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Biodiversity II: Understanding and Protecting Our

Biological Resources
Marjorie L. Reaka-Kudla, Don E. Wilson, and Edward O.
Wilson, Editors; A Joseph Henry Press book
ISBN: 0-309-52075-4, 560 pages, 6 x 9, (1997)
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Copyright © National Academy of Sciences. All rights reserved.

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Biodiversity II: Understanding and Protecting Our Biological Resources
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Contents

INTRODUCTION
1 Introduction 1
Edward O. Wilson

PART I. THE MEANING AND VALUE OF BIODIVERSITY

2 Biodiversity: What Is It? 7
Thomas E. Lovejoy
3 Biodiversity: Why Is It Important? 15
Ruth Patrick

PART II. PATTERNS OF THE BIOSPHERE:

HOW MUCH BIODIVERSITY IS THERE?
4 Biodiversity at Its Utmost: Tropical Forest Beetles 27
Terry L. Erwin
5 Measuring Global Biodiversity and Its Decline 41
Nigel E. Stork
6 Butterfly Diversity and a Preliminary Comparison with Bird
and Mammal Diversity 69
Robert K. Robbins and Paul A. Opler
7 The Global Biodiversity of Coral Reefs: A Comparison
with Rain Forests 83
Marjorie L. Reaka-Kudla
8 Common Measures for Studies of Biodiversity:
Molecular Phylogeny in the Eukaryotic Microbial World 109
Mitchell L. Sogin and Gregory Hinkle

iii

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 iv / BIODIVERSITY II

PART III. THREATS TO BIODIVERSITY:

WHAT HAVE
Biodiversity II: Understanding and Protecting Our Biological WE
LOST AND WHAT MIGHT WE LOSE?
Resources
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9 The Rich Diversity of Biodiversity Issues 125
Norman Myers
10 Human-Caused Extinction of Birds 139
David W. Steadman
11 Global Warming and Plant Species Richness: A Case Study
of the Paleocene/Eocene Boundary 163
Scott L. Wing
12 Plant Response to Multiple Environmental Stresses:
Implications for Climatic Change and Biodiversity 187
Irwin N. Forseth

PART IV. UNDERSTANDING AND USING BIODIVERSITY

13 Names: The Keys to Biodiversity 199
F. Christian Thompson
14 Systematics: A Keystone to Understanding Biodiversity 213
Ruth Patrick
15 Biodiversity and Systematics: Their Application to Agriculture 217
Douglass R. Miller and Amy Y. Rossman
16 Snout Moths: Unraveling the Taxonomic Diversity of
a Speciose Group in the Neotropics 231
M. Alma Solis
17 Phylogeny and Historical Reconstruction: Host-Parasite Systems
as Keystones in Biogeography and Ecology 243
Eric P. Hoberg
18 Comparative Behavioral and Biochemical Studies of
Bowerbirds and the Evolution of Bower-Building 263
Gerald Borgia

PART V. BUILDING TOWARD A SOLUTION:

NEW DIRECTIONS AND APPLICATIONS
19 Microbial Biodiversity and Biotechnology 279
Rita R. Colwell
20 The Impact of Rapid Gene Discovery Technology on Studies
of Evolution and Biodiversity 289
Carol J. Bult, Judith A. Blake, Mark D. Adams, Owen White,
Granger Sutton, Rebecca Clayton, Anthony R. Kerlavage,
Chris Fields, and J. Craig Venter

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 CONTENTS / v

21 Initial Assessment of Character Sets from Five Nuclear

Biodiversity II: Understanding and Protecting OurGene Sequences
Biological in Animals
Resources 301
http://www.nap.edu/catalog/4901.html Timothy P. Friedlander, Jerome C. Regier, and Charles Mitter
22 Gap Analysis for Biodiversity Survey and Maintenance 321
J. Michael Scott and Blair Csuti
23 Conservation of Biodiversity in Neotropical Primates 341
James M. Dietz
24 Using Marine Invertebrates to Establish Research and
Conservation Priorities 357
James D. Thomas
25 Ecological Restoration and the Conservation of Biodiversity 371
William R. Jordan, III
26 Tropical Sustainable Development and Biodiversity 389
Patrick Kangas
27 Wildland Biodiversity Management in the Tropics 411
Daniel H. Janzen

PART VI. GETTING THE JOB DONE:

INSTITUTIONAL, HUMAN, AND INFORMATIONAL INFRASTRUCTURE
28 Taxonomic Preparedness: Are We Ready to Meet
the Biodiversity Challenge? 435
Quentin D. Wheeler and Joel Cracraft
29 Museums, Research Collections, and the Biodiversity Challenge 447
Leslie J. Mehrhoff
30 Resources for Biodiversity in Living Collections and the
Challenges of Assessing Microbial Biodiversity 467
Richard O. Roblin
31 Integration of Data for Biodiversity Initiatives 475
David F. Farr and Amy Y. Rossman
32 Information Management for Biodiversity: A Proposed
U.S. National Biodiversity Information Center 491
Bruce L. Umminger and Steve Young

PART VII. CONCLUSIONS

33 Santa Rosalia, the Turning of the Century, and a New Age
of Exploration 507
Marjorie L. Reaka-Kudla, Don E. Wilson, and Edward O. Wilson

Photo Credits 525

Index 527

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CHAPTER
1

Introduction

EDWARD O. WILSON
Pellegrino University Professor, Museum of Comparative Zoology,
Harvard University, Cambridge, Massachusetts

“Biodiversity,” the term and concept, has been a remarkable event in recent
cultural evolution: 10 years ago the word did not exist, except perhaps through
occasional idiosyncratic use. Today it is one of the most commonly used expres-
sions in the biological sciences and subsequently has become a household word.
It was born “BioDiversity” during the National Forum on BioDiversity, held in
Washington, D.C., on September 21-24, 1986, under the auspices of the National
Academy of Sciences and the Smithsonian Institution. The proceedings of the
forum, published in 1988 under the title BioDiversity (later to be cited with less
than bibliographical accuracy by most authors as Biodiversity), became a best-
seller for the National Academy Press. By the summer of 1992, as a key topic of
the Rio environmental summit meeting, biodiversity had moved to center stage
as one of the central issues of scientific and political concern world-wide.
So what is it? Biologists are inclined to agree that it is, in one sense, every-
thing. Biodiversity is defined as all hereditarily based variation at all levels of
organization, from the genes within a single local population or species, to the
species composing all or part of a local community, and finally to the communi-
ties themselves that compose the living parts of the multifarious ecosystems of
the world. The key to the effective analysis of biodiversity is the precise defini-
tion of each level of organization when it is being addressed.
Even though the study of biodiversity can be traced back as far as Aristotle,
what finally has given it such extraordinarily widespread attention is the real-
ization that it is disappearing. In the late 1970s and through the 1980s, the first
convincing estimates were made of the rate of tropical deforestation, which
translates to the areal loss of habitat where most of living diversity is concen-

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2 / BIODIVERSITY II

trated. This information led to disturbingly high estimates of the rates of loss of
species in these forests. The magnitude of erosion also drew attention to ongo-
ing extinction in other habitats, from deserts to coral reefs, at all levels of bio-
logical organization from alleles to entire local ecosystems. It became clear that
the decline of Earth’s biodiversity was serious. Worse, unlike toxic pollution
and ozone depletion, it cannot be reversed.
Scientists who once had devoted their careers to bits and pieces of bio-
diversity now became holists, or at least more approving of the holistic approach,
and they were energized by a new sense of mission. For the good of society as
a whole, they now realized that the classification of such organisms as braconid
wasps and lauraceous shrubs mattered. Moreover, the ecologists also were in-
cluded: the processes by which natural communities are assembled and their
constituent species maintained have central importance in both science and the
real world. The study of diversity subsumed old problems in systematics and
ecology, and specialists in these and in related fields of biology began to talk in
common parlance as never before. Just as significantly, physical scientists, so-
cial scientists, geographers, and artists were drawn into the colloquy. The sub-
ject consequently has begun to be reshaped into a new, often surprisingly eclec-
tic field of inquiry. Today we now hear regularly of “biodiversity science” and
“biodiversity studies.”
Since the 1986 National Forum on BioDiversity, there has been an exponen-
tial rise in research and technical innovation. Scientists appreciate that only a
tiny fraction of biodiversity on Earth has been explored, and that its origin and
maintenance pose some of the most fundamental problems of the biological sci-
ences. These problems are also among the least technically tractable. Those
who have cut into the outer surface of ecology and evolution suspect that mo-
lecular and cell biology eventually will prove simple by comparison.
The present volume is a 10-year report on the state of the art in biodiversity
studies, with an emphasis on concept formation and technique. Overall, it makes
a striking contrast with the original BioDiversity, showing how extraordinarily
far we have come and at the same time mapping how far scientists yet must
travel in their reinvigorated exploration of the biosphere.
Some scientists and policy-makers have worried that the magnitude of the
biodiversity we now know to be present in the world’s habitats is so enormous,
the cost of exploring and documenting it so overwhelming, and the number of
biologists who can analyze and document it so small that the goal of understand-
ing the diversity of the world’s species is unattainable. The central message of
this volume is, to the contrary, that the potential benefits of knowing and con-
serving this biodiversity are too great and the costs of losing it are too high to
take a path of least resistance. By documenting the infrastructure of knowledge
and institutions that already are in place, this volume suggests that there is a
cost-effective and feasible way of approaching the conservation of the world’s
biological resources. The key to a cost-effective solution to the biodiversity

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INTRODUCTION / 3

crisis lies in the collaboration of museums, research institutions, and universi-

ties; the pooling of human and financial resources; and the shared use of physi-
cal and institutional structures that are already present. Rather than building
the knowledge, institutional and physical infrastructure for documenting bio-
diversity from the ground up, we need to build upon preexisting infrastructure
and increase support for systematics, training, and museums.
This volume is an outgrowth of one such endeavor, the recent establish-
ment of a Consortium for Systematics and Biodiversity between the Smithsonian
Institution, the University of Maryland at College Park, the U.S. Department of
Agriculture Systematics Laboratories, the University of Maryland Biotechnol-
ogy Institute, and the American Type Culture Collection. The Consortium, dedi-
cated to enhancing the conceptual understanding and documentation of bio-
diversity of organisms (from viruses and bacteria to invertebrate and vertebrate
animals, protists, fungi, algae and higher plants) in living and nonliving mu-
seum collections, represents the type of cooperation that will be necessary for us
to cost-effectively understand and protect our natural resources.

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4 / BIODIVERSITY II

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CHAPTER
2

Biodiversity: What Is It?

THOMAS E. LOVEJOY
Counselor to the Secretary for Biodiversity and Environmental Affairs,
Smithsonian Institution, Washington, D.C.

Biodiversity has to be thought of in a number of different ways. One would

begin by looking at the overall perspective of evolutionary time and more spe-
cifically by looking at a great radiation (such as that of the Hawaiian honey-
creepers) from a single ancestor. Another way of viewing biodiversity is as a
characteristic of natural communities. For instance, a forest in Southern New
England characteristically will contain about 20 or 30 tree species, but in a
marshy area in Southern New England or farther north, forests are composed of
only two or three species. In contrast, a tropical forest, such as in Amazonian
Peru, will contain hundreds of species of trees. Therefore, natural communities
each have their own characteristic biodiversity, both in terms of numbers and
composition of species.
Another way of looking at biodiversity is globally and collectively. While
the number of species currently described is on the order of 1.4 million, the big
question is how many species are there totally? Current estimates of the total
number of species run from 10-100 million. One can break it down and look at
certain segments of global totals, such as the diversity of higher plants, number
of species, or expressed as sheer weight (biomass). The degree of knowledge
about biodiversity varies with both location and taxon (classificatory groups of
organisms). For example, the British insect fauna is much better known than the
Australian insect fauna. (Indeed I believe that there are so many naturalists in
Britain that it is impossible for a bird to lay an egg without three people, includ-
ing at least one cleric, recording it). Within Australia, vertebrates are better
known than insects. That relation is true throughout most of the world, because

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8 / BIODIVERSITY II

we have tended toward vertebrate chauvinism in the exploration of biodiversity

(Wilson, 1985).
Another way to think about biodiversity is where it is most concentrated.
The best known concentration, of course, is in tropical forests—those places
near the equator where there is enough moisture sufficiently evenly distributed
through the year to maintain a tropical forest formation. These forests comprise
roughly 7% of the dry land surface of the Earth and may hold more than 50% of
all species. The reality, however, is that we do not know precisely how much
biodiversity is concentrated in a particular biological formation. A characteris-
tic pattern of biodiversity is a general increase in numbers of species as one
approaches the equator. For example, São Paulo, just within the tropics, holds
100 times more species of ants than Tierra del Fuego, and the number at the
equator will be even higher than at São Paulo (MacArthur, 1972). This is a
pattern that repeats itself again and again for many groups of organisms, but, of
course, not all. The marine realm has more representations of the major group-
ings of life than those on land, and the realm of soil biology is so poorly explored
that it is hard to tell what rich forms of life might exist there. So as we learn
more about life on Earth, the relative proportions of where life on Earth is con-
centrated can be expected to change.
In the tropical forest, the forest canopy is an entirely different realm that
can be studied with a tower or a crane like that used by the Smithsonian Tropi-
cal Research Institute. The only species that the canopy shares with the forest
soil are the canopy trees themselves. All the rest are almost entirely different.
The canopy is a vast, unexplored place for biodiversity. Terry Erwin, a Smith-
sonian entomologist, in the first major analysis of biodiversity of the canopy,
suggested that the number of species with which we share this planet had been
underestimated by at least a factor of three (Erwin, 1982). The larger point is
that the more people look at the tropical forest in different ways, as Terry Erwin
has done, the more biodiversity there seems to be. This does not mean that the
same thing will not happen also in the marine realm or in the area of soils and
microorganisms. It may well happen and is part of the excitement of exploring
life on Earth.
Biodiversity matters to human beings in a variety of ways (Lovejoy, 1994).
There are important aesthetic and ethical dimensions, but part of our existence
depends on direct use, whether it is the botanical species that flavor gin or the
wild relatives of a major agricultural crop such as the species of wild perennial
corn found in Mexico about 20 years ago. Previously there had been only one
species of perennial corn described, discovered in fact by a Smithsonian bota-
nist early in the century. But unlike the species discovered in the 1970s, it did
not have the same number of chromosomes as domestic corn. With the discov-
ery of this second species of perennial corn, it became relatively easy to transfer
some of the traits of perennial corn into corn agriculture, making the long-term
dream of a perennial corn crop, as well as the more short-term one of disease

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BIODIVERSITY: WHAT IS IT? / 9

resistance, an achievable goal. The importance of these kinds of contributions

to agriculture can be underscored by noting that corn is the third most impor-
tant grain supporting human societies. Another example in which a wild spe-
cies benefits agriculture is illustrated by a species of wild potato from Peru that
has a characteristic resistance to insect attacks that is being incorporated ac-
tively into potato agriculture to deal with potato beetles.
Another completely different way in which organisms can benefit humans
is the rapidly growing area known as bioremediation. For example, a species of
bacteria discovered in the sediments of the Potomac River by a scientist with the
U.S. Geological Survey is capable of breaking down chlorofluorocarbons (CFCs)
in anaerobic conditions (Lovley and Woodward, 1992). There are many organ-
isms in nature with unusual metabolisms and appetites that could prove to be
beneficial in cleaning up some pollution problems and could become of great
significance in the rapidly developing field of industrial ecology.
One of the most interesting aspects of biodiversity is the evolutionary ten-
sion between species of insects that exert grazing pressure on species of plants
and the chemical and biochemical defenses that these plant species produce to
reduce that pressure. This “tug of war” is a source of a wide range of useful
molecules for the field of medicine. The best-selling medicine of all time, aspirin
(salicylic acid which derives its name from the Latin, Salix, for willow), is based
on just one of these molecules, the discovery of which dates back to the time of
Hippocrates when he prescribed mashed willow bark as a painkiller. Today, of
course, the molecule is synthesized in a factory and there is no need to go back
to nature for it, but the idea behind it came from looking at natural biodiversity.
Discoveries for the advancement of medicine and understanding of the life
sciences constitute one of the most powerful ways in which biodiversity can
contribute to human society. Often going unnoticed and rarely documented,
extremely important discoveries have been made from organisms that were pre-
viously considered relatively peripheral to human society. For example, Penicil-
lium mold at one time was valued for what it did to flavor blue cheeses, but that
was dwarfed in subsequent times, when it sparked the concept of antibiotics.
There are interesting intellectual chains deriving from natural phenomena.
A South American pit viper might seem of little relevance to someone living in
Washington, D.C., or Chicago, yet studies on the venom of one species of these
vipers led to the discovery of the angiotensin system that regulates blood pres-
sure in human beings. Once that system was known, it became possible to
devise a molecule that alters blood pressure and is the preferred prescription
drug for hypertension. This compound brings the Squibb Company $1.3 billion
a year in sales and contributes to the well-being and longevity of millions of
Americans and others.
Yet another way to think about biodiversity is the way in which it collec-
tively provides us with “free services.” Consider the Amazon River, with its
tremendous drainage area and the important fishery on which people of the

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10 / BIODIVERSITY II

Amazon depend. The water chemistry of the Amazon basin is insufficient to

support the productivity of that fishery. Instead, the productivity depends on
a linkage between the terrestrial ecosystem and the aquatic one. When the
rivers of the basin flood (10-15, sometimes 20 m high), they spill over into the
floodplain forest. Fish then can swim into the forest and feed on the fruits, nuts,
seeds, and other organic material that fall into the water. The Amazonian fish-
ery thus depends on an ecological service in which nutrients are transferred
from the terrestrial ecosystem to the aquatic ecosystem, with major benefits to
people living in the area (Goulding, 1980).
Sometimes even a single species performs a vital service. In the Chesapeake
Bay, the oyster plays a very critical role. Today the oyster population of the
Chesapeake Bay filters a volume of water equal to that of the entire bay about
once a year. Before various factors, most human-driven, led to the decline of the
oyster population, it filtered a volume equal to the entire bay about once a week
(Newell, 1988). That is an interesting example in which a single keystone spe-
cies in an ecosystem can have profound implications for how, in this instance, a
grand estuary and major source of various types of seafood actually functions.
On larger landscape scales, biodiversity provides services such as under-
pinning the hydrological cycle in the Amazon, in which literally half of the
rainfall in the Amazon is generated within the basin. If the Amazon forest were
to be replaced with grassland, a rough computer model predicts that about one-
fourth of that rainfall would not occur, and would be accompanied by associ-
ated temperature increases (Nobre et al., 1991). These effects would spill over to
other geographical areas, for example, central Brazil, which also depends on the
Amazon as a source of moisture for rainfall. Thus, the hydrological cycle is
basically dependent on those vast natural forest communities.
Another extremely valuable way in which biodiversity serves human soci-
ety is as an indicator of ecological change. A few years ago, herpetologists
studying amphibians, particularly frogs, began to compare incidental notes and
realized that there was a major decline in populations of frogs throughout the
world in patterns that still are hard to understand and explain. Something or
some things are happening that appear to affect frog populations, and it would
be extremely valuable to identify these vectors of change before they affect
humans directly.
Stress in the biological community also reduces biodiversity. For example,
extreme air pollution in Cubatão in São Paulo state (often called the valley of
death) was so severe in the 1970’s and 1980’s that it killed most of the trees in
the surrounding Atlantic forest. It reduced biodiversity and vegetative cover to
the point that there were landslides. In another example, high loads of fertiliz-
ers that put stress on a pasture in England during the period 1856-1949 reduced
the number of species of native plants from 49 to 3. The good news, of course,
is that if you remove the stress (and the species are still in existence and nearby),
characteristic diversity will recover over time.

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BIODIVERSITY: WHAT IS IT? / 11

An excellent way to understand factors affecting biodiversity is by looking

at islands. They are small, confined areas, more easily managed for study, where
cause and effect often appear more clearly. In the Hawaiian islands, for example,
the loss of species from human activity has been taking place for centuries. A series
of Hawaiian bird species became extinct at the hands of the native Polynesians
prior to European arrival. Studies by Storrs Olson at the National Museum of
Natural History and David Steadman at the New York State Museum have shown
that this pattern repeats itself over and over again in the Caribbean and Pacific
islands (Steadman and Olson, 1985). The notion that indigenous peoples were
always in exquisite harmony with their environment is just not true.
One of the major problems in global biodiversity is introduced species.
Exotic faunas represent a very severe problem all over the world, but particu-
larly in island situations. The Stephen Island wren is a dramatic example. The
first and last specimen of that species confined to that single island was killed by
a species not indigenous to the island—the lighthouse keeper’s cat. The most
recent flora of Hawaii contains more alien or exotic species than native ones
(Wagner et al., 1990).
By far the biggest problem in protecting the world’s biodiversity is habitat
destruction, whether it is southern California, where the California gnatcatcher
and many other species live in declining patches of coastal sage scrub habitat, or
whether it is the rapidly shrinking tropical forests in many parts of the world.
The numbers of loss can be staggering. The state of Rondonia in western
Amazonia lost 20% of its forest in 5 years. Today Suriname and Guyana teeter
on the brink of losing much of their forest to foreign interests.
Another outcome of habitat destruction is that the available habitat is bro-
ken up into pieces. When we begin to look at what this means for biodiversity,
a very disturbing picture begins to appear. For example, in 1920 there were 208
species of birds known on the Smithsonian’s Barro Colorado Island, an island
that was created by the flooding of the area of the Gatun Lake for the Panama
Canal. Fifty years later, a number of these species were gone and, in the original
analysis by Ed Willis (1974) of that loss, a significant number of the species (18)
were thought to be lost simply because the isolated fragment of the island was
not large enough to support them. The fragmentation of habitats leaves rem-
nants no longer connected to a larger wilderness and hence species are lost over
time. This has serious implications for conservation. Among other study sites,
Smithsonian and Brazilian scientists are studying fragmentation in the middle of
the Amazon (Bierregaard et al., 1992; Lovejoy et al., 1983, 1984). Fragmentation
has serious implications for the use of landscapes. The good news is that if
riparian habitats (vegetation along watercourses) are restored, the landscape has
much more connectivity, eliminating some of the fragmentation problems.
There are also regional effects of pollution. Some examples include the air
pollution of Cubatão discussed above and acid rain, which is a problem in tropi-
cal as well as northern industrial countries. Taken together, all the different

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12 / BIODIVERSITY II

ways human activity affect biodiversity have driven extinction rates to a level
1,000-10,000 times the normal rate (May et al., in press; Wilson, 1985).
An additional and ultimate concern is global climatic change due to increas-
ing levels of greenhouse gases. Most of these gases come from the burning of
fossil fuels (essentially burning of old vegetation stored under the surface of the
Earth) that represent carbon reservoirs that have been stored for thousands or
millions of years, but which now are being oxidized and released into the atmo-
sphere in a very short geological time. Burning of the forests is also a major
contributor to the greenhouse gases, releasing nearly 1 billion tons of carbon as
carbon dioxide (CO2) annually.
The most famous graph of the twentieth century may well be that showing
the curve of increasing CO2 in the atmosphere as measured from the top of a
volcano in Hawaii. Every year, inexorably, there is an increase in the amount of
CO2. There is also an annual decrease in atmospheric CO2 caused by spring in
the Northern Hemisphere, when the trees leaf out and, together with other
plants, take up approximately 5 or 6 billion tons of CO 2. This is returned at the
end of the year as the leaves drop and plant materials decay. However, a signifi-
cant portion of the net annual increase in CO2 comes from the pool of carbon that
results from destroyed biomass and biodiversity.
Climatic change has serious implications for agriculture, but the resulting
problems probably can be solved much easier than can serious problems with
biodiversity. Biodiversity is dependent on an intricate web of factors that can
be upset by rapid climatic change. Climatic change is, in fact, nothing new in
the history of life on Earth. Climatic change has been extensive in the past 1
million years or so, which have been characterized by glacial and interglacial
periods. During these periods, species tracked their required conditions, each
migrating according to their particular dispersal rate—often moving up or down
slope, up or down latitude. Today, however, most biodiversity, or at least an
increasing proportion of it, is locked up in isolated patches. In the face of cli-
matic change, even natural climatic change, human activity has created an ob-
stacle course for the dispersal of biodiversity. This could establish one of the
greatest biotic crises of all time.
Beyond the immediate causes that threaten biodiversity, there are ultimate
causes, such as human population growth—which adds roughly 100 million
new people to the human population every year—and the massive impact of
economic activities. In addition to these activities and the per capita consump-
tion in the industrial world, there is an enormous, complex web of interactions.
When a product is purchased, there may be a long chain between that product
and some other part of this country or some other part of the world which often
go unnoticed. For example, had New Coke been successful, the lack of vanilla in
the formula would have undercut the only element (vanilla) in the economy of
one region of Madagascar, possibly forcing that island country to fall back on its
only other source of income—its remaining forests—which are already in peril.

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BIODIVERSITY: WHAT IS IT? / 13

It will be a major challenge to avoid a staggering loss of biodiversity in the

decades and centuries ahead. The increasing interest in ecosystem management
and attempts to implement it will be very helpful. South Florida is a prime
example. There, a channelized Kissimmee River feeds into Lake Okeechobee.
The increasing use of phosphates from agricultural areas pollutes the drainages
to the south of Lake Okeechobee. Also, ditching, diking, and draining to pro-
vide flood control and water supply for the benefit of large populated areas
along the coast has led to the ultimate arrival of only one-fourth to one-half of
the normal annual freshwater flow in Florida Bay. Correlated with this are algal
blooms, the collapse of the shrimp fishery, and hypersaline water pouring out
between the keys onto the already-stressed coral reefs. The only way to restore
the ecosystem of south Florida close to that approaching a natural condition
would require that all the major agencies of state and federal governments are
involved. All the stakeholders, such as business and environmental groups,
need to be involved. If we can bring about a more integrated approach to living
within our ecosystems, we are much more likely to save the fundamental struc-
ture of biodiversity.
As an understanding of sustainable development deepens, I believe a major
portion will turn out to be biologically based. A prime example is tied to the
1993 Nobel Prize for chemistry. Kary Mullis shared the prize for the conception
of the polymerase chain reaction (PCR). This reaction, which is just about the
only true science in the popular work of fiction, Jurassic Park, has made it pos-
sible to do esoteric work such as the positive identification of the remains of
Czar Nicholas II and his family. It is also a fundamental part of diagnostic medi-
cine today. It is now no longer necessary to wait 3 days for a culture to be
grown before receiving a diagnosis and prescription. The polymerase chain
reaction is an important part of biotechnology and molecular biology.
The polymerase chain reaction only works because of an enzyme discov-
ered in a bacterium found in the hot springs of Yellowstone. Science and society
have benefited from these protected hot springs. In 1872, the area was set aside
as the world’s first national park—an act undertaken only on the basis of
Yellowstone’s scenic wonders. The fundamental goal of the National Biological
Survey1 is to organize our knowledge of biodiversity and obviate the need for
that kind of luck. A survey indeed is a very old idea and a kind of activity that
was going on even in the colonial period of this country. The concept of a
biological survey received a great boost from Spencer Baird when he was Assis-
tant Secretary of the Smithsonian and through the encouragement of C. Hart
Merriam, the founder of the original U.S. Biological Survey. It is just basic
biological good housekeeping to try to find out what we have and where it is. In
turn, biodiversity can be enjoyed in a variety of ways and we can learn even
more about it and thus help ourselves achieve sustainable development.
1 The name of the National Biological Survey recently has been changed to the National Biological

Service by the Secretary of the Interior, Bruce Babbitt.

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14 / BIODIVERSITY II

REFERENCES
Bierregaard, R. O., Jr., T. E. Lovejoy, V. Kapose, A. A. dos Santos, and R. W. Hutchings. 1992. The
biological dynamics of tropical rainforest fragments. BioScience 42:859-866.
Erwin, T. L. 1982. Tropical forests: Their richness in coleoptera and other arthropod species.
Coleopt. Bull. 36(1):74-75.
Goulding, M. 1980. The Fishes and the Forest. University of California Press, Berkeley.
Lovejoy, T. E., R. O. Bierregaard, J. M. Rankin, and H. O. R. Schubart. 1983. Ecological dynamics of
tropical forest fragments. Pp. 377-384 in S. L. Sutton, T. C. Whitmore, and A. C. Chadwick,
eds., Tropical Rain Forest: Ecology and Management. Blackwell Scientific Publications, Ox-
ford, England.
Lovejoy, T. E., J. M. Rankin, R. O. Bierregaard, K. S. Brown, L. H. Emmons, and M. E. Van der
Voort. 1984. Ecosystem decay of Amazon forest fragments. Pp. 295-325 in M.H. Nitecki, ed.,
Extinctions. University of Chicago Press, Chicago.
Lovejoy, T. E. 1994. The quantification of biodiversity: An esoteric quest or a vital component of
sustainable development? Phil. Trans. R. Soc. Lond. B 345:81-87.
Lovley, D. R., and J. C. Woodward. 1992. Consumption of freons CFC11 and CFC12 by anaerobic
sediments and soils. Envir. Sci. Technol. 26:925-929.
MacArthur, R. H. 1972. Geographical Ecology: Patterns in the Distribution of Species. Harper and
Row, N.Y.
May, R. M., J. H. Lawton, and N. E. Stork. 19__. Assessing extinction rates. In press in J. H.
Lawton and R. M. May, eds., Extinction Rates. Oxford University Press, Oxford, England.
Newell, R. I. E. 1988. Ecological changes in Chesapeake Bay: Are they the result of overharvesting
the American oyster, Crassostrea virginica? Pp. 536-546 in M. P. Lynch and E. C. Krom, eds.,
Understanding the Estuary: Advances in Chesapeake Bay Research. Proceedings of a Confer-
ence. Chesapeake Research Chesapeake Research Consortium Publication CRC129, Baltimore,
Md.
Nobre, C. A., P. J. Sellers, and J. Shukla. 1991. Amazonian deforestation and regional climate change.
J. Climate 4:957-988.
Steadman, D. W., and S. L. Olson. 1985. Bird remains from an archaeological site on Henderson
Island, South Pacfic: Man-caused extinctions on an “uninhabited” island. Proc. Natl. Acad.
Sci. 82:6191-6195.
Wagner, W. L., D. R. Herbst, and S. H. Sohmer. 1990. Manual of the Flowering Plants of Hawaii.
University of Hawaii Press and Bishop Museum Press, Honolulu.
Willis, E. O. 1974. Populations and local extinctions of birds on Barro Colorado Island, Panama.
Ecol. Monogr. 44:153-219.
Wilson, E. O. 1985. The biological diversity crisis: A challenge to science. Issues Sci. Technol.
2(1):20-29.

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CHAPTER
3

Biodiversity: Why Is It Important?

RUTH PATRICK
Francis Boyer Chair of Limnology,
Academy of Natural Sciences of Philadelphia, Pennsylvania

The term biodiversity—the presence of a large number of species of animals

and plants—is now generally recognized as being important by many people.
To most people the existence of many species is important because their physi-
ological differences furnish various sources of food, clothing, shelter, and medi-
cine for man. Species also differ in their physical and chemical characteristics,
which is particularly true of plants. For example we have cotton, flax, and rat-
tan, which are all products of various species of plants and are used for different
types of clothing. Likewise, the structure of plants, be they trees or palm fronds
or bamboo poles, serve as a source of shelter for much of the human race. There-
fore, from the human standpoint, the presence of a great number of species with
different structures, different chemical compositions, and different lifespans
form one of the most important bases of life for humans throughout our planet.
Although these aspects are very important to society, there are far more
important aspects of biodiversity that many people do not realize. For example,
it is the presence of different kinds of plants that make up the food of grazing
animals, for example, grass, herbs, and fruits. It is this great diversity of plant
life, with its varying food values, that enables the existence of many different
kinds of animals.
Plants also, by their great diversity, form shelter and habitats for many
different species. McArthur (1965) was the first to point out that trees, such as
the conifers on Mount Desert Island, Maine, have many different habitats and
that different species of birds occupy each of these habitats.
The diversity of plants is important for all animals, herbivores and omni-
vores included. The different nutritional values of fruits and seeds enables a

15

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16 / BIODIVERSITY II

species to get the variety of the chemicals that are necessary for its diet and
hence to graze without exhausting the population of a given species. It has been
noted by Janzen (1978) and others that certain species will feed on a given plant
that is unpalatable to other species. This difference is due to secondary chemi-
cals. The so-called primary chemicals are those that are necessary for the pro-
duction of energy and nutrients for growth and reproduction of a species. The
secondary chemicals are those that act as defense mechanisms or, in some cases,
as attractants for reproduction. These chemicals vary greatly from species to
species, as does the tolerance of the predators.
Often there is a specific species of insect that feeds on a given species of
plant which contains certain secondary chemicals. In such cases, these second-
ary chemicals are not toxic at low concentrations to the predator. The predator
ceases to prey when the toxic threshold for that species is reached. This condi-
tion allows the reduced population of the prey species to exist and reproduce.
Many of these chemicals are known as allelochemics, allomones, and kairomones
(Janzen, 1978).
Seeds that are high in nutrient value may have three or more classes of
defensive compounds, such as one or more protease inhibitors or lecithins, alka-
loids, or uncommon amino acids, glycosides, polyphenols, etc. As each group of
compounds is known to be very diverse, it is unlikely that there would be many
seeds with the same defenses by chance alone. These secondary compounds of-
ten are found in vacuoles or other structures so that they do not interfere with
the ordinary metabolism of the plant.
Other secondary chemicals may be volatile and act as stimulators for polli-
nation. For example, with the genus Ophyrys of orchids, several volatile chemi-
cals that attract pollinators have been identified. The compounds so far have
been grouped into three classes: terpenoids, fatty acid derivatives, and others.
The terpenoids comprise mono-, sesqui-, and diterpenes (mainly hydrocarbons
and derived alcohols). Most are mono- or bicyclic. The second group are fatty
acid derivatives that are acyclic hydrocarbons, alcohols, keto compounds, and
esters of short- and medium-chain length. The third group includes partly iden-
tified constituents that are either aromatic or contain nitrogen. It is these volatile
chemicals that attract the pollinators (Bergström, 1978).
It is quite evident that the diversity of the biochemical composition of vari-
ous types of plants has a great part to play in their survival and in keeping the
predators from completely eliminating them.
Thus, we see that there is a great deal of chemical biodiversity in the natural
world. Some species produce toxins to limit the predation of predators, whereas
other species detoxify or destroy the toxicant so that the species can live in a
given area. It is this great chemical diversity of the living world—in the pro-
duction of toxicants that control predation, pheromones that stimulate repro-
duction, and the ability of some species to destroy chemicals that are toxic to

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BIODIVERSITY: WHY IS IT IMPORTANT? / 17

other species—that restores the availability of the habitat for the functioning of
the diverse natural fauna and flora.
Earth’s climate is continually changing, and it is the diversity of species
that allows the environment to be utilized throughout most of the year in tem-
perate climates and continually in the tropics. Thus, energy and nutrients are
transferred throughout the food web. The processes of decay and regeneration
of chemicals that are a source of food for the organisms are active all year and are
basic to the operation of terrestrial as well as aquatic ecosystems. Although
most of the macroscopic species in temperate and cold areas seem to have very
low metabolic rates during the cooler months, other small organisms and micro-
organisms that live in the soil may be very active. For example, there are certain
bacteria that release nitrogen as N2 to the atmosphere and thus prevent harmful
concentrations of nitrates and ammonia from accumulating in the soil. In con-
trast, there are other bacteria and plants that are able to fix molecular nitrogen,
or nitrogen in reduced forms, and convert it into a form that can be utilized
easily by legumes. This ability to fix nitrogen and thus provide nutrients in the
soil make the legumes and their associated bacteria one of the most valuable
crops for soil enrichment. These bacteria would become too numerous if it were
not for the protozoans, nematodes, small worms, and other micro- and macro-
scopic organisms in the soil that feed on them and control their populations.
From these examples, it is easy to understand that terrestrial ecosystems are
dependent on a high diversity of macro- and microscopic organisms if the func-
tioning of the ecosystem is to be efficient, so that the least amount of entropy
accumulates in the system. Realizing the important function that these microor-
ganisms play, considerable research is now being done, particularly with bacte-
ria, to see if the genes involved in bacteria that fix nitrogen can be transferred to
other crops so that agriculture would be less dependent on chemical fertilizers.
In the aquatic world, biodiversity is very important in maintaining the pu-
rity of the water for multiple uses by organisms as well as by man. The impor-
tance of biodiversity in streams and rivers was recognized first by my studies in
the Conestoga River Basin in 1948 and the resulting paper (Patrick, 1949), in
which I indicated that a large number of species with relatively small popula-
tions characterize natural streams that are unaffected by pollution. Furthermore,
these species represented many different groups of organisms belonging to a
great many different phyla. The importance of this diversity in the functioning
of the ecosystem was emphasized by this and later studies.
These studies clearly indicated that not only were the numbers of species
characteristic of natural ecosystems fairly similar in streams that were chemi-
cally and physically quite different, but the percentage of the total number of
species in each stream that performed each of various functions—primary pro-
ducers, detritivores, detritivore-herbivores, omnivores, and carnivores—were
quite similar (Tables 3-1, 3-2a, 3-2b, and 3-2c). High diversity ensures the con-

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TABLE 3-1 Numbers of Species

Guadalupe Potomac Savannah

Low Flow 1973 Low Flow 1968 Low Flow 1968
No. % No. % No. %

Algae 53 29.1 87 38.3 44 25.3

Protozoa 66 36.3 49 21.6 40 23.1
Macro-invertebrates 17 9.3 18 8.0 21 12.1
Insects 29 16.0 41 18.1 41 24.0
Fish 17 9.3 32 14.0 27 15.5
Total 182 227 173

tinuation of the functioning of the ecosystem, which typically consists of four

stages of nutrient and energy transfer (Figure 3-1).
The bases of the food web are typically detritivores and primary produc-
ers—organisms that can fix the sunlight and CO 2 into carbohydrates. The detri-
tus is made available by the action of a great many species (bacteria, fungi,
protozoans, and insects). Typically the bacteria and fungi break down the more
complex compounds present in the detritus into simpler forms which then are
utilized by other organisms. The main function of the protozoans and inverte-
brates is to feed on the bacteria and the fungi and keep their populations in
check so that overpopulation does not occur. It is well known that bacteria may
produce autotoxins and thus greatly reduce the efficiency of their own popula-
tions if they become too numerous.
The main function of the insects, mainly stoneflies and cranefly larvae, is to
break down detritus into various sized particles, so that it is more easily handled
by other organisms in the ecosystem. The interaction of these organisms in the
ecosystem is very important because it ensures that species do not overpopulate.
For example, the bacterial population will become too large if protozoans are not
present. Such overpopulation causes the system to function inefficiently and
entropy increases. Of course, the physical condition of the water—its rate of
flow and chemical constituents—affect these processes.
We do not understand all of the physical characteristics of the environment
that are important in maintaining the species diversity of these ecosystems. As
pointed out by Patrick and Hendrickson (1993), even though we tried to have
diatom communities develop in conditions that were as similar as possible, there
was a certain amount of variability that was unaccounted.
As in the terrestrial system, in riverine systems the transfer of energy and
nutrients through the ecosystem and the destruction of wastes continues
throughout the year at all seasons. An example is White Clay Creek in Delaware
County, Pennsylvania, which has been studied extensively by scientists at the
Stroud Water Research Laboratory, including myself.

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 TABLE 3-2a Guadelupe River—Food Types of Major Groups of Species
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Guadalupe River—1973
Macro- Total % of
Total Number of Species: 179 Algae Protozoa invertebrates Insects Fishes Feeding Type Distribution

Autotrophs 53 15 68 38.0
Auto- and Heterotroph
(Microphagocytes)
Detritus (Microphagocytes) 19 3 22 12.3
Detritus and Algae 32 4 7 43 24.0
Algae (Herbivore) 3 1 4 2.2
Detritus, algae, zooplankton,
Biodiversity II: Understanding and Protecting Our Biological Resources

macroinvertebrates, fish
(Omnivore) 7 4 8 19 10.6
Zooplankton, macroinvertebrates,
fish (Carnivore) 3 12 8 23 12.9
Total Species in each Category 53 66 17 26 17 179 100.0

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BIODIVERSITY: WHY IS IT IMPORTANT? / 19
 TABLE 3-2b Potomac River—Food Types of Major Groups of Species
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Potomac River —1968

20 / BIODIVERSITY II

Macro- Total % of
Total Number of Species: 227 Algae Protozoa invertebrates Insects Fishes Feeding Type Distribution

Autotrophs 86 14 100 44.3

Auto- and Heterotroph
(Microphagocytes)
Detritus (Microphagocytes) 20 4 24 10.6
Detritus and Algae 15 9 3 3 30 13.3
Algae (Herbivore) 5 2 7 3.1
Detritus, algae, zooplankton,
Biodiversity II: Understanding and Protecting Our Biological Resources

macroinvertebrates, fish
(Omnivore) 4 20 12 36 15.9
Zooplankton, macroinvertebrates,
fish (Carnivore) 1 13 15 29 12.8
Total Species in each Category 86 49 18 41 32 226 100.1

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 TABLE 3-2c Savannah River—Food Types of Major Groups of Species
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Savannah River —1968

Macro- Total % of
Total Number of Species: 173 Algae Protozoa invertebrates Insects Fishes Feeding Type Distribution

Autotrophs 44 12 56 32.4
Auto- and Heterotroph
(Microphagocytes) 1 1 0.6
Detritus (Microphagocytes) 12 3 15 8.7
Detritus and Algae 14 7 3 24 13.9
Algae (Herbivore) 10 1 11 6.3
Detritus, algae, zooplankton,
Biodiversity II: Understanding and Protecting Our Biological Resources

macroinvertebrates, fish
(Omnivore) 1 7 16 8 32 18.5
Zooplankton, macroinvertebrates,
fish (Carnivore) 4 12 18 34 19.6
Total Species in each Category 44 40 21 41 27 173 100.1

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BIODIVERSITY: WHY IS IT IMPORTANT? / 21
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22 / BIODIVERSITY II

FIGURE 3-1 Pathways of nutrient and energy transfer (from Patrick, 1984).

Contrary to what many people have thought in the past, this stream is ener-
getically active all year long. For example, Sweeney and Vannote (1981) found
that there were roughly 50 species of mayflies living in the stream throughout
the year. However, since they undergo developmental stages at different times
of the year, some species of mayflies were rapidly growing, entering diapause,
and emerging at different times throughout the year.
Figure 3-2 shows examples of the growth pattern of six mayflies. From this
figure, it is evident that Ephemerella subveria had it’s most active period of
growth from August through March, whereas E. dorothea had its most rapid
growth from March through May. We find that E. funeralis had a fairly rapid
period of growth in November and December and then again in April, whereas
E. verisimilis was growing rapidly from April through May. Ephemerella
deficiens had a fairly active period of growth in October and again in April and
May and part of June, and E. serrata grew most actively in May, June, and July.
Thus, throughout the year, one or another of the mayflies were grazing actively
and converting food into energy and nutrients. Some of the nutrients, of course,
were passed on to predators such as fish. The food of these mayflies is mainly
detritus and algae.
Diatoms have a similar pattern of life history. There are a great many species
of diatoms in White Clay Creek. Some of these species, such as Cocconeis pla-
centula and Surirella ovala, reach their greatest densities during the spring; some
form the largest populations during the summer and early fall months, such as
Melosira variens; and others show the greatest population growth in the short
day lengths of late fall and early winter, such as Nitzschia linearis and Gom-
phonema olivaceum.
Thus, we see that diatoms, which are the dominant source of food for these
mayflies, change throughout the year, just as do the mayflies. It is these vari-

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BIODIVERSITY: WHY IS IT IMPORTANT? / 23

abilities in population size that assure that the energy and nutrient transfer in
the system will continue all year, and it is accomplished by different species.
During each season of the year, there is a relatively high diversity of species
present. This illustrates the importance of biodiversity in assuring a continued
cycling of nutrients and energy.

FIGURE 3-2 Average larval growth of six species of Ephemerella mayflies in White
Clay Creek (from Sweeney and Vannote, 1981).

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24 / BIODIVERSITY II

Furthermore, there seem to be similar patterns of species diversity in streams

that are naturally very different. For this study, we selected rivers that, from a
chemical and physical standpoint, had very different characteristics of the wa-
ter. They were also in different geographic areas. The rivers were (1) the Guad-
alupe River in Texas (which is classed as a hard-water river because the calcium
carbonate hardness is between 150-200 parts per million [ppm]); (2) the Potomac
River, located between Maryland and Virginia (classified as a medium-hard river,
with calcium carbonate at 60 to about 110 ppm); and (3) the Savannah River,
located in the southeastern part of the United States (classified as a soft-water
river, with a calcium hardness of less than 60 ppm).
It is interesting to note that the percentage of species for each of the major
groups of organisms of the total number of species composing the fauna and
flora are quite similar in these very different rivers (Tables 3-2a,b,c). Further-
more, the various groups of organisms that compose the major steps in the trans-
fer of energy and nutrients through the system are similar (Tables 3-3a,b,c).
Thus, the total number of species may vary in each of these respective rivers,
but the percentage of the total number that is operative at a given functional
level is similar. The kinds of species, as one would expect, vary greatly because
of the many chemical and physical characteristics of the systems. From these
aquatic studies, it is evident that there is not only a large number of species
carrying out the functions of nutrient and energy transfer throughout the year,
but a definite pattern is present.
In conclusion, it is evident that the many species composing the ecosystems
of our planet have developed many unique chemical, physical, and structural
characteristics and that they utilize many diverse strategies that ensure the func-
tioning of the ecosystems of our planet.

REFERENCES
Bergström, G. 1978. Role of volatile chemicals in Ophrys-pollinator interactions. Pp 207-231 in J. B.
Harborne, ed., Biochemical Aspects of Plant and Animal Coevolution. Academic Press, N.Y.
Janzen, D. H. 1978. The ecology and evolutionary biology of seed chemistry as related to seed
predation. Pp. 163-206 in J. B. Harborne, ed., Biochemical Aspects of Plant and Animal Coevo-
lution. Academic Press, N.Y.
McArthur, R. 1965. Patterns of species diversity. Biol. Rev. 40: 510-533.
Patrick, R. 1949. A proposed biological measure of stream conditions based on a survey of Conestoga
Basin, Lancaster County, Pennsylvania. Proc. Acad. Nat. Sci. Phil. 101:277-341.
Patrick, R., and J. Hendrickson. 1993. Factors to consider in interpreting diatom change. Nova
Hedwiggia 106:361-377.
Sweeney, B. W., and R. L. Vannote. 1981. Ephemerella mayflies of White Clay Creek: Bioenergetic
and ecological relationships among coexisting species. Ecology 62(5):1353-1369.

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CHAPTER
4

Biodiversity at Its Utmost:

Tropical Forest Beetles

TERRY L. ERWIN
Curator, Department of Entomology, National Museum of Natural History,
Smithsonian Institution, Washington, D.C.

Life on Earth takes many forms and comes in all sizes, from microscopic
one-celled plants to blue whales and human beings. Together these organisms
and their interactions constitute our planet’s biodiversity. Among this profu-
sion of life are the beetles and their insect and arachnomorph relatives, which,
taken together, constitute most of Earth’s biodiversity (Erwin, 1982; Hammond,
1992; Robinson, 1986; Wilson, 1992). There are 1.4 million species of insects
described in the scientific literature (Hammond, 1992), which is about 80% of
all life currently recorded on Earth. Taxonomists, those who name and classify
species, have been describing species of insects at about 4,400 per year for more
than 235 years, and in the last 25 years, have described about 8,680 per year
(± 363). This written record is at best perhaps only 3.4% of the species actually
living on the planet (Erwin, 1983a). Recent estimates of insect species, mostly in
tropical forests, indicate that the descriptive process is woefully behind. These
estimates indicate there may be as many as 30–50 million species of insects
(Erwin, 1982, 1983b), making this pervasive terrestrial arthropod group 97% of
global biodiversity. The familiar ants and grasshoppers, bees and beetles, house-
flies and cockroaches, and spiders are but the tip of the iceberg of arthropod
diversity; most species are small to very small tropical forest-dwelling forms
that no one has seen or described on any adequate scale.
Insects and their relatives (spiders, ticks, centipedes, etc.) are the most domi-
nant and important group of terrestrial organisms, besides humans, that affect
life on Earth, often with an impact on human life. They affect human life in a
multitude of ways—both for good and bad. Profound ignorance about insect
life permeates most of human society, even among the highly educated. Insects

27

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28 / BIODIVERSITY II

and their relatives, in fact, are little credited

for their beneficial environmental services and
overblamed for their destructive activities.
Despite lack of general human interest in in-
sects, E. O. Wilson (1987:1) wrote that they
are “the little things that run the world.”
Insects and their relatives live on all conti-
nents and occupy microhabitats from deep in
the soil and underground aquifers to the tops
of trees and mountains, among the feathers of
penguins on Antarctica, and even deep into
caves and in our eyebrows. Many lineages
have evolved adaptations for living on and
under ice fields, others at the margins of hot
springs, and still others on the open ocean.
Land arthropods, by virtue of their pervasive-
Weevils are a very diverse group ness, are incredibly important to the balance
of rainforest beetles. of life within ecosystems, e.g., pollination,
nutrient recycling, and population control
through vectoring diseases. Insects and their relatives eat virtually everything
and compete even for the rocks under which they hide, mate, and rear their
young. What would happen if all insects were removed from a habitat or natu-
ral community overnight? For one thing, most broadleaf trees and shrubs
would not be pollinated, and there would be no fruits and seeds. For another,
instead of penetrating dead matter, decomposers such as bacteria and fungi
would live only on the surface, taking years or perhaps millennia to break the
substrate down into recyclable nutrients for plants, and thus soils would be
much less fertile. Many fish and birds, and even some mammals, would have no
food and would cease to exist. In fact, insects seem to be one of nature’s most
important cornerstones on which most other types of life depend in one way or
another.
Among the insects, the beetles are the most speciose, the most pervasive,
and the most widespread across the face of the globe. During dry seasons in
tropical forests, they are also the third most numerous individuals, after ants
and termites, making up a full 12% of the total insect community (Erwin, 1989).
Beetles are found everywhere on our planet except in the deep sea. How-
ever, they do occur commonly in the sea’s intertidal zone and estuarine salt flats
(Erwin and Kavanaugh, 1980; Kavanaugh and Erwin, 1992; Lindroth, 1980).
Beetles even occurred on Antarctica not long ago (Ashworth, personal commu-
nication, 1994). Most families of beetles, about 140 of them, are world-wide in
distribution, and their species provide equivalent ecological services wherever
they occur. The “play” is generally the same everywhere, only the “actors”
themselves change from place to place.

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BIODIVERSITY AT ITS UTMOST: TROPICAL FOREST BEETLES / 29

We know of beetles from the Permian Period to the present (Arnol’di et al.,
1992), a recorded history of some 250 million years. This history shows that two
major faunal changes took place, the first in the mid-Jurassic Period when primi-
tive lineages of beetles lost their dominance, and the second in the mid–Creta-
ceous Period, at which time modern forms acquired dominance over all other
terrestrial arthropods. In terms of species and number of guilds (groups of spe-
cies that fill similar ecological roles), they still have this dominance in nearly
every biotope. By any broad measure, beetles are the most successful lineage of
complex organisms ever to have evolved.
The described species of beetles, about 400,000+ (Hammond, 1992), com-
prise about 25% of all described species on Earth. This dominance of beetle taxa
(any systematic category, such as species, genus, family, etc.) in the literature
has resulted in Coleoptera being perceived as Earth’s most speciose taxon. Thus,
it has garnered further taxonomic attention from young taxonomists which in
turn has resulted in more species of beetles being described than in other groups.
Beetles are relatively easy to collect, prepare, and describe, significantly adding
to their popularity. Such unevenness in taxonomic effort may or may not give
us a false picture of true relative insect diversities. Nevertheless, the dominance
of beetles has been used to arrive at an estimate of 30 million insects overall
(Erwin, 1982), and even to designate the group most endeared to God (Gould,
1993). While this dominance may be arguable either scientifically or philosophi-
cally, it is certainly interesting. However, it does not address the real power
that a knowledge of this extraordinary taxon might allow in evolutionary biol-
ogy and conservation. What is neglected in the science of “coleopterology” is
nearly everything except collecting, taxonomy, systematics, and a little auto-
ecology. Given that nearly everyone from naturalists, including Darwin and
Bates to Edgar Allen Poe has or had “an inordinate fondness” (see Gould, 1993)
for beetles, it seems strange that more attention is not given to them for use in
interpreting environmental perturbations (Ashworth et al., 1991; Ashworth and
Hoganson, 1993; Halffter and Favila, 1993), in understanding the rules (or
nonrules) of assembly in tropical communities and biotopes (Erwin, 1985), and
in environmental monitoring (Kremen, 1992; Kremen et al., 1993).
The reasons probably lie in the overwhelming numbers of species, indi-
viduals, and the ever-plodding course of traditional taxonomy. Potential users
of data on beetles simply have to wait too long to get names; taxonomists have to
wait too long to receive money to visit museums in which name-bearing type
specimens are held; monographers take too long to produce documents with
which users might identify their specimens by themselves; and specialists are
reluctant to take on a large identification load for other scientists, such as ecolo-
gists and conservation biologists.
Given that millions of data points can be gathered in a very short time by
sampling beetles (Table 4–1), far more than in any other group of diverse organ-
isms (Adis et al., 1984; Allison et al., 1993; Basset, 1990, 1991; Erwin, 1982,

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TABLE 4-1 Species level studies of tropical/subtropical canopy/subcanopy beetles using insecticidal fogging
30 / BIODIVERSITY II

techniques

Est. vol. of No. of No. of Specimen/

foliage (m3) species specimens Familes Density Species/m3/m species ratio % Singletons

Allison/Miller (New Guinea) 2150 633 4840 54 2.25 0.29 7.65 50.7
Basset (Australia) a 4040 68 863 48 4.68 0.02 12.69 est. 19
Erwin (Panama) 1065 1250 8500 60 7.99 1.17 6.8 ?
Erwin (Peru)b 2283 3429 15869 83 6.95 1.5 4.63 50.4
Stork (Brunei) 2690 859 4000 61 0.42 0.32 4.66 ?
Biodiversity II: Understanding and Protecting Our Biological Resources

Stork (Sulawesi) 56550 1176 9158 ? 0.16 0.02 7.79 ?

aRestricted canopy fogging method.

bIncludes six specific microhabitats, while others are predominately canopy rims with perhaps epiphytic growth.

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BIODIVERSITY AT ITS UTMOST: TROPICAL FOREST BEETLES / 31

1983a,b, 1988, 1989, 1991; Erwin and Scott, 1981; Farrell and Erwin, 1988;
Kitching et al., 1993; Stork, 1991), how might we digest those data, turn them
around to discern patterns that, once recognized and interpreted, can give us
powers of prediction about the environment. With such an understanding, we
could discern rich sites from slightly less rich sites for conservation (Rapid As-
sessment Program Team approach), or monitor life (environmental health) at
those sites at a much finer resolution than is possible with vertebrates; and we
could test much ecological theory also on a fine scale.
Neotropical beetles are second only to ants and flies (the latter in the wet
season only) in numbers of free-ranging individuals of arthropods in the cano-
pies and subcanopies of neotropical trees (termites are not usually free-ranging);
Psocoptera are a distant third (Erwin, 1989). However, per species, beetles are
not abundant (Figure 4–1). Beetles participate in virtually all aspects of ecosys-
tem processes; they are predators, herbivores, folivores, detritivores, scaven-
gers, fungivores, wood-eaters, and grazers, and they tunnel, mine, and chew
nearly every substrate. Some are ectoparasites, others are nest parasites, some
even live in the fur of vertebrates. Still others are subsocial, with adults partici-
pating in the raising of young. Knowledge of beetles, because they are the
hyperdiverse group on the planet, offers direct insights into total biodiversity
and the evolution of that biodiversity, as well as how this diversity is distrib-
uted in time and space across microenvironments, habitats, biomes, and seasons.
A global perspective based on beetles could provide a much more fine-grained
view of biodiversity than the coarse-grained one we get from less speciose groups
such as jaguars, birds, and monkeys, which heretofore have garnered most of
the attention.
The publication resulting from the National Forum on BioDiversity (Wilson

Erwin (Manaus)

Basset (Australia)

Stork (Sulawesi)

Allison/Miller (New Guinea)

Erwin (Panama)

Stork (Brunei)

Erwin (Peru)

0.00 5.00 10.00 15.00 20.00 25.00

Specimens/Species

FIGURE 4–1 Relative abundance of species (large beetle-sampling programs).

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32 / BIODIVERSITY II

and Peter, 1988), held in Washington, D.C. in 1986, included only 7 out of 521
pages devoted to insects (and only one speaker at the forum). At the most recent
Biodiversity Forum (the Inaugural Symposium of the Consortium of Systematics
and Biodiversity which formed the basis for this volume), there were six speak-
ers on insects and three others whose contributions were at least partially based
on insects (23%), a substantial realization in a mere 8 years within the biological
community that biodiversity and the environment are insect dominated! If we
are to understand the environment, which we must do if we are to successfully
manage it, then we must have a better picture of the processes that brought
about and maintained insect dominance since the Mesozoic Era.
Whether or not there are 30 million species (and, of that, 7.5 million species
of beetles) or only a little more than the 1.4 million species that are already
described, current human activity and that of the immediate future will exter-
minate a large percentage of these species (Erwin, 1988; Wilson, 1988). Atten-
tion must focus on the underlying evolutionary processes that have resulted in
such diversity and evaluate these in terms of present human activities.

COLLECTION OF DATA
Because the interface between insects and their environment is at a small
resolution, information they provide may well be critical for ecological restora-
tion. Management will depend on what we really know rather than what we
surmise. Conservation cannot now deal with insect information, but will be com-
pelled to do so in the not-too-distant future. We will need a system for data
gathering that is just now becoming available.
In Chapter 27 of this volume, Daniel Janzen describes his concept of an All
Taxa Biodiversity Inventory (ATBI) for a 110,000 hectare site in Costa Rica. Such
an undertaking, even in such a small area, will require methods other than those
now employed for inventory, because the beetles alone are so pervasive and
speciose anywhere in the tropics (along with all the other insects and their rela-
tives) that completing an inventory would require generations of investigators.
One goal of Janzen’s ATBI is to inventory all the taxa within a given area. A
biotic inventory includes finding the area’s species, classifying them, making
voucher collections, and storing these data in a way that they are easily retriev-
able. Additional information about the species, either gathered during the pro-
cess of inventorying or added later from literature or follow-up studies, can be
piled on top of the four basic elements in a growing database.
The first ATBI area is destined to be at the Guanacaste Conservation Area
(GCA), Costa Rica, a site with dry forest in lower elevations ascending through
cloud forest and containing intermediaries between these levels. Based on my
experience in (and data from) nearby Panama with a similar range of habitats, I
estimate that GCA should have about 50,000 species of beetles. Since this esti-
mate can be only a first approximation (but certainly within an order of magni-

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BIODIVERSITY AT ITS UTMOST: TROPICAL FOREST BEETLES / 33

tude), it is used for purposes of designing a sampling regime for the project;
budget and time must be considered to be modifiable as the project narrows to
better estimates.
Given GCA’s latitude and altitudinal gradient, there are a minimum of 24
distinctive communities (forested and open habitats), each forest with a set of 15
or so microhabitats and each open area with 5 or so microhabitats (Erwin, 1991),
all of which may contain different beetle faunules with perhaps as little as 20%
species overlap, as was observed in my studies of 6 forest microhabitats at
Pakitza, Peru. Each species of tree, shrub, and herb/grass may have its own
host-specific species of beetles. Riparian strands in various watersheds will have
different types of substrates, water quality, vegetation, etc., contributing to
their distinctive biodiversities. In addition, the GCA is distinctly seasonal, hence
both dry and wet seasons need to be sampled for each microhabitat (Erwin and
Scott, 1981).
The sampling regime must consider the above in its attempt to record as
many species as possible in the shortest amount of time. The guiding principles
are as follows:
• Phase 1: mass cooccurrence sampling; rapid processing with bulk cold
storage (dry and wet specimens, depending on Order); identification process
using matching specimens; interim naming with alphanumerics; accumulation
of data using linked spreadsheets, including curves showing sampling progress;
and character filing with the Quick Taxonomic Assessment System (QTES).
• Phase 2: send target taxa and QTES data into the taxasphere (formal sys-
tematic literature) for formal species names;
• Phase 3: replace EXCEL 4.0 spreadsheet and QTES interim names with
formal ones, transfer these data to the database at Instituto Nacional de Bio-
diversidad (INbio).
• Phase 4: generate illustrations and three-dimensional laser images; pro-
duce documents (lists, brochures, field guides, revisions, monographs, other
analyses).

AN AGENDA FOR SAMPLING BEETLES IN AN ATBI

Sampling
The following criteria must be met for acquiring samples of beetles that can
provide a reasonable inventory and serve both immediate and future needs of
research, as well as determine to an order of magnitude the species present in
the target area for use in subsequent sampling projects:
(1) Sampling assumes the use of a fogger and 3% Resmethrin (biodegrad-
able with an LD501 better than aspirin, gone in 2 hours) for all microhabitats
1 Dosage at which 50% of the organisms fail to survive.

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34 / BIODIVERSITY II

16
Erwin/Peru
14

12
Number of species

10
Erwin/Panama
8

4 Erwin/Manaus Stork/Brunei
Alison-Miller/New Guinea
2 Stork/Sulawesi

0
1 2 3 4 5 6 7 8 9 10
Cubic meters of foliage Bassett/Australia

FIGURE 4–2 Accumulation of species (per m3 of foliage).

from 1 m above ground through the canopy rim (Erwin, 1982, 1983b, 1989,
1991); this should capture 1.7 species per m3 of foliage (see Figure 4–2) and much
more in compacted microhabitats such as suspended dry leaves, vine tangles,
and complex canopies. Leaf litter and soil layers are sampled by photoeclectors
(Adis, 1984; Adis and Schubart, 1984) and sifting/Tolgren extractor techniques.
Berlese banks can substitute for Tolgren, if electricity is available. The stratum
of herbs and grasses is sweep-sampled by sweep-netting.
Methods of trapping by attraction and even passive traps that catch flying
insects produce catch without biocontext, i.e., specimens that are not tied to any
microhabitat, substrate, host plant, etc. Much time and effort goes into prepar-
ing, identifying, and storing such bulk lots, yet the quality of data is at the
lowest level. These methods of collecting simply are not worth the effort, unless
one is interested solely in recording presence of species in the general area or in
building collections. However, these techniques can be used as a test of the
methods that incorporate biocontext to determine if microhabitats exist that not
being sampled with the other techniques.
(2) A standard set of field data includes precise locality (latitude/longitude
to seconds, and notes on permanent trail markers and topographic features if
available; a Global Positioning System [GPS] device provides data on position
and elevation); type of forest; type of microhabitat and its volume or surface
area; information on species of plants (or other host); date; and collector(s). Lot
numbers are assigned to each individual fogging collection, sifting series, photo-
eclector sample, sweep series, etc. Thus, all specimens taken from the same

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BIODIVERSITY AT ITS UTMOST: TROPICAL FOREST BEETLES / 35

microhabitat or plant or trap at the same time get the same lot number so that the
set of species, including nonbeetles, can be reassembled at a later date if desired
(this faunule reassembly may be only a computer construct). Nonbeetle speci-
mens will be directed to another Taxonomic Working Group (TWIG), along with
appropriate sets of data.
(3) Specimens of beetles are preserved in 70% alcohol in the field. Alcohol
must be changed the same day at the lab and subsequently each time the speci-
mens undergo processing (see below). If specialists for nonbeetle groups are
available at the time of fogging, dry specimens may be extracted by hand before
the general sample goes into alcohol, so long as this does not delay the routine of
the inventory for beetles and appropriate lot numbers are defined. Egg carton
inserts are placed in funnels or on suspended sheets to catch specimens dry.
After these are selected from the carton surface, the remaining specimens are
dumped into the alcohol bottle.
(4) Sampling design involves taking replicate microhabitat samples in sets
of 10 throughout each type of forest and open area. During preparation and
data entry of the 10 samples, species accumulation curves and Chao’s estimator
(Colwell and Coddington, 1994) track the progress of the inventory. A complete
inventory for smaller families will require fewer replicates, but the leaf–beetles
and weevils will require many more than 10 replicates, based on data from over
5,000 species acquired at Pakitza, Peru, from 1988-1992. A decision needs to
made at the outset as to when to stop, because it will not be “humanly” possible,
given today’s resources, to get the “last” species on the list in the larger families.
However, 100% likely will be reached in smaller families.

Preparation
All tropical forest samples are replete with beetles. The object of prepara-
tion should be to make the species and their whereabouts and abundance known
in the shortest amount of time possible. Traditional preparation of all collected
specimens, therefore, is not feasible. The following method leads to one pre-
pared specimen per species per sample, with cold storage of the bulk lots (other
specimens of the species) that easily can be accessed later by taxonomists and
other workers who need series.
(1) Each sample lot is sorted to families using a 6.2 cm white ceramic dish
with 70% alcohol. Families are gathered in small plastic lids set inside the bot-
tom of a petri dish, the top of which is ringed with vaseline to create a seal when
the specimens are sitting unworked. Parataxonomists and beginning graduate
students can be trained to sort at this level quickly.
(2) Each family then is sorted in sequence to species, with one good speci-
men selected for pinning/pointing. The specimen is placed on damp filter paper
inside another petri dish. On the filter paper, numbers 1 to 20 are written and
the chosen specimen is placed next to a number according to its abundance in

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36 / BIODIVERSITY II

A collection of rainforest insects.

the sample. If over 20 specimens of a species are in a sample (which is rare), a

small label is written with the number, and this label is affixed to the pin to be
removed later in the process (see below). The rest of the counted but unprepared
specimens are returned to the lot vial of 70% alcohol, bar-coded, and sent to
cold storage. Sorting to species across the Coleoptera can be done only by a
highly trained taxonomist with long experience, and this person becomes the
key to the entire project. Preparation and storage procedures can be handled by
a technically trained person.
(3) Each specimen from the filter paper is pinned or pointed with Elmer’s
glue to pins or preprepared points in the traditional manner and placed in a unit
tray with strips of numbers sequenced from 1 to 20. Each specimen is aligned
next to one of these numbers according to its abundance in the sample.
(4) Preprinted labels are attached to each specimen as it is “identified-by-
matching” using the synoptic collection. The name of the species is an alphanu-
meric in the form of “family coden + number” and lot number. All families of
Coleoptera have a standard coden of four letters. The margin of the label is
color-coded with pencil for instant recognition of microhabitat, although the lot
number references this too. Once a family is represented by more than 100 spe-
cies, “identifying–by-matching” becomes less and less efficient. For very large
families, such as weevils, staphylinids, and chrysomelids, use of QTES is recom-
mended.

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BIODIVERSITY AT ITS UTMOST: TROPICAL FOREST BEETLES / 37

Interim Identification
Each prepared specimen from a sample is compared with its corresponding
family-level synoptic collection. Smaller families are easy to keep in one or a few
units. Larger families may be subdivided by subfamily so that the amount of
matching necessary for recognizing the specimen’s status is kept to a minimum.
As a specimen is identified or recognized as a species new to the synoptic collec-
tion, it is placed either in an interim unit tray awaiting entry of the data before
going to the duplicate collection (those identified previously) or added to the
synoptic collection (those determined as new), from where its data are entered.
All species of a family that are sorted from the sample are labeled, then the data
are entered in EXCEL before preparing the next family.

Data Storage
My EXCEL linked spreadsheet templates for families of beetles contain about
13 Kilobytes of forms that are based on microhabitats. Entry of data from a
sample involves simply number of specimens per species per lot. The program
automatically computes all basic information and accumulates the data on sum-
mary sheets for easy viewing. The program is exceedingly user-friendly.

Building Collections
The resulting synoptic-unit trays of families of beetles are ready for special-
ists at any time during the process if the specialist is on-site to make formal
identifications. The duplicate collection—built from second through n occur-
rences of a species across samples (hence, it will not contain “uniques” [species
known from single specimens] found only in the synoptic trays)—can be sent
through the taxasphere regularly and results can be fed back into the EXCEL
data system, making it easy to move the information to the INBio standard data
files. As additional microhabitat replicates are sampled and specimens processed,
those species represented by uniques in the synoptic collection will be dupli-
cated and then can be sent through the taxasphere.
Serious taxonomists who must do a revisionary study immediately can read
the database to find lots with series and arrange to extract those from cold stor-
age themselves. Common species that are found in many or most lots will have
that many more prepared specimens ready for study in the duplicate collection.

SUMMARY
The rate at which all the foregoing can be done is 58 specimens and 13
species per hour. Therefore, using the rate of accumulation for additional spe-
cies found in Panama forest foliage, 1.7 per m3 of microhabitat, we should be

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38 / BIODIVERSITY II

able to sample 70,000 m3 of microhabitat and process 50,000 species of beetles in

2½ years. In other words, we know the actors and where they are standing on
the stage, and each has a number hanging around its neck. The taxasphere is
another creature, and getting formal names on the inventoried species is highly
dependent on the group of beetles, its history of studies, and its current taxon-
omist(s).
The advantages of the TWIG protocol are that (1) it is far more rapid than
any of its predecessors; (2) data byproducts allow diverse follow-up studies be-
yond the inventory process; (3) targeted taxa known to be important to users
can be piped readily (and continuously) through the taxasphere; (4) space and
storage facilities are minimized because samples mostly are stored cold in two-
dram shell vials or petri dishes until needed by a dedicated specialist; and (5)
dedicated specialists will “donate” their time to the collections as they select and
prepare specimens from cold storage, hence building collections becomes a
shared taxaspheric process.
Beyond the inventory itself, such questions as “do beetles form discreet
assemblages in tropical forests, or in any biotope anywhere?” can be tested. If
so, how that information might be used for answering scientific questions and
for developing conservation strategies is of considerable interest. The objective
of this kind of study would be to fill a large gap in our understanding of hyper-
diversity. For example, (1) what percentage do beetles contribute to a sample?
(2) What is the fidelity of beetle faunules to microhabitats? (3) What is the rate
of species turnover across extensive geographic space in the tropics? (4) What is
the rate of local species replacement among and between tropical microhabitats?
(5) What proportion of the total beetle fauna inhabits arboreal versus forest floor
habitats? (6) What is the rate of change in composition of faunules with respect
to altitude?
This information does not now exist on any meaningful scale for any hyper-
diverse group of organisms. Without this information, it is impossible to scale
any kind of locally derived estimate of biodiversity to even a regional perspec-
tive. With this information, I believe we can get much closer to estimating the
magnitude of life on the planet. And with these kinds of data from three or four
ATBIs, much finer estimates can be made elsewhere of actual amounts of bio-
diversity that are based on fewer samples and made with quicker inventories.

REFERENCES
Adis, J. 1984. Seasonal igapo forests of Central Amazonian blackwater rivers and their terrestrial
arthropod fauna. Pp 245-268 in H. Sioli, ed., The Amazon Limnology and Landscape Ecology
of a Mighty Tropical River and Its Basin. W. Junk, Dordrecht, Netherlands.
Adis, J., Y. D. Lubin, and G. G. Montgomery. 1984. Arthropods from the canopy of inundated and
terra firme forests near Manaus, Brazil, with critical consideration of the Pyrethrum-fogging
technique. Stud. Neotrop. Fauna Envir. 19:223-236.
Adis, J., and H. O. R. Schubart. 1984. Ecological research on arthropods in Central Amazonian forest

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BIODIVERSITY AT ITS UTMOST: TROPICAL FOREST BEETLES / 39

ecosystems with recommendations for study procedures. Pp 111-114 in J. H. Cooley and F. B.

Golley, eds., Trends in Ecological Research for the 1980’s. NATO Conference Series I: Ecology.
Plenum Press, N.Y.
Allison, A., G. A. Samuelson, and S. E. Miller. 1993. Patterns of beetle species diversity in New
Guinea rain forest as revealed by canopy fogging: Preliminary findings. Selbyana 14:16-20.
Arnol’di, L. V., V. V. Zherikhin, L. M. Nikritin, and A. G. Ponomarenko. 1992. Mesozoic Coleoptera.
Oxonian Press, New Delhi, India. 284 pp.
Ashworth, A. C., and J. W. Hoganson. 1993. The magnitude and rapidity of the climate change
marking the end of the Pleistocene in the mid-latitudes of South America. Palaeogeogr.
Palaeoclimatol. Palaeoecol. 101:263-270.
Ashworth, A. C., V. Markgraf, and C. Villagran. 1991. Late Quaternary climatic history of the Chil-
ean Channels based on fossil pollen and beetle analyses, with an analysis of the modern vegeta-
tion and pollen rain. J. Quat. Sci. 6(4):279-291.
Basset, Y. 1990. The arboreal fauna of the rainforest tree Argyrodendron actinophyllum as sampled
with restricted fogging: Composition of the fauna. Entomologist 109:173-183.
Basset, Y. 1991. The taxonomic composition of the arthropod fauna associated with an Australian
rainforest tree. Aust. J. Zool. 39:171-190.
Colwell, R., and J. Coddington. 1994. Estimating the extent of terrestrial biodiversity through ex-
trapolation. In D. L. Hawksworth, ed., The Quantification and Estimation of Organismal
Biodiversity. Phil. Trans. R. Soc. Lond. (B) 345(1311):101-118.
Erwin, T. L. 1982. Tropical forests: Their richness in Coleoptera and other Arthropod species.
Coleopt. Bull. 36(1):74-75.
Erwin, T. L. 1983a. Tropical forest canopies, the last biotic frontier. Bull. Entomol. Soc. Amer.
29(1):14-19.
Erwin, T. L. 1983b. Beetles and other arthropods of the tropical forest canopies at Manaus, Brasil,
sampled with insecticidal fogging techniques. Pp. 59-75 in S. L. Sutton, T. C. Whitmore, and
A. C. Chadwick, eds., Tropical Rain Forests: Ecology and Management. Blackwell Scientific
Publications, Oxford, England.
Erwin, T. L. 1985. The taxon pulse: A general pattern of lineage radiation and extinction among
Carabid beetles. Pp. 437-472 in G. E. Ball, ed., Taxonomy, Phylogeny, and Zoogeography of
Beetles and Ants: A Volume Dedicated to the Memory of Philip Jackson Darlington, Jr., 1904-
1983. W. Junk, The Hague, Netherlands.
Erwin, T. L. 1988. The tropical forest canopy: The heart of biotic diversity. Pp. 123-129 in E.O.
Wilson and F. M. Peter, eds., BioDiversity. National Academy Press, Washington, D.C.
Erwin, T. L. 1989. Canopy arthropod biodiversity: A chronology of sampling techniques and re-
sults. Revista Peruana Entomologia 32:71-77.
Erwin, T. L. 1991. Natural history of the Carabid Beetles at the BIOLAT Rio Manu Biological Station,
Pakitza, Peru. Revista Peruana Entomologia 33:1-85.
Erwin, T. L., and D. H. Kavanaugh. 1980. On the Identity of Bembidion puritanum Hayward (Cole-
optera:Carabidae: Bembidiini). Coleopt. Bull. 34(2):241-242.
Erwin, T. L., and J. C. Scott. 1981. Seasonal and size patterns, trophic structure, and richness of
Coleoptera in the tropical arboreal ecosystem: The fauna of the tree Luehea seemannii Triana
and Planch in the Canal Zone of Panama. Coleopt. Bull. 34(3):305-322.
Farrell B. D., and T. L. Erwin. 1988. Leaf–Beetles (Chrysomelidae) of a forest canopy in Amazonian
Peru: Synoptic list of taxa, seasonality and host-affiliations. Pp. 73-90 in P. Jolivet, E.
Petitpierre, and T. Hsiao, eds., The Biology of the Chrysomelidae. W. Junk, The Hague, Neth-
erlands.
Gould, S. J. 1993. A special fondness for beetles. Nat. Hist. 102(1):4,6,8,10,12.
Halffter, G., and M. E. Favila. 1993. The Scarabaeidiae (Insecta:Coleoptera): An animal group for
analyzing, inventorying and monitoring biodiversity in tropical rainforest and modified land-
scapes. Biol. Int. 27:15-21.

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Hammond, P. 1992. Species inventory. Pp 17-39 in B. Groombridge, ed., Global Biodiversity: Status
of the Earth’s Living Resources. Chapman and Hall, London.
Kavanaugh, D. H., and T. L. Erwin. 1992. Extinct or extant? A new species of intertidal bembidiine
(Coleoptera: Carabidae: Bembidiini) from the Palos Verdes Peninsula, California. Coleopt. Bull.
46(3):311-320.
Kitching, R. L., J. M. Bergelson, M. D. Lowman, S. McIntyre, and G. Carruthers. 1993. The bio-
diversity of arthropods from Australian rain forest canopies: General introduction, methods,
sites, and ordinal results. Aust. J. Ecol. 18:81-191.
Kremen, C. 1992. Assessing the indicator properties of species assemblages for natural areas monitor-
ing. Ecol. Appl. 2:203-217.
Kremen, C., R. K. Colwell, T. L. Erwin, D. D. Murphy, R. F. Noss, and M. A. Sanjayan. 1993. Terres-
trial arthropod assemblages: Their use in conservation planning. Conserv. Biol. 7(4):796-808.
Lindroth, C. H. 1980. A revisionary study of the taxon Cillenus Samouelle, 1819, and related forms
(Coleoptera: Carabidae, Bembidiini). Entomol. Scand. 11:179-205.
Robinson, M. H. 1986. The fate of the tropics and the fate of man. Zoogoer 5:4-10.
Stork, N. E. 1991. The composition of the arthropod fauna of Bornean lowland rain forest trees. J.
Trop. Ecol. 7:161-180.
Wilson, E. O. 1987. The little things that run the world. Conserv. Biol. 1(4):344-346.
Wilson, E. O., and F. M. Peter. 1988. BioDiversity. National Academy Press, Washington, D.C. 521
pp.
Wilson, E. O. 1992. The Diversity of Life. Belknap Press, Cambridge, Mass. 424 pp.

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CHAPTER
5

Measuring Global Biodiversity

and Its Decline

NIGEL E. STORK
Research Entomologist, Biodiversity Division, Department of Entomology,
The Natural History Museum, London, United Kingdom

In recent years biologists have come to recognize just how little we know
about the organisms with which we share the planet Earth. In particular, at-
tempts to determine how many species there are in total have been surprisingly
fruitless. In this chapter, I examine this and a number of related issues. I first
consider the progress, or rather the apparent lack of progress, that we have
made in describing organisms. Second, I consider how much we know about
the biology, distribution, and threatened status of those species that have been
described. Third, I examine some of the different methods that have been used
to determine the global number of species. Finally, I examine the likelihood of
extinction of species.
My remarks focus in large part (but not exclusively) on terrestrial arthro-
pods, particularly insects. This is not simply because this happens to be my own
special interest group, but rather because the issues discussed above have been
pursued with greatest vigor for this taxon. In addition, on the basis of present
evidence, insects appear to be the most speciose taxon on Earth and the one
which is threatened with the greatest number of extinctions. In investigating
the magnitude of biodiversity, I focus at the level of species, again because this
is my own special interest. Those who might have greater interest in the genetic,
landscape, or ecosystem level of biodiversity would find that our understanding
of the magnitude of biodiversity is somewhat different. I do not examine local
species richness per se, except in the context of the measurement of global spe-
cies richness. For this subject, there are a number of important recent texts
(e.g., Colwell and Coddington, 1994; Hammond, 1994; Soberon and Llorente,
1993).

41

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42 / BIODIVERSITY II

THE LEGACY OF LINNAEUS

Some 237 years ago, Linnaeus published his Systema Naturae, a new bino-
mial system for the naming of organisms in a classification that linked their
morphological relationships (Linnaeus, 1758). He set in train a flurry of de-
scriptions of species by a new breed of scientists—taxonomists. Since that time,
some 1.4 to 1.6 million species have been named and described (Stork, 1988;
Hammond, 1992) (see Figure 5-1). The precise figure is uncertain for several
reasons, the main one being that there is no recognised central register of names
for described species (although such registers do exist for a few groups), and
therefore some species have been described many times. For example, someone
who may be describing a species from India may be unaware that the species
already has been described from Pakistan. In other cases, the natural variation
of a species is unknown, and different forms of the same species are given differ-
ent names. The common European “ten-spot ladybird,” Adalia decempunctata
L., for example, has at least 40 different synonyms, many of these having been
used for the color morphs! Gaston and Mound (1993) noted that, although only
some 4,000 species of mammals currently are recognised (Corbet and Hill, 1980),
the collections at the Natural History Museum in London contain “types” (see
“holotype,” below) for 9,000 names. They also suggest that, for insects, the

Coleoptera
Lepidoptera
Hymenooptera
Diptera
Other insects
Arachnids
Crustaceans
Other arthropods
Other invertebrates
Molluses
Nematodes
Vertebrtates
Plants (Embryophytes)
Algae
Fungi
Protozoans
Bacteria
Viruses

0 50,000 100,000 150,000 200,000 250,000 300,000 350,000 400,000 450,000

FIGURE 5-1 Number of species described for all organisms (after Hammond, 1992;
Stork, 1993).

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MEASURING GLOBAL BIODIVERSITY AND ITS DECLINE / 43

TABLE 5-1 Present Levels of Synonymy in Insects

Names
Total Currently %
Species Accepted Synonomy Source

Odonataa 7,694 5,667 26 Bridges (1991)

Isopterab 2,000 1,600 20 Snyder (1948)
Thysanoptera 6,479 5,062 22 L. A. Mound
(unpublished data,
1993)
Homoptera
Aleyrodidae 1,267 1,156 9 Mound and Halsey
(1978)
Aphididae 5,900 3,825 35 Eastop and Hille Ris
Lambers (1976)
Siphonaptera 2,692 2,516 7 D. J. Lewis
(unpublished data)
Diptera
Simuliidae 1,800 1,460 19 Crosskey (1978)
Lepidoptera
Noctuidae 35,473 28,175 21 Poole (1989)
Papilionidae and Pieridaea 9,075 1,792 80 Bridges (1988a)
Lycaenidae and Riodinidaea 13,108 5,757 56 Bridges (1988c)
Hesperiidaea 8,445 3,589 58 Bridges (1988c)
Hymenoptera
Chalcidoidea 22,533 18,601 18 Noyes (1990)

aSubspecific names are treated as synonyms.

bThese figures are estimates, due to problems in data interpretation.
SOURCE: Gaston and Mound (1993).

level of synonymy is about 20% (Table 5-1). Therefore, although there may be
some 1.8 to 2.0 million names used by taxonomists, in reality these probably
represent some 1.4 to 1.6 million species.
Why is it that taxonomists apparently make so many “mistakes”? In part,
this is because variation within species can make it difficult to assess whether a
series of individuals represents one or more species and because often it is diffi-
cult to obtain representative samples of species from all parts of their range.
However, a more practical problem for the high level of synonymies is that it
can be very difficult for taxonomists to look at specimens of previously de-
scribed species to check whether their specimens are of new species. When a
species is described, one specimen usually is designated as the “holotype” (often
called “type”) for that species, and comparisons therefore need to be made
against it. Probably more than 80% of all types are housed in the ancient collec-

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44 / BIODIVERSITY II

tions of various European museums and herbaria—reflecting the former tradi-

tion of exploration by many of these countries during the nineteenth and early
twentieth centuries. Someone working on the taxonomic revision of a group of
beetles from West Africa, for example, might have to compare their specimens
with types from many museums or herbaria in Europe or North America, and
often this task is not feasible.
Not surprisingly, therefore, the current rate of description of about 15,000
new species a year (Stork, 1993; Hammond, 1992) is only about twice the aver-
age of 6,000 to 8,000 species described over the last 230 years (Figure 5-2). Even
with the lowest estimates of global species diversity of 3 million, it would take
90-120 years to describe all species at this depressingly low rate. The solution to
increasing the rate of description of the Earth’s fauna and flora is not a simple
one, and those who might prescribe setting up of a factory-like “conveyor belt”
system of dedicated species describers should beware. Many entomologists are
familiar with the name of Francis Walker, who worked at the British Museum of
Natural History and described thousands of species of Coleoptera, Diptera, and
Hymenoptera in this way. Many of his species have since been synonymised,
involving an enormous amount of wasted time for later taxonomists. One obitu-
ary indicated that he died too late to save his reputation! Thus, the solution is
not just to establish a cadre of species describers but rather to train many more
taxonomists.

Nematodes
Fungi
Arachnids
Other insects
Hymenoptera
Diptera
Coleoptera
Lepidoptera
Crustaceans
Protozoans
Annelids
Platyhelminths
Sponges
Molluscs
Vertebrates

0 500 1,000 1,500 2,000 2,500

FIGURE 5-2 Average number of species described each year (from Zoological Record,
1978-1987) for selected animal groups (after Hammond, 1992).

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MEASURING GLOBAL BIODIVERSITY AND ITS DECLINE / 45

WHAT DO WE KNOW OF SPECIES?

The question of “how many species are there?” has been in many ways
rather overshadowed by other and perhaps more interesting and important ques-
tions. As Lawton (1993:4) wrote, “Intriguingly, I have never seen anybody
discuss what we actually know about the 1.7 million (species) that do have
names. Overwhelmingly the answer will be nothing, except where they were
collected and what they look like.” At modest (and, as I suggest later, probably
quite reasonable) global estimates of around 5-15 million species, it is clear that
we have named only about 10-30% of global species. And although many other
unnamed species are housed in the accessions of museums and herbaria, these
species or the information associated with them are effectively unavailable to
the scientific community.
So what do we know of these species? For groups such as birds and large
mammals, we have a very good understanding of their distribution, biology,
and often their threatened or nonthreatened status. Even so, there are still mas-
sive gaps in our understanding of even the best-known groups, as Figure 5-3
shows. What then for other less well-known groups, such as plants, inverte-
brates, and fungi? Clearly, again there are some groups that have particular
significance, whether for human health (e.g., mosquitos), agriculture (e.g., many
crop plants), or other human interest (e.g., orchids), and the biology of these is
sometimes much better known than for other related taxa. But for most groups,
almost nothing is known of their distribution and biology.
Stork and Hine (unpublished, 1995) analysed the distributions of beetles
from revisions and descriptions extracted randomly from the 1987 Zoological
Record. They found that 53% of the 186 species (whether newly described or
previously described) included in the 46 taxonomic papers they examined were
known only from a single locality. Furthermore, 13% were known from just
single specimens. Beetles are about 25% of all described species, and if most
other animals and plants are as little known as these, it would seem that more
than half of described species are known from single localities. This will come as
no surprise to those taxonomists working with some of the major collections in
the world, since so many species are known just from type specimens.
Most estimates of present rates of extinction would suggest that many hun-
dreds of thousands, if not millions, of species are threatened with extinction and
that we are witnessing a mass extinction spasm as greater or perhaps even greater
than any in the geological record (May et al., 1995). This is discussed more fully
at the end of the chapter. And yet only about 1,000 species are recorded as
having become extinct in recent years (since 1600). If we know so little of the
distribution and biology of most species, what then do we know of their “threat-
ened” status?
Over the last 20 years the International Union for the Conservation of Na-
ture has compiled Red Data Books for those species that are recognized as falling

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46 / BIODIVERSITY II

FIGURE 5-3 Distribution of the localities known for 962 species of African passerine
birds (from Hall and Moreau, 1970; Cotterill, personal communication, 1994). Birds are
the best-known group for Africa, as for most parts of the world, and yet this map shows
that there are still vast areas, such as in Angola, Mozambique, and some of the former
French territories in West Africa for which we have almost no distributional data.

into one of their different threatened categories. Some of these Red Data Books,
e.g., for groups such as primates and birds, are fairly comprehensive. For other
groups, such as insects, only a few species are included as tokens of the probable
but largely unknown threatened status of many other species. Some countries
have produced their own Red Data Books, and those for the United Kingdom
give an indication of just how high a proportion of species are threatened (see
below).
World-wide, some 11% of mammals and birds are threatened with extinc-
tion. Equivalent values for British mammals and resident breeding birds are
29.1 and 55.7% respectively. In contrast, data on the threatened status of in-
sects and other invertebrates are almost nonexistent. However, this does not
mean that few are threatened, but rather that we have little information, since

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MEASURING GLOBAL BIODIVERSITY AND ITS DECLINE / 47

an average of about 13% of all British species of insects, spiders, and molluscs
are threatened.
In summary, almost nothing is known of the distribution and threatened
status of most organisms. A global estimate of, for example, 10 million species of
all organisms would suggest that nothing is known of the distribution of 86% of
species, 7% are known from just one locality, only 7% are known from more
than one locality, and the threat of extinction is known for less then 0.5%.

HOW MANY SPECIES ARE THERE?

One of the central questions in the biodiversity debate has been “how many
species are there?,” for the answer has a bearing on other important and related
issues such as loss of biodiversity and where on the Earth to focus attention for
the conservation of biodiversity. As long ago as the 1800s, scientists were fasci-
nated by the global number of species. Westwood (1833), for example, quoted
another British entomologist, Ray, who suggested that there might be 20,000
species of insects in the world. We now know there at least that many species in
Britain alone! As more and more species have been described, the question of
how many species there are has received less attention. Until the 1980s, most
recent biology texts either ignored this issue or considered that the global total
of species was only a little above the number of described species (i.e., 2-3 mil-
lion species). Many thought that the total eventually would be found simply by
describing all species. Since then, several methods of estimating the global num-
ber of species have been used, and these are considered below. Most of the
methods used are based on simple or complex ecological or taxonomic patterns,
and use empirical data as the basis for some kind of extrapolation or other.

Ratios of Known to Unknown Faunas

The simplest estimates of number of species are based on known ratios of
groups of organisms. For example, Raven (1985) noted that, for mammals, birds,
and other large and well-documented animals, there are roughly twice as many
tropical as temperate species. If the same ratio is true for other organisms, he
argued, then with 1.5 million species described and two-thirds of these being
temperate, the global total would be 3 million. Although Gaston (1994) has
shown that most species described in the late 1980s are from nontropical regions
and from “nonmegadiverse” countries (Table 5-2), the distribution of most de-
scribed species is not known. However, a survey of the countries represented
by species in every one-hundredth drawer of the 11,500-drawer beetle collec-
tion at the Natural History Museum in London (Table 5-3) would suggest that
for this collection, at least, there are more tropical than temperate species of
described beetles (1,753 species sampled: 625 from temperate countries, 946 from
tropical countries, 182 both tropical and temperate [e.g., Australia]). Since the

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TABLE 5-2 Analysis of the Geographical Distribution of the 24,000

Newly Described Species of Coleoptera (49% of species), Diptera (25%),
and Hymenoptera (26%) That Are Referenced in the Volumes of Zoological
Record for the Years 1985-1989

Proportion of Species
Descriptions from the Proportion of the Sum Proportion of the Total
Ten Countries from which of Species Descriptions Number of Species Described
the Most Species were from the “Megadiversity” over the 5-year Period from
Described in Each Case Countries Different Faunal Regions
Country % Country % Country %

U.S.S.R. 8.7 China 6.2 Neartica 8.3

China 6.2 Australia 5.8 Neotropicalb 12.5
Australia 5.8 India 5.3 Palearcticc 19.2
India 5.3 Madagascar 3.6 Ethiopiand 12.1
United States 5.1 Brazil 2.8 Madagascar 3.7
Japan 4.6 Malaysia 2.0 Indian subcontinent 9.8
Papua New Guinea 4.1 Mexico 2.0 China, Japan, and Taiwan 13.7
Madagascar 3.6 Indonesia 1.7 Thailand to New Caledonia 12.7
South Africa 3.4 Peru 1.0 Australia and Tasmania 5.8
Brazil 2.8 Zaire 1.0 New Zealand 0.8
Ecuador 0.7 Oceanic Islands 1.3
Colombia 0.7

aIncludes the Arctic and temperate areas of North America and Greenland.
bIncludes South America, the West Indies, Central America, and tropical Mexico.
c Includes Europe, Arabia, and Asia north of the Himalayas, but not China, Japan, and Taiwan.
dIncludes the African subcontinent.

SOURCE: Gaston (1994).

estimated 175,300 species of beetles in this collection represent about half of all
described species of beetles, Raven’s suggestion that two-thirds of described
species are temperate would seem to be wrong.
Stork and Gaston (1990) used a slightly different approach to estimate the
number of insects world-wide. They first noted that the ratio of the number of
species of butterflies to all species of insects in the well-known British fauna is
67:22,000. They suggested that if this ratio were true world-wide, then (with an
estimated 15,000-20,000 species of butterflies world-wide) this would indicate a
total of 4.9 to 6.6 million species of insects.
These approaches are appealing in their simplicity, but how realistic are
such extrapolations based on ratios for different groups or geographical areas?
The evidence for this is conflicting. Geographical ranges for species are known
to increase with increasing latitude and altitude (Stevens 1990, 1992). How the
relative numbers of species for different groups varies with latitude is not pur-

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MEASURING GLOBAL BIODIVERSITY AND ITS DECLINE / 49

sued here, but some evidence suggests that the relative proportions of different
taxonomic groups or trophic groups, at least in terms of species, are the same in
arthropod communities from temperate and tropical forest trees (see below and
Stork 1987, 1988, 1993). This is in spite of the fact that the number of species of
arthropods in some tropical trees (up to 1,000 species per tree) is sometimes more
than three to four times the number on temperate trees of equivalent size (in
terms of canopy volume).
Hawksworth (1991) has used arguments based on the ratio of fungi to vas-
cular plants in different regions of the world to predict that possibly there are
more than 1.5 million species of fungi world-wide. He analysed several well-
known floras and recorded ratios of 1:1.4 to 1:6.0 for species of vascular plants
to species of fungi and suggested that a higher ratio was more representative of
floras world-wide. Given that there are an estimated 270,000 species of vascular
plants world-wide, Hawksworth argued that this would give a conservative es-
timate of about 1.5 million species of fungi (including allowances for fungi in
unstudied substrata). His data are for temperate floras, and the ratio of fungi to

TABLE 5-3 Number of Species of Beetles (and Predicted Total

Number of Species of Beetles) for the Top 15 Countries Represented
in the Natural History Museum in London

Number of Predicted Number of

Species Sampled Species in Collection Country

143 14,300 Australia

142 14,200 South Africa
139 13,900 United States
134 13,900 Brazil
118 11,800 India
86 8,600 Mexico
65 6,500 Philippines
61 6,100 Japan
60 6,000 Malaysia
58 5,800 U.S.S.R.
49 4,900 Indonesia
44 4,400 Colombia
44 4,400 Guatemala
39 3,900 Papua New Guinea
37 3,700 Madagascar

NOTES: These data were produced by examining the species in every one-hundredth
drawer of the 11,500-drawer collection of beetles. In total, 1,753 species were re-
corded, suggesting that the total holdings of identified species of beetles are 175,300.
This does not include unidentified species in the accessions and several small separate
collections of beetles. For “Megadiversity” countries, see Table 5-2. Data from Gaston
(1994) are in bold.

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50 / BIODIVERSITY II

plants may well be higher in tropical countries. If this is the case, then 1.5 mil-
lion could be an underestimate of the numbers of species of fungi in the world.

Extrapolations from Samples

Erwin’s 30 Million Species

The best known and most controversial estimates are those that have cen-
tered on the diversity of arthropods in the canopy of tropical forests (Figure 5-4).
Erwin (1982:74) sketched out a novel method of estimating global species num-
bers for insects from samples he collected by applying knock-down insecticides
to the tops of trees. His estimate has been quoted and misquoted so many times
that I provide the full text here.
“The tropical tree Luehea seemannii is a medium-sized seasonal forest evergreen
tree with open canopy, large and wide-spaced leaves. The trees sampled (n=19)
had few epiphytes or lianas generally, certainly not the epiphytic load nor-
mally thought of as being rich. These 19 trees over a three season sampling
regime produced 955+ species of beetles, excluding weevils. In other samples
now being processed from Brazil, there are as many weevils as leaf-beetles,
usually more, so I added 206 (weevils) to the Luehea count and rounded to
1,200 for convenience. There can be as many as 245 species of trees in 1 hectare
of rich forest in the tropics, often some of these in the same genus. Usually
there are between 40 to 100 species and/or genera, so I used 70 as an average

a b

FIGURE 5-4 (a) Insects can be sampled from the

canopy of trees through the use of a fogging ma-
chine. This machine produces a warm rising
cloud of a knock-down insecticide such as a syn-
thetic nonresidual pryrethroid or natural pyreth-
rum. (b) The insects fall to the ground within a
couple of hours and are collected on plastic sheets
or on conical fabric trays, each 1 m 2 in area.

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MEASURING GLOBAL BIODIVERSITY AND ITS DECLINE / 51

TABLE 5-4 Numbers of Host-Specific Species per Trophic Group on

Luehea seemannii

Number of Species Number of Host-

Trophic Group (estimated) % Host-Specific Specifics (estimated)

Herbivores 682 20 136.4

Predators 296 5 14.8
Fungivores 69 10 6.9
Scavengers 96 5 4.8
Total 1,200 162.9

SOURCE: Erwin (1982).

number of genus-group trees where host-specificity might play a role with regard to
arthropods. No data are available with which to judge the proportion of host-
specific arthropods per trophic group anywhere, let alone the tropics. So con-
servatively, I allowed 20% of the Luehea herbivorous beetles to be host-spe-
cific (i.e., must use this tree species in some way for successful reproduction),
5% of the predators (i.e., are tied to one or more of the host-specific herbi-
vores), 10% of the fungivores (i.e., are tied to fungus associated only with this
tree), and 5% of the scavengers (i.e., are associated in some way with only the
tree or with the other three trophic groups)” (see Table 5-4 in this chapter).
“Therefore, Luehea carries an estimated load of 163 species of host-specific
beetles, a rather conservative estimate of 13.5%. I regard the other 86.5% as
transient species, merely resting or flying through Luehea trees. If 1 hectare
has 70 such generic-group tree species, there are 11,410 host-specific species of
beetles per hectare, plus the remaining 1,038 species of transient beetles, for a total
of 12,448 species of beetles per hectare of tropical forest canopy.
Beetles make up an estimated 40% of all arthropod species, therefore there
are 31,120 species of arthropods in the canopy of 1 hectare of tropical forest.
Based on my own observation, I believe the canopy fauna to be at least twice as
rich as the forest floor and composed of a different set of species for the most
part, so I added 1/3 more to the canopy figure to arrive at a grand total of
41,389 species per hectare of scrubby seasonal forest in Panama! What will
there be in a rich forest? I would hope someone will challenge these figures
with more data.
It should be noted that there are an estimated 50,000 species of tropical trees
(R. Howard, via R. Eyde, pers. comm.). I suggested elsewhere (Erwin and Adis
1981) that tropical forest insect species, for the most part, are not highly vagile
and have small distributions. If this is so, and using the same formula as above,
starting with 162 host-specific beetles/tree species then there are perhaps as
many as 30,000,000 species of tropical arthropods, not 1.5 million!”
In this way, Erwin raised previous estimates for the number of species in the
world by almost a factor of 10, and because his estimate was based on real
samples, it was seen by many to be quite credible. The timing was also impor-

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52 / BIODIVERSITY II

tant, for his figure of 30 million species is used by many to show, first, how little
we know the Earth’s fauna and flora, but also, when coupled with esimates of
forest loss (Myers, 1989), to show that many species are threatened with extinc-
tion. Inevitably, the figure of 30 million species has become a political tool.
As May (1988, 1990) and Stork (1988, 1993) have suggested, the assump-
tions that Erwin made provide an agenda for research, and subsequently all of
these have been tested. These are discussed below.
The first assumption relates to the host-specificity of insects to trees, and
much evidence points to considerably lower numbers of species being specific
to trees than Erwin suggested. Gaston (1992) for example, found that one indi-
rect measure of host-specificity, the ratio of insect-to-plant numbers for differ-
ent regions, was typically 10, with a maximum recorded of 25. Following
Erwin’s argument that 40% of insects are beetles, this would suggest that only
4 of the 10 host-specific insects per plant are beetles. This is far less than the 162
suggested by Erwin, but again, as with Hawksworth’s estimate for the number
of species of fungi (Hawksworth, 1991), the data for plant/insect ratios are from
temperate countries only. In practice, although many species of insects may be
specific to a single species of tree, many feed on several species or even whole
genera or families. Canopy samples collected by Erwin and myself (Stork 1991)
(Figure 5-5) typically have many singletons (only one individual per species)

FIGURE 5-5 Preparation and sorting millions of individuals and thousands of species
from canopy-fogging and other samples collected in Sulawesi.

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TABLE 5-5 Diversity of Coleoptera (859 species; 3,919 individuals) and

Chalcidoidea (739 species; 1,455 individuals)

Coleoptera Chalcidoidea
N (individuals) N (species) N (individuals) N (species) N (individuals) N (species)
continued continued

1 499 26 1 1 437
2 133 30 1 2 160
3 62 31 2 3 54
4 24 32 1 4 31
5 35 35 1 5 18
6 21 36 1 6 10
7 8 39 1 7 8
8 13 40 2 8 4
9 4 45 1 9 6
10 4 49 1 10 3
11 4 53 1 11 2
12 5 66 2 12 1
13 4 77 1 13 1
14 2 81 1 17 1
15 2 90 1 19 1
17 4 112 1
18 2 129 1
19 1 137 1
22 3 140 1
23 2 194 1
24 3 235 1

NOTES: Collected from 10 trees in Borneo using knock-down insecticide fogging (Stork 1991, 1993).
The number of individuals is shown for each species. For example, 499 species of Coleoptera each
were represented by only one individual, 133 species each were represented by two individuals,
and so on.

that probably do not feed on the tree in question. Table 5-5 shows the rank
abundance curve for beetles and chalcid wasps fogged with knock-down insec-
ticides from 10 trees in Borneo. For both groups, more than half of the species
present were singletons. Botanists often record more than 100 species of trees in
single hectares of tropical forest, and with such immense diversity of trees and
other plants it should not be surprising to find that many species of insects are
collected from trees with which they have no close association.
Thomas (1990) examined the number of species of Heliconius butterflies
feeding on species of Passifloraceae. On 12 Central American sites, he found an
average of 7.2 species of Passifloraceae and 9.7 species of Heliconiinae. With
over 360 species of Passifloraceae being known for the neotropics, one might
scale up (9.7/7.2 × 360) to produce an estimate of 485 species of Heliconiinae.

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54 / BIODIVERSITY II

In practice, the total is only 66 species because these butterflies use different
species of Passifloraceae in different parts of their range. There are other com-
plications to this story as well, such as the fact that only 100-150 species of
Passifloraceae are found below 1,500 m (the upper limit for Heliconiinae), but
the principle is still the same. As May (1990) noted, the simple procedure of
multiplying the average number of species per tree by the number of species of
trees can be misleading, since the geographical ranges of plants and insects may
differ.
May (1990) looked at the theoretical distribution function pk(i), the fraction
of canopy insects found on tree species k which utilize a total of i different
species of trees. Further, he examined f, the proportion of species effectively
specialized to each species of tree. Using reasonably accurate data on the known
biologies of British beetles and their association with trees, he predicted that
10% were herbivores specific to the genus Quercus. A 5-year intensive study of
the beetle fauna of Richmond Park, an area dominated by oak woodlands
(Hammond and Owen, 1995), produced 983 species of beetles (the total is now
over 1,095 species), which is about 25% of all British beetles. Part of this study
included canopy-fogging of more than 40 oak trees plus several other species of
trees at different seasons over 2 years, which produced 198 species of beetles
(Hammond, 1994). Of the total (from all sampling methods), some 18% are spe-
cies-specifically associated with trees and some 3% are associated only with
oaks (Hammond, personal communication, 1995). First estimates of the tree-
specificity of tropical arthropods using May’s function, pk(i), and the beetle
data from canopy-fogging 10 trees in Borneo (Table 5-5) also support a figure of
less than 5% (Mawdsley and Stork, in press).
Erwin provided no data for his next assumption that beetles represent 40%
of tropical canopy arthropods. I and my colleagues from the Natural History
Museum in London sorted all arthropods to species in canopy samples from
Brunei and found that, of the 3,000+ species, about 20-25% (859 species) were
beetles (Stork, 1991). There has been no comparable tropical study to date with
which to compare these results, but this figure is similar to the 18% of all British
arthropods that is comprised by beetles (4,000 species). How the relative num-
ber of species for the four largest orders of insects (Coleoptera, Diptera, Hy-
menoptera, and Lepidoptera) vary in known (usually temperate) faunas was
examined by Gaston (1991), who concluded that there may be strong latitudinal
trends in the diversity of these taxa of which we are largely unaware. In spite
of this, I found that there was a remarkable similarity in (1) the relative propor-
tions of species from different guilds of insects from canopy samples from Brunei,
the United Kingdom, and South Africa (Stork, 1987), and (2) the relative num-
bers of species for different families of beetles in canopy samples from Brunei
and Panama (Stork, 1993). It is clear, then, that we are still some distance from
determining the relative contributions of groups such as beetles, parasitic wasps,
and flies to global diversity.

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MEASURING GLOBAL BIODIVERSITY AND ITS DECLINE / 55

There are no published data that might provide an indication as to the rela-
tive richness of the arthropods of the canopy and of the ground, but two recent
independent studies in Borneo and Sulawesi suggest that the 2:1 ratio in favor of
the canopy in Erwin’s estimate should be reversed. Hammond’s (1992) prelimi-
nary analysis of large samples of beetles from canopy and ground samples from
Sulawesi (see below), and subsequent more detailed analyses (Hammond, et al.,
in press), suggest that only about 10% of the 4,000+ species of beetles collected
in a hectare of lowland rain forest in Sulawesi are “canopy specialists” and that
there are more than twice as many “ground specialists” as “canopy specialists.”
The conclusions of this study are largely supported by an analysis of more than
3,000 species of beetles collected in similar ways in Borneo (Mawdsley, 1995).
Rather than exert too much effort in considering the ratio of species of arthro-
pods from the canopy to the ground (for as Hammond et al., in press, have
shown, a large part of the fauna is found in both ecotones), it might be better to
examine the ratio of functional groups, such as herbivores to other trophic
guilds.
In summary, Erwin probably has grossly overestimated the likely number
of host-specific insects associated with a species of tree, but underestimated the
contribution of insects other than beetles and those insects associated with the
ground.

Estimates from Intensive Sampling in Sulawesi

One of the obvious problems with Erwin’s method of estimating global spe-
cies diversity is that his base data are from samples collected only from the
canopy. In 1985, the Royal Entomological Society of London and the Indonesian
Department of Science carried out a year-long study of the Dumoga-Bone area of
north Sulawesi in Indonesia: Project Wallace. Some 200 entomologists carried
out studies in this area, including an intensive sampling program for insects that
was organized by the Natural History Museum in London. More than 6,000
species of beetles were collected by a wide variety of methods and then sorted to
species (Hammond, 1990; Stork and Brendell, 1990) (Figure 5-6). Other groups
of insects also were sampled intensively, and the data for one of these were used
by Hodkinson and Casson (1991) to estimate the number of species in the world.
Hodkinson and Casson (1991) examined 1,690 species of collected Hemi-
ptera and, after consultation with other specialists, estimated that 62.5% were
new to science. They suggested that if the same proportion of new species was
to be found world-wide (and they provided some statistical support for this)
then there should be 184,000-193,000 species of Hemiptera world-wide. If 7.5 to
10% of all insects are Hemiptera, they argued, this would give a world total of
1.84 to 2.57 million species of all insects. They also suggested that if there are
500 species of trees in the Dumoga-Bone area and this produced 1,056 new spe-
cies of Hemiptera, then 50,000 species of trees (see Erwin’s method above) would

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56 / BIODIVERSITY II

107

106

105
Number of species

104

103

102

10

1
0.0005 0.001 0.005 0.01 0.05 0.1 0.5 1 5 10
Characteristic size (meters)

FIGURE 5-6 Using the relationship between the number of species and their body size
for larger organisms, it is possible to back-predict for the less well-known smaller species
to estimate the total number of species in the world (after May 1978, 1988).

give 105,600 new species. These plus the described species would give 187,300
species of Hemiptera and a total of 1.84 to 2.57 million for all insects world-wide.
There are several problems with their arguments (Stork, 1993). First, they
assume that all species of Hemiptera in the area were collected and, since cumu-
lative curves for the even more thoroughly sampled beetles (Figure 2 in Stork,
1993) show little leveling off, this seems very unlikely. Second, they fail to dem-
onstrate that the ratio of described to undescribed species is representative of
other areas in the world. Third, since many groups of Hemiptera include eco-
nomically important species, it would seem probable that they have been sub-
ject to greater descriptive efforts than many other orders of insects. It would
seem likely therefore, that the proportion of the world’s species of insects that
are Hemiptera is much less than 7.5-10%.
With some 6,000+ species of beetles having been sorted and a projected
minimum total of 10,000 species estimated for the Dumoga-Bone area (Stork,
1993), it is possible to test their hypotheses. Using 15-20% as estimates of the
proportion of the world’s species of insects that are represented by beetles, there
should be 3-4 million (based on 6,000 species of beetles sampled) or 5 to 6.7
million (based on the minimum projected total of 10,000 species of beetles in the
Dumoga-Bone area) species of insects world-wide. What this clearly demon-
strates is that, if the samples represent only 50% of the species in the area con-
sidered, then the estimates will be 50% under the true figure.

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MEASURING GLOBAL BIODIVERSITY AND ITS DECLINE / 57

Inevitably, estimates based on such methods and on samples of insects will

be open to criticism until much more intensive sampling or even complete in-
ventories of some tropical areas are completed. Hopefully, much more accurate
estimates of regional and global diversity will be some of the many benefits of
the proposed All Taxa Biological Inventories (Janzen and Hallwachs, 1994).

Other Models for Estimation of Species

Many important ecological principles on the distribution and community
structure of organisms have been determined over the last 30 or more years, and
some of these have been used in the models discussed above. Several others also
show some promise and are discussed here.

Body Size and Number of Species

May (1978, 1988) noted that for a wide range of organisms larger than 1 mm
there is an inverse relationship between the number of species and body size.
Fractal arguments would suggest that, in the relationship S ~ L–x, where S is the
number of species and L is body length, the factor x should be between 1.5 and
3.0. Using these figures and extrapolating down to 1 mm, May (1988) suggested
global estimates of 10-50 million species (Figure 5-7). May’s (1990) later ex-

Coleoptera
Lepidoptera
Hymenooptera
Diptera
Other insects
Arachnids
Crustaceans
Other arthropods
Other invertebrates
Molluses
Nematodes
Vertebrtates
Plants (Embryophytes)
Algae
Fungi
Protozoans
Bacteria
Viruses

0 500,000 1,00,000 1,500.000 2,00,000 2,500,000 3,000,000 3,500,000 4,00,000

FIGURE 5-7 The projected number of species for different taxa based on an estimated
global total of 12.5 million species (after Hammond, 1992; Stork, 1993); shaded area is the
total number of described species from Figure 5-1.

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58 / BIODIVERSITY II

trapolation to 0.2 mm gave an estimate of 10 million species, based on the premise

that number of species increases 100-fold for a 10-fold reduction in length.
Having just discovered a complex and species-rich fauna of mites and Collembola
in sandy soils in France and Belgium, André et al. (1994) suggest that the extrapo-
lation should be to at least 136-65 µm, which would add another 10 million species
to May’s (1990) total. Addition of even smaller organisms (Protozoa, Nematoda,
Enchytraeidae, and Tardigrada), they argue, would further increase the total.
There are two major problems with this argument. First, the traditional
species concept based on sexual reproduction does not appear to apply to very
small organisms (or even to many larger organisms, such as some flowering
plants). For these, it might be more practical to look at functional characteristics
and genetic differences to separate them. Second, dispersal by air or by water is
easier for very small organisms than larger ones, and they are therefore less
likely to speciate, since the barriers necessary for the isolation of populations,
and hence allopatric speciation, are less likely to occur. In practice then, below
a body size of about 1.0 mm, number of species may decrease with decreasing
body size. The implications from arguments of André et al. are that there are 10
million species or more of groups such as Collembola, Acarina, and Nematoda.
So far, there is little evidence that this is the case. Intensive sampling of the
nematode fauna of soil and leaf litter of lowland forest in Cameroon produced
483 morphospecies, with evidence that the number of new species was falling
off with additional sampling (Lawton et al., in press). It is therefore probable
that, although the abundance of the soil invertebrate mesofauna is extremely
high, the number of species involved may well be considerably less than that for
insect groups such as beetles, flies, and Hymenoptera.

Species Turnover
One approach to measuring global species richness that has been employed
in the marine environment is to measure how species accumulate with time and
with distance. Theoretically, as additional samples are collected at increasing
distances away from a central point, the number of species added will increase
because of the added heterogeneity of the new habitats encountered. The differ-
ence between the species richness of samples from different sites is known as
beta diversity or species turnover. It is theoretically possible, therefore, to esti-
mate numbers of species based on estimates of beta diversity. Grassle and
Maciolek (1992), for example, studied data for a range of species of macro-
invertebrates from the deep sea that were collected over a 176 km transect of 14
stations at a depth of 2,100 m. They found 798 species of annelids, molluscs,
and arthropods in the 90,677 individuals in the samples. Of these, 480 species
had not been recorded before. They combined their samples over time at each
site to examine patterns in the addition of new species as they moved along their
transect (see Figure 11 in Grassle and Maciolek, 1992). The typical rarefaction

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MEASURING GLOBAL BIODIVERSITY AND ITS DECLINE / 59

curve they found showed a slowing down in the addition of species over the
transect. They suggested that a straight line prediction from the upper end of
this curve would indicate a linear rate of increase of one new species per km.
They generalized this to one new species per km2, which for an oceanic area of
3 × 10 8 km 2 deeper than 1,000 m would suggest several hundred million new
species. Recognizing that the densities of organisms are much lower at the bot-
tom of the deep sea than those on the continental shelf area they sampled, they
scaled their estimate of the total number of benthic species to 107.
May (1992) criticized their estimate, suggesting that they falsely assumed a
straight line for the upper part of their rarefaction curve, and that it would be
more reasonable to assume a doubling of the number of benthic species on the
basis of the number of new species relative to known species that they collected.
May also criticised other points of their arguments.
A similar problem exists with other data that at first glance also would
appear to support estimates of tens of millions of species. Erwin (1988, 1991)
found that in beetle samples of 1,080 species produced by canopy-fogging in
Amazonian forests, only 1% were shared between four different types of forest
in the same area. He also cites the example of two samples of moths from sites in
Bolivia and Peru that are 500 km apart which total 933 species (1,748 individu-
als) and 1,006 species (1,731 individuals) and which have only 60 species (3.2%)
shared between sites. Since most species of insects are extremely rare in canopy
(and other) samples (Table 5-5), the chance of catching the same species in two
samples even at the same site is extremely low. In other words, although these
are impressive figures for the number of species sampled, the data themselves
are not sufficient to support high levels of endemism, nor do they provide any
measure of how widespread these species are. Comparison of the percentage
shared between subsamples at the same site and the percentage shared between
different sites would provide more relevant information on local endemism.
Another way of looking at this problem is to consider the size of the re-
gional pool of species. If we assume a modest global figure of 5.3 million for all
species of insects (see Table 3 in Stork, 1993), that there are 1.2 million species in
tropical South America, that 300,000 of these are beetles, and that half of these
are widespread (but probably mostly not very abundant), then the regional
beetle fauna where Erwin collected his canopy samples might be as high as
100,000. If this is the case, then his sample of 1,080 beetles from four types of
forest in Manaus is very small and the 1% value for shared species hardly sur-
prising. The assumptions may be completely wrong, but they need testing with
the correct statistical tools and probably much larger samples.

Taxonomists’ Views
The arguments presented above all rely on one important factor and that is
the taxonomists’ views of what constitutes a species. These views will differ

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60 / BIODIVERSITY II

depending on the taxa studied, the biology of the groups concerned, the tech-
niques used to distinguish species, and how far individual taxonomists are pre-
pared to go in order to clarify the number of species involved. Most of the
above debate has concerned samples of beetles and other insects where a
“morphospecies” concept has been adopted. Sometimes single species that ap-
pear to be valid on normal morphological characteristics later are found to com-
prise several species which can be distinguished only with molecular techniques
(Adis, 1990). To this end, it is impossible at this stage to say how many such
molecular species might exist.

EXTINCTIONS
In recent years, many eminent scientists have made ominous predictions
about present and future rates of the extinction of species (Table 5-6). Why so
few species actually have been recorded as extinct is evident from how little we
know about the number of species on Earth and their distribution. One of the
major problems with predicted extinction rates is that the groups most likely to
be affected, in terms of numbers of species, are also those for which we have the
least information. That the threat of extinction is real can be seen through the
following analysis.
Mawdsley and Stork (1995) used British data on the threatened status of
different groups to make predictions on the number of extinctions for groups
such as insects (Table 5-7). They suggested that if the accuracy of the recorded
Red Data Book status of groups of British animals such as birds, mammals, and
invertebrates are comparable, and if these reflect their likelihood of extinction,
then it is possible to use these data to estimate a “relative rate of extinction.”
The relative rate for threatened birds to insects is 4.3, implying that a British
breeding bird is, on average, 4.3 times as likely to become extinct as an insect.
Figures for endangered species give a higher relative rate of 9.8. Smith et al.
(1993a) also used Red Data Book status in two ways to estimate extinction rates
for well-known groups such as birds, mammals, and palms, but not for insects.
They first examined the number of species added to the list of extinctions for
animals during 1986-1990 and for plants during 1990-1992. Using these data
and estimated numbers of species world-wide, they predicted that the time to
extinction for 50% of species was 1,500 years for birds and 6,500 years for
mammals. Second, they used data on the net changes of species in these groups
towards extinction during these periods (i.e., changes in Red Data Book status of
a species from “rare” through “probably extinct”) to predict 50% extinction
rates of 350 and 250 years for birds and mammals, respectively. Mawdsley and
Stork argue that since about 1% of birds and mammals have become extinct
since 1600, a mean relative extinction rate of 7.1 for birds to insects would sug-
gest that 0.14% of species of insects have become extinct since 1600. Assuming
a global total of 8 million species of insects, this would suggest that 11,200 have

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MEASURING GLOBAL BIODIVERSITY AND ITS DECLINE / 61

become extinct since that time. They also argue that, since the calculations of
Smith et al. would suggest a 12- to 55-fold increase in extinctions of birds in the
next 300 years, their relative extinction rate would predict an equivalent loss of
100,000-500,000 species of insects (i.e., 7-30 species per week). For an un-
described species of insect, it would appear that the chances of extinction may
be greater than the chances of description!
Whether the assumptions made by Mawdlsey and Stork (1995) match real-
ity and whether it is possible to use models from the British fauna and flora to
make global predictions is impossible to say, but their model at least can be
back-tested within the British context. Of the 13,746 species included in the
Red Data Book for insects (Shirt, 1987), 5% (99 species) have not been seen since
1900. Given a relative extinction rate of 7.1 for birds to insects, this would
suggest that 11 species of birds should have disappeared in the same period.
This prediction is confirmed by Sharrock (1974), who states that 11 species of
birds have become extinct in Britain and Ireland, with 2 species later recolonising
during 1800-1949.
If the estimates of loss of 100,000-500,000 species of insects in the next 300
years, as predicted using the relative extinction rate, seem comparatively low,
then perhaps it would be wise to look at the possible extinction threats for these
and other groups. Groombridge (1992) shows that the probable cause of extinc-
tion for many species of birds and mammals was the introduction of other spe-
cies and hunting. A comparable analysis of the extinct species of insects has not
been made, but Mawdsley and Stork (1995) show that, for British beetles and
butterflies, the overriding threats are land-use change and habitat destruction.

CONCLUDING REMARKS
What these arguments show is how little we actually know about some of
the fundamental aspects of the biology and distribution of organisms. We can-
not say how widespread species are, we do not know the size of the species pool,
and we do not know how specific species are to a particular habitat, type of soil,
type of forest, or, in some cases, a species of tree. They also indicate that for
some of the most species-rich groups of organisms such as arthropods, annelids,
nematodes, and fungi, the scale of sampling we have used so far is not sufficient
to answer some of the most important questions in biology. If such questions are
to be answered in the next 10-20 years, then we will need a program of action to
inventory and assess the scale of biodiversity, such as Systematics Agenda 2000
(Systematic Agenda 2000, 1994), which matches the Human Genome Project in
scale and scope. Without such action, it is clear that many species will be
doomed to extinction.
Estimating the number of species in the world has been bedeviled by the
lack of evidence of biological patterns on a global scale that are supported by
sound empirical data and anecdote. On present evidence, there seems little case

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 TABLE 5-6 Estimated Rates of Extinction

% Global Loss
Estimate Per Decade Method of Estimation Reference

One million species 4 Extrapolation of past Myers (1979)

between 1975 and 2000 exponentially increasing trend
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15-20% of species between 8-11 Estimated species-area Lovejoy (1980)

1980 and 2000 curve; forest loss based on
62 / BIODIVERSITY II

Global 2000 projections

50% of species by 2000 or 20-30 Various assumptions Ehrlich and Ehrlich (1981)
soon after; 100% by
2010-2025

9% extinction by 2000 7-8 Estimates based on Lovejoy’s Lugo (1988)

calculations using Lanly’s (1982)
estimates of forest loss
Biodiversity II: Understanding and Protecting Our Biological Resources

12% of plant species in — Species-area curve (z=0.25) Simberloff (1986)

neotropics, 15% of bird
species in Amazon basin

2,000 plant species per 8 Loss of half the species in Raven (1987)
year in tropics and area likely to be deforested
subtropics by 2015

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25% of species between 9 As above Raven (1988a,b)
1985 and 2015

At least 7% of plant species 7 Half of species lost over next Myers (1988)
next decade in 10 “hot-spots”
covering 3.5% of forest area
 0.2 to 0.3% per year 2-6 Half of rain forest species Wilson (1988, 1989, 1993)
assumed lost in tropical rain
forests are local endemics
and become extinct with
forest loss

2-13% loss between 1990 1-5 Species-area curve Reid (1992)

and 2015 (0.15<z<0.35); range
includes current rate of
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forest loss and 50% increase

Red Data Books for selected 1-10 Extrapolating current recorded Smith et al. (1993a,b)
taxa: 50% extinct in extinction rates and using the
50-100 years (palms), 300- dynamics of threatened categories
400 years (birds, mammals)

Red Data Books for selected 0.6-5 Fitting of exponential Mace (1994)
vertebrate taxa extinction functions based
on World Conservation Union
categories of threat
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NOTE: The estimated rates include species “committed” to extinction; see Heywood et al. (1994).
SOURCES: Mawdsley and Stork (1995), Reid (1992).

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MEASURING GLOBAL BIODIVERSITY AND ITS DECLINE / 63
 TABLE 5-7 “Relative Rates of Extinction” Estimated for Different Groups of British Animals

1 2 3 4 5 6 7 8 9
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Relative Relative Mean

Number of Number of Extinction Extinction Relative
64 / BIODIVERSITY II

Number of Threatened Endangered % of British % of World % of British Rate: Rate: Extinction

British British British Species Species Species Threatened Endangered Rate (from
Species Species Species Threatened Threatened Endangered (from [4]) (from [6]) [7] and [8])

Mammals 55 16 No data 29.1 11 — 2.3 — 2.3

Birds 210 117 76 55.7 11 36.2 4.3 9.8 7.1
Insects 13,746a 1,786 506 12.9 0.07 3.7 1 1 1
Araneae 622 86 22 13.8 — 3.5 1.1 0.9 1
Mollusca 210b 30 10 14.2 0.4 4.8 1.1 0.8 1
Biodiversity II: Understanding and Protecting Our Biological Resources

aThere are more than 22,000 species of British insects, but the Red Data Book (Shirt, 1987) only considers some of these.
bOnly terrestrial, brackish and freshwater molluscs are included.

NOTES: “Threatened” includes all categories and “endangered” is category 1 in the Red Data Book. Columns 7 and 8 are derived by comparing the
relative percentages between taxa in columns 4 and 6, respectively. Note that the percentage of threatened British birds is an overestimate because
of the data used to calculate this figure.
SOURCE: Mawdsley and Stork (1995).

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MEASURING GLOBAL BIODIVERSITY AND ITS DECLINE / 65

to be made for estimates of 30 million or more global species; a more probable

total is 5-15 million. If a single figure is to be selected, then that proposed by
Hammond (1992) of 12.5 million species would seem reasonable at this stage
(Figure 5-7). However, upward or downward revisions of this number could
easily occur through the compilation of new and sound data on the species con-
cept for some groups and on the distribution of major taxa such as insects, fungi,
and other microorganisms in terrestrial systems, and for annelids, molluscs, and
arthropods in marine systems.

ACKNOWLEDGMENTS
I thank F. Cotterill for drawing my attention to the distributional data for
Passerine birds. I am most grateful to Harriet Eeley for assistance in preparing
the figures and the manuscript.

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CHAPTER
6

Butterfly Diversity and a

Preliminary Comparison with
Bird and Mammal Diversity
ROBERT K. ROBBINS
Research Entomologist, Department of Entomology, National Museum of
Natural History, Smithsonian Institution, Washington, D.C.

PAUL A. OPLER
Director, Editorial Office, Information Transfer Center,
National Biological Service, Fort Collins, Colorado

Butterflies are among the best-known insects—an estimated 90% of the

world’s species have scientific names. As a consequence, their biology has been
extensively investigated (Vane-Wright and Ackery, 1984), and they are perhaps
the best group of insects for examining patterns of terrestrial biotic diversity
and distribution. Butterflies also have a favorable image with the general public.
Hence, they are an excellent group for communicating information on science
and conservation issues such as diversity.
Perhaps the aspect of butterfly diversity that has received the most atten-
tion over the last century is the striking difference in species richness between
tropical and temperate regions. For example, Bates (1875) wrote that it would
convey some idea of the diversity of butterflies (in the neighborhood of Belém,
a town near the mouth of the Amazon River) when he mentioned that about 700
species are found within a hour’s walk of the town, whereas the total number
found in the British Islands does not exceed 66, and the whole of Europe sup-
ports only 321. This early comparison of tropical and temperate butterfly rich-
ness has been well-confirmed (e.g., Owen, 1971; Scriber, 1973).
A general theory of diversity would have to predict not only this difference
between temperate and tropical zones, but also patterns within each region, and
how these patterns vary among different animal and plant groups. However, for
butterflies, variation of species richness within temperate or tropical regions,
rather than between them, is poorly understood. Indeed, comparisons of num-
bers of species among the Amazon basin, tropical Asia, and Africa are still mostly
“personal communication” citations, even for vertebrates (Gentry, 1988a). In

69

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70 / BIODIVERSITY II

other words, unlike comparisons

between temperate and tropical
areas, these patterns are still in
the documentation phase.
In documenting geographical
variation in butterfly diversity,
we make some arbitrary, but
practical decisions. Diversity,
number of species, and species
richness are used synonymously;
we know little about the even-
Butterflies are conspicuously
diverse in tropical forests. ness of butterfly relative abun-
dances. The New World fauna
makes up the preponderance of examples because we are most familiar with
these species. By focusing on them, we hope to minimize the errors generated
by imperfect and incomplete taxonomy. Although what is and is not a butterfly
is technically controversial (e.g., Reuter, 1896; Kristensen, 1976; Scoble, 1986;
Scoble and Aiello, 1990), we follow tradition (e.g., Bates, 1861; Kuznetsov, 1915,
1929; Ford, 1945) in which butterflies consist of skippers (Hesperioidea) and
true butterflies (Papilionoidea).
The first three sections of this chapter summarize general patterns of but-
terfly diversity throughout the world, within the conterminous United States,
and in the Neotropics, respectively. The fourth section points out, albeit pre-
liminarily, how the distributions of butterflies—and presumably other insects—
paint a different biogeographical picture of the world than the distributions of
birds and mammals. Finally, we briefly discuss the significance of the observed
patterns for conservation and for the study of diversity.

GLOBAL PATTERNS OF BUTTERFLY DIVERSITY

There are about 13,750 species of true butterflies in the world. Ehrlich and
Raven (1965) estimated 12,000-15,000, and Robbins (1982) narrowed the range
to 12,900-14,600 (including an estimate for undescribed species). Shields (1989)
tabulated 13,688 described species. Since Robbins used sources published after
1965 and Shields used post-1982 papers for information, these estimates are
somewhat independent, and their similarity indicates that 13,750 species of true
butterflies is a reasonable “ballpark” figure, almost assuredly accurate within
10% and probably within 5%.
There are about 17,500 species of butterflies (true butterflies plus skippers)
in the world. Ehrlich and Raven did not tabulate numbers of all butterflies, but
Robbins estimated 15,900-18,225 species in the world, including estimates of
undescribed species. Shields counted 17,280 species, including many synonyms
but excluding undescribed species. The estimate of 17,500 species of butterflies
in the world is again probably accurate within 10% (15,750-19,250 species).

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BUTTERFLY DIVERSITY / 71

The number of species of butterflies in each of the world’s major biogeo-

graphical realms is presented in Figure 6-1, modified from Ackery et al. (1995)
for the Ethiopian realm and from Robbins (1982) for the others. The estimates for
the Nearctic, Palearctic, and Ethiopian realms are reasonably accurate because
their faunas are fairly well-documented. The numbers for the more poorly
known Oriental-Australian (innumerable islands) and neotropical realms (liter-
ally hundreds of undescribed metalmark, skipper, and hairstreak butterflies)
are less accurate, probably within 10% of actual species richnesses.
Species diversity is greater in tropical than temperate areas (Figure 6-1). Of
the two northern temperate realms, the Palearctic has greater area and more
species than the Nearctic. These temperate realms have fewer species than the
primarily tropical neotropical, Ethiopian, and Oriental-Australian realms.
Among all realms, the Neotropics has the richest butterfly fauna, approximately
equal to that of tropical Africa and Asia combined (Figure 6-1).
The area of lowland rain forest is greatest in the Neotropics (Raven, 1990),
but is not responsible for the greater butterfly richness of Latin America. Liberia,
the Malay Peninsula, and Panama have similar areas at about the same latitude
(Figure 6-2), and their butterfly faunas are documented (Owen, 1971; Robbins,
1982; Eliot and D’Abrera, 1992). Panama is smaller than Liberia and the Malay

1,550

750

3,650
4,500
7,500

NEARCTIC ETHIOPIAN
NEOTROPICAL ORIENTAL
PALEARCTIC AUSTRALIAN

FIGURE 6-1 Number of species of butterflies by biogeographical realm. The 4,500 to-
tal is for the Oriental and Australian Realms combined. Ackery et al. (1995) listed 3,607
Ethiopian species. Robbins (1982) gave estimates for the other realms. There are an
estimated 17,500 species of butterflies world-wide.

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72 / BIODIVERSITY II

Michigan
134 Species
58,200 sq. mi.

Liberia
Panama 720 Species
1,550 Species 42,000 sq. mi. Malay Peninsula
32,000 sq. mi. 1,031 Species
50,700 sq. mi.

FIGURE 6-2 Area and number of species of butterflies for the Malay Peninsula (Eliot
and D’Abrera, 1992), Liberia (Owen, 1971), and Panama (Robbins, 1982). Michigan (see
Table 6-1) is included for comparison with an area in the temperate zone.

Peninsula, but has more than twice the number of species of butterflies than the
latter areas (Figure 6-2). Since Central America is not an unusually rich part of
the Neotropics (see below), its area of lowland rain forest alone is not likely to
explain why the Neotropics have a greater butterfly diversity than the Old
World tropics.

SPECIES RICHNESS OF U.S. BUTTERFLIES

Species of butterflies have been surveyed relatively well in most of the
conterminous United States. For almost all states, it is reasonable to expect that
more than 90% of the resident fauna has been discovered. Atlases of the county-
by-county distribution of butterflies of the United States have been compiled
over the past 20 years from published literature records, data from specimens in
museums and private collections, and by conducting field surveys in poorly
known geographic areas (Stanford and Opler, 1993; Opler, 1994, 1995).
By reviewing these atlases, we counted the number of true butterflies and
skippers that are residents, regular colonists, and vagrants for each state (Table
6-1). Residents are species that reproduce yearly and can survive all seasons.
Regular colonists are species that do not survive the winter, but which annually
immigrate into the state and usually establish temporary breeding populations.
Vagrants are species that have been reported in the state, but do not breed there

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BUTTERFLY DIVERSITY / 73

TABLE 6-1 The Number of Recorded Species of Butterflies that are

Residents, Regular Colonists, and Vagrants for Each State of the
Conterminous United States
Butterfly Residents Butterfly Breeding
State and Colonists Vagrants Birdsa

Alabama 132 2 145

Arizona 246 80 246
Arkansas 127 25 130
California 225 25 286
Colorado 230 36 235
Connecticut 101 13 158
Delawareb 91 7 160
Florida 163 18 160
Georgia 151 8 160
Idahob 154 6 ?
Illinois 121 22 160
Indiana 123 19 151
Iowa 107 19 154
Kansas 133 50 175
Kentucky 116 17 153
Louisiana 117 15 158
Maine 88 13 176
Maryland 121 19 192
Massachusetts 93 19 177
Michigan 134 10 202
Minnesota 132 13 224
Mississippi 134 10 13
Missouri 125 31 175
Montanab 184 3 224
Nebraska 170 27 194
Nevada 181 26 224
New Hampshire 92 9 175
New Jersey 120 23 181
New Mexico 272 46 247
New York 119 19 220
North Carolina 140 11 178
North Dakota 132 11 171
Ohio 131 7 180
Oklahoma 146 16 180
Oregon 159 5 232
Pennsylvania 114 20 18
Rhode Islandb 83 4 141
South Carolina 133 9 152
South Dakota 149 21 207
Tennesseeb 112 12 160
Texas 290 133 300
Utah 197 18 220
Vermontb 66 6 175
Virginia 134 21 179
Washington 140 3 235
West Virginia 112 8 156
Wisconsin 133 12 203
Wyoming 197 13 222

aFrom Peterson (1963).

bIncomplete census for butterflies.

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except on rare occasions. These categories were based on biology, caterpillar

host plants, geographic range, and published reports of breeding. In some cases,
category determinations were arbitrary decisions. For example, Atalopedes
campestris is considered to be a resident in Maryland and Virginia and, although
it may not survive every winter, it is judged to be a vagrant where recorded to
the north.
The number of species of butterflies recorded per state ranges from 87 for
Rhode Island, an incompletely sampled state, to 423 for Texas. Number of spe-
cies increases from north to south. For example, along the Atlantic seaboard,
species richness of butterflies increases steadily from the 101 recorded in Maine
to the 181 in Florida. Among the Pacific coastal states, Washington has 143
species, Oregon 164, and California 250.
Texas has the richest butterfly fauna, influenced by the lower Rio Grande
Valley. Even though only a few thousand acres of dry tropical forest habitat
remain in a few parks, reserves, and refuges, many of Mexico’s species of tropi-
cal lowland butterflies have been recorded in Cameron, Hidalgo, and Starr coun-
ties, largely as vagrants. Nevertheless, quite a few butterflies have their only
breeding populations in the United States in the lower Rio Grande Valley.
A second trend is for high species richness to occur in states with greatest
topographic diversity. The Rocky Mountain states have the greatest topographic
diversity and have faunal connections through the mid-continental cordillera to
both the Arctic and species-rich Mexico, through west Texas and southeastern
New Mexico to its Sierra Madre Oriental, and through the very rich areas of
southeastern Arizona and southwestern New Mexico to the Sierra Madre Occi-
dental. These faunal connections are shown by species with southern biogeo-
graphic afffinities that range northward at low to intermediate elevations from
Mexico, and those that range southward at high elevations from the arctic and
subarctic. All Rocky Mountain states have endemic western North American
butterflies, but those bordering the Great Plains also include a significant num-
ber of eastern species in their faunas.
Another recognizable trend is for species richness to be greater in the west
than in the east. While partly the result of relatively larger size of the states,
greater topographic diversity, and their proximity to species-rich Mexico, it is
nonetheless true that more butterflies per unit area are found in the richest areas
of western states. Florida, the richest eastern state, has 163 species of residents
and regular colonists, while the only western states having fewer species are
Idaho (154), Oregon (154), and Washington (140).
The poorest region, relative to its latitude, is the alluvial Mississippi drain-
age, including the states of Arkansas (127), Illinois (121), Iowa (107), Louisiana
(117), Mississippi (134), and Missouri (125). The somewhat higher regional spe-
cies richness in Arkansas, Mississippi, and Missouri is no doubt due to their
modest topographic relief. Historical factors such as the relatively recent flood-
ing of the Mississippi embayment also may have had a role.

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BUTTERFLY DIVERSITY / 75

NEOTROPICAL DIVERSITY
To document how diversity varies within the Neotropics, we tabulated spe-
cies richness at single localities (Figure 6-3). We did not distinguish tropical
breeding residents from strays because, with the exception of some migrants
(e.g., Beebe, 1949-1951), there is little evidence that tropical butterflies stray to
areas where they do not breed.
La Selva field station is situated in lowland rain forest on the Atlantic side of
Costa Rica and is relatively well-collected for the larger butterflies. The number
of recorded Papilionidae, Pieridae, and Nymphalidae is 204 species (DeVries,
1994). These three families comprise about one-third of the fauna in Panama
(Robbins, 1982), the Amazon Basin (Robbins et al., 1995), and at Itatiaia, a na-
tional park primarily above 500 m in Rio de Janeiro state (Zikán and Zikán,
1968). Consequently, 600-650 species is probably a reasonable estimate of La
Selva’s species richness. Since Belem (Brazil) is not nearly so well-documented,
the 700 species recorded by Bates (1875) is a minimal value. For Madre de Dios,
Peru, 1,234 species have been recorded since 1979 at the Tambopata Reserve
(5,500 ha), and 1,300 species were recorded on five field trips averaging less
than 3 weeks each to Pakitza (<4,000 ha), Manu National Park (Robbins et al.,

Middles
Middlesex
ex Fells
Fells - 68- 68 Species
Species

La Selva - 600-650 Species

Belem - 700+ Species
Pakitza - 1,300 Species
Tambopata - 1,231+ Species Itatiaia - 912 Species
Serro do Japi 652-800 Species

FIGURE 6-3 Number of species of butterflies at neotropical sites. The Middlesex Fells
Reservation in Massachusetts is included for comparison with a site in the temperate zone
(from Robbins, 1993b).

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76 / BIODIVERSITY II

1995). For southern Brazil, 912 species of butterflies were found over 5 decades
at Itatiaia (Zikán and Zikán, 1968; 17 species of Acraeini were omitted in this
paper), and 652 species were collected in 8 years at Serra do Japi (750-1,286 m),
a reserve near Jundiai, São Paulo (Brown, 1992). Documentation for the Peru-
vian and Brazilian sites includes museum vouchers.
Even though the number of species at Pakitza and Tambopata continue to
increase with each field trip, each of these sites already has more species of
butterflies than most, if not all, countries in tropical Africa and Asia (Robbins,
1993a). Clearly, explanations for the greater butterfly diversity of the Neotropics
need to account for the extraordinary richness that may occur at single neo-
tropical sites (the within-habitat, alpha, and point diversity concepts of
MacArthur, 1969; Whittaker, 1972; Pielou, 1975).
The high butterfly diversity at Pakitza and the Tambopata Reserve is not
unique. From what we know about the distribution of neotropical butterflies,
there appears to be a band of high butterfly diversity from southern Colombia to
the Peru-Bolivia border, ranging eastward from the base of the Andes to the
Brazilian states of Acre and Rondônia. This band also appears to extend, with
slightly decreased diversity, along the eastern base of the Andes in Venezuela
and Bolivia, but documentation is poor.
The upper Amazonian band of high butterfly diversity very roughly con-
sists of two faunal zones and is not uniformly high in diversity. The Rio Ma-
deira drainage in the south has a distinct dry season from about May to Septem-
ber, approximately 2,000 mm annual precipitation (Erwin, 1983, 1991; Terborgh,
1983), and a well-documented high butterfly diversity. Besides Pakitza and the
Tambopata Reserve, Jaru and Cacaulandia, Rondônia, Brazil, appear to have simi-
larly high diversities (Brown, 1984; Emmel and Austin, 1990). Alternately, much
of the drainage of the Rio Solimões (upper Amazon River) in the north lacks a
distinct dry season, has more than 3,000 mm annual precipitation (Gentry,
1988b), and supports a poorly documented butterfly fauna. From museum col-
lections, we infer that parts of eastern Ecuador and the Iquitos, Loreto, Peru,
areas are very rich, although sites in the vicinity of Pantoja, Loreto, Peru, on the
Rio Napo are relatively poor in species. The faunas of the Rio Solimões and Rio
Madeira mix in parts of Acre, Brazil, and Ucayali, Peru, which consequently
may be the richest areas in the world for butterflies (Brown and Lamas, personal
communications, 1993).

BUTTERFLIES, BIRDS, AND MAMMALS

If patterns of species richness and endemism were similar for different
groups of organisms, then knowing these patterns for any group, such as mam-
mals, would be sufficient to determine “biological” priorities among potential
sites for conservation. However, at the scale of 100 km 2, butterfly diversity is
not well correlated with the diversity of other groups of organisms in temperate

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BUTTERFLY DIVERSITY / 77

England (Prendergast et al., 1993). For the Neotropics, although lakes and caves
do not affect butterfly diversity at a site, they can affect the diversity of bats
and freshwater birds. Further, species richness of lowland plants is correlated
with precipitation (Gentry, 1988b), and the same is probably true for butter-
flies. (The data are scanty, but areas with less than 1,500 mm annual precipita-
tion have fewer species of butterflies than wetter areas.) However, the diversity
of neotropical mammals does not appear to be correlated with precipitation
(Emmons, 1984). Consequently, patterns of butterfly diversity in the Neotropics
are not expected to be strongly correlated with the patterns of mammals.
We recorded the number of breeding birds for each state in the United
States (Table 6-1). Because diversity is a function of area, we expected the num-
bers of breeding birds and nonvagrant butterflies for each state to be positively
correlated. After omitting incompletely documented states, a Spearman rank
correlation coefficient was indeed highly significant (r=0.606, n=42, p<0.001).
However, the increase in butterfly diversity from north to south (discussed
above) is less pronounced in birds than butterflies. For example, Florida, Geor-
gia, and South Carolina each have fewer breeding birds (152-160) than Maine or
Massachusetts (176-177). Whereas the bird fauna of New Mexico is about 10%
greater than that of Wyoming, the butterfly fauna is nearly 40% greater.
We graphed the percentage of the world’s species of butterflies that occur
in each major biogeographical realm (Figure 6-4) with similar percentages for

Nearctic Mammals
Birds
Butterflies
Palearctic

Ethiopian

Oriental-Australian

Neotropical

0 5 10 15 20 25 30 35 40 45
Percent of biogeographical regions

FIGURE 6-4 Proportions of species of butterflies, terrestrial mammals (Cole et al., 1994),
and nonmarine birds (Welty and Baptista, 1988) that occur in each of the world’s major
biogeographical realms.

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78 / BIODIVERSITY II

breeding nonmarine birds (Welty and Baptista, 1988) and terrestrial mammals
(Cole et al., 1994). Although slightly different boundaries were used by each
author, species richness of butterflies is strongly correlated with diversity of
birds, but not with diversity of mammals. For example, the neotropical realm is
the richest region for butterflies and birds (40-43%), but fewer than 25% of the
world’s mammals are neotropical.
Perhaps the major difference between the diversities of butterflies, birds,
and mammals is that butterflies are more “tropical” than birds, which, in turn,
are more “tropical” than mammals. The percentage of the world’s species that
occur in the northern temperate Holarctic (including the Nearctic and Palearc-
tic) is 32% for mammals, 21% for birds, and 13% for butterflies. Although
there are approximately 2 species of butterflies for every species of bird world-
wide, birds greatly outnumber butterflies in the Arctic, have about equal num-
bers of species as butterflies in temperate North America, and are outnumbered
by butterflies in the Neotropics (Table 6-2). Very roughly, an upper Amazonian
site will have 3-4 times more species of mammals (including bats)(Emmons, per-
sonal communication, 1993), 5 times more species of birds, and 15 times more
species of butterflies than a temperate North American site.

DISCUSSION
Among the well-known taxonomic groups of terrestrial animals, butterflies
have the greatest number of species. With 17,500 species, they are three to five
times more numerous than mammals (Wilson and Reeder, 1993), amphibians
(Zug, 1993), mosquitos (Wilkerson, personal communication, 1993), termites
(Nickle, personal communication, 1993), or dragonflies (Louton, personal com-
munication, 1993). There are approximately two species of butterflies for every
species of nonmarine bird (Welty and Baptista, 1988), and a bit less than three
species of butterflies for every one of reptiles (Zug, 1993).

TABLE 6-2 Number of Breeding Birds and Butterflies

for Greenland, Georgia, Panama, and Colombia

Locality Butterflies Birds

Greenland 5 57
Georgia 151 160
Panama 1,550 710
Colombia 3,100a 1,556

aEstimate is probably low.

SOURCES: Birds: Panama (Ridgely, 1976); all others (Welty and
Baptista, 1988); Butterflies: Greenland (Wolff, 1964); Georgia (this
paper); Panama (Robbins, 1982); Colombia (Brown, 1991).

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BUTTERFLY DIVERSITY / 79

Approximately 90% of the world’s species of butterflies have been de-

scribed taxonomically (Robbins et al., 1995). The great majority of the more
than 1,500 undescribed species occur in the Neotropics, which means that di-
versity studies in this realm, even if restricted to the better-known families
(Papilionidae, Pieridae, Nymphalidae), need to include systematists specializing
on the neotropical fauna. Since the Papilionidae, Pieridae, and Nymphalidae
make up about one-third of this fauna, at least in the lowlands (Robbins et al.,
1995), it is possible to focus on these families and still estimate the number of
Hesperiidae, Lycaenidae, and Riodinidae.
Although hypotheses can be suggested to explain why butterflies and mam-
mals have different patterns of species richness, we have focused on the implica-
tions for conservationists. If butterfly distributions are representative of other
insects, then strategies for conserving insects should not be based on the diver-
sity patterns of terrestrial vertebrates, particularly mammals. Further, butter-
flies are far more “tropical” than mammals, which emphasizes the importance of
protecting tropical areas for conserving terrestrial arthropods. From a biological
viewpoint, it might be more reasonable to expect a high correlation between
butterfly and plant diversity, but this hypothesis appears to be largely un-
examined.
The attention given to the magnitude of differences between tropical and
temperate areas appears to have had the unfortunate effect of obscuring difficul-
ties in defining, measuring, and comparing diversity. Given that the abundance
of tropical insects fluctuates markedly, changing the species composition at a
site from year to year (e.g., Wolda, 1992), is the species richness of butterflies in
the vicinity of Belem the number of species occurring there in 1 day, 2 months,
or 5 years? If the comparison is with England’s depauperate fauna, it does not
matter which “definition” is used for Belem’s species richness. But, if the com-
parison is with Manaus and Iquitos, then it may first be necessary to understand
the dynamics of tropical butterfly communities.

CONCLUSIONS

There is much to be done in developing a general theory that will predict

the patterns of diversity that we are beginning to document. We do not know
of any current theory that predicted that the upper Amazon basin at the eastern
base of the Andes would have the highest species richness in the world or that
single sites there might have more species of butterflies than tropical countries
on other continents. The Rio Madeira drainage is the richest area for birds and
the Rio Solimões has the greatest diversity for canopy trees (Gentry, 1988a);
however, neither theory nor correlations of diversity with other groups allows
us to predict which of these areas will be richer for butterflies. There is yet a
long way to go before we understand tropical butterfly diversity.

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ACKNOWLEDGMENTS
For discussion, advice, and unpublished information, we thank P. Ackery,
K. Brown, J. Burns, M. Casagrande, G. Ceballos, R. Cole, L. Emmons, D. Harvey,
G. Lamas, J. Louton, O. Mielke, A. Navarro, D. Nickle, K. Philip, R. Stanford, R.
Thorington, G. Tudor, R. Wilkerson, and D. Wilson. For reading the manu-
script and making constructive suggestions, we are most appreciative to P.
Ackery, G. Austin, J. Brown, A. Gardner, J. Glassberg, G. Lamas, S. Miller, and
O. Shields.

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CHAPTER
7

The Global Biodiversity of Coral Reefs:

A Comparison with Rain Forests

MARJORIE L. REAKA-KUDLA
Professor, Department of Zoology, University of Maryland, College Park

There has been increasing concern over declining global biodiversity due to
overexploitation and habitat destruction by humans, who now consume 20-40%
of the global net terrestrial primary productivity (Ehrlich and Ehrlich, 1992;
Ehrlich and Wilson, 1991; Wilson, 1992). Tropical communities are particu-
larly important in the global economics of biodiversity, because it is here that
human populations are increasing most rapidly, monetary resources will be most
strained, and problems of food production, pollution, and environmental change
will be most acute during the twenty-first century.
Two of the most diverse natural communities on Earth, coral reefs and rain
forests, both occur in the tropics. Coral reefs resemble rain forests in their bio-
logically generated physical complexity, high species diversity, elaborate spe-
cializations of component species, and coevolved associations between species.
Rain forests and coral reefs usually are considered to represent the two pin-
nacles of biodiversity on Earth, yet no detailed attempts to quantify the total
species diversity on coral reefs have been made. This chapter describes why
coral reefs are important for all societies to conserve and manage for the future,
addresses the need for training specialists in the systematics of marine organ-
isms (particularly those who would study the rich and poorly known tropical
regions), and provides the first quantified estimate of the total biodiversity of
global coral reefs as compared to rain forests.

THE VALUE AND CURRENT STATUS OF CORAL REEFS

Although they generally inhabit nutrient-poor waters, coral reefs are one of
the most productive ecosystems on Earth (Grigg et al., 1984). Their fishes and

83

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invertebrates traditionally have been and continue to be a critical source of protein

for the world’s tropical coastal countries. This fact will become increasingly
important over the next century and beyond, because it is precisely these coun-
tries that are experiencing explosive population growth and some of the most
severe coastal degradation. Failure to ameliorate the deterioration of marine waters
and to provide management plans for the sustainable use of reef fisheries will
remove an essential source of protein for these human populations (Norse, 1993).
In addition, coral reefs form ramparts that enclose lagoons, which are the
primary nurseries and feeding grounds for fishes and other organisms. Histori-
cally, these protected embayments have facilitated the development of human
transportation and commerce systems along tropical coastal areas. Today, they
protect human populations from hurricane and wave damage, making coastlines
secure for navigation, fishing, and tourism. Bioerosion of the carbonate reef
framework and the calcareous shells of reef organisms provide almost all of the
sand that comprises most tropical beaches. Tourism on coral reefs is an increas-
ingly important economic resource for developing countries, but such activity
must be managed sustainably if tourism is to remain a viable source of income.
Geologically, reefs are associated with oil repositories. The diversity on reefs
represents a largely unknown and untapped source of genetic material that has
potentially great medical, pharmaceutical, and aquacultural use.
However, the coral reefs of the world are endangered by overexploitation,
chemical and oil pollution, sedimentation, and eutrophication (resulting from
deforestation, construction, and agricultural runoff), as well as large-scale envi-
ronmental hazards such as increased ultraviolet light exposure and temperature
anomalies (Allen, 1992; Hallock et al., 1993; Hughes, 1994; Kuhlmann, 1988;
Sebens, 1994). World-wide episodes of coral “bleaching” (loss of symbiotic al-
gae that provide nutrients and increase rates of calcification; Brown and Ogden,
1993; Glynn, 1993; Ogden and Wicklund, 1988; Williams and Bunkley-Will-
iams, 1990), mass mortalities of reef-dwelling organisms (sometimes encompass-
ing entire geographic regions, such as the Caribbean-wide mortality of an eco-
logically important sea urchin; Hughes et al., 1985; Lessios et al., 1984), and
declining abundances of coral and other reef species (Porter and Meier, 1992)
have been documented over the last decade.
Some of the above trends have received attention from the media and have
been recognized by congressional hearings or other institutional initiatives (e.g.,
D’Elia et al., 1991). However, the value, risk of loss, and even the amount of
biodiversity on coral reefs (and in the marine environment in general) has re-
ceived relatively little attention by the scientific community, which is based
largely in northern temperate zones and is focused primarily on the terrestrial
environment (Gaston and May, 1992). Also, although ecotourism and recreation
in tropical environments, including coral reefs, has become increasingly popu-
lar in recent years, the public generally may be unaware of the urgency and
importance of environmental degradation in these tropical marine habitats. In

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GLOBAL BIODIVERSITY OF CORAL REEFS / 85

particular, the public has not been

adequately informed of the declin-
ing numbers of trained biologists
who are capable of estimating the
amount of biodiversity on coral
reefs, documenting how reef bio-
diversity is biogeographically dis-
tributed, and targeting where the
biodiversity on global coral reefs is
most at risk.
There is a crisis of declining
numbers of trained systematists
(scientists who analyze the relation-
ships between lineages, the evolu-
tionary trajectories, and the biogeo-
graphic distributions of organisms,
and signify these patterns in hierar-
chical taxonomic classifications so
that field-caught organisms can be
identified and their ecological roles
studied). This crisis is especially
acute for systematists of marine in-
Along with rainforests, coral reefs represent
vertebrates and algae (Feldmann and the second pinnacle of biodiversity on earth.
Manning, 1992; Gaston and May,
1992; John, 1994). There is an urgent need for major national and international
initiatives in the systematics and biodiversity of the global marine biota, par-
ticularly of the richest and least known components, the tropical marine biota.
The next section provides an estimate of the global biodiversity of coral
reefs and suggests that the lack of prior availability of such information is due to
the fact that marine environments in general and tropical marine habitats in
particular are understudied and relatively poorly known. This prevents us from
assessing which marine habitats of the world are in the most serious jeopardy
and, most importantly, prevents us from being able to recognize extinctions if
they occur or even from assessing the potential for extinctions. I argue that
extinctions in marine macrofauna (particularly on coral reefs) are likely to have
been more frequent than we have thought, and that the potential for loss of
coral reef species—with all of their inherent genetic and ecological value—over
the next 100 years is great.

A QUANTIFIED ESTIMATE OF BIODIVERSITY ON CORAL REEFS

There currently are about 1.8 million described species in all environments
on Earth, although various authors have estimated that 5-120 million species

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86 / BIODIVERSITY II

exist and that <10-50% of the Earth’s species may be known (Ehrlich and Wil-
son, 1991; Erwin, 1982, 1988; Gaston, 1991; Grassle and Maciolek, 1992; May,
1988, 1990, 1992; National Science Board Task Force on Biodiversity, 1989;
Stork, 1988; Wilson, 1988, 1992). Most international concern over declining
biodiversity has been focused on terrestrial environments, particularly the rap-
idly vanishing rain forests. This concern is justified, given the discoveries over
the last decade of how many species are present in these tropical wonderlands,
the potential uses of such genetic diversity, the potential effect of burning rain
forests on global climate, and the shocking rates—graphically relayed by satel-
lite—at which these habitats are being eclipsed by the activities of humans.
Until recently, however, the amount of biodiversity and its possible decline in
marine environments has received little attention.
It has been recognized that marine environments have more higher-level
taxonomic diversity than terrestrial environments. Among all macroscopic or-
ganisms, there are 43 marine phyla and 28 terrestrial phyla (of the 33 animal
phyla, 32 live in the sea and only 12 inhabit terrestrial environments), and 90%
of all known classes are marine (Angel, 1992; May, 1994; Pearse, 1987; Ray,
1985, 1988, 1991). Many of today’s marine animal phyla originated or diversi-
fied during the Cambrian evolutionary radiation more than 500 million years
ago, whereas plants and then animals invaded land later in the Paleozoic Era
(approximately 200-400 million years ago; Signor, 1994). This long separation
of evolutionary pathways among marine lineages has resulted in a greater vari-
ety of body plans, greater functional and biochemical diversity, and greater
“endemism” in major groups of marine compared to terrestrial animals (64% of
animal phyla inhabit only the sea, while only 5% of animal phyla live exclu-
sively on land; May, 1994).
In addition to containing great higher-level taxonomic diversity, some marine
environments also contain high species diversity. For example, the deep seas are
repositories of biodiversity. Based on samples of 1,597 species of marine macro-
fauna from soft bottoms off the east coast of North America (255 to 3,494 m
depths), Grassle and Maciolek (1992) calculated that the global deep sea fauna,
because of the huge area it occupies, may include 10 million species (mostly poly-
chaete worms, crustaceans, and molluscs; but see lower estimates in May, 1992,
1994; Poore and Wilson, 1993). Most of these species from the deep sea are rare
(90% of the species sampled by Grassle and Maciolek comprised <1% of the
individuals, and 28% of the species in the entire fauna were collected only once).
Local marine habitats also contain high numbers of species. Grassle and
Maciolek (1992) reported 55-135 species in individual 30 × 30 cm cores of ocean
floor sediment at 2,100 m depth. In a shallower soft-sediment environment in
south Australia, more than 800 species were found within a 10 m 2 area (Poore
and Wilson, 1993). Hughes and Gamble (1977) obtained 350 species from inter-
tidal soft substrates around a reef flat on Aldabra Atoll, and 6 liters of sediment
on Oahu yielded 158 species of polychaete worms (Butman and Carlton, 1993).

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GLOBAL BIODIVERSITY OF CORAL REEFS / 87

Coral reef communities also contain high local diversities of species. These
communities can be divided into three main components: (1) the suprabenthic
fishes; (2) sessile epibenthic organisms that provide the complex structure of the
reef (hard and soft corals, sponges, coralline and fleshy algae); and (3) the
cryptofauna, which includes organisms that bore into the substrate (primarily
sponges, polychaete and sipunculan worms, and bivalves), sessile encrusters
living within bioeroded holes and crevices (e.g., bryozoans, sponges, tunicates,
polychaete worms), and motile nestlers inhabiting bioeroded holes and crevices
(e.g., polychaete and sipunculan worms, echinoderms, molluscs, and especially
crustaceans). Although we usually think of coral reefs in terms of the first two
components, in fact most of the diversity as well as biomass of coral reef commu-
nities is included within the cryptofauna, which is the functional equivalent of
insects in the rain forest.
On the Great Barrier Reef of Australia, 350 species of hermatypic (reef-build-
ing) corals (33 of them endemic) are recognized, and 242 species are known from
one island (Ishigaki) in the Indo-West Pacific (Veron, 1985). Fifteen hundred
species of reef fishes have been reported from the Great Barrier Reef (Sale, 1977),
496 species of fishes are known from the Bahamas and adjacent waters (Bohlke
and Chapin, 1968), 442 species of fishes have been recorded in the Dry Tortugas
(Florida)(Longley and Hildebrand, 1941), and 517 species of fishes occur on Al-
ligator Reef (Florida) alone (Starck, 1968). Using rotenone to sample the fishes
on small areas of reef, single collections have yielded 67-200 species in the Baha-
mas and Palau, respectively (Goldman and Talbot, 1976; Smith, 1978a).
Bohnsack (1979) reported 10-23 species of reef fishes living around single coral
heads on Big Pine Key, Florida.
The reef-associated cryptofauna also is diverse at several scales. Taylor
(1968) found 320 molluscan species in a 31,000 km2 area of the Seychelles.
Peyrot-Clausade (1983) documented 776 species of motile cryptofauna (four
phyla) in dead coral from one reef flat in Moorea. One species of coral, Oculina
arbuscula, in Florida provided habitat for 309 species of organisms larger than
0.2 mm (McClosky, 1970). Fifty-five species of decapod crustaceans have been
reported to live in the coral Pocillopora damicornis in the Pearl Islands, Panama,
and up to 101 species of decapod crustaceans were found in P. damicornis in the
Indo-West Pacific (Abele, 1976; Abele and Patton, 1976; Austin et al., 1980).
Bruce (1976) documented 620 species of shrimps and prawns that are commensal
on different species of corals. Jackson (1984) documented 46 species of encrust-
ing cheilostome bryozoans between 0-21 m depth in Jamaica. On a smaller scale,
Gibbs (1971) found up to 220 species (8,265 individuals) of boring cryptofauna
in single colonies of dead coral, and Grassle (1973) reported 103 species of poly-
chaete worms in one colony of living coral. Thus, although no comprehensive
all taxa biodiversity inventories (Yoon, 1993) of coral reef habitats have been
made, it seems likely that diversity within as well as between coral reef habitats
is extraordinarily high.

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88 / BIODIVERSITY II

The total species diversity on global coral reefs has been difficult to quan-
tify precisely, however. The most current information on the number of species
contained within a group of organisms is found in monographic treatments of
the systematics and evolutionary biology of individual taxa, but different mono-
graphs often target different taxonomic levels (groups of species within a genus,
or groups of genera, families, or superfamilies) and usually include species from
all of the habitats occupied by the taxon (freshwater, estuarine, terrestrial, ma-
rine), making it difficult to tally the numbers of species on global coral reefs
among all taxa.
Using the concepts of island biogeography, known and calculated areas of
the major marine and terrestrial regions of the globe, and several testable as-
sumptions about the biogeographical distribution and abundance of marine spe-
cies, one can calculate the described and expected species diversity of coastal
marine organisms, tropical coastal marine organisms, and coral reef organisms
in comparison to that of rain forests. My laboratory at the University of Mary-
land is in the process of testing with empirical data the generalities about rela-
tionships between species richness in different habitats and biogeographical
realms that are present in or inferred from the literature and used in the present
calculations. Further additions to the database may alter the numerical results
slightly, but are not expected to substantially change the conclusions. Also,
the results presented here can be modified and updated easily as more data
become available, since the assumptions and mathematical relationships are
identified.
Available data and calculations (Table 7-1) reveal that the terrestrial realm
includes about 33%, global rain forests 2%, coastal zones 8%, tropical seas
24%, and tropical coastal zones 2% of the global surface area. Global coral reefs

TABLE 7-1 Area Relationships of Coastal Marine Zones and

Terrestrial Regions of the Globe (all areas are n × 106 km2)

Zones and Regions km2 % of Earth

Global surface area 511 100

Global land area 170.3 33.3
Global rain forests 11.9 2.3
Global oceans 340.1 66.7
Tropical seas 123.0 24.0
Global coastal zones 40.9 8.0
Tropical coastal zones 9.8 1.9
Coral reefs 0.6 0.1

SOURCES: Data were taken or calculated from information provided in

Kuhlmann (1988), the Rand McNally Atlas (1980), Ray (1988), Smith (1978b),
and Wilson (1988).

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GLOBAL BIODIVERSITY OF CORAL REEFS / 89

comprise about 0.1% of the Earth’s surface, 6% of tropical coastal zones, and
5% of the area of global rain forests.
Table 7-2 shows that there are approximately 1,450,000 currently described
species of terrestrial organisms (about 78% of the global biota), about 100,000
currently described species of symbiotic organisms (about 5% of the total), and
approximately 318,000 described species of aquatic organisms (17% of the glo-
bal total). Of aquatic organisms, my calculations from data in Pennak (1989) and
other sources revealed that about 26,000 species, or about 13% of the species of
macroscopic invertebrates overall, inhabit freshwater. Although about 40% of
the world’s species of fishes occur in freshwater (Ray, 1988), only 5-10% of
macroalgal species live in freshwater environments (John, 1994, and personal
communication, 1995). The above independently derived figure of about 13%
freshwater invertebrates is in good agreement with May’s (1994) data (drawn
from a tabulation of species in all benthic and pelagic marine and freshwater
animal phyla), which show that about 12% of all aquatic species live in freshwa-
ter. Consequently, to assess the number of marine species within the relatively
little-known microscopic algae, viruses and bacteria, and protistans (all of whose
affinities for freshwater or marine habitats might be expected to be closer to that
of macroalgae and invertebrates than to fishes), the proportion of marine versus
freshwater species was estimated to be about 90% and 10%, respectively.
Thus, of the 318,000 described species of aquatic organisms, a total of about
274,000 species was estimated to be marine (including approximately 180,000
species of macroscopic marine invertebrates; 36,000 species of micro- and mac-
roscopic marine algae; and 58,000 species of other marine groups such as verte-
brates, protistans, viruses and bacteria; Table 7-2). Therefore, about 15% of
global described species are marine (a figure independently obtained by May,
1994). If only macroscopic marine species are included due to uncertainties in
the taxonomy of microorganisms, there would be about 200,000 described spe-
cies of marine macroalgae, macroinvertebrates, and chordates, or about 11% of
the total described global species.
From the total numbers of described species of marine animals and plants
(above), one can calculate the number of species in global coastal zones by esti-
mating that about 80% of all marine species occur in the coastal zones (National
Science Board Task Force on Biodiversity, 1989; Ray 1988, 1991). This figure
probably is conservative. Over 90% of all marine species are benthic (bottom-
living) rather than pelagic (May, 1988, 1994). Almost all marine macroalgae live
in benthic (John, 1994, and personal communication, 1995) sunlit environments,
and oceanic phytoplankton comprise only 9-11% of all algal species (Sournia
and Ricard, 1991).
One then can calculate the number of described marine species that should
occur in tropical coastal and coral reef environments based on the global area of
these regions and current knowledge of biogeographic patterns. These calcula-
tions employ known theoretical and empirical relationships between the rate at

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90 / BIODIVERSITY II

TABLE 7-2 Species Diversity of Major Groups of Living Organisms

Number of % of Total
Described Species Described Species
Organisms (to nearest 1,000) (@ 1.87 million)

Terrestrial Organisms
Terrestrial chordates 23,000 1.2
Insects 950,000 50.8
Noninsect and noncrustacean arthropods 80,000 4.3
Other terrestrial invertebrates
(molluscs, nematodes, annelids,
platyhelminths, etc.) 57,000 3.0
Fungi 70,000 3.7
Terrestrial plants 270,000 14.4
Total Terrestrial Species 1,450,000 77.5
Aquatic Organisms
Algae 40,000 2.1
All marine algaea 36,000 1.9
All freshwater algaea 4,000 0.2
Marine macroalgae 4,000-8,000 0.2-0.4
Freshwater macroalgae 450 <0.1
Viruses and procaryotes 10,000 0.5
Marine viruses and procaryotesa 9,000 0.5
Freshwater viruses and procaryotesa 1,000 <0.1
Protozoa 40,000 2.2
Marine protozoansa 36,000 1.9
Freshwater protozoansa 4,000 0.2
Macroinvertebrates
Marine macroinvertebrates 180,000 9.6
Freshwater macroinvertebrates 26,000 1.4
Chordates
Marine chordates 13,000 0.7
Freshwater chordates 9,000 0.5
Total Marine Species
All taxa 274,000 14.7
Macrobiota 197,000-201,000 10.5-10.7
Total Freshwater Species
All taxa 44,000 2.4
Macrobiota 35,000 1.9
Total Aquatic Species 318,000 17.0
Symbiotic Organisms
Total Symbiotic Species 100,000 5.3
Total Global Described Biodiversity 1,868,000 —

aAssumes that the proportions of marine and freshwater species are 90% and 10%, respectively
(see text).
SOURCES: Data were taken, calculated, or updated from Barnes (1984), Brusca and Brusca (1990),
Ehrlich and Wilson (1991), Hammond (1992), Hawksworth (1991), John (1994, and personal commu-
nication, 1995), Margulis and Schwartz (1988), May (1988, 1991, 1992, 1994), Parker (1982), Pearse
(1987), Pennak (1989), Raven and Wilson (1992), Ray (1988, 1991), Systematics Agenda 2000 (1994),
and Wilson (1988).

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GLOBAL BIODIVERSITY OF CORAL REEFS / 91

which numbers of species change with area (S=cAz, where S is number of spe-
cies, c is a constant, A is area, and z is a scaling factor that usually falls between
0.2 and 0.3; MacArthur and Wilson, 1967; May, 1975, 1994; Wilson, 1989, 1992).
Where z=0.25, a reduction of 90% in area coincides with a reduction of about
half of the species present, which approximates natural situations for faunas on
islands of different sizes or where habitat destruction has reduced the amount of
area available to species.
Using the above biogeographical equations and the assumptions that tropi-
cal coastal zones are approximately twice as rich in species (or, more precisely,
that z, the rate of increase in species per unit area, is twice as high in tropical as
in temperate faunas) and are as well studied as those at higher latitudes, tropical
coastal zones should include about 195,000 total described species and 143,000
described species of macrobiota, given their area (Table 7-3). A review of data
and inferences in the literature suggests that the assumption of double area-
specific diversity in the tropics is realistic but may be conservative. Although
data often are not available on an area-specific scale, there are two to at least
three times more species in tropical than temperate environments for most
(though not all) groups of organisms (Angel, 1992; May, 1986a, 1988; Raven and
Wilson, 1992; Rex et al., 1993; Stevens, 1989; Stork, 1988). Also, because of the
assumption that the tropical coastal zone is as well studied as the global coastal
zone (which likely is not met), the values presented likely underestimate true
biodiversity in tropical coastal zones.
Similarly, using the above area relationships and assuming that the complex
coral reef substrate contains approximately twice as many species per unit area
(or, that z is twice as large) and is as well studied as level-bottom (sand, mud)
habitats in the same biogeographical region, there are about 93,000 described
species of all coral reef taxa and 68,000 species of described coral reef macrobiota
on Earth. Although Abele (1976) reports that 53 species of crustaceans occupy
coral habitat (P. damicornis) compared to 16 species in sandy beach habitats on
the Pacific coast of Panama, biodiversity in coarse- versus level-bottom marine
habitats probably needs to be more extensively quantified to document this
assumption. Thusly calculated, though, the total described species on coral
reefs represents only about 5% of the described global biota.
In contrast, rain forests may account for more than 70% of the described
global biota (Table 7-3). If 90% of currently described terrestrial species oc-
curred in rain forests (as do primates; Mittermeier, 1988) and if all groups were
as well known as primates, then rain forests would include about 1,305,000
described species. This yields an underestimate of the true number of species in
rain forests, however, since about two-thirds of currently described species
(mostly insects) are thought to occur in temperate regions (due to more intensive
study there), and there probably are two undescribed species of tropical insects
for every described species of temperate insect (May, 1986a, 1988). Other esti-
mates, incorporating the high probability that large numbers of undescribed

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TABLE 7-3 Calculated and Expected Species Diversity on Global Coral Reefs
for all Taxa and Macrobiota
Number of % of Total
Described Species Described Species
Organisms (to nearest 1,000) (@ 1.87 million)

Total Described Marine Speciesa 274,000 14.7

Macroscopic Described Marine Speciesa 200,000 10.7
Animals 193,000 10.3
Algae 4,000-8,000 0.2-0.4
Total Described Coastal Species
(if 80% of all marine species
are coastal) 219,000 11.7
Macroscopic Described Coastal Species
(if 80% of macroscopic
marine animals and most marine
macroalgae are coastal) 160,000 8.6
Animals 154,000 8.2
Algae 4,000-8,000 0.2-0.4
Total Described Tropical Coastal Species
(if communities in the tropical
coastal zone are as well studied
and twice as diverse as those at
higher latitudes; tropical coastal
zone=24% of global coastal zone b) 195,000 10.4
Macroscopic Described Tropical Coastal Species
(same assumptions) 143,000 7.6
Animals 138,000 7.4
Algae 3,000-7,000 0.2-0.4
Total Described Coral Reef Species
(if reef communities are as well
studied and twice as diverse as
those on nonreef level bottoms;
coral reefs=6% of tropical coastal
zonec) 93,000 5.0
Macroscopic Described Coral Reef Species
(same assumptions) 68,000 3.6
Animals 66,000 3.5
Algae 2,000-3,000 0.1-0.2
Global Rain Forest Species
(1) if 90% of all currently
described terrestrial speciesa
live in rain forests 1,305,000 72.5
(2) independent conservative
estimate of described and
undescribed species in rain
forests (see text) 2,000,000 —
(3) potential number of described
and undescribed species in rain
forests (see text) 20,000,000 —

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GLOBAL BIODIVERSITY OF CORAL REEFS / 93

TABLE 7-3 Continued

Number of % of Total
Described Species Described Species
Organisms (to nearest 1,000) (@ 1.87 million)

Expected Global Coral Reef Species

(if coral reefs are as diverse
and as well studied as rain
forests; global coral reefs=5%
of the area of global rain
forestsd):
From (1) above 618,000 34.3
From (2) above 948,000 —
From (3) above 9,477,000 —

aFrom Table 7-2.

bS=cAz; S=number of species obtained empirically from the number of described marine and
coastal species above; z=0.265 and 0.133 for species in tropical and high latitudes, respectively;
A=area known from Table 7-1; and c is provided by solution of the equation.
c S=cAz; A is known from Table 7-1; z=0.265 and 0.133 for reef and level-bottom tropical coastal

habitats, respectively; c is determined aboveb, and S is provided by solution of the equation.

dS=cAz; A is known from Table 7-1 for rain forests and coral reefs; S is known and c is calculated

for rain forests; z=0.25 for rain forests and coral reefs; c is the same as for rain forests and S is
calculated for coral reefs.

species occur in tropical rain forests, indicate that rain forests likely contain 2 to
>20 million species (Ehrlich and Wilson, 1991; Wilson, 1989). Two million spe-
cies will be used as a conservative estimate of species in rain forests hereafter.
Although rain forests cover 20 times more global surface area than coral reefs
(Table 7-1), and thus one would expect fewer species on global coral reefs than
rain forests, the calculated number of described species on coral reefs (93,000)
still is extraordinarily low.
Based on the area of the globe that they occupy compared to that of rain
forests, coral reefs should be comprised of about 600,000-950,000 total species
(34-53% of currently described global species; Table 7-3), assuming that rain
forests have 1-2 million species, that the two environments are equally studied,
and that similar ecological and evolutionary processes operate on coral reefs as
in rain forests (i.e., coral reefs would have the same biodiversity as rain forests
if they occupied equal global area). If rain forests included 10 million species
and coral reefs had equivalent area-specific diversity, coral reefs would contain
4,739,000 species; and if 20 million species existed in rain forests, coral reefs
would contain more than 9 million species (Table 7-3). The true number of
species on global coral reefs probably is at least 950,000, because 2 million spe-
cies in rain forests is likely to be a conservative figure.

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EVALUATION OF THE RESULTS AND THEIR IMPLICATIONS

The difference between the figures for described species on global coral reefs
(93,000 for all species and 68,000 for macrobiota) versus expected total species on
global coral reefs (at least 950,000) suggests two hypotheses: (1) only about 10%
of all species on reefs have been studied and described, or conversely, that ≥90%
of the species on the world’s coral reefs remain undiscovered (note that these
calculations are based on conservative figures for the number of species in rain
forests, so that the expected number of species on coral reefs may be larger and
the proportion of described species lower on coral reefs [especially for microor-
ganisms] than is represented here); (2) alternatively, the assumption that similar
ecological and evolutionary processes generate and maintain diversity in coral
reef and rain forest communities may be incorrect, and coral reefs indeed may
have lower area-specific diversity than rain forests due to biological or historical
constraints that affect diversification or extinction.
Several lines of evidence suggest that the first rather than the second hy-
pothesis is correct. High numbers of undocumented species are likely in coral
reef environments because, being far from the location of most systematists and
biologists, tropical environments are less studied than those in temperate lati-
tudes (Diamond, 1989; Erwin, 1988; Gaston and May, 1992; May, 1994; Wilson,
1985, 1988). For example, 80% of ecological researchers and 80% of insect
taxonomists are based in North America and Europe, in contrast to 7% in Latin
America and tropical Africa, and about 78% of borrowed botanical specimens
go to North American and European institutions compared to those in the
Neotropics or African tropics (Gaston and May, 1992). Tropical marine environ-
ments provide even further barriers to study because they require scuba diving
and fairly extensive logistic support for investigation.
In addition, as Gaston and May (1992) have shown, both the number of
taxonomists and the level of scientific effort devoted to the systematics of
“other” invertebrates (crustaceans, molluscs, echinoderms, cnidarians, sponges,
and helminths, most of which are marine) is 2 orders of magnitude less than that
devoted to the systematics of tetrapod vertebrates and 1 order of magnitude less
than that devoted to plants. These authors also document the aging of the work
force (see also Feldmann and Manning, 1992; Manning, 1991). The small num-
bers within this aging but dedicated and productive cadre of marine system-
atists are particularly alarming at a time when technological advances and steady
progression of knowledge about marine diversity is bearing spectacular fruit.
For example, two new phyla of marine invertebrates, the Loricifera (small
worm-like organisms that live between sand grains) and the Vestimentifera (large
tube-dwelling worms without a mouth or intestine but a large proboscis-like
structure that contains millions of symbiotic bacteria) were described from soft
sediments and hydrothermal vents, respectively, as recently as 1983 and 1985
(Grassle, 1986; Raven and Wilson, 1992). Since the communities associated with

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GLOBAL BIODIVERSITY OF CORAL REEFS / 95

hydrothermal vents were first discovered in 1977, more than 20 new families or
subfamilies, 50 new genera, and over 100 species have been described (Grassle,
1989). One of the largest species of sharks, the megamouth, was described within
a new family as recently as 1976 (Raven and Wilson, 1992).
Recent systematic studies indicate that concealed sibling species (morpho-
logically similar and previously classified within one species) are more common
in marine taxa than previously thought. Even in large commercially important
decapods, 18 distinct new species were recognized within 2 previous species of
deep-dwelling crabs (Feldmann and Manning, 1992). One of the commonest and
most important species of reef-building corals in the relatively well-known Car-
ibbean region (Montastrea annularis) recently was found to consist of 4 species
(Knowlton et al., 1992). Despite only slight morphological differences, non-
overlapping biochemical characteristics (coincident with differences in life his-
tory) clearly distinguished 6 sibling species in a worm that is a well-known
indicator of pollution, Capitella capitata (Grassle and Grassle, 1976). Recently
established specific differences between the endangered Kemp’s ridley sea turtle
and the widespread olive ridley (Bowen et al., 1991) demonstrate the lack of
systematic effort that has been devoted to marine organisms as well as the im-
portance of systematics in conservation and management issues.
As recently as 1992, researchers discovered in the marine plankton a major
new archaebacterial group in which genetic relationships to their nearest rela-

Smithsonian Tropical Research Institute marine station in the San Blas Islands, Panama.

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96 / BIODIVERSITY II

tives (microorganisms in hot springs) are as distant as those between plants and
animals (Fuhrman et al., 1992). Similarly, scientists discovered only in the 1980s
that photosynthetic marine picoplankton, too small to have been detected previ-
ously, are extremely abundant and account for a significant proportion of global
primary productivity. In 1988, Chisholm et al. described a new group of these
picoplankton that are free-living relatives of Prochloron, the hypothesized an-
cestor of chloroplasts in higher plants. As recently as 1989, newly discovered
marine viruses (bacteriophages) were found to be so abundant that one-third of
the marine bacterial population could experience a phage attack each day (Bergh
et al., 1989).
Further evidence that large numbers of species on coral reefs remain undis-
covered comes from the fact that the percentages of described species (about
10%) generated in the above calculations (Table 7-3) are in the same general
range as those found for other relatively little studied or tropical groups in which
the number of known versus unknown species were counted or estimated. For
example, calculation of the overall proportion of described versus unknown
species in the Systematics Agenda 2000 Technical Report (1994) shows that only
1-12% are thought to be described (this range represents the percentages ob-
tained when the minimum and maximum estimates of species remaining to be
discovered are summed for all groups, divided by the total known plus un-
known species, multiplied by 100, and this percentage substracted from 100%).
Tabulation of data for individual groups in the Systematics Agenda 2000 Techical
Report reveals that only 21% of global crustacean species and 26% of global
molluscan species have been described, although these taxa represent some of
the best-studied groups of marine invertebrates and are commercially impor-
tant. In other studies, Grassle and Maciolek (1992) found that 31% of the
peracarid crustaceans (mostly isopods and amphipods) had been described in
soft sediments from the deep sea off eastern North America. From shallower
sediments in southern Australia, however, Poore and Wilson (1993) reported
that only 10% of the relatively well-studied isopods were known; they suggest
that, due to great regional differences in the extent to which the oceans have
been studied, probably only 5% of marine invertebrates are known from the
oceans overall. About 36% of the species of polychaete worms and about 63%
of the relatively well-known molluscan species in Grassle and Maciolek’s (1992)
samples from the deep sea off North America had been described. About 17%
of the total species of algae have been described (John, 1994; Systematics Agenda
2000, 1994). Only 1%, 1-10%, 4-7%, and 2-3%, respectively, of the estimated
total species of the poorly studied viruses, bacteria, fungi, and nematodes are
described (Systematics Agenda 2000, 1994).
Among terrestrial organisms, only about 7-9% of the global species of spi-
ders and mites, and only about 9-11% of global species of insects have been
described (Systematics Agenda 2000, 1994), despite the fact that entomologists
who work on insects and spiders represent about 30% of taxonomists and these

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GLOBAL BIODIVERSITY OF CORAL REEFS / 97

large groups receive considerable taxonomic attention because of their economic

importance (Gaston and May, 1992). Estimates within taxa of insects (Gaston,
1991) indicate that 11-33% of beetles are described; only 10-13% of some beetle
families (e.g., the speciose staphilinids) have been described, but 25-50% of
others (pselaphids, curculionids, carabids, chrysomelids) are known. Up to half
of the flies and the large, relatively well-known butterflies and moths probably
have been described (but a much lower proportion of the small, more cryptic
microlepidopterans are known). Except for the bees (where about half of the
species are described), the proportions of described species in the major hy-
menopteran superfamilies (e.g., ichneumonoid and chalcidoid wasps, ants) are
lower, ranging from 17-25%. Similarly, in the hemipteran and some homopteran
(cicadellid) bugs, only 20-33% of the total species are described (although about
50% of the economically important coccoid Homoptera are known).
Thus, an estimate of 10% described species on global coral reefs is not un-
reasonable in terms of what is known of other (especially predominantly tropi-
cal) groups. This estimate is further considered realistic because all of the less
well-known marine groups are included in this total estimate for coral reefs, the
estimate encompasses some very poorly known regions (e.g., areas in the Indo-
West Pacific), and marine realms are still relatively little studied.
Additionally, although we tend to think of coral reef communities in terms
of their flamboyant fishes, large sessile organisms such as corals, and large col-
orful benthic invertebrates such as lobsters, most species on coral reefs are small
in body size, as shown in Figure 7-1 for reef-dwelling mantis shrimps. Indeed
most cryptic species on coral reefs are constrained to small body sizes by the
sizes of bioeroded holes in the reef, whose refuge they must obtain in order to
survive intense fish predation (Moran and Reaka, 1988; Reaka, 1985, 1986, 1987;
Reaka-Kudla, 1991; Wolf et al., 1983). Several authors (Hutchinson and
MacArthur, 1959; May, 1986b, 1988; Morse et al., 1985) have documented this
skewed size distribution, with vastly more small than large species, for almost
all groups of animals (but see Fenchel, 1993; May, 1994; and Stork, Chapter 5,
this volume; for the microbiota; i.e., those smaller than 1-5 mm).
Small organisms almost always are poorly observed and known (Gaston,
1991; May, 1978; Mayr, 1969) because they often live in cryptic or interstitial
environments. This is true in coral reefs as well, where my laboratory has re-
corded several hundred thousand small macroscopic (>5 mm) motile reef organ-
isms of 12 or more phyla living within holes and crevices in the upper 10 cm of
1 m2 of reef substrate (Moran and Reaka, 1988; Moran and Reaka-Kudla, 1990;
Reaka, 1985, 1987; Reaka-Kudla, 1991; also see other references on cryptofauna
given above). In addition to their cryptic habits, these motile organisms often
are crepuscular or nocturnal (and thus often are unobserved even by field biolo-
gists; Dominguez and Reaka, 1988). Collection of organisms from these three-
dimensional calcareous crypts is difficult and labor intensive, leading to their
strong underrepresentation in many ecological and systematic studies. Com-

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98 / BIODIVERSITY II

35

30

25
No. species

20

15

10 ▲
▲
▲
▲▲
▲▲
5 ▲ ▲ ▲▲
▲ ▲ ▲▲
▲ ▲ ▲▲
▲ ▲ ▲▲▲ ▲▲
▲▲ ▲ ▲ ▲ ▲▲ ▲
0
50 100 150 200 250 300 350 400
Body size (mm TL)

FIGURE 7-1 Size frequency distribution of all species of Atlanto-East Pacific mantis
shrimps (Stomatopoda, Crustacea). Closed triangles represent species with known abbre-
viated larval development, and open circles signify species with known long-distance
larval dispersal.

prising the greatest proportion of species on reefs, these cryptic invertebrates

are the ecological equivalents of insects in the rain forest, and they usually are
overlooked when the diversity of a coral reef is considered.
In addition to inadequate study of these species on local scales, the number
of small species is likely to be underestimated on a global scale because of their
restricted geographic distributions. One of the strongest correlations in marine
biology is the association between small body size of macroscopic marine ani-
mals and the production of only a few relatively large larvae that have abbrevi-
ated developmental times (where the brooded young either emerge from the
parent’s protection as relatively large juveniles or the parents produce large
larvae with short planktonic stages; both are characterized by short dispersal
and restricted geographic distributions; Hansen, 1978; Jablonski, 1986a;
Jablonski and Lutz, 1983; Reaka, 1980; Reaka and Manning, 1981, 1987;
Strathmann and Strathmann, 1982). In contrast, species that attain large body

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GLOBAL BIODIVERSITY OF CORAL REEFS / 99

sizes within their lineage commonly produce large numbers of small swimming
larvae that feed in the plankton for extended periods, resulting in broad geo-
graphic distributions.
Figure 7-2 shows that the body sizes of species of reef-dwelling mantis
shrimps are significantly correlated with the sizes of their geographic ranges
(Reaka, 1980). Fenchel (1993) has suggested that there may be fewer rather than
more species at the smallest end of the range of body sizes (1-5 mm), and that
these microscopic species have larger geographic ranges, larger population sizes,
and may be less vulnerable to extinction than the species just above this size (see
also May, 1986b, 1988, 1994; Stork, Chapter 5, this volume). The lack of eco-
logical and detailed systematic knowledge for most of these minute taxa, how-
ever, may obscure the number of species and the sizes of the geographic ranges,
and this argument does not affect the macrobiota (generally larger than 5-10
mm) discussed in the present study. Therefore, because most macroscopic spe-

FIGURE 7-2 The relationship between body size (maximum mm total body length) of
species and extent of the geographic range (number of 5 × 5° latitudinal × longitudinal
quadrants in which each species has been recorded) in world-wide lineages of coral-
dwelling mantis shrimps (Stomatopoda, Crustacea). Each species is signified by one da-
tum, and different symbols represent different taxonomic lineages. See Reaka (1980) for
different analyses in which body size of species correlated significantly with other mea-
sures of the size of the geographic range for species within and between lineages.

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100 / BIODIVERSITY II

cies are small (e.g., 10-50 mm) on

coral reefs and most small species
have relatively small geographic
ranges, poorly sampled areas (e.g.,
some areas of the Indo-West Pacific)
are very likely to contain undocu-
mented species with endemic distri-
butions that do not extend into bet-
ter sampled areas.
It seems highly likely, therefore,
that global coral reefs contain a very
large number of species that are
undescribed. Rapid environmental
degradation in coastal environments
thus is likely to place at risk great
amounts of genetic and species diver-
sity that we have not yet even dis-
covered.
On the other hand, if the ecological
and evolutionary processes that gov-
ern the diversity of coral reef com-
Coral with black band disease. munities differ from those operating
in rain forests, and if coral reefs truly
are less diverse per unit area than rain forests (the second hypothesis given in
the introduction to this section), the estimate of the number of species expected
on global coral reefs (≥950,000), and thus the percentage of unknown species on
coral reefs, would be too large.
Although much remains to be learned, considerable evidence suggests, in
contrast to the second hypothesis, that many ecological processes governing
local diversity in coral reef and rain forest communities are similar (Connell,
1978, 1979; Jackson, 1991; Ray and Grassle, 1991). Both reefs and rain forests
are continually exposed to disturbance (including predation), and species diver-
sity is maximized at intermediate intensities of these disruptions (Connell, 1978).
On larger scales, similar patterns of recruitment, life history and resource spe-
cializations, physical gradients, and other historical factors generate the extraor-
dinary adaptations and species richness seen in both environments (although
the specific combinations of these factors affecting diversity of reefs and rain
forests at any one time may vary; see Jackson, 1991; May, 1986b, 1988; Ray and
Grassle, 1991; Reaka, 1985, 1987; Reaka-Kudla, 1991; and Sebens, 1994, for ad-
ditional discussions of ecological processes affecting diversity in these environ-
ments). Further support for the idea that similar evolutionary processes govern
diversity in coral reefs and rain forests is provided by graphs that trace the
history of biodiversity in marine invertebrates, vascular plants, vertebrates, and

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GLOBAL BIODIVERSITY OF CORAL REEFS / 101

insects from the Paleozoic Era onward, showing parallel patterns over time
(Signor, 1994).
On the other hand, the overwhelming abundance of species of insects
(Erwin, 1982, 1988; May, 1978, 1988, 1994; Stork, 1988) and their Paleozoic
radiation (apparently even before the rise of the flowering plants)—accompa-
nied by relatively low extinction rates throughout their history and continuing
increases in diversification (Labandeira and Sepkoski, 1993)—suggests that
something (perhaps related to their small body size and its relationship to their
habitat; May, 1978, 1988) fosters exceptionally high diversity in this lineage of
terrestrial arthropods. It is probably still too early to know whether or not
similar high diversity might be found in comparably sized small marine inverte-
brates in structurally complex habitats if they were adequately studied.
To accommodate the perceived relatively low diversity of described marine
species versus the terrestrial biota, it has been suggested that the geographic
ranges of marine organisms are large, extinctions are unlikely, and diversifica-
tion (at least after the Cambrian radiation of major body plans) is relatively slow
because of the presence of a fluid medium. The aqueous medium is considered
to buffer local variations and promote long-distance dispersal, which in turn
allows recolonization of locally disturbed sites and connects distant populations
genetically (see Angel, 1992; Hutchinson, 1959; May, 1994; Norse, 1993; Pielou,
1979). The fact that relatively few marine extinctions have been observed
(Carlton et al., 1991) bolsters the opinion that marine organisms are at a rela-
tively low risk of extinction in the modern world compared to terrestrial spe-
cies. Indeed only 195 molluscs and crustaceans (0.2% of present described spe-
cies) compared to 229 vertebrates (0.5% of present described species) have been
certified as extinct since 1600 (Smith et al., 1993). The latter authors caution,
however, that figures of endangered and extinct species strongly reflect the
intensity of scientific study devoted to the group and thus should be applied
only to well-known groups such as vertebrates and palms.
It is true that dispersing larvae can swamp genetic differences among adja-
cent populations, retard rates of diversification, and confer resistance to extinc-
tion (Hansen, 1978; Jablonski 1986a,b, 1991; Jablonski and Lutz, 1983; Reaka
and Manning, 1981, 1987). However, the common inference that most marine
species have dispersing larvae and are at low risk of extinction relies on the most
conspicuous species in marine environments (e.g., some starfish, crustaceans,
molluscs, and fish), which are large in body size and hence produce large num-
bers of dispersing larvae and have large geographic ranges. This perception
ignores the fact that the greatest proportion of species within marine macro-
scopic lineages are small in body size and thus are likely to have relatively ab-
breviated larval development and small geographic ranges (Figures 7-1, 7-2).
These small, numerous species are relatively vulnerable to extinction.
Paleontological data show that, at normal background levels of extinction,
species with restricted geographic ranges are more susceptible to extinction than

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102 / BIODIVERSITY II

those with broader ranges (Hansen, 1978, 1980, 1982; Jablonski, 1980, 1982,
1986a,b, 1991; Scheltema, 1978; Valentine and Jablonski, 1983; Vermeij, 1987;
see also Reaka, 1980; Reaka and Manning, 1981, 1987). Vermeij (1993) and
Stanley (1986) did not find a correlation between small geographic range and
high rates of extinction in certain molluscs, but Stanley points out that species
with large geographic ranges can be fragmented by heavy predation into smaller
populations which then suffer high extinction, reducing the strength of the
correlation in some cases. Also, tropical species are particularly susceptible to
extinction, as evidenced by the striking demise of reef communities at each of
the major mass extinctions (Jablonski, 1991). The background rates of extinc-
tion for marine invertebrates (1-10% of species per million years, Jablonski,
1991) are vastly lower than the extinctions that potentially could result from
present-day environmental alterations (Diamond, 1989; Ehrlich and Wilson,
1991; Smith et al., 1993), and the long narrow coastlines of coral reefs are espe-
cially vulnerable to habitat degradation and fragmentation.
Therefore, this study proposes that undocumented diversity and—of par-
ticular importance at the present time—undocumented contemporary extinc-
tions are likely to be higher than we realize in marine environments because
there are many more relatively small, cryptic, and unstudied macroscopic spe-
cies in coral reef environments than generally recognized. Not only is it likely
that undocumented extinctions already have taken place, but the potential for
future extinction in macroscopic species on coral reefs is higher than generally
realized because of the preponderance of diminutive species with small geo-
graphic ranges in these environments.

CONCLUSIONS
These analyses suggest that about 93,000 total described species of all taxa
occur on coral reefs, which represents about 5% of the described global biota.
These numbers are considerably lower than the number of species that are esti-
mated to occur in rain forests. However, coral reefs occupy only 5% of the
global area of rain forests. If coral reefs were equivalently studied and con-
tained as much biodiversity as rain forests per km2, and if rain forests contained
2 million species, then coral reefs should include approximately 950,000 species.
The difference between the numbers of described (93,000) versus expected
(950,000) species suggests that coral reefs are repositories of very high undocu-
mented species diversity. Most species on coral reefs are relatively small and
cryptic, and difficult to observe and collect. This, in combination with the fact
that tropical environments and particularly tropical marine habitats receive less
study than those at higher latitudes or terrestrial sites, suggests that many coral
reef taxa are indeed very poorly known.
Furthermore, associated with their relatively small size and abbreviated lar-
val dispersal, most species on coral reefs are likely to have small geographic

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GLOBAL BIODIVERSITY OF CORAL REEFS / 103

ranges, rendering them vulnerable to extinction. Although coral reef communi-

ties do not achieve the phenomenal global diversities found in rain forests be-
cause of their smaller area, and although it remains unclear whether or not the
cryptic reef biota may rival the extraordinary diversity exhibited by insects per
unit area, this study suggests that coral reefs may contain far more species than
previously supposed (which is congruent with the elaborate specializations and
biological interactions found in reef communities), and that very large amounts
of this biodiversity may be lost due to human activities before they are even
discovered if appropriate scientific study and conservation measures are not
taken.

ACKNOWLEDGMENTS
I extend my greatest appreciation to Edward O. Wilson for his encourage-
ment and support throughout my professional career. His scholarship; his intui-
tive sense of the crucial, central issues of the field; and his personal integrity
and warmth have inspired a generation of naturalists. In addition, I thank Hector
Severeyn for his participation in gathering data during the early stages of this
work, David John and Rita Colwell for information on biodiversity in algae and
microbes, Joel Cracraft for the provision of a new reference, Mitchell Tartt for
another important reference and assistance during preparation of the manu-
script, and Donald Wilson for helpful comments on the manuscript. Dr. Paul
Mazzocchi, Dean of Life Sciences at the University of Maryland, devoted con-
siderable time, logistic, and financial support during development of the Inau-
gural Symposium of the Consortium for Systematics and Biodiversity and the
present volume, for all of which I am grateful.

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CHAPTER
8

Common Measures for Studies of

Biodiversity: Molecular Phylogeny in
the Eukaryotic Microbial World
MITCHELL L. SOGIN
Director, Program in Molecular Evolution

GREGORY HINKLE
Post-Doctoral Researcher, Marine Biological Laboratory,
Woods Hole, Massachusetts

Biodiversity is surveyed at many different levels using a broad array of

criteria. For many naturalists, richness in biodiversity is measured in terms of
the number of species of a given genus per m2. Others are more concerned with
the number of genera, classes, kingdoms, etc., within an ecosystem. Although
the fundamental concepts in systematic biology that underlie these studies are
well established, different properties are used to infer evolutionary relation-
ships for different kinds of organisms. Consequently, above the level of species,
equivalence among taxonomic ranks for fungi, plants, and animals is rather poor.
Within the microbial world, the assignment of taxa to a particular species is
generally meaningless. Accordingly, systematic descriptions of biodiversity can
be contentious, and sometimes are more appropriately described as forms of
political ecology. If systematic biologists and ecologists are to complete an in-
ventory of the taxosphere, its full importance will be appreciated only if a “com-
mon currency” can be established, one that will allow genetic diversity in one
group to be calibrated against that observed in any other evolutionary assem-
blage.
Systematic biology is the oldest of biological disciplines, yet it is a dynamic
field that periodically undergoes major change in response to novel ideas or new
technology. More than 100 years ago, Haeckel (1894) revolutionized taxonomy
by establishing the concept of phylogeny, while improvements in the micro-
scope paved the way to discovery of the microbiota. Today biologists employ
new methodologies to gain insights into evolutionary events that gave rise to
today’s biosphere. The use of “macromolecular sequences as documents of evo-
lutionary history” (Zuckerkandl and Pauling, 1965), coupled to advances in com-

109

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110 / BIODIVERSITY II

putational biology, rapidly have

transformed systematics and
hence studies of biodiversity
into experimental sciences.
Molecular techniques and
databases offer a means to sur-
vey and quantify biodiversity
through the acquisition, storage,
and comparison of linear se-
quences of amino acids and
nucleotides, the very fundamen-
Fungi: a highly diverse, but poorly known group. tals of life. The comparison of
genetic elements that have been
transmitted from generation to generation makes possible the measurement of
genetic differences between members of populations, species, and even between
kingdoms of organisms. Molecular data provide a practical metric for assessing
biodiversity and registering organisms in the same evolutionary framework in
which morphological and biochemical differences among organisms arose. Phy-
logenetic inferences generated from comparisons of homologous sequences of
nucleotides or amino acids provide more than simple dichotomous branching
topologies; they offer quantitative measures of phylogenetic depth and hence
information about antiquity of genetically distinct lineages. Although it seems
unlikely that field biologists ever will collect complete genome information, tools
for acquiring sequences for a limited number of genes that meet the criteria of
reliable evolutionary markers may one day go hand-in-hand with monoculars
and butterfly nets.
Nowhere has the impact of molecular approaches on systematics been more
significant than in the microbial world (Woese, 1967). In response to the failure
of more traditional taxonomic approaches (those based on comparisons of phe-
notypic characters), the microbiological research community has seized upon
molecular tools not only to reevaluate ideas about the composition of major
groups of organisms but also to probe for novel biodiversity (Pace et al., 1986).
In some cases, previously unknown microbial taxa may constitute significant
components of the community biomass (Fuhrman et al., 1993).
Sequence comparisons of the larger ribosomal RNAs (rRNAs) or their cod-
ing regions have gained widespread acceptance among microbial systematists
for inferring phylogenetic frameworks because these molecules are evolution-
arily homologous and functionally equivalent in all organisms, their sequence
changes sufficiently slowly to allow measurements of even the largest genea-
logical distances, and they do not undergo transfer between species (Sogin,
1989). Unlike small molecules such as the 5S rRNAs, the 16S-like rRNAs contain
a large number of variable sites (>1,400-2,000 positions) that provide large sets
of characters for phylogenetic inferences. Of equal importance to broad studies

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COMMON MEASURES FOR STUDIES OF BIODIVERSITY / 111

of biodiversity is the mosaic-like arrangement of genetic elements that display

different rates of evolutionary change within 16S-like rRNA (Sogin and
Gunderson, 1987). Regions with high rates of change are interspersed among
moderately conserved or nearly invariant domains. The genetic difference be-
tween even the most distantly related organisms can be estimated from compari-
sons of well-conserved regions of small subunit rRNAs, and yet rapidly evolv-
ing domains permit use of the very same genes to infer relationships between
species within the same genus.
Several thousand complete sequences of small subunit rRNAs that are de-
posited in public databases are curated by the Ribosomal RNA Database Project
(RDP) (Larsen et al., 1993). Unlike archival databases such as EMBL and
GenBank, the RDP collection of sequences is a dynamic data structure that main-
tains the aligned sequences required for phylogenetic inference. The explosive
growth in the number of sequences in the RDP mirrors the remarkable track
record of rRNA sequence comparisons as a molecular tool for inferring ancient
evolutionary history. More than any other molecule, small subunit rRNA offers
phylogenetic frameworks that are consistent with the biology of the representa-
tive taxa.
Comparisons of rRNA genes have exerted a profound influence on system-
atics and our understanding of early evolution. Unlike the standard “five king-
doms” (plants, animals, fungi, protists, and bacteria) (Whittaker, 1969) that are
presented in today’s textbooks, molecular studies define three primary lines of
descent (Eukarya, Bacteria, and Archaea) (Woese et al., 1990). The evolutionary
tree shown in Figure 8-1 is based on similarities in small subunit rRNAs and
hence can be regarded as a phylogenetic framework describing early events in
the history of life in this biosphere. Just within the eukaryotic subtree, there
are numerous revelations. For example, instead of being relatively recent inno-
vations, eukaryotes represent a lineage that may be as old as the archaebacterial
and eubacterial kingdoms (Sogin et al., 1989). The earliest diverging lineages
are represented by diplomonads, microsporidians, and trichomonads (Leipe et
al., 1993). These organisms lack many features characteristic of eukaryotic cells,
e.g., mitochondria, typical golgi, and complex cytoskeletons. The early lineages
are followed by a series of independent branches of protists, and then by the
“higher” kingdoms of fungi, plants, animals, and at least two additional com-
plex evolutionary assemblages, the stramenopiles and the alveolates.
The stramenopile assemblage includes diatoms, oomycetes, bicosoecids,
labyrinthulids, brown algae, and many chromophytes (exclusive of dinoflagel-
lates, cryptomonads, and haptophytes). Many of these species are photosyn-
thetic autotrophs containing plastids with chlorophylls a and c. At one time,
they were classified as eukaryotic algae along with rhodophytes (red algae),
chlorophytes (green algae most closely related to plants), and chromophytes (rec-
ognized today as a polyphyletic group containing similar plastid pigments).
Other stramenopiles are nonpigmented heterotrophs that feed on microorgan-

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112 / BIODIVERSITY II

FIGURE 8-1 An unrooted molecular phylogeny of eukaryotes. A computer-assisted

method was used to align the 16S-like rRNA sequences from 600 diverse eukaryotes.
Pairwise comparisons of all positions that could be aligned unambiguously were used to
compute values of structural similarity for all pairs of sequences. After conversion to
evolutionary distances using a Kimura correction, a Neighbor Joining tree was inferred
using the computer program PHYLIP. The length of segments indicates extent of mo-
lecular change. The scale bar represents 10 nucleotide changes per 100 positions.

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COMMON MEASURES FOR STUDIES OF BIODIVERSITY / 113

isms. They can be important inter-

mediates in the food chain, and bi-
cosoecids may be responsible for
consuming as much as 10% of the
marine prokaryotic biomass or pico-
plankton.
The alveolates include ciliates,
dinoflagellates, and apicomplexans
(Leipe et al., 1994; Patterson, 1989;
Patterson and Sogin, 1992). Ciliates
are defined by the presence of both
macro- and micronuclei and fre- Testate amoeba with pseudopods.
quently have many flagella. The
micronucleus harbors germline genetic information, while the macronucleus
contains “processed” DNA used by the cell’s transcription machinery. At one
time, ciliates were regarded as protists most closely related to animals. In con-
trast, dinoflagellates (including photosynthetic and nonphotosynthetic forms)
were thought to represent an eukaryotic lineage that diverged very early be-
cause of their unusual chromatin structure. Apicomplexans are united by an
ultrastructural feature described as the apical complex. Generally parasites of
mammalian species, apicomplexa cause such devastating diseases as malaria
or histoplasmosis. Molecular studies of rRNA and actin genes demonstrate
the phylogenetic affinity of apicomplexans, ciliates, and dinoflagellates
(Bhattacharya et al., 1991; Gajadhar et al., 1991). They are described as alveolates
because ciliates, dinoflagellates, and apicomplexans have alveoli (membranous,
spherical structures found at the flagellar base).
The nearly simultaneous separation of plants, fungi, animals, alveolates,
and stramenopiles (described as the eukaryotic “crown”) occurred approxi-
mately 1 billion years ago1. Although we are unable to resolve the exact branch-
ing sequence among the crown groups, it is now apparent that animals and
fungi shared a more recent common evolutionary history that excluded all other
eukaryotic groups (Wainright et al., 1993).
Glimpses of other important events in the evolution of eukaryotes are of-
fered by the detailed branching patterns within the crown groups. For ex-
ample, stramenopiles (see Figure 8-2A) include morphologically diverse organ-
isms with very different lifestyles. Yet all members of the group have flagella
with tripartite flagellar hairs that are not found in any other eukaryotes. The
flagellar hairs may have conferred a major ecological advantage for these organ-

1 This calibration is based on knowledge of the time of divergence for organisms that are well

preserved in the fossil record and by calculating the rate of change of nucleotides in their rRNAs.
Assuming a relatively constant incorporation of mutations—a “molecular clock”—we can estimate
when the crown groups first arose.

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114 / BIODIVERSITY II

FIGURE 8-2a Maximum likelihood phylogenetic inference for 16S-like rRNAs from
stramenopiles and outlying eukaryotes. The percentage of 110 bootstrap resamplings
that support topological elements in maximum likelihood inferences are shown. Branch
lengths represent relative evolutionary distances. The scale bar corresponds to 10 changes
per 100 positions. A bootstrap value of 82% lends some support to the notion of a close
relationship between alveolates and stramenopiles. Given the low bootstrap value for the
common branch that unites haptophytes, cryptomonads, and red algae, the relationship
among these outgroups is completely unresolved.

isms by allowing thrust reversal during swimming and thus enhanced ability to
entrap prey (Patterson, 1989).
Even more important to our understanding of eukaryotic history is the early
divergence of nonphotosynthetic taxa within the stramenopiles. Heterotrophs
including the slime net Labyrinthuloides minuta and the heterotrophic marine
flagellate Cafeteria roenbergensis diverged prior to the relatively late separation
of oomycetes from photosynthetic groups (Leipe et al., 1994). This branching
pattern affects how we interpret the evolution of plastids. The simplified phy-
logeny in Figure 8-2B summarizes our current understanding of the evolution of
stramenopiles. A heterotrophic protist with two flagella and tubular mitochon-

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COMMON MEASURES FOR STUDIES OF BIODIVERSITY / 115

drial cristae developed tripartite tubular hairs. This adaptive morphology gave
rise to the labyrinthulids, bicosoecids, and the oomycetes. The last common
ancestor of the stramenopile assemblage was probably a heterotrophic flagellate.
If true, autotrophy within the stramenopiles was independent of the other major
autotrophic assemblages: the green plants, cryptomonads, dinoflagellates, hapto-
phytes, and rhodophytes. Endosymbiotic origins of plastids in eukaryotes there-
fore must have occurred several times. At this time, we cannot distinguish
between multiple primary events involving cyanobacterial ancestors or a single
primary event followed by multiple secondary endosymbioses of heterotrophic
and phototrophic eukaryotes. In light of the emerging molecular data, the alter-
native hypothesis (independent loss of chloroplasts in bicosoecids, labyrinth-
ulids, oomycetes, and other heterotrophic stramenopiles) is no longer the most
parsimonious explanation for the distribution of photosynthetic phenotypes in
eukaryotic phylogenies.

FIGURE 8-2b Interpretive drawing of stramenopile evolution. The diagram is derived

from the rRNA framework. The last common ancestor to the crown groups was a bi-
flagellated heterotroph with tubular mitochondrial cristae. Areas of uncertainty (the
unresolved polytomy at the base of the eukaryotic crown and the relative branching
pattern of oomycetes, diatoms, and the remaining stramenochromes) are indicated by a
shaded square. The occurrence of chloroplasts with chlorophyll a and c is indicated by a
shaded circle at the taxon’s name. Other autotrophic groups are marked with an open
circle.

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116 / BIODIVERSITY II

In addition to identifying assemblages at the level of kingdoms, compari-

sons of rRNA genes have resolved relationships between nearly identical taxa.
Phylogenetic studies of the rRNAs from fungal symbionts of neotropical leaf-
cutting (tribe Attini) ants reveal a remarkable evolutionary story (Chapela et al.,
1994; Hinkle et al., 1994). The symbiotic relationship of attine ants with fungi
has allowed exploitation by the ants of a range of food resources that are not
otherwise available (Wilson, 1971). Because of a rich fossil record and numerous
morphological characters for cladistic analyses, relationships among attine ants
are well understood. In contrast, there has been much disagreement concerning
the phylogenetic affinities of the symbiotic attine fungi due to the general ab-
sence of useful morphological characters. Some investigators perceive attine
fungi as a polyphyletic group made up of both Ascomycotines and Basidio-
mycotines (Kermarrec et al., 1986; Weber 1966, 1972). Others argue that the
attine fungi are all closely related species (Cherrett et al., 1989). Because of these
uncertainties, many authors refer to all strains of attine fungi collectively as
Attamyces bromatificus (Cherrett et al., 1989) within the polyphyletic Fungi
Imperfecti. The rRNA phylogeny in Figure 8-3 clearly demonstrates that four of
the five taxa sampled represent distinct basidiomycete genera. Only the fungal
symbionts of Sericomyrmex and Trachymyrmex are sufficiently similar (two
nucleotide changes) to permit assignment within the same genus. More impor-
tant, the evolutionary relationships of the “higher” attine ants (Atta, Cyph-
omyrmex, Sericomyrmex, and Trachymyrmex) and their fungal symbionts are
entirely congruent. Although we are not able to resolve the branching order of
free-living Agaricus, Lepiota, and the fungal symbiont of Apterostigma, the con-
gruency of the trees for ants and fungi is evidence of stable coevolution over
millions of years. This observation prompts one to consider what the fate of one
of these ant lineages would be if an environmental insult were to cause the
fungal partner to become extinct; it is quite likely that such an event would lead
to loss of the ant lineage as well. In nature, there are many examples of symbio-
ses that involve animals or plants and physically distinct, yet metabolically in-
tegrated, fungal or microbial partners. In those cases where coevolution has
occurred over extended periods of time, preservation of biodiversity may re-
quire maintenance of both members of the partnership. Molecular systematics
offers a tool for assessing coevolution of symbiotically linked, but evolution-
arily distant taxa.
The value of the molecular databases extends beyond the inference of phy-
logenetic trees. Given the large collection of rRNA gene sequences, molecular
systematists can pinpoint taxonomic positions or phylotypes for organisms of
uncertain phylogenetic affinity. The gut symbionts of surgeonfish are just one
of many examples where traditional morphological criteria lead to the incorrect
taxonomic description of a microbe. Because of its enormous size (typically 80 ×
600 ), the surgeonfish symbiont Epulopiscium fishelsoni was originally described
as an unusual protist (Fishelson et al., 1985). Contrary evidence indicative of

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COMMON MEASURES FOR STUDIES OF BIODIVERSITY / 117

FIGURE 8-3 Distance matrix tree for homobasidiomycete fungi based on sequences of
16S-like rRNA genes and ant phylogeny based on parsimony analysis of morphological
data. The tree for fungal phylogeny was inferred from the comparison of positions that
can be aligned unambiguously in all sequences of full-length 16S-like rRNA genes that
have been reported for homobasidiomycetes. In this tree, distance matrices were used to
infer relationships for the fungal symbionts of attine ants and representatives of diverse
lineages of basidiomycetes. Mrakia frigida was used as the outgroup. The topology of
the phylogeny for attine ants is derived from a cladistic analysis of 44 morphological
characters in prepupal worker larvae from 51 species of attines (Schultz and Meier, 1995).
The topology of the phylogeny for the corresponding symbionts of the “higher” attine
ants and fungi is delineated with a thick line.

affinity to prokaryotes came from electron microscopical studies (Clements et

al., 1991). Instead of nuclei, the giant symbionts contain nucleoids with no hint
of surrounding membranes, similar to those of bacteria. Their flagella resemble
those of bacteria rather than the classic 9+2 microtubular structures found in
eukaryotic cilia. Gross morphology and ultrastructure presented two contradic-
tory phylogenetic hypotheses. When portions of the 16S rRNA genes of the
Euplopiscium symbiont were sequenced, the molecular data demonstrated in-

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118 / BIODIVERSITY II

controvertibly their phylogenetic affinity with the low g+c Gram positive
eubacteria (Angert et al., 1993). Carefully controlled in situ hybridizations with
fluorescent rRNA probes confirmed that the symbionts were the source of the
sequenced rRNA genes.
The discovery of prokaryotic giants forces biologists to reconsider one of
the dominant paradigms of microbial evolution and diversity. Size is a fre-
quently cited but incorrect criterion for differentiating eukaryotes and prokary-
otes. Although cell volumes in eukaryotes are typically 100- to 1,000-fold
greater than in prokaryotes, their size range overlaps. The chlorophyte Nano-
chlorum eukaryotum contains a mitochondrion, chloroplast, and a nucleus within
a 1-2 cell. Very long, skinny bacteria (>200 × 0.75 to 8.0 ) have been described
that contain nominal amounts of cytoplasm due to their spiral morphology or
presence of large liquid vacuoles. Since the 80 × 600 cell dimensions of prokary-
otic symbionts in surgeonfish are far greater than the examples cited above, the
theoretical constraints on cell size imposed by prokaryotic cell architecture and
apparent absence of intracellular vesicular transport are no longer credible.
Perceived size constraints for prokaryotes, and hence interpretations of
microfossils according to size, have dominated traditional hypotheses about the
evolutionary history of eukaryotes (Schopf and Oehler, 1976). The evolution of
large size is considered to be a consequence of the emergence of the most funda-
mental eukaryotic characters, the endomembrane system and cytoskeleton. The
absence of large cells from the fossil record predating 1.5 to 2.0 billion years ago
is taken as evidence for the more recent appearance of cells with nuclei. It now
becomes clear that the assignment of eukaryotic status to microfossils is strictly
an operational definition; the existence of small eukaryotes such as Nanochlorum
and the discovery of giant prokaryotes lacking cytoskeletons and a known ve-
sicular transport system raises suspicions about the phylogenetic significance of
size differences between eukaryotes and prokaryotes. This forces reexamina-
tion of the fossil record as it pertains to the evolutionary origins of eukaryotes.
Molecular data in the form of unanticipated diversity of rRNA sequences is con-
sistent with the interpretation that eukaryotic lineages diverged before 3.0 bil-
lion years ago (Sogin, 1991).
The radical departure of the bacterial symbionts in surgeonfish from normal
prokaryotic cell architecture underscores the likelihood of unknown diversity
among microorganisms that cannot be cultured in the laboratory. Molecular
methods now offer a window for viewing diversity in natural microbial popula-
tions. Polymerase chain reaction (PCR) methods permit the isolation of genes
that represent evolutionary homologues from natural populations (Pace et al.,
1986). As in the case of rRNA genes from the symbionts of surgeonfish, rRNA
genes isolated from natural populations of organisms can authenticate phyloge-
netic affinity and assess organismal diversity in natural populations. This can
be achieved without the requirement that the organism is isolated and cultured.
This molecular strategy for assessing microbial diversity has been used recently

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COMMON MEASURES FOR STUDIES OF BIODIVERSITY / 119

to characterize organisms from extreme environments as well as more mundane

ecosystems, including blue water open ocean. Both have dramatically extended
our knowledge and changed our perspective of microbial biodiversity.
Among the three primary domains of life, the Archaea (or archaebacteria)
are the least well-understood in terms of phylogenetic diversity and physiology.
Such “extremophiles” are difficult to isolate and propagate in the laboratory.
Barnes et al. (1994) used a combination of polymerase chain reaction (PCR) tech-
niques and rRNA sequence analysis to describe the enormous phylogenetic
depth of the Archaea present in the sediment from “Jim’s Black Pool,” a hot
spring in Yellowstone National Park. The difficulty in culturing the organisms
that thrive in boiling or near-boiling water with traditional techniques made
suspect any assessment of the microbial diversity in these extreme environments.
Using PCR techniques that forestall the need to culture organisms, Barnes et al.
discovered that the majority of the 98 16S-like rRNA clones they recovered were
from previously undescribed Archaeal species; the sequences of a significant
fraction of clones bore very little similarity to those from previously described
Archaea. The genetic distances estimated from comparison of the rRNA se-
quences are indicative of distant phylogenetic relationships. Thus, the physi-
ological variation within a group heretofore thought to be well circumscribed in
all likelihood is much greater than commonly believed. Since many of these
gene sequences were represented by single clones, it is highly unlikely that the
samples have exhaustively measured the diversity of even a simple 27 m 2 pool.
The potential usefulness of temperature-stable, biologically active products from
Archaea such as those sampled by Barnes and colleagues should be an incentive
for the identification and cataloging of the species comprising these unusual
communities.
While assessment of microbial diversity in extreme environments is a rela-
tively recent phenomenon, scientists have been studying the microbes living in
the open oceans for many years. Nevertheless, the general inability to culture
the majority (by some estimates 99%; Fuhrman et al., 1992) of the bacteria found
in the open ocean has left enormous gaps in our knowledge of marine biological
processes. Certain groups with easily identifiable characteristics, such as cyano-
bacteria and their photosynthetic pigments, are well known and have been the
subject of extensive study. More recently, however, the use of molecular tech-
niques has established the presence of entire groups of microorganisms that had
escaped detection by marine scientists who employed traditional methods.
Analyses of 16S-like rRNA genes that have been amplified randomly by
PCR from marine water samples by a number of investigators (DeLong, 1992;
Fuhrman et al., 1992, 1993; Schmidt et al., 1991) have demonstrated the pres-
ence of great numbers of novel organisms. Furthermore, the general absence of
duplicates in analyses of surface and deep water from the Pacific Ocean demon-
strates the absence of any dominant group of marine microorganisms, and hence
greater than anticipated microbial diversity. Since the evolutionary distance

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120 / BIODIVERSITY II

between these undescribed lineages and those of other well-studied groups is so

large, we must presume that they have evolved substantially different physiolo-
gies. Ecosystem models of marine processes based on preconceived notions of
the composition of marine microbial communities may be seriously in error
(Fuhrman et al., 1993).
Another surprise has been the discovery of marine archaebacteria in coastal
surface waters (DeLong, 1992) and at depths of up to 500 m (Fuhrman et al.,
1992) in environments that long have been thought to contain only bacteria
(eubacteria) and eukaryotes. Since archaebacteria generally thrive in extreme
environments (e.g., high temperature, low pH, high salt), there is now great
interest in learning how these organisms survive in the sea alongside eukaryotes
and bacteria. The discovery of archaebacteria throughout the upper layers of
the ocean is another example of how molecular techniques can perceive organ-
isms that somehow have escaped notice despite their general ubiquity and great
numbers. Taken together, the few studies to date that have quantified the di-
versity of marine microorganisms show that we know surprisingly little about
the majority of the organisms living in by far the largest environment on the
Earth. Comparisons of universally conserved homologous DNA sequences such
as 16S-like rRNA offer the opportunity to both quantify this diversity as well as
identify organisms with physiologies that are potentially of use to man.

ACKNOWLEDGMENTS
We are grateful for support from the G. Unger Vetleson Foundation and the
National Institutes of Health Grant GM32964.

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CHAPTER
9

The Rich Diversity of Biodiversity Issues

NORMAN MYERS
Visiting Fellow, Green College, Oxford University, Oxford, United Kingdom,
and Senior Fellow, World Wildlife Fund-US, Washington, D.C.

As the biodiversity question becomes more prominent among scientists and

the public, it becomes more challenging. It is turning out to be a rich complex
of interacting factors (did you ever hear that phrase applied to an ecosystem?).
In this chapter, we shall look at a selection of these issues.
While biodiversity, and indeed life itself, is the key characteristic of our
planet, we know more about the total numbers of atoms in the universe than
about Earth’s complement of species. We spend more on exploring distant plan-
ets than on documenting the abundance and variety of life here on Earth. Scien-
tific absurdity as this may be, taxonomists and systematists themselves are be-
coming an endangered entity. In fact, the one thing we know for certain about
biodiversity is that it is declining at ever faster rates.

HOTSPOTS REVISITED
Fortunately, we are learning that much biodiversity is located in small areas
of the planet. As much as 20% of species of plants and a still higher proportion
of species of animals are confined to 0.5% of Earth’s land surface. These species
are endemic to their areas, so if the local habitats are eliminated, these species
will suffer extinction. The areas in question are indeed threatened with immi-
nent habitat destruction. It is the two attributes together that cause the areas to
be designated “hotspots” (Myers, 1988, 1990a). The concept has been much
advanced in recent years. In some localities, it applies well, in others less so
(Bibby et al., 1992; Curnutt et al., 1994; Dinerstein and Wikramanayake, 1993).
From the start, the hotspots concept explicitly was not intended to apply much

125

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126 / BIODIVERSITY II

outside the tropics and subtropics, since species in temperate and boreal zones
tend to feature far less localised endemism than those from lower latitudes (cf.,
Prendergast et al., 1993). The hotspots thesis has underpinned the MacArthur
Foundation’s investment of $148 million in its biodiversity program during 1985-
1995, and it has featured prominently in the Global Environment Facility’s $335
million funding of biodiversity during the program’s first 3 years.
The hotspots approach has been limited largely so far to tropical forests and
Mediterranean-type zones. This is not to say that other tropical and subtropical
biomes do not qualify; they simply have not been subjected to much analysis for
hotspots. For example, coral reefs are likely to feature hotspots (see Reaka-
Kudla in Chapter 7, Thomas in Chapter 24). Something similar applies to certain
tropical lakes and wetlands, and we shall briefly review them here.

Tropical Lakes
A number of lake and river ecosystems are unusually rich in biodiversity.
World-wide lakes and rivers contain at least 8,400 species of fish, or roughly
40% of Earth’s species of fish that have been identified to date (and almost 20%
of all vertebrates). In turn, this means that these freshwater ecosystems support
almost one-quarter of the planet’s known biodiversity in less than 0.01% of the
planet’s water (Groombridge, 1992; Nelson, 1984).
At the same time, freshwater areas overall probably are being degraded and
eliminated globally at a rate faster than that of tropical forests, i.e., the fastest
rate in the world for extensive biomes, even though their expanse is but a small
part of that of tropical forests. In the United States, for instance, half of the 5.8
million km of rivers and streams are polluted to a significant degree, and 360,000
km have been channelized in the name of flood control, while 75,000 sizeable
dams block nearly every river outside Alaska, leaving only 2% of rivers free-
flowing (Carr, 1993; Palmer, 1994). As a result, 20% of species of fish, 36% of
crayfish, and 55% of mussels are endangered or have become extinct, by con-
trast with only 7% of the mammals and birds in the United States (Master, 1990;
Williams et al., 1993).
Much the same applies in other regions of the developed northern hemi-
sphere (Dynesius and Nilsson, 1994). Despite this downside assessment, fresh-
water ecosystems—wetlands too—receive little conservation attention compared
with tropical forests, coral reefs and Mediterranean-type regions (Greenwood,
1992; Stiassny and Raminosoa, 1994).
By virtue of their isolation, lakes often form “ecological islands.” In turn,
this situation can lead to a high degree of speciation and endemism, producing
exceptional biodiversity in terms of fish faunas, especially in the tropics (Lowe-
McConnell, 1993; Payne, 1986). Yet lakes generally do not feature large floras—
not, at least, so far as has been determined. But they may well feature sizeable
invertebrate faunas alongside the fish communities, presumably with parallel

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THE RICH DIVERSITY OF BIODIVERSITY ISSUES / 127

levels of endemism—though, again, all too little is known about this aspect of
their species richness. Note, however, that in Lake Baikal in Russia—with its
2,000+ species, of which 1,500 are endemic—there are 800 species of plants and
1,100 species of invertebrates to go with 50 species of fish (Brooks, 1950;
Kinystautas, 1987).
If we assume that the fish concentrations count as an “indicator” of unusual
biodiversity in other species categories as well, then three East African lakes
may well merit hotspot status. Moreover, many observers would urge conser-
vation for them on grounds of their remarkably speciose fish faunas alone, with
all that it implies for evolutionary radiation. That is to say, and as we shall see
below, there is a qualitative rationale for enhanced conservation beyond sheer
numbers of species.
Lakes Victoria, Tanganyika, and Malawi feature at least 1,167 identified
species of fish, with a true total of perhaps 1,450 species. Around 885 (76%) of
the known species are endemic. These “fish swarms” occur in approximately
121,500 km2, which means that 11% of Earth’s species of freshwater fish are
confined to 0.08% of Earth’s land surface (Barlow and Lisle, 1987; Keenleyside,
1991; Lowe-McConnell, 1993). Another two smaller lakes, Edward and George,
contain at least 60 endemic species. The evolution of these Rift Valley lakes has
produced a phenomenon of explosive speciation, generating exceedingly rich
fish communities with far greater differentiation than in any other tropical lakes.
Indeed the chain of lakes, encompassing some 775 endemic species of cichlid
fish (plus almost 100 other endemic species of fish), must be regarded as more
significant for the study of evolution than the Galapagos Islands (Echelle and
Kornfield, 1984; Greenwood, 1981). It even is considered that certain of the
cichlids can speciate in as little as 200 years (Greenwood, personal communica-
tion, 1995). However, the basic biology of the leading lake in the chain, Lake
Malawi, has yet to be elucidated, and there is next to no scientific program for
long-term research of a substantive and systematized sort.
Lake Malawi’s expanse—28,231 km2—contains at least 500 species of cich-
lids, 495 of them (99%) endemic, plus roughly 40 other species of fish, approxi-
mately 20 of them (50%) endemic (Tweddle, 1991). Each year a good number of
new species is discovered, which means that the true total could be rather higher
than the accepted figure (the same applies to the other two lakes). Indeed the
latest estimate (Greenwood, personal communication, 1995) suggests a total of
800 species of cichlids. Yet Lake Malawi is only one-eighth the size of North
America’s Great Lakes, which feature only 173 species of fish, fewer than 10 of
them endemic. Lake Malawi is suffering from sediment deposition due to soil
erosion in its watersheds, pollution from industrial installations and hinterland
agriculture, extensive overfishing, and proposed introduction of alien species.
In Lake Victoria’s 65,000 km2, there are—or rather there used to be—more
than 300 species of cichlids, around 130 (43%) of them endemic, plus almost 40
other species, some 20 of them (ca. 50%) endemic (Witte et al., 1992). On top of

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the speciocity of the lake’s fish flock, the evolutionary youth of the biota (the
lake is less than 750,000 years old) and its ecological diversity make the fish
community an unrivalled subject for comparative biology and evolutionary
study of vertebrates. Yet introduced predators, among other problems, already
have reduced the cichlid stock by 200 species (some 67%), and are likely to
reduce the endemics by 90% within another decade at most (Kaufman, 1992;
Lowe-McConnell, 1993; Witte et al, 1992). This must rank as the greatest ex-
tinction spasm of vertebrates in recent times.
As for Lake Tanganyika with its 28,399 km2, there are 172 species of cichlids
and 115 other species of fish, 220 of them (76%) endemic (Lowe-McConnell,
1993). The least rich lake in the chain, Lake Tanganyika nonetheless features
almost one-quarter more species of fish than Europe’s total of 192 species. (How-
ever, when one considers the invertebrates as well, the lake may turn out to be
the most species rich of the three; Coulter, 1991.) Fortunately, Lake Tanganyika
is subject to little pervasive degradation as yet, though there is much sediment
deposition from rivers draining eroded catchments, and there are plans for vari-
ous forms of disruptive development in the lake and its environs, notably oil
extraction.
Indeed, both Lake Malawi and Lake Tanganyika could rapidly follow the
impoverishing experience of Lake Victoria, unless there are precautionary con-
servation measures put in place ahead of time. To this extent, and on the basis
of their spectacular cichlid faunas alone, there is much scope for anticipatory (as
opposed to salvaging) conservation. It is likely that conservation of these lake
ecosystems would safeguard large numbers of species of invertebrates as well,
though the scale of this spinoff benefit is impossible to determine at this stage.
In sum, these three lakes probably feature some 1,450 species of fish, or
17% of the world’s 8,400 species of freshwater fish (and 48% of continental
Africa’s ca. 3,000 species of fish) in 0.08% of Earth’s land surface. Almost 900
known species (76% of the known species) are endemic. Apart from these three,
few other lakes could qualify even as subsidiary hotspot areas. The next two
candidates, Lake Atitlan in Guatemala and Lake Lanao in the Philippines, pos-
sess only a few dozen endemic species of fish each.

Tropical Wetlands
Wetlands are areas that contain, for part of the year at least, enough water
to foster the development of specialized communities of plants and animals
adapted to waterlogged conditions. They include marshes, fens, bogs, swales,
wet heaths and moorlands, peatlands, floodplains, deltas, and estuaries. Some of
these types of ecosystems are as different from one another as are forests and
savannahs (Dugan, 1993; Finlayson and Moser, 1991; Kusler et al., 1994; Mitsch
and Gosselink, 1993; Whigham et al., 1993; Williams, 1991). Many dense hu-
man communities live in or near wetlands, and they traditionally have sought to

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THE RICH DIVERSITY OF BIODIVERSITY ISSUES / 129

drain or otherwise modify wetlands

in order to make them better suited
to human needs. As a result, we
have lost half the world’s wetlands
during the course of this century. In
the year 1800, there were 80,000 km2
of wetlands in the “lower 48” United
States, but by 1975 there remained
less than half that much, and today
an additional 1,800 km2 are drained
and filled each year (Groombridge,
1992; see also Tiner, 1984). In Asia,
more than 5,000 km2 of wetlands are
lost each year to agriculture, irriga-
tion, dam construction, and the like.
With 8.5 million km2 or almost
6% of Earth’s land surface (roughly
the same as the expanse of tropical
forests or the United States), wet-
lands include such areas as the
Pantanal Swamp in Brazil, the Sudd
Swamp in Sudan, the Usumacinta Disappearing wetlands threaten wading
Delta in Mexico, the Okavango bird populations.
Swamp in Botswana, the inner Niger
Delta in Mali, the Kafue Flats in Zambia, the Indus Delta in Pakistan, and the
Sundarbans in Bangladesh. They are unusually rich in both plant and animal
life—though, while there are lots of data on mammals and birds, there is all too
little information on other vertebrates, let alone invertebrates. Of the United
States and Canada’s 17,000 species of plants, almost 4,700 are aquatic species
and another 2,000 are associated with wetlands. North American wetlands, com-
prising 8% of the land area, feature 39% of the region’s species of plants.
Regrettably, we do not know much about endemism—a key factor in
hotspots—in wetlands. Because wetland areas within one country or region
often are interconnected by virtue of their aquatic continuum, there may not be
much endemism. The global situation in this respect remains almost entirely
undocumented.
An area with prime potential to rank as a wetlands hotspot is the Pantanal
Swamp. It is the largest wetland in South America and perhaps in the world,
with almost 130,000 km2 (an area similar to that of Illinois). Four-fifths of its
expanse are in Brazil, other sectors being in Paraguay and Bolivia (Alho et al.,
1988; Mittermeier et al., 1987). Consisting mostly of the low-lying (100 m alti-
tude) floodplain of the River Paraguai and several tributary rivers, and inter-
spersed with various types of mesic to dry forest, savannah and grassland, the

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130 / BIODIVERSITY II

area is the most important in South America for waterfowl. Well over 500 spe-
cies of plants are reported from the Pantanal Swamp. Little is known concern-
ing vertebrates, let alone invertebrates, and there is little documentation of ende-
mism. One reasonably can assume that the species complement is sizeable, and
that endemism is moderate.
The area has been disturbed since the early 1970s by agricultural encroach-
ment (some ranches exceed 1,000 km2), plus a good deal of deforestation, dam
construction, and mining and industrial installations. The water stocks have
been contaminated by chemicals from agriculture, mining and industry. There
is also a growing problem with fires, commercial overfishing, and poaching for
wildlife products (e.g., caiman skins) and the live-animal trade. In short, a
largescale biota is being progressively depleted. The Brazilian government has
placed less than 1,500 km 2, hardly 1%, under protected status, and this seems to
be theoretical protection for the most part.
Another notable wetland area is the Sudd Swamp on the River Nile in south-
ern Sudan. In fact, it comprises a series of large swamps enclosing several sub-
stantial lakes, making up a present expanse of 16,500 km2 of permanently
flooded lands and an additional 15,000 km2 of seasonally flooded lands. There
are at least 500 species of plants, of which only 100 or so occur in the central
sector that is permanently flooded and features 7,000 km 2 of a monoculture of
papyrus, but only one such species is known to be endemic. Over 500 species of
birds have been recorded, and just under 100 species of fish. The area also
supports 400,000 people and 800,000 cattle (Carp, 1988; Cobb, 1983; Dryver and
Marchand, 1985; Howell et al., 1988; Moghraby and Sammani, 1985).
Much of the biota is threatened by the Jonglei Canal, a 360 km conduit that
would cause much of the Nile’s water to bypass the Sudd, reducing the perma-
nent swamps by 21-25% and the floodplains by 15-17% compared to the late
1980s. A fully operational canal could well cause the Nile to decline to the level
characteristic of the early 1950s, whereupon there would be an 80% reduction
in the expanse of the swamp and a 58% loss of floodplains, hence entraining all
manner of adverse repercussions for the biota. As it happens, the construction
of the canal has been suspended since 1983, due to political, technical, and fi-
nancial factors—mainly the civil war that persists in southern Sudan.
This summary account of two prime wetland areas indicates that there is
substantial biodiversity at stake there. At the same time, this review, like that
of the three East African lakes, shows that, while certain areas may contain
unusual concentrations of biodiversity facing unusual threat, they cannot
qualify as other than second-order hotspots because their stocks of species
hardly compare with those of hotspot areas in tropical forests, coral reefs, and
Mediterranean-type zones, especially as concerns endemism. The poorest tropi-
cal forest hotspots are the southwestern Ivory Coast, with 2,770 species of
plants, 200 of them (7%) endemic, in an area of 4,000 km2 of primary forest; and
southwestern Sri Lanka, with some 1,000 species of plants, 500 of them (50%)

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THE RICH DIVERSITY OF BIODIVERSITY ISSUES / 131

endemic, in 700 km2 of primary forest. Nonetheless, tropical wetlands and cer-
tain lakes are generally richer, at least in particular categories of species, than
any other terrestrial sectors except the three biomes cited.

OTHER CATEGORIES OF BIODIVERSITY

Biodiversity occurs not only at the level of species, but embraces both spe-
cies subunits and ecosystems. Consider species populations. If, as is likely, an
average species comprises hundreds of genetically distinct populations, there
are billions of such populations world-wide (Ehrlich and Daily, 1993). Because
of their ecological differentiation, some populations will be better equipped than
others to adapt to the swiftly changing environmental conditions of the foresee-
able future. We may well find that, if the depletion of biodiversity continues
unabated, we shall lose, say, 50% of all species, and many if not most of the
surviving species will have lost, say, 90% of their populations and perhaps 50%
of their genetic variability. This latter outcome is all the more probable insofar
as human-induced attrition of populations’ habitats tends to occur around the
fringes of populations’ ranges—precisely the sectors that often feature the great-
est genetic variability insofar as it is here that populations encounter the great-
est variety of environmental conditions. Given this prognosis, we might well
ask a key question: which form of biodepletion (species, populations, genetic
variability) eventually will induce the more adverse biospheric repercussions?
To illustrate the point of population depletion, consider the case of wheat.
In 1994, the species flourished across an expanse of 232 million hectares, featur-
ing a rough average of 2 million stalks per hectare. This means that the total
number of individuals in 1994 exceeded 450 trillion, probably a record (Myers,
1995). As a species, then, wheat is the opposite of endangered. But because of
a protracted breeding trend toward genetic uniformity, wheat has lost the great
bulk of its populations and most of its genetic variability. In extensive sectors
of the original range of wheat, wild strains have all but disappeared, there is a
virtual “wipeout” of endemic genetic diversity. Of Greece’s native wheats, 95%
have become extinct; and, across Turkey, wild progenitors of wheat find sanc-
tuary from grazing animals only in graveyards and castle ruins. Collections of
wheat germplasm are viewed as quite inadequate (Damania, 1993; Knutson and
Stoner, 1989).

ARE EARTH’S BIOTAS STRESSED?

Let us now consider a further dimension of the biotic crisis that receives
next to no attention and that could markedly affect the eventual outcome. Cer-
tain biotic communities may be “stressed” following events of the late Pleis-
tocene, leaving them unduly prone to extinction. For want of a better term,
they may lack “ecological resilience” or “survival capacity” of a long-term sort.

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132 / BIODIVERSITY II

The evidence for this, such as it is, lies in the fact that a mini-mass extinc-
tion started to overtake Earth’s biotas during the late Pleistocene. After very
long periods of steadily growing biodiversity (Signor, 1990), there was a marked
decline starting some 30,000 years ago and continuing until about 1,000 years
ago. Whether through human overhunting or climatic change or both, the large
mammalian fauna of several entire regions—notably North and South America,
Oceania and Madagascar—lost more than 100 genera (including 70% of large
North American mammals; Martin and Klein, 1984). Following this spasm of
extinction, there has been continuing elimination of species of vertebrates (plus
some species of plants), albeit not on such a spectacular scale as the late-Pleis-
tocene episode, until the onset of the present mass extinction, which started
roughly in the middle of this century. These recent eliminations were due al-
most entirely to human activities. We have no idea how many associated spe-
cies—especially species of invertebrates—likewise have been lost, but they must
have been quite numerous.
So today’s biodiversity already was somewhat depauperate before the ar-
rival of the unprecedentedly severe human impact from around 1950 onwards.
Many surviving biotas surely have been affected adversely along the way, at
least through depletion of their subspecies and populations (Kauffman and
Walliser, 1990). Large numbers of species must have lost much of their genetic
variability, hence their ecological adaptability—leaving them the more vulner-
able to summary extinction.
In short, the present mass extinction may have had some of its origins in
events long past. It would be difficult indeed to determine how far today’s
biotas are not only impoverished but have been subject to stress in the manner
postulated. How should we define and document the stressing factors involved?
What criteria could we invoke to evaluate the processes at work, let alone their
present-day upshot? Thus far, the overall question has received scant research
attention, despite its possibly potent signficance for the capacity of today’s bio-
tas to resist extinction pressures.

CONSEQUENCES FOR EVOLUTION

The loss of large numbers of species, let alone species subunits, will be far
from the only outcome of the present biotic debacle, supposing it proceeds un-
checked. There is likely to be a significant disruption of certain basic processes
of evolution (Myers, 1985). The forces of natural selection and speciation can
work only with the “resource base” of species and subunits available (Eldredge,
1991; Raup, 1991)—and, as we have seen, this crucial base is being grossly re-
duced. To cite the graphic phrasing of Michael Soule and Bruce Wilcox (1980:8)
“Death is one thing; an end to birth is something else.” Given what we can
discern from the geologic record, the recovery period, i.e., the interval until
speciation capacities generate a stock of species to match today’s in abundance

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THE RICH DIVERSITY OF BIODIVERSITY ISSUES / 133

and variety, will be protracted. After the late Cretaceous crash, between 5 and
10 million years elapsed before there were bats in the skies and whales in the
seas. Following the mass extinction of the late Permian, when marine inverte-
brates lost roughly half their families, as many as 20 million years were needed
before the survivors could establish even half as many families as they had lost
(Jablonski, 1991).
The evolutionary outcome this time around could prove yet more drastic.
The critical factor lies with the likely loss of key environments. Not only do we
appear set to lose most if not virtually all tropical forests, but there is progres-
sive depletion of tropical coral reefs, wetlands, estuaries, and other biotopes
with exceptional abundance and diversity of species and with unusual complex-
ity of ecological workings. These environments have served in the past as pre-
eminent “powerhouses” of evolution, meaning they have thrown up more spe-
cies than other environments. Virtually every major group of vertebrates and
many other large categories of animals have originated in spacious zones with
warm, equable climates, notably the Old World tropics and especially their for-
ests (Darlington, 1957; Mayr, 1982). The rate of evolutionary diversification—
whether through proliferation of species or through emergence of major new
adaptations—has been greatest in the tropics, especially in tropical forests.
Tropical species, notably those in tropical forests, appear to persist for only
brief periods of geologic time, which implies a high rate of evolution (Jablonski,
1993; Stanley, 1991).
As extensive environments are eliminated wholesale, moreover, the current
mass extinction applies across most if not all major categories of species. The
outcome will contrast sharply with the end of the Cretaceous, when not only
placental mammals survived (leading to the adaptive radiation of mammals,
eventually including man), but also birds, amphibians, and crocodiles, among
many other nondinosaurian reptiles, persisted. In addition, the present extinc-
tion spasm is eliminating a large portion of terrestrial plant species world-wide,
by contrast with episodes of mass extinction in the prehistoric past, when ter-
restrial plants survived with relatively few losses in many parts of the world
(Knoll, 1984)—and thus supplied a resource base on which evolutionary pro-
cesses could start to generate replacement species of animals forthwith. If this
biotic substrate is markedly depleted within the foreseeable future, the restor-
ative capacities of evolution will be the more diminished.
All this will carry severe implications for human societies throughout the
recovery period, which is estimated to be a minimum of 5 million years, possibly
several times longer. Just 5 million years would be 20 times longer than human-
kind itself has been a species. The present generation is effectively imposing a
decision on the unconsulted behalf of at least 200,000 follow-on generations.
This must rank as the most far-reaching decision ever taken on behalf of such a
large number of people during the whole course of human history. Suppose
that Earth’s population maintains an average of 2.5 billion people during the

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134 / BIODIVERSITY II

next 5 million years (rather than the present 5.7 billion), and that the generation
time remains 25 years. The total number affected will amount to 500 trillion
people.

WHAT SHALL WE DO ABOUT IT ALL?

We are reaching a stage when there is less and less scope for protection of
biodiversity through the traditional strategy of parks and reserves. These pro-
tected areas total more than 8,000 units covering 7 million km2, or 5% of Earth’s
land surface (Western et al., 1994). True, there is great need for many more such
areas. Ecologists and biogeographers consider that, in tropical forests alone, we
should at least triple the expanse protected, while recognizing that one-third of
existing parks and reserves already are subject to agricultural encroachment
and other forms of human disruption (Groombridge, 1992). Additional forms of
degradation are likely to stem in the future from pollution: as much as 1 million
km2 or almost 15% of remaining tropical forests soon could become subject to
acid precipitation (Rodhe and Herrera, 1988). There eventually could be further
and more widespread degradation from enhanced UV-B radiation and global
warming (Gates, 1993; Peters and Lovejoy, 1992; Woodwell, 1990). We could
set aside the whole of Amazonia, declaring it one huge park, and then build a
fence around it 50 m high. That still would not prevent it from being depleted
through atmospheric pollution and climatic change.
This all means that protected areas are becoming far less of the sufficient
conservation response they once were considered to be. The time has arrived
when, as a bottom-line conclusion, we must recognize that we ultimately can
safeguard biodiversity only by safeguarding the biosphere as well—with all
that this entails for agriculture, industry, energy, and a host of other sectors,
especially the growth of both population and consumption (Myers, 1994). In-
creasingly too, it is apparent that we ultimately may find that we inhabit a
world where there are no more protected areas: either because they have been
overrun by landless peasants and grandscale pollution, or because we have
learned to manage all our landscapes in such a manner that there is automatic
provision for biodiversity (McNeely, 1990).
Let us conclude with a reflection on the Global Environment Facility, an
initiative that has provided $335 million over the program’s first 3 years to assist
biodiversity. This is quite the largest such dispensation ever made. But com-
pare it with what is at stake. Every year, just the commercial value to just the
rich nations of just the present array of plant-derived pharmaceuticals is 150
times greater (Principe, in press). More significant still, the world-wide amount
spent annually on “perverse” subsidies, i.e., subsidies that inadvertently foster
overloading of croplands, overgrazing of rangelands, profligate burning of fos-
sil fuels, wasteful use of water, overcutting of forests and overharvesting of
fisheries (to cite but a few examples of activities that also reduce biodiversity) is

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THE RICH DIVERSITY OF BIODIVERSITY ISSUES / 135

almost 20 times greater again. Note too that the shortfall in spending to support
those 120 million couples of the developing world who possess the motivation to
reduce their fertility but lack facilities for family planning, is $2.4 billion. If we
were to take care of these unmet needs—which should be catered on humanitar-
ian grounds even if there were no population problem at all—we would reduce
the ultimate total of the world’s population by at least 2 billion people
(Bongaarts, 1994) and massively reduce pressures on species’ habitats.

HOW LONG DO WE HAVE?

While formulating our responses to the mass extinction crisis, we need to
bear in mind the length of time still available to us. The critical criterion for our
efforts is not whether we are doing far more than before, but whether it will be
enough—and that in turn raises the question of “enough by when?” How soon
might we cross a threshold after which our best efforts could prove to be of little
avail?
Of course, not all habitats are going to be destroyed outright within the
immediate future. But that is hardly the point. What looks set to eliminate
many if not most species in the long run will be the “fragmentation effect,” i.e.,
the break up of extensive habitats into small isolated patches that are too small
to maintain their stocks of species into the indefinite future. This phenomenon
has been widely analysed through the theory of island biogeography, and ap-
pears to be strongly supported through abundant empirical evidence, albeit with
a good number of variations on the general theme. True, the process of ecologi-
cal equilibriation, with its delayed fall-out effects, will take an extended period
to exert its full depletive impact; in some instances, it will be decades and even
centuries before species eventually disappear. But the ultimate upshot, which is
what we should be primarily concerned with, will be the same.
Consider the environmental degradation that already has occurred.
Through dynamic inertia, it will continue to exert an increasingly adverse effect
for a good way into the future, no matter how vigorously we try to resist the
process: much potential damage is already “in the pipeline.” An obvious ex-
ample is acid rain, which will keep on inflicting injury on biotas by reason of
pollutants already deposited though not yet causing apparent harm. Similarly,
tropical forests will suffer desiccation through climatic changes induced by de-
forestation that already has taken place. Desertification will keep on expanding
its impact through built-in momentum. Ozone-destroying CFCs now in the at-
mosphere will continue their work for a whole century even if we were to cease
releasing them forthwith. There is enough global warming in store through past
emissions of greenhouse gases to cause significant climatic change no matter
how much we seek to slow it, let alone halt it.
In light of this on-going degradation of the biosphere, let us suppose, for
the sake of argument, that in the year 2000 the whole of humankind were to be

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136 / BIODIVERSITY II

removed from the face of the Earth in one fell swoop. Because of the many
environmental perturbations already imposed, with their impacts persisting for
many subsequent decades, gross biopheric impoverishment would continue and
thus serve to eliminate further large numbers of species in the long term (Myers,
1990b).
To consider a specific calculation, note Simberloff’s (1986) calculations as
concerns Amazonia. If deforestation continues at recent rates until the year
2000 (it is likely to accelerate in much of the region), but then halts completely,
we should anticipate an eventual loss of about 15% of the species of plants in
Amazonia. Were the forest cover to be ultimately reduced to those areas now
set aside as parks and reserves, we should anticipate that 66% of the species of
plants would disappear, together with almost 69% of the species of birds and
similar proportions of other major categories of animals.
As a result of the potential biodiversity depletion that humankind already
has engendered, it is realistic to prognose that there will be large numbers of
extinctions in a post-2000 world, even if it were relieved of humankind’s con-
tinuing disruptions. For sure, this is a highly pessimistic prognosis. The writer
is anxious to avoid undue doom and gloom: we must do all we can, while we
can, to limit the biotic debacle ahead. There is certainly a great deal that we still
can do to contain the ultimate catastrophe. But let us not delude ourselves into
supposing that there is plenty of time to make leisurely plans—“leisurely,” that
is, in light of the corner into which we already have painted ourselves, together
with millions of fellow species. Time is of the essence, and we should take a cool
look at how much manoeuvering room is left to us for response. Incisive and
urgent action is at a premium—which seems an appropriate point on which to
end this chapter.

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CHAPTER
10

Human-Caused Extinction of Birds

DAVID W. STEADMAN
Curator of Birds, Florida Museum of Natural History,
University of Florida, Gainesville

Because they are so conspicuous and appealing to the human senses of sight
and sound, birds always have attracted more than their fair share of our zoologi-
cal attention. Almost by necessity, therefore, birds have played a prominent
role in our understanding of the processes by which species become rare, endan-
gered, and finally extinct. The resulting literature on avian conservation biol-
ogy has proliferated for decades and now is part of the information explosion,
with all of its benefits and frustrations.
Each year we read of additional species of birds whose existence no longer
can be demonstrated. One of the latest is the Colombian grebe, Podiceps andinus,
whose demise in highland Colombia is attributed to the loss of wetlands, the
introduction of exotic fish, and hunting (Fjeldsa, 1993). Declaring a species
extinct can be a tricky business (Diamond, 1987); the discovery of even one
living individual, regardless of the long-term viability of the species, refutes the
claim. In other words, negative evidence (such as finding no grebes) can be
refuted by even one bit of positive evidence (finding a grebe). To discover a few
living Colombian grebes, however, is unlikely to prevent extinction of the spe-
cies, given the vulnerability of very small populations to demographic stochas-
ticity (Caughley, 1994; Gabriel and Burger, 1992), catastrophes (Lande, 1993),
genetic viability (Lynch and Gabriel, 1990), and disease (Wilson et al., 1994).
Most species declared extinct by ornithologists never have been rediscov-
ered. One exception is the Cebu flowerpecker, Dicaeum quadricolor, endemic to
the Philippine island of Cebu (5,088 km2), where 8 of the 12 endemic subspecies
of birds already are gone (Dutson et al., 1993). Considered extinct since 1906,
up to four individuals of the Cebu flowerpecker were observed in 1992 and 1993

139

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140 / BIODIVERSITY II

in the last remaining patch (<2 km2) of closed canopy forest on the entire island.
The prospect of long-term survival for the Cebu flowerpecker is remote, given
the scarcity of its habitat and its small population. Only 2 years after its redis-
covery, the Cebu flowerpecker may be gone for good.
This chapter discusses extinction, the final stage of endangerment. Extinc-
tion really is forever, in spite of what we are led to believe in dinosaur movies.
Extinction is occurring today at unprecedented rates across a broad range of
terrestrial and aquatic habitats (McNeely, 1992). Because species richness of
birds is so high in tropical forests, the single most prolific cause of endanger-
ment and extinction in birds (and many other groups of organisms) is the de-
struction of tropical forests (Phillips et al., 1994; Whitmore and Sayer, 1992;
Wilson, 1992). Deforestation and other types of habitat loss also deplete avian
communities in temperate (Willson et al., 1994; see Figure 10-1) and high lati-
tude areas, which typically have fewer species of birds to lose than tropical
areas.
We have no evidence that any of the species of birds now endangered or
that have gone extinct in recent millennia would be in their predicament if not
for human activity. While extinction does occur naturally, human impact has
increased rates of extinction by orders of magnitudes over background rates
(Steadman et al., 1991; Wilson, 1992), and therefore is the only significant cause
of our current “biodiversity crisis.”

FIGURE 10-1 An adult and three

downy chicks of the Least Bittern (Ixo-
brychus exilis) at Presque Isle State
Park, Pennsylvania. Like so many spe-
cies of birds, the Least Bittern is strictly
dependent upon wetlands, and there-
fore becomes rarer and more localized
as wetlands are lost to human activities.
Photo by Sam Stull.

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HUMAN-CAUSED EXTINCTION OF BIRDS / 141

BACKGROUND
A comprehensive attempt to set global conservation priorities for birds (i.e.,
to avoid further extinction) has been compiled by Bibby et al. (1992), who iden-
tify 2,609 species of birds (27% of all living species) with breeding ranges of less
than 50,000 km2, designating these as “restricted-range species” (RRS). Sets of
these species tend to occur together on islands or in well-defined areas of a
particular continental habitat, especially tropical or montane forests. An “en-
demic bird area” (EBA) is any place where two or more RRS are sympatric. The
221 EBAs each contain 2-67 RRS. Many of the EBAs correspond roughly or
rather exactly with centers of endemism in other organisms, such as vascular
plants, butterflies, amphibians, reptiles, or mammals. The total numbers of both
EBAs and RRS are about evenly divided between islands and continents. The
tropics have 76% of all EBAs and more than 90% of all RRS.
The data on EBAs and RRS provide a rough but informative idea of the
potential for extinction of birds in upcoming decades. For example, the country
with the most RRS is Indonesia (Table 10-1), where most islands are unpro-
tected. The EBA with the most RRS is the Solomon Islands, where none of the
land is officially protected (Table 10-2). Of the 10 EBAs with the most RRS, only
one has more than 15% of its land under protection. We are rapidly approach-
ing the point of no return for hundreds of species.
Humans cause the extinction of birds in four major ways: (1) direct preda-
tion; (2) the introduction of nonnative species; (3) the spread of disease; and (4)
habitat degradation or loss. Direct predation includes hunting (killing living
birds), gathering eggs, or removing nestlings for captive rearing. The introduc-

TABLE 10-1 Ten Countries With the Most Restricted-Range Species (RRS)
of Birds

Occurring Confined Threatened Number of

Country RRS RRS RRS EBAsa

Indonesia 411 339 95 24

Peru 216 106 51 18
Brazil 201 122 67 19
Colombia 189 61 51 14
Papua New Guinea 172 82 18 12
Ecuador 159 32 38 11
Venezuela 120 40 17 8
Philippines 111 106 36 9
Mexico 102 59 23 14
Solomon Islands 96 43 16 4

aEndemic bird areas.

SOURCE: Modified from Bibby et al. (1992:Appendix 2).

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142 / BIODIVERSITY II

TABLE 10-2 Ten Endemic Bird Areas (EBA) With the Most Restricted-Range
Species (RRS) of Birds

Occurring Confined Threatened Land Area % Land Area

EBAa RRS RRS RRS (103 km2) Protected

Pacific Islands, Indonesia

Solomon Islands 67 42 10 32 0
New Britain
and New Ireland 57 34 4 46 0-5
Tanimbar and associated
islands 46 23 10 5.6 0-5
Northern Moluccas 44 27 6 29 0
Central New Guinean 41 27 2 98 5-10
midmountains
Central America
Costa Rican and Panamanian
highlands 54 51 2 27 10-15
South America
Ecuadorian dry forests 51 44 14 57 5-10
Southeast Brazil 48 41 23 50 10-15
Tepuis 42 36 0 35 60-70
Western Andes of
Colombia and Ecuador 41 35 12 27 10-15

aUnder natural conditions, each of these EBAs is primarily tropical forest of some sort.
SOURCE: Modified from Bibby et al. (1992:Appendix 1).

tion of nonnative animals exposes indigenous birds to new predators, competi-

tors, parasites, or pathogens, and thus is related to categories (1) and (3). Habitat
degradation or loss can be direct (deforestation, draining wetlands, plowing
prairies, toxic pollution, etc.) or due to encroachment by nonnative plants (cat-
egory 2).
Much of our biodiversity crisis is due to human impact of recent centuries,
especially the past few decades. Cooperative research by archaeologists, geolo-
gists, and biologists has shown, however, that most plant and animal communi-
ties were not pristine in preindustrial times. Our skills with tools and fire have
set us apart from other animals for tens of millennia. All human societies, even
nonagricultural hunter-gatherers, have had various effects on their environment
(e.g., Betancourt and Van Devender, 1981; Burney, 1993; Diamond, 1992; Klein,
1992; Martin, 1990; Martin and Klein, 1984; Steadman, 1991). Hunting, fishing,
and gathering often focus on certain species or groups of species (Redford, 1992).
Agriculture affects natural ecosystems in more diverse ways, including modifi-
cations of landscape, soils, and water supply through deforestation, erosion,
channeling, flooding, draining, etc., as well as the elimination or propagation of
selected species of plants and animals.

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HUMAN-CAUSED EXTINCTION OF BIRDS / 143

An understanding of past plant and animal communities is important for

long-term estimates of community stability and change (Betancourt et al., 1990;
Webb et al., 1993), such as how thoroughly and rapidly ecosystems might re-
cover from disturbances. The responses of plants and animals to future climatic
changes will be compromised by human-caused habitat fragmentation (Peters,
1988). Some species may be unable to disperse across tracts of disturbed habitat.
When feasible, past distributions can aid in planning translocation programs,
with an overall goal of preserving species assemblages that at least approach
those of a less disturbed state.

CONTINENTS
The distinction between continents and islands is useful, although there is
a continuum in land area and isolation from small, remote oceanic islands, such

Barranca del Cobre, Chihuahua, Mexico. On level ground, corn is cultivated here by
the Tarahumara. The largest pine trees have been removed, resulting in the extinction of
the Imperial Woodpecker (Campephilus imperialis), a close relative of the Ivory-billed
Woodpecker (C. principalis), which is extinct in the United States and nearly so in its
only other locale, Cuba. Photograph by Virginia Carter Steadman.

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144 / BIODIVERSITY II

as Ascension or St. Helena, to large “continental” islands, such as Madagascar,

Borneo, or New Guinea, to a relatively small and isolated continent such as Aus-
tralia. Regardless, we now may be at a threshold where human-caused extinc-
tions of birds—heavily biased thus far toward species on islands (compare Tables
10-3 and 10-4)—will occur at comparable rates on continents. For example, the
number of threatened restricted-range species on continents compared to is-
lands is 247 versus 165 (Table 10-1) and 51 versus 32 (Table 10-2). The most
influential factor in this new trend is habitat loss, fueled by advances in human
technology and population pressure.
Another important factor in endangerment and extinction, much more spe-
cies-specific than habitat loss, is direct exploitation. This may take the form of
hunting (often for food; “gamebirds” such as waterfowl, currasows, guans,
chachalacas, pheasants, quail, grouse, pigeons, and doves are most affected) or
taking young as pets (raptors, parrots, and songbirds are the most exploited,
although many other types of birds are also taken; see chapters in Beissinger and
Snyder, 1992). The combination of habitat loss and direct exploitation has had
verifiable impacts on one or more species from virtually every family of birds.
Unlike on some islands (see next section), we know little about the prehis-
toric impact of people on birds on most continents. A partial exception is North
America, where people first arrived about 11,000 years ago (Haynes, 1992).
Between 20 and 40 species of birds became extinct at this time, probably be-
cause of ecological dependencies on the more than 40 species of ground sloths,
mammoths, mastodons, horses, tapirs, camels, and other large mammals that
died out across the continent (Steadman and Martin, 1984). If humans were
involved in the mammal extinctions (Martin, 1990), then they indirectly caused
the extinctions of the birds as well. Before the large mammal communities col-
lapsed, the carrion-feeding California condor lived as far away from California as
Texas, Florida, and New York (Emslie, 1987; Steadman and Miller, 1987). Most

TABLE 10-3 Minimum Estimates of Human-Caused

Extinction of Continental Birds since A.D. 1600

Continent Number of Species

North America 5-7

Central America 3
South America 3
Africa 1
Europe and temperate Asia 3-4
Tropical Asia 1
Australia 1
Total 17-20

SOURCES: Mountfort (1988) and herein.

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HUMAN-CAUSED EXTINCTION OF BIRDS / 145

TABLE 10-4 Minimum Estimates of Extinction of Island Birds

Number of Species
Region Prehistorica A.D. 1600-1899 A.D. 1900-1994

Pacific Ocean 90 28 23
Indonesiab 0 0 2
Indian Ocean 11 30 1
Philippinesb 0 0 1
Caribbean Sea 34 2 1
New Guinea and Melanesia 10 2 3
Atlantic Ocean 3 3 1
Mediterranean Sea 10 0 0
Total 158 65 32

aThe prehistoric category consists of species from prehistoric cultural contexts, and includes only

species already described. Many other prehistoric extinct species have been found but remain
undescribed. For each region, an even greater number of extinct species are undiscovered because
of incomplete archeological sampling.
bThere is no interpretable prehistoric record of birds from Indonesia or the Philippines.

SOURCES: Modified from Johnson and Stattersfield (1990) and Milberg and Tyrberg (1993).

other scavenging birds perished completely. In the next 10,000 years before the
arrival of Europeans, however, only two North American birds are known to
have become extinct: a flightless duck, Chendytes lawi, of the Pacific coast
(Guthrie, 1992; Morejohn, 1976) and a small turkey, Meleagris crassipes, from
the Southwest (Rea, 1980).
Bones from late prehistoric archaeological sites in North America document
birds such as the trumpeter swan, Mississippi kite, swallow-tailed kite, whoop-
ing crane, sandhill crane, long-billed curlew, great auk, Carolina parakeet, ivory-
billed woodpecker, common raven, and fish crow in localities well outside of
their modern ranges. While intertribal exchange of birds might account for
some of these range extensions, most seem to reflect former indigenous popula-
tions. Prehistoric hunting, trapping, and habitat modification, as well as natural
climatic change, may have caused these range contractions. It probably is no
coincidence that three of these same species (the great auk, Carolina parakeet,
ivory-billed woodpecker) are now extinct and the whooping crane is endan-
gered. Some birds, such as the California condor, bald eagle, and golden eagle,
were hunted for feathers, bones, or ceremonial purposes more than for food
(Bates et al., 1993; Emslie, 1981; Rea, 1983; Simons, 1983).
In the past 200 years, at least five species of North American birds have
been lost (great auk, Labrador duck, passenger pigeon, Carolina parakeet, ivory-
billed woodpecker). Each of these, except the woodpecker, represented a mono-
typic genus. Two other species, the Eskimo curlew and Bachman’s warbler, are
either extinct or virtually so. The California condor, whooping crane, red-

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146 / BIODIVERSITY II

cockaded woodpecker, black-headed vireo, golden-cheeked warbler, and

Kirtland’s warbler persist today only in dangerously small, localized popula-
tions. Without management, three of these species already would be extinct.
Even if no more habitat is lost, some of these last eight species are likely to
become extinct in the next 200 years, as may others that are known to be endan-
gered, in decline, or localized today (such as greater and lesser prairie chickens,
sage grouse, piping plover, bristle-thighed curlew, common nighthawk, red-
headed woodpecker, sedge wren, loggerhead shrike, California gnatcatcher, cer-
ulean warbler, and Henslow’s sparrow; reviewed in Ehrlich et al., 1992). Losing
20-25 species per millennium may seem slow to politicians and economists, but
is a devastatingly high rate of extinction from an evolutionary standpoint. We
have no evidence that speciation will offset any of these losses.
As serious as this potential situation seems, North American birds may be
facing much less extinction in the next century than avifaunas in many other
parts of the world, especially in the tropics. Each country or EBA listed in
Tables 10-1 and 10-2 is tropical. With its many social, economic, political, legal,
and ethical complexities (Rudel, 1993; Rush, 1991), tropical deforestation con-
tinues at rates far beyond sustained yield. Many tropical regions, especially
those that are mountainous or covered with swamp forests, remain poorly sur-
veyed for birds. In fact, it is often the case that regions are not surveyed until
after human disturbances (clearing for roads, airstrips, settlements, etc.) allow
access.
Long-term (decadal or more) ecological data are lacking for most tropical
localities. Where such data have been gathered, decreases in species richness
have been detected. At the San Antonio cloud forest in the western Andes of
Colombia, for example, the approximate number of species of forest birds de-
clined from 128 in 1911, to 104 in 1959, to 92 in 1989-1991 (Kattan et al., 1994).
Caused primarily by forest fragmentation, these “local extinctions” are steps
leading toward full extinction of species. Although all feeding guilds are in-
volved, large canopy frugivores and understory insectivores have lost the most
species at San Antonio.
Throughout the tropics, but perhaps especially in South America and
Melanesia, the extent of local, regional, and full extinction of birds is undocu-
mented for many species. This clearly justifies the call for more surveys (Kattan
et al., 1994). Many such surveys will be fascinating biologically but ultimately
futile for preventing extinction as long as so much habitat continues to be lost.
How personally frustrating it must be for scientists such as Gretton et al. (1993),
who determined that only 20-30 pairs of Gurney’s pitta (Pitta gurneyi) still exist,
yet territories of this colorful but secretive songbird are being lost each year to
deforestation in Thailand. The gap between scientific knowledge and conserva-
tion policy often is large. It may be safe to say that no single country on any
continent has preserved enough habitat to secure the long-term survival of its
current avifauna.

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HUMAN-CAUSED EXTINCTION OF BIRDS / 147

ISLANDS
The relatively small land areas of islands result in small populations of or-
ganisms that tend to be more vulnerable to extinction than those on continents
(Diamond, 1985). Of 108 species of birds known to have become extinct since
A.D. 1600, 97 (90%) lived on islands (Johnson and Stattersfield, 1990). By their
calculations (97 extinct versus 1,750 extant species on islands, 11 extinct versus
7,500 extant species on continents), the probability of extinction during the past
4 centuries has been about 40 times greater on islands than continents. Al-
though both 97 and 11 are underestimates, this ratio probably is more or less
valid.
The plight of island birds did not begin, however, in A.D. 1600. As summa-
rized in Table 10-4, even more human-caused extinctions already had occurred
on islands in prehistoric times (Milberg and Tyrberg, 1993; Steadman, 1995).
Because of how incompletely we have sampled the zooarchaeological record of
island birds thus far, the known prehistoric extinctions are a small fraction of
those that actually occurred. These losses seem to have been due to the same
processes that still exterminate species on islands today: predation by humans
and introduced species, nonnative pathogens, and habitat destruction (Collar
and Andrew, 1988; Kirch, 1983; Olson, 1977; Olson and James, 1982; Savidge,
1987; Steadman et al., 1984, 1990).
The losses of birds on oceanic islands consist of: (1) extinction (loss of all
populations of a species); (2) extirpation (loss of a species on an entire island,
with other population[s] surviving elsewhere); and (3) reduced population (loss
of individuals from a surviving population). The last two categories are steps
leading toward genuine extinction, which represents irreversible losses rather
than the short-term fluctuations in populations near continental source areas
that biogeographers often call “extinctions” when studying faunal turnover.
Research in the Galapagos Islands (Steadman et al., 1991), Hawaiian Islands
(James, 1987), and Tonga (Steadman, 1993) has shown that the natural (prehu-
man) rate of genuine extinction in island birds may be at least 2 orders of mag-
nitude less than the posthuman rate.
Nearly all islands in Oceania (Melanesia, Micronesia, and Polynesia; Figure
10-2) were inhabited prehistorically by humans (Irwin, 1992). Birds provided
fat, protein, bones, and feathers for the human colonists, who also cleared for-
ests, cultivated crops, and raised domesticated animals (Steadman, 1989). The
prehistoric extinction of Pacific island birds is known from studying bones from
archaeological sites. Micronesia is not as well studied as Polynesia, but seems to
differ only in details of taxonomy and chronology (Steadman and Intoh, 1994).
Although Melanesian islands also have lost a variety of seabirds and landbirds
(Balouet and Olson, 1989), a larger percentage of the indigenous avifauna sur-
vives on large Melanesian islands than on Polynesian or Micronesian islands, or
on small Melanesian islands. This may be due to the buffering effects that steep

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148 / BIODIVERSITY II

FIGURE 10-2 The Pacific Ocean, showing major island groups.

terrain, cold and wet montane climates, and human diseases have had on human
impact. As predicted from biogeographic theory (MacArthur and Wilson, 1967),
birds tend to be easier to extinguish on low, flat islands (which often are small)
than on high, steep islands (which often are large).
While Pacific islands have a well-earned reputation as the source of much
modern extinction of birds, most species of landbirds already were extinct when
Captain Cook opened the region to European influence 220 years ago. Lost were
as many as 2,000 species of birds, dominated by flightless rails, but also includ-
ing moas, petrels, prions, pelicans, ibises, herons, swans, geese, ducks, hawks,
eagles, megapodes, kagus, aptornithids, sandpipers, gulls, pigeons, doves, par-
rots, barn-owls, strigid owls, owlet-nightjars, and many types of passerines
(Milberg and Tyrberg, 1993; Steadman, 1995). Assuming that about 9,600-9,700
species of birds exist today (Monroe and Sibley, 1993; Sibley and Monroe, 1990),
the world avifauna would be about 20% richer in species had islands of the
Pacific remained unoccupied by humans.
In the Hawaiian Islands alone, at least 62 endemic species of birds have
become extinct since the arrival of Polynesians nearly 2,000 years ago (James
and Olson, 1991; Olson and James, 1991). As is true throughout Oceania, the
number of extinct species known from the Hawaiian Islands increases with each
new season of archaeological or paleontological field work. Most of the extinct
Hawaiian species were gone before the arrival of Europeans, including most
species within the spectacular endemic radiations of cardueline finches (the
Hawaiian “honeycreepers”) and flightless geese, ducks, ibises, and rails (James
et al., 1987; Olson and James, 1982, 1984). In New Zealand, at least 44 endemic
species of landbirds have become extinct in the past millennium, featuring many
endemic species of moas, waterfowl, hawks, rails, and passerines (Anderson,
1989; Holdaway, 1989; Worthy and Holdaway, 1993).

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HUMAN-CAUSED EXTINCTION OF BIRDS / 149

Outside of the Hawaiian Islands and New Zealand, prehistoric Polynesian

birds are known from the Marquesas Islands, Society Islands, Cook Islands,
Henderson Island, Easter Island, Samoa, Tonga, and Polynesian outliers in
Melanesia (Steadman, 1995). In these island groups, rails, pigeons, doves, and
parrots have undergone the most extinction. Rails have lost more species than
any other family. Most island rails, in the Pacific and elsewhere, were flightless
forest species rather than volant wetland or grassland species. Any Pacific is-
land with a relatively thorough prehistoric record of birds has yielded bones of
one or more endemic species of flightless or nearly flightless rails. The three
islands with the best fossil records (Ua Huka, Mangaia, and ‘Eua) each have
produced two to four endemic species of flightless rails; the records from even
these islands are incomplete. Two species of rails occur among only seven bones
of landbirds known from remote Easter Island (see below). If not for human
activities, at least 800 islands in Oceania probably would be inhabited today by
flightless rails. Assuming one to four endemic species per island, rails alone may
account for as many as 2,000 species of birds that would be alive today had
people not colonized Oceania. The only surviving flightless rails in the tropical
Pacific (east of New Guinea) are three species of Gallirallus (from Okinawa,
Guam, and Solomon Islands; Diamond, 1991), Nesoclopeus woodfordi of the
Solomon Islands (Hadden, 1981), and Porzana atra of Henderson Island (Graves,
1992). All except the last species is endangered. Just think of the possibilities
for studying comparative systematics, evolution, biogeography, ecology, and
behavior if hundreds or thousands of species of flightless rails still were alive.
Sadly, we have wiped out nearly everything, leaving only some bones from one
of nature’s most dramatic examples of adaptive radiation.
Seabird losses in Polynesia have been greatest for petrels and shearwaters,
although the distribution and population size of various albatrosses, storm-pe-
trels, tropicbirds, frigatebirds, boobies, gulls, and terns have been reduced as
well. Species nesting on or within the ground have been lost to predation from
nonnative mammals and erosion of topsoil associated with deforestation.
Abbott’s booby, now confined to Christmas Island in the eastern Indian Ocean,
once was widespread in the South Pacific (Figure 10-3). One island away from
extinction, Abbott’s booby is one of many examples of seabirds whose modern
breeding range is but a tiny fraction of what it once was.
The loss of native birds is more complete on remote Easter Island (160 km 2,
elevation 507 m) than on any other island of its size in Oceania. Although Easter
Island was forested at first human contact about 1500 years ago, deforestation
was virtually complete by about 550 years ago (Flenley et al., 1991). Small
samples of bird bones, associated with Polynesian artifacts 600-900 years old
(Steadman et al., 1994), show that Easter Island once sustained at least 22 species
of seabirds, including 12 tubenoses (albatrosses, fulmars, petrels, prions, shear-
waters, storm-petrels). Only 1 of the 22 species of seabirds still nests on Easter
Island itself, while 7 of them occur on one or two of its offshore islets. When

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150 / BIODIVERSITY II

FIGURE 10-3 Because so many spe-

cies and populations already are lost,
determining the natural distribution
of island birds depends on studying
bones. The tibiotarsi (A-D) and tarso-
metatarsi (E-H) of Abbott’s booby
Papasula abbotti are shown. A, C, E,
and G are modern specimens of P.
abbotti abbotti from Christmas Island,
Indian Ocean. B, D, F, and H are ar-
chaeological specimens of an extinct
subspecies from the Marquesas Is-
lands, P. abbotti costelloi. The Mar-
quesas Islands are 11,200 km east of
Christmas Island, the only remaining
breeding site for the species. Scale
bars=20 cm. Drawing by Virginia
Carter Steadman.

fully known, the prehistoric seabird fauna of Easter Island probably will exceed
30 species, more than any other Polynesian island. Bones also provide the only
evidence that indigenous landbirds once lived on Easter Island, these being 6
extinct endemic species (a heron, 2 rails, 2 parrots, and an owl).
On Ua Huka (78 km2, elevation 855 m), Marquesas Islands (Table 10-5), the
Hane archaeological site has yielded thousands of bird bones (Steadman, 1989,
1991). Eight of the 20 species of seabirds from the Hane site no longer nest on Ua
Huka or its tiny offshore islets. Most of the 12 other seabirds nest only on the
islets, not on Ua Huka itself. The most common landbirds from Hane are 6
species of pigeons and doves, only 1 of which survives on Ua Huka. One sub-
species of seabird and 8 species of landbirds from Hane are extinct.
The prehistoric exploitation of birds can be evaluated precisely at Tanga-
tatau Rockshelter (site MAN-44), Mangaia (52 km2, elevation 169 m), Cook Is-
lands (Kirch et al., 1992; Steadman and Kirch, 1990). The age of MAN-44 ranges
from about 1,000 years old (zones 1A-1B) to 200 years old (zone 17). The eight
extinct and five extirpated species of landbirds from MAN-44 are rails, sandpip-

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HUMAN-CAUSED EXTINCTION OF BIRDS / 151

TABLE 10-5 Resident Native Birds from Ua Huka, Marquesas Islands

Bones from Modern

Native Birds Hane Site Recorda

Seabirds
Shearwaters, Petrels
Puffinus pacificus x x
Puffinus nativitatis x —
Puffinus lherminieri x —
Bulweria cf. bulwerii x x
Pterodroma rostrata x —
Pterodroma cf. alba x —
Pterodroma small sp. x —
Storm-Petrels
Nesofregetta fuliginosa x x
Fregetta grallaria x —
Tropicbirds
Phaethon lepturus x x
Boobies
Sula sula x x
Sula leucogaster x x
Sula dactylatra x —
*Papasula abbottii costelloi x —
Frigatebirds
Fregata minor x x
Fregata ariel x x
Terns
Sterna lunata — x
Sterna fuscata x x
Anous stolidus x x
Anous minutus x x
Procelsterna cerulea — x
Gygis microrhyncha x x
Landbirds
Herons
Egretta sacra x x
Sandpipers
Prosobonia cf. cancellata x —
Rails
*Porzana new sp. x —
*Gallirallus new sp. x —
Pigeons, Doves
Gallicolumba rubescens x —
*Gallicolumba nui x —
*Ptilinopus mercierii x —
Ptilinopus dupetithouarsii x x
Ducula galeata x —
*Macropygia heana x —

continued

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TABLE 10-5 Continued

Bones from Modern

Native Birds Hane Site Recorda

Landbirds—continued
Parrots
Vini ultramarina x —
*Vini vidivici x —
*Vini sinotoi x —
Swifts
Collocalia ocista — x
Kingfishers
Halcyon godeffroyi x —
Monarch Flycatchers
*cf. Myiagra new sp. x —
Pomarea iphis — x
Warblers
Acrocephalus mendanae x x
Seabirds
Total species 20 14
Combined total species 22
Landbirds
Total species 15 5
Combined total species 18

*=extinct taxon.
aNineteenth or twentieth century specimen or sight record from Ua Huka or its off-

shore islets.
NOTE: Dashes indicate no record.
SOURCE: Modified from Steadman (1991).

ers, pigeons, doves, and parrots whose bones dominate zones 1-4 and decline
sharply by zone 5 (Table 10-6). Most species of indigenous landbirds are not
recorded above zones 5-7, which are approximately 700 to 500 years old. The
most common flightless rail, Porzana rua, is last recorded in zone 8. Two species
of doves are the only extinct/extirpated landbirds recorded above zone 8. Each
of the four surviving landbirds from MAN-44 (a duck, rail, kingfisher, and war-
bler) tolerates forest clearance. The bristle-thighed curlew (Numenius tahiti-
ensis), a rare shorebird that nests in Alaska, has been killed and eaten for centu-
ries on its Pacific island wintering areas (Table 10-6), where about 50% of the
adults become flightless during wing molt (Marks, 1993).
Because of its depauperate modern avifauna, the Kingdom of Tonga did not
qualify as an EBA in Bibby et al. (1992). Bones from caves on ‘Eua (85 km 2,
elevation 300 m) indicate, however, that at least 27 species of landbirds lived on
this Tongan island before the arrival of people about 3,000 years ago (Steadman,

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HUMAN-CAUSED EXTINCTION OF BIRDS / 153

TABLE 10-6 Bones of Landbirds from Tangatatau Rockshelter (site MAN-

44), Mangaia, Cook Islands, ranging from zone 1A (oldest) to 17 (youngest)
Zone
Native Birds 1A 1B 2-3 4 5-7 8 9-14 15 17 Total

Migratory Shorebirds
Plovers
Pluvialis dominica — — 2 — — — — — — 2
Curlews
Numenius tahitiensis 5 — 2 2 — — — 1 — 10
Native Landbirds
Ducks
Anas superciliosa — — 3 1 2 2 8 11 3 30
Rails
**Gallirallus ripleyi 10 5 12 16 1 — — — — 44
Porzana tabuensis — — 2 1 — 1 — 1 1 6
**Porzana rua 11 44 41 21 2 1 — — — 120
**Porzana new sp. — 2 1 1 — — — — — 4
**Porphyrio? new sp. — 1 — — — — — — — 1
Sandpipers
**Prosobonia new sp. 1 1 1 1 — — — — — 4
Pigeons, Doves
*Gallicolumba erythroptera 3 5 3 5 — — — — — 16
**Gallicolumba new sp. — — — — — — 7 1 3 11
**Gallicolumba nui 3 3 — 3 — — — — — 9
*Ptilinopus rarotongensis 1 4 4 2 — — — 1 — 12
*Ducula aurorae 1 2 1 1 — — — — — 5
*Ducula galeata 3 1 5 2 — 1 — — — 12
Parrots
*Vini kuhlii 14 41 15 23 1 — — — — 94
**Vini vidivici 42 14 3 14 2 — — — — 75
[*/**Vini kuhlii/vidivici] 2 2 — 5 — — — — — 9
Kingfishers
Halcyon mangaia 1 2 2 2 — — — — 1 8
Warblers
Acrocephalus kerearako 6 6 1 2 — — — — — 15
Total NISP
All Species 103 133 98 102 8 5 15 15 8 487
Migratory Shorebirds 5 0 4 2 0 0 0 1 0 12
Native Landbirds 98 133 94 100 8 5 15 14 8 475
*/** Native Landbirds 91 125 86 94 6 2 7 2 3 416
% NISP */** Native Landbirds
of All Nonfish Bones 72 57 5 21 4 0.4 2 0.5 2 11
Total Species
All 13 14 16 16 5 4 2 5 4 19
Migratory Shorebirds 1 0 2 1 0 0 0 1 0 2
Native Landbirds 12 14 14 15 5 4 2 4 4 17
*/** Native Landbirds 10 12 10 11 4 2 1 2 1 13

*=extant species, extirpated on Mangaia.

**=extinct species.
NOTES: Dashes indicate no record. Taxa in brackets are not different from others listed more spe-
cifically. NISP represents number of identified specimens.
SOURCE: Updated from Steadman and Kirch (1990).

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154 / BIODIVERSITY II

1993, 1995; Table 10-7). Only 6 of these same species still survive on ‘Eua. If
they were still alive, most species of ‘Eua’s extinct forest birds probably would
qualify as RRS under the criteria of Bibby et al. (1992), thereby changing consid-
erably the international conservation priority of Tongan birds.
The ‘Euan avifauna has been depleted irreversibly. As sampled thus far,
the prehuman landbirds consisted of 27 forest and no nonforest species, com-
pared to 9 forest and 4 nonforest species today (Table 10-7). Forest frugivores/
granivores have declined from 12 to 4, nectarivores from 4 to 1, omnivores from
3 to 0, insectivores from 6 to 3, and predators from 2 to 1. These losses are more
complete for ground-dwelling than midlevel/understory or canopy species,
which might be expected with predation from humans, rats, dogs, and pigs.
The means of pollination and/or seed dispersal for various Polynesian forest
trees undoubtedly has been restricted or eliminated by the loss of so many
nectarivorous, frugivorous, and granivorous birds (Franklin and Steadman,
1991).

DISCUSSION
Humans cause the extinction of birds by overhunting, by introducing non-
native species, by spreading disease, and through habitat destruction. For many,
perhaps most, species of birds in danger of extinction today, habitat destruction
is the most serious threat. Loss of habitat is why tropical regions now have more
potential for extinction than temperate or polar regions. Even in the United
States, however, with our many and often admirable environmental laws, much
natural habitat has been lost or seriously degraded. We are fortunate that more
species are not already gone. Given current trends in human population growth
and habitat loss, this good fortune is unlikely to persist in the United States or
anywhere else. That 20% of all living species and 70% of all threatened species
of birds are confined to only 2% of the Earth’s land surface (Bibby et al., 1992)
is both a blessing and a curse. On the one hand, it means that we might be able
to save many species by protecting relatively small areas. On the other hand, we
can lose many species by allowing just these same places to be degraded.
Across the world, extinction rates of birds increase whenever humans enter
a previously uninhabited region. Human colonization of the Pacific islands alone
led to the extinction of as many as 2,000 species of birds, dominated by flight-
less rails, but also including species in many other families. A crude but conser-
vative estimate of overall losses of birds in Oceania is that an average of at least
10 species (including 2-3 that are endemic to the island and 2-3 that are endemic
to the island group) has been lost already on each of the approximately 800
major islands, yielding a minimum total loss of perhaps 2,000 species. Each of
the 16 Polynesian islands that has yielded 300 or more prehistoric bird bones
approaches or exceeds 20 extirpated species, and none of these records is com-
plete.

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HUMAN-CAUSED EXTINCTION OF BIRDS / 155

TABLE 10-7 Chronology and Community Ecology of Indigenous Resident

Landbirds from ‘Eua, Tonga

Pre-human Archaeological Extant

Resident Landbirds Recorda Recordb in 1988 Guild c

Herons
Egretta sacra — X X NF
**Nycticorax new sp. X — — GP
Ducks
Anas superciliosa — — X NF
Hawks
*Accipiter cf. rufitorques X — — DR
Megapodes
**Megapodius alimentum X X — GF
*Megapodius pritchardi X — — GF
**Megapodius new sp. X X — GF
Rails
**Gallirallus new sp. X — — GO
Gallirallus philippensis — X X NF
*Porzana tabuensis — X — NF
**Gallinula new sp. X — — GO
Porphyrio porphyrio — X X NF
Pigeons, Doves
*Gallicolumba stairi X X — GF
**Didunculus new sp. X X — MF
Ptilinopus porphyraceus X X X CF
Ptilinopus perousii X X X CF
**Ducula david X X — CF
**Ducula new sp. X X — CF
Ducula pacifica — X X CF
Parrots
*Vini solitarius X — — CN
*Vini australis X X — CN
**Eclectus new sp. X X — CF
Barn-Owls
Tyto alba — X X NR
Swifts
Collocalia spodiopygia — X X AI
Kingfishers
Halcyon chloris X X X MI
Trillers
Lalage maculosa X X X MI
*/**cf.Lalage sp. — X — MI
Whistlers, Robins
*/**Eopsaltria sp. X — — MI
Monarchs
*Clytorhyncus vitiensis X X — MI
*Myiagra sp. X X — MI
Warblers
*/**Cettia sp. X — — MI
Thrushes
*Turdus poliocephalus X X — MF
continued

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156 / BIODIVERSITY II

TABLE 10-7 Continued

Pre-human Archaeological Extant
Resident Landbirds Recorda Recordb in 1988 Guild c

Starlings
Aplonis tabuensis X X X MF
Honeyeaters
*Myzomela cardinalis X X — CN
Foulehaio carunculata X X X CN
White-Eyes
**Zosteropidae new sp. X — — CO
Total Species 27 26 13
Total */** Species 21 14 3
# of Sites/# of Bird Bones 1/401 14/888 —
Guild Totalsc
AI 0 1 1
CF 5 6 3
CN 4 3 1
CO 1 0 0
DR 1 0 0
GF 4 3 0
GO 2 0 0
GP 1 0 0
MF 3 3 1
MI 6 5 2
NF 0 4 4
NR 0 1 1
Total Forest Species (All
Categories of Guilds
except NF) 27 22 9
Food Categories
Frugivores 12 12 4
Nectarivores 4 3 1
Omnivores 3 0 0
Insectivores 6 6 3
Predators 2 1 1
Height Categories
Aerial 0 1 1
Canopy 10 9 4
Midlevel/understoryd 10 9 4
Ground 7 3 0

*=extirpated species.
**=extinct species.
a>3000 years before the present (BP)(1 site).
b3000-200 years BP (15 different sites).
c AI=aerial insectivore; CF=canopy frugivore/granivore; CN=canopy nectarivore; CO=canopy
omnivore; DR=diurnal raptor; GF=ground frugivore/granivore; GO=ground omnivore; GP=ground
predator; MF=midlevel/understory frugivore/granivore; MI=midlevel/understory insectivore;
NF=nonforest species; NR=nocturnal raptor. Certain distinctions between C and M are arbitrary.
dIncludes the hawk and owl.

NOTE: Dashes indicate no record.

SOURCE: From Steadman (1993, 1995).

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HUMAN-CAUSED EXTINCTION OF BIRDS / 157

The rapidity of extinction on oceanic islands has been influenced by the

ruggedness of terrain and the size and permanence of human populations. After
the arrival of humans, extinction of birds is what we have come to expect; sur-
vival is the exception. While it is too late to maintain or restore the entire
natural avifaunas of most oceanic islands, rigorous habitat protection, predator
control, and translocation can save much of what is left (Franklin and Steadman,
1991). Nevertheless, because most island biotas are so degraded, programs for
endangered species on islands face difficult challenges to ensure the long-term
survival of the species that remain. We know what needs to happen to save
most species, but without improved conservation funding and coordinated
changes in human activities, many of the challenges will not be met.
On tropical islands in all oceans, the prehistoric and ongoing extinction of
birds has consequences far beyond losing the birds themselves. For example,
the loss of hundreds of populations and a few entire species of Pacific seabirds
probably has influenced marine food webs, in which seabirds are top consum-
ers. Extinct Pacific island landbirds undoubtedly were involved in the pollina-
tion and seed dispersal of indigenous plants, many of which may lack natural
means of intra- or interisland dispersal today.

CONCLUSIONS
Rather than despair at what already is lost, I would argue that the extinct
species of birds should inspire us to save those that remain. I also would hope to
elevate the scientific status of recently extinct species so that their study is re-
garded as an important component of modern biology. Hundreds of species that
should be living today exist now only as skins or bones in museums. Who will
study these “relics of a lost world” (Graves, 1993) to learn more about their
phylogeny, biogeography, and ecology? Very few young ornithologists are
being trained in systematics, especially in areas other than molecular systemat-
ics. This is a serious situation, given that even such a widespread and locally
common species as the yellow warbler (Dendroica petechia), when studied more
comprehensively than ever before (2,500 skins examined by Browning, 1994),
has been found to include two previously unnamed subspecies in Alaska and
northern Canada. As pointed out so clearly by Trombulak (1994:590), training
in conservation biology should include much more than “applied ecology and
field population genetics.”
Whether their last gasp was thousands, hundreds, or only tens of years
ago, virtually all birds lost since the last ice age would still be alive if not for
humans; they would be feeding, preening, singing, nesting, molting, and doing
anything else that living birds do. You could use them to test behavioral hy-
potheses. You could see them during field work, vacations, or maybe on the
way to work. They would be illustrated in field guides and be part of your
overall biodiversity consciousness. (A field guide to South Pacific birds would

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158 / BIODIVERSITY II

depict as many species as a field guide to South American birds!) Pacific island
rails would compete with Darwin’s finches and Hawaiian finches as “textbook”
examples of adaptive radiation.
We need to squeeze out as much knowledge as we can about recently ex-
tinct species of birds. This chapter began by noting that, relative to other ani-
mals, birds are conspicuous and therefore more studied. This is supported by
the low rate at which new living species are being discovered. The number of
“good” new species of birds described per year has varied from 6.0 in 1938-1941
to 2.6 in 1941-1955, 3.5 in 1956-1965, 3.1 in 1966-1975, 2.4 in 1976-1980, and
2.4 in 1981-1990 (Vuilleumier et al., 1992). While estimates of valid descriptions
of species, just like estimates of extinction, have margins of error, sometime
within the past decade we probably reached the point where more living species
of birds are going extinct per year than are being newly described. This is a
debt that cannot be repaid.

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CHAPTER
11

Global Warming and Plant Species

Richness: A Case Study of the
Paleocene/Eocene Boundary

SCOTT L. WING
Associate Curator, Department of Paleobiology, National Museum of
Natural History, Smithsonian Institution, Washington, D.C.

There is widespread concern over the possibility that greenhouse gases gen-
erated by human activity may cause global warming. Much effort is being de-
voted to monitoring changes in climate and organisms, and to modeling the
possible effects of greenhouse gases on climatic and biological systems. Pro-
grams of monitoring and modeling clearly are necessary, but the geological his-
tory of the Earth and its biota have not been mined thoroughly enough for
information about global climate and ecosystem response to climatic change.
Fossils and sedimentary rocks form a record of changes in the Earth’s cli-
mate and of biotic responses over geological time. This record can be used in
two main ways to develop a more complete understanding of global climate and
of the long-term effects of climatic change on ecological systems. First, compar-
ing climatic conditions indicated by fossils and sedimentary rocks with com-
puter simulations of global climate for the same period is the only way we have
of testing the ability of climate models to simulate conditions other than those
that exist today. If models can successfully simulate climatic patterns known to
have existed in the past, then we can have greater confidence in their predic-
tions about the future. Second, the fossil record provides our sole opportunity
to examine the biological consequences of climatic change without waiting for
them to happen in “real time.” If particular kinds of climatic change are associ-
ated with specific patterns of faunal and floral turnover, then we have some
basis for anticipating future biotic responses to climatic change.
This chapter focuses on climatic changes and biotic events that took place
during the Paleocene-Eocene transition, about 55 million years ago. With the
exception of the Holocene deglaciation, the Paleocene-Eocene transition is prob-

163

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164 / BIODIVERSITY II

ably the best documented example of a geologically rapid warming of global

climate, although just how rapidly it occurred is still a matter of investigation.
Our distance in time from these events places severe limitations on our ability to
determine the rates of environmental and biological changes, and especially the
synchroneity of events over large geographic areas. Typically, events that are
less than 10,000 years apart appear synchronous, and records from different
parts of the world cannot be correlated with greater than 100,000 year resolu-
tion. Still, the Paleocene-Eocene warming event is a close match for extreme
predictions of human-induced global warming in terms of the absolute magni-
tude of warming and final climatic conditions. This makes the Paleocene-Eocene
interval a valuable example for improving our understanding of the effect of
rapid global warming on terrestrial ecosystems.

RECONSTRUCTING CLIMATES OF THE PAST

Climatic conditions for the distant past can be inferred in a variety of ways,
but the two techniques most widely applied to continental paleoclimates are
based on fossil plants. One method, called the nearest living relative (NLR)
method, relies on the assumption that fossil species grew in climates similar to
those preferred by their extant relatives. The validity of the NLR method de-
pends on how closely related the fossil and extant species are, how much evolu-
tionary change there has been in climatic preferences of the lineage, and the
degree to which the range of the extant species is controlled by climate. Living
taxa that have relictual distributions or few species are especially unreliable
paleoclimatic indicators because they are far from occupying the full range of
climatic conditions they can tolerate physiologically (e.g., Ginkgo, Metasequoia).
NLR inferences about early Cenozoic climate are more reliable if they are based
on diverse, nonrelictual taxa that have strong climatic limitations on their
present-day distribution.
Palms are a good example of a speciose group with clear climatic limits on
their distribution. Palms do not naturally occur in regions where means of cold
months are less than about 6°C, or where frosts persist for more than two days
(Wing and Greenwood, 1993; Figure 11-1). Experimental work on a wide vari-
ety of living species of palms shows that sensitivity to cold temperatures is typi-
cal of the whole family and results from absent or poorly developed physiologi-
cal mechanisms of frost hardening (Sakai and Larcher, 1987). The combination
of geographic and physiological information on palms makes a convincing case
that extinct species in the family are unlikely to have had significantly more
frost tolerance than their living relatives, so palms can be used with confidence
to fix lower limits on paleotemperature estimates for early Cenozoic floras.
The second major method for inferring paleoclimate from fossil plants, leaf
physiognomy, relies on correlations between the shape and size of leaves and
climate that are observed in living floras. Generally, floras growing under

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GLOBAL WARMING AND PLANT SPECIES RICHNESS / 165

6 days 7°

6°
5°

1 day Palms

10° Frost
Duration

4 days Cold Month

Mean

FIGURE 11-1 Natural distribution of living palms in relation to cold-month mean tem-
perature (CMM) and average number of days of frost per year. Note close correspon-
dence between the 6°C CMM and the limit of palms in both North America and New
Zealand. Data were compiled by Wing and Greenwood (1993).

warmer climates will have a higher proportion of species that have leaves with
entire margins (nontoothed leaves). The correlation between mean annual tem-
perature (MAT) and the proportion of species with entire margins was first
observed over 80 years ago, but has been documented and quantified most
extensively by Wolfe (1979) using floras from East Asia (Figure 11-2). However
the high correlation exhibited in Wolfe’s data set is due in part to the exclusion
of living floras from seasonally dry climates. Although the relationship be-
tween the percentage of species with entire margins in a local flora and MAT
has been used widely to obtain numerical estimates of MAT for Cenozoic fossil
floras, it may give misleading results for fossil floras that grew under season-
ally dry conditions.
More recent attempts to make leaf physiognomic analysis more general and
robust have used additional descriptors of leaves and climate (Wolfe, 1993).
Many characteristics of leaf shape and size are correlated with temperature and
rainfall conditions and can be used to infer paleoclimatic conditions. Wolfe
(1993) scored a large number of Central and North American floras based on
characteristics of leaf size and shape (Figure 11-3a). These leaf characteristics
then were compared with parameters of temperature and rainfall for the sites
using ordination analysis (Wolfe, 1993). Relationships between physiognomic
variables of leaves and climatic variables (Figure 11-3b) then can be used to infer

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FIGURE 11-2 Correlation between the percentage of species in a local flora with entire-
margined leaves (leaf on left) and the mean annual temperature (MAT) of the site. Data
are from mesic East Asian forests (Wolfe, 1979). Linear regression of this data set yields
the equation: MAT=1.14 + (0.31 × percentage of species with entire leaf margins).
R2=0.98, p<0.001, standard error of the estimate is 0.79°C.

climatic conditions for fossil leaf assemblages based on their physiognomy.

Wolfe’s Central and North American data set also has been analyzed using mul-
tiple regression techniques (Wing and Greenwood, 1993). Mean annual tem-
perature estimates based on the multiple regression approach have errors of 2-
4°C; precipitation estimates generally are no more than ballpark figures.
In spite of the limitations on the precision of paleoclimate inferences, there
is strong agreement between estimates using the different paleobotanical meth-
ods and between estimates derived from plant and vertebrate fossils (Hutchison,
1982; Markwick, 1994; Wing, 1991; Wing and Greenwood, 1993). There is also
general congruence between marine temperature curves derived from oxygen
isotope studies and terrestrial temperature curves derived from fossil plant and
animal evidence (Wing et al., 1991; Wolfe and Poore, 1982). The consistency of
paleoclimate estimates based on different fossil data sets and methodologies sug-
gests that the estimates are robust. This is important, because paleoclimate esti-
mates based on paleontological data indicate a world sharply different from the
modern one with climatic conditions that are difficult to explain in terms of the
climate systems observed today.

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GLOBAL WARMING AND PLANT SPECIES RICHNESS / 167

FIGURE 11-3a Leaf character states used in multivariate analysis of relationships be-
tween physiognomy and climate (Wolfe, 1993). Character states: A-C=general margins,
A=untoothed leaf, B=palmately lobed untoothed leaf, C=pinnately lobed untoothed leaf;
D-K=toothed margins, D=irregularly spaced, E=regularly spaced, F=distantly spaced,
G=closely spaced, H=rounded, I=appressed, J=acute, K=compound; L-S=shapes of the
apex, L=apex emarginate, M-O=apex rounded, P-Q=apex acute, R-S=apex attenuate;
T-Z= shapes of the base, T-U=base cordate, V-W=base rounded, X-Z=base acute;
AA-CC=shapes of the leaf, AA=obovate leaf, BB=elliptic leaf, CC=ovate leaf. Leaf-size
categories are approximately 0.5×.

THE EQUABLE CLIMATE PARADOX

Global climate through most of Earth’s history has been much warmer than
a present. The early Eocene has long been recognized as the warmest part of the
Cenozoic and one of the warmest periods of global climate in the last 100 million
years (Miller et al., 1987; Savin et al., 1975; Wolfe, 1978). During the early
Eocene, polar icecaps were absent in both hemispheres (Crowley and North,
1991), and midlatitude continental interiors had much warmer winters than they
do now (Hickey, 1977; MacGinitie, 1974; Wing, 1991; Wing and Greenwood,
1993).
The causes for such globally warm climate are not well understood. Higher
sea levels, lack of polar icecaps, and more dispersed land masses all have been
thought to play a role in maintaining a warmer world. In recent years, general
circulation models (GCMs) have been applied to paleoclimates (e.g., Crowley and
North, 1991). To produce “predictions” for temperature and precipitation for a

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Temperature (Axis 1)
Leptophyll 1
1000

400

Apex emarginate 400

No teeth
400

200
Water stress (Axis 2)

–1000 –800 –600 –400 –200 200 400 600 800 1000
Mesophyll 1
Apex attenuate –200

–200
Teeth regular

–200 L:W <1:1

Teeth acute
Teeth compound
–200

–200

FIGURE 11-3b Reciprocal averaging plot showing relationship of climatic and physi-
ognomic variables (Wolfe, 1993). The largest leaf-size category and attenuate apices are
more abundant in wetter climates. All tooth features are more abundant in colder cli-
mates, as are narrow leaves with a length to width ratio of less than 1:1. Entire margins
and emarginate apices are correlated with warmer climates.

time in the past, GCMs use starting conditions such as ancient coastline posi-
tions, paleotopography, continental positions, sea-surface temperature gradients,
and global ice distribution. Weather patterns are generated using the same equa-
tions that describe the dynamics of the atmosphere today, then the weather
patterns are averaged to yield a paleoclimate.
Application of these models to past periods of equable climate like the early
Eocene consistently yields simulations that are more like the modern world than
paleontological data indicate. The early Eocene is arguably the most interesting
case of conflict between proxy data and model output, because it is close enough
to the present that the proxy data are extensive, and uniformitarian assump-
tions about the climatic tolerances of animal and plant lineages are probably
valid. Additionally, there is little evidence for very high CO2 levels in the early

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GLOBAL WARMING AND PLANT SPECIES RICHNESS / 169

Eocene atmosphere, so this factor cannot be invoked in an unconstrained fash-

ion to explain differences between proxy data and model output.
The sharpest discrepancy between model output and proxy data occurs in
mid- to high latitude continental interiors because the low thermal capacity of
land and the isolation of continental interiors from the moderating influence of
the oceans result in model predictions of high seasonal variation in temperature
in these areas (Sloan, 1994; Sloan and Barron, 1990, 1992). There are literally
hundreds of early Eocene plant and animal fossil localities scattered across much
of the continental interior of North America. The distribution of frost-intolerant
forms (e.g., palms, cycads, crocodilians), as well as weak development of sea-
sonal growth rings in some fossil wood, high diversity of small arboreal frugi-
vores and insectivores requiring year-round food resources, and the physiog-
nomy of fossil dicot foliage, all yield similar conclusions. In the Early Eocene,
the interior of North America as far as 50°N experienced no significant winter
freezing (e.g., annual minimum temperatures were >–10°C, frost durations were
less than 1-2 days). Mean temperatures in cold months were certainly above
freezing, and probably higher than 5°C in most areas. Mean annual temperature
was 15-20°C (Wing and Greenwood, 1993). There are fewer proxy data avail-
able for the interiors of other continents, but southern Australia, which was 50-
60°S in the early Eocene, has fossil faunas and floras indicating even warmer
winter temperatures than similarly high latitudes in the interior of North
America (Greenwood and Wing, in press). The proxy data consistently show
equable climates with low seasonality of temperature and warm winters. GCM
simulation results consistently yield highly seasonal climates in continental in-
teriors, with freezing temperatures far south of fossil sites containing frost in
tolerant forms (Sloan and Barron, 1990, 1992; Figure 11-4).
There are three basic kinds of explanation for warmth in the mid- to high
latitudes during the early Eocene: (1) more heat was transported from equatorial
to polar regions by ocean currents or winds, (2) more solar radiation was ab-
sorbed at high latitudes because albedo was lower, and (3) more heat was re-
tained at high latitudes, and everywhere else, because of higher concentrations
of “greenhouse” gases such as water vapor, methane, or CO2. The persistent
discrepancy between GCM output and proxy data arises because mechanisms in
the first two categories—such as increased heat transport by ocean currents or
no polar ice—are not strong enough to explain the levels of warmth indicated
by proxy data, especially in continental interiors (Walker and Sloan, 1992). The
last mechanism, a CO2, methane, or water-vapor greenhouse, implies that tropi-
cal as well as high-latitude regions would have been substantially warmer than
at present. The best proxy data for the Eocene tropics, however, indicate little
difference from present temperatures (Adams et al., 1990; Graham, 1994). Fur-
thermore, neither proxy data nor geochemical modeling are consistent with
Eocene CO2 levels more than about 900 parts per million (ppm), and it is possible

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FIGURE 11-4 Eocene paleogeographic reconstruction of North America, showing frost-

sensitive plants and high MAT estimates far north of the line where GCM simulation
results indicate freezing temperatures. Numbers next to sites are MAT estimates based
on multiple regression analysis of physiognomic data as described by Wing and Green-
wood (1993). Proxy data are from Wing and Greenwood (1993). Model results are from
Sloan (1994); simulation is based on present CO2 level without large lakes in Wyoming.

that Eocene CO2 levels were no different from those at present (Berner, 1991;
Cerling, 1991).
The resolution of the equable climate paradox apparently will come from
better GCMs, not from reinterpretation of the fossil record. The significance of
the “equable climate paradox” is that it reveals the strong tendency for climate
models to yield results that are more like the present than they should be. If
similar problems plague the prediction of future climates under higher levels of
atmospheric CO2, our predictions about the magnitude and rate of global cli-
matic change may be far less accurate than we think.

THE TERMINAL PALEOCENE EVENT

The global climate warmed considerably from the late Paleocene to the early
Eocene, roughly 57-52 million years ago. This warming trend has been quanti-

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GLOBAL WARMING AND PLANT SPECIES RICHNESS / 171

fied in the marine realm by measuring changes in oxygen isotope ratios in the
tests of benthic and planktonic foraminifera (one-celled, amoeba-like organisms
that secrete calcareous shells) recovered from deep sea cores (Miller et al., 1987,
Pak and Miller, 1992; Figure 11-5) and in North America by physiognomic and
floristic analyses of fossil plant assemblages (Hickey, 1977, 1980; Wing et al.,
1991; Wolfe, 1978). In the mid-latitudes of interior North America, MAT in-
creased from approximately 10°C to nearly 20°C between the late Paleocene and
the mid- to early Eocene, a period of about 3 million years (Wing et al., 1991).
Although this rate of change averages to only a few thousandths of a degree per

δ 18Ο
3.0 2.0 1.0 0.0 –1.0 –2.0

Plio-pleistocene

Miocene

Oligocene

Eocene

Paleocene

Cretaceous

2° 6° 10° 14° C

Colder Colder

FIGURE 11-5 Cenozoic δ18O curve showing major fluctuations in deep ocean tempera-
ture over the last 65 million years (redrawn from Miller et al., 1987). Temperature equiva-
lents for δ18O scale assume no polar icecaps.

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172 / BIODIVERSITY II

millennium over the whole period, there is growing evidence that the rate of
climatic warming was not constant.
In cores that recover laminated ocean bottom sediments, it is possible to
resolve time in tens of thousands of years, even in the early Cenozoic (Kennett
and Stott, 1991). Recent detailed stratigraphic studies of the Paleocene/Eocene
boundary interval recovered in cores from the southern Pacific and southern
Indian Oceans have shown an excursion in isotope values that occurred ap-
proximately 100,000 years before the Paleocene/Eocene boundary (approxi-
mately 55.1 million years ago; Kennett and Stott, 1991; Pak and Miller, 1992;
Figure 11-6). The sudden increase in the light isotope of oxygen (decrease in
δ18O values) took place over less than 10,000 years and is thought to represent
an interval when the temperature of bottom waters and surface waters in mid- to
high latitude oceans increased by 5-8°C. This geologically short period of time,
marked by isotopic shifts, is referred to here as the “Terminal Paleocene Event.”
Oxygen isotope analyses of planktonic foraminifera tests indicate that sur-
face waters in the equatorial Pacific maintained a temperature of about 20°C
during the Terminal Paleocene Event, but analyses of the tests of tropical benthic
species imply warming similar to that seen in the benthic and planktonic fora-
minifera of higher latitudes (Zachos et al., 1993). The isotopic shift coincides

δ 13C δ 13C
–2 –1 0 1 2 3 1 0 –1
Eocene

Eocene
mid.

mid.
early Eocene

early Eocene
Paleocene
late Paleocene

late

Terminal Terminal
paleocene paleocene
event event

FIGURE 11-6 Terminal Paleocene excursion in carbon and oxygen isotope values (re-
drawn from Pak and Miller, 1992). The Terminal Paleocene Event occurred about 100,000
years before the Paleocene/Eocene boundary and was associated with a major extinction
of benthic foraminifera (Kennett and Stott, 1991).

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GLOBAL WARMING AND PLANT SPECIES RICHNESS / 173

with the most severe extinction (about 50% of species) of benthic foraminifera
from the deep ocean during the Cenozoic; the extinction is believed to have been
caused by rapid warming of deep ocean waters and a concomitant decrease in
their dissolved oxygen levels (Kennett and Stott, 1991; Zachos et al., 1993). Fol-
lowing the negative isotopic excursion (warming) there was a rapid rebound in
the positive direction (cooling), followed by a renewed decrease in δ18O values
that continued to a Cenozoic minimum in the mid- to early Eocene about 52-53
million years ago. This minimum indicates the time of maximum global warmth
during the Cenozoic.
The terminal Paleocene oxygen isotopic excursion is paralleled by a similar
excursion in carbon isotope values (Kennett and Stott, 1991). The shift from 13C
to 12C is probably related to the source and rate of delivery of organic carbon to
the deep ocean, and possibly to decreased rates of oxidation of organic material
in bottom waters (Kennett and Stott, 1991). The rapid isotopic and biotic changes
during the Terminal Paleocene Event all may relate to a change in ocean circula-
tion in which the source for bottom waters shifted from cool high latitudes to
warm low latitudes (Kennett and Stott, 1989, 1991; Rea et al., 1990).
In this hypothesis, global warming during the later Paleocene increased the
warmth, and therefore decreased the density, of high-latitude surface waters.
At some point, warm, oxygen-poor saline waters generated by evaporation in
the equatorial regions exceeded the density of cooler, more oxygenated waters
from the polar regions, and deep ocean circulation began to move in a poleward
direction. This is the opposite of present-day conditions in which dense bottom
water is created in cold, moderately saline high-latitude oceans. The hypoth-
esized “reversed” bottom-water flow at the end of the Paleocene transported
heat to mid- and high latitudes very effectively, resulting in a rapid increase of
bottom water temperatures, but also a sudden warming of mid- to high latitude
surface waters and continental surfaces as the warm bottom water upwelled
(Brass et al., 1982; Pak and Miller, 1992; Rea et al., 1990; Zachos et al., 1993).
Although the precise triggering mechanism that led to the sudden reversal of
bottom water circulation is not understood, the effects of the Terminal Pale-
ocene Event appear to have been global, because rapid changes are seen at this
time in sediments deposited in continental and shallow marine environments as
well as in the deep sea.
One effect of increased poleward heat transport by deep ocean currents
would have been a decrease in latitudinal temperature gradients. There is direct
evidence for decreased temperature gradients both in ocean surface waters and
on the continents (Greenwood and Wing, in press; Zachos et al., 1992). De-
creased surface temperature gradients would be expected to lead to a reduced
intensity of zonal atmospheric circulation, which is largely driven by equator-
to-pole temperature contrasts. Reduced surface wind velocities were respon-
sible for the sharp decline in the size of wind-blown dust grains in Paleocene/
Eocene boundary sediments of the central Pacific; sluggish winds are not ca-

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174 / BIODIVERSITY II

pable of carrying larger dust particles far out to sea (Janecek and Rea, 1983; Rea
et al., 1985). A secondary effect of reduced wind velocities may have been a
decrease in coastal upwelling zones, which are powered by wind shear (Stott,
1992).
Greater warmth at mid- to high latitudes also may have resulted in increased
precipitation and chemical weathering on land surfaces. Evidence for increased
chemical weathering is seen in the sudden, widespread increase during the Ter-
minal Paleocene Event of kaolinitic clays that are characteristic of leached soils
formed under “tropical” weathering regimes (Robert and Chamley, 1991; Hovan
and Rea, 1992; Gibson et al., 1993).

THE PALEOCENE-EOCENE TRANSITION ON LAND

The carbon isotope excursion associated with the Terminal Paleocene Event
is a geochemical marker that can be detected in continental carbon sources such
as hydroxyapatite preserved in tooth enamel of fossil mammals and calcium car-
bonate preserved in fossil soil nodules. Because the largest short-term reservoir
in the global carbon budget is the ocean, shifts in the 13C/12C ratio of the oceans,
such as those observed during the Terminal Paleocene Event, should force simi-
lar isotopic shifts in the carbon reservoirs represented by the atmosphere and
continental ecosystems. Investigations of Paleocene/Eocene boundary sections
in the Bighorn Basin of northern Wyoming have detected a carbon isotope ex-
cursion that corresponds to the Terminal Paleocene Event in direction, magni-
tude, and timing, thus establishing a datum that permits correlation of terres-
trial and marine events (Koch et al., 1992).
The terrestrial carbon isotope excursion coincides with the Clarkforkian/
Wasatchian boundary, a major and rapid change in the composition of mamma-
lian faunas which has long been thought to be approximately correlated with
the Paleocene/Eocene boundary (Wood et al., 1941). It is at the beginning of the
Wasatchian that North American faunas first included representatives of the
perissodactyla (odd-toed ungulates), artiodactyla (even-toed ungulates), and
euprimates (Gingerich, 1989; Rose, 1981a). Similar faunal changes are known to
have taken place at about the same time in Europe and Asia (Rose, 1981a; Russell
and Zhai, 1987), and in Europe the faunal change also is associated with the
carbon isotope excursion (Sinha and Stott, 1993). The nearly simultaneous ap-
pearance of these forms on all three northern continents indicates that high lati-
tude land corridors in Greenland and Beringia were open to mammalian mi-
grants (Maas et al., 1995; McKenna, 1983; Rose, 1981a), but the place of origin
for these groups is still not known. Although rates of mammalian taxonomic
turnover were high near the Paleocene/Eocene boundary, there is no evidence
for a substantial decline in the number of mammalian genera (Wing et al., 1995).
In spite of maintaining high numbers of genera, there is evidence that, at the
level of species, latest Paleocene mammalian faunas from North America were

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GLOBAL WARMING AND PLANT SPECIES RICHNESS / 175

characterized by high dominance of a few species, possibly an indication of

stressful conditions (Rose, 1981b).
The effect of the Terminal Paleocene Event on terrestrial floras is less well
understood, although it has been known for some time that floral similarity
between North America and Europe reached a maximum in the early Eocene
(Tiffney, 1985). Two studies have shown a substantial (about 30%) reduction in
the number of species of plants near the end of the Paleocene in North America,
approximately coincident with the mammalian faunal exchange and the Termi-
nal Paleocene Event (Frederiksen, 1994; Wing et al., 1995; Figure 11-7). This
rapid decrease in the number of species of plants at the end of the Paleocene was
geologically short-lived (about 1 million years); by the mid- to early Eocene
(about 53 million years ago), as global climate reached its maximum Cenozoic
warmth, floral richness had recovered to levels considerably higher than those

80 20°

Mammalian genera
70 Plant species 18°

Mean annual temp.

16°

Mean annual temperature (in °C)

60

50 14°
Species/Genera

40 12°

30 10°

20 8°

10 6°

Cretaceous Paleocene e. Eocene

PU TO TI CF WA
0 4°
70 65 60 55 50
Millions of years

FIGURE 11-7 Comparison of MAT with the number of plant species and mammalian
genera through the Paleocene and earliest Eocene. MAT estimates are based on physiog-
nomic analysis of floras from western Wyoming. Plant and mammal taxonomic richness
are based on data compiled from Wyoming and southern Montana. Abbreviations for
provincial ages: PU=Puercan, TO=Torrejonian, TI=Tiffanian, CF=Clarkforkian. Figure
was redrawn from Wing et al. (1995).

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176 / BIODIVERSITY II

preceding the Terminal Paleocene Event. Stratigraphic resolution of the termi-

nal Paleocene drop in floral richness is not yet sufficient to determine whether it
coincides with increasing temperatures at the start of the Terminal Paleocene
Event, decreasing temperatures at the end of the Terminal Paleocene Event, or is
spread throughout the entire excursion.
The fluctuations in numbers of species of plants near the Paleocene/Eocene
boundary are part of a long-recognized change in the composition of North
American floras (Leopold and MacGinitie, 1972). Paleocene assemblages are
dominated by species belonging to largely deciduous groups with modern north
temperate distributions (e.g., Metasequoia, Betulaceae, Cercidiphyllaceae,
Hamamelidaceae, Juglandaceae; Figure 11-8), whereas Eocene floras typically
have many species belonging to largely subtropical evergreen families (e.g.,
Annonaceae, Lauraceae, Leguminosae, Myristicaceae, Palmae, Zamiaceae; Figure
11-9).
In the present, warmer climates are correlated positively with larger num-
bers of species of plants per unit area, particularly if regions of strong aridity are
excluded (Gentry, 1988). In view of this correlation, a simplistic expectation for
the response of plant species richness during the Paleocene/Eocene transition
would be an increase in number of species as global temperatures warmed. In-
stead, the number of species of plants declined in two widely separated areas of
North America: the northern Rocky Mountains (Wing et al., 1995), and the Gulf
Coastal Plain (Frederiksen, 1994). The geographic scope of the decline argues
against it being an artifact of local sampling or preservational effects, and im-
plies that the cause is of continental or greater geographic scope.

A SCENARIO FOR PALEOCENE/EOCENE PLANT EXTINCTIONS

What causal connection is there, if any, between the climatic changes of the
Terminal Paleocene Event, the decrease in plant diversity, and the shift in mam-
malian faunal composition? The stratigraphic resolution and geographic scope
of our knowledge of faunal and floral change across this time period is increas-
ing rapidly, but it is not yet sufficient to provide a clear answer. What follows
is a preliminary hypothesis that is amenable to testing as the paleontological
database improves.
A key to understanding the cause of the loss of species among plants is the
difference between the curves of species richness for mammals and plants. In
the present, the diversity of both groups of organisms generally increases to-
ward the equator, but the migrational abilities are obviously quite different.
The difference in rates of migration provides an explanation for greater loss of
species among plants than mammals at the Paleocene/Eocene boundary.
The Paleocene flora of the northern continents long has been noted for its
relatively low diversity and high homogeneity, with many lineages of decidu-
ous plants distributed throughout the middle and high latitudes of North

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GLOBAL WARMING AND PLANT SPECIES RICHNESS / 177

FIGURE 11-8 Typical Paleocene plant fossils of interior western North America. Based
on thickness of the fossil organic compression and living relatives, most of these were
probably deciduous trees. Toothed leaves are typical of the Paleocene midlatitude floras.
A. Cercidiphyllum sp., related to katsura tree, a native of East Asia; B. Ulmus (Chaetoptelea)
microphylla, related to living elms in Central America; C. Betulaceous leaf (birch family),
probably an extinct genus; D. Alnus (alder) sp. leaf.

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178 / BIODIVERSITY II

FIGURE 11-9 Typical early Eocene plant fossils of interior western North America.
Based on thickness of the fossil organic compression and living relatives, most of these
were probably broad-leaved evergreens. Large, entire-margined leaves are typical of
Eocene midlatitude floras. A. Leaf of a legume similar to a living species of Machaerium
B. Menispermaceous leaf (moonseed family), probably a vine or liana; C. Lauraceous leaf
(avocado family); D. Salvinia preauriculata, a floating aquatic fern characteristic of Eocene
floras in midlatitude North America. Living Salvinia species occur in subtropical to
tropical climates; E. Apocynaceous leaf (oleander family).

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GLOBAL WARMING AND PLANT SPECIES RICHNESS / 179

America, Europe, and Asia (Boulter and Kvacek, 1989; Brown, 1962; Guo et al.,
1984; Koch, 1963). Warming at middle and high latitudes during the Terminal
Paleocene Event and the early Eocene is likely to have caused local extinction at
the southern ends of the ranges of cool-adapted lineages with broad circumpolar
distributions. Warming at middle and high latitudes also would have permitted
the poleward migration of subtropical and tropical taxa in both mammals and
plants. For floras in the northern Rocky Mountains and the Gulf Coastal Plain of
North America, there was a significant delay, as much as several hundred thou-
sand years, between the loss of species at the Terminal Paleocene Event and the
arrival of subtropical elements in the early Eocene. It was this lag that created
the rapid drop and rapid recovery of plant richness at middle latitudes. What in
mammals shows up as a rapid intercontinental mixing of faunas manifests itself
among plants as an extinction event at mid- to high latitudes, followed perhaps
100,000 years later by a major immigration of species from the south.
The migrational lag explanation seems at first glance unlikely because plant
“migration” can be very rapid geologically; the movement of forest taxa in the
wake of the retreating Holocene glaciers totally modified the vegetation of vast
areas of North America in 5,000-10,000 years (Overpeck et al., 1992). The Ho-
locene example is not wholly applicable to the Eocene situation, however, be-
cause of the different continental configuration in the Eocene, and because Ho-
locene plants were migrating into a recently denuded landscape that probably
was not occupied by established forest vegetation.
In the early Eocene, the Tethys Sea still formed a wide barrier between the
northern and southern continents; it separated Africa from Europe and South
America from North America, although there were probably islands in both the
proto-Mediterranean and the proto-Caribbean (Figure 11-10). This ocean cross-
ing may have been one factor that slowed the migration of subtropical and tropi-
cal plants into North America. Tropical taxa may have had limited access to
Europe along the northern shore of the Tethys, but the straits of Turgai divided
Europe from eastern Asia at about the present-day position of the Caspian Sea,
so the appearance of subtropical forms in Europe also might have been delayed.
By contrast, Asia had a broad land connection with tropical continental areas
during the Eocene, so that the ranges of terrestrial plants could have shifted
northward without confronting an oceanic barrier.
The paleogeographic differences between Asia and North America can be
used to help resolve whether a migrational lag was important in creating the
pattern of change in number of species across the interval of the Paleocene-
Eocene boundary. Because of eastern Asia’s connection to tropical land masses,
the migration of lineages from warm climates into middle latitudes should have
been much easier than in North America or Europe. If this hypothesis is correct,
Paleocene-Eocene floral immigration into mid-latitude Asia should have been
more rapid, and the sharp drop in plant species richness should have had a
duration of thousands or tens of thousands of years—almost certainly too short

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180 / BIODIVERSITY II

FIGURE 11-10 Global paleogeographic reconstruction of the early Eocene. Note ocean
barriers that separated the European and North American land masses from Africa and
South America. Only Asia had a significant land connection to tropical latitudes. Figure
was redrawn from Smith et al. (1994).

to detect in the fossil record. Finding the same pattern of diversity change in
Asia and North America would remove migrational delay as a reasonable hy-
pothesis for the decline in species numbers observed in North America.
The cause of the loss of species during the Paleocene-Eocene transition also
can be evaluated by comparing the pattern of floral immigration within North
America. If the delayed immigration of subtropical forms to the northern Rocky
Mountain region was largely a consequence of the water gap between North
America and South America rather than slow migration across the North Ameri-
can continent, then forms from warm climates should appear at essentially the
same time in the southern and northern part of the continent. If migrants
adapted to warm climates show up detectably earlier in the south, this would
indicate a slow rate of migration across the continent, suggesting that the rate of
northward shift in the ranges of plants was limited by the pace of warming, or
by the ability of the immigrant species to gain footholds in the established veg-
etation of North America.
Two possible general patterns emerge from a consideration of events at the
Paleocene/Eocene boundary. First, species richness of plants is much more dra-
matically affected by the climatic change than is taxonomic richness of mam-
mals. This should not be surprising in light of the sensitivity of plants to cli-
mate, but it has been proposed that plants are generally more “extinction

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GLOBAL WARMING AND PLANT SPECIES RICHNESS / 181

resistant” than other groups of organisms (Knoll, 1984). This conclusion was
based on the observation that most major lineages of plants survived mass ex-
tinctions at the Permian/Triassic and Cretaceous/Tertiary boundaries, whereas
higher taxonomic groups of animals were decimated. Analysis of the Paleocene/
Eocene extinctions of plants supports the idea that the cause of an extinction
(e.g., climate versus bolide impact) may be more important in understanding its
effects than its “size,” as measured by the percentage of taxa that are lost.
The Paleocene/Eocene extinction of plants also illustrates the principle that
the rate of climatic change may be as or more important than its direction in
causing extinction of plants. Rapid climatic shifts initially may decrease species
richness of plants through accelerated local extinction regardless of whether
climate is warming or cooling.
Through the last 65 million years of Earth’s history, the middle and high
latitudes have been more affected by both warming and cooling events than the
tropics because their temperature is more easily influenced by changes in the
efficiency and direction of heat transport by oceanic and atmospheric circula-
tion. Although the image of the tropics as climatically invariant has been thor-
oughly debunked by increased understanding of the Miocene through Pleis-
tocene history of Amazonia (Hoorn, 1994; Van der Hammen and Absy, 1994),
over the long term it is the middle and high latitudes that have been most dra-
matically affected by fluctuations in global climate and most frequently afflicted
by large-scale extinction of plants. During the Pleistocene, the comings and
goings of glaciers in the north temperate regions resulted in the intermittent
sterilization of large areas, certainly a more severe form of disruption than the
rainfall and temperature fluctuations experienced at lower latitudes. Relative
climatic stability on geological time scales is probably one important factor lead-
ing to larger numbers of species in the tropics.

CONCLUSIONS
The fossil record can be used in two different and very productive ways to
understand global climatic change and its effects on biotic systems. First, it is a
testing ground for climate models—the only way we can find out if they are
overtuned to reproduce present conditions. The example of the enigma of eq-
uable climate suggests that there is a great deal of room for improving general
circulation models of climate, and that predictions generated through GCMs have
a bias toward reproducing conditions similar to those of the present. This is a
very serious problem for understanding the probable effects of anthropogenic
addition of CO2 or other greenhouse gases to the atmosphere.
The fossil record also provides our sole opportunity to examine the biologi-
cal consequences of climatic change without waiting for them to happen in “real
time.” Although causation is difficult to prove in an historical record (or, often
enough, even in the laboratory), the pattern of biotic response to environmental

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182 / BIODIVERSITY II

change can indicate probable processes. In particular, we should be on the alert

for patterns that are consistent with threshold responses to climatic forcing fac-
tors (DiMichele and Phillips, 1995).
Paleontologists have invoked climatic change as a major factor in extinction
and biotic turnover for as long as there have been paleontologists. But generally
this has been an afterthought. A concerted study of the biotic effects of climatic
change involves choosing time intervals for the climatic events that are known
to occur, rather than searching for climatic change once a dramatic biotic change
has been noted. This is the only way to find out if some climatic change occurs
without catastrophic biological effects. Such studies require combining research
on paleoecology, the history of biotic diversity, and extinction, with paleo-
climatic reconstructions. Mixing these approaches will provide results of prac-
tical importance, but also will raise fascinating biological issues relating to eco-
system response, threshold effects, and biogeography.
Some view the globally warm periods of the past as a prologue to the fu-
ture. Are they? This is not a question we can answer yet. We do know that
climatic models “tuned” to the present do a poor job of reproducing the climate
of past greenhouse worlds. We also know that the present is an unusual time in
Earth’s history, and not a simple key to the past. Clearly this raises doubts
about our ability to predict climatic change or biotic responses under elevated
CO2 conditions.
If the present is not the key to the past, is the past likely to reveal much
about the future? Here I think the answer is a cautious “yes.” The process of
interpretation is not simple, but by enlarging the set of “worlds” we have to
explain, study of the past will increase the generality of our understanding of
the hypercomplex climatic and biological systems that we are trying to predict.
The fossil record is difficult to use, but it provides the only examples we have of
events and states that occurred but can no longer be observed directly. Figur-
ing out how to interpret the fossil record is now more important than ever. So
is the advice given by Herodotus: “Study the past.”

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CHAPTER
12

Plant Response to Multiple

Environmental Stresses: Implications for
Climatic Change and Biodiversity

IRWIN N. FORSETH
Associate Professor, Department of Botany, University of Maryland, College Park

Currently it is estimated that about 25,000 of the more than 250,000 species
of plants on Earth are classified as extinct, endangered, or vulnerable (Prance,
1990). Causes of past extinctions and present endangerments encompass a vari-
ety of activities associated with the growing human population, including
browsing and overgrazing, land clearing for agriculture, deforestation, collec-
tion of rare or valuable species, loss of interactive organisms, and the introduc-
tion of aggressive exotic species of plants. Documentation of the effects of de-
forestation or invasion of alien species has occurred. However, the assessment
of human-caused climatic changes on present and future plant biodiversity lev-
els is a more difficult undertaking.
Anthropogenic sources of tropospheric gases such as carbon dioxide (CO2),
methane (CH4), chlorofluorocarbons (CFCs), sulfur dioxide (SO2), and nitrogen
oxides (NOx) have been rising dramatically since the start of the Industrial Revo-
lution (Bolin, 1991). These gases have the ability to absorb infrared radiation
and reradiate it back to Earth. The “greenhouse effect” that this process causes
is well established in the atmospheric sciences. In fact, it is calculated that with-
out the preindustrial concentration of these trace gases, average global tempera-
tures would be approximately 33°C lower than they are presently (Bolin, 1991;
Schneider, 1993). Thus, the increase in concentration of these gases has resulted
in predictions of an increase in mean global temperatures. Predictions of this
effect range from 1.5 to 4.5°C if CO2 levels double over the next century
(Schneider, 1993).
Many of the projections about future global climates come from general
circulation models (GCMs). These models have variations and uncertainties in

187

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their projections and in their ability to model the Earth’s climate. However,
they do provide plausible regional scenarios of climatic change that ecologists
can use to examine community and ecosystem responses (Schneider, 1993). All
models show substantial changes in climate when CO2 is doubled. Most models
project greater temperature increases in midlatitude, temperate regions and in
midcontinental regions, relative to overall global means (Schneider, 1993). In
addition, many of these models predict that changes in regional precipitation
patterns will occur, with decreases in midlatitude areas. These areas are cur-
rently major crop-producing regions of the world. A final prediction of many
GCMs is that doubling CO2 concentrations in the atmosphere may lead to in-
creased occurrences of extreme events, such as major storms, long droughts,
severe cold spells, or prolonged heat waves (Schneider, 1993). Because of the
vulnerability of small populations to extreme climatic events, these latter occur-
rences are of special concern to ecologists and issues of biodiversity.

LESSONS FROM THE PAST

Paleoecologists study the way biological communities have responded to
environmental changes in the past. Davis (1989) lists four valuable insights
gained from paleoecological research that are important to research on global
change. The first insight is that species respond individually to climate. For
example, over the last 18,000 years, species composition of forests in North
America has changed considerably (Davis, 1981; Webb, 1987). Some forest com-
munities have reached their present species composition only within the last
2,000 years (Davis, 1981). Thus, it is unrealistic to assume that whole communi-
ties or biomes will change in concert in response to climatic change.
A second insight is that responses of species to climatic change often occur
with time lags (Davis, 1989). These lags vary among species, and those with long
time constants may be particularly vulnerable to rapid climatic changes. With
the rapid changes predicted for the next 200 years, the capacity for most species
to disperse and establish new populations in suitable regions will be over-
whelmed (Davis and Zabinski, 1992). For example, Davis (1990) examined the
fossil record of eastern hemlock (Tsuga canadensis) pollen over the last 10,000
years in North America. The frontier of the species moved northward and west-
ward at an average rate of 20-25 km per century (Davis, 1981, 1990). Using
current predictions of temperature change, temperature isotherms will move
northward at a rate of 300 km over the next 100 years (Davis, 1990). Even the
most rapid rate of 50 km per century documented for hemlock in eastern upper
Michigan (Davis et al., 1986) is too slow to keep up with this rate of temperature
change. In the past, T. canadensis has expanded from outlying populations that
are 50-100 km past the main boundary of the population (Davis, 1990). How-
ever, such populations may not play as large a role in future expansion of the
species due to a reduction in their number from logging and other forms of

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PLANT RESPONSE TO MULTIPLE ENVIRONMENTAL STRESSES / 189

human disturbance. Other impediments to the response of T. canadensis to cli-

matic change are: a reduction in the strength of seed sources due to human-
caused decreases in hemlock abundance throughout its range; a loss of old
growth forests, which provide dead logs that are sites for germination and es-
tablishment of hemlock seedlings; and increased herbivory by dense popula-
tions of deer that reduce hemlock reproduction (Davis, 1990).
A third relevant insight is that disturbance regimes will change as climate
changes. For example, in the White Mountains of New Hampshire, wind always
has been an important source of disturbance near the treeline (Spear, 1989).
However, at low elevations, fire was the most important source of disturbance
up to 7,000 years ago, when more mesic conditions caused it to be supplanted in
importance by windstorms (Davis, 1985). Changes in disturbance regime may
produce a larger change in vegetation than would have resulted from the effects
of climatic change alone (Davis, 1989).
The final insight is that multiple environmental changes will be important
and produce ecosystems that have no modern analogs (Davis, 1989). Evidence
for this comes from the increasing divergence seen in plant assemblages from
present-day counterparts as we go further into the past. Thus, analogy with
present-day and past assemblages of species will have limited utility for predic-
tion of future ecosystems. Rather, a functional understanding of the responses
of individual species to multiple impacts will be needed to predict vegetation
responses (Davis, 1989).

RESPONSE TO CO2
Plants have strong responses to virtually every aspect of global change. For
example, many plants increase their photosynthetic carbon gain and growth in
response to increased CO2 concentration (Woodward et al., 1991). However,
there are key differences among species of plants in their response to increased
CO2. Plants with the photosynthetic pathway called C4 metabolism (because the
first products of CO2 fixation are four carbon acids) are already saturated by CO2
at current atmospheric levels. Thus, they show little, if any, increase in photo-
synthesis as CO2 concentrations increase (Woodward et al., 1991). In contrast,
plants with the C 3 photosynthetic pathway increase photosynthetic rates up to
concentrations of 1,000 parts per million (ppm) CO2 and beyond (Pearcy and
Ehleringer, 1983). These plants typically show enhanced growth rates along with
their increased photosynthetic performance.
There are also differences in response to increased CO2 levels associated
with plant life history. Hunt et al. (1991) examined the vegetative growth re-
sponses of 25 native herbaceous species of widely varying ecology to increased
CO2 concentrations. The response to a doubling of CO2 concentration varied
from no increased growth to increases up to 3.66 times that found in ambient
CO2 concentrations. Species that were classified as having a “competitive” (C)

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life history (sensu Grime, 1979) showed the greatest enhancements, while those
naturally found in stressful habitats (i.e., low nutrient or saline habitats) (S life
history), and those found in highly disturbed habitats (R or ruderal life history)
showed no enhancement in growth. Hunt et al. (1991) concluded that vegetative
communities of intermediate productivity, those that contain a combination of
suppressed competitors and more stress-tolerant species, may experience dra-
matically altered species composition under the eutrophying effects of increased
CO2 concentrations.
Plants may increase the efficiency with which they use other resources,
such as water and nitrogen, when grown under increased levels of CO2 (Morison
and Gifford, 1984). Both CO2 fixed in photosynthesis and water lost through
transpiration must pass through pores in the leaf epidermis called stomata. Gen-
erally, stomata close in response to increased CO2 concentrations. This stomatal
closure would reduce transpiration without a concomitant reduction in photo-
synthesis. Hence, water-use efficiency (the ratio of photosynthesis to transpira-
tion) may increase (Woodward et al., 1991). Countering this effect is the re-
sponse of leaf temperature to stomatal closure. With reduced stomatal apertures,
leaf temperatures generally rise, resulting in increased transpiration from the
leaf. Thus, it is not always possible to predict the exact water-use response of
plants to increased CO2. However, some plants have been found to perform bet-
ter under limited water conditions when CO2 concentrations are higher than
ambient (Marks and Strain, 1989).

RESPONSE TO TEMPERATURE
Plant response to temperature is quite variable. In terms of photosynthesis,
many plants have very broad temperature optima (Berry and Björkman, 1980),
maintaining high photosynthetic rates across a large temperature range. Addi-
tionally, photosynthesis in many plants has the ability to acclimate to changes in
temperature that occur over the span of days to weeks (Berry and Björkman,
1980). Thus, it is more likely that extreme conditions, such as unexpected frosts
or extremely hot temperatures, are more important limits to plant distribution
than is photosynthetic response to an increase in the mean ambient temperature
of a few degrees.

RESPONSE TO WATER
Water availability, either through low soil water levels or through high
evaporative demands, is the single most important environmental parameter lim-
iting plant distribution and productivity on a world-wide basis (Schulze, 1986).
There is great variability in the ability of different species of plants to survive
periods of drought. Some species are effective drought avoiders, dropping leaves

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PLANT RESPONSE TO MULTIPLE ENVIRONMENTAL STRESSES / 191

16 800

700
14

Jan-July Precip. {mm)

600
12
Species/plot

500

10
400

8
300

6 200
1982 1983 1984 1985 1986 1987 1988 1989 1990

Year
FIGURE 12-1 Species per plot (bars) in four old fields at Cedar Creek Natural History
Area from 1982-1990. Also plotted is precipitation for January through July (line). In
1988, precipitation was at a 50-year low. Data are from Tilman and El-Haddi (1992).

or closing stomata in order to reduce the incidence of water stress. Others are
capable of osmotic adjustment, which lowers the water potential at which sto-
mata close and photosynthesis ceases. One particularly illuminating study on
the potential effects of drought on biodiversity was that performed by Tilman
and El-Haddi (1992) at the University of Minnesota. Using long-term records of
the presence of species in permanent plots, they were able to examine the effect
of rare severe drought on species richness. Local species richness in four differ-
ent grassland fields fell an average of 37% during the drought year of 1988
(Figure 12-1). Even though plant biomass and precipitation recovered in 1989
and 1990, species richness did not recover. The authors attributed this to either
a lack of available propagules or a failure of young seedlings to reestablish local
populations within plots containing other established species (i.e., they were
recruitment limited). There were differences between the chance that a species
was lost and its abundance prior to 1988. In perennial grasses, forbs, legumes,
and woody species, the predrought abundance was negatively correlated with
loss from plots. These results show that some assemblages of rare species are
especially vulnerable to extinction during environmental stress, and have grave
implications for the effects of global climatic change on biodiversity.

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RESPONSE TO CO2 AND WATER

Plants rarely encounter single stresses in their environment. Rather, they
are faced with multiple environmental stressors, cooccurring in various combi-
nations and at various intensities at different times during growth. The effects
of these multiple environmental stresses can be far from additive. Some may
even counter the effect of others, e.g., increased CO2 concentrations may reduce
the effect of drought by reducing plant water loss and increasing water-use
efficiency. Thus, the ability of plants to respond to future global changes will be
complicated by the interaction of environmental variables. There have been
many studies of the response of plants to single factors, such as CO 2. Fewer
studies have been conducted under multiple environmental stresses, or in com-
bination with biotic interactions such as competition. Examples of studies that
did include multiple factors include Bazzaz and Carlson (1984), who observed
that competitive interactions changed with CO2 concentration and water avail-
ability. Under well-watered, high CO2 conditions, C3 plants were competitively
superior. However, under water-limited conditions, C4 plants were competitively
superior, regardless of CO 2 concentration. In contrast, Marks and Strain (1989)
found that under elevated levels of CO 2 Aster pilosus, an early successional C3
weed, was competitively superior to Andropogon virginicus, a C4 grass that usu-
ally displaces A. pilosus in the successional sequence, regardless of water sup-
ply. Another study that involved different levels of CO2 along a moisture gradi-
ent was conducted by Miao et al. (1992). These authors found that the magnitude
of gray birch and red maple seedling response to elevated CO2 was contingent
on soil moisture levels (Figure 12-2). Elevated CO2 modified the overall pattern
of response of these species to the soil moisture gradient. Red maple was en-
hanced preferentially at wetter ends of the gradient than was gray birch. Hence,
the niche overlaps between the species were reduced.
These studies illustrate that experiments combining various CO2 levels with
gradients of other resources can result in species-specific, nonintuitive results.
However, even these experiments lack the scale of time and area needed to effec-
tively predict ecosystem responses to climatic change.

RESPONSE TO INCREASES IN UV-B RADIATION

In addition to their effects as greenhouse gases, CFCs have the capability to
catalytically destroy stratospheric ozone. Stratospheric ozone is the primary at-
mospheric attenuator of ultraviolet-B (UV-B) radiation (280-320 nm) penetrating
the Earth’s atmosphere. For every 1% decrease in stratospheric ozone, we may
see approximately a 2% increase in UV-B radiation at the Earth’s surface. Plant
response to UV-B radiation runs the gamut from little effect to large reductions
in photosynthesis and growth (Teramura, 1983). An elegant, long-term study
conducted by Barnes et al. (1988) illustrates the type of subtle effects that in-

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PLANT RESPONSE TO MULTIPLE ENVIRONMENTAL STRESSES / 193

80 Birch Maple
Niche breadth -5% -23%
Niche overlap -11% Gray birch
60
Red maple
% Increase 350 – 700

40

20

0
Very dry Dry Moist Flooded

FIGURE 12-2 Percentage increase in biomass of gray birch (solid bars) and red maple
(shaded bars) when grown in 700 ppm CO 2 versus 350 ppm CO2. Plants were grown in
different moisture conditions, as indicated on the graph. Also shown is the degree of
niche breadth for moisture when plants were grown in 700 ppm CO2 compared to 350
ppm CO2 . Niche overlap represents the reduction in overlap in moisture regimes for the
two species when grown in 700 ppm CO2 compared to 350 ppm CO2 . From Miao et al.
(1992).

creased UV-B may have on species mixtures. The authors found that supple-
mental UV-B radiation had little effect on wheat or wild oat plants grown in
monoculture. However, enhanced UV-B did alter the competitive balance be-
tween the two species studied, especially during wet years (Table 12-1). The
mechanism of this effect was a change in the amount of leaf area with height that
the two species showed when grown in mixtures. The authors concluded that
changes in competitive balance in terrestrial plants may be a more sensitive
indicator of solar UV augmentation than changes in total biomass of plants.
There have been several studies of the interaction of UV-B radiation with
other environmental variables, such as light level, nutrient availability, and
water stress. In general, the effects of UV-B radiation are reduced under water
stress and low nutrient availabilities, and enhanced under low ambient light
levels (Sullivan and Teramura, 1989; Tevini and Teramura, 1989). Recently, sev-
eral studies have examined the interaction between UV-B radiation and increased
CO2 concentrations. In several species of crops, the effects of increased CO2 con-

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TABLE 12-1 Results of a Four-Year Study of Competition Between

Wheat (Triticum aestivum) and Wild Oat (Avena fatua) Exposed to
Enhanced UV-B Radiation

Precipitation Crowding Coefficient

Year (mm) Control UV-B

1981 17 0.94 1.28

1982 37 1.16 1.39a
1983 17 1.36 1.11
1984 91 1.24 1.82a
1985 43 1.66 1.65
1986 3 1.28 1.44

aSignificantly different at p<0.05.

NOTE: Enhancements of UV-B ranged from that expected from a 16% reduction in
stratospheric ozone to that expected after a 40% reduction in stratospheric ozone.
Any value of crowding coefficient above 1.0 indicates superior competitive ability for
wheat.
SOURCE: Barnes et al. (1988).

centrations were eliminated or reduced by supplemental levels of UV-B radia-

tion (Teramura et al., 1990; Ziska and Teramura, 1992). In Pinus taeda (loblolly
pine), supplemental UV-B radiation not only reduced the growth enhancements
caused by high levels of CO2 but also altered allocation patterns to above-ground
versus below-ground organs (Sullivan and Teramura, 1994). The authors con-
cluded that this may have ramifications for seedling establishment, growth, and
competitive interactions of this species in the field.

RESPONSES OF NATIVE VERSUS EXOTIC SPECIES

An important aspect of the response of native plants to global change is the
potential for altered interactions with introduced species. For example, in the
southeastern United States, two weedy vine exotics are especially successful,
Kudzu (Pueraria lobata) and Japanese honeysuckle (Lonicera japonica). These
two species have several properties that may allow them to spread even more in
future environments. Since they are exotics to North America, they have few
natural enemies. They are weedy, with very good colonization abilities. They
are vines, with large allocation of carbon to above-ground stems and leaves.
They respond very strongly to increased levels of CO2 with increased elongation
and above-ground growth (Sasek and Strain, 1988, 1989, 1991). Presently, their
northern distribution limits are set by low winter temperatures and the date of
the first hard fall frost. As temperatures and CO2 levels rise, they may become
even more aggressive competitors in their spread northward. Competition be-

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PLANT RESPONSE TO MULTIPLE ENVIRONMENTAL STRESSES / 195

tween these weedy aggressive exotics and rare native species—already endan-
gered and placed under stress by high temperatures and increased periods of
drought—may further reduce the biodiversity of native floras.

CONCLUSIONS
Human activities such as land clearing and burning of fossil fuel have caused
a continuing increase in the concentration of greenhouse gases, especially CO 2 in
the atmosphere. These gases are long-lived enough to remain in high concentra-
tions in the atmosphere for the next century or more, even with immediate re-
ductions in their emission. Projections of their effects on global climate include
increased ambient temperatures, increased ambient UV-B radiation, changes in
precipitation patterns and amounts, and increased occurrences of extreme
weather events. Plants have strong responses to all of these predicted changes.
Of primary importance is the fact that species of plants all respond individually
and in different degrees to environmental conditions. Hence, the composition
and distribution of species within present-day communities are likely to change.
Altered competitive interactions and climatic conditions are bound to lead to
loss of more species. This response may be exacerbated by the continuing spread
of aggressive weedy exotics. So far, research has been concentrated at the level
of responses of species to single environmental variables. New studies incorpo-
rating multiple environmental factors and multiple species have shown com-
plex, species-specific results. Larger, longer-term studies of this type are needed
before we can predict accurately the extent and nature of global change on plant
biodiversity.

REFERENCES
Bazzaz, F. A., and R. W. Carlson. 1984. The response of plants to elevated CO 2. I. Competition
among an assemblage of annuals at two levels of soil moisture. Oecologia 62:196-198.
Barnes, P. W., P. W. Jordan, W. G. Gold, S. D. Flint, and M. M. Caldwell. 1988. Competition,
morphology and canopy structure in wheat (Triticum aestivum L.) and wild oat (Avena fatua
L.) exposed to enhanced ultraviolet-B radiation. Func. Ecol. 2:319-330.
Berry, J., and O. Björkman. 1980. Photosynthetic response and adaptation to temperature in higher
plants. Ann. Rev. Plant Physiol. 31:491-543.
Bolin, B. 1991. Man-induced global change of climate: The IPCC findings and continuing uncer-
tainty regarding preventive action. Envir. Conserv. 18:297-303.
Davis, M. B. 1981. Quaternary history and the stability of forest communities. Pp. 132-153 in D. C.
West, H. H. Shugart, D. B. Botkin, eds., Forest Succession: Concepts and Application. Springer-
Verlag, N.Y.
Davis, M. B. 1985. History of the vegetation on the Mirror Lake watershed. Pp. 53-65 in G. E. Likens,
ed., An Ecosystem Approach to Aquatic Ecology: Mirror Lake and its Environment. Springer-
Verlag, N.Y.
Davis, M. B. 1989. Insights from paleoecology on global change. Bull. Ecol. Soc. Amer. 70:222-228.
Davis, M. B. 1990. Climatic change and the survival of forest species. Pp. 99-110 in G. M. Woodwell,
ed., The Earth in Transition. Patterns and Processes of Biotic Impoverishment. Cambridge
University Press, Cambridge, England.

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Davis, M. B., K. D. Woods, S. L. Webb, and R. P. Futuyma. 1986. Dispersal versus climate: Expan-
sion of Fagus and Tsuga in the upper Great Lakes region. Vegatatio 67:93-103.
Davis, M. B., and C. Zabinski. 1992. Changes in geographical range resulting from greenhouse warm-
ing: Effects on biodiversity in forests. Pp. 297-308 in R. Peters and T. Lovejoy, eds., Global
Warming and Biological Diversity. Yale University Press, New Haven, Conn.
Grime, J. P. 1979. Plant Strategies and Vegetation Processes. John Wiley and Sons, N.Y.
Hunt, R., D. W. Hand, M. A. Hannah, and A. M. Neal. 1991. Response to CO 2 enrichment in 27
herbaceous species. Func. Ecol. 5:410-421.
Marks, S., and B. R. Strain. 1989. Effects of drought and CO2 enrichment on competition between
two old-field perennials. New Phytol. 111:181-186.
Miao, S. L., P. M. Wayne, and F. A. Bazzaz. 1992. Elevated CO2 differentially alters the responses of
co-occurring birch and maple seedlings to a moisture gradient. Oecologia 90:300-304.
Morison, J. I. L., and R. M. Gifford. 1984. Plant growth and water use with limited water supply in
high CO2 concentrations. II. Plant dry weight, partitioning and water use efficiency. Aust. J.
Plant Physiol. 11:375-384.
Pearcy, R. W., and J. R. Ehleringer. 1983. Comparative ecophysiology of C 3 and C 4 plants. Plant Cell
Envir. 7:1-13.
Prance, G. T. 1990. Flora. Pp. 387-391 in B. L. Turner II, W. C. Clark, R. W. Katz, J. F. Richards, J.
T. Mathews, and W. B. Meyer, eds., The Earth as Transformed by Human Action: Global and
Regional Changes in the Biosphere Over the Past 300 Years. Cambridge University Press, N.Y.
Sasek, T. W., and B. R. Strain. 1988. Effects of carbon dioxide enrichment on the growth and mor-
phology of kudzu (Pueraria lobata). Weed Sci. 36:28-36.
Sasek, T. W., and B. R. Strain. 1989. Effects of carbon dioxide enrichment on the expansion and size
of kudzu (Pueraria lobata) leaves. Weed Sci. 37:23-28.
Sasek, T., and B. Strain. 1991. Effects of CO 2 enrichment on the growth and morphology of a native
and an introduced honeysuckle vine. Amer. J. Bot. 78:69-75.
Schneider, S. H. 1993. Scenarios of global warming. Pp. 9-23 in P. M. Kareiva, J. G. Kingsolver, R. B.
Huey, eds., Biotic Interactions and Global Change. Sinauer Associates, Sunderland, Mass.
Schulze, E.-D. 1986. Carbon dioxide and water vapor exchange in response to drought in the atmo-
sphere and in the soil. Ann. Rev. Plant Physiol. 37:247-274.
Spear, R. W. 1989. Late-Quaternary history of high-elevation vegetation in the White Mountains of
New Hampshire. Ecol. Monogr. 59:125-151.
Sullivan, J. H., and A. H. Teramura. 1989. Field study of the interaction between solar ultraviolet-
B radiation and drought on photosynthesis and growth in soybean. Plant Physiol. 92:141-146.
Sullivan, J. H., and A. H. Teramura. 1994. The effects of UV-B radiation on loblolly pine. 3. Interac-
tion with CO2 enhancement. Plant Cell Envir. 17:311-317.
Teramura, A. H. 1983. Effects of ultraviolet-B radiation on the growth and yield of crop plants.
Physiol. Plantarum 58:415-427.
Teramura, A. H., J. H. Sullivan, and L. H. Ziska. 1990. Interaction of elevated ultraviolet-B radiation
and CO2 on productivity and photosynthetic characteristics in wheat, rice, and soybean. Plant
Physiol. 94:470-475.
Tevini, M. M., and A. H. Teramura. 1989. UV-B effects on terrestrial plants. Photochem. Photobiol.
50:479-487.
Tilman, D., and A. El-Haddi. 1992. Drought and biodiversity in grasslands. Oecologia 89:257-264.
Webb, T., III. 1987. The appearance and disappearance of major vegetational assemblages: Long-
term vegetational dynamics in eastern North America. Vegatatio 69:177-187.
Woodward, F. I., G. B. Thompson, and I. F. McKee. 1991. The effects of elevated concentrations of
carbon dioxide on individual plants, populations, communities and ecosystems. Ann. Bot.
67:23-38.
Ziska, L. H., and A. H. Teramura. 1992. CO2 enhancement of growth and photosynthesis in rice
(Oryza sativa): Modification by increased ultraviolet-B radiation. Plant Physiol. 99:473-481.

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CHAPTER
13

Names: The Keys to Biodiversity

F. CHRISTIAN THOMPSON
Research Entomologist, Systematic Entomology Laboratory,
Plant Sciences Institute, Beltsville Agricultural Research Center,
United Stated Department of Agriculture, Washington, D.C.

Besides biodiversity, the one thing that all the chapters included in this
volume have in common is scientific names. These names form the essential
language, the means we use to communicate about biodiversity. To avoid a
Tower of Babel, a common system of nomenclature is required: a system that is
effective and efficient (and at minimal cost). Presented below are the essential
aspects of this language for biodiversity and a discussion of where we are in
respect to their implementation.
The long-term conservation of biodiversity can be achieved only through
the approach used by the Instituto Nacional de Biodiversidad (INBio)—“save
it,” “characterize it,” and “sustainably use it” (Janzen, Chapter 27 of this vol-
ume). Characterization requires that we have a language with which to commu-
nicate about biodiversity: a way of describing it, so that we all know what we
are talking about and that we are talking about the same things. How do we
characterize biodiversity? The first step is to name its components. Biodiversity
is divisible into three levels: ecological, taxonomic, and genetic. Of these levels,
taxonomic diversity is critical because taxa are the units that contain genetic
diversity and are the units that make up ecological diversity. Since taxa are the
core of biodiversity, names for taxa are the most critical component of any lan-
guage of biodiversity.

A UNIVERSAL LANGUAGE OF BIODIVERSITY

What are names? Names are tags. Tags are words, short sequences of sym-
bols that are used in place of something complex which would require many

199

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200 / BIODIVERSITY II

more words to describe. Hence, tags save time and space. Instead of a long
description, we use a short tag. A scientific name differs from a common name
in that the scientific name is a unique tag. In other languages, there may be
multiple tags for the same thing. Imagine the various words in English that are
used to describe Homo sapiens. In computer (database) jargon, data elements
that are used to index information are termed keys, and keys that are unique are
called primary keys. Scientific names are primary keys. The word “key” has
another meaning in English, which is “something that unlocks something.” Sci-
entific names are those critical keys that unlock biosystematic information, all
that we know about living organisms. Scientific names are tags that replace
descriptions of objects or, more precisely, concepts based on objects (specimens).
Scientific names are unique, there being only one scientific name for a particular
concept, and each concept has only one scientific name.
Scientific names are more than just primary keys to information. They rep-
resent hypotheses. To systematists, this is a trivial characteristic that sometimes
is forgotten and thereby becomes a source of confusion later. To most users, this
is an unknown characteristic that prevents them from obtaining the full value
from scientific names. If a scientific name were only a unique key used for
storing and retrieving information, it would be just like a social security num-
ber. Homo sapiens is a unique key used to store and retrieve information about
man, but that key also places the information about man into a hierarchical
classification. Hierarchical classifications allow for the storage, at each node of
the hierarchy, information common to the subordinate nodes. Hence, redun-
dant data, which would be spread throughout a nonhierarchical system, are
eliminated.
Biological classifications, however, do more than just hierarchically store
information. Given that one accepts a single common (unique) history for life
and that our biological classifications reflect this common history in their hier-
archical arrangement, then biological classifications allow for prediction: they
allow us to predict that some information stored at a lower hierarchical node
may belong to a higher node that is common to all members of the more inclu-
sive group. These predictions take the form of the following: if some members
of a group share a characteristic that is unknown for other members of the same
group, then that characteristic is likely to be common to all members of the
group.
So scientific names are tags, unique keys, hierarchical nodes, and phyloge-
netic hypotheses. Thus, systematists pack a lot of information into their names
and users can get a lot from them.
Scientific names are hypotheses, not proven facts. Systematists may and
frequently do disagree about hypotheses. Hypotheses, which in systematics
range from what is a character to what is the classification that best reflects the
history of life, are always prone to falsification, and, hence, change. Disagree-
ments about classification can arise from differences in paradigm or information.

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NAMES: THE KEYS TO BIODIVERSITY / 201

Systematists use different approaches to construct classifications, such as cladis-

tic versus phylogenetic versus phenetic methods. Given the same set of data that
underlies a given hierarchy, cladists can derive classifications that are different
from those derived by the phenetists (Figure 13-1). Even among cladists, there
can be differences as to the rank (genus, family, order, etc.) and thereby the
hierarchical groups used. These are disagreements based on paradigm. There
can be disagreement about the hypotheses that underlie the information used to
construct the classifications, such as what are the characters. Disagreement can
arise among systematists because they use different information. While dis-
agreements will affect the ability to predict, they need not affect the ability to
retrieve information.
The desirable attribute that must be preserved to ensure complete access to
information across multiple classifications is uniqueness. Our scientific nomen-
clature must guarantee that any scientific name which is used in any classifica-
tion is unique among all classifications. This can be assured by having two
primary keys. Unfortunately, having two keys increases the overhead of our
information systems. Most systematists and all users want to avoid this problem

FIGURE 13-1 Multiple classifications for identical cladistic hypotheses.

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202 / BIODIVERSITY II

by mandating that there be only one classification. Although in theory there is

only one correct classification, as there was only one history of life, in reality
there have been multiple classifications in the past, there may be multiple clas-
sifications in use today, and there will be multiple classifications in the future.
That is the price of scientific progress, of the increase in our knowledge of the
world. If information is to be retrieved across time, if we want to extract infor-
mation stored under obsolete classifications, and if we want to avoid dictating
“the correct” classification, then we need a nomenclatural system that supports
two unique keys.
The two keys for our language of biodiversity are the valid name and the
original name. The valid name is the correct name for a concept within a classi-
fication; the original name is the valid name in the classification in which it was
proposed. Valid names may be different among classifications, but the original
name is invariant across classifications (Table 13-1). Valid names are the best
names to use because they provide the full value of scientific names. These are
the names that provide a basis for prediction. The original name is useful only
for retrieval of information across multiple classifications. Although valid and
original names may be and frequently are the same, users must know the differ-
ences between them. Specifically, they need to know that a valid name is a
powerful tool for inference, that a valid name provides for prediction of un-
known attributes of the organism that bears the name. But they must under-
stand that there may be multiple valid names in the literature or in use, and that
valid names represent hypotheses that may change as our knowledge is tested
and improved. Most importantly, if there are multiple valid names in use, then
the users must be aware that there are conflicting scientific hypotheses being
advocated and that they must select the name that best serves their purpose. If
users do not want to decide, do not want to use classifications to organize and
synthesize their information, then they may use the original name to index their
information, being assured that it will always be a unique key.
There are other problems today with our classifications: synonymy (having
two names for the same concept) and homonymy (having the same name for

TABLE 13-1 Multiple Classifications and Primary Keys to Information

Year Valid Name Original Name Authority

1776 Musca balteata Musca balteata De Geer

1822 Syrphus balteatus Musca balteata Meigen
1843 Scaeva balteatus Musca balteata Zetterstedt
1917 Episyrphus balteatus Musca balteata Matsumura
1930 Epistrophe balteata Musca balteata Sack
1950 Stenosyrphus balteatus Musca balteata Fluke
Today Episyrphus balteatus Musca balteata Vockeroth

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NAMES: THE KEYS TO BIODIVERSITY / 203

different concepts). These problems are, however, largely due to ignorance. If

we knew all names and their types and could agree on what are species, then by
applying the rules of nomenclature we immediately could eliminate all problems
of synonymy and homonymy. Homonymy is eliminated by the rule of unique-
ness. Synonymy is addressed by the rules of typification, which tie a physical
instance of a concept to a name. Synonymy is resolved by logic of circumscrip-
tion and the convention of priority (or usage). The name of a concept is the
name affixed to one and only one of the types that falls within its circumscrip-
tion. The name used is determined by which name is the oldest (priority) or
most widely used (usage). The specific rules for resolving homonymy and syn-
onymy, as well as for the proper formation and documentation of names, are our
Codes of Nomenclature (IBC, 1988; ICZN, 1985; Lapage et al., 1975). These rules,
however, do not address the problem of multiple classifications or ignorance of
the universe of applicable names and their typification.
There is one final problem, the species problem. This is the problem of the
basic unit of information or data. The basic unit of information for nomencla-
ture is the species (or more precisely the species-group, which includes the cat-
egory of subspecies). The problem is that the species is not a single element of
datum, but consists of information—data derived from specimens that have been
identified as belonging to that species. Mistakes can be made during this iden-
tification, which is another hypothesis. Information ultimately is not derived
from species, but from specimens. Information management in biodiversity re-
ally begins with data management of specimens. The problems of specimen-
based data management are not intractable, but are readily addressed by the use
of bar-codes, another form of unique keys.
The species problem is also one of circumscription, the definition of the
limits of a taxon. A group with the same name and type may be more or less
inclusive, depending on the characters used to define its limits. Zoologists differ
from botanists in not considering circumscription to be a problem because, mini-
mally, all identically named taxa have at least some characteristics in common.
The problem of how much is held in common, therefore, is best resolved by
enumeration of the included taxa or specimens. The history of circumscription
can be tracked by use of an additional key that uniquely identifies the person
who defined the limits and the date of that action. It is sufficient for our pur-
poses to know that data based on specimens always will be summarized into
information units based on species and that all such information should be based
on specimens.

THE REAL WORLD: DIVERSITY AND DISPERSION

The All Taxa Biodiversity Inventories (ATBIs), taxasphere, national bio-
logical surveys, etc., are means of addressing the problem of characterization of
biodiversity, the most important step in conserving biodiversity. To character-

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204 / BIODIVERSITY II

ize, a language is needed. To characterize biodiversity, all our available resources

will be needed because the task is immense (WCMC, 1992). The resources for
characterizing biodiversity are diverse and dispersed. The only way the job is
going to get done is by forming partnerships, by working together. That re-
quires communications that can accommodate the diversity and dispersion.
If there were only one classification, if that classification were controlled by
one person, and if all information were stored in one system at one place under
that classification, then there would be one source for answers to questions about
biodiversity. Unique and comprehensive information systems are powerful
tools. In reality, however, things are different. Different classifications exist
and resources are dispersed. To share resources, therefore, different classifica-
tions must be understood. To utilize distributed resources, a universal commu-
nication system that allows multiple classifications is needed. Scientific nomen-
clature provides the basis for this system: a set of unique keys to traverse the
world of distributed databases, to find information anywhere on our future in-
formation superhighways. However, to make the system work, a universal data
dictionary is required. Such a dictionary would allow users with any name to
find the keys to unlock information about biodiversity. A universal data dictio-
nary requires that the problems of synonymy and homonymy are solved and
ensures that all classifications and names are accommodated.

PROGRESS AND PROMISE

The present language of biodiversity is binominal nomenclature that was
introduced by Carolus Linnaeus, a Swedish professor of natural history. This
system was the direct result of an earlier governmental biodiversity project.
The Swedish Crown had some far-flung possessions and wanted to know what
use could be made of them. They sent Linnaeus to investigate, to survey what
today is called biodiversity, and to write a report characterizing what was found,
with recommendations on how to use it. At the time, there was only a binary
system of nomenclature: one word for the genus, with the species being de-
scribed by a series of adjectives. Given the diversity Linnaeus found, he did not
want to waste time repeating the long strings of adjectives that were required to
characterize the biodiversity. Because the characterizations were in his flora of
Sweden, he used a combination of the genus name and a single word (an epithet)
for each species to form a unique key to those descriptions (see Stearn, 1957, for
more details). The system was an immediate success. Linnaeus codified the
system, built and maintained a universal information database for all names (his
Systema Naturae, 1758), and trained a cadre of students to carry on his work.
The students dispersed and converted others. But because no one could be the
master except Linnaeus, they divided nature up. There were to be no more
Systema Naturae. At first, there were a series of Systemae for parts of nature,
maintained by the students as the authorities for this kingdom or that area, but

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NAMES: THE KEYS TO BIODIVERSITY / 205

authorities in many countries quickly became involved. Two hundred years

later, systematists cannot tell society how many organisms have been described
or what are all their names.
What can systematists do? They can cooperate and, as a whole, recreate
what Linnaeus started: a system of nature. They can agree on and follow a set of
standards for nomenclature; ensure that those standards are adequate for our
informational needs; eliminate the chaos of the past, first by gathering together
the names that are today dispersed across a vast sea of literature, second by
putting a limit on searching the past, and finally by accepting what is found
after a reasonable search. They can ensure that the chaos will not return by
requiring wide dissemination or registration of new names.
Where are systematists today in accomplishing these tasks? On standards,
we are almost there. For bacteria, there is already a modern system of nomencla-
ture (Ride, 1991; Sneath, 1986). For zoology and botany, we will have one
shortly, and a start has been made on a universal code for all life (Hawksworth,
1994). Information about proposed changes in the botanical code are published
regularly in the journal Taxon, and those for the zoological code in Bulletin of
Zoological Nomenclature. A new draft version of the International Code of Zoo-
logical Nomenclature is now available for comment and can be adopted as soon as
a year hence. With the acceptance of this new Code, the problems of name
changes due to nomenclature will be eliminated. Some systematists are afraid
that the new Code will be used to enforce the acceptance of one classification,
rather than allow for a diversity of them. Such fears are unfounded because the
new draft will preserve the “freedom of taxonomic thought and action.” The
draft includes new requirements stating that zoologists must document prop-
erly their classifications (implicit typification will be required for all names) and
publish them where the whole community can evaluate them. This will be
achieved by a registration system for new names. Bacteriology already requires
this and botany has adopted it for the future. The new draft will be simpler to
use, since the strict requirement of Latin grammar will be eliminated. Stability
and universality will be enhanced by allowing zoologists to balance usage and
priority more effectively in the determination of valid names. Finally, the new
draft will provide the means to certify names and the associated nomenclatural
data en masse, so as to free zoologists of the burdens of historical searches.
The last 250 years have left scientific names scattered across the most di-
verse array of media possible. No other science requires its practitioners to be
responsible for such a mess. Scientists are expected to know the common and
current hypotheses. They should not be required to know what was printed
200 years ago, distributed, and subsequently forgotten and largely lost. Sys-
tematists must deal with such ancient history, regardless of whether the concept
had been published previously, was rediscovered subsequently, or was invalid.
That forgotten name need not even be in the domain of the systematist’s exper-
tise to cause problems.

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206 / BIODIVERSITY II

The solution for systematics is simple: change the rules of nomenclature.

This is being done. Then make a reasonable effort to gather together all the
existing names and associated data and accept those names and data as correct.
That will free systematists of the burden of history for nomenclature’s sake.
The Systematic Entomology Laboratory of the U.S. Department of Agricul-
ture has embarked on a voyage to do just this for insect names. We have pro-
posed to the entomological community that together we develop a comprehen-
sive database of names of terrestrial arthropods. We christened our ship BIOTA
(Biosystematic Information on Terrestrial Arthropods). The most immediate and
highest priority is to document all the names of terrestrial arthropods known to
occur in North America. This represents the official adoption of the goal of the
Entomological Collections Network, originally proposed by Miller (1992). We
expect to reach this point within 2 years. We already have accumulated nearly
100,000 names and have commitments from cooperating specialists for another
40,000. This nomenclatorial database will include the essential keys, both the
valid name and the original name for each species, that our specialists have
recognized. The specialists will be identified in the data record, and minimal
classificatory data, such as subfamily, family, order, and class, will be included.
All synonyms, homonyms (all available names, sensu Zoological Code [ICZN,
1985]) and common invalid combinations (names valid under other classifica-
tions) and misidentifications will be included. This information will provide the
community with the necessary keys to the biodiversity of arthropods.
BIOTA also includes more comprehensive cataloging efforts, such as the
Biosystematic Database of World Diptera. These efforts will include data on
typification of names. The resultant catalogs will be submitted to the appropri-
ate user-community for review and eventually to the International Commission
of Zoological Nomenclature for certification. The Diptera database project has
been endorsed by the International Congresses of Dipterology and is overseen
by a committee of the Council for those Congresses (the committee is a scientific
member of the International Union of Biological Sciences). The family-group
names, those names that may apply to the higher levels of classification, are
nearing completion as the result of a 50-year effort by Curtis W. Sabrosky, one
of our U.S.D.A. specialists. Some 4,296 names have been documented. Genus-
group names have been entered and shortly will be distributed to specialists.
Some 17,271 names were found, representing perhaps 8,000 valid genera. Names
of species-groups are being entered now, with some 45,994 already in the data-
base, perhaps 40% of the world total. All names for the flies of the Nearctic
region have been entered and will be published shortly (28,890 names for 19,562
species and 2,356 genera).
Similar efforts are underway or already completed for other major groups of
organisms (Bisby, 1994). Given continued support, we are likely to see the prob-
lems of names solved by the year 2000. Nomenclature no longer will be an
impediment to efforts to characterize our biodiversity. We then will have a set

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NAMES: THE KEYS TO BIODIVERSITY / 207

of keys to what we know of biodiversity and a language capable of effectively

and efficiently incorporating new information and accommodating diverse keys
to that information.

SERVICE TO SOCIETY
Names are the keys to biodiversity, but what does one do when one has no
name, only a specimen? How does one discover the proper name for a speci-
men? If it is a bird, one can use a field guide, like Peterson’s (1980), to identify
it. If not, one asks an expert. If it is an insect, one will find those experts at the
Systematic Entomology Laboratory (SEL), which identifies more insects than
any other organization. But identification has costs: when experts identify speci-
mens, they are not building classifications nor describing new biodiversity.
Realizing the existing shortage of experts to classify specimens, SEL sought new
approaches to relieve their experts of the burdens and distractions of identifica-
tion.
The obvious answer was found within the question: if one does not need
experts to identify birds, why does one need them to identify flies? Peterson
(1980) proved that, if users were presented with the critical characters (his field
marks) in a graphic way, then users readily could identify birds. Many of the
field marks used in Peterson’s field guides were known to Linnaeus 200 years
ago, but Linnaean descriptions are difficult for users to understand. Compare,
for example, the plate of common ducks in Peterson’s field guide (Peterson,
1980:51) and the corresponding page from Linnaeus’ Systema Naturae (Linnaeus,
1758: 126) (Figure 13-2). As good as Peterson field guides are, they, like the
traditional identification key, are rather inflexible. To identify, for example, a
pintail, one must first know that it is a duck, a freshwater dabbler, or one must
thumb through the pages of the field guide until the appropriate picture is found.
With a computerized identification system, the user can select the most obvious
character, such as the long tail. Then the computer would list the dozen or so
species that have long tails. The user could ask the computer what are the best
characters to discriminate among these species, and the computer would re-
spond with a ranked list of the most useful characters, some of which may be
head color, body shape, habitat, and geography.
A computerized identification system that builds on and extends the visual
approach of Peterson has been produced. The Fruit Fly Expert System allows
users to identify some 200 fruit flies, including all the important species of pests
(Thompson, et al., 1993). The system uses data encoded in the standard DELTA
(DEscriptive Language for TAxonomy; Pankhurst, 1993) format, so other data
sets can be prepared easily. The system is extremely flexible. Many taxa can be
eliminated immediately by restricting the data set according to geographic loca-
tion (Figure 13-3B) or other biological data. Any character can be chosen in any
order, or the computer can list the best characters based on their ability to sepa-

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FIGURE 13-2 Examples of identification aids. A. Systema Naturae (1758); B. Peterson’s

Field Guide to the Birds (1980).

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FIGURE 13-3 Computer screens from the Fruit Fly Expert System. A. Menu for commands; B. Character image for biogeographic regions; C.
Character image for body color; D. Taxon image for Mediterranean fruit fly, Ceratitis capitata.
NAMES: THE KEYS TO BIODIVERSITY / 209
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210 / BIODIVERSITY II

rate the remaining taxa. Characters are illustrated and multiple states are al-
lowed (Figure 13-3C). This speeds the identification process in two ways, by
enabling direct comparison of images with the specimen and by reducing the
total number of decisions that must be made, because more than the traditional
two alternatives can be evaluated efficiently at one time. Characters and com-
puter commands are explained in help files that can be accessed at any time.
Computer commands are either selected from menus or entered directly (Figure
13-3A). How closely a specimen must match characters (the error limit) can be
set, so more matches must be made before a taxon is rejected. Errors, once
detected, can be corrected easily without stepping through all the characters
again. The identification can be verified easily. The computer can generate a
complete description and image of any taxon (Figure 13-3D), list only the differ-
ences between the specimen and another taxon or between any two taxa, or
generate a list of all the diagnostic characters for a particular taxon. The Expert
System is not a panacea: unusual specimens, those outside the domain of the
data set or with distorted features, still will have to be sent to systematists.
Systematists are still needed, but by relieving them of most routine identifica-
tions, they can be more productive, and users will get their identifications faster.

CONCLUSION
The Systematic Entomology Laboratory has been and is committed to the
characterization of biodiversity to help society develop an understanding of
biodiversity and the ability to use it wisely. We are building classifications, a
set of keys to enable us to better communicate about biodiversity. We also are
committed to developing tools, such as expert systems and biosystematic infor-
mation databases, to allow users to obtain these keys (names) and to know what
are the best keys (valid names).

REFERENCES
Bisby, F. 1994. Global master species databases and biodiversity. Biol. Int. 29:33-38.
Hawksworth, D. L. 1994. Developing the bionomenclatural base crucial to biodiversity programmes.
Biol. Int. 29:24-32.
International Botanical Congress. 1994. International Code of Botanical Nomenclature (adopted by
the Fourteenth International Botanical Congress, Berlin, July - August 1987). Regnum
Vegetabile 131. Koeltz Scientific Books, Königstein, Germany. 328 pp.
International Commission on Zoological Nomenclature. 1985. International Code of Zoological No-
menclature, third ed. International Trust for Zoological Nomenclature, London. 338 pp.
Linnaeus, C. 1758. Systema Naturae, tenth ed. L. Salvii, Stockholm. 824 pp.
Miller, S. E. 1992. Specimen databases and the lack of standard nomenclature: A proposal for North
American insects. Insect Coll. News 7:7-8.
Pankhurst, R. J. 1991. Practical Taxonomic Computing. Cambridge University Press, Cambridge,
England. 202 pp.

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NAMES: THE KEYS TO BIODIVERSITY / 211

Peterson, R. T. 1980. A Field Guide to the Birds. A Completely New Guide to All the Birds of
Eastern and Central North America. Houghton Mifflin, Boston. 384 pp.
Ride, W. D. L. 1991. Justice for the living. A review of bacteriological and zoological initiatives in
nomenclature. Pp. 105-122 in D. L. Hawksworth, ed., Improving the Stability of Names: Needs
and Options. Regnum Vegetabile 123. Koeltz Scientific Books, Königstein, Germany. 358 pp.
Sneath, P. H. A. 1986. Nomenclature of Bacteria. Pp. 36-48 in W. D. L. Ride and T. Younès, eds.,
Biological Nomenclature Today. IRL Press, Eynsham, England. 70 pp.
Sneath, P. H. A., ed. 1992. International Code of Nomenclature for Bacteria. 1990 Revision. Ameri-
can Society for Microbiology, Washington, D.C. 232 pp.
Stearn, W. T. 1957. An introduction to the Species Plantarum and cognate botanical works of Carl
Linnaeus. In C. Linnaeus, Species Plantarum (a facsimile of the first edition of 1753). The Ray
Society, London. 176 pp.
Thompson, F. C., A. L. Norrbom, L. E. Carroll and I. M. White. 1993. The fruit fly biosystematic
information database. Pp. 3-7 in M. Aluja and P. Liedo, eds., Fruit Flies: Biology and Manage-
ment. Springer-Verlag, N.Y.
World Conservation Monitoring Centre. 1992. Global Biodiversity. Status of the Earth’s Living
Resources. Chapman and Hall, London. 585 pp.

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CHAPTER
14

Systematics: A Keystone to
Understanding Biodiversity

RUTH PATRICK
Francis Boyer Chair of Limnology, Academy of Natural
Sciences of Philadelphia, Pennsylvania

Systematics is the science by which species are recognized. Understanding

and analyzing species and their relationships is essential in order to evaluate
biodiversity.
Many of the aspects of biosystematics that are now being explored are based
on understanding the similarities, differences, and the chemicals associated with
such similarities and differences. Unless we know the relationship of taxa, it is
very difficult to determine the significance of a single chemical difference. Sys-
tematics also is very important to determine the potential distribution of a chemi-
cal of interest. In other words, similar species are liable to contain similar chemi-
cal compounds and behave in similar ways.
Most children are curious about the natural world around them. They like
to explore waterbugs and how they move or the pleasant odors of plants and the
brightness of their colors. Children are innately classifiers, putting together those
things that they think are similar. These basic desires to classify and recognize
differences between organisms often has led to a deeper understanding of what
is the species.
Unfortunately, when a child enters the elementary grades this interest some-
times is lost, often because their teachers do not have any interest in the natural
world and do not excite the child’s curiosity about how flowers grow or where
animals live and why. Thus, in childhood, this great interest in the natural world
often is lost temporarily as the student studies other topics such as mathematics,
literature, and history.
Academic institutions that have collections of organisms should take a spe-
cial interest in encouraging the interests of children. Some of our most effective

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systematists started their careers in sorting specimens in museums. This may

seem like a dull task, but it is exciting if you are doing it for the first time and
are just beginning to learn how to classify plants or animals.
This interest in the organization of the natural world should be encouraged,
and the faculties throughout high school and college should be available to whet
the interest of the young student. Often this is done by having a young scholar
spend time sorting collections. It is very important that the collection manager
take time to instruct the young person, as to why they are doing what they do,
and how one tells differences.
Museums and colleges with a systematics program and collections available
for student use offer an excellent opportunity to give the basic training neces-
sary to understand systematics. Museums particularly are able to take young
high school students and encourage them in their great interest in some particu-
lar group of organisms such as insects or flowers or molluscs. Often these young
students then go on to college and make a great success in a career having to do
with biodiversity or ecology.
It is the opportunity to handle specimens and to observe them critically
with the help of a mentor that encourages a budding interest in a career of
worthwhile research. For example, with a relatively small grant extending over
3 years that was provided by the Pew Charitable Trusts, a committee consisting
of Dr. Peter Raven, Missouri Botanical Garden; Dr. Edward O. Wilson, Harvard
University; Dr. Thomas Lovejoy, the Smithsonian Institution; Dr. Phil
Humphrey, University of Kansas; and myself organized a program that has
started the careers of some 25 students in the field of systematics.
In this program, we invited 18 institutions to submit programs to train
young, beginning college students or students halfway through their college
careers in systematics. The requirement was that each student must have a men-
tor who is willing to devote at least 1 day a week or its equivalent to helping
them in their work. Each student was to have a special project that would result
in a seminar or a publishable paper at the end of their training. Their training
usually extended over 1.5 years.
The main requirement was that the students learn the modern techniques
for carrying out the studies of systematics. As a result of this effort carried out
by Cornell University, the Philadelphia Academy of Natural Sciences, the Smith-
sonian Institution, and the University of Kansas, 25 students have achieved a
basic knowledge in systematics and are well on their way to writing a thesis in
their chosen subject in graduate school.
These systematic programs have been in fish, insects, reptiles, paleobotony,
and plants (particularly angiosperms). Several publishable papers have resulted
from these studies, usually written with the mentor, and, most importantly,
these students have acquired a basic interest in systematics and have chosen it
for their academic careers. The college students were taught how to compare
and contrast species according to certain traits. They have learned how to use

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SYSTEMATICS / 215

Students collecting specimens in the field.

computers and to do simple statistical analyses to objectively evaluate differ-

ences in the analysis of the specimens. These students have learned cytology
and how to prepare slides or smears to identify chromosome numbers and un-
derstand the importance of genetic differences which enabled them to differen-
tiate species of plants and animals. The student should be taught how to com-
pare and contrast species according to certain traits. Learning to use the
computer and to do simple statistical analysis is a very important part of this
training. The students should learn techniques for studying the chromosome
numbers and gene differences in plants and animals.
Field trips are very important in the training of students. It is most impor-
tant for the student to realize that a species is not a single specimen but a collec-
tion of specimens, in other words a population. This population, in the natural
world, will undoubtedly show variance, and being able to distinguish between
those types of variances that are ephemeral or that are rather superficial and
those that are essential to the functioning of the organism is important.
It is most important that each student work closely with a mentor. At fre-
quent intervals the student should be asked to define clearly the similarities and
the differences between two species in question. Many techniques should be
used to determine whether this difference is significant.
Today we have computer techniques that enable us to compare many differ-
ent factors in a relatively short period of time. A few years ago this was a very
labor-intensive process. We also have developed various mathematical formulae

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216 / BIODIVERSITY II

which help us to see whether differences are significant. However, I caution that
using a computer to tell differences alone is not sufficient. One needs to examine
the species and determine if the differences found by different types of study
correspond with those determined by the computer.
Computers also enable us to examine genetic differences and thus determine
whether some of the differences we find are truly significant from a reproduc-
tive standpoint or whether they are frivolous variations.
The question “What is a species?” has long been an intriguing question and
continues to be. It is very important that we use as many techniques as possible
to determine what are the differences between species and how significant they
are. Which ones are stable? Which ones are ephemeral?
We have changed our analyses of what is a species considerably over the
last 30 years. It used to be largely based on visual differences. Today we also are
able to analyze for functional differences and cytological differences that are not
so easily seen when one encounters a species in the field.
As a result of this increased complexity in the science of systematics, one
needs to have a well-equipped laboratory, large collections to work on, and a
mentor who is wise and willing to be easily available to the student. Access to
cytologists, geneticists, and their methodology also is important. It takes a great
deal more money and more time to become an effective systematist today than it
did when Linnaeus or Bailey or Gray or Parker were alive.
Systematics as a science is a necessity for understanding biodiversity,
whether one is seeking new chemicals for medicine or food, whether one is
trying to determine the effectiveness of various fibers for clothing and shelter,
or whether one is looking for energy-producing substances such as coal and oil.
The science of systematics and knowing what are the organisms that produced
the substance that you desire is important.
Systematics is not only important to the business person and to the theoreti-
cal biological scientist, but also to the regional planner and environmentalist for
the maintenance of our natural environment. We now know that biodiversity is
a keynote to naturalness, and that this biodiversity must be maintained if the
important functions of the production of oxygen, the transfer of nutrients
through the ecosystem, the disappearance of wastes by digestion by organisms,
and the availability of many species for man’s use are to continue.
Unfortunately, interest in systematics is dwindling. In many groups of organ-
isms, there are only one or two specialists in the world today. Some groups have no
living specialists concerned with their identification. For these reasons, the train-
ing of systematics should be a number one priority of our country in order to
supply the most nutritious food at the least cost and with the least impact on the
environment, to be at the forefront in the development of new medicines to im-
prove human health, and to maintain a natural environment suitable for recreation.
Providing many more scholarships and assistantships to students pursuing a
career in systematics would go a long way toward achieving these goals.

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CHAPTER
15

Biodiversity and Systematics:

Their Application to Agriculture

DOUGLASS R. MILLER
Research Entomologist, Systematic Entomology Laboratory

AMY Y. ROSSMAN
Research Leader, Systematic Botany and Mycology Laboratory, Agricultural
Research Service, U.S. Department of Agriculture, Beltsville, Maryland

Systematics and biodiversity are the threads that form and hold the fabric
of agriculture together. Agricultural development is increasingly dependent on
the interactions and knowledge base of systematics and biological diversity.
Biodiversity itself is the grist for the agricultural mill—the germplasm. System-
atics is the explorer, describer, organizer, and predictor of biological diversity.
Agriculture is a primary user of the products of the interactions between bio-
diversity and systematics. This chapter examines the history of this interaction
and shows how current and future practices in agriculture increasingly require
more detailed knowledge of the world’s biota. This chapter also focuses on a
series of examples demonstrating the importance of systematics and biodiversity
in agriculture and suggests a solution to a serious dilemma that faces agriculture
today and in the future.

HISTORY AND THE FUTURE

Before the advent of pesticides, herbicides, and inorganic fertilizers, the
need to understand the biology and biological requirements of agricultural or-
ganisms was of considerable importance. Control strategies for insect pests, for
example, depended on knowledge of life histories so that agricultural practices
could be used to circumvent high pest population levels. With the development
of chemical pesticides and fertilizers came the complacent attitude that these
products would solve the world’s agricultural problems, and there was no longer
a need to know the identity and interactions of the organisms that comprised
agricultural systems. For example, the solution to a problem with the Japanese

217

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Diamondback moth larva, Plutella xylostella (L.) (Plutellidae), is a minor

pest on cabbage and other planst in the mustard family (Cruciferae).

beetle (Popillia japonica Newman) defoliating a vineyard was to spray the grapes
with DDT. Solutions to problems with parasitic helminths relied heavily on
antihelminthic compounds, with little regard for understanding the identity or
bionomics of the organisms involved. In agricultural fields where production
was limited by low nitrogen, the solution was to apply high levels of inorganic
nitrogen and not to worry about the presence or effects on microorganisms such
as mycorrhizal fungi. Rachael Carson’s book Silent Spring (1962) drew attention
to the devastating effects that pesticides could have on the environment. Ento-
mologists, parasitologists, mycologists, and others rapidly became aware of the
adaptability of pestiferous species to chemical control agents with their remark-
able capacity to develop resistance. Suddenly, it became obvious that, once
again, it was important to know the identities of the complex of organisms that
occurred, or should occur, in agricultural fields, livestock, orchards, and back-
yards, and to discover how they interact.
The most important organisms in agricultural systems are the most poorly
understood in the context of biodiversity and systematics, including fungi, free-
living and plant-parasitic nematodes, other microorganisms, endoparasitic hel-
minths, insects, mites, and other arthropods. Even for many important species
of pests, superficial understanding of the group is a major impediment to solv-
ing important problems in agriculture. In collaborative research between the

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BIODIVERSITY AND SYSTEMATICS / 219

Systematic Entomology Laboratory of the U.S. Department of Agriculture and

the Department of Entomology of the University of Maryland, it has been dem-
onstrated that the tobacco budworm complex of pestiferous moths (Heliothis
virescens complex) encompasses 13 species, not 5 as previously thought (Poole et
al., 1993). It is unbelievable that the group containing the second most serious
agricultural pest in the Western Hemisphere (Poole et al., 1993) is so poorly
known. Although this research summarizes all available information on the
species that are represented by specimens in collections, it probably does not
encompass even a majority of the species in the complex. Only through compre-
hensive inventories of the biodiversity of Mexico, Central America, and South
America will currently undescribed species become known to science and soci-
ety. Only then will agricultural scientists know the extent of the threat posed
by this group of moth pests and be prepared to develop strategies against poten-
tial new introductions.

AGRICULTURAL DILEMMA
The agricultural community now finds itself in a difficult situation. It
increasingly espouses environmentally positive approaches such as biological
control, sustainable agriculture, and pest management, but lacks a comprehen-
sive understanding of many of even the most common organisms that form the
foundation for these approaches. Further, destruction of native ecosystems for
new agricultural lands (Myers, 1988) eliminates the organisms upon which ag-
riculture must depend for its future. Ehrlich (1988) points out that it is the
“less cuddly” organisms that are the most important for the future of human
existence.
In the following sections, we discuss several of the areas of agriculture that
are strongly dependent on products from biodiversity and systematics.

Biological Control
Biological control programs mandate detailed knowledge of both the pests
to be controlled and the natural enemies that prey on them (Rosen, 1977). Is it
any wonder that programs in biological control are difficult to implement when
so little is known about the systematics of the organisms involved? In general,
the first step is to seek out systematic information known about the target pest
and its natural enemies, and, based on this information, to survey the natural
enemies in the field.
An example of insufficient systematic knowledge that caused the delay of a
biological control program concerns a mealybug that was decimating the coffee
plantations of Kenya (Le Pelley, 1968). The mealybug was misidentified for
many years as Planococcus citri (Risso) and later P. lilacinus (Cockerell). Discov-
ery, evaluation, and introduction of the natural enemies of these species had no

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220 / BIODIVERSITY II

effect on the pest and was a waste of time and resources. Ultimately, a system-
atist was asked to study the mealybug, who described it as a new species that
formerly was restricted to Uganda. Natural enemies were located in Uganda,
introduced to Kenya, and within a few years the pest became rare.
A more recent example concerns whiteflies that occur in the United States
and are part of the Bemisia tabaci complex. Considerable confusion centers
around the status of the sweet potato whitefly or type A, which has occurred in
the United States for nearly 100 years, and type B, or the silverleaf whitefly,
which apparently has been introduced recently (Perring et al., 1993). There are
two camps of thought on the status of the silverleaf taxon; some believe that it is
a separate species from the sweet potato whitefly (Perring et al., 1993), and have
described it as B. argentifolii (Bellows and Perring, 1994), and others contend
that it is the same (Campbell et al., 1993). This distinction is important, since it
is unclear where the silverleaf whitefly is indigenous and therefore where to
search for effective natural enemies. If the Bemisia fauna of the world already
were known and monographed and the associated natural enemies were studied
as part of biological diversity research, then the biological control community
could implement its programs with less delay and farmers would not suffer mil-
lions of dollars in damage while systematists and biocontrol explorers provide
needed information.
A similar dilemma prevails when knowledge of biodiversity in the United
States is lacking. Because of insufficient information on North American biota,
it is not uncommon for a species of natural enemy to be introduced even though
it already occurs here. In insects this happens because only about half of the
species that occur in the United States are known (Kosztarab and Schaefer,
1990), and there is no single source or database that provides information on
species that compose the insect fauna. In other circumstances, repeated intro-
ductions occur because of insufficient systematic knowledge. For example, in
the 1970s a parasitic wasp, Elachertus argissa (Walker) was introduced from
Austria and Italy to control a moth, the larch casebearer (Ryan et al., 1975,
1977). In a revision of Elachertus, Schauff (1985) demonstrated that the species
already occurred in the United States under the name of a synonym E.
proteoteratis Howard. He also found that the species parasitizes a wide range of
moth hosts and suggested that it was unlikely to be an effective biological
control agent.
In the future, biological control will have an increasing importance in pest
control. With the reality of bioengineered organisms, it now becomes possible
to alter a pest organism so that it is beneficial rather than harmful (Freeman and
Rodriguez, 1993). Development of pesticide-resistant natural enemies also adds
an innovative new dimension to biological control (Hoy, 1982). Such strategies
will be much more effective if they can draw on the genes of the millions of
natural enemies that currently exist in the pool of biological diversity, but are
unknown to science.

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BIODIVERSITY AND SYSTEMATICS / 221

Integrated Pest Management

Integrated pest-management strategies depend heavily on knowing the
identity of the organisms that occur in the crop system, understanding the com-
plex interactions among these organisms, introducing biological control agents
that are compatible with management schemes, understanding the ecological
dynamics of the system, and developing minimally disruptive methods for man-
aging the pests without diminishing the value of the agricultural product. Two
examples demonstrate the importance of information on biodiversity in urban
pest-management systems in Maryland. Euonymus japonica was a common orna-
mental shrub in most areas of the state, but in recent years it has become less
common because it is killed by the euonymus scale when not treated with insec-
ticides. A systematist in Korea and a researcher at the Beltsville Agricultural
Research Center discovered a lady beetle that controls the scale (Drea and
Carlson, 1987). University of Maryland Extension personnel have conducted
further research on the beetle and now use it as part of their pest-management
strategies. Results of collaborative research among a systematist, biocontrol
specialist, and extension scientist have reduced pesticide usage for euonymus
scale control and have provided the means for E. japonica to again become com-
mon (Davidson, personal communication, 1993).
Another example involves the control of certain moth borers in ornamental
trees. Until recently, the only control for these pests has been to drench the
bark with a pesticide at the time that the larva bores through the bark. Once the
larva successfully penetrates living plant tissue below the bark, chemical con-
trol is no longer possible; this leaves only a small window of time when even
insecticides can kill these pests. In recent years, considerable research has been
conducted on exploiting the biodiversity of entomophagous nematodes as bio-
logical control agents in agroecosystems. One of the first major successes was
with Steinernema carpocapsae in controlling tree borers (Davidson et al., 1992).
As part of urban pest-management strategies, these nematodes are sprayed on
infested trees whenever damage is detected, and they control nematodes in about
80% of the cases. The discovery and use of this nematode has reduced pesticide
usage and enhanced the likelihood of control at many times of the year. One can
only wonder what other benefits might be available if the biodiversity and clas-
sification of nematodes were more completely understood.

Sustainable Agriculture
Sustainable agriculture depends on detailed systematic knowledge of the
organisms that occur in agroecosystems, and attempts to maximize the use of the
native biota and natural resources and to minimize the use of nonindigenous
organisms and external influences such as inorganic chemicals. Even in areas
such as the Beltsville Agricultural Research Center, where agricultural research

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222 / BIODIVERSITY II

has been underway for more than 50 years, the native biota is only partially
known. An example involves a study on the genus Trichogramma, a group of
small wasps that primarily parasitize moth eggs, and have been useful in bio-
logical control. Over a period of 3 years, unparasitized moth eggs were placed
around a field of corn or soybeans to determine the diversity of species of
Trichogramma. After exposure to the indigenous wasp fauna for 3-5 days, the
eggs were brought into the laboratory and parasites were allowed to emerge.
Fifteen different species of Trichogramma were reared from the moth eggs, in-
cluding nine that were new to science (Thorpe, 1984). The identity and role of
these wasps and other organisms in the agroecosystem are crucial bits of infor-
mation for successful implementation of sustainable agriculture programs. Even
in areas of the United States where the biota is perceived as being well known,
the biodiversity of the small and diverse organisms such as small wasps requires
considerable study before strategies such as integrated pest management and
sustainable agriculture can be truly successful.

Pest Introductions and Quarantine

Estimates of cumulative loss for adventive species in the United States up to
1991 were $96,944,000,000 (Office of Technology Assessment, 1993). This fig-
ure apparently does not include the cost of control of pest species, which would
more than double the amount. A total of over 4,500 nonindigenous species has
been introduced into the United States, and this figure includes only species
that have been detected and classified (Office of Technology Assessment, 1993).
Clearly, introduction of unwanted species into the United States is a major prob-
lem! It is the difficult task of the Animal and Plant Health Inspection Service
(APHIS), of the U.S. Department of Agriculture to exclude these organisms.
Unfortunately, the knowledge base and tools to assess biodiversity that this
organization needs to make better-informed decisions are not always available.
APHIS generally does not allow plant-associated organisms identified as pest
risks into the country if they currently do not occur here. With few exceptions,
the general corollary is: if an organism already occurs in the United States, no
action will be taken against it, even if it is intercepted at a port of entry. The
supposition then is that APHIS knows the identity of all of the organisms that
occur in the United States. Furthermore, APHIS, or its cooperators, must be able
to identify all organisms that are intercepted at ports of entry. APHIS also has
the responsibility of determining if organisms unwanted by other countries oc-
cur in areas in the United States that export agricultural products to that coun-
try. Clearly, the information required by APHIS is derived from systematic
research and mandates a world-wide knowledge of the Earth’s agriculturally
important biodiversity.
Some examples of the impact of systematic knowledge on APHIS decisions
are as follows. A smut associated with wheat imported into Canada from the

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BIODIVERSITY AND SYSTEMATICS / 223

European corn borer larvae, Ostrinia nubilialis, Hübner (Crambidae),

a major pest of corn in the United States, introduced from Europe.

United States was initially determined to be Tilletia indica, a high-risk exotic

pathogen. A ban on the import of wheat from the United States to Canada was
suggested. A systematist was asked to study the material and correctly identi-
fied the smut as T. barclayana. This species occurs on rice and apparently be-
came a contaminant on the wheat in question when it was stored in a warehouse
that previously contained rice. This identification was confirmed with isozyme
analysis and a potentially costly international incident was averted (Palm, per-
sonal communication, 1993). A second example involves a nematode, Nematodi-
rus battus, which was first discovered in North America and the Western Hemi-
sphere in 1985 (Hoberg et al., 1985). Since its original description from sheep in
Great Britain, this nematode has been one of the most pathogenic parasites of
lambs in Great Britian and Europe in spite of concerted control efforts (Rickard
et al., 1989). Consequently, in recognition of the potential economic impact
related to this parasite, N. battus was the only nematode of sheep rated by APHIS
as a serious foreign agent of animal disease. The parasite is cryptic, and because
of an unusual life cycle, outbreaks of disease generally occur only after popula-
tions of high density have developed over several years (Rickard et al., 1989).
Accurate identification is confounded because disease is not associated with
adult parasites, and both parasitic larvae and adults are morphologically similar
to other less pathogenic species. However, due to the efforts of systematists in

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Oregon and Maryland, populations of this nematode were detected soon after
first introduction into North America (Hoberg et al., 1986). Surveillance pro-
grams, measures of control, and extensive epidemiological studies were initiated
to limit the potential impact of this newly introduced nematode (Hoberg et al.,
1986; Rickard et al., 1989). Aside from this highly visible parasitic helminth,
there has been a history of introductions of nematode parasites with exotic bovid
hosts from Africa, camelids from South America, and cervids from Europe (e.g.,
Rickard et al., 1993). Many of these parasites represent potential threats to wild
and domestic ruminants in North America, further highlighting the importance
of systematics within the context of cosmopolitan groups, and the necessity to
develop accurate inventories of the world fauna.

Plant Germplasm
In the area of plant germplasm, botanists have come a long way in expand-
ing science’s understanding of species of crops and the world’s vascular plant
flora, but, even in this relatively well-known group of organisms, much remains
to be done. The now famous examples of discoveries by plant systematists of
important but nondescript species of tomatoes and corn document the mind-
boggling potential that plants hold for the future of agricultural crops. Millions
of dollars have been added to the tomato industry through increased levels of
soluble solids derived from an inconspicuous species of Andean tomato, and
disease resistance has been added to the genome of cultivated corn from a nearly
extinct species discovered in Mexico (Iltis, 1988). With recent developments in
genetic engineering, nearly any species of plant has the potential to contribute
genes of importance in enhancing agricultural crops. Ethnobotanical data sug-
gest that of the approximately 250,000 species of plants (Wilson, 1988), more
than 7,000 species have been used for human benefit as food (Ehrlich and Wil-
son, 1991). Understanding the diversity and systematics of these plants will add
significantly to the goal of developing a much broader spectrum of agricultural
products and will enhance sustainable approaches without destroying forests
and more natural environments.

THE BRUSH-FIRE APPROACH TO AGRICULTURAL SYSTEMATICS

Under current conditions of small budgets and reduced personnel, resources
devoted to systematics and biodiversity are woefully small and stretched to the
limit (House of Lords, 1991). The impact is that each of the small number of
agricultural systematists must serve many roles, including those of researchers,
identifiers, curators, database managers, illustrators, and technicians. The best
strategy to support the biodiversity and systematic needs of agriculture is to
direct resources toward the groups of organisms that are most likely to cause
future agricultural problems or toward the beneficial groups that show promise

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BIODIVERSITY AND SYSTEMATICS / 225

of enhancing agricultural systems, and undertake monographic research on these

groups. Unfortunately, there rarely is time or resources to take a coordinated
approach, and this leaves agriculture with a systematic support system that is
patched together with chewing gum and rusted wire. In most instances, agri-
cultural problems are solved using the brush-fire approach of reacting when an
emergency arises, undertaking a narrow research program on the pest causing
the problem, hoping to find a solution to the immediate problem, and going on
to the next agricultural brush fire. This approach does not solve problems of the
future and does not add significantly to the development of a predictive classi-
fication system. In fact, in many situations, systematic analysis of a single spe-
cies removed from the context of phylogeny and biogeography and not care-
fully integrated into the classification system detracts rather than adds useful
information.
An example of a circumstance where comprehensive research followed a
brush-fire solution involved a pest in Africa. An unknown mealybug was at-
tacking cassava in West Africa and was costing farmers $1.4 billion each year
(Anonymous, 1986). A systematist described the species (Phenacoccus manihoti)
as new and suggested that natural enemy exploration be undertaken in Central
or South America (Matile-Ferrero, 1977). A mealybug identified as P. manihoti
was discovered in northern South America and several of its parasites were im-
ported to Africa. Unfortunately, none of the biological control agents were
effective, and a mealybug systematist was asked to study the South American
material. The systematist determined that the mealybug from northern South
America actually was a second species different from P. manihoti (Cox and Wil-
liams, 1981). True P. manihoti was located further south and effective parasites
were discovered and successfully introduced into West Africa (Herren and
Neuenschwander, 1991). After this brush fire was put out, the International
Fund for Agricultural Development offered substantial financial support for a
study on the mealybugs of South America. A recently published book (Will-
iams and Grana de Willink, 1992) serves as a first step towards understanding
the diverse mealybug fauna of the area and partially prepares the world for the
emergence of the next South American mealybug pest.

SYSTEMATICS: THE PREDICTOR OF BIODIVERSITY

Classification systems serve as the knowledge base from which predictions
about organisms are made. Too frequently this predictability is taken for granted
as an innate capacity of the human mind, but in fact it is part of the classification
process. A simple example involves a person who sees a hornet sitting on
someone’s arm. The prediction is that the hornet will sting the arm if disturbed
or crushed. Such a prediction could be made in any part of the world where
hornets occur. As long as the hornet is a female, the prediction will have a high
level of predictive accuracy. Similar, but more sophisticated predictions can be

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226 / BIODIVERSITY II

made from other classification systems. For example, recent research on the
Trichoderma-like fungi used in biological control has demonstrated that a spe-
cies previously placed in Gliocladium (G. virens) shares many characters with the
genus Trichoderma and should be placed in the latter genus. This is important
because many species of Trichoderma have mycotoxins that are useful for the
biological control of plant-pathogenic ascomycetes, rather than basidiomycetes,
as is the case for true species of Gliocladium (Rehner and Samuels, 1994). The
sexual state of T. virens is Hypocrea gelatinosa or a closely related species, and it
is predicted that other closely related sexual states of Hypocrea will prove to be
valuable agents of biological control similar to T. virens. Scientists already have
found high levels of mycotoxins in isolates of Hypocrea.
A second example comes from research carried out by Farrell and Mitter
(1990) at the University of Maryland. They hypothesized that the leaf beetles in
the genus Phyllobrotica and their Scutellaria plant hosts coevolved, and they
supported this hypothesis by showing close congruence between the phylog-
enies of the beetle and host. One species of beetle had no information on host
association, so Farrell and Mitter predicted the host species based on the phy-
logenies of the beetles and the plant; this prediction proved to be correct.
Another example involves an anticancer compound that was screened from
extracts of the plant Maytenus buchananii collected from a small population in
Kenya. Because the species would be eliminated if further collections were made,
a systematist was consulted to provide information on related species. Based on
the classification system of the genus, the systematist predicted that M. rothiana
in India would most likely have the desired compound. This prediction proved
to be correct (Shands and Kirkbride, 1989).
Specialists in biological control often ask systematists where to look for
natural enemies and which species are most closely related to the pest that is the
subject of the project. For example, the sugar beet leafhopper, Circulifer tenellus,
was originally placed in the genus Eutettix, which occurs in South America.
Exploration for natural enemies in South America was unsuccessful. A system-
atist examined the species and placed it in Circulifer, which is of Old World
origin. Natural enemies subsequently were located in the Mediterranean area
(Rosen, 1977).

THE SOLUTION
The question is where do we go from here? How can we describe and
classify the components of Earth’s biodiversity and find ways to preserve, en-
joy, and use it sustainably? An initiative from the systematics community called
Systematics Agenda 2000: Charting the Biosphere (Systematics Agenda 2000,
1994:1) proposes “to discover, describe, and classify the world’s species.” If we
can walk on the moon or search for life in outer space, we can fully explore life
on Earth. We know that life occurs here, but we have only an inkling of its

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BIODIVERSITY AND SYSTEMATICS / 227

diversity, grandeur, and wonderment. The benefits to humanity will be enor-

mous. Imagine if all natural enemies of the silverleaf whitefly were known, a
biological control program could be implemented more quickly and millions of
dollars might be saved. APHIS would have information on all of the organisms
that occur in the United States and could make better-informed quarantine deci-
sions at ports of entry. Species of Trichogramma would be classified, and sus-
tainable farming would benefit from systematic knowledge of all organisms that
interact to maintain and stabilize the system. Crop plants would be enhanced by
genes from plants that currently are unknown or are poorly known. High-risk
adventive species would be well known and their distribution would be moni-
tored so that some of the billions of dollars that might be spent on these organ-
isms in the future could be saved.
Other chapters of this volume discuss the significant progress that system-
atics has made in the recent past. Some larger-sized organisms are well known,
and even groups of smaller-sized organisms have a knowledge base many times
larger than that which existed at the turn of the century. But progress is too
slow if the currently suggested rates of extinction are correct. If we are to
understand and benefit from major parts of the extant biota, we must make an
all-out effort now. Through computer technology, imaging systems, morpho-
metric analysis, molecular techniques, and recent theoretical innovations, the
systematics community is poised and capable of carrying out the Systematics
Agenda 2000 initiative. Armed with comprehensive knowledge of the compo-
nents of Earth’s biological resources, we will be better able to maintain high
levels of agricultural productivity and reduce environmental impact so that fu-
ture generations can continue to enjoy the mysteries and aesthetics of complex
biological systems.

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Bellows, T. S., Jr., and T. M. Perring. 1994. Description of a new species of Bemisia. Ann. Entomol.
Soc. Amer. 87:195-206.
Campbell, B. C., J. E. Duffus, and P. Baumann. 1993. Detemining whitefly species. Science 261:1333.
Carson, R. 1962. Silent Spring. Houghton Mufflin, Boston. 368 pp.
Cox, J. M., and D. J. Williams. 1981. An account of cassava mealybugs with a description of a new
species. Bull. Entomol. Res. 71:247-258.
Davidson, J. A., S. Gill, and M. J. Raupp. 1992. Controlling clearwing moths with entomopathogenic
nematodes: The dogwood borer case study. J. Arboriculture 18:81-84.
Drea, J. J., and R. W. Carlson. 1987. The establishment of Chilocorus kuwanae in eastern United
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Ehrlich, P. R. 1988. The loss of diversity: Causes and consequences. Pp. 21-27 in E. O. Wilson and
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Farrell, B. D., and C. Mitter. 1990. Phylogenies of insect/plant interactions: Have Phyllobrotica leaf-
beetles and the Lamiales diversified in parallel? Evolution 44:1389-1403.
Freeman, S., and R. J. Rodriguez. 1993. Genetic conversion of a fungal plant pathogen to a non-
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Herren, H. R., and P. Neuenschwander. 1991. Biological control of cassava pests in Africa. Ann.
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Hoberg, E. P., G. L. Zimmerman, and L. G. Rickard. 1985. Nematodirus battus: A review of recent
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Hoberg, E. P., G. L. Zimmerman, and J. R. Lichtenfels. 1986. First report of Nematodirus battus in
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House of Lords. 1991. Systematic biology research. Select Committee on Science and Technology.
HL Paper 22-I. HMSO, London. 234 pp.
Hoy, M. A. 1982. Genetics and genetic improvement of the Phytoseiidae. Pp. 72-89 in M. A. Hoy,
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Iltis, H. H. 1988. Serendipity in the exploration of biodiversity: What good are weedy tomatoes?
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Kosztarab, M., and C. W. Schaefer. 1990. Conclusions. Pp. 241-247 in M. Kosztarab and C. W.
Schaefer, eds., Systematics of the North American Insects and Arachnids: Status and Needs.
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Matile-Ferrero, D. 1977. Une cochenille nouvelle nuisible au manioc en Afrique équatoriale,
Phenacoccus manihoti n. sp. Ann. Soc. Entomol. Fr. (new series) 13:145-152.
Myers, N. 1988. Tropical forests and their species: Going, going...? Pp. 28-35 in E. O. Wilson and
F. M. Peter, eds., BioDiversity. National Academy Press, Washington, D.C.
Office of Technology Assessment. 1993. Harmful Non-indigenous Species in the United States.
OTA-F-565. U.S. Government Printing Office, Washington, D.C. 391 pp.
Perring, T. M., A. D. Cooper, R. J. Rodriguez, C. A. Farrar, and T. S. Bellows, Jr. 1993. Identification
of a whitefly species by genomic and behavioral studies. Science 259:74-77.
Poole, R. W., C. Mitter, and M. Huettel. 1993. A revision and cladistic analysis of the Heliothis
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partment of Information Services, No. 4, Mississippi Entomological Museum. 51 pp.
Rehner, S. A., and G. J. Samuels. 1994. Taxonomy and phylogeny of Gliocladium analysed from
nuclear large subunit DNA sequences. Mycol. Res. 98:625-634.
Rickard, L. G., E. P. Hoberg, J. K. Bishop, and G. L. Zimmerman. 1989. Epizootiology of Nematodi-
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56:104-115.
Rickard, L. G., E. P. Hoberg, N. M. Allen, G. L. Zimmerman, and T. M. Craig. 1993. Spiculopteragia
spiculoptera and S. asymmetrica from red deer (Cervus elaphus) in Texas. J. Wildlife Dis. 29:512-
515.
Rosen, D. 1977. The importance of cryptic species and specific identifications as related to biological
control. Pp. 23-35 in J. A. Romberger, Biosystematics in Agriculture. Beltsville Symposium
on Agricultural Research. Allanheld, Osmun and Co., Montclair, N.J. 340 pp.
Ryan, R. B., W. E. Bousfield, R. E. Denton, R. L. Johnsey, L. F. Pettinger, and R. F. Schmidtz. 1975.
Additional releases of larch casebearer parasites for biological control in the western United
States. U.S.D.A. Forest Service Research Note PNW-242, Pacific Northwest Forest Range Ex-
periment Station, Portland, Oreg. 7 pp.
Ryan, R. B., W. E. Bousfield, R. E. Denton, R. L. Johnsey, L. F. Pettinger, and R. F. Schmidtz. 1977.
Releases of recently imported larch casebearer parasites for biological control in the western

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United States, including Agathis pumila. U.S.D.A. Forest Service Research Note PNW-290,
Pacific Northwest Forest Range Experiment Station, Portland, Oreg. 4 pp.
Schauff, M. E. 1985. Taxonomic study of the Nearctic species of Elachertus Spinola. Proc. Entomol.
Soc. Wash. 87:843-858.
Shands, H. L., and J. H. Kirkbride. 1989. Systematic botany in support of Agriculture. Symbolae
Botanicae Upsalienses 28:48-54.
Systematics Agenda 2000. 1994. Systematics Agenda 2000: Charting the Biosphere. Technical
Report. Systematics Agenda 2000, a Consortium of the American Society of Plant Taxono-
mists, the Society of Systematic Biologists, and the Willi Hennig Society, in cooperation with
the Association of Systematics Collections, N.Y. 34 pp.
Thorpe, K. W. 1984. Seasonal distribution of Trichogramma species associated with a Maryland
soybean field. Envir. Entomol. 13:127-132.
Williams, D. J., and M. C. Grana de Willink. 1992. Mealybugs of Central and South America. CAB
International and Cambridge University Press, Cambridge, England. 635 pp.
Wilson, E. O. 1988. The current state of biodiversity. Pp. 3-18 in E. O. Wilson and F. M. Peter, eds.,
BioDiversity. National Academy Press, Washington, D.C.

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CHAPTER
16

Snout Moths: Unraveling the

Taxonomic Diversity of a Speciose
Group in the Neotropics

M. ALMA SOLIS
Research Scientist, Systematic Entomology Laboratory,
U.S. Department of Agriculture, Washington, D.C.

Biodiversity studies often ignore the insects, one of the most important and
diverse groups of organisms on this planet. With estimates of 5-30 million spe-
cies of insects, the simple request to provide a scientific name can be nearly
impossible for insect taxonomists, in strong contrast with the capability of ver-
tebrate taxonomists who work with smaller and better-known taxa. Within the
insects, butterflies have been regarded as good subjects for biodiversity studies
because there are relatively fewer species and they are taxonomically well
known. Butterflies constitute about 15% of the 140,000+ species of Lepidoptera
(approximated from Heppner, 1991); the rest are moths. However, it would be
a mistake to utilize only less diverse groups in biodiversity studies, because the
more speciose groups such as moths may have a greater impact on the Earth’s
sustainable resources. Moths have many positive attributes for biodiversity
studies: they are found in almost all habitats and niches, possess many special-
ized behaviors, are good indicators of areas of endemism, show rapid responses
to environmental disturbance, can be sampled easily with quantitative methods,
and have many taxa that are readily identifiable (Miller and Holloway, 1991).
The Pyraloidea, or snout moths, are endowed with all the attributes for
investigations in biodiversity. Although they contain over 16,000 described
species (Table 16-1) and at least 16,000 remain to be described (Munroe, per-
sonal communication, 1994), a project to study the taxonomic diversity of a
smaller subgroup within the pyraloids is possible and will advance our knowl-
edge and communication about this economically important group of moths.
The Pyraloidea, like every group of organisms, has had many unique biological
and historical influences that affect its present taxonomic status. This is a spe-

231

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TABLE 16-1 Subfamilies of the Pyraloidea and Numbers of Species

for the Western Hemisphere

Subfamilies World Totala Neotropicalb Costa Rica

Pyralidae
Pyralinae 900c 23 2
Chrysauginae 437 378 48
Epipaschiinae 572d 282 65
Galleriinae 261 43 3
Phycitinae 2,629 341 SPS
Total 4,927 1,105 118

Crambidae
Midilinae 47e 47e 8
Linostinae 3 3 1
Musotiminae 166 79 16
Scopariinae 479 30 26
Nymphulinae 716 218 40
Odontiinae 367 84e 17
Glaphyriinae 200 161e 30
Evergestinae 137 24 3
Pyraustinae 7,381 1,450 363
Schoenobiinae 169 72 8
Cybalomiinae 55e 9 0
Crambinae 1,877 433 SPS
Wurthiinae 7 0 0
Noordinae 6 0 0
Cathariinae 1 0 0
Total 11,611 2,534 512

Total for Pyralidae

and Crambidae 16,538 3,639 630

aHeppner (1991), unless otherwise indicated.

bMunroe et al. (1995).
c Solis and Shaffer (manuscript).
dSolis (1992, 1993).
eMunroe and Solis (in press).

NOTE: SPS=still at preliminary stage.

cific report on the initiation, management strategies, and progress of a study on

the taxonomic diversity of the Pyraloidea of Costa Rica.

SNOUT MOTHS AND BIODIVERSITY

Snout moths are primarily tropical in distribution, but occur world-wide,
including most oceanic islands. They are known from low and middle eleva-

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SNOUT MOTHS / 233

tions in the tropics to the high

arctic. While many pyraloids
may have broad continental
and even world-wide distribu-
tions, there are many sub-
groups that are endemic to is-
lands and continental areas and
that contain examples of ex-
treme disjunction (Clarke,
1986; Munroe and Mutuura,
1971; Zimmerman, 1958). Neo-
tropical pyraloids comprise (Colorful) snout moth larva feeding on host plant.
about 20% of the world fauna
(Table 16-1). The largest subfamily is the Pyraustinae, and to date 363 species
have been delineated in Costa Rica. There are a few small subfamilies found
only within the Western Hemisphere, such as the Midilinae and Linostinae.
Others, such as the Chrysauginae and Glaphyriinae, are found primarily in the
Neotropics and have only a few species in the Neartic, Oriental, or Palearctic.
All but three small subfamilies of the Pyraloidea occur in Costa Rica.
Pyraloid caterpillars have diverse habits. They consume dried or decaying
plant or animal matter, wax in bee and wasp nests, and living plants. Some are
known to be inquilines in ant nests (some Galleriinae), predators of scale insects
(some Phycitinae), and aquatic scavengers in flowing water (some Nymphulinae).
The Nymphulinae, with over 700 species, is the only taxon in Lepidoptera with
truly aquatic caterpillars. Snout moth caterpillars are associated with non-
vascular and vascular plants, feeding on both gymnosperms and angiosperms.
They demonstrate plant specificity at different taxonomic levels. For example,
the Midilinae are known to bore in the plant family Araceae, and the genus
Diaphania Stephens is known to feed only on Cucurbitaceae. Snout moth cater-
pillars are intimately associated with their plant hosts either as external or con-
cealed feeders. They have developed a broad array of concealed feeding strate-
gies: folding, rolling, webbing or tying of leaves; making tunnels or tubes of silk
or frass; mining leaves; and boring into stems, roots, buds, and fruits.
Because of the close association of the immature stages with plants, moths in
general have shown a rapid response to environmental disturbance (Holloway
and Barlow, 1992). Changes in plant communities can be monitored easily and
studied efficiently because adult moths can be sampled in a qualitative and quan-
titative manner with lights, such as mercury-vapor lamps placed in front of a
white sheet or a Robinson-pattern light trap (Barlow and Woiwod, 1990;
Holloway et al., 1990; Robinson and Tuck, 1993). Although the Pyraloidea have
been included in many qualitative diversity studies (i.e., a list of snout moths
from a particular area), they have been included only recently in quantitative
studies. Barlow and Woiwod (1990) utilized pyraloids to compare the seasonal

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234 / BIODIVERSITY II

and overall diversity of two lowland sites in Sulawesi. Robinson and Tuck
(1993) compared the diversity of primitive moths, specifically delineating sub-
families in the Pyraloidea, in three vegetational areas of Borneo.
Pyraloids can be used in diversity studies because many are large enough to
be sorted visually to species and are readily identifiable using collections such
as the Natural History Museum in London or the National Museum of Natural
History in Washington, D.C. The Pyraloidea consist of two families. The
Pyralidae are the smaller group, with only about 5,000 species and 5 subfami-
lies, and the Crambidae are the larger group, with over 11,000 species and 15
subfamilies (Table 16-1). Some groups of pyraloids are brightly colored, large in
individual size, small in numbers of species, and have been well collected. The
Midilinae (Munroe, 1970) and Cliniodes Guenee (Odontiinae) (Munroe, 1964) are
over 2.5 cm in wing length; have distinctive wing patterns and colors, such as
white, orange, and yellow; and have had a history of taxonomic work and illus-
tration. In contrast, many pyraloid groups are not visually pleasing and are
small in individual size and large in numbers of species. For example, the
Glaphyriinae and Scopariinae are small in size and have a homogeneous color
pattern; the Pyralinae in Africa and Nymphulinae in southeast Asia are speciose
in poorly collected areas. Nevertheless, some pyraloid groups have been treated
recently in revisionary or phylogenetic studies, such as the Phycitinae (Shaffer,
1976) and Epipaschiinae (Solis, 1993), or in geographic studies, such as the
Phycitinae (Heinrich, 1956; Neunzig, 1986; 1990), Pyraustinae and related sub-
families (e.g., Munroe, 1972, 1973a, 1976).

SNOUT MOTHS AND AGRICULTURAL DIVERSITY

Many pyraloids are pests to a wide array of crops and stored products.
Some pyraloids rank among the most destructive pests to graminaceous crops
such as corn, sugarcane, and rice. Table 16-2 illustrates the diversity of com-
modities affected by pyraloids and lists species that have been targets of concen-
trated world-wide efforts of control with parasites and predators. Although not
listed, each genus may include closely related species that are also pests. For
example, Chilo Zincken includes 41 species in the world, and although C. sup-
pressalis (Walker) is one of the worst pests on rice, there are other species of
Chilo that are pests: two on rice, five on sugarcane, and five on corn (Bleszynski,
1970). Hundreds more pyraloids are minor pests to many major fruits and
vegetables (e.g., tomatoes, beans, squash, cabbage, celery) and of forest trees,
both conifers and hardwoods, where they feed on foliage and fruits. Members
of Etiella Zeller, Cadra Walker, and Plodia Guenée are major pests of stored
products (e.g., grains, dried fruit, nuts) and have been dispersed world-wide.
Although the impact of snout moths on the human condition is based on
their adverse effect, it is these same characteristics that have prompted testing of
species of pyraloids for the biocontrol of noxious weeds. The most striking

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SNOUT MOTHS / 235

TABLE 16-2 Commodities and Pyraloid Targets of Major

Biocontrol Efforts

Commodity Pest

Rice Chilo suppressalis (Walker)

Scirpophaga incertulas (Walker)
Sugarcane Diatraea saccharalis (Fabricius)
Hedylepta accepta (Butler)
Corn Ostrinia nubilalis (Hübner)
Coconut Tirathaba complexa (Butler)
Lima beans Etiella zinckenella (Treitschke)
Oranges Amyelois transitella (Walker)
Teak Hapalia machaeralis (Walker)
Karoo Loxostege frustralis Zeller
Banana Nacoleia octasema (Meyrick)

SOURCE: Clausen (1978).

success story is Cactoblastis cactorum (Berg)(Phycitinae). It was introduced into

many countries for the control of Opuntia Mill, the prickly pear cactus. In 1787,
Opuntia was introduced into Australia and, by 1925, it had infested more than
24,000,000 hectares. But by 1934, after introduction of C. cactorum, 90% of the
Opuntia stands were eliminated and the land restored for agricultural use
(Clausen, 1978). Some pyraloids, including species in the Nymphulinae with
aquatic caterpillars, have been investigated for the control of aquatic weeds
such as water hyacinth, hydrilla, and alligatorweed (Habeck and Allen, 1974).
The study of the taxonomic diversity of pest species and their relatives is
important for biocontrol studies, primarily for the importation of effective para-
sites and predators, and in the case of noxious weeds, for the diversity of insects
feeding on the plants for experimentation as control agents. As a result of their
notoriety as pests and control agents, some pyraloids have been well studied
taxonomically, for example in the Schoenobiinae (Common, 1960; Heinrich,
1938; Lewvanich, 1981), Crambinae (Bleszynski, 1970; Dyar and Heinrich, 1927),
and Pyraustinae (Munroe, 1973b; Mutuura and Munroe, 1970). In addition there
have been studies of snout moth guilds on economically important host plants
such as legumes (Neunzig, 1979), cacti (Heinrich, 1939), and aquatic plants (Cen-
ter et al., 1982).

BIODIVERSITY IN COSTA RICA: AN OPPORTUNITY

In 1989, I initiated a project to study the taxonomic diversity of the Pyra-
loidea of Costa Rica. A combination of the following historical and ongoing

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236 / BIODIVERSITY II

events allowed a taxonomic diversity project in Central America, and specifi-

cally in Costa Rica: creation of the Instituto Nacional de Biodiversidad (INBio) in
Costa Rica, organization of the largest neotropical pyraloid collection in the
world at the National Museum of Natural History, a group of pyraloid taxono-
mists interested in biodiversity research, and publication of a checklist of snout
moths for the entire neotropical region by Munroe et al. (1995). Two prerequi-
sites for a biodiversity study of an area are thorough collections from the study
area and detailed taxonomic research. Large collections with long series of speci-
mens from the entire range of the species are absolutely necessary to study
variation and permit accurate identification of the species. Taxonomic research
demands knowing the names and identities of all the species that have been
described of a particular group from the area. This list, in turn, allows the
taxonomist to solve basic problems such as synonymy and recognition of new
species.
The decision to undertake a study of the diversity of neotropical snout
moths with Costa Rica as a taxonomic center was fueled in part by the creation
of INBio (Gamez et al., 1993), because it fulfills one of two important criteria,
that is, thorough collections in the area of study. The Institute was created to
document the country’s flora and fauna in a creative and organized way (Janzen
et al., 1993). INBio, through the efforts of parataxonomists, has extensive col-
lections of Pyraloidea from national parks and conservation areas in Costa Rica.
Parataxonomists are Costa Ricans trained by INBio to collect and prepare bio-
logical organisms near their homes, and they are providing a thorough survey of
Costa Rica in a relatively short period of time. The parataxonomists deposit the
material at INBio where moth specimens are first labeled: a traditional insect
label and a bar-code label. The bar-code label represents information about
locality, collector, date of collection, and a unique number for each specimen.
The label is read by a bar-code laser light and placed into a computer database
which is then made available to taxonomists working on the material. The in-
ventory manager of pyraloids at INBio sorts, organizes, sends material to tax-
onomists, and enters information (e.g., the scientific name determined by a tax-
onomist) into a database (Figure 16-1). Another important consideration with
respect to collections is the Pyraloidea collection at the National Museum of
Natural History. Although it is the largest neotropical pyraloid collection in the
world, in 1989 over two-thirds was unsorted material and the remaining one-
third was based on nineteenth century taxonomy. Over the past 4 years, a
massive sorting and reorganization of the snout moth collection has made the
material more accessible for taxonomic research and general retrieval of data.
Munroe (personal communication, 1990) estimated the total snout moth
fauna in Costa Rica to be 2,000 species. To date, over 600 species from Costa Rica
(Table 16-1) have been identified. Because of the size of the group, it was nec-
essary to make decisions concerning the type of research required to answer
specific taxonomic problems in each of the 17 subfamilies occurring in Costa

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SNOUT MOTHS / 237

LOCALE PERSONNEL PRODUCT

COSTA RICA
Biodiversity office Parataxonomist Properly prepared
specimens

Technicians Labeled,
barcoded
INBio specimens

Inventory Sorting, loans;

Manager Interaction
with taxonomists,
parataxonomists;
Computerized
information on
specimens

INTERNATIONAL

Facilitating Material and

Taxonomist information
to collaborating
taxonomists and
Libraries inventory manager
Collections

Collaborating Identifications;
Taxonomists Research papers;
Phylogenetic
analyses

FIGURE 16-1 Simplified flow chart of material and information between Costa Rica and
the international taxonomic community.

Rica (Table 16-1). Some subfamilies (e.g., Glaphyriinae) or certain genera (e.g.,
Neurophyseta Hampson in Musotiminae) with moths that are individually very
small, and where very few species have been described from Central America,
were targeted for preliminary taxonomic research papers primarily to describe
the fauna. This approach has been found to be fruitful. For example, the
Glaphyriinae of Costa Rica comprise about 19% of the total neotropical glaph-
yriine fauna. Approximately 27% of the glaphyriine species in Costa Rica are
new; specifically, 22 species had been described previously and 8 are new spe-

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238 / BIODIVERSITY II

cies. While this propor-

tion of new species may
seem high, it was ex-
pected because the moths
are small and had not
been well collected. Al-
though the work contin-
ues in all subfamilies,
the Phycitinae and Cram-
binae are the only two
speciose groups that are
still in the preliminary
Snout moths are a diverse, economically important group.
stage of identification.
The Pyraustinae, one of
the largest subfamilies with about 1,500 species in the Neotropics and over 350
in Costa Rica, are still a major area of research because they have a number of
genera, such as Omiodes Guenée, which are riddled with problems of synonymy
and species complexes.
The goal of this project is to produce a handbook for the identification of
pyraloid moths in Costa Rica. But to solve many of the taxonomic problems,
such as synonymies, complexes, and discovery and description of new species,
research papers prior to the handbook would be more efficient, appropriate, and
useful. The first step in a study of taxonomic diversity is to know the names of
all the species that have been described from the area. In the field of taxonomy,
this is known as a checklist or a catalog derived from the literature. To be
taxonomically informative and useful for future systematic studies, a list of the
species should be based on a study with world-wide scope. This is especially
true for snout moths because many genera are pantropical. Fortunately, such a
study has been conducted by Munroe et al. (1995) for the neotropical region,
based on world-wide generic concepts; this study provides the basis for the
study of a geographical subset within the neotropical region. A checklist is just
that, a list of names. What a taxonomist really needs is the identity, or morpho-
logical criteria, for assigning a name to a particular species of snout moth. Tech-
nically, this and many other taxonomic problems are solved by studying and
dissecting type specimens, a single specimen on which a species name and its
description is based. Dissection and comparison of Costa Rican species to type
specimens help to maintain nomenclatural stability and enhance world-wide
communication. Type specimens of species usually are deposited by the taxono-
mist who described them in collections of museums, such as the National Mu-
seum of Natural History in Washington, D.C., and the the Natural History Mu-
seum in London. Although both are large repositories for type specimens of the
Pyraloidea, type specimens also can be found in many other museums through-
out the world.

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SNOUT MOTHS / 239

A checklist also provides the basis for efficiently solving the common prob-
lems of classification and indirectly aids in the discovery and description of new
species. In any group that has not been revised recently, there are usually a
large number of synonyms, i.e., many names for the same species described
from different countries over the years by different people. For example, the
same species could have been described by Möschler from Puerto Rico, by Dyar
from Panama, by Schaus from Costa Rica, by Druce from Mexico, by Amsel from
Venezuela, and by Dognin from Ecuador. It was common practice in the last
century to describe new species from different countries without communicat-
ing with museums, other workers, or the literature to determine if the species
previously had been described. Another problem is that of a species complex or
one name for what is really many species. This occurs usually because the moths
externally look the same and no one has studied them in detail over their entire
distribution. Discovery of new species is an automatic byproduct of studying
the entire fauna taxonomically, not regionally. If the identity of all previously
described species is known, a species that is undescribed will be recognized as
such. The actual description of all new species is not necessary or feasible at this
point, and the decision of which new species will be described is based on a
biological need to unravel complexes of species and to provide information about
groups or taxa that have been historically underrepresented in the taxonomic
literature.

BENEFITS OF RESEARCH ON PYRALOIDEAN BIODIVERSITY

The ultimate benefit of the Costa Rican project is transfer of information
within and from the field of taxonomy to all levels of society via several differ-
ent vehicles such as literature and education. The project will summarize infor-
mation held in libraries, collections, and by taxonomists and place this knowl-
edge at the fingertips of ecologists, conservationists, quarantine officers, and
farmers in Central America. It will also be the first step to “taxonomic self-
sufficiency” of pyraloid moths for Central American countries (Janzen et al.,
1993). This self-sufficiency will be accomplished by producing accurate scien-
tific names and detailed characters that allow individuals to identify and com-
municate specifically and comparatively about the diversity of organisms on a
global basis. The most tangible product that will reach a diverse audience is a
handbook for the identification of pyraloid moths in Costa Rica with photo-
graphs, the correct scientific name, distribution, and taxonomic and biological
notes on each species. Analysis of the distribution of Costa Rican species
throughout the Western Hemisphere also will be included and will form the
foundation for other kinds of studies in other areas of Central America.

Transfer of information via education has occurred at all levels of this

project. In 1990, a group of parataxonomists participated in a month-long train-

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240 / BIODIVERSITY II

ing course on how to collect, identify, and prepare pyraloids. The inventory
manager at INBio is encouraged and able to learn via research projects with the
taxonomists and serves as a link between the parataxonomist and taxonomist, as
well as with a wide variety of other users of such information in Costa Rica.
Two others working on this project have Ph.D.s in systematics, but have little or
no experience working with Pyraloidea, and are learning about pyraloids as
they conduct collaborative research. Education and hands-on experience, from
the parataxonomists to Ph.D.s in systematics, have been important components
in the transfer of information and have made it possible for the project to
progress more rapidly than if a single taxonomist proceeded alone to conduct a
diversity study of a speciose group of moths.

CONCLUSION
The keys to the transfer of information about a speciose group of insects in
a short period of time (e.g., 10 versus 30 years) are collections and taxonomists.
The Costa Rican project became a reality through the study, development, and
organization of pyraloid collections throughout the world. In turn, the Pyra-
loidea collections at the National Museum of Natural History in Washington,
D.C., and INBio will become more accessible and useful for phylogenetic re-
search and other biological studies. In addition, all other collections throughout
the world involved in this project will have been improved. Taxonomic refine-
ment and computerization of pyraloid collections will provide an impetus for
studies of diversity and faunistic composition of snout moths in other tropical
areas of Central America. Finally, the most difficult aspect, but the most impor-
tant, has been the transfer of information from taxonomists (unaffiliated or af-
filiated in some other capacity with other organizations) who have volunteered
their time, and from the past work of taxonomists that we now build on and use
to answer some of our present questions.

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CHAPTER
17

Phylogeny and Historical Reconstruction:

Host-Parasite Systems as Keystones in
Biogeography and Ecology

ERIC P. HOBERG
Research Parasitologist and Associate Curator, U.S. National Parasite
Collection, Agricultural Research Service, Biosystematics, and National Parasite
Collection Unit, U.S. Department of Agriculture, Beltsville, Maryland

“Parasites furnish information about present day habitats and ecology of their
individual hosts. These same parasites also hold promise of telling us some-
thing about host and geographical connections of long ago. They are simulta-
neously the product of an immediate environment and a long ancestry reflect-
ing associations of millions of years. . . . Eventually there may be enough pieces
to form a meaningful language which could be called parascript—the language
of parasites which tells of themselves and their hosts both of today and yester-
year.” (Harold Manter, 1966:70).
Biodiversity represents the complex interaction of phylogeny, ecology, ge-
ography, and history as determinants of organismal evolution and distribution.
Accordingly, our perception of biotic diversity is a function of scale with re-
spect to populational, genealogical, and ecological identity (Eldredge, 1992;
Ricklefs, 1987), spatial relationships (Barrowclough, 1992), and temporal dura-
tion (Brooks and McLennan, 1991). Conceptually, biodiversity includes a range
of micro- to macroassociations extending from the enumeration of taxa and elu-
cidation of interactions within contemporary ecosystems to the recognition of
ancestral areas, regions of endemism, and significant centers of organismal evo-
lution. At one end of this continuum is historical biogeography, which encom-
passes the study of pattern and process in the distribution of organisms, and
historical ecology, which is involved with macroevolutionary process in com-
munity development. Thus, with phylogenetic analyses, a record of geological
change and knowledge of ecological interactions, hypotheses may be posed
about production of biological diversity and evolution of community structure
within a rigorous macroevolutionary context (Brooks and McLennan, 1991). In

243

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244 / BIODIVERSITY II

this framework, parasites constitute elegant indicators of the historical and eco-
logical development, temporal longevity, current health, and prospects for con-
tinuity of biotas.
Current research in biodiversity has focused on regions already profoundly
influenced by anthropogenic perturbations and predicted to be strongly affected
by climatic change (Ehrlich and Wilson, 1991; Soulé, 1991; Wilson, 1988). How-
ever, many of these approaches to faunal assessment have been limited in scope
taxonomically, geographically, and temporally. Recent attempts in assessment
of biodiversity, although covering a range of local, biomic, and global scales
(Barrowclough, 1992), often have concentrated on modern communities and on
taxonomically restricted groups, thus obscuring a broader historical and eco-
logical context. There has been a notable, but often necessary, focus that has led
research to be largely centered on birds, mammals, selected groups of arthro-
pods, and vascular plants in an often nondimensional framework that has em-
phasized contemporary biotic associations.
Most components of the world’s vertebrate and invertebrate fauna are para-
sitized, and the helminth parasites of these hosts (Platyhelminthes, Nematoda,
Acanthocephala; Table 17-1) can provide a new dimension to understanding
ecological interactions, patterns of distribution, and the complex history of many
geographic regions and biotas. An interesting perspective on parasites is sug-
gested by recent evaluations of global biodiversity (Barrowclough, 1992; Ehrlich
and Wilson, 1991; Erwin, 1988; Wilson, 1988) which noted that there may be in
excess of 30-100 million species, primarily represented by arthropods. How-
ever, if the ubiquitous nature of zooparasitic nematodes among vertebrates and
invertebrate hosts is considered, along with the realization that many will be
host-specific in their distributions, it is clear that parasites represent a substan-
tial facet of biodiversity that yet has to be evaluated in detail. Even with the
small fraction of parasitic helminths so far described, a wealth of data on life

TABLE 17-1 Species Diversity of the Major Phyla of

Helminthic Parasites of Vertebrates: The Numbers of
Described Species

Platyhelminthes
Monogenea >5,000
Digenea >5,000
Eucestoda ~4,000
Nematoda >12,000
Acanthocephala ~700
Perspectives on Diversity
45,000 species of potential vertebrate hosts
~4,000 species of tapeworms are described
~ 20% of ~850 species of elasmobranchs have been examined
hundreds of species of Tetraphyllidea (Eucestoda) are described

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PHYLOGENY AND HISTORICAL RECONSTRUCTION / 245

history and distribution exists for application in ecological and historical assess-
ments of biotas. Such information, although traditionally of interest only to para-
sitologists, is now considered to directly complement and augment knowledge
derived solely from the study of free-living organisms on which parasites are
dependant. Because of the unique insights gained from parasitological studies
about evolution of ecological interactions and community structure, parasitol-
ogy is becoming recognized as an integral constituent of biodiversity research
programs (Brooks, 1985; Brooks and McLennan, 1991, 1993). Biodiversity stud-
ies thus are promoting a revitalization of systematics and a renewed apprecia-
tion of parasitology as one of the most integrative of the biological disciplines.

HISTORICAL RECONSTRUCTION
Historical reconstruction deals with estimation of organismal diversifica-
tion, distributional history, ecological interactions, and continuity of commu-
nity structure over evolutionarily significant time frames. It is the study of pat-
tern and process in the origin and development of biotas emphasizing the
historical components of diversity. The basic facets of such research involve an
integration of phylogeny (Hennig, 1966; Wiley, 1981; Wiley et al., 1991), his-
torical biogeography (Cracraft, 1982; Nelson and Platnick, 1981; Wiley, 1988a),
and historical ecology (Brooks, 1985) in the construction of a macroevolutionary
framework to understand biological evolution (Brooks and McLennan, 1991;
Brooks et al., 1992). The organization of past environments and the faunal and
floral assemblages that they constituted is of critical interest to this research
program. Primary issues emphasize how communities (biotas) have been struc-
tured by climatological, geological, and biotic factors and the utilization of his-
torical analysis as a key to understanding attributes of contemporary diversity
patterns (Brooks et al., 1992; Cracraft, 1980).
Utilization of phylogenetic methodologies allows researchers to develop
hypotheses about the history of biotic associations (Brooks, 1985). By focusing
on patterns of species distribution and speciation (largely an allopatric process),
these hypotheses examine the relationship of diversification within and among
clades as a function of past and present environments (Brooks et al., 1992).
Analyses of the historical sequence of addition of species and longevity within
communities allows identification of elements that are residents (as a function of
vicariance) or colonizers (via dispersal) of specific biotas. As a logical extension,
it becomes possible to consider the nature and duration of ecological associa-
tions, stability of ecological interactions, and the evolution and maintenance of
specific life history traits.
The significance of historical reconstruction, and the disciplines subsumed
within this program, to current approaches in biodiversity assessment resides in
the observation that the past is the key to the present. Historical reconstruction
allows identification of historically important centers of diversification (ances-

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246 / BIODIVERSITY II

tral areas), provides a predictive framework to assess the importance of specific

habitats, geographic regions, and biotas and areas of critical genealogical and
ecological diversity (Brooks and McLennan, 1991; Erwin, 1991; Vane-Wright et
al., 1991). Identification of the most vulnerable members of a community sub-
sequently is based on phylogenetic distinctiveness (Vane-Wright et al., 1991),
degree of endemism (Brooks et al., 1992; Erwin, 1991) and unique historical
ecological associations (Brooks et al., 1992). Recognition of these facets in turn
allows us to make more reliable predictions about the impacts of natural and
anthropogenic perturbations on ecosystem structure and stability (Brooks et
al., 1992). In this regard, it is becoming increasingly evident that parasites con-
stitute probes for the elucidation of complex linkages among organisms across
the genealogical, ecological, spatial, and temporal scales that characterize
biodiversity.

PARASITES AND HISTORICAL RECONSTRUCTION

Associations of hosts and parasites generally are not random and tend to
reflect some degree of stability indicative of long-term (evolutionary) relation-
ships. This is not a recently recognized phenomenon among parasitologists,
many of whom have investigated the predictable nature of parasite-host assem-
blages (for review, see Klassen, 1992a). For example, Krabbe (1869) and
Fuhrmann (1909) were among the earliest biologists to note the narrow distribu-
tions of specific cestode taxa among phylogenetically related taxa of birds. It
was von Ihering (1891, 1902), however, who first utilized helminthic parasites
in a zoogeographic context. His recognition of an old (Gondwanan) connection
between South America and New Zealand formed the conceptual foundation for
parasitology as an integral facet of studies in historical biogeography and coevo-
lution (Brooks and McLennan, 1993; Klassen, 1992a).
The rich and longstanding tradition of an interplay between parasitology,
coevolution, and biogeography is reflected in a series of rules that outline the
determinants of the parasite-host relationship (Brooks and McLennan, 1993;
Klassen, 1992a). Among the most prominent is Fahrenholz’s Rule, which states
that parasite phylogeny mirrors host phylogeny; and Manter’s Rules that deal
with host-specificity and its relationship to coevolution and aspects of historical
biogeography. Manter (1966) believed that parasites could serve as keystones
for understanding the history of biotas because he recognized the importance of
helminths as phylogenetic, ecological, and biogeographic indicators of their host
groups (Brooks and McLennan, 1993). This message was implicitly understood
among parasitologists, based on the empirical evidence of host-specificity, com-
plex life cycles that were dependant on specific and predictable trophic rela-
tionships (Figure 17-1), and definable geographic distributions for many assem-
blages (Brooks and McLennan, 1993; Klassen, 1992a). Although these generalities
were recognized and codified, testing of their universality was limited until the

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PHYLOGENY AND HISTORICAL RECONSTRUCTION / 247

FIGURE 17-1 Representation of a complex parasite life cycle dependant on trophic link-
ages, showing the putative cycles for a number of genera of tetrabothriid cestodes that
infect marine homeotherms. Adult tapeworms occur in seabirds (Tetrabothrius), ceta-
ceans (Tetrabothrius, Trigonocotyle, and Priapocephalus), and pinnipeds (Anophryo-
cephalus); larvae or metacestodes develop in crustaceans as intermediate hosts. Larval
parasites also become available to seabirds and marine mammals via fish or cephalopods
that serve as paratenic or ecologically-transported hosts. In this life cycle, transmission is
dependant on specific predator-prey relationships.

advent of phylogenetic methodologies (Hennig, 1966) and their application to

historical analysis of host-parasite systems (Brooks, 1979a, 1981; Brooks and
McLennan, 1991, 1993).

Conceptual Foundations
Host and geographic ranges of parasites historically are constrained by ge-
nealogical and ecological associations (Brooks, 1979a, 1981, 1985) that can be
examined within a phylogenetic context (Brooks and McLennan, 1991, 1993).
This framework allows us to examine the origin, temporal continuity, and dis-
tribution of a parasite-host assemblage with respect to alternative, but not mu-
tually exclusive, hypotheses for coevolution or colonization (Mitter and Brooks,
1983).
Coevolution refers to “association by descent” and may be reflected in
vicariant geographical patterns for parasites or in ancestor-descendant relation-
ships for hosts and parasites (Brooks and McLennan, 1993). Coevolutionary hy-
potheses are corroborated by congruence between area relationships (i.e., con-
gruence in the distributional relationships of multiple parasite clades across a
definable geographic region) and parasite phylogenies, or between host-parasite
phylogenies. Predictions that follow from coevolutionary hypotheses include a
protracted association for hosts and parasites, a high degree of cospeciation and
coadaptation, and possible recognition of numerical and phylogenetic relicts

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248 / BIODIVERSITY II

(Brooks and Bandoni, 1988; Brooks and McLennan, 1991, 1993; Hoberg, 1992).
Although host-specificity may be observed in coevolutionary associations, it is
a phenomenon that should not be considered to reflect the temporal extent of a
host-parasite relationship (Brooks, 1985; Hoberg, 1986). Congruence of biogeo-
graphic patterns among parasite clades permits identification of general area
relationships that are indicative of faunal assemblages that have been influenced
by the same physical and biotic processes as determinants of distribution. Such
general patterns are employed to recognize historically important regions of
ongoing organismal evolution and areas of endemism that are indicative of
relictual communities.
Alternatively, uncovering incongruencies between parasite and host phy-
logenies or area relationships highlights the components of a biota that have
been structured by colonization (host-switching). Predictions based on a coloni-
zation hypothesis include a similarity in host-trophic ecology, geographically
delimited faunas, and associations of variable temporal extent and degree of
cospeciation or coadaptation as determined by the time frame for colonization of
an area or host clade (Brooks and McLennan, 1991; Hoberg, 1986, 1992, 1995).
Within the context of coevolution or colonization then, the temporal duration of
an assemblage may be elucidated with respect to host-parasite distribution, his-
torical biogeography of hosts, and aspects of regional history and physical geol-
ogy (Hoberg, 1986; Hoberg and Adams, 1992).
Historical evaluations of host-parasite associations have been termed “para-
script studies” in recognition of the messages conveyed by parasites to investi-
gations of evolution, ecology, and biogeography (Brooks and McLennan, 1993;
Manter, 1966). Such studies are minimally based on an integration of genealogi-
cal hypotheses for parasites and hosts, distributional patterns, and geological
history (Brooks and McLennan, 1993; Wiley, 1988b). Typically, data from para-
sites are optimized onto a host tree or area cladogram to provide an historical
context for hypotheses about the development of specific parasite-host assem-
blages. However, even in the absence of robust hypotheses for the host group,
substantial historical ecological and biogeographic conclusions may be derived
from reconstruction of area and host relationships based on assessments of mul-
tiple groups of parasites (Brooks, 1981, 1988), a process termed Brooks Parsi-
mony Analysis (Wiley, 1988b; Brooks and McLennan, 1991). Indeed, phyloge-
netic studies for a variety of helminth groups, formulated solely on the characters
intrinsic to parasites, have provided parasitologists with a means to indepen-
dently evaluate the history of host taxa or geographic regions for which there is
currently a paucity of information (Brooks and McLennan, 1993).

Current Research Programs

Parasites constitute “biodiversity probes” that can be applied directly to
questions of contemporary diversity and the historical development of commu-

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PHYLOGENY AND HISTORICAL RECONSTRUCTION / 249

nity structure (Brooks and McLennan, 1993; Brooks et al., 1992; suggested by D.
R. Brooks in Gardner and Campbell, 1992a). The dual phenomena of host-para-
site evolution (coevolution, colonization, or host-switching) and faunal distribu-
tion (endemism and elucidation of ancestral areas for biotas) are keystones to
examining patterns of diversity. In addition, complex life cycles of helminths
are strongly correlated with intricate foodwebs and are dependant on specific
ecological interactions and climatological conditions (Figure 17-1). Dependance
on a series of intermediate (usually invertebrate), paratenic (invertebrate and
vertebrate), and definitive hosts (vertebrates) indicates that each species of para-
site exquisitely represents an array of organisms within a community and tracks
broadly and predictably across many trophic levels (Brooks, 1985; Brooks and
McLennan, 1993; Hoberg, 1986, 1992, 1995). Thus, knowledge of the evolution
of parasite-host assemblages provides direct estimates of the history of ecologi-
cal associations and community development and is indicative of the temporal
continuity of trophic assemblages (e.g., Hoberg, 1987). Not surprisingly, studies
of helminthic parasites in terrestrial, aquatic, and marine systems have shown
these organisms to be elegant markers of contemporary and historical ecological
relationships, biogeography, and host phylogeny (Table 17-2; and reviewed in
Brooks and McLennan, 1993).
Parasites are thus critical to the recognition of historically important centers
of organismal diversification and the spatial and temporal continuity of biotas.
At a contemporary level, a predictive framework, with parasites as indicators,
exists for elucidating the impacts of natural or anthropogenic perturbations to
faunas and ecosystems. It then becomes possible to examine the influence of
faunal introductions, extirpations, extinctions, and habitat alterations within a
rigorous framework employing parasites as ecological indicators.
The range of explicitly phylogenetic and historical studies of parasites spans
the time frame from the Mesozoic era through Recent time, and covers a full
spectrum of habitats and taxa of vertebrates (Table 17-2). These studies have
indicated that coevolution is not a universal phenomenon and, interestingly,
that entire faunas have originated by host-switching and subsequent coevolu-
tion—e.g., colonization of pelagic marine birds and mammals by tetraphyllidean
cestodes of elasmobranchs in the Tertiary (Hoberg, 1987). This reinforces the
importance of the dual components of parasite evolution, guild associations, and
evolutionary time in the development of biotas and the utility of parasites in
historical reconstruction. These concepts can be examined in greater detail us-
ing specific examples from freshwater, terrestrial, and marine communities.

Freshwater Rays, Parasites and the Amazon: A Pacific Origin

Among the elasmobranchs, only stingrays of the family Potamotrygonidae
are restricted in their distributions to riverine habitats and occur only in the
major drainages of eastern South America. They were traditionally considered

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250 / BIODIVERSITY II

TABLE 17-2 Key Papers Using Helminthic Parasites in Historical

Reconstruction in Terrestrial, Aquatic and Marine systemsa

Historical
Parasites/Hosts Region Age Conceptsb

Terrestrial Systems
Platt (1984)
Nematoda/Cervidae Holarctic Pliocene- C,B
Pleistocene
Glen and Brooks (1985, 1986),
Brooks and McLennan (1993)
Nematoda/Primates Africa Late Tertiary C,B
Gardner (1991)
Nematoda/Rodentia Neotropical Tertiary C,B,E
Gardner and Campbell (1992a,b)
Cestoda/Marsupials Gondwanan Cretaceous C,B,E
Hoberg and Lichtenfels (1994)
Nematoda/Artiodactyla Cosmopolitan Tertiary C,B
Aquatic Systems
Von Ihering (1891, 1902)
Turbellaria/Crustacea Gondwanan Cretaceous B
Brooks (1977), Brooks and McLennan (1993)
Digenea/Anura Gondwanan Cretaceous C,B
Brooks and Overstreet (1978)
Digenea/Crocodilia Pangean Mesozoic C,B
Brooks (1978a, 1978b)
Eucestoda/Fish, Amphibians Pangean Mesozoic C,B
Brooks (1979b, 1980),
Brooks and O’Grady (1989)
Helminths/Crocodilia Pangean Mesozoic C,B
Brooks et al. (1981),
Brooks and McLennan (1991, 1993),
Brooks (1992)
Helminths/Stingrays Neotropical Cretaceous C,B,E
(Amazon)
Bandoni and Brooks (1987a)
Amphilinidea/Teleosts Pangean Mesozoic C,B
Klassen and Beverley-Burton (1987)
Monogenea/Siluriforms Nearctic Cretaceous C,B,E
Klassen and Beverley-Burton (1988)
Monogenea/Centrarchids Nearctic Pliocene- C,B
Pleistocene
Boeger and Kritsky (1988),
Van Every and Kritsky (1992)
Monogenea/Cypriniforms Neotropical Pliocene- C,B
(Amazon) Pleistocene
MacDonald and Brooks (1989)
Digenea/Turtles, Snakes Nearctic — C
Beverley-Burton and Klassen (1990)
Monogenea/Fishes Laurasian Cretaceous C,B
Platt (1992)
Digenea/Freshwater Turtles Pangean Triassic C,B

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PHYLOGENY AND HISTORICAL RECONSTRUCTION / 251

TABLE 17-2 Continued

Historical
Parasites/Hosts Region Age Conceptsb

Marine Systems
Manter (1966)
Digenea/Fishes — — B,E
Hoberg (1986, 1992)
Eucestoda/Seabirds Holarctic Pliocene- C,B,E
Pleistocene
Bandoni and Brooks (1987b)
Gyrocotylidea/Holocephala Pangean Mesozoic C,B
Brooks and Deardorff (1988)
Helminths/Elasmobranchs Gondwanan Cretaceous C,B
Hoberg and Adams (1992),
Hoberg (1992, 1995)
Eucestoda/Pinnipedia Holarctic Pliocene- C,B,E
Pleistocene
Klassen (1992b)
Mongenea/Tetraodontiforms Indo-Pacific, Tertiary C,B
Caribbean

aAdditional studies cited in Brooks (1988) and Brooks and McLennan (1993).
bHistorical concepts: C=coevolution; B=historical biogeography; E=historical ecology.

to be of marine origin, having ascended each river system from the Atlantic
basin in the late Tertiary (see Brooks 1992; Brooks et al., 1981). However an
alternative hypothesis suggesting relatively archaic origins from faunas present
in the eastern Pacific was based on the study of multiple taxa of helminthic
parasites typical of these rays (Brooks and Deardorff, 1988; Brooks et al., 1981).
This alternative hypothesis was based on the discovery that the sister-
groups for some helminths inhabiting potamotrygonids occur in marine rays in
the Pacific, not in the Atlantic (Brooks and Deardorff, 1988; Brooks and
McLennan, 1991). When the phylogenetic hypotheses for helminths of potamo-
trygonids were expressed as an area cladogram, an historical geological or
vicariant backbone sequentially linking faunas in the upper Amazon, Parana,
Orinoco, and Magdalena drainages of eastern South America was revealed (Fig-
ure 17-2). This sequence corresponds to the geological history of the region
beginning with the southern Andean orogeny in the late Cretaceous. Notably,
the ancient Amazon flowed into the Pacific until the Miocene, when it was
blocked by the northward trend of the Andean orogeny, and later developed
into a major inland sea prior to flowing into the developing Atlantic basin
(Brooks, 1992). Thus, entrapment and subsequent diversification of the ancient
Amazonian fauna coincided with the uplifting of the Andes (Brooks, 1992;
Brooks et al., 1981, 1992).

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FIGURE 17-2 Area relationships and history of the helminthic parasite fauna of the
potamotrygonid freshwater stingrays endemic to South America (after Brooks and
McLennan, 1993; Brooks et al. 1981). This area cladogram shows the vicariant backbone
for the origins and diversification of the helminth fauna, with an ancestral region in the
eastern Pacific, initial entrapment in the upper Amazon (UA), and sequential vicariance
and diversification in the Parana (P), Orinoco (O), and Magdalena (M) drainages. The
stippled region depicts the present position of the Andes Mountains, which developed
by orogeny from the south to the north starting in the Cretaceous. The secondary history
of dispersal for the fauna among adjacent river basins is not depicted, but is shown in
Brooks and McLennan (1993).

A Pacific origin for the freshwater stingrays and many of their parasites is
compatible with similar hypotheses for the derivation of freshwater anchovies
and needlefish in the Amazon basin (Brooks, 1992). However the occurrence of
a riverine/lacustrine parasite fauna with marine affinities is dependant on the
availability of suitable intermediate and definitive hosts to support specific life

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PHYLOGENY AND HISTORICAL RECONSTRUCTION / 253

cycles. In this instance, suitable molluscan and arthropodan species must have
been isolated with the stingrays over an extended period of time in estuarine
systems that coincides with the Andean orogeny (Brooks, 1992). This leads to
the striking conclusion that a sizable component of current diversity in freshwa-
ter systems of the Neotropics might have been derived from marine ancestors in
the eastern Pacific in the late Cretaceous to Tertiary (Brooks, 1992). Thus, his-
torical biogeographic and ecological analysis of parasites of potamotrygonids
highlights the unique nature of what is now a nonrenewable constituent of
biodiversity in tropical freshwater communities (Brooks et al., 1992).

Tapeworms and Transantarctic Marsupials

Similar archaic origins also have been suggested for the linstowiid cestode
faunas of marsupials and some monotremes in the Neotropics and Australia
(Gardner and Campbell, 1992a,b). For example, some cestodes of didelphid mar-
supials in South America have a limited range in the Yungas-Chaco ecotone of
Bolivia, a region considered
to contain a relictual biota.
Phylogenetic analysis of the
known species of Linstowia
corroborates this contention,
suggesting ancient trans-
antarctic connections for hosts
and parasites extending from
the late Cretaceous (Figure
17-3; also see Gardner and
Campbell, 1992a).
This fauna has implica-
tions for understanding long-
term ecological stability of
habitats in South America and
Australia. Life cycles of spe-
cies of Linstowia are complex,
requiring both an arthropo-
dan intermediate and a mam-
malian final host. This implies
that specific life history asso-
ciations and patterns of trans-
mission that are currently
evident existed prior to the
geological separation of South
America, Antarctica, and Aus-
tralia in the late Mesozoic to Mouse opossum, a South American marsupial.

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FIGURE 17-3 The transantarctic distributional history for Linstowia from didelphid
marsupials and monotremes in South America and Australia is summarized (based on
Gardner and Campbell, 1992a). This area cladogram depicts the current distribution and
phylogenetic relationships of the fauna that developed following vicariance of an ances-
tral host-parasite assemblage in the Cretaceous. The following species are depicted: in
South America, IH=Linstowia iheringi, SC=L. schmidti, and SP=a currently unnamed
species; in Australia, SE=L. semoni, EC=L. echidnae, and MA=L. macrouri. The paleo-
reconstruction of the southern Gondwanan continental land masses is based on Dietz and
Holden (1976).

early Tertiary (Gardner and Campbell, 1992a). Cestode faunas continue to exist
in endemic regions that have remained intact over the past 60 million years. It is
apparent that such historically important biotas can be identified using a combi-
nation of information on current distribution and life cycles in conjunction with
phylogenetic analyses of a fauna. In this case, the occurrence of a particular
parasite-host assemblage has provided extensive information about ecological
interactions across a temporal scale from the contemporary to the archaic.

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PHYLOGENY AND HISTORICAL RECONSTRUCTION / 255

Seabirds, Pinnipeds, and Pleistocene Marine Refugia

Although much of the historical research using host-parasite phylogeny has
involved faunas with relatively ancient origins, often structured by vicariant
(usually tectonic) processes (Table 17-2), it is also possible to examine associa-
tions that have relatively recent derivations. For example, consider the congru-
ent and synchronic patterns in distribution and speciation that have been postu-
lated for phylogenetically disparate groups of tapeworms that parasitize
pinnipeds and seabirds in the Holarctic (Hoberg, 1986, 1992, 1995; Hoberg and
Adams, 1992). Combined results of phylogenetic analyses of tetrabothriid ces-
todes of the genus Anophryocephalus, a largely host-specific group inhabiting
phocids and otariids, and dilepidid cestodes of the genus Alcataenia among the
Alcidae (principally in puffins, murres guillemots, and some auklets) yielded a
general area relationship or pattern for host and parasite diversification in the
North Pacific basin, North Atlantic, and adjoining areas of the Arctic. Although
the host groups are relatively old (Miocene), the parasite groups are not, with
host-parasite associations having developed via colonization of pinnipeds and
alcids over the last 3 million years (since the late Pliocene and Pleistocene)
(Hoberg, 1992). In the absence of a phylogenetic reconstruction, this is not an
obvious conclusion.
Two primary areas of diversity are recognized for these groups: (1) a puta-
tive ancestral area for both faunas in the North Atlantic sector of the Arctic
basin that coincides with the current distribution of basal members of both as-
semblages; and (2) a region of secondary diversification for hosts and parasites
in the North Pacific (Figure 17-4). This general pattern resulted from early
vicariance of a Holarctic fauna across the Beringian region, followed by radia-
tion in the North Pacific with subsequent range expansion into the Arctic basin
and Atlantic for alcids, phocids, and their respective parasites. Diversification
during the late Pliocene and Pleistocene was tied to climatic factors. During
glacial maxima, refugial habitats were distributed in marginal zones of the North
Pacific, Sea of Okhotsk, Aleutian Islands, and Arctic basin as a function of
eustatic reduction in sea level. These changes resulted in the isolation of small
populations of hosts and parasites, establishing the initial conditions for either
peripheral isolates or microvicariance speciation (e.g., Lynch, 1989; Wiley, 1981).
During interstadials (warm periods between glacial advances), ranges of hosts
and parasites expanded, increasing the potential for host-switching. The para-
site fauna in this region thus is characterized by a pattern of sequential coloni-
zation, vicariance, and speciation of peripheral isolates that is driven by the
fluctuating geographic ranges of the definitive host groups in response to ref-
ugial expansion and contraction (Hoberg, 1995). Although the phylogenetic his-
tories for parasites and hosts were highly incongruent (as would be expected for
instances of host-switching), there was a general synchrony in speciation events
during radiation of these phylogenetically unrelated tapeworms in marine birds

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256 / BIODIVERSITY II

FIGURE 17-4 Historical summary of the congruent and synchronic relationships of

marine parasite faunas among pinnipeds and alcids in the Holarctic during the late
Pliocene and Pleistocene showing distributional history (solid lines), current geographi-
cal limits for the faunas (dashed lines delimiting the Pacific and Atlantic basins), and
emergent continental shelf during glacial maxima (stippled regions)(after Hoberg, 1992;
also see Hoberg, 1986, 1995; Hoberg and Adams, 1992). (1) Putative ancestral area for
Alcataenia and Anophryocephalus in seabirds and pinnipeds, respectively (ca. 3.0 to 3.5
million years ago). (2) Early Holarctic distributions for host-parasite assemblages attained
by ca. 2.5 to 3.0 million years ago. (3) Initial submergence of Beringia (ca. 3.0 million
years ago) was followed by range expansion for hosts and parasites into the North Pacific
and subsequent colonization and radiation in refugial habitats during the Pleistocene. (4)
Secondary Holarctic ranges for some species of Alcataenia and Anophryocephalus were
attained during the Quaternary. (5) Diversification of Anophryocephalus continued with
the colonization of sea lions during the Quaternary.

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PHYLOGENY AND HISTORICAL RECONSTRUCTION / 257

and mammals (Hoberg, 1992; Hoberg and Adams, 1992). Given the complexity
of these parasite distributions, the high degree of biogeographic congruence
indicates that these systems have been strongly influenced by the same geologi-
cal and climatological factors.
These host-parasite assemblages are indicative of specific ecological associa-
tions via food webs that have been maintained since at least the late Pliocene
(Hoberg, 1992, 1995). Trophic interactions, food habits, and foraging behavior
also appear to have influenced the potential for colonization among feeding
guilds where hosts exploited a common prey source (Hoberg, 1984a,b, 1986,
1987). Although ecologically cohesive and characterized by a high level of host-
specificity, it is apparent that these faunas are not relicts of a previous biota, but
were structured by host-switching, geographical colonization, and cyclic clima-
tological fluctuations that characterized the late Pliocene and Pleistocene
(Hoberg, 1992, 1995). In other words, the dramatic climatic changes associated
with the Pliocene-Pleistocene glaciations promoted speciation, not extinction, in
these Holarctic marine faunas. These marine parasite-host systems thus provide
a counterintuitive view of diversification at high latitudes over the past 3 mil-
lion years.

CONCLUSIONS: PARASITES AS HISTORICAL

PROBES FOR BIODIVERSITY
Parasites are elegant indicators of historical ecological associations and bio-
geography. The complexities of parasite life cycles, dependant on a series of
intermediate, paratenic, and definitive hosts, indicate that each species of helm-
inth represents a broader array of organisms within a community. Thus, knowl-
edge of the evolution of a parasite-host assemblage can provide direct estimates
of the history of ecological associations and is indicative of the continuity of
trophic assemblages through time. The genealogical and biogeographic histories
of parasitic helminths provide considerably more information than that avail-
able only from the evaluation of phylogenetic hypotheses for free-living organ-
isms alone (e.g., Erwin, 1991; Stiassny, 1992). This means that parasites are ad-
mirably suited for a role as historical and contemporary biodiversity probes
(Brooks and McLennan, 1994; Brooks et al., 1992; Gardner and Campbell, 1992a)
and for augmenting the development of conservation strategies through recog-
nition of regions of critical diversity and evolutionary significance.
Considered from a conservation standpoint, the phylogenetic history of
parasite-host assemblages allows direct predictions about the age and duration
of specific faunal associations, identification of regions of endemism and evolu-
tionary “hot spots,” and the historical structure of ecosystems and communi-
ties. These data can be applied to complex decisions in conservation biology
through recognition of distinctive clades (e.g., Stiassny, 1992; Vane-Wright et
al., 1991), geographic regions of past (and future) evolutionary importance (e.g.,

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258 / BIODIVERSITY II

Brooks et al., 1992; Erwin, 1991), and unique historical ecological associations
(Brooks and McLennan, 1991, 1994).
The focus of Brooks et al. (1981) and Gardner and Campbell (1992a) on hel-
minthic faunas of South American elasmobranchs and mammals highlights the
importance of phylogenetic studies of parasites in identifying significant areas
of endemism in the Neotropics. Succinctly stated by Brooks and McLennan
(1994:23): “Areas of endemism are important because they have been the focus
of biodiversity production in the past and thus may be `hot spots’ of evolution-
ary potential for the future.” In this regard, the distinctive community associ-
ated with the Yungas-Chaco ecotone of Bolivia indicates that this region could
merit reserve status (Gardner and Campbell, 1992a). In addition, the drainages
of the upper Parana River, Amazon River, and Magdalena River support vital
faunal assemblages, represented by unique parasite and elasmobranch faunas,
which are currently isolated and “... represent good compromises between the
need to protect and the need to develop...” (Brooks et al., 1992:58).
Historical studies of parasite-host associations also have applications in out-
lining potential climatological determinants of biodiversity. It has been predicted
that communities in the Arctic may respond dramatically to environmental al-
teration driven by changes in global climate (e.g., Danks, 1992; Douglas et al.,
1994). Historically, patterns of diversification and biogeography among seabirds,
pinnipeds, and parasites across the Holarctic have been strongly influenced by
environmental fluctuations during the Quaternary (Hoberg, 1986, 1994). Ap-
plied as an analog, altered patterns of distribution among contemporary parasite
assemblages in the Arctic may serve as indicators of natural and anthropo-
genically driven perturbations in climate.
The past is the key to the present, where historical reconstruction involving
parasites contributes to a predictive framework for discovering the interaction
of biotic communities, environment, and climate. As a consequence, parasites
constitute powerful tools and represent keystones to be applied to questions of
the origin, maintenance, and distribution of organismal diversity.

ACKNOWLEDGMENTS
The conceptual foundations for this paper were developed through discus-
sions over the past several years with D. R. Brooks, G. J. Klassen, D. Siegel-
Causey, and D. A. McLennan. Critical and insightful evaluations of the manu-
script by D. A. McLennan, A. Y. Rossman, D. R. Miller, and J. R. Lichtenfels
were greatly appreciated.

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PHYLOGENY AND HISTORICAL RECONSTRUCTION / 259

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CHAPTER
18

Comparative Behavioral and

Biochemical Studies of Bowerbirds, and
the Evolution of Bower-Building

GERALD BORGIA
Professor, Department of Zoology, University of Maryland, College Park

Unprecedented human-induced changes in the environment are causing a

rapid loss of species and their habitats. Common responses to the loss of bio-
diversity include habitat conservation and increased efforts to understand the
origin and maintenance of biodiversity. While there is no doubt that these are
critical activities, it is unclear the extent to which these and related conservation
approaches can stem the tide of extinctions. Global threats such as climatic
warming and ozone depletion place all species on the planet at risk and compli-
cate attempts to determine the level of threat for particular species or communi-
ties.
There must be an intensive effort to collect information about species before
they go extinct or are relegated to reserves in degraded habitats. Otherwise, we
never will have detailed information about the life history, specialized adapta-
tions, social behavior, or relationships with other species for the vast majority of
species that go extinct. For those left close to extinction in degraded habitats, in
zoos, or in preserves, our ability to understand their ecological and evolutionary
relationships to other species and the surrounding habitat will be greatly com-
promised.
Wilson (1992) describes “unmined riches” locked in the diverse and poorly
known biotas. He offers recent discoveries of natural seed stocks and the use of
secondary compounds from plants as pharmaceutical agents as examples of such
riches. But biologists have been less emphatic about the unmined intellectual
resources that are lost with extinction. As species go extinct and habitats are
degraded, the opportunity to use natural communities as sources of information
about basic physiological, ecological, and evolutionary processes is lost forever.

263

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As with basic research in other areas, the natural historical sciences also offer
prospects for unforeseen intellectual and economically important discoveries.
The grim prospect of the loss of much biodiversity is tempered somewhat
by the availability of many well-trained experts in a variety of natural historical
fields, by the maturation of these fields in which intellectually significant issues
have been identified, and the explosion of new tools to decode the information
locked up in natural systems. Molecular methods for phylogenetic reconstruc-
tion, methodologies for comparative studies, and automated equipment that al-
lows collection of data on diverse sorts of organisms all are becoming available
and are being put to use in field studies. It is a sad coincidence that, as we are
gaining sophisticated tools for exploring the natural history of organisms, there
is a dramatic loss of species that can be studied. We are at a critical time when
we have the opportunity to collect some of the most detailed and useful natural
history information before many species go extinct. A broadly based bio-
diversity initiative that emphasizes both conservation and natural historical
studies directed at species in still vibrant populations must be considered the
only appropriate response to the loss of biodiversity.

EVOLUTION OF BOWERBIRDS
In this Chapter, I present information from a comparative study of bower-
birds (Ptilonorhynchidae) on the likely causes of the evolution of bowers. This
work has been motivated by an interest in the causes of mate choice in species
with extreme displays. It serves to illustrate the importance of studies that
involve comparisons between species.
Bowerbirds occur across the Australio-Papuan region and are unique in that
males build structures on the ground called bowers that appear to function in
mate attraction and related activities. The first 7 years of my work on bower-
birds focused on the satin bowerbird (Ptilonorhynchus violaceus). Previously,
there had been no detailed quantitative study of any aspect of bowerbird be-
havior. After those 7 years, I felt that I had a good understanding of typical
bowerbird behavior. This belief was shaken after a preliminary study of spot-
ted bowerbirds (Chlamydera maculata) that showed fundamentally different
patterns of courtship and male interactions from those observed in satin bower-
birds. Since then, my students and I have studied nine additional species of
bowerbirds.
As an example demonstrating the value of comparative studies involving
a large number of species, this work shows that even among closely related
species there can be very large differences in behavior. One cannot character-
ize a group like bowerbirds based on studies of single species, and there is no
typical species that fully represents this group. Information from numerous
species often is needed to understand the evolution of complex traits like
bower-building.

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COMPARATIVE STUDIES OF BOWERBIRDS / 265

Bower bird moving through undergrowth.

Mate selection in species with elaborate male display traits was a topic cen-
tral to Charles Darwin’s (1859, 1871) seminal writings on sexual selection. Promi-
nent in his discussion of sexual selection were the bowerbirds and their unique
behavior of building bowers. Bowers typically are made of sticks. In some
species, bowers can reach 1.5 m high and are built near display courts decorated
with more than 2,000 decorations. These elaborate decorated structures fre-
quently have been described as one of the wonders of the animal world.
There are now numerous hypotheses explaining how extreme displays
evolve, although clear answers remain elusive. “Good genes” models propose
that extreme sexual displays function as indicators of male quality to females
choosing mates (e.g., Andersson, 1982, 1986; Borgia, 1979; Hamilton and Zuk,
1982; Trivers, 1972; Zahavi, 1975). Alternatively, the runaway model (Fisher,
1930; Kirkpatrick, 1982; also see Lande, 1981) posits that female preferences can
produce greatly elaborated male display traits without providing enhanced vigor
to offspring. Other models include: passive choice (Andersson, 1982; Parker,
1983), intrasexual signaling (Halliday, 1978; LeCroy et al., 1980), proximate ben-
efits (e.g., protection to females provided by well-constructed bowers; Borgia et al.,
1985) and innate preferences (Burley, 1985; Kirkpatrick, 1987; Ryan et al., 1990).
Recent empirical studies have shown that elaborate displays in polygynous
species are typically not single traits, but a complex sets of traits (Andersson,
1989; Borgia, 1985; Gibson et al., 1991; McDonald, 1989; Moller and
Pomiankowski, 1993; Prum, 1990; Zuk et al., 1990). In bowerbirds, bowers and
decorations are part of a generalized display that includes plumage, acoustical,

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266 / BIODIVERSITY II

and dancing elements directed at females during courtship. Recent studies indi-
cate that females prefer males with well-built and well-decorated bowers (Borgia,
1985; Borgia and Mueller, 1992), indicating that an important current function
of bowers and decorations is to attract mates. The large number of models for
explaining elaborated display traits, the lack of specific predictions from some
of these models, and the complex array of traits involved in the display of po-
lygynous species have made it difficult to develop clear-cut conclusions about
the evolution of extreme male displays. Elsewhere it has been suggested (Borgia
et al., 1985) that bowers may function in female assessment of male quality as
sires (good genes), as a protective device for females being courted (proximate
benefit), or as a structure with no direct functional significance outside the con-
text of sexual selection (runaway or latent preference).
Comparative studies of the evolution of traits among related species can
provide critical information about the sequential evolution of the components of
display and their initial and derivative functions (Basolo, 1990; Brooks and
McLennan, 1991; Kusmierski et al., 1993; Prum, 1990).
Several recent developments have made it possible to carry out a detailed
comparative analysis of the function of bowers. First, the use of remote-con-
trolled cameras aimed at bowers where males display and mate has allowed my
students, field assistants, and me to simultaneously monitor all activity at as
many as 30 bowers through an entire mating season. Because bowers are widely
separated and the mating periods may last several months, it would have been
impossible otherwise to obtain detailed information from numerous bowers.
Second, the advent of molecular techniques has made it possible to build a phy-
logeny of bowerbirds based on mitochondrial DNA sequence information. The
independent derivation of this phylogeny makes it possible to infer the histori-
cal pattern of the evolution of display traits by using maximum parsimony meth-
ods to map the distribution of particular male display traits and their occurrence
in ancestors onto the phylogeny. By combining these techniques, my students,
collaborators, and I have been able to gather detailed information on the display
traits of bowerbirds and map this information onto an independently derived
phylogeny of the bowerbirds.
Building bowers is restricted to the family Ptilonorhynchidae, which is made
up of six genera. One genus, the catbirds (Ailuroedus, three species), is monoga-
mous and does not clear a display court. Members of the remaining five genera
are polygynous, clear a court, and typically build a bower. There are two major
designs of bowers. Maypole bower-builders decorate a sapling with sticks.
Males of species in the genus Amblyornis (four species) typically decorate a single
spire surrounded by a mossy circular court, and two species build a hut-like
dome that covers part of the court. Prionodura newtoniana builds a two-spired
structure with a cross perch connecting the spires. Avenue-builders (three
genera, eight species) build a two-walled structure with a display court near
the end of the bower. Two other species, toothbills (Scenopoeetes dentirostris)

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COMPARATIVE STUDIES OF BOWERBIRDS / 267

Ptiloris paradiseus
100
Epimachus albertsil

Gymnorhina tibicen
Alluroedus crassirostris no bower

Prionodura newtoniana maypole

100
98
84 Amblyomis macregoriae maypole

Scenopoeetes dentirostris stage

81 Chlamydera maculata avenue
96
95 Chlamydera nuchalls avenue
99 Ptilonorhynchus violaceus avenue

Sericulus chrysocephalus avenue

FIGURE 18-1 Phylogeny of the bowerbirds based on information from mt-DNA se-
quences taken from Kusmierski et al. (1993). The topmost grouping represents two Birds
of Paradise (paradise riflebird and the brown sickelbill) and the Australian magpie. The
bowerbirds are represented in three clades represented by the monogamous catbirds
(Ailuroedus) that build no bower, the maypole-builders (including the toothbill bower-
bird, Scenopoeetes dentirostris), and the avenue-builders. Recent results (Kusmierski, per-
sonal communication, 1995) indicate that Archibold’s bowerbird (Archboldia papauensis)
is a member of the clade that builds maypoles. Like Scenopoeetes in the same clade, the
most probable pattern of evolution is that Archibold’s bowerbird has lost its tendencies
to build bowers and these losses are independent. Numbers at nodes represents the
percentage of times a group occurred in 1,000 bootstrap replicates.

and Archibold’s (Archboldia papuensis), clear display courts but do not build a
characteristic bower.
A phylogeny based on sequences of mitochondrial DNA from the cyto-
chrome-b gene, developed in cooperation with Kusmierski and Crozier
(Kusmierski et al., 1993), indicates that there was an initial separation of lineages
that led to the monogamous catbirds and the remaining polygynous species.
Later, a separation in the clade that led to bower-builders produced a lineage
that led to the avenue-builders, and another that produced the maypole-build-
ers (Archboldia and Prionodura) and the two polygynous species that do not
build bowers (S. dentirostris and A. papuensis) (Figure 18-1). Because building
bowers is the dominant pattern in both lineages and it occurs in no other avian
family, it most likely evolved once, preceding the split of the ancestors of the
avenue- and maypole-builders.

HYPOTHESES FOR THE EVOLUTION OF BOWERS

Many of the models of the evolution of extreme displays can be used to
develop specific models for the origin and evolution of bowers. For example,
the placement of sticks in an incipient bower could have been the result of an

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268 / BIODIVERSITY II

arbitrary female preference (as part of a runaway or latent preference model).

Such a hypothesis, however, posits no particular functional role for bowers apart
from mate attraction and fails, by itself, to account for the variation in form of
bowers. Evidence of a function for bowers, especially if it is consistent among
different types of bowers, would weigh against this hypothesis.
Another possibility is that bowers could have functioned to provide protec-
tion from various threats (Borgia et al., 1985). Sources of threat include preda-
tors that might attack males and females, marauding males that force copula-
tions on females while they view the court owner’s courtship, and court owner
himself forcing copulations on females not ready to mate.
The hypotheses of predation and marauding-males are not well supported.
There is no evidence of predation on females or males while males are displaying
on courts in more than 100,000 hours that cameras monitored the display courts
of males. This is especially relevant because, in most species, males are not
protected from predators by the bower during courtship. In addition, females
are not protected in some types of bowers, including the open bowers of
MacGregor’s bowerbird (Amblyornis macgregoriae, which may be similar to an-
cestral bowers) and those of the streaked bowerbird (where the male occupies
the covered part of the bower during courtship, opposite to what is predicted
by the female protection hypothesis; Sejkora and Borgia, in preparation). Last,
females change their behavior from being very reluctant to stand outside the
bower before copulation to being quite willing to stand there afterward. The
observations that many types of bowers do not confer protection, that the sexes
stand in the wrong place, and that the female’s behavior changes after copula-
tion also fail to support the hypothesis that bowers provide protection from
marauding males.
The remaining hypothesis, protection from the courting male, is not limited
by these difficulties. Species from the two clades that build bowers show gen-
erally similar patterns of how they use bowers during courtships that lead to
copulations. In both lineages, males display facing the female. The bower en-
hances the female’s ability to escape unwanted matings by blocking the male’s
direct path to her and forcing him to run around the wall of the bower or may-
pole to mate. The increased distance that males must travel to reach a female
enhances her ability to escape unwanted matings.
Several issues emerge in attempts to evaluate this hypothesis. First, why
should males build a structure that decreases their prospects of forced copula-
tion? If males are programmed to maximize their reproduction and forced copu-
lations can contribute to their reproductive success, it at first seems counter-
intuitive for males to build a structure that limits this type of reproductive
benefit. A plausible solution is that building bowers may offer a compensating
benefit that outweighs losses from forced copulation. If the reduced threat of
forced copulation causes more females to be attracted to courts with bowers
than those without, then gains from increased visitation by females could more

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COMPARATIVE STUDIES OF BOWERBIRDS / 269

than compensate for the lost ability to force copulations with females. Female
attraction might arise for several reasons, as discussed above.
Second, how do we test the hypothesis that females prefer males with bow-
ers that function to protect them from forced copulation? It is rather tricky to
infer the function of a trait at its evolutionary origin, given no fossils or other
record of the ancestral form of the bower. Information from observations of the
different species of bowerbirds and knowledge of their evolutionary relation-
ships can be used to establish likely hypotheses. The criteria that would strongly
support a hypothesis for an incipient function of bowers are: (1) the proposed
function should be consistent with the design of the likely ancestral bower, (2)
this function should be significant across all types of bowers, and (3) species
that do not build bowers should show alternative solutions to the problem solved
by the bower. There is no guarantee that even the correct answer will meet all
three criteria. It is possible, for example, that bowers could have taken on a
variety of secondary functions that have replaced the incipient function of the
bower.
In the following section, I present descriptions of courtship for four species,
two with bowers and two without. Examples from two different types of bow-
ers, avenue and maypole, illustrate how these bowers are used in courtship.
The species described here characterize a modal type in their clades. For each,
there are related species that show widely divergent behaviors but which are
consistent with the use of the bower for protection.

Display in the Satin Bowerbird: An Avenue-Builder

Satin bowerbirds (Ptilonorhynchus violaceus) are representative of species
that build avenues. They occur in rain forests that fringe eastern Australia.
The bowers of satin bowerbirds have two walls of sticks separated by a central
avenue where females stand and then crouch when they are courted. The bower
is aligned in a north-south direction with a decorated display court on the north
end. The male displays while facing the female from the display court with a
decoration held in his beak.
The females visiting the bower and the court typically alight in the vegeta-
tion on the south side of the bower and then move directly into the avenue of
the bower. Initial vocalizations consist of numerous guttural chortles and
squeaks that progress into a typical call sequence that consists of an initial me-
chanical buzzing followed by mimicry of a kookaburra (Declio gigas), a Lewin’s
honeyeater (Meliphaga lewinii), and less frequently, a crow (Corvus) (Loffredo
and Borgia, 1986). The buzzes in the mechanical calls occur in conjunction with
rapid movements by the male across the north entrance of the bower accompa-
nied by flicks of one or both of his wings.
Females signal their willingness to copulate by lowering from an upright
stance to a crouch. To copulate, the male circles to the opposite side of the

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270 / BIODIVERSITY II

bower to mount the female. After a brief (3-second) copulation, the female
shakes intermittently in or near the bower for up to several minutes and then
leaves. Females usually visit the bowers of several males, but mates with only
one. The average courtship lasts slightly more than 4 minutes.
In satin bowerbirds and other avenue-builders, most courtships end with
the female leaving from the north entrance of the bower as the male moves from
the court toward the south entrance in his attempt to copulate. Only 9% of satin
bowerbird’s courtships are successful, although the most attractive males mate
in 25% of their courtships. There is a significant relationship between the num-
ber of decorations and the mating success of males, indicating that it is impor-
tant for females to enter the bower and see the display in order to assess the
males.

Display in Macgregor’s Bowerbird: A Maypole-Builder

Macgregor’s bowerbird (A. macgregoriae) occurs at high elevations in the
mountain ranges across central and eastern New Guinea. Its bower is a simple
maypole, a sapling decorated with sticks and moss. Commonly, the sapling is
rather thin and sticks are placed nearly horizontally, increasing the diameter
around the sapling to approximately 25 cm. The low part of the maypole and
the floor of the round court surrounding it are covered with a fine compressed
moss mat that rises to form a circular rim approximately 40 cm from the may-

Bower of MacGregor’s bowerbird.

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COMPARATIVE STUDIES OF BOWERBIRDS / 271

pole. Many small decorations are used on the court, including insect parts and
seed pods. Regurgitated fruit pulp is hung near the ends of the sticks of the
maypole bower. Numerous large woody black fungi are arrayed on the rim of
the court and on nearby logs.
Females arriving for courtship often land on the maypole, move down it,
and then hop onto the court. The male usually is already present on the court
and may have been calling prior to the female’s arrival. The male positions
himself on the opposite side of the maypole from the female with his chest
pressed up against it and with his head plume concealed. He calls and, as the
female moves around the maypole, he makes a counter move so as to keep the
bower between him and her. Calling and counter moves continue for approxi-
mately 4 minutes before the male increases the intensity of display by expand-
ing his bright orange head plume and violently shaking his head from side to
side. The side-to-side shaking is associated with a rapid foot movement that
appears to counterbalance the rapid movement of his head. Seen from the
female’s side of the bower, this display creates rapid orange flashes on each side
of the maypole. After several bouts of head-shaking, the male moves around the
bower toward the female in an attempt to copulate with her.
Although the shape of avenue and maypole bowers is fundamentally differ-
ent, there is a striking similarity between maypole bowers and those of avenue-
builders in the way in which the bower is used to separate the male and female.
In each case, the male develops a prolonged courtship display. He watches the
female and, when she signals her readiness to mate by crouching, he moves
around the bower to mount her. If the female is not prepared to copulate, the
bower serves as a dodge that allows her to leave from the opposite side from
where the male is approaching.

Display in Toothbill Bowerbirds: No Bower with Leks

Toothbill bowerbird courtship is very different from that of other species of
bowerbirds. Males clear courts but do not build bowers. Male courts are close
together and aggregated into a lek (a group of displaying males not associated
with resources needed by females). Males interact with frequent loud calls,
with dominant males interrupting the calls of males on adjacent courts. Unlike
other bowerbirds, they use large objects (e.g., leaves) as decorations on their
courts. Courts surround several trees of small diameter, the bases of which have
been cleaned meticulously of debris.
Females arrive on the court and stand very still, as if waiting for the male.
Toothbill courtship is very brief. The male aggressively mounts the female with
little or no display after she arrives on the court. The average time of courtship
is 3.8 seconds. However, copulations are prolonged and violent relative to the
brief and more cooperative behavior seen in other species. During these copu-
latory bouts, the male continues to display with characteristic low buzzing calls

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272 / BIODIVERSITY II

and wing beats. Females leave the court immediately after mating without the
prolonged flapping of wings that is characteristic of other species.
By far, toothbill males spend less time on their court than any other species,
and it appears that the adjustments in their display and mating behavior reflect
an especially high susceptibility to predation while they are on the ground. The
aggressive nature of the courtship suggests that females might not be fully pre-
pared to copulate when they arrive, but the need to reduce time on the ground
has caused males to attempt to speed this process.
The loud vocal interactions of males on courts and the use of large decora-
tions suggest that females can evaluate male qualities such as dominance before
they arrive on the court. At lek centers, males that preliminary studies show are
dominant in vocal interactions have the highest mating success. This correla-
tion suggests that females are choosing mates. Observations by Cliff and Dawn
Frith (1993) and our group show that males hiding behind a tree on their court
sometimes call to females on nearby perches. However, we have not seen this
calling lead to copulation.
In toothbills, if male calling interactions and large leaves allow females to
choose mates before they arrive on the courts, then bowers may not be neces-
sary. The female already may have selected the male before arriving at his
court, so the prospect of forced copulation is not threatening. The capture of
females by males indicates that forced copulations are possible in bowerbirds.
The hiding of males behind trees during calling displays suggests a situation
analogous to the initial condition of bower evolution in which females seek some
protection from the courting male.

Archibold’s Bowerbird: No Bower and No Lek

Archibold’s bowerbird (Archboldia papuensis) is the other polygynous spe-
cies that does not build a bower. Male Archibold’s clear a large display court
overlain with a mat of ferns where males place a variety of decorations, includ-
ing snail shells, dark fruit, beetle wings, and King of Saxon Bird-of-Paradise
(Pteridophora alberti) head plumes. Typically, small decorations are in piles near
the fringes of the display court and are arrayed on the limbs overhanging the
court. Male Archibold’s bowerbirds neatly drape limbs that cross up to 1.5 m
above the display court with a uniform curtain of flowerless orchid vines that
nearly touch the display court and subdivide it. The cumulative array of the
curtains provides a rather dramatic visual effect.
Male Archibold’s bowerbirds are large and uniformly black, with a bright
yellow head crest that extends from between the eyes, over the top of the head,
to the neck. The crest covers more area on the bird’s head than the crests in
species of Amblyornis, but the individual plumes are much shorter.
Courtship in Archibold’s bowerbird also is unique. Males chase females
around the court. Occasionally the female pauses, and the male stops near her

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COMPARATIVE STUDIES OF BOWERBIRDS / 273

and attempts to approach her with his body pressed close to the court. If the
male is successful in approaching her, he faces toward the female with his head
near the ground. He emits a chattering call and rapidly moves his head with
slight side-to-side movements. If the female does not move after the initial fron-
tal display, he slowly moves behind her while maintaining a position near the
ground and then rises up to copulate. Copulation is brief and lasts only 3 sec-
onds, as is typical for all bowerbirds except toothbills.
In Archibold’s bowerbird, courtship is not constrained to a particular site,
as it is in species with bowers. The preliminary phase of courtship involves
chases about the court, and the large size of the court may accommodate these
chases. The walls may function in constraining the direction females can move.
Male Archibold’s bowerbirds have evolved an alternative solution to the
problem of copulating with females in the absence of a bower. Unlike toothbills,
they do not interact over long distances or have leks, and they do not attempt to
grab and copulate females by force. Like most other bowerbirds, they have pro-
longed courtship and frequent female rejections, suggesting that choice occurs
on the display court. The low position of males during courtship does not com-
promise the female’s ability to escape the courting male, even when he is nearby.
One explanation for the loss of bower-building in Archibold’s bowerbird
may be related to the widely ranging displays that females use to test males. In
most species of bowerbirds, males can be directly compared because they com-
pete by stealing their competitor’s decorations and destroying their bowers.
Visiting females may assess male competitive ability by the quality of his dis-
play (Borgia, 1985; Borgia et al., 1985). In Archboldia, the bowers are spread
very far apart, and the possibility of male interaction is low. The frequent
chases may be a means by which females test male athleticism. Elsewhere I have
suggested that intense displays which span large areas in male spotted bower-
birds function similarly for female assessment (Borgia and Mueller, 1992; Borgia,
1995). In Archboldia, where the bowers of males are spread apart in small forest
islands, there may be a similar need for males to demonstrate fitness in athletic
rather than interactive components of display. Comparisons among all of the
species of bowerbirds that I have studied indicate that the two species with
interbower distances of >700 m (Archboldia and Chlomydera maculata) have es-
pecially large display courts and male displays that range over these courts,
whereas the displays of the remaining nine species with bowers that are closer
together have relatively small courts and male display is restricted to these courts
( 2=3.14, df=10, p=0.02).

A MODEL FOR THE EVOLUTION OF BOWERS

The hypothesis that protection from the courting male is important in the
evolution of bowers is supported by the patterns of evolution in bowers and its
consistency with the diversity of types of bowers. The ancestor to the lineage

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274 / BIODIVERSITY II

that led to modern species that build bowers probably displayed on a decorated
ground court. Females favored courts with a natural barrier, such as a sapling,
that separated them from males during courtship because it allowed them to
approach the male and closely observe his display and decorations while still
retaining the ability to leave if not stimulated by the display. Males who en-
hanced this barrier, e.g., placed sticks around the sapling and enlarged its diam-
eter, offered females a safer vantage point for observing display. Males could
gain from this elaboration by exploiting the female preference for mating in a
protected environment. Increased female visitation and lessened threat during
courtship contributed to an overall increase in matings over what might be
achieved by forced copulations. Gains for females from the avoidance of forced
copulations might include eschewal of genetically inferior males and reduction
of direct physical costs (e.g., parasite transmission and time lost in remating).
Remating of females which have been forced to copulate with other males would
lower the value of forced copulations to court owners and may have caused
males to shift efforts toward attraction of females.
The simple bower described above is similar to the bower built by
MacGregor’s bowerbird. Once the tendency to use sticks to build a bower
evolved, however, it was possible to build a bower that functioned in female
protection but did not require a central sapling. The loss of dependence on the
use of saplings could have allowed males more freedom in selecting sites for
bowers, in orienting their decorations, and in displaying their decorations. The
ancestors of avenue-builders probably added a second barrier because it ori-
ented females toward illuminated parts of the court where males could concen-
trate their decorations on a well-lit stage. The orientation of bowers in a north-
south direction, the consistent placement of most decorations on the north side,
and the clearing of leaves over display courts support this hypothesis.
This hypothesis is consistent with all types of bower-construction and our
observations of how bowers are used in courtship. In both avenue and maypole
bowers, males are forced to run around a barrier in order to reach the rear of the
female where they can copulate. The delay caused by this extra traveling time
gives females an opportunity to escape males that are unattractive to them. The
behavior of the two species that do not build bowers also is consistent with the
protection hypothesis. In toothbills, there is no bower, but because females
appear to move to the ground for copulation only after they make their mating
decision, they leave the court without mating proportionately less often than
females in other species (Borgia, in preparation). In Archibold’s bowerbird, by
lying close to the ground as they approach females, males are not threatening as
forced copulators.

CONCLUSIONS
We rarely can be sure about the evolutionary origins of a trait, but we can
use information from comparisons among extant species to formulate reasonable

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COMPARATIVE STUDIES OF BOWERBIRDS / 275

hypotheses. In the case of the hypothesis that bowers provide protection from
courting males, the great diversity of behaviors among species of bowerbirds
with very consistent elements within species gives surprisingly strong support
for this hypothesis of the origins of bower-building. This work has the added
benefit of suggesting an important role for models of proximate benefit in ex-
plaining elaborated male traits. This work could not have been accomplished
had the number of species of bowerbirds available to study been limited by
extinctions. This places an immediate imperative on carrying out detailed com-
parative studies of behavior before there are large reductions in numbers of
species. It also suggests that attempts to preserve representative species may
not be productive because there are no typical species.

ACKNOWLEDGMENTS
This research was supported by funds from the National Science Founda-
tion (BNS 85-10483 and BSR 89-11411), from the Graduate Dean and Dean of Life
Sciences, University of Maryland, and from the University of Maryland Com-
puter Science Center. The New South Wales and Queensland National Parks,
the Australian Bird and Bat banding scheme, and the Papua New Guinea Wild-
life and Conservation Department provided permits. R. Crozier, J. Dimuda, G.
Harrington, I. Hayes, J. Hayes, N. Hayes, J. Lauridsen, M. J. Littlejohn, J.
Kikkawa, N. Raga, J. Hook, and M. and J. Turnbull provided various important
forms of support. C. Depkin, D. Bond, A. Day, and J. Morales served as team
leaders. More than 100 volunteer assistants provided excellent help in field.
This paper is dedicated to the memory of Iris, Jack, and Ned Hayes, who were
great friends and critics.

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Andersson, M. 1986. Evolution of condition-dependent ornaments and mating preferences: Sexual
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Andersson, S. 1989. Sexual selection and cues for female choice in leks of Jackson’s widowbird
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Borgia, G. 1979. Sexual selection and the evolution of mating systems. In M. Blum and A. Blum,
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Borgia, G., and U. Mueller. 1992. Bower destruction, decoration stealing, and female choice in the
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Borgia, G., S. Pruett-Jones, and M. Pruett-Jones. 1985. Bowers as markers of male quality. Zeit. für
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Brooks, D. R., and D. A. McLennan. 1991. Phylogeny, Ecology, and Behavior: A Research Program
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Burley, N. 1985. The organization of behavior and the evolution of sexually selected traits. Pp 22-
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Gibson, R., J. Bradbury, and S. Vehrencamp 1991. Mate choice in lekking sage grouse revisited: The
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Kirkpatrick, M. 1987. Sexual selection by female choice in polygynous animals. Ann. Rev. Ecol.
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Sexual Selection and the Descent of Man. Aldine Press, Chicago.
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Zahavi, A. l975. Mate selection—a selection for a handicap. J. Theor. Biol. 53:205-214.
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Zool. 30:235-244.

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CHAPTER
19

Microbial Biodiversity
and Biotechnology

RITA R. COLWELL
President, University of Maryland Biotechnology Institute,
College Park, Maryland

Biodiversity and biotechnology are strongly interrelated and interdepen-

dent. With respect to microbial diversity, microorganisms have been used in a
variety of ways in the food industry. A good example is the dairy industry, in
which microorganisms have been used to produce butter, yogurt, and cheese.
Genetic modification of key microorganisms used in the manufacture of these
foods has been accomplished to improve flavor, texture, and taste of the final
product. Thus, the enormous diversity of the Earth provides the foundation for
biotechnology, not only in food production, but also in agriculture to improve
soil fertility, in the pharmaceutical industry as a source of antimicrobial and
antitumor agents, and in production of compounds of value in the chemical
industry, e.g., dextran, a bacterial polymer.
Despite the popular press’ view of biotechnology, it is not a field that was
discovered only recently. In fact, it enjoys a long history of contribution to the
well-being of humans, since leavening of bread and the fermentation of grapes
to make wine were activities practiced in China and Egypt centuries ago. How-
ever, following on the steps of the Industrial Revolution, development of large-
scale fermentation processes, coupled with major discoveries in genetics provid-
ing an understanding of genes and chromosomes and the molecular basis of
heredity, the explosive developments in modern biotechnology were made pos-
sible during the past 20 years.
The new “era” of biotechnology includes a myriad of innovations based on
recombinant DNA. In addition to recombinant DNA, the tools of molecular
biology include protoplast fusion and production of hybridomas to provide
monoclonal antibodies. The value of these tools is that they make possible the

279

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280 / BIODIVERSITY II

production of biological hybrids otherwise not possible by classical mating and

selection. Gene cloning also provides the capacity to introduce genes into or-
ganisms to provide a new function for that organism. An example of this is the
luminescent tobacco plant, which results when the lux gene (a gene or genes
responsible for production of enzymes involved in bioluminescence) has been
cloned from a bioluminescent organism, usually a microorganism, and inserted
into the genetic structure of the host plant. The lux gene is inserted next to a
gene whose function is to be studied so that both genes are activated at once and
the plant glows whenever the adjacent gene produces its product. This has
allowed major advances in our knowledge of the structure and function of genes.
Furthermore, biotechnological products such as the “pomato,” a result of proto-
plast fusion of the tomato and potato, have advanced our basic knowledge of
manipulating the properties of organisms for human benefit, including plants of
agricultural importance. Beside these novel results, which have contributed to
our basic knowledge of how organisms function, the more apparent benefits of
biotechnology, such as the production of human insulin through genetic manipu-
lation of easily cultured microorganisms, sometimes have been overshadowed.
Faced with burgeoning human populations, many government leaders ex-
pect the biotechnology “revolution” to provide a solution for the ever-increas-
ing global demand for food and to resolve human medical and epidemiological
issues. Unfortunately, there is a significant distance between this hope and
actual fulfillment. Nevertheless, without the contributions of biotechnology to
agriculture and medicine, it is unlikely that these problems will be overcome.
This paper provides a brief description of the biotechnology industry, simi-
larly reviews the biodiversity of microorganisms, examines the significance of
this biodiversity for a sustainable biosphere, and evaluates the significance of
microbial biodiversity for the further development and application of biotech-
nology for human needs.

GROWTH OF THE BIOTECHNOLOGY INDUSTRY

Major sectors of the biotechnology industry currently include agriculture,
food processing, industrial chemicals, and pollution control. When environ-
mental biotechnology, which includes pollution control and bioremediation (the
restoration of a damaged or disturbed ecosystem to a functional ecological state
through the activities of living organisms), begins to fulfill its promise, the bio-
technology industry will increase both its markets and its economic diversity
significantly.
Biotechnology companies in the United States now number well over 1,300.
Projections for the growth of the biotechnology industry made in the early 1980s
were that, by 1990, the industry would be valued at approximately $5-7 billion.
In fact, the Annual Report on the Biotechnology Industry (Burrill and Lee, 1993)
noted that, in the United States alone, biotechnology sales were $10-12 billion in

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MICROBIAL BIODIVERSITY AND BIOTECHNOLOGY / 281

1993. Sales of the U.S. biotechnology industry are projected to be about $100
billion by the year 2035.
Funding for marine biotechnology has increased in the United States from a
negligible amount of less than $1 million in 1983 to approximately $100 million
1994 (Zilinskas et al., 1994). In Japan, investment in marine biotechnology is
estimated to be in the range of $1 billion during the past decade.
Strong interactions between universities and the industry have developed
in recent years. Components of technology transfer between universities and
the biotechnology industry include intellectual property sharing, technology
marketing, formation of start-up companies, and establishment of incubator fa-
cilities. Basic research undertaken in universities provides the knowledge nec-
essary for understanding the diversity of organisms (especially microorganisms)
and is the basis for the biotechnology industry, providing critical understand-
ing of genetic and cellular mechanisms and thereby allowing application of bio-
technological principles to the improvement of the human condition. The well
educated and highly trained work force supplied by universities provides the
technical staff, enables technology transfer, and ensures success of the industry.

BIODIVERSITY OF MICROORGANISMS
The driving forces of microbial (bacterial, viral, viroid, filamentous fungal,
yeast, microalgal, and protozoan) diversity include the genetic constitution of
these organisms, the environment in which they are found, and ecological inter-
actions with other components of the biosphere. The result is an extraordinary
richness of microbial diversity, most of which remains to be explored.
Microorganisms inhabit virtually every ecological “nook and cranny” in
the biosphere. Because of their very small size, direct observations of species
diversity of microorganisms in natural environments rarely can be made unless
an unusual abundance of a single species occurs, producing a characteristic tex-
ture of growth (e.g., that found in geothermal springs). New biotechnological
methods, however, are beginning to reveal a vast, previously unrecognized
realm of microbial life that has tremendous ecological and medical importance.
Of the above microorganisms, this paper emphasizes the spectacular functional
diversity of bacteria and viruses as they relate to biotechnological developments.
Bacteria exhibit significant diversity in size and morphology. Most plank-
tonic bacteria in lakes and oceans that have been cultured successfully are coc-
coid or spherical cells, approximately 0.2 to 0.6 µ in diameter, or short, rod-
shaped cells about 1 to 3 µ in length and 0.2 to 0.6 µ in diameter. Many species
of bacteria demonstrate unusual shapes and forms (e.g., helical, coiled, triangu-
late, etc.). Other bacteria show unusual biochemical and biomechanical proper-
ties, such as the magnetotactic bacteria, which possess intracellular magnetic
particles allowing the cells to orient to the Earth’s magnetic poles. Although
many bacterial species can be grown easily in culture, the vast majority either

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are not easily cultured or are unculturable by present methods. Consequently,

we have little idea of the true morphological and functional diversity of all mi-
croorganisms extant on the Earth.
Viruses are intracellular parasites containing only one type of nucleic acid,
either RNA or DNA, and usually a protein coat. Following invasion of the host
cell, most viruses incorporate themselves directly into the DNA or RNA of the
host cell’s genetic machinery. They then rely on their host cell to provide part
or all of the materials for replication and expression of the viral genetic informa-
tion. Unlike host cell genetic elements, however, some viruses also can exist func-
tionally as extracellular particles (e.g., as seen in the viruses that attack bacteria).
Although these viruses are capable of surviving for long periods of time in the
external environment, their ecology and reproduction is linked intimately with
their host. They may serve as a vector in the transfer of genetic information
from one host to another. Viruses are especially valuable in human medicine,
i.e., gene therapy, in serving as the “carrier” of a fully functional gene that can
correct an inborn error of metabolism by gene substitution or replacement.
Viruses are far more common and ecologically important than previously
thought. For example, in water samples collected from the Chesapeake Bay,
viruses (observed with the electron microscope) are more abundant than bacte-
ria in late summer and early autumn (Wommack et al., 1992). Recent studies
also indicate that there are more viruses than bacteria in the open ocean. Many
of these viruses attack bacteria, and may represent a significant control agent
for the ubiquitous bacterial flora in the environment, and they may control algal
abundance as well. We are only beginning to comprehend the ecological sig-
nificance and diversity of these submicroscopic organisms in the environment.
Another aspect of microbial diversity, not readily recognized, is the rela-
tively limited number of species that have been described and the even greater
number of estimated species not yet known. Only 3,000-4,000 species of bacte-
ria have been described (Hawksworth and Colwell, 1992). It has been estimated
that there may be as many as 300,000 species of bacteria, but more likely the
number is closer to 3,000,000. The number of species of viruses has been esti-
mated to be approximately 5,000, but only about 500 have been described.
About 17% of known species of fungi have been cultured, but less than 1%
of known fungal species are available in the world’s culture collections; described
species represent only 1-3% of the total estimated species of fungi (Hawkins and
Colwell, 1992). Thus, the bulk of undescribed species are microorganisms (bac-
teria, viruses, viroids, filamentous fungi, yeasts, microalgae, and protozoans).

THE ECOLOGICAL IMPORTANCE OF MICROBIAL BIODIVERSITY

Microorganismal diversity provides essential ecological services for the bio-
sphere by regulating the composition of the atmosphere, controlling the struc-
ture and fertility of the soil, and regulating agricultural pests.

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MICROBIAL BIODIVERSITY AND BIOTECHNOLOGY / 283

Microbial activities comprise vital links in the chain of geochemical events

that occur when nutrient elements are cycled. For example, in the carbon cycle,
methanogenic microorganisms can influence the climate by producing methane
gas, which is a major greenhouse gas. Although not uniquely produced by
microorganisms, carbon dioxide, also a greenhouse gas, is produced by respira-
tion and heterotrophic decomposition by many bacteria and fungi. Plankton
and some species of bluegreen bacteria produce dimethyl sulphide, a compound
that promotes cloud formation and rainfall. The evidence suggests that microor-
ganisms may affect climate through cloud formation. In marine ecosystems,
some algae and cyanobacteria produce dimethyl sulphide (DMS) in large quan-
tities. DMS is volatile and is readily oxidized in the atmosphere to form first
dimethyl sulfoxide and then sulfate which acts as a nucleating agent in water
droplet formation. Thus, the more DMS that is produced, the more water drop-
lets formed, the more clouds produced, and the greater the rainfall.
In addition to the effects of carbon dioxide and methane in the atmosphere,
nitrifying and denitrifying microorganisms produce nitrous oxide which photo-
chemically reacts with ozone, contributing to events that admit increasing con-
centrations of ultraviolet radiation to the Earth’s atmosphere.
Photosynthetic organisms fix carbon dioxide and release oxygen to the at-
mosphere. Microbial respiration replenishes atmospheric carbon dioxide and
reduces significant amounts of atmospheric oxygen to water and other com-
pounds. Some bacterial species oxidize elemental nitrogen, which ultimately is
returned to the atmosphere by bacteria that reduce the nitrogen in nitrate com-
pounds to the elemental state. The bacteria in soil oxidize methane to carbon
dioxide and produce volatile compounds of sulfur, phosphate, and nitrate that
enter the atmosphere.
Microbial diversity is intimately related to soil structure and function. Bac-
teria generally occur at concentrations of ≥109 cells/gram of soil. Soil governs
the productivity of plants and, therefore, the sustainability of agriculture, for-
estry, and natural ecosystems. Some of the best soil is formed in grassland pas-
tures, where bacteria are associated with root material and are attached to clay
particles (Lynch and Poole, 1979). In most cases, these bacteria are responsible
for transforming and cycling carbon, nitrogen, phosphorus, iron, and sulfur in
the soil and for the manner in which aggregates and clumps of soil are formed.
In well-drained soil sustained by a healthy bacterial flora, much of the space
between soil aggregates is filled with air. Since oxygen is necessary for metabo-
lism in plant roots, this aerated structure of the soil is necessary for soil produc-
tivity. Unfortunately, if certain microbial species become dominant in the soil,
the system can become anaerobic (lacking in oxygen). Also, some bacteria ex-
crete gums and cements (Margulis et al., 1989) that can block pores in the soil.
Both of these effects can decrease soil fertility. It is essential to understand how
the biodiversity of microbes in soil maintains agricultural productivity.
Another example of the diverse ecological activities of bacteria is their abil-

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284 / BIODIVERSITY II

ity to control insects. Many insects carry a microbial flora on their surface and
in their gut. Populations of microorganisms pathogenic for the insect may de-
velop if the insect is injured. Bacteria also produce chemical compounds that
adversely affect insect growth. Thus, manipulation of microbial populations
provides a mechanism by which agricultural pests can be controlled.
In summary, microbial biodiversity represents the foundation of a sustain-
able biosphere and is fundamental to sustainable agriculture. The activities of
microorganisms, in the aggregate, and the diversity of species, most of which
still remains undescribed, provide a rich source of genetic variation for applica-
tion to biotechnology.

THE SIGNIFICANCE OF MICROBIAL

BIODIVERSITY FOR BIOTECHNOLOGY
Recently, the bacterium Agrobacterium tumefaciens has been used to geneti-
cally engineer plants. Agrobacterium tumefaciens carries a plasmid that nor-
mally causes plant disease. However, by inserting specific genes into the bacte-
rial plasmid, desirable characteristics can be transferred to the plant genome
where the plasmid DNA is integrated. Thus, herbicide resistance, pesticide ac-
tivity, and designer fruits and vegetables can be produced.
In the marine sphere, many of the unique compounds of potential medical
value that are retrieved from the tissues of a range of marine invertebrate and
vertebrate organisms are produced by marine bacteria. An example of a com-
pound produced by marine microorganisms is tetrodotoxin, a toxin found in the
fatty tissues and reproductive organs of the puffer fish, and originally thought
to be produced by the fish itself. Tetrodotoxin is a very powerful analgesic
(about 300,000 times more powerful than cocaine) that resembles procaine in its
ability to inhibit transmission of nerve cells. Tetrodotoxin has been used in
Japan to treat pain in neurogenic leprosy and cancer. Thus, tetrodotoxin is a
compound produced by bacteria found on the puffer fish and, more recently,
bacteria associated with benthic invertebrates, as well. Tetrodotoxin is one ex-
ample of a compound that may have wide pharmaceutical value in the future.
Diversity “hot spots,” such as the Great Barrier Reef off the coast of Austra-
lia, provide a wide array of known and unknown microorganisms. The diver-
sity of corals and other marine invertebrates on these reefs have long been ap-
preciated, but their bacterial symbionts have been described only recently.
Tunicates (Didemnidaceae), i.e., sea squirts, produce compounds (didem-
nins) that have antileukemic properties. Collections of sponges (Sclerospongia)
from Caribbean coral reefs also have yielded bacterial species that produce un-
usual antimicrobial compounds. Cross sections of the sclerosponge revealed that
50% of the sponge mass is comprised of procaryotic structures concluded to be
bacteria. Most of these bacterial species have not yet been cultured (Santavy
and Colwell, 1990). Of those cultured, several have been found to produce com-

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MICROBIAL BIODIVERSITY AND BIOTECHNOLOGY / 285

pounds of potential pharmacological value. In general, marine sponges are

widely known for production of chemicals that deter predators or even cause ill
effects in divers exposed to them; many of these compounds may be produced
by the diverse bacteria living within the tissues of the sponge.
In another application of microbial diversity to biotechnology, an enzyme
active at high temperatures was prepared relatively recently from Thermus
aquaticus, a microorganism which had been isolated from the hot springs of
Yellowstone National Park many years ago. Using this enzyme, the polymerase
chain reaction (PCR) was developed, an enormously powerful molecular genetic
tool that cuts and splices DNA and allows detailed examination of gene se-
quences. Application of PCR in criminology is already well known.
An important aspect of microbial diversity in biotechnology is utilization of
microorganisms as “janitors” of the planet, i.e., in bioremediation. Microorgan-
isms are useful in restoring habitats to a functional ecological state because they
are capable of degrading pollutant compounds, purifying water and soil in the
process. Genetically engineering microorganisms to degrade toxic compounds
more rapidly and completely offers great promise for bioremediation and bio-
restoration in the future.

RELATION OF LOSS OF MACROORGANISMAL BIODIVERSITY

TO MICROBIAL ECOLOGY AND DIVERSITY
While loss of diversity obviously results in lost products and lost markets,
an insidious and often unrecognized result of disturbed environments and
biodiversity loss is the effect on human health. Deforestation, for example, not
only creates problems of environmental degradation, but enhances the potential
for epidemics of new and unpredictable diseases that may be devastating for
human populations. An example is an epidemic that occurs when native or
introduced macroorganisms reach high densities in the course of extreme popu-
lation fluctuations associated with the disturbed environmental conditions, such
as destruction of native vegetation for logging or farming, weather changes re-
lated to the El Nino Southern Climatic Oscillation, or anthropogenic effects on
atmospheric warming and precipitation. For example, deforested areas may al-
low massive increases in mosquito populations, leading to malaria outbreaks in
humans. Another example is that of rodents, which harbor microorganisms that
are pathogenic for humans but occur in sufficiently low frequency, when ro-
dent populations are low, that the risk of human disease also is relatively low.
When rodent population densities reach unusually high levels, however, seri-
ous outbreaks of disease caused by viruses that are carried by rodents may oc-
cur in humans. In other instances, a microorganism normally found in rodents
may shift hosts, once rodent populations reach critical densities, and cause a
pathogenic epidemic among humans in the area. The recent Hanta virus out-
break in the southwestern United States is but one example of such phenomena

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286 / BIODIVERSITY II

(Epstein et al., 1993; Epstein, 1995). The Hanta virus is carried by a deer mouse,
but can be transmitted to humans in certain circumstances. A proliferation of
deer mice associated with a change in weather patterns resulted in outbreaks of
the virus in humans who inhaled dust contaminated with dried mouse urine;
these outbreaks resulted in a number of deaths.
Thus, the biodiversity of microbial populations, the biology of which is not
understood, may impact human populations adversely as global populations
continue to increase and environmental disturbances become more common.
Research is needed to document and understand not only the biodiversity and
population dynamics of macroorganisms in disturbed conditions, but also the
biology and diversity of associated microorganisms, to avert such epidemics.
Cholera offers a useful example of disease outbreaks whose biology and
relationship to natural environments needs to be understood in order to mini-
mize adverse effects on human populations. Beginning in 1991, cholera out-
breaks began devastating Latin America. Initially, approximately 285,000 cases
occurred in Peru, with about 108,000 hospitalizations and 3,000 deaths. The
disease subsequently moved to Ecuador and then to Columbia. Coastal areas
were the first impacted. The migration pattern of the disease can be related to
disturbances in the weather and in the pattern of upwelling in the East Pacific
Ocean caused by the El Nino Southern Oscillation Event (Epstein et al., 1993).
The epidemic strain of cholera, Vibrio cholerae 01, has been demonstrated to be
associated with zooplankton that occur in coastal waters in Asia (Colwell and
Huq, 1994), providing an explanation for the greater intensity of the disease in
coastal areas of South America. A useful biotechnological product of these stud-
ies was a highly specific detection agent, a monoclonal antibody prepared against
V. cholerae 01, allowing detection of V. cholerae 01 in environmental samples. A
diagnostic kit, now manufactured commercially, permits detection in the field
so that the organism can be tracked in the environment (Colwell et al., 1992).

CONCLUSIONS
There is much yet to be learned about microorganisms in natural ecosys-
tems. An improved understanding of microbial community structure, ecology,
and population genetics is needed, as well as more information on microbial
diversity and interactions of microorganisms at the species level. A workable
species concept for microorganisms is lacking, but nucleic acid sequencing, a
highly promising development in microbial systematics, may offer a pragmatic
approach to the definition of microbial species. However, information for cata-
loging species and developing databases is just beginning to be collected at the
level necessary for reproducible definition and description of species, i.e., for
polyphasic definition of species.
Microbial diversity already has contributed significantly to biotechnology,
but until a full understanding of microbial diversity and microbial interactions

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MICROBIAL BIODIVERSITY AND BIOTECHNOLOGY / 287

is gained, the benefits for biotechnology will not be realized completely. Micro-
bial diversity, as a significant component of overall biological diversity, plays a
major role in maintaining human health and sustaining the well-being of the
environment. In any prospective search for compounds of medical or agricul-
tural value, whether in a tropical forest of Latin America, in Maryland soil, or in
off-shore Atlantic or Pacific ocean water, the microbiological resources that re-
main to be discovered undoubtedly will enrich the lives of the human race, and
will reveal the intricate interlocking mechanisms of biodiversity that underlie
the well-being of humans and the balance of our biosphere.

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Hawksworth, D. L., and R. R. Colwell, eds. 1992. Biodiversity amongst microorganisms and its
relevance. Biodiv. Conserv. 1:221-345.
Lynch, J. M., and N. J. Poole. 1979. Microbial Ecology: A Conceptual Approach. John Wiley and
Sons, Inc., N.Y.
Margulis, L., J. O. Corliss, M. Melkonian, and D. J. Chapman, eds. 1989. Handbook of Protoctista.
Jones and Bartlett Publishers, Boston. 914 pp.
Santavy, D. L., and R. R. Colwell. 1990. Comparison of the symbiont bacterial community associ-
ated with the Caribbean sclerosponge Ceratoporella nicholsoni and ambient seawater. Mar.
Ecol. Prog. Ser. 67:73-82.
Wommack, K. E., R. T. Hill, M. Kessel, E. Russek-Cohen, and R. R. Colwell. 1992. Distribution of
viruses in the Chesapeake Bay. Appl. Envir. Microbiol. 58:2965-2970.
Zilinskas, R. A., R. R. Colwell, D. W. Lipton, and R. Hill. 1994. The Global Challenge of Marine
Biotechnology. National Sea Grant College Program Report. Maryland Sea Grant College,
College Park. 330 pp.

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CHAPTER
20

The Impact of Rapid Gene

Discovery Technology on Studies of
Evolution and Biodiversity
CAROL J. BULT, JUDITH A. BLAKE, MARK D. ADAMS, OWEN WHITE,
GRANGER SUTTON, REBECCA CLAYTON, AND ANTHONY R. KERLAVAGE
Science Research Faculty and Staff, The Institute for
Genomic Research (TIGR), Gaithersburg, Maryland

CHRIS FIELDS
Scientific Director, National Center for Genome
Resources (NCGR), Santa Fe, New Mexico

J. CRAIG VENTER
Director, The Institute for Genomic Research (TIGR), Gaithersburg, Maryland

Topics of critical concern for biodiversity include the development of stan-

dards to assess levels and distributions of diversity and the creation of a global
network of interoperable databases to manage, analyze, and distribute large
amounts of information to researchers and policymakers. The technical chal-
lenges confronted by researchers working to map and sequence the human ge-
nome (National Center for Human Genome Research, 1990) have led to new strat-
egies for rapid gene discovery and informatics (Fields, 1992; Kerlavage et al.,
1993; Venter et al., 1992) that we, the authors, are applying to large-scale mo-
lecular assessment of biodiversity. In this chapter, we describe our research
efforts in areas relevant to biodiversity assessment; specifically, we outline the
development of (1) multiple molecular markers for identification and classifica-
tion of species, (2) new algorithms for multiple sequence alignment, and (3) da-
tabases that link taxonomic, phylogenetic, geographic, and molecular data.

WHAT IS RAPID GENE DISCOVERY?

Rapid gene discovery is the process of “tagging” transcribed genes by ob-
taining partial sequences of cloned DNA copies of many randomly selected
messenger RNA (mRNA) transcripts. In the laboratory, the isolated mRNAs are
reverse transcribed into cDNA (complementary DNA) that is then cloned and

289

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290 / BIODIVERSITY II

sequenced. The partial cDNA sequences which are typically 200-400 basepairs
(bp) in length, are called Expressed Sequence Tags (ESTs; Adams et al., 1991).
Single-pass, automated sequencing of ESTs from randomly selected clones from
cDNA libraries permits the rapid identification of genes expressed in cells, tis-
sues, or whole organisms (Adams et al., 1991, 1992, 1993a,b; Khan et al., 1992;
McCombie et al., 1992; Okubo et al., 1992; Waterston et al., 1992). The genes
that ESTs “tag” are putatively identified by evaluation of the degree of similar-
ity between the nucleotide and amino acid translations of an EST sequence and
previously described DNA and protein sequences from public sequence data-
bases (e.g., GenBank, EMBL, SwissProt). Significant similarity is evaluated us-
ing computer-assisted algorithms such as BLAST (Altschul et al., 1990) and
BLAZE (Brutlag et al., 1993).
Automated single-pass DNA sequencing is more than 98.5% accurate, on
average, for up to 400 bp per sequencing reaction (Adams et al., 1993a). For
abundant ESTs, we observe an average of seven- to eight-fold redundancy,
which provides an additional measure of quality assurance for sequence accu-
racy. The EST approach to gene discovery differs from previous methods in that
it does not rely on screening for and sequencing of full-length cDNA clones. We
estimate that the EST approach reduces the costs (in time and materials) associ-
ated with gene discovery by 2-3 orders of magnitude.
In 1993, the sequencing core at The Institute for Genomic Research (TIGR)
generated up to 300,000 bp from 1,000 DNA templates per day (Adams et al.,
1994). In comparison, the submission of sequence data to GenBank from all other
DNA sequencing labs combined averaged just over 309,000 bp per day (based
on submissions to GenBank from January to July 1993). Our current maximum
sequencing throughput is 500,000 bp per day; with modifications of existing
hardware and software, throughput is expected to reach 1 million bp of se-
quence each day within the next 3 to 5 years. Since the genome size of many
microorganisms are in the range of 2-4 million bp, it is feasible that the complete
genomes of some organisms will be sequenced in a single week in the near fu-
ture.
ESTs were first used for rapid identification of genes expressed in the hu-
man brain (Adams et al., 1991, 1992, 1993a,b). Beginning in late 1992, research-
ers at TIGR extended the EST approach to include other human tissues and
organs to determine patterns of gene expression during human development. As
of April, 1994, over 200,000 ESTs have been sequenced from 300 human cDNA
libraries that were constructed from 37 distinct tissues and organs (Adams et al.,
in press). Over 40,000 unique genes are represented by these EST sequences,
including more than half of the estimated 60,000 genes in the human genome.
The results of the human EST sequencing project provide the most comprehen-
sive picture of gene expression patterns during human development to date.
When human ESTs are compared to existing public sequence databases,
approximately 33% find exact matches among sequences already published,

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THE IMPACT OF RAPID GENE DISCOVERY TECHNOLOGY / 291

2% identify (by similarlity of nucleotide sequences) potential new members of

existing gene families (genes that arise via duplication events), 7% identify (by
similarity of amino acid sequences) potential human homologs of genes from
other species, and 57% do not match any published DNA or protein sequence.
The gene identification rates are comparable to those obtained for ESTs or ge-
nomic sequences from Escherichia coli (a common enteric bacterium), Saccharo-
myces cerevisiae (baker’s yeast), and Caenorhabditis elegans (a nematode), and
from human chromosomal DNA sequencing (Adams et al., 1993a). We use the
term isolog to describe ESTs that either have a significant but nonexact match to
a nucleotide sequence within the same species or whose only significant match
is to a protein sequence from a different species. This nomenclature distin-
guishes identity based solely on similarity of sequences from explicit hypoth-
eses of common ancestry associated with the term homolog.
Although still a new approach to genome characterization, EST studies are
proving to be a rich source of data, not only for gene discovery, but also for
comparative evolutionary analyses. EST projects have proved useful for identi-
fying potential homologs, identifying new members of gene families, genome
nucleotide composition analysis (White et al., 1993), gene mapping
(Polymeropoulos et al., 1993), and the analysis of synteny (genes that are lo-
cated on the same chromosome) (Helentjaris, 1993).

MOLECULAR DATA IN SYSTEMATICS

Although the use of “informational macromolecules” (Zuckerlandl and
Pauling, 1965) for systematics has become commonplace, molecular approaches
to systematics have been criticized recently as not providing the degree of phy-
logenetic resolution that had been predicted. This assessment is premature given
the limited sampling of possible molecular markers that have been tested em-
pirically (Doyle, 1993). A brief survey of the relevant literature reveals that only
about 40 molecular markers (nuclear and organellar combined) have been used
for phylogenetic analyses to date. The small subunit of ribosomal DNA (rDNA),
the largest subunit of ribulose bisphosphate decarboxylase (rbcL), and cyto-
chrome-b are by far the most commonly employed markers in molecular system-
atic studies. Molecular phylogenetic studies to date have relied on single exem-
plars of large speciose groups and on the information content of one or two
genes, research strategies that can lead to a distorted representation of evolu-
tionary history (Lecointre et al., 1993). Overall, the potential of molecular data
for systematic studies has barely been tapped (Doyle, 1993).
The development of new molecular markers has proceeded at a relatively
slow rate because the process has depended in large part on retrospective analy-
ses of gene sequences present in public sequence databases (Friedlander et al.,
1992). The sequences currently available in these databases are biased in kinds
and numbers of genes and species represented, making it difficult to design

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292 / BIODIVERSITY II

markers that are applicable across a wide range of species or to distinguish be-
tween orthologs (genes related by speciation events) and paralogs (genes related
by gene duplication events) (Fitch, 1970). Distinguishing between orthologs
and paralogs is a critical concern for molecular systematists because the evolu-
tionary histories of species and genes do not always coincide (Fitch, 1970; Page,
1993; Sanderson and Doyle, 1992).

ESTs as a Tool for Marker Development

Two qualities of ESTs make them a valuable tool for designing molecular
markers. First, the rapid generation of large numbers of candidate markers means
that a diverse pool of sequences can be screened in a short period of time. Sec-
ond, ESTs provide sensitive probes for identifying potential gene homologs
across species. The population of cDNAs represented by EST sequences are bi-
ased only in that the transcripts present in a cDNA library will represent the
gene expression patterns of a particular cell, tissue, organ, or lifecycle. Many of
the transcripts we identify by ESTs are “housekeeping” genes essential for basic
cellular function (e.g., elongation factor-1a, actin, ribosomal proteins, etc.).
Housekeeping genes often contain regions that are highly conserved and, there-
fore, are good candidates as markers for tracking deep evolutionary divergences.
EST sequences can be used to identify potential homologs in much the same
way that DNA hybridization probes identify homologs on Southern blots. ESTs
have the advantage of being more selective as probes, because direct compari-
son of sequences reveals differences not detectable even with quantitative hy-
bridization. ESTs are also more sensitive as probes because the protein transla-
tion of an EST can be used to detect similarity at the level of amino acids even
when the match for nucleotide sequences is low. For example, we identified a
novel human very-low-density-lipoprotein (VLDL) receptor via a protein match
(87% similarity over 39 amino acid residues) of a translated EST to a rabbit
VLDL receptor (Adams et al., 1993a). Detection of the novel human VLDL
receptor by standard hybridization procedures was not possible because of the
many nucleotide differences between the probe and the genes sequences of the
novel human receptor.
Recent findings suggest that it will not always be necessary to isolate full-
length cDNAs to confirm an identification based on an EST match. Because most
of the cDNA clones in a library will be represented by many different ESTs, the
complete cDNA sequence can be determined by assembling multiple overlap-
ping ESTs. For example, the complete cDNA of a new human isolog of the yeast
sui1 translation initiation factor gene was assembled using overlapping, inde-
pendent EST sequences (Fields and Adams, 1994).
In addition to the dozen or so EST projects world-wide that focus on hu-
mans, EST sequencing currently is underway in a number of laboratories for
such diverse organisms as Arabidopsis thaliana (mouse-ear cress; Newman et al.,

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THE IMPACT OF RAPID GENE DISCOVERY TECHNOLOGY / 293

1994), Brassica napus (oilseed rape; Kwak et al., 1994), Pinus taeda L. (loblolly
pine; Kinlaw et al., 1994), Ceanorhabiditis elegans (nematode; McCombie et al.,
1992; Waterston et al., 1992), Mus musculus (domestic house mouse; Hoog, 1991),
Saccharomyces cerevisiae (baker’s yeast; Weinstock, personal communication,
1994), Oryza sativa L. (rice; Rice Genome Newsletter, 1992), Zea mays (maize;
Shen et al., 1994), Pyrococcus furiosus (Robb, personal communication, 1993),
Plasmodium faciparum (malaria parasite; Reddy et al., 1993), and Macrops eugenii
(tammar wallaby; Collet and Joseph, personal communication, 1994) . The Na-
tional Center for Biotechnology Information (NCBI) maintains and distributes
EST data via its EST database (dbEST; Boguski et al., 1993). As of November
1994, there were over 60,000 EST sequences from 24 different species in dbEST.
(Information on how to use the dbEST server can be obtained by sending an
electronic mail message with the word “HELP” as the text to est_report@
ncbi.nlm.nih.gov.)
The phylogenetic breadth represented by the organisms listed above is still
quite limited and will not provide data adequate for testing many of the funda-
mental questions in molecular evolution (Sogin, 1991). However, we have begun
several collaborative EST projects to encompass a broader sampling of phyloge-
netic diversity. These data will be invaluable as a starting point for designing
new molecular markers and for addressing basic questions in molecular evolu-
tion, such as the extent and significance of ancient conserved regions (Green et
al., 1993), the nature of the last universal ancestor (Forterre et al., 1993), the
patterns and processes of gene and protein evolution, and the identification of
orthologs and paralogs.

An Annealing Algorithm for Multiple Sequence Alignment

The critical starting point in any systematic analysis is the hypothesis of
common ancestry for each character in the analysis (i.e., character homology).
For morphological characters, hypotheses of homology are based on some un-
derstanding of common developmental processes. For molecular data, a multiple
sequence alignment serves as the basis for hypotheses of homology at each nucle-
otide or amino acid position. Alignments are critical for the analysis of EST data,
as the putative identification of ESTs are made on the basis of sequence compari-
sons to genes of known function. Most of the alignment algorithms available
commercially and in the public domain rely on clustering by sequence similar-
ity. With these algorithms, sequences are compared to each other and a matrix
of similarity scores is generated. The two sequences having the closest similarity
scores are aligned and a consensus sequence is calculated. The consensus se-
quence is then aligned with the next closest sequence, and the process is re-
peated until all of the sequences are aligned. A major limitation of this “greedy”
alignment method is that, once a pairwise alignment is made, regions of low
similarity are locked in place for all subsequent iterations. As a result, subopti-

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294 / BIODIVERSITY II

mal alignment is perpetuated in some regions when sequences having varying

degrees of similarity are compared.
In collaboration with colleagues at Maspar Computer, Inc., we have devel-
oped an “annealing” alignment algorithm that does not use the distance metric
approach described in the preceding paragraph and that can take advantage of
the processing power of a parallel computer (Sutton and Busse, 1993). The an-
nealing process starts by searching for pairwise regions of high similarity. Only
regions of high similarity are aligned initially for each pairwise comparison,
leaving regions of lower similarity free to find a better alignment in subsequent
pairwise comparisons. Each iteration of the algorithm is made at progressively
lower match stringency until a stable alignment is achieved. As with distance
metric algorithms, scoring matrices for amino acid replacements can be used to
optimize matches when highly divergent protein sequences are compared. The
annealing alignment method is superior to distance metric approaches in align-
ing sequences that are significantly different in length or that contain long gaps.

Databases and Biodiversity

A current limiting factor in research on molecular systematics is not the
generation of data, but the effective management, analysis, and distribution of
data (Fields, 1992; Kerlavage et al., 1993). Researchers need access to a federated
system of databases linking diverse data resources that can answer basic and
applied questions about biodiversity (National Research Council, 1993). Three
databases developed at TIGR to support our research programs provide a model
for the development of seamless links between diverse information resources:
the Expressed Sequence Tag Database ( ESTDB; Kerlavage et al., 1993 ), the
Expressed Gene Anatomy Database (EGAD; Fields et al., 1993), and the Se-
quences, Sources, Taxa database (SST; Bult et al., 1994). The steady-state acqui-
sition and analysis of EST sequence data at TIGR is supported by a relational
database, ESTDB, together with a suite of custom-built and public domain tools
for analysis and user-interfaces. We have developed EGAD to link EST se-
quences with other relevant data, including allelic differences, map location,
gene expression, cellular role, and biochemical function. SST is designed to sup-
port large-scale systematics and gene discovery projects. SST links data on DNA
and protein sequences with information on specimens, collections, and tax-
onomy, and will serve to (1) document the use of specimens from curated collec-
tions in comparative molecular analyses, and (2) facilitate the proper documen-
tation of all taxa used in molecular studies.
The relational structure of SST and EGAD allows complex queries that are
not possible with any existing public database such as: “Return a list of all taxa
collected in Panama between 1988 and 1993 for which sequence data are avail-
able, together with names of the genes sequenced from each organism and
voucher specimen locations,” or “Which cell-surface receptors expressed in

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THE IMPACT OF RAPID GENE DISCOVERY TECHNOLOGY / 295

human embryos have sequence isologs in Drosophila or Caenorhabiditis?” Thus,

SST and EGAD will answer a wide range of biological questions that currently
can be addressed only by compiling a large amount of data by hand. We expect
that the ability to easily correlate the types of data handled by EGAD and SST
will lead to more complex questions being addressed both experimentally and
retrospectively. Together, ESTDB, EGAD, and SST support research efforts in
gene discovery, molecular systematics, and population-level genetic diversity.
EGAD and SST are being developed as publicly accessible resources as part of a
federated system of interoperable databases. Demonstrations of these databases
are available via the World Wide Web at http://www.tigr.org.

APPLYING RAPID GENE DISCOVERY TECHNOLOGY TO BIODIVERSITY

Many concepts of biodiversity exist, and what is meant by “assessing
biodiversity” evades precise definition. At the very least, the term biodiversity
incorporates genetic and ecological variation, through space and time, of indi-
viduals within populations as well as monophyletic (sensu Hennig, 1966) groups
of taxa. But biodiversity also is used to describe the numbers of species in de-
fined geographic areas (species richness). What then is an appropriate measure
of biodiversity that can be used by researchers and policy makers? Is it allelic
richness within individuals, populations, species, or larger groups? The number
of populations per species or of species per monophyletic group? The numbers
of species per hectare? How do measures based on organismal taxonomy relate
to measures based on sequence similarity considered independently of species
origin, and how do these different measures relate to patterns of ecological varia-
tion and to the biology of an organism? The key to addressing these related but
quite distinct questions is sampling of both markers and species. The impor-
tance of sampling is illustrated by work underway at TIGR on microbial diver-
sity. We have found high levels of sequence variation in the small subunit of
rDNA both within and between conspecific strains in a broad sample of eubac-
terial genera (Clayton et al., 1995). This is an unexpected result given that re-
gions of the small subunit of rDNA are conserved from eubacteria to vertebrates.
Are these differences due to sequencing error? Or contamination of a bacterial
culture? Or to different mechanisms of rDNA evolution in bacteria? Or to mis-
identification of bacterial species? Sequencing error and contamination are rela-
tively straightforward to detect, but to address the other possibilities will re-
quire a suspension of preconceived ideas of molecular and biological diversity
and a focus on collection of data and clear, unbiased analysis.
We are working to scale-up and automate the DNA extraction, amplifica-
tion, and sequencing steps associated with molecular systematics so that mul-
tiple exemplars and multiple molecular markers can be analyzed simultaneously
with the same accuracy and efficiency that we now achieve in sequencing ESTs.
Our current research focuses on the use of molecular markers to identify mono-

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296 / BIODIVERSITY II

phyletic groups of organisms (i.e., organisms that descend from a common an-
cestor) and their geographic distributions. Future research will include measur-
ing allelic variation at the population level. We use the term “Phylogenetic Spe-
cies Tags” (PSTs) to describe the sequence-based phylogenetic trees that are
generated from large-scale, molecular-based analyses. Just as ESTs are the start-
ing point for further characterization of a particular gene and its biological func-
tion and cellular role, PSTs represent a first pass at identification and classifica-
tion of taxa. As a tool for assessing biodiversity, PSTs are a form of molecular
triage to assist in identifying taxonomic priorities for conservation efforts
(Stiassny, 1992) and to identify unique species (Novacek, 1992). For example,
molecular surveys of specific taxonomic groups using suites of multiple genetic
markers could be used to compare geographic areas for evidence of loss of spe-
cies diversity or as a tool to monitor the reestablishment of species and popula-
tion diversity following remediation efforts.
The power of the molecular approach is not in the technology per se, but is
in the comparative methodologies that serve as the basis for phylogenetic sys-
tematics (Farris, 1983; Funk and Brooks, 1990). Its success depends not only on
the volume of data that can be generated, but on the development of molecular
markers appropriate for a given research question; the establishment of baseline
data on molecular variation; networks of databases that link molecular, geo-
graphic, ecological, and morphological data; and close collaborations with scien-
tists at collections-based research institutions world-wide.
At the National Forum on BioDiversity held in Washington, D.C., in 1986,
E.O. Wilson declared that “the magnitude and control of biological diversity is
not just a central problem of evolutionary biology; it is one of the key problems
of science as a whole” (Wilson, 1988:14). The authorship of this chapter consti-
tutes evidence that we share this belief, since it includes individuals with ex-
pertise in systematics, evolutionary biology, molecular biology, computational
biology, computer science, and protein biochemistry. The technological and
informational advances associated with the Human Genome project have cre-
ated the infrastructure necessary for exploring molecular variation on a large
scale. The union of the technology with the power of the comparative method
will undoubtedly lead to intriguing new insights into evolution and bio-
diversity assessment far into the twenty-first century.

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CHAPTER
21

Initial Assessment of Character

Sets from Five Nuclear Gene
Sequences in Animals1
TIMOTHY P. FRIEDLANDER
Research Associate, Center for Agricultural Biotechnology,
University of Maryland Biotechnology Institute

JEROME C. REGIER
Director, Center for Agricultural Biotechnology,
University of Maryland Biotechnology Institute

CHARLES MITTER
Associate Professor, Department of Entomology,
University of Maryland, College Park, Maryland

There is growing agreement that, because any single sequence alone may be
misleading, molecular systematic inferences can rest securely only on concor-
dant results from multiple independent sequences (Miyamoto and Cracraft,
1991). For nucleotide sequences, most inferences in animals have been based on
either the mitochondrial genome or the nuclear ribosomal gene family. The
analyses described herein are directed at documenting the informativeness of
additional nuclear gene sequences.
The selection of phylogenetically informative sequences from the nuclear
genome is not trivial. Current methods of inference deal most effectively with
point substitutions and simple insertion/deletion events within independently
evolving orthologous sequences. Problems such as distinguishing orthologs
from paralogs or detecting nonindependent evolution are often intractable. Even
data on point substitutions are hard to interpret when divergence is great and
multiple hits are common. For these reasons, most of the nuclear genome prob-
ably is not useful for any given systematic question. For example, non-
transcribed regions, which constitute the vast majority of the nuclear genome,
are unlikely to be informative about higher-level taxonomic relationships. The
1This publication is reprinted with slight modifications from Friedlander, T. P., J. C. Regier, and

C. Mitter. 1994. Phylogenetic information content of five nuclear gene sequences in animals: Initial
assessment of character sets from concordance and divergence studies. Syst. Biol. 43:511-525.

301

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302 / BIODIVERSITY II

difficulty of a priori selection of likely informative sequences currently limits

the exploitation of nuclear genes for phylogenetic studies.
In a previous study, we delimited 14 protein-encoding nuclear genes whose
sequences are likely to contain interpretable phylogenetic information, largely
in the form of point substitutions (Friedlander et al., 1992). The criteria for their
selection included appropriate levels of sequence conservation for deep taxo-
nomic splits, as inferred from comparisons of published sequences, and desir-
able features of gene structure. In particular, these genes are present in just one
or a few copies, simplifying identification of orthologous comparisons. They
each contain over 1,000 basepairs of fairly uniformly evolving coding regions,
hence many potential characters. They are free of internal repetitive elements
or obvious nucleotide bias that would complicate sequence alignments (homol-
ogy statements) and analysis.
In the current study, we have sought to gauge more directly the phyloge-
netic information content of five promising genes for animal phylogenetics.
They are dopa decarboxylase (DDC, EC 4.1.1.26), phosphoenolpyruvate carboxy-
kinase (PEPCK, EC 4.1.1.32), the nonrepeating portion of the largest subunit of
RNA polymerase II (POL II, EC 2.7.7.6), elongation factor-2 (EF-2), and elonga-
tion factor-1α (EF-1α, orthologs of the F1 gene in Drosophila melanogaster
[Walldorf et al., 1985]). All available, alignable animal sequences for these genes
(as of 1993), representing a range of divergence times from about 10 million
(Catzeflis et al., 1992; Jacobs et al., 1989) to more than 550 million years ago
(Bowring et al., 1993; Conway Morris, 1993), were examined for phylogenetic
informativeness in three ways.
First, the sequences were mapped onto accepted phylogenies strongly sup-
ported by previous evidence (Figure 21-1). This permitted the assessment of
character support for each clade and the temporal partitioning of characters by
their times of divergence. Mapping also permitted identification of homo-
plasious characters.
Second, the sequences were analyzed by parsimony and the resulting mini-
mum-length trees (Figures 21-2 to 21-6) compared with the accepted phylogeny
(Figure 21-1). Character sets consisting of amino acids, of total nucleotides, and
of nucleotides from each of the three codon positions were analyzed separately.
Characters were partitioned in this manner because nucleotides within protein-
encoding sequences evolve at different rates (Fitch, 1980; Li and Graur, 1991:67-
98), and thus are likely to be maximally informative at different taxonomic levels.
We collectively refer to the analyses listed in this and the previous paragraph,
comprising evaluation of new sequences in light of a previously well-established
phylogeny, as a “concordance test.” Such tests provide the strongest available
validation of the phylogenetic utility of a candidate gene.
A third, less direct but readily obtainable, predictor of phylogenetic infor-
mativeness is pairwise sequence divergence. Over the lowest part of its range,
pairwise divergence should be related to the number of informative characters.

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FIGURE 21-1 Accepted phy-

logenetic relationships for all
taxa used in this study. Spe-
cies names are listed in Table
21-1. Curved branches leading
to the nematode in this and
subsequent figures denote un-
certain placement with respect
to arthropods and vertebrates.

At higher levels, however, these differences can underestimate the actual num-
ber of substitutions to an ever-increasing degree due to “multiple hits” (Kimura,
1982; Saitou, 1989; Shoemaker and Fitch, 1989), with concomitant loss of phylo-
genetic information. Under the Jukes-Cantor model (Jukes and Cantor, 1969),
for example, when observed divergence is approximately 0.55, the actual aver-
age number of substitutions per site is 1.0, while divergence of 0.75 corresponds
to complete saturation, equivalent to comparisons between random sequences.
This model, in conjunction with empirical saturation plots, provides heuristic
guidelines for the onset of saturation. These guidelines, in combination with the
phylogenetic concordance studies, permit a first estimate of the taxonomic level
over which each character set in the five genes will be maximally informative
(Cracraft and Helm-Bychowski, 1991).

MATERIALS AND METHODS

Data
Nucleotide and amino acid sequences of animal genes were accessed through
the GenBank/EMBL and SWISS-PROT data banks. Sequences were aligned first
using the GAP program in the University of Wisconsin Genetics Computer
Group’s software package (Devereux et al., 1984) and then by eye in multiple
sequence comparisons. Sequence regions of uncertain alignment (and therefore

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FIGURE 21-2 Concordance study using the DDC gene sequences. (a,b) The two most
parsimonious trees for DDC amino acid sequences. Minimum and maximum branch
lengths under any character optimization rule are mapped onto appropriate branches.
Tree lengths (L)=652, consistency indices with autapomorphies removed (CI=CIadj.)=
0.827, retention indices (RI)=0.689, numbers of informative characters for the aligned
data set=145-158 (ambiguous because of missing data). (c) Most parsimonious tree for
DDC nucleotide sequences (identical to test phylogeny). Minima and maxima for both
amino acid and nucleotide substitutions are mapped, the latter by codon position (top to
bottom: aa, nt1, nt2, nt3, all nucleotides). Tree statistics are shown.

homology), mostly insertion/deletion neighborhoods, were removed before

analysis. Excluded portions amount to no more than 15% of the total coding
regions in any of the five genes. For POL II only, the carboxy-terminal 20% was
excluded from the outset because of multiple, internally repeating sequences
with problematical alignment across species (Suzuki, 1990). For DDC, the nema-
tode nucleotide sequence was excluded because it could not be aligned with any
confidence with the other four available sequences.
The five genes studied, the species in which they were examined, sequence
accession numbers, portions of sequences aligned in the analyses, and total num-
bers of aligned sites are listed in Table 21-1. EF-1α sequences from one fly (F2

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FIVE NUCLEAR GENE SEQUENCES / 305

gene, Walldorf et al., 1985) and one bee (probable F2 ortholog; Walldorf and
Hovemann, 1990) were excluded from this study owing to nonorthology with
other EF-1α sequences. The accepted (and, when different, most parsimonious)
cladograms for all character sets and test taxa are shown in Figures 21-2 to 21-6.

Test Phylogeny
The relationships depicted in Figure 21-1 among the taxa used in this study,
representing some of the most securely established relationships of those in any
organismal groups, are supported by morphology and in most cases by multiple
other lines of evidence. Thus, they provide a benchmark against which the
utility of new character sets can be assessed. These groups include tetrapods
and their subgroups, the Amniota and Mammalia (Benton, 1990); within mam-
mals, Artiodactyla (cow and pig) and rodents; and within rodents, the sub-
groups hystricognaths (guinea pig) and myomorphs (rat and mouse, hamsters)
(Luckett and Hartenberger, 1985). There is evidence that guinea pigs may not
be rodents (Graur et al., 1991). The remaining mammalian relationships are
controversial and left unresolved. Monophyly of the holometabolous insects
and their subgroups, Diptera (flies) and Lepidoptera (moths), is not in doubt
(Kristensen, 1991). Monophyly of the Arthropoda has been questioned, but a
closer relationship of Crustacea to insects than to either Nematoda or Vertebrata

FIGURE 21-3 Concordance study using the PEPCK gene sequences. Character mapping
as in Figure 21-2. Tree statistics are shown. (a) Most parsimonious tree for PEPCK amino
acid and nucleotide position 1 and 2 datasets. (b) Most parsimonious tree for PEPCK
nucleotide position 3.

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FIGURE 21-4 Concordance study using the

POL II gene sequences. Most parsimonious
tree for POL II sequence data sets (identical
to test phylogeny). Character mapping as for
Figure 21-2. Tree statistics are shown.

FIGURE 21-5 Concordance study using the

EF-2 gene sequences. Most parsimonious
tree for EF-2 sequence data sets (identical to
test phylogeny). Character mapping as for
Figure 21-2. Tree statistics are shown.

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FIGURE 21-6 Concordance study using the EF-1α gene sequences. Character mapping
as for Figure 21-2. Tree statistics are shown. (a) Test phylogeny for EF-1α sequences. (b)
Strict consensus tree of the two most parsimonious trees for amino acid sequences, with
uncertain placement of the mouse. There are either seven or eight characters mapping to
the mouse branch, and either two or three characters mapping to the mammal branch. (c)
Strict consensus tree of the two most parsimonious trees for nucleotides in codon position
1, with uncertain placement of the rabbit. (d) Strict consensus tree of six most parsimo-
nious trees for nucleotides in codon position 2, with uncertain placement of flies within
insects and of rodents and the rabbit within mammals. Numbers assigned to various
branches vary as shown. (e) Most parsimonious tree for nucleotides in codon position 3.

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FIGURE 21-6 Continued

has not (review in Eernisse et al., 1992). Monophyly of Nematoda has not been
questioned, but the position of this phylum with respect to the other two groups
(arthropods, vertebrates) is not resolved (Eernisse et al., 1992).

Phylogenetic Analyses
All analyses of parsimony were done with PAUP versions 3.0 (Swofford,
1991). Pairwise sequence divergences by gene and character set obtained with
this program are listed in Tables 21-2 and 21-3. Values from 0.01 to 0.30 are
underlined in Table 21-2 to discriminate more optimal values from more satu-
rated ones (see Discussion below). Most parsimonious trees were obtained using

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FIGURE 21-6 Continued

the branch-and-bound or exhaustive analyses options. Tree lengths (L), consis-

tency indices adjusted for uninformative sites (CIadj), retention indices (RI), and
informative characters are listed with each tree. In addition, the minimum and
maximum number of synapomorphies under any character optimization are
placed on branches of the accepted and most parsimonious trees.

RESULTS
Dopa Decarboxylase
Analysis of amino acid sequences from eight taxa (Table 21-1) yields two
most parsimonious trees differing only in the position of the rat (Figures 21-

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TABLE 21-1 Genes examined, animals studied for each, sequence

accession numbers, numbers of aligned sites, and sequence portions
used in concordance studies.

No./position of
Genes Accessions aligned sites

Dopa decarboxylase 1,422 nt

Bos taurus (cow) P27718 1-467 (aa only)
Caenorhabditis elegans (nematode) Z11576 1-467 (aa only)
Cavia porcellus (guinea pig) P22781 1-467 (aa only)
Drosophila melanogaster (fly) X04661, M2411, X16802 1-1413
Homo sapiens (human) M88700 1-1422
Manduca sexta (moth) (Hiruma and Riddiford, 1990) 1-1416
Rattus norvegicus (rat) M27716 1-1422
Sus scrofa (pig) P80041 1-467 (aa only)
Phosphoenolpyruvate carboxykinase 1,641 nt
Ascaris suum (nematode 2) L01787 124-372, 389-1176,
1213-1548, 1579-1693
1720-1761, 1784-1899
Drosophila melanogaster (fly) Y00402 154-402, 418-1200,
1234-1569, 1597-1710,
1735-1776, 1801-1917
Gallus gallus (bird) M14229 79-327, 340-1122,
1156-1491, 1525-1638,
1663-1704, 1726-1842
Haemonchus contortus (nematode 1) M76494 61-309, 325-1107,
1144-1479, 1510-1623,
1651-1692, 1714-1830
Homo sapiens (human) L05144 79-327, 340-1122,
1156-1491, 1525-1638,
1663-1704, 1726-1842
Rattus norvegicus (rat) K02299, K03243-K03248 79-327, 340-1122,
1156-1491, 1525-1638,
1663-1704, 1726-1842
RNA polymerase II (largest subunit) 4,360 nt
Caenorhabditis elegans (nematode) M29235 19-468, 508-588, 595-
1644, 1648-2730,
2761-3774, 3781-4444
Drosophila melanogaster (fly) M27431 16-102, 108-471, 505-
585, 589-1227, 1240-
1650, 1654-3471,
3480-3758, 3771-4434
Homo sapiens (human) X63564 28-114, 120-483, 529-
609, 613-1251, 1264-
1674, 1678-3495,
3505-3783, 3796-4459
Mus musculus (mouse) M12130, M14101 28-114, 120-483, 529-
609 613-1251, 1264-
1674, 1687-3504,
3514-3792, 3805-4468

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TABLE 1 Continued

No./position of
Genes Accessions aligned sites

Elongation factor-2 2,409 nt

Caenorhabditis elegans (nematode) M86959 1-267, 313-618, 625-
743, 841-2559
Drosophila melanogaster (fly) X15805 1-267, 289-594, 601-
717, 817-2535
Homo sapiens (human) M30456, X51466 1-267, 277-582, 592-
708, 859-2577
Mesocricetus auratus (hamster) M13708 1-267, 277-582, 592-
708, 859-2577
Rattus norvegicus (rat) Y07504 1-267, 277-582, 592-
708, 859-2577
Elongation factor-1a (F1 ortholog) 1,374 nt
Artemia species (brine shrimp) J01165, X00546, X03349 1-1374
Bombyx mori (moth) D13338 1-1374
Cricetulus longicaudatus (hamster) D00522 1-1374
Drosophila melanogaster (fly 1) X06869 1-1374
Homo sapiens (human) X03558 1-1374
Mus musculus (mouse) X13661 1-1374
Onchocerca volvulus (nematode) M64333 1-1374
Oryctolagus cuniculus (rabbit) X62245 1-1374
Rattus norvegicus (rat) X61043 1-1374
Rhynchosciara americana (fly 2) X66131 154-1374
Xenopus laevis (frog) M25504 1-1374

2a,b). Both trees are concordant with the expected topology from Figure 21-1.
Approximately one-third of the 471 aligned sites are potentially informative.
Least divergent pairs of taxa are found within mammals (d aa~0.11, Table 21-2)
and represent evolutionary splits of 65 million years ago or less (Novacek, 1982).
The moth/fly divergence, estimated at approximately 275 million years ago
(Kukalova-Peck, 1991), has a d aa of ~0.26. Mammal/insect divergences (>550
million years ago, daa~0.39) are less than those for either mammal/nematode or
insect/nematode comparisons (d aa~0.60).
All nucleotide character sets recover the test phylogeny for the four taxa
whose sequences could be aligned; 16% of the 1,422 aligned nucleotide sites are
informative (Figure 21-2c). Nucleotides in the first two codon positions and
amino acids analyzed for the same four taxa have RI and CIadj above 0.900, while
indices for nt3 are lower (e.g., RI=0.740). Pairwise nucleotide divergences vary
widely with character set and taxonomic depth (Table 21-2). For example, nt2 is
less divergent at all taxonomic depths than nt3, even within mammals. The
within-mammal comparison may be the only comparison for the nt3 set that is
not fully saturated (dnt3=0.314).

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TABLE 21-2 Pairwise sequence divergences by gene and character set.

Within each matrix, the values for the first of the two character sets listed in
the upperleft corner are given below the diagonal, while those for the second
are above the diagonal. Divergence values from 0.010 to 0.300 are italicized.

Dopa decarboxylase
aa\nt1 nem moth fly gpig rat human cow
moth 0.607 — 0.259 0.350 0.344
fly 0.604 0.262 — 0.352 0.340
guinea pig 0.596 0.387 0.387 —
rat 0.591 0.402 0.394 0.134 — 0.095
human 0.587 0.391 0.385 0.121 0.106 —
cow 0.598 0.402 0.404 0.153 0.123 0.108 —
pig 0.567 0.389 0.398 0.146 0.134 0.102 0.110

nt2\nt3 rat human fly moth

rat — 0.314 0.601 0.664
human 0.046 — 0.610 0.658
fly 0.211 0.215 — 0.626
moth 0.226 0.224 0.125 —

Phosphoenolpyruvate carboxykinase
aa\nt1 nem 2 nem 1 fly bird human rat
nematode 2 — 0.192 0.324 0.314 0.296 0.303
nematode 1 0.214 — 0.353 0.316 0.307 0.305
fly 0.373 0.378 — 0.285 0.287 0.293
bird 0.376 0.375 0.280 — 0.106 0.108
human 0.361 0.361 0.280 0.129 — 0.066
rat 0.359 0.355 0.290 0.122 0.071 —

nt2\nt3 nem 2 nem 1 fly bird human rat

nematode 2 — 0.580 0.614 0.669 0.644 0.614
nematode 1 0.119 — 0.618 0.623 0.640 0.623
fly 0.243 0.247 — 0.647 0.550 0.532
bird 0.239 0.229 0.194 — 0.495 0.486
human 0.229 0.225 0.197 0.048 — 0.351
rat 0.221 0.219 0.196 0.049 0.018 —

RNA polymerase II (largest subunit)

aa\nt1 mouse human fly nem
mouse — 0.020 0.216 0.266
human 0.000 — 0.210 0.262
fly 0.219 0.219 — 0.263
nematode 0.265 0.265 0.275 —

nt2\nt3 mouse human fly nem

mouse — 0.276 0.588 0.611
human 0.001 — 0.560 0.634
fly 0.108 0.108 — 0.617
nematode 0.149 0.149 0.146 —

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TABLE 2 Continued

Elongation factor-2
aa\nt1 nem fly human hams rat
nematode — 0.151 0.142 0.139 0.146
fly 0.188 — 0.159 0.153 0.158
human 0.193 0.199 — 0.020 0.124
hamster 0.195 0.200 0.008 — 0.011
rat 0.195 0.199 0.009 0.004 —

nt2\nt3 nem fly human hams rat

nematode — 0.529 0.598 0618 0.605
fly 0.083 — 0.514 0.531 0.503
human 0.092 0.091 — 0.365 0.325
hamster 0.092 0.091 0.002 — 0.283
rat 0.092 0.091 0.002 0.000 —

Elongation factor-1α
aa\nt1 nem shrimp moth fly 1 fly 2 frog hams rat mouse rabbit human
nematode — 0.179 0.175 0.175 0.199 0.177 0.170 0.170 0.175 0.162 0.166
shrimp 0.180 — 0.096 0.098 0.128 0.153 0.151 0.153 0.155 0.148 0.148
moth 0.160 0.101 — 0.050 0.081 0.131 0.124 0.133 0.131 0.129 0.129
fly 1 0.185 0.115 0.059 — 0.081 0.135 0.133 0.138 0.135 0.133 0.133
fly 2 0.210 0.151 0.095 0.100 — 0.167 0.162 0.170 0.170 0.170 0.165
frog 0.167 0.164 0.144 0.155 0.176 — 0.039 0.041 0.048 0.039 0.037
hamster 0.155 0.158 0.128 0.144 0.174 0.038 — 0.009 0.015 0.015 0.017
rat 0.155 0.158 0.128 0.144 0.174 0.038 0.000 — 0.020 0.015 0.017
mouse 0.167 0.169 0.140 0.155 0.187 0.054 0.018 0.018 — 0.026 0.028
rabbit 0.155 0.158 0.128 0.142 0.171 0.041 0.002 0.002 0.020 — 0.011
human 0.155 0.158 0.128 0.142 0.171 0.041 0.002 0.002 0.020 0.000 —

nt2\nt3 nem shrimp moth fly 1 fly 2 frog hams rat mouse rabbit human
nematode — 0.602 0.608 0.685 0.598 0.569 0.595 0.615 0.621 0.617 0.591
shrimp 0.096 — 0.476 0.533 0.485 0.480 0.524 0.511 0.521 0.522 0.517
moth 0.088 0.048 — 0.443 0.463 0.500 0.507 0.485 0.488 0.517 0.502
fly 1 0.103 0.055 0.026 — 0.490 0.496 0.533 0.515 0.508 0.502 0.522
fly 2 0.121 0.076 0.049 0.052 — 0.530 0.547 0.564 0.558 0.539 0.527
frog 0.101 0.096 0.085 0.094 0.111 — 0.389 0.369 0.405 0.389 0.393
hamster 0.103 0.092 0.079 0.090 0.115 0.017 — 0.183 0.173 0.207 0.192
rat 0.103 0.092 0.079 0.090 0.115 0.017 0.000 — 0.133 0.201 0.234
mouse 0.105 0.096 0.083 0.094 0.121 0.022 0.007 0.007 — 0.221 0.239
rabbit 0.103 0.090 0.076 0.087 0.113 0.017 0.002 0.002 0.009 — 0.164
human 0.103 0.090 0.076 0.087 0.113 0.017 0.002 0.002 0.009 0.000

Phosphoenolpyruvate Carboxykinase
Of the four character sets tested for six taxa (Table 21-1), only the nt3 set
failed to recover the test phylogeny (Figure 21-3a), grouping the rat with the
bird instead of with the human (Figure 21-3b). However, no character set
strongly supported one topology over the other.

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TABLE 21-3 Selected pairwise sequence comparisons

(divergence) of taxa by gene and character set.

Character set
Genes nt1 nt2 nt3 aa

nematode/flya,b
DDC 0.604
PEPCK 0.337 0.245 0.616 0.376
POL II 0.263 0.146 0.617 0.275
EF-2 0.151 0.083 0.529 0.188
EF-1a 0.187 0.112 0.642 0.198
nematode/humana,b
DDC 0.587
PEPCK 0.302 0.227 0.642 0.361
POL II 0.262 0.149 0.634 0.265
EF-2 0.142 0.092 0.598 0.193
EF-1a 0.166 0.103 0.591 0.155
fly/humanb
DDC 0.340 0.215 0.610 0.385
PEPCK 0.287 0.197 0.550 0.280
POL II 0.210 0.108 0.560 0.219
EF-2 0.159 0.091 0.514 0.199
EF-1a 0.149 0.100 0.525 0.157
human/ratc
DDC 0.095 0.046 0.314 0.106
PEPCK 0.066 0.018 0.351 0.071
POL II 0.020 0.001 0.276 0.000
EF-2 0.024 0.002 0.325 0.009
EF-1a 0.023 0.006 0.237 0.011
moth/flyb
DDC 0.259 0.125 0.626 0.262
EF-1a 0.066 0.038 0.453 0.077
hamster/ratec
EF-2 0.011 0.000 0.283 0.004
EF-1a 0.012 0.004 0.178 0.009

aNucleotide comparisons unavailable for DDC.

bAverage values for nematodes for PEPCK and for flies for EF-1a.
c Mouse substituted for rat in POL II comparisons; average values for rat/mouse

for EF-1a.

One-fourth of 510 amino acid sites, and one-third of 1,641 nucleotide se-
quence sites, mostly in nt3, are potentially informative. Pairwise divergences
(Table 21-2) for the bird/mammal split (~300 million years ago; Benton, 1990)
are relatively small for amino acids and nt1+2 (0.13 and ~0.16 average) but large
(dnt3=0.49) at nt3. Divergence between the two mammals (~65 million years
ago) is about half as large (daa~0.07, dnt1+2~0.04 average) as that for bird/mam-

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FIVE NUCLEAR GENE SEQUENCES / 315

mals in these characters. Divergence between the two nematodes is twice as

large as that observed for bird/mammals (d aa~0.21, dnt1+2~0.16 average). Nt3 is
saturated for all nematode/fly comparisons, almost saturated for bird/mammal
comparisons, but less so for rat/human comparisons.

RNA Polymerase II (Largest Subunit)

All character sets recovered the mammal clade (Figure 21-4) among the four
available sequences (Table 21-1). Approximately 10% of the alignable sites
(1,495 aa/4,360 nt) were informative, and homoplasy was low for all character
sets except nt3. Mouse/human (divergence ~65 million years ago) differences
are entirely synonymous changes (Table 21-2, daa=0, dnt3=0.276); all other nt3
divergence comparisons are nearly saturated (d>0.5). Nonsynonymous diver-
gences between fly and mammal (>550 million years ago) are less than those
between either taxon and nematode (daa~0.26 versus daa~0.33).

Elongation Factor-2
All character sets recover the expected phylogeny (Figure 21-5) for these
five taxa (Table 21-1), although support for the rodent clade, as opposed to the
mammal clade, is largely limited to nt3. Seven percent of 844 amino acid sites
and 15% of 2,409 nucleotide sites were potentially informative. Homoplasy is
low (RI>0.925) for all but nt3 (RI=0.545).
Amino acid differences (Table 21-2) within mammals (divergence ~65 mil-
lion years ago) are few (daa<0.01). Synonymous site comparisons are saturated
except within mammals, where dnt3 values range from 0.283 to 0.365. The nema-
tode and fly are roughly equally divergent from mammals and from each other.

Elongation Factor-1α
Published EF-1α sequences are more numerous (11) and thus permit more
taxonomic levels to be tested in concordance studies than the previous character
sets (Figure 21-6a). Fifteen percent of 440 amino acid sites were potentially
informative. Two most parsimonious trees were found, both concordant with
the test phylogeny, but neither tree resolves how rodents are related to each
other or to other mammals (Figure 21-6b).
One-third of 1,374 nucleotide sites were potentially informative. Nt1 yields
two most parsimonious trees, neither of which resolves insect or rodent relation-
ships correctly (Figure 21-6c). The rabbit shares a minimum of one change with
either rodents or humans. Only two additional changes are required to recover
the test phylogeny.
Six most parsimonious trees result from the analysis of nt2 (Figure 21-6d).
Their strict consensus is concordant with the test phylogeny (Figure 21-6a), but

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not all minimum length trees group the two taxa of flies. Most phylogenetic
trees group the human and rabbit and recover rodents. Some do both, but
rodents are never resolved. The position of rabbits with regard to rodents and
primates is controversial (Goodman et al., 1985; Li et al., 1990; Pesole et al.,
1991).
One most parsimonious tree was found for nt3 (Figure 21-6e), one step
shorter than the concordance tree. The former differs from the latter only by
grouping one fly with the moth in preference to the other fly. All nucleotide
sites analyzed together give this same result as equally parsimonious with the
concordance tree (data not shown).
Least divergent pairs of taxa occur within mammals (~65 million years ago,
daa<0.02, Table 21-2). Maximum dnt3 within mammals is still comparatively
small (<0.24). Frog/mammal divergences (~365 million years ago; Benton, 1990)
are about twice as large as those for mammals. Between-insect comparisons
(200-275 million years ago; Kukalova-Peck, 1991) are even greater (d aa~0.10,
dnt3~0.47), followed by crustacean/insect, arthropod/vertebrate, and finally, all
nematode comparisons (daa~0.17, dnt3~0.61). Nt3 divergences appear saturated
except within mammals (see below).

DISCUSSION
Our concordance tests on all available animal sequences provide evidence
that these five genes contain substantial phylogenetic information. For each
gene, parsimony analysis of amino acid and most nucleotide character sets re-
covered the test phylogeny (Figure 21-1), although with varying quantity and
quality of support and resolution (Figures 21-2 to 21-6). While more evidence is
needed, we predict that these five genes will prove widely applicable to phylo-
genetic studies.
The pairwise divergences in Table 21-3 illustrate that these five genes evolve
at greatly different rates. DDC evolves most rapidly, followed by PEPCK. POL
II, EF-2, and EF-1α are the slowest, and are well known for their extreme pro-
tein sequence conservation (Cammarano et al., 1992; Creti et al., 1991; Gropp et
al., 1986; Iwabe et al., 1991; Rivera and Lake, 1992). Within each gene, nt3 is
the fastest among sequence character sets, reflecting a preponderance of syn-
onymous substitutions, while nt2 is slowest, presumably because all nt2 substi-
tutions are nonsynonymous. Amino acids are intermediate, owing to the fact
that amino acid changes may result from nucleotide changes in any codon posi-
tion. Nt1 is also intermediate because changes can be both synonymous (leucine
and arginine codons) and nonsynonymous. In our concordance studies, non-
synonymous substitutions and amino acid replacements largely agree with the
test phylogenies, but are not fast enough to track relatively recent splits. Syn-
onymous substitutions track recent splits, but are increasingly noisy with re-
gard to deeper splits.

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Given this variation in rates, it should be possible to preselect particular

combinations of these genes and character sets which are most likely to be use-
ful for resolving phylogenetic splits of a given temporal range. The current
paucity of sequences prevents our concordance tests from specifying precise
ranges of utility for these genes. However, a useful interim predictor of such
ranges can be obtained from pairwise sequence differences. As a first approxi-
mation, we suggest divergences of 0.20 to 0.30 as a threshold, above which
multiple hits are likely to lead tree construction astray. Plots of divergence
against time and/or apparent transition/transversion ratios for a number of both
mitochondrial and nuclear genes (e.g., Liu and Beckenbach, 1992; Mindell and
Honeycutt, 1990; Shoemaker and Fitch, 1989) suggest that, above this level, an
approach to saturation frequently becomes evident. This is also the point at
which observed differences start to depart noticeably from actual ones in the
Jukes-Cantor model (Jukes and Cantor, 1969), which predicts that our suggested
interval corresponds to actual divergences of 0.23 to 0.38. Under models in-
corporating more constraints, including nucleotide bias and natural selection,
underestimation of evolutionary divergence should be still more pronounced
(Fitch, 1986). Above this level of divergence, suites of characters on long
branches might converge.
On the other hand, the suggested threshold might be too conservative in
some cases, because it ignores the ability of phylogenetic trees to reveal substi-
tutions undetected by pairwise comparisons when there are taxa that branch off
between the pair being compared (Saitou, 1989). Indeed, in several cases in our
study, nt3 recovered the test phylogeny despite saturating divergence levels.
At the other extreme, pairwise divergences less than 0.01, for example, will
yield very few characters even from gene sequences hundreds of basepairs long.
Thus, while the models for estimating actual divergence values from observed
pairwise divergences provide heuristic guidelines, divergence levels correspond-
ing to maximal phylogenetic utility will depend on the nature of the phyloge-
netic problem, including the pattern of taxon sampling, rates of evolution in
different lineages, and the divergence times to be resolved.
Based on these divergence criteria and the estimated divergence times of
our test taxa, we provide in Table 21-4 a first estimate of the time frames over
which the different character sets for the five genes are likely to prove optimally
informative with more extensive concordance testing. Perhaps the strongest
practical implication of Table 21-4 is the importance of separate consideration of
the different character sets within each gene (partitions of Bull et al., 1993). One
advantage of such discrimination lies in avoiding faulty inferences. For ex-
ample, for extremely conserved genes such as POL II, EF-2, and EF-1α, there is
likely to be an intermediate time span in which no character set is appropriate,
even though overall divergence levels might appear to lie within the useful
range. This is because sites undergoing synonymous changes can become fully
saturated before enough nonsynonymous changes have accumulated to provide

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TABLE 21-4 Predicted time spans of optimal phylogenetic utility for

nucleotide position and amino acid character sets in each gene, based on
concordance and divergence studies among test taxa with known times of
separation.

Approximate Ages of Divergences

Cenozoic Paleozoic
Character sets ~35 MYA 50-65 MYA 275-365 MYA ~550 MYA

all nt DDC POL II

PEPCK EF-2
POL II EF-1a
EF-2
EF-1a
nt1, nt2, aa DDC PEPCK POL II
PEPCK POL II EF-2
EF-2 EF-1a
EF-1a
nt2 only DDC PEPCK

substantial phylogenetic information. We have evidence that this is so for EF-

1α sequences applied to relationships among moths (unpublished observations).
Conversely, emphasizing character sets highlights a use for highly con-
served protein-encoding genes that has gone largely unexploited. Because EF-
1α is so conservative overall, it has been applied heretofore mostly to the very
earliest divergences, e.g., those among major lineages of prokaryotes. Third
position nucleotides in that same gene sequence, however, evolve rapidly
enough to be useful at much lower taxonomic levels, with the advantage over
introns or other rapidly evolving sequences that amino acid conservation should
make both alignment and primer definition straightforward. Indeed, third po-
sition characters in all conservative, protein-encoding genes may be useful at
lower taxonomic levels. We have preliminary evidence that, for EF-1α, nt3 sites
will be highly informative about generic and subfamilial relationships in the
moth family, Noctuidae (Cho et al., 1995).

ACKNOWLEDGMENTS
The authors gratefully acknowledge constructive comments on earlier ver-
sions by Drs. Grace Wyngaard and Michael Miyamoto and by two anonymous
reviewers. We thank Soowon Cho for his contributions in the study of EF-1α
sequences. This research was supported by funds from the National Science
Foundation grant #DEB-9212669, the Center for Agricultural Biotechnology, the

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U.S. Department of Agriculture-NRI CGP grant #90-37250-5482, and the Mary-

land Agricultural Experiment Station (MAES Scientific Article No. A6539, Con-
tribution No. 8750).

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CHAPTER
22

GAP Analysis for Biodiversity

Survey and Maintenance
J. MICHAEL SCOTT
Unit Leader

BLAIR CSUTI
Research Associate, National Biological Service, Idaho
Cooperative Fish and Wildlife Research Unit, College of Forestry,
Wildlife and Range Science, University of Idaho, Moscow

Ehrlich (1988) postulated that reversing the loss of biodiversity will require
a “quasi-religious transformation” of the way contemporary cultures view the
value of human life and the intrinsic values of organic diversity. Even if that
transformation were to occur today, we would be faced with a cruel reality:
maintaining viable examples of every natural community, including the myriad
of species they support, is the fundamental mechanism for conserving bio-
diversity (Noss and Cooperrider, 1994), but you cannot conserve biodiversity if
you do not know where it is located. The elements of biodiversity, from genes
and species to ecosystems, have distributions, but they have not been mapped
at scales useful for developing a national biodiversity conservation and manage-
ment strategy.
Centuries of scientific collectors have deposited tens of millions of speci-
mens in the world’s museums and herbaria. These form the foundation of our
knowledge of species distributions, yet many areas and taxa remain poorly
sampled. The Gap Analysis Program, a program of the National Biological Ser-
vice, uses two relatively new technologies, satellite remote sensing and geo-
graphic information systems (GIS), to assist in the assessment of the status and
distribution of several elements of biodiversity (Scott et al., 1993). While not a
substitute for traditional biological surveys, we feel that gap analysis can pro-
vide a preliminary, landscape-scale assessment of the distribution of both spe-
cies and ecosystem diversity in the United States that can be used to guide fu-
ture field research and to provide a spatial framework for a preliminary national
biodiversity conservation strategy. The gap analysis approach to biodiversity
surveys holds promise for the rapid development of information on the distribu-

321

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322 / BIODIVERSITY II

tion of several indicators of biodiversity in areas of the world that have been less
well sampled.
Burley (1988) identified four steps in gap analysis: (1) identify and classify
biodiversity, (2) locate areas managed primarily for biodiversity, (3) identify
biodiversity that is un- or underrepresented in those managed areas, and (4) set
priorities for conservation action. While these steps remain essential to gap
analysis, the distribution of vegetation cover and species, gathered as a precur-
sor to analysis, has considerable application to natural resource inventory and
monitoring in and of itself.

HISTORY OF GAP ANALYSIS

Kepler and Scott (1985) used the distribution of endangered Hawaiian forest
birds, gathered through field surveys (Scott et al., 1986), to perform a simple
“gap analysis” on the island of Hawaii (Figure 22-1). They found little overlap
between the distribution of endangered forest birds and the location of nature
reserves. The Nature Conservancy of Hawaii and the U.S. Fish and Wildlife
Service responded by establishing the Hakalau Forest National Wildlife Refuge
in one of the areas where distribution of three endangered species overlapped.
Extensive field inventory, at the level of detail undertaken in Hawaii (Scott
et al. 1986), is prohibitively expensive for large continental regions. To avoid
these expenses, the Gap Analysis Program has developed methods to take ad-
vantage of currently available information and to produce vegetation cover and
terrestrial vertebrate distribution maps (Scott et al., 1993). Other taxa, such as
butterflies, can be added to data layers where sufficient information is available.
Pilot programs of gap analysis were initiated in Idaho in 1987 and in Oregon
in 1988. By 1995, there were active programs in 36 states, and programs in 4
states—Utah, Idaho, Oregon, and Arizona—had been completed. Cooperation
with state and federal agencies and private conservation groups has been an
essential component of successful programs. Over 200 different public coopera-
tors and private businesses now are involved in various state programs. Com-
mon needs, such as access to satellite imagery and databases on species, have
encouraged cooperators to pool resources. While programs are state-based for
administrative reasons, biodiversity analyses are best carried out for entire bio-
logical regions or at the national level. State-level information eventually will
be merged to facilitate regional and national analyses.

CLASSIFYING AND MAPPING ECOSYSTEMS

Gap analysis requires three primary GIS data layers: vegetation cover, spe-
cies range maps, and the location of land managed primarily for native species
and natural ecosystem processes. Where available, information on other envi-
ronmental factors, such as elevation, slope, aspect, soils, aquatic features, and

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GAP ANALYSIS / 323

FIGURE 22-1 Ranges of four endangered forest birds on the island of Hawaii in com-
parison to the distribution of areas managed for biodiversity in 1982.

climate, can be used to improve the accuracy of maps of vegetation and species
distributions. Additional information on socioeconomic attributes of landscapes
(e.g., projected population trends, projected housing starts, ownership of land
by state and federal agencies, zoning, etc.) can be examined to refine planning
efforts for land use (Machlis et al., 1994).
Orians (1993:206) correctly pointed out that there is “no previously estab-
lished, generally accepted taxonomy of habitats, communities, or ecosystems.”
Plant communities are the most visible component of ecosystems and have been

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324 / BIODIVERSITY II

widely considered to be acceptable surrogates for ecosystems (Austin, 1991;

Austin and Margules, 1986). Gap analysis assumes that plant communities serve
as integrators of many physical factors (type of soil, moisture regime, aspect,
elevation, temperature) that interact at a site (Thomas, 1979). Floristic compo-
sition (described by the dominant or codominant species in the uppermost veg-
etation layer) provides a common denominator for description of plant commu-
nities. These communities then can be aggregated into any of a number of
taxonomic schemes, such as that proposed by the United Nations Educational,
Scientific and Cultural Organization (1973).
In 1993, cooperating with the U.S. Geological Survey (USGS), the Environ-
mental Protection Agency (EPA), and the National Oceanic and Atmospheric
Administration (NOAA), the National Biological Service’s Gap Analysis Program
purchased complete LANDSAT Thematic Mapper satellite imagery for the con-
terminous United States. Imagery from one or two dates with favorable weather
conditions in the years 1991-1993 will be made available to state programs and
cooperators. The imagery will be preprocessed and archived by the U.S. Geo-
logical Survey’s EROS Data Center in Sioux Falls, South Dakota. With coopera-
tion from the EPA, USGS, and other groups, interpretation of this imagery will
serve as the framework for a seamless national vegetation map.
LANDSAT Thematic Mapper imagery measures reflectance of 30 × 30 m
pixels (picture elements) on the Earth’s surface at seven wavelengths (see Scott
et al., 1993, for details). Upland vegetation cover is mapped by aggregating
pixels of similar reflectance into polygons using a minimum mapping unit of 100
hectares. Smaller minimum mapping standards have been used by most states to
meet local needs.
Gap analysis programs use GIS software with vector data structure as a
standard for vegetation mapping (ARC/INFO, Environmental Systems Research
Institute, Inc., Redlands, California). Stands are delineated either by on-screen
digitizing or by computer algorithms (Figure 22-2). Many plant communities
are mapped as stands larger than 100 hectares. These usually contain consider-
able internal heterogeneity. An attribute file is created for each vegetation
polygon containing information about primary, secondary, and tertiary plant
communities within the polygon as well as other special features, such as the
presence of small wetlands and other microhabitats. Wetlands larger than 40
hectares are mapped when identifiable from satellite imagery. Ultimately,
1:24,000 scale maps produced by the USGS National Wetlands Inventory will be
available in digital form to represent this critical habitat element.
Although LANDSAT Thematic Mapper imagery provides a geographically
consistent and repeatable spatial framework for vegetation mapping, identifica-
tion of floristic dominant or codominant species often requires ancillary infor-
mation, such as aerial photographs, low altitude airborne videophotography
(Graham, 1993), existing large-scale vegetation maps, or field reconnaissance.

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GAP ANALYSIS / 325

Image acquisition and preprocessing

Pattern delineation

Photointerpretation Per pixel spectral

imagery classification

Scene-by-scene Supervised-
on screen digitizing unsupervised hybrids
of vegetation polygons

Label polygons using:

Aerial photos
Existing regional vegetation maps
Ground point sample data
Dominant plant species range maps

Data validation
Local expert review
Ground truthing

Data editing and revision

Data accuracy assessment

FIGURE 22-2 Flow chart showing steps in development of vegetation cover map from
LANDSAT Thematic Mapper imagery and ancillary information. Two widespread ap-
proaches to pattern delineation are used by various states. Photointerpretation offers
advantages for pattern recognition in complicated landscapes, while machine classifica-
tion is more consistent and repeatable. National minimum mapping unit and labeling
protocols must be followed regardless of the pattern delineation technique.

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326 / BIODIVERSITY II

State gap analysis programs use a variety of available sources to label vegetation
maps, keeping a record of the sources used for each polygon.

DISTRIBUTION MAPS OF SPECIES

Museum and herbarium specimens are the ultimate source of knowledge
about the classification and distribution of species. Specimen locality records
can be supplemented by reliable observations that are published in the litera-
ture or maintained in quality-controlled databases, such as the U.S. Fish and
Wildlife Service’s Breeding Bird Survey (see also Farr and Rossman, Chapter 31,
and Umminger and Young, Chapter 32, in this volume). Continued scientific
specimen collection is vital to more fully understand the distribution and varia-
tion among living organisms, but the rapid decline of many natural communities
places urgency on development of a comprehensive biodiversity conservation
strategy in the absence of a truly complete biological survey.
All distribution maps are statements of the probability of encountering a
species in time and space. The distributional limits of many species fluctuate
from year to year and may display long-term expansion or contraction. Within
those distributional limits, populations appear and disappear from patches of
suitable habitat (e.g., Dipodomys deserti in Joshua Tree National Monument,
California; Miller and Stebbins, 1964) and may occur sporadically in unsuitable
habitat. Specimen records are sparse even for many common species, and most
collecting has taken place along transportation corridors, leaving vast areas un-
surveyed. With some qualifications, these shortcomings can be overcome by
interpolating and extrapolating the probable presence of a species in suitable
environments between verified collection localities within the outer bounds of a
species’ range. Gap analysis uses this approach to develop distribution maps of
species for which distributional and ecological data are readily available. To
date, distribution mapping has focused on terrestrial breeding vertebrates, al-
though distributional data for other well-studied groups, such as butterflies, are
being gathered by some programs.
The distributional limits of each species are defined by specimen locality
records or confirmed observations. They are represented as attributes of a geo-
graphic unit, in effect creating a rasterized distribution map. Raster data struc-
ture divides an area into units and assigns each a unique attribute (presence or
absence of a species in this case). A 635 km 2 hexagonal grid array (White et al.,
1992), developed to create a sampling framework for the EPA, is being used as
the geographic unit of reference by several state programs, while the traditional
county of occurrence is used by others.
The ancients recognized the relationship between species and natural com-
munities (Morrison et al., 1992), and early concepts of the ecological niche had
their foundation in natural history observations of the links between species
and environmental features (Grinnell, 1914, 1917; Hutchinson, 1978). With cer-

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GAP ANALYSIS / 327

tain qualifications, it is possible to relate the distribution of most species to that

of plant communities in which they normally occur (Scott et al., 1993). Final
maps of species’ distributions are created by overlaying distributional limits
with a vegetation map (Figure 22-3). A database indicating which plant commu-
nities provide suitable habitat for each species then identifies those vegetation

Existing Museum Other confirmed

range maps locality observations,
records literature records

Wildlife/habitat Species-specific
relationships, accounts of
documents, habitat
databases preferences

Predicted
Predicted presence
presence in a
in a vegetation
geographic
cover type
unit

GIS
overlay

Physical or
ecological filters
(if available and
appropriate)

Predicted distribution in a
vegetation polygon within
known distributional limits

FIGURE 22-3 Flow chart showing steps in development of predicted distribution maps
for breeding terrestrial vertebrates.

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328 / BIODIVERSITY II

polygons within a species’ range that probably are occupied (Figure 22-4). In
this way, areas of unsuitable habitat are excluded from the predicted distribu-
tion. For example, species typical of coniferous forests are not predicted to
occur in desert scrub or alpine fell fields.
The two most important limitations in this approach concern scale: (1) Many
species will be present in a plant community only if certain microhabitat re-
quirements also are present, and (2) many important habitat components are
physical features (streams, cliff-faces, snags) that are too small to map. For this
reason, species maps based on wildlife-habitat relationships can best be used “to
predict the occurrence of species in general vegetation types and in environ-
mental conditions across broad regions rather than at the scale of an individual
stand” (Morrison et al., 1992:246). Put another way, it is virtually certain that
California Thrashers (Toxostoma redivivum) occur in the Berkeley Hills, as they
did in Grinnell’s day (Grinnell, 1917), but there is less chance of encountering
one in a particular 1-hectare stand of coyote bush (Baccharis pilularis) on any
particular spring morning.
Maps of species distribution generated for gap analysis are intended to be
used and validated at landscape scales (“kilometers in diameter,” Forman and
Godron, 1986:11), not at individual field sites. The total number of species
expected to occur in each vegetation stand can be displayed, creating a state
map of species richness (Figure 22-5). Because of different biogeographic histo-
ries, areas of similar species richness in different ecoregions are likely to differ in
species content. The richness maps used in any conservation evaluation will
vary with the questions being asked (e.g., what is the distribution of endemic
species, or what is the distribution of declining species of neotropical migrant
birds?).
A further caveat concerns endangered, rare, or locally distributed species.
Gap analysis does not predict that these species will occur other than at docu-
mented locations. Occurrences of virtually all the rarest and most endangered
elements of biodiversity are tracked in databases of the Conservation Data Cen-
ter which are established in all 50 states by The Nature Conservancy (Jenkins,
1988). The location of habitat for rare species can direct searches for additional
populations, but only known occurrences, obtained from cooperating Conserva-
tion Data Centers, are used for developing a conservation strategy.

LOCATIONS OF AREAS MANAGED PRIMARILY FOR NATIVE

SPECIES AND NATURAL ECOSYSTEM PROCESSES
As in the example from Hawaii (Figure 22-1), and others from Idaho (Fig-
ures 22-6 and 22-7), gap analysis compares the distribution of elements of
biodiversity with that of areas in which the maintenance of biodiversity is a
primary management goal. The boundaries of state and federal management
units that meet this criterion are placed in a GIS format. State Conservation Data

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GAP ANALYSIS / 329

FIGURE 22-4 Predicted distribution of four species produced by intersection of occur-

rence in a geographic unit (counties, in this example) and polygons of suitable vegetation
cover during the breeding season: (a) sage grouse (Centrocerus urophasianus), (b) chest-
nut-backed chickadee (Parus hudsonicus, (c) hoary marmot (Marmota caligata), (d) black
bear (Ursus americanus).

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FIGURE 22-5 Species richness for native terrestrial vertebrates in Idaho.

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GAP ANALYSIS / 331

FIGURE 22-6 Distribution of Idaho ground squirrel (Spermophilus brunneus) and Ash-
throated Flycatcher (Myiarchus cinerascens) in Idaho versus areas managed for long-term
maintenance of natural communities.

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FIGURE 22-7 Distribution of western red cedar as a dominant type of cover in Idaho
versus areas managed for long-term maintenance of biodiversity.

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GAP ANALYSIS / 333

Centers and Natural Heritage Programs maintain files on each of these public
management units, and their managed area files are the usual source for man-
aged area boundaries for state programs. Examples of such areas include na-
tional parks, wilderness areas, research natural areas, and some national wildlife
refuges (see Scott et al., 1993, for further details).

GAP ANALYSIS AS A CONSERVATION STRATEGY

It is impossible to manage for the long-term maintenance of biodiversity
unless all the elements of biodiversity are represented in the areas to be man-
aged in the first place (Margules et al., 1988). Gap analysis is a conservation
evaluation technique (Margules, 1989; Usher, 1986) that identifies areas in which
selected elements of biodiversity are represented. Once those areas are identi-
fied, other principles of conservation biology, such as population viability analy-
sis, ecosystem patch dynamics, and habitat quality can be used to select specific
sites and determine appropriate management area boundaries.
Noss (1987) and Noss and Cooperrider (1994) describe “coarse filter” and
“fine filter” conservation strategies. Coarse filter strategies assume that most
common species, including those of groups difficult to inventory, such as most
invertebrates, will be represented in a reserve network that contains viable ex-
amples of all natural communities. Some species, especially those with restricted
distributions, will be missed by the coarse filter. These species are captured by
a fine filter that tracks the location of populations of individual species or rare
natural communities.
The United States currently has no strategy to conserve biodiversity (Noss
and Cooperrider, 1994). The most visible program to conserve biodiversity is
the Endangered Species Act of 1973, a fine filter approach that protects one
species at a time. The Endangered Species Act is a powerful tool with which to
rescue species from the brink of extinction, but it is a reactive strategy that is in
danger of being overwhelmed by growing numbers of species in peril and inad-
equate funding. Furthermore, many species that are not currently endangered
will become so as their habitats are lost to human activities (Margules 1989).
The Endangered Species Act needs to be supplemented with a strategy to iden-
tify places that must be managed for their natural values if all communities and
species are to persist (Scott et al., 1987; Tear et al., 1993). Like the Endangered
Species Act, the ranking system of The Nature Conservancy’s Conservation Data
Centers provides a standard methodology for evaluating potential natural areas
on the basis of threatened or endangered species or rare natural communities
(Pearsall et al., 1986), but directs conservation action to elements of biodiversity
already in peril.
Gap analysis provides a hierarchical approach to address conservation needs
of both species and communities. Scott et al. (1987) called for an ecosystem
approach to protecting biodiversity, supplemented by protecting species-rich

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334 / BIODIVERSITY II

areas for a variety of taxa. These areas should be selected to maximize their
complementarity (see below). Finally, species not already captured in the net-
work would be added on an individual basis, as would currently unmappable
elements of biodiversity (e.g., many invertebrates, soil microfauna, ecological
processes) as information becomes available.
Despite the contribution of biodiversity management areas to a conserva-
tion strategy, many mobile species and landscape processes require far more
area than will ever be managed strictly for biodiversity (Brussard, 1991). The
fate of these species will rest on the management of multiple-use lands surround-
ing nature reserves (Scott et al., 1990). Gap analysis data layers provide infor-
mation about the context of areas being managed for different values, as well as
opportunities to maintain connectivity between natural areas through landscape
linkages (Csuti, 1991).

METHODS OF ANALYSIS: SELECTING COMPLETELY

REPRESENTATIVE BIODIVERSITY MANAGEMENT NETWORKS
The simplest way to ensure that all ecosystems and species are represented
in areas managed for biodiversity is to designate several areas for each species or
ecosystem. Given sufficient time, local populations or ecosystems will experi-
ence catastrophic stochastic events. Species persist because populations else-
where escape these events (Goodman, 1987). This strongly argues for multiple
representation of species or ecosystems throughout their geographic range. Tear
et al. (1993) suggest protecting at least three viable examples of each element of
biodiversity (e.g., vegetation type, species) within each ecoregion.
Evidence from the study of island biogeography further suggests that only
large areas will maintain anything like their original complement of species over
evolutionary time. Barro Colorado Island, with an area of 16 km2, has lost one-
fourth of its species since its isolation in 1914 (Wilcox, 1980). Brown (1986)
suggests that areas smaller than 500 km2 are likely to lose more than half their
species in a few thousand years.
There is a practical limit to the amount of land that any nation can manage
primarily to maintain biodiversity (Pressey, 1990). The need for relatively large
areas for management of biodiversity (e.g., >500 km2) demands that those areas
be maximally efficient in capturing all species and ecosystems. It simply is not
possible to designate an appropriately large area (let alone several areas) for
management of each and every species and ecosystem. By taking advantage of
the fact that examples of many ecosystems occur in close proximity to one an-
other and that species ranges overlap, it is possible to identify a subset of areas
in which most elements of biodiversity are represented.
Pressey et al. (1993) articulate three principles for selecting reserve net-
works: (1) complementarity: the greatest efficiency in adding species or com-
munities to a set of areas will be achieved if the areas are maximally different (or

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GAP ANALYSIS / 335

complementary); (2) flexibility: there are usually alternative areas that can add
particular species or communities to a reserve network, therefore the selection
process is somewhat flexible; and (3) irreplaceability: some elements of bio-
diversity will occur only in one area, therefore these areas must be a part of any
completely representative biodiversity management network—they are irre-
placeable.
Considerable progress on quantitative approaches to efficient selection of
reserve networks using iterative algorithms has been made in Australia (Bedward
et al., 1992; Margules, 1989; Nicholls and Margules, 1993). A simple reserve
selection algorithm identifies the area with the most species or types of vegeta-
tion, then the area with the most species or types of vegetation not represented
in the first choice, and so on. In some cases, it is more efficient to use an algo-
rithm that selects the area with the rarest element first, then the area with the
next rarest element that also contains the largest number of other elements, and
so on (Pressey and Nicholls, 1989). Iterative algorithms can be extended to
insure that each element (species or ecosystem) is represented a number of times
(once, twice, three times, etc.).
Similar results can be obtained if all possible combinations of two, three,
four (and so on) areas are examined to identify those combinations that capture
the most diversity at each step (Figure 22-8). This analysis (an example of an
exact set coverage problem; Pennisi, 1993) identifies a family of areas, one of
which is selected at each step. It also presents a more difficult computational
problem and can be calculated for only a small number of steps for state or
regional data sets. For example, for the state of Idaho, there are 25.3 x 10 13
possible combinations of 389 hexagons taken 7 at a time.
While maximizing species richness (or diversity of types of vegetation) at
each step in a selection process can lead to an efficient reserve network (Scott et
al., 1987; Terborgh and Winter, 1983), some species may not occur in centers of
richness. An area may contain relatively few species but still be a necessary part
of a completely representative biodiversity management network due to the
presence of species not found in other areas. Kareiva (1993), Prendergast et al.
(1993), and Saetersdal et al. (1993) have pointed out that centers of species rich-
ness for different groups, such as birds and butterflies, may not coincide (see
also Robbins and Opler, Chapter 6 in this volume). The analysis of data layers is
therefore a complex process, proceeding hierarchically from the community level
of organization to complementary areas of high species richness and finally to
species still not represented. Separate analyses for major taxonomic groups or
ecoregions may identify priority areas with higher internal diversity than an
analysis of all species throughout a political unit, where earlier choices are domi-
nated by the taxon with the most species (i.e., birds) and later choices add only
a few species but are otherwise redundant with earlier choices.
Because most species or plant communities occur in more than one area, the
analysis itself becomes iterative. As an element of biodiversity occurs in more

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336 / BIODIVERSITY II

FIGURE 22-8 An exact set coverage algorithm identified four 635 km 2 areas in Idaho in
which underrepresented species in existing reserves are predicted to occur. One choice
from each of the four families will yield a set of four hexagons in which 97% of unpro-
tected species are predicted to occur. Hexagon boundaries are arbitrary and are disre-
garded when designing boundaries for biodiversity management.

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GAP ANALYSIS / 337

management areas, the priority of other areas which contain that element is
reduced. Other factors can be used to assign priority among management areas,
including threat, proximity to other areas (Nicholls and Margules, 1993), and
taxonomic distinctness (Faith, 1994; Vane-Wright et al., 1991). Pressey and
Bedward (1991) and Stoms (1994) have pointed out the influence of scale on
biodiversity analysis. Determining the optimally sized subunits of a region for
analysis remains an important research issue in conservation evaluation.
Predicting the biological value of priority areas for managing biodiversity
is an efficient first step toward developing a conservation strategy. It must be
followed by field reconnaissance to verify the value and condition of each area
and to apply the principles of conservation biology to boundary delineation.
Patterns of land ownership and economic activities affect the potential of man-
aging any particular area solely for biodiversity and can be factored into the
iterative process of building a reserve network.

AN EXAMPLE FROM IDAHO

The distribution of 119 types of vegetation and 357 species were mapped
for the Idaho gap analysis. The representation of types of vegetation in man-
aged areas is discussed elsewhere (Caicco et al., 1995). An analysis performed by
A. R. Kiester (U.S.D.A. Forest Service, Forestry Sciences Laboratory, Corvallis,
Oregon) determined that 49 terrestrial vertebrates were inadequately repre-
sented on existing managed areas in Idaho. Species were defined as inadequately
represented on existing managed areas if they occurred less than three times on
at least 10,000 contiguous hectares of land managed primarily for native species
and natural ecosystems. The state was divided into 635 km2 hexagonal sam-
pling units following White et al. (1992). An exact set coverage algorithm iden-
tified 119 combinations of 4 hexagons in which 47 of 49 unprotected species
were represented (Figure 22-8). Predicted distributions of unprotected species
need to overlap hexagon boundaries only slightly to be assigned to a hexagon;
therefore, actual areas that would support viable populations of these species
will differ considerably from hexagonal sampling units. Analyses of the same
data set using different definitions for unprotected species or different sample
unit sizes are expected to identify somewhat different priority areas. The analy-
sis presented here is one of many that can be integrated into a flexible conserva-
tion strategy for a completely representative network of areas that can be man-
aged for the long-term maintenance of biodiversity.

ACKNOWLEDGMENTS
We thank Christopher R. Margules and Robert L. Pressey for their com-
ments on Australian approaches to conservation evaluation. Bart R. Butterfield
developed distribution maps for species in Idaho (Figures 22-5 and 22-6), and A.

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338 / BIODIVERSITY II

Ross Kiester carried out the exact set coverage analysis for Idaho that is illus-
trated (Figure 22-8).

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Austin, M. P., and C. R. Margules. 1986. Assessing representativeness. Pp. 45-67 in M. B. Usher,
ed., Wildlife Conservation Evaluation. Chapman and Hall, London. 394 pp.
Bedward, M., R. L. Pressey, and D. A. Keith. 1992. A new approach for selecting fully representa-
tive reserve networks: Addressing efficiency, reserve design and land suitability with an itera-
tive analysis. Biol. Conserv. 62:115-125.
Brown, J. H. 1986. Two decades of interaction between the MacArthur-Wilson model and the
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CHAPTER
23

Conservation of Biodiversity
in Neotropical Primates

JAMES M. DIETZ
Assistant Professor, Department of Zoology, University of Maryland, College Park

In 1986, the year of the National Research Council and Smithsonian Insti-
tution’s National Forum on BioDiversity, compilations were published on the
distribution and conservation status of most neotropical primates. These con-
tributions, largely the effort of Russell Mittermeier (then of World Wildlife
Fund, now of Conservation International), established regional and taxonomic
priorities for conservation and research initiatives on neotropical primates
(Mittermeier, 1986a,b; Mittermeier and Oates, 1985).
Since that time, considerable progress has been made in our understanding
of the biology of neotropical primates and in the application of appropriate con-
servation methods to ensure that these species will survive to be considered in
future biodiversity symposia. In this chapter, I select a few examples from the
recent literature to illustrate progress in our understanding of neotropical pri-
mate biodiversity in the contexts of geographic distribution and taxonomy, habi-
tat evaluation, studies on ecology, evolution and behavior, and conservation
strategy. For each of these areas, I also identify important topics for future
research and development.

SYSTEMATICS, PHYLOGENY, AND GEOGRAPHIC DISTRIBUTION

New World primates, called platyrrhines because of their flat noses and
widely spaced nostrils, are thought to have evolved as forest dwellers, never
descending to occupy the terrestrial niches widely used by Old World primates.
The split between Old and New World primates took place some 40 million

341

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years ago (Rosenberger, 1992) and resulted in an extremely diverse array of

platyrrhines at all taxonomic levels.
Most authorities recognize 16 extant platyrrhine genera, including Ateles
(spider monkey), Brachyteles (muriqui), Lagothrix (wooly monkey), Alouatta
(howler monkey), Pithecia (saki), Chiropotes (bearded sakis), Cacajao (uakari),
Aotus (owl monkeys), Callicebus (titi monkey), Cebus (capuchin monkey),
Saimiri (squirrel monkey), Cebuella (pygmy marmoset), Callithrix (marmosets),
Leontopithecus (lion tamarins), Saguinus (tamarins), and Callimico (Goeldi’s
monkey) (review by Rosenberger, 1981).
In contrast with the general concordance of reviewers working at the genus
level, considerable disagreement exists among authorities working at higher
taxonomic levels (see reviews by Mittermeier and Coimbra-Filho, 1981, and de
Vivo, 1991). Traditional classifications divided New World primates into “mar-
mosets” or “callitrichids” and “nonmarmosets” or “cebids,” in which the mar-
moset patterns of morphology were seen as primitive and those of cebids as
advanced (e.g., Hershkovitz, 1977). In a 1986 revision, Ford reorganized recent
platyrrhine genera using a cladistic approach. In 1992, Rosenberger of the Na-
tional Zoological Park, Smithsonian Institution, launched a new synthesis based
on phylogenetic relationships, adaptive change, and the fossil record. He recog-
nized four monophyletic subfamilies in that classification. Callitrichids became
callitrichines, closely related to squirrel monkeys and capuchins (Cebinae).
Many features of callitrichines are now thought to have resulted from selection
for small size and thus are derived and not ancestral or primitive traits.
Identification of the phylogenetic link between the Cebinae and Calli-
trichinae was made possible by the discovery of a new set of fossils at La Venta,
Colombia, with morphological characteristics intermediate between those of the
two subfamilies (Rosenberger, 1992). The rate of description of fossil platyr-
rhine genera has increased markedly in recent years. Of 16 known fossil genera,
7 were described since 1985 and 4 of these since 1990 (Fleagle and Rosenberger,
1990). Our understanding of phylogenetic relationships and extinctions of
neotropical primates certainly will continue to improve if the trend toward in-
creased description of fossil forms continues.
New advances in molecular genetic techniques now make it possible to ob-
jectively test hypotheses about the phylogenetic relationships among the platyr-
rhines. The Brazilian geneticists Maria Sampaio and Horácio Schneider exam-
ined sequences of DNA in nuclear globin genes and found close relationships
between Alouatta and the atelines (Ateles, Brachyteles, and Lagothrix), between
Cebus and Saguinus, and among Pithecia, Chiropotes, and Cacajao (Schneider et
al., 1993), adding additional support to the phylogenetic model developed by
Rosenberger.
Much of what we know about the diversity of neotropical primates at the
species level is due to the painstaking descriptive detail provided in the pub-
lished works of Hershkovitz (e.g., Hershkovitz, 1977). That author and a few

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CONSERVATION OF BIODIVERSITY IN NEOTROPICAL PRIMATES /

343
others generally used pelage and cranial descriptions to classify the majority of
extant species of neotropical primates. However, there has been considerable
recent controversy about the criteria used in assigning species status to many of
these forms (e.g., Forman et al., 1986, for Leontopithecus spp.; Rylands et al.,
1993, for the Callitrichidae; Coimbra-Filho, 1991, for Leontopithecus caissara; and
Meireles et al., 1992, for Callithrix spp.).
Geographic ranges of many forms have been altered by recent anthropo-
genic habitat modification. As a result, correlations between patterns of geo-
graphic distributions and morphological characteristics become increasingly dif-
ficult to interpret. The biological accuracy of taxonomic designations becomes
particularly important because legislative protection and conservation funding
for full species is significantly greater than those for subspecies (e.g., Ryder,
1986). In addition, conservation objectives of reintroduction and translocation
of isolated populations are predicated on the conservation of genetic diversity
within a species. If genetic management is to have its desired effect in situ, it is
imperative that we be able to distinguish conspecifics from less closely related
forms. Revision of neotropical primates at the species level should be given high
priority, both in terms of contributions to primate conservation and basic re-
search. Recently developed noninvasive genetic techniques such as sequencing
of mitochondrial DNA extracted from hair follicles of museum specimens (e.g.,
Woodruff, 1993) may make it possible to resolve some of these controversies.

Golden Lion Tamarin group in Brazilian rainforest.

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Living neotropical primates are found from central Mexico to northern Ar-
gentina and include some 68 species, comprising about one-third of all living
species of primates (Mittermeier, 1986b; Mittermeier et al., 1992). In the mid-
1980s, much emphasis was put on identification of major phytogeographic re-
gions that contained relatively large numbers of primates, particularly rare, en-
dangered, or endemic species (Mittermeier, 1986a,b; Mittermeier and Cheney,
1986). These analyses resulted in maps of priority areas for primate conserva-
tion and research. For example, the Brazilian Atlantic forest reportedly con-
tained 6 genera and 15 species of primates, including 2 endemic genera and 9
endemic species, all of which were considered in danger of extinction
(Mittermeier, 1986b).
In the past 3 years, four new species of primates were described in Brazil:
Cebus kaapori (Queiroz, 1992), Callithrix mauesi (Mittermeier et al., 1992), and
Callithrix nigriceps (Ferrari and Lopes, 1992), all from the Amazon region; and
Leontopithecus caissara (Lorini and Persson, 1990), found not far from the large
cities of Curitiba and São Paulo. The discovery of four unknown primates in
such a short period of time, including one species in the backyard of one of the
largest cities in the world, underscores how little we really know about the
diversity of even well-studied taxa such as nonhuman primates and emphasizes
the need for more basic research and surveys on primates in the Neotropics.
However, if conservation efforts on behalf of any species of primates are to
succeed, it will be necessary to go beyond the identification of its geographic
distribution and taxonomic relationships with other primates. Among other
things, we will need a reliable estimate of how many individuals of that species
remain in the wild and information about their population structure. Pioneers
in Brazilian primatology, such as Coimbra-Filho, recognized decades ago that
the geographic distribution of golden lion tamarins and other Atlantic forest
primates had been reduced to small and degraded forest fragments (e.g.,
Coimbra-Filho, 1977).
Although biologists have been conducting censuses of neotropical primates
for decades, lack of standardization of methods and the difficulty of observing
primates in closed forest has made it difficult to assess the accuracy of the
results of these surveys. Nonetheless, numbers of many neotropical primates
appear to be decreasing. For example, in 1969, the Brazilian conservationist
Alvaro Aguirre estimated that 2,000-3,000 muriquis (Brachyteles arachnoides)
survived in Brazil’s Atlantic forest (Brownlee, 1987). In the mid-1980s, the mini-
mum number of muriquis known to exist in 10 locations was published as 240
(Mittermeier, 1986b). However, it was not until 3 years ago—when Kierulff
(1993), a Brazilian graduate student, used play-backs of golden lion tamarin
(Leontopithecus rosalia) vocalizations in virtually every forest that might contain
these primates—that an accurate estimate of the number of individuals in the
wild became known. This, the first exhaustive census for any neotropical pri-
mate, suggested that only 559 individuals in 103 groups remain in the wild and

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CONSERVATION OF BIODIVERSITY IN NEOTROPICAL PRIMATES /

345
that the species is subdivided into 16 isolated subpopulations, 12 of these con-
taining only 1 group. The accurate nature of this information removed any
question about the degree of threat to this species and prompted significant
changes in the focus of conservation and related research activities.

MONITORING CHANGES IN QUANTITY AND QUALITY OF HABITAT

In 1986, critical regions for conservation of neotropical primates were iden-
tified as huge phytogeographic areas such as the Amazon basin and “mega-
diversity countries” (Mittermeier, 1986b) that contained a large diversity of pri-
mate taxa. Since that date, our ability to pinpoint regions for conservation has
improved markedly. In 1990, approximately 100 specialists on Amazonian
fauna, flora, soils, and climate met in Manaus, Brazil, to produce a map of bio-
logically important regions in the Amazon Basin based on criteria of endemism,
rarity, and diversity. Important here is the diversity of specialists contributing
information and the speed with which the results were disseminated.
Perhaps the most significant recent advance in our ability to quantitatively
evaluate primate habitat is the combination of remote-sensing technology and
geographic information system (GIS) analysis. A decade ago satellite images of
regions of South America were expensive, difficult to acquire, and could be
analyzed in only a very few locations. Currently, a variety of high-quality,
inexpensive magnetic image data are available from several sources and cover
virtually every region on Earth. Recent improvements and reduction in price of
hand-held geographic position system (GPS) equipment now allow a researcher
to precisely determine latitude and longitude for samples of habitat, thus simpli-
fying the ground-truthing (verifying the interpretation of images obtained via
remote observation devices in local habitats) of satellite data. Desk-top com-
puter versions of GIS software make it possible to conduct sophisticated habitat
analyses without acquiring specialized equipment. New techniques such as gap
analysis (Scott et al., 1993, and Chapter 22, this volume), which evaluate the
protection status of plant and animal communities by GIS overlay of distribu-
tional data on maps of existing protected areas, help conservationists to be pro-
active rather than reactive in their efforts to preserve biodiversity.
The accessibility of satellite data and new analytical techniques (Sader et
al., 1990) resulted in three large steps forward in terms of establishing conserva-
tion and research priorities in the Neotropics. First, we now are able to quantify
changes in vegetation patterns over time. For example, in the 1980s, wide-
spread disagreement over rates of deforestation in the Brazilian Amazon ham-
pered efforts at international collaboration in conservation (reviewed in Skole
and Tucker, 1993). In the 1990s, independent reports by Brazilian and Ameri-
can scientists agreed that previous estimates were several-fold larger than actual
rates of deforestation (Skole and Tucker, 1993). Since future treaties on bio-
diversity and climatic change are likely to require countries to limit their emis-

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346 / BIODIVERSITY II

sions of greenhouse gases, including those resulting from deforestation, esti-

mates of deforestation based on satellite data acquire additional political and
economic importance.
Second, we now can use satellite data to test hypotheses about the effects of
anthropogenic factors on habitat quantity and quality. For example, we can use
archival data to document habitat changes that followed the construction of a
road into a forested area in the Amazon and subsequently use that information
to predict how a proposed road might alter undisturbed forest in another re-
gion. Third, based on any criteria that can be mapped (e.g., forest type, socio-
economic variables, or distance from villages), it is now possible to quantita-
tively evaluate areas for creation as reserves, annexation to reserves, or as
corridors between reserves (Figure 23-1). Remote sensing and GIS techniques

FIGURE 23-1 False color composite of data from Landsat’s Thematic Mapper showing
original boundary (black line) of Una Biological Reserve, Bahia state, Brazil, and forest
tracts purchased and annexed to the Reserve through international collaborative efforts
(green line). Dark brown represents areas covered by dense forest, yellow is secondary
forest, blue is areas that have been recently cleared, and white and black are clouds and
their shadows. Satellite data were acquired from Brazil’s Instituto Nacional de Pesquisas
Aeroespaciais by WWF-Brazil. The image was produced by R. DeFries and D. Van Wie,
Deptartment of Geography, University of Maryland.

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CONSERVATION OF BIODIVERSITY IN NEOTROPICAL PRIMATES /

347
are becoming increasingly powerful research tools and should be included in
the tool kit of any researcher or conservationist doing field work on neotropical
primates.

FIELD STUDIES ON ECOLOGY, EVOLUTION, AND BEHAVIOR

Hundreds of scientific reports have been published in the past decade on
the ecology and behavior of neotropical primates. I have selected a few ex-
amples to illustrate three categories of field research that have been particularly
useful from a conservation perspective: field research using the comparative
method, long-term demographic studies, and research addressing the effects of
human disturbance factors on primate population size and structure.
Although the principles of evolutionary biology should be useful in ex-
plaining primate behavior, primates rarely have been at the forefront in this
work (Richard, 1981). Cheney et al. (1986) identify several reasons why pri-
mates are rarely used to test evolutionary theory. Most species of primates are
difficult to identify individually or even to observe under field conditions.
Many species are so long-lived that accumulation of data on life histories may
require decades of observation. In addition, the social behavior of
many species is sufficiently complex that it becomes difficult to collect informa-
tion on a sufficient number of individuals to obtain a complete picture of pat-
terns of social organization (Dunbar, 1986). Seasonal and annual variation fur-
ther complicates the design of field studies examining the effects of ecological
variables or the adaptive significance of specific behaviors in tropical ecosys-
tems. Finally, formulation of generalizations often is impeded by differences in
researchers’ methodology.
One approach that has proved useful in circumventing these obstacles is to
ask how several primate taxa behave under the same circumstances and when
the same observational methodology is used. Conclusions then may be inferred
from differences between species. This comparative approach has the added
advantage of focusing on an interesting question rather than on an interesting
primate.
A good example of the comparative method applied to field research on
primates is Terborgh’s (1983) long-term study of the comparative ecology of five
New World primates in Manu National Park, Peru. Comparisons across species
allowed Terborgh to make inferences about, for example, the function of territo-
rial defense, factors that influence size of the group, and the relationship be-
tween size of the group and the social system in primates. Another fruitful
comparative study was conducted by Peres (1993) at a remote site in Amazonas,
Brazil. Peres compared the feeding ecology and habitat use of 13 primate species
for a period of 20 months. The comparative method allowed Peres to conclude
that seasonal migrations by several species living in large groups were the result
of “bottlenecks” in food availability in their habitats.

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An interesting example of the comparative method is the comparison of

wild- and captive-born reintroduced golden lion tamarins on private property
adjacent to Poço das Antas Reserve, Rio de Janeiro, Brazil (Beck et al., 1991).
Parallel studies of native and reintroduced tamarins allowed researchers to gen-
eralize about the effects of captivity on locomotion, communication, range use,
foraging, and reproduction. Ninety-one tamarins were introduced between 1984
and 1991, and were closely monitored by local observers. Thirty-three survived
until June, 1991, and 57 infants were produced. Deficits in food-finding, orien-
tation, and locomotion, which ultimately caused most losses of reintroduced
tamarins, were less severe in their wild-born offspring than in the originally
introduced individuals (Beck et al., 1991).
A second approach that has proved useful both in terms of basic research
and conservation application is long-term monitoring of demographic variables
for a single primate population. During the past decade of study on golden lion
tamarins in Poço das Antas Reserve, researchers individually marked 80% of
the tamarins in the reserve and these became habituated to the presence of hu-
man observers. Continuous monitoring of all births, deaths, emigrations, and
immigrations in 22 study groups allowed the researchers to compare average
fecundity and survivorship for tamarins following specific behavior patterns,
e.g., males that emigrate at an early age from the natal group versus those that
remain as nonreproductive helpers (Baker, 1991; Baker et al., 1993; Dietz and
Baker, 1993; Dietz et al., 1994a). The conservation implications of these data are
discussed below.
Calculation of reproductive success under field conditions can be problem-
atic, particularly for species of primates in which more than one male copulates
with a reproductive female. Under these circumstances, new molecular genetic
techniques, notably DNA fingerprinting, may allow paternity exclusion (identi-
fication of which males did not father the offspring in question) and thus direct
determination of male reproductive success (reviewed in Martin et al., 1992).
It long has been thought that deforestation and hunting have negative ef-
fects on most primate populations. However, the effects of these and other
anthropogenic factors rarely have been quantified for neotropical species. In
recent reviews of the impact of habitat disturbance on a variety of species of
primates, Johns (1991) and Johns and Skorupa (1987) reported that body size
and degree of frugivory were negatively correlated with a species’ probability
of survival. Redford and Robinson (1991) surveyed the available literature and
predicted that hunting by humans would cause primate population density to
decrease as prey body mass increases. Freese et al. (1982) surveyed primate
densities in Bolivia and Peru and suggested that predation by humans was the
most important factor affecting primate densities. Peres (1990, 1991) used
transect censuses of primates in hunted and unhunted areas to test hypotheses
about the effect of hunting on primate densities. Peres found that body size
alone largely determined the choice of primates hunted in Amazonian forests

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and that large species, such as woolly monkeys (Lagothrix lagotricha), often were
hunted to extinction in areas near human settlements, even in the absence of
habitat disturbance. Redford (1992) reached similar conclusions for a variety of
large animals in neotropical forest. Two conclusions are suggested by these
studies. First, conservation efforts need to focus on large-bodied primates with
low rates of reproduction, even before habitat destruction begins. Second, past
and present hunting pressure must be included in calculating population dy-
namics of large-bodied primates, even in areas of apparently intact habitat.

CONSERVATION STRATEGIES
The alarm that sounded in the mid-1980s about the immediate threat to
most species of neotropical primates was answered in a number of ways. I have
classified these strategies as information management and networking, applica-
tion of scientific method, captive breeding, conservation education, and inter-
national collaboration.

Information Management and Networking

The advent of wide-spread use of electronic mail dramatically increased the
speed and decreased the cost of international communication. Transfer of data
files, even from remote field stations, has become routine in the past few years.
Computerized bulletin boards are available on a number of relevant topics, in-
cluding conservation biology, primates, ecology, the Neotropics in general, as
well as several tropical countries.
Many international nongovernment conservation organizations (NGOs) sup-
port regional programs to develop and conduct conservation and research ac-
tivities in neotropical countries. Some of these initiatives, e.g., the Golden Lion
Tamarin Conservation Program in Brazil, which has been supported for 10 years
by grants from the World Wildlife Fund and other NGOs, focus on conservation
of primates and their habitat. The Nature Conservancy sponsors the establish-
ment of Conservation Data Centers in 13 Latin American and Caribbean coun-
tries to aid in decision-making in conservation and sustainable development.
Conservation International supports a Rapid Assessment Program in which teams
of experts census diverse taxa of fauna and flora to set priorities for conserva-
tion action.
Several scientific journals and newsletters reporting on topics relevant to
conservation of neotropical primates have appeared in the past decade, and some
of these include articles or abstracts in Spanish or Portuguese. Examples in-
clude Neotropical Primates (newsletter of the IUCN/Species Survival Commis-
sion Primate Specialist Group), CBSG News (newsletter of the Captive Breeding
Specialist Group), Conservation Biology (journal of the Society for Conservation
Biology, Blackwell Press) and Boletim da Sociedade Brasileira de Primatologia
(bulletin of the Brazilian Primatological Society).

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350 / BIODIVERSITY II

Application of the Scientific Method

The past decade has seen a heartening increase in the generation of conser-
vation theory and the application of rigorous scientific method and problem-
solving techniques to conservation questions. Graduate degrees in conserva-
tion biology now are offered at many universities in the United States and
Europe (reviewed in Jacobson, 1990, and Jacobson et al., 1995). The National
Science Foundation now funds grant proposals in conservation and restoration
biology.
Although the primary concern of conservationists is the survival of ecosys-
tems, much of the theoretical and applied research in conservation biology is
conducted at the population level. The link between population and ecosystem
conservation is thought to be the appropriate selection of populations of “flag-
ship species” that serve as the focus of conservation campaigns, “umbrella spe-
cies” that have ranges large enough to include significant portions of natural
ecosystems, and “keystone species” whose presence or absence determines the
abundance and distribution of a number of other species. Appropriate selection
of populations for conservation can conserve habitat and associated biodiversity
effectively. The charismatic nature and ecological role of many neotropical pri-
mates makes them well-suited to be flagship species (reviewed in Dietz et al.,
1994b).
A new approach to determining conservation action plans at the population
level is the Population Viability Analysis or Population and Habitat Viability
Analysis (PVA or PHVA; reviewed in Foose et al., 1995). This concept is predi-
cated on the need to establish quantitative conservation goals for the population
under study, e.g., a 95% probability of survival over a period of 100 years.
Computer models such as VORTEX (Lacy, 1993) are used to estimate the prob-
ability of population extinction and time to extinction, based on the effects of
stochastic events such as inbreeding, environmental variation, and catastrophes
on population demographic variables. The probability of survival of multiple
subpopulations in a metapopulation also may be estimated (Gilpin and Hanski,
1991). Examples of PHVA applied to four species of lion tamarins are presented
in Seal et al. (1990).
The advantages of PHVA include the simultaneous treatment of several vari-
ables, the collaborative process by which the best available information is as-
sembled for all interested parties, the quantitative nature of the results, and the
versatility in evaluating management options. The shortcomings of PHVA are
related to the assumptions implicit in the computer model and the effects of
estimating unknown values. For example, the impact of environmental varia-
tion on fecundity and survivorship rarely is known for populations in nature.
Small changes in the specified effects of environmental variation on reproduc-
tion or mortality can produce 10-fold differences in the predicted probability of
extinction of the population.

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CONSERVATION OF BIODIVERSITY IN NEOTROPICAL PRIMATES /

351
Captive Breeding and Reintroduction
Not long ago, zoos were seen as consumers of primates and other animals,
competing to assemble a collection of the rarest and most valuable examples for
public exhibit. Recent changes in the objectives of modern zoological parks
make these institutions important contributors to in situ conservation of neo-
tropical primates. The principal objective of captive propagation now is seen as
the reestablishment or reinforcement, not replacement, of wild populations
(Ballou and Cooper, 1992). With over 13,000 specimens in zoological collec-
tions, primates are overrepresented relative to other mammalian orders. Never-
theless, only about 50% of primate taxa are represented in captivity (Magin et
al., 1994). International management committees, organized to maximize reten-
tion of genetic diversity and minimize probability of extinction in captivity and
the wild, are increasing for many vertebrate taxa, including primates.
A number of advisory groups work to coordinate the ex situ and in situ
primate conservation activities of zoos. The Species Survival Commission (SSC),
consisting of world experts on approximately 100 taxa or conservation topics, is
the main source of advice to The World Conservation Union (IUCN) regarding
the technical aspects of conservation of species. The SSC promotes action on the
part of the international conservation community on behalf of species threat-
ened with extinction and those important for human welfare. Two SSC Special-
ist Groups are particularly important for primate conservation: the Primate Spe-

Golden Lion Tamarin feeding.

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352 / BIODIVERSITY II

cialist Group, comprised of about 200 experts working in the conservation of

primates, and the Captive Breeding Specialist Group, whose objective is the con-
servation or establishment of viable populations of threatened species.
In 1992, a Taxon Advisory Group (TAG) to the American Association of
Zoos and Aquaria (AAZPA) was formed to coordinate and facilitate captive
breeding of New World Primates in support of in situ conservation efforts. Fau-
nal Interest Groups (FIGs) coordinate conservation activities in zoos for fauna
and flora from a specific geographic region, e.g., Brazil.
Studbooks, containing complete demographic records for a species in cap-
tivity, facilitate the scientific management of captive populations, e.g., by facili-
tating selection of appropriate individuals for pairings to reduce loss of genetic
diversity (reviewed by Ballou and Lacey, 1995; Lande, 1995). Studbooks are
maintained for 15 species of neotropical primates, and have been proposed for
several others. For a few species, information on native populations is sufficient
for inclusion in studbooks. For example, the studbook for golden lion tamarins
soon will include all individuals in the species: captive, reintroduced, and na-
tive subpopulations.
The reintroduction of captive-born neotropical primates has been initiated
for several species in the past few years. In addition to the reintroduction of
golden lion tamarins mentioned above, reintroduction and monitoring of Calli-
thrix geoffroyi (Geoffroyi’s marmoset) in Espirito Santo state, Brazil, began in
1991 (Chiarello and Passamani, 1993). The costs and criteria for success in a
primate reintroduction are reviewed by Kleiman et al. (1991). The IUCN-SSC
Reintroduction Specialist Group and the AAZPA Reintroduction Advisory
Group both were created in the past few years to facilitate in situ conservation
through integration of wild and captive population management.

Conservation Education
The role of community education in directing the attitudes and behaviors of
local peoples toward sustainable use of natural resources long has been recog-
nized as an essential component of any viable conservation strategy. This is
particularly true where charismatic species such as primates can be used as flag-
ships for conservation efforts (Dietz et al., 1994b). However, only in the past
few years have rigorous evaluation techniques been used to quantify the effects
of community education in primate conservation projects.
Illustrating the value of quantitative evaluation of community education,
educators conducted a survey after 2 years of activities related to the golden lion
tamarin conservation project and documented a significant increase in the per-
centage of respondents who recognized golden lion tamarins in a photograph.
Whereas 42.5% of these responses were attributed to project activities, only
6.9% reported seeing tamarins in the forest. The project activities that were
mentioned most often included television (14.9% of responses) and radio (6.9%

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CONSERVATION OF BIODIVERSITY IN NEOTROPICAL PRIMATES /

353
of responses), a total effect roughly equivalent to all other project activities com-
bined (Dietz and Nagagata, 1986; Dietz et al., 1994b). Graduate training in con-
servation education for South and Central American nationals is one of the best
investments that can be made to ensure the future of neotropical primates.

International Collaboration
A final example illustrates progress in international collaboration. In this
case, private lands were purchased and annexed to a Brazilian federal reserve
too small to guarantee the survival of an endangered primate. A PHVA for
golden headed lion tamarins (L. chrysomelas), conducted in the Una Biological
Reserve, southern Bahia State, Brazil (the only protected area containing that
primate), suggested that the probability of extinction of that primate was rela-
tively high (Dietz et al., 1994c; Seal et al., 1990).
Based on the findings of the PHVA, a coalition of eight international conser-
vation organizations conducted fundraising efforts to buy out squatters and
purchase land to annex to Una Reserve. Funds were transferred in several in-
stallments to Fundaço Biodiversitas, a Brazilian NGO, which purchased lands at
market price from local landowners and immediately conferred title to the Bra-
zilian agency responsible for administration of the Reserve. To date, the area of
the Reserve has been increased from 5,342 hectares to 7,059 hectares (Figure 23-
1; Coimbra-Filho et al., 1993). Cooperation that spans disciplines, agencies, and
nations is rare indeed, but if neotropical primates are to be conserved in nature
it will be through collaborative efforts of this type in which the world’s scien-
tific and economic resources can be brought to bear on the problem.

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CHAPTER
24

Using Marine Invertebrates to Establish

Research and Conservation Priorities

JAMES D. THOMAS
Curator of Crustacea, Department of Invertebrate Zoology,
Smithsonian Institution, Washington, D.C.

Current methods and applications used to identify and select coral reefs for
conservation efforts are seldom based on scientific methodology. Instead, pro-
tection efforts are focused on a series of coral reefs under direct or imminent
threat of impact or alteration, resulting in a reactive policy approach. What is
needed in light of current changes occurring in coral reef systems are programs
with a strong preventative component designed to establish research and con-
servation priorities in coral reefs before they come under significant levels of
threat. In this chapter, I outline inadequacies of current approaches to identify-
ing and managing biodiversity in coral reefs, recommend new ways to establish
selective criteria through taxonomic surveys and inventories, and provide an
example from a coral reef system of exceptional biodiversity in Madang Lagoon,
Papua New Guinea. While not visually spectacular, this reef system houses
remarkable levels of marine invertebrate biodiversity.

CORAL REEFS
Coral reefs have provided scientists with a rich source of facts and theory
and have helped to forge fundamental views on evolution, biodiversity, and
geology in the ocean realm. Scientists such as Darwin and Wallace recognized
distinct patterns in biological distribution of coral reef organisms and attributed
part of this pattern to geological events. With the acceptance of plate tectonic
theory and accurate radiometric dating, these patterns have assumed biogeo-
graphic importance. Tectonic plate movements over fixed mantle hotspots pro-
duce accurate plate circuitry measurements (Yan and Kroenke, 1993), producing

357

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358 / BIODIVERSITY II

linear volcanic arcs and island archipelagos that encode a history of past geo-
logical events. According to Pandolfi (1992), a correlation exists between bio-
geographic pattern and geological history, and modern marine distribution pat-
terns can best be interpreted by incorporating the geological history of the area
under study.
Numerous hypotheses have been proposed to explain patterns of bio-
diversity on coral reefs. These include dispersal models (Kay, 1984), the Pacific
plate vicariance theory (Springer, 1982), a “Pacifica” continental fragmentation
theory (Nur and Ben-Avrahm, 1977), an expanding Earth theory (Carey, 1958,
1976), and a variety of ecological explanations (Vermeij, 1990). However, the
systematic study of comparative levels of endemism in coral reef invertebrates
to see which paradigm, or combination of paradigms, best explains biogeo-
graphical patterns remains to be engaged by the scientific community. Funda-
mental knowledge of biodiversity at the level of species is a prerequisite for
such investigations.
Integrated studies of marine biodiversity are just beginning. To date, many
taxonomic and most biogeographic studies of reef systems have been random
and opportunistic, focusing on easily accessible islands. Taxonomic literature
on tropical marine invertebrates is scattered, dealing mostly with large, spa-
tially obvious components such as fish, scleractinian corals, and molluscs, and
thus creating a biological bias for larger organisms that may not be the best

Fish swarm over a coral reef.

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MARINE INVERTEBRATES / 359

indicators or measures of biodiversity (Thomas, 1992). Platnick (1992) refers to

the condition of concentrating on the obvious spatial components as the “mega-
fauna bias.” The most informative invertebrate groups in terms of biogeogra-
phy are those without a dispersive (pelagic) larval stage. Wide dispersal capa-
bilities can mask small-scale distribution patterns. Thus, animals with restricted
distributions more accurately reflect levels of endemism. Information on those
groups of invertebrates with restricted distributions is needed to integrate the
many competing hypotheses on distribution mechanisms.
While coral reefs contain the highest levels of biodiversity in any marine
ecosystem, virtually nothing is known about possible extinctions or natural
trends in biodiversity. World-wide reports of changes in coral reef systems are
largely anecdotal and based primarily on ecological research. Human impact is
suspected as a contributing factor in these changes, but the interaction of natu-
ral change versus human-induced impacts remains speculative (Roberts, 1988;
Williams and Williams, 1990). The rate at which marine areas now are being
designated for protected status as sanctuaries, refuges, preserves, parks, etc.,
creates a problem in setting priorities and selecting among the many candidates
suggested for protection. The goal of maintaining native levels of biological
diversity requires that knowledge regarding historical sources and levels of
biodiversity be known so that competent decisions about research, conserva-
tion, and management action can be made.

DISTINGUISHING TYPES OF BIODIVERSITY

Above the generic level, the marine environment is more diverse than ter-
restrial systems (Ray and Grassle, 1991), yet most of what we know about
biodiversity comes from studies in tropical moist forest systems. Biodiversity
studies in marine environments, particularly the tropics, suffer from diffusion
of scientific effort and an inability to identify critical sites based on biodiversity.
Present management and conservation efforts in marine systems are driven
mainly by concepts other than biodiversity, e.g., species of special human inter-
est, areas of spectacular natural beauty, and economics (Thomas, 1993). Such an
approach places the highest priority on unusual areas with regard to levels and
trends of biodiversity. In some instances where biodiversity surveys have been
conducted, emphasis is on “spatially obvious” organisms such as fish and corals
that may not be the best indicators to identify the processes of environmental
change (Angermeier and Karl, 1994).
Successful management of marine ecosystems must rely on relevant infor-
mation about levels and trends of biodiversity, information that is almost en-
tirely lacking in current management approaches. Biodiversity survey and in-
ventory programs that are are designed to identify and select those marine areas
of highest scientific value are needed. Resources such as existing collections in
natural history museums and coordination of ongoing taxonomic surveys and

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360 / BIODIVERSITY II

inventories need to be organized according to selective criteria. The limited

number of active field systematists and taxonomists currently working in ma-
rine environments must be deployed effectively. Training programs to allow a
wider dissemination of taxonomic expertise also are a critical element in a uni-
fied approach to marine biodiversity. Use of data from disciplines outside tax-
onomy and systematics must be incorporated into a marine biodiversity pro-
gram for the twenty-first century. Information from fields such as plate
tectonics, paleogeography, cladistics, ecology, and anthropology must be
brought together in concert to fully understand what is happening in marine
environments and what can be done to improve our understanding of system
processes. At the administrative level, specific shifts in policy goals to include
reliance on preventative rather than reactive management strategies must be-
come a priority (Angermeier and Karl, 1994).

TAXONOMY AND BIODIVERSITY IN CORAL REEFS

Available taxonomic data tell us more about varying attention given to dif-
ferent groups of animals, the “taxonomy of taxonomists,” than about the level
of taxonomic knowledge (May, 1994). The information summarized by May
(1994) illustrates the great disparity of attention received by different groups.
Roughly one-third of taxonomists work on plants, while the remaining two-
thirds spilt roughly equally between invertebrates and vertebrates. The esti-
mated total number of species of vertebrates is 40,000; species of plants is
300,000; and species of invertebrates is about 1 million (with estimates up to 10
million; Grassle and Maciolek, 1992). Therefore, for every n taxonomists work-
ing on vertebrates, there are 0.1n taxonomists investigating plants and 0.01n
taxonomists specializing in invertebrates. When we consider that a majority of
invertebrate taxonomists study a single group, the insects, the great disparity
within the current taxonomic work force that specialize in marine invertebrates
becomes apparent. Estimates of millions of new species, with an estimated nov-
elty rate of 40-80% for undescribed taxa, places an absolute accounting of all
marine species outside the realm of possibility in any time frame that would
make any significant difference in the current biodiversity crisis. I suggest that
what is needed is sufficient effort directed toward taxonomic inventories of se-
lected groups of bioindicators that are chosen by established taxonomic proto-
cols. Such a selection process would target not only areas that are threatened or
in crisis, but would incorporate objective scientific criteria to predict possible
centers of evolutionary diversification that act as genetic sources for existing
biodiversity (Thomas, 1992). Approaches that focus existing taxonomic exper-
tise on areas that may be historical sources of biodiversity will help us under-
stand how patterns of biodiversity at the level of species are maintained and
replenished.

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MARINE INVERTEBRATES / 361

DOCUMENTING BIODIVERSITY IN TROPICAL MARINE ECOSYSTEMS

Despite extensive reports of large-scale change in coral reef systems, the
scientific, conservation, and management community does not currently have
the capability to investigate every region or problem that gains public attention.
Lack of comprehensive marine biodiversity protocols to identify areas of
particular scientific, conservation, and management value have lead to a diffuse
approach to the systematic investigation of coral reef biodiversity. Most re-
search taking place now on reefs is ecological in nature, with little or no system-
atic effort directed toward taxonomic surveys and inventories of reef systems
world-wide. This lack of focus is further compounded by the shortage of expe-
rienced field systematists and taxonomists. Training programs that would in-
crease the number of personnel available for surveys and inventories on coral
reefs, while frequently discussed, have resulted in few active programs. The
need is especially acute for the marine invertebrates, particular groups of which
are sensitive indicators of change in coral reefs (Thomas, 1993).
The scientific community must develop a process to assess biodiversity that
uses selective criteria and sets priorities, in effect a form of “environmental tri-
age.” Every reef system cannot be investigated with current personnel and
levels of funding. Difficult choices must be made that maximize existing per-
sonnel, equipment, and organizational structure. Numerous coral reef sites al-
ready enjoy protected status, while numerous additional sites are being sug-
gested for protection. In many cases, the site selection process is driven from a
perception that a particular site is in a stressed or deteriorating condition. This
approach focuses limited resources on a series of crisis situations and perpetu-
ates a reactive management posture. Ideally, the scientific community should
provide theoretical guidance and taxonomic information regarding appropriate
site selection. The conservation community, capable of rapid response and adept
at raising public awareness, then should use scientific data to target specific
sites or regions for protection. The resource management community does not
become established until an administrative structure is created. Every effort
should be made to incorporate high-quality science in management approaches
that document biodiversity. Coral reef sites that enjoy preexisting protected
status should be encouraged to adopt programs that adequately document levels
of biodiversity if such information is lacking. These major groups—scientists,
conservationists, and resource managers—must work in concert along estab-
lished guidelines to maximize the application of diffuse resources and funding
to help identify and protect coral reefs.

ESTABLISHING PRIORITIES IN MARINE BIODIVERSITY

Priorities vary depending on individuals, agencies, and processes involved.
For example, taxonomists place the highest priority for research on reefs that

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362 / BIODIVERSITY II

contain the highest biodiversity at the level of species or are the least impaired
or impacted by man. Conservation groups may target areas that house species of
special interest or support high proportions of endemics, while resource manag-
ers might focus on reef areas that seem threatened by human impacts. It must be
emphasized that most coral reef systems, except for limited areas in the Carib-
bean and the Great Barrier Reef in Australia, are claimed by developing coun-
tries with little or no scientific or administrative resources. Therefore, any sys-
tem of establishing priorities must take into account a variety of factors.

Developing Selection Strategies

The following approaches should be employed to develop priorities for
marine biodiversity initiatives:
(1) Identify centers of evolutionary diversification, or major centers of ge-
netic biodiversity by surveys and inventories, existing museum collections, and
cladistics.
(2) Target areas where geological history indicates a history of vicariant
events that might lead to high levels of endemic species or areas of composite
biodiversity.
(3) Implement surveys and inventories to determine biodiversity baselines.
While entire protected areas must be surveyed initially, ongoing monitoring of
biodiversity could be restricted to special protected areas, such as replenish-
ment zones located within a protected area (Bohnsack, 1993). It is important to
stress that our understanding of biodiversity in coral reefs is rudimentary; there-
fore, initial surveys must incorporate a representative cross section of the entire
area. Once levels of biodiversity have been determined, decisions can be made
as to the location of permanent monitoring sites and schedules.
(4) Publish comprehensive identification guides to biota. Most information
regarding marine invertebrates from coral reefs is uneven in terms of taxonomic
and geographic coverage. Computer-based identification manuals should be a
priority for development and distribution.
(5) Establish parataxonomic training programs to augment survey and in-
ventory capabilities. Basic biodiversity surveys and inventories of many pro-
tected areas remain to be initiated and are not currently a primary management
concern. Two of the largest marine protected areas in the world, the Florida
Keys National Marine Sanctuary and the Great Barrier Reef Marine Park, Aus-
tralia, have yet to institute systematic biotic inventories, despite stated manage-
ment concerns to “monitor biodiversity.”

A Geological Frame of Reference for Biodiversity

The term “hotspots,” a geological term originally used to describe fixed
volcanic sources, has recently gained popularity in the biological sense to indi-

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MARINE INVERTEBRATES / 363

cate areas of high biodiversity. This unfortunate amalgamation of terminology

confuses the original use of the term. In this chapter, the term “hotspot” is used
in a geological context.
Recent efforts to test the hypothesis that geologic hotspots accurately record
the passage of lithospheric plates generally have shown it to be valid (Duncan,
1981, 1991; Duncan and Richards, 1991; Fleitout and Moriceau, 1992; Morgan,
1981, 1983). If hotspots indeed are fixed with respect to one another over sig-
nificant periods of geological time, then they would constitute an accurate frame
of reference that could be used to determine precise lithospheric plate move-
ment and allow reconstruction of plate positions back into time. Morgan (1981)
estimated that hotspots migrate less than 5 mm per year relative to each other.
Hotspot trails have been clearly delineated for the time span of zero to 100 mil-
lion years, thus allowing reconstruction of southwest Pacific tectonic elements.
This is done by first determining linkages between individual rifted continental
fragments and island arcs and then by assigning correct plate motion derived
from hotspot models, thus providing a “plate circuit” (Yan and Kroenke, 1993).
Such approaches to tectonic plate circuitry allow visualization of the complex
movements of plates through space and time. Yan and Kroenke (1993) provide
a CD-ROM that contains animated sequences of the southwest Pacific plate move-
ments from zero to 100 million years ago in 0.5-million year increments that
provides additional insight on how and when marine organisms may have dis-
persed or been constrained by various geological events over the last 100 million
years.

THE MADANG LAGOON, PAPUA NEW GUINEA

The island of New Guinea, composed of Papua New Guinea (PNG) and Irian
Jaya, is located on the leading edge of the Australian plate that has been moving
rapidly northward. The country of PNG comprises a landmass slightly larger
than California (457,000 km2). The north coast of PNG has been formed by
collision events along the north edge of the Australian plate and subsequent
“docking” of the east Papuan composite and other terranes (a series of continu-
ously related geological formations) in the mid-late Miocene 15-20 million years
ago (Pigram and Davies, 1987). I suggest that the composite marine fauna of the
Madang Lagoon is the result of the accretionary process along the north coast of
PNG, involving rapid volcanic uplift as islands, archipelagos, submerged pla-
teaus, and continental terranes are thrust rapidly upward in the collisional pro-
cess. This process differs from other areas of the circum-Pacific, where terranes
are predominantly of oceanic affinity.
This “docking” process introduced a number of previously discrete biotic
assemblages that then intermingled with established floral and faunal elements.
Reefs in the Madang Lagoon illustrate the importance of taxonomic data in
identifying areas of scientific concern. At first glance, the reefs in the Madang

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364 / BIODIVERSITY II

Lagoon appear “less spectacular” (in a visual sense) than their southern counter-
parts on the Great Barrier Reef. However, taxonomic surveys of marine inverte-
brates suggest that Madang reefs are some of the most biologically diverse reefs
yet documented. Sustaining native levels of biodiversity in these reefs as a
potential genetic seed source for other South Pacific reefs is important in the
larger context of regional biodiversity.

Marine Invertebrates of the Madang Lagoon

Over the past several years, increasing numbers of scientists have focused
their research efforts in the Madang Lagoon in an attempt to document the un-
usual levels of biodiversity found there. The following information summarizes
briefly some of the results and trends that have been documented. A more
complete discussion can be found in the Proceedings of the Seventh Interna-
tional Coral Reef Symposium (Richmond, 1992).

Scleractinian Corals. While much attention has been given to the sclerac-
tinian corals of eastern Australia (Veron and Pichon, 1976, 1979, 1982; Veron
and Wallace, 1984; Veron et al., 1977) the nature of reef corals from northern
New Guinea was not well understood due to lack of distributional data. Potts
suggests that the Madang Lagoon may prove to be the single most diverse site in
the world for scleractinian corals (Potts, personal communication, 1994).
Hoeksema’s recent treatment of fungiid corals (1992) represents the only reef
coral family on which detailed distribution and taxonomic data are available for
the Indo-Pacific region. According to Hoeksema (1992), northern New Guinea
appears to have the highest fungiid biodiversity (39 species), with a fauna most
similar to that of the Philippines and eastern Indonesia (37 species). Diversity in
eastern Australia was the next highest (31 species), followed by western Austra-
lia and Taiwan (26 species), northwest Java (25 species), southern Papua New
Guinea (24 species), and northeast Borneo (19 species). Hoeksema (1992) stresses
that the generic diversity of hermatypic corals in the Indo-Pacific region is quite
large, and that lists of genera are not as informative as species diversity and
monospecific genera. Because all taxonomic categories above the species level
are arbitrary, lists that include species and monospecific genera are more likely
to reflect evolutionary history, and thus allow for a more precise comparison of
biodiversity.

Octocorals. Winston (1988) estimates that only 50% of the octocoral fauna
from the Indo-Pacific region is known at present. Like most other marine inver-
tebrate groups, our basic taxonomic knowledge of the Indo-Pacific octocorals is
poorly known (Williams, 1992). A recently described species of octocoral from
the Madang Lagoon was unlike any species of the genus previously recorded
(Bayer, 1994).

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MARINE INVERTEBRATES / 365

Polyps of an organ pipe coral.

Amphipods. Thomas (1992) found that the amphipod fauna from coral
reefs of the Madang Lagoon exhibited exceptional levels of species diversity.
The amphipod fauna of Madang reefs is a composite, consisting of approximately
180 species, 60% of which are new to science and exhibit multiple biogeographic
affinities. The Madang Lagoon amphipod fauna is taxonomically distinct from
other South and Indo-Pacific sites, and the amphipod biodiversity on the north
coast of PNG likely exceeds that of any coral reef area studied thus far. How-
ever, many coral reef systems in the Indo-Pacific have never been systematically
analyzed for smaller crustaceans. The author suggests herein that future bio-
diversity inventories and surveys be undertaken with regard to selective crite-
ria. Due to the limited dispersion capabilities and habitat specificity of amphi-
pods, amphipods may be of use in biogeography and environmental monitoring
in coral reef systems.
Crinoids. Messing (1992) reported 39 species of comatulid crinoids from
the Madang Lagoon and, with limited sampling, found the crinoid fauna of the
Madang Lagoon comparable to other more intensively studied sites such as Liz-
ard Island and Davies Reef (Australia, Great Barrier Reef), and Palau.
Gastropod Molluscs. Working in the Madang Lagoon, Gosliner (1992)
found that the north coast of PNG supports a more diverse fauna of opistobranch
gastropods (538 species) than has been reported from any single geographical
area studied thus far. The next richest tropical site is Guam (395 species), fol-

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366 / BIODIVERSITY II

lowed by Hawaii (244 species), the Caribbean (232 species), and Japan (184 spe-
cies). Gosliner’s faunal records are significant because of intensive field efforts
in numerous tropical localities using snorkeling and SCUBA that enable com-
parative studies. Other areas that are known or suspected to house high diver-
sity have not been studied adequately to allow comparisons of opistobranch
biodiversity (Gosliner, 1992).
Other Biota and Habitats. Kristian Fauchald (personal communication,
1994) reported that the polychaete fauna of the Madang Lagoon exceeded that of
any area yet sampled. Clyde Roper and Mike Sweeney (personal communica-
tion, 1994) reported similar findings for cepahlopod molluscs. In a preliminary
survey of the marine algae of the Madang Lagoon, Mark and Diane Littler (per-
sonal communication, 1994) reported that not only were there more species of
algae collected, but the number of undescribed species surpassed that of any
region previously sampled.
The geological history that may have contributed to the extraordinary lev-
els of marine invertebrates in the shallow waters of the north coast of PNG also
may have influenced the fauna in deeper waters of the region. Studying a col-
lection of deep sea crustaceans from the Bismarck Sea region (1,200 m), Austin
Williams of the National Marine Fisheries Service Systematics Laboratory re-
ports unusual levels and types of biodiversity (personal communication, 1994).
More investigation of the deep sea component of this region is warranted in
light of this preliminary information.

SELECTING CORAL REEF SITES BY ATTRIBUTES

Most current approaches to protecting biodiversity place emphasis on ar-

eas or species of special human interest and natural beauty or areas with novel
biological features (endemics). Therefore, highest value is placed on unique
and unusual biota, with little regard to the nature and quality of biodiversity
on a larger scale. It is imperative to develop priorities using the geological past,
the nature of the ecosystem, the characteristics of the region, and the available
specialists.

Developing Action Strategies

The following tactics can be used to initiate biodiversity inventories in
marine areas of particular interest and importance:
(1) Initiate surveys and inventories that document biodiversity in those
areas (known or suspected to be) of extraordinary scientific or conservation
value as determined by a rigorous selection process.
(2) Establish biologically based monitoring programs using selected groups
of organisms that have an established reputation as bioindicators of high quality.

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MARINE INVERTEBRATES / 367

(3) Inventory existing historical collections from reef systems deposited in

natural history museums. Many museums house historical collections of organ-
isms from tropical regions. Such collections could serve as a “biodiversity
baseline.”
(4) Publish primary taxonomic monographs, identification guides, keys,
and manuals, especially computerized, graphically based manuals for nonspe-
cialists and resource managers.
(5) Develop parataxonomic training programs targeted for specific taxa and
geographic regions.
(6) Implement scientific taxonomic training programs coordinated through
a network of natural history museums, academic institutions, government agen-
cies, and other organizations.

SUMMARY
Oceanic islands and their associated coral reefs have provided scientists with
a wealth of biogeographic information. Levels of biodiversity on modern coral
reefs provide a window on past evolutionary events that detail the correlation
between biogeographic pattern and geological history. Reefs of the Madang
Lagoon in Papua New Guinea exhibit levels of biodiversity exceeding all other
reef systems studied thus far. Because of this, the Madang Lagoon represents a
scientific and conservation resource of the highest priority. While biodiversity
research on coral reefs is in its infancy, the need for this information is acute.
Within PNG, a complex pattern of land ownership combined with negli-
gible developmental pressures and resource exploitation have allowed the reefs
to remain relatively unaffected by anthropogenic impacts. That situation prom-
ises to change as the country seeks to modernize its largely subsistence economy
and as rich mineral deposits and timber resources are developed. The rugged top-
ography of the interior of the country virtually assures that the majority of this
developmental pressure and impact will be in the coastal region, adjacent to reefs.
The reefs of the north coast of PNG provide an unequaled opportunity to
study marine biogeography in what is probably a major source of biodiversity
for a large area of the South Pacific. Research and conservation efforts must be
focused on this invaluable biotic resource before significant impacts occur that
will affect yet unstudied and undocumented groups of organisms.

ACKNOWLEDGMENTS
The author wishes to thank the Christensen Research Institute in Madang
for research support on coral reef systems in and around the waters of Madang.
Former Director Matthew Jebb and current Director Larry Orsak graciously have
provided facilities and equipment to marine researchers working in the Madang
region.

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368 / BIODIVERSITY II

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Williams, G. C. 1992. Biotic diversity, biogeography, and phylogeny of pennatulacean octocorals
associated with coral reefs in the Indo-Pacific. Pp. 729-735 in R. Richmond, ed., Proceedings
of the Seventh International Coral Reef Symposium, Guam, Vol. 2. University of Guam Press,
Mangilao.
Williams, L. B., and E. H. Williams. 1990. Global assault on coral reefs. Nat. Hist. 4:47-54.
Winston, J. E. 1988. The systematists’ perspective. Pp. 1-16 in D. Fautin, ed., Biomedical Impor-
tance of Marine Organisms. Mem. California Acad. Sci. 13:1-157.
Yan, C. Y., and L. W. Kroenke. 1993. A plate tectonic reconstruction of the southwest Pacific, 0-100
Ma. Pp. 697-707 in W. H. Berger, L. W. Kroenke, and L. A. Mayer, eds., Proceedings of the
Ocean Drilling Program, Scientific Results 130. Texas A & M University, College Station.

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CHAPTER
25

Ecological Restoration and the

Conservation of Biodiversity

WILLIAM R. JORDAN, III

Editor and Outreach Officer, University of Wisconsin Arboretum, Madison

Through its effects both on the land and on the human community, restoration
has a crucial role to play in the conservation of diversity.

Discussions about the conservation of biological diversity generally con-

centrate on strategies for preserving existing habitat for native species, but of
course preservation of what exists is only part of a comprehensive program of
biodiversity conservation. The other, complementary, part is restoration, the
active attempt to return an ecological system—whether conceived as an ecosys-
tem, an ecological community, or a landscape—to some previous condition fol-
lowing a period of change or disruption, usually resulting from human activities
such as agriculture, development, waste disposal, or mining.
Ecological restoration in its most ambitious and ecologically sophisticated
form, involving the attempt to actually recreate ecological systems that closely
resemble specific historic systems in composition, structure, dynamics, and func-
tion, is a relatively new form of environmental technology, and environmental-
ists have tended to be wary of it. There are good reasons for this. There are
serious questions about our ability, given the present state of technology and
understanding of the ecosystems involved, to actually recreate ecologically ac-
curate examples of many kinds of systems. Even when reasonably high-quality
restoration is possible on a scale of a few hectares or tens of hectares, this is often
labor-intensive and costly, and it may not be feasible economically on an eco-
logically significant scale. In addition to these technical and economic concerns,
environmentalists have tended to regard restored ecosystems, even those of the
highest ecological quality, as inherently inferior to, less natural, or even less

371

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372 / BIODIVERSITY II

“real” than the historic systems they are intended to represent. For all these
reasons, people concerned about the conservation of biodiversity and about the
quality of the environment in general have tended to be skeptical about the
promise of restoration and to regard it less as a promising way to reverse envi-
ronmental damage than as a false promise that may be used to undermine argu-
ments for the preservation and protection of existing natural areas.
These are not unfounded concerns. Restoration is, in fact, an immature
discipline, and the success of restorationists’ efforts varies widely. Moreover,
the promise of restoration frequently has been used to circumvent efforts at
preservation, especially of wetlands. This is obviously a matter of deep con-
cern, and it is a concern that is shared by most restorationists, including those
who make their living doing restoration to compensate for or “mitigate” envi-
ronmental damage, as required by law under certain conditions. At the same
time, while this may be a legitimate concern at the political level, it should be
clear that, at a more fundamental level, the dichotomy between preservation
and restoration is a false one. This is true because vast areas of the Earth already
have been profoundly altered by human activities, so that in many cases there
are valuable opportunities to expand preserves or even create new ones through
restoration. Also, and more fundamentally, everything within an ecosystem
interacts with everything else so that, whether we choose to regard ourselves as
outside of “nature” or as part and parcel with it, we cannot actually disengage
ourselves from it or avoid influencing it. In the last analysis, then, preservation
of natural landscapes is in the strictest sense impossible—or rather is properly
seen not as a conservation strategy at all, but rather as a conservation goal or
objective that can be achieved only through a continual effort to identify novel
influences on a given landscape and to find ways of compensating for these
influences in ecologically effective ways.
This of course amounts to a continual program of restoration. This may be
intensive in situations where influence is severe and has dramatic effects on the
landscape—for example, where prairie has been plowed down to grow corn or
wheat. Or it may be less intensive in situations where the influence is subtle or
indirect—a change in the frequency of fire, an alteration in a hydrological cycle,
or the extirpation of a native plant or animal, for example. Nevertheless, the
principle is the same: influence is inevitable, and conservation depends not on
eliminating novel (or “external”) influences, but on finding ways of compensat-
ing for them in such a way that the system resumes behaving—or can continue
to behave—as if these influences were absent.
Preservation, in other words, depends on restoration. Of course, when
people talk about restoration, what they generally have in mind is intensive
restoration, such as the wholesale replanting of prairie in an abandoned corn-
field. There is a tendency to avoid use of this term when referring to attempts to
compensate for subtler forms of influence, and to use softer-edged terms such as
“management,” “maintenance,” or “stewardship.” The distinction, however, is

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ECOLOGICAL RESTORATION / 373

Regular burning restores native species of prairie plants.

an arbitrary one and can be seriously misleading. Strictly speaking, all attempts
to compensate for novel influences in order to allow an ecological system to
remain on its “natural” or historic trajectory are really restorative acts. Restora-
tion in its more dramatic forms differs only in degree from other kinds of man-
agement aimed at the conservation of the classic ecosystem. Properly under-
stood, it is not a peculiar activity, distinct from these other forms of management,
but is of a piece with them. In fact, precisely because it is dramatic and con-
spicuous and because it makes such explicit claims and raises so clearly and
forcefully all the questions involved (about the role of humans, the quality of
the resulting ecosystem, and so forth), restoration is best regarded not as pecu-
liar but as a paradigm for all activities aimed at the conservation of classic eco-
systems against the unavoidable pressure of novel influences.
There are several reasons why it is desirable to be explicit about this, and to
recognize much of what is called “management” or “stewardship” as “restora-
tion.” Doing so clearly establishes the crucial fact, rooted in ecological prin-
ciple, that preservation is not a strategy but a goal, and that achieving it will in
the last analysis always entail some kind of compensatory manipulation. Also,
terms such as “management,” “stewardship,” and even “preservation” imply no
commitment to any particular end result. “Management,” for example, prom-

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374 / BIODIVERSITY II

ises only to manipulate the system, while “preservation,” construed as a strat-

egy or means for conservation, promises only to leave it alone, which of course
is impossible. Neither represents any clear commitment to actually ensuring the
existence or the well-being of the system over the long term.
Only “restoration” does that. And of course this is one reason why restora-
tion has been peculiarly vulnerable to criticism. Environmentalists often point
out that “restoration” in the strictest sense is usually impossible, and of course
they are right. Restoration in fact may be impossible in a particular situation.
But at least the restorationist is committed to a particular objective and is clear
and explicit about what he or she is trying to accomplish. In this sense, the very
vulnerability of restoration to criticism is one of its great values. Besides this,
the very notion of restoration brings into the open a series of fundamental ques-
tions that may be overlooked under headings such as “management” or “stew-
ardship.” Is restoration (i.e., ecologically effective compensation for novel in-
fluences on an ecosystem) actually possible for a given system under a given set
of conditions? How are model systems to be selected? Why choose this sys-
tem—or period—rather than another? And how are standards to be defined
and the results of a project evaluated? This process also forces us to acknowl-
edge the unavoidable fact of our influence on the system, the specific ways we
have influenced it, and the fact that in many if not all situations the quality of
the so-called “natural” landscape will depend at least in part on our understand-
ing of it and our ability to conserve it through an ongoing process of restoration,
or what might be called compensatory maintenance. Acknowledging all this is
important. It not only clarifies what is going on, it also opens the way to certain
experiential and performative benefits that may remain otherwise inaccessible.
In this chapter, I summarize some of my own ideas about the role of resto-
ration in the conservation of biodiversity. In doing so, I take into account not
only the direct value of restoration as a technology for conserving classic eco-
systems against the pressure of novel influences, but also what might be called
its indirect value as a way of changing people and bringing them into a positive,
mutually beneficial relationship with the classic landscape. So far, evaluations
of restoration have concentrated almost exclusively on its products—the re-
stored ecosystem itself—and have overlooked what may well be the most im-
portant (and are unquestionably the most immediate and the most ecological)
aspects of restoration—restoration as an experience and a performance, and as a
way of bringing about changes in the practitioner and in his or her audience. As
a result of this one-dimensional evaluation, many of the benefits of restoration
simply have been overlooked. Indeed, as I try to make clear, most of them have
been overlooked. Not that the product of the restoration effort is unimportant.
Restoration is defined—and distinguished from other forms of agriculture—by
its product, and it deserves to be evaluated on the basis of its ability to produce
it. At the same time, whenever there is a product, there is also a process. And
when humans carry out a process, there are also experience and performance.

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ECOLOGICAL RESTORATION / 375

Taken together, these four dimensions—of product, process, experience, and

performance—define any act. Value is to be found in all of them, not just the
first.
The chapter briefly explores each of these dimensions, considering what
each has to contribute to the value of ecological restoration as a strategy for
conserving biological diversity.

THE PRODUCT: THE RESTORED ECOSYSTEM

I begin with the most obvious benefit of restoration—the product of the
restoration effort, the restored ecosystem itself. Clearly, restoration has an im-
portant role to play in conserving diversity in the direct, technical, or ecological
sense. To begin with, in the case of ecological systems that have been more or
less protected from the more dramatic forms of human influence, an ongoing
program of low-key restoration generally will be required to prevent the system
from drifting ecologically in response to subtle influences and in the process
losing native species, picking up exotics, and perhaps suffering the impairment
of various ecological functions and processes. This is perhaps not a serious issue
among environmental managers, most of whom are fully aware of the pervasive-
ness of human influence on the natural landscape and accept the responsibility
of identifying these influences and finding ways of compensating for them.
What needs to be stressed in this regard is simply that even these relatively low-
key forms of ecological management are in fact forms of restoration and entail
many of the same technical and philosophical problems—and also offer many of
the same opportunities—as do the more dramatic forms of restoration. A crucial
point here is that the very fact of recognizing the necessity for low-key restora-
tion efforts, even in relatively remote areas that may be protected from the more
conspicuous forms of human influence, draws attention to the reality of ecologi-
cal interrelatedness and the extent to which the conservation of diversity actu-
ally depends on deliberate human effort to compensate for influences that may
be indirect, obscure, or even unintentional.
The ultimate example of this would be global climatic change. If the Earth’s
climate actually changes significantly as a result of human activities, massive
restoration and relocation efforts will be required to maintain existing ecosys-
tems or to move them to areas offering suitable conditions, perhaps at higher
latitudes or elevations. Of course, this is an extreme case and may or may not
actually transpire. In the meantime, however, there are already many natural
areas that are changing more or less irreversibly as a result of changes in the
landscape around them. A classic example is the fragments of tallgrass prairie,
often less than an acre in size, that still survive in old cemeteries and odd ne-
glected areas in many parts of the Midwest, but that are now tiny islands of
native biodiversity in a monocultural ocean of corn. Another example is the
tiny, isolated relics of tropical dry forest in Central and South America, which

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376 / BIODIVERSITY II

ecologist Dan Janzen has referred to

as examples of the “ecological walking
dead.” By this vivid phrase, Janzen
means quite simply that, existing under
altered conditions, these forests are
no longer viable ecological entities.
Though biologically alive, they are eco-
logically dead. No amount of protection
will enable them to survive, and their
future, like that of the prairies of the
Midwest, will depend wholly on an ef-
fective, sustained program of restoration
and recreation to compensate for their
altered circumstances.
This may seem an extreme example,
and in some ways it is. But it is at the
same time paradigmatic. Though we
hesitate to admit it, the same thing is
true in some degree of all ecosystems ev-
Restorationist at work.
erywhere. This fact may be obscured
by the subtlety of influence in some
cases and also by the ecological inertia that may enable an ecosystem to persist
for a time in the presence of changing conditions (Magnuson, 1990). Neverthe-
less, it is unavoidable, and it provides the bedrock principle on which all con-
servation thinking, policy, and practice must be based. With the possible ex-
ception of some areas that may be large enough and remote enough to preserve
a high level of ecological integrity—and that have no history of shaping by
human influence—the conservation of natural or classic levels of biodiversity
always will depend on some degree of restoration as I have defined it. The
question, then, is not whether to restore, or even whether we can restore per-
fectly (usually we cannot). The question is simply how close we can come to
restoring the natural or historic features of a given ecosystem. In the long run,
“natural” landscapes everywhere on the planet will be necessarily (and we might
say naturally) to some extent artificial landscapes. Indeed, the best and most
“natural” of these will be those that have been most skillfully and diligently
restored (restoration being taken here to include protection to minimize novel
influences). It is important that we not only recognize this, but that we learn to
celebrate it—indeed to make a celebration of it—rather than to deplore it.
Of course, the question of restorability takes on a special urgency in the
case of restoration projects that are carried out to reverse the effects of the most
dramatic kinds of environmental damage—plowing, for example, or surface
mining—and that entail not just tinkering with key processes or the reintroduc-
tion of a few extirpated species, but the wholesale reassembly of the entire sys-

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ECOLOGICAL RESTORATION / 377

tem. This is what most people have in mind when they talk about ecological
restoration, and the question of the quality of the resulting ecosystems has led to
a considerable amount of discussion and debate and, in recent years, to some
systematic research. The answer, not surprisingly, is complex and depends on
many factors, including the nature of the ecosystem, the nature and degree of
disturbance to which it has been subjected, the conditions under which the
work is carried out, the resources available for the project and, of course, the
skill of the restorationist. Obviously, this question is far too complex to answer
in detail here, but there is a growing literature on the ecological quality of re-
stored ecosystems, and it is possible to make a few generalizations based on this
emerging body of knowledge (for earlier overviews see also Jordan et al., 1988;
MacMahon and Jordan, 1994).
Of all ecosystems that have been the subject of intensive restoration efforts,
wetlands are perhaps the most intensively studied, at least in part because the
restoration of wetlands is mandated by law under certain conditions, and recent
research in this area has led to a considerable amount of new information about
the quality of several kinds of restored wetlands, and also to a considerable
amount of debate over the meaning and significance of this information. A
prime example is an evaluation of a restored coastal marsh near San Diego that
recently was carried out by ecologist Joy Zedler and her colleagues at San Diego
State University (Zedler and Langis, 1991). Zedler and Langis’ report on this
project is generally downbeat. They found that the restored wetland differed
markedly from a natural reference wetland with respect to a number of indica-
tors, including biomass, plant height, soil organic matter content, and eight other
indicators of structural and functional quality. Of special importance to us here,
Zedler and Langis found that, 5 years after restoration began, the wetland did
not yet provide the habitat for the endangered light-footed clapper rail, which
had been a primary objective of the project. They concluded that the restored
wetland resembled the reference wetland by only about 57% (a figure obtained
by averaging values for the 11 attributes of the ecosystem) and suggested that,
because of this low value and because the restored wetland was not yet a suit-
able habitat for the rail, the project had been disadvantageous from an environ-
mental point of view.
Welcome as these data were as a contribution to the relatively small body of
published information on restored ecosystems, Zedler and Langis’ conclusions
did not go unchallenged. Restorationist John Rieger, for example, pointed out
that the marsh Zedler and Langis chose for study was only 5 years old, so that it
was unreasonable to compare it with a natural marsh that is thousands of years
old (Rieger, 1991). Rieger also argued that the San Diego project had suffered
from several years of unseasonably dry weather, and he called into question the
validity of averaging measurements of different features as an index of quality.
In similar situations, restorationists also have questioned the techniques
involved in restorations, arguing that projects chosen for evaluation have not

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378 / BIODIVERSITY II

been the best examples of the restorationist’s craft. This point, which I have
generally encountered in conversation and not in print, is of considerable inter-
est because it points toward the disparity in outlook between ecologists, who
may have little knowledge of horticulture or other practical aspects of restora-
tion, and restorationists, who somehow have to combine horticultural skill with
ecological understanding into a kind of ecological horticulture.
Overall, ecologists’ assessment of the quality of restored wetlands generally
has been guarded. A good example is the comment by Mary Kentula and Jon
Kusler in their executive summary of a recent survey of techniques for restoring
and creating wetlands (1990:xviii):
“Total duplication of natural wetlands is impossible due to the complexity and
variation in natural as well as created or restored systems and the subtle rela-
tionships of hydrology, soils, vegetation, animal life, and nutrients which may
have developed over thousands of years in natural systems. Nevertheless, ex-
perience to date suggests that some types of wetlands can be approximated and
certain wetland functions can be restored, created, or enhanced in particular
contexts. It is often possible to restore or create a wetland with vegetation
resembling that of a naturally-occurring wetland. This does not mean, how-
ever, that it will have habitat or other values equaling those of a natural wet-
land nor that such a wetland will be a persistent, i.e., long term, feature in the
landscape, as are many natural wetlands.”
As Kentula and Kusler acknowledge, restoration is a complex and uncertain
business, yet projects can have strikingly positive results. Two examples are
appraisals of the attempt to restore the estuary of the Salmon River in Oregon
(Morlan and Frenkel, 1992) and the restoration of Henry Greene Prairie, a classic
project begun at the University of Wisconsin-Madison Arboretum in the mid-
1940s (Kline, 1992). In the first case, success was attributed partly to the fact
that the disturbance involved had been relatively mild—a change in hydrology
that could be reversed by removal of an artificial dike, allowing the ecosystem
to recover more or less on its own. But in the case of Greene Prairie, the situa-
tion was quite different. The historic prairie on this site had been virtually
eliminated as a result of three-fourths of a century of intensive farming, and the
entire plant community had to be reassembled virtually plant by plant. More-
over, this project, undertaken in the 1940s, was only the second large-scale prai-
rie restoration ever attempted and so necessarily involved a great deal of trial
and error. Despite this, parts of Greene Prairie now closely resemble natural
prairies in southern Wisconsin, at least with respect to the species, abundance,
and distribution of vascular plants. Less is known about other features of the
system, including animals and ecosystem processes. In fact, the neglect of ani-
mals and functional aspects, both of which are often relatively difficult to study
quantitatively, is often a weakness of evaluations of restored ecosystems. Nev-
ertheless, it is fair to point out that restoration projects have at times resulted in
the creation of habitat for rare and often difficult-to-restore species—for ex-

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ECOLOGICAL RESTORATION / 379

ample, a number of rare and endangered plants now growing in restored prai-
ries such as Greene Prairie and the least Bell’s vireo along the Kern River in
California (Baird, 1989). In landscapes now profoundly altered by development,
the expansion of habitat, even for relatively common native species, may be an
important contribution to the native biodiversity of an area. Indeed, a site like
Greene Prairie, harboring several hundred species of native plants and animals,
many of which are now rare in the area, represents a biodiversity hotspot of
great beauty and inestimable ecological, biological, cultural, and spiritual value.
Moreover, while intensive restoration projects have generally been carried out
on a modest scale in the past, restorationists are developing techniques that
allow them to undertake projects on a much larger scale without compromising
ecological quality. An example is the recent development of a technique some-
times called “successional restoration” for restoration of tallgrass prairies in the
Midwest (Packard, 1994).
Overall, the answer to the question of the quality of restored ecosystems is
both complex and incomplete, but will no doubt become clearer, more compre-
hensive, and more accurate as the craft of restoration develops and as ecologists
learn more about how to evaluate the quality—or assess the health—of an eco-
logical community or ecosystem.
Beyond the essentially technical question of ecological quality or “accu-
racy”, however, there is the larger question of authenticity. Even supposing
that a restored ecosystem is a faithful replica of the “natural” or model system,
closely resembling it in all technical features, including function and dynamics
as well as composition and structure, questions remain as to its authenticity, its
ontological status or value or, simply, its realness. Is the restored ecosystem as
“real” as its natural counterpart? Or is it, as some have suggested, merely a
“copy” or even a “fake”?
Most discussions of this issue have taken for granted that restoration does
in some sense compromise nature, and that the restored ecosystem is not only
less “natural” but even in a sense less real than a natural or historic system that,
even if humans played a role in shaping it historically, may be perceived as
“given” and therefore fully “natural” (see Elliott, 1994, for example).
On this assumption, the restored ecosystem is unauthentic simply by defi-
nition. But the real issue here is not actually whether the system is “authentic”
in some final sense. It is rather what we mean by authenticity—what we mean
by the word “real,” what we take to be the basis for realness, what is the ground
or touchstone of reality. Curiously, the assumption that an artificial copy of a
thing is inherently less real than the original is rooted in two philosophical tra-
ditions, both of which are now widely recognized as being antiecological in
their implications. The first of these is the platonic idea that what is most real is
the changeless form of a thing. In this view, actual objects such as a prairie are
mere representations of the ideal form or idea of “prairie,” and are therefore less
real or of lower status ontologically. By the same reasoning, representations of

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380 / BIODIVERSITY II

objects (e.g., a restored prairie), being mere representations of representations,

are of even lower status. The second philosophy is the Cartesian idea that being
is—or at least can be—known only by the solitary individual, and that relation-
ships of any kind can only be inferred, not experienced, and are therefore of
doubtful ontological value. From this perspective, the restored ecosystem is
ontologically suspect because it does not exist in and of itself, but is contingent
on entities outside itself. In fact, it is the product of relationships. To us, this
simply means that it is ecological. But from the Cartesian perspective, it means
that its reality has been compromised. Curiously, this kind of thinking is clearly
evident in modern environmental thinking, as indicated by the conventional
environmental critique of restoration. 1
In any event, both conceptions of the “real”—the platonic and the Carte-
sian—result in a conception of authenticity within which a restored ecosystem
will be judged unauthentic. But both take for granted a conception of the world
and our relationship with it that is inimical to the conception of radical related-
ness that is at the heart of an ecological sensibility. In fact, the ecological sensi-
bility takes for granted a quite different idea of authenticity, in which the real-
ness and ontological value of things emerges precisely from the way they interact
with, register on, and we might even say “contaminate” each other. This under-
lies, for example, the conception, common among people of archaic and pre-
modern cultures, that the realness of the world depends on its participation in a
higher or sacred reality, mediated by human awareness expressed in ritual
(Eliade, 1971). This ecological sensibility is also integral to the conception of
“performed being” developed by the poet and philosopher Frederick Turner
(1985). In Turner’s deeply ecological view, realness is not compromised by re-
lationship, but emerges from it. Realness is, in fact, the product of interaction
and engagement—of the mutual registration of objects on each other—and the
more intense and the more reflexive and self-aware the engagement becomes,
the more realness there is. From this perspective, nature is neither compro-
mised, or made less real, by deliberate human participation in it, nor is the
restored ecosystem in any way less real because it is partly the result of human
effort. In fact, nature is actually more real in the precise sense that through the
very process of restoration it is more fully realized.
Interestingly, the ontological status of a restored ecosystem in this view
bears comparison with that of objects or landscapes made real or sacred through
ritual action in certain archaic traditions as interpreted by historian of religion,
Mircea Eliade. This seems to me a matter of considerable importance in the
evaluation of restoration, in part because our conception of the authenticity of
the restored ecosystem will affect profoundly the way we interpret this work
and the spirit in which we undertake it, which will in turn largely determine its

1I am indebted to Professor Gene Hargrove of the Department of Philosophy at the University of

North Texas for an introduction to these ideas and their implications for restoration.

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ECOLOGICAL RESTORATION / 381

effectiveness as an occasion for social- and self-transformation. (For further dis-

cussion of this point, see Jordan, 1993; Jordan, in preparation.) My point here
is simply that there are many ideas of authenticity; some are more “ecological”
than others, and they provide a more favorable perspective of restoration than
those rooted in either the platonist or the Cartesian/modernist tradition.
The discussion so far pertains to the direct contribution that restorationists
can make to the conservation of biodiversity through the restorative mainte-
nance of existing ecosystems, or through the wholesale creation or recreation of
native ecosystems on more or less severely disturbed sites. This is the most
obvious contribution of restoration to biodiversity conservation, but it is by no
means the only one. The effects of the restorationist’s efforts on the landscape
are obviously important. Just as important, however, are their effects on those
who carry out the work and on those who merely witness it and act as an audi-
ence. Since the well-being of the natural landscape ultimately will depend to a
considerable extent on its relationship to humans and on how people under-
stand and value it, this is an important matter. Indeed, it may well be that what
is most important about restoration in the long run will be the way it affects the
human community by providing the basis for a repertory of experiences and
rituals for negotiating the intellectual, psychological, and spiritual, as well as
the purely physical, reentry of nature. This being the case, I conclude with a
few comments on the other three dimensions of the act of restoration—restora-
tion as process, as experience, and as performance—and on the implications of
these for the conservation of biodiversity.

THE PROCESS: RESTORATION ECOLOGY

One outcome of the act of ecological restoration is the restored ecosystem
itself. But restoration is more than a way of creating ecosystems. It is also a
powerful way of learning about them. Indeed, the history of both ecology and
of restoration clearly illustrates the value of restoration—the attempt to repair,
heal, or reassemble a living ecosystem—as a way of raising questions and testing
ideas about it. A classic example from the University of Wisconsin Arboretum
in Madison was the discovery of the importance of fire in the ecology of prairies
that resulted from the Arboretum’s early attempts at prairie restoration (Curtis
and Partch, 1948). But ecology provides endless examples of the heuristic value
of the reassembly process applied to ecological systems, all pointing toward an
obvious fact: we can change a complex system without understanding very
clearly what we are doing, but we generally cannot restore that system to its
former condition without having a clear idea of how we have influenced it and
of the ecological implications of that influence.
Reflecting on this early in my career at the Arboretum, I coined the term
“restoration ecology” to refer to restoration efforts that were undertaken spe-
cifically to raise questions or to test ideas about the system being restored (Jor-

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382 / BIODIVERSITY II

dan et al., 1987). It seemed to me that it was important to introduce this term in
order to call attention to this approach to ecological research and to encourage
its systematic development. But this is of more than academic or purely intellec-
tual importance. In the long run, the well-being of these ecosystems will de-
pend in part on how well we understand them and are able to care for them. An
important value of restoration, then, is its value as a way of booting us up intel-
lectually to become competent stewards of the natural landscape. Indeed,
through this process of heuristic reassembly, the ecosystem may be said to be-
come more aware of itself through transcription into human understanding, and
in this sense even to acquire a kind of immortality, i.e., viability in the context
of a landscape dominated by human beings.

THE EXPERIENCE: REENTERING THE FOREST

We all know that we are shaped by experience and that we are to some
extent the product of our experiences. The question for us here, then, is what
kind of experience is ecological restoration, and in what way might we expect it
to affect or shape the person who carries it out? This is obviously a complicated
question. But it is not too difficult to sketch at least the broad outlines of an
answer. To begin with, restoration
provides an opportunity to partici-
pate in a constructive way in the
ecology of the ecosystem being re-
stored. In this sense, then, it makes
us one with other species of animals
and plants which, in their various
ways, also contribute to the shap-
ing and well-being of the system.
This makes us members of the
biotic community in a purely eco-
logical sense. But it does something
else as well. If we consider the act
of restoration carefully, we can see
that it is a form of agriculture, and
that, like any form of agriculture, it
entails the manipulation of nature.
At the same time, it is in some ways
a peculiar form of agriculture.
While other, more traditional forms
of agriculture manipulate nature
creatively, the restorationist ma-
nipulates it conservatively; i.e., his
or her objective is not to change na- Classic experience of the gatherer.

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ECOLOGICAL RESTORATION / 383

ture or improve on it, but rather to maintain it, or we might say to turn it back
into itself. Thus, while the farmer or gardener attempts to imitate nature, the
restorationist attempts something similar but psychologically very different, i.e.,
not to imitate, but actually to copy nature. This entails great humility, and even
a measure of self-abnegation, a setting aside of creativity and preference in def-
erence to nature. Restoration is then, among other things, an act of humility in
the exercise of technology. And like the ritual abasement that often accompa-
nies rites of initiation, this helps prepare the restorationist psychologically for
initiation into the ecological community.
Finally, it is worth pointing out that the act of restoration is itself complex
and rich, drawing on a wide range of human abilities and interests. Specifically,
it entails not only the work of the farmer and the gardener, but also of the
hunter and gatherer and, as we have seen, of the scientist as well. As a result, it
provides an opportunity to explore all these classic ways of experiencing and
interacting with nature by reenacting them. In other words, it provides a way
of reentering nature without ceasing to be fully ourselves—without abandon-
ing what naturalist Loren Eiseley referred to as the lessons learned on the path-
way to the moon. In this way, we may hope to become more fully at home in
nature, more, as Thoreau wrote, “a part of herself.” This obviously has impor-
tant implications for the conservation of biodiversity in any area that is subject
to any significant amount of human influence. And the fact that the work of
restoration draws on and appeals to a wide range of human aptitudes and inter-
ests has important political implications as well.

PERFORMANCE: A NEW COMMUNION WITH NATURE

When we think of ecological restoration, we tend to think of it primarily as
a more or less effective process, but like any human activity it is more than this.
It is also an expressive act—in fact an act in the dramatic, theatrical, or ritual
sense of the word: an action that not only accomplishes work, but that also
conveys information, meaning, and feeling. This is an aspect of work that a
puritan society, with its deep-seated skepticism regarding ritual and the experi-
ence of performance, tends to overlook. Nevertheless, there are reasons to be-
lieve that it is of immense importance to us in the task of negotiating a healthy
relationship between human communities and the larger biotic community.
Relationship, as noted earlier, is crucial to the ecological sensibility—the
bedrock of its conception of what is real. Yet, as Frederick Turner and others
have pointed out, the relationship between nature and culture, like many kinds
of relationships, entails deep tensions that actually cannot be resolved in literal
terms, but only in psychological terms, and only by stepping out of the literal
dimension and into the dimension of make-believe, of performance and of ritual
(Turner, 1991). This is true of many kinds of relationships, e.g., among humans,
among many other kinds of animals, and certainly between humans and the rest

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384 / BIODIVERSITY II

Working in the Curtis Prairie.

of nature. A convenient example is the conflict between the urge to mate and
the urge to defend territory in a territorial species. Another is the irreducible
tension between predator and prey. Yet another is the tension that exists be-
tween creatures endowed with different levels of reflexivity or self-awareness.
Such tensions, Turner suggests, cannot be resolved literally, but only in per-
formative, often counterfactual, terms. It is at such points of irreducible tension
that ritual develops or is invented as a way of negotiating and resolving psycho-
logically (and in the imagination) a tension that cannot be resolved in literal
terms—hence the mating rituals of many species of animals, including humans.
Hence, too, the rituals human communities commonly provide as ways of nego-
tiating the deeply problematic entry of the individual into the community, or
the relationship between the human and the larger biotic community.
Simply put, community depends on ritual. The anthropologist Victor
Turner, a pioneer in the study of ritual, argued that what he called communitas,
or the full experience of community, is available only in the central and climactic
phase of community-making rituals (Driver, 1991). Though Turner is concerned
primarily with the human community, his ideas clearly have profound implica-
tions for the nature-culture relationship, and so ultimately for the conservation
of biodiversity. Since the development of a relationship between the human

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ECOLOGICAL RESTORATION / 385

community and the biotic community is essentially an act of community-mak-

ing, it may well be that the failure of modern environmentalism to deal success-
fully with a wide variety of environmental problems, including the loss of natu-
ral habitat, is due in part to its failure to provide rituals suitable for the purpose
and, more deeply, to a wariness of ritual experience and a skepticism as to its
efficacy that is part of the puritan heritage of modern culture.
This being the case, it would seem that we at least should explore the value
of ritual as a way of addressing what is really the central problem of environ-
mentalism: the negotiation of a satisfactory relationship between the human
community and nature in its wilder, more primitive, or less reflexive forms.
Hence the importance of viewing the act of restoration as a kind of performance
and as a basis for ritual—specifically rituals for negotiating our relationship
with the rest of nature. As I discussed earlier, we tend to regard an activity such
as restoration primarily, if not exclusively, as a form of technology—simply a
way of fixing the landscape. In other words, we see restoration simply as a more
or less effective process, overlooking its value as an experience and an expres-
sive act. In this way, our culture is the obverse of archaic cultures, for which
the expressive, ritual value of an act is often taken as being of primary impor-
tance, the culture often devoting a large fraction of its resources to activities that
have no technical or literal efficacy at all, but that are rich in expressive value
and the power to bring about some desirable inner transformation of individuals
and groups.
An example is the tradition of world-renewal common to archaic cultures in
many parts of the world (LaChapelle, 1988). These characteristically entail elabo-
rate rituals that both inform and transform the participants, but that have little
or no direct effect on the “world” or the landscape at all. In fact, what is re-
newed by rituals of this kind is not the landscape but the community’s idea of
the landscape and its place in it. The crucial observation, however, is that this
frequently works, resulting in at least a measure of reconciliation between na-
ture and culture, while literal acts of restoration or management, undertaken in
a purely technical spirit, commonly do not work as well, even in the purely
literal sense in which they are intended. They may be successful in the short
term, and they may meet regulatory requirements and ecological specifications,
but, having failed to bring about the inner changes—the renewal of ideas and
belief within the human community—on which the well-being of the “natural”
landscape typically depends, they inevitably will fail in the long run.
Hence the crucial importance of construing the work of ecological restora-
tion not only as a process and technique but also as an expressive and transfor-
mative action and the basis for modern rituals of world-renewal (Jordan, 1994).
Indeed, conventional technical activities such as ecological restoration have a
crucial role to play in the invention of ritual. According to Victor Turner, ritual
commonly emerges from ordinary acts such as mating, the eating of a meal, or
the killing of animals for food. Ritual, Turner suggests, is the “quintessence of

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386 / BIODIVERSITY II

custom” (Turner, 1968)—an idea that points to the futility of importing rituals
from other cultures and attempting to graft them onto one’s own. Since ritual—
like story, dance, and other art forms—emerges from experience and custom, it
follows that we ought to look to custom—the shared work and experience of a
particular human community—to provide a foundation or starting point for the
invention of the repertory of rituals needed to negotiate the relationship be-
tween industrial and postindustrial societies and nature in its primitive or clas-
sic forms.
Fortunately, restoration is already a “custom” for a growing number of
people who are participating in community-based restoration projects. Besides
this, restoration incorporates many activities such as gardening, birding, hik-
ing, and even hunting that are conventional activities in our society, and are in
fact partly ritualized avocations for millions of people. What remains is the
integration of these activities into the task of restoration and the self-conscious
development of this work as the basis for festival and other ritual activities
needed to bring the human community together and to negotiate its relationship
with the biotic community. Construed and developed in this way, restoration
no longer will be merely a way of patching up environmental damage but will
become in the deepest sense a basis for world-renewal.
In fact, this is already happening in the case of some community-oriented,
volunteer-driven restoration projects. In Lake Forest, Illinois, just outside Chi-
cago, the burning of brush piles created by volunteers working on the restora-
tion of oak savannas has become the occasion for an annual community festival,
complete with hot-air balloons and a parade of bagpipes reflecting the com-
munity’s Scottish heritage. In the view of those involved, this seasonal festival
plays a vital role in bringing the Lake Forest community together and orienting
it toward the reinhabitation of the ancient oak groves (Christy, 1994; Holland,
1994).
What this kind of experience, together with the experience of traditional
cultures, suggests is that in the last analysis it is the ritual that matters most. If
we get that right, then technique will follow. In fact, in my view, it is not any
lack of technical know-how or even ecological understanding that currently is
limiting the conservation of biodiversity in most situations—it is the inadequacy
of our ritual tradition. If, as Victor Turner and others have argued, ritual is
crucial to the process of community-building, then it clearly will be crucial to
the process of developing the human community and bringing it into a positive
relationship with the larger biotic community. One value of restoration, then,
will be its value as a basis for the creation of new rituals for this purpose. Thus,
in my view, the ritualization of restoration, its development as a basis for com-
munity-building ritual and festival, is a matter of great urgency, and ought to
proceed hand in hand with the development of restoration as a science and an
art of environmental healing.

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ECOLOGICAL RESTORATION / 387

REFERENCES
Baird, K. 1989. High-quality restoration of riparian ecosystems. Restor. Managemt. Notes 7(2):60-64.
Christy, S. F. 1994. A local festival. Restoration and Management Notes 12(2):123.
Curtis, J.T., and M. L. Partch. 1948. Effect of fire on the competition between blue grass and certain
prairie plants. Amer. Midl. Nat. 39(2):437-443.
Driver, T. F. 1991. Pp. 160-173 in The Magic of Ritual: Our Need for Liberating Rites that Transform
Our Lives and Our Communities. Harper, San Francisco.
Eliade, M. 1971. The Myth of the Eternal Return. Princeton University Press, N. J.
Elliott, R. 1994. Extinction, restoration, naturalness. Envir. Ethics 16(2):135-144.
Elliott, R. 1994. Extinction, restoration, naturalness. Envir. Ethics 16(2):135-144.
Holland, K. 1994. Restoration rituals: Transforming workday tasks into inspirational rites. Restor.
Managemt. Notes 12(2):121-125.
Jordan, W. R., III, R. L. Peters, II, and E. B. Allen. 1988. Ecological restoration as a strategy for
conserving biological diversity. Envir. Managemt. 12(1):55-72.
Jordan, W. R., III. 1993. The ghosts in the forest. Restor. Managemt. Notes 11(1):3-4.
Jordan, W. R., III. 1994. Sunflower forest. Pp. 17-34 in A. D. Baldwin Jr., J. De Luce, and C. Pletsch,
eds., Beyond Preservation: Restoring and Inventing Landscapes. University of Minnesota Press,
Minneapolis.
Jordan, W. R., III. Sunflower Forest: Ecological Restoration and the New Communion with Nature.
In preparation.
Jordan, W. R., III, M. E. Gilpin, and J. D. Aber. 1987. Restoration Ecology: A Synthetic Approach
to Ecological Research. Cambridge University Press, N.Y.
Kentula, M. E., and J. A. Kusler. 1990. Executive summary. Pp. xvii-xxv in J. A. Kusler and M. E.
Kentula, eds., Wetland Creation and Restoration: The Status of the Science. Island Press,
Washington, D.C.
Kline V. M. 1992. How well can we do? Henry Greene’s Prairie. Restor. Managemt. Notes 10(1):36-
37.
LaChapelle, D. 1988. Sacred Land. Sacred Sex. Rapture of the Deep. Kivaki Press, Durango, Colo.
Pp. 239-249.
MacMahon, J., and W. R. Jordan, III. 1994. Ecological restoration. Pp. 409-438 in G. K. Meffe and C.
R. Carroll, eds., Principles of Conservation Biology. Sinauer Associates, Sunderland, Mass.
Magnuson, J. 1990. Ecological research in the invisible present. BioScience 40(7):495-501.
Morlan, J. C., and R. E. Frenkel. 1992. How well can we do? The Salmon River Estuary. Restor.
Managemt. Notes 10(1):21-23.
Packard, S. 1994. Successional restoration: Thinking like a prairie. Restor. Managemt. Notes 12(1)32-
39.
Rieger, J. 1991. San Diego Bay mitigation study: A response. Restor. Managemt. Notes 9(2):65-66.
Turner, F. 1985. Performed being: Word art as a human inheritance. Pp. 3-58 in Natural Classicism:
Essays in Literature and Science. Paragon Press, N.Y.
Turner, F. 1991. Beauty: The Value of Values. University of Virginia Press, Charlottesville.
Turner, V. 1968. Introduction. P. 21 in The Drums of Affliction: A Study of Religious Processes
among the Ndembu of Zambia. Clarendon Press, Oxford, England.
Zedler, J. B., and R. Langis. 1991. Comparison of constructed and natural salt marshes of San Diego
Bay. Restor. Managemt. Notes 9(1):21-25.

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CHAPTER
26

Tropical Sustainable Development

and Biodiversity

PATRICK KANGAS
Coordinator, Natural Resources Management Program,
University of Maryland, College Park

Sustainable development is one of the great hopes for the conservation of

biodiversity. It is a complicated concept that has arisen to synthesize ideas that
simultaneously address environmental impacts and the needs of people. The
idea of sustainability, or long-term renewable use, is old in terms of fisheries and
wildlife harvest management. However, recently it has been applied more
broadly to cover a variety of development activities. Although much work is
now being classed as sustainable development, the term did not even appear less
than a decade ago in the 1986 BioDiversity Forum (Wilson and Peter, 1988). The
purpose of this chapter is to review the concept of sustainable development and
its relationship with biodiversity. The focus of the chapter is on the tropics,
where biodiversity is high and environmental impacts are increasing.
Sustainable development commonly is defined as the process of meeting the
needs of the present generation without compromising the ability of future gen-
erations to meet their needs (Goodland and Ledec, 1987). This concept arose in
the late 1980s as an approach to balance economics and environment. Sustain-
able development embodies several advancements over other models that have
characterized the development process (Norgaard, 1990). One advancement is
drawing distinctions between the growth component and the efficiency compo-
nent of development (Costanza and Daly, 1992; Goodland and Daly, 1992). The
growth component refers to an increase in size or dimension of an economy.
Assuming that an economy draws on a finite resource base, growth cannot con-
tinue indefinitely, i.e., it cannot be sustained (Daly, 1990). The efficiency com-
ponent refers to the “realization of potential,” which is a more qualitative sense
of development that may be able to be sustained on a finite resource base. Thus,

389

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390 / BIODIVERSITY II

the recognition of the different components of development can lead to more

effective policies for resource use that focus on efficiency rather than growth.
These ideas, along with recognition of the importance of future generations and
the value of the environment, make sustainable development an attractive phi-
losophy for planning. Although sustainable development is still just an alterna-
tive to more conventional economic development models, it is beginning to be
adopted at the national level, as seen in the sustainable biosphere initiative of
the Ecological Society of America (Lubchenco et al., 1991), and at the interna-
tional level, as seen in Agenda 21 (Piel, 1992).
Sustainable development is tied indirectly to biodiversity through the need
to maintain overall environmental values. Its purpose is to sustain both man
and nature, and thus it is directly related to conservation and the wise use of
resources, including biodiversity. In the tropics, conservation has focused on
controlling the deforestation process (Table 26-1; see also Gradwohl and
Greenberg, 1988). All of the strategies listed in Table 26-1 can be thought of as
forms of sustainable development, but the extraction of products and values
from existing forest may be the approach that most directly links biodiversity to
sustainable development. This is the “use it or lose it” approach that is receiv-
ing much recent attention (Bawa, 1992; Dobson and Absher, 1991; Janzen, 1992).
The idea is that forests or other habitats can be maintained if they can be shown

TABLE 26-1 Techniques for Mitigating Deforestation and Maintaining

Tropical Forest Habitat

Strategy Mechanism Examples

Preservation Deforestation is National parks

eliminated as a Community sanctuaries
land-use option Biosphere reserve

Conversion from Less land is used Polycropping

extensive to to produce the Intercropping
intensive forms same amount of Fertilization
of agriculture yield, thus freeing Agroforestry
other land for Intensive pasture
forest preservation

Extraction of Forest is maintained Selective logging

of products and because of demonstrated Ecotourism
values from market values Harvest of nontimber products
existing forest

Reforestation Restored forest Managed succession

directly replaces Tree planting
deforested land

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TROPICAL SUSTAINABLE DEVELOPMENT / 391

Rainforest canopy.

to provide direct value to people, especially rural people who coexist with the
forests. Direct market values of forests are derived from the ecosystem as a
whole for ecotourism (e.g., Tobias and Mendelsohn, 1991) and from harvest of
individual species for timber or nontimber resources. Of course, the value of
logging or the harvest of trees for timber is well known, but assessments of
value of nontimber products are very recent. The much-cited paper by Peters et
al. (1989) led the way in showing that harvest of nontimber products (i.e., latex
and fruits) from intact forests can generate more revenue than other forms of
forest land-use that are more destructive, such as logging or conversion to pas-
ture or tree plantations. Although the estimate of the value of the forest given
by Peters et al. (1989) may not be representative of tropical forests in general
(Godoy et al., 1993), their study has led to a new vision of rain forest economics.
Harvest of medicinal plants is another important example of this approach
(Akerele et al., 1991; Balick and Mendelsohn, 1992; Elisabetsky and Nunes,
1990), but many other nontimber resources potentially can be sustainably har-
vested from intact tropical forests (Anderson, 1990; Anderson et al., 1991;
Durning, 1993; Nepstad and Schwartzman, 1992; Panayotou and Ashton, 1992;
Plotkin and Famolare, 1992; Robinson and Redford, 1991).

THE MCKELVEY BOX CLASSIFICATION OF BIODIVERSITY

In viewing extraction as a form of sustainable development, biodiversity is
a resource to be utilized by people. In fact, each species is a potential resource.

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392 / BIODIVERSITY II

To clarify the role of species in sustainable development, an analogy can be

made with a classification used for mineral deposits (McKelvey, 1972; U.S. Geo-
logical Survey, 1980). The McKelvey box separates mineral deposits based on
the knowledge of their existence and their economic concentration (Figure 26-
1). The term “reserves” is applied only to those deposits that have been identi-
fied and are in sufficiently high concentrations to be mined economically. All
other deposits are termed “resources.” This classification provides a status as-
sessment or inventory that is useful for decision-makers. Hypothetical examples
for two forms of biodiversity (higher plants and insects) are given in Figures 26-
2 and 26-3. Obviously, the numbers shown in these McKelvey boxes are tenta-
tive, but several patterns are evident. First, there are relatively few species that
currently and directly are utilized by people and therefore fall into the “re-
serves” category. Also, there is a high proportion of undiscovered species, es-
pecially insects. Many and probably most of these undiscovered species occur
in tropical forests, most of which are undergoing deforestation. Although these
undiscovered species present conceptual problems (Kangas, 1992), their loss to
extinction certainly would be significant.
It is important to recognize that the McKelvey box represents a single time
frame and that over time the numbers inside the box change. As taxonomic
exploration continues, the number of undiscovered species will go down. As
technology advances, the number of economically useful species will increase.
New mechanisms are developing to stimulate these changes. Biodiversity pros-
pecting (Reid, 1993; Reid et al., 1993; Rubin and Fish, 1994) is being advocated,

Identified Undiscovered
Economic

"RESERVES"
Subeconomic

"RESOURCES"

FIGURE 26-1 The McKelvey box classification of mineral deposits from geology
(McKelvey, 1972; U.S. Geological Survey, 1980).

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TROPICAL SUSTAINABLE DEVELOPMENT / 393

Identified Undiscovered
Economic

100a

About 29,100,000c
Subeconomic

874,061b

FIGURE 26-2 An hypothetical McKelvey box classification of biodiversity of insects

and other species of arthropods. aAssumption. bFound by subtraction of known species
(Wolf, 1987) and economically important species from a. cFound by subtraction of esti-
mated total species and known species (Wolf, 1987).

Identified Undiscovered
Economic

5,000a

25,00 – 150,000c
Subeconomic

243,400

FIGURE 26-3 An hypothetical McKelvey box classification of biodiversity of species of

higher plants. aNational Research Council (1982). bFound by subtraction of known spe-
cies (Wolf, 1987) and economically important species from a. cFound by subtraction of
estimated total species and known species (Wolf, 1987).

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394 / BIODIVERSITY II

and mechanisms for distributing income that is generated from biodiversity are
being developed. These mechanisms include the work of national institutions
such as the Instituto Nacional de Biodiversidad de Costa Rica (INBio) (Gamez et
al., 1993; Tangley, 1990) and, at the international scale, the Biodiversity Treaty
(Broadus, 1992; Stone, 1992).

IMPEDIMENTS TO SUSTAINABLE DEVELOPMENT

The idea of sustainable development is attractive but there are a number of
problems or impediments in practice (Table 26-2). This should not be surpris-
ing, since the system of man and nature that is to be sustained is complex. Some
of the problems with sustainable development are described below. To a greater
or lesser extent, these and other problems must be addressed for success to be
achieved.
Overharvesting or overuse is a critical issue in most resource systems (e.g.,
Bodmer et al., 1990; Vasquez and Gentry, 1989). Because income often is per-
ceived to be directly proportional to harvest, users of resources easily can be
enticed into overharvest. Thus, attention must be given to harvest and use
schedules. This requires the best scientific knowledge (Ewel, 1993; Hall and
Bawa, 1993; Levin, 1993), but it also requires that users of resources face the
issue of limitation. In some cases, short-term sacrifices in harvest may be needed
to achieve long-term benefits of sustainability. In this regard, management of
people is just as important as management of resources in sustainable develop-
ment (Fiske, 1990).
One approach to supplement income of rural people is to develop new mar-
kets, either for existing products or products of new resource-use systems, such
as harvest of nontimber products from forests (Jukofsky, 1993). The hope is
that, by providing additional income derived from forests, there will be less
incentive to cut the forests. An interesting example of this strategy is the open-
ing of markets in the developed countries for tropical forest products. This is

TABLE 26-2 Summary of Impediments to Sustainable Development

Overharvesting of renewable resources

Lack of markets for products from sustainably developed operations
Short-sighted political economies that do not properly value sustainability or the
contributions of nature to economies
Land-tenure problems and the uneven distribution of land-holdings
Government subsidization of counterproductive land-use programs
Political backlash caused by the influence of developed countries on land-use and
on conservation decisions of lesser-developed countries
Violent conflicts, especially over natural resources

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TROPICAL SUSTAINABLE DEVELOPMENT / 395

difficult to achieve (e.g., Pinedo-Vasquez et al., 1992), but strategies are being
developed (Clay, 1992a,b,c).
Existing political economies in the tropics can promote environmental im-
pacts (Hecht, 1993; Schmink, 1987). The recognition of this problem has led to
an exciting new approach, termed “political ecology” (Schmink and Wood, 1987;
Thrupp, 1990). This approach goes beyond combining economic and ecological
perspectives to add the political context within which land-use decisions are
made. Political ecology is helping to identify the complexity of tropical prob-
lems, but new political economies are needed. Accounting systems are being
developed that may fill these needs (Ahmad et al., 1989; Costanza and Daly,
1992; Godoy, 1992; Odum, 1984; Repetto, 1992), but they are difficult to imple-
ment. Areas that are undergoing economic upheaval, such as Brazil and the
Eastern European countries, may be the most likely candidates for the imple-
mentation of these new approaches to accounting and valuation.
The typical pattern of land-holdings for a tropical country is where a large
portion of land is controlled by relatively few wealthy people and the remaining
small portion of land is divided among a large number of poor people. This
uneven distribution leads to social problems that can inhibit wise land-use strat-
egies and encourage deforestation (Eckholm, 1979; Rudel, 1993). Approaches
for redistributing wealth, such as the development of new markets for rural
people described earlier, may help mitigate this problem. The concept of extrac-
tive reserves was developed in part to deal with this problem. Rural people
would have access to these lands to generate income through harvest of non-
timber products (Fearnside, 1989). However, controversy exists as to whether
or not sufficient income can be derived from extractive reserves, at least under
conditions in the Amazon (Browder, 1990; 1992a,b; Vantomme, 1990).
The problem with government subsidy of bad land-use has been demon-
strated by analyses given in Repetto (1988) and Repetto and Gillis (1988). These
authors provide many examples, perhaps the best known of which is the tax
incentive program that was provided to ranchers in the Amazon during the
1970s and 1980s. This program led to much deforestation and subsequent de-
clines in productivity of pastures. These subsidy programs can be difficult to
overcome because they have support for political reasons, which can supersede
the wise use of land.
Political backlash can occur when one country interferes with the sover-
eignty of another. Several examples of this phenomenon are known from Brazil,
whose government has been criticized for deforestation by conservation groups
in developed countries (Guimaraes, 1991). Stimulated by a World Bank publica-
tion, a major controversy arose concerning rates of deforestation in the Amazon
(Fearnside, 1990; Golden, 1989; Mahar, 1989; Neto, 1989a). As a consequence,
the President of Brazil even stopped accepting financial support from foreign
conservation organizations because he feared that they were having too much
influence on Brazilian land-use decisions. This position was soon reversed, but

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396 / BIODIVERSITY II

it illustrates the potential magnitude of political backlash (Radulovich, 1990).

Other Amazonian examples of backlash have involved a benefit rock concert
(Neto, 1989b) and the advocacy actions of a foreign anthropologist (Anonymous,
1989).
War and violent conflict can severely inhibit conservation and sustainable
development (Homer-Dixon et al., 1993). During such times, priorities change
and environmental values frequently are overlooked as conflicts are resolved.
An example from the Neotropics was the “Soccer War” between El Salvador and
Honduras in 1969 (Durham, 1979). The “war on drugs” in tropical countries
also leads to both social and environmental problems (Goodman, 1993a; Kangas,
1990).

HISTORY LESSONS FOR TROPICAL SUSTAINABLE DEVELOPMENT

One way to gain perspective on the problems associated with sustainable
development is to look to history. Analogous examples of conservation strate-
gies from Table 26-1 and impediments to sustainable development from Table
26-2 have occurred in the past. Comparative analysis of these examples poten-
tially can provide inspiration and insight for present-day issues. Historical fail-
ures or problems can be lessons to learn from, and historical successes can be
models to emulate. Thus, using Deevey’s metaphor for historical ecology
(Deevey, 1969:40), we “coax history to conduct experiments” in sustainable
development with 10 examples.

The Titanic Effect and the Collapse of the Maya

The Mayan civilization of Middle America reached remarkable achieve-
ments in art, architecture, science, and social organization from approximately
A.D. 300-900. This civilization developed a sophisticated culture in a rain forest
environment that supported a high population density with intensive agricul-
ture. However, in spite of all of their achievements, the Mayan civilization
collapsed after A.D. 900, with depopulation of urban sites, loss of cultural knowl-
edge, and dramatic social transformations (Culbert, 1973; Lowe, 1985). A num-
ber of causes have been suggested for the collapse, including malnutrition, dis-
ease, foreign invasion, internal civil uprisings, and agricultural decline.
Environmental degradation certainly occurred and played a role in the collapse
(Abrams and Rue, 1988; Deevey et al., 1979). The dimensions of the collapse of
Mayan civilization remain a mystery, but the lesson seems clear (Rice and Rice,
1984). Sustainability is not assured, not even for a high civilization such as that
of the Maya. This seems to be an example of what Watt (1974) has termed “the
Titanic effect.” The Titanic was considered to be so unsinkable that it was not
even equipped with an adequate supply of life preservers. When it struck an
iceberg and sank, there was considerable loss of life. During their classic period,

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TROPICAL SUSTAINABLE DEVELOPMENT / 397

the elite of the Maya, surrounded by their beautiful cities and volumes of books,
must have thought their society and economy was without limit. They were
wrong, and we must learn from their failure to develop systems that were sus-
tainable.

Henry Ford’s Sustainable Villages

Henry Ford was a dynamic man who revolutionized America through his
contributions to the auto industry in the early 1900s (Wik, 1972). He developed
an effective line of automobiles and an industry that could mass-produce them.
In developing this industry, he also pursued related social agendas that included
worker benefits, international relations, and the state of agriculture. One of his
agendas was the decentralization of his industry and the back-to-the-farm move-
ment. This philosophy became embodied in his “village industry” network in
southeastern Michigan. In each small town, he built a factory for automobile
parts, usually manned by part-time farmers and supported by a hydroelectric
power plant. Each community had an element of self-sufficiency, but they also
were connected to each other through the parts of the automobile that they
produced. This was a type of utopian plan that was fairly successful until the
region became more diversified with the growth of the country. Perhaps Ford’s
village industry philosophy could be a model for tropical landscapes with sus-
tainable mixtures of wilderness, agriculture, and towns (Janzen, 1990; Lugo,
1991).

The American Civil War and the North-South Dichotomy

The Civil War in the United States was the most costly war in American
history in terms of loss of life. It originated from a North-South dichotomy that
is reminiscent of the current global dichotomy between developed (“North”)
and less-developed (“South”) countries. The American North-South dichotomy
arose early in colonial times from differences in cultural background of the set-
tlers and differences in land-use as determined by geography and climate. The
dichotomy solidified after the revolutionary war, with the North becoming pri-
marily industrial and commercial and the South remaining primarily agrarian.
At the beginning of the Civil War, these differences were dramatic. The North
had five times as many factories and more than double the population of the
South, which was dominated by monoculture crops such as cotton, tobacco, and
rice, as well as pastures for beef cattle production (Flato, 1960). Slavery was
common to both the North and the South before the American Revolution and
was not the primary factor that originally distinguished the two regions. How-
ever, slavery quickly declined in the North, and by the early 1800s became an
important issue in distinguishing the North and the South.
The end of the Civil War (1861-1865) was followed by the Reconstruction

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398 / BIODIVERSITY II

Era, which lasted 10-15 years and consisted of political attempts to manage the
process of reuniting the divided country (Franklin, 1961; Lynd, 1967). In general,
Reconstruction was dominated by corrupt politicians and shrewd businessmen
(i.e., carpetbaggers) who failed to generate economic and social development.
The obvious lesson of the American Civil War is that dichotomies, such as
that between the North and South, which are characterized by extremely un-
equal distributions of wealth and industrial development and strong relations of
dependency, are not stable and can result in violent conflict. (The slavery issue
is not a critical qualification to this analogy. Brazil was able to emancipate slaves
without violent conflict, in part because there was no major regional dichotomy
underlaying slavery.)
The Reconstruction Era also may provide lessons on how not to stimulate
development in a depressed region. There are similarities with recent develop-
ment efforts in Africa, which have been described by the metaphor of “tropical
gangsters” (Klitgaard, 1990). Thus, some nations in the tropics now are facing
some of the same problems of development that the South had to face after the
Civil War.

Tropical Partnerships for Transportation and Development

An important aspect of tropical development has involved the actions of
large foreign companies. The American-owned fruit companies of Central
America are good examples: Standard Fruit (Karnes, 1978) and United Fruit
(Adams, 1914; May and Plaza, 1958). These companies began operations in the
Atlantic lowlands of Central America in the late 1800s with the primary focus of
production being bananas. Towards this objective, thousands of hectares of
rain forest were converted to banana plantations in an export business which
was established to supply the demands of a rapidly growing market in the United
States. As time passed, the negative aspects of this form of land-use became
obvious: loss of watershed protection, reduction in diversity, local economic
dependence on a monoculture, exportation of the crop, and degradation of wa-
ter quality. Certainly these are social and environmental impacts that perhaps
could and should have been avoided. However, at least in some cases, there also
were positive aspects of the presence of foreign companies in the tropics, includ-
ing improvements in health care and infrastructure. In particular, the construc-
tion of roads and railroads was a benefit in the sense that capital would not have
been available for these developments without foreign input. Often the trans-
portation networks were designed to meet the needs of the company, i.e., move-
ment of bananas to coastal ports, but they also were used for the benefit of local
populations. Transportation infrastructure, especially roads, has been recog-
nized as leading to deforestation and nonoptimal land-use by opening terrain
that previously was not available to land-poor farmers. The tropical road has
become “the symbol of modern deforestation” (Forsyth and Miyata, 1984). Per-

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TROPICAL SUSTAINABLE DEVELOPMENT / 399

haps this negative view needs to be balanced by the positive aspects of transpor-
tation networks. One example of the positive aspect has been noted by Clay and
Clement (1993:21): “The development of markets for sustainably harvested com-
modities and the destruction of the rainforests both depend, ironically, on the
same thing: improved transport systems . . . Forest residents have long realized
that roads are both their salvation and their demise.” Although alternative trans-
portation systems need to be researched, roads will continue to play an impor-
tant role in tropical development. In this regard, partnerships between conser-
vationists and foreign companies, such as the old United Fruit Company, may
provide the means for this planning.

The Columbian Exchange and Marketing of Nontimber Products

Although Christopher Columbus may have been disappointed that his voy-
ages did not discover the trade route to Asia, the “Columbian Exchange” of
materials, species, and cultures that he initiated was dramatic (Crosby, 1972;
Viola and Margolis, 1991). One of these exchanges (New World foods) may
represent a model for current efforts to develop markets for rain forest products.
The New World provided many species of food for the Old World, including
maize, potatoes, cacao, and others (Foster and Cordell, 1992). Some of these
were similar to species used for food in the Old World and diffused easily. Oth-
ers, such as potatoes and tomatoes, were unlike anything in the Old World and,
thus, took longer to be accepted. Davidson (1992) describes some reasons why
people were reluctant to take up certain New World foods and why other foods
were accepted quickly. The process of acceptance of a foreign food item that
occurred with these species from the New World may provide ideas and inter-
esting contrasts with efforts being made to market rain forest products in the
United States and Europe. Clay (1992a,b,c) discussed this new marketing chal-
lenge, drawing heavily on his experience with the organization called Cultural
Survival. This effort requires information on biology, ethnology, food science,
international trade, and business. Several nongovernmental conservation orga-
nizations are working on these exchanges, which involve paying producers a
fair world price or sending a portion of the profits back to the tropical cultures
that produced the item, as with other forms of biodiversity prospecting. The
marketing of rain forest products is not limited to food items, and the New
World to Old World “Columbian Exchanges” also may provide useful insights
for facilitating other efforts in present-day marketing of products related to con-
servation.

Ideas From the Origin of Agriculture

The origin and spread of agriculture was one of the most important devel-
opments in human history (Anderson, 1956; MacNeish, 1991). It occurred be-

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400 / BIODIVERSITY II

tween 7,000 and 12,000 years ago and marked the transition between the old
Stone Age (Paleolithic) and the new Stone Age (Neolithic) periods. The advent
of agriculture and the related sedantism that more or less occurred simulta-
neously changed the cultural capacity of humans and led to urban civilization.
This process has been called the Agricultural Revolution, and it embodied a
number of changes resulting in new forms of land-use. As we now search for
new and sustainable land-uses, the literature on the original Agricultural Revo-
lution may represent a source of ideas. For example, the idea of cultivation of
crop species is thought to have spread from centers of origin to prospective
farmers in surrounding regions through a diffusion process (Harlan, 1971; Sauer,
1952). This process must have involved communication of the benefits and risks
of new crops or cultivation methods. The current need in the tropics is similar
to some extent in that we must spread new forms of sustainable agriculture and
forest-use to rural peoples. Perhaps the theories for how agriculture originally
spread can help us now devise new forms of technology transfer. Kangas and
Rivera (1991) suggested that existing agricultural extension services may pro-
vide a mechanism for the flow of information about sustainable land-use. Exist-
ing models of the diffusion process (Fliegel, 1993; Rogers, 1983) can readily be
adopted for this purpose.
Another example involves the role of women in the origin of agriculture.
Women probably played a critical role in all aspects of the Agricultural Revolu-
tion, including selection, domestication, harvest, storage, and preparation of
new crops and food products (Ehrenberg, 1989). Women recently have been
seen to be a significant element in planning for sustainable development
(Abramovitz and Nichols, 1992; Braidotti et al., 1994), and perhaps they can be
targeted to play important roles in the adoption of sustainable land-use options,
as they did in the original Agricultural Revolution.

Amazonia and the Louisiana Purchase

The vastness of the Amazon basin long has been a stimulus to the imagina-
tion of people who wish to exploit its resources. This has led to explorations
from the time of Orellana (Gheerbrant, 1992) to recent times (Cousteau and
Richards, 1984). These explorations resulted in both a romantic literature (Preto-
Rodas, 1974) and assessments of resources that have been used as a basis for
public policies (Tambs, 1974). Unfortunately, the images of the Amazon have
not always been accurate and have lead to unrealistic expectations. Jordan
(1982) describes one example in relation to agricultural potentials, which never
were realized.
A somewhat similar situation existed in American history with the Louisi-
ana purchase of 1803. The United States acquired land from France that, in one
stroke, more than doubled the size of the country. This land extended from the
colonial frontier through the Mississippi and Missouri River watersheds. It con-

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TROPICAL SUSTAINABLE DEVELOPMENT / 401

Aerial view of the Amazon River.

tained unknown resources that were the basis for ambitious images of rich and
rapid development (Allen, 1975). Thomas Jefferson commissioned the Lewis
and Clark expedition to explore the northwest, and the work of this expedition
both qualified and expanded the development images. The lesson here is that
images are an important part of the development process, but that they also can
be detrimental to the extent that they mislead development (Lugo and Brown,
1981). Perhaps careful analysis of historical examples, such as the development
of the American northwest, can provide useful information for the development
of tropical areas such as the Amazon.

Export Agriculture in Central America and the Chesapeake Tidewater

Central America’s economy has been characterized by a reliance on export
agriculture. Originally, the focus was the “dessert economies” or luxury crops
of coffee, sugar, and bananas. After World War II, cotton and beef gained in
production. These exports primarily have gone to Europe and the United States,
where the crops either cannot be grown or, at least, cannot be grown as cheaply
as in Central America. The resulting relationship of dependency has negative
effects on many aspects of the Central American economy, environment, and
society (Boucher et al., 1983; Pelupessy, 1991; Williams, 1986).
A similar situation has characterized the southern region of the United
States. In fact, Persky (1992) uses the Latin American example as a model for

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402 / BIODIVERSITY II

southern economic history. One example was the colonial tobacco agricultural
system of the Chesapeake Tidewater areas of Maryland and Virginia. From the
late 1600s until after the Revolutionary War, large plantations of tobacco were
developed in the tidewater area for export to England (Breen, 1985; Goodman,
1993b; Kulikoff, 1986). A strong dependence arose, with the American planters
exchanging tobacco for clothes, farm machinery, and other supplies from En-
glish merchants. This was a classic case of exchange of raw materials for manu-
factured goods with a trade deficit. Accordingly, the planters fell seriously into
debt over time. Many went bankrupt and were thrown into debtors’ prison,
but a few were able to switch to more balanced agricultural production that
served a domestic market. The best example was George Washington, who
gradually switched from production of tobacco to wheat and corn, which he
exchanged with merchants in nearby Philadelphia for American-made goods
(Mee, 1987). Other examples are described by Clemens (1980) for Maryland’s
Eastern Shore. Thus, some of the colonial planters were able to diversify their
production and reach new markets. This is a strategy that has been recom-
mended for Central America (Tucker, 1992). The transition will be difficult, but
helpful insight might come from analysis of the colonial Americans who were
able to escape dependence on England some 200 years ago.

Puerto Rican Deforestation and Reforestation

The history of Puerto Rico provides an interesting microcosm of tropical
land-use dynamics and development (Dietz, 1986). When Columbus visited the
island in 1494, people of the Taino culture occupied the landscape with a rela-
tively low population density. Over the following 400 years, the Spanish colo-
nized the island and converted the landscape from tropical forest to a mix of
export crops (primarily sugar cane, coffee, and tobacco) and subsistence farms.
Puerto Rico was ceded to the United States after the Spanish American War of
1898, but the agricultural focus continued until the 1940s, when industrializa-
tion became dominant. During this period, there was a shift in social structure,
with a decline in agriculture and an increase in industrial employment. The
island became more strongly tied to the mainland United States and, in a sense,
the people became uncoupled from the land. Although there were problems
with this development process (Sanchez-Cardona et al., 1975; Weisskopf, 1985),
a byproduct has been a net conversion of land-use from agriculture to forest.
This has been a dramatic change; forest area has increased from a low of about
9% of the island in the early 1900s to nearly 35% in the 1980s (Birdsey and
Weaver, 1982, 1987).
Although this is a special case involving a unique set of sociopolitical cir-
cumstances, it does demonstrate that tropical forests are resilient and that defor-
estation is not irreversible. In this case, there was no active reforestation, and
the increase in forest area was due to natural succession on abandoned crop land

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TROPICAL SUSTAINABLE DEVELOPMENT / 403

and pastures. If active programs of reforestation had been employed, the results
could have been larger. Thus, the historical case of Puerto Rico provides incen-
tives to develop programs that will allow restoration of tropical forests on de-
graded landscapes.

The Civilian Conservation Corps and Tijuca Forest

The Civilian Conservation Corps (CCC) probably was the most massive pro-
gram of human and natural resource management in American history (Lacy,
1976). From 1933-1937, more than a million young men were employed by the
federal government to work on a variety of natural resource projects. The CCC
program was devised by Franklin D. Roosevelt as part of the New Deal, prima-
rily as a way to increase employment during the Depression. The program was
restricted to unemployed and unmarried young men between 18-25 years of age
who signed up for tours of between 6 months and 2 years. During work tours,
men were clothed, housed, fed, and paid a modest wage. Men lived in simple,
rustic camps located near work projects, which included such activities as for-
estry, prevention of soil erosion, and flood control. The program involved a
rapid, large-scale mobilization of both manpower and facilities and was accom-
plished by incorporating the War Department in a supervisory role. The U.S.
Army played a major role in organizing the men, while other departments, in-
cluding Interior, Agriculture, and Education, supervised the actual work in the
field. The program also had the goal of training the men so that they could find
employment after they left the Corps. Thus, the CCC was both an ambitious
social program that provided employment and training to primarily unskilled
men and a major capital works program that resulted in the following significant
accomplishments, which occurred after just the first year: “. . . construction of
25,000 miles of truck trails; 15,000 miles of telephone lines; 420,000 erosion
check dams; disease and insect control on 3 million acres of forest; 98 million
seedlings planted; forest stand improvement on a million acres; and 687,000
man-days of fire fighting” (Lacy, 1976:38).
Another example of this type of large-scale deployment of manpower oc-
curred with the reforestation of Tijuca Forest in Rio de Janeiro during the late
1800s (Por, 1992). The Emperor of Brazil had the coffee plantations converted to
forests in order to save the water supply of the city. It was a massive program,
organized by the army and carried out by slaves, that involved the planting of
more that 100,000 trees. Today, Tijuca Forest is a national park with a magnifi-
cent rain forest that is surrounded by the city of Rio de Janeiro.
In both historical cases described above, a large-scale, labor-intensive pub-
lic works program in natural resource management was conducted in re-
sponse to a crisis. Perhaps similar programs can be initiated now in response
to the current crisis of tropical deforestation. If properly managed, they could
have multiple positive effects, as did the historical examples of the CCC and

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404 / BIODIVERSITY II

Tijuca Forest. Perhaps some aspects of the historical examples could be used in
the new programs, such as the use of the military as a positive, organizing
authority.

CONCLUSIONS
The 1986 National Forum on BioDiversity (Wilson and Peter, 1988) focused
interest on biodiversity and helped to bring the subject to the attention of both
policy-makers and the general public. Sustainable development is needed to
improve the standard of living of tropical people, but it is especially needed to
conserve biodiversity (National Research Council, 1992). In fact, as Janzen (1990)
noted, these goals are not independent, but instead they must be tied closely
together if conservation is to be successful. Biodiversity is needed to help main-
tain the global life-support system of humanity and as a direct source of prod-
ucts for the economy of humans. Thus, a symbiotic relationship between sus-
tainable development and biodiversity in the tropics must be designed.
The main value of the history lessons described in this chapter (Table 26-3)
may be to illustrate that at least some of the current problems of development in
the tropics are not new. Although the tropics present unique problems
(Kamarck, 1976), many ideas for sustainable development are being tested, and
history can provide more models. However, there is an urgency for tropical
sustainable development that is new.
Sustainable development presents multidisciplinary and interdisciplinary
challenges and has led to hybrid approaches such as political ecology, conserva-
tion biology, and ecological economics. Thus, biologists are learning how to
market rain forest products and economists are learning the importance of spe-
cies diversity in ecosystems. One hopes that there is time to learn these lessons
before tropical biodiversity becomes seriously degraded.

TABLE 26-3 Summary of Historical Lessons for Sustainable Development

Sustainability should not be taken for granted

Self-sufficiency should be a development goal, but it should be balanced with linkages to
other communities
North-south dichotomies are a liability
Cooperation between conservationists, foreign companies, and other large businesses should
be encouraged rather than focusing on negative aspects
New markets for exotic items, such as nontimber rain forest products, should be encouraged
Technology transfer is necessary for communicating ideas about sustainable development
There may be unique roles for women in sustainable development
Images and expectations of development should be explicitly analyzed and should be realistic
A regional agricultural system of exportation with strong dependency can be diversified
Deforestation is not necessarily irreversible
Large-scale public works projects can provide employment and achieve environmental goals

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TROPICAL SUSTAINABLE DEVELOPMENT / 405

ACKNOWLEDGMENTS
Campbell Plowden and the editors provided many useful comments. Staff
at the National Colonial Farm and the Accokeek Foundation in southern Mary-
land provided inspiration for many of the historical analogies presented here.

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CHAPTER
27

Wildland Biodiversity Management

in the Tropics1

DANIEL H. JANZEN
Professor, Department of Biology, University of Pennsylvania, Philadelphia

Humans have been studying the biodiversity of wildlands as long as there

have been humans. The goal was extirpating, eating, avoiding, inhaling, do-
mesticating, controlling, and predicting. We have sought simplification and
homogenization of the natural world to facilitate these activities.
The outcome is that today any given tropical nation or large multinational
region has three basic kinds of land-use: urban, ever more intensively managed
agroscape, and ever dwindling wildlands. The latter are generally patches of
comparatively biodiverse habitats on socially or physically inaccessible sites or
on “poor” agricultural soils.
The urban habitat is viewed as productive even if restive. The agroscape is
productive, with largely pacific and homogenized biodiversity. The wildlands
largely are viewed as removable, conservable, or conserved; i.e., they have been
set aside by someone “else” for strip-mining of their natural products or for
social fossilization, outside of the national economy. They are like cash in a
shoebox under the bed, neither earning interest nor circulating, but of value to
someone.
This perception of tropical wildlands is unfortunate, and fortunately it is
waning in popularity. There are encouraging nuclei of voices dotted across the
tropical (and extra-tropical) landscape arguing that conservable and conserved
tropical wildlands are a category of highly productive land-use. Conserved
wildlands are a different kind of field, just as ecotourists are a better kind of

1Derived from D. H. Janzen. 1994. Wildland biodiversity management in the tropics: Where are

we now and where are we going? Vida Silvestre Neotropical 3:3-15.

411

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cow, just as drug precursors are another kind of cotton, just as literacy in
biodiversity is another kind of rice. In contrast to pastures, fields, and paddies,
all three products of biodiversity—and many more—can come from the same
hectare.
Such a shift in social and economic attitudes demands that a conserved wild-
land be blessed with the level of planning, knowledge, investment, oversight,
budget, technology, and political attention that long has been characteristic of
the more productive sectors of the agroscape, and also of a nation’s institu-
tions—highway systems, hospitals, education, and communication. Traditional
tropical conserved wildland management—”fence it and put a guard on it”—is
to such a blessing as a guard at the bank’s front door is to the stock market,
Federal Reserve, free market economy, taxes, and trade barriers all rolled into
one.
We may anticipate a new edition of “potential land-use” maps for tropical
countries. This is really what the “thou shalt inventory thy biodiversity” com-
ponent of the Biodiversity Treaty is all about. No longer will there be a soil and
contour map marked “apt for agriculture,” “apt for forestry,” and “apt for con-
servation,” with conservation meaning “useless” and therefore to be assigned to
the national park service or its equivalent. Rather, these maps will show what
has been explicitly designated as agroscape and wildlands conserved for their
biodiversity and its nondestructive use, with awareness that any hectare of a
nation can be developed as either, depending on society and history rather than
on soil type, rainfall, slope, and distance from a road or border war. The overall
goal will be to render both types of land-use to be sustainably productive, high
quality, and much valued by a nation and a region.
Up to the present, relatively nondamaging consumption from wildlands—
humanity’s hallmark during the first 99% of human evolution—gradually has
lost out in competition with the agroscape. Today’s wildlands appear to be
substantially less productive than are many kinds of agroscapes. Humanity has
cleared the way for its domesticates—including humans that function as urban
or rural draft animals—and invested huge amounts in domestication. However,
as the agroscape becomes ubiquitous across the tropics, the value of conserved
wildland that is multiply used increases for society as a whole, and for nations
specifically, because of its scarcity. Simultaneously, as the desires of humanity
become more diverse and more perceptive, the value of a unit of wild bio-
diversity increases. Finally, as the knowledge base of humanity increases in
bulk and interconnectivity, the intrinsic potential for multiple use of a unit of
biodiversity increases. All of these increases are proportional to our investment
in them.
The outcome is that a smart, modern, tropical government explicitly farms
and ranches the information in an explicitly designated portion of its wildland
biodiversity, just as a smart government resists pulping its national library dur-
ing a newsprint shortage or using Internet cables to construct fences. It uses the

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WILDLAND BIODIVERSITY MANAGEMENT IN THE TROPICS / 413

income generated, in many currencies, to support the costs of managing the

conserved wildland, further its development, and meet its costs of opportunity.
This builds employment and capacity. This is sustainable development—living
off the interest rather than consuming the capital.

WHERE ARE WE NOW, AND WHERE ARE WE GOING?

We are at a crossroads. Do we allow the progression of tropical land-alloca-
tion to conserved wildland biodiversity to continue as has been the case for the
past 2,000 years? If so, 10-30% of tropical terrestrial biodiversity eventually
will be conserved in 1-2% of the tropics. The locations of this remnant will be
the serendipitous outcome of a multitude of social and economic forces acting
largely irrespective of biodiversity’s traits. One example of this process is that
there are no unambiguously conserved large tropical wildlands on “good” agri-
cultural soils. This “happy accident” strategy for conservation of tropical
biodiversity will continue unabated if there is no major shift in social attitudes
and economic processes. This strategy is quite comfortable for the majority of
individual, national, and institutional agendas in the contemporary tropics.
The “use it or lose it” strategy is the other road. Less comfortable, it envi-
sions 80-90% of tropical terrestrial biodiversity conserved in 5-15% of the
tropics. The locations will be the serendipitous and planned outcome of a
multitude of social forces acting irrespective of, and with respect to, the traits
of biodiversity.
The major shift in social attitude and economic forces that are required by
the “use it or lose it” strategy is that tropical conserved wildlands are conserved
for nondamaging use by all sectors of society rather than because they are waste-
lands, for our grandchildren, for the sake of conservation, crown jewels, bio-
diversity-prospecting pits, observation posts for bar-coded horses, or to fill the
agenda of any other single social sector. Each of these seven sacred and reason-
able cows, and a whole herd more, become byproducts and ingredients, rather
than the goal. This needs to be true even if each today is of major importance
somewhere in the tropics. This attitude is somewhat akin to recognizing that
the value of good agricultural soil or quality roadworks is not in the specific
crop or the specific truck, but rather in being a platform on which society car-
ries out a multitude of diverse activities.
The unhidden agenda is to move tropical wildlands into that social category
of “so useful to society that no matter what form a society or nation takes, tropi-
cal wildland biodiversity will be woven into and through it”—as is the case
with health, education, welfare, market economics, and communication.
Should someone mistake this essay as an argument for the simple commer-
cialization of tropical wildland biodiversity, please note that humanity has in
fact won the basic battle against terrestrial nature. It is not if, but how. Wild-
lands are rapidly becoming historic events. We are no longer afraid of the dark,

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414 / BIODIVERSITY II

spirits are no longer The Cause. We are in fact polishing the globe clean of most
wild biodiversity that weighs more than a gram through species-specific har-
vest, habitat destruction, and contamination. Even the little things—fungi,
bacteria, insects, and their brethren—are being removed or thoroughly impacted
by these processes.
If we do indeed sweep the battlefield of the wild things, if we do reduce our
globe to the playground of domesticates, we consign humanity to the doldrums
of just those things that humans can imagine, invent, and control. We as thor-
oughly deprive ourselves as if we excise our color vision, our sense of smell but
for frying chicken, our taste but for salt and sugar, our hearing but for high,
low, and middle C. The brain is a computer with tens of thousands of applica-
tions invented to deal with nonhuman nature. By the removal of tropical wild-
land biodiversity, we are permanently relegating it to word processing. But the
other side of the coin is that our appreciation for superlative architecture does
not demand that we have only those buildings that will win international prizes.
There is a place on the landscape for a healthy agroecosystem as well as the
wildland crop.
Because the emphasis throughout this chapter is on “use it or lose it,” there
are several caveats, all of which are traditional in other social sectors but have
been slow to be applied to conservation. They boil down to several equivalent
expressions. The frontier is gone. You are always in someone’s living room.
Tropical biodiversity must escape the Tragedy of the Commons. There is no free
lunch. The only sure things are death and taxes. Applying these age-old con-
cepts to the case at hand:
• The more we know about wild biodiversity, the more we can use it with-
out destroying it.
• Not all persons can use wild biodiversity as much as they would like.
• The use of wild biodiversity must be scheduled and monitored.
• There are all sorts of users.
• Users pay in all sorts of currency.
Tropical wildland biodiversity needs detailed, knowledgeable and dedi-
cated management as much as does any other social sector. Ironically, since it
is so underdeveloped, the returns on an additional unit of investment in fact
are likely to be often substantially greater than is the case with many well-
developed sectors.

THE MORE WE KNOW ABOUT WILD TROPICAL BIODIVERSITY,

THE MORE WE CAN USE IT WITHOUT DESTROYING IT

What Do We Need To Know?

In order to begin to use wildland biodiversity, we must come to know:

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• What it is: Identification and taxonomy.

• Where it is: Microgeography.
• How to get it in hand: Trappers’ tricks and husbandry.
• What it does: Basic natural history.
All of this must come to be in the electronic public domain, because hard
copy is not functionally public, is out of date the minute it is published, and
does not have the opportunities for massage and recombination that is so easy
with electronic media.
Identification and Taxonomy. We need to know what biodiversity is so
that we can:
• know its parts when we see them,
• communicate about it today,
• pool and massage our information about it, and
• link what we find out with what others have found out.
The latter is of particular importance with tropical biodiversity, much of which
has geographic distributions spreading across many countries. With an accu-
rate identification, the user in one country has potential access to all the infor-
mation that has been accumulated about that species across its range, rather
than being dependent solely on local knowledge.
There is a second and equally powerful reason to know what are the compo-
nent parts of biodiversity. By knowing what it is—that is, by putting a Latin
binomial on it—the species is placed within the purview of taxonomy’s enor-
mous power of inference. This inference is based on relatedness as expressed
through grouping into genera and higher taxa and is derived from gene to whole-
organism similarity. Placement of a species in a higher taxon is more than for
filing convenience. It tells one what to expect of that species, based on what we
know of the others in its taxon. Full realization of this kind of knowing de-
mands a electronic database based on observations and specimens. These must
back up the derivative information bases and knowledge bases that are derived
from information on species.
Microgeography. We need to know where biodiversity resides, or at
least where a portion of it resides, so that we can get to its location “on call.” A
catalog of the books in a Library of Congress is of severely reduced use if there
is no knowledge as to where the books are to be found, even if they can be
recognized and read once in hand.
Trappers’ Tricks and Husbandry. We need to know how to get bio-
diversity to hand or eye so as to get the information that we seek or can use from
it. All hunter-gatherers and their field-biologist counterparts long have experi-
enced the circumstance where a species is known and appears to be absent,
yet—with the appropriate collection method—the species appears in droves.

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416 / BIODIVERSITY II

We also need to know how to get biodiversity to hand so that we can care for it
and multiply it, so that with this husbandry we can introduce it to the
agroscape—rural or urban.

Basic Natural History. We need to know what biodiversity does—its

natural history in the broadest sense—so as to:

• give us clues as to what it offers by itself and through its interactions;

• suggest how to farm it elsewhere;
• allow us to know the impact of our presence, studies, and sampling; and
• allow us to know when it is in trouble and what to do about it.

The first three of these four needs tend to be open-ended and cumulatively
solved and, for a given site, require progressively less investment per species
across time. However, understanding of natural history is ever-expanding and
peaks much later, if ever, in the cycle of involvement.

How Do We Get This Information?

Taken in collaboration, the four activities above represent genuine bio-
diversity inventorying, and they constitute the real base on which biodiversity
management is constructed. They also fully recognize that management for a
given site can be built on one or more inventorying activities as the others are
being developed.
These four activities can be, and will be, carried out by a diversity of per-
sons for a diversity of agendas in a diversity of wildland sites. However, a
tropical nation with species-rich conserved wildlands may well be fortunate
enough to have >100,000 hectare blocks containing 100,000 to a million species
and all their interactions. In such cases, a major strategy for biodiversity man-
agement and development is to select—in the context of a nation’s full gambit of
users and managers—a site, and rapidly inventory all of its species. This is an
All Taxa Biodiversity Inventory (ATBI). The function of an ATBI is to set up a
major block of a nation’s wildland biodiversity for all users. It:
• projects a massive block of diverse raw materials onto society’s table,
• enjoys substantial economies of scale,
• foments mutualistic gains among executors as well as among users, and
elevates biodiversity inventory far beyond being a taxonomist’s tool or a con-
servationist’s listing.
When ATBIs occur in various countries and are firmly networked, a global
network of these four advantages of an ATBI can and should be achievable. For
example, this has been envisioned through the DIVERSITAS network as visual-
ized by the United Nations Educational, Scientific, and Cultural Organization
(UNESCO), and will be realized in the biodiversity clearinghouses of the Bio-

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diversity Convention. An ATBI is a major advance over the diffuse and dilute
approach currently in play, an approach clearly rooted in the time-honored tra-
ditions of curiosity-driven and highly individualistic field biology as performed
by taxonomists and ecologists.
Why must all this activity be in the electronic public domain? First, in
contrast to the past centuries of “public” publication of information on wildland
biodiversity, which was aimed almost entirely at the very specialized audience
of the scientific community, we now have the technical opportunity and ability
to put information about tropical biodiversity truly in the national and global
public domain through world-level electronic networks. Second, the goal of
tropical wildland biodiversity management is to imbed it in society—all sectors
of society and not just those with access to scientific journals and preprints.
Third, the greater part of tropical terrestrial biodiversity is international; bio-
diversity represents a global effort even if a nation is the primary custodian.
What we know, and will come to know, of the wild silkmoth Rothschildia lebeau
is based on the aggregation of information from studies in Texas, Mexico, Costa
Rica, Venezuela, and Colombia, among others, and conducted for a multitude of
reasons—schoolyard exercises, pharmaceutical prospecting, ecotourism guid-
ing, silk research, insect disease transmission, and religious symbolism. Ques-
tions of the ownership of information, costs, and charges—such unfamiliar
ground for the community of taxonomists, ecologists, and conservationists—
have very much in common with the well-worked terrain of ownership, costs,
and charges for other social sectors such as trails, roads, highways, waterways,
and airports.
The other side of public domain is the responsibility to actually conduct
ATBIs and other kinds of inventories and the subsequent management and de-
velopment of wildland biodiversity. Much of what commonly has been the
social responsibility of the traditional academic/museum community on the one
hand, and “park guards” or distant government offices in the capital city on the
other hand, can be passed most profitably to parataxonomists, paraecologists,
ecologists, educators, ecotourism guides, administrators of biodiversity, and
other forms of site-based paraprofessionals. There is huge potential in training
residents that neighbor the conserved wildland or live in it. They can accept a
major portion of the responsibility to carry out nondamaging management and
user-processes. This transfer of power and decentralization is essential for mov-
ing beyond what is today largely management of tropical wildlands by absen-
tee-landlords.
This transfer, however, does meet with two major classes of social resis-
tance. First, the scientific community understandably is reluctant to invest the
energy and modification of tradition that will bring this about without compen-
sation by senior administrators of science and by society at large. There are
widespread benefits that could result from such a leveling of the playing field,
and some of these need to feed back to its contributors. Second, such a transfer

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418 / BIODIVERSITY II

of political and economic power to rural areas—in modern parlance, decentrali-

zation and management horizontality—is theoretically attractive but very diffi-
cult to bring about in the face of contemporary vertically organized society. A
large and properly managed conserved wildland dances dangerously close to
secession from the federal state in virtually all tropical countries.

What Do We Not Need To Know?

I have tried to stay away from counterproductive commentary on alternate

trade routes to the same new world. However, to put the above schema for site
management and ATBIs in clearer perspective, I would like to suggest ever so
gently a few areas in biodiversity biology where energy might be more produc-
tive for long-term conservation of biodiversity if spent elsewhere. These com-
ments are likely to receive mixed reviews from the ranks of biodiversity biolo-
gists. These comments run in direct conflict with the very human behavior of
attempting to mold the newly emerging activity of conservation of biodiversity
so that its energy feeds one’s entrenched agenda rather than targets the goal that
elicited the activity—conservation of biodiversity.
• We do not need to know how many species there are in the world, in a
country, in a large conserved wildland. We already know that there are hun-
dreds of thousands to millions of species, and most are unknown in most re-
spects. That is enough information to get on with knowing biodiversity and
setting it up for nondestructive use. It is not shameful that “science” does not
know whether there are 10 million, 30 million or 100 million species of organ-
isms, and it is a waste of precious time and human resources to focus on refining
this estimate. Would the conservation of biodiversity be aided for us to know
that there are 502,451 species in Costa Rica? Would the Library of Congress be
substantially more effective if someone counted all the books or the kinds of
books? All of these estimates of biodiversity seem to have forgotten the exist-
ence of bacteria and the oceans. The count of species in a large aggregate of
biodiversity is a by-product, not a goal. One can use a telephone directory to
count approximately how many telephone numbers there are in a city, but that
is not why one makes a telephone directory. What does need our attention is
our ignorance of biodiversity in organisms and processes. This ignorance does
not imply that the numbers of species per se are of importance, though numeri-
cal relationships do play their usual role in sampling community properties.
• We do not need to know the world-level or even national-level detailed
geographic distributions of all butterflies, birds, or trees (or some other con-
spicuous taxon). The world is simply not a sandbox offered to scientists to
reorganize as they wish so as to save their favorite higher taxon. The function
of detailed biodiversity inventory is not to choose sites for conservation. One

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invests inventory attention on an area that already has been seriously desig-
nated for conservation status, with the goal of ensuring that status through un-
derstanding. The bulk of the significant blocks of conserved or conservable
biodiversity in the Earth’s terrestrial tropics already are known and largely de-
limited. Where this is not the case, there already exist knowledgeable field
biologists and conservationists—national and international—who can quickly
set the majority of those limits through rapid ecological assessments and other
protocols. What is needed is not many international “choose your favorite site
to conserve” exercises, but rather a focus of the world’s scientific, conservation,
and user energy on making those 5-15% of the world’s tropics into places that
society really wants to keep.
• We do not need to know about one more set of data on traditional wild-
life management about this or that turtle, macaw, tiger, or deer. Yes, there are
some large conspicuous tropical organisms that need a close look—vis a vis the
real biological and social context of where they live. But, in general, it is the
other 98% of biodiversity that needs much of our attention in natural history.
The attention should be in the context of the society that surrounds and infuses
the biodiversity of the focal site and not in the context of the time-honored
initiation rituals of academic titles and institutions. Let us stop making conser-
vation science be the science of trying to figure out how to get more money for
biological research by piggybacking on the biodiversity crisis.
• We do not need to know where each individual of every species is (or
was) over the surface of the tropical landscape. Far more than in extra-tropical
habitats, the living dead and the population fragments sprinkled across the tropi-
cal agroscape are slated for the dust bin. We long have been deceived by the
ability of extra-tropical species to persist as the sum of minute fragments in
severely impacted landscapes. Sixty to 80% of North America’s biodiversity
probably can survive in a scattered and porous network of many small reserves
and on marginal farmland or ranchland. The analogous lifeboat in the tropics
would do well to save 30%. Our tropical resources, always in short supply,
should be directed toward saving the bulk of biodiversity in a few large and
well-distributed blocks, hopefully robust in the face of climatic change through
their elevational and multihabitat diversity. This comment is not meant to deni-
grate the small patches and fragments of widespread tropical species and the
occasional isolated endemic—at times of high value to their immediate owners
and neighbors irrespective of their eventual demise or impoverishment of bio-
diversity. Rather, it is meant to suggest that we coldly practice a biologically
realistic triage so as to bring conserved wildland biodiversity into peace with
tropical society at large and, more specifically, the agroscape. I would argue
that it is a much wiser investment to assure the survival of a few large blocks
than to continue to harass the agroscape over the unsustainable survival of tiny
remnants.

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420 / BIODIVERSITY II

WHAT DO WE DO WITH BIODIVERSITY

ONCE WE KNOW SOMETHING ABOUT IT?
When one begins to be familiar with biodiversity in a large conserved tropi-
cal wildland, what does one do with it? This is somewhat akin to asking what
does society do with the Library of Congress, Internet, a university, the Mis-
souri Botanical Garden, a supermarket, and Disney World all tied up in one.
The answer is “everything.” This reply stresses the importance of conducting
an ATBI on a very large area, an area large enough that it can be used for mul-
tiple purposes without the users destroying it. It is of restricted use to know a
huge amount about an area so small that its biodiversity must be treated like the
rare book section of the public library. The following begin to answer the ques-
tion:
• All conserved tropical wildlands are islands (or shortly will be), and an
ATBI is the beginning of providing a ground zero for asking how its biodiversity
reacts to such things as global climatic change, pesticide contamination, use,
and insularization. Tropical wildlands, fractured into habitat islands with dis-
tinctive conditions, and perhaps subject to severe global change, will be the
sites of a global speciation event that will dwarf anything generated by, for
example, Pleistocene drying. An ATBI sets up a gigantic canary in the mine for
these reactions.
• The known universe of an ATBI site can be a standard for calibration
(and development) of any and all kinds of inventorying, sampling, and monitor-
ing technologies and protocols that can be applied in lesser known circumstances
for a multitude of reasons. Virtually all of today’s methods and protocols for
inventorying biodiversity have been developed in the process of inventorying
the unknown, rather than the known, universe.
• The known universe of each ATBI site will serve as the foundation on
which to construct an extremely diverse array of question-driven ecological,
behavioral, demographic, and ecosystem studies. The possibilities are mind-
boggling with respect to what sorts of ecological work can be done with a com-
plex habitat where virtually every species can be identified and categorized
ecologically.
• An ATBI site is, in effect, a well-organized wild zoo, greenhouse, and
culture facility in which to prospect for wildland organisms, genes, and their
products. An ATBI will remove the single largest obstacle to serious examina-
tion of large arrays of wild biodiversity for human use. This information has
enormous applied value for the further development of the millions of hectares
of serendipitously developing agroscape throughout the tropics. A happy
agroscape is far more likely to live in peace with its neighboring wildland crop
than is an agroscape at war with itself, a war brought on by monocultures,
synthetic product substitution, and bored human draft animals.

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WILDLAND BIODIVERSITY MANAGEMENT IN THE TROPICS / 421

• An ATBI site is a national museum, national library, art gallery, concert

hall, national zoo, national botanical garden, and national university for eco-
tourists and other forms of students ranging from grade-school children to se-
nior citizens. How can we hope to even begin to develop biological literacy for
the tropics when wild nature appears as a homogeneous green wall, when its
incredible array of solutions, questions, and examples are illegible and undeci-
pherable?
• An ATBI site can be a major provider of ecosystem services, especially if
the site is chosen with that as an additional criterion, and simultaneously can be
known well enough to study the internal mechanics of ecosystem services. Car-
bon sequestration can be a boring monoculture, or it can have complex value-
added properties.

The Limiting Resource: Knowledge Itself

Today we are in the throes of determining how to record, manage, and
transmit information about wildland biodiversity—the structure of databases,
networks, distribution of databases, image transmission, authority files, author-
ship attribution, clearinghouses, bar-coding, retroactive data-capture, and com-
puter-capture of literature—but tomorrow these technologies and protocols will
have been resolved for the most part. Then, and for centuries thereafter, the
resource in short supply will be the information about biodiversity itself. Who
eats what, what breeds when, why is this pond green and that blue, when will
the mushrooms bloom, when are the birth peaks? What genes code for magne-
sium resistance, for morphine synthesis, for dry season dormancy, for sex? What
does a complex tropical ecosystem do when the annual rainfall declines by 40%?
How ironic that just as the great bulk of tropical humanity flees the countryside
or polishes it clean, humanity is coming to have the wherewithal to record for-
ever what some grandparents knew, and the grandchildren will want to find
out, about the vaporizing wildlands. How ironic that tidbits of natural history
gleaned from local naturalist’s publications, birdwatchers’ notes, and schoolyard
exercises—properly collated through the Internet—may turn out to be as valuable
as the information on specimen labels in the world’s natural history museums.
Are we going to shed our distorted visions of tropical biodiversity gained
from centuries of touristic field biology, and really begin to offer society an
understanding of biodiversity in its heartlands? What is a keystone species? It
is a species that is so well known that we can recognize the ecological ripples
that occur when it is removed. All species are keystone species on some scale,
though not necessarily on the scale and ruler of a 1.6 m-tall diurnal vertebrate.
We need to look at more than our big woolly relatives. What is a redundant
species? It is a species that does not yield what you want. This is not a biological
trait. What is an indicator species? Any species can be a miner’s canary in the
right circumstances. Please let us leave the Holy Grail for other social sectors.

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Computerization and The Transfer of Knowledge

The all-invasive wave of computerization represents a quantum and quali-
tative change in the acquisition, massage, distribution, and archiving of infor-
mation about biodiversity. It will change humanity’s relationship with bio-
diversity more than has the printing press, the camera, or the chainsaw.
Computerization is a great part of what allows the realization of all the prognosis
mentioned or alluded to here and elsewhere in biodiversity management. For
the first time in human history, there is the opportunity of open and massive
intra- and intersociety flows of information about biodiversity, something that
was alluded to through “publication” but in fact has not been achieved even
minimally compared with what is to come.
For the first time, it is possible for an individual and a site to acquire, mas-
sage, distribute, and archive the unimaginably large quantity of highly particu-
late information—images, specimen descriptors, species descriptors, habitat de-
scriptors, circumstances, previous knowledge—that is pertinent to the
management and use of a conserved wildland that contains hundreds of thou-
sands of species and has been or is being studied by tens to thousands of observ-
ers over the years or even at one time. The essentiality of bar-coded uniquely
tagged vouchers and specimen-based information becomes self-evident. The
primal necessity of attributing authorship and evaluating input for all these data
is written in stone. The real art is how to massage information and put it in a
multitude of formats for a multitude of users. The real question in biodiversity
then becomes whether the developed world is willing to accept the leveling of
the global playing field that all this implies. Most evident of all, the last thing
biodiversity management needs is new hard-copy journals, more hard-copy
books (except as temporary reports for some kinds of convenience), and a con-
tinuation of the stultifying hard-copy traditions of biodiversity information
management from the past several centuries. What tropical wildland bio-
diversity management needs is for all the holders of information about bio-
diversity to get that information as fast as possible into the Internet, rather than
waiting decades (if ever) to see it frozen onto thin sheets of wood.

Taxonomy and the Taxasphere

Taxonomy is the basic philosophical and technological infrastructure for
wildland biodiversity management. Without taxonomy, there is no inventory,
no collation and distribution of information about biodiversity in space and
time, no inference among species. But taxonomy, like conservation, ecology,
and other specialities in science, has evolved to its own drumbeat. Most encour-
agingly, taxonomy currently is reexamining its mission through efforts such as
Systematics Agenda 2000 and a multitude of international symposia. Govern-
ment agencies of the United States are beginning to undertake and support a

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WILDLAND BIODIVERSITY MANAGEMENT IN THE TROPICS / 423

global responsibility in taxonomy, and taxonomy once again is coming to be

supported as a form of national development.
Some things are evident in the changes that biodiversity management asks
of taxonomy. No more turgid keys, please. Expert systems, picture keys,
Intkey, and the like are a major step forward. Give top priority to the coming
together of standards for taxonomic and specimen data, data models, and user-
friendliness in computerization. We all need to be headed toward identification
guides that allow us to flip through an electronic (or hard-copy) picture book,
with centralized or networked processors where an image or discussion of a
doubtful organism can be sent for taxonomic confirmation. Close on our heels is
the magic box into which a piece of a bug is dropped, sequenced, sequences
compared with a library, and a name spit out if it matches. Then, with the name
in hand, one calls up what the greater global network already knows about the
biology and biodiversity of that species or population—a global field guide in a
pocket. Once again, it is the information about genetics and biodiversity from
the field that becomes the resource in short supply.
Where is most of that information pool today? It is in the heads of retiring
taxonomists. Speaking quite coldly, these most honorable systems should be
data-based, information-based, and knowledge-based—the brain dump—to say
nothing of put diligently into mentorships for the next generation of those who
will manage this (to date) highly personal tradition. The new PEET initiative
(Partnership for Enhancing Expertise and Taxonomy) of the National Science
Foundation is a major step in this direction. This information-capture might
well be done in conjunction with the retroactive data-capture that is possible in
the world’s large museums, but, if not, the highly perishable should be given
priority over the pinned and dried.
Taxonomy is really a taxasphere with nodes of specialists, collections,
knowledge-bases, and hard-copy data—all strung together on an Internet lat-
tice and variably plugged into the world’s biodiverse sites. The nodes intercon-
nect as much for taxonomy’s own work as for all the other users of biodiversity.
There is a major question as to whether, and to what degree, it is worthwhile to
retroactively capture the information in museums. Ironically, museums were,
on the one hand, the expressions of interest in species as manifest through speci-
mens. Information contained in museums therefore often was not gathered in a
manner conducive to its maximum use in biodiversity management. On the
other hand, museums are the depositories of the raw material on which taxono-
mists have largely built their science. To someone concerned with a given con-
served wildland, the international and national distribution of a species (as re-
corded on selectively and serendipitously collected museum specimens over
previous decades) may be of limited interest. What may be of greater interest is
whether and where that species occurs today within one’s local or national gam-
bit of interaction.
At the very time when extant museums are rethinking the value of their

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424 / BIODIVERSITY II

collections, they are the logical recipients of the new and enormous responsibil-
ity of curating the mass of voucher specimens that will appear from inventories
and other kinds of biodiversity management. While many of these specimens
are perhaps of lesser direct taxonomic interest, they are of huge importance in
underpinning the current mass of information about biodiversity, a base on
which much more information will be built. We find ourselves in the ticklish
position of explaining to the tropical world at large that the specimen is of little
or no value per se, and thus should not be the focus of nationalistic possessive-
ness, while at the same time it may be a voucher specimen or source of genetic
information that merits long-term maintenance costs. The more the bio-
technologists tell us, the closer that specimen comes to being a legible cookbook
for many of the things that it did in nature.
The taxasphere has long run on the engine of personal interest in organisms
by taxonomists and other kinds of field biologists, rather than on a true eco-
nomic and social recognition of the critical nature of the taxonomic underpin-
ning of the use of biodiversity (though an impressive amount of research on
wildland biodiversity was conducted in previous centuries in the name of eco-
nomic interests). To the degree that society neglectfully accepts that taxonomy
is run by such a volunteer work force, we are confronted with the advantages
and disadvantages of trying to run an army or national park staffed with unsala-
ried volunteers, even very competent ones. While the taxasphere needs to reach
out with joy for the finances and responsibility that should come with a reversal
of this trend, this same taxasphere then is confronted with an increased account-
ability to the funder, a kind of accountability not usually associated with those
who operate in a free-spirited and artistic social sector. It will be most helpful if
the taxasphere can manifest some self-directed willingness to spread responsi-
bility to those taxa and technologies previously unconsidered, as a response to
society’s willingness to put resources behind this action.

Targeting the Small Stuff

The bulk of biodiversity comprises very small organisms—easily 80% of a
conserved wildland’s biodiversity weighs less than a few grams even as an adult.
However, many of the traditions of information management, field ecology, spe-
cies-use, conservation, wildland education, and evaluation of biodiversity have
been little affected by the biology of the small stuff. On the other hand, the
enormous biodiversity of small species constitutes much of the potential for the
use of biodiversity and offers a huge part of the complexity of managing this
biodiversity.
This means that finding out which aspects of biodiversity reside in a site
and getting it in order for society will involve a very large number of field
taxonomists and ecologists spending their time getting their (easily inventoried)
big organisms into situations where they can be poked and searched by the

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people who work with viruses, bacteria, fungi, mites, small insects, protozoans,
parasites, algae, and other little things. This means that the quality of onsite
laboratory facilities will need to take a megastep upward to complement the old
tent and machete. This means that the conserved wildlands will be brought yet
closer to society.

MANAGING WILDLAND BIODIVERSITY FOR SUSTAINABLE USE

As I mentioned at the outset, the frontier is gone. Sustainability is eating

the interest, not the principal. The use of wildland biodiversity must be scheduled,
planned, and monitored. There will be all sorts of users, and they will compen-
sate for their impact through payment in a very wide range of currencies.
It is no secret that tropical wildland biodiversity currently is threatened by
the nearly invisible symphony of a multitude of threats that are exponentially
gaining force from unseen and unexpected directions. They impact simulta-
neously in different countries, and the well-established lack of intercountry
communication renders them even yet more invisible. That little farmer in the
forest with his chainsaw is now unexpectedly given a huge boost by the fall of
trade barriers, by pharmaceuticals abruptly rendering yet another major tropi-
cal disease less of a barrier to wildland clearing, by the introduction of newly
genetically engineered domesticates, and by the speeding of the process of do-
mestication through biotechnology. Knockout punches are gathering silently in
the wings. Yet the left hand needs to be doing something quite noticeable be-
fore the right hand takes note. Conserved wildlands require aggressive and
eager succor from society at large if they are to survive the very onslaught that
often is generated quite innocently by that same society.
But do extinction rates really matter? Does it matter if this or that species
goes extinct? The fact is, we will lose 10-20% of them over the coming century,
important or not. So let’s get busy delimiting the areas that will be conserved
tropical wildlands, largely forget about those things that live outside, and get on
with making high-quality conservation areas out of the 10-15% of the Earth’s
surface that contains the remaining 80-90% of the species. And let’s make very
high-quality agroscapes and urbanized habitats in which these areas are imbed-
ded. All the mental energy and all the funds put into anguishing over the losses
could be spent far better on quality survival of the survivors.
It might be useful to note that the current extinction differs from the Creta-
ceous extinction in the following ways:

• We are not about to give the terrestrial world back to biodiversity to

reevolve after this is all over.
• We will have reduced terrestrial biodiversity to tens of thousands of
analogs of the Galapagos Islands and New Guinea, where speciation and higher
taxon evolution will work apace (and generate a plethora of endemics).

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426 / BIODIVERSITY II

• The surviving subset of species will be defined by area and habitat,

rather than being ecological groupings such as those small vertebrates that could
aestivate or stay warm (microreptiles, micromammals, and feathered hotblooded
microdinosaurs) and survive on a diet of plant and animal carrion, seeds and
other dormant organisms, and the insects and fungi that feed on the same, dur-
ing a winter induced by meteor-impact.

So the first self-denial that must become characteristic of users of bio-

diversity and practitioners of biodiversity management is the temptation to have
different government agencies and nongovernment organizations (NGOs) har-
vest their own information about biodiversity and wield it to their own end.
We hopefully are about to enter an era of interagency and inter-NGO coopera-
tion. The Oaxaca Declaration, the U.S. National Biological Service, much inter-
museum collaboration in the development of databases, the information clear-
inghouse of the Biodiversity Convention, and databases moving onto the Internet
are recent examples. ATBIs, institutions like INBio, national biological surveys,
and the Internet itself are all manifestations of this process of collaboration
among users.
Terrestrial conserved wildlands are habitat islands and will become more
so. They are habitat islands joined only by a selected few (largely) aerially
mobile organisms, islands positioned in an ocean of intensely managed domesti-
cates. This insularity means that no matter how large and how well planned and
inventoried, each conserved wildland will have a different and heterogenous
ceiling for intensity of impact by on-site users. We even have the irony that
established conserved wildlands can render the concept of “endangered species”
an anachronism. If species are in truly conserved wildlands, they survive in
those habitats at their naturally achievable densities or they go extinct. Outside
of the conserved wildland, they are basically forgotten. Yes, some will survive
as society’s pet trees and animals, or as domesticates and weeds, but these are
not the focus here. The question is not whether we can bustle across the agro-
scape feeling valiant in the protection of the living dead, but whether we can
design rules for maximum nondamaging use of significantly large conserved wild-
lands and tempt society to live by these rules. Let us use our energy now to make
the wildlands into better islands, rather than dream that we are being effective
conservationists by saving a noble tree left standing in a tropical bean field.
Introduced organisms would seem to be a sort of unconscious use of con-
served wildlands and marginal farmland. First, please stop the introductions
until the sink as a whole has been taken into account. No matter how many
firewood trees have been cut down in Africa or India, the solution is not the
introduction of new species of firewood trees from the Neotropics. No matter
how little water can be allocated to Hawaiian home ornamentals, the solution is
not the massive introduction of drought-resistant plants from Costa Rican dry
forest to Hawaiian gardens.

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Second, recognize the extreme contradiction inherent in biodiversity. At

least in mainland habitats of broad extent, virtually every organism in the natu-
ral community evolved as a little population somewhere else. It is an immigrant
in most of where it is found today, and wildland biodiversity programs on main-
lands are put together mostly through ecological interactions rather than through
onsite evolutionary fine-tuning. The horse is an instructive example. The horse
is a New World native and could be argued to be a proper part of Mesoamerican
conserved wildlands, albeit a machine gun is needed to substitute for the saber-
toothed cats. The survival of the horse in the Old World, while we extinguished
it in the New World and then reintroduced it, really is not that different from
reducing the North American bison to a tiny herd and then building it back up
(and partly domesticating it as well). Use should be measured by real impact,
not by the license plate on the “immigrant.” All wildlands are strongly im-
pacted by humans already—extinction of the Pleistocene megafauna, extinction
of contemporary vertebrates, global warming and other change, hunting, road-
side secondary succession, and introduction of bacteria, fungi, algae, mites, and
herbs. There is no “pristine” nature, free of “introduced species” and human
influence, to conserve.
Once designated as conserved wildland for the nondamaging use of its
biodiversity, this land-use categorization needs to be inviolate. In this respect,
wildlands conserved for their biodiversity are qualitatively different from other
kinds of land-use, and are not easily interchangeable with other kinds of land-
use. The agroscape easily can move from peanuts to sorghum to cows to pea-
nuts over the years, but moving a given hectare from rice to forest to rice to
forest requires considerably more cost and long-range structure, and often is
not biologically possible. Restoration is a limited tool, not a panacea. How-
ever, restoration does offer enormous potential in the siting of conserved wild-
lands throughout the tropics.
A conserved wildland is far more sensitive to context than is an equally-
sized portion of the agroscape, and a conserved wildland cannot afford to go
bankrupt—unless society also is willing to then leave it in peace until wildland
production starts up again. In the same vein, we must come to recognize that a
conserved wildland is no more or less responsible for contributing to a country’s
national budget and the solution of its social ills than is any other kind of land-
use. A successful rice farm is not held accountable for the social welfare of all of
its neighbors ills except through some variety of national income tax distribu-
tion. There is no reason to expect that the earnings of a conserved wildland will
provide the solution to all of its neighbor’s ills except through the same kind of
distribution of earnings, employment opportunities, and taxes as for other forms
of land-use.
Ironically, the direct use of a conserved site by people is perhaps one of the
easiest of all facets of biodiversity-use to manage. Society at large, and specific
individuals, are very good at using or visiting a conserved wildland area to the

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428 / BIODIVERSITY II

level of intensity allocated—if they are clearly informed of the limits and if the
method of explanation is clear and cast in a socially perceptible format. This
communication requires more or less direct human presence and interpretation,
depending on the society and circumstance. The more specific harvesters—
researchers, staff, biodiversity-prospectors, inventoriers, ecosystem service per-
sonnel—likewise are proving themselves to be highly responsible socially in
conserved tropical wildlands if they find themselves cast in a responsibly man-
aged and forward-directed interaction between society and biodiversity. But
we can never forget that the finest farm or ranch easily can be destroyed through
overgrazing of pastures, improper irrigation, failure to rotate crops, poor selec-
tion of varieties, or sloppy agrochemical application. Wildland biodiversity is
another kind of farm or ranch.
Throughout the tropics, lured by the ecotourism dollar, there has been a
very strong tendency to use the dollar as the primary currency in valuating
conserved wildlands. While this has its valid points, what seems to be forgot-
ten—largely through the inconvenience of leveling the national social playing
field—is that the “poor” national user of a conserved wildland pays in votes (as
well as through some decentralization of cash flow) and in emotional attachment
to the conserved wildland. When the fourth grade schoolchild is voting on the
irrigation district board as a 55-year-old adult, that person will remember what
was learned in the conserved wildland 46 years ago, what experiences were had
there, and visualize the grandchildren as doing the same. This phenomenon is
reinforced when the conserved wildland and its associated processes constitute
a major local employer, spends millions of dollars per year locally in operations
costs, and uses its income to establish its own management endowment.
Equally revealing, and long-term, is the biodiversity-prospecting loop.
When a conserved wildland or its facilitators bring home the first contract for
biodiversity-prospecting, the returns seem very large when set against the back-
ground of tropical conserved wildlands—viewed as all cost and no visible in-
come other than piddling ecotourism entrance fees. However, a ministry of
natural resources will take notice when the first actual royalties from a drug
discovery flow into the national budget for conserved wildlands or, better yet,
into the endowment fund of the conserved wildland from which the raw mate-
rials were collected. But even then, a ministry of the economy will not take
notice. That will occur when the pharmaceutical company decides to move
some substantial portion of the development process—more than $200 million
per successful drug—into the source country. Once again the leveling of the
playing field reappears, with all its advantages and impediments. The North
American Free Trade Agreement (NAFTA) and the General Agreement on Tar-
iffs and Trade (GATT) relate directly to conservation of biodiversity.
The art of valuation of nondestructive use of biodiversity rests heavily on
being able to work in many currencies, to recognize the market value of infor-
mation to many different sectors. A field guide to the birds of a tropical coun-

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WILDLAND BIODIVERSITY MANAGEMENT IN THE TROPICS / 429

try is not just “a bird book.” It is essential technology in the ecotourism indus-
try. It is fertilizer for the ecotourism crop. Yet also, without a conserved
wildland in which to observe the birds and the things they do, it becomes just
a bird book. The value of information about biodiversity is extremely depen-
dent on context. A country may “have” (really, may be custodian for) the most
marvelous set of endemic species or bizarre habitats, but if the information
they contain and display is not put into various social currencies, those species
and habitats will contribute little or nothing to their very survival in a world
dominated by humans.
All of this can do nothing but reemphasize the critical need for institutions
and processes that accept the responsibility and challenge of the specific task of
gathering, collating, massaging, and distributing information from and about a
nation’s conserved wildlands. This essential process must occur at the level of
each specific wildland and at the level of the national synthesis, at the least.
You, society, hardly can be expected to value that which is invisible to you.
Ironically, the very salvation of biodiversity—its valuation by society—is a
multiedged sword.
First, if the area is conserved for its value on just one or a few axes, then it
is in the same risk zone as the country that depends on a monocultural agro-
scape—coffee, bananas, and Costa Rica are close to mind. Fortunately, wildland
biodiversity is in fact far more diverse than is the agroscape and, as such, diver-
sification of crops as well as diversification of markets is very feasible (though
hardly developed).
Second, information differs from agricultural produce in that one consumes
produce today and needs more tomorrow. Once consumed, information is pub-
lic domain and continually widely available, and is even more so in the elec-
tronic and computerized age. Therefore, a given piece of new information is
unlikely to have nearly the same value in next year’s market as in this year’s
market. There is a high premium on rapid development of products, almost as
one encounters in the newspaper business. However, as in the news business,
naive consumers of information about biodiversity continually do appear
through human biological processes (birth, forgetting, nostalgia), and the
amount of absolutely new information about biodiversity to be gathered and
developed certainly is limitless for many decades to come. Information about
biodiversity also can become “new” through the appearance of a new use.
Finally, it is no secret that a nation’s conserved wildlands are its package of
local varieties. All that a nation does to both share and profit from the varieties
in its agroscape is pertinent by analog to the treatment of the breeding stock and
genes from its conserved wildlands. Just like petroleum, which occurs in a
multitude of countries, the value of any one of these species depends on what
the country constructs on top of its national supply of this basic raw material.
Any conserved wildland will need to struggle with the question of physical
use and the impact of sampling, observing, studying, experimenting, and visit-

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430 / BIODIVERSITY II

ing. Given that all conserved wildlands are in fact impacted already by human-
ity, and always will be, the question is basically what level of use falls within
the “natural” ups and downs and expansions and contractions of behavior, de-
mography, and interactions. What level of use is “nondamaging”? Any user
does leave a footprint or a beer can if one knows enough biology to see it. How-
ever, just as the tapir-nibble out of the top of a bush blurs into biological “noise”
within a few days to weeks, the biodiversity-prospecting sample taken from
that bush blurs as well over time. Just as the loss of the annual baby agouti to
a boa constrictor changes the mother’s foraging pattern for a year, the monkey-
watcher’s trail changes the sleeping site of the local peccary herd. But the next
year, both perturbations are indistinguishable from the multitude of other
nonanthropogenic changes.
At present, perhaps the largest single near-sighted user of detailed tropical
biodiversity is the international academic and museum community. In what
currency will they pay for and value their use? Long we have cast our graduate
students in our own image, and now and then we have done the same to a
student from a tropical country. But it is not at all clear that this is the kind of
payment we would make if we really were to think out what a tropical resident
needs, for example, to be part of the managerial cadre of biodiversity. Even
more basic is whether we should be expending so much energy on producing
yet more graduate students in a steady-state system, or expending that energy
in collaborating with the tropics as it comes up to speed. We are letting the
lifestyles in our developed world define the way that we examine and study
tropical biodiversity. That is okay, more or less, if the biodiversity is in our
backyards in Minnesota or California, but it definitely is not if the biodiversity
is in Madagascar or Colombia and the training is in England or Illinois.
The upcoming Presidents of tropical countries often will have advanced
degrees from universities in the developed world as well as from those in their
home countries. Will they have learned about biodiversity around those north-
ern universities? Or will they have learned how to deal with the biodiversity in
their home countries, a situation that desperately needs their political attention?
Costa Rica’s new President, José María Figueres (1994-1998), has accepted the
challenge of steering his country in the direction of sustainable development
and management of conserved biodiversity for society’s nondamaging use. Has
his university training, and that of his advisors, prepared him for this?

IN CLOSING
A peculiarity of taxonomy and natural history—those pivotal professions
for the management of biodiversity—raises its hand here. Taxonomy and natu-
ral history represent some of the very few subsectors of science that strongly
depend on people—amateurs and professionals alike—who really love the ac-
tual objects of their research as well as being intensely curious about their traits.

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WILDLAND BIODIVERSITY MANAGEMENT IN THE TROPICS / 431

High-quality managers of biodiversity—wildland and urban, taxonomists and

many other kinds—are largely born and then facilitated, just as are musicians,
politicians, scientists, basketball players, and others. The expression of their
genes requires an accepting society, and the facilitation of their abilities costs
money and job security. Retooling people and institutions from other areas into
biodiversity management has the usual advantages and drawbacks, with insti-
tutions being the most difficult. Who is going to crawl around in the hot tropi-
cal sun doing natural history without being in love with the organisms? Who is
going to spend 50 years of their life peering intently at some organism that is 1
mm long in return for just salary and prestige? We would do far better to feed
and support those who are by nature inclined in this direction, as we do with
musicians and many other professions, than to issue a call for all good people to
come and be good taxonomists and natural historians. They will not be. But we
can reinforce those with a propensity in this direction, and draw out the best in
them.

ACKNOWLEDGMENTS
This manuscript is the result of many discussions with many people, but I
would like to particularly acknowledge the time and attention of F. C. Thomp-
son, K. Krishtalka, J. Edwards, W. Hallwachs, R. Gámez, D. E. Wilson, P. Jutro,
I. D. Gauld, F. Chavarría, A. M. Solis, P. Rauch, J. Busby, A. Chapman, J. Croft,
P. Raven, T. Duncan, E. Hoagland, D. Brooks, A. Rossman, M. M. Chavarría, J.
Jiménez, A. Sittenfeld, W. Reid, R. Curtis, J. Burns, D. Miller, G. Barnard, D.
Brooks, M. Carvajal, J. Croft, R. Espinosa, R. Moraga, J. Hester, M. Ivie, N.
Zamora, D. Schindel, F. Harris, N. Chalmers, K. MacKinnon, F. Talbot, E. Nielsen,
M. Boza, C. Quintela, J. Sarukhan, L. Tilney, S. Ulfstrand, A. Ugalde, J.
Coddington, A. Umaña, S. Marin, A. Pescador, R. Blanco, M. Zumbado, A. Solis,
C. Wille, J. Corrales, J. Ugalde, R. Castro, J. Phillips, E. Sancho, A. Piva, M.
Koberg, M. Molina, M. Segnestam, J. Burley, R. Poole, R. Hodges, Q. Wheeler,
T. Erwin, H. Daly, T. Eisner, E. O. Wilson, J. Soberon, H. Kidono, J. Jensen, M.
Bystrom, P. Froberg, G. Hubendick, R. Rimel, D. Martin, N. Meyers, D. Johnson,
S. Viederman, O. T. Sandlund, F. Joyce, J. M. Figueres, and the INBio para-
taxonomists.

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CHAPTER
28

Taxonomic Preparedness: Are We Ready

to Meet the Biodiversity Challenge?
QUENTIN D. WHEELER
Professor, Department of Entomology and L. H. Bailey Hortorium,
Cornell University, Ithaca, N.Y.

JOEL CRACRAFT
Curator, Department of Ornithology, American Museum of Natural History,
Central Park West at 79th Street, N.Y.

Taxonomic and genetic diversity—essential for human health, agriculture,

and ecosystem function—are being eroded as wildlands are converted to other
uses. Many species already have become extinct as a result, and thousands,
perhaps millions, of others soon face a similar fate. Equally alarming, the rate of
habitat conversion is accelerating, along with—by implication—extinction of
species. Consider, for example, the approximate doubling of the estimated an-
nual rate of tropical deforestation in the 1980s (Myers, 1991), which has led
some to predict that one-fourth or more of our planet’s species may disappear
within a few decades (National Science Board, 1989).
Humans use tens of thousands of species in their daily lives for food, shel-
ter, medicines, and diverse forms of commerce. As population pressures in-
crease and more and more people must make use of other species for subsistence,
managing these resources in a sustainable manner will become increasingly dif-
ficult. Modern forms of transportation have reached all corners of the globe so
that people, whatever their economic circumstances, are now more mobile than
at any other time in human history. As a consequence, thousands of species are
being transported around the world, both intentionally and unintentionally.
New diseases are emerging; agricultural systems are being exposed to a multi-
tude of new crop pests; the natural structure and function of ecological commu-
nities are being torn apart by the introduction of exotic species; and intricate
distributions of species produced over thousands or millions of years rapidly are
being shuffled. Laissez-faire public policies regarding the management of natu-
ral ecosystems that once were considered benign now are seen to carry serious

435

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436 / BIODIVERSITY II

societal consequences that seldom can be reversed, and then only at substantial
expense.
Discovering new biological resources and managing existing ones depend
on access to reliable scientific knowledge about biodiversity. Yet as implied
above, the challenges to effective management of the world’s species are multi-
plying at a rate that far outstrips our acquisition of the information needed to
confront them (Cracraft, 1995; Systematics Agenda 2000, 1994a,b). Ironically,
the biodiversity crisis has emerged as a global issue at the same time that sup-
port for basic research and training in the biodiversity sciences has declined
sharply (Holden, 1989; House of Lords, 1991; Nash, 1989; Schrock, 1989;
Wheeler, 1995a). The absence of adequate scientific infrastructure in most coun-
tries, especially in those that are species-rich, constitutes a major impediment to
an international response by the scientific community. Even those countries
with substantial scientific resources cannot meet their management needs (Na-
tional Research Council, 1993). In these countries, for example, systematic col-
lections are not funded at a level that is capable of keeping up with the existing
rate of specimen acquisition, let alone at a level appropriate for the biodiversity
crisis. Existing data in herbaria and museums remain largely inaccessible by
modern technologies for data management. Funds available for investigating
fundamental questions about biological diversity are severely limited relative to
the task at hand. And, finally, the numbers of students trained in systematics
and organismal biology have diminished, contributing to what many, including
the DIVERSITAS program of the International Union of Biological Sciences, the
Scientific Committee on Problems of the Environment, and the United Nations
Education, Scientific, and Cultural Organization, have called the “taxonomic
impediment.”
Of all the biological information that is needed to manage the world’s spe-
cies, the most fundamental is that provided by the discipline of systematic biol-
ogy. The four primary components of systematics—discovery and description
of species, phylogenetic analysis, classification, and biogeography—provide
basic biological information about species, including their name, characteriza-
tion, relationships to other species, and geographic distribution, thus establish-
ing the foundation for all the other biodiversity sciences, such as ecology, popu-
lation biology, genetics, and behavior. Taken in aggregate, these components
support the ultimate aim of systematics to know and understand the taxonomic
and phylogenetic diversity of life on Earth.
The need for systematics has never been greater. Despite having accumu-
lated significant knowledge about the world’s species over the past 2 centuries,
we still cannot provide accurate answers to the simplest of all questions about
biodiversity. How many species are there? Estimates vary from 3 to 100 million
species. What are the relationships among species? Except for a small number
of taxa, the pattern of life’s history remains an enigma. Where among the myriad
of Earth’s habitats are these species distributed? Detailed answers exist for no

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TAXONOMIC PREPAREDNESS / 437

more than a few species; indeed, the distributions of many of the most thor-
oughly studied vertebrates, including groups such as birds, remain imprecisely
known.
The continuing loss and degradation of the world’s biological resources
compromises the ability of nations to create a sustainable future for their citi-
zens. Managing these resources will necessitate an increased commitment on
the part of the world community to support the biodiversity sciences, especially
in the species-rich countries where scientific capacity is least developed. This
should include programs to build new or to improve existing infrastructure,
enhance human resources, and establish a world-wide biodiversity information
network.
The systematics community, through its initiative Systematics Agenda 2000,
has established a framework that can be used to develop the science of system-
atics world-wide (Systematics Agenda 2000, 1994a,b). Advances in the theory
and methods of systematics, computer management of vast collections of speci-
mens, and existing descriptions for more than a million of Earth’s species pro-
vide a context and starting point for creating the knowledge-base in systematics
that will be required to confront the challenges of managing species and their
ecosystems.

DEVELOPING A SYSTEMATIC UNDERSTANDING OF THE WORLD:

LIMITATIONS OF THE ECOLOGICAL APPROACH
Maintaining global ecological systems and achieving sustainability of bio-
logical resources are now widely recognized goals of the world’s nations. For
this to happen, however, each nation must adopt management policies that are
based on, and consistent with, credible scientific knowledge. A key component
of this knowledge is derived from systematic biology. Unfortunately, sufficient
systematic information neither exists today in the quality or quantity required,
nor does the scientific community have the capacity to acquire it rapidly.
Given that systematics is of clear importance for successfully managing glo-
bal biodiversity, and that resources to support systematics science will need to
be increased, we may ask “What is the most cost-effective and efficient means of
developing a systematic understanding of biodiversity?” The broad, compara-
tive scope of systematics research is unique among the biological sciences (Nelson
and Platnick, 1981), suggesting that the best returns will be gained from strate-
gies that meet its special needs for research resources.
Perhaps no more than 5% of the world’s species have been discovered,
described, or classified. There is broad agreement that human societies would
benefit immensely from having knowledge of this unknown diversity, yet un-
til recently no coherent research programs have been proposed to address this
problem.
One approach to providing a taxonomic understanding of global bio-

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438 / BIODIVERSITY II

diversity has been developed largely from an ecological perspective on diver-

sity. It begins with the concept of an All Taxa Biodiversity Inventory (ATBI) at
a single, geographically localized site, in which an effort is made to collect and
identify “all” the species at that site (Janzen and Hallwachs, 1994; Janzen, Chap-
ter 27, this volume). The overriding purpose of an ATBI is to contribute to the
sustainable development activities of the country in which the site is located,
and for that purpose an ATBI has obvious potential. Because of the substantial
systematic activity necessary to undertake and support an ATBI, global knowl-
edge of biodiversity seems certain to increase, and the results of such an exercise
are likely to have important benefits for basic and applied biology, as well as for
conservation and economic development. But are ATBIs the most logical and
efficient way to approach an inventory of Earth’s biological diversity (Wheeler,
1995b)?
In addition to their function in the development of nations, ATBIs also are
being proposed as a model for achieving a systematic understanding of global
biodiversity (Janzen, 1993; Langreth, 1994). It has been suggested that a dozen
ATBIs, carefully sited and successfully completed, would sample as much as 40-
50% of the world’s species diversity and could be undertaken for about $1
billion (Janzen, quoted in Langreth, 1994:81). Leaving aside the fact that we
currently do not have the necessary collections-based infrastructure or system-
atic expertise to complete a single ATBI, the application of what is essentially an
ecological approach to sampling will result, over the long term, in an ineffective
and cost-inefficient program, whether the goal of that program is to develop a
systematic understanding of the world’s species or a credible and predictive
understanding of the local biodiversity.
The reasons for this are several. First, a dozen ATBIs barely would begin to
provide the geographic coverage necessary to discover a sizable percentage of
the world’s estimated species diversity. This follows from the fact that when
groups are investigated in detail, it is found that most species are rather nar-
rowly distributed (see also Reaka-Kudla, Chapter 7, this volume). To sample the
Earth’s diversity adequately, therefore, would require an ATBI in each of the
major areas of endemism in the world. A dozen ATBIs, in fact, would be a small
number for some continents. In Australia, for example, the vertebrate fauna is
partitioned into many areas of endemism, and an ATBI in only one of them
would recover a very small portion of the Australian biota (Cracraft, 1991). As
a consequence, an ATBI in one country will have limited utility for representing
the diversity of other countries, including in many cases those in relatively close
proximity to the ATBI site. An ATBI in one country, moreover, often will have
limited relevance for the development process in others, except perhaps in the
sense that they contribute to global systematic knowledge. Because adequate
knowledge for any given taxon may dictate studies in a unique number and
combination of geographic locations and habitats, it is doubtful that any finite
number of ATBI sites ever would prove to be fully adequate for a detailed sys-

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TAXONOMIC PREPAREDNESS / 439

tematic understanding of more than a few taxa. While periodic collecting at

known sites is a prerequisite for documentation of the status and trends of
biodiversity, the very notion of long-term study at a few anointed sites is inher-
ently an ecological approach while the resolution of fundamental questions about
biodiversity require answers grounded in a systematic biological approach.
Ironically, were most species found to have broad geographic ranges, in
contradiction to 2 centuries of experience and observation, then comparative
studies throughout their ranges would be of critical importance. Widespread
species often can be recognized definitively only after their full range of genetic
variation has been studied (Mayr, 1963). The history of taxonomy suggests that
the isolated description of local floras and faunas frequently results in confusion
about species identities and a proliferation of redundant names. If most species
actually were narrowly distributed, perhaps this problem could be avoided and
provincial ATBIs could succeed in recognizing endemic species without creat-
ing such confusion. But then the assumption that species are widespread would
be violated, and the ATBI model would fail to capture a significant representa-
tion of the world’s biological diversity.
Second, ATBIs are particularly inefficient for setting global priorities for
systematic research or for facilitating the growth of systematic knowledge, be-
ing biased as they necessarily are by the geographic location of the site and by
the development and conservation needs of that particular country. Systemat-
ics can contribute far more to meeting the international need for knowledge by
working with all nations to set priorities for revisionary studies, such as on
those groups that are important for agriculture, human health, ecosystem func-
tion, and growth of scientific knowledge. Designing a global program to target
such groups and to share the resulting discoveries would more efficiently meet
diverse international needs for knowledge of biodiversity than investment of
human and financial resources in documenting the biodiversity at a limited num-
ber of sites. For taxa of demonstrated economic or societal relevance, it is un-
likely that either the majority of species or the most promising underutilized
species will be found in a handful of ATBI sites, regardless of how carefully they
are identified. For taxa of unsuspected or unappreciated importance, a world-
wide perspective is even more essential. No one yet can predict where valuable
discoveries will take place. Opportunities are enhanced by assuring an explora-
tion of the most disparate branches of the evolutionary tree of life, rather than
restricting our discoveries to the species and clades that happen to live in a
dozen or so places on Earth.
Third, collecting organisms is typically the easiest, least labor-intensive as-
pect of systematic activity. Specimens cannot be identified reliably to species
without access to synoptic collections of previously described species, special-
ized expertise, and extensive comparative analysis. This takes considerable time
and access to resources for systematic study. Thus, current conceptual schemes
for ATBIs significantly underestimate the time and scientific resources that will

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be required to identify and classify specimens collected during the ATBI pro-
cess. With the exception of a few well-known groups, or species that are wide-
spread or “weedy,” identifications frequently will be a slow process, if they can
be done at all. As is well known, there is exceedingly little taxonomic expertise
or background knowledge for many groups of organisms.
Finally, ATBIs will not fulfill their potential for many development pur-
poses until the relationships of the species are understood, inasmuch as it is the
knowledge provided by an understanding of the close relatives of species and
their biological characteristics that makes newly discovered species useful to
society. Unless studies of phylogenetic relationships go hand-in-hand with the
inventory process, we will neither make maximal use of these discoveries, nor
will we be able to construct maximally efficient and useful information systems
or predict where research, development, or conservation dollars are most prof-
itably spent. Thus, systematic research is a prerequisite for the successful
completion of any ATBI and as a consequence should have priority when build-
ing scientific capacity.
Drawing on extensive experience in the discovery, description, and classi-
fication of biodiversity and a remarkable recent theoretical revolution within
the discipline, systematists are uniquely qualified to propose an alternative strat-
egy for inventorying biodiversity that draws on what we already know and
takes full advantage of research expertise and resources.

REALIZING SYSTEMATICS AGENDA 2000: AN ACTION PLAN

FOR MEETING THE BIODIVERSITY CHALLENGE
In contrast to a world-wide network of ATBIs, the most efficient and cost-
effective mechanism for developing a systematic understanding of the world’s
biodiversity is to promote capability in systematics for all nations (Systematics
Agenda 2000, 1994a,b). This entails an integrated research program of global
inventories, revisionary taxonomy and phylogenetic analysis, and electronic
access to this knowledge via a biodiversity information system. It also involves
setting priorities for research that benefit all nations, not just a few, which can
be accomplished within a time-line that meets the needs of countries over the
short term.
It is impossible to identify, classify, or understand the biota of one nation
without also knowing and studying the same or related taxa from other coun-
tries. Assessing variation within species or the diversity of characters among
species necessitates access to correctly identified specimens of all species of the
group under study world-wide.
Because it is impractical to house a complete collection of the world’s spe-
cies in each country, comparative systematic research will rely on a limited num-
ber of institutions focused on particular groups and networked electronically
and programmatically. By creating such centers with special expertise on spe-

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TAXONOMIC PREPAREDNESS / 441

cific taxa, resources for research can be concentrated at that location. Such
resources would include collections, systematic experts, specially trained sup-
port staff, and databases. This results in cost-effectiveness for original research
as well as training new generations of experts, validating and updating data
included in vast databases, and providing a source for taxonomic expertise and
services wherever they are needed around the globe. Such laboratories typi-
cally would be located within museums and universities that at the same time
support reference collections of the species indigenous to their own countries.
Because no country can support experts on all groups living within its borders,
each country must depend on a network of international scientists in order to
have duplicate, accurately identified specimens of as many of their species as
possible.
For many branches of science, such global vision and international coopera-
tion are taken for granted. Imagine astronomical, seismological, or global change
research without data gathered world-wide or without relatively open exchange
of data and scientists among nation states. In each case, data must be gathered
at many sites around the globe and integrated in order to make sense of the local
data. At the same time, budgets for such “big science” are assumed to be a
shared, multinational responsibility. Similarly, an understanding of the Earth’s
species diversity will require no less than a globally conceived research effort.
Acceptance of the premise that research should be organized around par-
ticular groups affects virtually every aspect of research in biodiversity. Re-
search centers should be structured and staffed so as to maximize and take full
advantage of accumulated knowledge of a taxon. Field inventory work must be
organized to document all species of a group throughout its geographic range
rather than to concentrate efforts at one or a few study sites. Ultimately, this
information needs to be summarized, interpreted, and communicated—in either
printed or electronic form—through comprehensive monographs. Databases
should be kept current and accurate by locating them where experts, libraries,
and voucher specimens exist. In each case, research, funds, and personnel would
be organized around the unique requirements for the study of specific taxa.
What kinds of research infrastructure are necessary in order to mount an
effective scientific response to the biodiversity challenge? While existing num-
bers of specialists, institutions, and funding sources are grossly inadequate to
address the biodiversity challenge, there is little doubt about what needs to be
done or that the organizational components of an effective scientific program
exist. Theoretical advances in systematic biology over the past 3 decades have
revolutionized and rejuvenated the field, arming it with the ideas and methods
appropriate for the exploration and analysis of biodiversity (e.g., Eldredge and
Cracraft, 1980; Forey et al., 1992; Nelson and Platnick, 1981; Schoch, 1986;
Wiley, 1981). Collection and data management practices have incorporated mod-
ern computational capabilities so that they are prepared for the acquisition of
large numbers of specimens and vast quantities of data. The tragic erosion of

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442 / BIODIVERSITY II

systematic expertise, moreover, could be reversed in a single generation of schol-

ars, given adequate resources to recruit, train, and employ such scientists.

PLANETARY EXPLORATION: TAXON INVENTORIES

The process of discovering, discriminating, and describing the world’s spe-
cies is an enormous undertaking, amounting to the scientific exploration of all
forms of life on an entire planet (Raven and Wilson, 1992). In order to accom-
plish this ambitious undertaking efficiently and rapidly, it is critical that such
work be approached so as to take full advantage of current taxonomic expertise
and research resources. What does this mean?
Just as systematic research is focused on taxa, as opposed to geopolitical
areas or ecosystems, so too an efficient scientific program must be aimed at gen-
erating systematic knowledge of Earth’s species. Scientists studying a particu-
lar group must collect specimens from wherever on the globe such organisms
live. Short-term or intermittent study sites in diverse geographic locations are
most appropriate for meeting the global needs for systematic knowledge. In
essence, systematics views biodiversity differently than experimental or func-
tional biology by making broad comparisons across all species of a clade. The
following, then, represent top priorities:
• Action Item 1: Provide for diverse world-wide inventorying efforts,
each of which is directed at one (or several related) taxa, making full use of
specialized expertise and research resources.
• Action Item 2: Increase the effectiveness of the inventorying effort,
and the systematic research derived from it, by expanding support for the con-
struction, improvement, management, and growth of natural history collections
in museums, botanical gardens, and universities. These should include institu-
tions that build comprehensive, global research collections as well as reference
collections that hold representatives of the species indigenous to each nation.
• Action Item 3: Establish international networks of taxonomic experts
with the goal of ensuring that there is open access to expertise for every group
of organisms somewhere in the world. Each country should have sufficient sys-
tematics expertise to coordinate cooperative international research and to link
with and interpret existing data.

DOCUMENTING DIVERSITY: MONOGRAPHY, REVISIONARY

TAXONOMY, AND PHYLOGENETIC ANALYSES
The scientific documentation of biodiversity goes far beyond the descrip-
tion of species, and ultimately extends to providing access to all that is known
about related species in larger taxa as well as enabling a logical classificatory
scheme to be constructed from which predictions about their properties, distri-
butions, and attributes can be made.

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TAXONOMIC PREPAREDNESS / 443

Drawing on powerfully predictive phylogenetic analyses, monographers

pull together, analyze, and interpret all that is known about the species of a
taxon, elucidate the clade’s evolutionary history, and produce a classification
that makes data easily retrieved and understood. Consequently, the following is
imperative:
• Action Item 4: Competitive research funds should be made available to
support comprehensive, comparative revisions and monographs that are focused
on taxa at all levels from individual genera to phyla.

ACCESS TO KNOWLEDGE ABOUT BIODIVERSITY

Because more and more nations, managers of natural resources and scien-
tists will make ever-increasing demands for accurate and detailed knowledge
about biodiversity, it is critical that what is learned from this global inventory
effort and subsequent systematic analysis be accessible as part of the world’s
emerging information highway. Much of the information on biodiversity that is
housed in the world’s collections remains inaccessible electronically. Further-
more, descriptions of the approximately 1.5 million existing species are widely
scattered in the technical literature, making an accurate count of species, not to
mention retrieval of the descriptions themselves, problematic. Two hundred
million specimens exist in natural history collections in the United States alone
(Edwards et al., 1985), yet databases permitting access to their data do not yet
exist. Therefore, the following must receive priority attention:
• Action Item 5: A network of world-wide taxon databases should be
created which make specimen-based knowledge accessible and guarantee that
those data are maintained by institutions possessing the collections, libraries,
and taxonomic specialists necessary for ensuring their integrity over time.
• Action Item 6: An international effort should be made to electronically
capture the specimen-based information in major natural history collections of
the world and to make that information freely available to all nations for their
use and benefit.

HUMAN RESOURCES AND TRAINING:

MEETING NEEDS FOR TAXONOMIC EXPERTISE
A major challenge facing the study of biodiversity is the creation, reestab-
lishment, and expansion of taxonomic expertise on neglected taxa, thus con-
fronting the “taxonomic impediment.” Evidence from around the world indi-
cates that taxonomic expertise has declined and continues to do so at just the
time when the world is expressing its desire for credible taxonomic knowledge
(e.g., Edwards et al., 1985; National Science Foundation, 1990). In the United
Kingdom, for example, about one-half of the botanical taxonomists teaching in

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444 / BIODIVERSITY II

leading universities have disappeared in recent years (House of Lords, 1991). A

recent survey of universities in the United States which offer doctoral degrees in
systematic entomology shows that 60% of existing faculty have an average of
one Ph.D. student and the remaining 40% have none (Daly, 1995). In many
universities, faculty positions in systematics have been replaced by non-
taxonomic, often molecular, ones (Holden, 1989; Nash, 1989). And even in mu-
seums, efforts to be “modern” and compete for limited research dollars have
resulted in the deemphasis of traditional taxonomic research, particularly
monography.
Steps must be taken immediately to train and support experts on diverse
taxa, to clarify the unique responsibility of museums, herbaria, and universities
to conduct taxonomic research, and to educate administrators to understand
that good biology involves asking and answering questions at many levels of
organization using a wide range of techniques. Each nation and its systematics
institutions must accept responsibility for facilitating taxonomic work that is
not only relevant to its own interests and objectives but which also contributes
to the global knowledge-base.
Despite the urgency for additional systematic expertise, the contributions
of the limited number of taxonomists working today can be increased immedi-
ately and significantly to meet the demand for knowledge about biodiversity if
given the requisite support. Support personnel who are knowledgeable about
the group being studied can multiply the productivity of single or teams of
scientists. Collectors, preparators, curatorial assistants, illustrators, database
managers, laboratory technicians, and others can perform tasks that today oc-
cupy a significant proportion of systematists’ time. Such personnel, familiar with
common species, proper collecting protocols, and procedures for handling speci-
mens, also could extend the field activitia˜ of a taxonomist to many sites simul-
taneously.

EPILOGUE: AN OPTIMISTIC FUTURE

Systematics Agenda 2000 must be seen for what it is: big science. It is noth-
ing short of planetary exploration, requiring the resolve to understand the biota
of Earth for the future benefit of humanity and the conservation of the natural
world. The use of biodiversity already contributes trillions of dollars to the
world economy through the goods and services it provides. Thus, it is not only
a good investment to have scientific knowledge about the world around us, it is
a matter of survival.
Because many aspects of taxonomic research are not perceived as being ex-
pensive or technologically intensive, it has been falsely assumed that the mis-
sions of systematics do not meet the contemporary criteria for status as “big
science.” Yet the missions of systematic biology constitute an immense and
complex scientific enterprise, ultimately accounting for the biodiversity of the

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TAXONOMIC PREPAREDNESS / 445

present and past world (see Systematics Agenda 2000, 1994a,b). The dimensions
of the biodiversity crisis are immense, and the extinction of several million spe-
cies over the next few decades seems certain unless nations respond forcefully.
This, and the lack of sufficient scientific information to confront the biodiversity
crisis with effective policies, contributes to a sense of doom. We are, nonethe-
less, cautiously optimistic. Whereas taxonomic expertise has declined sharply,
the field is more intellectually vibrant and exciting than ever, and existing sci-
entists are eager to train a new generation of experts. With adequate resources
for the kind of research taxonomists do, positions would open, and students
would gravitate to the field. Given successful examples of the knowledge and
understanding that would emerge from world-wide inventories of targeted taxa,
benefits to nations participating in this global exploration of biodiversity would
become evident.
In the industrialized countries, at least, construction of a massive scientific
infrastructure from scratch to meet the biodiversity challenge would not be nec-
essary. A first step would be to expand, amplify, and support more fully those
scientists and infrastructure that are already in place and to make accessible data
from the hundreds of millions of specimens already housed in our museums.
Recent advances in the theory of systematics have been rapid and profound,
giving a promising conceptual context for understanding the origin and diver-
sification of organisms on Earth. New and diverse sources of comparative data
have been developed, extending and enhancing our means of critically testing
phylogenetic hypotheses. The expanding capacities of computational tools pro-
vide hope for managing facts about tens of millions of species around the globe.
Systematic biologists thus know what must be done in response to the bio-
diversity challenge and have the conceptual and practical tools to accomplish it.
Society now needs the courage and foresight to invest in the growth of the
fundamental taxonomic knowledge that will make scientifically informed deci-
sions about resource management and conservation possible in the future.

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among the areas of endemism of Australian vertebrates. Aust. Syst. Bot. 4:211-227.
Cracraft, J. 1995. The urgency of building global capacity for biodiversity science. Conserv.
Biodiv. (in press).
Daly, H. V. 1995. Endangered species: Doctoral students in systematic entomology. Amer. Entomol.
41:55-59.
Edwards, S. R., G. M. Davis, and L. I. Nevling. 1985. The Systematics Community. Association of
Systematics Collections, Lawrence, Kans.
Eldredge, N., and J. Cracraft. 1980. Phylogenetic Patterns and the Evolutionary Process. Columbia
University Press, N.Y.
Forey, P. L., C. J. Humphries, I. L. Kitching, R. W. Scotland, D. J. Siebert, and D. M. Williams. 1992.
Cladistics: A Practical Course in Systematics. Clarendon Press, Oxford, England.
Holden, C. 1989. Entomologists wane as insects wax. Science 246:754-756.

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House of Lords. 1991. Systematic Biology Research. Select Committee on Science and Technology,
First Report. HL Paper 22-I. HMSO, London.
Janzen, D. H. 1993. Taxonomy: Universal and essential infrastructure for development and manage-
ment of tropical wildland biodiversity. Pp. 100-113 in O. T. Sandlund and P. J. Schei, eds.,
Proceedings of the Norway/UNEP Expert Conference on Biodiversity. NINA, Trondheim,
Norway. 190 pp.
Janzen, D. H., and W. Hallwachs. 1994. All Taxa Biodiversity Inventory (ATBI) of Terrestrial Sys-
tems. A Generic Protocol for Preparing Wildland Biodiversity for Non-damaging Use. Report
of National Science Foundation Workshop, 16-18 April, 1993, in Philadelphia. National Sci-
ence Foundation, Washington, D.C. 132 pp.
Langreth, R. 1994. The world according to Dan Janzen. Pop. Sci. 245:78-82, 112, 114-115.
Mayr, E. 1963. Animal Species and Evolution. Harvard University Press, Cambridge, Mass.
Myers, N. 1991. Tropical forests: Present status and future outlook. Climate Change 19:3-32.
Nash, S. 1989. The plight of systematists: Are they an endangered species? Scientist (16 Oct):7.
National Research Council. 1992. Conserving Biodiversity: A Research Agenda for Development
Agencies. National Academy Press, Washington, D.C.
National Research Council. 1993. A Biological Survey for the Nation. National Academy Press,
Washington, D.C.
National Science Board. 1989. Loss of Biological Diversity: A Global Crisis Requiring International
Solutions. National Science Foundation, Washington, D.C.
National Science Foundation. 1990. Systematic Biology Training and Personnel. U.S. Higher Edu-
cation Survey, No. 10. National Science Foundation, Washington, D.C.
Nelson, G., and N. Platnick. 1981. Systematics and Biogeography: Cladistics and Vicariance. Co-
lumbia University Press, N.Y.
Raven, P. H., and E. O. Wilson. 1992. A fifty-year plan for biodiversity studies. Science 258:1099-
1100.
Schoch, R. M. 1986. Phylogeny Reconstruction in Paleontology. Van Nostrand Reinhold, N.Y.
Schrock, J. R. 1989. Pre-graduate education in systematics and organismic biology. Assoc. Syst.
Coll. Newsletter 17:53-55.
Systematics Agenda 2000. 1994a. Systematics Agenda 2000: Charting the Biosphere. Technical
Report. Systematics Agenda 2000, a Consortium of the American Society of Plant Taxono-
mists, the Society of Systematic Biologists, and the Willi Hennig Society, in cooperation with
the Association of Systematics Collections, N.Y. 34 pp.
Systematics Agenda 2000. 1994b. Systematics Agenda 2000: Charting the Biosphere. Systematics
Agenda 2000, a Consortium of the American Society of Plant Taxonomists, the Society of Sys-
tematic Biologists, and the Willi Hennig Society, in cooperation with the Association of Sys-
tematics Collections, N.Y. 20 pp.
Wheeler, Q. D. 1995a. The “old systematics”: Phylogeny and classification. Pp. 31-62 in J. Pakaluk
and S. A. Slipinski, eds., Biology, Phylogeny, and Classification of Coleoptera: Papers Celebrat-
ing the Eightieth Birthday of Roy A. Crowson. Muzeum i Instytut Zoologii PAN, Warszawa,
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Conserv. 4:476-489.
Wiley, E. O. 1981. Phylogenetics. John Wiley and Sons, N.Y.

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CHAPTER
29

Museums, Research Collections, and

the Biodiversity Challenge

LESLIE J. MEHRHOFF
Supervising Biologist, Connecticut Geological and Natural History Survey;
and G. Safford Torrey Herbarium, Department of Ecology and
Evolutionary Biology, University of Connecticut, Storrs

A few years ago a young student asked a very straightforward question in

response to my statement that there were about 1.5 million species currently
known to science and that there could be anywhere from 5 to 30 million species
on this planet. He wanted to know who counted them. I explained how Wilson
(1988) arrived at the number of 1.5 million and that seemed to suffice. In retro-
spect, I missed a chance to explain the importance of museum collections in
documenting global biodiversity.
Museums are important tools for inventorying our planet’s biological diver-
sity, second only to the discerning eyes, love of field work, and innate senses of
the naturalists1 who collect the specimens. Natural history collections through-
out the world house over 2 billion specimens (Duckworth et al., 1993). Many of
these specimens represent the 1.5 million species currently known to science.
Most museums have specimens that await processing and some of these may be
new to science. Since it is possible that there may be as many as 100 million
species of organisms in the world (Wilson, 1992), the specimens already in mu-
1 The term “naturalist” is used here in the classical sense of a field biologist who is knowledgeable

about the systematics and ecology of organisms and their environment and who gathers data in
order to speculate on scientific problems. Examples such as Charles Darwin, William Beebe, Will-
iam Morton Wheeler, or Edward O. Wilson quickly come to mind. I do not mean naturalist in the
sense of park naturalists (who would be better called interpreters) or people who simply enjoy the
outdoors and who are really nature-lovers. If “naturalist” be thought of as an archaic or atavistic,
if not somewhat derogatory, distinction, I suggest Mehrhoff (in press), Wheeler (1923), or Wilson
(1992:243, 1994b) be consulted. Perhaps the late Raymond Fosberg (1972:633) said it best: “The
better scientist may be the one who can validly claim to be both systematist and ecologist, better
called a naturalist.”

447

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448 / BIODIVERSITY II

seum collections may represent only a portion of the Earth’s biological diver-
sity. Inventories must be conducted, specimens collected, identified, and—if
new to science—named and classified, and the current museum backlog must be
processed if we are going to have a complete understanding of biodiversity.
There are daunting tasks ahead for natural history museums, research collec-
tions, and the curators, systematists, and staff who are responsible for them.
There are two types of natural history museums. To most biologists, the
word “museum” means research collections. These museums are the subject of
this chapter. The kind of natural history museum with which most people are
familiar, however, emphasizes public exhibits. The importance of this kind of
natural history museum in inspiring young naturalists or in educating the mil-
lions of people who visit them annually should not be overlooked.
Outreach and education are components of most modern research museums.
Museum exhibits depict biological diversity and serve as a valuable tool for
stimulating an interest in natural history as well as educating people about many
things. These are important and necessary services in the name of biological
diversity. Not the least of the important messages is the challenge of maintain-
ing global biodiversity.
No one can forget his or her first visit to a natural history museum. Most of
us were fortunate to visit a large museum when we were young and impression-
able. For some it was the dinosaurs that were the most memorable, for others the
cases of beautiful butterflies. Still others marvelled at the birds, or beetles, or
turtles. The diversity of interests were bounded only by the breadth of the
museum’s collections and exhibits.
The natural history museum was a place to which the many youngsters who
grew up with an interest in natural history could return to see specimens of
animals that fascinated them. For those of us who grew up in northern, temper-
ate climates where much of the biota becomes dormant each winter, the museum
represented a mental sanctuary where we could continue to absorb more natural
history until the spring thaw once again brought an abundance of life to the
fields and woods.
Museums shaped the lives of countless young naturalists whose interests
have withstood the test of time and the rigors of education. Unfortunately,
many budding careers were derailed later in life for any of a thousand different
reasons. I suspect, however, that memories of those early visits to museums are
still in the subconscious of those who chose different roads, and can be brought
out, dusted off, and the interests rekindled.
Research natural history museums are collections of specimens that docu-
ment the diversity of organisms that exist, or have existed, on this planet 2. These
usually are associated with research institutions (e.g., the Academy of Natural
2 These collections may be botanical (usually referred to as herbaria), including vascular or non-
vascular plants, or zoological, including vertebrates and invertebrates. Other kingdoms of organ-
isms also can be included.

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MUSEUMS AND RESEARCH COLLECTIONS / 449

Sciences of Philadelphia, the Smith-

sonian Institution, the Missouri Bo-
tanical Garden, and the American Mu-
seum of Natural History) or major
universities (e.g., Harvard Univer-
sity’s Museum of Comparative Zool-
ogy and Gray Herbarium, the Univer-
sity of Kansas’ Museum of Natural
History, and University of California
at Berkeley’s Jepson Herbarium and
Museum of Vertebrate Zoology). Of-
ten the lines between research muse-
ums and universities are not clear,
with curators from the museums serv-
ing joint appointments on the univer-
sity faculty and vice versa.
The building blocks of any mu-
seum are its specimens. Specimens
can be of whole organisms or parts,
such as bones, fur, fruits, or spores.
Professor Edward O. Wilson with a student Specimens are mounted on microscope
in the Entomology Division of the Museum of slides, kept in alcohol, or preserved in
Comparative Zoology, Harvard University. more esoteric ways. Museums have a
diversity of types of specimens and
have developed sophisticated ways of preparing and maintaining the specimens.
There are many helpful books, pamphlets, or other aids for the preparation of
specimens. Much time and effort usually has gone into the preparation and
curation of the final specimens.
Some of the larger research museums have millions of specimens. In addi-
tion, there are many smaller collections, usually at colleges and universities,
whose numbers of specimens are not as large but are also important. These
smaller collections frequently specialize in particular taxonomic groups or geo-
graphic areas and have curators or faculty who are specialists in these areas.
The unique value of collections to conservation is that they are an irreplace-
able library of knowledge on the diversity of life. Each specimen is part of a
composite picture. They can be used to document biodiversity over both time
and space. If maintained properly, specimens in every collection provide a per-
manent record of life on Earth.

FROM CABINETS OF CURIOSITIES TO MODERN

NATURAL HISTORY MUSEUMS: A BRIEF HISTORY
In Europe, the collection of natural history specimens for the purpose of
displaying the variety of living organisms in museums began in earnest in the

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sixteenth century. The first natural history museums belonged to wealthy indi-
viduals who maintained them both as a hobby and as an indication of social
standing. Wealthy patrons supported these collections because it was fashion-
able to do so or because of noblesse oblige, not to facilitate the dissemination of
knowledge. Even in the sixteenth century, knowledge of the living world rep-
resented power. Many early collectors were doctors, clerics, or teachers. Their
specimens either were commissioned by the wealthy or sold by subscriptions.
Social interests provided economic support for naturalists and their cabinets of
curiosities (Bowler, 1992).
The utilitarian basis for these museums was to show what God had placed
on Earth to benefit mankind. There were strong religious overtones in the dis-
play of God’s creations (Bowler, 1992). To study nature was to worship God’s
work that was manifest on Earth. There was no need to collect or display mul-
tiple specimens because of the fixity of nature in God’s creations. For the most
part, there was little or no recognition of diversity within a species. In addition,
the fact that many collections had few individuals of the same species was prob-
ably a practical consideration of space and costs of maintenance as well.
Exploration in the seventeenth, eighteenth, and nineteenth centuries pro-
duced many plants and animals never before seen by Europeans. Many of the
early museums in Europe were built from the vast collections brought back from
abroad by voyages of exploration (Mayr, 1982). By the last half of the eigh-
teenth century, the number of known species was becoming cumbersome for
naturalists. The establishment of a species concept and binomial nomenclature
were of paramount importance to natural history (Mayr, 1946). Specimens had
to be described and classified to be of use to naturalists (Bowler, 1992). The
naturalists in Europe who described and classified species had to rely on speci-
mens in museums because they had little or no field experience with these or-
ganisms. The best known of the early naturalists, Carolus Linnaeus 3 (1701-1778)
built a highly respected collection representing the world’s known biota. His
students and correspondents sent back specimens from all around the globe
(Blunt, 1971).
The Procrustean explanations of some religious doctrines were beginning to
be challenged. Even the religious Linnaeus questioned how the 5,600 species of
animals that he had named, not to mention all others then known, could have
been saved in Noah’s Ark. In addition, distributions of animals could no longer
be made to fit with Biblical interpretations. The diversity of vertebrates alone
made a literal translation of Genesis and the account of the “Great Flood” unten-
able. The Noachian story was abandoned for scientific reasons (Browne, 1983).

3 When Linnaeus died, his personal herbarium and library were offered to Sir Joseph Banks, but

later were sold to James Smith. His specimens and books were used to found Britain’s oldest natural
history society in 1788, the Linnean Society of London. After Smith left London, the Linnean
Society purchased the collection from him. The fact that anyone was willing to pay for a collection
of dried plants was indicative of the value that naturalists placed on specimens (Bowler, 1992).

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In the United States, Charles Willson Peale’s natural history museum opened
in Philadelphia in 1786. It attracted the public, who wished to see wonders from
the natural world, more than naturalists, who wished to study organisms. Many
of the early museums had a decidedly “circus side-show” flair (Barber, 1980).
Natural history museums prospered in the nineteenth century because the
people who came to see them were interested in the bizarre, strange, unfamiliar,
or unknown (Barber, 1980). Exploratory voyages returned from far-off lands
loaded with specimens that differed from anything previously known. Many
novelties were put on public display long before they were interpreted by natu-
ralists. These were the harvest days of museums (Goode, 1901a).
While museum visitors viewed the public displays, naturalists relied heavily
on museums to show similarities and differences between species. Taxonomic
research on the diversity of organisms was done in museum collections. Natu-
ralists could no longer be expected to be familiar with all known species (Huxley,
1861). As the number of species grew, naturalists were forced to specialize
(Mayr, 1946).
Many natural history museums were started in larger cities of the United
States during the nineteenth century. Philadelphia’s Academy of Natural Sci-
ences was established in 1812 (Bennett, 1983). The Boston Society of Natural
History began in 1830 (Creed, 1930). The Smithsonian Institution was created in
1846 and by 1850 included 6,000 specimens (Rivinus and Youssef, 1992). The
American Museum of Natural History opened in 1877 (Preston, 1986).

The National Museum of Natural History, Smithsoniam Institution, Washington, D.C.

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The Smithsonian Institution’s first Secretary was Joseph Henry, who was
not overly enthusiastic about collections (Dupree, 1957). His assistant secretary,
Spencer F. Baird, however, was a collector, and was good at persuading others
to collect for him (Yochelson, 1985). He was the champion of a national museum
and did much to catapult it into international prominence (Rivinus and Youssef,
1992). The term “National Museum” was not used for the collections until 1851
(Goode, 1901b). The first collections came to the Smithsonian from the Patent
Office’s “National Cabinet of Curiosities,” where they had been moldering for
years (Dupree, 1957). The original natural history museum was housed in the
Smithsonian “Castle” in Washington, D.C., but a new building, the present Na-
tional Museum of Natural History, was opened across from the Castle in 1909
(Yochelson, 1985).
Swiss-born Louis Agassiz came to the United States in 1846 to deliver a
series of lectures at the Lowell Institute in Boston. His charismatic nature and
his reputation as a naturalist so impressed the people of Boston that they encour-
aged him to stay. He remained and taught at Harvard University from 1848
until his death in 1873 (Lurie, 1960). Agassiz was a collector who envisioned a
natural history museum in Cambridge, Massachusetts, that would resemble the
best European museums. His museum would illustrate patterns of similarities in
nature. He would have complete control over this museum, allowing him to
teach zoology the way he thought it should be taught. Agassiz’s method of
studying nature was to amass a large collection of individual specimens in order
to make comparisons. Agassiz reasoned that many specimens of the same taxon
were needed in order to truly interpret natural history (Winsor, 1991). The
Museum of Comparative Zoölogy, “Agassiz’s Museum,” opened in 1859. It is a
monument to his far-sighted vision.
By the end of the nineteenth century, many large collections of natural
history specimens existed in the United States, rivaling the holdings in Euro-
pean museums. Many universities had large research museums that were used
by biologists—the name biologist having replaced the earlier professional name
of naturalist—to study and classify organisms. These collections formed the
basis for an increasing knowledge of global biological diversity.
Interest in museums, biological research, and the value to education of their
collections was apparent by the beginning of the twentieth century. In 1903,
the New York State Museum published a catalog of the natural history museums
of the United States and Canada (F. Merrill, 1903). This catalog resulted from a
survey of both large and small museums in order to fill the “lack of general and
specific information concerning the natural history museums of this country
and their collections.” Two hundred sixty-four museums from the United States
and Canada responded to the survey. The catalog attempted to inventory the
holdings of each museum as to kinds of specimens they maintained (botanical,
vertebrate-skin, skull, liquid, etc.), numbers of each kind, and important his-
torical collections contained in the museum.

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The beginning of the twentieth century also saw an expansion of interest in

the world’s tropical regions. Many universities and museums in temperate coun-
tries began detailed floristic and faunistic surveys of tropical natural history.
These yielded numerous publications and many thousands of specimens to be
identified, classified, and curated. World War II brought another resurgence of
interest in the biology of tropical countries. During the war, many biologists
were sent to tropical countries to collect new or better sources of medicines.
Biologists collecting in tropical countries brought back specimens to major mu-
seums (E. Merrill, 1946).
Today, museums that house research collections are an invaluable and irre-
placeable source of knowledge on the flora and fauna of the world. New collec-
tions are being added while the older, historically significant specimens are be-
ing maintained for research. This represents a large scientific and financial
responsibility for the museums. These collections are the very basis of our
knowledge of biodiversity.

GOVERNMENT BIOLOGICAL SURVEYS:

STATE NATURAL HISTORY SURVEYS
An important component for inventorying the biological diversity of the
United States are the state and national biological surveys. These surveys have
collected many specimens that help document biological diversity. Although
their current roles are expanded greatly beyond museum collections, they still
maintain an active interest in their collections. Their specimens increasingly are
used in conservation work.
Many states established state natural history surveys to inventory their re-
spective biotas. Some of the early surveys were combined with geological sur-
veys of the state’s mineral resources (Socolow, 1988). The earliest of these was
the New York State Geological and Natural History Survey. The New York
Survey was established in 1836 and later was split into a biological survey and
a geological survey (Miller, 1986). Some state geological surveys provided much
biological information. A well-known example was the early California Geologi-
cal Survey, which began in 1860 (Brewer, 1966). Other state natural history
surveys were disbanded, reorganized, or shifted to other programs. The Illinois
Natural History Survey, by far the biggest and most active of remaining state
natural history surveys, began in 1858. Connecticut’s State Geological and Natu-
ral History Survey, begun in 1903, is one of two active surveys that includes
both biology and geology. The youngest state survey is the Rhode Island Natu-
ral History Survey. It was initiated in 1993 and incorporated in May 1994.
Unfortunately, there are less than a dozen active state biological surveys cur-
rently in existence.
Most of the remaining state biological surveys perform a variety of activi-
ties within the state (Risser, 1986). They conduct inventories of species and

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TABLE 29-1 Consortium of Biological Surveys

Year
Name Established Government Affiliation

Connecticut Geological and 1903 Department of Environmental Protection

Natural History Survey
Hawaii Biological Survey 1992 Bernice P. Bishop Museum, and State
Museum of Natural and Cultural History
Illinois Natural History Survey 1858 Department of Energy and
Natural Resources
Kansas Biological Survey 1959a University of Kansas
New York State Biological Survey 1836 New York State Museum, and State
Education Department
North Carolina Biological Survey 1976 North Carolina State Museum of
Natural Resources
Ohio Biological Survey 1912 The Ohio State University
Oklahoma Biological Survey 1988b University of Oklahoma
Pennsylvania Biological Survey 1988c Private Consortium
Rhode Island Natural History Survey 1993 Private Consortium

aInitiated in 1911.
bInitiated in 1927.
c Initiated in 1979.

habitats and publish the results. Most surveys function as clearinghouses for
information for other state agencies, academia, and the public. Publishing has
been a major part of many state biological surveys. A few surveys are involved
in environmental review or provide management recommendations. The State
Heritage Program is part of the state survey in Connecticut, Kansas, and Okla-
homa. Most states maintain collections that document their state’s biological
heritage. Some of the state surveys, such as those of Hawaii and New York, are
associated with state natural history museums and share collections. Others, such
as those in Kansas, Oklahoma, Ohio, and Illinois, are associated with the state uni-
versity and deposit their specimens in the university’s research collections.
In 1993, 10 state biological surveys formed a Consortium of State Biological
Surveys (see Table 29-1). These surveys have a unifying interest in collections
and common goals of inventory, research, and dissemination of information. At
its initial meeting held in Columbus, Ohio, in December 1993, the Consortium
passed a resolution to support the goals of the National Biological Survey 4 and to
work with the National Biological Survey to make the best use of their existing
information and collections. It was exciting that both the oldest and the newest
state surveys were founding members of the Consortium.

4 The Secretary of the Interior, Bruce Babbitt, recently has changed the name to the National

Biological Service.

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GOVERNMENT BIOLOGICAL SURVEYS:

THE NATIONAL BIOLOGICAL SURVEY
Biologists and conservationists were encouraged by the announcement of
the Secretary of the Interior, Bruce Babbitt, of the formation of a National Bio-
logical Survey in 1993. His intention was to unite the biological research that
currently is underway within the eight agencies of the Department: the Bureau
of Land Management, Bureau of Mines, Bureau of Reclamation, Fish and Wild-
life Service, Geological Survey, Minerals Management Service, National Park
Service, and Office of Surface Mining (Corn, 1993). One of the primary objec-
tives of the National Biological Survey is “to develop comprehensive ecosystem
management strategies...” (Corn, 1993:CRS-1). An additional objective is to “give
land and resource managers more timely, objective scientific information essen-
tial for decision-making...” (Corn, 1993:CRS-1).
This was really the second beginning of a National Biological Survey. The
earlier national survey mostly has been forgotten, even by the scientific commu-
nity. Although it had a convoluted nomenclatural history, it played an impor-
tant role in attempting to understand the natural history of the United States.
In 1885, Congress created a Section of Ornithology within the U.S. Depart-
ment of Agriculture’s Division of Entomology. Within a year, this became the
Division of Ornithology and, by 1888, it was officially called the Division of
Economic Ornithology and Mammalogy (Osgood, 1943). “Economic” usually
was dropped from the title, simplifying it to the Division of Ornithology and
Mammalogy. This was probably at the insistence of its first director, C. Hart
Merriam, who favored the subordination of the economic nature of the Division’s
work to the scientific (Cameron, 1929). By 1889, Merriam was advocating the
establishment of a “systematic Biological Survey.” Finally, in 1896, Congress
transformed his agency into the Division of Biological Survey. This gave official
recognition to what Merriam and his staff had been doing for almost a decade
(Sterling, 1974).
In 1905, the title of the Division again was changed, this time to the Bureau
of Biological Survey. In 1940, the Bureau was transferred to the U.S. Depart-
ment of the Interior, where it was joined with the former Fish Commission to
become the Fish and Wildlife Service (Osgood, 1943).
The Bureau of Biological Survey was under the direction of Merriam from
1885 until 1910, when he stepped down to pursue independent research. He
felt that the Bureau should be primarily a research program aimed at gathering
information on the biology of the United States. He was best known for his
pioneering work on “life zones.” Merriam led by example, much preferring to
spend his summers in the field and winters in Washington, D.C. (Osgood, 1943).
Merriam was a prodigious collector of natural history specimens, first of birds
and eggs and later—mostly during his work with the Bureau of Biological Sur-
vey—of mammals. He began collecting in 1870 when he was 15 years old, and

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by 1940 his mammal collection was reported to contain 136,613 specimens with
full data and in prime condition (Osgood, 1943).
While there seemed not to be a direct governmental mandate to collect speci-
mens, Merriam’s field method was to collect mammals, birds, reptiles, and am-
phibians from a study site. Representative plant specimens were taken, as were
photographs when possible. All these served as the basis for the reports he was
compiling. This method later was adopted by other members of the Bureau
(Sterling, 1974). Many specimens collected under the auspices of the Bureau of
Biological Survey are in the Smithsonian’s Natural History Museum (Hampton,
personal communication, 1994).
The current National Biological Survey hopes to increase the degree of com-
munication and collaboration between federal agencies and the museum com-
munity (National Biological Survey fact sheet, no date). The U.S. Department of
the Interior signed a memorandum of understanding with the Association of
Systematic Collections in February 1994. The memorandum recognizes the com-
mon mission and mutual interest in collections and biological inventory. The
National Biological Survey and the Association of Systematics Collections, which
represents member institutions, societies, and individuals, have formed a work-
ing group to determine the policies of the National Biological Survey regarding
museums and collections (Hoagland, personal communication, 1994). Further-
more, they hope to ensure that specimens gathered during the work of the Na-
tional Biological Survey will be accessioned and curated efficiently (National
Biological Survey fact sheet, no date). The National Biological Survey may be
able to encourage inventory of the biotic resources of the United States and
support basic taxonomic work on priority groups.

SYSTEMATISTS AND THE USE OF COLLECTIONS

The two primary roles of the research collection are education and docu-
mentation. I have divided these roles into five greatly overlapping functions:
systematic research, documentation in space and time, identification, education,
and specimen maintenance (Mehrhoff, in press). Every museum that maintains
research collections, large or small, must serve these roles and functions if it is to
continue to play an important part in the preservation of biological diversity.
Each specimen in a museum is a data set of useful information. Information
can be gleaned on identification, classification, morphology, phenology, and
distribution. Collections also meet the needs of applied biology, such as health
sciences, agriculture, resource management, and biotechnology (Systematics
Agenda 2000, 1994).
In addition to the value of the specimen for systematic and scientific re-
search, there are other, less frequently considered, values of collections (Mayr
and Goodwin, no date). Museum collections are the only place to see examples
of extinct species. If we are to understand where these taxa fit in classification

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MUSEUMS AND RESEARCH COLLECTIONS / 457

Researcher sorting bat specimens.

schemes, or reevaluate phylogenetic relationships, we must have the specimens.

Given the backlog of material waiting to be curated in many collections, one
wonders how many of Wilson’s “centinelan extinctions 5” will come to light.
Specimens also document a previously existing biota. This documentation also
can work for recent arrivals (Mehrhoff, in press). Specimens represent expendi-
tures in obtaining them, especially if they were collected in inaccessible areas
(Mayr and Goodwin, no date).
Specimens must be properly curated and maintained for all of these reasons.
If specimens are lost, damaged, or discarded, the value of the information they
represent will be severely decreased. Stewardship of collections should be a
primary concern for everyone in charge of natural history collections. This is
very nicely addressed in a project report of the National Institute for the Conser-
vation of Cultural Property (Duckworth et al., 1993). Every curator should have
a copy of this report.
5 Silent, undocumented extinctions—named after a cloud-forested ridge in the western foothills of

the Andes that was cleared for farming, causing the extinction of a large number of rare, endemic
species within a few months. The extinctions of Centinela were observed only through an accident
in timing, when Alwyn Gentry and Calaway Dodson of the Missouri Botanical Gardens happened to
visit the site immediately before its demise (Wilson, 1992:243).

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Museum collections represent cumulative knowledge, with each museum

representing a piece of that knowledge. No museum exactly duplicates the hold-
ings of any other collection. A network of museums can make their specimens
available for research through national and international loan programs. It is
much more efficient to send specimens to researchers at their home institutions
rather than expect the researchers to visit each museum where material is avail-
able (Quicke, 1993). The means by which electronic data can be transferred to
expedite certain aspects of research should be explored (Alberch, 1993).
The most important way for a museum to address the roles of their collec-
tions is to maintain an active research and education program for students inter-
ested in careers in systematics. This would solve many of the problems revolv-
ing around the needed biological inventories. Systematists do systematic
research so that the classification of known organisms can be improved and the
proper placement of newly discovered taxa can be accomplished. Specimens for
this systematic research, which also document biodiversity, will come into mu-
seums from naturalists in the field as well as from the systematists themselves.
Students can be trained to take on parts of larger projects.
This is a simplistic solution, especially when considering the current prob-
lems facing museums. Things are always more complex than they seem. The
two problems produced by this simple recommendation are space for the new
specimens and curatorial costs. Some scientists are calling for a global inventory
of biodiversity. Additional trained field people will be necessary. Museums
will be forced to expand their holdings. New material for mounting specimens,
cabinets, space, and curation will be necessary. Ultimately these all lead to the
other major problem: cost. Who will pay for this education and expansion?
Space is not a small issue by itself, let alone in conjunction with cost. A few
years ago, three Australian “botanical taxonomists” suggested that only type
specimens and a few important vouchers were really necessary to maintain in
herbaria (Clifford et al., 1990). Their suggestion was to save these limited collec-
tions, and all other material could have the data recorded into a database and
then the specimens could be “pulped.” There was an outpouring of disagree-
ment in a subsequent issue of the same journal (West et al., 1990) and, fortu-
nately, no curators seem to have followed their suggestion.
Just at a time when the world is losing species at an unprecedented rate,
collections are being forced to be selective about acquisitions (Quicke, 1993). If
collections swell from the influx of new specimens, then both space and curato-
rial costs will increase concomitantly. Clearly, these two issues may become
important limiting factors in completing global inventories of biodiversity.
The curators of many collections are forced to consider unofficial policies
on what to collect or accession. I formulated guidelines to help determine what
to collect for the Connecticut Geological and Natural History Survey’s project
on state flora. I am attempting to use these same guidelines in determining

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which student collections should be accessioned into the G. Safford Torrey Her-
barium at the University of Connecticut. While funding previously may not
have been a primary consideration for curators, it now has become one of para-
mount importance. At the very least, major granting sources such as the Na-
tional Science Foundation must increase their grants to systematists and system-
atic collections. Grants from other less traditional sources also must be sought.
It is conceivable that curators might find new sources of money if their museum’s
specimens were viewed as part of our natural heritage.
Systematists must see as part of their responsibility the funding of collec-
tions holding the specimens that are necessary for their work. Ecologists and
other scientists who routinely deposit voucher specimens to document their re-
search also should support collections financially to ensure their long-term main-
tenance (Quicke, 1993).
Scientists must consider museums when budgeting for research work. This
becomes especially important for museums in other countries. When working
in developing countries, scientists should budget for extra time to be spent in
those countries visiting national museums and universities in order to annotate
specimens, give short courses, or present seminars on their research. They
should hire field assistants from those museums and universities. Biologists
should allow for costs of extra publications resulting from their research so that
they can be made available at no cost to scientists and conservationists in devel-
oping countries.
Additional sources of funds for both systematic research and for collection
maintenance must come from the conservation community. In the past, conser-
vation programs—both in government and private nonprofit organizations—
have taken museum work for granted, especially when it comes to funding and
support (Mehrhoff, in press). All too often, they use the collections due to the
good-will of the curators and institutions. This has to change. Collections are
basic not only to every scientific discipline but to the majority of conservation
issues as well (Lutz, 1994). We must realize that the limited funds for conserva-
tion also must be used to assist collections and their long-term maintenance.
Interest in systematics seems to be waning just at a time when it is most
necessary (Kosztarab and Schaefer, 1990; Mehrhoff, in press; Parnell, 1993;
Quicke, 1993; Systematics Agenda 2000, 1994). If museums are to function as
research centers, then they must be staffed by competent curators and system-
atists who are using their specimens. I suspect that there are few deans or de-
partment heads who could support the long-term existence of unused research
collections. As we face a paucity of trained systematists, it becomes increasingly
difficult to imagine who will use existing collections. Biodiversity inventories
can create problems of increased needs for space and increased expenses, but
they also can suggest a solution. Museum staff must attempt to meet the chal-
lenging task of preserving global biodiversity.

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CONCLUSIONS
Scientists and conservationists acknowledge that we must have accurate
information in order to protect biological diversity (Committee on the Formation
of the National Biological Survey, 1993; McNeely et al., 1990; Norton, 1987;
Wilson, 1992; World Resources Institute et al., 1992). Basic to this need is a
global inventory of the world’s biota (Wilson, 1992). No single person, agency,
program, or institution is capable of this task. It must be a collaborative effort of
Herculean proportion. While some scientists are calling for a full-scale inven-
tory of the world’s biota, others are advocating more realistic approaches (Raven
and Wilson, 1992; Wilson, 1994a).
Given the magnitude and estimated costs of a global inventory, there is no
room for duplication of effort. We are fortunate that research museums have
been involved in biotic inventories for centuries. The specimens from these
museums can tell us not only what organisms exist or have existed, but they also
can give us an indication over time of distribution and, in some cases, abun-
dance (Mehrhoff, in press).
Naturalists are needed to participate in these inventories. No matter how
sophisticated equipment and techniques become, they cannot produce results
without dedicated, trained scientists to conduct the field work. Naturalists of
this caliber are becoming scarce. This is why the loss of Al Gentry and Ted
Parker (Stevens, 1993) was so keenly felt by the scientific community (Forsyth,
1994; Hurlbert, 1994).
Systematists also are necessary to deal with the increase of specimens that
will come into existing museums (Systematics Agenda 2000, 1994). The de-
crease in trained systematists to deal with the increased specimens obtained by
this renewed interest in inventorying biodiversity is not only paradoxical; it is
both noticeable and lamentable (see Lutz, 1994).
The current picture of systematic research is bleak. There presently are
only about 4,000 specialists in the United States and Canada capable of classify-
ing the organisms occurring in those countries. According to Kosztarab and
Schaefer (1990), there are only a few hundred specialists who are competent to
identify or conduct systematic research on some of the insect and arachnid
groups in the United States. It is important to remember that most of these
specialists only work part-time on the taxonomy of their group because they
teach at universities (Kosztarab and Schaefer, 1990). Some have additional ad-
ministrative responsibilities. Add to this the loss of positions in taxonomy at
universities and in government work. If positions vacated by taxonomists are
not being filled by taxonomists, who will teach the next generation of taxono-
mists? If we do not train students to become systematists, who will direct the
inventories necessary to assess biodiversity or name the plethora of new species
that will come from the specimens collected? The magnitude of the problem
quickly becomes sobering.

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The situation is even bleaker for the species-rich tropics. There are prob-
ably no more than 1,500 professional systematists capable of dealing with the
myriad of tropical organisms (Wilson, 1992). Most of the museums that have
large holdings of tropical organisms are in Europe, North America, and Austra-
lia (Alberch, 1993), adding to the difficulties in studying biological diversity in
developing countries. There are more practicing plant taxonomists in Europe
(about 1,000) and the United States (about 650) than in the tropics (about 520)
(Parnell, 1993). The area involved is small, yet tropical species represent over
70% of the world’s biodiversity.
Larger museums have a responsibility to developing countries. They must
make their holdings available to researchers working in tropical groups or in
tropical countries. This, however, places the financial burden on the museums
to support their collections, curate their material, pay their staff, and process
loans to researchers in other museums. These are all increasingly expensive in
today’s financial environment. Who will pay for these services? The financial
conundrum becomes more complex if you consider the alternative. It would be
almost prohibitively expensive for developing countries to build a comparable
reference collection (Alberch, 1993). It is likely that existing museums will re-
main the centers for taxonomic research, so we must find ways to support their
continued existence. Funding for museums, systematics, and for training future
systematists must be increased. Federal and state governments and the conser-
vation community all must do their share. The loss of any major museum or
research collection is unacceptable.
One program beyond the scope of this chapter deserves special mention.
Costa Rica’s Instituto Nacional de Biodiversidad (INBio) should be used as a
model for other countries who wish to develop an inventory of their nation’s
biological diversity (Valerio Gutierrez, 1992). This highly publicized program,
started in 1989, employs local people as parataxonomists who are trained to
collect museum specimens. These specimens later can be sorted and identified
at INBio’s main office and museum on the outskirts of San José. INBio is ex-
panding its services to meet the needs for data by government agencies, scien-
tists, educators, planners, and industry (World Resources Institute et al., 1992).
We have a long and venerable history of biological inventory that should
not be overlooked. More importantly, these collections represent a composite
picture of everything we currently know about the world’s biodiversity. We
need to increase support for systematics and collections. This increased support
has to be in services, such as training new field naturalists, systematists, and
curators, as well as in financial backing. The value of collections must be ac-
knowledged by government and private conservation programs.
Museum collections must be made “user-friendly.” Museum staff must do
their part to encourage students, faculty, and conservationists to use the collec-
tions. In addition to the roles and functions of museums already addressed,
curators must try to meet the realistic needs of conservationists.

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462 / BIODIVERSITY II

Curators and systematists, those most familiar with the value of collections,
must convince the public of their importance. Museums should increase the
number of exhibits that tie their collections to the preservation of biodiversity.
Too often, collections and those who work with them are taken for granted. A
worthwhile effort would be to publicize the value of collections via the popular
press.
Curators and systematists must take time from their research to spread the
word about biological diversity. Increased support for collections and system-
atic research will come only with increased understanding of the roles that col-
lections play in protecting biological diversity.
The word “enthusiasm” comes from the Greek word “enthousiamos”, mean-
ing “to inspire.” What is education if it is not to inspire? Enthusiasm for natu-
ral history can excite people. Many biologists became interested in science by
studying plants or animals. The only place better than in a museum to kindle an
interest in natural history is the field. Museum and field research are necessary
to renew interest in systematics. I suspect it was not thoughts of gene sequenc-
ing, electrophoresis, or cladistics that got many of today’s systematists inter-
ested in their work. The excitement of youth that pushed many of us toward
careers in systematics, inventory, or museums must be encouraged.
Most curators and systematists are enthusiastic about their work. Most
people who work in museums find them exciting places, not the dark, musty
images that some would paint. Since most systematists and curators spend a
portion of their time collecting, students can be hired as field assistants who will
learn by direct experience, especially from contagious enthusiasm. Future sys-
tematists should be encouraged by example. If more students take an interest in
systematics, either from a pure perspective or as an approach to the global
biodiversity challenge, then support likely will follow.
In our zeal to protect biodiversity, we cannot afford to ignore our collec-
tions. Collections of natural history specimens represent a priceless heritage as
well as an increasingly important database. It is of paramount importance that
no bits of this collective knowledge be lost.

ACKNOWLEDGMENTS
I wish to thank the many biologists and conservationists who have know-
ingly or unknowingly contributed to this paper by discussing with me over the
years the roles and functions of research collections. I have acknowledged many
of these in another paper on this subject and will not repeat them here. In
addition, I wish to thank those who have contributed information or helped me
find obscure references for this paper: Stefan P. Cover, Joseph J. Dowhan, Craig
Freeman, Michelle Hampton, K. Elaine Hoagland, John Ketchum, Gordon L.
Kirkland, Julie Lungren, Norton G. Miller, Robert M. Peck, Robert S. Ridgely,
Gary D. Schnell, David L. Wagner, and Alfred G. Wheeler.

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MUSEUMS AND RESEARCH COLLECTIONS / 463

Jane E. O’Donnell critically proofread the manuscript and made many helpful
and much-appreciated suggestions. Susan Carsten helped with word processing.

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CHAPTER
30

Resources for Biodiversity in Living

Collections and the Challenges of
Assessing Microbial Diversity

RICHARD O. ROBLIN
Associate Director for Science, American Type
Culture Collection, Rockville, Maryland

Although not generally visible to the naked eye, ubiquitous microbes are a
crucial element in the biological infrastructure of our planet. They break down
complex organic materials for reuse by new generations of plant and animal
cells, are central to the proper functioning of vital geochemical cycles, and their
genes code for the synthesis of a wide variety of drugs that are essential to the
treatment of human diseases (Bull et al., 1992). Because they spread easily, they
are found in air, water, and soil, as well as on the exterior and interior surfaces
of essentially all plants, birds, insects, and other animals. Microorganisms may
make up as much as 25-50% of the biomass of the Earth. Because microbes are
ubiquitous and functionally important, they clearly belong on the biodiversity
research agenda.
In this Chapter, I first review some of the authenticated microorganisms
that living collections, such as the American Type Culture Collection (ATCC),
can provide for use as reference standards in the assessment of microbial bio-
diversity. Second, I highlight some of the substantial challenges that will be
encountered in attempts to even partially describe the extent of microbial diver-
sity in even the smallest areas of the Earth. Finally, I stress the importance of
collaborative transnational efforts among scientific institutions in the develop-
ment of programs for measuring and developing the riches of the microbial cor-
nucopia.
Like macroorganisms, microorganisms are classified using genus and spe-
cies names. However, because the concept of a species is less definitive for
microorganisms than for higher organisms, there are multiple definitions for
this term in different subfields of microbiology. For bacteria, a microorganism

467

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where the concept of species is perhaps the most well-defined, I use the follow-
ing definition:
“A bacterial species may be regarded as a collection of strains that share many
features in common and differ considerably from other strains. (A strain is
made up of the descendants of a single isolation in pure culture, and usually is
made up of a succession of cultures ultimately derived from a single colony. )
One strain of a species is designated as the type strain; this strain serves as the
name-bearer strain of the species and is the permanent example of the species,
i.e., the reference specimen for the name. The type strain has great importance
for classification at the species level, because a species consists of the type
strain and all other strains that are considered sufficiently similar to it to war-
rant inclusion with it in the species” (Staley and Krieg, 1984:1).
As microbiologists isolated single-colony microbial strains from different
habitats around the world during the last 120 years, they described the organ-
isms and their properties in the scientific literature. More and more strains
accumulated, and the field of microbial systematics developed through attempts
to determine whether new microbial isolates were the same as or different from
those previously described. Fro-
zen storage of microorganismal
samples was introduced as a way
of minimizing the changes in prop-
erties observed when microorgan-
isms are cultured continuously for
long periods of time. As new fields
of science developed, they were
successively applied to determine
the degree of relatedness among
different microbial isolates.
Founded in 1925 by scien-
tists desiring to preserve and dis-
tribute useful microbial strains,
the ATCC serves as a repository of
authenticated type strains, the fun-
damental reference materials of the
system of microbial classification.
As of early 1994, the ATCC had
approximately 13,500 strains of
bacteria (including about 2,600
type strains representing different
species), approximately 26,000
strains of fungi and yeasts (includ-
Removal of frozen samples from a ing about 3,800 type cultures), and
liquid nitrogen container. approximately 1,200 protozoan

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RESOURCES IN LIVING COLLECTIONS / 469

strains (including about 60 “authenti-

cated” 1 strains). These cultures are
available to the scientific community
of the world for use as reference mate-
rials in studies of microbial diversity.
Their availability is limited only by
the requirements to obtain permits
from the U.S. Department of Agricul-
ture and U.S. Public Health Service
for shipment of agricultural, human,
or animal pathogens, respectively,
and the requirement for a valid export
license for shipment of materials out-
side the United States.
Although the numbers of micro-
bial strains (and species) in collections
like those of the ATCC are large, one
estimate puts the number of known
bacterial species at 4,800; known fun-
gal species at 69,000; and known A peritrich ciliate growing on a hydroid.
protozoan species at 30,800 (Wilson,
1992). Using this estimate and the ATCC as examples, the collection contains
about 54% of the type strains for the known bacterial species, about 5.5% of the
type cultures for the known fungal species, and only 0.2% of the “authenti-
cated” strains for the known protozoan species.
While this situation may appear somewhat reassuring (at least for bacteria),
many bacteriologists think that the number of known bacterial species is only a
small fraction of the total number of different bacterial species that currently
exist on Earth. For example, Palleroni (1994:538) writes:
“. . . the four volumes of Bergey’s Manual of Systematic Bacteriology describe
about 3,000 species, a number now considered to represent from a fraction of
one percent to a few percent of the total bacterial species in nature.”

With fungi and protozoans, the estimates are even less reassuring. One recent
well-documented estimate puts the total number of different species of fungi on
Earth at 1.5 million (Hawksworth, 1991). Thus, living culture collections such
as the ATCC contain only a small fraction of the bacterial, fungal, and protozoan
species thought to exist on Earth. We therefore are likely to encounter many
new microbial species through projects that assess microbial diversity.

1Protozoan type specimens generally are nonliving preparations on microscope slides. “Authen-

ticated” protozoan cultures are those obtained from the original describer of the species and subse-
quently grown and cryopreserved by ATCC.

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470 / BIODIVERSITY II

At the current level of resources, new bacterial type strains are being added
to the ATCC at an annual rate of about 100-125 per year, while the total number
of new bacterial strains added is 250-300 per year. A total of 500-700 new
fungal and yeast strains are added to the mycology collection each year. There
are usually more useful strains identified than the ATCC can accession each
year. Thus, the ATCC would not be able, at the current level of resources, to
absorb a major increase in the number of new bacterial, fungal, yeast, and pro-
tozoan strains accessioned per year.
The ATCC provides information on each strain in the collections in several
different media formats. The most recent versions of the written catalogs that
list each bacterial, fungal (including yeast), and protist strain total about 1,700
pages. This information is also available in CD-ROM and diskette form for per-
sonal computers and on the Internet via a Gopher server at the ATCC (gopher
culture.atcc.org). Together with specialized monographs on the distinguishing
features of different microbial species, the information and the cryopreserved
living specimens housed by collections such as the ATCC provide the frame-
work of previously known microbial species that is used to assess the novelty of
new isolates from the environment.
A broad variety of other general and specialized microbial collections can
provide information and examples of microbial type cultures. The Microbial
Germplasm Data Net (Moore, 1993) provides data on many microbial research
collections that is searchable over the Internet. The World Directory of Collec-
tions of Cultures of Microorganisms (Sugawara et al., 1993) provides data on 481
collections in 51 countries and includes the scientific names of 334,312 strains of
bacteria and 351,263 strains of fungi and yeasts. It also can be searched over the
Internet. These resources should be useful to researchers studying biodiversity
as points of contact and centers of expertise on the properties of a wide variety
of microorganisms.
Can this network of culture collections absorb the increase in new microbial
species that likely would result from implementation of an All Taxa Biodiversity
Inventory (ATBI)? Probably not, in my view, without a substantial additional
investment in this critical component of infrastructure. Many of the collections
are small and specialized, and primarily reflect the research interests of single
investigators or a small group of researchers. Even at current levels of support,
important specialized microbial collections periodically become “endangered”
through loss of financial support or retirement of the interested scientist.

THE CHALLENGES OF MEASURING MICROBIAL DIVERSITY

Recent molecular biological measurements estimate that about 4,000 differ-
ent bacterial species reside in a gram of Norwegian forest soil (Torsvik et al.,
1990; Wilson, 1992:143-144). Assuming that this is a reasonable measure of the
bacterial species complexity in such an environment, one begins to see the mag-

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RESOURCES IN LIVING COLLECTIONS / 471

nitude of the task that is required to enumerate even the bacterial species (much
less the fungal and protozoan species) present in the air, soil, and water, and on
the outer and inner surfaces of all the plants, insects, birds, and other animals in
a chosen area of tropical rain forest.
Part of the difficult nature of the task comes from my assumption that
many of the bacterial species isolated from the aforementioned different habi-
tats of the tropical rain forest will be very similar to those encountered in adja-
cent environments. Thus, much work may be expended to identify what ulti-
mately will turn out to be very similar strains of the same microbial species.
While this initially might seem like “wasted effort,” it will aid in answering
fundamental questions about the lateral spread of some microorganisms in a
specific environment.
Research on microbial diversity also will continue to isolate many organ-
isms that apparently are previously unknown. Only through more detailed bio-
chemical, immunological, or molecular biological tests will it become clear, how-
ever, whether the new isolates are sufficiently novel to be called new microbial
species. Depending on which combination of techniques is chosen, a reasonably
large amount of laboratory research will be required to answer the question of
novel species even for a single isolate. As the number of apparently novel iso-
lates increases, the amount of effort to characterize them quickly will become
more than any one institution can handle.
For this and other reasons, the ATCC joined forces with four other institu-
tions in the Washington, D.C., area (the Smithsonian Institution’s National Mu-
seum of Natural History, the U.S. Department of Agriculture’s Agricultural Re-
search Service, the University of Maryland at College Park, and the Maryland
Biotechnology Institute) to form the Consortium for Systematics and Bio-
diversity. The application of systematics, ecology, and evolution to biodiversity
will be a primary emphasis for Consortium members, who have agreed to coop-
erate in developing and enhancing research and training programs and facilities
for systematics and biodiversity. In this context, the ATCC will provide both
expertise in systematics and living examples of the type specimens that form the
current framework of microbial systematics.
Visionary proposals to carry out an ATBI (Janzen and Hallwachs, 1994) are
exciting in their promise to provide an integrated estimate of the total species
diversity in a selected area. However, if “all taxa” includes the microbes, as I
believe it should, some differences between the objectives for microorganisms
and macroorganisms will have to be introduced into the program in order to
develop practical plans. In the February 1994 draft of the ATBI planning docu-
ment, Janzen and Hallwachs (1994) discuss the microbes and several other
groups of organisms under the heading “Group G3. Species-rich taxa that are
sufficiently problematical that it may not be feasible to inventory a noticeable
fraction of their species in a 5 year period.”
The ATBI proposal nevertheless stimulates thinking about how large-scale

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472 / BIODIVERSITY II

investigation of microbial diversity

might be done. For example, Tiedje
(1995) recently has described the out-
lines of an experimental approach.
This approach emphasizes reduction
in the number of organisms analyzed
through identification of those that
have unique value for intensive
study. It advocates use of rapid, semi-
automated methods that generate
results in a form that can be placed
immediately into large computer data-
bases. Finally, it can serve as a useful
starting point for further discussion
among microbiologists about the most
fruitful and cost-effective methods for
characterizing microbial diversity in
the context of an ATBI.
Living culture collections should
study and selectively implement ac-
Growth of microorganisms in a petri dish. tions that will increase the utility of
their resource materials for the assess-
ment of microbial diversity. First, they can make detailed information about
their microorganisms available on a world-wide basis over the Internet. Second,
they can enhance the usefulness of the descriptive information about their col-
lection materials via multifaceted databases that include pictorial as well as text
descriptions. Finally, they can implement ways to increase their rate of acces-
sions so that, as new microorganisms are identified through ATBIs and other
initiatives to describe microbial diversity, more strains can be authenticated and
cryopreserved for further study and use by the scientific community of the
world.

INTERNATIONAL COOPERATION
The days when one could walk into any country with interesting habitats
for microbial diversity and walk out with one’s pockets full of interesting
samples appear to be over. Countries containing such habitats now are aware
that they may harbor microorganisms with commercial potential. Following the
Rio Conference in 1992, the United Nations Convention on Biological Diversity
(Reid et al., 1993:303-324) is in the process of being ratified by many nations.
This Convention sets out a framework for cooperation between nations in sus-
taining and developing biodiversity (including microbial diversity), but will
require implementing legislation in many nations before it is broadly effective.

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RESOURCES IN LIVING COLLECTIONS / 473

If an international consortium of scientists were to work on the identifica-

tion and characterization of microbial samples identified through an ATBI, then
some new mechanisms may have to be put in place to delineate the rights and
responsibilities of the cooperating parties. For the next few years, before na-
tional legislation implementing the U.N. Convention on Biological Diversity is
passed, specific contractual arrangements may have to be used as a substitute.
In the context of an ATBI, these should spell out the rights and responsibilities
of funding agencies, incountry institutions, and international collaborators. The
experience of the Instituto Nacional de Biodiversad (INBio) in Costa Rica can
provide useful models for some of the necessary arrangements (Reid et al.,
1993:53-67).
New modes of international scientific interaction may help manage the costs
and increase the feasibility of such studies. The Internet is being used increas-
ingly for international collaborative work on scientific projects. Video-
conferencing by small groups of international collaborators may be useful in
bringing taxonomic expertise in close proximity to ATBI sites. Video-
conferencing and the Internet also may be able to facilitate transnational train-
ing in microbial systematics.

CONCLUSION
There are clearly many technical, financial, and administrative problems to
be solved on the way to implementing an ATBI. Nevertheless, the allure of
participating in a large, international, collaborative project to describe in detail
a small part of the Earth’s species-scape remains. Living microbial culture col-
lections can play multiple constructive roles in such projects as suppliers of
information and standard specimens of currently known microbes, as sources of
taxonomic and educational expertise, and as eventual repositories of some of the
new microbes discovered.

REFERENCES
Bull, A. T., M. Goodfellow, and J. H. Slater. 1992. Biodiversity as a source of innovation in biotech-
nology. Ann. Rev. Microbiol. 46:219-52.
Hawksworth, D. L. 1991. The fungal dimension of biodiversity: Magnitude, significance and
conservation. Mycol. Res. 95: 641-655.
Janzen, D. H., and W. Hallwachs. 1994. All Taxa Biodiversity Inventory (ATBI) of Terrestrial Sys-
tems. A Generic Protocol for Preparing Wildland Biodiversity for Non-damaging Use. Report
of National Science Foundation Workshop, 16-18 April, 1993, in Philadelphia. National Sci-
ence Foundation, Washington, D.C. 132 pp. (Available over the Internet via Gopher to
huh.harvard.edu; see Biodiversity Information Resources for All Taxa Biological Inventory.)
Moore, L. 1993. Microbial Germplasm Data Net, Vol. 3, No. 4. (Internet address mgd-feedback@
bcc.orst.edu.)
Palleroni, N. J. 1994. Some reflections on bacterial diversity. Amer. Soc. Microbiol. News 60:537-
540.

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474 / BIODIVERSITY II

Reid, W. V., S. A. Laird, C. A. Meyer, R. Gamez, A. Sittenfeld, D. H. Janzen, M. A. Gollin, and C.

Juma. 1993. Biodiversity Prospecting. World Resources Institute, Washington, D.C. 341 pp.
Staley, J. T., and N. R. Krieg. 1984. Classification of prokaryotic microorganisms: An overview. Pp.
1-4 in N. R. Krieg and J. G. Holt, eds., Bergey’s Manual of Systematic Bacteriology, Vol. 1.
Williams and Wilkins, Baltimore, Md.
Sugawara, H., J. Ma, S. Miyazaki, J. Shimura, and Y. Takashima. 1993. World Directory of
Collections of Cultures of Microorganisms, fourth ed. World Federation of Culture Col-
lections Data Center on Microorganisms, Saitama, Japan. 1185 pp. (Internet address
http://www.wdcm.riken.go.jp.)
Tiedje, J. M. 1995. Approaches to the comprehensive evaluation of prokaryote diversity of a
habitat. Pp. 73-87 in D. Allsopp, D. L. Hawksworth, and R. L. Colwell, eds., Microbial Diver-
sity and Ecosystem Function. CAB International, Wallingford, England.
Torsvik, V., J. Goksoyr, and F. L. Daae. 1990. High diversity in DNA of soil bacteria. Appl. Envir.
Microbiol. 56:782-787.
Wilson, E. O. 1992. The Diversity of Life. Belknap Press, Cambridge, Mass. 424 pp.

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CHAPTER
31

Integration of Data for Biodiversity

DAVID F. FARR
Research Mycologist

AMY S. ROSSMAN
Research Leader, Systematic Botany and Mycology Laboratory,
Plant Sciences Institute, Agricultural Research Service, U.S. Department
of Agriculture, Beltsville, Maryland

“Science is built up with facts, as a house is with stones. But a collection of

facts is no more a science than a heap of stones is a house” (taken from Jules
Henri Poincaré, La Science et L’Hypothése [1908], in Beck, 1980:673).

Vast amounts of information about biological diversity exist in forms rang-

ing from systematic monographs and regional checklists to the data associated
with the millions of specimens held in the nations’ collections. This wealth of
information should be organized and integrated into a readily accessible, com-
prehensive knowledge base. Such a knowledge base is needed for global land-
use planning to ensure the long-term economic and environmental benefits of
these vital biological resources.
Although some data about biological diversity are available electronically,
most are scattered in the literature, associated with specimens in museum collec-
tions, and contained in other resources of the biological disciplines. In addition,
existing data often must be edited laboriously before they can be integrated
with other data in electronic form. Yet integration of data about biological di-
versity is the key to preservation of these biological resources. Capturing this
information electronically and integrating it into an accessible knowledge-base
is a significant step toward cataloging, developing, and preserving the world’s
biodiversity.
In order to integrate databases of biological information, two types of ac-
tivities must be undertaken: (1) the actual process of obtaining and integrating
data in electronic form, and (2) reviewing and reconciling differences in consis-
tency of data. The first activity is computer-oriented and is thus generally easier

475

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476 / BIODIVERSITY II

to complete than the second. Although the second activity should be the pur-
view of the publishing scientist, in reality, those who attempt to integrate data
must wrestle with and resolve problems of inconsistencies.
Two projects are discussed as examples in which biological data have been
successfully integrated to provide a source of information that is useful in man-
aging biological diversity. This is not to imply that these projects are the only
examples of such activity or that they are necessarily the most sophisticated.
However, the projects discussed below have integrated large data sets success-
fully and can be used as a frame of reference for developing additional ap-
proaches to the integration of data for biodiversity initiatives.

FUNGI ON PLANTS AND PLANT PRODUCTS: A SPECIALIZED

PROJECT MANAGED BY A SINGLE INSTITUTION
This project illustrates the activities and procedures required to provide a
diverse community of users with a well-researched, authoritative, and compre-
hensive body of specialized biological information. The goal of the project was
to develop a database of current information on the occurrence and distribution
of fungi associated with vascular plants in the United States. The immediate
objective of the project, and major result to date, has been a book entitled Fungi
on Plants and Plant Products in the United States (Farr et al., 1989). Because this
product was intended to meet the needs of plant regulatory officials and exten-
sion agents as well as scientists from a variety of disciplines, considerable effort
was devoted to reviewing and consolidating data and presenting it in a format
that was easy to retrieve. The book includes two major sections (Figures 31-1
and 31-2). The first lists species of vascular plant hosts that are arranged by
family of plants and the fungi that are associated with each species of vascular
plant. The distribution of each fungal species is listed state by state, based
primarily on reports from the literature (Figure 31-1). The second section pre-
sents the accepted scientific name of the 13,000 fungal species with their basio-
nym, important synonyms, the names of alternate life forms, comments on
world-wide geographic and host distribution, citations to relevant systematic
literature, and the genera of vascular plants upon which that fungus is reported
in the United States (Figure 31-2).
The amount of effort required to complete a project such as this depends on
the group of organisms involved. In the case of fungi associated with plants, it
was a major effort because standard references, such as lists of authoritative
scientific names, did not exist, and the number of both fungal and vascular
plant host names was high—much higher than expected at the outset of the
project. As a result of this project, authoritative information on over 24,000
scientific names of fungi is now available. Four major steps were involved: (1)
compiling the information; (2) entering information into the computer or obtain-
ing data in some electronic form; (3) analyzing the new data for accuracy and

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INTEGRATION OF DATA / 477

Aquifoliaceae host family

Ilex host genus

generic synonym
(= Byronia Endl.)

authority
host species

1. I. x aquipernyi J.B. Cable ex W. Clarke. I aquifolium x. I. pernyi.

2. I. cassine L. [cassina, dahoon, dahoon holly] hybrid
parents
3. I. coriacea (Pursh) Chapm. (= Prinos coriacea Pursh)
[baygall-bush, large gallberry, sweet gallberry]
synonym
4. I. cornuta Lindl. & Paxt. [Chinese holly, horned holly]

Oomycetes fungus class host

common name

Phytophthora cinnamomi. Root rot. 2 :NC(1302)

reference citation
Ascomycotina
fungus species

Discochora philoprina. Leaf spot. 3 :NC(1302. 4 :FL(35,83).

[Titaeospora equiseti.] Leaf tip necrosis. 4 : FL(35)
state

questionable record comment host number

FIGURE 31-1 Components of a record in the host-fungus list (Farr et al., 1989).

consistency, particularly of the scientific names and reports of the host-fungus

association; and (4) producing the desired output, in this case, as both hard-
copy and on-line information.

Compilation
By far the most important source of data in this project was the literature,
although other sources were included. Ease of access to sources of information
is important and confines such projects to organizations that have comprehen-
sive literature or herbarium resources. A project such as this one must be thor-
oughly documented and based on primary literature, rather than extracting in-
formation from other databases (e.g., from a library reference database). Such
databases rarely are cataloged in sufficient detail to satisfy the needs of a nar-
rowly defined project. In addition, the information derived from the primary

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478 / BIODIVERSITY II

genus authority

Claviceps Tul. Pyrenomycetes,

Clavicipitales higher taxonomic classsification

Notes: Brady (Lloydia 25:1. 19062); Langdon (Univ. Queensland

Dept. Bot. Pap. 3:651. 1954).
notes relating to whole genus

Clasviceps purpurea (Fr.:Fr.) Tul. accepted name

synonym
Claviceps microcephala (Wallr.) Tul.
Sphacelia segetum Lev. (anamorph) alternate state

Distr: Worldwide on grasses. generalized host, distribution statement

Notes: Ergot. Occurs on about 200 species of grasses

in about 50 genera. comments about species

Hosts: Agrohordeum, Agropyron, Agrostis, Alopecurus,

Ammophila, Andropogon, [Arctagrostis], Arctophila....

hosts in literature surveyed questionable record

FIGURE 31-2 Components of a record in the fungus list (Farr et al., 1989).

resource may be incomplete or erroneous. For this project, several relevant

journals were examined page by page by a knowledgeable individual. A second
consideration is that primary resources must be readily available to the project
coordinators because rarely is a piece of literature passed through the system
once and then not needed again. Questions arise that require returning to the
original piece of literature. For example, in reviewing the accumulated informa-
tion on a particular host-fungus distribution, one record may appear anomalous,
as in the questionable record shown in Figure 31-1. Reexamination of the origi-
nal literature is required to resolve this suspected erroneous information. Lack
of documentation of the primary source of a report, such as in the Index of Plant
Diseases in the United States (Anonymous, 1960), the predecessor to Farr et al.
(1989), creates confusion and devalues the information because questionable
reports cannot be verified through either the literature or a specimen.
Herbarium specimens provided an additional source of data for this project.
The primary obstacle to incorporating a large quantity of specimen information,
assuming that the specimen has been correctly identified, concerns problems

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INTEGRATION OF DATA / 479

that arise in computerizing data from specimens, namely inconsistencies in and

legibility of labels. Handwritten labels often represent a challenge to personnel
who enter the data. The specimens themselves also may require special han-
dling that can introduce labor-intensive steps in the process of entering data. If
specimen labels are photocopied, they then can be handled similarly to a piece
of literature.
Regardless of the source of information, a rarely discussed but time-con-
suming activity is locating and marking specialized data in the primary litera-
ture. This step is required to make the information comprehensible to those
who enter the data. In the case of this project, the name of the fungus and the
corresponding name of the vascular plant host were marked lightly in pencil to
be read by the personnel entering the data. Although editing can be coordi-
nated with entry of the data, editing data from primary resources as an initial
separate step affords greater efficiency by matching skills to job requirements.
For example, the knowledgeable individual who scans the journals for data
readily can indicate whether a scientific name is that of the fungus or the vascu-
lar plant host. Such information greatly assists those who enter the data but
lack a background in biology. In addition, accurate preliminary editing reduces
errors during the entry of data and saves time in the later editing phases of the
project.

Data Input
Electronic validation by the computer of the information entered is a com-
mon feature in most data-entry programs and greatly increases the accuracy and
consistency of entering the data. Simple types of validation include checking
that the entered data is in the correct format. More powerful validation includes
comparing entered data against data that is in a separate authority file (data
dictionaries). A common use of this technique is to check a country name against
a previously established computer file of accepted country names. This type of
validation not only assures accurate entry of data but also assumes an editing
role in that it requries consistency of abbreviations and format. Since only
certain place names are used, the information is edited to meet these require-
ments. Although this type of validation requires that the entered data matches
that in the authority file, such editing does not necessarily ensure that the en-
tered data reflects that in the primary source. Often some interpretation and
editing of the primary data are necessary.
Verifying the accuracy of entered data is a laborious process. Although it is
tempting to bypass this step, proofreading against the original source is neces-
sary during the initial stages of a project both to uncover errors and to deter-
mine if information was skipped during the entry of data. Specialized editing
printouts such as alphabetical listings of certain fields can be an important and
helpful component of the proofreading process. For this project, printouts were

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480 / BIODIVERSITY II

proofread on a daily basis during the data-entry stage. At the conclusion of the
project, the database included 120,000 reports of fungi derived from over 4,000
sources of literature.

Analysis of Raw Data

The analysis and consolidation of data obtained from various sources are
important steps in producing a database that is of value to a range of potential
users. Users of the database on hosts and fungi generally lack the background,
expertise, or the time needed to properly analyze the original unedited informa-
tion. This is particularly true for outdated scientific names that are now syn-
onyms. Without thorough analysis and consolidation, the raw data are likely to
be underutilized or possibly used in an unreliable manner. In the case of fungi
associated with plants in the United States, and probably for many projects that
integrate data on biological diversity, the inconsistencies due to differing taxo-
nomic concepts and changing nomenclature must be reconciled.
Conversion of the primary data to reflect, for example, accurate scientific
names of taxa, can be handled by the computer in at least two ways. The sim-
plest involves altering the data in the original records to reflect the current
concepts, i.e., using flat files. Although straightforward logistically, this ap-
proach has severe disadvantages. One significant drawback is that the original
entry no longer can be verified against the primary source. On several impor-
tant occasions, it has been necessary to refer back to the original entry and
primary resource, e.g., when the validity of a report has been questioned. Sec-
ond, errors cannot be traced that are introduced during the original process of
extracting data from the primary sources and during entry of data. Because
considerable labor is involved in these initial steps, there is significant opportu-
nity for the introduction of errors, which cannot be traced if the original record
has been changed.
The second approach, the one that we followed—building relational data-
bases—, is more complicated but produces a reliable, flexible result. In order to
convert the “raw” data extracted from the primary sources, authority files were
built that were used to compare entered data with the “correct” data and con-
vert the data into an acceptable form. In this case, a file of accepted scientific
names of fungi and a file of accepted scientific names of vascular plant hosts
were used to relate the data entered from the primary resource to the final data-
output, i.e., fungi on vascular plant hosts (Fig. 31-2). This method requires
increased software support, but has the significant advantage of leaving the
original record intact, thus providing an important resource for future refer-
ence. Questions arising about the original information are easier to answer, and
the original records do not have to be changed, thereby avoiding the continuous
introduction of errors.
The process of reviewing the scientific names to produce an authoritative

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INTEGRATION OF DATA / 481

database must be accurate and represent a consensus from the information avail-
able in the literature (see Thompson, Chapter 13, this volume). Professionally
trained systematists have the required expertise to complete such work, but it is
rarely feasible to add this work to the activities of those already conducting
active research programs. Despite a need for authoritative information about
biological resources, little professional recognition is attached to the consolida-
tion and dissemination of these most fundamental data. The issue was resolved
by employing knowledgeable individuals trained in systematic mycology, usu-
ally with a Ph.D., with some background in plant pathology. Other resources
were essential in reviewing the fungal names, particularly the continuously
updated databases of taxonomic literature.
When this project was initiated, authoritative lists of scientific names of
fungi were simply not available, and, even for vascular plants in the United
States, an agreed-upon computerized list of scientific names was lacking. There-
fore, for the fungi, each name from the literature was reviewed to determine if it
was an accepted taxon, was a synonym, or belonged in some other category.
Thus, a database of fungal names was built that contained the following core
information:
Accepted scientific name
basionym
synonyms
alternate state names (e.g., anamorph, teleomorph).
For the vascular plant hosts, scientific names derived from the literature
were compared electronically with several authoritative lists. If the name from
the literature agreed with those on the lists, that name was accepted. Discrepan-
cies between the names of the vascular plants in the data-source (i.e., the report
of a fungus on a host) and the authoritative lists (used to verify the names of the
vascular plants) were resolved by consulting additional literature. The litera-
ture used to verify the scientific name of the vascular plant was recorded in the
database.
Two databases of scientific names were constructed, one for the names of
the fungi and one for names of the vascular plants. Every name extracted from
the literature was included in one of these databases. Many anomalies were
encountered that were difficult to resolve, including errors in the primary lit-
erature. In all cases, an electronic record was maintained of which authority
was followed and how anomalies were resolved.

Producing the Output

In order to produce an output, either electronically or as hard-copy, it was
necessary to integrate the original data derived from the literature, including
geographic information, with the reviewed scientific names of both the fungi

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482 / BIODIVERSITY II

and the vascular plants. An application was developed that converted records
from the literature to output based on the currently accepted scientific name. In
other words, a new checklist was synthesized that reflected the most recent
taxonomy and nomenclature of the fungi and their hosts (Figure 31-3). Follow-
ing the review of the taxonomic literature and the development of an authorita-
tive database of scientific names for fungi, specialized lists were printed and
sent for review to systematic experts. Such reviews by experts throughout the
world served to include the scientific community in this project and were not
considered a burdensome task. The taxonomic literature on vascular plants is
more comprehensive, thus the reviewing and updating of vascular plants was
based solely on the literature. In the printed version, accurate scientific names
of fungi and their synonyms are listed with a summary of their hosts. For both
the hard-copy and on-line output, synonymous scientific names on which the
report may be based are converted to the accurate scientific name. For example,

Literature

Host-fungus
associations

Fungus Host
data data

Verticillium dahilae
Gossyplum hirsutum AR(3001), CA(3001), MS(2437)
Persea americana CA(3893, 3929)
Pistacia vera CA(2428,3929)

FIGURE 31-3 Data source and relational databases used to generate output.

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INTEGRATION OF DATA / 483

if data were requested about the occurrence of Verticillium ovatum, the follow-
ing would be displayed:

Hosts and distribution for the fungus Verticillium ovatum, a synonym of

Verticillium dahliae.
Verticillium dahliae
Gossypium hirsutum AR(3001), CA(3001), MO(3001), MS(2437),
NE(3090), TX(3001)
Persea americana CA(3893,3929)
Pistacia vera CA(2428,3929)
Prunus armeniaca CA(3929)
Prunus cerasus CA(3929)
Prunus dulcis CA(3929)
Prunus salicina CA(3929)
Rubus idaeus CA(3929)
Solanum melongena var. esculentum MA(94), NY(94), WA(94)

Because V. ovatum is now considered to be a synonym of V. dahliae, the infor-

mation for both of these names is included as one entry under the currently
accepted name, V. dahliae. The entry for Massachusetts (MA) under S. melongena
var. esculentum is actually a report of the fungus in the literature in which the
name V. ovatum is used, a name that now is considered a synonym of V. dahliae.
Although this was a project strongly driven by computers, the primary
objective was the publication of a hard-copy book. Without a book as a prod-
uct, the project probably would not have been funded. Although this project
technically was completed with the publication of Farr et al. (1989), several ad-
ditional products and services have resulted from the project. A second hard-
copy and on-line product derived from this project was a book, Scientific and
Common Names of 7,000 Vascular Plants in the United States (Brako et al., 1995),
with emphasis on those plants that are reported to be hosts for fungi. Over
Internet, outside users have on-line access to data in Fungi on Plants and Plant
Products in the United States (Farr et al., 1989), in addition to the other electronic
resources developed at the Systematic Botany and Mycology Laboratory (Anony-
mous, 1994). Ad hoc queries (Clay, 1994), construction of look-up files for other
projects, and use of subsets of data in other database projects (Alfieri et al., 1994;
French, 1989) are some of the additional products that have resulted from the
database. Fortunately, the files were constructed with the flexibility required
to accommodate such unanticipated uses. Once data exist in electronic form,
there is nothing more frustrating than not being able to use them fully. This
inability can come from restrictions on software, lack of appropriate restrictions
of software, or restrictions of institutional systems (e.g., inability to provide
access to data to those outside the institution). In general, computer databases

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484 / BIODIVERSITY II

do not exist for a single purpose. They are meant to be manipulated in new
ways, divided, updated, and modified with new and additional information.
They become part of the universe of computer databases, waiting to be inte-
grated with other data to provide information to solve unanticipated problems.

ENVIRONMENTAL RESOURCES INFORMATION NETWORK: A

COMPREHENSIVE PROJECT INVOLVING MULTIPLE INSTITUTIONS
The Australian Biological Resources project, called the Environmental Re-
sources Information Network (ERIN), is an example of integration of data at a
national level. The mission of this project is to provide geographically-related
environmental information of the extent, quality, and availability that is re-
quired for planning and making decisions (Slater, 1993). As governmental bodies
in Australia were making decisions about issues that affected the environment,
they recognized that they lacked adequate information on the environmental
attributes and characteristics of the areas under discussion. To address this
problem, ERIN was developed to produce various kinds of computer maps that
integrate biological and geographical data.
To develop a comprehensive database that would meet the goals of this
project, rapid access to accurate information was needed about the distribution
of targeted groups of organisms. These biological data then could be combined
with geological and cultural features to present a graphical overview of a par-
ticular area of land. The organizational approach used for this project was to
build a computer network that linked the sources of information (e.g., databases
of the localities from which herbarium specimens were collected) to a central
node that coordinates information (Figure 31-4). One node on the network is the
ERIN database, which contains data (“point data”) that are derived from speci-
mens, information on taxa, and information on the sets of data that are available
on the network. At this centralized unit, various kinds of data were integrated
and made available to those requesting information, such as government offi-
cials making decisions about land-use.

Compilation
How were the point data obtained? In the case of the localities for vascular
plants, information was based on the collections in various Australian herbaria.
ERIN initiated a contract with each herbarium to supply the required locality
data. Each contract was specific and included details about the fields and format
of the data that were needed. Other kinds of data included in the ERIN system
were data on specimens for mammals, amphibians, insects, and fungi, as well as
geologic, climatologic, and cultural data that were derived from both govern-
mental and nongovernmental sources.

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INTEGRATION OF DATA / 485

Managed
areas Specimen

Data dictionary
& Catalogue

Management
information
Site Taxon
survey information

FIGURE 31-4 Interactions in ERIN database between data sources, validation points,
and user-interface (Slater and Noble, 1991).

Data Input and Analysis of Raw Data

How were these data integrated? After passing through two validation
points, the data were integrated continuously at the central node of the ERIN
computer. The first validation point was a check on the scientific name of an
organism. Reports with unacceptable scientific names were rejected for resolu-
tion at the source database. After the scientific name had been accepted by the
central node, information about the locality that was associated with the record
was validated by comparison with other data. Anomalous data were readily
apparent when integrated with other data (i.e., the report of a plant specimen
that occurred outside its range or on an unusual type of soil). When both crite-
ria were satisfied, the data were loaded into the Geographic Information Sys-
tem—the common reference through which decision-makers can extract point
data for analysis. The ERIN computer maintains, for example, lists of acceptable
scientific names of vascular plants with associated information on localities that
can be integrated with other kinds of data.

Producing the Output

Core data are provided to a centralized database via a network so that infor-
mation is immediately available to a potential user. The detailed data from which
the core data are extracted are not stored centrally, but rather exist in separate
nodes where they are under the control of the custodian. This ensures that the

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data will be updated at the point of origin and thus maintained by those best
able to do so. All data, regardless of source, are available through an interface
that is easy to use, incorporating a comprehensive directory. Analytical and
modeling tools are available through the same user-interface as the data. Prior-
ity is given to the acquisition of primary point data, rather than aggregated or
interpreted information. This ensures that conclusions based on those data can
be reviewed rigorously, alternative analyses can be performed, and baselines for
monitoring can be established. Using these centralized data, computerized maps
can be produced in response to queries and specialized requests.
The ERIN project is a functioning database system that addresses issues that
arise when discussing the integration of biological information. This informa-
tion resource is the result of a national effort to provide environmental informa-
tion related to geography using a centralized database. As a result, planning,
research, development, and management is based on environmental information
provided through a well-coordinated interdisciplinary and multi-institutional
collaboration. Data are readily accessible, both at reasonable cost and without
encumbrances that otherwise might impede responsible environmental decision-
making.

COMPARISONS OF THE TWO PROJECTS

The project on associations between fungi and plants in the United States
and ERIN in Australia share two important features. Both use a taxon-based list
of accepted scientific names to allow the integration of data from diverse sources.
The importance of a list of accurate scientific names of taxa cannot be overesti-
mated. These lists are the linchpin on which all attempts to integrate biological
information are dependent. Integration of biological information will be pos-
sible only with the availability of such lists. In addition, these two projects
demonstrate the need for validation of data if information from diverse sources
(either from the literature or from collections of specimens) is to be integrated
meaningfully.
The important differences between the projects are the means by which
data are handled and the number of institutions which are involved. For the
database on fungi, all of the data were generated, edited, and manipulated within
one computer at a single institution. The ERIN project has developed a system
that uses distributed sets of data at several institutions. Most of the resources
for the project on fungi were devoted to verifying and updating the informa-
tion. For ERIN, the responsibility for verifying and updating the information
was contracted out to multiple institutions. Project resources were directed to
developing the network with a central node and a user-interface that could pro-
vide the data. Quality-control was ensured by validating incoming data as well
as contracting with institutions that had strong systematic expertise to serve as
the custodian for the entry and review of specimen-based data. The ERIN data-

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INTEGRATION OF DATA / 487

base demonstrates that multiple institutions can be involved in the development

and maintenance of integrated sets of data.

AVAILABILITY OF INFORMATION ON BIODIVERSITY

Information on biodiversity is available from a number of sources, includ-
ing those used in the examples cited above—reports from the literature and data
from herbarium or museum specimens. The most important and authoritative
sources are comprehensive taxonomic monographs. Such monographs reflect
the state of knowledge about particular groups of organisms based on years of
accumulated experience, detailed scrutiny of specimens from throughout the
world, and the synthesis and analysis of many kinds of data. Unfortunately, the
data accumulated in monographs often are not stored in well-developed data-
bases. Integration of the wealth of data in systematic monographs with other
sources of information requires orientation toward the databases during the col-
lection and collation of the information. Currently, the software program DELTA
(DEscriptive Language for TAxonomy) provides this capability (Askevold and
O’Brien, 1994; Dallwitz et al., 1993; Fortuner, 1993). All of the character states
for an organism are treated as distinct entries in the database. The recent mono-
graph of Cucumis, a genus of vascular plants that includes melons, squashes,
and gherkins, was produced using DELTA (Kirkbride, 1993). Although pub-
lished as a book, it includes a disk with data in DELTA format. Ad hoc queries
based on any of the types of data used in the monograph are possible. In addi-
tion to providing a user-friendly synoptic means of identification, the data can
be used for secondary analyses, e.g., PAUP programs. Subsets of data for spe-
cialized purposes are created easily. For example, one can select only those
species found in a certain geographic area and produce a key to those species for
a local user-community. Integration of data sets that have used the DELTA
format is easily accomplished, and thus the treatment of two related genera could
be combined into a single data set. Most importantly, the DELTA format allows
for the manipulation, extraction, and display of data to meet the needs of a large
and diverse user-community, and these data can be made available. Users of
biological information in DELTA format range from plant-explorers and plant-
breeders to phylogeneticists and molecular biologists.
Large-scale integration of data about biological diversity requires that much
of the primary information be in an electronic form. How can this electronic
information be located and accessed? Currently, Internet provides the best
means of accessing such information. Internet is a series of connections between
computers that allows for the transfer of data. Having been built from the
ground up, there is no overall structure to the Internet. For example, when a
computer that is part of our Laboratory system at Beltsville communicates via
Internet with a computer at Harvard University, it connects with 19 other com-
puters along the way. The recent surge in users attached to Internet means that

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488 / BIODIVERSITY II

millions of individuals now have access to computerized information through-

out the world. Through Internet, electronic systematic data can be made avail-
able to everyone.
Internet facilitates finding and disseminating data in several ways (Krol,
1992). One is the use of Gopher software to locate subject-specific files through-
out the world. For example, this program can be used to gain access to informa-
tion about biodiversity located on the Biodiversity and Biological Collections
Gopher at Cornell University, the Harvard University Gray Index of vascular
plants described from North America, or the Register of Type Specimens in the
Botany Department available through the Smithsonian Gopher. Another means
of accessing data is through Telnet, the Internet remote login application. Using
Telnet, the user actually logs onto another computer and then can work with the
databases on that computer. Our Systematic Botany and Mycology Laboratory
computer in Beltsville, Maryland, has such a capability, which allows our major
databases on fungi to be accessed by the outside world (Anonymous, 1994). File
Transfer Protocol (FTP) is a procedure available over Internet that allows the
rapid transfer of computer files. FTP can be used to attach to another computer,
select the file of interest, and copy it in a matter of seconds. A final method of
communication through Internet is the use of mail groups. These communica-
tion tools permit groups of individuals in specific disciplines to ask questions
and discuss current subjects of interest to that group. Most recently, the use of
Mosaic and the World Wide Web server has made locating relevant data that are
available through Internet increasingly easy. Clearly, the suite of tools available
over Internet has greatly improved progress toward the integration of data.

FUTURE CHALLENGES
Abundant data about biological diversity exist in various forms; the infor-
mation and technology needed to integrate these data are also readily available.
In fact, no significant hardware or software problems constrain the develop-
ment of systems for integrating data. The projects discussed in this chapter
provide examples of procedures that can be used to develop the data integration
of data on a large scale. Two developing large-scale projects that integrate taxo-
nomic and distributional information are the International Organization of Plant
Information (IOPI) project (Bisby et al., 1993) for vascular plants, and the Bio-
systematic Information on Terrestrial Arthropods (BIOTA) project for insects
(Hodges, 1993). Such projects always require a strong motivating force backed
by fiscal and intellectual resources.
Several factors have impeded progress in large projects on biodiversity.
One is a lack of clear goals and objectives. What are the goals of research on
biodiversity? The ultimate goal is global planning of land-use that would yield
long-term economic and environmental benefits. Intermediate goals must be
defined with objectives that can be achieved using available or obtainable fi-

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INTEGRATION OF DATA / 489

nancial and personnel resources. Two of the most urgent attainable objectives
for biodiversity initiatives are: (1) the development of authoritative databases
of scientific names of organisms that are available over Internet (efforts are
underway to provide and continuously update such data as part of the U.S.
Department of the Interior’s National Biological Survey1; National Research
Council, 1993), and (2) electronic access to baseline data of the presence/ab-
sence of species, particularly of speciose groups such as insects and fungi that
are sensitive to environmental pollution and habitat alteration. Baseline data
exist in collections of specimens as well as in the literature, but they must be
made available and reviewed prior to integration with climatological and other
abiotic data.
A second factor hindering the integration of information for biological di-
versity is a lack of stable resources. Long-term commitments from funding
agencies and research organizations are needed to foster long-term mega-
projects. The Australian government recognizes the economic value of making
judicious decisions on land-use based on data from ERIN, and thus has made a
long-term financial commitment to this project. Long-term financial commit-
ments from national and international science and environmental funding agen-
cies would strongly motivate projects to integrate information about biological
diversity.

CONCLUSION
The multidisciplinary integration of biological and nonbiological data re-
quires a coordinating organization to spearhead initiatives in biological diver-
sity from talk to action. The Australian plan, with its centralized decision-mak-
ing, is an extremely successful example of a centrally coordinated program that
should be emulated around the world. An organization is needed that will set
goals, promulgate standards, consolidate information about available databases,
develop procedures for integrating data, and make available a comprehensive
database of information relevant to biological diversity. Such an organization
for the United States has been proposed in the U.S. Department of Interior’s
National Biological Service1 (National Research Council, 1993). At the interna-
tional level, the United Nations Environmental Programme could provide the
leadership to bring into reality the information resources that are needed to
wisely direct international biological diversity initiatives. Within the next 10-
20 years, it is essential that data on the world’s biological resources be inte-
grated in order to fully explore, sustainably utilize, and preserve these vital
resources.

1The National Biological Survey subsequently was renamed to the National Biological Service by

Secretary Babbitt.

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490 / BIODIVERSITY II

REFERENCES
Alfieri, S. A., Jr., K. R. Langdon, J. W. Kimbrough, N. E. El-Gholl, and C. Wehlburg. 1994. Diseases
and disorders of plants in Florida. Florida Dept. Agri. Conserv. Serv., Bull. No. 14:1-1114.
Anonymous. 1960. Index of plant diseases in the United States. Agri. Handbook 165:1-531.
Anonymous. 1994. On-line information available about U.S. National Fungus Collections.
Phytopathol. News 28:159-160, 163.
Askevold, I. S., and C. W. O’Brien. 1994. DELTA, an invaluable computer program for generation
of taxonomic monographs. Ann. Entomol. Soc. Amer. 87:1-16.
Beck, E. M., ed. 1980. Familiar Quotations. A Collection of Passages, Phrases and Proverbs Traced
to Their Sources in Ancient and Modern Literature, by John Bartlett, fifteenth ed. Little,
Brown and Company, Boston. 1540 pp.
Bisby, F. A., G. F. Russell, and R. J. Pankhurst, eds. 1993. Designs for a Global Plant Species
Information System. Clarendon Press, Oxford, England. 346 pp.
Brako, L., A. Y. Rossman, and D. F. Farr. 1995. Scientific and Common Names of 7,000 Vascular
Plants in the United States. American Phytopathological Society, St. Paul, Minn. 304 pp.
Clay, K. 1994. Patterns of biodiversity in plant pathogens (abstract). P. 39 in Fifth International
Mycological Congress, Vancouver, British Columbia, Canada.
Dallwitz, M. J., T. A. Paine, and E. J. Zurcher. 1993. User’s Guide to the DELTA System: A General
System for Processing Taxonomic Descriptions, fourth ed. CSIRO Division of Entomology,
Canberra, Australia. 142 pp.
Farr, D. F., G. F. Bills, G. P. Chamuris, and A. Y. Rossman. 1989. Fungi on Plants and Plant Products
in the United States. American Phytopathological Society, St. Paul, Minn. 1259 pp.
Fortuner, R. 1993. Advances in Computer Methods for Systematic Biology: Artificial Intelligence,
Databases, Computer Vision. Johns Hopkins University, Baltimore, Md. 560 pp.
French, A. M. 1989. California Plant Disease Host Index. California Department of Food and Agri-
culture, Sacramento. Pp. 1-394.
Hodges, R. W. 1993. Biosystematic Information on Terrestrial Arthropods. Assoc. Syst. Coll.
Newsletter 21:72.
Kirkbride, J. H., Jr. 1993. Biosystematic Monograph of the Genus Cucumis (Cucurbitaceae). Park-
way, Boone, N.C. 159 pp.
Krol, E. 1992. The Whole Internet. User’s Guide and Catalog. O’Reilly and Associates, Sebastopol,
Calif. 376 pp.
National Research Council. 1993. A Biological Survey for the Nation. National Academy Press,
Washington, D.C. 205 pp.
Slater, W. 1993. Introductory remarks. International Workshop, Designing Spatial Information
Systems to Manage Biodiversity Information, March 1-5, Canberra, Australia. 5 pp.
Slater, W. R., and S. J. Noble, eds. 1991. ERIN Program Brief, June, 1991. Commonwealth of
Australia, Canberra.

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CHAPTER
32

Information Management for

Biodiversity: A Proposed U.S. National
Biodiversity Information Center
BRUCE L. UMMINGER
Senior Advisor on Biodiversity

STEVE YOUNG
Advisor on Biodiversity Information, Office of the Assistant Secretary for Envi-
ronmental and External Affairs, Smithsonian Institution, Washington, D.C.

To explore the essential role that information management must play in

biodiversity conservation, consider the arenas of finance, weather, and sports.
For many, one’s quality of life is affected by one’s financial posture—more and
diversified assets are preferable, and it is desirable that income exceed spend-
ing. Try to imagine a world in which one lacks reliable information about one’s
assets, income, and expenditures. Imagine no payroll statements, no bank state-
ments, no records of checks written and charges made, and so on. Life would be
a perilous joust with bankruptcy.
Fortunately, most of us do not face this problem. We receive ample infor-
mation about assets, income, and liabilities. One merely has to put the informa-
tion to use; guesswork should not be necessary. In most cases, we get the infor-
mation we need to empower us to manage our personal finances, whether or not
we proceed to manage them well.
Consider weather information. Mark Twain pointed out that everyone talks
about the weather, but no one does anything about it. Strictly speaking, that is
not true. When one hears that rain is in the forecast, one may pick up an um-
brella or raincoat. If the weather is predicted to be cold and windy, one wears
a warm coat. One responds to current and forecasted weather conditions. One
cannot change the weather, but one does something about it by reacting, by
adapting.
The United States and other nations have worked together to build a mar-
velous weather information infrastructure. Consider how pervasive weather
information is. One hears about the weather on the radio, sees it in the newspa-
per, and now television provides spectacular satellite images and movies, Dop-

491

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492 / BIODIVERSITY II

pler radar displays, animated graphics, and lively human commentary to ex-
plain current conditions and forecasts. Weather is part of every local news
show, and in the United States we have the Weather Channel on cable. We have
spent billions of dollars on capabilities to gather weather data and generate and
disseminate forecasts. Weather satellites and information networks provide glo-
bal coverage. By most reckoning, thousands of lives have been saved by im-
proved forecasting and warning capabilities, and large economic losses have
been avoided through timely responses to better predictions.
Finally, consider sports, another area of pervasive flow of information. For
most of us, professional sporting events lack the immediate, direct impacts on
our lives that financial outcomes and weather events have. Nonetheless, mil-
lions of people are keenly interested in sports, and another elaborate informa-
tion infrastructure has been built to satisfy that interest. One can speculate
about which came first: the overwhelming interest in professional sports, or the
vast information infrastructure that stimulates and satisfies that interest. Sports
information captures large sections of the printed media and is inescapable in
broadcast media. Sports has its own publications and radio and television net-
works. And the wide availability of sports information influences behavior.
How many people would follow their favorite sports teams fanatically if they
could not get information about team standings and catch some of the games on
television and radio? One might say that sports information “programs” people
to take a greater interest in sports and protect sporting interests.
Now consider biodiversity, which affects our lives in the most fundamental
ways possible. People are extraordinarily interested in the environment and
biodiversity. Recent polls indicate that approximately 80% of Americans call
themselves “environmentalists.” That interest extends to the natural environ-
ment. More Americans visit museums and zoos every year than attend profes-
sional sporting events. Tens of millions of Americans enjoy various activities
outdoors in ecosystems: hiking, birding, fishing, hunting, camping, and so on.
When they are exposed to good information about biodiversity, young children
show great interest—comparable to the levels of interest that they later demon-
strate for sports.
Not only is interest keen in biodiversity and the environment, but, unlike
the weather, humans can do something to change the situation; and we do a
great deal. We eliminate species like the ivory-billed woodpecker and passen-
ger pigeon. We introduce species like the gypsy moth and zebra mussel. We
alter and destroy habitat. Sometimes we restore ecosystems and reintroduce
native species that had been extirpated. In short, unlike the weather, we can do
much to change the environment for the better or worse. Each of us takes ac-
tions that to various degrees help or harm.
The present administration of the United States is committed to an ecosys-
tem management approach to the environment and the economy. The concept
of ecosystem management explicitly recognizes the linkages between ecology

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PROPOSED NATIONAL BIODIVERSITY INFORMATION CENTER / 493

and economy and rejects the assumption that there is an inherent conflict be-
tween jobs and the environment. The United States also is committed to a policy
of sustainable development; conservation of biodiversity and management of
ecosystems are vital approaches toward sustainability.
There are strong parallels between financial management and conservation
of biodiversity. If we do not know what our ecological assets are, we are poorly
equipped to safeguard those assets through wise use and management. If we
“spend” too much of the natural production and capital of an ecosystem, we see
symptoms of impending bankruptcy, e.g., the collapse of fisheries, endangered
species, and loss of jobs. Managing ecosystems by deficit-spending results in
what Secretary of the U.S. Department of the Interior, Bruce Babbitt, calls “train
wrecks”, with examples like the forest and fish crisis in the Pacific Northwest.
Information is equally critical to financial and ecosystem management.
Without information, we cannot manage finances at the personal, corporate, or
governmental levels; without information, we cannot manage personal “back-
yard,” local, or regional ecosystems so as to conserve biodiversity.

THE U.S. NATIONAL INFORMATION INFRASTRUCTURE:

ROOM FOR THE ENVIRONMENT?
We have looked at the pervasiveness of financial, weather, and sports infor-
mation. Now, the United States is building its national information infrastruc-
ture (NII), a national system of information superhighways. It is a given that the
NII will offer all the financial, weather, and sports information that we could
possibly want, in fact more than we can possibly absorb. Through a National
Biodiversity Information Center (NBIC), the NII also could be a rich source of
information on biodiversity for the public.
Is information on biodiversity pervasive in our lives today? How much
information is readily available about the species and ecosystems in your area?
Have they been inventoried? Are their populations, health, and trends known?
Regrettably, in the United States, information on biodiversity receives a minus-
cule fraction of the attention that is paid to finances, weather, and sports.
Lack of information is the silent partner to the more prominent agents of
environmental destruction. If the destruction happens gradually enough and
invisibly enough without galvanizing incidents like the catastrophes of Bhopal
and the Exxon Valdez, by the time a threshold is crossed and the train wreck
occurs, it is too late. We need to make the gradual, seemingly invisible changes
visible to people. Financiers and meteorologists know this lesson. Financiers
build indicators to track changes that otherwise would be hidden, and meteo-
rologists use sensing technologies to “see” events that cannot be seen by the
eyes of observers on the ground. And in sports, instant replays help us see what
happened when we missed it during the live action.
The U.S. National Performance Review, Vice President Albert Gore’s initia-

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494 / BIODIVERSITY II

tive for “reinventing government,” suggests that the federal government should
place greater reliance on strategies of empowerment that help people do the
right thing. Recall that 80% of the public say they are environmentalists. Are
there ways to empower them to do more for the environment, to act on what
they say?
Information is the key to an effective strategy of empowerment for the en-
vironment. If we were to build a robust environmental information infrastruc-
ture, comparable in capabilities to those of finance, weather, and sports, we
could provide people with environmental information to empower them. This
kind of empowerment would work the same way that financial information
empowers us to make informed choices in our financial management, weather
forecasts empower us to prepare for the weather, and sports coverage empowers
us to feel a strong emotional involvement with sporting events.
Empowerment through environmental information requires a new way of
thinking. Our robust weather information infrastructure follows an implicit
“observe-forecast-warn-react” model, as shown in Figure 32-1. This works quite
well for the weather, since we cannot change it and can only react to it. But this
model is too limited for the environment, where the relationship is more com-
plex—the environment changes us, but we also change the environment.
We need to follow a “feedback” model that acknowledges the feedbacks

WEATHER MODEL

Observe

The Environment
Forecast &
Warn

Receive &
Asses

React

FIGURE 32-1 Model for inferring information about the weather.

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PROPOSED NATIONAL BIODIVERSITY INFORMATION CENTER / 495

between humans, information, and our environment. Figure 32-2 illustrates

such a model. It shows that the flow of information can influence human behav-
ior, thus changing our impacts on the environment—one hopes for the better.
Financiers understand that this model also applies to financial markets. Con-
sider the well-known impact that information has on the stock market. Re-
sponses to information about actual events and rumors can cause waves of buying
or selling, moving prices up and down. Analysts know that there is a highly
dynamic feedback process between information and markets. We need to apply
this same insight to information and ecosystems. We need to put information to
work as a tool that will empower us to protect, restore, and manage our ecosystems.
If we adopt this feedback model, we see that information is the fundamental
mechanism that influences human behavior toward the environment. Initia-
tives for the conservation of biodiversity can succeed only to the extent that we
put information to work as a stratagem, resource, and tool.
Unfortunately, today it is not clear that information on biodiversity will be
a prominent part of the NII. The weather model has been the dominant model in
thinking about the application of the information infrastructure to the environ-
ment. If the weather model is the controlling paradigm, then it seems that there
is not much to observe, forecast, warn of, and react to, because most environ-
mental changes take place, seemingly invisibly, on a longer time scale than

FEEDBACK MODEL

Observe

The Environment
Forecast &
Warn

Empower with
general Receive &
environmental Asses
information

Human Change
Impacts Behavior

FIGURE 32-2 A model that acknowledges feedbacks between humans, information,

and the environment.

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496 / BIODIVERSITY II

weather events, which happen on scales of minutes to a few days and pose
immediate and obvious threats to life and property.
On the other hand, if the feedback model is the controlling paradigm, it is
imperative that we create an “environmental channel” to provide people with
the information they need for empowerment and to create feedback loops that
change behavior and result in positive changes for the environment.
Key components of a vision that is both possible and necessary for an effec-
tive environmental information infrastructure have been demonstrated techni-
cally in other contexts (the financial, weather, and sports realms referenced
above). Also, the Environmental Resources Information Network (ERIN) in
Australia, the Right-to-Know Network (RTKNet) in the United States, and other
advanced practitioners already have demonstrated some of these capabilities in
the environmental arena.
Imagine the time, not very distant in the future, when virtually every home
is connected to the information highway. It is a given that one will be able to
“surf” through video entertainment and engage in interactive home shopping.
It is also a given that one will have access to a tremendous range of financial,
weather, and sports information. But, in our vision, one also will have interac-
tive access to a vast range of environmental information—in effect, an “environ-
mental channel” on the information highway. The proposed U.S. NBIC may
function as a major resource center for the channel.
An environmental channel will offer six major capabilities. First, it will
allow its users to explore past, present, and predicted future environmental con-
ditions at local, state, regional, national, and global scales, using ecosystem or
political boundaries. Second, it will provide capabilities for “what-if?” model-
ing, visualization, and simulation to explore alternative future scenarios. Third,
it will provide information about biodiversity and other natural resources in
local areas and about stresses on those resources. Fourth, it will provide infor-
mation oriented toward solutions that will empower individuals to identify what
can be done to minimize harm and improve the environment. Fifth, it will allow
individuals to “publish” observations, ideas, and questions about the environ-
ment. Sixth, one will be able to find information, other resources, and collabo-
rators for environmental efforts.
For example, an environmental channel will allow one to view detailed com-
puter maps and select an ecosystem of interest. For that ecosystem, one will be
able to review current environmental data and view animations showing changes
over time, e.g., changes in land-use and land-cover over the last 200 years. One
will be able to forecast the continuation of such changes into the future and use
simulation models to explore alternative futures. One will be able to review the
known species within the ecosystem; their status, trends, and natural histories;
and the known threats to the health of each species. One will be able to access
information about recommended management practices to conserve biodiversity
within the ecosystem. One will be able to publish data that one collects and

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PROPOSED NATIONAL BIODIVERSITY INFORMATION CENTER / 497

ideas that one generates for conservation. And finally, one will be able to find
others who are interested in the same ecosystem and develop collaborations with
them.

INTERNATIONAL MODELS

ERIN
The Australian Environmental Resources Information Network (ERIN), a unit
of the Department of Environment, Sport, and Territories, provides an excellent
model for the sophisticated application of information tools, technologies, and
stratagems to the challenges of conservation of biodiversity and ecologically
sustainable development. ERIN demonstrates attributes of the needed capabili-
ties of an environmental channel and of a biodiversity information center.
ERIN’s mission is to provide geographically-related environmental infor-
mation of the extent, quality and availability that is required for planning and
decision-making, fulfilling an “infrastructure support” role. With a relatively
small staff (approximately 24) and budget (approximately $2.5 million per year
in Australian dollars), ERIN has been able to make a disproportionately large
impact on environmental decision-making in Australia.
ERIN takes a distributed network approach, in which it identifies the custo-
dians of high-priority data, such as standard spatial data sets, and works with
those custodians to make their data available over the information network.
The agencies retain custodial responsibilities. ERIN seeks to ensure that pri-
mary data are available, so that users are free to make their own interpretations
rather than being forced to rely on derivative data such as classification schemes
for land-use or land-cover. Finally, ERIN emphasizes the need for standards to
facilitate sharing, synthesis, and understanding of data and information.
ERIN operates a World Wide Web server that is accessible internationally
over Internet through the popular Mosaic client software interface. Its uniform
resource locator (URL) is http://kaos.erin.gov.au/erin.html. The ERIN web
server demonstrates advanced information technology that brings together a
wide range of environmental information and presents it to users, along with
tools for spatial display of geographical information, modeling, and viewing.

BIN21
The Biodiversity Information Network (BIN21) initiative, managed by the
Base de Dados Tropical in Brazil, was created to provide informational support
that would further the purposes of the Convention on Biological Diversity and
Agenda 21. BIN21 is developing a distributed, international network of sources
of information to support research on biodiversity and conservation. Like ERIN,
BIN21 now operates a World Wide Web server (URL http://www.ftpt.br).

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498 / BIODIVERSITY II

BIN21 is working to create international “nodes” on the Internet and foster

international exchange of information and collaboration. A U.S. National Bio-
diversity Information Center logically might join BIN21 as a node in the United
States.

A PROPOSED U.S. NATIONAL BIODIVERSITY INFORMATION CENTER

Background
The concept of a focal point for efforts to understand and sustainably man-
age biodiversity in the United States has been discussed for over 20 years. In
1974, The Nature Conservancy pioneered the first of its State Natural Heritage
Inventories in South Carolina. Natural Heritage Data Centers now exist in al-
most every state of the United States, using methodology that has been improved
continuously since 1974 (Jenkins, 1988).
In 1986, a report of the Association of Systematics Collections (ASC), Foun-
dations for a National Biological Survey, and a background paper of the Office of
Technology Assessment (OTA), Assessing Biodiversity in the United States: Data
Considerations, brought increased attention to this area. In 1987, the OTA made
a modest recommendation for “a small clearinghouse for biological data” in its
report, Technologies to Maintain Biological Diversity.
More recent examples of the continuing interest in the management of in-
formation about biodiversity include the 1991 policy dialogue report of the Key-
stone Center, Biological Diversity on Federal Lands, the 1993 report to the Smith-
sonian Institution on the National Center for Biodiversity by the ASC (Hoagland,
1993), and the 1993 report from the Council on Environmental Quality, Incorpo-
rating Biodiversity Considerations Into Environmental Impact Analysis Under the
National Environmental Policy Act. The discussions in these reports dealt with a
broad array of activities designed to improve the management of biodiversity,
including regulation, conduct of government activities, and improvements in
the amount and availability of information.
A Proposal for a National Institute for the Environment, published by the
Committee for the National Institute for the Environment (1993), recommended
that the proposed agency include a National Library for the Environment with
modern information services and electronic technologies. Both the 1993 report
from the National Research Council, A Biological Survey for the Nation, and the
1994 Systematics Agenda 2000: Charting the Biosphere cited decentralized com-
puter networks of databases as absolutely central to the study and preservation
of biodiversity.
From 1987-1992, several Congresses (with 1 Senate and 10 House of Repre-
sentatives hearings on four versions of legislation on biodiversity) considered
bills that would have instituted various regulatory programs, required consid-
eration of biodiversity in environmental impact statements under the National

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Environmental Policy Act (NEPA), and established a center of national bio-

diversity. The Bush administration resisted these efforts, primarily due to con-
cerns over NEPA and other regulatory and quasiregulatory provisions.
In these bills, the concept of a center was quite broad. A center would be
the home of fairly ambitious efforts to (1) locate information that is available on
the nation’s biological resources; (2) assess the completeness of that base of in-
formation; (3) catalyze and, in some cases, actually fund efforts to fill gaps in
information; (4) serve as a clearinghouse, or “database of databases,” that would
facilitate improved access to information by users; and (5) generate its own prod-
ucts, such as maps, flora, and other types of publications and media.
At the Earth Summit in Rio, in June 1992, the Bush administration em-
braced the idea of a national center of biodiversity, based on a more limited
conception of its scope and role. A center was envisioned to include three gen-
eral functions: (1) developing methods to access widely scattered information
on biodiversity, (2) assessing the state of knowledge and identifying gaps, and
(3) providing leadership in understanding and communicating about bio-
diversity. Plans were developed to establish by Executive Order a center at the
Smithsonian Institution, but the order was not signed before President Clinton
took office.
In 1993, the U.S. Department of the Interior established the National Bio-
logical Survey (later renamed the National Biological Service, NBS), with infor-
mation management as an integral component. A report from the National Re-
search Council, A Biological Survey for the Nation (1993:103), recommended that
“Under the leadership of the NBS, the National Partnership for Biological Sur-
vey1 should develop a National Biotic Resource Information System...(The NBS)
should also participate in interagency initiatives to coordinate collection and
management of biodiversity data by the federal government.”

Recent Planning
With the establishment of a National Biological Survey, the Environmental
Protection Agency provided funds to the Smithsonian Institution to lead an
interagency planning study, beginning in the fall of 1993, to clarify the concept
of a National Biodiversity Information Center (NBIC). A small ad hoc working
group of staff that represented several federal agencies developed background
materials to prepare for the establishment of a center. The materials included a
“strawman” description of what might be included in a National Biodiversity
Information Center and questions to be addressed in the planning process.

1A term the National Research Council uses to refer to a broad spectrum of federal and nonfederal

agencies and organizations that are carrying out activities which, in effect, constitute the National
Biological Survey as broadly defined.

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500 / BIODIVERSITY II

The Office of Management and Budget shared the results of this working
group with the assistant secretaries of over 10 federal agencies involved in
biodiversity research at a meeting in January, 1994. After receiving advice on
policy from the assistant secretaries, the Smithsonian Institution began the next
phase of planning with representatives of federal agencies, state agencies, acad-
emia, museums, nongovernmental organizations, and industry. An Advisory
Planning Board chaired by Dr. Thomas E. Lovejoy, Smithsonian Assistant Secre-
tary for Environmental and External Affairs, guided the process with represen-
tation from the organizations mentioned above. The Board held two meetings,
March 21-22 and November 15, 1994, and published a consensus paper, The
National Biodiversity Information Center, in December, 1994.
The Board was responsible for setting the specific charge for and overseeing
the work of the Drafting Committee, which was chaired by Dr. Robert S.
Hoffmann, Assistant Secretary for Science at the Smithsonian Institution, and
included members from the full spectrum of stakeholder organizations. The
Drafting Committee produced a draft report that was taken to the meeting of the
Board on November 15 for adoption. The report provided both a conceptual
framework and a detailed account of the structure, location, and institutional
setting of the Center and its principal tasks. Relationships between the Center
and other organizations (including federal agencies) also were addressed.
Changes to the draft report, suggested at the Board meeting of November
15, were incorporated into the final consensus paper published in December,
1994. The full text of the final report, minutes of the two meetings of the Advi-
sory Planning Board, and a list of Board members can be obtained on the World
Wide Web through the Biodiversity and Ecosystems NEtwork (BENE), URL
http://straylight.tamu.edu/bene/nbic/nbic.html; via anonymous FTP from
keck.tamu.edu/pub/bene/bene_texts; or from the NBIC area on the Smithsonian
Institution’s National Museum of Natural History Web and Gopher servers. The
principal concepts coming from this report are presented below.

Mission and Objectives

The idea of the National Biodiversity Information Center is simple: it pro-
vides a focal point where the many parties that generate, manage, or use data on
biological resources can collaborate and make decisions leading to broader ac-
cess to that information. The Center will direct users to sources of the data they
seek, while working with funding agencies to encourage development of tools
and strategies to make data more accessible. The Center will not duplicate exist-
ing databases or information, but will provide directory services for the large
array of information that is available. It also will identify gaps where new data-
bases are needed, and assist the development, transfer, and application of new
technologies. Further, the Center could coordinate access to data outside the
usual realm of the biological sciences.

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PROPOSED NATIONAL BIODIVERSITY INFORMATION CENTER / 501

NBIC’s mission will be to provide leadership and a neutral venue in which

to facilitate collaborative discussions about the availability of data and informa-
tion on biodiversity. It also will be a clearinghouse to provide knowledge of,
enable access to, and facilitate the use and exchange of data and information on
biodiversity. The Center’s objectives will be to promote and encourage the use
of well-documented data and information on biodiversity, address the full scope
of biodiversity from molecular data through ecosystems, connect those seeking
information and data on biodiversity to those having custody of such data, and
facilitate structured identification of and access to data that is pertinent to a
user’s needs. This will be accomplished through an interactive computer sys-
tem that uses metadata (data about the data) on geographic location, species,
ecosystem, or other keywords to sort, aggregate, or integrate data sets, identify
gaps in existing data and knowledge, and provide a forum for collaborative
approaches to issues in biodiversity information.

Guiding Principles
The Center must be responsive to the needs of users, providing both data
and information services that are tailored for different audiences. NBIC also
must be responsive to the needs of providers, and must offer incentives and
encouragement for them to provide their data through NBIC. The Center will
facilitate the development of standards for metadata (minimum criteria for the
documentation and format of data) and the establishment and provision of pro-
tocols for collecting and reporting data. Guidance on appropriate uses of data or
information also will be provided. NBIC will facilitate the improvement in the
quality of data sets with a feedback system that allows comments on the quality
and utility of data. Custody of data will reside largely with primary collectors
and producers of data, and users will be referred to original sources of data.
Therefore, data holdings by NBIC will be reduced. NBIC will use appropriate
technologies for the integration and analysis of information and will promote
the adoption and use of appropriate standards of information.

Structure and Location

The Center will have a distributed structure that will function on a demo-
cratic, consensus-building, and partnership approach. NBIC will serve as a con-
vener, facilitator, and host. Center experts will move discussions along and
involve key constituencies. An Advisory or Governing Board from the broad
community of contributors and users will provide general direction. A Techni-
cal Advisory Committee will ensure that NBIC receives computer and technical
advice. NBIC must establish partnerships with the other organizations, such as
the NBS, whose activities include collection of data and information and assess-
ment of biodiversity issues.

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502 / BIODIVERSITY II

NBIC’s location should be decided by open competition, with a review after

3 years and recompetition every 5 years if so recommended by the review. NBIC
should be designed to be moved if needed. Individual institutions or consortia
of institutions should be invited to apply for selection as the Center host. Desir-
able characteristics of the host institution should include strong support for
computational and information management services; a creative and active pro-
gram in biological sciences, especially involving the use of computers in bio-
diversity information management; broadly based expertise and strong links to
systematics, ecological research, and information management of collections;
understanding of modern and historical North American collections; history of
service and support to users; reasonable access to national and international
transportation; and comfortable, modern facilities for conferences and the staff
of the Center.

The National Biodiversity Information Center (NBIC),

the National Biological Service (NBS), and the National Biological
Information Infrastructure (NBII)
Both the NBS and the report of the National Research Council, A Biological
Survey for the Nation, conceived of the establishment of a highly distributed
information resource that would involve participants from federal, state, pri-
vate, academic, and other institutions at scales ranging from local to national
and global. Participants in this National Biological Information Infrastructure
(NBII)2 would work to develop tools, strategies, and collaborative activities that
will bring coherence to the collection, storage, and management of data and
increase access to biological information.
The newly created NBS has as a significant component of its mission the
augmentation of access to biological information, relying upon a “distributed
federation of databases” in accordance with the recommendations of the Na-
tional Research Council. To achieve this goal, NBS plans to gather and make
available information on sources of biological information (an electronic “card
catalog” will be available in late 1994 or early 1995), encourage the development
of standards for metadata, and make investments in both its own and its part-
ners’ hardware and software capabilities to move toward a highly distributed
communications and access environment.
These activities and objectives closely complement those of the NBIC. The
Center will assume the clearinghouse function of the NBII as envisioned by the
NBS. NBS views the Center as a powerful tool for achieving key NBS objectives.
The development of the “National Partnership for Biological Survey” requires

2A term used by NBS to reflect a parallel with the existing National Spatial Data Infrastructure and

equivalent to the National Biotic Resource Information System described in the report of the Na-
tional Research Council.

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PROPOSED NATIONAL BIODIVERSITY INFORMATION CENTER / 503

that a wide range of partners meet regularly to work toward common strategies
for achieving specific partnership goals (in this case, to increase the accessibility
of information). NBIC provides the “neutral forum” around which those com-
mon strategies can be developed. The relationship between NBS and NBIC will
evolve, with a shared goal of improving the accessibility of data and information
on biodiversity.
In addition, the Center—by representing not solely a single government
agency or the federal government but the entire biological information commu-
nity in the United States—can provide important international linkages and
make an important statement regarding the need for broad collaboration. The
Convention on Biological Diversity encourages nations to develop such inte-
grated information networks. Collaboration with the nongovernmental sector
provides a powerful example for other nations.
It should be noted that, as this article is being written, the NBIC, NBS, and
NBII and their interrelationships are still in a stage of formulation and flux. For
this reason, the descriptions, roles, and interactions of these entities should be
viewed as preliminary and are likely to change as technology advances and
policies evolve.

CONCLUSION
The United States is beginning to recognize the critical role that information
performs in supporting conservation of biodiversity. The Nature Conservancy’s
Natural Heritage data program pioneered more aggressive and systematic ap-
proaches to collect, process, and share information about the occurrences of
biodiversity (Jenkins, 1988). The calls for creation of a new U.S. National Bio-
logical Survey have been answered, and the National Biological Service (NBS)
now exists. The NBS will be leading a National Partnership for Biological Survey
and helping to build a National Biological Information Infrastructure for the
United States. International efforts such as ERIN and BIN21 are improving the
global biological information infrastructure. A vision for a global “environmen-
tal channel” is emerging. The proposed U.S. National Biodiversity Information
Center likely will play a key part in helping a wide range of users to gain aware-
ness of and access to information on biodiversity in the United States.

ACKNOWLEDGMENTS
Many of the ideas in this paper have been expressed previously by Jonathan
Z. Cannon, Assistant Administrator for Administration and Resource Manage-
ment, U.S. Environmental Protection Agency, in his presentation on “Informa-
tion—The Key to Ecosystem Management” to the Environmental Information
and Computing Technologies Conference on June 9, 1994. We thank Dr. David
Blockstein of the Committee on the National Institute for the Environment and

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504 / BIODIVERSITY II

Dr. K. Elaine Hoagland of the Association of Systematics Collections for back-

ground information on the history of activities relating to the establishment of a
National Biodiversity Information Center. The final concept for a National
Biodiversity Information Center is taken from the report of the National Bio-
diversity Information Center Advisory Planning Board. We also acknowledge
the ideas and other contributions of Dr. John R. Busby and Jacques Kapuscinski.

REFERENCES
Association of Systematics Collections. 1986. Foundations for a National Biological Survey. Asso-
ciation of Systematics Collections, Lawrence, Kans. 215 pp.
Committee for the National Institute for the Environment. 1993. A Proposal for a National Institute
for the Environment: Need, Rationale, and Structure. Committee for the National Institute for
the Environment, Washington, D.C. 99 pp.
Council on Environmental Quality. 1993. Incorporating Biodiversity Considerations Into Environ-
mental Impact Analysis Under the National Environmental Policy Act. U.S. Government Print-
ing Office, Washington, D.C. 29 pp.
Hoagland, K. E. 1993. A National Center for Biodiversity: A Report to the Smithsonian Institution.
Abridged version for the National Research Council Committee on the National Biological Sur-
vey. Association of Systematics Collections, Washington, D.C. 16 pp.
Jenkins, R. E., Jr. 1988. Information management for the conservation of biodiversity. Pp. 231-239
in E. O. Wilson and F. M. Peter, eds., BioDiversity. National Academy Press, Washington,
D.C.
Keystone Center. 1991. Biological Diversity on Federal Lands. Report of a Keystone Policy Dia-
logue. Keystone, Colo. 96 pp.
National Biodiversity Information Center Advisory Planning Board. 1994. The National Biodiversity
Information Center. Washington, D.C. 13 pp.
National Research Council. 1993. A Biological Survey for the Nation. National Academy Press,
Washington, D.C. 205 pp.
Office of Technology Assessment. 1986. Assessing Biodiversity in the United States: Data Consid-
erations—Background Paper #2. OTA-BP-F-39. [NTIS-PB-86-181-989/AS] U.S. Government
Printing Office, Washington, D.C. 72 pp.
Office of Technology Assessment. 1987. Technologies to Maintain Biological Diversity. OTA-F-
330. U.S. Government Printing Office, Washington, D.C. 334 pp.
Systematics Agenda 2000. 1994. Systematics Agenda 2000: Charting the Biosphere. Technical
Report. Systematics Agenda 2000, a Consortium of the American Society of Plant Taxono-
mists, the Society of Systematic Biologists, and the Willi Hennig Society, in cooperation with
the Association of Systematics Collections, N.Y. 34 pp.

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Copyright © National Academy of Sciences. All rights reserved.

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CHAPTER
33

Santa Rosalia, the Turning of the

Century, and a New Age of Exploration
MARJORIE L. REAKA-KUDLA
Professor, Department of Zoology, University of Maryland, College Park

DON E. WILSON
Director, Biodiversity Program, National Museum of Natural History,
Smithsonian Institution, Washington, D.C.

EDWARD O. WILSON
Pellegrino University Professor, Museum of Comparative Zoology, Harvard
University, Cambridge, Massachusetts

Although a number of scientists (including several contributors to this vol-

ume) previously had targeted the origin and maintenance of diversity in biologi-
cal communities as a central issue in biology, the scientific community and the
public began to be generally aware of declining biodiversity—and the tragically
coincidental decline in numbers of scientists trained to analyze the diversity of
the world’s organisms—only within the last 10 years. One of the primary means
by which these dual crises became known to the scientific community and the
public was through the publication of BioDiversity by the National Academy
Press (Wilson and Peter, 1988).
Since that time, national and international interest in the issue of bio-
diversity has risen to an all-time high. The public has become informed about
the natural diversity of communities such as rain forests, prairies, wetlands, and
coral reefs, and alarmed at the rate at which these natural wonders are being
lost. Policy-makers have advocated or argued about our responsibility for sav-
ing endangered species and the costs and benefits of preserving them. Major
strides have been made by the scientific community in understanding the pro-
cesses that regulate biodiversity, predicting how much will be lost if habitats
are degraded, and developing new technologies for the conservation and sus-
tainable use of biodiversity. There has been a pervasive realization, however,
that the number of trained specialists is low and the job of understanding the
world’s biodiversity is vast; and vigorous discussions have raged about how to
approach the all-important task of documenting and conserving the world’s

507

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508 / BIODIVERSITY II

biodiversity. Thus, some might think that the speed of destruction is too fast
and that even to survey the world’s resources in biodiversity is a task too over-
whelming and expensive to undertake. The fact remains that far-reaching
changes in the infrastructure of our knowledge have occurred since the seminal
publication of BioDiversity.
The goal of the present volume is to summarize important conceptual and
technological developments that have occurred in the field of biodiversity since
the publication of the original volume, with a view to whether or not and how
we can cost-effectively assess, understand, and manage our total global bio-
diversity. It is critically important to present this information in a format that is
accessible to scientists, students, policy-makers, and the public, for only with
their collective concurrence and support will the effort succeed.

THE HISTORICAL CONTEXT OF BIODIVERSITY

IN WESTERN CULTURE
Humans always have been fascinated by biodiversity. As pointed out by
Patrick (1983), an appreciation of the diversity of animals in included in the
book of Genesis. Furthermore, the history of the modern science of biodiversity
can be traced from the writings of the Greek philosopher, Aristotle, in the fourth
century B.C., through medieval myths and manuscripts, which were ornamented
with all manner of animals, including invertebrates (Hutchinson, 1974; Waddell,
1934). In his Systema Naturae (1758), Carolus Linnaeus consolidated western
knowledge of the names, pedigrees, and descriptions of all of the kinds of ani-
mals that were known at the time (4,379 species, of which 1,937 were insects).
The academic appreciation of the diversity of life continued into the nine-
teenth century, as represented especially in the work of Charles Darwin and
Alfred Wallace, and experienced a resurgence during the synthesis of genetics,
paleontology, comparative anatomy, and modern evolutionary theory in the
“new systematics” of the 1940s and 1950s. A flurry of papers (mostly published
in the young journal Systematic Zoology) raised questions about how many of
the world’s species from different major taxa and different environmental realms
were known (Hyman, 1955; Muller and Campbell, 1954; Sabrosky, 1953a;
Thorson, 1957). Citing how little still was known and how variable were the
estimates of the numbers of species of different animal groups, Sabrosky (1953b)
called for the Society of Systematic Zoologists to sponsor a global census of the
animal kingdom that would be completed in 1958—the two-hundredth anniver-
sary of the tenth edition of Systema Naturae.
Building upon earlier traditions in ecology (Elton, 1930; Hutchinson, 1957),
G. Evelyn Hutchinson (1959) provided an icon for the synthesis of evolution,
systematics, and ecology in his presidential address to the American Society of
Naturalists, “Homage to Santa Rosalia, or why are there so many kinds of ani-
mals?” A stalactite-encrusted skeleton of Santa Rosalia, a twelfth century Sicil-

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SANTA ROSALIA / 509

ian saint, had been found in a cave near a hillside pond where Hutchinson found
two species of water boatmen (Corixidae) living in abundance. This aquatic
community stimulated Hutchinson to muse about how so few or so many species
can coexist in any given environment. The query led Hutchinson, his students,
and coworkers to formulate theories of the niche and species packing—and thus
to address the number and functional assembly of species in natural communi-
ties—through their investigations of food webs, the structure of environmental
mosaics, body size relationships among components of the community, and the
evolutionary biogeography of island biotas. Thus, Santa Rosalia was erected as
the “patroness of evolutionary studies” (Hutchinson, 1959:146).
Although it is clear how Hutchinson’s question was connected to Santa
Rosalia, an exploration of medieval manuscripts, which recognized the impor-
tance of human harmony with the world’s biodiversity even then, suggests that
some other saints might have been more appropriately tied to ecological and
evolutionary studies of biodiversity than Santa Rosalia. For example, the medi-
eval St. Kevin of Ireland lived among “the wild things of the mountains and the
woods” that “came and kept him company, and would drink water ... from his
hands,” and “there were times that the boughs and the leaves of the trees would
sing sweet songs to St. Kevin” (Waddell, 1934:129; Figure 33-1). A huntsman
and his hounds who chased a wild boar into the vicinity were so impressed with

FIGURE 33-1 St. Kevin surrounded

by beasts of the woods (from the trans-
lation of medieval legends from Latin
by H. Waddell, with woodcuts by
R. Gibbings; Waddell, 1934).

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510 / BIODIVERSITY II

FIGURE 33-2 St. Brendan and his

men above innumerable beasts of
the sea (Waddell, 1934).

the diversity of animals flitting around St. Kevin and perched on his shoulders
that the hounds lay down, refusing to attack the boar, and the hunter returned
to tell the King of Leinster. Similarly for the marine realm, another medieval tale
tells of St. Brendan and his men, who were celebrating the Feast of St. Paul in a
boat on the Irish Sea when the men said “Sing lower, Master, or we shall be
shipwrecked. For the water is so clear that we can see to the bottom, and we see
innumerable fishes great and fierce, such as never were discovered to human
eye before ... The creatures rose on all sides, making merry for joy of the Feast,
followed after the boat for the day, and then returned to the deep” (Waddell,
1934:111; Figure 33-2). An additional legend chronicles an appreciation for the
utility of biodiversity. St. Colman eschewed earthly possessions, but kept a
mouse, a cock and a fly as companions. The rooster crowed to wake him for his
prayers, the mouse nibbled at him to remind him of the time for his holy vows,
and the fly treaded up and down his codex to sit on the line where St. Colman
had halted his reading so that he could refind his place (Figure 33-3). The leg-
end describes his sorrow when his small companions died and he was left alone
(Waddell, 1934).

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SANTA ROSALIA / 511

Consequently, an appreciation of biodiversity runs deep in western culture,

and an awareness of how much of the abundance and variety of animal life has
declined, even since medieval times, can be gained from this literature. While
the academic tradition of studying the diversity of life continued into the nine-
teenth century and flourished beyond the first half of the twentieth century
during the development of the “new systematics,” the science of biodiversity
was overshadowed in the 1960s, 1970s, and early 1980s by the spectacular
growth of molecular biology (Wilson, 1994), during which time the numbers of
systematists contributing to the “new synthesis” declined unnoticed by most
academics. Interest in the field by academicians, policy-makers, and the public
was reawakened by publication of BioDiversity.
Aside from the academic tradition of biodiversity, another powerful influ-
ence, related to biodiversity, brought our culture to its current level of techno-
logical development: the exploration of the New World. From the thirteenth to
the nineteenth centuries, technological developments in navigation allowed
European voyagers to embark on an unprecedented exploration of the globe.

FIGURE 33-3 The utility of beastly

companions to St. Colman (Waddell,
1934).

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512 / BIODIVERSITY II

These expeditions revolutionized knowledge of the geography, human culture,

and biology of the world at the time. This ultimately led to a reevaluation of
human society’s place in the world and an understanding of the evolution of all
living things. But the explorations also allowed the acquisition of untold wealth
in living and nonliving natural resources (see also Kangas, Chapter 25, and
Mehrhoff, Chapter 29, this volume), which was brought back from the New
World and invested in the culture of western Europe.
In North America, the Louisiana Purchase in 1803 was followed by the
Lewis and Clark Expedition (1804-1806), which culminated Thomas Jefferson’s
long-planned (and congressionally approved) effort to chronicle the natural
wealth of the continent. This widely celebrated geographic and scientific ex-
pedition mapped the natural history of the central and northwestern part of the
continent and brought back many plant and animal specimens that were un-
known previously (including the prairie dog, jackrabbit, black-tailed deer,
pronghorned antelope, and mountain sheep), providing perhaps the first “na-
tional biological survey” (also see Mehrhoff, Chapter 29 of this volume, for the
historical role of museums and surveys). The subsequent acquisition of Florida,
Texas, and California from France and Spain by the middle of the nineteenth
century and the expansion of settlers into these regions widened knowledge of
the natural resources of the continent. Continuing the earlier European explo-
rations, the knowledge that was gained and the use of the newly discovered
natural resources from the exploration of the American continent changed west-
ern civilization forever, bringing us to our current level of technological devel-
opment (but which, in turn, has drawn us to the current brink of environmen-
tal disaster).

THE NEED FOR A NEW EXPLORATION OF THE BIOSPHERE

Five centuries beyond the beginning of New World explorations and 150
years after the opening of the American West, we now have the technological
knowledge to embark on a new age of exploration of the globe that is of compa-
rable importance for human culture and knowledge to those historical events.
For the first time, we have the potential capability (with a skeletal infrastructure
of scientific personnel and institutions) to undertake a thoughtful inventory of
global biotic resources (Raven and Wilson, 1992); to understand and predict the
processes that govern the amount, location, and sustainability of these resources;
and to provide the information that is necessary to protect as much of the re-
maining global biota as possible so that humans and the biosphere may persist.
What is essential now is a coordinated effort—comparable in scale and idealism
(and very likely of greater importance for our long-term survival) to the Human
Genome Project—to explore and describe (and only thusly to understand, pre-
dict, and manage) the biota of planet Earth.

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PROGRESS SINCE 1986, PRESENT AND EMERGING

INFRASTRUCTURE, AND COST-EFFECTIVE SOLUTIONS

Status of the Field

This volume, an outgrowth of the Inaugural Symposium of the Consortium
for Systematics and Biodiversity (comprised of the University of Maryland at
College Park, the Smithsonian Institution Natural History Museum, the U.S.
Department of Agriculture Systematic Laboratories, the University of Maryland
Biotechnology Institute, and the American Type Culture Collection), is orga-
nized developmentally. Edward O. Wilson opens the book with a discussion of
the historical context of biodiversity and demonstrates how biodiversity in-
cludes all facets of biology and even all fields of science. It is a field of synthesis,
forged by necessity. As when any society faces a threat to survival, the chal-
lenge of declining biodiversity offers unification. All scientific fields can (and
do) contribute to the advancing front of knowledge in biodiversity; we are lim-
ited only by our vision of how to employ their contributions most effectively to
conserve biodiversity. This introductory chapter addresses the opportunity and
the need to explore the biosphere.

The Meaning and Value of Biodiversity

Part I of this book is devoted to an exposition of biodiversity by two early
explorers of the field, Ruth Patrick and Thomas Lovejoy. The purpose of this
volume is to educate students, teachers, scientists, policy-makers, and the pub-
lic about what biodiversity is and how important it is to understand it. These
authors eloquently explain to this broad audience why biodiversity has become
a central issue at local, national, and international levels. Chapters elsewhere in
the volume also address the meaning and value of biodiversity. For example,
Miller and Rossman, as well as Solis, stress the critical importance of the science
of biodiversity for agriculture (Part IV). Janzen champions the use of bio-
diversity as a primary means of making society aware of its value so that it can
be conserved (Part V). Jordan describes the process of restoration of biodiversity
as meaningful in itself to human society (Part V).

Patterns of Biodiversity
Part II assesses the question of how much and where biodiversity occurs on
the globe—a fundamental question that, astonishingly, is still unknown, al-
though, as the chapters and their citations demonstrate, phenomenal progress
has been made on this issue during the last decade. Erwin, pioneer of the revo-
lutionary figures for the global diversity of insects that spurred debate on how
many millions of species exist on Earth, provides an update to the long-standing
question of why the greatest proportion of species on Earth are insects (Erwin,

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1982; Gaston, 1991; Hutchinson, 1959; Labandeira and Sepkoski, 1993; Linnaeus,
1758; May, 1978; Muller and Cambell, 1954; Sabrosky, 1953a; Stork, 1988; Wil-
son, 1988). Focusing on beetles in rain forest canopies, Erwin shows how con-
centrated studies in local geographic areas can improve our understanding of
which and how many species occur in natural communities; importantly, he
delineates the practical steps that make the acquisition of this knowledge fea-
sible within a reasonable time frame. Stork carefully evaluates the progress
made over the last decade in our estimates of global biodiversity. He concludes
that 5-15 million (perhaps near 12 million) species probably occur on Earth. His
chapter culminates in a sobering, carefully considered discussion of current ex-
tinction rates and prospects. Robbins and Opler also address the most speciose
group of organisms on Earth, insects. They provide the important result that
biogeographic patterns of butterfly diversity are similar to those of birds, so
that conservation efforts targeted at particular regions will protect both compo-
nents of the biological community. However, mammals show a different pat-
tern, heralding caution in conservation policies (also see chapters by Myers,
Scott and Csuti, Dietz, and Thomas in Parts III and IV of this volume for elucida-
tion of emerging technology and recommendations on how to prioritize bio-
diversity efforts among different areas, habitats, and organisms).
Moving to the little-known aquatic realm, Reaka-Kudla employs biogeo-
graphic theory to provide the first quantified estimate of the number of species
that inhabit the second pinnacle of diversity and extravagant adaptation on
Earth, coral reefs. The results show that only about 93,000 species of described
species live on global coral reefs, a paltry figure compared to the number of
described species that inhabit rain forests (less than a million, although at least
2 million described and undescribed species almost certainly occur there). How-
ever, this chapter determines that global coral reefs occupy 20 times less area
than global rain forests, and the data suggest that less than 10% of the species
on coral reefs are known. A conservative estimate indicates that about a million
species exist on global coral reefs. Moreover, Reaka-Kudla’s results suggest that
the possibility of current and future extinction of coral reef species (which are
predominantly small in body size with restricted geographic ranges) is high,
rather than low, as some workers have suggested for species in marine environ-
ments. All of the authors in this section and several authors elsewhere in the
volume stress that the greatest undocumented diversity is found in organisms of
small body size and in tropical regions, and that many species in these groups
and regions are likely to become extinct before they are even known if swift
conservation measures are not adopted.
Sogin and Hinkle provide a fascinating view of the evolution of microbial
diversity (another enigma whose international profile has been elevated by in-
creasing interest in biodiversity over the last decade). Their results are gar-
nered with new molecular techniques that are only beginning to sketch the
true dimensions of the biosphere. This approach elucidates the antiquity of

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genetically distinct lineages in the global biota. Instead of five organismal king-
doms (bacteria [prokaryotes], protistans [protozoans and relatives], fungi,
plants, and animals), these authors show three lines of descent in the evolution
of living organisms: the Archaebacteria (Archaea), Bacteria, and Eukarya (eu-
karyotes [protistans and multicellular organisms]). Startlingly, the Eukarya are
nearly as ancient as the other two groups, and the diversity and antiquity of
relationships among the various microbial organisms is no less than astounding.
Colwell also addresses the significance of microbial diversity for biotechnology
in a later section of the volume (Part V). Other chapters (Part IV) provide addi-
tional contributions to our understanding of patterns in biodiversity, such as
the studies of the evolution of bower-building in birds (Borgia), hyperdiversity
in an economically important group of moths (Solis), and coevolutionary pat-
terns in several groups of parasites and their hosts (Hoberg).

Threats to Biodiversity
The topic of Part III of the volume is as ominous as it is imperative to scru-
tinize: the threat of extinction. Myers provides a riveting examination of sev-
eral issues related to the decline of biodiversity. He notes that, although lakes
and rivers contain a quarter of the known species in 0.01% of the planet’s wa-
ter, these freshwater ecosystems are being degraded faster than any other biome.
In the United States, only 2% of the rivers are free-flowing and 20-55% of their
major taxa are endangered or extinct. In the spectacular species swarms of
cichlid fish in the African rift lakes (where 44-95% of the species are endemic),
introduced predators and other disturbances have reduced species by 67%, and
these losses are likely to accelerate. Discussing the decline of biodiversity over
the last 30,000 years (during which time 70% of North American mammals have
been lost) as well as the accelerating current impacts of humans, Myers notes the
importance of the loss of populations and genetic variability for the future survival
of species. He concludes that, because of the scale of anthropogenic changes in the
environment, we must conserve the biosphere rather than only parks and re-
serves, and that, if recovery takes 5 million years, this decision will affect more
people (an estimated 500 trillion) than any other decision in human history.
Steadman examines human-caused extinctions in birds, which began long
before the impact of Europeans. Whereas prehistoric extinctions caused by
humans were greatest on islands (especially in the Pacific), population declines
and extinctions now have begun in earnest on the continents. Steadman’s stud-
ies identify what regions and countries (e.g., Indonesia, Solomon Islands) are
most at risk of losing species of birds. The most significant agent of bird extinc-
tion, habitat destruction, is greatest in the tropics (see also Stork and Reaka-
Kudla in Part II). Later in the volume (Part IV), Borgia also points out the
dangers that accelerating contemporary extinctions in birds pose for our under-
standing of biodiversity. Comparative information from many species is neces-

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sary to understand the evolution of complex or extreme traits such as building

bowers, elaborate plumage, and nuptial dances in bowerbirds; this window to
knowledge soon may be closed. Now is not a good time to reduce funding for
basic research.
Wing provides a longer-term perspective on the risks of extinction in his
examination of the causes and consequences of the rapid global warming event
that occurred during the late Paleocene and early Eocene. This chapter de-
scribes different mechanisms that caused extinctions in marine versus terrestrial
organisms during this period (which was warmer than now), shows that differ-
ential capability for migration may cause different patterns of declining diver-
sity in paleontological data (e.g., in mammals versus plants), and cautions that
models in current use may not accurately predict the trajectory of global cli-
mate. Forseth also cautions that plant assemblages are likely to change in new
ways in response to climatic change, and that we need to understand how spe-
cies respond to multiple environmental stresses—and how these responses trans-
late to ecosystem responses, biogeography, and potential extinction—in order
to sustain biodiversity in the future.
Other chapters in the volume echo the thought that we need to evaluate the
responses of organisms to changing environments through historical analysis.
For example, Hoberg (Part IV) uses historical reconstruction of the phylogenies
of parasites and their hosts to evaluate how patterns of biodiversity are influ-
enced by climatic, geological, and biotic factors. Studies of freshwater stingrays
and their parasites in the Amazon and tapeworms and their marsupial hosts in
South America and Australia indicate that these ecological associations have been
stable for 60 million years. On the other hand, phylogenetic relationships of
pinnipeds and seabirds and their relatively recent tapeworm parasites suggest
that climatic changes associated with the Pliocene-Pleistocene glaciations pro-
moted isolation and speciation rather than extinction in the North Atlantic and
North Pacific regions. Comparing behavior patterns with phylogenies derived
from mitochondrial DNA, Borgia (Part IV) evaluates the history of displays in
bowerbirds and examines alternative hypotheses for the selective pressures that
shaped the diversity of bowers and species in this group. Friedlander et al. (Part
V) show how molecular data can be used to estimate times of divergence among
major taxa. From such data, one can estimate how many millions of years will be
required to replace lineages lost through extinction, and thus how grave the
threat of current extinctions is.

Understanding and Using Biodiversity

Part IV addresses the means we use to comprehend and use biodiversity.
Patrick explains why the study of systematics is central to the biodiversity
agenda. With the description of a systematics training program that was char-
tered by several leading institutions to provide mentoring for critically needed

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young systematists, she provides an inspiring example of how relatively small

programmatic efforts can have a significant impact. Wheeler and Cracraft also
provide an eloquent plea for the training of young systematists in a later section
of the volume (Part VI). They indicate that a single generation of young scholars
could reverse the erosion of systematic expertise that has occurred over the last
several decades.
Embellishing a tradition begun with Linnaeus, Thompson shows how im-
portant precise names for organisms are for the effectiveness of the current
biodiversity agenda (also see Farr and Rossman, Part VI of this volume). Miller
and Rossman and Solis demonstrate the overwhelming economic importance of
research in systematics and biodiversity. They show that, as we progress be-
yond a period in which agriculture was dominated by the use of pesticides, we
need to know the world-wide taxonomy and distribution of pests and their natu-
ral enemies in order to implement effective mechanisms of biological control and
integrated pest management. For example, inaccurate identification of a mealy-
bug—which was costing African cassava farmers $1.4 billion per year—led to
the introduction of ineffective natural enemies from the wrong geographic re-
gion and delayed control of the pest for several years (at which time a system-
atist studying the entire group identified the pest as a new species from another
region; only then were successful natural enemies obtained). Miller and Rossman
document the economic importance of introduced pests into the United States—
over $196 trillion for the >450,000 species that had been detected and identified
up until 1991. The systematics of these pests must be accurately known before
the U.S. Department of Agriculture APHIS quarantine and pest exclusion sys-
tem can be effective (e.g., a near-international incident was averted when a tax-
onomist found that smut on Canadian wheat was a contaminant from the storage
of rice rather than a new species that afflicted wheat; incorrect identification
could have caused a ban on all wheat from Canada). Focusing on a group of
hyperdiverse moths that are major pests of crops and stored grains as well as
important agents of biological control for weedy plants, Solis’ chapter is an ex-
cellent example of how to use systematics and education to rapidly generate and
transfer essential information about biodiversity in a tropical country (e.g., in
10 versus 30 years). She demonstrates that, in order to increase the taxonomic
self-sufficiency of tropical countries and to be effective in pest control, taxo-
nomic studies in individual countries must be framed in a global context—in-
corporating information from the literature, collections, and taxonomists
throughout the world—and placed at the fingertips of ecologists, conservation-
ists, quarantine officers, and farmers in usable form.

Building Toward a Solution

Part V focuses on new technology and new directions which offer hope
that the biodiversity crisis can be effectively addressed in a timely fashion.

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Colwell describes the current state of the biotechnology industry, the promise
it offers for agricultural and medical developments that would improve human
conditions, and its critical dependence on the preservation of biodiversity in
the wild. Showcasing research that emanates from a laboratory intimately in-
volved with the Human Genome Project, Bult and her coauthors describe revo-
lutionary new genetic technology that can be used to identify and quantify
genetic diversity at the levels of populations, species, and lineages more rap-
idly than ever before. Combined with the techniques for data management that
have been developed in the authors’ institute (see also Farr and Rossman,
Umminger and Young, Part VI) and the interdisciplinary collaboration (involv-
ing systematists, evolutionary biologists, molecular biologists, computational
biologists, computer scientists) that is modeled in Bult et al.’s chapter, these
technological breakthroughs offer real hope for an assessment and understand-
ing of global biodiversity that was not possible even 5 years ago. Similarly, the
chapter by Friedlander and his coauthors represents rapid advancement in con-
ceptual and molecular analyses of phylogenetic relationships—and hence our
understanding of the patterns and processes that generate diversity within lin-
eages. In an earlier section of the volume (Part IV), Thompson also dicusses
how taxonomic identifications in biodiversity inventories can be made more
rapidly with computerized technology.
In quite another new direction of the field, Scott and Csuti describe their
Gap Analysis Program, which uses remote-sensing from satellites, geographic
information systems, and sophisticated integration of data to assess the status
and distribution of several important elements of biodiversity on a landscape
scale. Gap analysis provides a layered framework for integrating data on species
(abundance, distribution), types of habitats, topography, soils, climate, and hu-
man components (land-use, zoning, development, population density) so that
critical areas or habitats that contain species or assemblages at risk can be iden-
tified, monitored, and their trajectories predicted on computer-generated maps.
This type of analysis has shown that endangered assemblages often are not in-
cluded in protected areas or management plans. For example, only 5% of
Hawaii’s endangered forest birds live in forest preserves (Scott et al., 1986). Gap
analysis also can be used to identify how widespread or abundant species must
be to avoid precipitous declines in population, and can identify which of several
combinations of contiguous areas would provide the most overall diversity if
conserved. The latter allows for some flexibility in conservation policies in
response to constraints imposed by human needs or costs.
Building upon a foundation of knowledge about the systematics, geographic
distribution, ecology, genetics, and behavior of golden lion tamarins and other
neotropical primates, Dietz also employs images derived from satellite-borne
instruments, geographic information systems, and sophisticated technology to
integrate large sets of data and construct conservation strategies. He outlines
several specific approaches—including application of the scientific method, in-

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formation management, captive breeding and reintroduction, and educational

and collaborative activites—to provide hope that these endangered primates
will be sustained.
Thomas advocates selecting areas of evolutionary diversification for conser-
vation (also see Myers, Part III of this volume) and indicates that interdiscipli-
nary approaches (including plate tectonics, paleogeography, cladistics, ecology,
and anthropology) are necessary to understand and pinpoint critical areas of
biodiversity. Using the exceedingly diverse coral reefs of Papua New Guinea as
an example, he points out that small, spatially inconspicuous organisms may be
better indicators of environmental change than large, conspicuous, and less
abundant species. The technological and conceptual developments presented in
this section of the volume suggest that assessment and continued monitoring of
global natural resources is a feasible goal within the next decade or two.
In an evocative treatment of emerging ideas in the relatively new field of
ecological restoration, Jordan emphasizes that “restoration” is not the complete
rebuilding of a damaged environment, but is any attempt at conservation that
ensures the existence of the system in the long run. Rather than focusing on the
products of restored ecosystems, he suggests that the experience and perfor-
mance of restoration—getting people involved with the environment—is the
most immediate and valuable payoff from restoration activities.
Similarly, the concept of sustainable development—the long term renew-
able use of biotic resources—is undergoing a renaissance in biodiversity studies
from its prior use in fisheries and related harvestables. In a humanistic treat-
ment of sustainable development in tropical forest lands, Kangas discusses the
practical interdisciplinary aspects of how to make conservation work. He pro-
vides a suite of illustrative historical examples (Mayan culture, Henry Ford’s
sustainable villages, the roots of the American Civil War, extranational compa-
nies, the biotic and economic exchanges fostered by Christopher Columbus, the
origin of agriculture, the Louisiana Purchase, the American colonial tobacco
agricultural system, Puerto Rican deforestation, the Civilian Conservation Corps,
and a Brazilian forest) from which we can learn about interactions between hu-
mans, their economic activities, and the environment. These examples of what
can be done, of approaches that worked (and some that did not), are very wel-
come. However, even this chapter cites a new urgency—not seen in the ex-
amples from prior centuries—in the need for sustainable development that pro-
tects the long-term function of biotic communities.
Janzen indicates that we are at the crossroads of biodiversity and wildland
management. One route is to preserve biodiversity without heavy use, which
he argues ultimately will result in less biota being conserved in a smaller total
area. The other avenue is to use the biodiversity. Because of the attendant
valuation of biodiversity, he suggests that a larger percentage of the remaining
biota and larger amounts of land can be conserved if the second route is taken.
Due to the urgency of declining biodiversity, Janzen indicates that we need

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to streamline collection of knowledge about biodiversity and gather information

only on the taxonomy, biogeography, and natural history of organisms. This
emphasizes the need to reinstate these traditional and important fields in our
university curricula and national priorities.
The architect of All Taxa Biodiversity Inventories (ATBIs), Janzen suggests
that these intensive field samples provide the best and most cost-effective way
to sample biodiversity and assess its trajectory over time, one that is most tai-
lored to the needs of local and national peoples. Others have questioned how
many ATBIs would be necessary and whether they would sample global bio-
diversity adequately. Some scientists think that intensive local or regional pro-
grams can sample biodiversity adequately if located properly (chapters by
Erwin, Myers, Scott and Csuti, and Thomas in Parts II, III, and V in this volume
address aspects of this issue), but other scientists worry that the patterns of
species richness and endemism may vary for different taxa (chapters by Wheeler
and Cracraft, Robbins and Opler in Parts VI and II) or that too few sites could be
sampled and species with restricted ranges would be missed (e.g., see chapters
by Wheeler and Cracraft, Reaka-Kudla in Parts VI and II).
Whereas Janzen’s vision (Yoon, 1993) contrasts to some extent with that of
some systematists (Wheeler and Cracraft, Part VI) and has been termed an “eco-
logical” approach, Janzen’s agenda does emphasize the validity and importance
of focusing on taxonomy and on genetic variants, populations, species, and lin-
eages of organisms, as opposed to geochemical cycles, nutrient flow, or other
ecological attributes that are not directly tied to evolutionary units. In contrast
to this view, some researchers have suggested that the function and productiv-
ity of ecosystems should be the essential targets of research and conservation as
environments deteriorate, and that the number of species present is not relevant
(see discussions in Baskin, 1994; Walker, 1992). This position ignores the present
and future value of all the agricultural, medical, genetic, and other products
contained within the species of the global biota (as discussed by Lovejoy,
Patrick, Miller and Rossman, Solis, and Colwell in Parts I, IV, and V of this
volume; see also “The Fundamental Unit” in Wilson, 1992). Exclusive concen-
tration on the function of ecosystems, rather than on genetic and species units,
also ignores the aesthetic and moral values of biodiversity (see Jordan, this sec-
tion; and Wilson, 1984, 1992). We cannot afford to lose the historical legacy of
lineage diversity or the prisms that allow its comprehension and use—systemat-
ics, taxonomy, and natural history.

Getting the Job Done

Part VI concentrates on the infrastructure that is in place for assessing and
understanding biodiversity. In a chapter that touches on many of the issues
addressed throughout the volume, Wheeler and Cracraft document the present
and needed infrastructure for undertaking a global systematic survey of biota,

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as proposed by the Systematic Agenda 2000. Mehrhoff documents the historical

role that biological surveys and museums—centerpieces in the struggle to docu-
ment global biodiversity—have played in understanding and ultimately pro-
tecting our biota. Their contemporary role may be even more important. By
fostering knowledge of systematics and taxonomy, surveys and museums offer
the only hope of understanding how our current living resources evolved and
how natural communities function. Discussing a technological realm about
which most people have little knowledge, Roblin also indicates the promise and
the challenge of maintaining living collections (especially of the microorganisms
of which we know so little) to facilitate our stewardship of biodiversity. These
papers emphasize the need for changes in our approach to elementary, second-
ary and higher education. The interest of many well-known contemporary bi-
ologists was kindled first in museums or by their experiences in natural history.
Will there be a comparable generation 50 years from now? We need more hands-
on laboratory experiences and courses that expose students to the emotional
thrill and the intellectual challenge of biodiversity that is seen in museums and
in the field (see also Wilson, 1994).
The enormously complex task of managing data in an endeavor the magni-
tude of a global biodiversity assessment is one of the greatest logistical problems
faced by scientists, but this problem can and is being solved. Farr and Rossman
provide a detailed examination of two approaches to the management and inter-
pretation of data that are effective, accurate, and in place (also see chapters by
Bult et al., Scott and Csuti, and Dietz in Part V). Umminger and Young describe
the explosion of national and international electronic systems that allow summa-
rization and communication of environmental data. Stressing that information
management is critical for the success of the international agenda in biodiversity,
these authors describe the development, status, and goals of a U.S. National
Biodiversity Information Center related to the National Biological Survey.

CONCLUSIONS
The most important message in this volume is also a hopeful one: the insti-
tutional infrastructure (museums and their collections; state, national and global
biological surveys and their associated data banks; universities, institutes, and
governmental and nongovernmental agencies that support research, training,
and conservation policy) is already in place or in developmental stages. The
infrastructure to solve the biodiversity crisis does not need to be built from the
ground up; but current institutions must increase their linkages, and they must
have enhanced support. The human resources are in place: a small but expert
and committed community of systematists already is active. It will be essential
to augment funding, especially for training young people in systematics and
collection management, in order to make this infrastructure more effective for
the great task at hand. As is well indicated in this volume, the knowledge-base

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about biodiversity and how to manage it is substantial, is growing rapidly, and

is still very deficient for our needs. We must focus it, enlarge it, and fuse it
inextricably with systematics.
Interinstitutional links (maximizing shared human, financial, and institu-
tional resources between museums, universities, and governmental and non-
governmental agencies) will provide the key to cost-effective accomplishment of
a global biodiversity agenda. Representing a sea change that already is under-
way, 10 of the 33 chapters (30.3%) of the present volume are multiply authored,
in comparison to 2 of the 57 chapters (3.5%) that were presented in the first
biodiversity symposium (Wilson and Peters, 1988), indicating that larger, more
interdisciplinary research groups—often representing linkages among several
institutions—are increasingly common. Of the 10 chapters with multiple au-
thors in this volume, half result from collaborations among researchers from
more than one institution.
Interdisciplinary sharing of knowledge and resources is evident in several
chapters of this volume. The Consortium for Systematics and Biodiversity of the
greater Washington, D.C., area, one of the stimuli for the present volume, is an
example of sharing physical, institutional, and human resources in order to
maximize our potential impact on global biodiversity issues. Collectively, this
group of institutions includes one of the largest groups of systematists, evolu-
tionists, ecologists, and biotechnologists, and one of the largest biological collec-
tions (from molecular to organismal, all kingdoms) in the world. Each institu-
tion brings a unique research or training capability to the Consortium. Another
example of highly effective collaboration is represented by a group of scientists
from British universities and museums who, through individual and joint ef-
forts, have made many significant contributions to understanding biodiversity.
The collaborative training program in systematics between a number of major
American universities and the Smithsonian Institution described by Patrick (Part
IV, this volume) represents an example of productive collaboration among insti-
tutions and scientists. Mehrhoff (Part VI, this volume) describes the effective
union of 10 state biological surveys into a Consortium. The widely known pub-
lications and biodiversity agenda of Systematics Agenda 2000 resulted from the
joint efforts of a consortium of professional associations in systematics (Wheeler
and Cracraft, Part VI, this volume). The emerging Informational Center of the
National Biological Service (Umminger and Young, Part VI, this volume) will
involve collaborations among government agencies, universities, museums, re-
search institutes, and individual scientists. We need more and better-funded
cooperative efforts to maximize the ability of museums, universities, govern-
mental and nongovernmental organizations, and the systematic community to
implement the biodiversity agenda.
The contributions to this volume suggest that understanding and managing
global biodiversity is an attainable, cost-effective, and vitally important goal for
human society, and that increased public and governmental support for muse-

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SANTA ROSALIA / 523

ums and associated institutions is justified and essential. This support should be
directed toward enhancing an existing physical, human, and informational in-
frastructure in systematics and biodiversity, and especially toward training new
young specialists in this area. One of the objectives of the volume has been to
educate students who may be stimulated to enter the field, teachers, scientists,
policy-makers, and the public about the infrastructure that already exists for
understanding biodiversity, and about the urgent need to build upon this
strength. We hope to have instilled in this broad audience the idea that we can
and must act now.

ACKNOWLEDGMENTS
We wish to express our special appreciation to Valerie Cappola, Jocelyn
Kasow, and Mitchell Tartt for their dedication and assistance during the final
stages of preparation of this volume.

REFERENCES
Baskin, Y. 1994. Ecosystem function of biodiversity. BioScience 144:657-660.
Elton, C. 1930. Animal Ecology and Evolution. Clarendon Press, London. 296 pp.
Erwin, T. L. 1982. Tropical forests: Their richness in Coleoptera and other Arthropod species.
Coleopt. Bull. 36:74-75.
Gaston, K. J. 1991. The magnitude of global insect species richness. Conserv. Biol. 5:283-296.
Hutchinson, G. E. 1957. Concluding remarks. Cold Spring Harbor Symp. Quant. Biol. 22:415-427.
Hutchinson, G. E. 1959. Homage to Santa Rosalia, or why are there so many kinds of animals?
Amer. Nat. 93:145-159.
Hutchinson, G. E. 1974. Aposematic insects and the Masters of the Brussels Initials. Amer. Sci.
62:161-171.
Hyman, L. H. 1955. How many species? Syst. Zool. 4:142-143.
Labandeira, C. C., and J. J. Sepkoski, Jr. 1993. Insect diversity in the fossil record. Science 261:310-
315.
Linnaeus, C. 1758. Systema Naturae, tenth ed. L. Salvii, Stockholm.
May, R. M. 1978. The dynamics and diversity of insect faunas. Pp. 188-204 in L. A. Mound and N.
Waloff, eds., Diversity of Insect Faunas. Blackwell Scientific Publications, Oxford, England.
Muller, S. W., and A. Campbell. 1954. The relative number of living and fossil species of animals.
Syst. Zool. 3:168-170.
Patrick, R. 1983. Introduction. Pp. 1-5 in R. Patrick, ed., Diversity. Benchmark Papers in Ecology,
Vol. 13. Hutchinson Ross Publishing Company, Stroudsburg, Pa.
Raven, P. H., and E. O. Wilson. 1992. A fifty-year plan for biodiversity surveys. Science 258:1099-
1100.
Sabrosky, C. W. 1953a. How many insects are there? Syst. Zool. 2:31-36.
Sabrosky, C. W. 1953b. An animal census for 1958? Syst. Zool. 2:142-143.
Scott, J. M., S. Mountainspring, F. L. Ramsey, and C. B. Kepler. 1986. Forest bird communities of
the Hawaiian Islands: Their dynamics, ecology, and conservation. Stud. Avian Biol. 9:1-431.
Stork, N. E. 1988. Insect diversity: Facts, fiction and speculation. Biol. J. Linn. Soc. 35:321-337.
Thorson, G. 1957. Bottom communities. In J. W. Hedgepeth, ed., Treatise on Marine Ecology and
Paleoecology, Vol. 1. Mem. Geol. Soc. Amer. 67:461-534.
Waddell, H. 1934. Beasts and Saints. Translations by H. Waddell, woodcuts by R. Gibbings. Henry
Holt and Company, N.Y. 151 pp.

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Walker, B. H. 1992. Biodiversity and ecological redundancy. Conserv. Biol. 6:18-23.

Wilson, E. O. 1984. Biophilia. The Human Bond with Other Species. Harvard University Press,
Cambridge, Mass. 157 pp.
Wilson, E. O. 1988. The current state of biological diversity. Pp. 3-18 in E. O. Wilson and F.
M. Peter, eds., BioDiversity. National Academy Press, Washington, D.C.
Wilson, E. O. 1989. Threats to biodiversity. Sci. Amer. (September):108-116.
Wilson, E. O. 1992. The Diversity of Life. Belknap Press, Cambridge, Mass. 424 pp.
Wilson, E. O. 1994. Naturalist. Island Press, Washington, D.C. 380 pp.
Wilson, E. O., and F. M. Peter, eds. 1988. BioDiversity. National Academy Press, Washington,
D.C. 521 pp.
Yoon, C. K. 1993. Counting creatures great and small. Science 260:620-622.

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Biodiversity II: Understanding and Protecting Our Biological Resources
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Photo Credits

Page Credit Page Credit

i Chip Clark, Smithsonian 223 Agriculture Research Service

Institution 233 David Dussourd
5 Chip Clark, Smithsonian 238 Kjell Sandved, Smithsonian
Institution Institution
25 R. DeFries and D. Van Wie 253 Chip Clark, Smithsonian
28 Chip Clark, Smithsonian Institution
Institution 265 Gerald Borgia
36 Terry L. Erwin 270 Gerald Borgia
50 Nigel E. Stork 277 Lucy B. Williams
52 Nigel E. Stork 343 James M. Dietz
70 Carl C. Hansen, Smithsonian 346 R. DeFries and D. Van Wie
Institution 351 James M. Dietz
85 Lucy B. Williams 358 Lucy B. Williams
95 Carl C. Hansen, Smithsonian 365 Lucy B. Williams
Institution 373 William R. Jordan, III
100 Lucy B. Williams 376 William R. Jordan, III
110 Carl C. Hansen, Smithsonian 382 William R. Jordan, III
Institution 384 William R. Jordan, III
113 Tim Maugel 391 Smithsonian Institution
123 Carl C. Hansen, Smithsonian 401 Chip Clark, Smithsonian
Institution Institution
129 Chip Clark, Smithsonian 433 Chip Clark, Smithsonian
Institution Institution
140 Sam Stull 449 Leslie J. Mehrhoff
143 Virginia Carter Steadman 451 Smithsonian Institution
177 Scott L. Wing 457 Smithsonian Institution
178 Scott L. Wing 468 National Geographic Society
197 Smithsonian Institution 469 Tim Maugel
215 Chip Clark, Smithsonian 472 Richard O. Roblin
Institution 505 Chip Clark, Smithsonian
218 Agriculture Research Service Institution

525

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Biodiversity II: Understanding and Protecting Our Biological Resources
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Index

A pest introductions and quarantine, 222–224,

Acanthocephala, 244 227, 517
Acarina, 58 pesticides, 218–219
Accipiter cf. rufitorques (short-winged hawk), pests, 218, 219–223, 225, 234, 517
155 pollution,127
Acid precipitation, 11, 134, 135 sustainable, 221–222, 390, 399–400, 401–
Acraeini, 76 402
Acrocephalus sp. (warblers), 152, 153 systematics, 219–220, 224–225, 227, 517
Adalia decempunctata (ten-spot ladybird), 42 wetlands losses, 129, 130
Adams, Mark D., 289–299, 518 Agrobacterium tumefaciens (bacterium), 284
Africa Aguirre, Alvaro, 344
birds, 46, 144 Ailuroedus sp. (catbirds), 266, 267
extinctions, 144, 515 Alaska, 152, 157
Agaricus bisphorus (fungus), 116, 117 Albatrosses, 149
Agassiz, Louis, 452 Alcataenia (cestodes), 255, 256
Agenda 21, 390 Alcidae, 255
Agriculture. See also Crops; Fertilizers Aldabra Atoll, 86
biodiversity losses due to, 10, 13, 127, 134, Alder, 177
378 Aleutian Islands, 255
bioengineering, 220, 518 Algae
biological pest control, 219–220, 222–224, brown, 111
225, 226, 234–235, 283–284, 517 described species, 96
climate change and, 12 dimethyl sulphide production, 283
contributions of biodiversity, 8–9, 217–219, freshwater, 18–22, 89, 90
220, 224, 513 green, 111–113
ecosystem effects, 142, 218 marine, 89, 90, 96
export, 401–402 number of species, 90, 366
integrated pest management, 221, 517 red, 111–113
origin, 399–400, 519 Algal blooms, 13

527

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 528 / INDEX

All Taxa Biodiversity Inventories (ATBI) Aptornithids, 148

benefits,
Biodiversity II: Understanding and Protecting 57, 203, 416–417,
Our Biological Resources420–421, 438 Aquatic organisms and systems. See also
http://www.nap.edu/catalog/4901.html effectiveness, 438–439, 520 Freshwater; Marine; individual species
microbial diversity, 472–473 caterpillars, 233
resource requirements, 439–440 helminthic parasites, 250–251
sampling regimes, 32–37, 87, 520 number of species, 89, 90
Alligator Reef, Florida, 87 weeds, 235
Alligatorweed, 235 Aquila chrysaetos canadensis (golden eagle), 145
Alnus sp. (alder), 177 Arabidopsis thaliana (mouse-ear cress), 292–
Alouatta sp. (howler monkey), 342 293
Alveolates, 113 Araceae, 233
Amazon River basin Araneae, 64
biodiversity services, 9–10 Archaea, 111, 119–120, 515
birds, 78 Archboldia papuensis (Archbold’s bowerbird),
butterflies, 69, 75, 76, 78, 79 267, 272–273, 274
extractive reserves, 395 Aristotle, 508
fishery, 9–10 Arizona
habitat fragmentation, 11 butterflies, 73, 74
hydrological cycle, 10 gap analysis of biodiversity, 322
mammals, 78 Arkansas, butterflies, 73, 74
Pacific Ocean linkages, 249, 251–253, 258, Artemia sp. (brine shrimp), 311
516 Arthropods. See also Insects; Crustaceans
Amazonia, 11, 134, 136, 181, 400–401 BIOTA database, 206
Amblyornis macgregoriae (Macgregor’s Ascaris suum (nematode), 310
bowerbird), 268, 270–271, 274 Ascomycetes, 226
Amblyornis sp. (maypole bower builders), 266, Ascomycotines, 116
267, 270–271, 272 Asia
Amblyornis subalaris (streaked bowerbird), 268 birds, 144
American Association of Zoos and Aquaria, 352 wetlands, 129
American Museum of Natural History, 451 Assessment of biodiversity. See Gap analysis;
American Type Culture Collection, 3, 467–471, Measurement of biodiversity
513 Aster pilosus, 192
Amoeba, 113 Atalopedes campestri, 74
Amphibians, 78 Ateles (spider monkey), 342
Amphipods, 365 Athelia bombacina, 117
Amyelois transitella (naval orangeworm), 235 Atitlan, Lake, 128
Anas superciliosa (duck), 153, 155 Atlantic Ocean, 145
Anchovies, 252 Atta cephalotes, 117
Andes mountains, 142, 146, 224, 251–252, 457 Atta sp. (ants), 116
Andropogon virginicus (grass), 192 Attamyces bromatificus, 116
Anophryocephalus (pinniped), 247, 255, 256 Auricularia polytricha, 117
Anous sp. (tern), 151 Australia
Antarctica, insects, 28 birds, 144, 267
Ants climate, 169
attine, 116–117 extinctions, 144
number of species, 8, 31, 97 insects, 7, 48, 49
phylogeny, 117 introduced species, 235
Aotus (owl monkeys), 342 marine species, 86, 96
Apicomplexans, 113 plants, 235
Aplonis tabuensis (starling), 156 reserve selection, 335
Apterostigma sp., 116, 117 vertebrates, 7–8

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Australian Environmental Resources Bemisia tabaci complex (sweetpotato whitefly),

Biodiversity II: Understanding and ProtectingInformation Network
Our Biological (ERIN), 484–487,
Resources 220
http://www.nap.edu/catalog/4901.html 497 Berlese banks, 34
Avena fatua (wild oat), 192 Bicosoecids, 111, 113, 115
Avocado, 178 Big Pine Key, Florida, 87
BIN21. See Biodiversity Information Network
Biodiversity Forum. See National Forum on
B Biodiversity
Babbitt, Bruce, 13, 454, 489 Biodiversity Information Network, 497–498
Baccharis pilularis (coyote bush), 328 Biodiversity losses. See also Extinctions
Bacteria. See also Microbial diversity; specific agriculture-related, 10
bacteria behavioral variability, 263–264, 516
aquatic, 89, 119, 285 coral reefs, 85
autotoxins, 18 ecosystem effects, 154
benefits, 9, 282–284 evolutionary consequences, 132–134, 263
diversity, 281–282 extirpations, 147, 150, 153, 154
evolution, 111, 515 genetic variability, 131, 352, 515
in extreme environments, 13, 119, 285 from human activities, 1, 61, 103, 126–136,
nitrogen-fixing, 17, 283 140–158, 164, 187, 359, 404, 411–414,
spiral, 118 435, 492, 507–512, 515–516
Bacteriophages, 96 pollution and, 10
Bahamas, 87 populations, 131, 147, 515
Baikal, Lake, 127 projected, 136
Baird, Spencer, 13 recovery, 10, 132–133
Bald eagle, 145 Biodiversity Treaty, 412. See also Convention
Banana, 235 on Biodiversity
Barn-owls, 148, 155 Biogeographic realm. See also individual realms
Barranca del Cobre, Mexico, 143 butterfly distribution, 71–72, 77–78, 514
Barro Colorado Island, 11, 334 Biogeography. See also Island biogeography
Basidiomycotines, 116 historical, 243, 245
Bats, 77, 133 Biomass, 7
Bees, 97 Bioremediation, 9, 280, 285. See also Ecological
Beetles (Coleoptera). See also Tropical forest restoration
beetles Biosystematic Database of World Diptera, 206
biological control agents, 221 Biosystematic Information on Terrestrial
collections, 47–48 Arthropods (BIOTA), 206
described species, 29, 97 Biotechnology
discrete assemblages, 38 growth of industry, 280–281, 518
distribution, 28, 32, 45, 47–48, 49, 54 history, 279
diversity, 53, 514 innovations, 279–280
ecological implications of data, 29, 31 microbial diversity, 279, 284–285, 515
ecosystem roles, 31 Birch trees, 177
host specificity, 54, 221 Birds. See also individual species
number of species, 32–33, 49, 51, 53, 56 African passerines, 46
recorded history, 29 butterfly diversity, 76–78, 514
threats to, 61 concordance patterns, 305–308
Belém, Brazil, 75, 79 conservation, 141
Belgium, 58 continental species, 143–146, 515
Beltsville Agricultural Research Center, 221 discovery rates, 158
Bemisia argentifolii (silverleaf whitefly), 220, distribution, 46, 78, 79
227 endemic areas, 141, 142

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extinctions, 11, 60, 61, 64, 139–158, 515– deforestation, 345–346

Biodiversity II: Understanding and Protecting516
Our Biological Resources insects, 48, 49, 75, 76, 79
http://www.nap.edu/catalog/4901.html extirpations, 147, 150, 153, 154 Itatiaia National Park, 75, 76
habitat destruction, 11, 129–130, 142, 144, Poço das Antas Reserve, 348
154, 515 primates, 344, 348, 349, 352, 353
island species, 147–156, 515 Serra do Japi Reserve, 76
number of species, 78 Tijuca Forest, 403–404
parasites, 247 Una Biological Reserve, 346, 353
range contractions, 145 wetlands, 129
restricted-range species, 141, 142 Breeding Bird Survey, 326
threatened species, 45, 126, 154, 518 British Museum of Natural History (London),
tropical forests, 140 44, 47–48, 54, 234, 238, 522
United States, 77, 154 Brunei, insects, 54
waterfowl, 129–130 Bryozoans, cheilostome, 87
wetlands, 130 Bulletin of Zoological Nomenclature, 205
Birds of paradise, 267 Bult, Carol J., 289–299, 518, 521
Bismarck Sea, 366 Bulweria cf. bulwerii (petrel), 151
Black-headed vireo, 146 Bureau of Biological Survey, 455
Blake, Judith A., 289–299, 518 Butterfly diversity. See also individual families
Boletus santanas (fungus), 117 and species
Bolivia biogeographic realm, 71–72, 77–78, 79, 514
insects, 59, 76 bird/mammal diversity and, 76–78, 514
marsupials, 253 geographic variation, 69–72, 78
primates, 348 host-specificity, 53–54
wetlands, 129 insect species estimates from, 48
Yungas-Chaco ecotone, 253, 258 named species, 69, 79, 97
Bombyx mori (silkworm), 311 neotropical, 75–76
Borgia, Gerald, 263–276, 515–516 number of species, 70–71, 78, 231
Borneo, insects, 53, 54, 55, 234 regular colonists, 72–74
Bos taurus (cattle), 310 residents, 72–74
Botswana, wetlands, 129 threats to, 61
Bowerbird evolution. See also individual species United States, 72–74
avenue builders, 266, 267, 269–270 vagrants, 72–74
bowers, 265–271
comparative studies, 264, 266, 515–516
courts, 266, 267, 272–273 C
displays, 265–271, 516 Cacajao (uakari), 342
distribution, 264 Cacaulandia, Rondônia, Brazil, 76
hypothesis, 265–266, 267–273, 516 Cactoblastis cactorum (cactus moth), 235
leks, 271–272 Cadra Walker (almond moth), 234
mate selection, 265 Caenorhabditis elegans (nematode), 291, 293,
maypole-builders, 266, 267, 270–271 310, 311
model, 267–268, 273–274 Cafeteria roenbergensis (marine flagellate), 114
non-bower-building, 271–273 California, butterflies, 73, 74
phylogeny, 266, 267 California Geological Survey, 453
Brachyteles sp. (muriqui), 342, 344 California gnatcatcher, 11, 146
Brassica napus (oilseed rape), 293 Callicebus sp. (titi monkey), 342
Brazil Callimico sp. (Goeldi’s monkey), 342
birds, 142 Callithrix sp. (marmosets), 342, 343, 344, 352
conservation politics, 345–346, 395–396, Cameroon, 58
403–404, 519

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 INDEX / 531

Campephilus imperialis (imperial woodpecker), Chrysauginae, 233

Biodiversity II: Understanding and Protecting143
Our Biological Resources Chrysomelids, 36, 97
http://www.nap.edu/catalog/4901.html Campephilus principalis (ivory-billed Cicadellid bugs, 97
woodpecker), 143, 145 Ciliates, 113
Canada, 157, 222–223 Circulifer tenellus (sugar beet leafhopper), 226
Capitella capitata (polychaete worm), 95 Civilian Conservation Corps, 403–404, 519
Captive breeding and rearing, 141, 351–352, Classification of species
519 approaches, 201–202
Carabids, 97 bacteriological code, 205
Carbon cycle, 283 binomial nomenclature, 204
Carbon dioxide botanical code, 205
bacteria and, 283 butterflies, 69, 79
global warming, 12, 168–170, 188 cataloging, 206
plant response to, 189–190, 192, 193–194 circumscription, 203
Cardueline finches, 148 cladistic, 201
Caribbean Sea, 145, 366 Codes of Nomenclature, 203
Carolina parakeet, 145 common names, 199
Carson, Rachel, 218 DELTA format, 207
Caspian Sea, 179 disagreements, 200–201
Cassava, 225, 517 family-group names, 206
Caterpillars, snout moth, 233 hierarchical, 200
Cavia sp. (guinea pig), 305, 310 history, 204–205
Cebuella sp. (pygmy marmoset), 342, 344 holistic approach, 2
Cebus sp. (capuchin monkey), 342 holotypes, 43–44
Cenozoic era, 164, 165, 167, 171, 173, 175, 318 homonymy, 202–203, 206
Central America identification aids, 207–210, 215–216, 238–
birds, 142, 144 239, 518
butterflies, 72 importance, 199, 517
extinctions, 144 information management, 203, 206–207,
plants, 165 236; see also specific databases
Centrocerus urophasianus (sage grouse), 146, Latin grammar, 205
329 multiple, 201–202
Ceratitis capitata (Mediterranean fruit fly), 209 nomenclature, 199
Cercidiphyllum sp., 177 number named and described, 27, 42–60,
Cetaceans, 247 89–97
Cettia sp. (warblers), 155 original name, 202
Chalcidoid, 97 phenetic, 201
Chendytes lawi (flightless duck), 145 phylogenetic, 201; see also Molecular
Chesapeake Bay, 10, 282 phylogeny; Phylogeny
Chilo sp. (rice borers), 234, 235 primates, 342–343
China. See People’s Republic of China priority, 203
Chiropotes sp. (bearded sakis), 342 problems, 202–203, 238
Chlamydera maculata (spotted bowerbird), 264, rate of description, 444–445
273 registers, 42
Chlorofluorocarbons, 9, 135, 192 resources, 204
Chlorophytes, 111–113 scientific names, 200–201
Cholera, 286 species problem, 203
Chordates, 90 standardization, 205–206
Chordeiles minor (nighthawk), 146 synonymy, 42–43, 202–203, 206, 220, 238,
Christmas Island, 149, 150 239
Chromophytes, 111 tags, 199–200

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 532 / INDEX

two-key, 201–202 Population Viability Analysis, 350

universal
Biodiversity II: Understanding and Protecting data dictionary,
Our Biological 204
Resources preventive approach, 360
http://www.nap.edu/catalog/4901.html valid name, 202 primates, 344, 345, 349–353, 518–519
zoological code, 205 priorities, 76, 141, 154, 258, 296, 344, 357,
Clayton, Rebecca, 289–299, 518 359, 367, 514
Climate. See Global climate change Rapid Assessment Program Team, 31
Cliniodes Guenée (snout moth), 234 scientific methods, 350, 357, 518–519
Clytorhyncus vitiensis (monarch), 155 training, 157, 350
Coastal zones Conservation International, 349
degradation, 84, 100 Conserved wildlands
marine archaebacteria, 120 management, 424–430, 519–520
species diversity, 88, 89, 91–93 perceptions, 411–413
surface area, 88–89 use, 427–430
tropical, 88, 89–92; see also Coral reefs Consortium for Systematics and Biodiversity,
Coastal sage scrub habitat, 11 3, 32, 513, 522
Cocconeis placentula (diatom), 22 Consortium of State Biological Surveys, 454,
Coconut, 235 522
Coleophora laricella (larch casebearer), 220 Consumption, human
Collections, 43–44, 45, 47–48, 359. See also net terrestrial primary productivity, 83
Research collections Continents, extinction of birds on, 143–146,
Collembola, 58 515
Collocalia sp. (swift), 152, 155 Convention on Biological Diversity, 394, 472
Colombia Cook Islands, 149, 150, 153
birds, 78, 139, 141, 146 Coprinus cinereus (fungus), 117
epidemics, 286 Coral reef biodiversity. See also specific reefs
insects, 48, 49, 76, 78 and species
primates, 342 complexity, 83
wetlands, 139 components, 87
Columbus, Christopher, 399, 519 conservation, 357, 362, 366–367
Colwell, Rita R., 279–287, 515, 518, 520 cryptofauna, 87
Conestoga River Basin, 17 described species, 91–94, 102, 514
Conifers, 15 distribution patterns, 99, 357–358, 514
Connecticut State Geological and Natural documentation, 361
History Survey, 453 endemism, 358–359
Conservation. See also Captive breeding estimates, 85–93, 94
birds, 141, 154, 157 extinctions, 85, 284, 359, 514
characterization, 203–204 global, 88
coral reefs, 357, 359, 366–367 hotspots, 130
ecosystem approach, 333–334 known vs. unknown, 94, 96–97
education strategies, 350, 352–353 rain forests compared to, 86, 87, 88, 91–93,
gap analysis, 333–334, 518 100–101, 514
genetic diversity, 343 size of species, 97–100, 102–103, 519
habitat fragmentation, 11 status, 84–85
hotspots, 128 taxonomy, 360
INBio approach, 199 threats to, 84
information management and networking, value, 83–84
349 Coral reefs
insects, 79, 514 black band disease, 100
international cooperation, 352, 519 bleaching, 84
Population and Habitat Viability Analysis, hypersalinization, 13
350, 353 reef-building species, 95

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 INDEX / 533

site selection, 366–367 Data collection. See also Information

surface
Biodiversity II: Understanding and Protecting Ourarea, 88–89 Resources
Biological management
http://www.nap.edu/catalog/4901.html Corn, 8–9, 143, 222, 223, 224, 234, 235, 375 bar-code labels, 236
Cornell University, 214 spreadsheet templates, 37
Corvus corax (raven), 145 field data sets, 34–35
Corvus coronoides (crow), 269 sampling regimes, 32–33
Corvus ossifragus (fish crow), 145 Databases. See also specific databases
Costa Rica biodiversity, 294–295
birds, 142 Diptera, 206
butterflies, 75 fruit fly, 207, 209–210
Guanacaste Conservation Area, 32–33 genetic sequence, 111, 290, 291–292, 294–
La Selva field station, 75 295, 518
snout moths, 232, 233, 235–239 identification aids, 207–210, 518
sustainable development, 430 molecular, 116–117
Cover, Stefan P., 449 RNA sequences, 111
Crabs, 95 terrestrial arthropods, 206
Cracraft, Joel, 435–446, 517, 520–521, 522 Davies Reef, 365
Crambidae, 234 DDT, 218
Crambinae, 235, 238 Declio gigas (kookaburra), 269
Craneflies, 18 Deep sea
Cretaceous period, 251, 253, 425 extinctions, 172–173
Cretaceous/Tertiary boundary, 181 species diversity, 86, 95, 96, 366
Cricetulus longicaudatus (hamster), 311 temperatures, 171
Crinoids, 365 Definition of biodiversity, 1, 15
Crops Deforestation, 129
germplasm, 224, 227 control, 390–391
pest resistance, 8–9, 224 effects, 285, 348
UV radiation effects, 193–194 erosion, 149
Crustaceans extinction, 52, 140, 149
amphipod, 96, 365 habitat loss, 1–2, 335–336
coral reef, 87, 91 oceanic islands, 149
decapod, 87, 95 projections, 135
deep sea, 86 rates, 11, 133, 135
described, 96 reversibility, 402–403
extinctions, 101 tolerant species, 152
isopod, 96 transportation infrastructure, 398–399
stomatopod, 98–99 tropical, 1–2, 11, 133, 140
Cryptomonads, 111–112, 115 Dendroica cerulea (cerulean warbler), 146
Csuti, Blair, 321–340, 514, 518, 520, 521 Dendroica kirtlandii (Kirtland’s warbler), 146
Cuba, 143 Dendroica petechia (yellow warbler), 157
Curculionids, 97 Desertification, 135
Cucurbitaceae, 233 Detritivores, 18
Curlews, 146, 152, 153 Diaphania Stephens (snout moth), 233
Curtis Prairie, 384 Diatoms, 22–23, 111–112
Cyanobacteria, 115, 119, 283 Diatraea saccharalis Fabricius (sugarcane
Cyphomyrmex sp. (ant), 116, 117 borer), 235
Dicaeum quadricolor (Cebu flowerpecker), 139–
140
D Didemnidaceae, 284
Dams, 129, 130 Didemnins, 284
Darwin, Charles, 265, 357, 508 Didunculus sp. (pigeon/dove), 155

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 534 / INDEX

Dietz, James M., 341–356, 514, 518–519, 521 Ecology, historical, 243, 245
Dimethyl
Biodiversity II: Understanding and Protecting Oursulphide,
Biological283Resources Ecosystem management, integrated approach,
http://www.nap.edu/catalog/4901.html Dinoflagellates, 111, 113, 115 13
Dipodomys deserti, 326 Ecosystems
Diplomonads, 111 classifying and mapping, 322–326
Diptera (flies), 48, 305–309 indicators of change, 10, 29, 31, 519
Dispersal, 12, 98, 101 niche concept, 326–327
Distribution of species. See Gap analysis; perspectives on biodiversity, 9–10, 17–24
Geographic distribution and range Ecotourism, 84, 391, 427–429
DIVERSITAS network, 416–417, 436 Ecuador
Doves, 148, 149, 150, 151, 152, 153, 155 birds, 141, 142
Dragonflies, 78 epidemics, 286
Drosophila melanogaster (fruit fly), 302, 310, insects, 48, 76
311 Edward, Lake, 127
Drought, 190–191, 192 Egretta sacra (heron), 151, 155
Drugs and pharmaceuticals Eiseley, Loren, 383
analgesics, 284 El Niño Southern Oscillation, 285, 286
antibiotics, 9, 284 El Salvador, 396
antihypertensives, 9 Elachertus sp. (parasitic wasp), 220
antileukemic, 284 Elasmobranchs, 249, 251–253, 258
aspirin, 9 Eliade, Mircea, 380
plant-derived, 9, 84, 134, 279, 280, 284–285, Elm trees, 177
391 EMBL database, 111, 290, 303
Dry Tortugas, 87 Endangered species. See Threatened and
Ducks, 145, 148, 152, 153, 155 endangered species
Ducula sp. (pigeons, doves), 151, 153, 155 Endangered Species Act, 333
Endemic bird areas, 141, 142
Endemism
E assessment, 59
Eagles, 148 birds, 139, 141
Easter Island, 149–150 coral reef species, 358–359
Eclectus sp. (parrot), 155 and extinction, 100
Ecological processes, and local diversity, 100– genetic diversity, 131
101 host-parasite systems and, 248, 257–258
Ecological restoration lakes, 125–127, 515
authenticity, 379–381 marine vs. terrestrial, 86
community building, 383–386, 519 moths, 233
conservation role, 374–375, 381, 519 wetlands, 129, 130–131
definition, 372–373, 374 Entomological Collections Network, 206
estuary, 378 Environmental monitoring, 29, 345–347, 519
experience, 382–383 Eocene epoch, 167–170, 171–173, 175, 176–181
forms, 372–374, 375, 379 Eopsaltria sp. (whistlers, robins), 155
impediments, 369–370 Ephemerella sp. (mayfly), 22–23
potential, 374, 427 Epimachus albertsil (brown sickelbill), 267
prairies, 373, 375–376, 378–379, 381, 384 Epipaschiinae, 234
preservation, 372–373 ERIN. See Australian Environmental Resources
principles, 371 Information Network
process, 378, 381–382 Erosion, 2, 84, 127, 149
quality issues, 375–379 Erwin, Terry L., 8, 27–40, 513–514, 520
successional, 379 Escherichia coli (bacteria), 291
wetlands, 377–378 Estuarine salt flats, 28

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 INDEX / 535

Ethiopian realm, 48 estimation/prediction, 2, 60, 62–63, 136,

EtiellaOur
Biodiversity II: Understanding and Protecting sp. (snout moth),
Biological 234, 235
Resources 141, 350
http://www.nap.edu/catalog/4901.html ’Eua, 149, 152, 154, 155–156 freshwater species, 126, 128
Eubacteria, 118 geographic range, 101–102, 103
Eukaryotes, 111–114, 115, 118, 515 global warming, 172–173, 176–181, 182, 516
Euonymus japonica (Japanese evergreen human-caused, 103, 132, 139–158
euonymus), 221 insects, 41, 52, 60–61, 101
Euplopiscium fishelsoni (surgeonfish symbiont), island, 147–157
116–118 marine, 85, 99–103, 359, 514, 516
Europe mass, 45, 102, 132, 133, 181
birds, 144 naturally occurring, 140, 147
fish, 128 Paleocene/Eocene, 176–181
insects, 69 plants, 176–181, 187
Eutrophication, 84 rates, 12, 45, 60–64, 102, 135–136, 140, 146,
Evolution, 86. See also Bowerbird evolution; 147, 425, 514
Historical reconstruction recovery, 133, 179
biodiversity losses and, 132–134 spasms, 128, 132, 133
body size, 97–103, 118 tropical species, 102
coral reefs/rain forest similarities, 100–101 vulnerability, 99–100, 102, 103, 131–132,
coevolution, 116, 226, 246, 247–248, 515 139, 147, 191
comparative molecular studies, 291–292 Extreme environments
divergence of species, 311–318, 341–342, biodiversity, 119–120, 188, 285
516 plant response, 189
eukaryotes, 113–114, 118
eukaryotic crown, 113, 118
genetic markers, 110–111 F
inferring relationships, 109, 243, 245, 266– Family planning, 135
267, 291, 296, 301, 317, 436 Farr, David F., 475–490, 517, 518, 521
of plastids, 114 Fatty acid derivatives, 16
primary lines of descent, 111, 515 Fauchald, Kristian, 366
of primates, 341–342, 347 Fertilizers, 10, 13, 17
rates of change, 111, 133, 316 Fields, Chris, 289–299, 518
stramenopiles, 114–115 Figueres, José Maria, 430
Exotic species. See Introduced species Fires, 130, 189, 373, 381
Expressed Gene Anatomy Database (EGAD), Fish
294–295 cichlids, 127, 128, 515
Expressed Sequence Tags (ESTs) coral reef, 83, 87
applications, 290–291 distribution in riverine systems, 18–22
database, 294–295 freshwater, 89, 126–128
molecular marker design, 292–293 marine, 89
multiple sequence alignment, 293–294, 301; sampling, 87
see also Nuclear-gene-sequence character threatened and endangered, 126
assessment wetlands, 130
Extinctions Fisheries
background, 102 biodiversity services, 9–10
birds, 60, 61, 139–158, 515–516 collapse, 13
body size of species, 99–101, 103 coral reef, 87
causes, 11, 52, 61, 99–102, 147, 180, 181– overfishing, 127, 130
182, 187 Fishing, 142
continental, 143–146 Flies, 31, 97
ecosystem effects, 157 Flightless geese, 148

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Flightless rails, 148, 149, 152, 154 Gallicolumba sp. (pigeons, doves), 151, 153,
Flood control
Biodiversity II: Understanding and Protecting projects,Resources
Our Biological 13, 126 155
http://www.nap.edu/catalog/4901.html Floods/flooding, 74 Gallinula sp. (gallinule), 155
Florida Gallirallus sp., 149, 151, 153, 155
birds, 77 Gallus gallus (bird), 310
butterflies, 73, 74 Gap analysis
ecosystem management, 13 areas managed for biodiversity maintenance,
coral reefs, 87, 362 328, 331–333
Florida Keys National Marine Sanctuary, 362 classifying and mapping ecosystems, 322–
Foggers/fogging, 33–34, 50, 53, 54, 59 326
Food webs, 17–24, 113, 157, 249, 257 conservation, 333–334, 345, 518
Ford, Henry, 397, 519 history, 322
Forests. See also Tropical forests reserve network selection, 334–337, 346–
burning, 12 347
old growth, 189 species distribution maps, 326–330
species composition, 188 steps, 322
Forminafera, 171, 172–173 technology, 321–322, 518
Forseth, Irwin N., 187–196, 516 Gatun Lake, 11
Fossils Geese, 148
climate record, 164–167, 168, 169, 171, 177– GenBank, 111, 290, 303
178, 188–189 Gene therapy, 282
primate, 342 General Agreement on Tariffs and Trade, 428
Foulehaio carunculata (honeyeater), 156 Genetic diversity
France, 58 adaptability, 132
Fregata sp. (frigatebird), 149, 151 losses, 131, 132, 515
Fregetta grallaria (storm petrel), 151 measurement of, 110–113; see also Molecular
Freshwater ecosystems. See also Riverine phylogegy
systems population size, 139
loss, 126, 515 Genetic sequences. See Molecular phylogeny;
species, 89, 90, 249, 251–253, 515 Nuclear-gene-sequence character
Friedlander, Timothy P., 301–320, 516, 518 assessment; Rapid gene discovery
Frogs, 10, 307–309 concordance study, 302, 305–308
Fruit Fly Expert System, 207, 209–210 databases, 111, 290, 291–292, 294–295
Fulmars, 149 mitochondrial DNA, 266, 267, 343, 516
Fundação Biodiversitas, 353 rRNA sequence analysis, 110–112, 114, 116–
Fungi, 18 117, 118, 119
biological control agents, 226 Geographic distribution and range. See also
cultures, 468–470 Biogeographic realm
Imperfecti, 116 body size, 98–100, 102–103
information management, 476–484 and extinction, 101–102, 103
number of species, 90, 282 knowledge of, 45–47
phylogeny, 117 latitudinal trends, 54, 69, 71, 74, 91
plant ratio, 49–50 mapping, 326–328
symbionts, 116 primates, 343–345
Fungiid corals, 364 ranges, 48–49, 54
Geographic information systems (GIS), 321,
322–323, 345–347, 518
G George, Lake, 127
Galapagos Islands, 127, 147 Georgia
Galleriinae, 233 birds, 77, 78
butterflies, 73, 78

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 INDEX / 537

Germplasm collections, 131. See also Research Guadalupe River, 18, 19, 24
Biodiversity II: Understanding and Protectingcollections, livingResources
Our Biological Guam, 149, 365–366
http://www.nap.edu/catalog/4901.html Glaciers, 179, 181 Guanacaste Conservation Area, Costa Rica, 32–
Glaphyriinae, 234, 237–238 33
Gliocladium sp. (fungus), 226 Guatemala, 49, 128
Global climate change Gulls, 148, 149
carbon dioxide, 188, 195 Guyana, deforestation, 11
carbon isotopes, 173 Gygis microrhyncha (tern), 151
disturbance regimes, 189 Gymnogyps californianus (California condor),
ecological restoration, 375–376 144, 145
effects, 12, 84, 134, 135, 173–175, 187, 195, Gymnorhina tibicen (Australian magpie), 267
255, 257, 258
environmental stresses, 190–192, 516
Eocene epoch, 167–170, 171 H
equable climate paradox, 167–170 Habitat loss. See also specific habitats
extinctions, 172–173, 176–181, 182, 516 biodiversity, 11
general circulation models, 163, 167–168, birds, 11, 129–130, 142, 144, 154
181, 187–188, 516 deforestation, 1–2
greenhouse gases, 12, 187, 195, 283 extinctions, 61, 142, 144, 154
Holocene deglaciation, 163, 179 fragmentation, 11, 102, 135, 143, 146, 375
host-parasite systems, 255, 257 rates, 86
introduced species, 194–195 Habitat monitoring, primate, 345–347
leaf physiognomy, 164–167, 168, 169, 171 Haemonchus contortus (nematode), 310
nearest living relative, 164 Hakalau Forest National Wildlife Refuge, 322
oxygen isotope studies, 166, 171 Halcyon sp. (kingfisher), 152, 153, 155
Paleocene-Eocene boundary, 163–164, 172, Hamsters, 306, 307–309
176–181, 516 Hanta virus, 285–286
paleoclimate reconstructions, 164–167, 170, Hapalia machaeralis (snout moth), 235
181–182, 188–189 Haptophytes, 111–113, 114
plant response, 188–189, 194–195 Hargrove, Gene, 380 n.1
Pliocene-Pleistocene glaciations, 255, 256, Hawaii Biological Survey, 454
257, 516 Hawaiian honeycreepers, 7, 148
proxy data, 163, 164, 166, 188 Hawaiian islands, 11, 86, 147, 148, 322, 366,
research approach, 182 518
response of species, 143, 179, 188–189, 257, Hawks, 148, 155
258, 516 Health, human, biodiversity losses and, 285
Terminal Paleocene Event, 170–176, 179 Hedylepta accepta Butler (sugarcane leafroller),
Global Environment Facility, 126, 134 235
Glyphyriinae, 233 Heliconius sp. (butterfly), 53–54
Golden-cheeked warbler, 146 Heliothis virescens (tobacco budworm), 219
Golden Lion Tamarin Conservation Program, Helminths. See Parasitic helminths
349 Hemiptera, 55, 97
Gomphonema olivaceum (diatom), 22 Henderson Island, 149
Gray birch, 192 Henry Greene Prairie, 378–379
Great auk, 145 Henry, Joseph, 452
Great Barrier Reef, Australia, 87, 284, 362, 364 Herons, 148, 150, 151, 155
Great Lakes, 127 Hesperiidae, 70, 79
Greater prairie chicken, 146 Heterotrophs, 111–113, 114, 115
Greece, 131 Hinkle, Gregory, 109–122, 514–515
Greenhouse gases, 12, 169, 187, 195, 283 Histoplasmosis, 113
Greenland, 78 Historical contexts of biodiversity, 509–512

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Historical reconstructions tropical wetlands, 128–131

Pacific
Biodiversity II: Understanding and Protecting Ourorigin of Amazon
Biological River, 249, 251–
Resources Hot springs, 13, 96, 119, 285
http://www.nap.edu/catalog/4901.html 253 Human Genome Project, 61, 296, 512, 518
paleoclimate, 164–167, 170, 181–182, 188– Humphrey, Phil, 214
189 Hunting, 61, 139, 141, 142, 144, 348–349
parasites and, 246–257, 516 Hutchinson, G. Evelyn, 508–509
Pleistocene marine refugia, 255–257 Hydrilla, 235
principles and applications, 245–246 Hydrological cycle, 10
transantarctic connections, 253–254 Hydrothermal vents, 94–95
Hoberg, Eric P., 243–261, 515, 516 Hymenoptera, 48, 97
Holarctic realm Hypocrea gelatinosa (fungus), 226
host-parasite systems, 255, 256, 257, 258
species richness, 78
Holocene epoch, 179 I
Homo sapiens (human), genetic concordance Ibises, 148
study, 291, 303–315 Ichneumonoid, 97
Homoptera, 97 Ictinia misisippiensis (Mississippi kite), 145
Honduras, 396 Idaho
Honeyeaters, 156 butterflies, 73, 74
Host-parasite systems. See also Parasitic gap analysis of biodiversity, 322, 328–333,
helminths; Parasitic wasps; Parasites 336, 337
agricultural, 221, 226 Identification of species, aids, 207–211, 215–
biodiversity probes, 248–249 216, 238–239, 518
Brooks Parsimony Analysis, 248 Illinois, butterflies, 73, 74
caterpillar-plant, 233 Illinois Natural History Survey, 453, 454
climate change, 255, 257 India, insects, 48, 49
coevolution, 116, 226, 246, 247–248, 249, Indian Ocean, bird extinctions, 145
515, 516 Indonesia
colonization (host-switching), 248, 249, 255– birds, 141, 145, 515
256, 257 Department of Science, 55
conceptual foundations, 247–248 insects, 48, 49, 55–57, 233–234
Fahrenholz’s Rule, 246 Project Wallace, 55
freshwater rays-helminths, 249, 251–253 Indus Delta, Pakistan, 129
host specificity, 53–54, 221, 246, 248, 255, Industrial ecology, 9
257 Information management. See also Data
Manter’s Rule, 246 collection; Databases; specific networks
marsupial-tapeworm, 253–254, 516 analysis of raw data, 480–481, 485
parascript studies, 248 availability of information, 487–488
phylogenetic methodologies, 247, 248, 257– challenges, 488–489, 521
258 classification of species, 203, 206–207, 236
pinniped-helminth, 255–257, 516 compilation of data, 477–479, 484
predictable nature, 246 data entered, 479–480, 485
research programs (current), 248–249 data output, 481–484, 485–486
seabird-helminth, 255–257, 516 fungi, 476–484
Hot spots international models, 497–498, 521
concepts, 125–126, 357–358, 362–363 primates, 349
coral reefs, 284, 362–363 specimen locality records, 326
extinctions, 62, 63 U.S. National Biodiversity Information
identification, 257–258 Center, 491–497, 498–503
prairies, 379 Insects. See also individual families and species
tropical lakes, 126–128 agricultural pests, 218, 219, 220, 517

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 INDEX / 539

canopy/ground ratios, 55 marine, 366–367

classification,
Biodiversity II: Understanding and Protecting 43 Resources
Our Biological priorities, 360, 424–425, 442
http://www.nap.edu/catalog/4901.html described species, 27, 43, 91, 96–97 small organisms, 424–425
distribution, 48, 70–76 strategies, 366–367
extinctions, 41, 60–61, 64, 101 Invertebrates
host-specific, 51–53 coral reef, 83, 86–87, 92–93, 97–100, 358,
importance, 27–28 362
knowledge about biodiversity, 7–8 freshwater, 89–90
number of species, 27, 29, 32, 55–56, 90, hotspots, 128
231, 513–514 macro-, 18–22, 89–91
paleobiology, 29, 101 marine, 86, 89–90, 96, 102, 364, 366
plant resistance, 9, 15 number of species, 360
riverine systems, 18–22 Iowa, butterflies, 73, 74
temperate forests, 49 Iquitos, Loreto, Peru, 76
threatened status, 46–47 Irrigation, 129
tropical forests, 27, 49 Ishigaki island, 87
Instituto Nacional de Biodiversidad (INbio), 33, Island biogeography, 88, 135, 148, 334, 357,
37, 236, 240, 461 358, 365, 367, 514
International Code of Zoological Nomenclature, Islands, oceanic
205 birds, 142, 145, 147–157, 515
International Commission of Zoological insects, 48
Nomenclature, 206 species losses, 11, 147–153
International Congresses of Dipterology, 206 Itatiaia National Park, Brazil, 75, 76
International cooperation Ivory Coast (Africa), 130
microbial biodiversity, 472–473 Ixobrychus exilis (least bittern), 140
primate conservation, 352
sustainable development, 426
systematics and biodiversity science, 437,
J
521–522 Janzen, Daniel, 32, 376, 411–431, 513, 519–520
International Fund for Agricultural Japan, 48, 49, 281, 366
Development, 225 Jaru, Rondônia, Brazil, 76
International Union for the Conservation of Jefferson, Thomas, 401, 512
Nature, 45–46 Jim’s Black Pool, 119
International Union of Biological Sciences, 206, Jonglei Canal, 130
436 Jordan, William R., III, 371–387, 513, 519, 520
Intertidal zones, 28, 86 Joshua Tree National Monument, 326
Introduced species Jurassic Park, 13
agricultural pests, 220, 517
control, 426–427
and extinctions, 11, 61, 139, 141–142, 149,
K
515 Kafue Flats, Zambia, 129
fish, 127, 139 Kagus, 148
global warming and, 194–195 Kangas, Patrick, 389–409, 512, 519
plants, 194–195, 235 Karoo, 235
Inventories. See also Surveys, biodiversity; Katsura tree, 177
specific inventories Kemp’s ridley sea turtle, 95
dissemination of information, 417–418 Kentula, Mary, 378
documentation, 442–443 Kenya, 219
elements, 32 Kerlavage, Anthony R., 289–299, 518, 521
information management, 421–422, 443, 518 Kern River, 379
information needs, 414–420 Kiester, A. R., 337

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Kingfishers, 152, 153, 155 Macrops eugenii (tammar wallaby), 293

Kissimmee
Biodiversity II: Understanding and Protecting Our River, 13 Resources
Biological Madagascar
http://www.nap.edu/catalog/4901.html Kusler, Jon, 378 insects, 48, 49
resource economics, 12
Madang Lagoon, Papua New Guinea, 357, 363–
L 366, 367, 519
Labrador duck, 145 Madre de Dios, Peru, 75
Labyrinthulids, 111, 115 Magdalena River, 251–252, 258
Labyrinthuloides minuta (slime net), 114 Maine
Lady beetles, 221 birds, 77
Lagoons, 84 butterflies, 73, 74
Lagothrix (woolly monkey), 342, 349 Malaria, 113, 285, 293
Lake Forest, Illinois, 386 Malawi, Lake, 127, 128
Lakes, tropical, hotspots, 126–128 Malaysia, insects, 48, 49, 71–72
Lalage sp. (triller), 155 Mali, 129
Lanao, Lake, 128 Mammal diversity
Land-use by biogeographic realm, 78
changes, and extinctions, 61 and butterfly diversity, 77, 78
planning, 323 extinction rates, 64
sustainable, 395–396 parasites, 113
LANDSAT Thematic Mapper satellite imagery, threatened species, 45, 64, 126
324–326, 346 Manduca sexta (tobacco hornworm), 310
Lanius ludovicianus (loggerhead shrike), 146 Mangaia, 149, 150, 153
Latin America, butterflies, 71 Manter, Harold, 243
Leaf beetles, 35, 226 Manter’s Rules, 246
Legumes, 17, 178, 235 Mantis shrimps, 97, 98, 99
Leontopithecus (lion tamarins), 342, 343, 344, Manu National Park, Peru, 75–76
348, 351–352, 353, 518 Marine ecosystems. See also Coral reefs
Lepiota procera (ant), 116, 117 biodiversity, 8, 86, 89, 101, 359–360
Lesser prairie chicken, 146 documenting biodiversity, 361
Lewis and Clark Expedition, 512 extinctions, 101–102
Liberia, 71–72 global warming, 171
Lima beans, 235 helminthic parasites, 251
Linnaeus, Carolus, 42, 204, 450, 508, 517 integrated studies, 358–359
Linostinae, 233 number of species, 90
Linstowia (tapeworm), 253–254 research priorities, 361–363
Littler, Mark and Diane, 366 protected areas, 359
Lizard Island, 365 species turnover, 58–59
Lonicera japonica (Japanese honeysuckle), 194 tropical ecosystems, 361
Loricifera, 94–95 Marmota caligata (hoary marmot), 329
Louisiana, 73, 74 Marquesas Islands, 149, 150
Louisiana Purchase, 400–401, 512, 519 Marsupials, transantarctic, 253–254, 516
Lovejoy, Thomas E., 7–14, 214, 500, 513, 520 Maryland, butterflies, 73, 74
Loxostege frustralis (webworm), 235 Maspar Computer, Inc., 294
Luehea seemannii (evergreen tree), 50 Massachusetts
Lycaenidae, 79 birds, 77
butterflies, 73, 75
Mayan civilization, 396–397, 519
M Maytenus sp., 226
MacArthur Foundation, 126 McKelvey box classification, 391–394
Machaerium sp. (legume), 178 Mealybugs, 219–220, 225, 517

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 INDEX / 541

Measurement of biodiversity. See also Models/ Midilinae, 233, 234

Biodiversity II: Understanding and Protectingmodeling
Our Biological Resources Miller, Douglass R., 217–229, 513, 517, 520
http://www.nap.edu/catalog/4901.html extinction predictions, 60–64 Mining, 130
extrapolation from samples, 50–57 Miocene epoch, 251, 255
geographic ranges, 48–49, 54, 99–100, 326– Mississippi River drainage area, butterflies, 73,
328 74
island biogeography concepts, 88, 90–91, 93 Mites, 58, 96–97
Linneaus, 42–44, 508 Mitter, Charles, 301–320, 516, 518
molecular techniques, 109–120, 267, 291– Mittermeier, Russell, 341
292, 317 Moas, 148
number of species, 47–60, 70–76, 89–93 Models/modeling
ratios of known-to-unknown fauna, 47–50, bowerbird evolution, 267–268, 273–274
96–97 climate change, 163, 167–168, 181, 187–188,
scaling, 38, 91 516
Medicines. See Drugs and pharmaceuticals species estimates, 57–60
Mediterranean Sea, 145 Molecular clock, 113 n.1
Mehrhoff, Leslie J., 447–465, 512, 521, 522 Molecular phylogeny, 109–120, 342, 514–515,
Melanesia, 145, 146, 147, 149 518. See also Nuclear-gene-sequence
Meleagris crassipes (turkey), 145 character asessment
Meliphaga lewinii (Lewin’s honeyeater), 269 Mollusca, 64, 86, 87, 94, 96, 101, 102, 365–366
Melosira variens (diatom), 22 Moluccas, northern, 142
Megamouth shark, 95 Monarchs, 152, 155
Megapodes, 148, 155 Montastrea annularis (reef-building coral), 95
Megapodius sp. (megapode), 155 Moonseed, 178
Merriam, C. Hart, 13 Moorea, 87
Mesocricetus auratus (hamster), 311 Mosquitos, 78
Methane, 283 Moth borers, 221
Mexico Moths. See also Snout moths
birds, 141, 143 attributes for biodiversity studies, 231, 234
corn, 8–9, 143, 224 concordance studies, 307–309, 318
deforestation, 143 number of species, 59
insects, 48, 49, 74 pests, 218, 219, 221
wetlands, 129 Mount Desert Island, Maine, 15
Mice, 306, 307–309 Mouse opossum, 253
Microbial diversity. See also Bacteria; Fungi; Mrakia frigida (ant), 117
Viruses Mullis, Kary, 13
and biotechnology, 279, 284–285, 515 Mus musculus (domestic house mouse), 293,
ecological importance, 282–284 310, 311
international cooperation, 472–473 Museum of Comparative Zoology, Harvard, 452
measurement, 470–472 Museums. See Natural history museums;
number of species, 282 Research collections; specific museums
relation to macroorganismal biodiversity, Musotiminae, 237
285–286 Mussels, 126
repositories, 467–470, 521 Mutations, 113 n.1
Micronesia, 147 Mycotoxins, 226
Microorganisms. See Algae; Bacteria; Microbial Myers, Norman, 125–138, 514, 515, 519, 520
diversity; Viruses and procaryotes; Myiagra sp. (monarch flycatcher), 152, 155
specific organisms and species Myiarchus cinerascens (ash-throated flycatcher),
Micropygia heana, 151 331
Microsporidians, 111 Myzomela cardinalis (honeyeater), 156

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 542 / INDEX

N New Mexico
Biodiversity II: Understanding and Protecting Our Biological Resources birds, 77
http://www.nap.edu/catalog/4901.html Nacoleia octasema (snout moth), 235 butterflies, 73, 74
Names. See Classification of species New synthesis, 511
Nanochlorum eukaryotum (chlorophyte), 118 New systematics, 508, 511
National Biological Survey (Service), 13, 321, New York State Museum, 11
324, 426, 454–456, 521, 522 New York State Survey, 453, 454
National Center for Biotechnology Information New Zealand, 48, 165
(NCBI), 293 Niger Delta, Mali, 129
National Forum on BioDiversity, 2, 31–32, 296, Nile River, 130
341, 389, 404 Nitrogen, use by plants, 189
National Marine Fisheries Service Systematics Nitzschia linearis (diatom), 22
Laboratory, 366 Nomenclature. See Classification of species
National Museum of Natural History, Nongovernmental organizations, 349. See also
Washington, DC, 11, 234, 236, 238, 240, specific organizations
451, 513, 522. North America
National Oceanic and Atmospheric birds, 144, 145
Administration, 324 climate, 169, 171, 175
National Science Board Task Force on east coast, 86, 96
Biodiversity, 89 extinctions, 144, 145, 515
National Science Foundation, 350, 423, 459 floral immigration patterns, 180
National Wetlands Inventory, 324 forests, 188
National Zoological Park, 342 insect pests, 220, 223
Natural Heritage Programs, 333 plants, 165, 171, 175, 176, 179, 180
Natural history museums. See also Inventories; terrestrial arthropod database, 206
Research collections North American Free Trade Agreement, 428
funding, 522–523 North Carolina Biological Survey, 454
history, 449–453 Nuclear-gene-sequence character set
role, 521 assessment
types, 448–449 data, 303–305
Natural selection, 132 dopa decarboxylase, 302, 304, 309–313, 316
(The) Nature Conservancy, 322, 328, 333, 349 elongation factor-1α, 302, 304–305, 307–
Nearctic realm, 48 309, 311, 313, 315–316, 317–318
Needlefish, 252 elongation factor-2, 302, 306, 311, 313, 315,
Nematoda, 58, 96, 221, 223, 244, 291, 305–308 316, 317
Nematodirus battus (nematode), 223 GAP analysis program, 303
Neotropical realm phosphoenolpyruvate carboxykinase, 302,
beetles, 31, 48; see also Tropical forest 305, 310, 312, 313–315, 316
beetles phylogenetic analysis, 308–309
birds, 78 RNA polymerase II, 302, 304, 306, 310, 312,
butterflies, 75–76, 77, 78, 79 315, 316, 317
mammals, 78 selection of sequences, 301–303
moths, 233 test phylogeny, 305–308
Nesoclopeus woodfordi (flightless rail), 149 Numenius americanus (long-billed curlew), 145
Nesofregetta fuliginosa (storm petrel), 151 Numenius borealis (Eskimo curlew), 145
Neurophyseta Hampson (snout moth), 237 Numenius tahitiensis (bristle-thighed curlew ),
New Britain, 142 146, 152, 153
New Coke, 12 Nymphalidae, 75, 79
New Guinea, 142, 145, 270 Nymphulinae, 233, 235
New Ireland, 142 Nycticorax sp. (heron), 155

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 INDEX / 543

O Paleocene/Eocene boundary, 176–181, 516

Biodiversity II: Understanding and Protecting Our Biological Resources Paleozoic era, 101
http://www.nap.edu/catalog/4901.html Oak (Quercus sp.), 54 Palms, 164, 165
Oaxala Declaration, 426 Panama
Oceania, 147–148, 154 birds, 78, 142
Oceans and seas. See also Coastal; Deep sea; coral reef taxa, 87, 91
Marine; Open ocean; individual oceans insects, 54, 71–72, 75, 78
and seas Panama Canal, 11
surface area, 88 Pantanal Swamp, Brazil, 129–130
Octocorals, 364 Pantoja, Loreto, Peru, 76
Oculina arbuscula (coral), 87 Papasula abbotti (Abbott’s booby), 149, 150,
Odontiinae, 234 151
Ohio Biological Survey, 454 Papilionidae, 70, 75, 79
Oil extraction, 128 Papua New Guinea, 48, 49, 141, 363–366
Okavango Swamp, Botswana, 129 Papyrus, 130
Okechobee, Lake, 13 Paraguay, 129
Okhotsk, Sea of, 255 Paraguai River, 129–130
Okinawa, 149 Parana River, 251–252, 258
Oklahoma Biological Survey, 454 Parasitic helminths
Oleander, 178 described species, 244
Olson, Storrs, 11 food webs, 249
Omiodes Guenée (snout moth), 238 in freshwater rays, 249, 251–253
Onchocera volvulus (nematode), 311 historical reconstruction, 239–258
Oomycetes, 111–112, 114, 115 host specificity, 244
Open ocean, bacteria and viruses, 119, 282 in marsupials, 253–254
Ophyrys sp. (orchids ), 16 in pinnipeds, 255–257
Opler, Paul A., 69–82, 514, 520 in seabirds, 255–257
Opuntia Mill (prickly pear cactus), 235 Parasitic wasps, 220, 222
Oranges, 235 Parasites. See also Host-parasite systems
Oregon historical probes, 244
butterflies, 73, 74 of mammals, 113, 223–224
gap analysis of biodiversity, 322 Parrots, 148, 149, 150, 152, 153, 155
Orinoco River, 251–252 Partnership for Enhancing Expertise and
Ornithologists, 157 Taxonomy, 423
Oryctolagus cuniculus (rabbit), 311 Parus rufescens (chestnut-backed chickadee),
Oryza sativa (rice), 293 329
Ostrinia nubilalis (European corn borer), 223, Passenger pigeon, 145
235 Passerherbulus henslowii (Henslow’s sparrow),
Owlet-nightjars, 148 146
Owls, 150 Passerines, 46, 148
Oysters, 10 Passifloraceae, 53–54
Ozone, stratospheric, 192 Patrick, Ruth, 15–24, 213–216, 513, 516–517,
520, 522
P Peale, Charles Wilson, 451
Pearl Islands, Panama, 87
Pacific islands, 141, 145, 148, 154
Pacific Ocean, temperatures, 172 Pelicans, 148
Pakistan, 129 Penicillium mold, 9
Pennsylvania Biological Survey, 454
Pakitza, Peru, 33, 75, 76
Palau, 87 People’s Republic of China, 48
Palearctic realm, 48 Permian/Triassic boundary, 181
Peromyscus sp. (deer mouse), 286
Paleocene epoch, 170–176

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 544 / INDEX

Perspectives on biodiversity. See also Plankton, marine, 95–96, 286

Biodiversity II: Understanding and ProtectingBiodiversity losses
Our Biological Resources Planococcus sp. (mealybug), 219–220
http://www.nap.edu/catalog/4901.html aesthetic/ethical, 8–9, 520 Plants
community (natural), 7 aquatic species, 129
concentration of species, 8, 125–126, 257– carbon-dioxide, 189–190, 192, 193–194
258, 284 chemical, 16–17
economic, 12–13, 389–404 competitive balance, 189–190, 192, 193–
evolutionary, 7, 9, 109, 243 195
global/collective, 7–8, 411, 435 defenses, 9, 16–17
services/ecosystem, 9–10, 17–24, 282–284 drought avoiders, 189–190
sustainable development, 389–404 endemic species, 130–131
Peru evolution, 115
birds, 141 extinctions, 176–181, 187
epidemics, 286 fibers, 15
insects, 33, 48, 59, 75–76 fossils, 164–167, 168, 169, 171, 177–178
Manu National Park, 75–76, 347 fungi ratio, 49–50
potato, 9 global warming effects, 175–181, 187–195,
primates, 347, 348 516
Tambopata Reserve, 75, 76 human dependence, 15
Peterson’s field guides, 207, 208 introduced species, 194–195
Petrels, 148, 149, 151 leaf physiognomy, 164–167, 168, 169, 171
Pets, 144 losses, 133
Pew Charitable Trusts, 214 lowland, 77
Phaethon lepturus (tropicbird), 151 medicines, 9, 84, 134, 279, 280, 284–285
Phenacoccus manihoti (mealybug), 225 migration, 179–180, 188–189, 516
Philadelphia Academy of Natural Sciences, nearest living relative inferences, 164
214, 451 number of species, 90, 176, 360
Philippines, 49, 128 nutrient availability, 190, 193
birds, 139–140, 141, 145 Paleocene/Eocene boundary, 176–181
Phosphates, 13 pollination and seed dispersal, 16, 157
Photoelectors, 34 precipitation, 77
Phycitinae, 234, 235, 238 species richness, 180–181
Phyllobrotica sp. (leaf beetle), 226 stressful habitats, 190
Phylogeny. See also Molecular phylogeny temperatures, 164, 190
applications, 243 threatened and endangered, 187
bowerbird, 267 ultraviolet radiation increases, 192–194
historical reconstructions, 245 vegetation mapping, 323–326
host-parasite systems, 247, 248, 257–258, water use, 189–192, 193
516 wetlands, 129–130
primate, 342–343 Plasmodium faciparum (malaria parasite), 293
Phytoplankton, 89 Platyhelminthes, 244
Picoplankton, photosynthetic marine, 96 Pleistocene epoch, 181, 255–257
Pieridae, 75, 79 Pliocene epoch, 255, 256, 257
Pigeons, 148, 149, 150, 151, 152, 153 Plodia Guenée, 234
Pine trees, 143 Plovers, 153
Pinus taeda (loblolly pine), 194, 293 Plutella xylostella (diamondback moth), 218
Pinnipeds, 247, 516 Pluvialis dominica (plover), 153
Piping plover, 146 Poaching, 130
Pit vipers, 9 Pocillopora damicornis (coral), 87, 91
Pithecia (saki), 342 Podiceps andinus (Colombian grebe), 139
Pitta gurneyi (Gurney’s pitta), 146 Political ecology, 109, 395

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 INDEX / 545

Pollution. See also specific types of pollution Prionodura newtoniana (maypole bowerbird),
deforestation,
Biodiversity II: Understanding and Protecting 134 Resources
Our Biological 266
http://www.nap.edu/catalog/4901.html indicator species, 95 Prions, 148, 149
marine, 84 Procelsterna cerulea (tern), 151
regional effects, 11–12 Prochloron, 96
Polychaete worms, 86, 87, 95, 96, 366 Project Wallace, 55
Polymerase chain reaction, 13, 118–120, 285 Prokaryotes, 90, 118
Polynesia, 147, 149, 154 Prosobonia sp. (sandpiper), 151, 153
Pomarea iphis (monarch flycatcher), 152 Protected areas, 134
Popillia japonica Newman (Japanese beetle), marine, 359
218 reserve network selection, 334–337, 518
Population (human) Protists, 89, 111, 113, 116–117
and extinctions, 157 Protozoa, 18–22, 90
growth, 12, 83, 84, 154 Pselaphids, 97
reduction, 135 Psocoptera, 31
Population and Habitat Viability Analysis, 350, Pteridophora alberti (King-of-Saxon bird of
353 paradise), 272
Porphyrio sp. (rail), 153, 155 Pterodroma sp. (petrel), 151
Porzana sp. (flightless rail), 149, 151, 152, 153, Ptilinopus sp. (pigeons, doves), 151, 153, 155
155 Ptilonorhynchidae, 266
Potamotrygonidae, 249, 251–253 Ptilonorhynchus violaceus (satin bowerbird),
Potato, wild, 9 264, 265, 269–270
Potomac River, 9, 18, 20, 24 Ptiloris paradiseus (paradise riflebird), 267
Prairies, restoration, 373, 375–376, 378–379, Pueraria lobata (kudzu), 194
381, 384 Puerto Rico, deforestation and reforestation,
Precipitation, 77 402–403, 519
Preservation Puffinus sp. (shearwater), 151
definition, 373 Pyralidae, 234
forests, 390 Pyraloidea. See Snout moths
importance, 518 Pyraustinae, 233, 234, 235, 238
restoration, 372–373 Pyrococcus furiosus, 293
samples, 35
wetlands, 372 Q
Presque Isle State Park, Pennsylvania, 140
Priapocephalus (cetacean), 247 Quaternary period, 256, 258
Primary producers, 18 Quick Taxonomic Assessment System (QTES),
33, 36
Primates
captive breeding and reintroduction, 351–
352, 519 R
conservation strategies, 344, 349–353, 518– Rabbits, 307–309
519 Rails, 149, 150, 151, 152, 155, 158
education on, 352–353, 519 Rain forest biodiversity
field studies, 347–349 complexity, 83
geographic distribution, 343–345 coral reefs compared to, 86, 87, 88, 91–93,
habitat quantity and quality, 345–347 100–101, 102–103, 359, 514
information management and networking, described species, 91–93, 102
349, 518–519 distribution, 71
international cooperation, 352 economics, 391
phylogeny, 341–343, 347 extinctions, 62, 63
publications, 349 importance, 86
systematics, 341–342 insects, 71–72, 87, 91

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 546 / INDEX

Rain forests energy-nutrient transfers, 17–24

burning,
Biodiversity II: Understanding and Protecting 86
Our Biological Resources Robbins, Robert K., 69–82, 513, 514, 520
http://www.nap.edu/catalog/4901.html surface area, 88, 93 Robins, 155
Rallus sp. (light-footed clapper rail), 377 Roblin, Richard O., 467–474, 521
Rapid Assessment Program Team, 31, 349 Rodents, 285
Rapid gene discovery. See also Expressed Rondonia, 11
Sequence Tags Roper, Clyde, 366
applications to biodiversity, 295–296 Rossman, Amy Y., 217–229, 475–490, 514, 517,
Phylogenetic Species Tags, 296 518, 520, 521
process, 289–291 Rotenone, 87
Rats, 305–309 Royal Entomological Society of London, 55
Rattus norvegicus (Norway rat), 310, 311
Raven, Peter, 214
Rays, freshwater, 249, 251–253 S
Reaka-Kudla, Marjorie L., 83–108, 507–523 Sabrosky, Curtis W., 206, 508
Recreation, 84 Saccharomyces cerevisiae (baker’s yeast), 291,
Red Data Books, 45–46, 60, 61, 63 293
Red-cockaded woodpecker, 145–146 Saimiri (squirrel monkey), 342
Red-headed woodpecker, 146 Saguinus sp. (tamarin), 342
Red maple, 192 Saint Colman, 510–511
Reforestation, 390, 402–404 Saint Brendan, 510
Refugial habitats, 256 Saint Kevin of Ireland, 509–510
Regier, Jerome C., 301–320, 516, 518 Salinization, 13
Reintroduction of captive species, 343, 348, Salmon River estuary, 378
351–352, 519 Salvinia preauriculata (aquatic fern), 178
Relictual communities, 248, 253 Samoa, 149
Reptiles, 78 Sample preparation
Research collections bar-code labels, 236
living, 467–470, 521 beetles, 35–36
use, 456–459 Sampaio, Maria, 342
Resmethrin, 33–34 Sampling
Restoration. See Ecological restoration beetles, 33–35, 37–38
Rhode Island, butterflies, 73, 74 training in, 215
Rhode Island Natural History Survey, 453, 454 fish, 87
Rhodophytes, 111–113, 115 rates, 37–38
Rhynchosciara americana (fly), 311 San Antonio cloud forest, 146
Ribosomal RNA Database Project, 111 San Blas Islands, Panama, 95
Ribosomal RNA (rRNA) sequence analysis, San Diego State University, 377
110–112, 114, 116–117, 118, 119 Sandhill crane, 145
Rice, 223, 234, 235 Sandpipers, 148, 151, 152, 153
Rieger, John, 377 Santa Rosalia, 507–509
Rift Valley, 127 São Paulo, 8, 10
Rio Grande Valley, butterflies, 74 Satellite remote sensing, 321, 324–326, 345–
Rio Madeira drainage area, 76, 79 347, 518
Rio Napo, 76 Savannah River, 18, 21, 24
Rio Solimões, 76, 79 Scenopoeetes dentirostris (toothbilled
Riodinidae, 79 bowerbirds), 266–267, 271–272, 274
Riparian habitats, 11, 33 Schizophyllum commune (ant), 117
Riverine systems. See also Freshwater Schneider, Horácio, 342
ecosystems Schoenobiinae, 235
degradation and losses, 126

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 INDEX / 547

Scientific Committee on Problems of the Society Islands, 149

Biodiversity II: Understanding and ProtectingEnvironment,
Our Biological436Resources Society of Systematic Zoologists, 508
http://www.nap.edu/catalog/4901.html Scientific method, 350, 357, 518–519 Sogin, Mitchell L., 109–122, 508, 514–515
Scirpophaga incertulas (rice moth), 235 Soil
Scleractinian corals, 364 bacteria, 283
Sclerospongia, 284–285 biology, 8
Scopariinae, 234 moisture, 192
Scott, J. Michael, 321–340, 514, 518, 520, 521 Solis, M. Alma, 231–242, 513, 515, 517, 520
Scutellaria sp., 226 Solomon Islands, 141, 142, 149, 515
Sea lions, 256 Soulé, Michael, 132
Sea urchins, 84 South Africa, insects, 48, 49, 54
Sedge wren, 146 South America
Sedimentation, 84, 127, 128 birds, 142, 144, 146
Sediments, marine, 94–95 extinctions, 144
Seeds, defensive compounds, 16 insects, 225
Sequences, Sources, Taxa (SST) database, 294– South Carolina
295 birds, 77
Sericomyrmex sp. (ant), 116, 117 butterflies, 73
Serra do Japi Reserve, 76 Soviet Union (former), insects, 48, 49
Seychelles, 87 Soybeans, 222
Sharks, 95 Speciation, 58, 126, 127, 132
Shearwaters, 149, 151 Species
Sheep, pathogenic parasites, 223–224 adaptation, 100–101, 115, 131, 132, 149, 158
Shrimps and prawns, 13, 87, 97, 98, 99, 307– definition, 216
309 discovery rates, 158
Silent Spring, 218 distribution and biology, 45–47, 48–49
Size of population (nonhuman), and distribution maps, 326–328
vulnerability, 139, 147, 518 morphospecies concept, 59–60, 95–96
Size of species turnover, 58–59, 147, 182
coral reefs, 97–100, 102–103, 514, 519 Species, number. See also Classification of
eukaryote/prokaryote differentiation, 118 species; Measurement of biodiversity
extinction rates, 101, 103, 514 aquatic, 89, 90
geographic distribution, 98–100, 101–102 beta diversity, 58–59
vulnerability, 348–349 body size, 56, 57–58
Smithsonian Institution, 3, 8, 95, 214, 342, concentration, 8
451, 452, 513, 522. See also National coral reefs, 85–94, 102, 514
Museum of Natural History estimated, 7, 8, 45, 55–57, 65, 85–86, 91–93,
Smut, 222–223, 517 244, 360, 514
Snakes, venom, 9 fungi, 90, 282
Snout moths (Pyraloidea) insects, 29, 32, 55–56, 90, 232, 513–514
and agriculture, 234–235, 517 marine, 86, 89, 101
benefits of research, 239–240 microbial, 282
biodiversity studies, 234, 515 named and described, 42, 45, 85, 89, 90, 91,
caterpillars, 233 102
in Costa Rica, 232, 233, 235–239 rain forests, 102, 514
families and subfamilies, 232, 234 riverine systems, 17
geographic distribution, 232–233 Sulawesi, 55–57
identification aids, 238–239 symbiotic, 89, 90
number of species, 232 taxa, 57, 90
response to environmental disturbance, terrestrial, 89, 90, 96–97, 101
233–234 Species losses. See Extinction

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Species Survival Commission, 351–352 political/economic dichotomies, 397–398,

Spermophilus
Biodiversity II: Understanding and Protecting brunneusResources
Our Biological (ground squirrel), 330 519
http://www.nap.edu/catalog/4901.html Spiders, 96–97 transportation-development partnerships,
Sponges, 87, 94, 284–285 398–399, 519
Sri Lanka, 130–131 tropical, 389–404
Staphylinids, 36, 97 “use it or lose it” approach, 390–391, 413–
Starlings, 156 414
State Heritage Program, 454 women’s role, 400
Steadman, David, 11, 139–161, 515 Sutton, Granger, 289–299, 518, 521
Steinernema carpocapsae (nematode), 221 Swallow-tailed kite, 145
Stephen Island wren, 11 Swans, 148
Sterna sp. (tern), 151 Sweeney, Mike, 366
Stingrays, 249, 251–253, 516 Sweet potato whitefly, 220
Stoneflies, 18 Swifts, 152, 155
Stork, Nigel E., 41–68, 97, 99, 514, 515 SwissProt database, 290
Storm-petrels, 149, 151 Symbiotic organisms, 89, 90, 116–118
Stramenopile assemblage, 111–114 Systema Naturae, 42, 204, 208, 508
Strigid owls, 148 Systematic biology, 108–109
Stroud Water Research Laboratory, 18 Systematic Entomology Laboratory (USDA), 3,
Subsidies, economic, 134–135, 395 206, 207, 219, 513
Sudan, 129, 130 Systematic Zoology, 508
Sudd Swamp, Sudan, 129, 130 Systematics Agenda 2000, 61, 96, 226–227, 437,
Sugarcane, 234, 235 440–442, 444–445, 521–522
Sula sp. (booby), 149, 151 Systematists and systematics, 85. See also
Sulawesi, Indonesia, 52, 55–57, 233–234 Classification of species
Surgeonfish, 116–117, 118 agricultural, 219–220, 222–226, 517
Surinam, deforestation, 11 components, 436
Surirella ovala (diatom), 22 ecological approach, 437–440, 520
Surveys, biodiversity. See also Gap analysis education and training, 157, 213–216, 239–
breeding bird, 326 240, 360, 423, 443–444, 516–517, 521–
marine, 359–360 522, 523
state natural history, 454 institutional infrastructure, 521–522
wetlands, 324 interinstitutional links, 522
Sus scrofa (pig), 310 molecular approaches, 157, 291–295; see also
Sustainable development/management, 13 Molecular phylogeny
agriculture, 221–222, 399–400, 401–402, 519 need, 436–437, 511, 517, 520–521
Amazonia, 400–401 predictive nature, 200–201, 202, 225–226
biodiversity, 390 primate, 341–342
coral reefs, 84 resources, 204, 224–225, 511, 512
biosphere initiative, 390 status, 460–462
definition, 389–390, 519
extractive reserves, 395
Ford village industry concept, 397, 519
T
forests, 390–391, 402–403, 519 Tambopata Reserve, Peru, 75, 76
historical lessons, 396–404 Tanganyika, 127, 128
impediments to, 394–396 Tangatatau Rockshelter, 150, 153
international cooperation, 426, 519 Tanimbar, 142
Maya civilization collapse, 396–397, 519 Tapeworms, 247, 253–254, 516
McKelvey box classification, 391–394 Tarahumara, 143
nontimber product marketing, 399, 519 Taxon, 205
political backlash, 395–396 Taxonomic Working Group (TWIG), 35, 38

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 INDEX / 549

Taxonomists, need for, 44, 94 tropical forest, 51, 53

Taxonomy.
Biodiversity II: Understanding and Protecting See also Classification
Our Biological Resourcesof species Trichoderma sp., 226
http://www.nap.edu/catalog/4901.html coral reef biodiversity, 360 Trichogramma sp., 222, 227
morphospecies concept, 59–60 Trichomonads, 111
number of taxonomists, 360 Trigonocotyle, 247
wildland biodiversity management, 422–424 Trillers, 155
Teak, 235 Triticum aestivum, 193, 194
Temperatures, environmental. See also Global Tropical coastal zone, 88–89, 92
climate change Tropical forest beetles
plant response, 164, 189, 194–195 collection-building, 37
Tepuis, 142 collection of data, 32–33
Termites, 31 host specific, 51–53
Terns, 149, 151 insecticidal fogging method, 30, 50
Terpenoids, 16 interim identification, 37
Tertiary period, 249, 251, 253–254 number of species, 28, 51, 54, 59
Tethys Sea, 179 preparation, 35–36
Tetrodotoxin, 284 sampling, 33–35
Tretrabothrius (cetacean), 247 species-level studies, 30
Tetraphyllidean cestodes, 249 storage of data, 37
Texas, butterflies, 73, 74 Tropical forests
Thailand, birds, 146 beetles, see Tropical forest beetles
Thanatephorus praticolo (ant), 117 birds, 140
The Institute for Genomic research (TIGR), 290 canopy, 8, 50, 79
Thermus aquaticus (bacteria), 285 deforestation, 1–2, 11, 133, 135, 140
Thomas, James D., 357–369, 514, 519, 520 dry, 74
Thompson, F. Christian, 199–211, 517, 518, fragmentation, 146, 375–376
519 hydrological cycle, 10
Thoreau, Henry David, 383 insects, 27, 74
Threatened and endangered species nontimber products, 390, 391, 394–395, 399
birds, 149, 154, 323 protected areas, 134
freshwater ecosystems, 126 species, 8, 27, 51, 53, 91–93, 359
gap analysis and, 328, 518 sustainable use, 390–391, 519
insects, 46–47 Tropical lakes, 126–128
knowledge base, 45–47, 101 Tropical wetlands, 128–131
morphospecies concept, 95 Tropicbirds, 149, 151
plants, 187, 379 Trumpeter swan, 145
and relative rates of extinction, 60–61, 64 Tsuga canadensis (Eastern hemlock), 188–189
Thrushes, 155 Tunicates, 284
Tierra del Fuego, 8 Turdus poliocephalus (thrush), 155
Tilletia sp. (smut), 223 Turkey, 131
Tirathaba complexa (coconut moth), 235 Turner, Frederick, 380, 383
Tolgren extractor techniques, 34 Turner, Victor, 384–386
Tomato, 224 Tyto alba (barn owl), 155
Tonga, 147, 149, 152, 154, 155–156
Toxins and detoxins, 16–17
Toxostoma redivivum (California thrashers), 328
U
Trachymyrmex sp. (ant), 116, 117 Ua Huka, 149, 150, 151–152
Trapping, insects, 34 Ucayali, Peru, 76
Trees Uganda, 220
carbon dioxide uptake, 12 Ulmus (Chaetoptelea) microphylla, 177
number of species, 51, 53, 55–56, 79 Ultraviolet radiation, 84, 134, 192–194, 283

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Umminger, Bruce L., 491–504, 518, 521, 522 Vertebrates

Unaspis
Biodiversity II: Understanding and Protecting euonymi
Our (euonymus
Biological scale), 221
Resources knowledge of biodiversity of, 7–8
http://www.nap.edu/catalog/4901.html United Kingdom number of species, 360
extinction rates, 64, 76–77 Vestimentifera, 94–95
insect fauna, 7, 54, 69 Vibrio cholerae 01, 286
threatened species, 46, 64 Victoria, Lake, 127–128
United Nations Educational, Scientific, and Vini sp. (parrot), 152, 153, 155
Cultural Organization, 324, 416–417, 436 Vireo bellii (least Bell’s vireo), 379
United States Virginia, butterflies, 73, 74
agriculture, 220, 222–223, 517, 519 Viruses and procaryotes, 89, 90, 96, 282
biotechnology industry, 280–281
birds, 77, 143, 154
butterflies, 72–74
W
Civil War, 397–398, 519 Walker, Francis, 44
conservation strategy, 333 Wallace, Alfred, 357, 508
extinctions, 126, 143 Warblers, 146, 152, 153, 155
habitat losses, 154 Wars and conflicts, and conservation, 396
insects, 48, 49, 72–74, 220, 222–223 Washington, George, 402
plant species, 129 Washington state, butterflies, 73, 74
riverine systems, 126, 515 Wasps (Chalcidoidea), diversity, 53, 97
threatened and endangered species, 126 Water boatmen (Corixidae), 509
wetlands, 129 Water hyacinth, 235
University of Kansas, 214 Water pollution, 13, 126, 127
University of Maryland Water supply projects, 13
Biotechnology Institute, 3, 513 Water use, by plants, 189, 192
College Park, 3, 219, 513 Weather, extreme events, 188; see also Global
University of Wisconsin climate change
Genetics Computer Group, 303 Weeds, biocontrol, 234–235, 517
Madison Arboretum, 378–379, 381–382, 384 Weevils, 35, 36
Ursus americanus (black bear), 329 Western red cedar, 332
Usumacinta Delta, Mexico, 129 Wetlands. See also specific wetlands
U.S. Biological Survey, 13 birds, 140
U.S. Department of Agriculture losses, 128–129, 139
Animal and Plant Health Inspection Service mapping, 324
(APHIS), 222–223, 517 restoration, 372, 377–378
Systematics Laboratories, 3, 206, 207, 219, threats, 129
513 tropical, 128–131
U.S. Environmental Protection Agency, 324, Whales, 133
326 Wheat, 131, 193, 194, 222–223, 517
U.S. Fish and Wildlife Service, 322, 326 Wheeler, Quentin D., 435–446, 517, 520–521,
U.S. Geological Survey, 324 522
U.S. National Biodiversity Information Center, Whistlers, 155
491–497, 498–503, 521, 522 White Clay Creek, Pennsylvania, 18, 22–23, 517
Utah, gap analysis of biodiversity, 322 White, Owen, 289–299, 518, 521
White-eyes, 156
Whiteflies, 220
V White Mountains, New Hampshire, 189
Vanilla, 12 Whooping crane, 145
Venezuela, 76, 141 Wilcox, Bruce, 132
Venter, J. Craig, 289–299, 518 Williams, Austin, 366
Vermivora bachmanii (Bachman’s warbler), 145 Willis, Ed, 11

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 INDEX / 551

Wilson, Don E., 507–523 Y

Wilson,
Biodiversity II: Understanding and Protecting Edward
Our O., 1–3,
Biological 28, 214, 296, 449,
Resources Yellowstone National Park, 13, 119, 285
http://www.nap.edu/catalog/4901.html 507–523
Young, Steve, 491–504, 518, 521, 522
Wing, Scott L., 163–185, 516
World Bank, 395
World Conservation Monitoring Centre, 498 Z
World Conservation Union, 63, 351 Zaire, 48
World Wildlife Fund, 349 Zambia, 129
Wyoming
Zea mays (maize), 293
birds, 77 Zedler, Joy, 377
butterflies, 73 Zooarcheology, island birds, 147–153
Zoos. See Captive breeeding; specific
X institutions
Xenopus laevis (frog), 311 Zosteropidae sp. (white-eyes), 156
Xerocomus chrysenteron (ant), 117

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Biodiversity II: Understanding and Protecting Our Biological Resources
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