
boreal tree species and their possible ecosystem- markedly in the extent to which they promote
level implications, but a similar exercise has not yet sequestration of soil C (e.g. Jobbagy and Jackson
been carried out for tropical and subtropical eco- 2000, Rhoades et al. 2000, Resh et al. 2002, Matamala
systems. et al. 2003, Russell et al. 2004), in a large part
Ecosystems consist of not just a producer but also because they differ in their effects on the balance
a decomposer subsystem, and C sequestration is between C gain and C loss. For example, N-fixing
determined not just by ecosystem C gain (driven by trees will often accumulate more soil C than non-N-
net primary productivity, or NPP) but also by C fixing trees (Resh et al. 2002). Systems dominated by
loss (driven by decomposition). Thus, whether or slow-growing tree species that produce well-
not C accumulates in soils is driven to a large extent defended leaves (and hence poor litter quality)
by the difference between C input to the soil frequently promote substantial soil C accumulation
(through litterfall, dead root production, and rhi- relative to tree systems dominated by plants that
zosphere release) and C loss from the soil (through grow rapidly and produce litter of high quality
decomposition and respiration). Although decom- (Wardle et al. 2003a). The effectiveness of C
position at local (within-stand) scales is determined sequestration initiatives depend on the magnitude
largely by litter quality (and hence the traits that and accumulation rate of soil C stocks, as well as
drive litter quality), the linkages between above- the persistence of these stocks. Soil organic carbon
ground (producer) and belowground (decomposer) (SOC) can be accumulated in short-lived pools,
communities are often relatively weak (Hooper such as the microbial and labile pools (mean resi-
et al. 2000, Wardle et al. 2004a, Hättenschwiler dence time of < 5 years), and long-lived pools in
2005). Thus decomposition rates need not respond which SOC is protected by association to colloidal
to ecological gradients (e.g. succession, climate, materials and the formation of stable micro-
diversity) in the same direction or to the same aggregates or recalcitrant compounds (mean resi-
extent as does NPP. For example, decomposition is dence time of thousands of years) (Lal 2005); tree
promoted by temperature more than is NPP, lead- species affect both of these pools. Dominant plant
ing to reduced soil C sequestration at higher tem- species have a clear influence on short-lived pools
peratures (Anderson 1991) and decomposition rates through root output and litter, and longer-lived
may decline across successional gradients while pools through their litter quality (Wardle et al.
NPP is increasing, leading to rapid soil C accumu- 2003a), although their capacity to influence longer-
lation (Wardle et al. 2004b). Further, plant species lived pool is not always clear (Lal 2005, Jandl et al.
that produce high-quality litter may induce a 2007). Shallow rooting coniferous species tend to
‘priming effect’ that accelerates the losses of native accumulate SOC in the forest floor, but they will
organic matter in the soil and thus promotes net sometimes accumulate less in deeper layers than
ecosystem C loss (Jenkinson 1971). This may also comparable deciduous trees that often have dee-
explain why in some situations an increase in NPP per, more ramified roots. This is presumably in
 INCORPORATING BIODIVERSITY IN CLIMATE CHANGE MITIGATION INITIATIVES 155

part due to the effective way in which root growth may play an important role as a group, for
and subsequent root death can directly result in example through ecosystem engineering (Jones
incorporation of organic matter inputs beneath the et al. 1994), through keystone species effects (e.g.
soil surface (Jobbagy and Jackson 2000, Trumbore plant species that form mutualisms with nitrogen-
2000, Vesterdal et al. 2002). fixing bacteria, Vitousek and Walker 1989), and
The mass ratio hypothesis does not deny that less through participating in complex indirect interac-
abundant species can sometimes play a major eco- tions (Eviner and Chapin 2003). Non-abundant
system role or face similar life history tradeoffs to species might be important in providing an
those of abundant species (Grime 1998, Eviner and insurance effect (a type of temporal niche com-
Chapin 2003, see below), but puts the emphasis on plementarity) that helps sustain ecosystem func-
the functional composition of local dominants (Nilsson tioning in the long term, particularly in a changing
and Wardle 2005, Wardle and Zackrisson 2005). The environmental context (Walker 1995, Walker et al.
niche complementarity hypothesis, in contrast, high- 1999, Yachi and Loreau 1999). There are few
lights the functional differences between coexisting examples of insurance effects in the literature and
species. These hypotheses are not mutually exclusive, it is therefore still too early for a formal assessment
and both processes can be operating in the same of their strength and occurrence.
system (Loreau and Hector 2001, Fox 2005b, Potvin The role of genetic differences between popula-
and Gotelli 2008). Many of the differences in life tions or genotypes of the same species in natural
history traits reviewed above with regard to the mass ecosystems has been little studied. In the case of
ratio hypothesis may also be relevant to the discus- herbaceous communities, Joshi et al. (2001) found
sion of niche complementarity that follows. that the performance of different genotypes was
always best in the sites from which they were
sourced, and Booth and Grime (2003) reported that
11.2.4 The niche complementarity hypothesis
communities composed of genetically uniform
This hypothesis is based on the idea that a greater populations appear to be more variable in canopy
range of physiological, structural, and phenologi- structure, and to lose more species over time, than
cal traits represented in the local community pro- communities composed of genetically heteroge-
vides opportunities for more efficient resource use neous populations. Reusch et al. (2005) showed
in a spatially or temporally variable environment that genotypic richness of the cosmopolitan sea-
(Trenbath 1974, Vitousek and Hooper 1993, Tilman grass Zostera marina enhanced biomass production
et al. 1997c). This hypothesis is also compatible despite near-lethal water temperatures due to
with the existence of trait tradeoffs, and indeed extreme warming across Europe. Crutsinger et al.
such tradeoffs are the basis for niche differences (2006) showed that increasing population geno-
between species. But here there is less emphasis on typic richness in the old-field herb Solidago altis-
the tradeoffs of the dominants as major drivers of sima determined arthropod diversity and increased
ecosystem properties. When species show com- above-ground net primary productivity. However,
plementary niche differences it is likely – but not it is difficult to know how general these patterns
automatic (Hector 1998, Hector et al. 2002) – that a are, and whether they apply to woody ecosystems.
mixture of species may show greater overall Genetic variability among spatially separated
resource uptake and rates of ecosystem processes populations of the same tree species has been
than the same species grown in monoculture. shown to be an important driver of litter quality
Niche complementarity may relate to resource use, and ecosystem processes such as decomposition,
but mixtures may also perform better if rates of herbivory and nutrient cycling (Treseder and
attack by natural enemies – either pests or patho- Vitousek 2001, Whitham et al. 2003, Schweitzer
gens – are higher in monocultures, in low-diversity et al. 2004, Schweitzer et al. 2005b), but experi-
patches, or near parent trees (e.g. Janzen 1970). mental evidence on the effects of tree intraspecific
Less abundant species are often minor players in genetic richness on ecosystem processes is still
ecosystem resource dynamics (Grime 1998) but lacking (Hughes et al. 2008). Indeed, most of the
156 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

evidence of the positive effects of high species and plants (Laakso and Setälä 1999, Setälä and McLean
genotypic richness comes from the field of sub- 2004, Hättenschwiler et al. 2005).
sistence agriculture and forestry practiced by tra-
ditional peoples (Pretty 1995, Altieri 2004). This
11.2.5 Where does the available
diversity is often lost during the process of selec-
evidence stand and what else do we need
tion for the production of high-yielding varieties.
to know?
Therefore the possibility exists that the loss of
inter- and intra-specific genetic variation could In summary, the predictions of these different
also lead to instability of plantations and other hypotheses for the incorporation of biodiversity in C
managed woody ecosystems in the face of a sequestration initiatives vary markedly. Taken to an
changing environment. extreme, the mass ratio hypothesis predicts that C
As for processes related to C loss, there are now storage would be maximized by planting a mono-
a number of litter-mixing studies that collectively culture of the species with the combination of traits
suggest that generally plant species composition (stature, lifespan, timber density, decomposition
of litter rather than its richness plays an important rate, resistance to fire, wind-throw, and pests) that
role in decomposition and nutrient cycling rates. produces the highest species specific C storage for a
Although the additive effects of species richness given area. The niche complementarity hypothesis
on litter decomposition cannot strictly be consid- predicts that C storage will be impacted by inter-
ered a niche complementarity effect in the sense of specific differences among coexisting species, in
complementarity of resource use, they are dis- terms of resource use and tolerance to biotic and
cussed here because they involve ‘richness- abiotic factors. It also predicts that it may be possible
related’ effects, as does the niche complementarity to increase C storage by planting complementary
hypothesis. Litter mixing studies have found litter mixtures of species, sets of species with known
species richness to exert generally idiosyncratic or mutually facilitative effects, and/or ensuring that a
weak effects on litter mass loss (e.g. Wardle et al. mosaic of late- and early-successional patches is kept
1997a, Bardgett and Shine 1999, Hector et al. 2000, (e.g. Caspersen and Pacala 2001). Finally, the neutral
reviewed by Gartner and Cardon 2004), while hypothesis predicts that the C storage capacity of
plant species richness has generally been found to natural forests will vary randomly with stochastic
exert weak or neutral effects on soil processes shifts in species abundances. In plantations it may be
(Chapman et al. 1988, Hooper and Vitousek 1998). possible to influence C storage by controlling the
Further, it has been shown experimentally that recruitment stage, for example by increasing seed or
addition of a greater richness of C substrates to seedling input of species that are good at seques-
the soil (such as might be expected in a more tering C but are poor recruiters.
species-rich plant community) did not exert strong The three hypotheses all stem from strong
or consistent effects on C loss rates from soil, or on theoretical developments and are all supported
soil C storage (Orwin et al. 2006). However, in by empirical evidence to varying degrees in for-
instances in which NPP is promoted by plant ested systems. Most of the experiments from
species richness, it is likely that decomposition which this evidence is derived were not origin-
rates would be less unresponsive, in which case ally designed to test these hypotheses. Moreover,
greater C sequestration would be expected over there is an important body of results of experi-
time. The mechanistic basis through which plant ments specifically designed to test the effect of
richness might affect soil processes is relatively biodiversity (and most commonly species rich-
poorly understood. However, the available evi- ness) on the functioning of grasslands (reviewed
dence suggests that plant species richness is not a in Loreau et al. 2001, Díaz et al. 2005, Hooper et al.
powerful driver of soil decomposer richness 2005) but there are few corresponding experi-
(Hooper et al. 2000) and that decomposer richness mental studies in woody ecosystems, which may
is not a major determinant of soil process rates not necessarily behave in similar way to herba-
such as decomposition or nutrient supply rates for ceous ecosystems.
 INCORPORATING BIODIVERSITY IN CLIMATE CHANGE MITIGATION INITIATIVES 157

Table 11.1 provides an overview of recent studies An experimental test of the neutral hypothesis
of the role of different components of plant biodi- through the removal of dominant species has
versity in C gain and loss of forest ecosystems. They recently been performed for intertidal communi-
include primary forests, traditionally managed ties (Wootton 2005), but the feasibility of this
forests, and commercial and experimental planta- approach for use in other systems is unclear.
tions. Our synthesis, which is intended to be illus- Experiments to definitively establish the relative
trative rather than exhaustive, reflects the scarcity importance of the mass ratio and niche comple-
of published studies involving woody plants. This mentarity mechanisms for determining ecosystem
is true for all continents, but particularly dramatic properties in forests will ideally require the
in Latin America, Africa, and Asia, precisely where establishment of monocultures and mixtures of all
most remaining high-diversity forests are located. component species under the same environmental
There have been some studies that can be inter- and management conditions (e.g. Redondo-Brenes
preted in the light of the mass ratio or niche com- and Montagnini 2006, Potvin and Gotelli 2008).
plementarity hypotheses to varying degrees. As for This may be practical for species-poor ecosystems
the neutral hypothesis, we found no study directly (e.g. boreal forests), but it quickly becomes
linking it with the way in which biodiversity could unfeasible if one is to incorporate even a fraction of
affect ecosystem processes. According to the origi- the high richness of tree species characteristic of
nal authors’ interpretation of their own results many tropical forests. We also emphasize that
(Table 11.1, third column) there seems to be more experimental approaches of this type are not the
support for the mass ratio hypothesis than for the only way to formally test for the role of biodiver-
niche complementarity hypothesis, in the sense that sity in ecosystem functioning, and ideally the
the authors conclude that composition (the pres- results of such studies should be considered
ence of certain tree species) appears to play a more alongside other approaches that have recently
important role than species richness. However, been employed to test how biodiversity affects
compositional differences could arise from either forest C sequestration, such as simulation- and
mass ratio or niche complementarity effects or some modelling-based approaches (Bunker et al. 2005),
combination of the two (Loreau and Hector 2001). field removal experiments (Díaz et al. 2003,
Distinguishing the relative contributions of these Wootton 2005), observational studies using well
two mechanisms will require future studies that are characterized gradients of plant diversity (Wardle
explicitly designed to discriminate among the two et al. 2003a), and forestry projects that incorporate
classes of causes. Evidence for relationships diversity components into their design (i.e. ‘enrich-
between species richness and stability of forests and ment planting’, e.g. Evans and Turnbull 2004). In the
plantations is mixed. It follows that particular end, even being able to successfully distinguish
attention should be paid to the identity of the spe- between the relative importance of mass ratio, niche
cies chosen for afforestation, reforestation and complementarity, and neutral hypothesis effects
rehabilitation projects, with the actual richness of may not necessarily be crucial to the practical
species planted taking second place. However, (1) purposes of C sequestration, especially as these
positive effects on ecosystem functioning are often hypotheses are not all mutually exclusive. For
found in mixtures of two or more species compared example, experimenting with mixtures that contain
to monocultures; (2) virtually all the reported non-random combinations of species (such as those
studies were not specifically designed to distin- that represent traditional mixtures), or maximize key
guish between the three different hypotheses, and ecosystem services like C sequestration plus food
the patterns observed may fit more than one of production, or are the most economically and
them (e.g. Chave 2004, Volkov et al. 2005); and (3) socially feasible in each region, might make more
mass ratio, niche complementarity, and neutral practical sense than incorporating all the possible
hypothesis mechanisms may all be acting simulta- mixtures of component species within the experi-
neously (e.g. Potvin and Gotelli 2008). mental design.
Table 11.1 A summary (representative rather than exhaustive) of studies published during the last 13 years on the effects of different components of biodiversity on C sequestration through impacts on C gains or
losses in woody ecosystems.

Ecosystem type and location Main biodiversity Findings Source

component involved

C gain
Experimental plantations of fast-growing tropical tree Species and functional Ecosystem productivity and resource capture were increased when the Haggar and Ewel
species Hyeronima alchomeoides, Cedrela odorata, and group richness monocots were grown with C. odorata and C. alliodora, but not with H. (1997)
Cordia alliodora; each species grown alone and with alchomeoides
two perennial, large-stature, monocots (Euterpe
oleracea and Heliconia imbricata)
Boreal forest trees and understorey vegetation on Species and functional Species-rich islands less productive at large spatial scale (between islands) Wardle et al. (1997),
Swedish lake islands group richness because more productive species dominate on less diverse islands; some Wardle et al. (2003),
evidence of greater understorey species richness promoting overall forest Wardle and
productivity within islands Zackrisson (2005)
Young plantations of four indigenous tree species: Species richness and Total tree biomass production rate of the mixture was not significantly Stanley and
Hieronyma alchorneoides, Vochysia ferruginea, identity higher than that of the most productive monocultures Montagnini (1999)
Pithecellobium elegans, and Genipa americana, growing
in mixed and pure stands at La Selva Biological Station,
Costa Rica
Stand productivity in USA Forest Inventory and Analysis Species richness Positive correlation between tree species richness and stand productivity, Caspersen and Pacola
database especially when comparing monocultures vs. mixtures of two or more (2001)
species; variations in abiotic factors not considered
Stand biomass in global forest dataset Species richness Forest stand biomass not associated with tree species richness Enquist and Niklas
(2001)
Experimental plantations of three native tree species, Species richness and Tree species richness influenced ecosystem nutrient use efficiency in tree- Hiremath and Ewel
Hyeronima alchoreoides, Cedrela odorata, and Cordia composition only stands. Aboveground net primary productivity after four years was (2001)
alliodora, in monoculture and in mixtures with the palm and functional group significantly higher in polycultures than in monocultures of C. odorata,
Euterpe oleracea and the giant perennial Heliconia richness and C. alliodora, but not in the case of H. alchomeoides. The presence of
imbricata, in Costa Rica Atlantic lowlands the additional life forms increased nutrient uptake and uptake efficiency,
but only in some systems and years
Although species and life forms exerted considerable influence on
ecosystem nutrient use efficiency, this was most closely related to soil
nutrient availability
Stand productivity of boreal forests dominated by Betula Species richness and Mixtures of Betula spp. and P. abies more productive than Picea Frivold and Frank
spp., Picea abies and Pinus sylvestris, under the same composition monocultures, but mixtures of Betula spp. and P. sylvestris were less (2002)
environmental conditions and management productive than P. sylvestris monocultures; species richness effect
significant only at early successional stages
Long-term experimental comparison of different Species richness and Multistrata agroforestry system showed more accumulation of above- and Schroth et al. (2002)
agroforestry systems in Brazilian Amazonia; peach palm composition belowground biomass than cupuaçu, rubber, or peach palm for heart-of-
(Bactris gasipaes) for fruit and heart-of-palm production, palm, but less than peach palm for fruit
cupuaçu (Theobroma grandiflorum), and rubber Secondary forest accumulated 50%, and primary forest likely 500% more
(Hevea brasiliensis) planted n multistrata mixtures total biomass than the most productive plantation
and in monocultures, also compared with adjacent
primary rainforest and 14-year old secondary
forest
Wood production in Catalonian forests with different Species richness In P. sylvestris forests wood production was not significantly different Vilà et al. (2003)
degrees of species richness, dominated by Pinus between monospecific and mixed plots. In P. halepensis forests wood
sylvestris or Pinus halepensis production was greater in mixed plots than in monospecific plots. No
significant effect of species richness when environmental factors were
considered.
Experimental plantations of three native tree species, Species composition Light particulate organic matter C and soil C:N ratio were significantly Russell et al. (2004)
Hyeronima alchoreoides, Cedrela odorata, and Cordia and functional higher, and total soil organic matter C was slightly higher, under H.
alliodora, in monoculture and in mixtures with the palm group richness alchoreoides, as compared to under the other two tree species
Euterpe oleracea and the giant perennial Heliconia Functional group richness had a positive effect on total and light/
imbricata, in Costa Rica Atlantic lowlands particulate soil organic matter as compared to monocultures of C.
odorata and C. alliodora, but not in the case of those of H.
alchoreoides.
Litter production in Catalonian traditionally managed Species richness, Litter mass larger in 2–5 species mixtures than in monospecific stand. In Vilà et al. (2004)
forests species and mixed forests, identity of trees determined whether litter stocks increase
functional trait with tree diversity.
composition
Simulation study of the magnitude and variability of Species richness and Different trait-based scenarios (e.g. order of extinction determined by Bunker et al. (2005)
aboveground C sequestration in 18 scenarios of tree functional trait wood density, height, growth rate, drought tolerance, also a random
species extinction within a species-rich tropical in composition extinction scenario) resulted in strong differences in magnitude and
Panama variability of C stocks
Long-term tree-planting experiment, established in 1955 Species richness and All mixtures involving Pinus sylvestris showed more growth in pure stands Jones et al. (2005)
in NW England; Quercus petraea, Alnus glutinosa, Pinus composition of either species; A. glutinosa mixtures not involving P. sylvestris did not
sylvestris and Picea abies planted in monocultures and outperform monocultures, P. abies/Q. petraea mixture showed less
in 2-spp mixtures growth than monocultures

(Continues)
Table 11.1 (continued)

Ecosystem type and location Main biodiversity Findings Source

component involved

Review of the 20th century forestry literature with Species and functional Increased productivity in mixtures of species with different spatial, Pretzsch (2005)
emphasis on commercial trees in the temperate and group richness phenological or successional niches (e.g. Larix/Picea, Quercus/Betula,
boreal zones and composition Pinus/Picea, Pinus/Betula)
Some mixtures (e.g. Picea abies/Betula pendula) sustain production over a
larger range of densities than monocultures and are thus more tolerant to risks
Natural and seminatural forests, plantations and Species richness, Stemwood production increased from single-species to Vilà et al. (2005)
secondary woodlands in the Ecological and Forest species and functional 5-species stands, but stand age and richness were negatively correlated
Inventory of Catalonia (IEFC), including 95 tree species trait composition Species richness had a significant positive effect on stemwood production
in stands dominated by sclerophyllous species (e.g. Quercus, Arbutus),
and low-productivity conifer stands, but not deciduous species stands in
humid or warmer climates
Experimental mixed plantations of native trees Balizia Species richness Although some individual species were more productive in mixtures than in Redondo-Brenes and
elegans, Callophyllum brasiliense, Dipteryx panamensis, monocultures, none of the mixtures showed significantly higher growth Montagnini (2006)
Hyeronima alchorneoide, Jacaranda copaia, Terminalia or C storage than the monocultures of the most productive species
amazonia, Virola koschny, Vochysia ferruginea and involved in each mixture
Vochysia guatemalensis in Costa Rican tropical rainforest
Monocultures were compared to 3-species mixtures, all of
them consisting of one fast-growing sp., one slow-
growing sp., and one legume, to keep functional
richness as constant as possible
More than 5000 permanent forest plots in the National Species richness, Stemwood production was positively associated with tree species richness Vilà et al. (2007)
Forest Inventory of Spain in the Catalonia functional group and with functional group identity (deciduous forests were more
region, including 51 tree species, growing in richness and identity productive than coniferous or sclerophyllous forests). Functional group
monocultures and in 2- to 5-species mixtures richness did not significantly explain stemwood production once the
effects of environmental and structural variables were taken into account

Experimental plantations of native tropical trees Species richness and Plot biomass (estimated from basal area) did not differ between mixtures Potvin and Gotelli
representing a range of relative growth rate (Cordia composition and monocultures or among mixtures. There was a significant species (2008)
alliodora, Luehea seemannii, Anacardium excelsum, richness effect on growth, attributed to complementarity, in the 3-species
Hura crepitans, Cedrela odorata, and Tabebuia rosea) in mixtures as compared to monocultures, but there was no significant
monocultures, and 3- and 6-spp. plots, in Central effect in 6-species plots. Mortality was strongly dependent on species
Panama identity, and independent of species richness. Overall, there was a
positive complementarity effect (using the additive partitioning method of
Loreau and Hector 2001) of species richness on plot biomass and a
negative selection effect, resulting in no net species richness effect
C loss
Boreal forest trees and understorey Species and functional Species-rich islands supported less soil respiration, microbial biomass and Wardle et al. (1997),
vegetation on Swedish lake islands group richness decomposition at large spatial scale (between islands), contributing to Wardle et al. (2003),
net C sequestration in the soil Wardle and Zackrisson
Some evidence of greater understorey species richness promoting these (2005)
processes within large (but not small) islands
Differences among islands in belowground processes and C sequestration
are explicable by traits of dominant plant species but not species richness
Damage by beetle Phratora vulgatissima and rust Genetic richness and Mixtures showed less damage by rust and beetles than monocultures; no Peacock et al. (2001),
Melampsora spp. on five Salix genotypes in spatial significant effect of structural design was detected, but the trend was for Hunter et al. (2002)
monocultures and mixtures in regular and random heterogeneity decreased damage in random configurations
spatial arrangements
Microcosms experiments using litter of nine phenotypes Intraspecific phenotypic C and N fluxes within single phenotype treatments were significantly, but Madritch and
of Quercus laevis in monocultures and in mixtures richness unpredictably, different from those of mixtures Hunter (2002),
and composition No effect of phenotype identity on soil bacterial or microarthropod Madritch
communities and Hunter (2005)
Literature review of European forests Species richness and/or Different species and functional types differed in wind resistance; mixtures Dhôte (2005)
(especially N Europe) composition were not more stable than monospecific stands against windstorms
Literature review of decomposition rate of single-species Species richness and Sometimes faster decomposition in mixtures; in other studies the effect Hättenschwiler et al.
litter vs. litter mixtures of several N Hemisphere tree composition was similar to that predicted from the decay rates of individual species (2005)
species and their relative contribution to the mixture; in two cases lower decay
rate in mixtures; different mixtures involving Pinus or Quercus showed no
consistent effect as compared to monocultures
Meta-analysis of 54 studies of insect herbivory on trees, Species richness and Tree species growing in mixed stands overall suffer less damage by Jactel et al. (2005)
with emphasis on temperate systems composition specialized herbivore insects than do pure stands; generalist insects
showed a highly variable response
Heterobasidium annosum (butt rot) in pure vs. mixed Species richness Incidence of H. annosum negatively correlated with tree species richness Korhonen et al. (1998),
stands under different climatic conditions (mostly N as cited in
Europe) Pautasso et al. (2005)
Cronartium ribicola rust and Phellinus weirii root rot in Species richness and Disease spread associated with certain host tree species, rather than with Pautasso et al. (2005)
North American forests composition tree richness
Literature review of boreal forests Species richness and/or Mixed stands not more resistant to fire than Wirth (2005)
composition monospecific stands

(Continues)
Table 11.1 (continued)

Ecosystem type and location Main biodiversity Findings Source

component involved

Review of 26 experimental studies on the effect of the Tree species Species-rich stands not consistently less prone to pest outbreaks and Koricheva et al. (2006)
diversity of trees in boreal forests on the damage by richness and disease epidemics than monocultures. Composition appeared to play a
invertebrate and vertebrate herbivores and pathogen composition, land- greater role than species richness per se
species scape heterogeneity
Susceptibility to inspect pests decreased with increased isolation of stand
within a forest mosaic of non-host species
Experimental boreal forests of Betula pendula, Pinus Species richness and Monocultures of B. pendula and mixed stands containing 25% of B. Vehvilaäinen et al.
sylvestris, and Picea abies in Sweden and Finland composition pendula and 75% of P. sylvestris showed higher defoliation by insects (2006)
early in the season than B. pendula monocultures or 50–50 mixtures of B.
pendula and P. sylvestris. No difference between monocultures and
mixtures late in the season
Experimental plantations of native tropical trees Species richness, After c. 4 years from establishment, no consistent general effect of species Scherer-Lorenzen et al.
representing a range of relative growth rate (Cordia species and functional richness was found on either litter production or decomposition. Litter (2007a)
alliodora, Luehea seemannii, Anacardium excelsum, trait composition production was significantly affected by tree species richness and
Hura crepitans, Cedrela odorata and Tabebuia rosea) in identity, with the majority of intermediate-richness mixtures showing
monocultures, and 3- and 6-spp. plots, in Central higher litter yields than expected based on monoculture. Litter
Panama decomposition also varied with species identity and functional attributes.
High-richness mixtures decomposed at rates that were no different from
expected on the basis of their component species. However, individual
species changed their decomposition pattern depending on the richness
of the litter mixture
Experimental decomposition of monocultures and Species richness, When up to five species were included, both species richness and Pérez Harguindeguy
mixtures of 2, 3, 4, and 5 dominant species of central species and functional functional composition showed non-additive, mostly positive effects on et al. (2008)
Argentina mountain woodlands, representing a range of trait composition litter mixture decomposition. The synergistic effects of species richness
functional groups decomposition rates (Acacia caven, were significant when the richness of the mixtures changed from 2 to 3–4
Lithraea molleoides, Bidens pilosa, Hyptis mutabilis, and species. A greater positive effect was found in mixtures with higher mean
Stipa eriostachya) nitrogen content and a higher heterogeneity in non-labile compounds.
Litter mean quality and chemical heterogeneity were the most important
factors explaining decomposability of mixtures
 INCORPORATING BIODIVERSITY IN CLIMATE CHANGE MITIGATION INITIATIVES 163

11.3 Making the most of biodiversity accumulating it for centuries (Luyssaert et al. 2008).
in the design of climate change There is less empirical information for tropical for-
mitigation initiatives ests, but their C exchange appears to be approxi-
mately balanced, or even slightly positive (Schimel
The major hypotheses examined above, and the 2007, Stephens et al. 2007). This points to a gross sink
evidence available so far, indicate that the incor- that compensates for emissions due to tropical
poration of biodiversity considerations has the deforestation and fires. Primary forests often show a
potential to influence the magnitude and long-term lower uptake of C per unit time than do newly
persistence of C-sequestration initiatives. The lead- established plantations (Gower 2003) but on the
ing role of the functional traits of locally dominant other hand they sequester it for a longer time. Also,
plant species is supported by strong evidence from the process of land conversion, for example during
a variety of ecosystems. However, considerably the establishment of a new plantation, often releases
more experimental, observational, and modelling very large amounts of C from the soil to the atmo-
work is needed to elucidate many specific details, sphere (Valentini et al. 2000, Guo and Gifford 2002,
such as to what extent increasing the small-scale Pregitzer and Euskirchen 2004). As a consequence,
species richness of reforestation or afforestation the net balance of C sequestered per hectare is
actions can increase their ability to store C. Never- usually more strongly positive in the case of primary
theless, we believe that some practical recommen- forests than for new plantations, with the benefits
dations can already be made based on the current from the latter being more transitory and uncertain
level of knowledge. (Schulze 2005). Primary forests are being destroyed

Protecting primary forests is the best C seques- at accelerated rates, especially in the African and
tration option. For obvious practical reasons, to Latin American tropics (Lambin et al. 2003, Fearnside
date there is no published biodiversity experiment and Barbosa 2004, Shvidenko et al. 2005). The
involving formal experimental manipulation of tree amount of forested area lost is still impossible to
species richness beyond six species. However, pri- match by plantation initiatives, and this is likely to
mary forests usually have a larger number of species continue to be the case for the next several decades.
and a wider range of plant functional attributes than Plantations can also involve high monetary and
do planted forests. They also tend to be dominated environmental costs. For example, the monetary cost
by large-sized, slow-growing species that are con- of sequestering 1 Mg of C by forestation and agro-
servative with resources. Therefore, under both the forestry activities has been estimated as being more
niche complementarity and mass ratio hypotheses, than triple than that of sequestering the same
we expect them to maximize C stocks. Available amount by conservation of already existing forests
evidence from the biodiversity and biogeochemistry (van Kooten et al. 2004). Another recent study shows
literature supports this idea. Primary forest ecosys- that monospecific plantations of fast-growing trees in
tems represent the most important biological C sinks southern South America have strong negative
on the planet in terms of both quantity and likely impacts on water supply and soil fertility (Jackson
stability through time (Buchmann and Schulze 1999, et al. 2005). An additional reason to protect primary
Valentini et al. 2000, Schimel et al. 2001, Schulze 2005, forests is that changes in the functional attributes of
Luyssaert et al. 2008). With very few exceptions, they vegetation over large areas can affect climate directly
contain larger C stocks than younger forests in all through water and energy exchange (Chapin et al.
biomes (Pregitzer and Euskirchen 2004, Schulze 2008).
2005). Recent studies suggest that C outputs and
The maximization of short-term C sink strength
inputs in primary forests are frequently not at equi- is unlikely to be the best option for C sequestration
librium, and that such forests are active, albeit in the longer term. As explained in previous sections
sometimes small, C sinks (Schimel et al. 2001, Schulze and illustrated in Fig. 11.2, the well-supported mass
et al. 2002, Sabine et al. 2004, Schulze 2005, Luyssaert ratio hypothesis predicts that there is fairly a uni-
et al. 2008). In temperate and boreal zones, forests versal tradeoff between a suite of plant attributes
contain large quantities of carbon and can continue that promotes fast C and mineral nutrient
164 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

acquisition and loss (‘acquisitive’ syndrome), and genotypes, species and functional types can benefit
another that promotes slower acquisition but long afforestation, reforestation, agroforestry, secondary
retention of resources within well-protected tissues forest recovery and solid biofuel plantation initia-
(‘conservative’ syndrome). This suggests that a man- tives. However, thousands of years of agricultural
agement regime that simultaneously maximizes rapid experience point to the use of polycultures as a
C uptake from the atmosphere and its long-term promising precaution to buffer forest production
sequestration is unlikely to be found. This is directly throughout the year and also against environmental
relevant to C sequestration initiatives, since at any change and variability and pest and weed damage.
time a C-sequestering project is launched, a decision Tree monocultures often, but not always, promote
should be made in favor of one or the other side of less SOC accumulation than primary or secondary
the tradeoff (Aerts 1995, Caspersen and Pacala 2001, forests (see Lal 2005, Jandl et al. 2007 for reviews). But
Noss 2001). For example, early-successional, light- even in cases where the amount of C sequestered by
demanding, fast-growing species should be selected a monoculture is higher, the use of mixtures of more
when the goal is to maximize short-term productivity. than one tree species may be a good alternative for
However, C sequestration in the longer term will be small or medium-sized farms, especially in tropical
greater in areas dominated by later-successional spe- and subtropical areas. This is because mixed plan-
cies that are slower growing but have denser timber, tations provide a wider range of products and
and whose litter decomposes more slowly. In view of opportunities. For instance, fast-growing and slow-
this, high sink capacity in the short term should not be growing species provide revenues in the short and
considered as the major criterion in reforestation/ long term, respectively; different species provide
afforestation initiatives. In general, careful consider- non-forest products such as fruit at different times of
ation of the species and genotypes chosen for each C the year and thus improve food security and buffer
sequestration project is needed (Lal 2004). There are market risks (Piotto et al. 2004, Montagnini et al.
strong ecological bases to suggest that fast-growing, 2005). These ancillary benefits of mixed plantations
genetically homogenous, easy-to-manage, wide- and agroforestry systems increase the interest of local
spread forestry species and genotypes (e.g. members stakeholders in establishing and protecting forests
of Eucalyptus, Pinus, and Acacia widely planted in and diminish incentives for changing to other land
South America, Africa, and East Asia) may not rep- uses (Liebman and Staver 2001, Pretty and Ball 2001,
resent the most effective option in terms of long-term Schroth et al. 2002, Piotto et al. 2004, Montagnini et al.
C sequestration. Also, the choice of species and gen- 2005). Sometimes the recovery of the natural forest is
otypes with the appropriate attributes for local limited by animal dispersal of propagules, soil
(present and projected) climatic and disturbance moisture, and competition from herbaceous plants.
conditions (e.g. fire proneness, storm, or frost fre- Mixed plantations offer an alternative in these cases.
quency) is very important. The same considerations For example, in Costa Rica, more individuals and
apply to plantations that serve as sources of solid species of native trees were found to regenerate in
biofuel, although permanence is obviously less of an the understorey of mixed plantations than those
issue in that case. under monocultures (Guariguata et al. 1995, Powers

Mixed forestry systems might be more stable in the et al. 1997, Carnevale and Montagnini 2002).
face of environmental variability and directional change
Plantations established with the specific purpose of C
than monocultures, and they might sequester C more sequestration or biofuel production can, and should, be
securely in the long term. This recommendation is compatible with biodiversity conservation. It is vitally
consistent with the niche complementarity hypothe- important that projects supported through the
ses, as well as the results of several experiments in CDMs or other initiatives aimed at increasing C
herbaceous communities. The evidence from forest uptake do not come at the direct or indirect cost of
ecosystems is still inconclusive, and long-term field- clearing natural ecosystems, and that they maintain
scale experimental, observational and theoretical a high ecosystem-service value from the point of
studies are needed to rigorously test whether, how view of local communities rather than simply
generally, and for how long increasing the number of meeting the C credit priorities of external investors
 INCORPORATING BIODIVERSITY IN CLIMATE CHANGE MITIGATION INITIATIVES 165

(Niesten et al. 2002, Prance 2002, Fearnside 2006a). tems involved. A practical way to increase our
Niesten et al. (2002), Schulze et al. (2003) and understanding of how, where, and why different
Chadzon (2008) provide examples of forestry pro- biodiversity components affect the C-sequestration
jects that, rather than decreasing pressure on natural capacity of different ecosystems would be to incor-
ecosystems, may contribute to their destruction, in porate an experimental component to climate change
the name of the creation of C sinks. Agroforestry mitigation and agroforestry and forest rehabilitation
practices have the potential to store large amounts initiatives (e.g. Ewel 1986, Montagnini et al. 2005,
of C while at the same time protecting biodiversity. Scherer-Lorenzen et al. 2005b). Moreover, we are
For example, Brandle et al. (1992) and Noss (2001) aware of a wealth of information being produced by
highlighted the potential of planted shelterbelts and the forestry sector, but this is not often reflected in the
riparian forests that store C and at the same time peer-reviewed literature. In this sense, the recent book
provide wildlife habitat and permanent regional edited by Scherer-Lorenzen et al. (2005a) has made a
vegetation connectivity. Modeling efforts by Bolker valuable contribution through making available a
et al. (1995) and Pacala and Deutschman (1995) large body of difficult-to-access and diffuse literature
suggest that species-rich and spatially heterogeneous from the forestry sector. A similar effort with specific
forests could have a C sequestration potential of up focus on key regions (e.g. Latin America, Africa,
to 50 per cent more than monospecific, spatially Southeast Asia) including the wealth of information
homogeneous forests. As in the case of managed accumulated by governmental and non-governmen-
forests not specifically designed for C sequestration tal grassroots initiatives, would be valuable for help-
processes, high inter- and intraspecific genotypic ing find the best options for simultaneous C
richness, the inclusion of local genotypes, and the sequestration and biodiversity protection in primary,
maintenance of a rich and heterogeneous landscape managed and planted forests.
increases the value of plantations for local societies,
and thus their willingness to protect them. This
11.4 Final remarks
enhances their potential to preserve their long-term
survival and C sequestration capacity (Prance 2002, In the past few years, the focus of international
Díaz et al. 2005). On the other hand, local commu- mitigation efforts seems to have shifted from cut-
nities have little to win and much to lose (e.g. tra- ting fossil fuel emissions to enhancing C seques-
ditional medicine, cultural and spiritual values, tration, with the remarkable exception of some
employment) from reliance on monospecific stands actions taken during the most recent COPs (see
of fast-growing (and often introduced) tree species Introduction). The potential contribution of C
and varieties. The incorporation of what is ‘valuable sinks to climate change mitigation is clearly less
biodiversity’ from the local community’s point of important in terms of C released to the atmo-
view is essential for striking the right balance sphere, than that of decreasing emissions from
between biodiversity and C sequestration and for fossil fuel burning (IGBP 1998, Prentice et al. 2001).
ensuring the long-term protection of C-sequestering Therefore, by no means do we believe that miti-
plantations (Díaz and Cáceres 2000, Prance 2002, gation initiatives are a substitute for cutting fossil
Saunders et al. 2002, Díaz et al. 2005, Canadell and fuel emissions, however beneficial for the conser-
Raupach 2008). vation of biodiversity they would be. That said,

Decisions about the species and genotype richness and there is considerable potential for increasing the
composition of protected or newly established plantations or world’s C stocks through management practices
agroforestry systems should be tailored to the local context. (Watson et al. 2000, Niles et al. 2002, Fischlin et al.
It is important to keep an open perspective and to 2007, Canadell and Raupach 2008). Considering
avoid mechanical application of general principles to the dramatic observed and projected consequences
individual projects without careful consideration of of climate change (IPCC 2007), we must exploit
the resource base, prevailing disturbance conditions, this potential to the largest possible extent. Equally
scale of the project, and attributes of the organisms important is making sure that C sequestration
(including not only the planted species) and ecosys- measures do not backfire in the long term, for
166 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

instance by ensuring that their overall environ- probably the most appropriate way forward. This is
mental costs do not offset their benefits. not free of technical difficulties, but its long-term
On the basis of the findings summarized above, cost–benefit ratio appears low when all economic,
and in accordance with other authors (IGBP 1998, social, and environmental factors are considered.
Schulze et al. 2002, Schulze et al. 2003, Fearnside In view of this, the lack of biodiversity considera-
2006b, Luyssaert et al. 2008), we suggest that the tions in the main body of the Kyoto Protocol is
conservation of natural ecosystems is the best C unfortunate to say the least. Particularly worrying is
sequestration option available. Natural ecosys- the fact that in the first commitment period of the
tems, with their ability to simultaneously maintain CDMs only afforestation and reforestation are
C stocks, biodiversity, and ecosystem services, and included, considering that more than half of the
their built-in capacity to cope with environmental world’s forested area is located in developing coun-
change and variability, are the ultimate ‘win-win’ tries and that they are facing accelerating deforesta-
climate mitigation option. There is no substitute tion rates (Lambin et al. 2003, Shvidenko et al. 2005). In
for the C-sequestration capacity of natural forests, our view, in order to reverse this trend, biodiversity
nor any practical way to reproduce the biodiversity considerations should be incorporated into C
of some of them (Myers et al. 2000) or to substitute sequestration initiatives. In this sense, the request of
for the ecosystem services they provide (Millennium some developing countries to incorporate the pro-
Ecosystem Assessment 2003, Shvidenko et al. 2005). tection of tropical forests into the second commitment
There is evidence suggesting that their functional period of the Kyoto Protocol (http://unfccc.int/
composition is changing and that they are losing resource/docs/2005/cop11/eng/misc01.pdf), and the
species at an alarming rate due to land use change new international interest in avoided deforestation
(e.g. Sala et al. 2000, Brook et al. 2003, Gaston et al. with explicit mention to biodiversity (e.g. REDD) are
2003), and climate change (Parmesan and Yohe 2003, signs that the tide might be turning towards a more
Root et al. 2003, Lenoir et al. 2008). In view of this, positive direction.
probably the best long-term C sequestration option
would be to encourage scientific and policy efforts
Acknowledgements
that preserve their integrity.
In those areas where afforestation and deforesta- This chapter greatly benefited from input by D. E.
tion will not come at the cost of destroying natural Bunker, O. Canziani, and N. Pérez-Harguindeguy,
ecosystems (e.g. in degraded, not recently deforested and from critical review by M. Loreau. It is a
areas, or areas where the forest is unlikely to recover product of Núcleo DiverSus (endorsed by
naturally, Appanah and Weinland 1992, Montagnini DIVERSITAS and the Global Land Project). It has
et al. 2005), our findings strongly suggest that built-in also benefited from fruitful interactions between
biodiversity considerations will not only increase its authors and the participants in the DIVERSI-
their overall ecosystem-service value (Millennium TAS ECOServices Meeting ‘Biodiversity and Car-
Ecosystem Assessment 2003), but also specifically bon Sequestration’ (7–10 September 2005, Danum
enhance their long-term C sequestering capacity. In Valley Field Centre, Sabbah). SD was supported
order to make a difference for mitigating the effects of by FONCyT, CONICET, Universidad Nacional de
global warming, the size, longevity, and reliability of Córdoba (Argentina), the J. S. Guggenheim Memo-
biological C stocks are more important considerations rial Foundation and the Inter-American Institute for
than sink rates. Consequently, preserving the integ- Global Change Research (CRN II 2015, supported by
rity of natural systems, and building diverse systems the US National Science Foundation Grant GEO-
with a careful consideration of the most suitable 0452325) while carrying out research leading to this
dominant and subdominant species and genotypes, is chapter.
 CHAPTER 12

Restoring biodiversity and ecosystem

function: will an integrated approach
improve results?
Justin Wright, Amy Symstad, James M. Bullock, Katharina
Engelhardt, Louise Jackson, and Emily Bernhardt

12.1 Introduction scape architecture (Fabos 2004); and earth sciences

Twenty years ago, Bradshaw (1987) stated that such as soil science (Bradshaw 1997) and hydrology
ecological restoration should be an acid test of (Morris 1995); as well as the subfields of population
ecological understanding. In fact, the practice of (Rosenzweig 1987) and landscape ecology (Van
restoration has developed more through trial and Diggelen 2006). This diversity of influences has led
error than by the application of any scientific to many different approaches and goals for resto-
framework. Since Bradshaw’s statement, restora- ration projects. However, given the primary focus
tion ecology has undergone a rapid increase in on restoring the structure and function of ecosys-
conceptual development and basic research, as tems, the strongest conceptual basis for most of
indexed by the rising number of peer-reviewed restoration ecology stems from community and
publications (Young et al. 2005), the creation of the ecosystem ecology (Ehrenfeld and Toth 1997, Palmer
journal Restoration Ecology in 1993, and the recent et al. 1997, Young 2000, Falk et al. 2006). Simply
publication of a number of edited volumes dedi- put, restoration ecology is typically interested in
cated to exploring the conceptual underpinning of restoring either biodiversity, ecosystem functioning,
restoration ecology (Falk et al. 2006, Van Andel and or both.
Aronson 2006). In addition, meta-analyses of res- Despite these overlapping areas of interest, little
toration studies (e.g. Pywell et al. 2003) are begin- crossover is evident between restoration ecology and
ning to draw out some general patterns and relate ‘classical’ biodiversity-ecosystem function research
them to broader ecological theory. In this chapter (Naeem 2006a). With few exceptions (Bullock et al.
we contribute to this development by exploring the 2001, Callaway et al. 2003, Bullock et al. 2007), BEF
applicability of the biodiversity-ecosystem func- experiments have not taken place in restoration set-
tioning (BEF) framework to restoration science. tings. Although BEF research might inform restora-
Restoration ecology is the subdiscipline of ecol- tion (Aronson and Van Andel 2005, Young et al. 2005,
ogy that informs the ‘intentional activity that initi- Naeem 2006a), thus far few concrete suggestions have
ates or accelerates the recovery of an ecosystem been offered on how restoration ecology might ben-
with respect to its health, integrity and sustain- efit from a consideration of BEF research and theory
ability’(S.E.R. 2004). Like the broader field of ecol- or vice versa. In this chapter, we start by comparing
ogy, restoration ecology is an integrative discipline, community and ecosystem approaches to restoration
having drawn important influences from fields as and suggest how a BEF approach might differ from
diverse as applied sciences such as agronomy and these. We then draw on BEF theory and empirical
engineering (Mitsch 1993); social sciences such as research to suggest three broad areas where
sociology (Geist and Galatowitsch 1999) and land- understanding the links between biodiversity and

167
168 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

ecosystem functioning could have significant has not always yielded restoration of the whole
impacts on the success of restoration: ‘classical’ BEF community. In both California grasslands and
impacts (i.e. higher diversity leads to improved English meadows, plant composition and relative
functioning); the effects of biodiversity on the abundance of species have been restored to resemble
stability of ecosystem functioning; and the effects the reference condition, but the soil microbial com-
of biodiversity on the provisioning of multiple munity has remained significantly different, implying
ecosystem services. that functions such as decomposition and nutrient
For this chapter, we constrain the scope of what turnover may not have been restored (Smith et al.
we consider to be restoration to management activ- 2003, Potthoff et al. 2005, Steenwerth et al. 2006, Pywell
ities whose primary goal is to improve ecosystem et al. 2007). Although greater understanding of factors
services other than provisioning services, although influencing community assembly may overcome
improved provisioning services may result from the some of these problems, it may not overcome the
activities. Management activities whose primary common assumption of the community approach that
goal is to improve provisioning services are consid- functioning will be restored if the community is
ered in Chapter 13, which formally examines the role restored. This was explicitly studied in two con-
of BEF research in managed ecosystems. structed Spartina marshes. In both, vegetation com-
position, cover, and biomass of planted sites were
similar to those of natural marshes within 18 months
12.2 Community, ecosystem, and BEF
of planting, but in one case, the height structure failed
approaches to restoration
to meet the needs of the endangered bird for which
BEF research combines elements from community and the marshes were constructed (Zedler 1993), and in
ecosystem ecology. Consequently, Naeem (2006a) another, soil organic matter and nutrient accumula-
contrasted community and ecosystem approaches to tion, denitrification rates, and tidal export of nutrients
restoration with an approach based on the BEF per- required much longer to resemble reference levels
spective. A community approach largely focuses on (Craft et al. 1999).
the restoration of the biotic components of an ecosys- The ecosystem approach makes the opposite
tem – which species are present, their relative abun- assumption, in that a habitat template that restores
dance, and their interactions (trophic, competitive, ecosystem processes (e.g. hydrology of a wetland)
facilitative). It is often used when starting from is created, but most or all species are left to colonize
essentially bare ground, as in tallgrass prairie or hay on their own in a process of self-assembly (e.g.
meadow plantings in former agricultural fields, and Bradshaw 2000). The approach, which is charac-
when the goal of restoration is to enhance the con- teristic of many early restoration efforts (Bradshaw
servation value of a protected landscape – restoration and Chadwick 1980), may more accurately be
for biodiversity’s sake. This approach has evolved described as ‘rehabilitation’ rather than ‘restoration’
over time from assuming that restoration is essentially (S.E.R. 2004). Some examples of this approach
the speeding up of a linear approach to a specific, include constructing mechanical barriers in eroded
predictable, equilibrium state, to accepting the gullies in an overgrazed rangeland in order to slow
dynamic nature of communities, possible alternative surface water flow and enhance water percolation
stable states (Bullock et al. 2002, Hobbs 2006), and the into the soil (King and Hobbs 2006) and increasing
influences of disturbance and dispersal limitation on meandering of a stream in order to reduce flash
diversity (Pywell et al. 2003, Walker et al. 2004). flooding and increase habitat complexity and sedi-
This evolution may help overcome some of the ment and nutrient retention (Rosgen 1994). Other
problems encountered when using the community activities using the ecosystem approach include
approach. For example, restoring the target commu- ecological engineering and reclamation. Ecological
nity is often more difficult than expected, even in engineering strives to achieve and maintain a spe-
systems where community restoration has been cific ecosystem service within a relatively strict
practised for decades (Kindscher and Tieszen 1998). range, such as reducing nitrogen in wastewater to
Furthermore, restoration of one part of a community regulator-accepted standards via a constructed
 RESTORING BIODIVERSITY AND ECOSYSTEM FUNCTION 169

wetland. In contrast, reclamation strives to make a to long-term problems. For example, some of today’s
highly altered system serve some useful purpose by most troublesome invasive species were introduced
achieving an acceptable level of safety and aes- as a rehabilitation measure in over-grazed, drought-
thetics, such as stabilizing mine tailings with stressed rangelands (Christian and Wilson 1999,
vegetation that can tolerate the harsh conditions but Clarke et al. 2005, Schussman et al. 2006, Williams
are not necessarily native to the site (S.E.R. 2004). and Crone 2006). Finally, the approach does not take
Both use ecological processes and biotic compo- advantage of the multiple functionality and resil-
nents to achieve their goals, but these goals do not ience potentially provided by systems with an
include creating a system whose functioning or actively restored biotic community.
composition resemble a reference ecosystem. In contrast, a restoration approach based on BEF
Although economically attractive, the ‘Field of theory and empirical results stresses the relation-
Dreams’ approach of solely manipulating the phys- ship between the biotic community and ecosystem
ical environment (‘If you build it, they will come’; functioning. Although the BEF perspective does not
Hilderbrand et al. 2005) is risky because dispersal encompass all of the topics relevant to ecological
barriers limit the colonization of desired biotic restoration, it does cover the majority of a more
components and, even if these can be overcome, general framework recently proposed for restora-
interactions with species not yet present (e.g. polli- tion ecology (King and Hobbs 2006). A BEF
nators or mycorrhizae) may be necessary for estab- approach to restoration is based on the asymptotic
lishment or reproduction of important species. relationship between biodiversity and ecosystem
Furthermore, initial seeding with native or exotic functioning. This relationship is what sets the BEF
species that may grow quickly and provide good approach to restoration apart from the other two
cover can prevent establishment of desired later approaches. Restoration strives to restore an eco-
successional species. For example, in old field sites in system to that relationship by removing anthropo-
England, sowing of a few native grasses limited genic inputs that maintain high functioning but low
successful colonization by desired species (Pywell diversity in managed systems (e.g. fertilizer or pes-
et al. 2002). In addition, projects using the ecosystem ticides) or by enhancing functioning in degraded
approach with no attention to the composition of the systems by adding key sets of species (Naeem
biotic component may achieve their physio-chemical 2006a). Debate about the applicability of BEF theory
goals, but the narrow focus of these goals may lead outside of experimental settings (Huston 1997,

(a) (b)
Managed
Ecosystem function

Ecosystem function

Degraded

Biodiversity Biodiversity

Figure 12.1 The BEF perspective for ecological restoration. (a) The fundamental assumption of the BEF perspective is that biodiversity affects ecosystem
function, often in the manner depicted here, where adding diversity when diversity is low has a stronger effect on ecosystem functioning than adding diversity
when diversity is high, until the point at which increasing diversity has no effect on functioning. Restoration (vertical arrows), in this perspective, is the
restoration of this relationship in degraded systems, which have lower functioning than expected, or in managed systems, in which anthropogenic inputs
produce functioning at a higher level than expected given the system’s diversity. (b) The theoretical realm of possible ecosystem functioning in relation to
biodiversity. The hatched area incorporates the assumption, supported by empirical evidence, that it is possible to have greater functioning with a low number
of species than with the most diverse system, as well as the assumption that the range of variability in functioning decreases as biodiversity increases. The
latter assumption has less support from empirical evidence (see text). Figure is adapted from Naeem (2006).
170 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Box 12.1 Should the BEF restoration approach apply to all ecosystems?

Ecological restoration, like most things ecological, is physical template is primarily controlled by hydrology and
inherently and frustratingly context-dependent. Restoration geomorphology.
is being carried out in habitats as diverse as streams, However, we would argue that a BEF perspective can and
rivers, forests, wetlands, grasslands, estuaries, deserts, should inform river restoration in two important respects. First,
and alpine habitats to achieve an equally diverse suite of terrestrial vegetation can play very important roles in river
goals. Given the diversity of contexts in which restoration ecosystems, and thus BEF approaches can directly inform
occurs, it is appropriate to ask whether the BEF approach riparian management aspects of river restoration. The majority
is relevant to all forms of restoration. We see great of small stream ecosystems are primarily fueled by leaf litter
potential for the BEF perspective to improve the practice inputs (Fisher and Likens 1973), and higher diversity litter
of ecological restoration in many cases. However, it is inputs can lead to greater secondary production (Swan and
important to recognize that in systems where abiotic Palmer 2006). Riparian trees themselves contribute large
structure serves as the dominant control of ecosystem wood to stream channels which can play important roles as
properties, the BEF approach may not be as relevant to both habitat and biogeochemical hotspots in rivers (Wallace
successful restoration. et al. 1995, Valett et al. 2002, Wright and Flecker 2004,
Streams and rivers are an instructive case study of Warren and Kraft 2006).
restoration in ecosystems that are strongly controlled by Second, a BEF perspective should inform the evaluation
abiotic forces. River restoration is one of the most extensive of river restoration projects. Even when aquatic organisms
forms of restoration in the USA, with at least $1 billion cannot be directly introduced, monitoring changes in
dollars invested annually (Bernhardt et al. 2005). A growing community composition following restoration activities can
body of scientific literature has documented biodiversity provide important insights into what is and what is not
effects on ecosystem function in stream ecosystems (e.g. working. For example, the absence of shredding functional
Jonsson and Malmqvist 2000, Cardinale et al. 2002). Yet feeding groups from restored streams relative to reference
because the dominant taxa in river ecosystems are easily conditions may indicate that organic matter dynamics have
dispersed, short-lived, and small it is difficult to apply these not been effectively restored, the presence of nitrogen-fixing
BEF perspectives to river restoration projects. Seeding blue–green algae may indicate that phosphorus loads are
streams with the appropriate algae, macroinvertebrates, excessively high, or the absence of a diverse hyporheic
and fish is no guarantee that those organisms will establish. meiofauna may suggest that groundwater and surface
In terrestrial ecosystems, where vegetation itself provides waters have not been effectively reconnected. While
much of the physical structure of the environment on which restoration practitioners may not be able to actively manage
other organisms depend, it is easy to see how planting the diversity of all ecosystems to affect services, recognizing
diverse native species assemblages can effectively ‘restore’ the links between biodiversity and ecosystem functioning
not only an ecosystem function (¼ productivity) but also key that exist even in ecosystems strongly controlled by abiotic
components of ecosystem structure (e.g. canopy forces can lead to improved assessment of the success or
architecture). This is not the case in rivers, where the failure of restoration projects.

Wardle 1999, Naeem 2000, Grace et al. 2007) has tion of the entire community (Lehman and Tilman
highlighted that restoring a highly diverse commu- 2000, Naeem 2006a). The rest of this chapter explores
nity does not necessarily guarantee a high level of these implications for restoration in greater detail.
functioning – environmental factors such as soil
fertility and climate are also crucial determinants of
12.3 ‘Classical’ BEF implications
ecosystem functioning (Huston and Mcbride 2002,
for restoration
Naeem 2002b). However, when environmental fac-
tors are held constant, the BEF approach suggests Since its earliest inception BEF research has largely
that greater biodiversity provides a high level of been focused on testing the hypothesis that the loss
ecosystem functioning, although achieving the high- of diversity of species (or functional groups) leads to
est level of functioning does not require the restora- changes in ecosystem functions such as productivity
 RESTORING BIODIVERSITY AND ECOSYSTEM FUNCTION 171

et al. 2006a). For example, Cardinale and colleagues

Box 12.2 Diversity of grassland plantings (2006a) found that diversity enhanced both plant
productivity and nutrient uptake. These biodiversity
Grassland restoration in the central portion of the effects can be tied to two ecosystem services that are
USA illustrates the relatively low level of diversity used in often the focus of restoration efforts. It should be
some restorations compared to their reference systems noted that while the most represented ecosystem in
and the implications. this meta-analysis were grasslands, these comprised

Native northern mixed-grass prairie in western only 34% of the studies, with the rest coming from a
Nebraska and South Dakota has approximately 37–80 broad diversity of other terrestrial and aquatic eco-
native plant species per 0.1 ha (Symstad et al. 2006), systems. Thus there is a growing body of work
whereas the recommended seed mixtures for native addressing BEF questions in other ecosystems such
rangeland plantings (> 0.1 ha) in this region have a as streams (Jonsson and Malmqvist 2000, Cardinale
maximum of 13–25 species and a minimum of four et al. 2002), wetlands (Engelhardt and Ritchie 2001,
species (http://www.nrcs.usda.gov/technical/efotg/). Callaway et al. 2003, Sutton-Grier et al. In Review),

The federal Conservation Reserve Program (CRP) pays
forests (Bunker et al. 2005, Scherer-Lorenzen et al.
farmers to plant or maintain perennial vegetative cover,
2005a), and marine systems (Duffy et al. 2001, Solan
grassland being one allowable type, in areas that would
otherwise be used for agricultural production. The program, et al. 2004, France and Duffy 2006b, Worm et al.
which affects more than 10 million ha of grassland 2006). For most systems in which restoration is being
nationwide, rewards plantings that provide ecosystem conducted, potentially relevant BEF experiments
services such as reduced soil erosion, increased wildlife have been conducted. Applying the findings from
habitat, water quality protection, soil salinity reduction, and BEF research to restoration practices should be a
carbon sequestration (Barbarika 2005). The diversity of natural extension of existing research. Indeed, a
these plantings is difficult to track, but typical values are study that examined the consequences of restoring
4–10 species. plant communities on ecosystem functioning in a

The species planted in restorations like these are often
California estuarine salt marsh demonstrated that
dominants (e.g. warm-season bunchgrasses) that drive
increasing plant richness led to higher rates of
major aspects of ecosystem functioning (Camill et al. 2004),
nitrogen uptake and greater above- and below-
but low functional diversity, particularly the lack of nitrogen-
fixing legumes in some plantings, may limit a restoration’s ground biomass (Callaway et al. 2003). Grassland
functioning potential (Kindscher and Tieszen 1998). and wetland restorations typically start from bare
ground and try to recreate natural communities
through the addition of seed. The seed mixes used
are not particularly diverse relative to the natural
or nutrient cycling (Naeem et al. 1994, Hooper and ecosystems that serve as restoration targets (Box
Vitousek 1997, Tilman et al. 1997b). Since these early 12.2). Thus, many terrestrial restoration activities are
studies, the field of BEF research has flourished, with operating in the region of diversity where varying
over 100 published experiments testing this general species richness is most likely to have a significant
hypothesis (Cardinale et al. 2006a). Contentious effect on ecosystem functioning, since most ecosys-
debates have ensued about the proper experimental tem functions saturate at relatively low levels of
design or how best to interpret the results of these species richness (Cardinale et al. 2006a).
experiments (Garnier et al. 1997, Huston 1997, However, the application of classical BEF
Wardle et al. 1997a, Thompson et al. 2005, Wright research to restoration activities may still be limited
et al. 2006), and considerable work still needs to be given our current knowledge. First, while average
done to determine the mechanisms that might link ecosystem function has been shown to increase
diversity to ecosystem functioning. Despite these with increasing diversity (Balvanera et al. 2006,
uncertainties, several recent meta-analyses have Cardinale et al. 2006a), meta-analysis of BEF
demonstrated that, on average, ecosystem function- experiments has also demonstrated that the highest
ing does increase with increasing numbers of species performing species in monoculture produces a level
in BEF experiments (Balvanera et al. 2006, Cardinale of ecosystem function that cannot be distinguished
172 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

from the level observed in the highest diversity in northern California grasslands. Their results
treatment (Cardinale et al. 2006a). Second, due to suggest that when in mixture, the species’ con-
the constraints of experimental design, BEF tributions to ecosystem functions would vary
experiments do not always include low-diversity throughout the season, providing a mechanism for
polycultures capable of outperforming the highest maintaining these nutrient cycles throughout the
diversity treatment (Chapter 2). Thus, if the goal of season. In addition, they investigated the relation-
restoration is to provide a maximum level of eco- ship between a variety of plant traits (live tissue
system services, arguments could be made for and litter chemistry and biomass, modification of
establishing a high-performing species to rapidly bioavailable C and soil microclimate) and the eco-
achieve a high level of functioning early in the system functions. The influence of individual traits
restoration process. However, because these high- on N mineralization and nitrification also varied
performers are usually dominant species, subordi- throughout the growing season, illustrating how
nate species may be more difficult to establish after response traits (to seasonal changes in moisture and
the fact, as observed in tallgrass prairie plantings temperature) are not necessarily correlated with
(Weber 1999), hay meadows (Pywell et al. 2002) and functional effect traits (Landsberg 1999, Lavorel and
coastal marshes (Keer and Zedler 2002). This is Garnier 2001, Hooper et al. 2002, Naeem and
particularly important because there is some evi- Wright 2003).
dence that the effects of greater diversity on func- Several reviews describe this and other mechan-
tioning take some time to develop (Tilman et al. isms in greater detail and show the strong theore-
2001, Cardinale et al. 2007), and because these tical support for the diversity–stability hypothesis
subordinate species may contribute to stability of (McCann 2000, Cottingham et al. 2001, Loreau et al.
functioning. 2002, Hooper et al. 2005, Chapter 6), and empirical
support for the hypothesis exists from experiments
in systems relevant to ecological restoration. In
12.4 BEF and stability of services plots in which plant species richness varied because
in restoration of nitrogen manipulations, aboveground biomass
The question of whether biodiversity contributes to was more resistant to, and recovered more fully
stability (e.g. resistance to disturbance, resilience from, a major drought in more diverse grassland
after disturbance, and moderate range of variability plots in central Minnesota, USA (Tilman and
through time) has been a topic in ecology for more Downing 1994). In the same system, but in plots in
than half a century (e.g. Macarthur 1955, May which plant species richness was directly manipu-
1972). The recent development of the BEF per- lated, temporal stability (measured as temporal
spective has provided resolution to some aspects of mean/standard deviation) of aboveground plant
this question by suggesting that species that share biomass over ten years increased linearly, from
functional effects traits (characteristics that affect approximately 3.5 to 5.8, as planted species richness
ecosystem functioning in a specific way) often differ increased from one to 16 species, with the diverse
in their functional response traits (characteristics plots having lower temporal standard deviations
that determine how they respond to a specific for a given mean biomass than the monocultures
perturbation). As a result, a relatively low number (Tilman et al. 2006b). Despite these encouraging
of species may provide a certain level of an eco- examples, there are also counter-examples. More
system function in a constant environment, but if diverse plots had lower resistance of primary pro-
these species are adversely affected by a perturba- ductivity to drought in a Swiss grassland experi-
tion (e.g. drought, flood, fire, or herbivory), that ment (Pfisterer and Schmid 2002); individual
level of functioning will only be maintained if species, rather than species richness, affected bio-
species with a similar effect on functioning respond mass stability in constructed or natural wetlands
positively to this perturbation. For example, Eviner (Rejmankova et al. 1999, Engelhardt and Kadlec
et al. (2006) identified a strong seasonality in the 2001); and rocky shore intertidal communities with
effects of individual species on N and P cycling the greatest diversity were most severely affected
 RESTORING BIODIVERSITY AND ECOSYSTEM FUNCTION 173

by heat stress (i.e. had low resistance) but were the into ecological restorations. As was discussed
quickest to recover from the stress (i.e. high resil- above, high diversity plots in BEF experiments do
ience) (Allison 2004). A recent meta-analysis of a not, on average, significantly outperform the high-
large number of studies confirmed this inconsis- est performing monoculture (Cardinale et al. 2006a).
tency – averaged across experiments, more diverse However, what is not clear from this analysis is
systems were more resistant to nutrient perturba- whether a single species can maximize the provi-
tions or invasions, but diversity had either a neutral sioning of multiple ecosystem functions. Evidence
or negative effect on resistance to drought, response from a biodiversity, carbon dioxide, and nitrogen
to warming, and variation in response to long-term manipulation experiment in a Minnesota grassland
environmental variability (Balvanera et al. 2006). context (Reich et al. 2001, Reich et al. 2004) suggests
Maintaining ecosystem services within a reason- that this is not the case. In this experiment, the total
able range of variability is an important component above- and belowground biomass produced by a
of restoration projects focused on restoring func- species and the amount of inorganic nitrate left in
tioning. The balance of evidence is currently not the soils after plant uptake were strongly correlated
very strong that biodiversity plays a large role in in the first year after planting (Fig. 12.2(a)). Such a
determining this variability. However, relatively result would suggest that a single species might be
few field-scale studies have investigated this ques- capable of both fixing high amounts of carbon and
tion, and there is no evidence that diversity improving water quality by reducing nitrogen
strongly negatively affects stability, particularly export. However, in subsequent years of the
over the long term, so the cost of increasing the experiment, this correlation broke down (Fig. 12.2
diversity of a restoration is likely only the direct (b,c)), making it more difficult to suggest a single
cost associated with adding that diversity. species maximizes both ecosystem services. In fact,
Hector and Bagchi (2007) found that maximizing
seven ecosystem functions required between 8 and
12.5 Biodiversity and the restoration
16 species at eight grassland sites across Europe. In
of multiple ecosystem functions
a recent review, Gamfeldt et al. (2008) found that
Restoration activities are not typically conducted multifunctional redundancy (i.e. the degree to
with the goal of restoring a single ecosystem ser- which multiple species could sustain multiple
vice. Rather, there is an implicit understanding functions) was generally lower than single-function
that ‘healthy’ ecosystems provide a large number redundancy (i.e. the degree to which multiple spe-
of services (Duraiappah and Naeem 2005), and that cies could sustain a single function).
restoration can serve to increase multiple ecosystem Species effects on ecosystem functions are func-
services (N.R.C 2001, Bernhardt et al. 2005). For tions of key morphological and ecophysiological
example, the restoration of Iraq’s Mesopotamian traits (Engelhardt and Kadlec 2001, Eviner and
marshes has been assessed based on five separate Chapin 2003, Diaz et al. 2004), and BEF research is
ecosystem functions: productivity of the dominant increasingly focused on how particular traits inter-
plant Phragmites australis, redox status, hydrologic act to determine the effects of diversity on ecosys-
function, salinity, and bird diversity (Richardson tem functioning (Eviner and Chapin 2003, Naeem
and Hussain 2006). Similarly, the US National and Wright 2003, Solan et al. 2004, Bunker et al.
Resource Council suggested that five major func- 2005). While attempts to determine which traits are
tions of wetlands need to be considered in most important in regulating particular ecosystem
the construction or restoration of wetlands: hydro- functions are still in the early stages, it seems rea-
logic functions, water quality functions, support sonable to assume that different processes might be
of vegetation, support of fauna, and soil functions affected by different combinations of traits. Given
(N.R.C 2001). this assumption, the extent to which single species
This demand for multiple ecosystem services can maximize multiple functions will depend on
from a single restoration may be the strongest the extent to which the traits responsible for regu-
argument for incorporating greater biodiversity lating the ecosystem functions of interest are
174 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

(a) (b) (c)

5 9 5
r = 0.78 r = 0.18 LUPE r = 0.15
8 LUPE
4
Total inorganic N (0–60 cm)

LUPE 4
7
3 ASTU
6 3
LECA
AMCA
ANCY LECA
2 PEVI
5
POPR
PEVI
ANCY 4 ASTU 2 AMCA
ANGE KOCR
1 BOGR PEVI
POPR LECA AMCA BRIN
SONU ADRE
ANOE SCSC POPR
KOCR SORH
SORE 3 KOCR
AGRE
BOIP
ASTU
AGRE
ACMI ANCY 1
0 ACMI SCSO
2 BOGR SORI ACMI POGR
ANOESONU
SONU SONU SORI
1 0
0 200 400 600 800 1000 1200 1400 0 200 400 600 800 1000 1200 1400 1600 0 200 400 600 800 1000 1200
Total biomass (g/m2)

Figure 12.2 Relationship between two ecosystem functions, total above- and belowground biomass (a surrogate for carbon storage) and total extractable
soil inorganic nitrogen (a surrogate for nitrogen removal from groundwater) from monocultures of different species in control plots (ambient levels of
atmospheric CO2 and nitrogen) of the BioCON BEF experiment from (a) 1999, (b) 2000, and (c) 2001. Species codes of the monocultures are: Achillea
millefolium ACMI; Agropyron repens AGRE; Amorpha canescens AMCA; Andropogon gerardi ANGE; Anemone cylindrica ANCY; Asclepias tuberosa ASTU;
Bouteloua gracilis BOGR; Bromus inermis BRIN; Koeleria cristata KOCR; Lespedeza capitata LECA; Lupinus perennis LUPE; Petalostemum villosum PEVI; Poa
pratensis POPR; Schizachyrium scoparium SCSC; Solidago rigida SORI; Sorghastrum nutans SONU. Note that the scale changes on the axes between years.

correlated. Several recent large-scale analyses have worth to a level of ecosystem functioning other
found significant correlations between several than a vague ‘more is better’ for primary produc-
important traits in plants (Diaz et al. 2004, Wright tivity or nutrient capture (Srivastava and Vellend
et al. 2004, Reich et al. 2006) and animals (Brown et al. 2005). In contrast, in restoration, the relative worth
2004). These correlations yield suites of traits (e.g. of various levels of ecosystem services must be
those contributing to rapid acquisition of resources assessed and agreed to by many stakeholders when
vs. those that contribute to conservation of resources any but the simplest restoration project is com-
in well-protected tissues in plants) that typically menced (Fig. 12.3). Provisioning services, such as
occur together in organisms. The uniformity of these forage production, can be easily converted into
suites across broad taxonomic groups and geo- currency value (Bullock et al. 2007). However, while
graphical gradients argue for the existence of fun- Worm et al. (2006) showed dramatic increases in
damental tradeoffs in organismal development and tourism-related revenue following the closure of
life history. Whether or not these tradeoffs hold up fisheries in marine protected areas, which they
within local species pools, where selection might attribute to increases in diversity, this conversion is
push for diversification along trait axes (Grime 2006, not as easy for other types of ecosystem services
Ackerly and Cornwell 2007), and for the traits resulting from ecological restorations. For example,
actually responsible for ecosystem functions of results from BEF research might predict grams of
interest in restoration (Eviner 2004), remains an open carbon fixed per square metre, grams of nitrogen
and important question. removed through denitrification, and grams of the
greenhouse gasses N2O and methane produced by
different combinations of species used in a wetland
12.6 The economics of BEF in restoration
restoration project. Until markets exist that allow
For BEF research to be useful for ecological resto- translation of these ecosystem processes into a
ration, ecosystem functions must be related to the common currency, determining which mixture of
ecosystem services desired as the outcome of res- species maximizes benefits while minimizing costs
toration. A key issue in performing this translation is, at best, just a guess. The growth of carbon
is that BEF research often does not assign a specific trading markets (Bonnie et al. 2002) and early
 RESTORING BIODIVERSITY AND ECOSYSTEM FUNCTION 175

Total benefit ? academic journals (Palmer et al. 2004). This point is

reinforced by a recent survey of stream restoration
?

Nitrogen removal
practitioners that showed that less than 1 per cent
Carbon storage

? of over 300 restoration projects had specifically

been informed by results published in scientific
journals (Bernhardt et al. 2007). So what can be
done to improve the situation?
For scientists, we make a few suggestions. First,
continue basic BEF research, but keep in mind the
Monoculture Polyculture
information needed by restoration practitioners.
Figure 12.3 Hypothetical restoration scenario involving two ecosystem Deeper understanding of how functional traits
services: carbon storage (circles) and nitrogen removal (squares). Managers acting alone and in combination affect ecosystem
could choose between planting a monoculture of species 1 (filled symbols) functions that are related to ecosystem services is
that provides high levels of carbon storage but low levels of nitrogen particularly important. Although general relation-
removal, a monoculture of species 2 (open symbols) that provides low
ships between diversity and functioning explain
levels of carbon storage but high levels of nitrogen removal, or a mixture of
both species that provides intermediate levels of both carbon storage and why the restoration of biodiversity is important for
nitrogen removal. The total benefit of the ecosystem services provided by restoring ecosystem functioning, restoration practi-
these different management choices (straight lines) is unknown and will tioners ultimately need to know which specific
depend both on the shape of the relationship between diversity and these species combinations to restore to have confidence
two functions and on the relative economic weight placed on the two
in the outcome of restoration projects. However,
services.
BEF theory, while explanatory, is not yet predictive
(Hooper et al. 2005) and is therefore not yet ready to
attempts at nitrogen trading schemes such as the be embraced by the management community. Fur-
EPA’s Water Quality Trading Program (active in thermore, experimental perturbations in BEF
areas of 10 states in the USA) suggests that eco- experiments, and monitoring of experiments over
nomic valuations of at least some of the non- long time periods in which the environment fluc-
provisioning ecosystem services provided by restored tuates naturally, will help resolve what role biodi-
ecosystems are being developed. An even more dif- versity plays in stabilizing ecosystem services.
ficult task is deriving a common currency for services However, because species and communities
such as protecting higher trophic levels or maintain- respond to environmental fluctuations in seemingly
ing hydrologic services, although tools for evaluating idiosyncratic ways, investigations that tie these two
different options in the face of such uncertainties do themes together, by seeking patterns in traits that
exist (Lynam et al. 2007). determine species’ responses to environmental
variations, will yield the most relevant information
for restoration.
12.7 Recommendations
BEF research focusing on microbial diversity is
We argue that understanding the relationship particularly crucial because many of the most
between biodiversity and ecosystem functioning is critical ecosystem services are underpinned by
important in enhancing restoration success in many microbial processes (e.g. the nutrient transforma-
ecosystems and that restoration activities can serve tions that improve water quality). Our under-
as powerful tools for exploring some of the central standing of both how plant and animal diversity
BEF questions. However, information exchange affect microbial community structure and how
between the scientific community and restoration microbial diversity directly affects ecosystem
practitioners is too little and too slow for BEF functioning in real systems is relatively weak
research to be relevant in adaptive management of (Fierer et al. 2007, Jackson et al. 2007). To date there
degraded ecosystems. Ecologists are recognizing has been little focus on the importance of restoring
that performing policy-relevant science involves microbial communities or how to go about doing
more than simply publishing in high-profile so (Hasselwandter 1997). Restoration of the
176 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

microbial community in meadows was not erosion, little attention has been paid to whether the
achieved by a simple soil microbe addition tech- nutrient content of the biomass is sufficient for the
nique (Pywell et al. 2007), but experiments have purported foragers (see Bullock et al. 2007 for an
shown that microbial community composition is exception) and direct measurements of soil move-
related to both the diversity of the restored plant ment or long-term C sequestration are rare (though
communities and to particular ‘facilitating’ plant more common in wetland studies). Given the need of
species (Smith et al. 2003, Bardgett et al. 2006). A many restorations to restore multiple services, this
deeper understanding of the controls and con- connection needs to be made simultaneously for
sequences of microbial diversity is an area where multiple functions and their related services.
BEF research is well-poised to make important Addressing these issues is already one of the central
contributions to restoration ecology. thrusts of the next generation of BEF research (Naeem
Another aspect of diversity that may be critical to and Wright 2003) and should not require significant
restoration success, but has not been as extensively changes to how we proceed with our science beyond
studied in BEF research, is the importance of genetic the functions and properties measured in typical BEF
diversity. Many ecosystems, including many that are experiments.
important targets for restoration, are dominated by a Fourth, BEF researchers must evaluate the rele-
single species that controls ecosystem function, e.g. vance of experiments to real-world conditions.
giant kelp in kelp forests, Ponderosa pine in many There is some conflict between the typical BEF
forests of the Western US, seagrasses such as Zostera experiment, which is carefully designed to disen-
marina in shallow estuarine systems, and Spartina in tangle the effects of individual species, functional
intertidal zones. A growing body of work is showing traits, and diversity per se on the functions mea-
that genetic diversity within a species can be an sured, and restoration projects, which are con-
important regulator of ecosystem function (Hughes et cerned with achieving a desired result with
al. 2008). Work on Zostera, an important species in available materials and limited financial resources.
estuarine restoration, showed that clonal diversity Restoration practitioners may look at the high
measurably affects ecosystem processes or the stabil- density of expensive species (many forbs, for
ity of those processes (Hughes and Stachowicz 2004, example) planted in some BEF experiments and
Reusch et al. 2005). Williams (2001) demonstrated that question the applicability of the results to their
reduced genetic variation in Zostera used in restora- work: does the diversity effect require this rela-
tion efforts resulted in decreased population growth tively high input of normally subordinate or rare
and individual fitness. For both cottonwood (Populus species? They might also question the relatively
fremontii x augustifolia) (Schweitzer et al. 2005a) and controlled situations of the field experiments:
apsen (Populus tremuloides) (Madritch et al. 2006), would the results be the same if vertebrate herbi-
genotypic richness can affect decomposition rates and vores were not excluded from the plots, or if colo-
nutrient cycling. Clonal diversity of Solidago altissima nizing species were not removed? Finally, a
were shown to affect, not only primary productivity, practitioner would never think of restoring a Spar-
but the diversity of higher trophic levels (Crutsinger et tina alterniflora marsh without Spartina alterniflora,
al. 2006). Given these compelling examples, research but many BEF studies include treatments analogous
on the consequences of genetic diversity of species to this situation. Of greater interest to a restoration
commonly used in restoration is likely to yield bene- practitioner would be the question of how strong
fits both to basic science and restoration. the diversity effect is when the only portion of
Third, to make the results of any BEF research diversity manipulated is the subordinate and rare
applicable to practitioners, the connection from bio- species. These subordinate species may be essential
diversity to function to services needs to be stronger. to certain key functions which define the success or
For example, although the positive effects of plant failure of the restoration. For example, grassland
diversity on above- and belowground biomass pro- restoration in the UK to meet national Biodiversity
duction in grassland experiments have been vaguely Action Plan targets requires the presence of food
related to forage production, carbon storage, and soil plants of certain declining butterflies and other
 RESTORING BIODIVERSITY AND ECOSYSTEM FUNCTION 177

insects, but these plants are often uncommon and This scheme exemplifies the biodiversity or ecosystem
particularly difficult to establish (Pywell et al. 2003). service dichotomy. Certain activities aim to restore a
Thus, BEF researchers seeking to provide answers service, such as sowing field margins with a mix of
for restoration practitioners and other natural plants designed to provide pollen and nectar for bees
resource managers need to ensure that they design and butterflies or to provide winter seed for birds. In
their experiments with these issues in mind. these cases the plant mixture does not resemble any
Concurrently, restoration practitioners and ecolo- seen in (semi-) natural systems and often contains
gists can potentially contribute significantly to non-natives. Other activities are focused on biodi-
strengthen BEF research. For them, we stress the versity, such as the sowing of specific plant mixtures
utmost importance of monitoring and reporting into bare arable land or species-poor grasslands to
short- and long-term effects of various restoration restore particular target species-rich grasslands. Cer-
projects and practices. In the US, the federal govern- tain authors have criticized the effectiveness of
ment pays private land owners millions of dollars European agri-environment schemes (e.g. Kleijn et al.
each year to plant and maintain perennial grasslands 2006). This is partly because these authors have con-
through the Conservation Reserve Program. A land- fused the aims of different activities (e.g. expecting the
owner’s proposal is more likely to be funded if s/he bird-seed mixtures to restore rare arable weed com-
plants a higher diversity of species (U.S.D.A 2006), munities), but also because monitoring of outcomes
but follow-up on the establishment success and has been poor. The limited monitoring (e.g. Critchley
environmental benefits of individual plantings is rare, et al. 2004, Feehan et al. 2005) of vegetation has shown
and only recently have comparisons among the eco- some success, but suggests that better targeting and
system services provided by plantings of different more precise methods are required. This is leading to
diversity levels been explored. In the USA, a major planning for more extensive and repeated monitoring
source of funding for stream and wetland restoration programs and consideration of how biodiversity and
is associated with mitigation of wetland losses under ecosystem service aims might be integrated (e.g. for
the Clean Water Act (N.R.C 2001). Guidelines for soil conservation).
successful restoration vary from state to state, but Clearly, BEF research still has many avenues to
typically involve recommended species lists and some explore before the majority of questions surround-
assessment of total vegetation cover. Some states are ing the relationship between biodiversity and eco-
currently developing improved vegetation assess- system functioning are answered. Just as clearly,
ments that include repeated measurements of the restoration ecology still has a long way to go before
cover of all planted and unplanted species. In the case the results of reconstructing an ecosystem can be as
of North Carolina, this improved monitoring scheme predictable as the construction of a bridge or even a
has been developed in coordination with the Carolina space station. Although not all restoration projects
Vegetation Survey to ensure that monitoring data can are suited to answering basic science questions
be directly incorporated into an existing vegetation regarding the relationship between biodiversity and
database that is actively being used in ecological ecosystem functioning, they are crucial to making
research (Lee et al. 2007). As a member of the European BEF science applicable to real-world situations.
Union, the UK Government pays out many millions Direct partnerships between researchers testing BEF
of pounds a year in funding restoration on farm- concepts and restoration practitioners are crucial for
land under the Environmental Stewardship scheme ecological restoration to live up to its potential as an
(http://www.defra.gov.uk/erdp/schemes/es/). acid test for BEF ecology.
 CHAPTER 13

Managed ecosystems: biodiversity

and ecosystem functions in landscapes
modified by human use
Louise Jackson, Todd Rosenstock, Matthew Thomas,
Justin Wright, and Amy Symstad

13.1 Introduction that produce food, fibre, and a range of other

ecosystem services (Jordan et al. 2007).
There is growing agreement that the long-term
Human utilization of the Earth’s ecosystems is
sustainability of terrestrial landscapes that provide
progressing at a rapid rate (MEA 2005). This has
ecosystem services, such as food, fibre, and timber,
resulted in enormous loss of biodiversity, both in
will be increased by the conservation of existing
ecosystems that are managed for provisioning ser-
biodiversity and the adoption of biodiversity-
vices and in neighbouring unmanaged ecosystems
based practices (Collins and Qualset 1999, Kates
that are impacted by these management activities
and Parris 2003). The broad concept of sustain-
(Bawa et al. 2007). For example, the increase in
ability is characterized by a set of complementary
cropland (250 per cent) and pasture (440 per cent)
goals: optimizing production of food, fibre, and
in the last 300 years has resulted in the loss of
forest products while protecting the resource base
approximately 30 per cent of forests and 40 per cent
and social wellbeing. Biodiversity is increasingly
of steppe worldwide (Lambin et al. 2003) (Fig. 13.1).
recognized as a key component for the sustain-
At present, 10 per cent of the world’s terrestrial
ability of managed ecosystems for future genera-
land base is used for intensive, high-input agricul-
tions. For example, in the Millennium Ecosystem
ture, 15 per cent is associated with low-input agri-
Assessment (MEA 2005), biodiversity is viewed as
culture, and 40 per cent is in agricultural mosaics
an important coping strategy against agricultural
used for other extractive purposes, such as grazing
risks in an uncertain future. However, some would
(Mooney et al. 2005, Wood et al. 2000). With the
argue that this strategy should be viewed as
world’s population of 6.7 billion people projected to
‘received wisdom’ rather than substantiated proof
grow to 9 billion by 2050, increasing demand for
of process (Wood and Lenné 2005). Indeed, while
resources will continue to lead to major changes in
humans have always relied on biodiversity for
land use and conversion of natural biomes to
provisioning services within managed ecosystems,
managed ecosystems. Irrigated and pasture lands
understanding how biodiversity influences the
are both expected to double in area by 2050, with a
ecological functions that affect these services, such
net loss of 109 hectares of wildlands worldwide
as pollination, pest control, nutrient cycling, and
(FAO 2003), thereby increasing the global pressure
water purification, is incomplete. Yet with further
on biodiversity in natural ecosystems. To keep pace
research, the provision of multiple ecosystem
with population growth, it is expected that more
functions (multifunctionality) by different sets of
land will be converted to agriculture and further
species (Hector and Bagchi 2007), may become one
intensification of already converted land will
of the most viable tools for managing ecosystems
increase through greater reliance on non-renewable,

178
 MANAGED ECOSYSTEMS 179

70

60 1700

50 1990

40
%

30
Figure 13.1 Global historical (1700) and current (1990) percentage
20 of potentially arable land as a function of land use type, and the
percentage change in different types of land use during this period
10 (listed below each land use type on the x-axis). Steppe refers to natural
0 steppe/savannah/grassland ecosystems, while pasture refers to ecosys-
Forest Steppe Crops Pasture tems managed for livestock production. Based on data compiled by
(–31%) (–42%) (+250%) (+440%) Lambin et al. (2003).

off-farm inputs unless more sustainable paradigms relevant to management. Finally, acknowledging the
are developed (Clay 2004). influence of social and economic factors in managed
Incorporating biodiversity-ecosystem function systems, we consider the need to place ecological
(BEF) relationships in efforts to increase the sus- insights within an interdisciplinary context to link
tainability of managed ecosystems requires com- BEF research to end users.
bining biophysical and social sciences (Jackson et al.
2007, McNeely and Scherr 2003). Involving end
13.2 Management intensification
users when determining the context and design of
as a driver of biodiversity loss
research is widely recognized as an approach that
ensures research outcomes are relevant for decision Management intensification is defined as the pro-
makers. This is especially true for ecological pro- cess by which managed systems increasingly rely
cesses and biodiversity assets that determine the on the use of non-renewable or purchased inputs
wellbeing of resource-limited people, for whom that are indicative of higher energy and capital
poverty restricts their land management options. A costs per unit land area (e.g. synthetic fertilizers,
landscape perspective provides better insights on pesticides, and hybrid seeds). Here, substitution of
management options than solely ecosystem- or mechanization and fossil fuels for human labour is
plot-based research (Robertson and Swinton 2005, considered to be part of intensification, although
Tscharntke et al. 2005). These criteria are difficult for this might be viewed differently within a social
most ecological studies to achieve. How, then, do science context. Intensification is a huge source of
ecologists conduct meaningful research on biodi- biodiversity loss within managed ecosystems and
versity and its functions in managed ecosystems so in adjacent wildland ecosystems (Lambin et al. 2003,
that ecological processes are better understood and Mooney et al. 2005, Wood et al. 2000). Agricultural
outcomes are directly conveyed to land users and intensification leads to a loss of diversity of crop
other stakeholders? varieties, animal breeds, and associated agroeco-
This chapter addresses this central question con- system biodiversity (Brush 2004, Jackson et al. 2007)
sidering three essential components. First, we exam- such as farm birds (Butler et al. 2007, Green et al.
ine the effects of management and intensification 2005), insects (Wilby and Thomas 2002), and soil
processes on biodiversity in managed ecosystems, as biota (Loranger et al. 1998, Wardle et al. 1999).
well as the possible impacts of measures aimed at Additionally, intensification puts wild biodiversity
mitigating negative effects. Second, we review what is at risk through gene flow from domesticated vari-
known about the BEF relationships within managed eties to wild species (Thies and Devare 2007),
ecosystems and highlight challenges for future exposure to potentially virulent pathogens such as
research to deliver insights that embrace real-world avian flu, and adverse effects of agrochemicals on
complexity at temporal and spatial scales that are non-target species (McLaughlin and Mineau 1995).
180 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Since the full set of ecosystem functions are rarely polyculture, abandoned/fallow, or late successional
accounted for, understanding the range of impacts vegetation)
of intensification is difficult. Moreover, society has 3) Management: an integrative parameter subjec-
rarely mandated that the full social value of biodi- tively assigned according to the degree of manage-
versity conservation be assessed (Pascual and ment intensity. This degree was based on a
Perrings 2007). combination of fertilizer and pesticide practices,
disturbance, and energy source (human labour vs.
mechanization). Here we categorize mechanization as
13.2.1 Meta-analysis: biodiversity across
a form of intensified management due to the use of
landscape gradients
fossil fuel. Categories were high, medium, and low.
To better understand the effects of intensification, we
Clustering analyses used two different multivariate
conducted a meta-analysis of field studies across
statistical methods: Partitioning Along Metroids
ecosystem types in agricultural landscapes. Studies
(PAM) in R (R Development Core Team 2006) and
were located using a keyword search in ‘Web of
Hierarchical Ward Clustering in JMP (SAS Institute
Science’ (Thomson Scientific), using the search
1995). We chose these two methods because of the
phrases “biodiversity or species richness and (eco-
slightly different algorithms with which they parti-
system function or ecosystem service or productivity
tion observations into clusters. These clustering tech-
or yield or pollination or nutrient cycling)”, or
niques divided the data set into four clusters that were
“biomass and (agricultu* or agricultur* intensificat*)”.
arranged along a gradient of agricultural intensifica-
We also followed up on other references cited within
tion: (1) Forest, (2) Grassland/Pastures/Abandoned,
these studies. Studies were excluded if they used:
(3) Complex Agroecosystems, and (4) Intensified
inference of biodiversity across gradients from mod-
Agroecosystems. The first two categories represent
els; measurement of effects at a certain distance from a
ecosystems dominated by natural vegetation and
targeted ecosystem rather than within specific eco-
processes, while the two latter categories are both
systems; cursory descriptions of land use; or, data that
arable ecosystems, but differ in the management type
were difficult to attribute to taxa or functional groups
and source of inputs. Complex Agroecosystems were
(e.g. restriction length fragment polymorphism for
managed with a greater emphasis on renewable
soil microbial studies).
inputs, rotations, reduced tillage, polycultures, or
Out of 50 papers examined, these search criteria
hedgerows, and the category contained a wide range
yielded a total of 26 studies and 109 ecosystems
of management types. Contrasting examples classi-
that ranged from mature, climax forests to inten-
fied in this category are ‘traditional polyculture cof-
sively managed cropland (Table 13.1). The taxa
fee’ (Armbrecht and Perfecto 2003, Armbrecht et al.
included birds, reptiles, amphibians, insects, soil
2005) and ‘organic wheat’ (Holzschuh et al. 2007).
microbes, and vascular plants, and spanned many
PAM clustering resulted in 27 ecosystems in
biomes and continents. Studies contained two to
Forest, 62 in Grassland/Pasture/Abandoned, 44 in
nine ecosystems (mean ¼ 4.2, sd ¼ 2.1).
Complex Agroecosystem, and 43 in Intensified
Classification of ecosystems along an intensifica-
Agroecosystem, while Hierarchical Ward clustering
tion gradient used a multivariate clustering approach,
resulted in 28, 62, 27, and 59, respectively. The two
based on three parameters described for each eco-
methods thus gave fairly similar results, although
system within each study. These parameters were:
they varied in how systems were placed within the
1) Land use: a descriptive classification of the land two agricultural categories. The PAM clusters were
form and commodity into one of five categories chosen for further analyses because of the robust
(forest, grassland, perennial crop, annual crop, or nature of this methodology for smaller data sets and
fallow) the high proportion of the variation (80 per cent) that
2) Successional level: a snapshot of the temporal was explained by the first two components. Each
(past, present, and potential future) successional system’s cluster designation was examined for
stage into one of four categories (monoculture, accuracy. Three ecosystems were moved to a more
Table 13.1 Studies included in the meta-analysis, including ecosystem types, target species, the basis for assertions linking diversity to ecosystem functions, and the number of systems utilized in the meta-
analysis.

Reference Management category Target species

Forest Pasture/ Complex Intensified Birds Reptiles/ Insects Vascular Soil Ecosystem Number of
Grassland/ agroecosystem agroecosystem Amphibians Plants Microbes Function1 Systems2
Fallow

Armbrecht and Perfecto (2003) x x x 3 3

Armbrecht et al. (2005) x x x x 2 4
Baur et al. (2006) x x x x 2 4
Bullock et al. (2001) x x 3 2
Carney et al. (2004) x x x x 3 3
Debras et al. (2006) x x x 1 5
Fédoroff et al. (2005) x x x x x 2 6
Gabriel et al. (2006) x x x 2 4
Genghini et al. (2006) x x x 2 3
Gillison et al. (2004) x x x 1 7
Glor et al. (2001) x x x x x 1 9
Gordon et al. (2007) x x x x 3 5
Harvey et al. (2006) x x x x x 2 6
Holzschuh et al. (2007) x x x 3 2
Hutton and Giller (2003) x x 1 3
Joyce (2001) x x 1 3
Kremen et al. (2002) x x x 3 3
Loranger et al. (1998) x x x x 1 6
Perner and Malt (2003) x x x x 1 7
Philpott et al. (2006) x x x 3 2
Rundlof & Smith (2006) x x x 2 4
Sall et al. (2006) x x 3 2
Snelder (2001) x x x 3 2
Steenwerth et al. (2003) x x x x 1 9
Wardle et al. (1999) x x x 1 2
Wilby et al. (2006) x x x x 1 3

1
1 ¼ Cited, 2 ¼ Not cited, 3 ¼ Tested
2
Not all systems or treatments in a published paper were included. When many were similar, the extreme examples were used. For studies with a temporal gradient, the last time point was used.
182 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

appropriate cluster when a unique set of circum- not significant, probably due to the large differ-
stances was not captured in the simple criteria given ences in sample sizes. Thus there is a risk that the
above. Baur et al.’s (2006) extensive hay ecosystem means of the management categories are actually
was reassigned from Complex Agroecosystem to equal, but the less conservative t-test results at least
Grassland/Pastures/Abandoned due to use of show major trends in the data.
minor management inputs. The mogote hilltop (Glor For all of the management categories designated
et al. 2001) was reassigned from Forest to Complex by the PAM clusters, the mean ESs was within a
Agroecosystem since it was ‘relatively undisturbed’. range of –0.37 to –0.65 (Fig. 13.2). This indicates that
A hayfield (Steenwerth et al. 2003) that was classified the mean species richness for a given ecosystem
as Grassland/Pasture/Abandoned was reassigned represented about 50 to 75 per cent of the maxi-
to Complex Agroecosystem because it had recently mum observed for any ecosystem in that study,
been tilled and seeded (Table 13.1). regardless of the type of taxa surveyed. Biodiversity
To determine the effect size statistic (ESs) of bio- tended to be lowest in the Intensified Agroecosys-
diversity across this agricultural intensification tems, but was not significantly different from the
gradient, the mean species richness for each eco- more Complex Agroecosystems, based on t-tests
system, s, within each study, i, was extracted comparing the mean ESs. The arable ecosystems
(Osenberg et al. 1999). From these means, a pro- tended to have lower species richness compared to
portional effect size statistic for each ecosystem ecosystems that were dominated by natural vege-
within the study, i, was calculated as the log of the tation such as forests or grasslands, but only the
ratio of mean species richness for the ecosystem, tis, Intensified Agroecosystems were significantly dif-
divided by the species richness of the ecosystem ferent from the natural ecosystems.
with the absolute maximum species richness, mi: Even in Complex Agroecosystems, which usually
had lower use of pesticides, herbicides and fertili-
 
tis zers than Intensified Agroecosystems, agricultural
ESi;s ¼ ln
mi disturbance may be one of the main reasons for
the trend towards a decline in biodiversity. For
For each of the four management categories, the example, hilltops in a national park in the
means and standard errors of this effect size sta- Dominican Republic had many more lizard species
tistic were calculated, and t-tests were used to than were ever found in any agricultural habitats,
compare these means. Pairwise t-tests were com- and even abandoned agricultural areas still con-
puted for every combination (P  0.05) (Fig. 13.2). tained only 69 per cent of the region’s species (Glor
A Tukey’s HSD test for multiple comparisons was et al. 2001).

–0.2
a a ab b
Effect size: ln(mean/max)

–0.3
Figure 13.2 Response of species richness to manage-
–0.4 ment intensification quantified by meta-analysis of field
studies across four ecosystem types in agricultural landscapes,
–0.5 showing the mean effect size statistic for each ecosystem,
based on the mean species richness for an ecosystem within a
–0.6 site in relation to the maximum observed richness in the study
(see text). Ecosystem types were determined by Partitioning
–0.7 Along Metroids (PAM), and four clusters were identified:
Forest – Grassland/Pastures/Abandoned – Complex Agroe-
cosystems – Intensified Agroecosystems. Studies included
–0.8
many types of taxa and biomes (Table 13.1). Effect size means
Forest Grassland, etc. Complex Ag Intensified Ag
that share lower-case letters do not differ significantly (P 
Management category 0.05) based on pairwise t-tests; error bars are standard errors.
 MANAGED ECOSYSTEMS 183

Few studies utilized enough land use types in ently are small within the context of a greater land-
close geographic proximity to detect small-scale scape spectrum. A comparison between sets of
responses to intensification. Two exceptions, how- organic and conventional farms showed that up to
ever, showed different patterns. In six landscape 37 per cent of the beta diversity of plant species was
types, ranging from mature forest to arable crop- explained at the farm scale and up to 25 per cent at
land in a national park in Central France, plant the regional landscape scale (Gabriel et al. 2006),
biodiversity was highest in meadows and pastures, suggesting that the landscape matrix affects biodi-
which were managed under intermediate distur- versity, and that field management only partly
bance intensity (Fédoroff et al. 2005). This reconciles explains species richness.
well with the intermediate disturbance hypothesis, The trends for differences among management
which proposes that biodiversity is highest when categories (Fig. 13.2) suggest that practices such as
disturbance is neither rare nor frequent, such that agroforestry and complex rotations support greater
both highly competitive and more disturbance- biodiversity than does intense agricultural man-
adapted species can co-exist (Connell 1978). In agement, but they still create enough disturbance
contrast, in Sumatra, one of the world’s top five that species diversity tends to be reduced compared
biodiversity ‘hotspots’ (Myers et al. 2000), plant to pasture/grasslands or forests. One explanation
biodiversity increased progressively from simple may be that arable land use favours broad-niched,
monoculture farming systems through more com- ruderal (i.e. ‘weedy’) species that become ubiqui-
plex agroforests to late secondary and complex tous, even in situations where greater spatial het-
forests (Gillison et al. 2004). In this case, the diver- erogeneity in the past may have supported species
sity of the closed canopy rain forest surpassed any adapted to unique managed and unmanaged
of the disturbed systems. Both of these regions have habitats (Grau et al. 2003).
a long history of management (arable fields, pas-
toralism, and forest harvest in France, and rotating
13.2.2 Mitigation options
slash and burn agriculture in Sumatra (Palm et al.
2005)), but the intensity of management pressure in Complex Agroecosystems tended to have higher
France may have been more consistent in space and levels of biodiversity than the Intensified Agroeco-
time. This may have caused a relatively higher loss systems in the same agricultural landscape (Fig. 13.2).
of species dependent on unmanaged systems, as If this is true across a wider range of landscapes than
well as more selective pressure for evolution of examined here, then at least some forms of wildlife-
species adapted to intermediately disturbed mea- friendly farming may produce reasonable levels of
dows and pastures. More studies like these are agricultural commodities (although measurements of
needed to understand this discrepancy in the effect agricultural productivity are absent from our analy-
of management intensity on landscapes differing in ses) and still conserve a certain level of biodiversity.
their inherent species richness. The wildlife-friendly farming concept proposes that
Organic farms, which were usually classified as certain practices, such as lower agrichemical inputs,
Complex Agroecosystems, generally had higher reduced tillage, and polycultures instead of mono-
biodiversity than conventional farms. This was true cultures, would reduce impacts on non-target biota
for birds (Genghini et al. 2006), flower-visiting bees and could allow the expansion of low-intensity pro-
(Holzschuh et al. 2007), dung beetles (Hutton and duction into wildlands to meet food demands with-
Giller 2003), and butterflies (Rundlof and Smith out a concomitant loss of biodiversity (Donald 2004,
2006). Reviews specifically addressing the organic– Green et al. 2005).
conventional difference have shown that organic In contrast, the alternative approach to biodiver-
farms characteristically do harbour greater biodi- sity conservation in agricultural landscapes, land
versity than conventional farms (Gabriel et al. 2006, sparing, is to increase intensification while leaving
Hole et al. 2005). However, since many of the studies larger areas uncultivated for wildlife habitat. Land
in the meta-analysis encompassed a much broader sparing requires further intensification (e.g. more
range of ecosystem types, these differences appar- agrichemical inputs and monocultures) on lands
184 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

currently under low-input, extensive production, but benefits for wild species, which in turn provide eco-
promises little change in the area of cultivated lands, system services in human-dominated landscapes.
either locally or globally, to meet food demands. This is the essence of the ‘ecoagriculture’ concept
This may cause wildlife populations to decrease in (McNeely and Scherr 2003). Strategies thought to
and around farmland, but may ultimately reduce the increase both agricultural productivity and save bio-
human impacts on biodiversity overall (Green et al. diversity of wild species are often hampered, how-
2005, Mooney et al. 2005). Intensification, however, ever, by lack of inventories or local knowledge about
which requires more water, nutrient, and agro- regional biodiversity, as well as a lack of information
chemical inputs, has effects outside the allegedly on multiple ecosystem services provided by habitats
fixed area that is being cropped. Our meta-analysis targeted for conversion. Without such information, it
suggests that landscapes under arable production is difficult to determine what the impacts of different
have already lost substantial biodiversity; further management options might be.
intensification and homogenization across land-
scapes may result in even greater biodiversity losses
13.3 Biodiversity-ecosystem function
(e.g. Matson and Vitousek 2006, Rand et al. 2006,
relationships in managed ecosystems
Tscharntke et al. 2005). Another issue is that set-aside
lands can be put back into production, for example, Landscape gradients allow evaluation of biodiver-
the Conservation Reserve Program in the USA has sity and ecosystem services in relation to land use.
recently allowed grazing on some lands, as cattle In the same meta-analysis as described above, we
feed is in short supply due to artificially high corn tallied BEF relationships for each of the studies by
prices driven by interest in biofuels. recording if (1) there was a citation given for a
The concepts of wildlife-friendly farming and land relevant ecosystem function or service in the dis-
sparing may both be too simplistic in terms of their cussion section (Cited), (2) if no citation was made
potential tradeoffs between agricultural production for a relevant ecosystem function or service (e.g. the
and biodiversity conservation for other ecosystem main interest was in conservation or the intrinsic
services. Many regions are experiencing both rapid value of biodiversity), and an ecosystem was
expansion and intensification of agriculture across inferred by the authors (Not cited), or (3) if the
large areas (Morton et al. 2006), suggesting that nei- study tested ecosystem function or services (Tested)
ther pathway plays out as hypothesized when the (Fig. 13.3). Pollination/predation, productivity,
configuration of ecosystems in these agricultural stability/resilience, and nutrient cycling were con-
landscapes is changing rapidly. Intensification often sidered as the categories of ecosystem functions and
results in the complete loss of fragments of natural services. Since more than one ecosystem function or
vegetation, especially when the efficiency of agri- service was sometimes given, the total tally was
cultural production increases with the volume of greater then number of studies analyzed. For the
goods (i.e. economy of scale) so that land sparing ‘Not cited’ category, we subjectively differentiated
does not actually materialize. For example, historical the studies into possible ecosystem function cate-
accounts of agricultural intensification often dem- gories based upon the target species and their
onstrate that transformation is rapid and ubiquitous ecological roles, either as inferred or discussed. For
across a landscape, such as the clearing of native example, ants in coffee systems may impact pre-
vegetation for grain and livestock production after dation and pollination.
the Gold Rush in California (Vaught 2007). Conse- Only one-third of the studies actually tested an
quently, land sparing may be quite difficult to ecological function of biodiversity (Fig. 13.3). Most
achieve at the landscape level when a ‘boom’ cycle is commonly, measurements were made of pollina-
under way to intensify production. tion and predation, followed by productivity and
The challenge is to increase agricultural production nutrient cycling. Stability and resilience were never
in a way that utilizes biodiversity for sustainable tested, yet they were cited as potential functions in
alternatives to non-renewable and environmentally several papers in which no tests of ecological
damaging inputs, and that increases the positive functions were made. The lack of information on
 MANAGED ECOSYSTEMS 185

14
12 Cited Not cited Tested
Number of studies

10
8
6
4 Figure 13.3 Abundance of studies in the meta-analysis
2 invoking Tested, Cited, or Not Cited relationships between
0 biodiversity and ecosystem function. Tested studies
Pollination/ Nutrient Stability/ Productivity relied on actual measurements, Cited studies relied on
predation cycling resilience literature to support the relationship, and Not Cited studies
Ecosystem function inferred a relationship.

ecosystem functions and services along intensifica- and adaptive management to maintain evenness
tion gradients is evident from these studies; this levels, could increase production and reduce the
poses a major challenge for the ecological research propensity for invasions of undesirable species in
community, as well as for policy makers. agricultural grasslands.

13.3.1 Relevance of controlled experiments 13.3.2 Research approaches for biodiversity

to managed ecosystems and ecosystem functioning in managed
ecosystems
Many of the recent advances in the understanding
of BEF relationships have come from fairly narrow- In a distinctly different set of approaches, a grow-
scale, controlled experimental frameworks, such as ing number of ecological studies in managed eco-
grassland experiments where plant species and systems have developed methods to show BEF
functional group combinations are assembled in associations based on functional traits of organisms
homogeneous environmental conditions and the (Naeem and Wright 2003). For example, a set of
response variable is usually standing biomass stock analytical tools was developed to rank species
(Hooper et al. 2005 and other chapters in this book). according to their ecosystem function, and to
The extensive, low-input, species-rich assemblages determine those species that contribute dispropor-
used for this research make it difficult to infer tionately to function relative to their abundance
implications for ecosystem services in managed (Balvanera et al. 2005). Another approach was to
ecosystems, although there are exceptions (e.g. use indices of key features of plant biodiversity and
biofuel production potential from low-input, high- functional types that relate to land use types and
diversity mixtures of native grassland perennials their associated ecosystem services, such as above-
(Tilman et al. 2006a)). ground carbon storage and soil nutrients (Gillison
A novel approach to designing and analyzing BEF et al. 2004). Other studies have used landscape
relationships examined the effects of adding a small gradients to infer how changes in biodiversity relate
number of grass and legume species to species-poor, to management practices and ecosystem functions
intensively managed grasslands across 28 European such as productivity or soil carbon storage (Bullock
field sites, using different relative species abun- et al. 2001, McCrea et al. 2004, Steenwerth et al.
dances (Kirwan et al. 2007). The results showed 2003). In one such study, arthropod diversity did
transgressive overyielding (i.e. higher performance not recover after many years following disturbance,
of mixtures compared to the highest-yielding even though a typical indicator of recovery from
monoculture) in three of the four geographic loca- disturbance, soil carbon, increased (Loranger et al.
tions (Fig. 13.4), a positive effect of species evenness 1998) (Fig. 13.5). An ambitious and more controlled
on production, and a negative effect of diversity on approach was to plant genetically diversified rice
the abundance of unsown species. Thus small crops in all the rice fields in five townships in
increases in plant diversity, as well as sowing rates China; rice blast disease was > 90 per cent less
186 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

P < 0.01 P < 0.01 NS P < 0.01

14

12
Average yield (t ha–1)

Figure 13.4 Evidence for transgressive overyielding, in

10 which performance of overyielding mixtures exceeds that
of the highest-yielding monoculture. Mean yield is shown
8 over 28 intensive grassland sites in four locations (mid-
European (ME), north European (NE), moist Mediterranean
6
(MM), and dry Mediterranean (DM)) where two grass
4 species and two legume species were sown into species-
depauperate intensively managed systems. For each loca-
2 tion, a unique group of four species was sown at different
densities to create 11 mixture communities (closed symbols
0 (^) and four monocultures (open symbols (). From
ME NE MM DM Kirwan et al. (2007). Requested by Jackson et al. from
Kirwan et al. (2007). Copyright permission granted.

50
20
Arthropod groups shared
Arthropod groups gained
Soil C (mg C g–1 soil)
Soil carbon 40
Arthropod groups

15

10 30

5 20
Figure 13.5 The diversity of arthropods decreased along a
gradient of agricultural intensification (pesticides, tillage and
weed control) along a land use gradient in Martinique
0 10 (French West Indies). Arthropods were classified into 22
st

groups (19 orders and three larval groups). In the old

ur

ur

de
re

llo

llo
st

st
Fo

ar
fa

fa

pasture, diversity remained low despite higher accumulation

pa

pa

tg
nt

ld
nt

ld

ke

of soil C. Soil C was measured in the 0–10 cm depth. From

O
ce

O
ce

ar
Re

Re

Loranger et al. (1998). Copyright permission granted.

M

severe in mixtures than in monocultures (Zhu et al. involve spatial or temporal gradients within managed
2000). While these research contexts have direct landscapes. For example, to determine the role of
implications for biodiversity in agriculture and flower-visiting bee diversity on the fruit set by coffee,
managed grasslands and forests, they usually can- Olschewski et al. (2006) chose a set of agroforestry
not demonstrate the mechanisms by which changes farms near a national park in Indonesia, such that
in species composition and richness affect specific distance to the forest was not correlated with shade
ecosystem functions (Srivastava and Vellend 2005). density. Transitioning to a new management scenario
Some of the factors that complicate field studies in with increased biodiversity (e.g. conventional to
managed ecosystems beyond those of manipulation organic production (Smukler et al. 2008)), provides
experiments are redundancy of species or functional another approach for identifying correlated changes
groups, trophic complexity, and spatial heterogeneity in biodiversity and ecosystem functioning. These
(Naeem and Wright 2003). The challenge is to find types of approach benefit from the participation of
approaches that test hypotheses about the mechan- land managers, to ensure that sites and situations are
isms by which biodiversity affects ecosystem function well-paired, management records are accurate, and
while providing management relevance. Such app- that ecological interpretation is relevant to actual
roaches often depend on fortuitous ‘experiments’ that situations.
 MANAGED ECOSYSTEMS 187

13.3.3 Example: functions of biodiversity diversity of enemies increases the chance of antag-
for pest control onistic interactions among natural enemies that
generate sub-additive effects of enemy diversity on
Pest control provides examples that show the
consumption rates (Finke and Denno 2006, Rosen-
complex BEF relationships in managed ecosystems.
heim et al. 1995). In contrast, synergistic interactions
In their meta-analysis, Balvanera et al. (2006) found
between enemy species can generate super-additive
that increasing biodiversity increased resistance to
effects with overall prey consumption rates greater
consumption and to invasion by exotic species.
than the sum of the single species consumption
Landscape heterogeneity also contributes to higher
rates acting independently (Cardinale et al. 2003).
invertebrate diversity and to the effectiveness of
Furthermore, the expression of these different
natural enemies. In a literature review, natural
diversity effects can be dependent on ecological
enemy populations were higher and pest popula-
context, with factors such as habitat complexity
tions lower in complex landscapes comprising
(Finke and Denno 2006) and extent or diversity of
cropland intermixed with mid- and late-succes-
prey resource (Prasad and Snyder 2006, Wilby et al.
sional non-crop habitats vs. simple landscapes
2005) strengthening and/or weakening the emergent
(Bianchi et al. 2006). However, data to confirm
properties of even the same assemblages of natural
impacts on actual crop damage or yield were gen-
enemies.
erally lacking.
These potentially complex, and even idiosyn-
The patterns and relationships between different
cratic, effects of predator diversity on prey con-
measures of diversity and heterogeneity within
sumption appear to sit at odds with the key
agroecosystems and pest control functions are not
findings from the recent meta-analysis of Cardinale
consistent. In one study, complex landscapes gen-
et al. (2006a). This comprehensive evaluation of
erally had higher rates of parasitism and parasitoid
empirical BEF studies indicated that an increase in
diversity compared with simple landscapes com-
species richness increases, on average, the extent of
posed primarily of cropland (Menalled et al. 2001).
resource utilization regardless of trophic level. The
However, this pattern was not consistent across all
mechanism best explaining this trend was the
sites, so no clear effect of landscape complexity on
‘sampling effect’ whereby diverse communities are
parasitism could be determined. Other studies,
more likely to contain and be dominated by a
such as Weibull et al. (2003), indicate that while
functionally significant species. By implication, this
species richness generally increases with landscape
suggests that species identity is more important
heterogeneity at the farm scale, changes in diversity
than any emergent effects of biodiversity that might
do not clearly affect natural pest control. In simple
arise through, for example, resource-use partition-
landscapes, increasing non-crop habitat can have an
ing or species interactions. The evidence from
impact on biological control but in structurally
numerous multiple enemy studies, however, indi-
diverse landscapes that already have a high pro-
cates the potential for neutral and even negative
portion of non-crop areas, increasing the proportion
effects of diversity (i.e. not only positive), and also
of non-crop areas further has little effect (Thies and
clear significance of intra- and inter-specific inter-
Tscharntke 1999). Although more complex land-
actions in addition to species identity effects.
scapes can support increased parasitism, they also
Mechanistic understanding of BEF relationships is
tend to be subject to increased aphid colonization,
needed before it can be concluded that species iden-
with no net gain in biological control compared to
tity effects override trophic effects. First, the necessary
simpler landscapes (Thies et al. 2005).
data required to confirm that the species that does
A growing body of literature has explored the
best in monoculture actually dominates function in
effects of multiple natural enemies on predator–prey
the polyculture (i.e. the sampling effect) are generally
interactions. These studies indicate that as enemy
lacking in the majority of studies. Moreover, for most
diversity increases, so does the potential for a range
BEF studies, the diversity–function relationship for a
of density- and trait-mediated interactions within
given function begins to saturate after just one or two
and across trophic levels. For example, higher
species (Cardinale et al. 2006a), but many more species
188 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

may be required to deliver maximum and multiple 13.3.4 Insurance value of biodiversity
functions. At higher levels of diversity, complemen- in human-dominated landscapes
tarity effects and other emergent properties of biodi-
Temporal stability, resistance, and resilience are
versity deriving from trophic complexity are likely to
three types of stability conferred by biodiversity
play a role. First, just one or two species of natural
(Griffin et al. 2009). At present, the potential for
enemies may contribute 50 per cent of pest control
biodiversity to provide ecological resilience (i.e. the
function, but this may not be sufficient to deliver
capacity to recover from disruption of functions
enough control to maintain a pest below an economic
and the mitigation of risks caused by disturbance
threshold level; in the context of practical pest control,
(Holling 1996, Swift et al. 2004)) is compelling, but
we are interested in maximum function, not just the
evidence at the landscape level is limited. In a long-
shape of the curve. Second, a common approach is to
term controlled BEF experiment, higher plant
examine predation rates using simple food webs
diversity decreased the temporal variance in pro-
comprising a limited number of species. These species
ductivity (Tilman et al. 2006b), supporting the ideas
modules allow for interactions between the particular
that biodiversity can be used to buffer against high
species present (identity effects) but do not neces-
variance in productivity (Yachi and Loreau 1999),
sarily test for diversity effects per se (e.g. Finke and
and that high productivity in monocultures can
Denno 2004). Additionally, many studies are short-
only be consistently maintained through intensifi-
term and consider intra-generational effects only,
cation (Naeem 2006a). Yet some have suggested
yet recent modelling studies indicate that short-
that the functional significance of biodiversity may
term experiments and studies that ignore alternate
be most profound at larger spatial and temporal
resources can fail to capture the long-term signifi-
scales, by providing insurance value, especially
cance of interactions such as intraguild predation
when dispersal abilities of organisms allow for
(Briggs and Borer 2005). In a similar way, a char-
immigration within the landscape (Loreau et al.
acteristic of most controlled BEF experiments is that
2003, Swift et al. 2004). Species or phenotypes that
they restrict complexity (e.g. no alternative prey, no
appear to be functionally redundant for a specific
higher order predators or parasites, limited spatial
ecosystem process at a given time may diverge in
or temporal extent), and therefore reduce the
response to environmental fluctuations, thereby
potential for expression of properties of diversity
stabilizing the aggregate ecosystem function
beyond identity.
through time.
Even if we consider just niche partitioning and
Multifunctionality is another compelling argu-
complementarity, the ecological context and extent of
ment for greater biodiversity in managed ecosys-
each study has an important influence. This issue was
tems. Mixtures that simultaneously minimize crop
illustrated recently by Wilby and Thomas (2007)
environmental stress, contribute to pest control,
using a hypothetical example (Fig. 13.6). Essentially,
provide traditional foods or medicines, and lead to
the range of available spatial and temporal niches,
greater market potential for a range of agricultural
and the extent of the process under study influence
commodities exhibit the insurance value of biodi-
the potential for complementarity. Very different
versity in managed landscapes (Perfecto et al. 2004,
relationships occur between pest control functioning
Swift et al. 2004). The multifunctionality of biodi-
and predator diversity if we consider consumption of
versity has not been studied rigorously in this
one aphid species in one field in one year compared
context. However, it appears to operate in tradi-
with consumption of all insect herbivores across
tional farming communities that depend strongly
several crops and multiple years. This argument,
on landraces, as well as in situations where farmers
consistent with the insurance hypothesis, identifies a
select a large number of crop taxa not only to
need for BEF research at appropriate temporal, spatial
increase their direct marketing potential, but also to
and process scales, and cautions against extrapolation
minimize the risks from various types of crop
of existing results until scaling relationships are ade-
damage or failure.
quately understood (Wilby and Thomas 2007).
 MANAGED ECOSYSTEMS 189

(a) (b)
D D D

c1 c2 c3
Process D max
c4 C C C
D

Ecosystem functioning
C b1 b3 b2
c5

b4 B B B
C
Increasing extent
a2 a3 a1 (time, space, or process)
b5 B

a5 A A A
B

a4 A Space
e

Biodiversity
m

A
Ti

Figure 13.6 The influence of process, spatial extent, and temporal extent on biodiversity-ecosystem functioning relationships. (a) The role of elements of
biodiversity (shown as lower-case letters with subscripts) in the transition between states (boxes) within a process. For a given position in time and
space (i.e. a particular ecological context), the number of elements of biodiversity necessary to fulfill ecosystem function depends on the extent of the process
in question. If the extent of the process of interest is simply the transition from state A to state B, then just one biodiversity element (such as a species) is
required (e.g. a2). If, however, a process involves transition from state A to state D then three elements are required for full function (e.g. a2, b1, c1).
As the temporal or spatial extent of a study is expanded, then the number of elements necessary for maximal functioning increases further, since different
elements are likely to be most efficient at different points in space and time. For the full extent of the process A to D across all combinations of time and
space, a maximum of 27 elements is required for full function, based on these assumptions. (b) The increase in biodiversity required for maximum
function as the extent of process increases. Time or space changes the shape of the biodiversity–ecosystem functioning relationship from the baseline set
of ecological conditions. From Wilby and Thomas (2007). Copyright permission granted.

13.3.5 Cross-ecosystem exchanges A landscape mosaic with agroecosystems in close

of biodiversity and their functions proximity to fragments of natural habitats can
increase pollination (Greenleaf and Kremen 2006b,
The traits that permit species to move and persist
Kremen et al. 2002) and pest regulation (Bianchi et al.
across ecosystem boundaries will affect the eco-
2006). Predatory wasps and parasitoids that act as
system services that are provided by heterogeneity
natural enemies of crop pests are more abundant near
in the landscape (Gonzalez et al. 2009). Tscharntke
field edges than in field centres, and in more complex
et al. (2005) suggest three main possibilities of
landscapes with higher proportions of forest, hedge-
exchanges of organisms between crop and non-crop
rows, grassland, fallows, and wetlands (Bianchi et al.
habitats: (1) exchange among the non-crop habitats
2006). Higher diversity of bees and wasps, especially
as long as the landscape matrix allows the specia-
parasitoids, are observed in agroecosystems close to
lists in these habitats to disperse and persist, (2)
rainforests, probably because their populations build
non-crop habitat as a source of generalist species
up in the forests due to lack of disturbance (Klein et al.
that invade cropped ecosystems, with effects on
2006). This can result in higher fruit set near forest
pollination, biological control, or pest infestations,
remnants, and higher income for the farmer (Ricketts
and (3) crop habitat as a source of generalist species
2004). But in some areas in Nicaragua and Indonesia
that invade the non-crop ecosystems, and affect
potential crop revenues of forest land-sparing exceed
biotic interactions in natural habitats.
the value of coffee pollination from these adjacent
Some information exists on the traits that permit
forests, and thus the higher income derived from
species to move and persist across ecosystem
conversion from forests to coffee plantations drives
boundaries, and on the ecosystem services that result.
land use change, even when some compensation for
190 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

pollination services is available (Olschewski et al. In an example from the Great Plains of North
2006). At the landscape level, forest conversion may America, restoring native bison to areas now dedi-
outweigh the immediate financial benefits of con- cated to cattle ranching has been suggested to increase
serving biodiversity and its ecological functions biodiversity and ecosystem health – a viable economic
(Lambin et al. 2003). alternative in a region with declining human popu-
There are also spillover edge effects in the other lation density (Callenbach 2000, Popper and Popper
direction (Rand et al. 2006). For example, many 1987). This notion originally met with substantial
generalist insects that serve as natural enemies of resistance from many cattle ranchers, who felt that
agricultural pests feed on alternative hosts in bison would transmit disease to their cattle or that
nearby woodland and grassland fragments, with bison were biologically and economically inferior to
largely unknown effects on food webs. This is most cattle (Popper and Popper 2006). These examples
likely to occur when adjacent ecosystems differ in demonstrate that the general lack of information on
productivity and/or when the timing of temporally landscape-level interactions between wild and agri-
variable resources shifts across ecosystem edges. cultural biota can create strong human reactions that
Fragments of natural vegetation along wetland can ultimately result in decisions that may not favour
margins are another example of cross-ecosystem biodiversity conservation or ecosystem services.
exchanges. They filter agricultural nutrients and pol-
lutants, reduce erosion, improve water quality, and
13.3.6 Indicators for the functions
provide habitat for higher trophic level species (Lovell
of biodiversity in managed ecosystems
and Sullivan 2006). Multispecies riparian buffers with
herbaceous and woody species can result in higher Given the rapid loss of biodiversity, there has been a
total productivity, soil carbon sequestration, and strong effort by various agencies to develop indicators
nitrogen immobilization than monoculture plantings of biodiversity (OECD 2003) often with the implicit
(Hill 1996, Marquez et al. 1999, Rowe et al. 2005). assumption that increased biodiversity confers higher
There are situations where landscape-level het- ecological functioning. There has been less emphasis
erogeneity and its associated biodiversity may cause on indicators that demonstrate the function of biodi-
agricultural problems. Some crop diseases only versity, although some examples are given below. To
overwinter if there are hosts in the vicinity, leading date, three primary approaches are applied: correla-
to enforcement of crop-free periods and mandatory tions based on functional types, use of specific indi-
elimination of host species. In the Salinas Valley of cator taxa, and multitaxon studies. This is an
California, one of the most intensively managed emerging area of much needed science, and involves a
agricultural areas in the USA, lettuce mosaic virus great deal of ecological complexity.
infects both cultivated lettuce (Lactuca sativa L.) and Correlating trait-based functional types and spe-
its wild relative, prickly lettuce (Lactuca serriola L.), cific functions is one approach. In Sumatra, Indo-
which is a ruderal species along field margins and nesia, a biodiversity ‘hotspot’, plant species diversity
roadsides. One solution was the legal designation of is lowest in intensive non-shaded coffee systems and
a month-long period when lettuce cannot be present increases through more shaded and complex agro-
in any field, and another was the eradication of forests to late successional secondary forests and
prickly lettuce (Jackson et al. 1996) which entailed closed canopy mature forests (Gillison et al. 2004).
killing other annual species, including natives. The number of plant functional types was shown to
Another example from the same region is the viru- be correlated with soil carbon, nutrient availability,
lent strain of E. coli on spinach, which killed three aboveground carbon, biomass (based on allometric
people in 2006, and matches the DNA of E. coli in equations), land use, and plot age since disturbance.
cattle, wild pigs, and stream water of a nearby Birds serve as excellent indicators of biodiversity
grassland (Bailey 2007). A strong movement is now (Donald 2004), and species composition is known to
developing in this region to eliminate natural habi- be linked to agricultural intensification (Green et al.
tats, and landscape heterogeneity, around vegetable 2005). In orchards and vineyards in Northern Italy,
fields, in order to prevent future outbreaks. diversity of birds, especially insectivores, were
 MANAGED ECOSYSTEMS 191

highest in organic systems, and pest management functions in actual ecosystems and landscapes,
practices (number of pest control treatments and despite the typical results of controlled BEF studies
pesticides used) explained much of the variation (Cardinale et al. 2006a).
among systems (Genghini et al. 2006). Using this type
of knowledge about responses of different species to
13.4 Linking biodiversity, ecosystem
changes in management practices, Butler et al. (2007)
functions, management, and end-users
developed a trait-based risk assessment framework to
predict the effects of environmental change on bird As indicated in the introduction, mounting popula-
biodiversity. For six components of agricultural tion pressure is increasing the demand to maintain
intensification, they examined the potential foraging and enhance the productivity of agricultural sys-
and habitat responses of different bird species, and tems. To do this in a sustainable way without
assigned a risk score, with the end result of identify- impacting a range of non-provisioning ecosystem
ing particularly harmful management practices (e.g. services represents a significant ecological challenge,
that genetically modified herbicide-tolerant sugar- and must be set within a socioeconomic context of
beets would impact the ecological habitat of 39 bird market forces, social and economic policy, and
species). This framework could be expanded to human values (Robertson and Swinton 2005), and
include the response of specific functions, such as must consider the tradeoffs for different end-users,
pollination, seed dispersal, and predation, on either from farmers to policy makers (Jackson et al. 2007).
desirable or less desirable species. Broad assessments of the significance of ecosystem
Multitaxon studies of biodiversity draw inferences services suggest considerable value of regulating and
about multiple ecosystem functions and conserva- supporting services within managed systems. For
tion value. For example, the species richness and example, natural pest control services have been
abundance of forest birds was positively associated valued at > 400 billion USD per year globally
with shade cover, epiphyte abundance, and canopy (Costanza et al. 1997), with estimates specifically for
height in Mexican coffee agroecosystems, but no cropland of 100 billion USD per year (Pimentel et al.
such associations occurred for understory dwelling 2004). Indeed, it has been suggested that 99 per cent of
mammals, which were captured in only two of 15 the populations of pests and diseases are controlled
study sites (Gordon et al. 2007). Individual taxa by their natural enemies (de Bach 1974). While such
perceive the landscape in different ways, and indi- figures provide a measure of the overall economic
cators must reflect these differences. For example, significance of services provided by biodiversity,
different forms of tree cover provide habitat for there is a general lack of detailed field-level assess-
birds, bats, and insects in a pastoral landscape in ments of particular services, the mechanisms behind
Nicaragua (Harvey et al. 2006). In a study of subal- them, and their economic value.
pine hay meadows in Romania, each stage of suc- One recent study in New Zealand attempted to
cession held the maximum species richness for one address this gap by using experimental manipula-
of four taxonomic groups (plants, gastropods and tions to assess the value of natural pest control
diurnal and nocturnal Lepidoptera), indicating that all services in organic vs. conventionally managed
stages had high conservation value (Baur et al. 2006). arable production systems (Sandhu et al. 2008). The
There has been little work to assess the ecological approach used artificial prey to quantify back-
functions of different functional groups of taxa and ground predation rates coupled with knowledge of
the tradeoffs involved in managing for each within a prey economic thresholds to calculate an economic
given ecosystem or landscape. value of biological control, using estimates of
The same issues of complexity that have been the ‘avoided costs’ and ‘total avoided costs’ of insecti-
main theme of this section hinder the development cide applications. Avoided costs are the monetary
of indicators for specific functions resulting from savings derived from not needing to apply insecti-
particular aspects and levels of biodiversity in cides to control specific pests, whereas total avoi-
managed ecosystems. Species richness clearly is too ded costs also include a component for external
simplistic to be used as an indicator of ecosystem costs, such as the environmental impact of
192 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

insecticide application. Background biological con- (a)

Total benefit
trol of pests was severely reduced, four- to ten-fold

Cost or benefit
on average, in 14 organic fields compared with 15 Cost
fields under conventional management. The mean t
efi
economic value of this biological control in the en
tb
Ne
organic fields was estimated at 55 USD ha–1 yr–1
(avoided costs) and 22 USD ha–1 yr–1 (total avoided
costs) for both aphid and carrot rust fly. In contrast,
Adoption (scale)
little economic value of natural pest control services
occurred in the conventional fields due to extremely (b)
low predation rates. However, it should be noted

Cost or benefit
that the economic value of biocontrol varied across Cost
fields and positive economic values could not be
demonstrated for all organic fields.
t Total benefit
In this example, the avoided costs provide a mea- efi
t ben
sure of private benefit (i.e. benefit to the farmer) while Ne
the total avoided costs provide some measure of
additional public benefit due to externalities beyond Adoption (scale)
the farmer’s field. Variation creates further complex-
(c)
ity in valuation. Benefits varied with local ecological Total benefit
context, and positive effects were measurable in some t
efi
Cost or benefit

ben
field settings but not in others. Similar spatial varia- Ne
t

bility in biodiversity and pest control has been Cost

reported previously (Menalled et al. 2001, Weibull
et al. 2003), as both management intensity and land-
scape structure shape local arthropod communities
(Bianchi et al. 2006, Schweiger et al. 2005). The overall
Adoption (scale)
conclusion is that generating clear guidelines for
farmer and policy makers end-users is difficult, yet Figure 13.7 Costs and benefits of natural biological control as a
adoption of biodiversity-based practices may still be management strategy that promotes an ecosystem service, and effects of
advocated as a potential component of economic and the level of adoption of that strategy. (a) A simple linear relationship
whereby effect on biocontrol is independent of level of adoption and hence,
environmental risk reduction.
net benefit remains constant. (b) A non-linear relationship where
effectiveness is greatest at small scales such that net benefit decreases as
adoption increases. (c) A contrasting non-linear case where impact
13.4.1 Impacts of scale on managing for
increases with adoption. Here adoption needs to exceed some threshold
biodiversity and its ecosystem functions level before a net benefit is derived. From Griffiths et al. (2008). Copyright
permission granted.
Context and the scale of adoption or implementation
alter the impacts of management practices. This issue
was explored recently by Griffiths et al. (2008), who
used conceptual models to describe how a manage- Here, increased adoption led to an increase in total
ment strategy aimed at manipulating biodiversity cost and total benefit of the approach, but net benefit
affected an associated ecosystem service when the remained constant. In the second scenario, benefit
strategy was adopted at different scales. Non-crop was assumed to saturate with increasing adoption
habitats within agricultural landscapes were manip- (Fig. 13.7(b)). Such a pattern could arise if, for exam-
ulated to increase natural enemy diversity and ple, the effects of the habitat manipulation derived
abundance and increase natural pest control. Three largely from local redistribution of natural enemies.
scenarios were considered. First, benefits were At small scales (a single field), natural enemies might
assumed to be independent of scale (Fig. 13.7(a)). be drawn from adjacent habitats, thereby boosting
 MANAGED ECOSYSTEMS 193

pest control, but at larger scales (multiple fields), this deforestation when there is sudden change to
effect diminishes as the species pool for redistribu- more ubiquitous, intensive systems, often occur-
tion becomes exhausted. A technique might look ring with the knowledge and implicit support of
promising initially and favour early adopters, but local and federal governments (Geist and Lambin
then fail as it becomes implemented more widely. 2002). An example of the latter comes from the
The final scenario assumed that the benefit of a Veracruz state of Mexico, where immigration to oil-
technology increased with scale of adoption (Fig. producing areas led to intensive urban expansion
13.7(c)). This could occur if habitat manipulation accompanied by a 1400 per cent increase in crop-
increased natural enemy richness and abundance as lands and grasslands for cattle raising in 30 years;
more habitat was created. With this pattern, an these increases were at the expense of mature and
individual farmer might have little incentive for secondary forests (Garcia-Romero et al. 2004). The
adoption unless the technology was implemented loss of ecological functions from the biodiversity in
widely. Such negative scale or transition effects will these later successional ecosystems was apparently
likely hinder adoption whenever farmers try, or not a high priority for policy makers.
partially adopt, a practice in order to evaluate its Social institutions are needed to promote
performance. Since scaling effects are not well- incentives that ensure that biodiversity will be
understood, one of the key challenges for BEF conserved to its fullest potential of functional
research is to determine appropriate temporal benefits over the long term. An example is the
(season to multiple seasons) and spatial (field to wide price swings for coffee in the international
farm and landscape) scales to define optimum market. Price increases result in land clearing or
management strategies that link in a meaningful intensification, while price crashes lead to wide-
way to policy and market mechanisms. spread abandonment of coffee plantations, and the
end result is biodiversity loss (Donald 2004). Low-
input, floristically diverse, shade-grown coffee
13.4.2 Incentives for managing for
tends to be associated with higher biodiversity of
biodiversity and its ecosystem functions
many taxa. Due to lower input costs compared to
In most cases, people decide to utilize and conserve intensified, unshaded coffee, low-input systems
biodiversity because there is a private socioeconomic can be very profitable in Mexico, and are less likely
advantage, including rewards obtained from land to be converted to cattle pasture, sugar cane, or
stewardship (Pascual and Perrings 2007). As an housing developments when the price of coffee
example, in Austria, across a range of commodities falls (Gordon et al. 2007).
and farming styles, plant species richness was not Poverty also has profound implications for biodi-
correlated with agri-environmental subsidies per versity in managed ecosystems. When there is
hectare (Schmitzberger et al. 2005), suggesting that uncertain tenure over land, limited or no access to
stewardship was not limited by finances but rather credit, and poor market linkages, there may be little
by awareness and mentality. In general, agri- capacity to manage for biodiversity and its ecological
environmental schemes have not been particularly functions. When social programs increase credit
successful in protecting farmland biodiversity (Kleijn through micro-lending, and provide value addition to
and Sutherland 2003). The impact of financial support agricultural and forest products, there is greater
on agrobiodiversity conservation is still poorly potential to create viable enterprises that both con-
understood, but it may need to be specifically serve biodiversity and improve human wellbeing
targeted to well-defined ecosystem functions to be (Bawa et al. 2007, de Clerck et al. 2006).
successful (Gottschalk et al. 2007). In human-dominated landscapes, high levels of
Governmental backing of intensive land use can biodiversity are more likely to be maintained for
result in loss of biodiversity and ecosystem ser- reasons of intrinsic (‘option’ or ‘bequest’) values or
vices, such as agricultural subsidies for high-input utilitarian (‘direct use’) than for other functional
crops (e.g. corn for ethanol production in the values (Swift et al. 2004). Biodiversity at the farm/
USA). Tropical forest regions can rapidly undergo plantation and plot levels is most likely to be
194 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

maintained for solely utilitarian values. The chal- to develop indicators for the multiple functions of
lenge for ecologists is to provide meaningful biodiversity. This will be more beneficial than a
research on ecological functions of biodiversity at research focus on the effects of increasing species
different scales so that it is valued, used, and richness on one or a few ecosystem functions. Finally,
conserved by society, even as the current trend for since human decision-making plays a large role in
management intensification continues. land use in managed ecosystems, researchers must
involve land managers and other stakeholders to
grasp both the ecological and socioeconomic factors
13.5 Conclusions
that determine biodiversity, its functions, and trade-
This chapter has focused on management intensifica- offs between different management scenarios.
tion and the opportunities for conserving biodiversity Although much of earlier BEF research has focused
and ecological functions in ecosystems situated in on basic processes in community ecology, delaying
landscapes that have been modified by human land the so-called application phase for many years, this
use, and the ways that researchers can address eco- chapter indicates that there has been much recent
logical processes in managed ecosystems for multi- creativity and activity toward understanding these
functional outcomes. Three general messages emerge. processes in relation to ecosystem services, particu-
First, although there is much recent progress in larly in agricultural landscapes. Given the rapid rate
describing species diversity in managed ecosystems at which biodiversity loss is now occurring, and the
and landscapes, the functions of different components prognosis that climate change will further hasten
of biodiversity still remain unknown. Second, process- these losses, much greater understanding of biodi-
oriented research on functions of biodiversity may be versity and ecological functions in managed ecosys-
most effective if it focuses on unique traits or rela- tems is necessary to steer policy decisions toward
tionships between species, especially if this can serve more sustainable outcomes.
 CHAPTER 14

Understanding the role of species

richness for crop pollination services
Alexandra-Maria Klein, Christine Müller, Patrick Hoehn,
and Claire Kremen

14.1 Introduction monoculture plantings, and the modification of

natural habitats by humans, significantly impacts
Flower visitation and pollination by animals are the
pollinator communities across a variety of scales
first steps and therefore critical to the sexual
(Klein et al. 2007, Kremen et al. 2007, Ricketts et al.
reproduction of many plant species (Kearns et al.
2008). Local (field-level) alterations that impact
1998), including up to 90 per cent of Angiosperms
pollinators and pollination include changes in: (1)
in tropical rainforests (Bawa 1990). Flower visitors
the abundance and distribution of flower resources
are insects or vertebrates like hummingbirds or bats
(Holzschuh et al. 2007, Klein et al. 2002, Williams
visiting flowers for receiving nectar and/or pollen,
and Kremen 2007, Tylianakis et al. 2008), (2) species
and the visitation can, but does not necessarily,
richness of flowering plants (Ebeling et al. 2008,
result in pollination, the successful fertilization of
Ghazoul 2006, Potts et al. 2006), (3) availability of
the flower. Recent estimates showed that 35 per
nesting sites and materials (Shuler et al. 2005, Kim
cent of global food production directly consumed
et al. 2006), (4) light levels (Klein et al. 2003a, b),
by humans comes from crops that benefit from
and (5) temporal continuity of floral resources
flower visitation, primarily by bees and other
(Greenleaf and Kremen 2006b). Examples of land-
insects (Klein et al. 2007). Many of these crop plants
scape-level factors affecting bee communities are
increase fruit or seed quantity from 5–50 per cent
the proportion and quality of natural or semi-
when flower visitors are present under experimen-
natural habitats in the landscape (Greenleaf and
tal conditions, and a small number of crops (n ¼ 13)
Kremen 2006b, Kim et al. 2006, Kremen et al. 2002,
do not set fruit at all if pollinators are absent.
2004), the distance of natural or semi-natural habi-
Flower visitors can be also important for our dairy
tats from crop systems (Klein et al. 2003a, b, Ricketts
and meat industries, since many forage crops, like
et al. 2004, Ricketts et al. 2008), and the presence of
alfalfa, clover (Delaplane and Mayer 2000), and
mass-flowering resources (Herrman et al. 2007,
soybeans produced for cattle forage (Chiari et al.
Westphal et al. 2003). Therefore, resource availabil-
2005) benefit from insect pollination for seed pro-
ity and the area and isolation of natural habitats are
duction. Flower visitors are also often important in
all important for the conservation of pollinator
modern agriculture to mediate gene flow between
species richness, which provides a key service to
varieties in hybrid seed production (Greenleaf and
crop production.
Kremen 2006a, Van Deynze et al. 2005). Many wild
In this chapter, we discuss what is known about
plant populations have been shown to be limited by
the relationship between flower-visiting species
access to flower visitors (Ashman et al. 2004).
richness and pollination services. Following the
Intensification of land use by tilling, irrigation,
introduction (Section 14.1), the relative importance of
and fertilizer and biocide use, along with declining
species richness, individual numbers, and combined
habitat heterogeneity from increased field sizes,
effects in providing services to their mutualistic

195
196 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

plant partners are described (Section 14.2). Next, Consequently, under honey bee-scarcity scenarios,
the mechanisms underlying the role of species species richness of wild species may ensure adequate
richness in ensuring insect pollination (Section crop pollination services (Klein et al. 2003a, Winfree
14.3), and the evidence for and against sampling et al. 2008). Given the economic importance of bee
effects (Section 14.3.1), niche complementarity (Sec- pollination (Gallai et al. 2008), wild bee species
tion 14.3.2), and functional facilitation are discussed richness will be critical in ensuring pollination ser-
(Section 14.3.3). Since the pollination of crop spe- vices in the face of declining honey bee numbers.
cies is embedded within plant–flower visitor (PFv) Species richness of flower-visiting communities
webs including both other crop and wild plant may be important for several reasons, four of which
species, the utility of analyzing quantitative have been recently studied. First, more species-rich
plant–flower visitor interactions for managing and communities frequently have higher aggregate
restoring crop pollination services is discussed abundance and therefore contribute more to polli-
(Section 14.4). This section starts with a paragraph nation services (Kremen and Chaplin-Kramer 2007,
about web structure and characteristics (Section Larsen et al. 2005). With agricultural intensification,
14.4.1), to explain how general PFv characteristics both flower-visiting species richness and aggregate
buffer species extinction and integration (Section abundance decline, because compensation by pol-
14.4.2). The role of higher trophic levels in PFv linator species that tolerate agricultural intensifica-
webs is discussed, and in Section 14.4.3 ideas are tion is lacking (Larsen et al. 2005, Winfree and
summarized of how PFv webs provide informa- Kremen 2008). With lower species richness and
tion for crop pollination services. Section 14.5 individual numbers, pollination services become
presents the current knowledge concerning the inadequate, as was shown for watermelons that
consequences of current and projected pollinator were only sufficiently pollinated on the low-intensity
declines for global crop production and wild plant farms that supported the richest bee communities
populations. The chapter ends with outstanding (Kremen et al. 2002, 2004). Similarly, intensively
research gaps in the understanding of how flower- cultivated coffee was found to be pollinated inade-
visiting species richness contributes to pollination quately, except for plants growing close to forest
services (Section 14.6). fragments that supported the richest bee community
(Ricketts et al. 2004). The ubiquity of the positive
relationship between flower-visitor species richness
14.2 The importance of flower-visitor
and individual numbers across agricultural systems
species richness and individual numbers
(Kremen and Chaplin-Kramer 2007), and the possi-
for pollination services
ble lack of density compensation in these systems
Pollination services strongly depend on the total of (Winfree and Kremen 2008) suggest that high species
all individuals in a community, the so called aggre- richness is often necessary to provide sufficient pol-
gate abundance of flower visitors (Morris 2003, lination services through aggregate abundance of
Vázquez et al. 2005). The European honey bee, Apis flower-visiting species.
mellifera L., for example, is the world’s most impor- Second, temporal turnover between years is
tant crop-pollinating species because their high extremely high in bee communities and this turn-
sociality and large colonies yield large populations over affects crop pollination services (Herrera 1988,
that are readily managed and moved in and among Pías and Guitián 2006, Williams et al. 2001). Species
agricultural fields (Free 1993, McGregor 1976), richness on watermelon farms with high flower-
ensuring fruit set and increasing fruit production visitor species richness remained high from year
and yield (e.g. Chiari et al. 2005, Roubik 2002, Stern to year, but the identity of bee species changed
et al. 2001). Although honey bees can provide polli- (Kremen et al. 2002). Temporal stability of the
nation services for the majority of crop species (Klein pollination service between days within a season
et al. 2007), in some areas crops can be solely polli- (measured as the inverse of the coefficient of var-
nated by species-rich communities of wild non- iation), also increased on low-intensity farms
honey bees (Kremen et al. 2002, Winfree et al. 2008). (Kremen et al. 2004) that supported higher species
 UNDERSTANDING THE ROLE OF SPECIES RICHNESS FOR CROP POLLINATION SERVICES 197

Table 14.1 Similarity in flower-visiting communities among four different crops blooming in Yolo County, California. Almond blooms in early spring
(February), while the other three crops are summer-flowering (May–August). Jaccard index of similarity is presented. Data from Kremen et al. 2002, 2004,
Greenleaf and Kremen, 2006a, b, and unpublished data.

Almond Tomato Watermelon Sunflower Pollinator species richness

Almond 1 14
Tomato 0.313 1 7
Watermelon 0.179 0.219 1 32
Sunflower 0.231 0.171 0.32 1 34

richness. Thus high species richness may ensure about 30 per cent of their visitor community. Despite
that flower visitors and pollination services are blooming at the same time, watermelon and sun-
available to the plants over all days and years, but flower clearly attracted different flower-visiting
more studies are needed to test if temporal stability species, because they differ in flower morphology
of pollination services is related to bee species and pollen and nectar availability, and because of
richness or individual numbers. the dominance of specialists on sunflower, which is
Third, spatial preferences for different flower- the only one of these four crops native to North
visiting species using flowers located on different America. Similarly, in New Jersey, wild bee com-
parts of the plant (Lortie and Aarsen 1999, Hambäck munities visiting watermelon versus tomato crops
2001) or in different locations in the field (Klein and were found to be distinct as identified by non-metric
Kremen unpublished data) can also lead to the multidimensional scaling (an ordination method to
necessity of high species richness for adequate polli- analyze compositional differences among commu-
nation services. Spatial stability of pollination service nities). The community differences were visible even
between plants within sites along a land-use gradient when controlling for differences between farm sites
(measured as the inverse of the coefficient of variation) and the differential attractiveness of the two crops
can also be influenced by flower-visiting species (Winfree et al. 2008). Similarly, Meléndez-Ramirez
richness (Klein et al. 2003a), but more experimental et al. (2002) showed a low species overlap of bees
tests are needed before conclusions can be drawn (similarity and shared species) visiting different
about the generality of this relationship between spa- cucurbit crops (cucumber, melon, pumpkin, water-
tial characteristics in pollination stability and flower- melon) in Yucatán, Mexico.
visiting species richness and individual numbers. Fifth, different species respond differentially to
More aspects of spatial stability and spatio-temporal disturbances such as land-use intensification
species turnover will be discussed in Section 14.3.2. (response diversity, Elmqvist et al. 2003), potentially
Fourth, flower-visiting species richness is essential buffering the provision of pollination services across
when different crops are grown within the same land-use gradients. On watermelon fields in New
cultivation system. In California, four well-studied Jersey and Pennsylvania where bee communities
crops (watermelon, sunflower, tomato, and almond) provide a relatively consistent level of pollination
share only 17–33 per cent of the species that visit and services across a land-use intensity gradient (Winfree
potentially pollinate them (Table 14.1). Almond et al. 2008), differential responsiveness of bee species
blooms in February, March (winter to spring), while to land-use intensity may be a mechanism for
the other crops are all summer-flowering. Therefore, achieving stability across the gradient (Winfree and
it is not surprising that the bee community was Kremen 2008). In California, where pollination ser-
almost entirely dissimilar between almond and the vices decline dramatically across the landscape with
other crops, while watermelon, sunflower, and increasing intensification (Kremen et al. 2002), differ-
tomato shared a substantial proportion of their ential responsiveness among bee species may
visiting bee species. Flower visitors to tomato com- dampen the effect of increasing land use, which
prised a subset of the much richer visitor commu- would otherwise be even more dramatic (Winfree
nities to watermelon or sunflower, which shared and Kremen 2008).
198 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Table 14.2 Spatial variation (measured as CV, Coefficient of Variation) of insect-pollinated fruit set among highland (C. arabica) and lowland
(C. canephora) coffee trees per site across a gradient of pollinator species richness in different coffee agroforestry systems (Klein et al. 2003a,b, Klein et al.
2008). (A) Results of simple regressions; (B) selected glm (generalized linear model) that explains the highest variance when including functional
group richness, species richness, individual number and all interation terms. Models were selected according to lowest AIC and highest P-values. AIC
(Akaike Information Criterion) and significance level (*) p < 0.1, *p < 0.05; **p < 0.01; ***p < 0.001 of different Models were fitted. Analyses were
done in R, version 2.6.2.

Response variable Explanatory variable AIC

Coffea arabica
A Simple regressions
CV bee pollinated fruit set Functional group richness 190.7***
“ Species richness 195.9***
“ Individual number 195.9**
B Selected glm model
CV bee pollinated fruit set Functional group richness þ species richness þ 190.1**
individual number þ (functional group richness ·
individual number) þ (species richness · individual number)
Coffea canephora
A Simple regressions
CV bee pollinated fuit set Functional group richness 142.2*
“ Species richness 143.4(*)
“ Individual number 144.2
B Selected glm model
CV bee pollinated fruit set Functional group richness þ (species richness · individual number) 141.5*

Although species richness is often correlated with 2008). Hence the studies demonstrate that bee spe-
aggregate abundance in bee communities (Kremen cies richness is essential for overall pollination ser-
and Chaplin-Kramer 2007), data on three crop vices. Consequently, the following question arises:
species suggests that species richness may be even what are the mechanisms behind the relationship of
more important than aggregate abundance. The species richness and pollination services?
data were collected along land-use gradients in
Indonesia differing in habitat and landscape man-
14.3 Mechanisms for the effects
agement to ‘experimentally’ manipulate bee species
of flower-visiting species richness
richness and individual numbers in real world
on providing pollination services
ecosystems. Flower-visiting observations and pol-
lination experiments were conducted for three Three mechanisms known to be important in BEF
species representing three different breeding sys- patterns may explain why diverse flower-visiting
tems: (1) lowland coffee, C. canephora, a mainly self- communities can function better than depauperate
incompatible species, (2) highland coffee, Coffea communites. First, under sampling (selection) effects
arabica, a mainly self-compatible species (Klein et al. (Loreau et al. 2001), high species richness increases
2003a, Klein et al. 2008); (3) and pumpkin, Cucurbita the likelihood of random inclusion within the
moschata, a monoecious species, meaning that flower-visiting community on a given crop of an
female and male gametes are spatially and tempo- efficient and effective pollinating species. Second,
rally separated (Delaplane and Mayer 2000). For all under niche complementarity (Loreau et al. 2001),
three crop species flower-visitor species richness high species richness improves pollination services
was more important to explain pollination services because species differ in their foraging behavior
when factoring out for the effect of flower-visiting and may complement one another by visiting and
individual numbers (Hoehn et al. 2008, Klein et al. pollinating different flower species, or in the spatial
 UNDERSTANDING THE ROLE OF SPECIES RICHNESS FOR CROP POLLINATION SERVICES 199

or temporal distribution of visits within or among Generally, sampling effects might be more
flowers of a species. Third, under functional facili- important in more specialized plant–flower visitor
tation (Cardinale et al. 2002) a given species has a relationships, where a few visiting species, maybe
positive effect on the functional capability of other due to proboscis length, are much better adapted to
species. For example, interspecific interactions flower morphology than others and thus more
during foraging can lead to higher frequencies of effective as pollinators. In such cases a more spe-
cross pollination (Klein et al. 2008). cies-rich community has a higher chance of
All three mechanisms assume that different including the most effective pollinator species by
flower-visiting species differ in their morphology, random chance.
physiology, behavior, or other traits, so that high
species richness maximizes resource use and thus
14.3.2 Niche complementarity
pollination success, as discussed in more detail
and spatial stability
below.
The theory of complementarity between species
assumes that high species richness increases func-
14.3.1 Sampling (selection) effect
tional effectiveness by increasing the efficiency of
The sampling effect asserts that in experimental resource use over space and time. Therefore, con-
designs with varying species richness, increasing tributions of many species will increase resource use
richness results in a higher chance of including a with each additional, individual species through
species that makes a disproportionate contribution distinct resource partitioning, until a plateau is
to ecosystem functioning (Loreau 2000). In this case, reached. For example, a diverse flower-visiting
the species in the species pool that is the most community whose members exhibit species-specific
efficient (e.g. produces the most seeds per visit or or functional group-specific use of spatio-temporal
deposits the most high-quality pollen) in pollination niches during flower visitation should lead to more
would dominate the pollination service and mask efficient resource use. By exploiting different spatio-
minor benefits by other species in multi-species temporal niches (e.g. different parts of the flower,
communities whenever it was present. Due to the tree or field, different times of the day), different
difficulty of experimentally manipulating flower- flower-visiting species might maximize their ability
visiting communities, little evidence for or against to obtain pollen and nectar resources (Herrera 1988).
the role of random sampling effects in pollination Resource use for flower visitors consists of gathering
function is available. In natural experiments along pollen and nectar and this action simultaneously
land-use intensity gradients, Larsen et al. (2005) pollinates the plant. More efficient resource use
found that the most species-rich communities visit- through complementarity could thus lead to better
ing watermelon were the only ones contained the pollination services for the plants, for example, a
most effective flower-visiting species for pollination. greater number of flowers per plant are pollinated,
However, they showed that this was not due to or a better distribution of pollen on the stigma is
random sampling effects, but rather to non-random obtained.
local extinction processes. For pumpkin (Hoehn et al. 2008), characteriza-
The three crop studies from Indonesia (Hoehn tions of the species-specific differences in spatio-
et al. 2008, Klein et al. 2008) indicate that not sam- temporal pattern of flower visitation were also
pling effect but niche complementarity seems to be made in high and low-bee species richness systems.
the prodominant mechanism for high quality and In the high bee species richness sites, pumpkins
quantity in pollination services. This prediction is reached their maximum in seed numbers (hand-
based on the finding that functional group richness pollinated flowers served as reference) (319 ± 105
explained the pollination service better than species standard deviation), whereas in the low-bee species
richness per se. In all three studies, functional group richness sites, the number of seeds per pumpkin
richness was classified using a priori groups of was significantly lower (179 ± 44). Comparing the
morphological and behavioural pollinator traits. spatial (flower-visiting height of the plant) and the
200 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

(a) (b)
10:20 10:20
Flower visiting time of day

Flower visiting time of day

6 12

9:40 5
9:40
1 7 7
11
9:00 2 9:00
8 10
4 4
9
8:20 8:20
3

7:40 7:40
0.0 0.2 0.4 0.6 0.8 1.0 1.2 0.0 0.2 0.4 0.6 0.8 1.0 1.2
Flower visiting height (m) Flower visiting height (m)

Figure 14.1 Flower height and forage time preferred by the most abundant flower-visiting bee species of planted pumpkin plants in two different habitat
types: (a) grassland with high bee species richness and (b) forest with low bee species richness in Central, Sulawesi, Indonesia. Each habitat type was
replicated with four plots in spatially separated sites. Experimental pumpkin patches of 2 · 5m were planted in each plot and liquid fertilizer was applied
every other week (for more information see Hoehn et al. 2008). Arithmetic means ± standard errors are given. Numbers are presenting following bee species:
1 – Nomia concinna, 2 – Lasioglossum sp., 3 – Apis cerana, 4 – Xylocopa dejeani, 5 – Nomia fulvata, 6 – Ceratina cognata, 7 – Trigona sp., 8 – Amegilla
sp., 9 – Xylocopa confusa, 10 – Lasioglossum halictoides, 11 – Apis dorsata, 12 – Xylocopa nobilis.

temporal (flower-visiting time of the day) activity of dependent. Also, in the pumpkin system, species-
the flower-visiting species in both systems, it could specific flower-visiting behaviour (time of visitation
be shown for the high species richness sites, com- and height and duration of floral visit) was strongly
prising 10 species, that these species covered the related to the body size of the visiting species (Hoehn
entire spectrum of spatio-temporal niches. This et al. 2008). Therefore, morphological traits can be
increases the probability that flowers at any height responsible for differences in spatio-temporal floral
were visited and flower visitors were active during resource use.
the receptive period of the flowers (Fig. 14.1(a)). In Additionally, Table 14.1 shows the spatial varia-
contrast, the three bee species found visiting the tion of insect-pollinated fruit set among coffee
low species richness sites did not cover all the plants per site across different agroforestry systems
spatio-temporal niches (Fig. 14.1(b)). In other comprising different bee communities. Simple
words, in the low-bee species richness sites, spatial relationships between insect-pollinated fruit set and
and temporal niches become unoccupied when bee functional group richness or species richness or
species are lacking. individual numbers showed that for the spatial
Another study on strawberries (Chagnon et al. stability aspect, functional group richness seemed
1993) demonstrates complementarity due to spatial to play an important role. Nevertheless, models
factors. Here the crucial pollination trait was the including interaction effects between functional
species-specific behaviour of the bee interacting with group richness, species richness, and individual
the floral parts. Strawberries depend on pollen dis- numbers explained fruit set similar to simple
persion over the whole stigma to develop completely models using species richness alone (Table 14.1).
formed fruits. Small wild bees pollinated predomi- Here, statistical limitations were reached, because
nantly at the base of the stigma, while large honey of the collinear nature between functional group
bees were active on the centre of flowers, pollinating richness, species richness, and individual numbers
the apical part of the stigma. Absence of one of the in the real world (as opposed to experimental)
two functional guilds causes deformed fruits, due to study systems.
incomplete resource use by only one functional These case studies comprising species with dif-
group. This example demonstrates that within-flower ferent plant breeding systems show that high
foraging behaviour can be strongly body size- flower-visiting species richness including different
 UNDERSTANDING THE ROLE OF SPECIES RICHNESS FOR CROP POLLINATION SERVICES 201

functional groups of flower visitors can lead to 14.4 Plant–flower visitor interaction
optimal (high levels with enhanced stability) polli- webs in crop pollination systems
nation services for agricultural systems. Many
Crop pollination studies are based on a given crop
studies show that flower-visiting communities are
and its pollinating species, although crop plants
structured by behavioural niche differentiation, due
may be influenced by interactions of their flower
to body size, circadian rhythm (as a result of dif-
visitors with nearby wild plants, forming networks
ferences in temperature tolerance), competition
of dozens to hundreds of species. To date, mutu-
hierarchy, sociality, and other species-specific
alistic network approaches have only been applied
behavioural traits (Bishop and Armbruster 1999,
in non-crop systems in order to understand eco-
Pinkus-Rendon et al. 2005, Stone 1994, Stone et al.
logical and evolutionary processes, but their appli-
1999). Hence different functional traits of a species
cation to crop systems may provide underlying
rich flower-visiting community can be important
information for managing and restoring flower-
because niche complementarity between species
visiting species richness and crop pollination
maximize both resource use and pollination ser-
services. In Section 14.4.1 plant–flower visitor
vices provided.
interaction webs (PFv webs) are shown and specific
characteristics of the general structure highlighted,
14.3.3 Functional facilitation followed in Section 14.4.2 by a discussion of the
importance of PFv web characteristics for species
A study by Greenleaf and Kremen (2006a) showed
extinction and integration. Afterwards the role of
that wild bees contribute to sunflower pollination
higher trophic levels for PFv webs is described
indirectly via facilitation. Hybrid sunflower seed
(Section 14.4.3). Section 14.4.4 summarizes some
production depends on animal-mediated pollen
ideas of how quantitative PFv webs provide infor-
transfer from male (pollen- and nectar-producing) to
mation to manage and restore flower-visiting spe-
female (only nectar-producing) parents. Although
cies richness for crop pollination services.
honey bees have low sunflower pollination efficiency
per-visit, they are the only commercially available
pollinators. Much higher pollination per visit effi-
14.4.1 PFv web structure and characteristics
ciency of honey bees was achieved in areas with
higher wild bee individual and species numbers. Fully quantified plant–flower visitor webs provide
Encounters between honey bees and wild bees the clearest description of the flower-visiting com-
increased the likelihood that honey bees switched munity structure, since they express the species
between female and male plants, thus increasing per- individual numbers and the frequency of interac-
visit pollination efficiency. Otherwise, individual tions among species (e.g. Forup et al. 2008, Memmott
honey bee foragers tended to forage either on male 1999, Fig. 2). Within such webs, the integration into
plants for pollen or on female plants for nectar, and the community of certain plants, like very rare spe-
rarely transferred pollen between plants. Another cies or an abundant flowering crop, or a managed
potential facilitative mechanism could be dispersal pollinator, such as honey bees, can be studied
of clumped pollen by honey bees of pollen depos- (Gibson et al. 2006, Memmott and Waser 2002). Here,
ited on female sunflowers by the wild bees. In the four PFv webs collected in an agricultural landscape
sunflower case, both individual and species number in Dorset, UK, are shown to demonstrate the inter-
of the wild bee community significantly contributed actions between bees, crop, and wild plant species of
to increasing the per visit pollination effectiveness surrounding flowering strips for bean (Fig. 14.2(a)),
of honey bees (Greenleaf and Kremen 2006a). oilseed rape (Fig. 14.2(b)), and lupine (Fig. 14.2(c)).
However, in examples where only a few species are An additional PFv web in calcareous grassland is
involved in interspecific interactions, species iden- shown to visualize the differences between crop PFv
tity and individual numbers might be more webs and a PFv web of a semi-natural habitat
important than species richness per se (Jonsson and without crop species (Fig. 14.2(d)). The webs of
Malmqvist 2003). the crop fields are ordered from relatively poor
202 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

(a)
sb B.pr B.pa B.t/l B.j ps B.h B.l hb

7 77
140 Vicia faba
125 122

(b) sb ps
B.pr B.pa B.h B.t/1 B.1 hb

125 37 116 Linum Brassica napus

47 34 perenne
134 18 89

(c)
B.pa B.1 sb hb B.t/1 B.j B.h

35 41 34 120
37 Lotus uliginosus 116 134
59 71 Lupinus luteus

(d) B.pr

B.h B.h B.pa B.1 B.t/1 ps sb

133 33 126 8 14 113 88 67 119 60 134 29 99 117 64 3 40

125 24 37 135 34 55 20 131 22 4910681
124 116 130 118 82 71

Figure 14.2 Quantified PFv webs in (a) bean, (b) oilseed rape, (c) lupine, and (d) calcareous grassland. The area sampled ranged between 10 and 13 ha
and included a 10 m margin of flowering herbs around each crop field. Quantification was done by counting the specific interactions between a plant and a bee species
over a sampling time of two to three hours on a sunny, windless day, except in the case of the grassland, where sampling was done repeatedly over the
period of floral availability. All flowering plants were counted within one metre quadrates that were placed in a stratified manner over the area to estimate the
 UNDERSTANDING THE ROLE OF SPECIES RICHNESS FOR CROP POLLINATION SERVICES 203

plant-flowering strips of the bean field to relatively eralist insects (Bascompte et al. 2003, Bascompte
rich plant strips of the lupine field. The oilseed rape et al. 2006, Blüthgen et al. 2007, Montoya et al. 2006,
field was adjacent to a linseed field which was at the May 2006). This nestedness leads to an asymmetry in
end of its flowering period during sampling. The plant–flower visitor interactions with strong depen-
most abundant generalist bees were bumble bees, dence in one direction often linked to weak depen-
Bombus terrestris/lucorum, which were strongly dence in the reverse direction (Thompson 2006,
attracted to the flowering crop, while more special- Vázquez and Aizen 2004). Furthermore, mutualistc
ized bumblebees, such as B. pascuorum, B. lapidarius, networks are dominated by a few extreme generalists,
B. hortorum and solitary bees appeared to prefer meaning only a few species build the core of the
alternative flowering resources in the flowering nested web and are much more connected than
strips. There was little attraction for solitary bees to would be expected by chance (Jordano et al. 2003).
either bean or oilseed rape, while lupine was visited
frequently by leafcutter bees. In comparison, more
14.4.2 Species extinction and integration
evenly distributed interactions among plants and
in PFv webs
bees and a species-rich local community of solitary
bees were found in calcareous grasslands where bees Habitat loss or alteration, species extinction and
specialized on many different plant species (Fig. 14.2 addition of invasive species are the main factors
(d)). Honey bees as generalist foragers were strongly disrupting PFv webs. Given the current, accelerated
attracted to mass-flowering crop and were not biodiversity loss, it becomes important to under-
encountered in the grassland (non-crop) site. stand how whole networks of interacting plant and
The four quantitative PFv webs visualize the animal species are affected by extinction events and
interaction between crop and wild plants and their especially how extinction events might affect crop
flower-visiting species and can be used to identify pollination services. The characteristic structure of
whether the use of flowering strips adjacent to a crop PFv (nestedness and asymmetry) provides impor-
field attracts several species to forage and interact via tant alternative routes when species disappear and
facilitation and complementarity to benefit the crop or thus a certain insurance against biodiversity loss
divert flower-visiting species from the crop plants, (Bascompte et al. 2006, Memmott et al. 2004).
which could lead to reduced flower visitation. Simulated progressive extinction models are cur-
PFv webs are characterized by their highly nested rently only available for non-crop flower visitor
structure. This indicates that flower-visiting spe- webs. Memmott et al. (2004), for example, simulated
cialists mainly interact with generalized plants that flower-visiting species extinction to explore the
are visited by a whole array of other flower-visiting resulting extinctions in plants depending on flower
species. Specialist plants tend to be visited by gen- visitors for reproduction. The extinction scenarios

Figure 14.2 (continued)

abundance of floral resources per square metre. Bee counts were then extrapolated to the square metre unit. The upper represents bees and the lower bars plants.
Each bar depicts a species and the length of the bar contains information about its abundance. The wedges depict interactions between plants and pollinating bees. The
width at the basis of a wedge contains information about the interaction strengths. Honey bees (hb) did not occur in the grassland but were abundant on all three crop
species. Bumble-bee groups consisted of Bombus terrestris and B. lucorum (B.t/l: pooled because they were difficult to distinguish in the field), B. lapidarius (B.l), B.
pascuorum (B.pa), B. pratorum (B.pr), B. hortorum (B.h), B. jonellus (B.j) and parasitic Bombus species (ps; former Psythirus). Solitary bees (sr) were pooled because
straight identification in the field was difficult. The flowering crop plants were labelled by name and bars were depicted in grey; the other plant species were: 3 ¼
Achillea millefolium, 7 ¼ Anchusa arvensis, 8 ¼ Anthyllis vulneraria, 14 ¼ Bellis perennis, 18 ¼ Buddleja davidii; 20 ¼ Campanula glomerata,
22 ¼ Campanula rotundifolia, 24 ¼ Carduus nutans, 29 ¼ Centaurea nigra, 33 ¼ Cirsium acaulis, 34 ¼ Cirsium arvense, 35 ¼ Cirsium palustre, 37 ¼ Cirsium
vulgare, 40 ¼ Crepis capillaris, 41 ¼ Crepis paludosa, 47 ¼ Digitalis purpurea, 49 ¼ Echium vulgare, 55 ¼ Eupatorium cannabium, 59 ¼ Galeopsis tetrahit,
60 ¼ Genista tintoria, 64 ¼ Helianthemum nummularium, 67 ¼ Hippocrepis comosa, 71 ¼ Hypochaeris radicata, 77 ¼ Lamium purpureum, 81 ¼ Leontodon
autumnalis, 82 ¼ Leontodon hispidus, 88 ¼ Lotus corniculatus, 89 ¼ Lotus uliginosus, 99 ¼ Odontites verna, 106 ¼ Pilosella officinarum, 113 ¼ Ranunculus
repens, 116 ¼ Rubus fruticosus, 117 ¼ Scabiosa columbaria, 118 ¼ Senecio jacobaea, 119 ¼ Serratula tintoria, 120 ¼ Silene dioica, 122 ¼ Sinapis,
124 ¼ Stachys officinalis, 125 ¼ Stachys selvatica, 126 ¼ Succisa pratensis, 130 ¼ Teucrium scorodonia, 131 ¼ Thymus polytrichus, 133 ¼ Trifolium pratensis,
134 ¼ Trifolium repens, 135 ¼ Ulex europaeus, 140 ¼ Veronica persica.
204 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

were either random extinction of flower-visiting 2007). By analogy, these studies suggest that flow-
species, extinction from least linked to most linked ering crop species will be visited by flower-visiting
species, or vice versa. The webs were surprisingly generalist species and will integrate reasonably well
robust towards flower-visiting species extinctions in existent interactions webs.
unless the most generalist (most linked) species were
removed first. In this case, the extinction trajectory of
14.4.3 Higher trophic levels in PFv webs
plant species was tightly correlated to that of
declining flower-visiting species richness following a A further aspect that can be examined using the food
relatively rapid (essentially linear) decline. Further- web approach is to elucidate the role of higher trophic
more, some morphological features, such as body levels such as natural enemies of pollinators
size, may make certain flower-visiting species more like predators, parasites, and parasitoids. Because of
prone to extinction than others. Hence in systems habitat losses and modifications through agricultural
where generalist flower-visiting species are large practices, pollinator communities may become more
bodied, extinction would follow the worst-case sce- susceptible to some dominant enemies (Klein et al.
nario and pollination function would disappear as 2006). A well-documented case is the dramatic
quickly as flower-visiting species (Larsen et al. 2005). increase of managed (Downey and Winston 2001)
The opposite of extinction through habitat loss is and feral (Kraus and Page 1995) honey bees infested
the integration of alien species into existing mutu- by the Varroa mites and the subsequent declines or
alistic networks. In some ways, this occurs in crop losses of many colonies. PFv webs analyzed to date,
systems when sudden appearance of abundant floral however, exclude predators, parasitoids, and dis-
resources (the flowering crop) will change the eases. Higher trophic levels increase the connected-
behaviour of the flower-visiting species. Resident ness and nestedness of food webs (Lafferty et al. 2006),
plants may either facilitate (increase) or compete but food web properties are affected by more than just
with (decrease) visitation to the introduced (crop) the species present. Habitat modification through
plant. Experimental studies on such multi-species agriculture also affects food web properties. These
interactions typically have looked at the role of properties may negatively affect species richness,
invasive plants on wild plant reproduction and have composition of communities, and the diversity and
show various results from negative (Chittka and strength of interactions. Tylianakis et al. (2007), for
Schürkens 2001, Ghazoul 2002, Larson et al. 2006), to example, used 48 quantitative parasitoid–host (bee
positive (Johnson et al. 2003, Moller 2004), to neutral and wasp) webs and showed, although overall spe-
(Aigner 2004). Community studies that investigate cies richness were not affected by land-use intensity,
the impact of alien plant species on the whole that web properties, such as connectance, linkage
mutualistic network show substantial integration of density, compartment diversity, and interaction
these plants into native PFv webs, with generalist evenness, were all affected by land-use management.
flower-visiting speices most likely to visit introduced This can be explained by the high vulnerablility of the
plant species (Memmott and Waser 2002, Morales interaction structure to the presence, identity, phe-
and Aizen 2006). Studies on the effects of one alien nology, physiology, behaviour, and diversity of dif-
plant on an array of native plants find mixed results ferent species. Hence, parasitoid–host interactions
that depend on the species identity of native plants might show changes before species loss becomes
(Moragues and Traveset 2005) and on the stages of apparent (Tylianakis 2008).
invasion (Aizen et al. 2008b). Despite increased visi-
tation frequencies in plots with a highly rewarding
14.4.4 Quantitative PFv webs and the
invasive plant, pollination of native plant species is
management of crop pollination services
not necessarily facilitated by the co-occurrence of
these high-rewarding alien plant species, possibly In summary, quantitative food web analysis visua-
because of the large amount of alien pollen they lizes the structure and links between trophic levels
receive (Larson et al. 2006), as was shown by quan- and provides more detailed views of entire commu-
tified pollen transport webs (Lopezaraiza-Mikel et al. nities when assessing management effects on
 UNDERSTANDING THE ROLE OF SPECIES RICHNESS FOR CROP POLLINATION SERVICES 205

crop-flower visitor interactions. Nestedeness, asym- with historical records (pre-1980) have indicated
metry, and interaction strength are PFv characteristics significant regional declines in species richness of
that might indicate stability in crop pollination ser- major pollinator groups and the plants they polli-
vices, meaning insurance for flower-visiting species nate (bees and hover flies in Britain, bees alone in
losses and effects of added invasive species. the Netherlands) (Beismeijer et al. 2006). Despite the
Quantitative analyses can be also used to assess alternative routes in PFv webs when species disap-
crop pollination services of multi-cropping systems pear, a recent meta-analysis on effects of habitat
or to evaluate management or restoration plans fragmentation on plant reproduction demonstrated
using flowering strips. Here web analyses give that the reproductive success of self-incompatible
detailed information to help selecting appropriate (i.e. typically pollinator-dependent) but not self-
wild flowering plant species, which do not divert compatible plants is strongly negatively influenced by
flower-visiting insects from the crop plant and habitat fragmentation, and that effects on both polli-
provide additional resources for them. Conversely, nation and reproductive success were strongly cor-
quantitative webs can also help to understand related (Aguilar et al. 2006). These results strongly
whether crop flower resources benefit certain wild implicate pollinator loss as a major causative factor for
flower-visiting insect species and/or their enemies, the susceptibility of plant reproduction to one major
species of the higher trophic level. In this respect, disturbance, habitat fragmentation.
statistical analyses using replicated networks to Large reductions in species richness and individual
show, for example, degrees of specialization and numbers of bees have also been documented in
generalization of the enemy species, the flower- regions of high agricultural intensity in California’s
visiting species, and plant species and the number Central Valley (Kremen et al. 2002, Klein and Kremen
of shared species in different management condi- unpublished). Traits associated with bee and hoverfly
tions will help to understand management effects on declines in Europe included floral specialization,
the flower-visiting community and its services for slower (univoltine) development, and lower dispersal
crop and wild plants (Forup et al. 2008, Tylianakis (non-migratory) species (Beismeijer et al. 2006). In the
et al. 2008). most well-known taxon, bumble bees in Europe,
declining species are long-tongued specialists on
Fabaceae, and their increasing rarity may be due to
14.5 Consequences of pollinator
the loss of unimproved grasslands that are rich in
decline for the global food supply
their food resources (Goulson et al. 2008). Specializa-
Both wild and managed pollinators have suffered tion is also indicated as a possible correlate of local
significant declines in recent years. Managed Apis extinction in flower-visiting communities studied
mellifera, the most important global source of crop across a disturbance gradient in Canada. It could be
pollination services, have been diminishing around shown that communities in disturbed habitat con-
the globe and particularly in the USA, where colony tained significantly more generalized species than
numbers are now at < 50 per cent of their 1950 levels those associated with pristine habitats (Taki and
(NRC 2006). In addition, major and extensive colony Kevan 2007). Large-bodied bees were more sensitive
losses have occurred over the past several years in to increasing agricultural intensification in Cali-
North America and Europe, possibly due to diseases fornia’s Central Valley, and ominously, bees with the
and other factors (Cox-Foster et al. 2007, Stokstad highest per-visit pollination efficiencies were also
2007), causing shortages and rapid increases in the most likely to go locally extinct with agricultural
price of pollination services (Sumner and Boriss intensification (Larsen et al 2005).
2006). These recent trends in honey bee health Thus, in highly intensive farming regions such as
illustrate the extreme risk of relying on a single bee California’s Central Valley that contribute compara-
species to pollinate the 75 per cent of crops that rely tively large amounts to global food production (e.g.
to some degree on insect visitation. 50 per cent of the world supply of almonds), the
At the same time, although records are sorely supply of wild bee species is lowest in exactly the
lacking for most regions, comparisons of recent regions where the demand for pollination services is
206 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

highest. Published (Kremen et al. 2002) and recent Nutritional consequences may be more fixed and
studies (Klein and Kremen, unpublished) clearly more serious than economic consequences, due to
show that the services provided by wild bee flower- the likely plasticity of responses to economic
visiting species are not sufficient to meet the demand change. The 75 per cent of crop species that are
for pollinators in these intensive regions. These pollinator-dependent supply not only up to 35 per
regions are instead entirely reliant on managed honey cent of crop production by weight (Klein et al.
bees for pollination services. If trends towards 2007), but also provide essential vitamins, nutrients,
increased agricultural intensification continue else- and fibre for a healthy diet (Gallai et al. 2008,
where (e.g. as in Brazil, Morton et al. 2006), then pol- Kremen et al. 2007). The nutritional consequences of
lination services from wild species are highly likely to total pollinator loss for human health have yet to be
decline in other regions, based on a recent compre- quantified. However, food recommendations for
hensive analysis across 16 crops on five continents minimal daily portions of fruits and vegetables are
that showed how wild bee pollinators decline in spe- well known and already often not met in diets of
cies richness and individual numbers with distance both developed and underdeveloped countries.
from natural habitats (Ricketts et al. 2008). At the same
time, global food production is shifting increasingly
14.6 Conclusions and future directions
towards production of pollinator-dependent foods
(Aizen et al. 2008a), increasing our need for managed Pollination is a critical step in the reproduction of
and wild pollinators yet further. Global warming, many plant species and can significantly reduce pri-
which could cause mis-matches between flower- mary production in natural communities and crop
visiting species and the plants they feed upon, may fruit set and quality in agricultural systems if not
exacerbate pollinator decline (Memmott et al. 2007). provided or provided in adequate supply. Some
For these reasons, more serious shortages of pollina- landscapes promote high flower-visiting species rich-
tors in the future may indeed be faced. ness and frequency offering adequate crop pollination
A recent global assessment of the economic services because they offer season-around foraging
impact of pollinator loss (e.g. total loss of pollina- and nesting resources (Kremen et al. 2002, Winfree
tors worldwide) estimates our vulnerability (loss of et al. 2008). Simple landscapes with low proportion of
economic value) at (153 billion or 10 per cent of the natural and semi-natural habitats can negatively affect
total economic value of annual crop production flower-visiting species richness and frequency, which
(Gallai et al. 2008), a much larger figure than pre- sometimes affect fruit set (Ricketts et al. 2008). Con-
vious global estimates (e.g. Costanza et al. 1997). sequently, in intensively managed agricultural land-
Although total loss of pollination services is unli- scapes where pollinator-dependent crops are grown,
kely to occur and to cause widespread famine, they farmers are managing bees for pollination services, as
potentially have both economic and human health for example in alfalfa, almond, watermelon, and
consequences. For example, some regions of the sunflower production in California. The effect of iso-
world produce large proportions of the world’s lation from natural habitats on crop pollination in
pollinator-dependent crops. Such regions would 23 studies is summarized by Ricketts et al. (2008), but
experience more severe economic consequences more studies using fruit set and production data are
from the loss of pollinators, although farmers and needed to produce key synthetic results.
industries would undoubtedly quickly respond to Can high numbers of just one species like the
these changes in a variety of ways, passing the honey bee substitute for flower-visiting species
principle economic burden on to consumers glob- richness? Californian’s farmers are producing high
ally (Gallai et al. 2008, Southwick and Southwick yields and the honey bee pollination strategy seems
2002). Measures of the impacts on consumers to be successful. The examples discussed in this
(consumer surplus) are of the same order of mag- chapter indicate that in some situations managing
nitude ((195–310 billion based on reasonable esti- for one pollinator species will not only result in
mates for price elasticities, Gallai et al. 2008) as the higher pollination insurance but also result in
impact on total economic value of crop production. optimal pollination success. Different mechanisms
 UNDERSTANDING THE ROLE OF SPECIES RICHNESS FOR CROP POLLINATION SERVICES 207

lead to these effects, such as niche complemantarity trophic levels. These complex interactions outside
for resources, facilitation among species, or sam- the crop-flower visitor network itself have received
pling to reach highest pollination frequency. little attention to date. Quantitative PFv webs can
What further research is needed for a holistic be used to (1) assess crop pollination services of
understanding of the role of flower-visiting species muti-cropping systems or to evaluate crop pollina-
richness for crop pollination? To predict in which tion management or restoration plans using flow-
crop-flower-visiting system and under which condi- ering strips, (2) and help to understand whether
tions species or functional group richness can be a crop flower resources benefit certain wild flower-
limiting factor for pollination services, research in visiting insect species or their enemies.
experimental settings to separate for the effects of Studies in real systems need to include the complex
functional group richness, species richness, and indi- spatio-temporal multitrophic interactions among pol-
vidual numbers per se are needed. Flower-visiting linating species, their mutualistic partners, and their
community composition needs to be experimentally enemies. Ideally, all production limiting factors and
set up to separate out the effects of aggregate abun- services per crop production system should be studied
dance and species richness on pollination services. to calculate the exact value of pollination services to
Such experiments are frequenctly carried out for plant crop production (Bos et al. 2007). As many farmers will
communites to understand plant productivity. For only adopt restoration activities on their properties
pollination services, it is important to understand how when recongnizing an economic advantage, oppor-
much a species-rich, but individual-poor flower- tunity cost for restoration and conservation programs
visiting community can buffer pollination services loss needs to be calculated (Ghazoul 2007). Estimating
of an abundant species like the European honey bee. the costs and benefits of restoring pollinator habitat
Mechanisms of species richness–pollination ser- for increasing wild pollination services are also needed
vices relationships are complex, particularly when to assess the economic potential for conservation-
considering whole PFv webs including different incentive markets for pollination services.

Box 14.1 Economic value of bees as crop pollinators – the case of alfalfa seed production

Commercial pollination services are mainly provided by carried out, as it was noted already in 1940 that a high
managed honey bees through a standing and organized diversity of insect species are visiting alfalfa flowers. Some
market between beekeepers and farmers. At the global solitary bee species were also noted to forage under different
scale, alfalfa seed production depends on the services of environmental conditions (Bohart 1947, Olmstead and
managed honey bees (mainly in California) and other Wooten 1987, Mueller 1999). Even for California with the
managed species like alkali bees and leafcutter bees (mainly honey bee as the cheapest and most important pollinator,
in Canada, western USA), and managed bumble bees (in farm advisers recommended a combination of leafcutter bees
Turkey), but also on diverse wild insect communities, and honey bees to reach high seed production (Mueller
because seed production and quality is extremely low (4 per 1999). Experimental testing, however of whether the honey
cent) if pollinators are excluded (Cecen et al. 2008). bee alone or a combination with other bee species results in
Alfalfa or Lucerne, Medicago sativa L., is the most higher seed set or quality is missing.
important forage crop in many parts of the world (FAOStat Although bumble bees and solitary bees access the alfalfa
2006). Economic markets for pollination services for the blossoms in a more effective way, resulting in higher per visit
Californian alfalfa industry developed between 1949 and seed numbers relative to honey bee visits (Delaplane and
1951 (Sumner and Boriss 2006). Commercial pollination for Mayer 2000, Cecen et al. 2008), honey bees are dominant in
alfalfa started with honey bee pollination experiments in alfalfa seed production. In California, farmers usually prefer
1947 followed by increased renting of honey bees for short-term honey bee colony rental because these portable
alfalfa seed production. At the same time, research to use pollination units are cheap and beekeepers usually take the
alkali bees and leafcutter bees for alfalfa seed production was responsibility to provide strong units during bloom.
Continues
208 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Box 14.1 (Continued ) bees (Sumner and Boriss 2006). The cost to manage leafcutter
The establishment of solitary bee nests is expensive and bees on alfalfa-growing land is available and was calculated
farmers need additional training for successful long-term for a management period of 15 years (British Columbia
establishment. Losey and Vaughan (2006) estimated the value Ministry of Agriculture and Food 1998). Management costs of
of wild bees (excluding pollination by managed bees) for leafcutter bees to pollinate alfalfa are similar to those of
alfalfa seed production. They assigned an annual amount of honey bee renting during alfalfa bloom. This is only the case
$5.45 million to wild pollinators. This is 5 per cent of the when managing leafcutter bees over a longer time period, as
annual average US gross yield for alfalfa seed production, the main expenses are covered in the first year of leafcutter
assuming that 5 per cent of this production is provided by bee establishment (bee cocoons, nesting blocks, nesting
wild bees. This upper-bound value represents the contribution shelters). In other words, only long-term management of
of wild pollinators to gross production. Such a calculation solitary bees is economically reasonable.
does not consider future adaptive responses by farmers and The average annual value (gross yield) of the total alfalfa
consumers to pollinator decline (Muth and Thurman 1995). seed production in Montana is $4,729,400 (USDA-NASS
Such responses, like adopting alternative crops or farming 2008). The state-wide farmer’s cost and value for the
techniques that reduce the dependence of farmers on pollination services of honey bees was calculated to be
pollinators, will lower the value of pollination services from $1,220,550 and for leafcutter bees $1,394,620 (see table
wild pollinators, as would consideration of net rather than below). Thus pollination service values (farmer’s cost) represent
gross revenues (Olschewski et al. 2006). about 25.8–29 per cent of the value (gross yield) of this crop.
Another approach to assess pollination services by Relying on a single pollinator species is a risky strategy
managed bees is to estimate how many bee workers will be and this chapter highlights that in at least some cases
needed to fully pollinate a given area of crop production different species can complement each other to achieve the
(Robinson et al. 1989). Here, such a lower-bound value based best pollination results. An equivalent economic evaluation
on production and cost per area of alfalfa seed production in approach to estimate the pollination services provided by
Montana (USDA-NASS 2008) is calculated for pollination wild flower-visiting communities is to calculate replacement
services provided by rented honey bees and by managed costs for honey bees by wild insects (Kremen et al. 2007).
leafcutter bees (table below). Mean honey bee colony rental For this approach a calculation of the costs to restore
numbers and mean renting cost for the blooming period of agricultural landscapes for crops to get full pollination
alfalfa were used to calculate farmers’ costs for renting honey services by wild insects is needed, but to date not available.

Annual value of bee pollination of alfalfa seed production in Montana, based (a) on farmer’s mean annual cost of renting honey bees; or (b) managing
leafcutter bees, to fully pollinate alfalfa for seed production based on 1997–2007 production and yield data.

Area in Stocking rate Rental, management Cost/ha State-wide

production (ha) (hives/ha or cost ($/hive, $/10,000 cells)2 cost ($)
bee cells/ha)1

Honey bees 5150 7.9 30 237 1,220,550

Leafcutter 5150 74,100 36.6 270.8 1,394,620
bees

1
average number calculated by Delaplane and Mayer (2000)
2
HB¼ average annual value considering the years of 1996–2005 (Sumner and Boriss 2006); LCB ¼ average annual value for bee management of 15 years
(British Columbia Ministry of Agriculture and Food 1998).
 CHAPTER 15

Biodiversity and ecosystem

function: perspectives on disease
Richard S. Ostfeld, Matthew Thomas, and Felicia Keesing

15.1 Introduction here that the role of biodiversity may resonate with
Experimental and comparative studies increasingly citizens. Recent studies have shown that high bio-
reveal that certain ecosystem functions are maximized diversity can strongly reduce rates of disease trans-
in highly diverse ecological communities. Key among mission, and consequently that biodiversity loss can
the ecosystem functions correlated with high biodi- exacerbate disease risk. These studies themselves are
versity are rates of nutrient cycling, primary produc- diverse in the aspects of biodiversity under study, in
tion, and resistance to disturbances such as drought the taxa of pathogens, hosts, and vectors involved,
(see Chapters 1 and 2). Despite considerable interest and in the mechanisms postulated. For example,
among ecologists in this dynamic area of research, we high genotypic diversity within a species reduces
suspect that non-ecologists are unaware of or unim- transmission of bacteriophages that attack bacteria
pressed by these functions served by high biodiversity. (Dennehy et al. 2007), microsporidians that attack
A 2007 survey shows that considerably more respon- Daphnia water fleas (Pulkkinen 2007), and fungi that
dents in the European Union consider moral reasons attack rice plants (Zhu et al. 2000). On the other
stronger than utilitarian or economic reasons for pro- hand, high species richness reduces transmission of
tecting biodiversity (http://www.ec.europa.eu/pub- fungal pathogens of herbaceous plants (Roscher et al.
lic_opinion/archives/flash_arch_en.htm). In a 2002 2007), viral pathogens of birds and humans (Ezenwa
survey in the USA (http://www.biodiversityproject. et al. 2006), helminth parasites of snails and verte-
org/resourcespublicopinion.htm), utilitarian and eco- brates (Kopp and Jokela 2007), and bacterial patho-
nomic functions of biodiversity, with the exception of gens of humans and other mammals (Ostfeld and
human health, are not even mentioned. It would Keesing 2000a, LoGiudice et al. 2003). Reduced
appear that the ecosystem functions typically addres- structural diversity in tropical forests as a result of
sed by biodiversity scientists are not among the prin- deforestation has been associated with higher risk of
cipal concerns of many citizens when considering the exposure to malaria (Vittor et al. 2006). High diver-
consequences of biodiversity loss, even though there sity can reduce disease transmission by reducing
are increasing arguments for why we should be con- encounter rates between infected and susceptible
cerned (the Millennium Ecosystem Assessment hosts, and by regulating the abundance of species
(2005a) see Chapters 17–19). Globally, the Convention that are important for pathogen persistence, among
on Biological Diversity has been signed or ratified by other mechanisms (Keesing et al. 2006). Knowledge
the vast majority of the world’s nations, committing that biodiversity influences human health and that
them to preserve biodiversity in order to achieve sus- of valued wildlife and plants is likely to heighten
tainable development, but it has had little traction. interest among both scientists and non-scientists in
Thus, there is a disconnect between public perception the importance of biodiversity.
and governmental and scientific understandings. In this chapter we explore some of the major
The public, however, is interested in disease, both issues that have shaped recent explorations of the
newly emerging and resurgent diseases, and it is biodiversity-ecosystem function relationship and

209
210 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

apply these concepts to infectious diseases. These incidence. For West Nile virus incidence rates in
issues include: (1) the shape of the association humans (Ezenwa et al. 2006), and both prevalence
between biodiversity and ecosystem function; (2) the and severity of rust fungal infection in perennial
relative importance of species biodiversity per se ryegrass (Roscher et al. 2007), biodiversity–disease
(e.g. species richness or evenness) vs species com- curves were negative and apparently linear. In
position; (3) the relative importance of species bio- contrast, for Lyme disease risk (measured both as
diversity per se versus diversity of functional groups density of infected ticks and as tick infection prev-
or relevant life history traits; (4) whether functions alence), increases in biodiversity resulted in curvi-
are performed better by the most diverse commu- linear decreases to an asymptote (Schmidt and
nities or by monocultures of the species with highest Ostfeld 2001, Ostfeld and LoGiudice 2003). Dizney
performance of that specific function; (5) how and Ruedas (in press) show a strongly asymptotic,
natural sequences of species loss under environ- negative relationship between mammalian diversity
mental change (community disassembly) vs. ran- and prevalence of infection of deer mice with
dom sequences imposed experimentally influence hantavirus. Other studies linking biodiversity and
ecosystem function; and (6) the importance of disease dynamics cannot address this issue because
diversity at organizational levels other than (host) of insufficient variation in diversity; when com-
species in influencing ecosystem function. Because parisons are restricted to communities with one
the empirical basis for exploring these particular versus two or three species, curve shape cannot be
issues is limited, we focus on describing each issue estimated.
as it pertains to infectious disease and speculating on We suspect that, in some cases, the shape of the
what might be found in future studies. curve relating biodiversity to disease risk might be
more complex than simple linear or asymptotic
functions. In particular, for arthropod vectors or
15.2 Shape of diversity–disease curves
parasites with complex life cycles, some lower
When the performance of an ecosystem function threshold level of diversity might be necessary for
increases linearly with increases in biodiversity, the disease to exist. This would occur if the vector
three related conclusions can be drawn. First, each or parasite requires several host species to fulfil its
species contributes approximately equally to the life cycle. Beyond this lower richness threshold,
ecosystem function. Second, functional redundancy however, one might expect a negative relationship
among species is weak. Third, the loss of biodi- between diversity and disease transmission, leading
versity will result in reduced functioning, irrespec- to a unimodal distribution. We are not aware of
tive of initial diversity. In contrast, the performance specific tests of this hypothesis.
of an ecosystem function can increase asymptoti-
cally with increasing biodiversity, implying that
15.3 Diversity (richness) versus species
individual species contribute unequally, that some
composition
redundancy occurs (particularly in highly diverse
communities), and that loss of biodiversity has a When individual species have strongly disparate
stronger impact on ecosystem functioning when the effects on an ecosystem function, then the species
initial community is species-poor than when it is composition (identity and relative abundance of all
species-rich (Schwartz et al. 2000 and Chapter 1). species) of a community is likely to be more
The shapes of curves relating some measure of important than the number of species or the quan-
disease dynamics (e.g. risk or incidence) to species titative value of a diversity metric such as the
richness have only rarely been measured or pre- Shannon index or Simpson index. Much debate has
dicted, but the scientific basis for the relationships surrounded the issue of how to contend with this
between biodiversity and these properties of eco- issue (see Chapter 4). For researchers interested spe-
systems are the same for functions such as energy cifically in effects of species richness, the potential for
flow and nutrient cycling; each species contributes species to have unequal effects is sometimes consid-
in some way, uniquely or redundantly, to risk or ered a complication to be minimized by carefully
 BIODIVERSITY AND ECOSYSTEM FUNCTION: PERSPECTIVES ON DISEASE 211

designed experiments. Often, these researchers will functions (e.g. rate of resource depletion or of net
generate experimental communities by randomly primary production). As a consequence, researchers
selecting species and creating replicate communities have begun to classify species into functional
at each level of diversity, in order to account for groups (e.g. grouping herbaceous plant communi-
sampling artifacts. Such a design is intended to ties into legumes, non-leguminous forbs, and
reduce the probability that the random inclusion of grasses) and ask whether diversity of functional
species with particularly strong effects is responsible groups better explains ecosystem functions than
for the relationship between diversity and function does species diversity (e.g. Naeem and Wright
(see Chapters 1 and 2). However, these randomly 2003, Reich et al. 2004). Functional group classifi-
assembled communities might not represent real cations often are based on taxonomy or on physi-
communities of interacting species. To contend with ology directly relevant to the ecosystem function of
this possibility, researchers concerned with how interest (i.e. they represent ‘complementarity’ of
natural variation in diversity causes natural variation functions). In most cases, functional group diversity
in ecosystem functioning must attempt to constrain performs better than species diversity in explaining
species composition to mimic natural patterns and ecosystem functioning (Diaz and Cabido 2001,
determine the relative importance of richness versus Hooper et al. 2005, Reich et al. 2004). However, the
composition. predictive precision of standard classifications of
We are aware of only one study that explicitly species into functional groups rarely is significantly
contrasted species richness and community compo- higher than that of random classifications (Wright
sition in affecting disease dynamics. In this study, et al. 2006 and Chapter 4), and the most appropriate
LoGiudice et al. (2008) assessed the causes of varia- algorithms for classifying species into functional
tion in the proportion of nymphal blacklegged ticks groups are not yet clear.
infected with the Lyme disease spirochete among 49 Comparisons of species diversity versus diversity
forest fragments in three northeastern USA states. in functional traits have not, to our knowledge,
They found that species richness was significantly, been made for studies of the effects of biodiversity
but weakly, negatively correlated with nymphal on disease dynamics. Potentially, one could cate-
infection prevalence. However, when they predicted gorize hosts of a pathogen according to their abili-
nymphal infection prevalence using a model that ties to support pathogen population growth and
specifically incorporated species identity, their transmission (i.e. reservoir competence). Alterna-
results were significant and strong. Qualitatively tively, one could categorize species in a community
similar results were obtained in studies of foliar by trophic level relative to the predominant hosts
fungal pathogens on grassland plants (Knops et al. for the pathogen. Such a categorization would
1999, Mitchell et al. 2002, 2003). Although severity of allow researchers to ask whether diversity of nat-
fungal disease was negatively correlated with spe- ural enemies of the host, or of resources for the
cies richness, the effect of diversity on disease host, reduces or enhances disease transmission
severity was indirect; plots with higher diversity (Ostfeld and Holt 2004, Holt 2008).
had lower density of the most susceptible grass Increasingly, there is a move to abandon func-
hosts, and disease severity was positively correlated tional groups and focus on species traits, or the
with host density (Mitchell et al. 2002). As a conse- characters of species that represent what they do,
quence, it appears that community composition had but disease ecologists are only now evaluating this
a more direct impact on disease dynamics than did approach. For example, host quality, reservoir
species diversity per se. competence, body size, longevity, reproductive
rate, and other traits would cleanly identify species
into their roles in particular processes, which seems
15.4 Species diversity versus functional
far more useful than attempting to group species
or trait diversity
into discrete categories when most species overlap
In many ecological communities, some species are in what they do (see Chapter 4). Studies of plant
strongly similar in their performance of particular traits abound, but the study of traits of heterotrophs
212 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

lags behind, and of pathogens and their hosts, even shrews – are responsible for feeding and infecting a
further behind (see Chapter 20). large percentage of the tick vector of the bacterial
pathogen (Brisson et al. 2008). A large suite of other
mammals and birds feed many ticks, but infect very
15.5 Most diverse versus single
few of them, and are considered ‘dilution hosts’
highest functioning
(Ostfeld and Keesing 2000). The dilution hosts dif-
Niche theory predicts that natural communities will fer in the degree to which they reduce the propor-
consist of species that do not overlap completely in tion of ticks infected, with grey squirrels being the
their suite of functions. One consequence of this most potent of the group (Ostfeld and LoGiudice
expectation is that a diverse assemblage of species 2003, Ostfeld et al. 2006). Simulation models indi-
will tend to perform ecosystem functions more cate that a ‘community’ of dilution hosts consisting
efficiently than will a monoculture, even if the solely of grey squirrels would reduce disease risk to
species comprising the monoculture is more effi- lower levels than would a naturally diverse com-
cient than other single species. In other words, the munity of dilution hosts (R. S. Ostfeld, unpub-
functional complementarity arising from poly- lished). One caveat to generalizing from this result
cultures can cause them to out-perform all mono- is that the performance of an ecosystem function,
cultures. Selection effects, however, in which one or such as diluting disease risk, by a particular species
a few species have disproportionate impacts on is often contingent on the composition of the
ecosystem functioning, may dominate and mini- remaining community. For instance, shrews can act
mize the influence of complementarity. While there as a dilution host in some (species-poor) commu-
is strong evidence for complementarity in some nities, but as an amplification host in other (species-
studies, other experimental studies comparing per- rich) communities (Ostfeld et al. 2006). This is an
formance of diverse communities to monocultures example of context dependency that is well
suggest that selection effects are stronger than described in other studies of biodiversity-ecosystem
complementarity (reviewed in Cardinale et al. functioning (Chapter 4). Therefore comparisons of
2006a). On the other hand, this pattern may also be performance in monoculture vs. polyculture must
due to limitations in the existing empirical studies be made with caution. Even if monocultures of
and their interpretation. Cardinale et al. (2007) high-performing species outperform polycultures in
demonstrated that most of the reported plant-based diluting disease risk, applying this knowledge to
studies actually do exhibit complementarity, or at real-world situations seems difficult or impossible.
least do not support the sampling effect alone. The Returning to the Lyme disease example, replacing a
resolution of this issue is important because the diverse assemblage of vertebrates with a monocul-
consequences for both the biodiversity-ecosystem ture of squirrels seems neither practical nor desir-
function debate and the conservation of biodiver- able, even though it would reduce disease risk. Of
sity are so profound. course, these issues highlight the importance of
Whether, or under what circumstances, mono- defining what we mean by function. If the only
cultures can perform better than polycultures in function of interest is reducing risk of Lyme disease,
influencing disease dynamics has not, to our then one non-permissive species might suffice, but
knowledge, been assessed. Numerous examples of if we are concerned with other diseases (i.e. other
disease outbreaks in crop and livestock mono- functional roles), then it is likely that greater
cultures provide evidence that monocultures can diversity would be required.
have extremely high rates of disease transmission
(reviewed in Keesing et al. 2006). But for certain
15.6 Natural versus random sequences
disease systems, one might expect low diversity to
of community assembly or disassembly
be beneficial. For example, in the Lyme disease
system in eastern North America, a small number A common approach to assessing the consequences
of small mammals – white-footed mice, eastern of variation in biodiversity for ecosystem function-
chipmunks, short-tailed shrews, and masked ing is to assemble ecological communities by
 BIODIVERSITY AND ECOSYSTEM FUNCTION: PERSPECTIVES ON DISEASE 213

drawing species at random from a species pool and or in sequences suggested by natural disassembly
correlate functioning with species richness. A less rules. The roles of each species in contributing to
common approach is to remove species from intact Lyme disease risk had been empirically parameter-
communities, which is more appropriate in mim- ized (LoGiudice et al. 2003), allowing the aggregate
icking local extinction, but is far less tractable contribution of each community to be estimated.
(Symstad et al. 2001, Diaz et al. 2003). The main Random selection of species for removal resulted in
purpose of such experimental designs is to specifi- a strong, positive correlation between species
cally assess the importance of species diversity per se, diversity and disease risk. This result occurred
while avoiding the potential for species diversity, because one species – the white-footed mouse – has
species composition, and other factors to co-vary. Of a particularly large positive impact on Lyme disease
course, such experiments can also focus on func- risk, and more diverse communities had a higher
tional diversity or both, and often the two are cor- probability of including white-footed mice. But
related (Naeem 2002). Natural communities, when communities were disassembled under rules
however, appear not to be assembled or dis- with some empirical support, the opposite pattern
assembled randomly (Zavaleta and Hulvey 2004, was obtained – lower diversity caused increased
Bracken et al. 2008). More commonly, some species disease risk. This result occurred because white-
are widespread and highly resilient to disturbances, footed mice exist in all communities irrespective
while others are more restricted in occurrence and of diversity (LoGiudice et al. 2008, Nupp and Swi-
sensitive to disturbances. As a consequence, some hart 1996), and so less diverse communities had
species will tend to occur in most or all communities mice but few other hosts capable of diluting the
from rich to poor, whereas others will tend to exist impact of mice (Ostfeld and LoGiudice 2003).
only in species-rich communities. Studies in which A key question in understanding the effects of
species are added or removed in random order biodiversity loss on disease dynamics, or any other
cannot provide insight into the importance of natu- ecosystem function, is whether commonness, ubi-
ral sequences of species addition (community quity, or resilience are correlated with the perfor-
assembly) or loss (community disassembly) (e.g. mance of the function of interest. For disease
Fukami and Morin 2002). Moreover, given that systems, if dilution hosts tend to be common and
many directly transmitted diseases exhibit density- resilient and reservoir hosts rare and sensitive, then
dependent transmission, the nature of the method- decreases in diversity will reduce disease risk
ologies commonly used to assemble experimental because species-poor communities will be charac-
diversity treatments is likely to confound simple terized by many dilution hosts and few reservoirs.
richness effects. Additive designs, which maintain However, if reservoir hosts are common and resil-
similar abundance of individual species in single ient and dilution hosts tend to occur only in more
and multiple species assemblages, act to increase species-rich communities, then decreases in diver-
overall density as richness increases, whereas sub- sity will strongly increase disease risk. These cor-
stitutive designs, which maintain the same overall relations have not been adequately addressed in
abundance in single and mixed assemblages, act to zoonotic disease systems, although it appears that
reduce density of individual species as richness common and ubiquitous species tend to be the most
increases. However, it is important to note that competent reservoirs for zoonotic pathogens
sequences of species assembly or disassembly are (Ostfeld and Keesing 2000b). Potential evolutionary
often unpredictable. For example, extinction debt explanations for the correlation between ubiquity
theory argues that dominant species are sometimes and high reservoir competence have not yet been
highly sensitive to forces of extinction. Tests of the- explored. Two possibilities are that: (1) pathogens
ory will require approaches where communities are that are likely to experience a broad range of hosts
assembled in both random and orderly fashions. (e.g. because they are transmitted by a generalist
In a recent study, Ostfeld and LoGiudice (2003) vector) might tend to specialize on hosts they are
used a simulation model to disassemble virtual likely to encounter frequently; and (2) hosts whose
vertebrate communities either in random sequence life history traits promote commonness and
214 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

resilience (e.g. rapid reproductive rate and short life bacterial symbionts within the aphids (Scarborough
span) might tend to tolerate infections (Jolles, et al. 2005). How the symbionts differ between
Keesing, and Ostfeld, in litt.). clones and how function is affected by environ-
ment is not clear, but the example illustrates the
potential for considerable complexity in diversity–
15.7 Other levels of biodiversity
function relationships, even with just one host–
Researchers assessing relationships between biodi- pathogen combination.
versity and ecosystem functioning tend to focus on Biodiversity can also be a factor within hosts.
species diversity (and especially species richness), Recent studies have shown the potential impor-
but biodiversity at other levels – genotypic, habitat tance of host coinfection with multiple disease
type, landscape – can also potentially affect eco- agents. These mixed infections are common and
system functioning. These levels of diversity are have the potential to dramatically alter population
only beginning to be studied in disease systems. dynamics and evolution of a particular disease
Zhu et al. (2000) found that the incidence and agent (Cox 2001).
severity of rice blast (a fungal pathogen) was con- At the other end of the biodiversity spectrum,
siderably lower in agricultural fields with higher Vittor et al. (2006) found that decreases in tropical
diversity of rice cultivars. Dennehy et al. (2007) forest structural diversity that accompany defores-
found that two natural mutants of Pseudomonas tation strongly increase abundance and human-
bacteria were able to reduce prevalence of infection biting rates of the mosquito Anopheles darlingi,
with bacteriophages compared with monocultures which is the primary vector of malaria in tropical
of the wild type. Neither mutant genotype was a America. Similarly, increases in yellow fever
viable host for the phage, and genotypic poly- (Brown 1977), leishmaniasis (Sutherst 1993), and
cultures strongly diluted phage infection, some- Ebola virus (Walsh et al. 2003) have all been linked
times to extinction. to gross changes in habitat diversity and accom-
Diversity at the genotypic level may also influ- panying human encroachment on tropical forests
ence disease ecology. For example, Pulkkinen increasing contact with key disease organisms and/
(2007) determined that the presence of > 1 geno- or vectors. The exact nature of the diversity changes
type of Daphnia magna strongly reduced infection most potent in affecting disease transmission in
prevalence of a focal genotype with a parasitic these systems remains to be determined.
microsporidian, Glugoides intestinalis. Another
example is that of aphids and their fungal patho-
15.8 Looking forward
gens. Studies on susceptibility of pea aphids to a
fungal pathogen have indicated significant genetic Ecologists have developed strong empirical and
(between-clone) variability in fungal resistance theoretical foundations for understanding the rela-
(Ferrari et al. 2001). This suggests that a community tionship between biodiversity and ecosystem func-
with low genetic diversity comprising just the most tioning. Key issues include the shape of the
resistant clone would result in the greatest reduc- relationships between biodiversity and specific eco-
tion in disease risk. However, follow-up studies system functions, the mechanisms underlying these
revealed significant Genotype · Environment relationships (e.g. the importance of species diversity
interactions such that resistance ranking of individ- per se versus species composition, functional traits),
ual clones changed with temperature (Blanford et al. and how different patterns of community assembly
2003; Stacey et al. 2003). In this case, resistance under affect functioning. Debates about these issues pro-
just one set of environmental conditions could be vide important insights for advancing our under-
achieved with low genetic diversity, but to maintain standing of the effects of biodiversity on infectious
resistance under environmental variation would diseases.
require multiple clones. Further studies have now Considerable evidence is accumulating that bio-
suggested that resistance to fungus is at least partly diversity can strongly reduce disease transmission
conferred by the presence of certain secondary and risk (Dobson 2005, Rudolf and Antonovics
 BIODIVERSITY AND ECOSYSTEM FUNCTION: PERSPECTIVES ON DISEASE 215

2005, Keesing et al. 2006, Dobson et al. 2006, Begon Risk = hazard × likelihood
2008, Molyneux et al. 2008). However, as we
describe above, the issues of shape, mechanisms,
and assembly patterns are only beginning to be
High risk
addressed. Although we have limited our discus-

ss
sion to the effects of biodiversity on disease risk, we

ity lo
should also point out that diseases can strongly

ivers
Hazard
influence biodiversity.

Biod
Diseases play a fundamental (but largely unap-
preciated) role in shaping communities and medi-
ating interactions between and across trophic factors
onomic
levels. We cannot hope to fully understand the Socio-ec
consequences of biodiversity change for almost any
function without increasing our understanding of
Likelihood
the role of disease organisms in community-level
processes. Diseases can play important roles in Figure 15.1 Conceptual model defining risk of an emerging infectious
natural regulation of pests and pathogens, provide disease or disease spillover. Risk is the product of ‘hazard · likelihood’.
new tools controlling them (e.g. Thomas and Read Ecological changes such as loss of biodiversity can affect the prevalence of
2007), and can strongly influence the extent to a pathogen or parasite increasing disease hazard. However, transmission of
the disease into a new population of hosts depends on frequency of
which exotic plants and animals become damaging
exposure. For spillover of a zoonotic disease into a human population,
invaders in the introduced environment (Torchin likelihood of exposure is strongly determined by socio-economic factors.
et al. 2003; Mitchell and Power 2003).
Understanding the full relationship between
biodiversity and disease risk will require explora- Another research frontier is determining whe-
tion of both ecological and socio-economic factors ther increases in vertebrate species diversity might
(Fig. 15.1). Such exploration is particularly impor- increase the total burden of zoonotic disease. This
tant in understanding the relationship between might be expected if more vertebrate species sim-
biodiversity and disease emergence (as opposed to ply add more zoonotic pathogens capable of
tranmission dynamics of extant diseases). Risk is infecting humans. Thus, even if risk of any par-
defined as the product of ‘hazard · likelihood’. For ticular disease declines with increasing vertebrate
emerging diseases, which are often accompanied by diversity, the total risk from all zoonotic patho-
‘spillover’ from a few principal host to secondary gens might increase. Although such a relationship
hosts, we suggest that ‘hazard’ might be repre- might exist, the evidence to support it is weak to
sented by the prevalence of a particular pathogen non-existent. Interestingly, Jones et al. (2008) found
and ‘likelihood’ represented by the probability or that greater numbers of infectious diseases of
frequency of exposure to the pathogen. We further humans have emerged in the temperate zone,
suggest that ecological change, such as loss of bio- where vertebrate diversity is lower, than in the
diversity or change in host species composition, is tropics, where vertebrate diversity is higher.
likely to have the greatest influence on the nature Although a detection bias partially accounts for
and magnitude of the hazard. On the other hand, this pattern, a simple correlation between verte-
many socio-economic factors (such as urban brate diversity and numbers of emerging diseases
encroachment, land-use change, hunting, travel, does not appear to exist.
and trade) broadly determine the chances of expo- Finally, one of the most important areas of bio-
sure, given a particular hazard. If we are to diversity-ecosystem function research involves
understand and manage disease risk, we need making it relevant to real-world problems, a main
improved understanding of not just the ecology of focus of this volume. As noted earlier, ecosystem
infectious diseases, but also the social and economic functions like net primary productivity, nitrogen
contexts. mineralization, and trace gas efflux do not
216 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

resonate with the public at large; nor do they to structural, and a variety of mechanisms are at
readily translate into ecosystem services. Diseases, play. In a world where both biodiversity is
however, matter tremendously to humans, are changing dramatically and diseases are emerging
well studied, and the economic costs and con- and resurging, understanding the role of biodiver-
sequences of disease are well known. The role of sity in the ecology of diseases is arguably one of the
biodiversity appears to matter in virtually all its most important areas in biodiversity-ecosystem
levels, from genotypic to population to community function research.
 CHAPTER 16

Opening communities to colonization –

the impacts of invaders on biodiversity
and ecosystem functioning
Katharina Engelhardt, Amy Symstad, Anne-Helene
Prieur-Richard, Matthew Thomas, and Daniel E. Bunker

16.1 Introduction community and ecosystem-level impacts. However,

whereas biodiversity-ecosystem functioning research
Biodiversity is becoming increasingly homogenized
has generally not allowed immigration from a
as dispersal barriers are broken down (McKinney
regional species pool (but see Chapter 10), invasion
2004) and as species respond to global warming
ecology inherently focuses on open communities.
through range shifts (Moen et al. 2004, Thuiller et al.
Biodiversity-ecosystem functioning research focuses
2006b). Such homogenization is leading to a net
on the relationship and feedbacks between biodi-
decrease in global biodiversity (Sax and Gaines
versity and ecosystem functioning; invasion ecology
2003) with alarming consequences for the world’s
generally focuses on one or the other. Both fields are
life support systems. Locally, however, addition of
therefore ripe for cross-fertilization.
species through natural and anthropogenic causes
In this chapter, we explore the consequences of
can result in idiosyncratic, unpredictable, and
opening communities to colonization and the new
sometimes latent changes in biodiversity. As found
establishment of one or more species that strongly
by studies reviewed throughout this volume and
interact with resident species and the environment.
elsewhere (e.g. Hooper et al. 2005), changes in bio-
We focus on the factors that determine the coloniza-
diversity may translate into measurable changes in
tion, establishment, and impact of novel species on
ecosystem processes and the delivery of services to
community properties and ecosystem functioning.
human societies. Thus, the addition of novel species
We then use a risk analysis based on a bioeconomic
can have impacts on the processing of energy and
framework to illustrate approaches to invasive spe-
matter in ecosystems, either directly or indirectly,
cies management that would be appropriate for dif-
by affecting biodiversity.
ferent types of species. Most of our examples involve
Given the growing number of species additions to
terrestrial plant communities, as these are the most
ecosystems worldwide, we would like to know
commonly studied systems in the invasion ecology
whether it is possible to assess the risk of a large and
literature (Bruno et al. 2005), but we also draw from
potentially cascading and irreversible impact of a
other trophic levels and systems. To avoid confusion
novel species on biodiversity and ecosystem func-
in terminology regarding colonizers versus inva-
tioning so that the riskiest species can be targeted for
ders, we follow the nomenclature of Davis and
management. This requires linking two burgeoning
Thompson (2000; Box 16.1). Although our focus in
fields in ecology: invasion ecology and biodiversity-
this chapter is on the community and ecosystem-
ecosystem functioning research. Both fields are con-
level impacts of the colonist, a large body of litera-
cerned with the loss of species, changes to ecosystem
ture exists on the invasibility of the receiving
functioning, and measuring species traits to predict
community (Box 16.2).

217
218 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Box 16.1 Terminology

Inconsistent and imprecise use of terms referring to species Regardless of the dispersal type or impact on the new
entering a community confuses the science of invasion environment, all colonizers common to the region are
ecology. To avoid this problem, we adhere to the considered successional colonizers. Species with low
terminology recommended by Davis and Thompson (2000), impacts on the new environment that are novel to the
who emphasized dispersal rate of a colonizing species, its region are novel, noninvasive colonizers regardless of the
uniqueness to the region, and its impact on its new rate at which they disperse. These species comprise the
environment. bulk of exotic or non-native (terms we use interchangeably
In this scheme, colonizing species are split into eight with ‘novel’) species, since most species reaching a new
categories based on dispersal type (‘diffusion’ between environment fail to establish, and most of those that
adjacent or nearly adjacent environments or ‘saltation’ establish do not become pests (Williamson and Fitter
between widely distant environments), uniqueness to the 1996). Finally, only those species that are novel to the
region (‘common’ to the region or ‘novel’) and impact on region and have a large impact on the new environment,
the environment (‘low’ or ‘high’). Davis and Thompson whether they disperse via diffusion or saltation, are novel,
(2000) then lump these eight categories into three classes. invasive colonizers, or true invaders.

Box 16.2 The receiving end

Establishment success of a potential invader is not only exotic diversity (e.g. Levine 2000). The resolution of this
influenced by the traits of that species but also by the discrepancy comes largely from considering the scale at which
environmental characteristics of a site. Thorough reviews of the relationship is considered. Since competition for resources
the factors that influence a community’s invasibility are occurs between neighbouring individuals, it would be
published elsewhere (Lodge 1993; Levine and D’Antonio expected, and has been confirmed by some studies, that the
1999; Richardson and Pysek 2006; Fridley et al. 2007). relationship between native and exotic species would switch
Here, we briefly highlight three of these factors particularly from negative at the neighbourhood (0.1–1 m2) scale to
relevant to the focus of this chapter: diversity of positive at larger scales (Brown and Peet 2003).
competitors at a site, the presence of enemies, and the It must be recognized, however, that competition is not
disturbance regime. the only interaction that controls establishment success. Plant
Diversity of competitors: A generation of ecologists grew community diversity has been observed to modify the
up with the idea that diversity confers resistance to invasion composition of invertebrate herbivore communities (Koricheva
through greater competition for resources: more species ¼ et al. 2000, Symstad et al. 2000) and this may influence the
more resources being exploited, therefore fewer resources establishment success of a colonizing species (Prieur-Richard
available for a new species (Elton 1958). This idea remained et al. 2002). Also, previous invasive species may facilitate the
largely untested until the advent of biodiversity-ecosystem establishment of other species (Hacker and Dethier 2006,
functioning research in the early 1990s. Although the Kondo and Tsuyuzaki 1999) by modifying environmental
standard practice in biodiversity-ecosystem functioning conditions such as soil biotic community, pH, nutrients,
experiments is to prevent unplanned species from entering oxygenation of water or sediments, thus rendering the
the experimental units, when this practice has been relaxed, habitat more hospitable to colonizing species.
the diversity–invasibility hypothesis has largely been Enemy release: One essential advantage for species
confirmed. In fact, the relationship between diversity and colonizing a new region is the absence of some or all of the
invasibility is one the most consistent effects across enemies that attacked them in their home range (Lodge
experiments (Balvanera et al. 2006). However, results have 1993). This, of course, is the basis for biological control –
been contested by the fact that in surveys of natural and the introduction of host-specific enemies (e.g. herbivores,
semi-natural communities, exotic richness is often positively pathogens, parasites) from an invasive species’ region of
correlated with native richness, suggesting that conditions origin (Butler et al. 2006, Simberloff and Stiling 1996). The
conducive to high native diversity are also conducive to high role of natural enemies that are native to the invaded
 OPENING COMMUNITIES TO COLONIZATION 219

community in the establishment success of novel species is enter an undisturbed community. A wide range of
unclear, although examples do exist that illustrate the disturbance types have been shown to facilitate invasions:
control of exotic species by parasites or herbivores native to soil disturbance (e.g. Kotanen 1997, Burke and Grime
the receiving community (e.g. Soldaat and Auge 1998). 1996); nutrient enrichment (e.g. Burke and Grime 1996);
Disturbances: Disturbances have unanimously been modifications of fire regimes (e.g. D’Antonio and Vitousek
shown to favour plant invasions (Hobbs and Huenneke 1992); and grazing by non-native herbivores (McIntyre and
1992). Disturbances simultaneously increase resource Lavorel 1994, Landsberg et al. 1999). Interaction between
availability and decrease competition from resident species, several disturbance types frequently leads to the highest
allowing establishment of species that would not be able to rates of invasion (Hobbs and Huenneke 1992).

16.2 The relationship between metries are common in communities and species
biodiversity and ecosystem functioning partition resources through tradeoffs), they operate
simultaneously in most systems. Quantifying the
Biodiversity effects on ecosystem functioning are
contribution of each mechanism to a biodiversity
common, although the magnitude and direction of
effect can be challenging and has received consider-
effects can vary across ecosystems, trophic levels,
able attention in recent years (see Chapter 7).
response variables, experimental designs (see
Communities are not static, however, and the
Chapter 2), and, as we discuss in this chapter,
relative importance of these opposing community-
communities that are relatively open or closed to
structuring mechanisms may change as species
immigration from regional or global species pools.
immigrate, go locally extinct, and change in abun-
Mechanisms that explain the relationship between
dance. Hence the relationship between biodiversity
biodiversity and ecosystem functioning can be
and ecosystem functioning may shift between sam-
placed into two main categories that differ funda-
pling and complementarity effects depending on the
mentally in how species interact. The sampling effect
age of the community, the strength of interspecific
(or selection or dominance effect; see Chapter 7)
interactions, species presence, and the per capita con-
occurs when greater diversity increases the proba-
tribution of each individual within a community to
bility that a highly competitive species is present
ecosystem processes. Some biodiversity-ecosystem
and gains dominance in a community. Such species
functioning (BEF) studies report that the effects of
typically use more resources and produce more
biodiversity on ecosystem functioning grow increas-
biomass than the average species and are therefore
ingly positive through time (Tilman et al. 2001, Jonsson
associated with higher levels of ecosystem func-
2006, Fargione et al. 2007). In nitrogen-limited grass-
tioning (e.g. higher productivity and higher
land systems, for example, this effect is explained by a
resource use). An inverse sampling effect (Loreau
shift from the selection effect to the complementarity
2000, Engelhardt and Ritchie 2002, Jiang et al. 2008)
effect. In this case, complementarity in resource use
is a special case when the competitively dominant
increased the input and retention of nitrogen through
species does not have the greatest effects on eco-
time (Fargione et al. 2007). However, others have
system functioning, as can be the case when
found that the effect of biodiversity on ecosystem
resource depletion is not the primary means for
functioning grows weaker over time (Bell et al. 2005b),
interspecific competition. In contrast, the comple-
especially in systems where facilitative interactions
mentarity effect (or niche differentiation effect; see
early in the development of the community are
Chapter 7) arises from resource partitioning among
replaced by competitive interactions (Cardinale and
species. In this case, species-rich communities use
Palmer 2002). Still others report that a positive BEF
more resources and are more productive than species-
relationship is only transient (Hooper and Dukes 2004,
poor communities, up to a saturating point (Cardinale
Fox 2004a), possibly because interference competition
et al. 2006a), because species are using resources dif-
allows monocultures to outperform polycultures in
ferently. Since both mechanisms are necessary for the
the long term (Fox 2004a).
maintenance of biodiversity (i.e. competitive asym-
220 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

While instructive in understanding how the BEF Among plants and invertebrates, wind, water, and
relationship changes through time as constructed vertebrate dispersal modes, as well as small seed or
ecosystems mature, these long-term studies of closed body size and high propagule output, are associ-
communities do not address how the BEF relation- ated with dispersal ability (Fenner and Thompson
ship changes during succession and/or invasion, 2005). For birds and mammals, large body size and
which are processes that are inherent to open com- carnivorous diet type allow organisms to disperse
munities that allow immigration. Specifically, what long distances (Sutherland et al. 2000, Jenkins et al.
happens to the BEF relationship when new species 2007).
are allowed to immigrate? If some species traits confer greater dispersal
ability and allow a species to reach new locations,
are they effective predictors of the invasiveness of
16.3 Impacts of colonizing species on
a species? For plants, for which the greatest body
the biodiversity-ecosystem functioning
of literature is available, traits associated with
relationship
dispersal are indeed generally related to inva-
Immigration and extinction processes, which are a siveness. Broad, comparative studies associate
function of biogeographic, environmental, and high fecundity (including production of many
biotic constraints (Naeem and Wright 2003), offspring, short juvenile periods, and/or long
strongly determine the structure and composition flowering seasons), small propagule size, and
of all biological communities. A species will be long-distance dispersal capability with high
absent from a community if it cannot disperse to a abundance or broad distribution of invasive plants
site, survive in the new abiotic environment, and (Richardson and Rejmánek 2004, Hamilton et al.
successfully reproduce in the presence of the resi- 2005). For example, alien woody species with fle-
dent biota. Understanding the potential impact of shy fruits (which can be carried great distances by
a colonizing species on local biodiversity and their avian dispersers) expanded their ranges to a
ecosystem functioning will therefore depend on greater extent in New York City during the 20th
four factors. These are (1) the species’ likelihood of century than species with other fruit types (Aron-
colonizing a new area, (2) the species’ likelihood son et al. 2007). Having two modes of dispersal (e.
of establishing a viable population and increasing g. sinking seeds and floating vegetative fragments
in abundance, (3) the response of resident com- in Mimulus guttatus on rivers of northern Europe;
munities to the species’ presence, and (4) the Truscott et al. 2006) or high plasticity in seed mass
functional traits of the colonizing and resident (e.g. Ambrosia artemisiifolia along European rivers;
species that determine biodiversity’s effect on Fumanal et al. 2007) are other dispersal-related
ecosystem processes. Functional traits (see Chapter traits attributed to invasive plant species. For
4) are quantifiable biological properties of species vertebrates, in contrast, body size and diet type are
that affect how species respond to the biotic and less important in predicting an invasive species’
abiotic environment through changes in the dis- likelihood of reaching a new location than whether
tribution and abundance of organisms (‘response or not humans hunt it for sport – game species are
trait’) and that affect ecosystem processes (‘effect brought across oceans and continents more fre-
trait’; Lavorel and Garnier 2002, Naeem and quently than are non-game species (Jeschke and
Wright 2003, Engelhardt 2006). Strayer 2006).
For our purposes, the question is whether the
traits that increase the likelihood of a species
16.3.1 The likelihood of colonization
reaching a new location are those that are likely
The likelihood that a species will enter a new to affect biodiversity, ecosystem functioning,
location is a function of the species’ current range and the strength of the relationship between and
with respect to that location, characteristics of the biodiversity ecosystem functioning. In the absence
landscape surrounding that location, and the of human-mediated dispersal, the answer at this
organism’s dispersal ability within that landscape. time appears to be ‘no’: in plants, studies
 OPENING COMMUNITIES TO COLONIZATION 221

specifically addressing this question have generally output (Kolar and Lodge 2001), fast growth rate
shown that no consistent relationship emerges (Newsome and Noble 1986), and high adaptability
between the traits of the seed stage, which is (genetic variation in fitness traits or phenotypic plas-
responsible for most dispersal, and the traits of ticity; Poulin et al. 2007) appearing consistently across
the mature stage (Westoby 1998, Lavorel and a wide range of species. Novel weapons (Abhilasha
Garnier 2002), in which effects on ecosystem et al. 2008, Bais et al. 2003, Callaway and Ridenour
functioning are greatest. Many more empirical 2004, Callaway et al. 2008) and a release from enemies
tests of this relationship are needed to determine (Keane and Crawley 2002, Mitchell and Power 2003)
the robustness of this answer, however (Suding can also increase the chances of establishment by a
et al. 2008). novel species by conferring a competitive advantage
In contrast, species intentionally introduced and over native species. Most species that become estab-
cultivated by humans are sometimes chosen lished become part of the resident community with-
because they are robust in the new location and are out noticeable effects on diversity or ecosystem
useful to humans in some way; these character- functioning. Therefore, we ask again, which, if any, of
istics are related to successful establishment, these traits are most likely to cause a novel species to
spread, and effects on the new ecosystem (Alpert impact biodiversity, ecosystem functioning, and/or
2006) and therefore warrant special attention from the shape or strength of the relationship between
management and policy communities in deter- them?
mining the balance of their risks and benefits High propagule output and other traits associated
(Section 16.4). Other intentionally introduced spe- with juvenile stages are unlikely to have significant
cies are remarkably uninvasive. For example, effects for the same reasons that we discussed for
maize (Zea mays) survives in the Old World only dispersal traits above. Fast growth rate and high
because of intense care through the use of fertil- adaptability may be associated with biodiversity
izer, irrigation, and a variety of biocides. The case and/or ecosystem functioning changes under certain
of unintentional dispersal by humans is more circumstances, such as disturbed conditions, which
ambiguous. For example, freshwater zooplankton may result in an immediate or latent impact of the
disperse only slowly by natural means, but can invader on biodiversity or ecosystem functioning
drastically change ecosystem processes in new depending on when the disturbance happens during
unintended locations (Havel and Medley 2006). establishment. Competitive superiority, whether
Unintentionally introduced species are not con- caused by enemy release, novel weapons, or some
strained by a potential tradeoff between dispersal other mechanism, is more likely to have significant
ability and competitive ability. They may simply effects. In this case, only a one-for-one substitution
be in the right place at the right time, and whether within a functional group of a resident species by the
they affect resident diversity, functioning, or both novel species has no effect on biodiversity. A more
in their new location may depend on traits that likely outcome is a shift in species’ abundances,
allow them to become established and to spread. It which may include the complete elimination of one
is these species that represent the greatest uncer- or more species or a change in abundances among
tainty regarding their potential threats to ecosys- functional groups. In any of these cases, ecosystem
tems. Consequently, they should be the focus of functioning may be impacted through a direct or
investigations for traits that predict the impact of indirect sampling effect. For example, Argentine ants
colonizing species on biodiversity and ecosystem (Linepithema humile) invading sub-tropical and tem-
functioning. perate regions possess a different social structure
that allows the formation of fast-growing, high-
density ‘super colonies’ that deplete resources of an
16.3.2 The likelihood of establishment
area faster than native ants can (Holway 1999). A
Some species traits inherently confer a high likelihood direct effect of their resulting dominance may be
of establishment success (e.g. Rejmanek and changes in nutrient cycling due to differences in their
Richardson 1996, Daehler 1998), with high propagule nest construction from that of native ants (Holway
222 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

et al. 2002), whereas an indirect effect could act involves a reduction of native species abundance or
through their increased predation on other inverte- richness and/or a substantial change in ecosystem
brates that affect pollination or decomposition. functioning. However, most species that colonize
While sampling effects are common in BEF experi- and become established in new environments have
ments, their significance in nature is not known little or no impact (Williamson and Fitter 1996), and
(Cardinale et al. 2006a). Therefore, predicting novel others even have a positive effect on the resident
species’ effects on biodiversity, ecosystem function- community (Hacker and Dethier 2006, Kondo and
ing, or their relationship from traits that confer Tsuyuzaki 1999, Bruno et al. 2005). Determining the
competitive advantage is tenuous. traits of the species and the characteristics of the
On the other hand, some species become estab- corresponding receiving communities that lead to
lished not because of a specific trait that can be con- these different situations is a main goal of the sci-
sistently traced across many communities, but ence of invasion ecology, and it is equally impor-
because they use the environment in some novel way; tant for determining how a new species will affect
i.e. they are initially complementary. For example, the relationship between biodiversity and ecosys-
Clarke et al. (2005) showed that an invading grass can tem functioning.
take advantage of both summer and winter rains, in A crucial, often overlooked, step in determining
contrast to natives, which used rain in only one of the traits that cause large impacts is a quantitative
these seasons. Similarly, red brome (Bromus madri- demonstration that a suspected invasive species
tensis ssp. rubens) is an annual grass that can exploit actually does have an effect on the receiving com-
water and other soil resources for 2–3 months before munity. Perceptions of species’ impacts are often not
native perennials break dormancy in the Mojave substantiated by quantitative studies. For example,
Desert (DeFalco et al. 2007). We argue that traits that of 196 exotic species in the Chesapeake Bay region,
confer establishment success because of their com- 20 percent were thought to have a negative impact
plementarity (niche differences) will more consis- on a resident population, community, or process, but
tently affect ecosystem functioning and the BEF only 6 percent were actually documented to have a
relationship than will traits involved in a sampling negative impact (Ruiz et al. 1999). In addition, there
effect by conferring competitive advantage. This is are reports of species widely considered to be inva-
because complementarity implies a direct effect on sive actually having no impact on individual native
resource use, which is a key part of ecosystem func- species of concern (e.g. Menke and Muir 2004) or on
tioning (Vitousek 1990). Just how large these niche native richness or abundance (e.g. Treberg and
differences must be is a difficult question, however. Husband 1999). On the other hand, a novel species
The novel species needs to be similar enough to tol- may ameliorate limiting conditions and positively
erate local environmental conditions, and dis- affect native species. For example, a non-native larch
turbances can open space and release resources that species intensively planted on the lower slopes of a
allow species that do not differ from the residents to Japanese volcano after its eruption spread into
become established. The literature shows clearly that unplanted areas on the volcano, making some con-
exotic diversity patterns mirror native diversity, sider it invasive (Kondo and Tsuyuzaki 1999).
suggesting that novel species are tracking similar However, diversity and richness of native species
conditions and resources (Stark et al. 2006). On the during primary succession on the volcano was
other hand, if the novel species is too similar to the greater under this non-native tree than under a
resident species, its impact on biodiversity and eco- native tree (Titus and Tsuyuzaki 2003). In the US
system functioning will be negligible. Pacific Northwest, Spartina anglica, a marine grass
from the UK, facilitates the growth of native species
by quickly accreting sediment and creating more
16.3.3 The impact of a colonizer on resident
hospitable habitats for growth in unvegetated estu-
communities and ecosystem functioning
arine habitats, but decreases native species diversity
By definition (Box 16.1), an invader has a large in other habitats (Hacker and Dethier 2006). These
impact on the native ecosystem. This usually examples suggest that colonizers with positive
 OPENING COMMUNITIES TO COLONIZATION 223

impacts on residents often share traits with native 2006). A plant may impact dispersal of other plants
species that play a similar role in succession. by competing for pollinators or dispersers (Brown
Removal studies yield the strongest evidence for and Mitchell 2001), impeding dispersers (Traveset
negative impacts of novel species on native abun- and Richardson 2006), or augmenting populations
dance and richness (Levine et al. 2003). For exam- of generalist granivores (Ortega et al. 2004). For
ple, growth rates and recruitment of two shrubs these interactions to cause substantial negative
increased in response to the removal of three non- effects on the natives, however, these novel colo-
native grasses (D’Antonio et al. 1998). Hulme and nizers must somehow be more disruptive than the
Bremner (2006) observed a significant increase in a combined effect of all the other species already
and g diversity after the invasive riparian weed occurring in the community. Little information
Impatiens glandulifera was removed. In these studies exists as to the traits that would yield this effect, but
the role of competition is clear, but the traits that examples of such occurrences suggest that traits
drive this competition vary among situations. novel to the community, such as a carnivore in a
Gould and Gorchov (2000) found that survival and previously carnivore-free system, are those that will
fecundity of native annuals were greater when they have the largest impact.
were transplanted into forest plots without the Similarly, novel species that strongly affect eco-
invasive shrub Lonicera mackii than in plots where it system functioning also tend to do things differ-
was present. Although they did not investigate the ently than the residents (D’Antonio and Hobbie
specific traits responsible for interspecific competi- 2005). Vitousek (1990) described three ways that
tion, they suggested reduction of light availability novel species alter ecosystem functioning: by
early in the growing season due to the invader’s altering resource supply rates, by changing trophic
longer phenology as one possibility. Dyer and Rice structure, and by modifying disturbance regimes.
(1999) found that vegetative growth and repro- Plants that bring N2-fixing bacteria into naturally
ductive output of a native bunch grass were greater nitrogen-poor systems and thereby increase nutri-
when grown with conspecifics compared to when ent availability and cycling rates (Vitousek and
grown with exotic annual grasses at a variety of Walker 1989) are one of the classic examples of a
densities. In this case, the invasive species’ early trait that causes transformation by modifying
growth depleted shallow soil water resources and resource supply rates. Novel species can also
reduced light availability early in the growing sea- accumulate a resource (e.g. salt) to the point that
son, thereby suppressing the root growth that the concentrations are toxic to other species (Vivrette
native perennial required for acquiring deep soil and Muller 1977). Ponds created by North American
moisture later in the growing season. Other traits beavers in Chile increase retention of fine particulate
associated with competitive invasive species are organic matter in streams, leading to increased food
those that confer high resource capture ability and availability for, and therefore productivity of, stream
utilization efficiency (Feng et al. 2007), the ability to macroinvertebrates (Anderson and Rosemond 2007).
forage on low-quality resources (Gido and Franssen Novel fish that affect feeding behaviour of herbi-
2007), and the ability to alter soil biotic communi- vores alter the trophic structure of stream systems so
ties (Callaway et al. 2004). A recurring theme in that primary productivity increases and nitrogen
these traits is that they are somehow different from dynamics are altered (Simon et al. 2004). The fine,
those of the species in the receiving community quickly drying or highly flammable leaves of
(D’Antonio and Hobbie 2005). grasses, combined with their nearly continuous
Once established, a species may also negatively ground cover, allow novel grasses to carry fire
impact resident species by disrupting their repro- through woody ecosystems that previously burned
duction and dispersal. Animals may disrupt plant infrequently (D’Antonio and Vitousek 1992). This
dispersal through displacement of more effective, greater fire frequency, combined with the different
native pollinators; predation of pollinators or dis- structure of the novel and resident species, can shift
persers; or destruction (eating or trampling) of the ecosystem from being a carbon sink to a carbon
flowers, pollen, or seeds (Traveset and Richardson source (Bradley et al. 2006).
224 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Currently, predicting the magnitude and direction The traits of the species that substantially impact
of a species’ effects on biodiversity and ecosystem resident species or ecosystem processes vary con-
functioning is tenuous at best. Novel species with siderably with the situation. Nonetheless, the
traits similar to those of the resident species are less overarching theme is that the traits must differ
likely to have cascading effects on the ecosystem somewhat from those possessed by the species in
than novel species with different traits. Many the receiving community for novel species to
uncertainties remain, however. Myrica faya is a novel impact both biodiversity and ecosystem function-
functional type in Hawaii and has extensive effects ing. Because functional diversity is a critical com-
on biodiversity and ecosystem functioning (Vitousek ponent of the biodiversity-ecosystem functioning
and Walker 1989). In contrast, Acer platanoides has relationship (see Chapter 4; Petchey and Gaston
many similar traits compared to the resident Acer 2006; Wright et al. 2006), it is this difference
saccharum (Kloeppel and Abrams 1995); however, between the colonizer and the resident species that
the former can substantially reduce forest biodi- determines whether a new species will impact
versity in the northeastern United States whereas biodiversity and ecosystem functioning. The chal-
the latter does not (Webb et al. 2000). Acer plata- lenge is learning how large of a difference between
noides has a fertilizing effect of forest soils, which the colonizer and the resident species is required for
increases the growth of tree seedlings of four dif- the colonizer to have a significant effect on biodi-
ferent species (Gomez-Aparicio et al. 2008). Thus versity and ecosystem functioning.
the invasion of Acer platanoides may reduce forest The type of effect that the novel species has on
biodiversity but increase forest productivity. These the BEF relationship will depend on the species
uncertainties highlight the need to know whether interactions at play in the resident community and
and how current and future invaders will affect how the newcomer fits in. The diverse array of
the relationship between biodiversity and ecosys- interactions witnessed in BEF studies (e.g. facilita-
tem functioning. tion and competition) occur in experimental set-
tings where extinction could occur but colonization
of new species could not. Therefore it is to be
16.3.4 Tying it together: invaders’ effects
expected that the arrival of a new species could
on the BEF relationship
have equally diverse ramifications. When a colo-
We know that the breakdown of dispersal barriers nizer is common to the region (‘native’), this pro-
has allowed a degree of global biotic homogeniza- cess is referred to as succession. When the
tion. In most cases, species novel to an ecosystem colonizing species is new to the region and has not
will not gain dominance and will simply blend into coevolved with the resident species (‘non-native’ or
the saturating function of the complementarity ‘exotic’), this process is generally called invasion if
effect. These species join the community because the newcomer achieves dominance (Box 16.1). The
they have similar environmental tolerances to resi- processes are fundamentally the same: a single spe-
dent species; they displace few if any established cies can have a small or large impact on the resident
individuals because they are complementary or community or ecosystem functioning (Davis and
equally competitive; and they increase functioning Thompson 2000).
in a minor additive way, if at all. However, in some The lack of common evolutionary pressures
cases, novel species can have strong immediate or between an exotic species and a receiving commu-
latent effects on biodiversity and ecosystem func- nity makes it more likely that the new species will
tioning. Here, the novel species may change the have a novel set of traits that allows it to be a
shape and trajectory of the BEF relationship by ‘super-competitor’ that influences functioning
changing species richness, changing the point at through the sampling effect. The sampling effect is
which an ecosystem function saturates, and/or usually associated with a positive BEF relationship,
shifting the mechanism from complementarity to a but it can also create negative relationships when
sampling effect as the nature of species interactions the competitive dominant does not have the great-
shifts from resource partitioning to competition. est effect on functioning (the inverse sampling effect;
 OPENING COMMUNITIES TO COLONIZATION 225

Loreau 2000, Engelhardt and Ritchie 2001, Weis Invasion

et al. 2007, Jiang et al. 2008). We argue that the
chance of an inverse sampling effect is higher when Restoration Extinction
exotic species with novel sets of traits invade a
system because the exotic species are less likely to

Ecosystem process
follow the ‘rules’ that maintain biodiversity in the
receiving community. Thus, an exotic invader may
be a superior competitor but not be the most
effective processor and transformer of nutrients and
energy. Or, the exotic species might have a high
growth rate but be a poor competitor. Indeed, in an
experimental study that tested the effects of three
native and one exotic species on wetland ecosystem Species richness
functioning, Engelhardt and Ritchie (2001, 2002)
found that the exotic species was the most pro- Figure 16.1 The effects of extinction, restoration, and invasion on
ductive species that retained the most nutrients, but species richness that translate into effects on ecosystem processes given
linear, nonlinear, or idiosyncratic relationships between species richness on
it was a poor competitor. Hence ecosystem biomass
ecosystem processes. The filled circle depicts an intact system of resident
production and nutrient retention in mixed com- species, the open circle a degraded system. Depending on the traits of the
munities was lower than in the monoculture of the colonizing and resident species, invasion may increase, decrease, or not affect
exotic because interspecific competition led to the species richness, ecosystem processes, or the relationship between them.
dominance of a poor biomass producer.
There is still much to be done in order to reliably
predict the effects of individual species, no matter extinction, can be redesigned to incorporate the
what their origin, on ecosystem functioning. It is inevitable and non-random process of new coloniza-
clear, however, that understanding how the addi- tions, in the form of succession or invasion. This
tion of a species impacts ecosystem functioning will would probably entail long-term experimental stud-
require knowledge of species traits – those of the ies that would establish resident communities at a
new species and those of the resident species. This desired richness and then intentionally release one or
focus on traits will occur in a BEF framework that more potentially invasive species. Changes in biodi-
so far has focused on the consequences of extinction versity and ecosystem functioning would need to be
on ecosystem functioning in closed systems. This monitored through time using a design that accounts
framework is applicable to conservation biology for changes in covarying environmental factors.
and restoration science, which seek to understand B. The establishment of a new species is influenced
how species extinctions or community assembly, by biotic factors including the diversity of the
respectively, may impact ecosystem processes resident community and the presence of enemies
(Figure 16.1). Opening BEF theory and experiments (Box 16.2). It is also influenced by abiotic factors
to unplanned species colonization poses five real such as disturbances, which affect the resident
challenges that must be overcome to better under- community even in the absence of the new species
stand the effects of invasive species on biodiversity (Box 16.2). Thus, changes in a community’s diver-
and ecosystem functioning. These are: sity in the face of a new addition may not be caused
by the new species, but by abiotic conditions that
A. Biodiversity is both an independent and a drive changes in biodiversity and the successful
dependent variable when species are added to the establishment of the species. The challenge here is to
resident community through colonization, and spe- test the relative impact of the biotic and abiotic
cies are potentially deleted through competitive factors that drive changes in biodiversity of the
interactions with the colonizer. We need to know resident community. Again, a long-term experimen-
how BEF studies, which typically manipulate diver- tal approach may be required as well as long-term
sity as the independent variable and only allow monitoring of newly invaded systems.
226 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

C. Invaders can have a direct impact on ecosystem organisms create wealth, but measures to prevent
processes that can override or cancel the impacts of unintended movement of organisms have costs and
the resident community on ecosystem processes. there is potential for non-native species to cause
However, invaders can also have an indirect impact considerable economic and environmental harm.
on ecosystem processes by effecting change in the Bioeconomic theory and modelling incorporate
resident community. These direct and indirect current understanding of species’ impacts on bio-
effects of invaders need to be studied together to diversity and ecosystem functioning to quantify the
understand how the relationship between biodiver- impact of non-native species on ecosystem services.
sity and ecosystem functioning changes in commu- This is an essential step in developing effective
nities that are open to colonization. practices and policy for invasive species manage-
D. Many species that establish in a new location are ment. In this section, we take a brief look at how
not invasive and simply blend in to the saturating bioeconomic frameworks can be used to evaluate
function of the BEF relationship. These species may be the economic costs and benefits of various actions
‘time bombs’, however, that can have significant latent regarding non-native species; then we illustrate
effects on biodiversity and ecosystem functioning how BEF principles are incorporated into a strategy
when environmental conditions change. Similarly, for assessing the risk of economic impacts of non-
some species may be invasive as soon as they establish native species.
at a new location, but their impact decreases through
time. We need to know how frequent these latent
effects are and whether they can be predicted, 16.4.1 The use of bioeconomic frameworks
especially in the face of global climate change. Leung et al. (2002) presented a quantitative bioeco-
E. Finally, every species has a near endless number nomic modeling framework to analyze risks from
of traits. Thus it seems impossible to know whether non-native species to economic activity and the
a novel species will become invasive without environment. The model identifies the optimal allo-
knowing the traits of all species in a community cation of resources to prevention versus control,
and the traits of the colonizer. Little consensus exists acceptable invasion risks, and consequences of
about the functional traits of known invasive invasion to optimal investments (e.g. labour and
species and even less, if anything, is known about capital). When applied to invasive zebra mussels
the traits of those yet to come, raising the question (Dreissena polymorpha) in North America, the model
of whether the right traits have been measured. indicated that society could benefit by spending up
Instead of knowing all traits, which would be an to US$324,000 per year to prevent invasions into a
unrealistic proposition, it might be useful to single lake. By contrast, the US Fish and Wildlife
measure key functional traits that are reliable Service spent US$825,000 in 2001 alone to manage all
predictors of species’ impacts on biodiversity and aquatic invaders in all US lakes.
ecosystem functioning, and estimate the plasticity of A bioeconomic approach was also used by Cook
these traits. Species can vary broadly in their traits et al. (2007) to evaluate the economic benefit of
between their native and introduced range (Sie- biosecurity measures aimed at preventing the
mann and Rogers 2001), suggesting that under- arrival and establishment of the parasitic bee mite,
standing key traits and their plasticity under Varroa destructor, into Australia over the next
different abiotic and biotic conditions will be 30 years. Specifically, this study evaluated the
important to assess which species pose the greatest expected consequences of Varroa impact on feral bee
risk of changing the BEF relationship. populations and the flow-on effects in terms of loss
of pollination services for the horticulture industry.
The model estimated the benefits of exclusion to be
16.4 Invasions and ecosystem services:
between Aus$21.9 million and Aus$51.4 million per
assessing risk for better management
year, provided exclusion is maintained. The model
The globalization of international commerce pre- further revealed that existing cost-sharing arrange-
sents a policy challenge: sales and movement of live ments between government and industry do not
 OPENING COMMUNITIES TO COLONIZATION 227

accurately reflect the spread of potential benefits,

such as the substantial benefits derived by the hor-
ticulture industry from ‘free’ pollination services of

Magnitude of impact
Class 3 Class 4
feral bees when they are not impacted by the mite.
These studies are significant in demonstrating the
potential for ex-ante evaluations of the economic
impact of invasive species. Unfortunately, our
knowledge of key economic variables, such as the Class 1 Class 2
value of biodiversity and the societal discount rates
for environmental goods, is extremely limited and
currently makes evaluation of non-market effects Rate of impact
challenging. Identifying these gaps in our economic
Figure 16.2 Overall impact of an invasive species is determined by the
understanding highlights the need for interdisci-
magnitude of its impact (magnitude increases as species, communities,
plinary approaches in the development of improved ecosystems and ecosystem functioning are adversely affected, and/or as the
policy frameworks for biosecurity and invasive spatial and temporal extent increases) and rate at which this occurs (some
species management (Thomas and Reid 2007; species will spread slowly and/or take a long time to have an impact while
Wilson et al. 2007; and see Chapter 17). the impact of some invaders can be almost instantaneous). Species can be
classed according to these properties and used to inform biosecurity
strategy and control decisions.
16.4.2 Risk assessment
The bioeconomic examples above add weight to the Class 2' species have low impact but a more rapid
recent conclusion of Keller et al. (2007) that risk rate of impact, as might result from higher rates of
assessment and screening protocols to limit the spread and/or lower impact–abundance thresh-
introduction of damaging species can deliver positive olds. The higher a species is on the rate axis, the
net economic benefits. Determining how to conduct more important investment in biosecurity measures
an effective risk assessment and prioritize investment that prevent arrival and establishment (such as
in biosecurity measures is complex. Risk assessments trade or movement barriers, quarantine and
generally combine some measure of hazard with a inspection) will be compared to investment in
measure of likelihood to score risk. With an invasive management measures aimed at mitigating the
species, the threat or hazard is essentially determined problem after arrival – if impact is rapid then pre-
by the magnitude of its impact and the rate at which vention is better than cure. Nonetheless, with
this impact occurs. The magnitude of impact is nil to restricted impact magnitude class 2' species will still
little when it is restricted to a local scale. Impact assume fairly low priority compared with species
magnitude increases as species, communities, eco- with greater, community- or ecosystem-level
systems and ecosystem functioning are adversely impacts (classes 3 and 4). Of these, species whose
affected, and/or as the spatial and temporal extent of effects are rapid (class 4) represent the greatest
the impact increase. Similarly, some species will priorities for preventive biosecurity measures, since
spread slowly and/or take a long time to have an the implications of an incursion are severe (e.g. a
impact and, at the other extreme, the impact of some disease like foot and mouth, where a single case can
invaders can be almost instantaneous. impact a whole industry overnight). However, if
In Fig. 16.2 we combine impact and rate to create the rate of impact is slow (class 3), this could create
a matrix to inform biosecurity strategy and invest- options for investment not just in preventive mea-
ment priorities. In general, species populating the sures but also in mitigation measures aimed at
bottom left of the matrix (labelled class 1) might be longer-term control or eradication.
considered lowest threat since the rate and magni- This broad framework rests on an understanding
tude of impact is small. As such, they likely repre- of the traits we discussed in the first section: those
sent low priorities for biosecurity investment, as the that determine dispersal and establishment influence
costs might be expected to outweigh the benefits. the rate of impact, whereas those that determine
228 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

(a) (b)

Services or functioning
’
er
Biodiversity riv
‘D

‘Passenger’

Pre-control of Post-control Control of invasive

invasive control of invasive

Figure 16.3 Benefit from control of an invasive species depends on the causal relationship between invasive species abundance and biodiversity. (a) If
the invader is a ‘driver’ of biodiversity loss then decline in biodiversity will coincide with establishment of the species (indicated by the solid arrow) and
subsequent control of the invasive will deliver a biodiversity benefit (example given for a linear impact function). If, on the other hand, the invader
is a ‘passenger’ and biodiversity loss is due to some other environmental factor, then its arrival need not coincide with initial loss of diversity (indicated by
the broken arrow which appears slightly after biodiversity has begun to fall) and even complete control may fail to deliver a biodiversity benefit.
(b) Furthermore, even if there is a biodiversity benefit, the return of associated ecosystem services and function can be complex. Function can return
at a higher rate than biodiversity (upper line), at a slower rate (lower line), or can exhibit an idiosyncratic pattern (middle line) depending on the order and
rate at which functionally significant elements of biodiversity assemble.

how a species affects the receiving community and biodiversity will not necessarily result in restoration
its ecosystem processes govern the magnitude of of function (Thomas and Reid 2007; Fig. 16.3(b)).
impact. Equally critical for determining the benefit of Such factors identify a clear need for understanding
various actions, however, is the extent to which the impacts of non-native and potentially invasive
invasive species are a direct cause of biodiversity species (and their control) from a BEF perspective.
decline or whether they are simply responding to
other forms of ecosystem change (Gurevitch and
Padilla 2004). Whether an invasive species is a 16.5 Conclusions
‘driver’ of biodiversity change or a ‘passenger’
Like BEF science, invasion biology has become its
(MacDougall and Turkington 2005) has important
own branch of ecology. As we have shown here, the
implications for whether control of an invasive spe-
two branches are linked through their search for
cies is expected to increase biodiversity (Thomas and
traits that determine the mechanisms by which
Reid 2007; Fig. 16.3(a)). Moreover, even if an inva-
species impact communities and ecosystems. Much
sive species is the cause of initial biodiversity loss, it
still needs to be learned about how the traits can be
need not necessarily follow that management of the
used to forecast how novel species introduced to a
invader will result in biodiversity recovery (Thomas
new location will affect the relationship between
and Reid 2007) because of dispersal limitation or
biodiversity and ecosystem functioning. We offer
local extirpation (Laughlin 2003) or because of last-
the following conclusions as hypotheses that we
ing biotic (e.g. altered soil fauna and flora) or abiotic
hope will stimulate further research into the lin-
(e.g. altered stream flow) effects from the invader.
kages between biodiversity and ecosystem func-
Finally, even if structurally similar communities do
tioning in open communities.
re-establish, the order of species assembly can have a
marked impact on the pattern and rate of functional 1) Traits that allow species to be good colonizers are
recovery (Wilby and Thomas 2002; Kremen 2005; poor predictors of species impacts on ecosystem
Hooper et al. 2005). If functionally significant species functioning because traits at the juvenile stage are
respond quickly to removal of the invader, then poorly related to traits at the mature stage when
ecosystem services can recover at a more rapid rate impacts on ecosystem processes are most likely to
than biodiversity overall (Thomas and Reid 2007; occur. Good colonizers are often poor competitors.
Fig. 16.3(b)). On the other hand, if functional species Thus, good colonizers would be species with limited
respond slowly, then even substantial recovery in effects on biodiversity and ecosystem functioning
 OPENING COMMUNITIES TO COLONIZATION 229

and blend into the saturating function of the To forecast the impact of invasive species on BEF
biodiversity-ecosystem functioning relationship. and to evaluate risk of invasion, we need to know
2) Intentionally or unintentionally introduced spe- which species are most likely to cause cascading effects
cies do not need to be good dispersers to get to a new on biodiversity and ecosystem functioning. Much of
location. Thus, exotic species do not necessarily play this will rely on understanding similarities and dis-
by the rules, and therefore have the greatest potential similarities in species traits. This is a major task, but an
to affect biodiversity and ecosystem functioning. important one if we want to preserve biodiversity and
Two types of species with potentially large impacts ecosystem functioning within a changing world,
are (a) those that directly impact ecosystem processes where the introduction of novel species is an inevitable
by occupying a new niche and changing environ- consequence of global trade and human travel.
mental conditions to precipitate cascading effects on
biodiversity, and (b) those that establish dominance
Acknowledgments
by gaining a competitive advantage and affecting
ecosystem processes through effect traits that differ We thank the NSF-supported BioMERGE Research
from resident species. Coordination Network and the DIVERSITAS eco-
3) The magnitude and direction of a biodiversity SERVICES Core Project for supporting the workshop
effect on ecosystem functioning differs between ‘The consequences of changing biodiversity – solutions
open and closed systems. The relationship in closed and scenarios’ (30 November–5 December 2006,
systems becomes stronger with time and switches Ascona, Switzerland) and the workshop organizers for
from a sampling to a complementarity effect. The giving us the opportunity to participate in this volume.
relationship in open systems is less strong and will We also thank Shahid Naeem, Diane Larson, Qinfeng
be dominated by a sampling effect as an invasive Guo, and two anonymous reviewers for their
species, by definition, drives community abundance thoughtful feedback that substantially improved this
and/or ecosystem processes. chapter.
 CHAPTER 17

The economics of biodiversity

and ecosystem services
Charles Perrings, Stefan Baumgärtner, William A. Brock, Kanchan
Chopra, Marc Conte, Christopher Costello, Anantha Duraiappah,
Ann P. Kinzig, Unai Pascual, Stephen Polasky, John Tschirhart, and
Anastasios Xepapadeas

17.1 Introduction in this sense, differs from the economic problem of

individual biological resources. The question is not
The irreversible loss of genetic information (and the
at what rate to extract a particular resource, but
resulting loss of both evolutionary and technologi-
how to balance the mix of species to assure a flow
cal options) caused by the extinction of species
of benefits over a range of possible conditions.
involves a global public good, the gene pool.
Biodiversity conservation is frequently a public
Although important, it is not the only reason to be
good. In many cases, nobody can be excluded from
concerned about biodiversity change. As the Mil-
the benefits offered by the protection of assemblages,
lennium Ecosystem Assessment (2005b) points out,
and if one person benefits it does not reduce the
another reason for concern is the role of biodiver-
benefits to others. Because it is a public good, it will be
sity in the loss of ecosystem services. These also
‘undersupplied’ if left to the market. The incentive
involve public goods, but unlike the public good
that people have to free ride on the conservation
associated with species extinction, they are almost
activities of others means that people will collectively
always local or regional in extent. The conservation
conserve too little biodiversity. At the same time the
of species threatened with local extirpation protects
lack of markets for many of the biodiversity impacts
a number of provisioning and cultural services, as
of human activities mean that people are not con-
well as the capacity of the local system to function
fronted with the true cost of their decisions. Open
over a range of environmental and market condi-
access to scarce environmental resources is widely
tions. The latter may involve, for example, the
recognized to be a major cause of overexploitation.
regulation of specific biogeochemical cycles in dif-
Nowhere is this more clearly shown than in the
ferent climatic conditions, or the protection of crop
world’s fisheries. Worm et al. (2006) identified catches
yields in the face of an array of pests and patho-
from 1950 to 2003 within all 64 large marine ecosys-
gens. In almost all cases, however, conservation of
tems worldwide: the source of 83 per cent of global
the functionality of particular ecosystems provides
catches over the past 50 years. They reported that the
benefits to specific communities rather than to
rate of fisheries collapses in these areas (catches less
global society (Perrings and Gadgil 2003). Whether
than 10 per cent of the recorded maximum) has been
we focus on the gene pool or ecosystem services,
accelerating, and that 29 per cent of fished species
however, biodiversity – the composition and rela-
were in a state of collapse in 2003. Cumulative
tive abundance of species – is important because of
collapses affected 65 per cent of all species fished.
its role in supporting the capacity of the system to
While property rights are generally better developed
deliver services over a range of environmental
in terrestrial systems, many of the effects from
conditions. The economic problem of biodiversity,
anthropogenic land use change on biodiversity and

230
 THE ECONOMICS OF BIODIVERSITY AND ECOSYSTEM SERVICES 231

ecosystem services are also not reflected by markets. Thus, an ecosystem externality refers to the case
Since habitat loss through land use change is the where an individual’s economic activity generates a
greatest single source of biodiversity loss, this is a real change in ecosystem services that impacts the
major problem. Both the ‘public good nature’ of bio- wellbeing of others, but which is ignored by that
diversity conservation and the existence of biodiver- individual. This may be because the activity
sity externalities mean that private decision-makers involves the use of a public good (often a common
largely ignore the effect of their own behaviour on pool environmental resource) where there is scope
biodiversity, on ecosystem functioning, and, by and for free-riding, because of the incompleteness of
large, on the ecosystem services on which we all markets, or because of the system of governance.
depend. Where the change in ecosystem services is mediated
The economics of biodiversity and ecosystem ser- by a change in biodiversity, we refer to biodiversity
vices is largely about the failure of markets to signal externalities in ecosystem services.
the true cost of biodiversity change in terms of eco- For example, nitrogen oxides emitted from coal-
system services, the failure of governance systems to fired power plants and mobile sources are a serious
regulate access to the biodiversity embedded in air pollutant that can directly impact human health – a
‘common pool’ environmental assets, and the failure traditional externality. Urea, ammonia, or ammonium
of communities to invest in biodiversity conservation applied as fertilizer to agricultural lands contributes to
as an ecological ‘public good’. This chapter reviews nitrate pollution of ground and surface water. In bays
both the nature of the challenges posed by these fail- and estuaries, nitrate pollution is a serious problem
ures and the options for addressing them. It requires that causes algae blooms and reduces abundances of
that we are able to identify correctly both the private desirable food species. Nitrogen applied to land has a
and social decision problems, and hence that we are more direct effect on biodiversity. A twelve year study
able to value those non-marketed environmental of Minnesota grasslands (Tilman et al. 2001) showed
effects that are ignored in many private decisions. that added nitrogen decreased species diversity and
Chapters 18 and 19 address the issues associated with dramatically changed community composition. Spe-
the valuation and modelling, respectively, of the non- cies richness declined by 50 per cent and native bunch
market effects of private decisions on biological grasses were replaced by weedy European grasses. In
resources. In addition, however, it requires that we both cases there is an ecosystem externality. The pol-
are able to identify governance mechanisms, institu- lutant causes adaptations in the ecosystems affected,
tions, and instruments that will induce private deci- which in turn reduce the flow of ecosystem services in
sion-makers to behave in ways that are consistent the form of reduced fishing, grazing and recreational
with the social interest. This chapter focuses on the opportunities.
institutional and policy options for securing the The effect of biodiversity change on ecological
socially optimal mix of species, given the role of bio- functioning and the provision of ecosystem services
diversity in assuring ecosystem services over a range has been most convincingly demonstrated for
of environmental conditions. grasslands. In another set of Minnesota grasslands
experiments in which biodiversity was deliberately
varied across replicate plots, the capacity of the
17.2 Biodiversity externalities
system to function over a range of environmental
in ecosystem services
conditions was lowest where species richness was
Crocker and Tschirhart (1992) describe externalities lowest. These and other experiments suggest that
of the kind described in the Millennium Ecosystem the loss or removal of species that function effec-
Assessment (2005b) as ‘ecosystem externalities’. tively in specific conditions reduces the range of
They define ecosystem externalities as: market- conditions over which the system as a whole can
driven actions that impact the wellbeing of either operate (Tilman and Downing 1994, McGrady-
consumers or producers by altering the ecological func- Steed et al. 1997, Naaem and Li 1997). Tilman et al.
tioning on which consumption or production depends, (1996) describe this result, using reasoning from
but where the welfare effects of those actions are ignored. economics, as a portfolio effect. Increasing the
232 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

number of species that fluctuate independently will involves maintaining the options open to society in
decrease system volatility, just as increasing the an uncertain world, then the right way to think
number of independent assets in a financial port- about biodiversity is as a portfolio of biological
folio will decrease the volatility of returns. Greater assets or a risk-pooling mechanism. That is, bio-
species richness is equivalent to greater diversifi- diversity limits the variability in the supply of
cation, which leads to lower variance. provisioning and cultural services.
In a closely related line of reasoning, Perrings
et al. (1995, p. 4) state that ‘the importance of
biodiversity is argued to lie in its role in preserving 17.3 Biodiversity as insurance
ecosystem resilience, by underwriting the provi-
To be more precise about this, consider a manager
sion of key ecosystem functions over a range of
concerned to maintain the flow of some ecosystem
environmental conditions’. Conserving biodiver-
service – say food crops in an agro-ecosystem –
sity maintains species that may look unimportant
operating under uncertainty due to stochastic fluc-
for ecosystem function under current conditions,
tuations in environmental conditions. We can ana-
but which may play a crucial role in a drought,
lyze this problem using the approach developed by
pest infestation or other shock (Walker et al. 1999).
Baumgärtner (2007), Baumgärtner and Quaas (2006,
As above, conserving diversity can increase the
2008) and Quaas and Baumgärtner (2008). The
probability of maintaining the flow of desired
manager chooses a level, m, of agrobiodiversity by
services over a range of potential environmental
selecting a portfolio of different crop varieties. Given
conditions. Resilience has been defined in two
this choice the manager realizes a crop yield at level s
ways in the ecological literature. One, due to Pimm
which is random. For simplicity we may assume that
(1984), is the speed with which an ecosystem
the agro-ecosystem service directly translates into
returns to equilibrium after a shock. A second, due
monetary income and that the mean level, Es ¼ l,
to Holling (1973), is the magnitude of the shock
of yields is independent of the level of biodiversity
that can be absorbed by an ecosystem without
and is assumed to be constant. However, the var-
losing functionality – effectively the maximum
iance of agro-ecosystem service depends on the
perturbation that be accommodated without flip-
level of agrobiodiversity:
ping from one state (stability domain) to another.
The Holling resilience of a system increases with
var s ¼ r2 ðvÞ ð17:1Þ
both the resistance/robustness of that system (the
extent to which a perturbation moves it from the 0 00
where r2 (v) < 0 and r2 (v)  0. The farmer’s pri-
equilibrium) and its flexibility/adaptability (its
vate decision on the level of agrobiodiversity affects
ability to accommodate perturbation without loss
not only his private income risk, as expressed by
of functionality). The economics literature has
the variance of on-farm agro-ecosystem service, but
tended to adopt the second of these two ideas.
also causes external effects. Suppose that B(v)
Under either definition, though, if the reference
defines the sum of external benefits of on-farm
state is desirable, then greater resilience will
agrobiodiversity, and that this takes the form of a
increase welfare. If the reference state is undesir-
reduction in the variance of some public ecosystem
able, greater resilience will reduce welfare. The
service:
biodiversity problem, in this case, is to choose the
mix of species that will maximize some index of
EBðvÞ ¼ N ð17:2Þ
human wellbeing, given both the expected range
of environmental conditions (shocks) and people’s X2
aversion to risk. As Chapter 19 shows, the measure var BðvÞ ¼ ðvÞ ð17:3Þ
of biodiversity used will depend on the nature of X20 X200
the decision problem – on the aspects of biodi- where ðvÞ<0 and ðvÞ  0 To see the role of
versity that matter for human wellbeing. If that agrobiodiversity, suppose that the manager has the
 THE ECONOMICS OF BIODIVERSITY AND ECOSYSTEM SERVICES 233

option of buying financial insurance by choosing assumed, where r > 0 is a parameter describing the
some level a 2 [0,1] of insurance coverage, paying farmer’s degree of risk aversion:

aðEs  sÞ ð17:4Þ r
U ¼ Ey  var y ð17:9Þ
2
to the insurance company as an actuarially fair
premium if the farmer’s realized income is below Social welfare is assumed to be the expected
the mean income plus any transaction costs of welfare stemming from individual income and the
insurance. The latter are measured by: public benefits of on-farm biodiversity. Furthermore,
it is assumed that the private and the public risks
d a var s; ð17:5Þ associated with biodiversity are uncorrelated. Spe-
cifically, we assume an expected welfare function of
where the parameter d  0 describes the ‘costs’ of the mean-variance type, where the parameter X > 0
insurance. The higher the insurance coverage, a, the describes the degree of social risk aversion:
lower is the risk premium of the resulting income
lottery. The farmer chooses the level of agrobiodi- r X
W ¼ Ey þ EB  var y  var B: ð17:10Þ
versity, m, and financial insurance coverage, a. A 2 2
higher level of agrobiodiversity carries costs c > 0
In the private optimum, the farmer chooses the
per unit of agrobiodiversity. Hence the manager’s
level of agrobiodiversity and financial insurance
(random) income is given by
coverage so as to maximize his expected private
utility (17.9) subject to constraints (17.7) and (17.8).
y ¼ ð1  aÞs  cv þ aEs  d a var s: ð17:6Þ
The resulting allocation has the property that equi-
librium levels of both agrobiodiversity and financial
Increasing a to one allows the farmer to reduce
insurance coverage increase with the degree of risk-
the uncertain income component to zero. The mean
aversion:
and variance of the farmer’s income are determined
by the mean and variance of the agro-ecosystem
dv da
service, which depends on the level of agro- >0 and  0; ð17:11Þ
dr dr
biodiversity:
with strict equality at the corner solution a* ¼ 1. The
Ey ¼ l  cv  dar2 ðvÞ ð17:7Þ
equilibrium level v* of agrobiodiversity increases,
and the equilibrium level a* of financial insurance
var y ¼ ð1  aÞ2 r2 ðvÞ: ð17:8Þ coverage decreases, with the costs of financial
insurance:
Mean income is given by the mean level of agro-
ecosystem service, l, minus the costs of agrobiodi- dv da
>0 and  0; ð17:12Þ
versity, cm, and the costs of financial insurance, dd dd
dar2(v). For an actuarially fair financial insurance
contract (d ¼ 0), the mean income equals mean net with strict equality at the corner solution a* ¼ 0. The
income from agro-ecosystem use, lcv. The var- manager will choose the level of agrobiodiversity so
iance of income vanishes for full financial insurance as to equate its marginal benefits and marginal
coverage, a ¼ 1, and equals the full variance of costs, where the marginal benefits comprise both
agro-ecosystem service, r2(v), without any financial the insurance value of agrobiodiversity and the
insurance coverage, a ¼ 0. reduction in payments for financial insurance that
The farmer is assumed to be risk-averse with results from the reduced variance of agroecosystem
respect to his uncertain income y. Specifically, a service due to a marginal increase in agrobiodi-
general form of an expected utility function can be versity. Where financial insurance is available, the
234 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

manager will choose a level of agrobiodiversity that should align the private decisions with the social
is below the one he would choose if financial optimal agrobiodiversity level, i.e.:
insurance were not available.1
The socially optimal allocation (v^, â) is derived by X X2' ^
s^ ¼  ð vÞ > 0 ð17:16Þ
choosing the level of agrobiodiversity and financial 2
insurance coverage so as to maximize social welfare The size of the subsidy is increasing in the degree of
(17.10), subject to constraints (17.2), (17.3), (17.7), social risk aversion, X, and decreasing in the degree
and (17.8). The efficient allocation is such that of individual risk aversion, r, and the costs d per
both agrobiodiversity and financial insurance unit of financial insurance:
coverage increase with the degree of individual risk-
aversion, i.e.: d s^ d s^ d s^
> 0; < 0; < 0: ð17:17Þ
dX dr dd
d v^ d a^
> 0 and  0; ð17:13Þ
dr dr The optimal subsidy, ^s, can be interpreted as a
measure of the financial flow needed to internalize
with strict equality in the corner solution â ¼ 1. The the externality, i.e. to solve the public good prob-
efficient level of agrobiodiversity increases with the lem. Thus it can also be interpreted as a measure of
degree of social risk-aversion, but the efficient level the size of the externality.
of financial insurance coverage is unaffected by the Although this problem is posed in the context of
degree of social risk-aversion, i.e.: an agro-ecological problem, the same insights apply
to the management of biodiversity in regulating the
d v^ d a^ supply of the full range of provisioning and cultural
> 0 and ¼ 0: ð17:14Þ
dX dX services. Indeed, even though the Millennium
Assessment (2005b) described the regulating ser-
The efficient level ^v of agrobiodiversity increases vices in terms of a very specific set of buffering
with the costs of financial insurance, and the effi- functions, they actually summarize the role of the
cient level a^ of financial insurance coverage portfolio of biological assets in protecting us against
decreases with the costs of financial insurance: the vagaries of both nature and society.

d v^ d a^
> 0 and  0 ð17:15Þ 17.4 Biodiversity markets
dd dd
In all cases, appropriate policy interventions
where equality may hold in the corner solution a^ ¼ 0.
depend on both a comparison between the pri-
The difference between the socially and privately
vately and socially optimal outcomes, and the
optimal allocation is that the positive externality of
development of instruments that will induce pri-
a private farmer’s effort is fully internalized in the
vate decision-makers to behave in ways that are
socially optimal solution. By contrast, in the private
consistent with the social interest.
optimum the manager chooses a level of agrobio-
In some cases, markets are already developing
diversity that is too low. There are different ways
that allow biodiversity conservation to pay for itself
that the social optimal solution can be reached by
(e.g. by establishing property rights in the effects of
creating the right conditions for farmers. One pos-
biodiversity change). As with the agro-ecological
sibility is by providing a subsidy, ^s, on the con-
examples discussed in Section 17.3, these are cases
servation and utilization of agrobiodiversity. This
where biodiversity supports the production of
1
valuable goods and services that can, under the
This level can be determined from setting a = 0 in Eqn
right circumstances, be sold in the market. Doing so
(17.11) and maximizing over v. It is strictly smaller than v*
for all d < p and equals v* for d ≥ p, i.e. in cases where may generate enough revenue to make conserva-
financial insurance is so expensive that an optimizing tion financially viable. This point is the core thesis
farmer would not buy it. behind several recent books (Heal 2000, Daily and
 THE ECONOMICS OF BIODIVERSITY AND ECOSYSTEM SERVICES 235

Ellison 2002, Pagiola 2002, OECD 2004). Market vincristine and vinblastine found within the Rosy
creation stems from a simple but powerful idea, i.e. Periwinkle (Vinca rosea) or based on a synthetic
markets can be devised to signal the opportunity compound developed from the blueprint provided
cost to local land users of agricultural practices that by the natural compound. In either case, access to
affect biodiversity either positively or negatively. natural compounds is of great use in the research
Ideally, such incentives need to address both ‘for- and development process. It has been estimated
ward’ (or ‘downstream’) links from land users’ that 25 per cent of the drugs sold in developed
decentralized decisions to biodiversity levels and countries and 75 per cent of those sold in devel-
‘backward’ (or ‘upstream’) biodiversity linkages, i.e. oping countries were developed using natural
from changing the stock of biodiversity level and its compounds (Pearce and Puroshothamon 1995),
functional impacts on productivity to land users suggesting that extant biodiversity is of value to
such as farmers and, thus, work at the landscape pharmaceutical firms in their efforts to develop new
level (Pascual and Perrings 2007). But this implies drugs.
that such incentives may affect the livelihoods of The CBD recommends a structure for biopros-
large numbers of land users. This adds a further pecting agreements to accomplish three main goals:
layer of responsibility to public agencies to be the conservation of biological diversity, the sus-
aware of the distributional implications of alterna- tainable use of natural products, and the fair and
tive incentive measures. equitable sharing of benefits derived from genetic
One example in which conservation is currently resources (Article 1). They imply the existence of
being made financially attractive is ecotourism. The intellectual property rights in the face of current
World Tourism Organization estimates that tour- patent systems by which, for example, the phar-
ism generated revenues of $463 billion in 2001. One maceutical and seed industries can realize the
of the fastest growing segments of tourism may be monopoly benefits of new product development
nature-based or ecotourism. Some areas have had a that are guaranteed by the ability to patent dis-
long history of profiting from the richness of the coveries. Simpson, Sedjo, and Reid (1996) model the
local biodiversity, including Yellowstone National research and development process as a search
Park in the USA, Krueger National Park in South through a list of research leads and conclude that
Africa, and a variety of National Parks in Kenya the value of the marginal lead is generally insuffi-
and Tanzania. Costa Rica has also done well pro- cient for pharmaceutical firms to play a role in the
moting ecotourism, with approximately 1 million conservation of biodiversity (see also Costello and
tourists spending $1 billion in 2000 (Daily and Ward 2006). However, in the presence of competi-
Ellison 2002, p. 178.). Several economic studies have tion, it is no longer the case that discovery of a
found that ecotourism can generate significant single active compound is sufficient to guarantee a
revenues in a variety of developing country settings monopoly position within the market (Conte 2007).
(e.g. Aylward et al. 1996, Lindberg 2001, Maille and In a competitive search environment, the revenues
Mendelsohn 1993, Wunder 2000). associated with discovery will depend on the pro-
A second example is bioprospecting for useful portion of total successes controlled by the firm and
genetic material from plant or animal species that a firm may have the incentive to preemptively
may lead to the development of valuable pharma- exclude its competition from searching a portion of
ceuticals or other products. Pharmaceutical firms the research leads by signing bioprospecting
actively screen organisms in search of such active agreements with host nations.
compounds as part of their intensive research and In recognition of the importance of IPRs to
development programs. Bioprospecting is the term innovation, the Agreement on Trade Related
used to describe the process of testing natural Aspects of Intellectual Property Rights (1995)
organisms for these biochemically active com- (TRIPS Agreement), mandates that all member
pounds. If identified as active, a compound can nations of the World Trade Organization enact
result in the development of a new drug based on national legislation to provide minimum standards
the natural compound itself (as in the case of and scope of IPR protection (Strauss 1996). While
236 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

all member nations have complied, there is still with no financial stake in conservation or that in
heterogeneity in the security of these property fact suffer financial losses from conservation activ-
rights across nations, which might explain the pat- ities (e.g. wildlife damage to crops) might resent or
tern of existing agreements across countries. The actively oppose such activities, leading to a greater
importance of IPR security might also explain why probability that conservation will fail. Trying to
some companies have made agreements with give local communities a stake in conservation has
botanical gardens in developed countries for access led to efforts to promote community-based conser-
to samples from tropical countries, as there is less vation (Western and Wright 1994) and integrated
uncertainty associated with the IPRs in developed conservation–development projects, or ICDPs (Wells
nations (Sampath 2005). and Brandon 1992). The goal of community-based
There are unanswered questions about the opti- conservation is to give local communities control
mal allocation of rents from a bioprospecting over resources, thereby giving the community a
agreement. Consider, for example, the case of the stake in conservation. The most well-known com-
rosy periwinkle mentioned earlier, a plant native to munity-based conservation program is the Com-
Madagascar that contains vincristine, a powerful munal Areas Management Program for Indigenous
cancer-fighting compound. No synthetic substitute Resources (CAMPFIRE) in Zimbabwe (see Barbier
for vincristine exists, and one ounce of vincristine 1992 for an early review and economic assessment).
requires 15 tons of periwinkle leaves. This has ICDPs try to ‘link biodiversity conservation in pro-
resulted in depletion of nearly the entire native tected areas with local socio-economic development’
periwinkle habitat in Madagascar (Koo and Wright (Wells and Brandon 1992). Both approaches arose
1999), though the plant has been extensively culti- because of the failure of traditional protected areas
vated elsewhere. However, if drug companies do conservation strategies that ignored the needs of
not keep a significant fraction of rents from devel- local communities.
oping new drugs they may not have sufficient The extent to which conservation and local con-
incentive to develop new drugs via bioprospecting. trol over resources, or local economic development,
Mendelsohn and Balick (1995) found a significant are mutually consistent remains to be seen. Overall,
difference between likely social and private returns community-based conservation and ICDPs have
to development of new drugs. Koo and Wright had mixed success to date. There is no guarantee
(1999) also argue that biodiversity will be under- that once they are given the choice, local commu-
provided by the private sector via bioprospecting nities will in fact choose to conserve. Cultural,
on the grounds that although the value of biodi- social, or political factors may block conservation
versity is very large, market and social values are even when economic factors favour conservation.
grossly misaligned. There is also no guarantee that conservation and
It should also be noted that any added value of local economic development are in fact consistent
biological resources is created at each step of the goals. Certainly in some communities with eco-
innovation process – through the contributions of tourism potential, or where ecosystems provide
the local communities and research laboratories to valuable ecosystem services, conservation and
industrial applications – and not only at the final development may go hand in hand. In other cases,
stage of the innovation process. The existing IPR the conservation of biodiversity and economic
system only addresses the final stage of the inno- development may not be consistent. Because of the
vation process, thus casting doubt as to whether pervasive nature of external benefits created by
IPRs are sufficient to induce the socially optimal biodiversity conservation, it may require more than
level of conservation (Goeschl and Swanson, 2002; just allowing local control and market forces to
Dedeurwaerdere et al. 2007). achieve an efficient level of conservation.
Indeed, both ecotourism and bioprospecting have Recognition that the conservation of biodiversity
been subject to criticism that revenues generated by may generate benefits that reach well beyond the
conservation activities have not necessarily resulted local community provides a rationale for govern-
in benefits to local communities. Local communities ments and non-governmental organizations to
 THE ECONOMICS OF BIODIVERSITY AND ECOSYSTEM SERVICES 237

provide resources for conservation, and for the overkill’. Conservation easements that rule out certain
institution of national or international conserva- incompatible land uses, but not all land uses, are often
tion policies. At present, though there are a num- a far cheaper route to secure conservation objective
ber of policies to promote conservation, there are than acquisition. Recently, interest has shifted away
also a number of policies that have the opposite from land acquisition toward conservation easements
effect. Agricultural subsidies, subsidies to clearing and other ways of working with landowners to pro-
land, resource extraction, and new development mote both conservation and landowner interests. For
may all contribute to driving a further wedge example, The Nature Conservancy’s approach, once
between private and social returns from actions heavily weighted toward acquisition, now incorpo-
that conserve biodiversity. Perhaps the first rule rates mechanisms such as community development
for policy should be to ‘do no harm’. Beyond projects to reduce the demand for fuelwood and the
doing no harm by eliminating perverse subsidies, purchase of conservation easements to limit devel-
however, positive external benefits from conser- opment (see http://www.nature.org/ for examples).
vation require policies that create positive incen- Acknowledging that donors from high-income
tives to conserve. nations invest billions of dollars toward ecosys-
Both governments and non-governmental organi- tem protection in low-income nations, a related
zations, such as the Nature Conservancy and World literature debates the relative merits of direct
Wildlife Fund, are actively engaged in acquiring land conservation payments versus indirect mechan-
for conservation and in other activities promoting isms (e.g. payments to promote ecotourism which
conservation. Buying land is a direct and secure way generates ecosystem protection as a joint prod-
to promote conservation, but it is often a costly uct). Although indirect approaches are the pre-
instrument for protecting biodiversity. Boyd et al. dominant form of intervention in low-income
(1999) find that acquisition is often ‘conservation countries, Ferraro and Simpson (2002) argue that

Box 17.1 The impact of market and non-market institutions on forest biodiversity
and timber extraction: a study in northern India

The institutions that govern forests affect both the a weighted index of biodiversity in which prices are used
diversity of the forest stock and the mix of products and as weights for the different Yi. A loss of biodiversity is
services that are extracted. A study of timber extraction reflected in an increase in the value of the biodiversity
from forests of the north Indian state of Uttar Pradesh index, which ranges between 0 and 1. The effect of the
from 1975 to 2000 shows how timber harvest is related bio-economic diversity measure on timber productivity is
to institutional conditions, species richness and the captured by the introduction of an extra term, B, in the
ecological characteristics of the forest, as well as to forest timber production function:
stocks, and harvest effort. Using a modified
Gordon–Schaefer production function, and the Y ¼ qBEX ð17:1:1Þ
assumption that forests are managed for ‘sustainable
timber extraction’, the reduced form equations are where E is effort and X the aggregate biomass of all species.
derived and estimated (Chopra and Kumar 2004). The Eqn. (17.1.1) implies that Y/E ¼ F (B, X), i.e. that the effort
composition of products extracted is determined by their involved in timber extraction is inversely related to B. As B
value, high value products being given priority. The decreases (or as biodiversity increases), the extraction function
modified model shifts, resulting in a lower effort per unit effort. In other words,
X includes a2 bio-economic diversity index the model with the biodiversity index yields a lower level of Y
defined as ðP Y =TRÞ where Yi denotes harvest of
i i i for the same level of E, since 0 < B < 1. If the forest manager
the ith species,
X Pi denotes the price of the ith species, is primarily interested in timber extraction, this results in a
and TR ¼ P Y . The index is postulated to impact
i i i substitution of plantation forests for natural forests, so
extraction as a shift factor in the extraction function. It is changing the ecological properties of the forest.
238 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

To capture this, Chopra and Kumar introduce W (the significant. Extraction increases over time as the plantation
share of plantation forest in total area) in the growth area increases. Since W is inversely related to the level of
function for timber biomass: biodiversity in the forest, a decreasing biodiversity due to a
larger ratio of plantation to natural forest leads to rising

X ¼ rX ð1 þ eW  X =K Þ  qBEX ð17:1:2Þ trends in extraction. Extraction per unit effort increases as Ubt
increases. Further, assuming E to be constant, they show that
in which e is a coefficient for impact of W on growth of Ubt (defined as Y/BE) may increase under the following
timber stock. They postulate that extraction increases as W conditions with respect to the biodiversity index B.
increases. They further assume that B ¼ F (W). Since B
increases as W increases, forests become less diverse. The 1. With a rising B (falling biodiversity), if Y rises faster than
estimated harvest equation is: B (extraction rises faster than biodiversity falls) Ubt increases
and extraction of timber over time decreases. A rising
logðUbt =Ubt1 Þ ¼ r þ 0:0853 Et þ 0:00169Ub * t extraction with decreasing biodiversity of the forest pushes
the system towards a state in which increases in extraction
þ 8:7454Wt ** ð17:1:3Þ take place at an increasing rate.
in which Ubt is biodiversity adjusted extraction (per unit 2. With a falling B (rising biodiversity) Ubt could decrease
effort), * indicates significance of the coefficient at 5 per cent provided Y is not rising faster than B is decreasing, leading
level and ** denotes significance at the 1 per cent level. to a decreasing trend in extraction in subsequent periods.
Effort Et is not, by itself, a significant determinant of trends in 3. With a constant B (constant levels of biodiversity)
extraction in this formulation, but both Ubt and Wt are increases in Ubt are determined by changes in Y.

direct payments can be far more cost-effective, benefits that is consistent with national, and
often requiring no additional institutional infra- applicable international, legislation;
structure or donor sophistication. 2) make greater and more consistent use of domestic
economic instruments in the application of their
biodiversity policy frameworks, while attempting to
17.5 Economic instruments reach further agreement at the international level on
the use of economic-based policy instruments with
Where biodiversity markets do not exist, and where respect to biodiversity conservation and management;
market-driven behaviour leads people to select a 3) integrate market and non-market (i.e. non-price)
combination of species, ecosystems, and landscapes instruments – taking account of the respective
that is not socially optimal, economists have advantages of each in lowering information and
developed a range of market-like instruments for transactions costs, and in addressing the ‘public’
encouraging socially desirable behaviour. The values of biodiversity – into an effective and
application of these instruments has been widely efficient mix of policies; and
endorsed, and a number of countries make use of 4) integrate biodiversity policy objectives in a cost-
one or more of them. The OECD (2004), for exam- effective manner into government sectoral policies, in
ple, makes the following recommendation to order to avoid undue adverse effects on biodiversity
member countries: and its related resources.

1) establish and apply a policy framework aimed at The set of instruments proposed by the OECD is
ensuring the efficient long-term conservation and amongst those described in Table 17.1. In what
sustainable use of biodiversity and its related follows we highlight those instruments that are
resources. The overarching goal of such a frame- currently attracting attention.
work should be to ensure maximum net benefits, Payments for ecosystem services The most direct
both now and in the future, from the use and way to create positive incentives for conservation is
conservation of resources stemming from biodiver- to institute a system of payments for the provision
sity – as well as an equitable sharing of these of ecosystem services (ES). Payments (or Rewards)
 THE ECONOMICS OF BIODIVERSITY AND ECOSYSTEM SERVICES 239

Table 17.1 Instruments for encouraging the socially optimal use of biodiversity.

Category Type of instrument Example

Economic incentives Fees, charges, and environmental taxes Charges or non-compliance fees related to certain types of
Payments for ecosystem services forestry activities
Assignment of well-defined property Liability fees for the maintenance or rehabilitation of
rights ecologically sensitive lands
Reform or removal of harmful subsidies Fishing license fees or taxes (whose objective is resource management)
Levies for the abstraction of surface water or groundwater
Liability payments for biodiversity damages (including interim losses)
Charges for:
Use of public lands for grazing in agriculture
Use of sensitive lands
Hunting or fishing of threatened species
Tourism in natural parks
Payments to farmers within a watershed for using farming
techniques that maintain the quality of water resources
Auctioned conservation contracts
Funds Environmental funds and public financing Global Environment Facility funding of local biodiversity conservation
where there are global benefits
Framework incentives Information provision, scientific and Global Biodiversity Observation Systems
technical capacity building Development of natural resource accounts
Economic valuation Inclusion of biodiversity in Adjusted Net Savings Measures
Market creation Support for biodiversity-related labelling schemes
Institution-building and stakeholder Strengthening governance of local, regional and global common
involvement pool biological resources
Transferable development rights

for ecosystems services, P(R)ES, are voluntary generated by upland farmers who can maintain the
transactions, not necessarily of a financial nature, in flow of valuable services that benefit lowland
the form of compensation flows for a well-defined farmers or urban dwellers. However, a key obstacle
ES, or land use likely to secure it. The notion of in the successful implementation of P(R)ES arises at
‘rewards’ is used to acknowledge that transactions the ‘value demonstration’ stage, especially due to
from beneficiaries to providers may not need to be the scientific uncertainties underpinning the lin-
based on a financial flow. It can also involve in-kind kages between alternative land uses and the pro-
transactions that may include a myriad of valuable vision of the targeted environmental services.
goods and services from the beneficiaries’ point of The country that has moved furthest in this
view, which can take intangible forms in diverse direction is Costa Rica. The 1996 Forestry Law
situations, such as knowledge transfer. P(R)ES is instituted payments for ecosystem services. The law
paid/rewarded by the beneficiaries and shared by recognizes four ecosystem services: mitigation of
the providers of the ES after eventually securing greenhouse gas emissions, watershed protection,
such compensation. P(R)ES are often designed to biodiversity conservation, and scenic beauty. The
address problems related to the decline in some National Forestry Financial Fund enters into con-
environmental services, such as the provision of tracts with landowners who agree to do forest
water, soil conservation, and carbon sequestration preservation, reforestation, or sustainable timber
by upland farmers who manage forest-lands in management. Funds to pay landowners come from
upper watersheds. In essence, such compensations taxes on fuel use, sale of carbon credits, payments
are intended to internalize the positive externalities from industry, and the Global Environment Fund
240 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

(GEF). Many developed countries have adopted demonstration of an objective measure of its con-
some form of ‘green payments’ in which agricul- servation value on both biological and economic
tural support payments are targeted to farmers who grounds. In addition, the change in decentralized
adopt environmentally friendly management prac- behaviour needs to be sustained into the future,
tices or land uses (OECD 2001). which requires longer term political commitment.
P(R)ES cannot be properly designed or imple- Asymmetric information between landowners and
mented without a clear understanding of the the compensating government agency is at least
property right regimes. Property rights regimes in potentially problematic (Innes et al. 1998). If land-
natural resource management comprise a structure owners expect compensation that is lower than the
of rights to resources, rules under which those present value of the benefit stream arising from
rights are exercised, and duties binding both those developing the land holding, they have a motive to
who possess the right(s) and those who do not. As develop quickly. Furthermore, even when exact
Bromley (1991, pp. 2) puts it, ‘[p]roperty is not an compensation is foreseen by landowners, they may
object but rather is a social relation that defines the still have an incentive to intensify land use before
property holder with respect to something of compensation if this augments the market value of
value . . . against all others’. In this context, Costa their property.
Rica is one of the few examples where an elaborate Transferable development rights Another approach
nationwide PES program is in place under a clear to conservation is to institute a system of transfer-
property rights regime. Under this program, only able development rights (TDR). TDR are virtually
farmers with property rights to land can be paid for identical to cap-and-trade schemes to limit pollu-
the environmental conservation they provide tion emissions. In a TDR system, the conservation
(Pagiola 2002). planner determines how much land can be devel-
A recent illustrative example of the potential oped in a given area. Development rights are then
effectiveness and flexibility of P(R)ES programs is allocated and trades for the right to develop are
that of RUPES: Rewarding Upland Poor for Environ- allowed. Developers can increase density in a
mental Services. The RUPES partnership comprises growth zone (‘receiving area’) only by purchasing
the International Fund for Agricultural Develop- development rights from the preservation area
ment (IFAD), the World Agroforestry Centre (‘sending area’). The approach was developed and
(ICRAF) and a group of local, national, and inter- implemented extensively in the 1970s to direct
national partners.2 RUPES aims to conserve envi- development within urban areas (see Field and
ronmental services at both global and local levels, Conrad (1975) for what appears to be the first
while at the same time supporting the livelihoods of economic model of the supply and demand for
the upland poor in Asia. So far, the main focus has development rights; see Mills (1980) for a model of
been on Nepal, the Philippines, and Indonesia, and TDR and a discussion of their appropriateness for
the environmental services mostly include water use in protecting public goods).
flow and quality, biodiversity protection and car- Not until relatively recently have economists
bon sequestration. explicitly considered TDR as a mechanism to conserve
A variant of P(R)ES is the approach based on biodiversity. Panayotou (1994) developed the TDR
direct compensation payments (DCP) for taking pri- approach for conservation. He argued that ‘biodiver-
vate land out of production and into conservation sity conservation is ultimately a development rather
(Swart 2003). Similar to other incentive mechan- than a conservation issue’ (Panayotou 1994, p. 91).
isms, the identification of the level of the efficient Given that most biodiversity exists in the developing
compensation payments to landowners requires the world, and that the public good nature of biodiversity
requires a mechanism for paying developing coun-
tries to be stewards of this resource, Panayotou argues
2
Some of the insights reflected here come from personal that TDR may also be an effective way to protect
communication with Meine van Noordwijk, Tom Tomich
and ICRAF personnel involved in RUPES program in
global (as well as local) biodiversity. Merrifield (1996)
Sumatra, Indonesia. proposes use of a similar concept where ‘habitat
 THE ECONOMICS OF BIODIVERSITY AND ECOSYSTEM SERVICES 241

preservation credits’ would be required for develop- for example, for new land use restrictions to be
ment. There is no guarantee that TDR schemes, like imposed on ecologically sensitive sending zone
cap-and-trade schemes, will result in efficient out- upon obtaining additional information about its
comes unless the planner chooses the correct amount higher conservation value and assigning TDRs to
of rights/permits to allocate. An additional problem compensate for such additional restrictions.
faced in TDR for conservation is deciding what are Usually, tight restrictions are also imposed on the
appropriate trades. Land units, unlike air emissions, receiving zone so as to increase the demand for
have unique characteristics and may contribute to a TDRs (Chomitz 1999).
number of conservation objectives. What constitutes One of the forerunners of the TDR mechanism is in
an equal trade is not obvious. Similar problems over Brazil. While some initiatives have been proposed, the
establishing the proper trading ratios exist in mitiga- implementation is still under discussion. The basic
tion banking schemes for wetlands. idea is to give the opportunity for Brazilian agricul-
Having said this, TDR appears to be an innovative tural land owners not complying with the National
and cost-effective way to resolve the perverse incen- Forest Code (Law number 4771 approved on 15/09/
tives arising from DCPs. TDR extend the longstand- 1965) to buy forest reserves in other areas, normally in
ing ‘agro-ecological zoning’ schemes, which aim to close proximity to their property. However, as
direct development to areas of high productivity pointed out by Pascual and Perrings (2007), a fully
potential and to restrict agricultural land use in eco- operational market for forest reserves is still to be
logically significant and sensitive areas. However, implemented. Two examples are the National Provi-
such zoning programs do not allow for any substi- sionary Measure (Medida Provisória, Number 21666-
tutability between plots in meeting overall conserva- 67, approved on 24/08/2001), which amends the
tion goals. By providing a market-like alternative to Forest Code and in the State of Sao Paulo (State
the DCPs, flexibility in achieving conservation goals Decree number 50889, approved on 16/06/2006).
can be introduced. In this vein, the main advantage of Auction Contracts for Conservation (ACCs) One
TDR is that it can, in principle, encourage conserva- other way to induce private landowners to achieve
tion on lands with low agricultural opportunity costs, desired level of supply of biodiversity conservation
while providing appropriate incentives to the affected at the landscape level is by applying a competitive
landholders (Chomitz 1999). bidding or auction mechanism. An auction is a
In contrast to DCP, each landowner is issued quasi-market institution with an interesting feature,
tradable development permits by the government i.e. it has a ‘cost revealing’ advantage compared to
agency at an initial period. Subsequently, landowners P(R)ES and DCP and can, in principle, be incorpo-
hold the right to either develop or intensify their land rated into a TDR system. In fact, the cost-revelation
holding. However, to develop that fraction of land a feature provides a way of generating important cost
landowner needs to either use of one of the develop- savings to governments. This is especially so when
ment permits (s)he holds or buy it from other land- significant information asymmetry between farmers
owners, who upon selling it can no longer develop and conservation agencies exist regarding (i) the real
their land fraction and instead must give it up for opportunity cost of conservation and (ii) the eco-
conservation. In this case, the government can share logical significance of the natural assets existing in
the cost of the ‘takings’, i.e. compulsory government farmlands. While the former is often better known
land acquisition, with the landowners themselves. by farmers themselves, the latter is normally better
Two main types of TDR programs exist at the known by environmental experts. Such information
landscape level: single and dual zoning. The former asymmetries one reason for missing agrobiodiversity
is similar to permit systems such as those used in conservation markets. The idea is to use auctions to
transferable fishing quotas or pollution control. reveal the hidden information needed to recreate
After the initial allocation of quotas, anyone within voluntary conservation contracts between land-
the program area may buy or sell the permits. The holders and the government.
dual zone system instead explicitly designates both In essence, landholders submit bids to win con-
(permit) sending and receiving areas. This allows, servation contracts from the government. But while
242 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

the latter prefers low bids, landowners need to Perrings, 2007). Furthermore, if markets for biodi-
submit bids that at least cover the opportunity cost versity are recreated without proper institutional and
of carrying out conservation activities. The problem regulatory backup, then the social costs of such poli-
is that information about such opportunity costs is cies may well outweigh the benefits from conserva-
often better known by resource users than by the tion (Barrett and Lybbert 2000). In a second-best
government and the costs are also likely to be user- world where information is elusive, most policy
specific. Stoneham et al. (2007) provide a recent initiatives pragmatically focus on ensuring that insti-
small-scale pilot case study of an auctioning system tutions are developed so as to keep future options
for biodiversity conservation contracts in Victoria, open (Tomich et al. 2001). In fact, most conservation
Australia, known as BushTender. The ACC involved policies are aiming at developing flexible and open
98 farmers, of whom 75 per cent obtained govern- institutions that can mitigate the negative effects of
ment contracts to conserve remnant vegetation in intensification in agroecosystems, without foreclosing
their farms after all farmers submitted sealed bids future land (de)intensification options.
associated with their nominated conservation An important qualification is that many market-
action plans. The selection of the farmers who won like mechanisms have implications for the rights of
the contract was based on ranking the relative cost- the poor, particularly in low-income countries
effectiveness of each proposed contract. This where people depend heavily on environmental
involved weighting each private bid against the resources (Dasgupta 2001). Pricing access to eco-
associated potential ecological impacts at the land- system services can cause the socially disadvan-
scape level. Given a public budget of $400,000, taged and vulnerable to be excluded from those
contracts with bids that averaged about $4,600 were services, and mechanisms need to be developed to
allocated and specified in management agreements address this. For example, in 1991 the Government
over a three-year period. In total the contracts cov- of Uganda established a national park in the Bwindi
ered 3,160 ha of habitat on private land. Stoneham forest to protect the mountain gorilla. This park was
et al. (2007) have estimated that the BushTender established with little consultation with the local
mechanism has provided 75 per cent more biodi- populations who depended on the forests for their
versity conservation compared to a fixed-price pay- livelihood. As a result, poaching and encroachment
ment scheme (or DCP). In addition, they contend were common. In 1995, the Mgahinga and Bwindi
that given the relatively low enforcement costs in Impenetrable Forest Conservation Trust Fund was
their pilot study, this ACC has interesting cost- created, its proceeds being shared with the local
effective properties. The pilot case study shows that communities to encourage sustainable development
it is possible to recreate the supply side of a market activities and conservation.
for agrobiodiversity conservation. The general problem is that economic interven-
P(R)ES, DCP, TDP, and ACC all share an important tions that are efficient by the Pareto criterion (which
characteristic for successful market creation for bio- states that an economic intervention is efficient if it
diversity conservation. For these mechanisms to be benefits at least one person without leaving any
effective, accurate ecological and economic informa- other person worse off) may still leave people
tion at the demonstration, capture and sharing stages worse off in relative terms. One approach to this
is needed. If it is not possible, or very costly, to convey problem is to subject interventions to a second test:
clear and credible information about the nature of the that the equity gap between individuals or groups
services derived from biodiversity, the costs of sup- after an economic intervention should be no larger
plying them, and the benefits derived for society, then than the gap before the intervention. In this way, if
the effect of implementing these economic mechan- one individual has benefited from the economic
isms would be distorted and would lack precision. instrument, then some transfer will need to take
Moreover, it would be naïve to champion market place to ensure that the gap between that individual
creation for biodiversity conservation if other sup- and others will remain the same. In other words,
porting institutions are also lacking, such as property some form of social redistribution mechanism will
rights to the resources in question (Pascual and need to be institutionalized at the same time the
 THE ECONOMICS OF BIODIVERSITY AND ECOSYSTEM SERVICES 243

Box 17.2 The economics of the US Endangered Species Act (ESA)

While market-oriented policies have been of increasing benefits side of the equation also seems to affect listing
importance in recent years, other important policies and recovery spending even though the ESA does not base
directed at the conservation of biodiversity, including the such decisions on the popularity of the species. Metrick and
U.S. Endangered Species Act and the Convention on Weitzman (1996) found that more charismatic species were
International Trade in Endangered Species, are at their core likely to be listed than uncharismatic species, and that once
largely command and control regulatory regimes. The listed ‘visceral characteristics play a highly significant role in
Endangered Species Act (ESA), enacted in 1973, changed explaining the observed spending patterns, while the more
conservation policy from a largely voluntary and toothless scientific characteristics appear to have little influence’
regime that existed prior to 1973 into a powerful (Metrick and Weitzman 1996, p. 3).
environmental law capable of stopping large government While much of the early regulatory activity under the
projects and actions of private landowners (Brown and ESA targeted government actions under Section 7, the
Shogren 1998). Section 7 of the ESA prohibits federal 1990s saw an increase in the emphasis on conservation on
agencies from actions that cause ‘jeopardy’ (i.e. risk of private lands under Section 9. More than half of
extinction) to species listed as threatened or endangered. endangered species have over 80 per cent of their habitat
Section 9 prohibits public and private parties from ‘taking’ on private land (USFWS 1997). Conservation on private
listed species. ‘Taking’ includes causing harm to species lands presents a number of incentive issues (Innes et al.
through adverse habitat modification from otherwise legal 1998). A landowner whose parcel contains an endangered
land uses, such as timber harvesting or building, as well as species habitat may face restrictions on what activities may
more obvious prohibitions against killing, injuring or be undertaken. The landowner need not be compensated if
capturing a listed species. The way the law is written, the restrictions are imposed and losses to the landowner result
ESA appears to have very limited scope for economic (though the law on regulatory takings is quite unsettled;
considerations. Sections 7 and 9 are absolute prohibitions. see Polasky and Doremus 1998). The potential losses the
Biological criteria are the basis for listing species. In TVA ESA may impose on a landowner give rise to several
v. Hill, the US Supreme Court wrote: ‘The plain intent of perverse incentives. Innes (1997) shows that there can be a
Congress in enacting this statue was to halt or reverse the race to develop in order to beat the imposition of an ESA
trend toward species extinction, whatever the cost’ ruling. Similarly, there may be an incentive to ‘shoot, shovel
[437 U.S. 153, 184 (1978)]. When it looked like a small and shutup’ in order to lower the likelihood of imposition
unremarkable fish (the snail darter) that was previously all of restrictions under the ESA (Stroup 1995). Further,
but unknown would halt construction of a large dam backed because current law stipulates that acquiring specific
by politically powerful members of Congress, Congress information about species is a prerequisite to imposing
amended the ESA. They authorized the formation of the restrictions on a landowner, there is no incentive for the
Endangered Species Committee (‘The God Squad’) to allow landowner to cooperate in allowing biological information
an exemption to the ESA if the benefits of doing so would to be collected (Polasky and Doremus 1998).
clearly outweigh the costs. There are high hurdles to be met There are several possible ways to reform the ESA to
for convening this Committee and it has been used rarely. cure the worst of the perverse incentives. One method is to
Despite the fact that the law is written in a way that provide compensation. When eminent domain is used and
appears to marginalize economic considerations, it has there is a physical taking of property, the government is
proved impossible to administer the Act while totally required to provide compensation equal to the market
ignoring economics. Several writers have noted that value of the property. The same approach could be taken
economic and political considerations influence agency when the government mandates conservation on private
actions at all stages of the ESA process including the listing land. There are two potential problems with this approach.
stage, which is supposed to be done strictly on biological First, Blume et al. (1984) show that when landowners are
grounds (e.g. Bean 1991, Houck 1993). Endangered fully compensated in the event of a taking, there is an
species whose protection threatens to impose large costs incentive to over-invest. It is socially optimal to take
run into political opposition that translates into pressure on account of the probability of future takings that render the
the Fish and Wildlife Service. This pressure appears to investment worthless. The landowner is, however, fully
translate to lower probability of listing (Ando 1999). The reimbursed and so ignores this factor. Second, use of

Continues
244 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Box 17.2 (Continued) A different approach to reform is to allow landowners to

government funds to pay for compensation may be costly. avoid sanctions if they can prove that their proposed actions
On the other hand, others point out that there is an will not cause harm (Polasky and Doremus 1998). This type of
advantage to forcing regulators to understand the costs approach is exemplified in the ESA by the provision to allow
of imposing regulations by paying compensation (e.g. landowner actions that cause some minor and unintended
Stroup 1995). Rather than tying compensation to market harm to a listed species for landowners with approved Habitat
value, paying compensation tied to the value of Conservation Plans. The incentive for filing Habitat
conservation along the lines of green payments discussed Conservation Plans was further sweetened by promises of ‘no
above, can generate efficient incentives to conserve surprises’ and ‘safe harbors’ that put the burden on the
(Hermalin 1995). government for costs imposed by future regulatory actions.

economic instruments are being implemented. This trading partners and consumers are interested in
however keeps the status quo of the existing equity global rather than local levels of biodiversity, trade is
gaps within society. A third test, which can be unambiguously welfare-enhancing.
considered pro-poor, is that the net benefits accru- A second approach focuses on biological inva-
ing from the intervention are distributed according sions as an externality of trade (Perrings et al. 2000,
to some ratio whereby the increase in welfare of Perrings et al. 2002, Kohn and Capen 2002, Costello
the worse-off individual is proportionately greater and McAusland 2003, McAusland and Costello
than the welfare increase of the best-off individual 2004, Knowler and Barbier 2005). This literature
(Duraiappah 2006). considers both the problem of incentives to inter-
nalize biodiversity externalities of trade, and the
problem of insufficient investment in biodiversity
17.6 The international dimension
conservation as a public good. Costello and
The problem of transboundary externalities resulting McAusland (2003) explore the use of tariffs on
from the growth of international trade is the subject imports to reduce the damage costs from acci-
of a substantial literature. As with externalities in dental introductions. While they show that import
local markets, one focus has been the consequences tariffs will always reduce import volumes of
of ill-defined property rights in environmental potentially invasive species, they find that tariffs
resources (Chichilnisky 1994, Brander and Taylor can have adverse effects if they alter the compo-
1997, 1998, Rauscher 1997). The impact of trade on sition of imports, or change land use in ways that
biodiversity as a specific environmental problem has make ecosystems more vulnerable to invasive
been evaluated from two main perspectives. One species. McAusland and Costello (2004) consider
focuses on the link between specialization under the efficiency of port inspections combined
trade, habitat conversion, and species loss (Barbier with tariffs on imported goods, and find that the
and Schultz 1997, Polasky et al 2004). These studies optimal tariff covers inspection costs plus the
calculate the impact of trade on biodiversity from the potential damage costs from outbreaks of pests
proportion of the land area that is converted to the undetected during inspections. The optimal level
production of primary commodities, the impact on of tariffs in each case depends on the risk of bio-
existing species being taken from the species–area logical invasions and the expected level of damage
relationship (Macarthur and Wilson 1967). Polasky et they cause. The public good problem in the case of
al. (2004) extend the analysis to the two country case. invasive species involves the protection offered to
The same mechanism operates in each country. They all by measures to control the introduction of pests
argue that if there are high levels of endemism in and pathogens. Since it is a ‘weakest link’ public
each country, and if consumers are concerned to good, the protection to all is frequently only as good
protect local biodiversity, trade can reduce the level as the protection offered by the weakest link in
of welfare. But where species are common to both the chain. This has implications for the pattern of
 THE ECONOMICS OF BIODIVERSITY AND ECOSYSTEM SERVICES 245

international investment in invasive species control decline, as it was too easy to sell illegally harvested
(Perrings et al. 2002). ivory and because anti-poaching efforts of impo-
The persistence of international biodiversity verished governments were no match for well-
externalities, like the persistence of other environ- organized poaching gangs. Van Kooten and Bulte
mental externalities, has much to do with the ways (2000) summarize economic arguments about the
in which international markets and the rules of ivory ban and present results from application of
international trade are structured. Unlike many several dynamic models.
other environmental resources, however, there does The argument for trade restrictions of the CITES
exist a treaty on the trade of biological species. The type is that, in the absence of restrictions, there will
Convention on International Trade in Endangered be a ‘race to the bottom’. Firms will seek to exploit
Species (CITES) deals specifically with international the international advantages offered by relaxed
markets for biological resources (as distinct from labour and environmental conditions, and countries
markets for the international benefits of local con- will use the lack of environmental protection to
servation effort). Its role is to reduce the impact of induce inward investment (Wheeler 2000). By this
trade on the survival probability of rare and argument, biodiversity and other environmental
endangered species. It does this by imposing pro- externalities are not just an incidental product of
hibitions. Examples include international bans on market failures. They are the outcome of strategic
the trade in elephant ivory, and on timber obtained decisions by governments and firms seeking a
from certain endangered tree species (Barbier et al. competitive advantage. The claim is that where trade
1994, Swanson 1995). agreements make it impossible either to induce
CITES has arguably been the international inward investment or to protect domestic agriculture
agreement that has had the greatest impact on or industry through trade policy, countries may be
conservation outcomes (WCMC 1992). CITES encouraged to use environmental policies to the
authorizes banning international trade in species same effect. Specifically, they may be encouraged
listed under Appendix I, and regulating trade in either to allow ecological dumping by relaxing
species listed under Appendix II. In 1989, CITES environmental protection measures, or to use envi-
initiated a ban on trade in ivory. In the 1970s and ronmental regulation as trade protection measures.
1980s rampant poaching of elephants caused a drop The empirical evidence for a race to the bottom is
in elephant populations of roughly 50 per cent mixed. The relocation of polluting industries from
(Barbier and Swanson 1990). Particularly threa- high-income to low-income countries is a part of the
tened were elephant populations in east African explanation for changes in environmental indica-
countries. Elephant populations in southern African tors observed in the Environmental Kuznets Curve
countries were less threatened. Imposing the ivory literature (Barbier 1997, Cole et al 1997, Arrow et al.
trade ban was controversial. Southern African 1995). However, studies of the incentive effects of
countries with relatively healthy elephant popula- environmental regulation have concluded that the
tions (Botswana, Malawi, Namibia, South Africa, costs of compliance with environmental regulations
Zimbabwe) objected and did not sign on to the ban. are a sufficiently small proportion of total costs that
Opponents of a ban argued that it would likely they do not generally drive location decisions (Jaffe
result in high ivory prices as supply was choked et al. 1995, Levinson 1996). Wheeler (2000) argues
off, which would increase the rewards to poaching that the effects of income growth on environmental
(Barbier and Swanson 1990). Opponents also protection in low-income countries, along with the
argued that by denying rights to sell ivory legally progressive empowerment of local communities
there would be less financial reason to conserve affected by relocation, will be enough to avert a
elephant populations and less money available for race to the bottom.
enforcement efforts against poaching. Proponents In fact, the environmental impacts of trade are one
of the ban, including east African countries and of the few acceptable justifications for imposing trade
many developed countries, argued that without the restrictions under the General Agreement on Tariffs
ban elephant populations would continue to and Trade (GATT). The exceptions allowable under
246 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Article XX of the GATT, along with the Sanitary and public goods and biodiversity externalities. The
Phytosanitary (SPS) Agreement, authorizes countries second is the problem of international market failure,
to impose restrictions on trade in order to protect and is associated with the global public good pro-
human, animal and plant life. The evidence on the use tected by the international conservation effort and
of Article XX and the SPS Agreement provides some with the externalities of international trade. Both
support for the notion that low-income countries do require the development of incentives to decision-
not, in general, use environmental measures to restrict makers to take the full costs of their actions into
trade. Both Article XX and the SPS Agreement have consideration, institutions for the regulation of
been successfully invoked in many circumstances. For access to biological resources, and an appropriate
example, in 1995–97 there were 724 measures notified financial mechanism. The incentive problem has two
under the SPS Agreement. Of these, 55 per cent were elements. One is the generation of the correct
notified by high-income countries, 42 per cent by incentives for the socially optimal use of biodiver-
middle-income countries, and only 2 per cent by low- sity. The other is the discouragement of perverse
income countries (UNEP, 1999). incentives that work against this. The use of incen-
Despite Article XX and the SPS agreement, it is tives to protect local public goods necessarily oper-
generally argued that the WTO is not the place to ates at the local level, where the millions of foresters,
deal with the environmental effects of trade farmers, hunters, harvesters, herders, and fishers use
(Bhagwati 2000, Barrett 2000). This has led to environmental resources on a daily basis. It implies a
growing pressure for the establishment of an envi- package of direct incentives (taxes, subsidies, grants,
ronmental analogue to the WTO – either a World compensation payments, user fees, and charges),
Environment Organization (WEO) (Whalley and indirect incentives (via fiscal, social, and environ-
Zissimos 2000) or a Global Environment Organi- mental policies), and disincentives (prosecution
zation (GEO) (Runge 2001). It is interesting that the leading to fines and other penalties).
case for such an organization rests first and fore- Up to now the newer market-like mechanisms have
most on the fact that there is no other effective way emerged in areas where the capturable benefits are
of dealing with global environmental externalities. largest. The most direct attempts to do this involve the
It is thought that a WEO/GEO could create new widening and deepening of markets for individual
international markets for the global environmental biological resources. Amongst the best-known
benefits of local conservation effort. Existing exam- examples concern the markets for forest-based
ples of this, including joint implementation, biopros- pharmaceutical products. Bioprospecting contracts
pecting contracts, debt-for-nature swaps, and between individual pharmaceutical companies and
transferable development rights, are first steps developing countries, such as that between MERCK
towards the creation of global markets for environ- and INBIO in Costa Rica, have received a great deal of
mental benefits. The alternatives to date – multilateral publicity. They seek to mobilize investment in biodi-
environmental agreements – have been piecemeal, versity conservation by offering access to genetic
and have generally failed to address the important resources, protected by the assignment of intellectual
issues of compensation and penalties for non- property in genetic ‘discoveries’ (Schulz and Barbier
compliance. While agreements involving small num- 1997). Although they are very well known, however,
bers of parties concerned with specific issues have such contracts are not at all widespread, and have not
been reasonably effective, the framework agreements generally yielded competitive rates of return (Barbier
involving much larger numbers of parties have been and Aylward 1996, Simpson et al. 1996, Pearce et al.
less effective (Barrett 1994, Barrett 2003). 1999, Dedeurwaerdere et al. 2007).
A second set of markets offer biodiversity con-
servation benefits as a side-effect (an externality) of
17.7 Concluding remarks
markets for unrelated effects. Joint implementation,
The socially optimal use of biodiversity requires two or carbon offset arrangements, are promoted by the
problems to be solved. The first is the problem of UN Framework Convention on Climate Change
local market failure, and is associated with the local (FCCC). The arrangements allow one country – a
 THE ECONOMICS OF BIODIVERSITY AND ECOSYSTEM SERVICES 247

high-income country – to meet its carbon emission destroy, or at least not sufficiently to protect, bio-
targets under the Convention by investing in the diversity. The remedy to this problem is to design
reduction of carbon emissions or the sequestration of governance mechanisms and incentives that
carbon in another country. The high-income country encourage individuals to protect the common good,
gains from the lower costs of reducing carbon and to implement these incentives at all relevant
emissions or sequestering carbon in the low-income scales through suitable policies, institutions, and
country. The low-income country gains from the financial mechanisms. A number of working
additional investment. Most joint implementation examples of this approach already exist. They
projects refer to improvements in energy efficiency demonstrate its potential to improve the state of
along with investment in renewable energy or fuel biodiversity and ecosystem services, and through
switching. They do include some projects involving that, to enhance human wellbeing.
forest conservation and reforestation. However, the Recent work in the field of ecological economics
link between joint implementation and biodiversity shows that stability adds additional economic value
conservation remains tenuous. to ecosystem services in the form of insurance
In conclusion, people’s ability to maintain critical (Chapter 17), further underlining the importance of a
flows of ecosystem services are being lost because thorough understanding of the effect of biodiversity
individual decision-makers have an incentive to on ecosystem functioning and associated services.
 CHAPTER 18

The valuation of ecosystem services

Edward B. Barbier, Stefan Baumgärtner, Kanchan Chopra,
Christopher Costello, Anantha Duraiappah, Rashid Hassan,
Ann P. Kinzig, Markus Lehman, Unai Pascual, Stephen Polasky,
and Charles Perrings

18.1 Ecosystem services after the

their production or consumption, those prices bear
Millennium Ecosystem Assessment
some relation to the scarcity of resources.
The Millennium Ecosystem Assessment (2005b) The second category, cultural services, is similarly
has fundamentally changed the way in which sci- quite familiar. These services include a range of
entists are thinking about the value of ecosystems. largely non-consumptive uses of the environment,
By harnessing recent results on the relationship and reflect the fact that the diversity of ecosystems is
between biodiversity and ecosystem functioning to mirrored in the diversity of human cultures. Cultural
an assessment of the valued services that people services include the spiritual, religious, aesthetic, and
obtain from the natural environment, the Millen- inspirational wellbeing that people derive from the
nium Ecosystem Assessment has brought the anal- ‘natural’ world around them. They include the sense
ysis of ecosystems into the domain of economics. of place that people have, as well as the totemic
Ecosystem services are defined by the Millennium importance of particular landscapes and species.
Ecosystem Assessment as the benefits that people More importantly, they include (traditional and sci-
obtain from ecosystems. Since the value of any asset entific) information, awareness, and understanding
is simply the discounted stream of benefits that are of ecosystems and their individual components
obtained from that asset, the benefit streams associ- offered by functioning ecosystems. Some cultural
ated with ecosystem services may be used to esti- services, such as ecotourism, are offered through
mate the value of the underlying ecological assets. well-developed markets. Others are not. Many cul-
Those assets are not the traditional stocks of resource tural services are still regulated by custom and
economics – minerals, water, timber, and so on – but usage, or by traditional taboos, rights, and obliga-
the systems that yield flows of such things. tions. Nevertheless, they are directly used by people,
The Millennium Ecosystem Assessment (2005b) and so are amenable to valuation by methods
distinguishes four broad benefit streams: provi- designed to reveal people’s preferences.
sioning services, cultural services, supporting ser- The category of support services captures the
vices, and regulating services. The first of these is main ecosystem processes that underpin all other
the most familiar. Provisioning services cover the services. Examples offered by the Millennium Eco-
renewable resources that have been the focus of system Assessment include soil formation, photo-
much work in environmental and resource eco- synthesis, primary production, and nutrient,
nomics, including foods, fibres, fuels, water, bio- carbon, and water cycling. These services play out
chemicals, medicines, pharmaceuticals, and genetic at quite different spatial and temporal scales. For
material. Many of these products are directly con- example, nutrient cycling involves the maintenance
sumed, and are subject to reasonably well-defined of the roughly twenty nutrients essential for life, in
property rights. They are priced in the market, and different concentrations in different parts of the
even though there may be important externalities in system. It is often localized, and is therefore at least

248
 THE VALUATION OF ECOSYSTEM SERVICES 249

partially captured by the price of the land on which be maintained over time, and since capital includes
it takes place. Carbon cycling, on the other hand, produced, human, and natural capital, it is impor-
operates at a global scale, and is very poorly tant to understand how the value of ecosystems
reflected in any set of prices, although carbon may be changing relative to the value of other
markets are now in development. Since many of capital stocks.
these services are, in a sense, embedded in the other
services, they are frequently captured in the
18.2 The value of ecosystems
valuation of those services.
The final set of ecosystem services identified by In what follows, value is understood to mean eco-
the Millennium Ecosystem Assessment is the set of nomic value. According to a classic definition,
regulating services. These include air quality regu- economics is the science which studies human
lation, climate regulation, hydrological regulation, behaviour with regard to the satisfaction of human
erosion regulation or soil stabilization, water puri- needs and wants from scarce resources that have
fication and waste treatment, disease regulation, alternative uses (Robbins 1932, p. 15). That is, the
pest regulation, and natural hazard regulation. economic value of an asset lies in its instrumental
There is a rich and rapidly growing literature on the role in attaining human goals. The goal may be
services identified by the Millennium Ecosystem spiritual enlightenment, aesthetic pleasure, or the
Assessment. Interested readers will find many ways production of some marketed commodity. It does
into this literature through the references cited not matter. What matters is that there is a relation
below. However, it is quite uneven. There are many between the state of ecosystems and human well-
more studies of the provisioning and cultural ser- being. We do not therefore discuss what some
vices than of the regulating services. As a result we scientists refer to as intrinsic value, or value inde-
pay special attention to this topic. The regulating pendent of human wellbeing. This concept is gen-
services affect the impact of stresses and shocks to erally used very loosely as a way of trumping
the system. Some – such as climate or disease reg- arguments based on anthropocentric values – or
ulation – are global public goods. Many are local denying the trade-offs that people are willing to
public goods (Perrings and Gadgil 2003). That is, make between conservation and other objectives.
they offer non-exclusive and non-rival benefits to Instead, we focus on the values generated by the
particular communities. The rest of the world may preferences of the many individuals in the economy
have minimal interest in such benefits. The fact that acting both independently and in concert.
they are public goods means that, if left to the Value is not an inherent property of an asset.
market, they will be undersupplied. But they will Rather, it is attributed by economic agents through
be supplied at some level. Indeed, the greater the their willingness to pay for the services that flow
local benefits to the provision of environmental from the asset. This depends partly on the objective
public goods, the greater will be the local invest- (e.g. physical or ecological) properties of the asset,
ment in their provision. but also on the socio-economic context in which
While the Millennium Ecosystem Assessment valuation takes place – on human preferences,
offers a useful way into the problem for economists, institutions, culture, and so on. It accordingly
many others still have difficulty both with the reflects the current level of consumption of all
notion that species have finite value, and with the goods, current preferences, the current distribution
fact that people routinely trade off ecosystems ser- of income and wealth, the current state of the nat-
vices. In this chapter we discuss the value of eco- ural environment, current production technology,
systems and ecosystem services. We identify the and current expectations about the future – irre-
main methods for valuing different types of eco- spective of whether we would think of this state of
system service, and the role of valuation in devel- the world as being good or bad. Economic value is
oping sustainability indicators. The sustainability of also a marginal concept: it refers to the impact of
economic development requires that the value of small changes in the state of the world, and not the
the assets or capital stocks supporting development state of the world itself. In summary, the value of
250 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

ecological assets, like the value of other assets, is Woodward and Wui 2001). The Millennium Ecosys-
instrumental, anthropocentric, individual-based tem Assessment (2005b) itself had great difficulty in
and subjective, context dependent, marginal, and attaching values to the observed changes in physical
state-dependent (Goulder and Kennedy 1997, magnitudes.
Nunes and van den Bergh 2001, Baumgärtner 2006, One reason for this is that most ecosystem ser-
Baumgärtner et al. 2006). vices are the result of a complex interaction
The value of ecosystems derives from the services – between natural cycles operating over a wide range
the discounted stream of benefits – they produce. So, of space and time-scales (Daily 1997). Waste dis-
if Bt denotes the social benefits from the set of all posal, for example, depends both on highly local-
services provided by an ecosystem at time t, then the ized life cycles of bacteria and the global cycles of
present social value of that system is simply: carbon and nitrogen. Yet information on much of
this is scarce. Many valuation studies depend on
Ra
V0 ¼ 0
edt Bt dt elicitation of the preferences of people for ecosys-
tem stocks, when they have little information on the
where d is the social rate of discount. Bt is a measure role of those stocks in the generation of ecosystem
of society’s willingness to pay for that set of bene- services, or of the link between ecosystem services
fits. Resources only have value if they are scarce: i.e. and the production of commodities (Winkler
if they have an opportunity cost – if obtaining an 2006a). In fact, although the relationship between
additional unit of the resource implies that some- biodiversity and ecosystem functioning may be
thing else must be given up. What makes ecological well understood, the current state of ecological
resources special is that whereas the services from knowledge is frequently insufficient to link biodi-
most assets in an economy are marketed, the ser- versity and ecosystem functioning to the provision
vices yielded by ecosystems generally are not. If the of ecosystem services, or specific benefit streams. In
aggregate willingness to pay for these benefits, is other words, we may not understand ecosystem
not revealed through market outcomes, then effi- ‘production functions’ well enough to quantify how
cient management of such ecosystem services much service is produced, or how changes in eco-
requires explicit methods to measure its social value system condition or function will translate into
(e.g. see Freeman 2003, Heal et al. 2005, Just et al. changes in amounts of ecosystem services produced
2004). Indeed, the failure to take account of the (Daily et al. 1997).
value of non-marketed ecological services is one The central issue here is that ecosystems and the
reason for excessive land conversion, habitat frag- services they provide are, for the most part, inter-
mentation, and pollution in aquatic and land-based mediate inputs into the goods and services that
food systems. enter final demand – that satisfy people’s various
Although there are reasonable estimates of the desires. Intermediate inputs are those used to pro-
value of many provisioning services – where mar- duce the inputs that lead directly to economically
kets are most well-developed – there are few reli- valued goods or services. The value of intermediate
able estimates of the value of most cultural services inputs derives from the value of those goods and
and all regulating services. A number of studies services. The directness with which ecosystem
prior to the Millennium Ecosystem Assessment stocks are used is reflected in a literature that has
drew attention to the changes in ecosystem services sought to decompose total economic value into its
and the importance of quantifying the value of constituent parts (Pearce 1993, Turner 1999). In this
these changes to human societies in terrestrial (e.g. literature ‘use value’ normally comprises benefits
Daily et al. 1997, Daily 1997), marine (e.g. Duarte deriving from consumptive or non-consumptive
2000) and agroecosystems (Björklund et al. 1999). use by the individual, while ‘non-use value’
However, attempts to value these services at an comprises benefits from consumptive or non-
aggregate level have generally been seen as prob- consumptive use by others (Krutilla 1967, Weisbrod
lematic (Costanza et al. 1997, Bolund and Huhammar 1964). This includes, for example, the benefits
1999, Norberg 1999, Limburg and Folke 1999, stemming from the ethical, spiritual, or religious
 THE VALUATION OF ECOSYSTEM SERVICES 251

desire to conserve biodiversity for future genera- specific ecosystems to ask whether conservation or
tions of humans, or for other species. Direct use development options generate greater value. Their
value includes consumptive use, e.g. as food, fuel- study shows that conservation options are pre-
wood, or medicinal plants; productive use, e.g. as ferred, often by wide margins. Earlier work by
industrial resources, fuel, or construction material; Peters et al. (1989) reached a similar conclusion on
and non-consumptive use, e.g. recreation, tourism, conserving tropical forests. However, much of the
science and education. Indirect use value captures the work to date on ecosystem services requires making
derived demand for ecosystem stocks via ecosystem large leaps to overcome lack of data or under-
services (Barbier 1994, Hueting et al. 1998) that standing. Much greater understanding of ecosystem
contribute to human wellbeing. Examples include functioning, how these functions change with man-
the support of biological productivity in agro- agement actions, and how such changes impact on
ecosystems, climate regulation, maintenance of soil human values, is required before firm conclusions
fertility, control of water runoff, and cleansing of can be reached.
water and air.
Even if an ecosystem (or component of it) has no
18.3 The valuation of provisioning
current use, it may have an option value. For
and cultural services
example, the future may bring human diseases or
agricultural pests which are still unknown today. As a recent report from the US National Academy of
Today’s biodiversity would then have an option Science puts it, ‘the fundamental challenge of valu-
value in so far as the variety of existing plants may ing ecosystem services lies in providing an explicit
already contain a cure against the yet unknown description and adequate assessment of the links
disease, or a biological control of the yet unknown between the structure and functions of natural sys-
pest (Heal et al. 2005, Polasky and Solow 1995, tems, the benefits (i.e. goods and services) derived
Polasky et al. 1993, Rausser and Small 2000, Simpson by humanity, and their subsequent values’ (Heal
et al. 1996, Goeschl and Swanson 2003). In this sense, et al. 2005, p. 2). In recent years substantial progress
the option value of biodiversity conservation corre- has been made by economists working with ecolo-
sponds to an insurance premium (Perrings 1995, gists and other natural scientists to improve envi-
Weitzman 2000, Baumgärtner 2007, Quaas and ronmental valuation methodologies. Table 18.1
Baumgärtner 2008) which one is willing to pay indicates that there are now various methods that
today in order to reduce the potential loss should an can be used for valuing the services derived from
adverse event – such as a human disease or an ecological regulatory and habitat functions. A dis-
agricultural pest – occur in the future. cussion of these methods and their application to
Amongst non-use values, the same literature valuing ecosystem services can be found in Freeman
identifies vicarious use value (Watson et al. 1995) (2003), Pagiola et al. (2004), and Heal et al. (2005).
bequest value and existence value (Krutilla 1967). The For provisioning services (e.g. food, fuel, fibre,
first two derive from people’s altruistic willingness to and fresh water production), functions of agrobio-
pay (or to forgo benefits) to ensure that other mem- diversity are better understood than for supporting
bers of the present generation or future generations (e.g. nutrient cycling and soil formation) and regu-
can enjoy the benefits from ecosystems. Existence lating (e.g. climate, flooding, disease regulation, or
value, originally defined as people’s willingness to water purification) services that usually involve
pay (or to forgo benefits) to ensure the continued assemblages of species and guilds, each with a
existence of biodiversity irrespective of any actual or complex set of functions and interactions (Millen-
potential use by present or future generations of nium Ecosystem Assessment, 2005b). Where there
humans, may be seen as a form of altruism towards are prices for the outputs of activities, as is the case
non-human species or nature in general, and, in most with many provisioning services, then derived
cases, rests on ethical or religious motives. demand methods are appropriate – and there are a
Note that final use includes conservation. For growing number of studies that use such an
example, Balmford et al. (2002) used studies of approach (e.g. Barbier 2000, Matete and Hassan
252 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Table 18.1 Valuation methods applied to ecosystem services.

Valuation Types of value

methoda estimatedb Common types of applications Ecosystem services valued

Travel cost Direct use Recreation Maintenance of beneficial species, productive ecosystems
and biodiversity
Averting Direct use Environmental impacts on human health Pollution control and detoxification
behaviour
Hedonic price Direct and indirect Environmental impacts on residential property Storm protection; flood mitigation; maintenance of air
use and human morbidity and mortality quality
Production Indirect use Commercial and recreational fishing; agricultural Maintenance of beneficial species; maintenance of arable
function systems; control of invasive species; watershed land and agricultural productivity; prevention of damage
protection; damage costs avoided from erosion and siltation; groundwater recharge;
drainage and natural irrigation; storm protection; flood
mitigation
Replacement Indirect use Damage costs avoided; freshwater supply Drainage and natural irrigation; storm protection; flood
cost mitigation
Stated Use and non-use Recreation; environmental impacts on human All of the above
preference health and residential property; damage costs
avoided; existence and bequest values of
preserving ecosystems
Notes:
a
See Freeman (2003), Heal et al. (2005), and Pagiola et al. (2004) for more discussion of these various valuation methods and their application to valuing ecosystem
goods and services.
b
Typically, use values involve some human ‘interaction’ with the environment whereas non-use values do not, as they represent an individual valuing the pure
‘existence’ of a natural habitat or ecosystem or wanting to ‘bequest’ it to future generations. Direct use values refer to both consumptive and non-consumptive uses that
involve some form of direct physical interaction with environmental goods and services, such as recreational activities, resource harvesting, drinking clean water, breathing
unpolluted air and so forth. Indirect use values refer to those ecosystem services whose values can only be measured indirectly, since they are derived from supporting and
protecting activities that have directly measurable values.
Source: Barbier (2007), Table 2.

2006). Some of the most successful efforts to estimate New York City from watersheds in the Catskills.
the values of ecosystem services have focused on the Increased housing development with septic sys-
production of specific tangible outputs, such as the tems, runoff from roads, and agriculture were
production of fish and game species. Such outputs causing water quality to decline. Continued
tend to be readily measurable and frequently have declines in water quality would have forced the US
market prices (e.g. commercially harvested fish). Environmental Protection Agency to require New
The ecosystem (habitat) is a necessary input into the York City to build a water filtration plant. The total
production of the output (species). Focusing on the present value cost of building and operating the
input side, such work naturally fits into a classifi- water filtration plant was estimated to be roughly
cation of ecosystem services. One can just as easily $6–8 billion (Chilchilnisky and Heal 1998). Instead,
focus on the output side, however, in which case New York City decided to invest $1 to 1.5 billion to
such studies are best considered as studies of the conserve the Catskills watersheds to avoid building
values of individual species. Some research in eco- the water filtration plant. The value of the ecosys-
nomics has focused on how changes in ecosystem tem service here is the saving provided by avoided
conditions translate into changes in the value of cost – the cost of replacing the ecosystem service
output (e.g. Brown and Hammack 1974, Lynne et al. with some engineered alternative.
1981, Ellis and Fisher 1987, Swallow 1990). Market price-based ‘dose–response’ analysis is
One widely cited example of this approach another example of this approach. While ecosys-
relates to the provision of clean drinking water for tems may not be priced in the market, the
 THE VALUATION OF ECOSYSTEM SERVICES 253

commodities produced using ecosystems are. stated preference surveys – how changes in ecosys-
Hence, by directly relating the provision of the tem processes and components affect ecosystem
input to the level of the market output, it is possible regulatory and habitat functions and thus the spe-
to derive the financial returns provided by biodi- cific benefits arising from these functions that indi-
versity. For example, Ricketts et al. (2004) found viduals value. Since there is considerable scientific
that the pollination contributes 7 per cent of total uncertainty surrounding these linkages, is it difficult
farm income to coffee producers in Costa Rica (in not only to construct such scenarios but also to elicit
2002–03 when coffee prices were depressed). responses from individuals that accurately measure
Travel cost. Where there are no prices for the their willingness to pay for ecological services.
outputs, as is the case with many cultural services, Production function methods. Whatever the method
other methods are necessary. Many methods are used to value willingness to pay for provisioning or
specific to particular types of ecosystem services. cultural services, the value of the ecosystems that
So, for example, the travel cost method applies support those services can be obtained through the
primarily to the value derived from recreation and production function approaches. For many habitats
tourism, averting behaviour models are best where there is sufficient scientific knowledge of
applied to the health effects arising from environ- how these link to specific ecological services that
mental pollution and hedonic wage and property support or protect economic activities, it is possible
models are used primarily for assessing work- to employ the production function approach to
related environmental hazards and environmental value these services. The basic modelling approach
impacts on property values, respectively. underlying production function methods, also
Contingent valuation. The most widely used class of called ‘valuing the environment as input’, is similar
methods for estimating willingness to pay for cultural to determining the additional value of a change in
services are ‘stated preference methods’. These the supply of any factor input (Barbier 1994, 2000,
include contingent valuation, conjoint analysis and 2007, Freeman 2003). If changes in the regulatory
choice experiments. These valuation methods share a and habitat functions of ecosystems affect the
common approach with market research in that they marketed production activities of an economy, then
survey individuals who benefit from an ecological the effects of these changes will be transmitted to
service or range of services to elicit their willingness individuals through the price system via changes in
to pay for those services. They are flexible enough to the costs and prices of final good and services. This
include non-consumptive uses (Carson et al. 1996). means that any resulting ‘improvements in the
Similarly, choice experiments and conjoint analysis, resource base or environmental quality’ as a result
which ask respondents to rank, rate, or choose among of enhanced ecosystem services, ‘lower costs and
various environmental outcomes or scenarios, have prices and increase the quantities of marketed
the potential to elicit the relative values that indivi- goods, leading to increases in consumers’ and per-
duals place on different ecosystem services (see for haps producers’ surpluses’ (Freeman 2003, p. 259).
example Carlsson et al. 2003). An adaptation of the production function meth-
However, implementation of stated preference odology is required in the case where ecological
methods requires that two key conditions be met: (1) regulatory and habitat functions have a protective
the information must be available to describe the value, through various ecological services such as
change in a natural ecosystem in terms of service storm protection, flood mitigation, prevention of
that people care about, in order to place a value on erosion and siltation, pollution control, and main-
those services; and (2) the change in the natural tenance of beneficial species (Table 18.1). In such
ecosystem must be explained in the survey instru- cases, the environment may be thought of produc-
ment in a manner that people will understand (Heal ing a non-marketed service, such as ‘protection’ of
et al. 2005). For many ecosystem services, one or both economic activity, property, and even human lives,
of these conditions may not hold. For instance, it has which benefits individuals through limiting dama-
proven very difficult to describe accurately – ges. Applying production function approaches
through the hypothetical scenarios required by requires modelling the ‘production’ of this
254 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Box 18.1 Linking economic and ecological values of biodiversity using simulation
modelling for Keoladeo National Park, India

Biodiversity in Keoladeo National Park is first valued using where xi is a marketed good and Li is leisure. Demand for
conventional travel cost methods. This provides a short-run leisure is given by
valuation which assumes that the ecological health of the
park is sustainable over the longer run. There is, however, DðLi Þ ¼ Vi ¼ F ðWi ; Cij ; Hp Þ
uncertainty over the impact of various exogenous forcing
factors on the state of the park. Indices of ecological health where Wi is travel cost, Cij are other costs, and Hp is the
are constructed, along with scenarios of alternative states of ecological health of the park. The latter can be
ecological health of the park over a period of 25 years. This parameterized only on the basis of medium-run or long-run
makes it possible to investigate the linkages between the time series data and modelling of the wetland
economic value of the park in its current state, and its value ecosystem. Application of the travel cost model indicates
in alternative states (Chopra and Adhikari 2004). quite low elasticities with respect to cost incurred by
The literature on economic valuation typically focuses visitors, Wi and Cij.
on use value in the short run, whether within or outside By simulating ecology–economy interactions in the
the market. Conservation biologists, on the other hand, Keoladeo National Park it was possible to estimate the
are more concerned with the underlying long-run impact of exogenous changes, such as reductions in water
conservation value of the system being studied. Chopra inflow due to development of upstream agriculture, on
and Adhikari (2004) investigate the link between these both the ecological health and economic value of the park.
two aspects of value in the context of a wetland in Specifically, the simulations were used to estimate the
Northern India. Keoladeo National Park has been effect of changes in ecological health on economic value
designated as both a Ramsar site and a national park. (direct and indirect income derived from the park). The
Assigning a value to an eco-system good or service elasticities obtained varied from 0.6 to 1.7 in two
implies an ability to define its role in increasing scenarios. However, as pressured on the system increased
human welfare, whether or not it is marketed. This and the wetland became less attractive as an ecosystem,
requires identification of (a) the physical or environmental the values of the elasticities fell, with a range from 0.04
linkages which result in the provision of the service, and to 0.124.
(b) the economic linkages which help realize the value of Given the present profile of visitors to KNP, visitation
the service. rates are not responsive to private cost. However,
Chopra and Adhikari (2004) use the travel cost method direct and indirect income obtained from the park are
to estimate tourists’ willingness to pay to visit the responsive to ecological health indices. Moreover, the
wetlands. It is assumed that household i derives utility elasticity with respect to ecological health is greater, the
from the consumption of a bundle of marketed goods, and greater the value of the index, indicating that the impact
from recreation or leisure activities: of conservation on the attractiveness of the park is
cumulative, and hence that the value of the park increases
Ui ¼ f ðx1 ; x2 ; :::; xn ; Li Þ more than proportionately.

protection service and estimating its value as an conservation of species at higher trophic levels.
environmental input in terms of the expected Specifically, they derive the implicit willingness to
damages avoided by individuals (Barbier 2006). pay for the conservation of prey species from direct
An example of the use of production functions estimates of willingness to pay for top predators.
linked to stated preferences for the cultural services They refer to this as a form of quasi-benefit transfer.
offered by totemic species is given by Allen and They make the important point that it is not neces-
Loomis (2006). Following Goulder and Kennedy sary for people to understand the trophic structure of
(1997), they use such an approach to derive the an ecosystem, since their willingness to pay for top
value of species at lower trophic levels from predators effectively captures their willingness to pay
the results of surveys of willingness to pay for the for the whole system. Economists first modelled this
 THE VALUATION OF ECOSYSTEM SERVICES 255

by assigning species the status of ‘intermediate inputs’ use of value (benefit) transfer techniques. Benefit
(Crocker and Tschirhart, 1992) due to their role transfer implies the use of value estimates for some
in supporting more other species. The same idea can ecosystem service derived from one location (or one
be generalized to say that species have value deriving set of locations) to infer the value of the same eco-
from their role in the production of valuable goods and system service at another location, the ‘policy site’.
services, and that this is conditional on the state of the This is relatively straightforward in the case of, for
environment. So, for example, the derived value of example, carbon sequestration services, where the
members of a functional group of species, each of contribution of carbon sequestration to the general
which performs differently in different environmental circulation system is independent of where it takes
conditions, will vary with those conditions. Species place (e.g. Songhen and Brown 2006). However, it
that appear to be redundant in some conditions will raises more questions where the benefits of eco-
still have value depending on the likelihood that the system services depend heavily on local conditions,
conditions in which they do have value will occur in or the characteristics of the communities that
the future (Loreau et al. 2002). It follows that the cost of exploit those services are very different – in terms
species deletion is the cost of securing the same set of of age, income, asset holdings, education, culture,
services in the conditions to which those species were and so on (Vandenberg et al. 2001, Kirchoff et al.
adapted. 1997). Given the cost of original valuation studies,
However, production function methods have the use of benefit transfer is growing rapidly, and
their own measurement issues and limitations. For economists have been investing considerable effort
instance, applying the production function method into refining procedures to extract as much infor-
raises questions about how changes in the eco- mation as possible from valuation studies of sites
logical service should be measured, whether mar- that overlap with the policy site in some dimension.
ket distortions in the final goods market are One popular approach is the use of meta-
significant, and whether current changes in eco- regression models – regression models based on a
logical services may affect future productivity range of estimates of the value of some resource at
through biological ‘stock effects’. A common different sites that are designed to estimate the
approach in the literature is to assume that an value of resources at some policy site (Rosenberger
estimate of ecosystem area may be included in the and Loomis 2000, Shrestha and Loomis 2001,
‘production function’ of marketed output as a Johnston et al. 2005, Johnston et al. 2006). Although
proxy for the ecological service input. For example, meta-analyses have been applied most frequently to
this is the standard approach adopted in coastal stated preference studies where the cost of original
habitat–fishery production function models, as research is highest, they have also been applied to
allowing wetland area to be a determinant of fish studies based on other valuation methodologies,
catch is thought by economists and ecologists to including hedonic valuation (Smith and Huang
proxy some element of the productivity contribu- 1995, Smith and Pattanayak 2002, Mrozek and
tion of this important habitat function (Barbier Taylor 2002). The adoption of Bayesian approaches
2000, 2007, Freeman 2003). A further measurement in a meta-regression framework has significantly
issue arises when stock effects need to be modelled improved their capacity to estimate a relatively
explicitly. In the production function valuation lit- large set of parameters, even when the underlying
erature, approaches that ignore stock effects are meta-sample is small (Brunsdon and Willis 2002,
referred to as ‘static models’ of environmental Layton and Levine 2005, Moeltner et al. 2007).
change on a natural resource production system, In many cases, however, biodiversity impacts are
whereas approaches that take into account the highly context specific and thus not directly gener-
intertemporal stock effects of the environmental alizable. Moreover, all such pathways can be inter-
change are referred to as ‘dynamic models’ (Barbier related or at least cannot be isolated. As a general
2000, 2007, Freeman 2003). rule, a total valuation of the potential value of eco-
Benefit transfer. An important and growing trend logical stocks should not be estimated by a piecewise
in the valuation of all environmental impacts is the independent valuation of each impact, and a
256 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

subsequent aggregation of those impacts when these overlapping functional groups of species enhances
are interrelated (Randall, 2002). For instance if a the level of functional diversity, which, in turn,
dose–response approach to the value of agrobiodi- increases ecological stability (Tilman et al. 2005) and
versity were estimated and then added to the value resilience (sensu Holling 1988). Following Carpenter
derived from farmers themselves using a stated et al. (2001), the resilience of an ecosystem is
preference technique, it is likely that the double determined primarily by: (1) the amount of distur-
counting would occur. It is important to clearly bance that the system can absorb and still remain
delineate the different services and small number of within the same state or domain of attraction; (2)
different ecosystem functions. Then different valua- the degree to which the system is capable of self-
tion techniques can be used for each function. organization versus the lack of organization, or
An example of a study that attempts to decompose organization forced by external factors, and (3) the
the value of non-marketed environmental resources degree to which the system can build and increase
in this way is Rodríguez et al.’s (2006) study of the capacity for learning and adaptation.
Opuntia scrubland in Ayacucho, Peru. Opuntia is Maintaining a wider portfolio of options in eco-
important as the host plant for cochineal insects, the systems is likely to maintain or enhance the capacity
source of carminic acid, a natural dye used in the food, to respond to short-run shocks and stresses in con-
textile, and pharmaceutical industries. However, structive and creative ways. In agro-ecological sys-
besides being an agricultural asset for the production tems, for example, various recent studies have
of the cash crop of cochineal, the Opuntia scrubland analyzed the contribution of crop diversity to the
protects slopes against erosion and flooding, as well mean and variance of agricultural yields and farm
as rehabilitating marginal lands by improving the income (Smale et al. 1998, Schläpfer et al. 2002,
levels of humidity and soil retention capabilities. Widawsky and Rozelle 1998, Di Falco and Perrings,
Additionally, Opuntia scrubs are used for animal 2003, 2005, Birol et al. 2005). The ‘option-insurance
grazing all year round and can become an emergency value’ of agrobiodiversity refers to the capacity of the
feedstock in case of drought. In addition, its fruits and agricultural system to adapt to economic or envi-
young cladodes have a considerable nutritional value ronmental external changes by either returning to its
and provide food for Andean farmers. original state, thus making the agricultural system
stable, or by evolving into a state preferable to the
initial one. Extending genetic to species diversity,
18.4 The valuation of regulating
such as multi-crop and tree biodiversity in agro-
services
ecosystems can enhance the ability of farmers to
We have already noted that the Millennium Eco- remain economically viable by diversifying their
system Assessment drew attention – for the first revenues to cope with volatile international market
time – to the value of services that regulate the price changes of inputs, crops or tree products.
Earth’s capacity to respond to environmental Whereas the homogenization of agro-ecosystems can
shocks and stresses. Given current concern for the increase yields in the short run, it is often at the cost
sustainability of environmental management strat- of increasing vulnerability to pests and pathogens.
egies, this is of fundamental importance. While This in turn increases reliance on pesticides that are
there are as yet few studies of the value of the potentially damaging to both biodiversity and
regulating services, they are likely to be essential in humans. So the cost of reducing the resilience of
the future. It is therefore also appropriate to iden- agricultural systems to cope with market (price
tify the valuation options currently being consid- fluctuations) and environmental (pests and diseases)
ered for these services. The regulating services are vagaries can be seen as the loss in ‘insurance value’
closely connected to insurance role of functional of a portfolio of species.
diversity discussed in an economic context in Two things follow. First, the regulating services
Chapter 17 and in an ecological context in Chapters of ecosystems appear to be a function of biodiver-
4 and 6. Ecologists argue that over small scales an sity, and especially of functional diversity. Second,
increase in species richness and the diversity of the value of the regulating services is a function of
 THE VALUATION OF ECOSYSTEM SERVICES 257

people’s willingness to pay for a reduction in risk. willingness to pay for the effect of a change in
Taking the first of these, results from experiments in wetland area on expected damages from coastal
grassland plots (Tilman et al. 1996) and in con- storm events (Barbier 2007). This approach mea-
trolled environments (Naeem et al. 1995) found that sures willingness to pay, by measuring the total
increasing the number of species in the system expected damages, E[D(S)], resulting from the
tended to increase system productivity. Similar change in ecosystem stocks. The approach assumes
results were reported by Hector et al. (1999) in that the value of an asset that yields a benefit in
experiments across a number of European coun- terms of reducing the probability and severity of
tries. In heterogeneous environments, having more some economic damage is measured by the reduc-
species will generally allow the collection of species tion in the expected damage. The essential step to
to better utilize all ecological niches and so be more implementing this approach, which is to estimate
productive (the niche differentiation effect). Tilman how changes in the asset affect the probability of
et al. (1997a) develop a model of niche differentia- the damaging event occurring, has been used rou-
tion that is formally similar to the Polasky et al. tinely in risk analysis and health economics, as in
(1993) model of the probability that a set of species the case of airline safety performance (Rose 1990),
will contain a given trait. Both models show how highway fatalities (Michener and Tighe 1992), drug
coverage increases, either in niche space or genetic safety (Olson 2004), and studies of the incidence of
space, when more species are added. diseases and accident rates (Cameron and Trivedi
In sum, there remain a number of unanswered 1998, Winkelmann 2003).
questions about the production and value of eco- Barbier (2007) has shown that the EDF approach
system services. We currently lack understanding can also be applied, under certain circumstances,
of the link between management actions and to value the protection service of coastal wetlands
changes and ecosystem functioning. There remain that reduce the probability and severity of eco-
questions about the link between ecosystem func- nomic damages from natural storm disasters.
tioning and provision of ecosystem services. Two components are critical to implementing the
Finally, there remain questions about the link EDF approach to estimating the changes in
between the provision of ecosystem services and expected storm damages: the expected incidence of
value of these services to humans. Provision of economically damaging natural disaster events as
valuable ecosystem services may ultimately prove a function of wetland area, and some measure of
to be the most important reason to conserve bio- the additional economic damage incurred per
diversity. At present, however, it is hard to know event. Provided that there are sufficient data on
with any precision either the benefits of the provi- the incidence of past natural disasters and
sion of ecosystem services or the opportunity costs changes in wetland area in coastal regions, the
involved in ensuring their continued provision. marginal impact of wetland area on expected
A promising alternative is the expected damage storm damage can be estimated using a count data
function (EDF) approach to estimating the total model (see Box 18.2).

Box 18.2 The value of mangrove storm buffering

In the wake of the 26 December 2004 Asian tsunami, example, Indonesia has promised to spend $22 million on
there have been widespread calls by governments, NGOs, mangrove restoration and has already planted 300,000
and local communities to restore coastal mangrove forests seedlings in Aceh Province. Malaysia is planning to spend
and recover one of their putative ‘ecosystem functions’ – $25 million on rehabilitating 4,000 hectares of mangrove
the protection of low-lying coastal communities from area that has been deforested, and the state government
recurrent storm surges and unpredictable tsunamis. For of Kerala in India pledged $8 million for mangrove

Continues
258 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Box 18.2 (Continued ) wood for lumber, pulp (for rayon), fuel, and
restoration (Check 2005). The governments of charcoal production; construction within forests of housing
Sri Lanka and Thailand have also stated publicly their and ‘eco-resorts’; and outright neglect. Thus, while the
intentions to rehabilitate and replant large decision by many Asian governments in the wake of the
mangrove areas (Harakunarak and Aksornkoae 2005, tsunami to invest in mangrove replanting and restoration is
UNEP 2005). laudable, there are few intact, unfragmented mangrove
The rationale for these restoration schemes is the forests available to use as reference states for successful
growing evidence that mangroves, marshlands and other restoration efforts.
natural barriers are critical components to the overall Because of the lack of data on how this service arises
‘resilience’ of coastal areas to threats posed by tsunamis, from natural mangrove systems and how changes in these
hurricanes, and other natural disasters (Adger et al. 2005). systems translate into increased risk of damage from storm
In the case of mangroves, the scientific evidence is now events, the few valuation studies of coastal protection have
well documented. Mangroves are forested wetlands that used the ‘replacement cost’ method (Chong 2005). This
grow along sheltered tropical and subtropical shores and involves using estimates of the cost of ‘replacing’
estuaries. They attenuate wave amplitude and are thought mangroves with human-built alternatives, such as storm
to be particularly valuable in minimizing damage to walls and other artificial barriers, as approximations of the
property and loss of human life by acting as natural barriers value of the coastal protection service. Such estimates
against tropical cyclonic storms and tsunamis (Chong 2005, not only make the methodological error of estimating a
Massel et al. 1999, Mazda et al. 1997). Evidence from the ‘benefit’ by a ‘cost’ (thus always assuming a unitary
aftermath of the 2004 Asian tsunami suggests that those benefit–cost ratio) but also tend to yield unrealistically
coastal areas that had dense mangrove forests closer to high estimates because removing all the mangroves and
pristine conditions suffered fewer losses and less damage replacing them with constructed barriers is unlikely to
to property than those areas in which mangroves had been be the least-cost alternative to providing storm
degraded or converted to other land uses (Dahdouh- prevention and flood mitigation services in any coastal area
Guebas et al. 2005c, Danielsen et al. 2005, Kathiresan and (Heal et al. 2005).
Rajendran 2005, UNEP 2005, Dahdouh-Guebas and Barbier (2007) has demonstrated the use of the
Koedam 2006). expected damage function (EDF) method as a preferred
Mangrove forests are among the most threatened alternative to the replacement cost approach in valuing the
global ecosystems. At least 35 per cent of global storm buffer service of mangroves. Over the 1996 to 2004
mangrove area has been lost in the past two decades, and period, one estimate suggests that in Thailand mangrove
in Asia, 36 per cent of mangrove area has been deforestation was 3.44 km2 annually. Using the
deforested, at the rate of ~1.5 per cent per year replacement cost method, which assumes that the
(Farnsworth and Ellison 1997, Valiela et al. 2001). Such equivalent cost of protecting the shoreline with a 75 m
widespread mangrove deforestation is believed to have width stand of mangrove is approximately US$116,667
increased the vulnerability of coastal areas and their per ha (1996 prices), Barbier calculates an annual welfare
inhabitants to the economic damages caused by natural loss of over $4.2 million in the storm protection service
disasters. Large-scale replanting and restoration of associated with that deforestation. This is equivalent to a
mangrove forest ecosystems as ‘green shelterbelts’ is net present value (10 per cent discount rate) of $24.3
therefore seen as an important solution to providing million over the entire 1996–2004 period. In comparison,
adequate protection to coastlines exposed by extensive the EDF approach estimates an annual welfare loss in
mangrove loss. storm protection of just over $0.6 million, and a net
All mangrove forests are not identical, however. As one present value (10 per cent discount rate) of $3.7 million over
post-tsunami assessment concluded, ‘mangroves play a 1996–2004. The Thailand case study confirms that the
critical role in storm protection, but with the subtle point replacement cost method tends to produce extremely high
that this all depends on the quality of the mangrove estimates – almost 8 times greater than the estimate
forest’ (Dahdouh-Guebas et al. 2005c, p. 446). The provided by the EDF approach. This suggests that the
world’s remaining mangrove forests have been replacement cost method should be used with caution, and
fragmented, degraded, and mismanaged by over a century when data are available, the expected damage function
of small-scale conversion of forests to aquaculture approach may provide more reliable values of the storm
(notably tiger-prawn farms); unsustainable harvesting of protection service of coastal wetlands such as mangroves.
 THE VALUATION OF ECOSYSTEM SERVICES 259

18.5 Valuation of ecosystem assets Currently, most estimates of NNP still exclude
and national sustainability indicators depreciation of environmental capital. Moreover,
The dominant economic approach to oper- although they include transboundary flows,
ationalizing sustainability is the capital approach. they exclude transboundary environmental flows.
It requires that the value of a nation’s inclusive Since the capital stock that supports the flow
wealth or aggregate capital stock is non-declining. of services includes the ecosystems that are at the core
This is also implicit in the basic definition of of natural capital, and since environmental impacts
income: the maximum amount that can be spent involve transboundary effects, current NNP estimates
on consumption in one period without reducing are not adequate measures of sustainability. To make
real consumption expenditure in future periods NNP estimates an adequate measure of sustainability
(Hicks 1939). Conventional macroeconomic requires that it include a measure of the change in the
income indicators like gross domestic product aggregate capital stock – sometimes called inclusive
(GDP) are not suitable for assessing sustainability wealth.
as they do not adequately consider human and The World Bank’s adjusted net savings indicator
natural capital. Attempts to find better sustain- is a direct attempt to measure net change in the
ability indicators include the United Nations value of a country’s capital stocks, where that
Development Program’s Human Development includes both natural and human capital (Hamilton
Index (HDI), which adds proxies for human capi- and Clemens 1999). Dasgupta (2001) has developed
tal but is otherwise still based on GDP. Life the same idea, calling it genuine investment. It is a
expectancy at birth tells us something about the measure of the change in a country’s wealth, where
period over which we might expect people to be wealth includes not just produced capital, but also
productive, while adult literacy tells us something human capital (including the stock of knowledge)
about the average skill levels. But neither indicator and natural capital. If wealth is defined as the value
tells us about the depreciation of human capital, of the stock of all assets at some time, Vt, plus net
nor do they tell us anything about the balance investment at that time, dVt/dt, it follows that a
between depreciation and investment in human necessary and sufficient condition for wealth to be
capital. More importantly, the HDI tells us nothing increasing over time is that dVt/dt > 0. If the
more about the rate of change in the value of population is growing, then the appropriate mea-
natural capital than we get from GDP. sure of sustainability is the rate of change in per
The same requirement is explicit in the invest- capita wealth. Using preliminary estimates of
ment rule identified by Hartwick (1977, 1978) and Adjusted Net Savings, Dasgupta (2001) showed
Solow (1986) to satisfy the sustainability criterion that the average annual change in per capita wealth
proposed by Solow (1974). The rule reflects the fact in Sub-Saharan Africa over the period 1970–93 was
that a necessary condition for consumption based –3.4 per cent. This means that average wealth in
on the exploitation of natural resources to be sus- Sub-Saharan Africa in 1993 was only half what it
tainable is that investment be maintained at a level had been just twenty years earlier. This was partly a
that at least compensates for the depletion of those function of population growth, but it was also
resources. Current measures of net product, NDP because of a systematic ‘decumulation’ of all forms
and NNP, address the issue of depreciation of of capital. The implication is that millions of people
capital and so are to be preferred to measures of in Africa were dissaving to maintain consumption,
gross product. Similarly, measures of national often by running down environmental assets held
product, GNP and NNP, address transboundary in common property.
flows, and so are to be preferred to measures of More narrowly focused attempts to develop
domestic product. The most inclusive of all of these resource accounts at the country level show that
measures is therefore NNP. One starting point for conditions are far from uniform in Sub-Saharan
the development of improved economic sustain- Africa. The value of at least some components of
ability indicators is therefore the improvement of natural capital have been augmented in some
measures of NNP (Perrings and Vincent 2003). countries (see Hassan 2003; Box 18.3). Nevertheless,
260 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Box 18.3 Measuring net change in forest and woodland asset values in South Africa

The total contribution of forest and woodland resources to applied (Hulkrantz, 1992). As no attempt has been made in
production in South Africa, measured as value added, South Africa to estimate carbon values, the present study
amounted to R6,215 million in 1998 prices (Table 1). could only borrow and adapt estimates from other parts of
This included values already accounted for as well as values the world. Figures used in the literature to value carbon
currently missing from the SNA. Of the total value of covered a very wide range between US$5 to US$130 per ton
R6,215 million, 59 per cent came from natural forests and of C. If one uses Nordhaus’s (1994) estimate of 1 per cent of
woodlands and 26 per cent from cultivated plantations, GDP as the climate change damage cost, this will come to
while 15 per cent was contributed by fynbos. Consumptive the equivalent of US$9 per ton of C for SA at 1995 prices.
use value was the single largest component of total VAD, The fact that CO2 contributes about 60 per cent of total
accounting for 73 per cent of the total economic greenhouse gas emissions in South Africa (Rowlands 1996,
contributions of forest and woodland resources, most of Scholes and van der Merwe 1995) leads to a carbon value of
which is generated by natural forests and woodlands (59 $5.4/ton for South Africa at 1995 prices. This is comparable
per cent). Direct consumptive use activities in cultivated to Nordhaus’s (1994) global estimate of $5.2/ton of C in
plantations consist of commercial logging as no other direct 1994, and is used estimate to value carbon stocks in
use benefits were reported for this forest resource type. both cultivated plantations and natural forests and
Carbon stocks: While net change in the physical stock of woodlands.
carbon stored in forest and woodland resources is not difficult Derived asset values were used to calculate estimates of
to measure (usually proportional to timber volumes), asset depletion (or net accumulation). The change in assets’
establishing a value per unit of C released or sequestered is values indicates that the physical stocks and values of
the most difficult task in the valuation exercise. The common timber assets have been appreciating (net addition) in the
practice in the literature is to use global value estimates such case of cultivated plantations and natural forests and
as those generated by climate change impact models woodlands. The reverse however, is true for fynbos
(Nordhaus 1994). In countries where an environmental resources (net depletion). Net accumulation (depletion) of
carbon charge is levied, such as Sweden, the used charge is asset values in this case is derived simply as the difference

Table 1 Flow benefits of F&WLR resources in South Africa (Rm, 1998 prices).

Types of Values Cultivated forest Natural woodlands Fynbos Total Percent of total
a
Direct consumptive use values 1856 2613 79 4584 73.1%
Direct non-consumptive use valuesb NAPd NAVe 29 29 0.5%

Indirect use values 225 1021 799 1595 25.7%

Water 225 NAP NAP 225 3.6%
Honey and pollination NAP NAV 786 786 12.7%
Livestock grazing NAP 1021 13 1034 16.6%

Non-use valuesc NAV NAV 43 43 0.7%

Total value added (VAD) 1631 3634 950 6215 100%

Percent of total VAD 26.2% 58.5% 15.3% 100%

a.
Tangible timber and non-timber products for final consumption or intermediate use.
b.
Intangible forest amenities, e.g. recreation.
c.
Option and existence values
d.
Not applicable (the sector's contribution to such values is insignificantly small).
e.
Not available, indicating that the value of such services has not been estimated.

Continues
 THE VALUATION OF ECOSYSTEM SERVICES 261

Box 18.3 (Continued) plantations sector. Natural forests and woodlands,

between asset values estimated for each two consecutive however, showed a total positive net accumulation
periods. (appreciation) in timber asset values of R7.09 billion,
The potential yield of pristine fynbos services is affected which amounted to more than four times the contribution
by aliens only through a reduction of the area in which the of forestry to GDP and about 21 per cent of the value
indigenous species can grow. Accordingly, a percentage added in the combined agriculture, forestry, and fisheries
decrease in fynbos yield potential proportional to the in 1998. Net annual change in carbon stocks stored in
percentage cover of aliens was calculated for each cultivated plantations was equivalent to about 7 per cent
category of alien infestation. More specifically, this meant of its officially recorded contribution to GDP in 1998.
that there is negligible change under conditions of light Natural forests and woodlands contributed about 21 per
(occasional) infestation, but that only 87.5 per cent of the cent of the recorded value added of CPLNT in 1998 in net
value remains in scattered infestations (12.5 per cent carbon stock accumulations. The net effect of alien
cover), 50 per cent in areas of medium infestation (50 per invasion of fynbos resources led to a depreciation in its
cent cover) and 12.5 per cent in densely infested areas asset value of R0.62 billion in 1998 prices, equivalent to
(87.5 per cent cover) (Turpie et al. 2001). Net 36 per cent of the recorded contribution of cultivated
accumulation in timber values of cultivated plantations in plantations to GDP. In spite of the depreciation in fynbos
1998 (R1.09 billion) amounted to 0.15 per cent of the resources, building up of timber stocks, especially in
gross domestic product (GDP), 3.2 per cent of total value natural forests and woodlands, is the main source of net
added in agriculture, forestry, and fisheries combined, and accumulation, contributing 94 per cent of the total annual
63.4 per cent of value added generated in the cultivated change in the value of F & WLR assets.

25
Adjusted net savings rate %

20
15
10
5
0
–5
Figure 18.1 Adjusted Net Savings in high-,
–10 middle-, and low-income countries and in ‘heavily
–15 indebted poor countries’, 1970–2003. Negative Adjusted
1970
1972
1974
1976
1978
1980
1982
1984
1986
1988
1990
1992
1994
1996
1998
2000
2002
2004

Net Savings indicate declining wealth. Calculated from

World Bank data at http://web.worldbank.org/WBSITE/
EXTERNAL/TOPICS/ENVIRONMENT/EXTDATASTA/0,,
High income countries
Heavily indebted poor countries (HIPC) contentMDK:20502388 isCURL:Y menuPK:2935543
Low income countries pagePK:64168445 piPK:64168309 theSitePK:
Middle income countries 2875751,00.html

the most recent estimates of adjusted net savings tribute to both material and spiritual wellbeing. The
show that many poorer countries continue to dis- valuation of ecosystem services makes it possible to
save (Figure 18.1). identify the opportunity cost of using ecological
assets in particular ways. This in turn makes it
possible to design instruments (payments for eco-
18.6 Conclusions
system services, prices, taxes, access charges,
The Millennium Ecosystem Assessment has refo- property rights, standards, and so on) for the effi-
cused our attention on ecosystems as assets. They cient allocation of those assets. Beyond estimating
are important but often poorly understood com- the social opportunity cost of ecosystem services
ponents of wealth: the source of services that con- to support assessment of alternative uses of
262 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

biodiversity, valuation serves another important depends on many factors other than their extent or
purpose. It provides a means of testing the envi- productivity, so one may not be monotonically
ronmental sustainability of anthropogenic activity. related to the other. But it is more because the work
More particularly, it provides a means of testing has not yet been done to support such an analysis.
whether human activities are leading to a reduction The adjusted net savings estimates produced by the
in the value of ecosystems. World Bank are an important step in the right
It is worth emphasizing that this is not equivalent direction, but they are as yet limited to traditional
to a reduction in the physical extent of those sys- natural resource stocks that correlate poorly to
tems, or of aggregate productivity. The Millennium ecosystems. Nevertheless, since an understanding
Ecosystem Assessment recorded trends in such of changes in the value of ecosystem stocks is cen-
physical measures in a number of systems, but was tral to an understanding of the sustainability of
unable to record trends in the value of those sys- economic development, this is work that needs to
tems. This is partly because the value of ecosystems be done.
 CHAPTER 19

Modelling biodiversity and

ecosystem services in coupled
ecological–economic systems
William A. Brock, David Finnoff, Ann P. Kinzig, Unai Pascual,
Charles Perrings, John Tschirhart, and Anastasios Xepapadeas

19.1 Introduction tion of ecosystems in ‘close to natural’ states, and the

exploitation of ecosystems to produce foods, fuels,
Many of the changes in biodiversity and ecosystem
and fibres. The more general model involves the
services described in this volume are the result of
management of ecosystems to achieve a balance
anthropogenic factors: the direct and indirect
between a range of services. More particularly, the
impacts of human decisions about the conservation
first case encompasses the preservation of remnant
and use of biodiversity, ecosystem functioning, and
wilderness areas or protected parks and the resto-
ecosystem services. In reality, since these impacts
ration of altered ecosystems, and emphasizes non-
on biodiversity are seldom reflected in market pri-
consumptive cultural services. The second involves
ces, they are said to be external to the market and
the transformation of ecosystems to yield provi-
are generally ignored by decision-makers. Envi-
sioning services. The third encompasses mixed use,
ronmental, resource, and ecological economics are
balancing non-consumptive cultural services with
all concerned with the development of mechanisms
consumptive provisioning services.
to internalize such externalities, many of which are
Just as the objectives in each case are different, so
reviewed in Chapter 17. The way that feedbacks
are the concepts of biodiversity used. Indeed, these
between economic and ecological systems are cur-
concepts are not independent of the decision-
rently modelled by economists is reviewed by
maker’s objectives. In the first case, the measure of
Wätzold et al. (2006). In this chapter, we consider
biodiversity is the difference in both the number
how economists model biodiversity in coupled
and abundance of species from the ‘natural’ state.
social ecological systems, taking two polar cases
In the second case, we construct an index of bio-
along with a more general problem.
diversity in agro-ecological systems that includes
All human decisions are taken to be purposive:
field margins, hedgerows, and other semi-natural
that is, people have in mind some objective in
habitats embedded in the cropping area. That is, the
deciding between alternative courses of action. They
index reflects elements of landscape heterogeneity.
are assumed to optimize some objective function
In the more general model, we take the heteroge-
subject to some set of initial conditions, including the
neity of the landscape – its patch structure – as
availability of information, to some set of resource
given. The biodiversity in each patch is then mea-
constraints, and to the dynamics of the system being
sured by a vector, the components of which report
used. The two polar cases considered in this chapter
the biomass of all the species on that patch. The
involve quite different objectives, spanning the range
optimal level of biodiversity is achieved through
of ecosystem services identified by the Millennium
harvest (or equivalent controls), and the problem is
Ecosystem Assessment. They involve the preserva-
modelled for both private users and society.

263
264 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

While the constrained optimization technique If naturalness is a proxy for various types of non-
applied in all three cases may be unfamiliar to consumptive cultural services, then it is useful to
ecologists, we have tried to give the intuition behind measure naturalness in a concise and practical
it. We have also provided a verbal description of manner. Eichner and Tschirhart (2007) introduce a
each of the three model structures developed. For measure labelled the divergence from natural bio-
those used to modelling aspects of the physical diversity (DNB). Consumers’ preferences for bio-
system, the chapter should show how the inclusion diversity and naturalness are assumed to depend
of decision-makers adds to our understanding of the on DNB defined as:
dynamics of coupled systems. More importantly, it
should show how biodiversity affects and is affected XN  2
ni ðhÞ  ni ð0Þ
by the decisions that people make. In all cases the s ¼ SðhÞ ¼  ð19:1Þ
 ni ð0Þ
social and biogeophysical components of the cou- i¼1

pled system are interdependent – connected through

a series of feedback loops. Economists refer to such In Eqn. (19.1), s is a measure of deviation from
systems as ‘general equilibrium systems’. That is, the ‘natural’ biodiversity (DNB), h denotes consumptive
dynamics of the system in some state are driven by a use such as harvesting, N is the total number of
tendency towards the equilibrium corresponding to species, ni(h) is the population of species i as a
that state, and any perturbation has the potential to function of consumptive use, and ni(0) is the natural,
stimulate responses across the system. steady state population of species i. If there is no
consumptive use, then h ¼ 0 and s ¼ 0. Consumptive
use is a scalar here. However, h could be treated as a
19.2 Modelling the demand
vector and additional consumptive use could
for ‘naturalness’
include impacts on the ecosystem through pollution,
The first case of interest is the classic concern of habitat loss, introduction of invasive species, global
conservationists. This is the case where wellbeing climate change, and so on. As consumptive use
depends on the preservation of the ‘naturalness’ of increases, populations can be expected to diverge
ecosystems. That is, the natural state of the system further from their natural levels and s decreases
provides a higher level of non-consumptive (cul- owing to the negative sign in Eqn. (19.1). As s
tural) services than any other state. In this case approaches 0 from below, consumers are assumed to
people are assumed to value two ecosystem attri- be better off because non-consumptive opportunities
butes above all others: (1) the diversity of species increase, other things equal. Of course, knowing
they contain – ‘the appreciation for the variation or what configuration of populations is feasible and
richness we observe in the ecosystems . . . based on how populations diverge with changes in h is central
the contemplation of the ecosystem as an ensemble for using DNB, and this is taken up below.
of life forms . . . ’ (Goulder and Kennedy 1997, p. 34); DNB has several useful properties not shared by
and (2) the extent to which the ecosystem is not most biodiversity measures. First, the preferred
altered by humans (Eichner and Tschirhart 2007, value of DNB for ecosystems that are targeted for
Forsyth 2000).This preference for naturalness is preservation or restoration is zero, and this is
illustrated by the Council Directive 92/43EEC on independent of the natural richness or evenness of
the conservation of natural habitats and of wild species in the ecosystem. Second, consumptive use
fauna and flora (Habitat Directive) of the European increases the value of DNB. Third, two species that
Union, and by the 1964 Wilderness Act of the diverge from their natural populations by the same
United States. The latter defines wilderness as percentages contribute the same to DNB. Thus,
‘ . . . an area of undeveloped Federal land retaining evenness, which has been shown to be negatively
its primeval character and influence, without per- related to richness (Stirling and Wiley 2001), is not
manent improvements or human habitation, which per se a positive property in DNB as it is with the
is protected and managed so as to preserve its Shannon index. Species that have stronger interac-
natural conditions . . . ’. tions with their neighbours than other species are
 MODELLING BIODIVERSITY AND ECOSYSTEM SERVICES 265

often labelled ‘keystone’ species (Mills et al. 1993), incentives, and the individual decisions lead to
and are expected to play a larger role in determining aggregate outcomes that determine the external
community structure. The third property of DNB incentives. In other words, both systems are adap-
does not imply that all species have equal impacts tive. In adaptive systems individuals process infor-
on the ecosystem and on S(h). Population changes of mation about their environment and then alter their
keystone species relative to non keystone species will behaviour according to some objective (Hraber and
cause greater numbers of other species to deviate Milne 1997). Ecosystems are clearly adaptive because
from their natural steady state populations. There- individual plants and animals and even micro-
fore keystone species have a greater impact on S(h). organisms act as if they have objectives and they
Fourth, with divergences of species from their nat- alter their behaviour in response to environmental
ural populations DNB decreases (qS/qni < 0) at a changes. Moreover, the individual behaviours lead
decreasing rate (q2S/qni2 < 0). Species whose to population dynamics that are often the cause of
populations are declining become increasingly diffi- the environmental changes.
cult to recover (Beissinger and Perine 2001); there- The most complete economic models are referred
fore, DNB values reflect the difficulty of returning a to as general equilibrium models that take into
community to its natural state. account all the market activity in an economy,
If naturalness enters directly into social objec- whether that economy is a country, region, city, etc.
tives, we can write the social welfare function as: General equilibrium (GE) theory has been referred
to as the most important development in economics

 in the twentieth century (Sandler 2001). Including
W x; h; sðhÞ ð19:2Þ
ecological variables in economic analyses without
recognizing the general equilibrium (i.e. the inter-
where x is a vector of manufactured goods, h a connected and interdependent) nature of ecosys-
vector of harvest or other consumption of biological tems can introduce errors for the same reasons that
resources, and s(h) the naturalness measure from partial equilibrium compared to GE economic
Eqn. (19.1) and a proxy for non-consumptive eco- analyses can introduce errors in measuring welfare
system services. As described above, there is an (Kokoski and Smith 1987). Recently, theoretical GE
inverse relationship between h and s. Working with models have been developed for ecosystems
W(x,h,s(h)) requires a bioeconomic model that (Eichner and Pethig 2005), and applied versions
accounts for aspects of both economic and eco- have been integrated with economic partial equi-
logical systems. The often used single-species har- librium models (Finnoff and Tschirhart 2003a, b)
vesting models used in economics will not suffice and an economic GE model (Finnoff and Tschirhart
for two reasons. First, they are in partial equilib- 2007). The authors refer to the applied GE ecosys-
rium on the economic side. Only one good, the tem model as a General Equilibrium Ecosystem
harvested food, is present, so there is no account Model (GEEM).
taken of how manufactured goods in the economy GEEM involves a modified Computable General
are affected by the harvests, and how the demand Equilibrium (CGE) economic model of predator–
and supply of other ecosystem services are affected prey and competitive relationships. Predator–prey
by the harvests. Second, they are in partial equi- and competitive relationships are chosen because
librium on the ecological side. Only one species is they contain key elements that drive ecosystem
present, so there is no account taken of how other outcomes, and therefore can be building blocks for
species that provide ecosystem services are affected larger, ecosystem-wide CGE models. GEEM
by the harvests. explains a fairly wide range of standard, and some
At the same time, there are limits to how much not so standard, ecological outcomes. Applications
detail about the economy or the ecosystem can be include an Alaskan marine food web and the
included in the bioeconomic model. Both systems Alaskan economy (Finnoff and Tschirhart 2003ab),
are very complex and contain millions of agents an early twentieth-century rodent invasion in
making individual decisions in response to external California (Kim et al. 2007), invasions of sea
266 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

lamprey in the Great Lakes (Finnoff et al. 2004), together through predator–prey relationships
invasions of leafy spurge in the Western USA and several species provide consumptive and non-
(Finnoff et al. 2007), and plant competition generally consumptive ecosystem services. The prominent
(Finnoff and Tschirhart 2005, 2006). One advantage groundfish of the system, pollock, supports a very
of the approach is that ecosystem externalities that large fishery, and charismatic marine mammals –
follow from the consumption of an ecosystem ser- Steller sea lions (an endangered species), killer
vice can be taken into account. Thus, if economic whales, and sea otter – provide non-consumptive
decisions result in the consumptive use of an eco- ecosystem services to the state’s recreation sector.
system service, then the model can track how other Naturalness as defined in Eqn. (19.1) is not
ecosystem services are altered, and then what these included below, but in Eichner and Tschirhart
alterations mean for the economy. A model linking (2007) naturalness is included as a variable in a
the Alaskan economy to a marine ecosystem com- welfare function for the same Alaskan ecosystem
prising Alaska’s Aleutian Islands and the Eastern examined here.
Bering Sea is represented in Fig. 19.1. The three basic equations that comprise general
The economy consists of Alaskan households and equilibrium ecosystem model for this system are
producing sectors, linked to one another and the given by (19.3)–(19.5). The first equation is a general
rest of the world through commodity and factor expression for the fitness net energy flow through a
markets. All species in the food web are linked representative animal from species i.

Commodity Commodity Monetary flows

imports exports
Real flows

Commodity Ecosystem flows

markets Non consumptive
Ecosystem flows

Killer whale
Recreation
Composite
Fishery

goods

Households
Sea otter

Steller sea lion

Regulator

Pollock
Sea urchin
Factor Zooplankton
markets

Factor
imports
Kelp
Phytoplankton
Sun

Figure 19.1 The Aleutian Islands and Eastern Bering Sea model (source: Finnoff and Tschirhart 2007).
 MODELLING BIODIVERSITY AND ECOSYSTEM SERVICES 267

X
i1 X
m
escaping. ti is a tax on the individual because it
Ri ¼ ½ej  eij xij  ei ½1 þ ti eki yik
j¼1
loses energy above what it loses owing to being
k¼iþ1
X
i1 captured. The third and fourth terms in Eqn. (19.3)
fði
xij Þ  bi ð19:3Þ represent respiration energy lost to the atmosphere,
j¼1
which is divided into a variable component, f i(),

 that depends on energy intake and includes faeces,
Ni xij ðei Þ ¼ Nj yji xj ðej Þ ð19:4Þ reproduction, defending territory, etc., and a fixed
component, bi, that is basal metabolism.
  
2Nit Nit
Time in the ecosystem is divided into reproduc-
Nitþ1 ¼ Nitþ Nit ss 1  2N ss Ri ðÞ tive periods, usually a year. In each period a gen-
si vss
i Ni
 1
i
eral equilibrium is determined wherein the
þvi  ð19:5Þ populations of all species are constant, each plant
si
and animal is maximizing its net energy (using the
Ri is in power units (e.g. watts or kilocalories/time). derivatives of Eqn. (19.3) for first-order conditions),
According to Herendeen (1991) energy is the most and aggregate demand equals aggregate supply
frequently chosen maximand in ecological maxi- between each predator and prey species. For each
mization models, and energy per time maximization, price that equates a demand and supply transfer
as adopted here, originates with Hannon (1973) and there is an equilibrium equation given by Eqn.
is expanded in Crocker and Tschirhart (1992) and to (19.4). Each plant and animal is assumed to be
the individual level in Tschirhart (2000). Energy per representative of individuals from its species;
time is also the individual’s objective in the extensive therefore the demand and supply sums are
optimum foraging literature (e.g. Stephens and obtained by multiplying the representative indivi-
Krebs 1986). The species in Eqn. (19.3) are arranged dual’s demands and supplies by the species popu-
so that members of species i prey on organisms in lations given by the components of the vector N.
lower-numbered species and are preyed on by A representative plant or animal and its species
members of higher-numbered species. The first term may have positive, zero, or negative fitness net
on the right-hand side is the inflow of energy from energy in equilibrium. Positive (zero, negative) net
members of prey species (including plants) to the energy is associated with greater (constant, lesser)
representative individual of species i. The choice fitness and an increasing (constant, decreasing)
variables or demands, xij, are the biomasses (in population between periods. (The analogy in a
kilograms/time) transferred from the member of competitive economy is the number of firms in an
species j to the member of species i, ej are the ener- industry changing according to the sign of profits.)
gies embodied in a unit of biomass (e.g. in kilo- Fitness net energies, therefore, are the source of
calories/kilogram) from a member of species j, and dynamic adjustments. If the period-by-period
eij are the energies the member of species i must adjustments drive the net energies to zero, the
spend to locate, capture, and handle units of biomass system is moving to stable populations and a
of species j. These latter energies are the ‘energy steady state. The predator–prey responses to
prices’. changing energy prices tend to move the system to
The second term is the outflow of energy to steady state.
animals of species k that prey on i. The ei is the The adjustment equation for the ith species (a top
embodied energy in a unit of biomass from predator in this case) is given by Eqn. (19.5), where
the representative individual of species i, and yik is Ri() ¼ Ri(xij; Nt) is the optimum fitness net energy
the biomass supplied by i to k. The term in brackets obtained by substituting the optimum demands
is the energy the individual uses in attempts to and supplies as functions of energy prices into
avoid being preyed upon. It is assumed to be a objective function Eqn. (19.3). Nt is a vector of all
linear function of the energy that its predators use species’ populations and it appears in Ri() to indi-
in capture attempts: the more energy predators cate that net energies in time period t depend on all
expend, the more energy the individual expends populations in time period t. In the steady state,
268 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Ri() ¼ 0. Also, si is the lifespan of the representative Households first choose the proportion of income
individual, vi is the variable respiration, vss i is the allocated between current and future consumption,
steady state variable respiration, and Niss is the where savings fund future consumption by adding
species steady state population. The first and sec- to the capital stock in future periods. They then
ond terms in brackets in Eqn. (19.4) are the birth divide current disposable income between expen-
and death rates. Expression (19.4) reduces to the ditures on recreation and an aggregate commodity.
steady state if Ri() ¼ 0 (in which case vi ¼ vss i and Finally, income allocated for the aggregate com-
Nit ¼ Niss ). Because the biomass demands depend
modity is divided between purchases of fish and
on the period t populations of all species, the pop-
ulation adjustment for species i depends on the the composite good.
populations of all other species. In addition, out of When the capital stock grows at the same rate as the
steady state Ri() and vi change across periods. effective labour force, the economy is on a balanced
These changes distinguish the GEEM approach growth path; however, balanced growth is not a fea-
from most all ecological dynamic population mod- ture of the linked model, because species populations
els, because the latter rely on fixed parameters in cannot grow indefinitely. Unlike the growth of the
the adjustment equations that do not respond to effective labour force and capital stock, ecosystem
changing ecosystem conditions. populations are limited by photosynthesis and may
In more detail, the simplified Alaskan economy is converge to steady states, with zero net growth. Thus
modelled as having three production sectors: the the sectors reliant on ecosystem services will not be
fishery F, recreation and tourism R, and composite expected to grow at the rate of the human factor stocks.
goods C.The fishery is modelled as a single, vertically Our welfare measures comprise annual equivalent
integrated industry consisting of catcher vessels, variations EVt for any single period across policy
catcher processors, motherships, and inshore pro- scenarios. Cumulative aggregate welfare measures
cessors. Recreation and tourism represent the Census (including a terminal term) are found using dis-
Bureau’s classification of Wildlife Related Recreation counted summations of EVt given by PEV. These
(consumptive and non-consumptive), and composite provide a comparative measure as they are based
goods is a catch-all for the residual private industries upon a common baseline price vector.
in Alaska. Profit-maximizing, price-taking firms The recreation sector is reliant on marine mammals
employ harvests of pollock in the fishery, non-con- for a non-consumptive ecosystem service. The
sumptive use of marine mammals (Steller sea lions, industry combines labour and capital with popula-
killer whales, and sea otter) in recreation, and capital tions of marine mammals to deliver a ‘recreational
and labour in all sectors, to produce their outputs in a experience’. The recreation industry maximizes prof-
continuous, non-reversible, and bounded process. its subject to a Cobb–Douglas production function
Outputs from the fishery, recreation, and composite (consistent with the fishery specification):
goods are sold in regional markets and exported out
of the region, while regional production is differenti-
max ph ¼ PX
R XR  WLR  RKR s:t:
ated from imports for fish and composite goods fol- LR ;KR

lowing Armington (1969). Capital, K, and labour, L, R R

cR
XR ¼ dR LaR KRb NAT ð19:6Þ
are homogeneous, perfectly mobile within the region,
and defined in service units per period. Sector i factor where aR, cR, and dR are parameters, R subscripts for
employment levels are given by Ki and Li (i ¼ F, R, C). the recreation sector, and NAT the contribution of
As a high proportion of fishery factors are owned and Alaska’s natural resources to the sector. This measure
reside outside the region (specifically in Washington includes BSAI aggregate marine mammal popula-
state), factors in the fishery are modelled as being tions taken as a linear combination of the three marine
interregionally mobile. This treatment is not extended mammals. NAT enters recreation production as a shift
to other sectors to allow a focus on the regional effects parameter, exogenous to the recreation firms but
of policy changes. endogenous to the joint system. See Knowler (2002)
Households consume fish, recreation, and com- for a discussion of models of these types, i.e. models
posite goods and save for future consumption. that build on Ellis and Fisher (1987).
 MODELLING BIODIVERSITY AND ECOSYSTEM SERVICES 269

The linkage between the ecosystem and fishery reduced quota level of 30 per cent. A portion of the
requires two modifications to the standard fishery regional welfare gains from reduced quotas is due
models. First, where most of the fishery literature to the fact that the economy relies less on resource
employs effort as the single human factor of pro- extraction and more on non-extraction – i.e. less on
duction, capital and labour must be included in a consumptive ecosystem service and more on a
CGE so that the fishery interacts with other sectors. non-consumptive ecosystem service. This result is
Second, the non-fishery sectors hire capital and consistent with a report from the Panel on Inte-
labour in service units per time period, in this case grated Environmental and Economic Accounting
one year, but in the fishery factors are employed for which states: ‘economic research indicates that
considerably less than one year and may earn more many renewable resources, especially in the public
per unit than in other sectors. This is due to domain, are today more valuable as sources of envi-
restricted season lengths and potential unemploy- ronmental service flows than as sources of mar-
ment during the off season. keted commodities’ (Nordhaus and Kokkelenberg
Although ecosystems provide myriad services to 1999, p. 177).
economies, only one service is considered in most
renewable resource models, usually harvesting. The
19.3 Modelling biodiversity and land
bioeconomic model discussed here admits recrea-
use in agro-ecosystems
tion as a second service, and more importantly
accounts for how the two services are impacted by Our second case is at the opposite end of the con-
interactions within an eight species ecosystem. Here servation-use spectrum. It is the modelling of land
we illustrate some of the implications from creating use and biodiversity change in agro-ecosystems.
the linkage between systems, based around shocks The most important anthropogenic cause of agro-
to the system from National Marine Fisheries Ser- biodiversity loss is rapid land use and land cover
vice (NMFS) policies. The NMFS in 2001 issued a change (LUCC) and the subsequent transformation
Supplemental Environmental Impact Statement of habitats (Millennium Ecosystem Assessment
(SEIS) containing alternative management strate- 2005b). In agricultural landscapes LUCC usually
gies that specify various pollock catch limits and no takes the form of land development. Most land
fishing zones to protect both the sea lions and the development at the landscape level stems from
fishery. We consider rules for catch limits that are decentralized economic decisions of economic
given by a regulator’s choice of a quota for pollock. agents, including small-scale farmers, agribusiness,
Here we consider quotas equal to the 1997 harvest and governments at different scales. The ecological
levels and 30 per cent and 170 per cent of the 1997 causes and effects of such landscape transforma-
harvest levels. tions are increasingly well understood and docu-
Steller sea lion recovery measures via alternative mented, especially with regard to deforestation and
pollock quotas are shown to cause altered levels of desertification in developing regions (Perrings and
all ecosystem populations, economic factor reallo- Gadgil 2003). In agricultural landscapes, one impact
cation, changes in all regional prices, incomes, of LUCC that is attracting increasing attention is the
demands, outputs, imports, exports, and differen- alteration of the flow of ecosystem services that are
tial rates of factor accumulation. Of the eight spe- mediated by biodiversity (Millennium Ecosystem
cies modelled, four are used directly in the Assessment 2005b, Perrings et al. 2006). This has
economy either as consumption goods (fish) or non- significant implications for biodiversity conserva-
consumption goods (marine mammals). While non- tion strategies in agro-ecosystems.
use values associated with the ecosystem are not Once again, we are interested in exploring the
considered, all species matter for the economy wedge between individual agents’ perceived net
because the remaining species indirectly support benefits from LUCC actions and those realized by
the two modelled ecosystem services. the community that is affected by those same
The results (reported in Finnoff and Tschirhart actions (Swanson, 1995; Perrings, 2001; Millennium
2007) show that there are welfare gains from the Ecosystem Assessment, 2005b). Part of the problem
270 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

in understanding the social value of biodiversity concentration of disease-prone monocultures creat-

change is that while some of the opportunity costs ing spillovers to the extent that the diseases are
of conservation or foregone benefits from land infectious across farms; and the development of
development are easily identified, there remain resistance to pesticides.
important gaps in the understanding both the on- Omer et al. (2007) explore the economic effects
and off-farm benefits of agrobiodiversity conserva- of biodiversity loss on marketable agricultural
tion. The primary interest in agro-ecosystems is a output for intensive agricultural systems, which
set of provisioning services – the production of require an increasing level of artificial capital
foods, fuels, and fibres – for which there are well- inputs. They model the effect of the state of bio-
developed markets. There are, however, several diversity on the optimal crop output both in the
effects of agricultural production that are not con- longer run and in the transitional path towards
sidered in market transactions for these services. the steady state equilibrium. The hypothesized
One is the role of agricultural intensification as a positive relationship between biodiversity stock
means of reducing impacts on habitats for biodi- and optimal levels of crop output is then empir-
versity at the landscape level (Green et al. 2005). A ically tested via a stochastic production frontier
second is the contribution of crop diversity to pro- approach using panel data on UK cereal farms for
ductivity and variability of a main crop output and the period 1989–2000. The results show that
farm income (Smale et al. 1998, Widawsky and increases in associated agrobiodiversity can lead
Rozelle 1998, Omer et al. 2007) and its variability to a continual outward shift in the output frontier
under output uncertainty (Di Falco and Perrings (although at a decreasing rate), controlling for the
2003, 2005, Di Falco and Chavas 2007). The impacts relevant set of labour and capital inputs. Agri-
we consider here relate to the application of ferti- cultural transition towards biodiversity conserva-
lizers and pesticides. There are, of course, many tion may be consistent with an increase in crop
distinguishing features of agro-ecosystems includ- output in already biodiversity-poor modern agri-
ing modification of ecosystem processes (distur- cultural landscapes.
bance (tilling, burning), pest control, water input The model assumes that the allocation of agri-
(irrigation), nutrient input (fertilizer), and the cultural inputs, for a given area of farmland, is
effects of herbivory (in the case of pastures or grain- driven by levels of crop output and by on-site
fed livestock). All imply that nutrient cycling is biodiversity. It is assumed that decision-makers
spatially and temporally decoupled. Fertilizers and maximize the discounted present value of utility
pesticides are just special cases of the general flows derived from both outputs. The stylized
practice of regulating ecosystem processes to opti- direct utility function is specified as U ¼ U(yt, bt),
mize local production. where yt represents the flow of ‘marketable’ agri-
Soule and Piper (1992) mention a number of cultural output at time t, and bt is biodiversity loss,
adverse effects associated with industrial high- also a flow variable. This loss is attributable to
input agriculture, including spillovers from soil intensive use of artificial inputs, xt, which therefore
erosion into municipal water supplies, lakes, and negatively impacts on utility, i.e. Uy > 0,Uyy < 0,
reservoirs; erosion-induced suspended sediment and Ub < 0, Ubb < 0, for a strictly concave and
carrying unwanted nutrients and pesticides; linearly separable utility function. This specification
streams and wetlands filled with sediment causing reflects a subset of economic decisions that would
less resilience to floods; soil pesticides adding to air affect land use activities, and the welfare that these
pollution; salinization and other spillovers caused activities generate. The problem is to find the inter-
by irrigation; specialized breeding and failure to temporal optimal levels of utility yielding services
maintain the ‘common pool’ of genetic diversity (flows) based on (1) marketable agricultural sup-
because of optimization towards narrow produc- ply and (2) physical depreciation of biodiversity.
tivity goals; biodiversity loss due to pursuit of While bt is an argument in the direct utility func-
agricultural monoculture in tropical forests and tion, it depends on the level of application of
other common types of biodiversity reservoirs; artificial inputs and the ‘current’ level of
 MODELLING BIODIVERSITY AND ECOSYSTEM SERVICES 271

biodiversity (zt) through a ‘biodiversity impact ments, ct, and artificial input use, xt, that reflects the
function’. level of intensification.
Following recent studies (e.g. Tscharntke et al.
2005), the crop production function is assumed to z ¼ gðzt ; ct ; xt Þ ð19:8Þ
be affected by the stock of biodiversity, zt, alongside
the conventional agricultural input set xt. In addi- The evolution of biodiversity is captured by Eqn.
tion, the ‘state of the art’ of agricultural technology (19.8), which can be interpreted as a general form of
is captured by the parameter at, which acts as an the function:
exogenous shifter of the production possibility
frontier, representing neutral technical progress. z ¼ a1 zt ð1  zt =kÞ þ a2 ct  a3 xt ð19:9Þ
Normalizing the unit price of crop output, the value
production function is represented by f(xt, zt, at), The natural rate of growth of the biodiversity stock
which is assumed to exhibit well-behaved proper- is given by a1 > 0. The parameter k reflects the
ties, i.e. fi > 0, fii < 0 for i ¼ xt, zt, and at, and to be maximum potential diversity that could be sus-
linearly separable. tained in the ecological system. The parameter k,
Given some managerial input, the stock zt can be like the ‘carrying capacity’ in Lotka–Volterra pop-
increased by conservation investment, ct, which is ulation growth models, is the maximum potential
given by the residual from the total proceeds from level of diversity which could be sustained natu-
agricultural production, f(xt, zt, at), less the pro- rally. According to Eqn. (19.9), zt is density depen-
portion that is committed as ‘marketable (value) dent and increases with investment in conservation,
output’ yt: a2 being the rate of induced growth in zt.The
parameter a3 may be interpreted as the marginal
ct ¼ fðxt ; zt ; at Þ  yt ð19:7Þ degradation in zt caused by an increase in xt. It is
worth noting that while biodiversity is considered
If the focus is on the functional diversity of species, to be natural capital, it is assumed here that no
the effect of a change in zt on the marginal product depletion in biodiversity occurs as a result of its
of xt is likely to be different at each level or sublevel supporting role in the production process. In
of zt. For example, an increase in insect or micro- intensive agricultural systems, which are biodiverse
organism diversity would increase the marginal poor relative to their potential maximum (e.g. their
product of fertilizer if it enhances soil productivity ‘wild’ state), the term zt/k can be considered as
(fxz  0). On the other hand, an increase in natural negligible, and thus Eqn. (19.9) can be simplified
vegetation diversity might decrease the marginal through further approximation as:
product of fertilizer if it increases the competition
with cultivated crops (fxz  0). The biodiversity z ¼ a1 zt þ a2 ct  a3 xt ð19:10Þ
impact (or loss) function is expressed by bt ¼ b(xt, zt).
The ability of the agro-ecosystem to tolerate and The optimization problem is expressed, for a posi-
overcome the potential adverse effects of agricultural tive utility discount rate (r > 0) as:
land use activities depends on the current biodiversity
stock, zt such that bz < 0, bzz > 0. At the margin, R
1
max Wðyt ; bt Þ ¼ ert Uðyt ; bt Þdt ð19:11Þ
biodiversity loss increases (decreases) at an increasing y;x;c
t¼0
(decreasing) rate due to increases in input intensifi-
cation, i.e. bx > 0, bxx > 0; for simplicity, bt ¼ b(xt,zt) is subject to (1) the environmental conservation
also assumed to be linearly separable in xt and zt. investment function (Eqn. 19.7), (2) the evolution of
To maximize utility, the farmer chooses the level zt, (Eqn. 19.10), (3) the impact function b(.), (4) the
of the control variables yt and xt at each point in initial condition z(0) ¼ z0, and (5) the non-negativity
time, subject to the evolution of zt. This evolution constraints and x  0 and b  0. This yields the
reflects agrobiodiversity stock, conservation invest- current-value Hamiltonian:
272 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

~ XX
H ¼ Uðyt ; bt Þ þ uða1 z þ a2 fð:Þ  a2 yt  a3 xt Þ ð19:12Þ z¼ aj nij sij ð19:13Þ
j i

where u is the current shadow value of biodiversity.

Omer et al. (2007) show that where the stock of where, sij is the mean plant species richness on a
biodiversity at the steady state is greater than the given plot located in aggregate vegetation class
initial stock, the optimal supply of marketable (AVC) i within broad habitat (BH) type j; nij stands
output can increase (albeit at a declining rate) along for the measure of AVC-i dominance in BH type-j, i.
the transition path to the steady state. e. the number of AVC-i plots in BH type-j relative
In an application of the theoretical model sum- to the total number of plots of all AVCs in BH-j;
marized above, Omer et al. (2007) construct an and lastly aj is a scalar associated with BH-j domi-
aggregate biodiversity index that takes into account nance. In a second step, the evolution of the bio-
biodiversity of agricultural landscapes that include diversity index at the aggregate level is calibrated
non-cropped areas such as field margins, hedge- as a non-linear discrete-time aggregate version of
rows, and other semi-natural habitats embedded in Eqn. (19.10).
the cropping area using UK farm and biodiversity
data. The production data derive from a panel of ztþ1  zt ¼ a1 ln zt þ a2 ct  a3 ln xt ; ð19:14Þ
230 cereal producers from the East of England, for
the period 1989–2000, yielding a total sample size of where ct is proxied by a categorical dummy vari-
2,778 observations in an unbalanced panel. The able (1/0) showing whether the farmer is a benefi-
data are from the UK’s annual Farm Business Sur- ciary of the introduction of agri-environmental
vey (FBS) undertaken by the Department of Envi- schemes following the EU’s Common Agricultural
ronment, Food and Rural Affairs of the UK. The UK Policy reform in 1992, and xt is average per hectare
Countryside Surveys undertaken in 1978, 1990, and pesticide use on the sample farms.
1998 were used to construct a farm-level biodiver- To test the proposition from the theoretical
sity index (Haines-Young et al. 2000). The data set model, a reduced form dynamic parametric fron-
includes information on cereal output, level of tier model is used and fitted to data (Battese and
input application, participation in and payments Coelli 1995). A stochastic production frontier (SPF)
from agri-environmental schemes, and socioeco- approach then allows estimation of both the out-
nomic characteristics of the farm households. In put production frontier that represents best prac-
addition, a variable measuring on-farm functional tice among farmers (as assumed in the theoretical
biodiversity is constructed. The per-hectare vari- model) and the possibility of real deviations from
ables used in the econometric model are: crop the frontier attributed to the effects of variation in
enterprise output (marketed), hired and imputed the sampled farmers’ level of technical efficiency
family labour, use of machinery, fertilizers and (TE). Controlling for TE, it is possible to qualify the
pesticides, and the biodiversity index (BI). All the key relationships derived from the theoretical
variables, except for BI, are derived from value model along the production frontier as it evolves
measures deflated by the relevant agricultural price over time. It should be noted that the frontier
index (base year 1989), and are thus measures of provides a closer approximation to the ‘optimal
volume. path’ than a more traditional econometric specifi-
This is consistent with a number of ecological cation which (a) does not allow for technical inef-
studies (e.g. Altieri 1999, Tscharntke et al. 2005) that ficiency levels by farmers, (b) can be associated
emphasize the role of landscape level biodiversity with their managerial ability, and (c) in turn may
(associated and functional) affecting the ecological depend on factors such as information, experience,
functioning of arable agro-ecosystems. The aggre- etc. Hence the data on marketed crop output is
gation approach used to construct the biodiversity used to estimate the output optimal path via the
index is described by Wenum et al. (1999). The function y(xt, zt, at).
index (representing the variable z in the theoretical Omer et al. (2007) estimate a non-neutral ineffi-
model) is given by: ciency model fitted to the 12 years, t ¼ 1, 2, . . . , T,
 MODELLING BIODIVERSITY AND ECOSYSTEM SERVICES 273

and using farm-level data, i.e. for farmer i, which after 1996 the elasticity becomes positive. The net
takes the following general form: effect of biodiversity through the impacts on both
frontier output and technical efficiency suggests
X
yit ¼ b0 þ bk pkit þ vit  uit ð19:15Þ that agrobiodiversity has negatively affected
k yields (average elasticity of –0.1) from 1989 to
1993, the year after broad environmental payments
where: yit is the natural log of crop marketed output were introduced in the farming sector, as a stra-
of farm i at time t; p1 is the natural log of BI (bio- tegic agri-environmetnal scheme. After the incor-
diversity index); p2 is the natural log of fertilizer poration of the environmental payments for
input value; p3 is the natural log of labour input biodiversity conservation, the impact on mean
value; p4 is the natural log of machinery input output has reversed, with an elasticity in 2000 of
value; p5 is the natural log of pesticide input value; 0.26. This implies that on average, during such
and p6 is the year of observation, where p6 ¼ 1, agri-environmental scheme, a 1 per cent increase in
2, . . . , 12. The vits are assumed to be independently agrobiodiversity has positively affected mean
and identically distributed random errors Nð0; r2v Þ, wheat output by 0.26 per cent. These results sug-
independent of the non-negative random error gest that biodiversity conservation schemes have
term, uit, associated with technical inefficiency in not undermined the productive performance of the
production. bk is the parameter vector to be esti-
cereal sector.
mated. Furthermore, it is also assumed that the
inefficiency variable is also a function of farm-level
characteristics:
19.5 A generalized model of the
X XX consequences of biodiversity loss
uit ¼ d0 þ dj qjit þ djk pkit qjit þ wit ð19:16Þ in exploited ecological–economic
j j k
ecosystems
Allowing for interactions between farm-specific Although there is a high degree of uncertainty
variables and the input variables in the stochastic associated with species diversity and its loss, there
frontier the elasticity of crop output with respect to is evidence that declining species diversity may
all inputs, including agrobiodiversity, can be adversely affect the performance of terrestrial eco-
derived. The latter has two components: (1) the systems. Several empirical studies relate the num-
elasticity of frontier output with respect to the ber of species in ecosystems to plant productivity
agrobiodiversity and (2) the elasticity of technical (Vandermeer 1989, Naeem et al. 1995, 1996, Tilman
efficiency with respect to agrobiodiversity. et al. 1996, Hooper and Vitousek 1997) which find
The results from the econometric model indicate that functional diversity is a principal factor
that associated agrobiodiversity positively affects explaining plant productivity. Given the relation-
mean wheat output levels over the whole period, ship between human expansion, loss of biotic
even though greater levels of agrobiodiversity diversity and loss of ecosystem productivity, we
appear to have negatively affected technical need to be able to model the efficient management
(managerial) efficiency in the intensive agricultural of the biotic diversity of ecosystems.
sector. As regards the former result, this is con- Equilibrium species diversity in resource-based
sistent with the hypothesis that there is a positive, models is governed by an exclusion principle that
although declining, effect. The data indicate that characterizes the way that undisturbed natural
the frontier elasticities with respect to agrobiodi- systems move towards a steady state equilibrium.
versity, while positive, have tended to decrease This principle states that where there is multispe-
over the years. It also appears that the effect of the cies competition for a limiting factor, in a patch free
stock of biodiversity on technical efficiency has of disturbances, the species with the lowest
been different before and after 1996. While there is resource requirement will competitively displace all
initially a negative technical efficiency elasticity, other species in equilibrium. In this case the system
274 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

is driven to a monoculture, and the equilibrium this context private agents do not account for the
outcome of species competition is the survival of external costs and benefits of their management
the competitive dominant species, i.e. the species practices on ecosystem service flows. This means
with the lowest resource requirement. Of course that the private agent ignores all interactions
there are a number of ways in which nature can among patches, as well as any externalities that his
produce equilibrium polycultures with one or more or her actions might bring on other agents as these
limited resources. As noted in Pacala and Tilman actions could affect the whole range of ecosystem
(1994), temperature-dependent growth and tem- service flows in the ecosystem. The second is the
perature variation in a habitat, spatial or temporal socially optimal management problem (SOMP),
variations of resource ratios, differences in species where a social planner maximizes utility from the
palatabilities, and local abundance of herbivores, whole ecosystem. Utility is derived both from har-
can all result in spatial or temporal variation of vesting and from the state of the ecosystem, with all
dominant competitors. In this way Nature’s equi- interactions among species and resources both
librium is characterized by a Tilman set of species within and across patches taken into account. Thus,
determined by limiting factors. in the design of the socially optimal management
Given this, it is possible to develop a general rules values associated with flows of ecosystem
model of species competition in a landscape con- services are internalized into the management
sisting of potentially heterogeneous patches of land problem.
to explore the equilibrium state of an ecosystem By comparing the two management problems it
that is managed for economic objectives. The is possible to explore how the decisions of private
growth of species is limited by resource availability, agents (who ignore biodiversity externalities) may
while species interact among themselves and com- deviate from the social optimum. In this sense the
pete for the limited resources. In this sense this private and social optimal harvesting rules, and the
model can be regarded as a generalization of state of the ecosystem as reflected in equilibrium
Tilman’s mechanistic resource-based model of biodiversity under private and social management
competition, by including direct interactions among can be derived and compared. Brock and Xepapa-
species. The multi-species Kolmogorov model and deas (2004) show this in the following manner. Let
the Lotka–Volterra model can be also derived from i ¼ 1, . . . , n species exist in a given patch of land, for
this generalized model under appropriate assump- example, a hectare of forest stand, belonging to a
tions. The benefits from species diversity are broader landscape, and assume that the growth
reflected in the value of a potentially large and of the species in each patch is limited by resources
diverse set of service flows generated by the eco- j ¼ 1, . . . , r. They define a resource following Til-
system. Depending on whether these flows of ser- man (1982, p. 11) as: ‘any substance or factor which
vices are taken into account in the design of can lead to increased growth rate [of an organism]
management, the resulting management rules and as its availability in the environment is increased,
the corresponding equilibrium state of the ecosys- and which is consumed by the organism’. For
tem can be analyzed. In this analysis Tilman’s example, the growth rate of a plant measured as the
model with a single limited resource serves as a rate of weight gain may be increased by the addi-
special case that provides some very interesting tion of nitrate which is consumed by the plant.
insights into the issue of specialization and biodi- Further, they denote by c a patch or a site; by


versity preservation (Brock and Xepapadeas 2002). R c ðtÞ ¼ R1c ðtÞ; :::; Rrc ðtÞ 2 g ( Rrþ a vector of
In particular, two basic management problems
available resources in that patch at time t; and by
can be analyzed in this context. The first is the

privately optimal management problem (POMP) Bc ðtÞ ¼ B1c ðtÞ; :::; Brc ðtÞ 2 b ( Rrþ a vector of the
where economic agents maximize solely profits biomass of species in the patch at the same time. So
from harvesting in their patch, subject to the evo- R and B denote the vectors of resources and bio-
lution of the natural system, by regarding any masses respectively in every patch, and R-c, B-c the
vectors of resources and biomasses and biomasses
interactions outside their patch as exogenous. In
 MODELLING BIODIVERSITY AND ECOSYSTEM SERVICES 275

outside site c: i.e. (R, B) ¼ (Rc, R-c, Bc, B-c). From Sjc(Rc, Rc). It is further assumed that the resources
this they are able to specify a general model of cannot accumulate without bounds (even without
competition among species in each patch c by the consumption by species), and that Eqn. (19.18) is
system of differential equations: concave.
The model described by Eqns. (19.17) and (19.18)

Bic can be regarded as a generalization of a multispe-
¼ Fic ðBc ; Bc ÞGic ðR c ; dic Þ; Bic ð0Þ
Bic cies Kolmogorov model (Murray 2002) with the
¼ B0ic > 0; 8i; c ð19:17Þ explicit introduction of the resource dynamics
equation which makes it possible to directly ana-
lyze species competition through its influence on

Rjc ¼ Sjc ðR c ; R c Þ  Djc ðBc ; Bc ; R c ; R c Þ; Rjc ð0Þ resource availability. It constitutes a resource-based
model of competition between species in a given
¼ R0ic > 0; 8j; c ð19:18Þ
patch structure. A long-run equilibrium for every
patch is defined as a situation where the net
Equation (19.17) describes the net rate of growth of
growths of the species and the resources are zero,
the biomass of species i in patch c. The growth rates  
or equivalently B ¼ R ¼ 0. If such an equilibrium
of a species in a habitat depend on a number of
exists, then the equilibrium biomass vector Bec
exceptionally complex processes involving soil
describes the equilibrium biodiversity in patch c
building, nutrient uptake, and symbiotic relations
and B describes the equilibrium biodiversity of the
among fungi, insects, mammals, and flora which whole system. Species for which Bekc ¼ 0 are dis-
are still not entirely understood (Scott 1998). Thus, placed by other species in patch c. Note that
the growth equation (19.17) attempts to capture the Tilman’s mechanistic resource-based model (Tilman
dependence of the growth rate of each species on 1982, 1988, Pacala and Tilman 1994) is a special case
resource availability in the patch, as well as its of this generalized model. In this model each spe-
dependence on other species biomasses and cies affects all other species only through its effects
resource availability in the whole lattice. on the availability of the limiting resource, that is,
Equation (19.17) emphasizes the fact that the growth is density independent and no interactions
 among neighbouring patches take place. The single
biomass vector B has B ¼ 0 as a steady state. The
resource can be thought of, for example, as an index
function Gic(Rc, dic) captures the effects of resource
of soil quality that could include the health of
availability in the patch on a species’ rate of
microorganisms in the soil, the amount of useful
growth, with dic being a natural death rate param- humus, and so forth, and the resource supply can
eter. By assumption, all resources in the patch are be regarded as the soil genesis function. The
essential for species growth. The growth function is exclusion principle mentioned earlier is the main
non-decreasing in Rc by the definition of a resource, driving force in determining the long-run equilib-
and is assumed to be strictly concave in Rc rium for the ecosystem. If all species are ranked, by
(reflecting ‘diminishing returns’ in the resource use relabeling, according to their Reic such that
for all R  0. The effect (complementary or com- Re1c < Re2c <    < Renc , then according to the compet-
peting) of one species on the growth rates of other itive displacement mechanism, species one will
species is captured by the function Fic(Bc,Bc). displace all other species in equilibrium.
Equation (19.18) describes the resource dynamics. Note that the competitive displacement of species
Sjc(Rc, Rc) is the amount of the resource supplied according to Reic occurs in the long-run equilibrium.
Species with relatively high Reic show an initial
at time t in patch c and Djc(Bc, Bc, Rc, Rc) is
period of rapid growth relative to low species.
consumption of the resource by all species. Brock
However, as time goes by, the low Reic species
and Xepapadeas assume that the availability of a reduce the resource to levels insufficient for the
resource can be affected by the availability of other survival of the high Reic species, eventually displa-
resources both within and across sites, so that cing them. Thus high Reic species tend to grow rel-
resources are themselves interacting entities with atively faster than low Reic species, but are
the interaction mechanism captured in the function eventually displaced in equilibrium. In an
276 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

ecosystem with sites having different characteristics where Pi is the market price of the harvested species
the exclusion principle will provide a c-specific and Ci(Hic(t)) is a convex cost of harvesting func-
monoculture, with a dominant c-competitor. Envi- tion. The constraints on the above maximization
ronmental heterogeneity across patches, associated problem are the growth rate of the biomasses
with variations in temperature and the species adjusted to take into account the reduction in the
thermal optimum, spatial variations of resource
growth rate due to harvesting.
ratios, differences in species palatability, and local
Maximizing an objective function like (19.19)
abundance of herbivores (Pacala and Tilman 1994)
will lead to the coexistence of species (higher levels subject to Eqns. (19.17)–(19.18) implies that man-
of biodiversity) equilibrium. agement focuses only on species that can provide
Similar results can be explored in a multi- commercially valuable biomass for harvesting, i.e.
resource context. In this case depending on the only on the provisioning services. It neglects many
type of resources (e.g. substitutable, complemen- of the other services, especially the cultural and
tary, switching, essential), the species require- regulating services, identified by the Millennium
ments and the resource supply (Tilman 1982, 1988) Ecosystem Assessment. The private (optimal)
there might be species coexistence in equilibrium management problem (POMP) involves the maxi-
within the same c-patch. Allowing therefore for mization of private profits, through an objective
variation of characteristics across the lattice grid function defined solely in terms of harvesting and
and/or multiple limiting resources, the mechanis- where the private agent is sufficiently small that it
tic resource-based model predicts higher levels of treats the resources and the biomasses in the rest of
biodiversity not only during transitional dynamics the ecosystem as fixed. On the other hand, the
but also in equilibrium. social (optimal) management problem (SOMP) is
Given the parameters in Eqns. (19.17)–(19.18), defined in terms of an objective function that
undisturbed nature can produce a rich pattern of includes not only consumptive benefits but also
species in equilibrium. Therefore in an ecosystem other sources of benefits related to the full range of
where many species compete for limiting resources, services yielded by the ecosystem.
undisturbed nature will provide a biodiversity In terms of the Brock and Xepadadeas equations
pattern which depends mainly on the availability of for species dynamics, if some part of the ecosystem
resources and the variation of characteristics across has been converted into a monoculture, then terms
the landscape. In this context, the purpose of of the type qFic/qBc could be positive and large in
management of the ecosystem can be seen as pro- value when B-c ! 0, indicating that biodiversity
viding harvesting rules in order to optimize an loss ultimately reduces the growth of surviving
appropriately defined objective function, subject to species in the c-patch. Since each agent treats bio-
the constraints imposed by the dynamics of the diversity outside his patch as fixed, these interac-
resource-based model of species competition. tions are not taken into account in the private
To model the economic management problem, problem. Arguments have been put forward
Brock and Xepapadeas (2002) define an objective (Walker et al. 1999), suggesting that in a particular
function that captures the benefits accruing from the functional group, in an undisturbed ecosystem, one
landscape. A first type of benefit relates to the rev- species serving a particular function tends to
enue yield of species that can be harvested in a given squeeze out other species in the same group. The

 functional group will be characterized by a few
time period. Letting R c ðtÞ ¼ R1c ðtÞ; :::; Rrc ðtÞ 2
dominant abundant species and numerous species
g ( Rrþ denote a vector of harvest of species in with almost zero abundance (which will neverthe-
patch c at time t, the benefits of harvest are defined less be functionally very close to the dominant
by a function V(Hc(t)). They assume that this has the
species). Such minor species act as a kind of ‘reserve
following specific form:
species’. Walker et al. (1999) show evidence for this

 Xn  by looking at heavily grazed areas and lightly
V Hc ðtÞ ¼ i¼1
Pi ðtÞHic ðtÞ  Ci ðHic ðtÞÞ ð19:19Þ grazed areas for the same type of ranchland. In
 MODELLING BIODIVERSITY AND ECOSYSTEM SERVICES 277

heavily grazed areas cattle eliminated the dominant 1/(1 – g) > 1, if g ¼ 1 species are considered as
grass and one of the ‘minor’ grasses took its place. perfect substitutes regarding individuals’ tastes. If
If a shock destroys one or more of the abundant mi is assumed to be very large (tends to infinity),
species, then there is room for the reserve species to then the assumption that the marginal utility of
take their place. When ‘reserve’ species exist, bio- the biomass of a group of species becomes very
large as the biomass becomes very small, reflects
diversity provides resilience, especially for big
the fact that the particular species provides eco-
shocks. Again these effects are not taken into
system services that are essential at the margin
account by private decision-makers. when extinction of the species is near. Alterna-
While some of the services from existing species tively, if species biomass is measured in terms of
are internalized through the F functions, other consumables (as the numeraire), then technologi-
effects, such as flood/erosion problems or con- cal progress that makes consumables more plen-
tamination and salinization of water supplies, bio- tiful relative to species implies that the marginal
diversity loss, spillovers from energy use, are utility of a species near extinction becomes very
predominantly external. For example, erosion and high in terms of consumables. The assumption
flood control damages could be related to the that mi ! 1 can be regarded as an Inada con-
fraction of patches covered with plants which are dition for species biomasses. On the other hand, if
mi ! 0 then the services of the ith species are not
good at erosion and flood control like prairie. Other
valued even if that species is close to extinction. A
external effects associated with ecosystem state may
more general approach could be to think of some
be more direct. Suppose that in the exploitation of species as an invasive pathogen that can spread
an ecosystem, the function V(H) captures net rev- from patch to patch and destroy other species. In
enues from harvesting species (an Millennium such a case if we partition the biodiversity vector
Ecosystem Assessment provisioning service), while into (Bu, Bh), where the indices u, h correspond to
U(B) captures net benefits from the non-consump- useful and harmful species respectively, then
tive use of biodiversity (the sum of the Millennium marginal utilities will be defined as qU u/qBi > 0
Ecosystem Assessment cultural services – aesthetic, and qUh/qBi < 0.
spiritual, scientific, and so on). Since these effects
are external to the representative profit-maximizing 19.6 Conclusions
agent in a c-patch, they can only be taken into
account in the management problem for the eco- The modelling approaches described in this chapter
system if the optimization is carried out by some are far from exhaustive, but they do illustrate the
social planner. ways in which economists are beginning to
The social optimization management problem approach the challenge of modelling biodiversity
then supposes that the flow of benefits is determined change in complex ecological–economic systems.
both by consumptive (harvest) and non-consump- Building on the simple single-species harvesting
tive utility or V(H(t)) þ U(B(t)). Brock and Xepapa- models that still dominate natural resource eco-
deas (2002) assume that U(B) is non-decreasing and nomics, economists are beginning to explore the
strictly concave with qU/qBi ¼ mi  0 as B ! 0+. implications of the fact that the ecosystem – like the
This defines a utility index from biodiversity as: economy – is a general equilibrium system. Its

X
g 
n dynamics are given by the interactions between its
UðBÞ ¼ i¼1
u i ðB i Þ ; g 2 ð0; 1, where the ui(Bi) component parts. While the models described here

g1 have been developed by economists, they build on
are concave utility functions with g u'i ðBi Þ !1
insights from ecology into the implications of bio-
for B ! 0þ for all i. This specific utility index puts a diversity change for the structure, productivity, and
premium on biodiversity since aggregate utility resilience of ecosystems. They also build on a
increases when one more species with positive
growing body of collaborative research involving
biomass is added. Furthermore g parametrizes
both disciplines.
the substitutability among species regarding tastes
for them, since the elasticity of substitution The underlying economic problem remains – to
between the utility derived from any two species is identify allocations that best meet social goals in a
278 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

world where the pursuit of private wealth does not components of the coupled system. Understanding
yield the best outcome for all. However, economists and modelling those feedbacks is a first important
now understand that the gap between private and step in developing strategies for the sustainable use
social optima depends on a complex set of feed- of biodiversity, just as it is for the development of
backs between the ecological and economic plans to manage and restore ecosystems.
PART 4
Summary and synthesis
This page intentionally left blank
 CHAPTER 20

TraitNet: furthering biodiversity

research through the curation,
discovery, and sharing of species
trait data
Shahid Naeem and Daniel E. Bunker

20.1 Introduction: traits and as well as the response of species to environmental

ecosystem functioning change (Grime 1979, Tilman 1982, Huston and
Smith 1987, Brown 1995, Enquist et al. 2003, Brown
Trait-based ecological and evolutionary research
et al. 2004, Navas and Moreau-Richard 2005, McGill
has undergone an extraordinary expansion in the
et al. 2006).
last thirty years (Fig. 20.1), and species traits,
The BioMERGE Research Coordination Network
broadly defined, have been key to advances in
strove to expand biodiversity–ecosystem function-
many fields of natural science (Table 20.1). For
ing research to larger scales by developing models
example, the evolutionary ecology of species’
to predict functioning from species traits (Naeem
niches involves fundamental trade-offs in seed size
et al. (Chapter 1), Duffy et al. (Chapter 5), Naeem
(Moles et al. 2005), leaf economic traits (Ackerly
et al. 2007, Naeem 2008). For example, Solan et al.
2004, Wright et al. 2004), and allometric constraints
(2004) used traits to estimate changes in estuarine
(West et al. 1997). Traits have been used to predict
sediment turnover in the face of biodiversity loss
the risk of species invasions (Veltman et al. 1996,
and Bunker et al. (2005) forecasted changes in forest
Kolar and Lodge 2002, Lloret et al. 2005, Ruesink
carbon sequestration under different management
et al. 2005), the risk of species extinction (Gittleman
practices. Another example is that of McIntyre et al.
and Purvis 1998, Foufopoulos and Ives 1999, Purvis
(2007) who estimated the influence of fish biodi-
et al. 2000a), and crop responses to climate change
versity on freshwater ecosystem functions. These
(Lynch et al. 2004). Table 20.1 summarizes these and
early efforts primarily addressed selection effects
other examples of basic and applied research that
(SE; see Chapter 7) by utilizing traits that predict
are dependent on species trait data.
per capita effects on functioning in combination with
While early efforts to understand the effects of
various traits associated with extinction risk. These
biodiversity on ecosystem functioning focused on
efforts ignored complementarity effects (CE; see
species richness, recent efforts have recognized the
Chapter 7), in part because we still know relatively
role of functional diversity as the driver of these
little about which traits may lead to complemen-
effects (Petchey et al. (Chapter 4), Diaz and Cabido
tarity, but also because species trait data are, at
2001, Petchey et al. 2004b). The functional traits of
best, dispersed throughout the literature, and at
species are the means by which species interact
worst lacking altogether. Indeed, even as the
with their environment, and thus are directly
development of comprehensive vegetation data-
responsible for the effects of species on ecosystem
bases (e.g. VegBank, Center for Tropical Forest
processes (e.g. Gordon 1998, Eviner and Chapin
Science, and SALVIAS) and phylogenetic databases
2003, Kelso et al. 2003, Diaz et al. 2004, Eviner 2004),

281
282 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

1600

1400 Projected

1200
Publications per year

1000

800

600

400

200

0
Figure 20.1 Exponential increase in ecological and evolutionary
1960 1970 1980 1990 2000 2010
research using traits. Results from Scopus search for ((“ecology” or
Year “evolution”) and “traits”).

(e.g. Flora of North America, Tree of Life project) pursue five primary goals: (1) identify key ques-
has proceeded rapidly, trait databases, where they tions and core hypotheses in trait-based research,
exist at all, have remained specialized to particular (2) identify data gaps that hinder the advancement
regions, taxa, or sets of traits. This chapter describes of intra- and inter-disciplinary trait-based research,
TraitNet, a recently established research coordination (3) coordinate the standardization of collection and
network designed to facilitate trait-based research in curation of trait data, (4) build a model database to
general, and this new direction in biodiversity and address core hypotheses, and (5) facilitate the
ecosystem functioning research in particular. development of cross-disciplinary computational
tools for merging, disseminating, and sharing trait
data. There are several core activities, including
20.2 TraitNet: enabling
workshops, online collaboratories, and database
trait-based research
development (Fig. 20.2).
TraitNet aims to facilitate collaboration between TraitNet aims to bring together species trait data
ecologists and evolutionary biologists who utilize from a variety of taxa across different trophic levels
species trait data. Traits are used across a broad and from a variety of habitats and locations to
spectrum of disciplines, including ecology, evolution, address specific interdisciplinary hypotheses (see
and conservation biology. While each discipline has examples below). Our initial coverage will be
developed its own operational definitions, protocols, greatest among terrestrial plants because several
and databases, there is little coordination across dis- plant trait networks are well developed and will
ciplines. Because of these diverse uses and definitions serve as useful starting points (Table 20.2). The
of species traits, TraitNet takes an expansive view of interdisciplinary hypotheses chosen for study by
what may constitute a ‘trait’, including most any the network of participants will likely require traits
character that can be quantified at the individual of herbivores, predators, detritivores, and other
level. We take this approach because, while our efforts trophic groups in addition to traits of primary
are motivated by the need to understand and quantify producers. Additionally, TraitNet will not limit
the traits that drive ecosystem functioning, we intend itself to terrestrial systems. It will also examine
TraitNet to support the broad range of research that aquatic ecosystems or transition habitats such as
utilizes species trait data. wetlands. To that end, we have assembled a group
In order to facilitate this new, cross-disciplinary, of core participants that is weighted towards ter-
collaborative, trait-based research, TraitNet will restrial plant ecologists due to current advances in
Table 20.1 A broad sampling of trait-based research where trait is broadly defined. Note that additional research areas include trait-based taxonomy, trait-based phylogenetics, and morphometrics.

Subject area Description Example traits References

Bioremediation Using species to remediate pollution Heavy metal resistance, specific root length, root Von Canstein et al. 2002, Pulford and Watson 2003,
surface area, root volume and average root Merkl et al. 2005
diameter
Biodiversity and Mechanisms by which changes in biodiversity change Species response and effect traits Lavorel and Garnier 2002, Solan et al. 2004, Bunker et al.
ecosystem ecosystem functioning 2005, Thompson et al. 2005
functioning
Comparative Using phylogenies and traits to understand Traits such as leaf mass per area, seed mass, genome Ackerly 2004, Moles et al. 2005
method evolutionary adaptation size
Community ecology How trait filtering governs community composition Body size, height, leaf traits, trophic position, light Gaudet and Keddy 1988, Weiher and Keddy 1995a,
and structure, including assembly rules, requirements, clonality Weiher and Keddy 1995b, Weiher and Keddy 1999,
competition, facilitation and limiting similarity Ackerly et al. 2002, Suding et al. 2003, Cavender-Bares
et al. 2004, Suding et al. 2005, Grime 2006, McGill et al.
2006
Conservation biol- Estimate threat levels for species or likelihood of Gestation period, range size, number of offspring, Gittleman and Purvis 1998, Foufopoulos and Ives 1999,
ogy extinction trophic position Purvis et al. 2000a
Ecosystem ecology Trait-specific influences of organisms on ecosystem Woody caudices, multi-branched rhizomes, N-fixing Gordon 1998, Eviner and Chapin 2003, Kelso et al. 2003,
processes and biogeochemistry symbiotic associations, C3 or C4 pathway Diaz et al. 2004, Eviner 2004
Gradient analysis Mechanisms and patterns of biodiversity along R*, dispersal mode, reproductive structures, elements Tilman and Wedin 1991, Thuiller et al. 2004
ecological gradients of leaf design
Endemism Determining what traits are associated with Stature, dispersal, pollen/ovule ratios, number of Lavergne et al. 2003, Lavergne et al. 2004
endemism flowers
Fire ecology Predicting fires based on plant traits Resprouting capability, seed bank Saha and Howe 2003, Pausas et al. 2004
Food webs Structure and dynamics of communities governed by Dietary or energy transfer linkages and trophic Layman et al. 2005
trophic interactions position, body size, morphological traits
Functional diversity Identification and quantification of functional All functional traits Petchey and Gaston 2002a, Mason et al. 2003, Botta-
diversity Dukat 2005, Mouillot et al. 2005a, Mouillot et al. 2005c
Guild analysis Grouping species by environmental resource C3, C4, annuals and biennial forbs, ephemeral spring Simberloff and Dayan 1991, Kindscher and Wells 1995,
exploitation irrespective of taxonomy forbs, spring forbs, summer/fall forbs, legumes, Blondel 2003
woody shrubs
Heritability Quantifying the heritability of species traits Various traits Iyengar et al. 2002, Caruso et al. 2005, Garant et al. 2005
Macroecology Patterns of species adaptations at geographic scales Body size, photosynthetic pathway, dispersal Brandle et al. 2002, Burns 2004, Morin and Chuine 2006
syndrome

(Continues)
Table 20.1 (continued)

Subject area Description Example traits References

Metabolic theory of Metabolism as a basis for linking individual Body size, physiological traits, and correlates such as Brown 1995, West et al. 1997, Enquist et al. 2003, Brown
ecology organisms to population, community, and growth, range et al. 2004
ecosystem ecology.
Natural selection How species evolve in response to selective pressure Body size, fledging weight, dispersal syndrome, Boughman 2001, Etterson and Shaw 2001, Merila et al.
palatability, host specificity 2001, Nosil et al. 2002, Beatty et al. 2004, Hoskin et al.
2005
Palaeobiology Using leaf physiognomy to estimate past climate Leaf size, leaf morphology Royer et al. 2005, Royer and Wilf 2006
Plant ecological How plant species ‘secure carbon profit during Leaf-span-per-area, leaf-lifespan Hodgson et al. 1999, Westoby et al. 2002
strategies vegetative growth and ensure gene transmission
into the future’
Population ecology Predicting properties of dynamics (e.g. probability of Body size, age at first reproduction, or number of Fagan et al. 2001, McGill et al. 2006
extinction) offspring
Species invasions Predicting invasiveness of species based on traits Body size, endemism, reproductive rate Veltman et al. 1996, Kolar and Lodge 2002, Lloret et al.
2004, Hamilton et al. 2005, Lloret et al. 2005, Ruesink
et al. 2005
Succession Temporal change in communities predicted by traits Respiration rate, seed number, growth rate, Grime 1979, Tilman 1982, Huston and Smith 1987, Navas
maximum life span, induced dormancy, R*, stress and Moreau-Richard 2005
tolerance
Unified neutral Trait neutral core patterns in distribution and Dispersal, growth rates Hubbell 2001, Nee and Stone 2003, He and Hu 2005,
theory of abundance forms contrasting hypotheses to Hubbell 2005, Ostling 2005, Wootton 2005
biodiversity and trait-based patterns
biogeography
 TRAITNET: FURTHERING BIODIVERSITY RESEARCH THROUGH THE CURATION, DISCOVERY 285

larify key question

1. C tify data ga s
Information 2 . Iden s p
Definitions, theory,
inate standard
hypotheses, and o ord model d izatio
C d atab n
protocols. 3. . Buil ase s
4 s
Publications
training seminars
k
an
ent of TraitB

Working

Test and eval

TraitNet Groups
opm

Figure 20.2 Architecture of TraitNet. Five objectives

Facilitate structure TraitNet, an NSF-funded Research Coordination
v el

ua
the formation of Network that coordinates the development of cross-
te
e
ed

TraitBank
pr
ot
th ot disciplinary trait-based research. Working groups consist of
ate yp
ilit e members across trait-based disciplines that will collectively
5. Fac
clarify key questions within and across disciplines, identify
data gaps, coordinate standardizations, and build model
databases to test hypotheses that emerge from syntheses.
Data
Working groups will provide workshops and training
Submission and retrieval
(conversion, sessions to broadly disseminate TraitNet results. Finally,
permissions, TraitNet will coordinate the design of a prototype universal
classification)
database entitled TraitBank.

the field, but which also includes researchers who that a small number trade-off axes can explain the
specialize in insect, mammalian, microbial, aquatic, majority of variation in plant form and function
and disease ecology. These core participants are (Grime 1979, Coley et al. 1985, Charnov 1997, Reich
actively recruiting additional investigators within et al. 1999, Hubbell 2001, Westoby et al. 2002, Wright
their respective areas of expertise. TraitNet partici- et al. 2004). How are species life histories con-
pation is expected to grow substantially as we strained by these fundamental trade-offs, how
identify additional researchers who focus on other many axes of differentiation exist, and how does the
habitats, taxonomic groups, and trophic groups. extent of these trade-offs vary across environmental
Hypotheses derived from cross-disciplinary re- gradients and among biomes? These key questions
search are often characterized by a scope that require data on multiple traits, collected from mul-
requires multiple traits collected uniformly from a tiple species, from multiple sites, and standardized
diversity of species across widely dispersed locali- when different protocols were used.
ties. The TraitNet working groups will explore and
Mechanisms of exotic species invasions. The success
identify such hypotheses, determine data needs and of invasive species has often been attributed to an
gaps, develop and test model datasets for addres- escape from natural enemies, whereby one would
sing these hypotheses, and coordinate the estab- predict successful invaders to have ‘better’ traits
lishment of trait databases, guidelines, and training than the native species they displace, such as greater
for their use, and enable a variety of multidisci- height, lower R*, or lower construction costs (Miller
plinary research activities. As Table 20.1 illustrates, and Werner 1987, Gaudet and Keddy 1988, Nagel
the potential number of cross-disciplinary approa- and Griffin 2001, Seabloom et al. 2003, Bunker 2004).
ches is very large. Here we provide three of the Alternatively, the success of some invaders has been
many possible hypotheses TraitNet will explore: attributed to novel traits, such as nitrogen fixation
(Vitousek and Walker 1989) or allelopathic effects

Dimensionality of life-history trade-offs. While an (Bais et al. 2003), that allow them to dominate new
endless number of traits can be measured on indi- habitats. While both mechanisms certainly play a
viduals and species, many traits are highly corre- strong role, the relative importance of each in
lated with one another, and it has been suggested driving species invasions is not clear. An effective
286 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

Table 20.2 Examples of databases that include trait data. Current collaborators in bold.

Database name Description

BiolFlor Focuses on the German flora and includes > 60 traits and > 3600 plant species
BioPop Database of plant traits of the Mid-European flora including 60 traits and > 4,700 species
Center for Tropical Forest A newly initiated effort to collect functional trait data for 6,200 tree species found in 18 large forest dynamics plots
Science Trait Database located in 14 tropical countries
Ecological flora of the British Database of plant traits of the flora of the British Isles including > 130 traits and > 1700 plant species
Isles
Ecological flora of California A database of ecological characteristics, including life history, phenology, morphology and other traits for the
California flora. Under development by David Ackerly
FishBase Worldwide fish species database with more than 29,000 species
Glopnet Global compilation of leaf economic traits from > 2500 plant species. Initiated by Peter Reich, Ian Wright, and
Mark Westoby
Hawaii Plant Trait Database A database of systematic, biogeographic, functional, physiological, and ecological data for Hawaii’s native and
alien flora. Initiated by Rebecca Montgomery, Lawren Sack, Becky Ostertag, Susan Cordell, and Jon Price
LEDA Traitbase Focuses on the Northwest European flora and plant traits that describe three key features of plant dynamics:
persistence, regeneration, and dispersability
NatureServe Explorer Conservation data on more than 50,000 plants, animals, and ecological communities of the USA and Canada
NatureServe InfoNatura Conservation information on the more than 5,500 birds, mammals, and amphibians of Latin America and the
Caribbean
Seed Information Database, Database of seed characteristics, including storage behavior, weight, dispersal, germination, oil content, protein
Kew Botanic Garden content, morphology, for several thousand plant species, with plans to include > 24,000 species
TRY Global plant trait database to develop new plant functional classifications for earth system modelling
USDA PLANTS The PLANTS Database provides standardized information about the vascular plants, mosses, liverworts, hornworts,
and lichens of the USA and its territories. It includes names, distributional data, characteristics, images, and crop
information

test would require species trait data on plant 20.3 The challenges of data integration
invader species, on the native species they may
Much of what TraitNet aims to accomplish will rely
displace, on palatability to native herbivores, and
on integrating data from disparate sources. Inte-
data on traits of potential natural enemies such as
grating disparate data is a complex process with
body size, diet, and growth rate.
many challenges. These challenges are not trivial.

Predicting species, community and ecosystem res-
Here we outline the main issues and describe our
ponses to global change. Predicting the response of
approach to addressing them. In order to meet
species to climate change, pollution, and land use
these challenges, we have included several infor-
change is a key challenge to ecologists. These pre-
matics experts in our group of core participants,
dictions could be developed by correlating species
representing several organizations including the
traits with either observed responses to global dri-
Science Environment for Ecological Knowledge
vers or across natural environmental gradients. In
project (SEEK), the Pacific Ecoinformatics and
either case trait data from a wide variety of species,
Computational Ecology Lab, the National Center
across multiple trophic levels, from a variety of
for Ecological Analysis and Synthesis (NCEAS), the
habitats would be required. Similarly, predicting
National Evolutionary Synthesis Center, and the
the effects of these global drivers on ecosystem
Microsoft European Science Initiative. To address
function will require additional trait data that
our Core Hypotheses, we will build a model data-
mechanistically link species with their per capita
base that also will serve as a training ground for
effects on ecosystem functioning (Etterson and
building a fully accessible and open source trait
Shaw 2001, Solan et al. 2004, Bunker et al. 2005).
data archive termed TraitBank.
 TRAITNET: FURTHERING BIODIVERSITY RESEARCH THROUGH THE CURATION, DISCOVERY 287

20.3.1 Intellectual property rights the lumped species cannot be assigned to any one
of the split species, and a trait value measured on
Intellectual property rights are a critical issue for any
one of the split species cannot be assumed to rep-
research network and even more so when data
resent the entirety of the lumped species. In addi-
are aggregated from multiple sources. Trait-based
tion, species are often cited with only the name
research progresses best when data sharing is maxi-
authority, but not the underlying taxon concept
mal, but currently the sharing of raw data is not
reference. For these reasons, taxonomic names by
common except within groups. Workshops, colla-
themselves cannot be considered a unique index for
boratories, training sessions, and the TraitNet website
TraitNet datasets. This obstacle applies to all data
will provide a forum for discussion of the many issues
that are specific to individual species, such as
surrounding intellectual property rights and how
GenBank and VegBank.
they would affect database tools, resources, and the
Fortunately, efforts are under way to address this
design and implementation of TraitBank in the future.
complex issue. The SEEK Taxon project has created an
To that end, we propose that data owners will
internationally accepted standard for taxonomic data,
retain full rights and full control over their data.
the Taxonomic Concept Schema (TCS), and work is
TraitNet will facilitate collaborations between parti-
under way to implement the Taxonomic Object Ser-
cipants that would otherwise be less likely to occur.
vice (TOS), a repository and web service allowing for
Our model database will be fully searchable, whereby
translation between taxonomic concept authorities
one could search for all available traits for a particular
(Graham and Kennedy 2007). TraitNet will collabo-
species, or all species with a particular trait, or for a set
rate with SEEK Taxon to ensure that our database
of traits among a set of species. If participants so
schema will function with the TOS when it is fully
choose, we can set up the search system to return only
functional and populated with taxon concepts.
whether the data exist, and who owns the data. It
To ensure that TraitNet data will be compatible
would then be up to the participant to contact the data
with TOS, TraitNet will require that participants
owner and propose collaboration.
include name authorities and taxon concept refer-
ences, as well as subspecies when appropriate, in
their data submissions. Only in this way can we
20.3.2 Taxonomic standardization
specify, for each record, the taxonomic concept
Definitions of biological taxa change with taxo- upon which the measurement was taken. For
nomic revisions over time. For instance, a single instance, a full taxon concept reference might be:
species may be split by one revision into several “Aus beus Sarg. 1893 Smith 1989,” where Smith
species, and then lumped back into a single species 1989 is a link to the reference in which the concept
in subsequent revisions. A trait value measured on is described or defined (Fig. 20.3).

Datum Environmental
Taxon
observation metadata

Trait
observation
Taxon Location ppt
concept habitat temp
Measurement Trait Figure 20.3 TraitNet trait observation
biome PET schema. The ideal trait observation will
units concept
Taxon include critical metadata, such as trait
Taxon protocols, taxon concepts and environ-
name
concept Individual mental data. These metadata will make
authority Field,
reference Trait size, age, trait observations robust to various future
protocol garden, or
etc. uses of the trait data and thus ensure the
Taxon greenhouse
name longevity and usefulness of trait data
collections.
288 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

20.3.3 Trait protocol standardization However, future investigators may ask how wood
density varies within species at a given site, within
Variations in collection protocols introduce chal-
species across environmental gradients, among
lenges that are similar to those introduced by tax-
species, among size classes, or even throughout the
onomic revisions. A trait concept may remain fixed,
year. To ensure that a given trait observation con-
but the protocol used to quantify the trait may
tains maximum scientific value, the collector will
change as new protocols are introduced. A trait
want to document explicitly the conditions under
database must be able to incorporate revised trait
which it is collected, including latitude and longi-
collection protocols as they are developed to ensure
tude, habitat, individual age or body size, time and
that data produced though all protocols for a given
date of collection, etc. Many trait observations, such
trait concept are quantitatively comparable. For
as wood density, require substantial effort and/or
example, wood density is the trait concept of mass
expense to collect. Only minimal additional effort is
per unit volume. However the protocol to collect
required to collect substantial metadata that will
wood density varies. Wood mass may be measured
ensure that a trait observation has lasting scientific
on oven-dry wood samples or on air-dried samples
value (Fig. 20.3).
with 12–15 per cent moisture content. Both metrics
Finally, an ideal network environment would also:
quantify wood density, but data from air-dried
(1) allow for automated integration of trait data
samples must be corrected to account for the
contributions; (2) include a web-enabled search
moisture content. TraitNet will define trait concepts
engine that would allow user-friendly access to the
and associated trait collection protocols. Each trait
general public, including students, educators, and
protocol for a given trait concept must be quanti-
policymakers; and (3) enable seamless access to
tatively comparable (Fig. 20.3).
related community, phylogenetic, and environmen-
tal databases.
As the understanding and appreciation of func-
20.4 Integrating TraitNet into ongoing tional biodiversity grows among the public, Trait-
ecoinformatics frameworks Bank has the potential to be much more than a
TraitNet will build on current ecoinformatic efforts resource for natural scientists. For example, a birder
to address these issues. Ecological Metadata Lan- may wish to learn more about the functional traits
guage (EML) has been developed by NCEAS’ of a group of species found at a particular site, or a
Knowledge Network for Biocomplexity project and farmer or natural resource manager might want to
is widely considered the standard for documenting gain additional insights into the types of weeds or
metadata for ecological datasets. The SEEK project invasive species found on site. A teacher on a field
has extended and formalized critical aspects of trip may wish to design an exercise based on local
EML in the Observation Ontology (OBOE), a formal species, or a student may require trait data for their
model of scientific observations that includes trait paper or science project. In this way, TraitBank will
measurements (Madin et al. 2007, Madin et al. 2008). offer the public detailed trait data for individual
Thus TraitNet will use and extend EML to specify species, and thus augment existing resources such
the Taxon Concepts, Trait Concepts, and associated as the Global Biodiversity Information Facility
environmental data outlined in Fig. 20.3. Eventu- (http://www.gbif.org/).
ally, these trait concepts will be included in SEEK’s
formal ontologies such as OBOE.
20.5 Species traits, functional diversity,
Because species trait data are used for such
and the future of biodiversity research
diverse research ends, the data must be collected
and archived with sufficient metadata to ensure TraitNet is designed to coordinate a wide array of
wide applicability to potentially unforeseen scientific disciplines that are centred on a specific
research questions. For instance, an investigator research theme but would benefit enormously from
may collect wood density data with the intention of cross-disciplinary coordination. TraitNet will facili-
calculating above-ground biomass at a given site. tate cross-disciplinary research among ecological
 TRAITNET: FURTHERING BIODIVERSITY RESEARCH THROUGH THE CURATION, DISCOVERY 289

and evolutionary fields centered on trait-based both natural and managed ecosystems (Naeem
research. All of these diverse activities rely strongly et al., Chapter 5; Jackson et al., Chapter 13). Indeed,
on understanding the functional characteristics, or this shift towards trait-based ecology and func-
traits, of species. It is only through these traits that tional diversity will bring a new perspective on
scientists can understand and predict the responses biological diversity to a wide array of funda-
of species to their environment as well as species mental and applied scientists, students, and edu-
effects on ecosystem functioning and the ecosystem cators in ecology, evolution, and environmental
services that humans increasingly demand from biology.
 CHAPTER 21

Can we predict the effects of global

change on biodiversity loss and
ecosystem functioning?
Shahid Naeem, Daniel E. Bunker, Andy Hector, Michel Loreau,
and Charles Perrings

21.1 Efficacy, practicability, ecosystem functioning research, but the efficacy of

and social will the idea that the diversity of life, not just its mass,
influences both the biogeochemical and biotic prop-
The efficacy and practicability of an idea, and the will
erties of ecosystems, is well established. Even in
of individuals or society to explore it, determine whe-
1997, although they guessed a stronger, less complex
ther it catalyzes change or merely enters the vast store
role for diversity than meta-analyses would even-
of quiescent ideas that make up the bulk of humanity’s
tually support (Chapter 2), researchers had the
collective wisdom. As we noted in the Introduction, the
right sense of things with just a small number of
idea that biodiversity influences ecosystem function-
studies to hand. The rapid rise in numbers of
ing is not new. There are, for example, similarities
studies (Chapter 2), their influence on the literature
between the Hortus Gramineus Woburnensis experiment
(Chapter 3), incorporation of the idea into the Mil-
of 1817 (Hector and Hooper 2002) and BIODEPTH
lennium Assessment framework (Millennium Eco-
experiments (Hector et al. 1999) almost two centuries
system Assessment 2003), and the achievement of
apart. The Hortus Gramineus, however, was nearly
scientific consensus (Loreau et al. 2001, Hooper et al.
forgotten. Perhaps it was forgotten because the idea of
2005), all suggest that today the efficacy of the idea is
improving yield by manipulating vegetation gave way
no longer in doubt. Many questions concerning
in the 1840s to Justus von Liebig’s idea that yield was
mechanisms, generality, and the relative strength of
controlled by the availability of limiting mineral
biodiversity effects compared to other factors that
nutrients. In contrast, in the 1990s, individual and
influence ecosystem functioning, such as tempera-
social concerns over the environmental consequences
ture, precipitation, ocean depth, and physical sub-
of worldwide changes in biodiversity raised questions
strate, remain, but few question that changes in
about ecosystem functions in general, not just yield
biodiversity influence ecosystem functioning.
(Loreau et al. 2002). Because primary production is a
Although efficacy may be less of an issue than it
convenient measure of ecosystem functioning, it has
was in the 1990s, practicability and societal will
been emphasized in biodiversity and ecosystem func-
remain significant challenges. By practicability we
tioning work, which creates the uncanny resemblance
mean the ability to test the idea empirically and
between modern experiments and the Hortus Grami-
translate it into real-world applications, and by
neus. Although biodiversity and ecosystem function-
societal will we mean the willingness of individuals
ing research shows no sign of abating some 15 years
and society to adopt the idea as a foundation for
later, we might nevertheless ask whether it too will be
decision-making. In this chapter, we look across the
forgotten like the Hortus Gramineus?
many contributions in this volume and consider a
As in all science, there remain differences among
few messages the current field of biodiversity and
researchers on the interpretation of biodiversity and

290
 CAN WE PREDICT THE EFFECTS OF GLOBAL CHANGE 291

ecosystem functioning research give us concerning empirical ecology, establishing some of the largest
efficacy, practicability and societal will. (e.g. Roscher et al. 2005, Spehn et al. 2005, Tilman et al.
From a rich set of cross-cutting ideas embodied in 2001) and most elaborate micro- and mesocosm
this book we focus on just three that are shaping the studies ever conducted (e.g. Naeem and Li 1998,
trends in biodiversity and ecosystem functioning McGrady-Steed et al. 1997, Downing and Liebold
research. First, concerning efficacy, there is a struggle 2002, Fukami and Morin 2003, Fox 2004a, Bell et al.
in the discipline to make the research more realistic. 2005b, Cadotte and Fukami 2005). The trend of
Unfortunately, what constitutes realism in ecology increasing the size or the number of replicates and the
can sometimes be subjective, thus if biodiversity and complexity of experimental design reflects attempts
ecosystem functioning research is to avoid another to continuously improve experimental realism.
round of debate, further clarity on the issue of realism Increasing plot size, for example, is based on the
is needed. Second, concerning practicability, we notion that, in nature, some ecological processes
revisit the Millennium Assessment’s framework and operate at larger scales. Likewise, the use of microbial
restructure it based on current empirical and theore- communities whose small spatial scales can be readily
tical findings. Our hope is that this modified frame- accommodated using bottles and Petri dishes, allows
work points the way to practicable, coupled, for multiple generations. The presumption here is that
natural–social research and policy. Finally, in order to multiple generations better approximate the temporal
facilitate individual and societal will, we provide a scale at which ecological processes operate in nature
graphical device that may better communicate the (Petchey et al. 2002, Raffaelli et al. 2002). Microcosms
core idea of the importance of biodiversity to also allow for much more community and trophic
ecosystem functioning and link it more directly to complexity, again presuming that greater complexity
sustainable development. We suggest that the pres- better approximates nature (Petchey et al. 2002, Raf-
ervation, management, and intelligent use of bio- faelli et al. 2002). Exploration of different types of
diversity may be our only hope for achieving systems, such as wetlands (e.g. Engelhardt and
environmental sustainability which, in turn, is our Ritchie 2001), estuarine (e.g. Duffy et al. 2005) and
only hope for achieving overall sustainable develop- marine ecosystems (e.g, Emmerson et al. 2001, Sta-
ment and its many goals (e.g. the United Nations’ chowicz et al. 2002, Bracken et al. 2008), and organisms
Millennium Development Goals) of social and eco- other than plants, such as fungi (e.g. Tiunov and
nomic equity across the globe. Scheu 2005, Van der Heijden et al. 1998), soil fauna
(e.g. Mikola and Setälä 1998), and zooplankton (e.g.
Norberg 2000), also reflects attempts to test the gen-
21.2 Efficacy and realism in
erality of findings. With every year, the cumulative
biodiversity research
range of spatial and temporal scales, community
Since its inception, biodiversity and ecosystem func- complexity, and the scope of taxonomic and ecologi-
tioning research has sought to encapsulate the key cal diversity explored by biodiversity and ecosystem
elements of biodiversity and ecosystem functioning in functioning research has grown.
its theory and experiments, but every study has been The question of realism, however, continues to
hounded by the question of realism. The full com- dog biodiversity and ecosystem functioning
plexity of biodiversity, whose ecological and evolu- research (Raffaelli 2004). Clearly one should put
tionary processes scale from microscopic to planetary, more stock in the findings of a more realistic
can never be entirely captured in any one experiment, experiment, but how does one evaluate realism in
nor does it have to be. Rather, researchers ask focused ecological experiments? There are two features of
questions and make decisions about what is and is not biodiversity and ecosystem functioning studies that
necessary to test a particular idea. Even focused determine how comparable they are, both of which
questions about biodiversity and ecosystem func- are determined by a large number of decisions that
tioning, however, require fairly elaborate experiments researchers make when conducting their studies.
(see Chapters 2 and 7). Research in biodiversity and First, in any biodiversity and ecosystem functioning
ecosystem functioning has pushed the envelope of study, researchers must decide what biodiversity
292 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

gradient is appropriate for the question they wish to selecting only biogeographically coherent sets of
address. Decisions concerning the biodiversity species (i.e. only sets of species observed to co-occur
gradient include: in nature), to using all species in an ecosystem.
In silico studies represent a recent, promising trend
1) choosing the appropriate measure of diversity,
in biodiversity and ecosystem functioning experi-
2) determining the size of the species pool to be
ments, but their gains in realism made possible
used in the experiment,
through enormous numbers of replicates come at the
3) establishing the low-diversity endpoint (most
cost to realism in estimating ecosystem functioning.
often monocultures) and
In silico studies, such as those by Solan et al. (2004),
4) establishing the high-diversity endpoint of the
Bunker et al. (2005), McIntyre et al. (2007), and
gradient (most often all species in the pool).
Bracken et al. (2008) can generate thousands to
Biodiversity gradients in experiments range from millions of species combinations, thereby eliminating
high-diversity end points that are simply conve- the practical constraints of field research that is often
nient (e.g. the 16 plant species out of over 800 at limited to hundreds of species combinations. In silico
Cedar Creek, Minnesota, were selected in part experiments require researchers to make the same
because they were known to do well in experi- decisions concerning species selection and the bio-
mental settings and seeds were commercially diversity gradient, but with fewer constraints on the
available; S. Naeem, pers. comm.) to high-diversity size of the species pool, the number of levels of
endpoints that contain as many species as possible biodiversity, and the number of replicates. Ecosys-
in abundances commonly observed in the field (e.g. tem function, however, must be estimated, which is
when the high-diversity endpoint is an unmanipu- usually done by algorithms that translate individual
lated plot). Low-diversity endpoints are often sim- species abundances and functional traits into likely
ply monocultures, but here too one may elect to set ecosystem function, and it is here where uncertainty
the low-diversity endpoint at a higher richness level lies. Current in silico experiments ignore the multiple
(and use monocultures only to calculate null pre- interactions and modes of functional complemen-
dictions, as reviewed in Chapter 7). tarity between species, and hence have other lim-
Second, researchers must also make decisions itations regarding realism. In silico experiments will
concerning species selection, or which species should become more realistic and accurate as we develop a
be observed or manipulated, since it is generally greater understanding of the mechanisms of com-
not possible to study every species, especially plementarity and better data on the species traits
microorganisms, in ecosystems. Decisions concern- that lead to them (Chapters 5 and 20).
ing species selection include: Considering the biodiversity gradient and species
selections of multiple studies provides a basis for
1) whether or not one should include exotics
comparing studies. Figure 21.1 graphically illus-
(naturalized, domestic, invasive, or other non-
trates how studies relate to one another. The end-
resident species);
points of the biodiversity gradient axis reflect
2) what range of biotic interactions should be
extremes in decision making by researchers. ‘Fully
included among the selected species (i.e. should
combinatorial’ refers to an experiment that uses
predators, diseases, mutualists, and other interact-
every possible combination of species possible,
ing species be used or just competitors for the same
irrespective of what is found in nature. ‘Trait-based
limiting resources); and
extinctions’ refers to experiments in which combi-
3) whether the subset of species should be selected
nations are constrained to those in which the pres-
at random or based on some other criteria, such as
ence or absence of species is determined by the
commonness, cultivability, or traits related to the
particular traits of species. For example, for an in
likelihood of extinction.
silico study of mammalian bush meat production,
Species selections in experiments range from where body size determines probability of extirpa-
investigators using whatever is convenient (e.g. tion by hunting, the gradient will range from spe-
whatever can be cultivated or manipulated), to cies-rich communities with both small and large
 CAN WE PREDICT THE EFFECTS OF GLOBAL CHANGE 293

that the value of realism is its ability to provide a

Trait-based
extinctions System-driven
(‘Realistic’) reference for our findings, not to pass judgement on
the efficacy of a study. The day may come when
Biodiversity Gradient

In silico simulations
several million field plots, each fifty hectares in size,
Removal experiments
have had their diversity manipulated across every
Field experimental plots trophic level according to trait-based extinction
scenarios and at densities observed in nature, and
Mesocosms
both microbial to macrobial species are manipu-
Microbial microcosms lated, and run for a century or more. Such an
combinatorial

Theory-driven
experiment might be hailed as the ultimate realistic
(‘Abstract’) study, but it might not be the most efficient and
Fully

economical way to do science, and so laboratory

Arbitrarily Biogeographically
assembled informed
microcosm and in silico experiments would not lose
their value.
Species selection

Figure 21.1 The biodiversity gradient and species selection of different 21.3 Biodiversity, ecosystem
kinds of studies in biodiversity and ecosystem functioning research. Each
study makes decisions concerning how it establishes the gradient in bio-
functioning, and human wellbeing
diversity it explores as well as how it selects species. See text for discussion. The biodiversity ! ecosystem functioning ! eco-
system services ! human wellbeing framework of
the Millennium Assessment was a brilliant synthesis
sized animals to communities composed only of that united the natural and social environmental sci-
small sized animals, as large mammal populations ences by linking biodiversity, ecosystem processes,
will decline first in response to hunting pressure ecosystem functioning, and the services of ecosystems
(Cardillo et al. 2005). (see Introduction, Chapter 1). For the first time, it made
The endpoints of the species selection axis in it possible to see ecosystems as social assets whose
Fig. 21.1 consist of studies in which species were value lies in the flow of social benefits (services) they
selected by the researcher because they were con- yield. Although invaluable as a conceptual frame-
venient (e.g. common and cultivable) or through work, however, it is too simplistic to serve as a guide
other arbitrary decisions to selecting combinations for the development of practical biodiversity-based
of species currently found co-occurring in nature or solutions to environmental problems. The biodiver-
which are likely to be found in the future after sity and ecosystem functioning research reviewed in
extinction takes its toll. ‘Theory-driven’ studies are this volume suggest two areas that need to be refined.
often typified by biodiversity gradients and selec- First, the biodiversity ! ecosystem functioning part of
tion well suited to testing the theory, but are per- the Millennium Assessment conceptual framework
haps not reflective of what is observed in nature. needs to recognize the interdependency between the
‘System-driven’ studies tend to be closely modelled biotic and abiotic (the biological and geochemical)
on the ecosystem under investigation. Obviously, components of the system and its functioning. The
all experiments have their virtues, but whether their value of ecosystems lies in their capacity to deliver
findings refer broadly to theory or more specifically services. Since the supporting services identified in
to particular ecosystems depends on the biodiver- the Millennium Assessment are just the processes that
sity gradient and species selection of the study. We underpin ecosystem functioning, they are an integral
observe that there is a tendency to consider ‘real- part of the ecosystem as an asset – a functional unit.
ism’ in studies that are more system-driven. The supporting services accordingly need to be con-
The biodiversity gradient and species selection sidered separately from regulating, provisioning, and
properties of experiments make clear that realism in cultural services (see Chapter 18 for a detailed treat-
biodiversity and ecosystem functioning research is ment of ecosystem services). Second, while the con-
a complex issue. Our deliberations here illustrate ceptual framework provides a nice link between
294 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

ecosystem services and human wellbeing, it does not framework, stocks are functioning ecosystems and
reflect the critical importance of globalization – the flows are the services those systems yield. The ele-
closer integration of human society through trade and ments within the system comprise the biotic and
interactions among human populations. The inter- abiotic (atmospheric, lithospheric, and hydrospheric)
connections between ecosystem services at different pools of carbon, nutrients, and water, together with
spatial and temporal scales turn out to be highly the plants, animals, and microorganisms that move
sensitive to the degree of globalization. A variant of carbon, nutrients, and water into and out of these
the Millennium Assessment framework that reflects biotic and abiotic pools.
these concerns is illustrated in Fig. 21.2 and we If one eliminates the biota in the ecosystem, as we
explain these modifications below. did in the thought exercise in the Introduction, the only
The ecosystem as a functional unit. The assets from fluxes in the pools of carbon, nutrients, and water
which humans extract provisioning, cultural, and would be those induced by geochemical processes. In
regulating services are functioning ecosystems. a system with both biotic and abiotic elements, these
These comprise both abiotic and biotic components, fluxes are modified by biological processes. The
and biogeochemical processes that underpin ecosys- resulting ecosystem processes are the basis for the
tem functioning. In the absence of biological processes flows of interest to human societies: the provisioning
on Earth, geochemistry governs surface conditions as and cultural services, and their variability (the regu-
on any planet. The inclusion of biological organisms lating services). We note that flows, in this sense, are
alters geochemical processes. In this modified not generally the same as fluxes in pools of carbon,
Integrated global economy

Effects of linkages through trade, transport, and travel

Provisioning services Provisioning services

Cultural services Cultural services
Regulating services Regulating services
Ecosystems

Supporting services Supporting services

Biotic: Abiotic: Biotic: Abiotic:

plants CHN plants CHN
animals OPS animals OPS
microbes microbes
Ecosystem i Ecosystem j
Hydrosphere
Atmosphere

Effects of linkages on the general circulation system

Figure 21.2 A coupled social–natural biodiversity and ecosystem functioning framework. Individual ecosystems worldwide, such as ecosystems i and
j in this figure, are inextricably linked, both by market forces in the global economy and by biogeochemical fluxes through the atmosphere and
hydrosphere. While more complex than the Millennium Assessment’s framework, it eliminates ambiguities and facilitates integration of research, analyses,
and policy development. See text for further explanation.
 CAN WE PREDICT THE EFFECTS OF GLOBAL CHANGE 295

nutrient, or water. They are the benefit streams yiel- particular ecosystem services, it reduces the cost of
ded by durable assets – functioning ecosystems in this running down the associated assets – the ecosys-
case. It follows that the Millennium Assessment’s tems themselves. One manifestation of this is the
supporting services are distinct from the other eco- ‘roving bandit’ phenomenon in the exploitation
system services in that they are elements of the of open ocean fisheries, which has led to the
functioning ecosystems that yield the other ecosystem sequential depletion of one fish stock after another
services as flows. By analogy, an automobile is a (Berkes 2005, Worm et al. 2006). Another mani-
system whose components include a large number of festation is the substitution between, for example,
parts organized so as to yield a flow of personal food sources. So reductions in West African fish
transport services. The value of a functional auto- supplies due to overharvesting have increased
mobile is greater than the sum of its parts. The demand for bush meat as an alternative source of
transport services it yields depend, inter alia, on the protein (Brashares et al. 2004). The role of the
combustion processes occurring within the engine. integrated economy in affecting local ecosystems is
Like the Millennium Assessment’s supporting ser- captured in the trade-mediated feedbacks between
vices, combustion processes help make the vehicle those systems in Fig. 21.2.
functional. In most managed ecosystems, the sup- As the chapters in Part 3 all indicate, and espe-
porting services may be tailored to the production of cially Chapters 17–19, a more synthetic framework
specific services, either through direct modification of is needed if we are to move forward on finding
biogeochemical processes or indirectly through biodiversity-based solutions to environmental pro-
modifications of biodiversity, which influence bio- blems. Brock et al. (Chapter 19) note: ‘economists
geochemical processes. In Fig. 21.2 we therefore now understand that the gap between private and
depict these Millennium Assessment ‘services’ as social optima depends on a complex set of feed-
structuring elements of ecosystems. backs between the ecological and economic com-
Globalization and the closer integration of the bio- ponents of the coupled system’. Understanding the
sphere. Humans impact their local biota through pathways and feedbacks that link biogeochemical
direct exploitation of local ecosystems, but they also (i.e. ecological) and social (i.e. economic) systems is
impact biodiversity outside their geographic critical to the development of practicable solutions
boundaries through the indirect impacts of trade, to environmental problems that involve biodiver-
transport and travel (Chapter 17, but see also Kohn sity change of one kind or another.
and Capen 2002, Perrings et al. 2002). For example,
China’s increasing demand for natural resources
21.4 Implications for sustainable
affects its own biodiversity both directly, through
development
the exploitation of resources in China, and indi-
rectly, through the effect of species introduced What is the main message of biodiversity and eco-
along with resources imported from other parts of system functioning research? Can it be effectively and
the world. At the same time, imports to China affect clearly communicated to the public and policy-
biodiversity in the exporting countries through the makers? Is it likely to resonate with their perceptions
indirect impact they have on, for example, rates of of the environmental dimensions of a sustainable
land conversion (and biodiversity loss) in those development strategy?
countries (Aide and Grau 2004), while exports from The main message from this volume, but particularly
China to bioclimatically similar trading partners from Part 3, is that biodiversity conservation is an
increase the risks that accompanying species will essential element in any strategy for sustainable devel-
establish and spread in those countries (Costello et al. opment. In 1987, Our Common Future, also known as
2007). The same mechanisms operate for all trading the Brundtland Report (World Commission on
countries. Environment and Development 1987), laid down a
Closer integration of world markets has another convincing argument that the benefits to humanity
important impact on local biota. By increasing of the last century’s economic development were
the number and accessibility of substitutes for tremendous, but that they were experienced largely
296 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

by rich developed nations and came at the cost of culture, and social structure of people. Humans ben-
severe depletion of the world’s natural capital. efit from natural capital directly (e.g. natural resource
The goal of sustainable development currently extraction, such as lumber or fish harvesting) or indi-
enjoys an enormous subscription among policy- rectly (e.g. processing lumber in sawmills or trans-
makers (e.g. World Commission on Environment forming landscapes into agricultural systems). Fossil
and Development 1987, Reid 1989, Annan 2000, resources, such as petroleum, natural gas, and aquifers
National Research Council 2000, Kates et al. 2001, of fossil water, can supplement natural resource
Folke et al. 2002, Raven 2002, Sachs 2004). The inputs, but renewal of these resources is so slow
largest international summits in human history, the (tens of thousands to tens of millions of years) that
UN Conference on Environment and Development, they are best considered as non-renewable. Essen-
also known as the Earth Summit, held in Rio de tially, humanity controls the levers that open or close
Janeiro in 1992, and the 2002 World Summit on the flow of energy, nutrients, and water to either
Sustainable Development in Johannesburg, were manmade or natural capital.
centred on the ideas of sustainable development. Sustainable development requires that the value
The UN Convention on Biological Diversity and the of all three sets of assets is not declining over time.
Millennium Assessment are also founded on the It allows for substitution between the different
idea that biodiversity conservation is essential for forms of capital, but respects the fact that there are
achieving sustainable development. This has stim- not manmade substitutes for all forms of natural
ulated an intense effort to understand the scientific capital. It also respects the fact that ecosystems, like
implications of the concept (Clark 1987, Kates 2001). human technology and preferences, evolve over
Communicating a complex message simply. The time. Hence sustainable development involves a
Brundtland Commission’s call to abandon develop- strategy that builds the aggregate wealth of coun-
ment by unsustainable spending of natural capital tries whilst allowing for their evolution. Biodiver-
was essentially a call for biodiversity conservation in sity is critical in this for three main reasons.
some measure to secure ecosystem services. It has First, a mix of species enhances the functioning of
been interpreted as a call to protect the value of ecosystems and hence the value of those systems,
natural capital, where natural capital comprises both regardless of the state of nature. That is, in any
the biotic and the abiotic components of the natural given state of nature, any positive diversity–
environment. In the wake of the Millennium functioning relationship that does not rely on
Assessment we can think of the world’s ecosystems sampling effects (i.e. that enhances the efficiency of
as being amongst the most important elements of resource exploitation through niche partitioning)
this. It thus includes biodiversity – the mix of plants, implies complementarity between species. So too
animals, microorganisms – and the ecosystem pro- does any obligate or symbiotic relationship between
cesses it supports. Most ecosystems have been species. The complementarity between species in
shaped or at least impacted by human actions, but this sense, like the complementarity between factors
all still rely on a set of processes that are indepen- of production in economic systems, enhances the
dent of human action. Man may have structured the productivity and hence value of ecosystems.
system to promote or reduce particular processes, Second, the redundancy of some species in
but the processes – along with the organisms and functional groups provides insurance against
abiotic components they interact with – are proper- changes in conditions that compromise the ability
ties of the natural world. of other species in the same groups. In this sense,
Alongside natural capital, it is conventional to biodiversity is like a portfolio of assets. The value of
identify at least two other forms of capital: produced the portfolio depends on both the range of condi-
or manmade capital and human capital (Fig. 21.3). tions that is expected to occur, and the covariance
Manmade capital, by contrast, involves assets that are in the performance of all assets in the portfolio over
produced, and that do not replicate nature – factories, that range of conditions.
roads, bridges, power plants, financial institutions and Third, and related to this last point, the evolu-
assets, etc. Human capital is the store of knowledge, tionary potential of the system is an increasing
 CAN WE PREDICT THE EFFECTS OF GLOBAL CHANGE 297

Fossil
F u el
Fossil
Humanity and water
human capital
Labour
Knowledge
Culture
Government
Natural capital
Climate regulation,
Pollination, biological control,
Invasion regulation,
Soil production,
Natural goods and services Manmade capital
agriculture, aquaculture
Industrial goods and services
Alternative energy

Figure 21.3 Human domination of the biosphere: a graphical device for communicating the importance of biodiversity and ecosystem services in
environmental sustainability and sustainable development. This figure illustrates humanity and human capital supported by inputs from natural and manmade
capital as well as current inputs from fossil fuel and water supplies. The series of pipes and valves illustrate how humanity’s wellbeing and fate are
controlled by the ways in which we balance the flows of nutrients, energy, and water among the different compartments. For example, if we allocate greater
flows to manmade capital, natural capital shrinks, as do the services we derive from natural capital. See text for further explanation.

functioning of the gene combinations that enable wellbeing in many cases. The problem identified in
species to exploit novel conditions. In economic Chapters 17 and 18 is that neglect of the external
terms, gene combinations have an option value – effects of decisions to convert habitat to ‘produc-
more particularly a quasi option value (the poten- tive’ uses, or to eliminating pests, competitors,
tial value of the yet to be uncovered information predators, and pathogens to enhance productivity,
they offer). may have undesirable and potentially unexpected
Note that this does not mean that more biodi- consequences, for instance on other ecosystem ser-
versity is always more valuable than less biodi- vices whose costs and benefits are externalized.
versity. Indeed, simplification of ecosystems to Only by understanding the relationship between
enhance the productivity of one or more services biodiversity, ecosystem functioning, and the pro-
has been the cornerstone of development in the duction of ecosystem services is it possible to
past. The elimination of pests, predators, and identify the degree to which biodiversity in any
pathogens has substantially enhanced human given system should be conserved.
298 BIODIVERSITY, ECOSYSTEM FUNCTIONING, AND HUMAN WELLBEING

21.5 Concluding comments Current challenges to the field are multifold.

Researchers must strive to: (1) incorporate greater
Hooper et al. (2005) listed five areas in need of
realism into experimental approaches, (2) unify
expansion or resolution in biodiversity and eco-
natural and social science methodology to address
system functioning research. Although published in
the full scope of the effects of diversity on human
2005, the first outline of the consensus was pro-
wellbeing, and (3) convey our findings to the non-
duced in 2000, but even with this earlier date it
scientific community, where environmental deci-
remains remarkable that all five areas have been
sions are made and policy developed. These issues
explored. These five areas were: (1) the relationship
will dominate the field for the next phase of
between taxonomic and functional diversity, (2) the
research into the effects of biodiversity on human
importance of multiple trophic levels, (3) effects on
wellbeing. The loss of biodiversity beyond levels
temporal stability, (4) the relative influence of
that contribute to human wellbeing will decelerate
extrinsic factors versus biodiversity effects, and (5)
only once the interactions between biodiversity,
the exploration of a wider array of ecosystems.
ecosystem functioning, ecosystem services, and
Much, much more needs to be done, but expan-
human wellbeing are properly understood, since it
sion into these areas has strengthened the central
is only then that the consequences of excessive rates
message that biodiversity influences ecosystem
of biodiversity loss will become apparent.
functioning.
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 Index

Note: page numbers in italics refer to Figures and Tables.

abundance, influencing factors 5 temporal stability 80, 81 meta-data set 15

Acer platanoides invasion, impact on alien species integration, effect on PFv Barbarika, A. 171
native species 224 webs 204 Barbier, E.B. 257, 258
adaptability 232 Allen, B.P. and Loomis, J.B. 254 Bärlocher, F. and Corkum, M. 128
relationship to establishment Allison, G. 86, 88, 89 Baumgärtner, S. 232
success 221 Andow, D.A. 111 Baur, B. et al. 181, 191
adaptive foraging 90 animal traits, associated responses to bean, PFv web 202
adaptive systems 265 environmental changes 62, bee communities
additive experimental designs 213 63–4, 65 importance of species richness 198
additive partitioning methods 96–7, aphids temporal turnover 196
100–2, 103 biological control 119 bees
adjusted net savings indicator 259, genotypic diversity, relationship to decline, consequences 205–6
261, 262 infection risk 214 parasitoid diversity 83
aggregate abundance, flower visitors application of BEF research 32, 34, pollination services 120, 196
196, 198 41–2, 44–5 economic value 207–8
aggregate biodiversity index 263, 272 aquatic bacteria, microcosm studies functional facilitation 201
Agreement on Trade Related Aspects 127–8 PFv webs 202, 203
of Intellectual Property Rights aquatic fungi 131 realistic extinction scenarios 73, 74
(TRIPS Agreement) 235–6 Argentine ants (Linepithema humile) behavioural niche differentiation,
agricultural intensification 73, 179–80, 221–2 flower-visiting communities 201
193, 270 Armbrecht, I. et al. 181 Bell, G. 4
effect on pollinator communities Armbrecht, I. and Perfecto, I. 181 Bell, T. et al. 98, 102, 127, 128, 132
195, 196, 197, 206 Armington, P. 268 Bellwood, D.R. et al. 92
meta-analysis of field studies 180–3 arthropod diversity, relationship to Benedetti-Cecchi, L. 138
mitigation options 183–4 land use gradient 186 benefits from landscape, econometric
see also managed ecosystems aspen, genotypic richness 176 modelling 276
agriculture assassin bugs, value in biological benefit transfer valuation techniques
land use 178–9 control 119 255
microbial functions 124 assembly history, microbial Benton, T.G. et al. 34
overyielding 100 communities 126 bequest use value of ecosystems 251
agrobiodiversity, insurance value Auction Contracts for Conservation biocontrol 10, 26
232–4, 256 (ACCs) 241–2 BIODEPTH experiments 8, 54
agro-ecological zoning schemes 241 averting behaviour models 252, 253 drought resistance 87
agro-ecosystems 10 biodiversity
econometric model 269–73 bacteria definitions 150, 263
agroforestry 183 aquatic 127–8 divergence from natural
carbon sequestration 164–5 Bacillus thuringiensis 124–5 biodiversity (DNB) 264–5
Alaska, GEEM model 266–9 E. coli, presence on spinach 190 influencing factors 5
alerting behaviour valuation method nitrogen-fixing 128–9 importance relative to community
252 see also microbes species composition 210–11
alfalfa seed production, economic balanced diet hypothesis 109, 112 meta-analyses 14
value of bees 207–8 Bali Road Map 150 data sets 15
algae Balmford, A. et al. 11, 251 hypotheses 15–17
dispersal effects 145 Balvanera, P. et al. 14, 17, 110, 187 meta-data

357
358 INDEX

biodiversity (cont.) biotic feedback 3–4 carbon offset arrangements 246–7

distribution of studies 19–21, 20 biotic functions, impacts of carbon sequestration 149–51, 165–6
hypotheses to explain variation simplification 10–11 biodiversity effects 151
in biodiversity effects 21–4 bioturbation, effect of benthic marine empirical evidence 156–7
methods of analysis 17–18 invertebrates 73, 74 experimental studies 158–62
multivariate mixed-model birds, as indicators of biodiversity mass ratio hypothesis 152–5
analyses 19 190–1 neotropical trees 73, 74
biodiversity effects 15 bison, restoration to Great Plains 190 neutral hypothesis 152
differences between ecosystem, bivariate plots 4 niche complementarity
community and population body size hypothesis 155–6
responses 16, 22, 23, 27 animals 71–2 suites of plant attributes
differences between ecosystem relationship to extinction 152, 153
types 15–16, 21–2, 27 risk 64, 65, 77 carbon sequestration initiatives 163–5
differences between residents and plants, relationship to ecosystem carbon stocks, forest and woodlands,
invaders 17, 22, 23, 24, 28 function 70 South Africa 260, 261
differences between standing stocks Bolker, B.M. et al. 165 carbon uptake (capture) 151
and rates 16, 22–4, 27 Booth, R.E. and Grime, J.P. 155 Cardinale, B.J. et al. 14, 99, 100–1, 110,
future studies 28–9 Botta-Dukát, Z. 51, 52, 53 113, 119, 171, 212
multitrophic studies 16–17, 22, 23, bottom-up biodiversity effects 16, 17, meta-data set 15
24, 27–8 23, 24, 27, 107, 108, 109 Carlander, K.D. 4
shapes 17, 24–6, 28 empirical evidence 112 Carney, K.M. et al. 181
Biodiversity effects on Ecosystem Boyd, J. and Simpson, R.D. 237 Carolina Vegetation Survey 177
Functioning (BEF) 105–6, 120, Bracken, M.E. et al. 73, 74 cascading (secondary) extinction
219–20 Bradshaw, A.D. 167 67–8, 69, 90–1
BEF-6 36–8 Brandle, J.R. et al. 165 case study approach 11
information flow 39 Brazil, TDR programs 241 Caspersen, J.P. and Pacala, S.W. 158
BEF approach to restoration 169–70 Brock, W.A. et al. 295 cellulose utilization, bacteria 127
BEF database 33–4, 34–6, 35 Brock, W.A. and Xepapadeas, A. Center for Tropical Forest Science
citation rates 36, 37 274–7 Trait database 286
biodiversity gradients 292, 293 Brundtland Report (World central construct 11–12
impacts of colonizing Commission on Environment Chagnon, M. et al. 200
species 220–6 and Development 1987) 295–6 Chesapeake Bay, exotic species 222
trait-based research 283 Buenos Aires accords 149 Chesson, P. 113–14, 144
biodiversity index 263, 272 Bullock, J.M. et al. 181 China, demand for natural resources
biodiversity markets 234–8 bumble bees, declining species 205 295
bioeconomic risk analysis, colonization Bunker, D.E. et al. 73, 74, 76, choice experiments 253
226–8 159, 281 Chopra, K. and Kumar, P. 237–8
BioFlor 286 BushTender 242 citation rates 33–4, 36, 37
biological control 119, 120, 187–8, Butler, S.J. et al. 191 BEF-6 36–8
215 Bwindi national park, Uganda 242 functional diversity measures 52–4
economic value 191–2 in management plans 42, 43
scaling effects 192–3 calcareous grassland, PFv web 202 Clarke, P.J. et al. 222
value of landscape mosaics 189 Caldeira, M.C. et al. 80, 81, 84, 86, 87 Clean Development Mechanisms
biomass, relationship to microbial Callaway, J.C. et al. 171 (CMDs) 149, 164, 166
community diversity 126 Camill, P. et al. 171 Clean Water Act, USA 177
biomass compensation 66–7, 76 CAMPFIRE (Communal Areas climate
biomass production, roles 10 Management Program for effect of microbes 124
BioMERGE (Biotic Mechanisms of Indigenous Resources), effect of plant traits 153–4
Ecosystem Regulation in the Zimbabwe 236 climate change
Global Environment) xii, 9, candidate variables, biodiversity animal responses 64
281 experiments 29 effect on pollinator services 206
BioPop 286 carbon cycling 249 plant responses 63, 65
bioprospecting 235–6, 246 seasonality 172 prediction of responses 286
bioremediation, trait-based research carbon dioxide increase, plant climate change mitigation 149–50,
283 responses 63, 65 151, 165–6
biosecurity 227 carbon loss, experimental studies see also carbon sequestration
biosphere, human domination 297 161–2 clone libraries 122, 123
 INDEX 359

Cobb–Douglas production function biodiversity 183 'naturalness' of ecosystems 264–9

268 Computable General Equilibrium covariances 84–5
coefficient of variation (CV) 80 (CGE) models 265 Craft, C. et al. 168
meta-communities 142, 143 confirmatory experiments 8 Crocker, T.D. and Tschirhart, J. 231, 267
coexistence, mechanisms of 113–15 conjoint analysis 253 crop diseases 190
coffee production connectance, food webs 90–1 crop diversity 270
financial incentives 193 connected species, extinction risk 68, 69 cropland increases 178
pollination services, spatial connections 105 crop pollination services see
variation 198, 200 conservation 230 pollination
coinfections 214 biodiversity markets 234–8 crop production function 271
cold resistance 86 community-based 236 cross-ecosystem biodiversity
colonization 217, 220 economic instruments 238–42, 244 exchanges 189–90
biodiversity effects 17, 22, 23, 24, 28 Endangered Species Act, United Crutsinger, G.M. et al. 155, 176
establishment success 218–19, States 243–4 cultural services 248
221–2 government and NGO 'naturalness' of ecosystems 264–9
impact on BEF relationship 224–6 involvement 236–7 valuation 253
impact on native ecosystem 222–4, of primary forests 163, 166
227–8 value 251 Dang, C.K. et al. 81, 83, 128
likelihood of 220–1 conservation biology, trait-based Daphnia magna, genotypic diversity,
patch dynamics 117–18 research 283 relationship to infection risk
prediction of impact 228–9 conservation easements 237 214
risk assessment 226–8 conservation investment 271 Darwin, C. 4, 94–5
terminology 218 Conservation Reserve Program (CRP) Dasgupta, P. 259
communication of BEF concepts 171, 177, 184 databases 281–2
31, 43–5 consumer diversity, relationship to trait data 286
community approach to restoration resource fluxes 108, 109 see also TraitNet
168 consumptive use 264 data integration, TraitNet 286–8
community assembly/disassembly, contemporaneous disequilibrium Davis, M.A. and Thompson, K. 218
natural versus random, effect 140–1 De Bello, F. et al. 53
on disease dynamics 212–14 context dependence effect (CDE) 49, Debras, J.F. et al. 181
community-based conservation 236 97 DeClerck, F. et al. 81, 82, 86, 88, 89
community disassembly 135 contingent valuation 253 decomposition
community ecology, trait-based Convention on Biological Diversity carbon loss 154
research 283 40, 209 effect of fungal diversity 83, 128
community fingerprints 123 Convention on International Trade in aquatic fungi 131
community-level functions 16 Endangered Species (CITES) litter-mixing studies 156
community-level responses, 245 relationship to plant traits 71, 72
biodiversity effects 16, 22, 23, 27 convex hull volume (CHV) 51, 55 by soil microbes 129–30
community organization, link applications 52, 53 deforestation
to traits 66 relationship to species richness 56, effects on infectious disease risk 214
comparative microbial studies 132 57, 58 mangroves 258
soil communities 130 Cook, D.C. et al. 226 Degens, B.P. 130
comparative trait-based research 283 coral reefs dendrogram-based measures of
compensation, as response to bioerosion 54 functional diversity 52
extinctions 66–7, 76 stability 92 Dennehy, J.J. et al. 214
compensation for conservation Cornwell, W.K. et al. 51, 52 detrital food webs, biodiversity
measures 243–4 correlation coefficients, conversion to effects 17
compensatory dynamics, meta- Zr values 18 detritivore diversity effects,
communities 143, 144 Costa Rica, payments for ecosystem comparison with detrital
competition, Lotka–Volterra models services 239 diversity effects 112
114–15 Costello, C. and McAusland, C. 244 detritus processing, stream insects 73,
competitor diversity, role in cottonwood, genotypic richness 176 74
establishment success 218 Countryside Surveys, UK 272 Dhôte, J.-F. 161
complementarity effects 95, 96, coupled ecological–economic systems diffusion 218
99–100, 101, 188, 219, 281, 296 263, 277–8 Dillard, W. 113
role in establishment success 222 agro-ecosystems 269–73 dilution experiments, soil microbes 130
Complex Agroecosystems 181 generalized model 273–7 dilution hosts 212, 213
360 INDEX

dilution hypothesis 109, 111 ecoagriculture 184 bees as crop pollinators 207–8
Dimitrakolpoulos, P.G. and eco-engineered approach, sterilized forest and woodlands, South
Schmid, B. 101 Earth experiment 6 Africa 160–1
direct compensation payments (DCP) ecoinformatics frameworks, Keoladeo National Park 254
240 integration of TraitNet 288 mangrove storm buffering 257–8
direct use value of ecosystems 251 E. coli, presence on spinach 190 methods 252
direct utility function 270 ecological engineering 168–9 microbial functions 125
discrete functional groupings 54 Ecological Flora of the British Isles natural pest control 191–2
diseases see infectious disease risk; 286 provisioning and cultural
infectious diseases Ecological Flora of California 286 services 251–6
dispersal, disruption by colonizing Ecological Metadata regulating services 256–7
species 223 Language (EML) 288 ecosystem types, variability of
dispersal abilities, likelihood of ecological resilience 91 biodiversity effects 15–16,
colonization 220 economic decision modelling 12 21–2, 27
dispersal effects 117, 135, 138–9, economic instruments 238–42, 244 ecotourism 235, 248
143–4, 146 economic literature 12 Ecotron experiments 7–8, 59
empirical tests 145–6 economics 246–7 edge effects 134, 189–90
meta-community dynamics 141 biodiversity as insurance 232–4 effective dimensionality of trait space 55
meta-community productivity biodiversity markets 234–8 effect traits 66
141–3, 144–5 ecosystem externalities 231–2 relationship to ecosystem function
spatial insurance hypothesis 139–40 international dimension 244–6 70–2
distance-based measures, functional sustainability indicators 259 efficacy of research 290, 291
diversity 51–2 value of ecosystems 249–51 Eichner, T. and Tschirhart, J. 264, 266
disturbance regimes, impact of see also coupled ecological– Ellis, G.M. and Fisher, A.C. 268
colonizing species 223 economic systems Elmqvist, T. et al. 144
disturbances economic value 174–5, 230–1 emerging infections 215
effect on carbon sequestration 153 bees as crop pollinators 207–8 endangered species, CITES 245
role in establishment microbial functions 125 Endangered Species Act, United
success 219 natural pest control 191–2 States 243–4
divergence from natural biodiversity ecosystem approach to restoration endemism, trait-based research 283
(DNB) 264–5 168–9 enemy release, role in establishment
DIVERSITAS xii ecosystem ecology, trait-based success 218–19, 221, 285
diversity–disease curves 210 research 283 energy flow, GEEM model 266–7
diversity–interaction models 98–9, ecosystem engineers 105, 155 energy prices 267
102–3 ecosystem externalities 231, 244–5, Engelhardt, K.A.M. and Ritchie, M.E.
Dobson, A.P. et al. 137 246–7, 263, 277 225
domesticated species 9 international 244–5 Enquist, B.J. and Niklas, K.J. 158
dominance effect (DE) see sampling ecosystem function 6–7, 170–1 Environmental Kuznets Curve 245
(selection) effect measures 83 environmental microbiology 121
'dose–response' analysis 252–3, 256 relationship to effect traits 70–2 Environmental Stewardship Scheme,
drinking water provision, New York species effects 173–4 UK 177
City 252 trajectories 4, 17, 24–6 Epps, K.Y. et al. 53
drought resilience 88 ecosystem-level functions 16 equalizing forces 114
drought resistance 85, 86, 87, 172 ecosystem-level responses, equilibrium species diversity, general
drugs, bioprospecting 235–6, 246 biodiversity effects 22, 23, 27 model 273–7
dual zone TDR programs 241 ecosystem services 10, 11, 248–9 establishment success 218–19, 221–2,
Duarte, C.M. et al. 128 in managed ecosystems 191–2 225
Duffy, J.E. 107, 109 payment services 238–40 Eviner, V.T. et al. 172
Dukes, J.S. 73, 76 relationship to species richness 67, evolutionary potential 296–7
dung beetles, realistic extinction 68, 76 exclusion principle 273–4, 275–6
scenarios 73, 74 restoration of multiple services existence value of
Dyer, A.R. and Rice, K.J. 223 173–4, 176 ecosystems 251
socio-economic impacts 118–20 expected damage function
Earth Summit, (Rio de Janeiro 1992) stability 92–3 (EDF) 257, 258
296 in restoration 172–3 exploitation, animal responses 64, 65
Ebola virus infection risk, effect of valuation 11, 12, 174–5, 230–1, explorative approach, sterilized Earth
deforestation 214 249–51, 261–2 experiment 6, 7
 INDEX 361

externalities 231, 246–7, 263, 277 flower visitors non-grouping measures 50–1
international 244–5 aggregate abundance 196 relationship to plant productivity 273
extinction species richness 196–8 trait-based research 283
biomass compensation 66–7 food supply, consequences of functional facilitation, pollinator
cascading 67–8, 69, 90–1 pollinator decline 205–6 communities 199, 201
consequences 60–2 food web diversity, socio-economic functional group richness 50, 53
effect on PFv webs 203–4 impacts 118–20 applications 53–4
realistic scenarios 72–5, 115–17 food webs 105 functional groups 49–50, 70
reversed causation 14 complexity 106 functional redundancy 79, 83, 173,
extinction debts 136, 213 diversity effects across trophic 188, 296
extinction order prediction 66 levels 109–10 aquatic bacteria 127
extinction research, future empirical evidence 112–13 soil microbes 129–30
directions 77 diversity effects within trophic functional reorganization 61
extinction of resources 115 levels 107, 108, 109 functional response diversity 79
extinction risk empirical evidence 110–12 functional traits 5
relationship to response traits 62–5 effects of extinctions 116–17 invasive species 226
relationship to trophic level 107 protistan 126–7 plants, effects on climate 154
stabilizing properties 89–91 functioning debt, habitat
facilitation trait-based research 283 fragmentation 136–7, 146
bacterial species 127 see also plant–flower visitor (PFv) functioning ecosystems 294–5
by colonizing species 222 interaction webs funding of BEF research 34, 38–40
Farm Business Survey, UK 272 forestry, timber extraction study, funding of restoration 177
FD 52 Uttar Pradesh 237–8 fungi
applications 53 forests aquatic 131
relationship to species richness 56, carbon sequestration 163 diversity, effect on decomposition 83
57, 58 temporal stability 81, 82 microcosm studies 128
FDLD 52 Forest Service, USA, application
relationship to species richness 56, of BEF concepts 41, 42 Gabriel, D. et al. 181
57, 58 fossil fuel emissions 165 Gallai, N. et al. 206
FDvar 51 fossil resources 296 Gamfeldt, L. et al. 173
applications 52, 53 fragment area distribution 138 gene pool 230
relationship to species richness 56, fragmentation of habitat 134–5, 146 General Agreement on Tariffs and
57, 58 animal responses 64, 65 Trade (GATT) 245–6
fecundity, relationship to functioning debt 136 General Equilibrium Ecosystem
invasiveness 220 plant responses 63 Model (GEEM) 265–9
Fédoroff, E. et al. 181 source–sink meta-community general equilibrium models 264, 265
feedbacks 3–4, 12 model 140–1 Genghini, M. et al. 181
Ferrari, J. et al. 214 spatial variance of biodiversity genotypic richness 155, 176
Ferraro, P.J. and Simpson, R.D. 237 137–8, 139 relationship to disease risk
'Field of Dreams' approach to species loss estimation 136–7 209, 214
restoration 169 see also habitat loss; meta- Giller, P.S. et al. 15
field experiments 32 community models Gillison, A.N. et al. 181
Final Environmental Impact Framework Convention on Climate Global Biodiversity Information
Statements (FEISs), application Change (FCCC) 246–7 Facility 288
of BEF research 34, 42, 43 framework incentives 238, 239 Global Environmental Organization
fire ecology, trait-based France, K.E. and Duffy, J.E. 145 (GEO) 246
research 283 Frivold, L. and Frank, J. 158 globalization 294, 295
fire frequency, impact of colonizing Fukami, T. and Morin, P.J. 126 global warming
species 223 fully combinatorial studies 292 effect on pollinator services 206
FishBase 286 fumigation experiments, soil microbes plant responses 63, 65
fisheries 230 130 prediction of responses 286
GEEM model 268–9 functional attribute diversity (FAD) 51 Glopnet 286
production function models 255 functional diversity 8, 49, 58–9, 211, 281 Glor, R.E. et al. 181
'roving bandit' phenomenon 295 applications 52–4 Gonzalez, A. and Chaneton, E. 136, 145
stability 93 choice of measure 58 Gonzalez, A. and Descamps-Julien, B.
fitness net energy flow, GEEM effects of species richness 54–8 81
models 266–8 measures 51–2 Gordon, C. et al. 181, 191
362 INDEX

Gould, A.M.A. and Gorchov, D.L. 223 Heemsbergen, D.A. et al. 51 diversity–disease curves 210
governments, policies on herbivory, effect on impact of plant diversity versus species
conservation 237 diversity 109, 112, 113 compositions 210–11
gradient analysis, trait-based research Herendeen, R. 267 monocultures versus polycultures
283 heritability, trait-based 212
grassland plants research 283 natural versus random community
realistic extinction scenarios 73, 74 Hillebrand, H. and Cardinale, B.J. 111 assemblies 212–13
variations in fungal disease 211 Hiremath, A.J. and Ewel, J.J. 158 relationship to genotypic
grasslands Hoehn, P. et al. 199–200 diversity 214
effect of nitrogen pollution 231 holistic approach to research 31 species diversity versus functional
experimental variation of Holling, C.S. 91, 232 diversity 211
biodiversity 231 Holt, R.D. and Loreau, M. 109 infectious diseases 209–10
restoration 168, 169, 176–7 Holway, D. 221 information flow 31, 39, 43–5, 298
diversity of plantings 171 Holzschuh, A. et al. 181 in restoration ecology 175
multiple ecosystem services homogenization 217 in silico studies 292
173, 174 homologous characters 5 insurance hypothesis 79, 87, 91, 144,
temporal stability 80, 81, 82 honey bee (Apis mellifera) 146, 155, 188
grazing, plant responses 66, 71 decline, consequences 205–6 economic aspects 232–4
Great Plains, restoration of bison 190 pollination services 196 spatial insurance hypothesis 118,
Greenleaf, S.A. and Kremen, C. 201 economic value 207–8 139–40, 144, 145
'green payments' 240 functional facilitation 201 integrated conservation–development
Griffiths, B.S. et al. 85, 86, 88, 130 Varroa mite infestation 204 projects (ICDPs) 236
Griffiths, G.J.K. et al. 192 see also bees integration, effect on PFv webs 204
Grime, J.P. 152 Hooper, D.U. et al. 298 intellectual property rights 235–6
gross domestic product (GDP) 259 Hooper, D.U. and Vitousek, P.M. 8 TraitNet 287
Gross, K. and Cardinale, B.J. 116 citations 38 intensification 73, 179–80, 193, 270
growth equation 275 horizontal diversity 109 effect on pollinator communities
growth form, plants, relationship to horizontal gene transfer 125 195, 196, 197, 206
extinction risk 63, 65 Hortus Gramineus Woburnensis meta-analysis of field studies 180–3
growth rate, relationship to experiment 290 mitigation options 183–4
establishment success 221 Hubbell, S.P. 114, 152 see also managed ecosystems
guild analysis, trait-based research 283 Hughes, A.R. and Stachowicz, J.J. 87 intentional introductions 221
Hughes, T.P. 92 interactions 5, 6
Habitat Conservation Plans 244 Hulme, P.E. and Bremner, E.T. 223 ecosystem services 250
habitat loss 134–5 human capital 296 effect on extinction risk 76
animal responses 64, 65 Human Development Index (HDI) 259 effects on stability 90
community disassembly 135 human manipulations 9–11 intermediate disturbance hypothesis
plant responses 63 human-mediated introductions 221 183
see also fragmentation of habitat Hunter, T. et al. 161 intermediate inputs, ecosystem
Haggar, J.P. and Ewel, J.J. 158 Huston, M.A., citations 38 services as 250
Hairston–Smith–Slobodkin Hutchinson, G.E. 130 international trade 244–6
hypothesis 17 Hutton, S.A. and Giller, P.S. 181 inter-specific competition 16
Hannon, B. 267 intra-specific variation 59
Hartwick, J.M. 259 Impatiens glandulifera, removal introduced species 221, 229, 244
harvesting, extinction risk 62 study 223 invaders 60, 169, 218, 224
Harvey, C.A. et al. 181, 191 incentives for biodiversity biodiversity effects 17, 22, 23, 24, 28
Hättenschwiler, S. et al. 161 management 193–4, 209, effects of removal 223, 228
Hawaii Plant Trait Database 286 243–4, 246, 247 establishment success 218–19
hazard
likelihood product, incentives for conservation 238–42, as an externality of trade 244
disease risk 215 244 impact on native ecosystem 222–4,
heat resilience 88, 173 included (nested) niches 101 226, 227–8
heat resistance 86, 172–3 index of biodiversity 263, 272 mechanisms of invasion 285–6
Hector, A. and Bagchi, R. 28, 173 indicators of biodiversity 190–1 prediction of impact 228–9
Hector, A. et al. 257 indirect use value of ecosystems 251 risk assessment 226–8
citations 38 infectious disease risk 214–16 trait-based research 284
hedonic price valuation coinfections 214 see also colonization
method 252, 253 deforestation effects 214 invasiveness, related traits 220–1
 INDEX 363

inverse sampling effect 219, 224–5 LEDA Traitbase 286 relevance of controlled
investment rule 259 Leibold, M.A. et al. 117 experiments 185
Ives, A.R. and Cardinale, B.J. 66, 116–17 leishmaniasis risk, effect of research approaches 185–6
ivory trade ban 245 deforestation 214 ecosystem functions 191–2
lettuce mosaic virus 190 scaling effects 192–3
Jactel, H. et al. 161 Leung, B. et al. 226 incentives 193–4
Jensen's inequality 138, 139 life expectancy at birth 259 management decisions, application of
Jiang, L. et al. 53 life-history, relationship to extinction BEF research 34, 41–2, 43, 44–5
joint implementation projects 246–7 risk management intensification 179–80
Jones, H.E. et al. 159 animals, 64 meta-analysis of field studies 180–3
Jones, K.E. et al. 215 plants 63 mitigation options 183–4
Jonsson, M. et al. 74 life-history trade-offs 115 mangrove storm buffering, valuation
Joshi, J. et al. 85, 86, 155 dimensionality 285 257–8
Joyce, C. 181 lignin degradation 129 manipulative experiments, microbial
litter mixing studies 156 communities 130, 131, 132
Kahmen, A. et al. 86, 87 LoGiudice, K. et al. 211 manmade capital 296
Keller, R.P. et al. 227 Long, Z.T. et al. 126 marine benthic invertebrates,
Kemp, D.R. et al. 92 Lonicera mackii, removal studies 223 extinction scenarios 73, 74, 75
Keoladeo National Park, ecosystem Loranger, G. et al. 181, 186 marine protected areas, economic
valuation 254 Loreau-Hector additive partitioning value 174
keystone species 105, 155, 264–5 method 96 market failures 246
Kindscher, K. and Tieszen, L.L. 171 Loreau, M. 96 markets in biodiversity 234–8
Kirwan, L. et al. 98–9, 102, 186 Loreau, M. and Behera, N. 87 Marrakech Accord 149
Klein, A.M. et al. 120 Loreau, M. et al. 118, 140 Mason, N.W.H. et al. 51, 52, 53
Knowler, D. 268 citations 38 mass ratio hypothesis 152–5, 156,
Kolasa, J. and Li, B. 82–3 Losey, J.E. and Vaughan, M. 208 163–4
Kolmogorov model 274, 275 lost species experimental studies 157
Kondoh, M. 90 consequences 60–2 Matthiessen, B. and Hillebrand, H. 145
Koo, B. and Wright, B.D. 236 effect on functional diversity 49 maximal function, number of species
Korhonen, K.P.C. et al. 161 see also extinctions required 26, 28
Koricheva, J. et al. 162 Lotka–Volterra models 114–15, 274 meadows, restoration 168, 169, 176
Körner, C. 154 lupine, PFv web 202 mean dissimilarity (MD) 51
Kremen, C. et al. 93, 181 Lyme disease 73, 74, 120 applications 52–3
Kyoto Protocol 149, 166 diversity–disease curve 210 relationship to species richness 56,
effect of dilution hosts 212 57, 58
laboratory studies 32 impact of white-footed mouse 213 mechanisms of coexistence 113–15
limitations 30 variations in blacklegged tick mechanistic statistical models 94
ladybeetles, value in biological infection 211 media coverage of BEF concepts 40–1
control 119 Meléndez-Ramirez, V. et al. 197
land acquisition, conservation McAusland, C. and Costello, C. 244 Memmott, J. et al. 203–4
promotion 237 McCann, K.S. 90 Mendelsohn, R. and Balick, M.J. 236
land conversion, carbon loss 163 McGrady-Steed, J. et al. 126–7 Merrifield, J. 240–1
landscape complexity, relationship to McIntyre, P.B. et al. 73, 74, 281 Mesopotamian marshes, restoration of
natural pest control 187 macroecology, trait-based research 283 ecosystem services 173
landscape gradients 184, 185 Madritch, M.D. and Hunter, M.D. 161 metabolically inactive microbe cells
relationship to arthropod diversity maize (Zea mays), introduction to Old 132
186 World 221 metabolic theory of ecology, trait-
landscape mosaics, value 189–90 malaria 120 based research 284
land sparing 183–4 effect of deforestation 214 metabolome, microbial 124
land use change 178–9, 230–1 managed ecosystems 178–9, 194 meta-community models 117–18, 143–6
land use and land cover change BEF relationships 184–5 dynamics 141, 142
(LUCC) 269 cross-ecosystem exchanges of productivity 141–3
Larsen, T.H. et al. 67, 68, 73, 74, 199 biodiversity 189–90 source–sink model 140–1
leaf characteristics, relationship to indicators for functions of stability 143
ecosystem function 71 biodiversity 190–1 meta-genomics 123
leafcutter bees, pollination services, insurance value of biodiversity 188 meta-regression models 255
economic value 207–8 pest control 187–8
364 INDEX

Metrick, A. and Weitzman, mycorrhizal fungi 128–9 nitrogen-fixing trees, carbon

M.L. 243 Myrica faya, colonization in Hawaii 224 sequestration 154
Mgahinga and Bwindi Impenetrable nitrogen oxide pollution 231
Forest Conservation Trust Naeem, S. et al. 7, 59, 168 nitrogen uptake, seaweeds 73, 74
Fund 242 citations 38 nodes 105
Michaelis–Menten curves, limitations 26 National Center for Ecological non-governmental organizations 41
microarrays 123 Analysis and Synthesis non-use value 250–1
microbes 8 (NCEAS) 286 Noss, R.F. 165
biodiversity estimation 122–4, 123, Knowledge Network for novel, invasive colonizers 218
132 Biocomplexity project 288 see also invaders
diversity patterns, similarity to National Marine Fisheries Service novel, noninvasive colonizers 218
those of larger organisms 133 (NMFS) policies 269 numerical compensation 66–7, 76
species identification 124 National Park Service, USA, nutrient cycling 248–9
microbial communities 121 application of BEF concepts 41–2 freshwater tropical fishes 73, 74
restoration 175–6 national product measures (GNP, seasonality 172
microbial functions 124–5 NNP) 259 shapes of biodiversity effects 26, 28
in the wild 129, 131–2 natural capital 296 nutrition, consequences of pollinator
aquatic fungi 131 depletion 9 decline 206
microbe-plant interactions 130–1 'naturalness' of ecosystems 264–9
soil microbes 129–30 natural selection, trait-based research observational studies, microbes 124
microcosm studies 121, 124, 131–3, 291 284 Observation Ontology (OBOE) 288
algae, dispersal effects 145 Nature Conservancy 237 oilseed rape, PFv web 202, 203
aquatic bacteria 127–8 NatureServe databases 286 Olschewski, R. et al. 186
fungi 128 negative covariance effect 84 Omer, A. et al. 270, 272–3
model systems 125–6 negative selection effects 96, 100–1 omnivory 105
mutualistic microbe–plant nested niches 101, 102 optimization technique 263–4,
interactions 128–9 net biodiversity effect 96 271–2
protistan food webs 126–7 net carbon sequestration 150–1 private optimization management
spatial averaging 145 net primary productivity (NPP), problem (POMP) 274, 276
temporal stability 81, 82–3 relationship to carbon social optimization management
Millennium Ecosystem Assessment sequestration 154 problem (SOMP) 274,
11, 59, 178, 230, 234, 248–9, 250, net product measures (NDP, NNP) 276, 277
261–2, 293–5 259 option value of ecosystems 251
mixed forestry systems, carbon neutral theory of biodiversity option value of gene combinations 297
sequestration 164 114, 152 Opuntia scrubland 256
model systems, microbial experimental studies 157 organic farms, biodiversity 183
communities 125–6 New York City, drinking water Ostfeld, R.S. et al. 212
monocultures, carbon sequestration provision 252 Ostfeld, R.S. and LoGiudice, K. 73, 74,
164, 165 niche complementarity (niche 76, 213
Montoya, J.M. and Solè, R.V. 91 differentiation) 114, 155–6, Our Common Future (World
Morin, P.J. McGradySteed, J. 81 164, 188, 212, 219 Commission on Environment
moss communities, dispersal effects 145 experimental studies 157 and Development 1987)
Mouillot, D. et al. 53 pollinator communities 198–9, 295–6
Mulder, C.P. et al. 85, 86, 87, 113 199–201 overyielding 95–6, 100–2, 186
multifunctionality 10, 28, 178, 188 Pseudomonas fluorescens 127
in restorations 173–4 role in establishment success 222 Pacala, S. and Tilman, D. 274
multifunctional redundancy 173 niches, nesting 101, 102 Pacala, S.W. and Deutschman, D.H.
multiple stable states 91–2 niche theory 17 165
multiple traits, FDvar values 51 nitrate pollution 231 palaeobiology, trait-based research
multi-resource model 276 nitrifier communities, comparative 284
multitaxon biodiversity studies 191 studies 130 PAM (Partitioning Along Metroids)
multi-trophic biodiversity effects nitrogen cycling analysis, agricultural
16–17, 22, 23, 24, 27–8 impact of colonizing species 223 landscape studies 180, 181
multi-trophic communities, temporal seasonality 172 Panayotou, T. 240
stability 81, 82–3 nitrogen deposition, plant responses paradox of the plankton 130
mutualistic microbe-plant interactions 63 parasite diversity 54
128–9 nitrogen-fixing bacteria 128–9 parasitoid diversity 83
 INDEX 365

parasitoid wasps, value in biological interactions with microbes 130–1 predator diversity 113
control 119 mutualistic interactions 128–9 socio-economic aspects 119
Pareto criterion 242 PLANTS database 286 predator loss, implications 120
parrotfish, bioerosion 54 plant traits predator–prey interactions 187
partitions 98 associated responses to GEEM models 265, 266–8
Pascual, U. and Perrings, C.P. 241 environmental changes 62–3, Pretzsch, H. et al. 160
pasture increases 1878 65 Price equation partition 96, 97–8, 102,
pasture lands, stability 92 relationship to ecosystem function 103
patch dynamics 117–18, 144 70–1 primary forests, carbon sequestration
patents 235 Podani, J. and Schmera, D. 52, 53 163, 166
application to microbes 125 Polasky, S. et al. 257 primary production, shapes of
pathogenicity, microbes 124–5 policy frameworks 238 biodiversity effects 26
Pautasso, M. et al. 161 pollination 10, 195–6, 206 principle component axis 1(PCA1)
payments (rewards) for ecosystem economic value of bees 207–8 plants, ecosystem function 71,
services (P(R)ES) 238–40 flower visitor abundance 196 72
Peacock, L. et al. 161 flower visitor species richness privately optimal management
Pérez Harguindeguy, N. et al. 162 196–8 problem (POMP) 274, 276
periwinkle, as source of drugs 235, mechanisms of effects 198–201 production function valuation
236 future research areas 207 methods 252, 253–5
Perner, J. and Malt, S. 181 plant–flower visitor interaction production–simplification trade-off
Perrings, C. et al. 232, 269 webs 201 10
pest control see biological control higher trophic levels 204 productivity
pesticides use 270 quantitative analysis 204–5 meta-communities 141–3, 144–5
Petchey, O.L. et al. 80, 81, 84 species extinction and relationship to biodiversity 4
Petchey, O.L. and Gaston, K.J. 50, 52, integration 203–4 relationship to plant traits 71
53, 74 structure and characteristics property rights regimes 240
species richness, effect on 201–3, 202 protective value of ecosystems 253–4
functional diversity 55 realistic extinction scenarios, bees protistan food webs 126–7
Peters, C.M. et al. 251 73, 74 provisioning services 248
Pfisterer, A.B. and Schmid, B. 42, 86, socio-economic impacts 120 valuation 251–3
87, 88 stability 93 Pseudomonas species
pharmaceutical firms, bioprospecting valuation 253 bacteriophage infection risk 214
235–6, 246 value of landscape mosaics P. fluorescens 127
phases of BEF research 31, 32 189–90 public awareness 40–1, 43–4
Philpott, S.M. et al. 181 pollination characteristics, public goods 230–1, 249
phylogeny 5, 6 relationship to extinction risk Pulkkinen, K. 214
phytoplankton, functional diversity 54 63 Pullin, A. et al. 42
Pimm, S.L. 232 pollinator decline, consequences for pumpkin, pollinator services, spatial
planning documents, application of global food supply 205–6 stability 199–200
BEF research 34, 41–2, 43 polymerase chain reaction (PCR) 122–3 purposive decisions 263
plant community diversity, role in poor populations, impact of market-
establishment success 218 like mechanisms 242, 244 Q (Rao's quadratic entropy) 51–2
plant ecological strategies, trait-based population ecology, trait-based applications 52, 53
research 284 research 284 relationship to species
plant–flower visitor (PFv) interaction population growth 178 richness 56, 57, 58
webs 201 population-level functions 16 Quaas, M.S. 232
higher trophic levels 204 population-level responses, quantitative PFv web analysis 204–5
quantitative analysis 204–5 biodiversity effects 16, 22, 23,
species extinction and integration 27 race to the bottom, international
203–4 Potvin, C. and Gotelli, N.J. 160 trade 245
structure and characteristics 201–3, poverty, implications for managed random assembly experimental
202 ecosystems 193 design 60–1, 213
plant productivity, relationship to practicability of research 290, 291 random-loss scenarios 73–5
functional diversity 273 precipitation changes, plant random partitions design and
plants responses 63, 65 analysis 98, 103
functional traits, effects on climate predation, effects on microbial rangelands, stability 92
154 communities 126 Rao's quadratic entropy see Q
366 INDEX

rates, biodiversity effects 16, resistance 78, 188, 232 sampling, microbial communities
22–4, 27 empirical findings 83, 85, 86–7 122–3
Raviraja, N.S. et al. 128 insurance hypothesis 79 sampling (selection) effect 95, 96, 187,
realistic extinction scenarios 72–5 link to resilience 89 219
realistic research 291–3, 298 resource-based models 273–4 in colonization 221–2, 224–5
reassociation kinetics 123 resource concentration hypothesis pollinator communities 198, 199
reclamation 169 109 Sanderson, M.A. et al. 92
recreation, GEEM model resource depletion, biodiversity Sandhu, H.P. et al. 191
268, 269 effects 22–4 Sanitary and Phytosanitary (SPS)
red brome (Bromus madritensis ssp. resource diversity, relationship to Agreement 246
rubens), establishment resource fluxes 108, 109 scale of experiments 116, 117
success 222 resource dynamics equation 275 scaling effects, managed ecosystems
Redondo-Brenes, A. and Montagnini, resource extinction 115 192–3
F. 160 resource generalization 107 Schamp, B.S. et al. 53
Reducing Emissions from resource supplies, impact of Scherer-Lorenzen, M. et al.
Deforestation and Degradation colonizing species 223 162, 165
(REDD) initiatives 149–50 resource use, flower visitors 199 Schläpfer, F., et al. 17, 24, 26, 73, 74
regulating services 249 resource capture and utilization, Schmitz, O.J. et al. 113
valuation 256–7 relationship to plant traits 71 Schroth, G. et al. 159
rehabilitation 168 response diversity 144 Science Environment for Ecological
Reich, P.B. et al. 173, 174 pollinator communities 197 Knowledge (SEEK) 286, 288
relative yields (RYs) 96, 103 response traits 66 Taxon project 287
Relative Yield Total (RYT) 96 relationship to extinction risk 62–5 sea grass
removal studies restoration 11 genotypic richness 155
colonizing species 223 funding 177 meta-communities, dispersal
microbes 124 restoration ecology 167–8 effects 145
replacement cost valuation methods BEF approach 169–70 seasonality, nutrient cycling 172
252, 258 classical BEF implications 170–2 seaweeds, nitrogen uptake 73, 74
research community approach 168 secondary extinctions 67–8, 69, 90–1
application 34, 41–2 ecological approach 168–9 seed characteristics, relationship to
BEF database 33–4, 34–6, 35 economics of BEF 174–5 extinction risk 63
citation rates 36, 37, 42 multiple ecosystem services Seed Information Database, Kew
most cited papers (BEF-6) restoration 173–4 Botanic Gardens 286
36–8 recommendations 175–7 selection effect 95, 96, 100–1, 118
current challenges 298 stability of services 172–3 self-citation 33, 36
efficacy and realism 291–3 restorative approach, sterilized Earth semi-mechanistic statistical models 94
evolution 7–9 experiment 6 service flows 274
funding 34, 38–40 Reusch, T.B.H. et al. 155 set-aside land 183–4
history of 4, 30–1 Rewarding Upland Poor for shapes of biodiversity effects 4, 17,
information flow 31, 39, 43–5, 175, Environmental Services 24–6, 25, 28
298 (RUPES) 240 Sierra Nevada forest plan 42
limitations 95 rewards ( or payments) for ecosystem simplifications 10
in managed ecosystems 185–6 services (P(R)ES) 238–40 Simpson, R.D. Sedjo, R.A., and
real-world relevance 176 rice blast infection rate, relationship to Reid, J.W. 235
scale and duration of experiments genotypic diversity 214 simulation studies, extinction
116, 117 Ricketts, T.H. et al. 206, 253 scenarios 73–6
simplified communities 106 Ricotta, C. 53 single TDR programs 241
research approaches 31–3, 32 river restoration 170 'slow life history', relationship to
reserve species 276–7 Rodríguez, L.C. et al. 256 extinction risk 63, 64, 65
reservoir hosts 213 Romanuk, T.N. et al. 81, 82, 84 Snelder, D.J. et al. 181
resilience 78, 188, 232 Rundlof, M. and Smith, H.G. 181 socially optimal management
ecological 91 Russell, A.E. 159 problem (SOMP) 274, 276, 277
empirical findings 87, 88–9 ryegrass rust fungal infection, social welfare function 265
and insurance hypothesis 79 diversity–disease curve 210 societal will 290, 291
link to resistance 89 socio-economic aspects
reserve species 276–7 Sall, S.N. et al. 181 disease risk 215
role of mangroves 258 saltation 218 food web diversity 118–20
 INDEX 367

soil functioning, effect of plant species meta-communities 142, 143 taxonomic standardization 287
richness 131 multiple stable states 91–2 taxonomy of plants, relationship to
soil microbes, field experiments and relationship to biodiversity 10 extinction risk 63
observations 129–30 theoretical links to biodiversity 79 temperature, effect on decomposition
soil organic carbon (SOC) 154, 164 see also temporal stability rate 154
Solan, M. et al. 66, 73, 74, 281 stabilizing forces 114 temporal stability 78, 79–80, 172, 188
Solidago altissima Stanley, W.G. and Montagnini, F. 158 mechanisms of diversity's effects
clonal diversity 176 stated preference valuation methods 84–5
genotypic richness 155 252, 253 in multi-trophic communities 81,
Solow, R.M. 259 statistical averaging 79 82–3
Soule, J.D. and Piper, J.K. 270 statistical modelling 94, 103 pollinator services 196–7
source-sink meta-community diversity–interactions within a single trophic level 80, 81,
model 140–1 approach 98–9 82
South Africa, forest and woodland meta-analysis of results 99–103 temporal variability (CV) 80
asset values 260–1 random partitions design 98 BEF effects 219
Spartina anglica, facilitation of native Steenwerth, K.L. et al. 181 in impact of colonizing species 226
species 222 Steiner, C.F. et al. 80, 81, 82, 84, 85, 88, protistan food webs 126
Spartina marshes, construction 168 126 Thébault, E. and Loreau, M. 109
spatial autocorrelation 144 sterilized Earth thought experiment theory-driven studies 293
spatial averaging 138, 140, 143, 145 5–7 tick-borne encephalitis 120
spatial insurance hypothesis 118, stochastic production frontier (SPF) Tilman, D., resource-based model
139–40, 144, 145 approach 272–3 274, 275
spatial stability, pollinator services stocks, biodiversity effects 22–4, 27 Tilman, D. and Downing, J.A. 85, 86,
197, 199–201 Stoneham, G. et al. 242 88, 89
spatial storage effect 144 strawberry, spatial stability of Tilman, D. et al. 80, 81, 84, 231, 257
spatial variance pollinator services 200 citations 38
fragmented landscapes 137–8, 139 stream insects, detritus processing 73, timber extraction study, Uttar
pollinator services 198 74 Pradesh 237–8
specialization, animals, relationship to Strong, D.R. 110 top-down biodiversity effects 16–17,
extinction risk 64 strong interactors 105 23, 24, 27, 107, 108, 109, 137
species, composition, relative structural reorganization 61, 65–6 empirical evidence 111–12
importance 210–11 biomass compensation 66–7 tourism 235
species–area relationship 136–7 cascading extinction 67–8, 69 GEEM model 268
species complementarity 95, 99–100, Sub-Saharan Africa, wealth 259 tradeoffs 115, 155, 174
101 succession in carbon sequestration 163–4
species composition effect (SCE) 97 carbon sequestration 152–3, 164 life histories 285
species identification, microbes 124 trait-based research 284 trade restrictions 245
species richness successional colonizers 218, 224 traditional approach 3
effects on functional diversity suites of traits 70, 71, 152, 153, 173–4 TraitBank 288
54–8 Sumatra, biodiversity 183, 190 trait-based extinction scenarios 72–5,
relationship to disease risk 209 sunflower pollination, functional 76, 292–3
species richness effect (SRE) 97 facilitation 201 trait-based research 281, 283–4
species selections in research 292–3 super colony formation, Argentine see also TraitNet
species-sorting models 117–18 ants 221 trait data, databases 286
spillover, emerging diseases 215 super-competition, invasive species 224 trait-dependent complementarity
spinach, presence of E. coli 190 support services 248–9, 293, 294, 295 effect (TDCE) 96, 101–2
Srinivasan, U.T. et al. 73, 74, 76, 112 sustainability 178, 249 trait diversity 211
Srivastava, D.S. et al. 27 sustainability indicators 259 colonizing species 224, 226, 228
stability 78, 93, 188 sustainable development 295–7 trait-independent complementarity
of ecosystem services 92–3 Symstad, A.J. et al. 171 effect (TICE) 96
in restoration 172–3 system-driven studies 293 TraitNet 282, 285, 288–9
empirical findings 89 tariffs, effect on accidental areas of research 285–6
resilience 87, 88–9 introductions 244 architecture 285
resistance 83, 85, 86–7 data integration 286–8
temporal stability 79–83 Taxonomic Concept Schema (TCS) integration into ecoinformatics
food web properties 89–91 287 frameworks 288
measures of ecosystem function 83 Taxonomic Object Service (TOS) 287 trait observation schema 287
368 INDEX

trait protocol standardization 288 Unified Neutral Theory of West Nile virus 120
traits 54, 59, 61 Biodiversity and diversity–disease curve 210
inclusion in measurement of Biogeography 114, 152 wetlands
functional diversity 58 trait-based research 284 changes, expected damage
relationship to ecosystem function USDA PLANTS database 286 function 257
70–2 use value 250 ecosystem services 173
relationship to extinction risk 62–5 utility index 277 edge effects 190
relationship to secondary extinction Uttar Pradesh, timber extraction white-footed mouse, impact on Lyme
risk 69 study 237–8 disease risk 213
relationship to structural Wilby, A. et al. 181
reorganization 65–70 Valone, T.J. and Hoffman, C.D. 81, 82, Wilby, A. and Thomas, M.B.
trait space 188, 189
84
dimension reduction 70 valuation of ecosystems 11, 12, 174–5, Wilderness Act (1964), United
effective dimensionality 55 230–1, 249–51, 261–2 States 264
trait syndromes 70, 71 wildlife-friendly farming 183
bees as crop pollinators 207–8
trajectories of ecosystem function 4, Williams, S.L. 176
forest and woodland, South Africa
17, 24–6, 25, 28 260–1 Wirth, C. 162
transferable development rights (TDR) Keoladeo National Park 254 Wohl, D.L. et al. 127
240–1 wood density measurement 288
mangrove storm buffering 257–8
transgressive overyielding 95, 103, 186 methods 252 Wootton, J.T. 157
meta-analysis 99–100 microbial functions 125 working groups, TraitNet 285
travel cost valuation method 252, 253 natural pest control 191–2 World Bank, adjusted net savings
trees indicator 259, 261, 262
provisioning and cultural services
carbon loss, experimental studies 251–6 World Environmental Organization
161–2 regulating services 256–7 (WEO) 246
carbon sequestration 73, 74, 154–5, value production function 271 World Summit on Sustainable
163–5 Development (Johannesburg
Van Kooten, J. and Bulte, E.H. 245
experimental studies 158–60 Van Peer, L. et al. 86, 87 2002) 296
primary forests 163 variance in edibility hypothesis 107, World Tourism Organization 235
genotypic richness 155–6 World Trade Agreement 125
111
Treton, C. et al. 128 Varroa destructor, bioeconomic risk World Trade Organization (WTO)
tripartite additive partitioning 96–7, analysis 226–7 246
101 Vehvilaäinen, H. et al. 162 Worm, B. et al. 93, 174, 230
TRIPS Agreement 235–6
vertical diversity 109
trophic cascades 61, 108, 110 vicarious use value of ecosystems 251 yellow fever risk, effect of
experimental data 113 Vilà, M. et al. 159, 160 deforestation 214
trophic complexity 8 vincristine 235, 236
trophic groupings 53–4
Vitousek, P.M. and Hooper, D.U. 4 Zavaleta, E.S. and Hulvey, K.B.
trophic interactions, effects on Vittor, A.Y. et al. 214
stability 90 73, 74
Vogt, R.J. et al. 81, 82, 84, 85 zebra mussels (Dreissena polymorpha),
trophic levels
biodiversity effects 16–17, 22, 23, bioeconomic risk analysis 226
24, 27–8, 107–10 Walker, B. et al. 50, 51, 52, 53, 276–7 Zedler, J.B. 168
empirical evidence 110–13 Wardle, D.A. et al. 85, 86, 158, 161, 181 Zhang, Q.G. and Zhang, D.Y. 80, 81,
relationship to cascading extinction Wardle, D.A. and Zackrisson, O. 158, 82, 84, 86, 87
68, 69, 70 161 Zhu, Y. et al. 214
relationship to extinction risk 63, wasps, parasitoid diversity 83 zoonotic diseases 120, 215
64, 65, 115–16 water cycling, shapes of biodiversity reservoir hosts 213
tropical freshwater fishes, extinction effects 26, 28 see also Lyme disease
scenarios 74, 75, 76 Wätzold, F. et al. 263 zooplankton, temporal stability 80,
TRY database 286 wealth 259 81
Tschirhart, J. 267 Weibull, A.C. et al. 187 Zostera marina
two-way additive partitioning 96 Wenum, J. et al. 272 clonal diversity 176
Tylianakis, J.M. et al. 81, 83, 204 Wertz, S. et al. 124, 130 genotypic richness 155
 Concerns over consequences of biodiversity loss
• Economic • Ethical Schulze and Mooney (1994)
• Scientific • Religious Vitousek et al. (1997)

Hypothesis generation
• Rivet
• Redundancy
• Idiosyncratic

Hypothetical scenario Laboratory experiments Historical data Theoretical

Phase 1: Environmental

generation
Emmerson and Tilman et al. (1997b)
variation controlled

For reviews:
• Expert opinion Hooper et al. (2005) Huxham (2002) Cardinale et al. (2004)
Sala et al. (2000) Naeem et al. (2002)
Hughes and Petchey (2001)
Loreau et al. (2001)
Criticism, validation
Limitations
& modification
• Small scale
• Heterogeneity of variance
• Simple communities
• Confounding factors
Aarssen (1997), Huston (1997),
• One trophic level
Ieno et al. (2006) • No species interactions

Reality filter

Connection to real world Real world in Field experiments Combinatorial

laboratory Theoretical
Duffy et al. (2003) Bruno et al. (2005)
Emmerson et al. (2001) Bruno et al. (2006) Yachi and Loreau(1999)
Widdicombe et al. (2000) Cardinale et al. (2000)
Ives and Cardinale(2004)
Gross and Cardinale(2005)
Increasing system complexity In situ Sp. addition and removal
Phase 2: Inclusion of subset of

• Time (O’Connor and Crowe 2005) Biles et al. (2003) Hector et al. (1999)
environmental variation

• Multi-trophism (France and Duffy 2006a) Swan and Palmer (2004) Symstad and Tilman(2001)
• Community complexity (France and Duffy 2006b) O’Connor and Crowe (2005) Diaz et al. (2003)
• Multi-functionality (Hector and Bagchi 2007).

Biodiversity futures
based on data Model with validation
Naeem and Wright (2003) Emmerson and Raffaelli (2000)
Swan and Palmer (2005)
Fox (2006)
Empirically derived Summaries and
scenario generation meta-analyses
Controversy Covich et al. (2004) Relevance
Solan et al. (2004) Zavaleta and Hulvey (2004) Balvanera et al. (2006)
Bunker et al. (2005) McIntyre et al. (2007) Flint and Kalke (2005) Cardinale et al. (2006)
Bracken et al. (2008) Raffaelli et al. (2005a, b) Worm et al. (2006) Srivastava and Vellend (2005)

Movement to the real world

environmental variation
Phase 3: Incorporating

Natural and anthropogenic gradients of disturbance Field observations Indirect manipulations

Fukami and Wardle (2005) Wardle et al. (1997) • Diseases
Troumbis and Memtsas (2000) • Extractive industry
Cardinale et al. (2005) • Paleological record
Statistical partitioning Natural reduction of Ruesink et al. (2006) • ‘Freak’disturbance events

e.g. • partial linear regression confounding factors

• variance partitioning
Vitousek et al. (1994)
Austin (2002)

Application in the real world

Extension to landscape Connection with Translation Aid management and

and ecosystem scales ecosystem services to policy conservation issues
Diaz et al. (2006) Millennium Assessment (2005) Srivastava and Vellend (2005)

BEF indices
Expert advice Scholes and Briggs (2005)
Rouget et al. (2006)
Loreau et al. (2006) Zhang and Zhang (2007)

Plate 1. Summary of the research approaches adopted to address the relationship between biodiversity and ecosystem function in the peer-reviewed
scientific literature. Modified from Godbold (2008). See page 32.
 (a) 1.0 (b) 1.0

Proportion of citations
Proportion of citations
to Naeem et al. (1994)
0.8 0.8

to Huston (1997)
0.6 0.6

0.4 0.4

0.2 0.2

0.0 0.0
1994 1996 1998 2000 2002 2004 2006 1994 1996 1998 2000 2002 2004 2006
Year Year
(c) 1.0 (d) 1.0
Proportion of citations
to Tilman et al. (1997)

Proportion of citations
0.8 0.8

to Loreau et al. (2001)

0.6 0.6

0.4 0.4

0.2 0.2

0.0 0.0
1994 1996 1998 2000 2002 2004 2006 1994 1996 1998 2000 2002 2004 2006
Year Year
1.0 1.0
to Hooper and Vitousek (1997)

(e) (f)
Proportion of citations
Proportion of citations
to Hector et al. (1999)

0.8 0.8

0.6 0.6

0.4 0.4

0.2 0.2

0.0 0.0
1994 1996 1998 2000 2002 2004 2006 1994 1996 1998 2000 2002 2004 2006
Year Year

Plate 2. The influence of the six most cited papers from the BEF database since publication to December 2006 for (a) Naeem et al. (1994), (b) Huston
(1997), (c) Tilman et al. (1997), (d) Loreau et al. (2001), (e) Hector et al. (1999) and (f) Hooper and Vitousek (1997). These publications influenced
subsequent publications by contributing to discussion (red), development or reinforcement of theory (orange) or methodology (yellow), or by initiating or
informing laboratory experiments (green), field manipulations (turquoise), or field observations (blue), or they were used to underpin practical applications in
the real world (pink). Expanded from Benton et al. (2007). See page 38.
 Hooper & Vitousek 1997 [346]
Hawkins et al. 2003 [186]
Willig et al. 2003 [150]
Mittelbach et al. 2001 [220]
Hector et al. 1999 [383] Leibhold et al. 2004 [150]
Ricklefs et al. 2004 [183]
Tilman et al. 2001 [195] Cardinale et al. 2002 [122]
Schroeter et al. 2005 [44]
Folke et al. 2005 [38]
Worm et al. 2006 [35]
Balvanera et al. 2006 [0]
Lewin et al. 2006 [0]
Hooper et al. 2005 [117] Zobel et al. 2006 [0]
Srivastava & Vellend 2005 [8] Renne et al. 2006 [0]
MacDougall 2005 [3] MacDougall & Turkinton 2006 [0]
MacDougall et al. 2006 [2]
Chan et al. 2006 [0]
Lamb et al. 2005 [31]
Tilman et al. 2002 [103]
Newman 2003 [1007]
Loreau et al. 2001 [403] Dunne et al. 2002a [100]
Dunne et al. 2002b [80] Williams et al. 2002 [60]
Garlaschelli et al. 2003 [58]
Jordano et al. 2003 [57]
Folk et al. 2004 [48]
De Deyn et al 2004 [21]
Ruess et al. 2004 [15]
ISI Web of Knowledge
Yeates 2003 [36] Murder et al. 2003 [19]
(extracted records = 942)
Dufty 2002 [68] Mulder et al. 2005 [14]
Yeates et al. 2003 [11]
Dufty et al. 2003 [50]
Dufty 2003 [40]
Berlow et al. 2004 [39]
Diaz et al. 2004 [54]
Tilman et al. 1996 [544]
Naeem et al. 1994 [527] Tilman et al. 1994 [469]
van der Heijden et al. 1998 [579]
Purvis & Hector 2000 [140]
Huston 1997 [440] Waide et al. 1999 [305] Knapp & Smith 2000 [140]
Zhu et al. 2000 [133]
Foody 2002 [185]
Peterson et al. 2002 [151]
Whitham et al. 2003 [89]
Lavorel & Garnier 2002 [95]
Wardle et al. 2004a [85]
Chapill et al. 2000c [309]
Callaway & Ridenour 2004 [33]
Diaz & Cabido 2001 [108]
Ehrenfeld 2003 [58] Wolfe & Klironomos 2005 [10]
Tilman et al. 1997b [447] Zedler & Kercher 2004 [11]
Allison & Votosek [11]
Petchey & Gaston 2002a [59]
Sala et al. 2000 [423]
Sakai et al. 2001 [360]
Tilman 1999b [323] Gaston 2000 [311]
Loreau 2000 [154] Loreau & Hector 2001 [159] Naeem & Wright 2003 [53]

Plate 3. The rate, form, and connectivity of information flow within the BEF community and to multiple disciplines from the six most highly cited papers
(¼BEF-6) within the BEF database. For each generation of publications, the five most highly cited publications citing the previous generation were determined
and linked, either directly (solid lines) or indirectly (dotted lines) to the BEF-6 via other highly cited publications. Line colour indicates the generation
sequence (blue ! red ! green ! orange). Publications not included in the BEF database are presented as a citation. The number of cites (from publication
until December 2006) are indicated in square brackets. References listed are available in the electronic appendix. See page 39.
Plate 4. An example of the complexity of a real, yet still relatively simple natural food web in a salt marsh (from Lafferety et al. 2007). Note that within
this system there are dozens of species (nodes) and hundreds of feeding links (lines connecting nodes) among plants, herbivores, predators and parasites that
span six or more trophic levels. Figure reproduced with permission from K. Lafferty. See page 106.

1025
Size of study system (m2 or L)/mean organism size (g)

Sm
1022 < 1 generation > 1 generation

Cl
1019

1016
Bu
Spatial scale

13
10

1010 Un
Tr

107 Mo
Wo
104

101

10–2

10–5
10–3 10–2 10–1 100 101 102 103 104 105 106
Time-scale
Duration of experiment (d)/mean generation time (d)

Plate 5. The spatial and temporal scale of biodiversity-ecosystem functioning experiments. The experimental duration (in days) and spatial scale
(in m2 or L) of experiments reviewed by Cardinale et al. (2006) were standardized to the mean generation time and body sizes of the focal organisms. Data
were divided into four trophic groups: Plants ¼ green circles, Herbivores ¼ blue triangles, Predators ¼ red squares, Detritivores ¼ brown diamonds.
The scale of each individual study is given by smaller symbols while the medians for each trophic group are shown as larger symbols. The box denoted by the
dashed line gives the 10th and 90th percentiles for the scale of all experiments. For comparative purposes we show the scale of several natural extinctions:
Wo ¼ wolves from Yellowstone National Park, USA; Mo ¼ Moa from New Zealand; Tr ¼ Trout from Lake Superior, USA; Un ¼ Unionid mussels from
the lower Mississippi River, USA; Bu ¼ Various species of butterflies in Europe; Cl ¼ Loss of certain cladoceran zooplankton from Lake Superior, USA;
Sm ¼ Global eradication of the small pox virus. See page 116.