Ecology Letters, (2013) 16: 4–16 doi: 10.1111/ele.

12048

REVIEW AND
SYNTHESIS The problem of pattern and scale in ecology: what have we
learned in 20 years?

Abstract
J
^me Chave*
ero Over the past 20 years, major advances have clarified how ecological patterns inform theory, and how in
turn theory informs applied ecology. Also, there has been an increased recognition that the problem of

Paul Sabatier,
CNRS & Universite
scale at which ecological processes should be considered is critical if we are to produce general predictions.


UMR 5174 Evolution et Diversite
^timent 4R1, 118
Ecological dynamics is always stochastic at small scales, but variability is conditional on the scale of
Biologique, ba
route de Narbonne, Toulouse,
description. The radical changes in the scope and aims of ecology over the past decades reflect in part the
31062, France
need to address pressing societal issues of environmental change. Technological advances in molecular biol-
ogy, global positioning, sensing instrumentation and computational power should not be overlooked as an
*Correspondence: E-mail: jerome. explanation for these radical changes. However, I argue that conceptual unification across ecology, genetics,
[email protected] evolution and physiology has fostered even more fertile questions. We are moving away from the view that
evolution is played in a fixed ecological theatre: the theatre is being rapidly and relentlessly redesigned by
the players themselves. The maintenance of ecosystem functions depends on shifts in species assemblages
and on cellular metabolism, not only on flows of energy and matter. These findings have far reaching
implications for our understanding of how ecosystem function and biodiversity will withstand (or not) envi-
ronmental changes in the 21st century.

Keywords
Eco-evolutionary dynamics, global change, modularity, pattern, scale, spatial ecology.

Ecology Letters (2013) 16: 4–16

of which are described below. The second revolution has been bio-
INTRODUCTION
chemical. New techniques of molecular biology, notably the poly-
Pattern implies some sort of repetition, and the existence of repeti- merase chain reaction, have percolated into ecology labs and have
tion implies that some prediction is possible (MacArthur 1972). Few thrived to a degree that was initially difficult to imagine. The journal
research articles have been more influential to our discipline than Molecular Ecology, now one of the foremost outlets in ecology,
Simon Levin’s (1992) paper ‘On the problem of pattern and scale was launched in 1992. High-throughput sequencing techniques are
in ecology’. It has introduced a generation of ecologists to interdis- promising to transform again our research field. The third revolu-
ciplinary thinking, and to two crucial concepts for ecology, pattern tion has concerned environmental sensing. The seeds of change
and scale. He has also promoted the view that ecological processes were already present in the 1980s, with the development of land-
act at a variety of spatial and temporal scales, and they generate pat- scape ecology. Yet, reliable technology to develop research pro-
terns at scales that may differ from that at which processes act. To grams in global ecology. Transformative techniques such as Light
understand a system, it is important to study it at the appropriate detection and Ranging (LiDAR) or hyperspectral techniques have
scale, and develop models that bridge across scales. Twenty years offered new ways to look at the Earth system. Of course, many
after the publication of Levin (1992), and 40 years after that of more sensors have been implemented for ground-based applica-
MacArthur’s (1972) ‘Geographical Ecology’, I took this opportunity tions, to measure fluxes or environmental variables (Vargas et al.
to place the themes of this special issue in a historical perspective 2010), to follow the spatial movement of individuals or to record
with the key concepts of pattern and scale, and ask how this recent their behaviour, (Katz et al. 2011). The fourth and last revolution
history may hopefully help us to connect processes with pattern relates to our ability today to disseminate information and knowl-
and scale to set a path forward in ecology. edge at a global scale, with far-ranging consequences on our ability
Since 1992, ecology has witnessed and has been an actor of four to develop collaborative science among researchers but also foster
major technological revolutions. The first and foremost revolution the development of a vast knowledge base in natural history, with
is the advent of the numeric era. Moore’s law of the doubling contributions from concerned citizen (Silvertown 2009).
capacity of computers every 2 years has been outpaced: over the Central issues of ecology have also shifted significantly over the
past two decades, computer power has doubled every year. The past two decades. Global environmental changes have been an over-
computer on which this manuscript was typeset is one million times whelming factor of change. For instance, the human population has
faster than the one I was trained on as a student 20 years ago. This increased by 25% and fossil CO2 emissions by 40% (Le Qu
er
e et al.
has had innumerable consequences on the way we do science. 2009). Most models suggest that this should result in a doubling in
Questions that pertained to the realm of speculation have been radiative forcing by 2050 (Moss et al. 2010). These trends have been
revisited, such as bioinformatics projects in molecular biology, some accompanied by a regional shift of traditional foci of environmental

© 2013 John Wiley & Sons Ltd/CNRS

Review and Synthesis Pattern and scale in ecology 5

concern. The 20th anniversary of the Rio Earth Summit has been biology and ecology, largely driven by the analysis of network pat-
the occasion to confirm that the goals of reducing the threats to terns. Finally, I will revisit the classic theme of spatial patterns in
biological diversity have not been met today. If anything, things ecology.
have gotten worse.
Understanding the translation of dynamics across scales in ecosys-
COUPLING ECOLOGICAL AND EVOLUTIONARY SCALES
tems, and the response of life support systems to environmental
changes is a formidable challenge, which is addressed in several of Complex systems differ in one fundamental way from other sys-
the papers of this issue. The core of this issue amounts to under- tems, in that their organisation is changed by the environment they
standing how environmental changes at the global scale lead to themselves create through evolutionary processes. Traditionally, in
changes on individuals, but also impose selective pressures upon ecology the study of ecosystem processes has been disconnected
populations, and may lead to changes in diversity, at the genetic, from that of evolutionary processes, under the argument that eco-
phenotypic, and at the species levels. In essence, the problem is to logical processes acted over much smaller timescales than evolution-
bridge across very different spatial scales, from one cubic metre of ary ones. Over the past two decades, much progress has been made
ocean or one square metre of land, to the global scale, a change in towards an understanding of the coupling between ecological and
linear distance of a factor 107. To paraphrase Levin (1992), ‘the evolutionary temporal scales, as is briefly reviewed here.
description of pattern is the description of variation, and the quanti-
fication of variation requires the determination of scales’. A related
Pace of evolution
issue is that organisms that interact with the environment do not
probe the same physical space, although they are geographically How much does evolution impact population dynamics? This is not
located at the same position. This is because living creatures differ only the first natural question to ask in the study of complex adap-
in their life-history stages and traits, but also more simply because tive ecological systems but it is also of fundamental applied rele-
they vary enormously in size, from 10
6 m in oceanic picoplankton vance in studying the influence of climatic changes on biological
to ca. 100 m for a whale and the largest living trees, a change in diversity (Parmesan 2006; Savolainen et al. 2007). Evidence for an
body size of a factor 108 in eukaryotes only. These creatures also explicit coupling of temporal scales between ecology and evolution
experience widely varying spatial and temporal scale through dis- has accumulated relatively recently, although theoretical work had
persal and dormancy. been conducted in the 1990s (van der Laan & Hogweg 1995;
This review of the problem of pattern and scale in ecology is or- Abrams & Matsuda 1997). In experiments of rotifers preying on
ganised around four foci, each of which represents research areas algae, Yoshida et al. (2003) compared single-clone algal cultures to
where this problem has been of paramount importance in recent multi-clone cultures. They found that the period of oscillations and
years, and which are likely to drive much research in the years to the phase between predator and prey were dramatically affected by
come. First, I will review new approaches to reconcile the ecological whether the prey could evolve (Fig. 1). In the multi-clone experi-
and evolutionary temporal scales. Then, I will turn to a research ments, therefore with the possibility of prey to evolve, low-food
field that has long been disconnected from evolutionary and popu- value prey clones persisted in the over-grazed system and high-food
lation biology: ecosystem science. The study of global change biol- value prey clones achieved competitive dominance after the preda-
ogy is poised to bridge this gap, and research in this area places a tor population had crashed. This study shows that evolution may
strong emphasis on scale and pattern. Third, I will explore the fron- alter the trajectory of an ecological process if the heritable pheno-
tiers of the organism, with an emerging synthesis between systems typic change occurs sufficiently quickly. Rotifers (females ml–1)
Algae(106 cells ml–1)

5 30 5 30
(a) (b)
4 25 4 25
20 20
3 3
15 15
2 2
10 10
1 5 1 5
0 0 0 0
0 10 20 30 40 0 10 30 50
Time (day) Time (day)

Figure 1 Experimental cycles of the prey algae Chlorella vulgaris (green triangles) and the predator rotifer Brachionus calyciflorus (red circles) populations in a chemostat
system. In panel (a), the initial algal population was descended from a single algal cell, and the opportunity for advantageous algal genotypes to arise by mutation was
minimised. This system exhibited classical predator–prey cycles with increases in prey abundance followed by increases in predator abundance after a quarter-period lag.
In panel (b), the initial algal population was drawn from multiple sources and genetically variable. The cycles were longer and the oscillations in predator and prey
abundance were almost exactly out of phase. Redrawn from panels b & g in Yoshida et al. (2003).

© 2013 John Wiley & Sons Ltd/CNRS

6 J. Chave Review and Synthesis

A wonderful example of how evolutionary dynamics is coupled maturity at an earlier age and smaller size, produce more and smaller
with ecological dynamics in the wild is given by the Darwin’s finch offspring per litter and devote more resources to each litter. Food
Geospiza fortis. Grant & Grant (2006) reported spectacular changes in availability for guppies varies with environmental factors such as for-
beak size over a 40-year period (for a detailed review, see Grant & est canopy cover, such that less canopy cover favours the develop-
Grant 2008). In Darwin’s finches, beak size is essential to forage on ment of a larger algal crop, the primary food of guppies. Palkovacs
the seeds which they feed upon, and it is a heritable trait (Boag et al. (2009) developed an experimental set-up in mesocosms, where
1983). Further, beak size conditions the ability of the bird to crack they quantified how guppies that had been adapted to either high
seeds open, the major food income of G fortis (Herrel et al. 2005). In predation or low predation level differed in their impact on ecosys-
1977, a drought led to a decline of small-beaked G fortis, because of a tem structure and function. Guppy phenotypes were shown to have
shortage of small seeds. The situation returned to the pre-1977 situa- an impact on ecosystem processes independent of density: meso-
tion in 1983 after an intense rainy season. In 2004, the immigration cosms with the high-predation phenotype had higher algal standing
of a competitor, Geospiza magnirostris, resulted again in a character dis- stocks but lower biomass-specific gross primary productivity, and a
placement of the G fortis population towards smaller beak sizes. Even lower total invertebrate biomass (Palkovacs et al. 2009). A similar
more remarkable – and important for the point here – is the fact that study with the threespine stickleback yielded comparable results
the developmental basis for rapid changes in the shape of Darwin’s (Harmon et al. 2009). The guppy and stickleback studies, together
finch beaks has been unravelled (Mallarino et al. 2011), offering a with recent theoretical work (Fussmann et al. 2007) represent a for-
mechanistic basis for trait change observed in the wild. midable effort to test the effects of evolution on ecosystem function-
The interplay between ecological and evolutionary dynamics can ing, and they confirm that if the environment has a potential
be modelled by focussing on a single species using an extension of influence on species evolution, the reverse is also true.
Fisher’s covariance equation (Frank & Slatkin 1992). Its instanta- However, eco-evolutionary dynamics models are still restricted in
neous population growth rate r changes either because of changes their scope. In the aforementioned examples, the environment is
in a heritable trait z (think of beak size in Darwin’s finch), or modelled through the dynamics of another species, the plant
because of a change in its ecological environment k (think of seed resource in the case of Darwin’s finches and the copepod predator
abundance). Hence, Hairston et al. (2005) suggested that the partial in the case of the guppy. A general predator–prey model is thus
derivative of r(z, k) against z, denoted @rðz; kÞ=@z, reflects the sufficient to reproduce their dynamics (Abrams & Matsuda 1997). A
changes in the population growth rate due to trait change (and not perspective for this research is to explore how this dynamics scales
due to changes in abundance). According to the chain rule up from two species to the community level, which involves under-


standing how evolution shapes interacting networks (Meli
an et al.
dr @r

dz @r

dk
¼ k þ  2011), a theme that I will return to below. Another question is
dt @z
dt @k
z dt whether such patterns of eco-evolutionary dynamics will persist
The right hand side of the equation has two terms: the first includes across spatial scales. In normal situations, adaptive divergence
the effects of evolutionary dynamics and the second that of ecologi- should decline with weak selection and increasing gene flow, but
cal dynamics. Hairston et al. (2005) went on to partition out the counter-intuitive results are expected in the presence of eco-evolu-
two effects. They were able to show that in G fortis, evolutionary tionary dynamics of several interacting species in networks.
change in body and beak size of G fortis was twice as fast as the
ecological dynamics over the period 1976–1990. Of course, not all
THE SCALES OF GLOBAL CHANGE
trait variation can be ascribed to evolution, for non-heritable trait
variation is a conspicuous feature in populations (Gienapp et al. A second illustration of the problem of pattern and scale in ecology
2008), but this framework provides was successful at relating mod- that was in its infancy two decades ago is offered by global change
els and data. Since a central goal in ecology is to develop models biology. At that time, ecosystem science and evolutionary biology
that provide an integrative framework to understand how and when were perceived as disconnected, and Levin (1992) pointed out that
processes act at the same scale, the attempt to synthesise timescales, this disconnection was a great challenge. It would be an overstate-
and see how the players contribute to changing their theatre, is a ment to say that today this challenge has been overcome, but major
result of foremost importance in ecology (Schoener 2011). studies have emphasised the role of adaptation in mitigating global
climatic change (Hetherington & Woodward 2003), and have inter-
preted current biogeochemical functions in the light of the Earth’s
Ecosystem consequences of evolution
geological history (Wortmann & Paytan 2004; Falkowski et al. 2008).
The above research aims at unravelling the consequences of environ- Here, I briefly review how ecosystem science has attempted to solve
mental processes on species evolution. A parallel question is: what is its internal problems of scale.
the influence of species-level evolution on the dynamics of ecosys-
tems? Several theoretical approaches to this question have recently
Scaling primary production from cells to the globe
been reviewed by Fussmann et al. (2007), pointing to the profound
role that evolution may have on ecosystem functioning. Recent A natural currency to measure these couplings is the carbon unit.
experimental research has been conducted using a fish species as Net primary productivity (NPP) is the amount of carbon fixed in
models: the guppy (Poecilia reticulata). Long-term research on guppies the biosphere by unit area and time (Field et al. 1998). What are the
of Trinidad freshwaters has demonstrated the potential for evolution regional contributions to global primary productivity worldwide, and
on reproductive and foraging traits, traits that were shown heritable how should global change alter them? This is a difficult question
(Reznick et al. 1997). Specifically, populations that have been exposed because we know that the carbon cycle is highly variable at all
for a long period to a predator (a cichlid fish Crenichila alta), attain temporal scales (Falkowski et al. 2000; Fig. 2). One of the great suc-

© 2013 John Wiley & Sons Ltd/CNRS

Review and Synthesis Pattern and scale in ecology 7

cesses in ecosystem science since 1992 has been to wed empirical models (Antoine & Morel 1996; Behrenfeld & Falkowski 1997) has
data and models, and to move towards predictive models of the made it possible to infer NPP from chlorophyll concentration, result-
biosphere. Much effort is still ahead, but this should not over- ing in remarkably accurate oceanic NPP maps (Gregg et al. 2005).
shadow these achievements. Even more surprising is the finding that tiny creatures such as the
In terrestrial ecosystems, estimating the global NPP has relied on picoplankton (less than 2 lm), contribute a significant fraction of glo-
combining a number of independent techniques, some based on top- bal oceanic NPP (Uitz et al. 2010). Picoplankton differs from diatoms
down scaling, others based on bottom-up scaling. In the former cate- and other classically studied microplanktonic groups (> 5 0 lm), and
gory, remote sensing products have been critical to describe vegeta- still represents a poorly known reservoir of biodiversity (Vaulot et al.
tion types and their phenology (Running et al. 2004). Detailed 2008). Bottom-up scaling methods through mechanistic have also
measurements of the chemical composition of the atmosphere, com- been applied to the oceans. Various classes of primary producers of
bined with ingenious inversion techniques using global circulation plankton have now been integrated in dynamic green ocean models
models have also helped constrain regionally the carbon cycle (Tans (Le Qu
er
e et al. 2005). One remarkable example of such a modelling
et al. 1990; Gurney et al. 2002). Eddy-flux correlation techniques to effort is the attempt by Follows et al. (2007) to simultaneously simu-
measure exchanges of carbon dioxide between ecosystems and the late the oceanic biogeochemical cycles and the biogeographical orga-
atmosphere have also seen an exponential growth over the past two nisation of biological diversity. Because of the complex nature of the
decades (Malhi et al. 1999; Baldocchi 2003; Luyssaert et al. 2007). As couplings between the oceans and the atmosphere, scenarios for the
the CO2 molecules are drafted above vegetation canopies by wind, future remain hypothetical. For instance, there remains considerable
which form eddies at the contact with the ground boundary, the tem- uncertainty on future changes in oceanic NPP (Henson et al. 2010),
poral pattern of carbon fluxes at the atmosphere-vegetation interface and more generally for global change scenarios (Moss et al. 2010).
shows a power-law pattern typical of turbulent flows (Baldocchi
2003). Such eddy-flux covariance techniques have provided a tremen-
Scaling metabolism from cells to the globe
dous wealth of information across ecosystem types. Of course, these
data must be assimilated to get at estimates of NPP values, and this One of the most classical illustrations of the importance of scale in
is best done using vegetation models. Of special relevance to the biology is allometry, the relation of body size to anatomical, physio-
point made here is Moorcroft et al. (2001)’s Ecosystem Demography logical, behavioural and ecological features (Calder 1984; Niklas
(ED) model, which implements a method to up scale the individual- 1994). Animal metabolic rate appears to show a ¾ power-law
based processes of a forest model to the region. Specifically, ED relationship with body mass (Kleiber 1947). Extraordinary efforts
approximates a microscopic model by a macroscopic one (Durrett & have been paid to test the generality of this pattern empirically (see
Levin 1994) through a method for scaling from the forest dynamics e.g. Mori et al. 2010 in plants). West et al. (1997) attempted to
to a region through a system of differential equations. This approxi- derive the ¾ power-law scaling from first principles, assuming that
mation ignores the individual details and focusses on the ensemble respiratory and vascular systems are tree-like networks (e.g. from
averages (Bolker & Pacala 1997). If a suitable set of boundary condi- aorta to capillaries) and that exchanges at the capillary scale is limit-
tions is provided, together with a distribution of waiting times since ing metabolic rate. This result has spurred considerable controversy
the last disturbance of forest patches, this method offers a rapid because of its simplicity but also because the underlying assump-
means for determining the regional dynamics of the vegetation at a tions can be readily tested by physiologists (Biro & Stamps 2010).
coarse scale. This approach is currently one of the most promising Several excellent recent articles have reviewed the mathematical der-
ones for assimilating data across scales, especially including high-fre- ivation of this model, and the nature of the assumptions underpin-
quency environmental variables (Medvigy et al. 2010). ning it (Savage et al. 2008), and I will not further delve into this
The study of the oceanic carbon cycle has followed a parallel path. topic. The point I want to make here is simpler: the underlying idea
The development of optical imagery (McClain 2009) and scaling of allometry to factor out the role of body size should help bridge
across physiology and ecosystem science. This idea has been pur-
sued by Enquist et al. (2003), Allen et al. (2005) and L
opez-Urrutia
et al. (2006), but in these studies the problem of body-size scaling
10,000 has turned out to be far less relevant than that of the relationship
between ecosystem-level metabolic rate and temperature.
[CO2] (in ppm)

Glacial-interglacial At the ecosystem scale in terrestrial systems, metabolic rate is the

100 compound of plant respiration (both above and below-ground
Human perturbation
Annual cycle parts), plus heterotrophic respiration of soil decomposers (Malhi
et al. 1999). Across ecosystems, heterotrophic respiration varies
1
Diurnal cycle from 25% to 50% of total respiration (Luyssaert et al. 2007).
Recently, Vargas et al. (2010) have conducted a high-frequency
monitoring of soil respiration in three ecosystems. Using wavelet
0.01
transform analyses, they have explored the scale at which environ-
109 106 103 100 10–3
mental variables (soil moisture and temperature) should correlate
Period (in year)
with soil respiration (Fig. 3). Their analysis shows that although
soil respiration is expected to increase with moisture and with
Figure 2 Schematic variance spectrum for the concentration of atmospheric CO2
over the course of Earth’s history. The impact of human perturbations on the temperature, it is not easy to predict daily changes in soil respira-
decade-to-century scale is depicted in black, and show a unique signal. Redrawn tion. Thus, at fine temporal scales, the dynamics of soil respiration
from Falkowski et al. (2000). is far from simple to model. However, under the assumption that

© 2013 John Wiley & Sons Ltd/CNRS

8 J. Chave Review and Synthesis

(a)

(b)

(c)

Figure 3 An example of wavelet analysis for an ecological problem. Correlation between soil CO2 production and soil water content in three vegetation types: (a) mature
woody vegetation, (b) young woody vegetation and (c) herbaceous meadow, during 2 years. Colour codes for power values between the two variables: from dark blue
(low) to dark red (high). Black contour lines represent the 5% significance level. The phase difference is shown by arrows: in-phase pointing right (no lags between time
series), off-phase pointing in other direction (lags between time series). Thick black line indicates delimits the region not influenced by edge effects. Arrows at the top of
the panels indicate the approximate date of summer rainfall events. From Vargas et al. (2010).

all the cells of an ecosystem have similar temperature dependence For much of its history, ecosystem science has been concerned
of metabolic rate, one should be able to obtain a ‘macroscopic’ rela- only with the fluxes of matter and energy at a local scale (Golley
tionship. 1993). The problems of scaling from organism to ecosystem, and
At the cellular level, biochemical reaction rates are expected to vary from ecosystem to the globe are fortunately now better integrated
with temperature proportionally to a factor,expð
E=kT Þ where E is into this discipline.
the activation energy of the reaction, T is the temperature (measured
in Kelvin) and k is Boltzmann’s constant (k = 8.617 9 10
5 eV/K),
MODULARITY IN INTERACTION NETWORKS
as first derived by Arrhenius in the 19th century (Lloyd & Taylor
1994). At the ecosystem scale, Lloyd & Taylor (1994) showed that Levin’s (1992) study was also influential at bringing complex sys-
the dependence on temperature of soil respiration rate, RT, is mod- tems to the forefront of the ecological research agenda. Biological
elled by the following equation: RT ¼ R10 exp½Eð1=kT10
1=kT Þ. systems are inherently hierarchically structured and modular (Simon
Conventionally, R10 is the ecosystem respiration rate at 1962; Hartwell et al. 1999). Modularity allows redundancy because
T10 = 283.15 K (or 10 °C). Plotting empirical data, they found that the flow of information is quickly and evenly distributed within the
E = 0.55 eV yielded a relatively good fit. The same relationship was module, and also resilience since any disruption of the system is
proposed at the organism scale by Gillooly et al. (2001), who found buffered by this redundancy (for a mathematical definition of mod-
activation energies ranging between 0.41 and 0.74 eV across ularity, see Appendix S1). This has major consequences for the cel-
organism groups, close to Lloyd & Taylor’s estimate (see also lular and developmental machinery of organisms (Wagner et al.
Yvon-Durocher et al. 2012s recent analysis). This suggests that tem- 2007), but also for the stability of ecological systems (Ives &
perature change has a similar effect on all the living creatures in an Carpenter 2007). This concept was poised to become central to eco-
ecosystem, that is, it is invariant with scale. logical thinking back in 1992 (Sugihara et al. 1989), and it has

© 2013 John Wiley & Sons Ltd/CNRS

Review and Synthesis Pattern and scale in ecology 9

indeed risen to dominance, for it offers ways to relate local interac- is a division of labour to facilitate dispersal. Velicer & Yu (2003)
tions among individuals and emergent patterns at the community studied how the bacterium Myxococcus xanthus, has evolved the ability
level. There are two different issues to be discussed here. The first to display a multicellular stage, able to glide across soft surfaces (Ber-
is that individuals are generally not assorted randomly, and the scal- elman & Kirby 2009). They studied some strains of M. xanthus that
ing up of interactions from the individual scale to the community exhibited socially dependent swarming through enhanced production
scale depends on the details of the fine-scale assortment. The sec- of an extracellular fibril matrix that binds cells together. Though
ond issue is that, while addressing the issue of modularity across costly to individuals, fibril production greatly enhances population
scale in ecological systems, we should seek common features, and expansion in groups of interconnected cells (Velicer & Yu 2003).
possible conflicts, in the emergence of modularity among individuals The resulting multicellular structure behaves as an efficient predator
and within individuals. of other microbial species relying on chemotaxy to cue its prey.
Berelman & Kirby (2009) call such swarms a ‘bacterial wolfpack’, and
show impressive photographs of the predatory behaviour of these
Individual variation and interaction networks
swarms. A similar type of collective behaviour, biofilm development,
Ecologists have traditionally studied the patterns created by the tan- has been invoked to explain the increased virulence of the bacterium
gled web of ecological interactions among species (Paine 1980). The Pseudomonas aeruginosa in acute forms of infections (Diggle et al. 2007).
analysis of species-level interaction networks shows that they are In the above, the collective behaviour is beneficial to the species
typically modular (Sugihara et al. 1989; Meli
an & Bascompte 2004), but comes at a cost for the individual. However, another conflict in
and this has important implications for scenarios of biotic extinc- levels of selection occurs when the emergence of a novel strategy at
tions (Dunne et al. 2002). However, food web theory based on spe- the individual-scale results in a detrimental outcome at the macro-
cies graphs bears little empirical significance (Paine 1980; Polis scopic scale. A well-known example of such a selfish strategy is
1991): ecological interaction networks should be quantified based observed with the development of neoplastic cells within a cancer
on what individuals do, rather than just who eats whom among spe- tumour (Leroi et al. 2003; Merlo et al. 2006). This is a version of the
cies. Intraspecific variation leads to a modulation of the strength of commons problem, whereby ‘common-pool’ resources tend to be
interactions through time (Tylianakis et al. 2007; Ings et al. 2009), over-depleted by a few free-riders, at a cost for the society (Ostrom
and to a dynamic and individual-based view of ecological networks et al. 1999). This concept has been central in rethinking the manage-
(Ings et al. 2009; McCann & Rooney 2009; Meli
an et al. 2011). ment and institutional governance of environmental crises (Ostrom
Individual-based interaction networks build on a long-standing et al. 1999; Ostrom 2005). In ecology, understanding how conflicts
tradition in population ecology. Each individual differs from its operate among scales of organisation is essential to appraise the
neighbours, in part because its genetic makeup is unique, in part emergence of complexity and the modularity in individual-based
because its history is unique. Population biology and life-history the- interaction networks. As this principle is a general one, it should also
ory both strive to make sense of individual variation, and explore apply below the organismic level, an aspect to which I now turn.
whether regularities exist across individuals and what causes them
(for a recent review, see Bolnick et al. 2011). Even more impor-
Systems biology and reverse ecology
tantly, each individual typically interacts with a small number of its
conspecifics during its lifetime, and these opportunities are the One view of the emergence of complexity in biology involves auto-
means by which experience is acquired. In humans, the study of catalytic chemical reactions with molecules that are both substrates
networks of social interactions has become a large part of modern and catalysts (Maynard-Smith & Szathm
ary 1995). The resulting
sociology. The fact that individuals in conspecific assemblages are compartmentalisation of forms and functions appears to be one of
modularly related is of great importance for the parasites that thrive the most universal features of life, hinting to the fact that common
on us, because they may find it easier to spread within than across features of symmetry breaking lead to increasing complexity of life
modules. For instance, the rate of spread of an epidemic depends (Anderson 1972). Seeking for analogies between modularity in the
on the precise structure of this individual interaction network networks of cellular biology and that of ecology goes some way
(Keeling & Rohani 2008; Salath
e & Jones 2010). towards exploring the commonalities of pattern formation across
The problem of how to empirically measure individual-based net- scales. One illustration is Jeong et al. (2000)’s analysis of metabolic
works is a serious one. In food webs, both stable isotopic signatures networks showing that these display scale-free features: most of the
(Vanderklift & Ponsard 2003) and environmental DNA techniques enzymes within the network have only few connections, while a
may be used (Taberlet et al. 2012). In more generalised networks, few enzymes, so-called hubs, are highly connected. There is more
interactions can be measured directly via the real-time monitoring of than a point of analogy to make between metabolic networks and
individual movement (Salath
e & Jones 2010; Katz et al. 2011), or the ecological interaction networks: modular cell biology, sensu Hartwell
measurement of chemical cues, such as signalling across plants (Uns- et al. (1999), has now moved to the frontiers of ecology, and
icker et al. 2009) or quorum sensing in bacteria (Diggle et al. 2007). deserves special scrutiny here.
What if we could combine ecological networks and metabolic net-
works? Ecological interactions among species are often (though not
Conflicts among scales
always) mediated through chemical signalling. Exciting developments
In some cases of great relevance to ecology and evolution, individual have recently been achieved that shed a new light on this question.
interactions can lead to the emergence of altogether new behaviour Stolyar et al. (2007) studied the influence of a mutualism between a
at the macroscopic scale. In slime moulds, the multicellular habit is sulphate-reducing bacteria and a methanogen, which controls the
directly related to the formation of fruiting bodies (Bonner 1993). production of methane in many environments, such as the digestive
One major advantage of cell differentiation in multicellular organisms tract of ruminants. They were able to model this system as a single

© 2013 John Wiley & Sons Ltd/CNRS

10 J. Chave Review and Synthesis

metabolic network of the two mutualistic species. Their model accu-

rately predicted several ecologically relevant characteristics, such as ENVIRONMENT
the flux of metabolites and the ratio of cells in the two species dur-
ing growth. Hence, reconstructed metabolic networks and stoichiom-
etric models can serve not only to predict metabolic fluxes and
growth phenotypes of single organisms but also to capture key eco-
logical features in the interaction of simple bacterial communities. In
effect, this suggests that when the full metabolic network of a species
is known, its ecology is defined by the interactions of this network
with the environment, thus enabling us to infer from the structure of
biological system information about the environment in which it
evolved, a method called ‘reverse ecology’ (Parter et al. 2007).
Parter et al. (2007) computed the modularity of a large number of
bacterial species with known metabolic networks and justified that
the fraction of transcription factors out of the number of genes
could be used as a measure of environmental variability. They could Metabolic network boundaries
show that metabolic networks of organisms in variable environ-
ments were significantly more modular than networks of organisms
that evolved under more constant conditions (Fig. 4). This suggests Figure 5 Reverse ecology of a metabolic network. A schematic representation of
that modularity may be used as a measure of ecological niche the interaction of a metabolic network with its environment. Compounds
highlighted in red must be externally acquired from the environment. In the
breadth. Borenstein et al. (2008) further suggested that when the full
metabolic network of the bacteria Buchnera, the set of externally acquired
metabolic network of a species is known, its ecology is defined by compounds is of 61 chemicals of 314 compounds. Redrawn from Borenstein
the interactions of this network with the environment. Exploring et al. (2008).
formally which nodes of the network represents exogenously
acquired compounds results in defining an ensemble of ‘seed com- more labile across species. Core metabolic activities should be
pounds’ (Fig. 5). This concept was useful to distinguish which key highly resilient to failure, and this is achieved through a tight inte-
metabolic features were lost in parasitic organisms compared with gration. Together these studies suggest that the ‘reverse ecology’
free-living ones, and in confirming that the metabolic machinery of approach does not only help rethink classical questions in ecology,
parasites is simpler than that of free-living organisms. Finally, Pe- it is also an umbrella for a novel integration between ecology and
regr
ın-Alvarez et al. (2009) conducted a comparative study of the cell biology (Oberhardt et al. 2009; Gudelj et al. 2010).
structure of metabolic networks, and they have pointed to a limited Exploring network patterns across levels of organisation offers an
number of modules representing core activities, and conserved important lesson. The traditional scales of ecology are spatial and tem-
across the tree of life, while more peripheral activities tended to be poral, but the problem of scale could be also addressed in the
abstracted multidimensional space of an interaction network. A goal
0.5 of this section was to emphasise that reasoning about scales in ecol-
ogy leads naturally to question how modularity arises evolutionarily
and what its ecological consequences are. This viewpoint blurs the tra-
ditional view of the individual, and some central ecological questions
need to account for processes both within and among individuals.
0.4
Modularity (Qm)

SPATIAL PATTERNS OF DIVERSITY

The fourth and final theme is that of spatial patterning in biological

diversity. Looking at the spatial map of a tree species, the ecologist
0.3 asks why individuals are locally clustered and whether this clustering
changes across scales (Fig. 6). This is a general feature of spatial
species maps: individuals are patchily placed in space, and this
patchiness varies with the grain of observation (Hutchinson 1953).
A striking example is offered by glittering sea creatures. The unicel-
0.2 lular oceanic plankton Emiliana huxleyi forms massive blooms
Terrestrial
Facultative
Aquatic
association

generalist
specialist
Habitat

Habitat
Obligate

detectable using optical imagery (McClain 2009). If oceanic move-

ment is crucial in determining the spatial arrangement of E. huxleyi
populations over regions, other processes such as limited dispersal
explain the small-scale dynamics of these blooms (Tyrrell & Merico
Figure 4 Normalised modularity measure Q of bacterial metabolic networks vs.
2004). Indeed, dispersal limits the opportunities for species spread
the ecology of the organism. Organisms were grouped into classes ranging from
the most specialised to the least specialised. Terrestrial (soil) organisms appeared
even in the absence of environmental barriers. This feature is best
to have the most variable ecology. Mean and standard error of Q are presented illustrated using toy models of pattern formation (Box 1). One gen-
for each class, and the Q index was normalised to account for differences in eric feature emerging from toy models is that local dispersal is
network size across species. Redrawn from Parter et al. (2007). essential to explain pattern formation.

© 2013 John Wiley & Sons Ltd/CNRS

Review and Synthesis Pattern and scale in ecology 11

Ecologists have long been faced with the issue of scale mismatch
in the study of the dispersal process. In the late 19th century, the
British botanist Reid calculated that the recolonisation rate of Eng-
land by oaks after the last glacial period implied a colonisation
speed of c.a. 100 m/year (Clark et al. 1998). This was far more than
what ecologists had measured in the field. It is fortunate that theory
and empirical patterns may be reconciled. In a seminal mathematical
analysis, Kot et al. (1996) showed that the regional population
dynamics not only depends on the propensity of individuals to dis-
perse but also on the whole shape of the dispersal kernel (the prob-
ability P(r) that a propagule disperses r metres away from its parent,
in any direction).
R 1 The population front displaces at a speed propor-
tional to v ¼ 0 rPðr Þ  2prdr , the first moment of the distribu-
tion. If the dispersal kernel declines slowly with distance, for
example, a shape P(r) = A/(1 + ra), and if 2  a < 3, it may be
shown that the population spreads at an unbounded speed (Kot
Figure 6 Spatial distribution of 1404 trees of Mallotus penangensis, Euphorbiaceae et al. 1996). In this situation, traditional models of spatial dispersal
in the 50-ha plot of Pasoh, Malaysia. The Figure shows a three-dimensional fall apart: the speed of spread increases with time. Such anomalous
graph of clusters. The X- and Y-axes correspond to the length and width of the diffusion behaviours have been studied both in plants and animals
50-ha plot. The Z-axis corresponds to the value of the clustering parameter. The (Nathan 2006; Edwards et al. 2007), and they are of direct relevance
colour also corresponds to the value of this parameter (from green to black). As in the study of how species respond to global change and thus to
the clustering parameter increases down the Z-axis, larger clusters form. Each
determine the threshold for population and metapopulation extinc-
cluster is represented in the Figure by a circle centred at the centre of mass of
the cluster. The radius of the circle equals the mean distance of the trees in the
tions. Long-distance dispersal is also crucial to explain larger scale
cluster to its centre of mass. From Plotkin et al. (2002). biogeographical patterns such as beta-diversity (Chave & Leigh
2002) and island biogeography (Emerson & Gillespie 2008).

Figure 7 Dynamic patterning in two toy models: the voter model (top two rows) and the Ising model at zero temperature (bottom two rows) on a 256 9 256 lattice
with toroidal boundary conditions. Snapshots at time 4, 16, 64 and 256 (left to right). Lines 1 & 3 show an initial bubble of radius 180, whereas lines 2 and 4 show
random initial conditions with equal proportions. From Krapivsky et al. (2010).

© 2013 John Wiley & Sons Ltd/CNRS

12 J. Chave Review and Synthesis

of species, and species lifetime longer the tropics are a ‘museum of

Box1 Toy models of local dispersal biodiversity. Alternatively, the tropics may be more favourable to
speciation than temperate zones, and act as a ‘cradle’ of biodiversity
As dispersal is so closely related to pattern formation, it is useful
(perhaps because increased metabolism favours mutagenesis, Brown
to explore how this relation emerges in toy models. Fig. 7 illus-
et al. 2004). Unfortunately, observing latitudinal diversity patterns
trates two generic models of spatial patterning (the voter model
alone sheds no light on which of the alternatives is the more likely.
and the zero-temperature Ising model, see Krapivsky et al. 2010)
To disentangle this problem, as often in science, it is useful to look
where the local rules combined with the information exchange
out of the box, and explore alternative patterns. By reconstructing
between nearest neighbours generate a macroscopic pattern (see
phylogenetic trees in lineages that co-occur in tropical and temper-
more details in the Appendix S1). Both models of Fig. 7 are
ate regions, it is possible to test whether the tropical species are
assuming nearest-neighbour dispersal only. Now assume that,
more recent (suggesting higher tropical speciation rates) or more
with some probability m > 0, vacated sites are occupied by off-
ancient. Weir & Schluter (2007) applied this line of reasoning to
spring produced anywhere in the lattice. Even for very small m
birds and mammals. They plotted the time since divergence of sister
values, the spatial patterning depicted in the top part of Fig. 7 is
species pairs against the mid-point of occurrence of the species, and
destroyed, but the second model maintains its spatial structure
found that the splits in tropical species pairs tend to be older than
(for small enough m). One learns two important messages with
in temperate zones, pointing to a higher speciation rate at high lati-
these toy models. First, although both models could be used to
tudes compared with the tropics. This counter-intuitive result may
simulate the dynamics of two species in competition, apparently
be due to the fact that tropical lineages have undergone explosive
minor differences in the local dynamics of individuals result in
periods of diversification followed by a speciation slowing down
radically different emergent behaviours. Second, the addition of
(Rabosky & Lovette 2008). This analysis was criticised because the
long-distance dispersal strongly alters spatial patterning in some
molecular clock applied to infer times of divergence may not be
of the models. Hence, long-distance dispersal plays a key role on
accurate (Nabholz et al. 2009), and that the systematics of tropical
pattern formation in ecological community assembly.
birds remains poorly known (Mil
a et al. 2012). Also, in addition to
undergoing events of speciation and or extinction, lineages also
radiate in space: a tropical species may have a sister species outside
of the tropics (Wiens & Donoghue 2004). In a fascinating study of
the marine bivalve fossil record, Jablonski et al. (2006) reported the
Global diversity patterns
time of first occurrence of bivalve lineages, and they showed that
Patterns of regional species occurrence and abundance have long the vast majority of these lineages had originated in the tropics (in
been the focus of biogeography. A general biogeographical pattern spite of the strong sampling bias towards temperate zones). They
is the latitudinal diversity gradient, according to which the tropics thus proposed an explanation for latitudinal diversity patterns where
have more species than temperate zones (Hillebrand 2004). Thanks most of the lineages originate in the tropics, yet a fraction of these
to large-scale DNA-based screens of microbial diversity (Pace lineages subsequently expand polewards. This example illustrates
1997), latitudinal diversity gradients have now been also quantified that the latitudinal diversity gradient, indeed any spatial pattern, can-
in microorganisms (Fuhrman et al. 2008). not be studied in splendid isolation.
In an important meta-analysis, Hillebrand (2004) performed an
intriguing test. He included both studies where species richness was
Contingency in local species assemblages
known from occurrences in grids and studies where species richness
was known from local sites, possibly scattered unevenly across the Ecologists have long remained oblivious to large-scale process, and
globe. Although the latitudinal diversity gradient was observed in have ignored that the biodiversity problem is contingent on pro-
both cases, the decline of diversity with latitude was steeper and cesses that act over much larger scales than the ones of classical
more marked in the former case. The latitudinal gradient of diver- ecological enquiry and should be readdressed by incorporating data
sity is easier to detect if the local effects of biotic interaction, dis- from systematics, biogeography and palaeontology into analyses of
persal and stochasticity are averaged out in a coarse grained metric community assembly (Ricklefs 1987). Hubbell (2001) proposed a
of diversity. Whether to treat biological diversity in a spatially expli- quantitative framework to bridge these spatial scales. In Hubbell’s
cit setting or not, and whether to consider the individual-scale or a model, individuals effectively compete for space in a local area. A
grid-based description of diversity (Durrett & Levin 1994), has species may go extinct locally, but the diversity is replenished
come to be one of the most important cornerstones of ecological through the continuous immigration of individuals from outside.
enquiry. This distinction bears analogies with the distinction Thus, the local and the regional scale are coupled through dispersal.
between the Eulerian (grid-based) vs. Lagrangian (particle-based) Finally, species may go extinct at the regional scale, but the regional
description of fluid movement in fluid mechanics (Flierl et al. 1999). species pool is replenished through an implicit parameter that
One recent avatar of the debate of grid-based vs. individual-based defines speciation. This simple model couples some of the crucial
description has manifested itself in species distribution models features of species diversity: stochastic local dynamics, coupling
(Elith & Leathwick 2009). across scales and regional-scale dynamics. To facilitate the mathe-
Back to the latitudinal diversity gradient, attempts to provide a matical analysis of this model, Hubbell (2001) assumed that all indi-
mechanistic understanding must combine ecological and evolution- viduals have the same prospects of reproduction and or death. This
ary theory (Mittelbach et al. 2007). As the tropics tend to have a neutral premise has spurred considerable controversy: how could a
more stable climate, tropical organisms seldom are adapted to frost. theory of biodiversity be based on the ignorance of species differ-
Thus, tropical life is thought to be more suitable for a wide range ences? This is a case of exploring whether the details of the local

© 2013 John Wiley & Sons Ltd/CNRS

Review and Synthesis Pattern and scale in ecology 13

dynamics really matter to classical diversity patterns. Indeed, in spite been achieved through a thorough rethinking of old questions: the
of its simplicity, this model was successful at reproducing the spe- reconciliation of the ecological and the evolutionary time scales;
cies abundance distribution, or the species area curve (Hubbell advances in ecosystem science and biogeoscience; the emergence of
2001). Thus, arguably local details do not matter to understanding individual-based networks (and the increased focus on metabolic
some patterns of diversity at the regional scale, at least patterns such networks); and the integration of community ecology and biogeog-
as the species abundance distribution (for an explicit multi-scale raphy, with a focal role of dispersal as the fundamental process that
framework generalising Hubbell’s model, see Leibold et al. 2004). bridges across spatial scales. These themes are intertwined. For
Thus, if we are to quantify the imprint of biological processes on instance, I have purposefully left aside functional trait ecology, a
community assembly, beyond neutrality, we need to search for other topic that cuts across all four themes.
community-wide patterns than simply the species abundance distri- Although the problem of scale is arguably one of the most
bution. Measures of ecological distances based on ecological traits important in ecology, it should not be inferred that ecology is all
have been proposed to quantify community-wide character displace- about scale-free networks and power laws. As ecology was making
ment (Dayan & Simberloff 2005; Kraft et al. 2008; Losos 2008). In definite and rapid progress, a line of research was in search of the
addition, metrics related to the evolutionary distances of locally co- grand unified theory for ecology. Science always benefits from shar-
occurring species have featured prominently in this research area, in ing ideas across disciplines, but the notion that, unlike physics, ecol-
the wake of Webb (2000)’s seminal paper. Webb (2000) suggested ogy suffers from a lack of general laws (Lawton 1999) stems in part
that if competition really shapes community assembly, then co- from a misperception of the successes of physics (Anderson 1972).
occurring species should be phylogenetically more dissimilar locally Goldenfeld & Woese (2011) recently developed the view that phys-
than in the regional species pool. Conversely, they should be phylo- ics has not been much luckier than biology in grappling with the
genetically more similar locally than in the region if some lineages study of complex systems, a study that biology was faced to at the
have specific adaptations for the habitat that the species assemblage outset. This suggests that in approaching novel frontiers of the
occupies (think of succulence in desert-adapted plants). This idea study of complex ecological systems we need to pause about the
has generated much exciting recent research (Emerson & Gillespie challenge ahead of us, and avoid the development of language-cul-
2008; Cavender-Bares et al. 2009 for recent reviews). ture to explain away the conceptual difficulties (Goldenfeld & Wo-
Lawton (1999) famously wrote that it was time to move on from ese 2011). Once we enter the realm of complex systems, neither
community ecology. His point was that local species assemblages physics nor biology are well equipped to progress.
are too complex and that intermediate scales have so much contin- Levin’s (1992) message was that a key to develop a predictive the-
gency that useful generalisations are hard to find. The decade fol- ory for ecology was in examining the patterns in nature and in
lowing Lawton (1999) has shown that community ecology is developing theories that help assimilate observations across scales.
actually a most fertile ground for ecological research, not only I have argued that with the avalanche of data our discipline is accu-
because it is the scale at which key conservation issues should be mulating, this lesson remains very true today and it should motivate
addressed (Simberloff 2004) but also because generalisations can be us ecologists to combine empirical and theoretical research, but also
found across communities based on simple principles (Hubbell embrace both the holist and the reductionist approaches, rather
2001; Brown et al. 2004). To their profit, ecologists have now than specialise in either one of these.
abandoned the view that ecology should only be performed in
small plots or Petri dishes but across sites interconnected through
ACKNOWLEDGEMENTS
dispersal, and decoupled the details of the local community (Lei-
bold et al. 2004), and Ricklefs (1987)’s plea for more integration I am grateful to U Alon, D Baldocchi, S Ellner, P Falkowski, S
with systematics, biogeography and palaeontology has now been Redner, T Yoshida and R Vargas for allowing me to reprint illustra-
realised. tions, and to F Jabot, S Levin, M R
ejou-M
echain, C Th
ebaud and
two anonymous reviewers for their constructive critiques. It is a
pleasure to acknowledge financial support from Fondation pour la
OUTLOOK
Recherche sur la Biodiversit
e, CNES, Agence Nationale pour la
Reflecting on the recent past of such crucial concepts as pattern and Recherche (ANR; METABAR project), and from Investissement
scale illustrates how fast our discipline has advanced and how well it d’Avenir grants of the ANR (CEBA: ANR-10-LABX-0025; TULIP:
has assimilated a cross-disciplinary view of the study of nature. It ANR-10-LABX-0041).
also points to new frontiers. The increased realisation that environ-
mental problems impact our livelihoods across spatial and temporal
REFERENCES
scales has fostered much research in our discipline. An array of tech-
nological and conceptual developments has brought new inroads Abrams, P. & Matsuda, H. (1997). Prey evolution as a cause of predator–prey
into these key problems. Such developments have increased aware- cycles. Evolution, 51, 1740–1748.
Allen, A.P., Gillooly, J.F. & Brown, J.H. (2005). Linking the global carbon cycle
ness that it is essential to study ecological questions across scales,
to individual metabolism. Funct. Ecol., 19, 202–213.
although limits to this statement should be pointed out. For Anderson, P.W. (1972). More is different. Science, 177, 393–396.
instance, Wheatley & Johnson (2009) have recently reviewed the lit- Antoine, D. & Morel, A. (1996). Oceanic primary production 1. Adaptation of a
erature of wildlife research and reported that arbitrariness in the spectral light-photosynthesis model in view of application to satellite
choice of study scale remains prevalent today even though these chlorophyll obserevations. Global Biogeochem. Cycles, 10, 43–55.
questions are of obvious relevance to conservation planning. Baldocchi, D.D. (2003). Assessing the eddy covariance technique for evaluating
Here, I have selected four themes because they illustrate tradi- carbon dioxide exchange rates of ecosystems: past, present and future. Glob.
Change Biol., 9, 479–492.
tional questions in ecology where remarkable recent progress has

© 2013 John Wiley & Sons Ltd/CNRS

14 J. Chave Review and Synthesis

Behrenfeld, M.J. & Falkowski, P. (1997). Photosynthetic rates derived from Fuhrman, J.A., Steele, J.A., Hewson, I., Schwalbach, M.S., Brown, M.V., Green,
satellite-based chlorophyll concentration. Limnol. Oceanogr., 42, 1–20. J.L. et al. (2008). A latitudinal diversity gradient in planktonic marine bacteria.
Berelman, J.E. & Kirby, J.R. (2009). Deciphering the hunting strategy of a Proc. Natl. Acad. Sci. U.S.A., 105, 7774–7778.
bacterial wolfpack. FEMS Microbiol. Rev., 33, 942–957. Fussmann, G.F., Loreau, M. & Abrams, P.A. (2007). Eco-evolutionary dynamics
Biro, P.A. & Stamps, J.A. (2010). Do consistent individual differences in of communities and ecosystems. Funct. Ecol., 21, 465–477.
metabolic rate promote consistent individual differences in behavior? Trends Gienapp, P., Teplisky, C., Alho, J.S., Mills, J.A. & Meril€a, J. (2008). Climate
Ecol. Evol., 25, 653–659. change and evolution: disentangling environmental and genetic responses. Mol.
Boag, P.T. (1983). The heritability of external morphology in Darwin’s ground Ecol., 17, 167–178.
finches (Geospiza) on Isla Major, Gal
apagos. Evolution, 37, 877–894. Gillooly, J.F., Brown, J.H., West, G.B., Savage, V.M. & Charnov, E.L. (2001).
Bolker, B. & Pacala, S.W. (1997). Using moment equations to understand Effects of size and temperature on metabolic rate. Science, 293, 2248–2251.
stochastically driven spatial pattern formation in ecological systems. Theor. Goldenfeld, N. & Woese, C. (2011). Life is physics: evolution as a collective
Popul. Biol., 52, 179–197. phenomenon far from equilibrium. Annu. Rev. Condens. Matter Phys., 2, 375–
Bolnick, D.I., Amarasekare, P., Araujo, M.S., Burger, R., Levine, J.M., Nowak, M. 399.
et al. (2011). Why intraspecific trait variation matters in community ecology. Golley, F.B. (1993). A History of the Ecosystem Concept in Ecology: More Than the Sum
Trends Ecol. Evol., 26, 183–192. of the Parts. Yale University Press, New Haven, CT, 274 pp.
Bonner, J.T. (1993). Life Cycles Reflections of an Evolutionary Biologist. Princeton Grant, P.R. & Grant, B.R. (2006). Evolution of character displacement in
University Press, Princeton NJ, 209pp. Darwin’s finches. Science, 313, 224–226.
Borenstein, E., Kupiec, M., Feldman, M.W. & Ruppin, E. (2008). Large-scale Grant, P.R. & Grant, B.R. (2008). How and Why Species Multiply. The Radiation of
reconstruction and phylogenetic analysis of metabolic environments. Proc. Darwin’s Finches. Princeton University Press, Princeton NJ, 218 pp.
Natl. Acad. Sci. U.S.A., 105, 14482–14487. Gregg, W.W., Casey, N.W. & McClain, C.R. (2005). Recent trends in ocean
Brown, J.H., Gillooly, J.F., Allen, A.P., Savage, V.M. & West, G.B. (2004). chlorophyll. Geophys. Res. Lett., 32, L03606.
Toward a metabolic theory of ecology. Ecology, 85, 1771–1789. Gudelj, I., Weitz, J.S., Ferenci, T., Horner-Devine, M.C., Marx, C.J., Meyer, J.R.
Calder, W.A. (1984). Size Function, and Life History. Harvard University Press, et al. (2010). An integrative approach to understanding microbial diversity:
Cambridge, MA. from intracellular mechanisms to community structure. Ecol. Lett., 13, 1073–
Cavender-Bares, J., Kozak, K.H., Fine, P.V.A. & Kembel, S.W. (2009). The 1084.
merging of community ecology and phylogenetic biology. Ecol. Lett., 12, 693– Gurney, K.R., Law, R.M., Denning, A.S., Rayner, P.J., Baker, D., Bousquet, P.
715. et al. (2002). Towards robust regional estimates of CO2 sources and sinks
Chave, J. & Leigh, E.G. Jr (2002). A spatially explicit neutral model of beta- using atmospheric transport models. Nature, 415, 626–630.
diversity in tropical forests. Theor. Popul. Biol., 62, 153–168. Hairston, N.G. Jr, Ellner, S.P., Geber, M.A., Yoshida, T. & Fox, J.A. (2005).
Clark, J.S., Fastie, C., Hurtt, G., Jackson, S.T., Johnson, C., King, G.A. et al. Rapid evolution and the convergence of ecological and evolutionary time.
(1998). Reid’s paradox of rapid plant migration. Bioscience, 48, 13–24. Ecol. Lett., 8, 1114–1127.
Dayan, T. & Simberloff, D. (2005). Ecological and community-wide character Harmon, L.J., Matthews, B., Des Roches, S., Chase, J.M., Shurin, J.B. & Schluter,
displacement: the next generation. Ecol. Lett., 8, 875–894. D. (2009). Evolutionary diversification in stickleback affects ecosystem
Diggle, S.P., Griffin, A.S., Campbell, G.S. & West, S.A. (2007). Coorperation and functioning. Nature, 458, 1167–1170.
conflict in quorum-sensing bacterial populations. Nature, 450, 411–415. Hartwell, L.H., Hopfield, J.H., Leibler, S. & Murray, A.W. (1999). From
Dunne, J.A., Williams, R.J. & Martinez, N.D. (2002). Network structure and molecular to modular cell biology. Nature, 402, C47–C52.
biodiversity loss in food webs: robustness increases with connectance. Ecol. Henson, S.A., Sarmiento, J.L., Dunne, J.P., Bopp, L., Lima, I., Doney, S.C. et al.
Lett., 5, 558–567. (2010). Detection of anthropogenic climate change in satellite records of
Durrett, R. & Levin, S.A. (1994). The importance of being discrete (and spatial). ocean chlorophyll and productivity. Biogeosciences, 7, 621–640.
Theor. Pop, Biol., 46, 363–394. Herrel, A., Podos, J., Huber, S.K. & Hendry, A.P. (2005). Bite performance and
Edwards, A.M., Phillips, R.A., Watkins, N.W., Freeman, M.P., Murphy, E.J., morphology in a population of Darwin’s finches: implication for the evolution
Afanasyev, V. et al. (2007). Revisiting L
evy flight search patterns of wandering of beak shape. Funct. Ecol., 19, 43–48.
albatrosses, bumblebees and deer. Nature, 449, 1044–1049. Hetherington, A.M. & Woodward, F.I. (2003). The role of stomata in sensing
Elith, J. & Leathwick, J.R. (2009). Species distribution models: ecological and driving environmental change. Nature, 424, 901–908.
explanation and prediction across scales. Annu. Rev. Ecol. Evol. Syst., 40, 677– Hillebrand, H. (2004). On the generality of the latitudinal diversity gradient. Am.
697. Nat., 163, 192–211.
Emerson, B.C. & Gillespie, R.G. (2008). Phylogenetic analysis of community Hubbell, S.P. (2001). The Unified Neutral Theory of Biodiversity and Biogeography.
assembly and structure over space and time. Trends Ecol. Evol., 23, 619–630. Princeton University Press, Princeton, NJ.
Enquist, B.J., Economo, E.P., Huxman, T.E., Allen, A.P., Ignace, D.D. & Hutchinson, G.E. (1953). The concept of pattern in ecology. Proc. Acad. Nat. Sci.
Gillooly, J.F. (2003). Scaling metabolism from organisms to ecosystems. Philadelphia, 105, 1–12.
Nature, 423, 639–642. Ings, T.C., Montoya, J.M., Bascompte, J., Bl€uthgen, N., Brown, L., Dormann,
Falkowski, P., Scholes, R.J., Boyle, E., Canadell, J., Canfield, D., Elser, J. et al. C.F. et al. (2009). Ecological networks – Beyond food webs. J. Anim. Ecol., 78,
(2000). The global carbon cycle: a test of our knowledge of Earth as a system. 253–269.
Science, 290, 291–296. Ives, A.R. & Carpenter, S.R. (2007). Stability and diversity of ecosystems. Science,
Falkowski, P.G., Fenchel, T. & Delong, E.F. (2008). The microbial engines that 317, 58–62.
drive Earth’s biogeochemical cycles. Science, 320, 1034–1039. Jablonski, D., Roy, K. & Valentine, J.W. (2006). Out of the tropics: evolutionary
Field, C.B., Behrenfeld, M.J., Randerson, J.T. & Falkowski, P. (1998). Primary dynamics of the latitudinal diversity gradient. Science, 314, 102–106.
production of the biosphere: integrating terrestrial and oceanic components. Jeong, H., Tombor, B., Albert, R., Oltvai, Z.N. & Barab
asi, A.-L. (2000). The
Science, 281, 237–240. large-scale organization of metabolic networks. Nature, 407, 651–654.
Flierl, G., Gr€unbaum, D., Levin, S.A. & Olson, D. (1999). From individuals to Katz, Y., Tunstrøm, K., Ioannou, C.C., Huepe, C. & Couzin, I.D. (2011).
aggregations: the interplay between behavior and physics. J. Theor. Biol., 196, Inferring the structure and dynamics of interactions in schooling fish. Proc.
397–454. Natl. Acad. Sci. U.S.A., 108, 18720–18725.
Follows, M.J., Dutkiewicz, S., Grant, S. & Chisholm, S.W. (2007). Emergent Keeling, M.J. & Rohani, P. (2008). Modeling Infectious Diseases in Humans and
biogeography of microbial communities in a model ocean. Science, 315, 1843– Animals. Princeton University Press, Princeton, NJ, 408 pp.
1846. Kleiber, M. (1947). Body size and metabolic rate. Physiol. Rev., 27, 511–541.
Frank, S.A. & Slatkin, M. (1992). Fisher’s fundamental theorem of natural Kot, M., Lewis, M.A. & van den Driessche, P. (1996). Data and the spread of
selection. Trends Ecol. Evol., 7, 92–95. invading organisms. Ecology, 77, 2027–2042.

© 2013 John Wiley & Sons Ltd/CNRS

Review and Synthesis Pattern and scale in ecology 15

Kraft, N.J.B., Valencia, R. & Ackerly, D.D. (2008). Functional traits and Moss, R.H., Edmonds, J.A., Hibbard, K.A., Manning, M.R., Rose, S.K., van
niche-based tree community assembly in an Amazonian forest. Science, 322, Vuuren, D.P. et al. (2010). The next generation of scenarios for climate
580–582. change research and assessment. Nature, 463, 747–756.
Krapivsky, P.R., Redner, S. & Ben-Naim, E. (2010). A Kinetic View of Statistical Nabholz, B., Gl
emin, S. & Galtier, N. (2009). The erratic mitochondrial clock:
Physics. Cambridge University Press, Cambridge, UK. variations of mutation rate, not population size, affect mtDNA diversity
van der Laan, J.D. & Hogweg, J. (1995). Predator-prey coevolution: interactions across birds and mammals. BMC Evol. Biol., 9, 54.
across different timescales. Proc. R. Soc. Lond. B, 259, 35–42. Nathan, R. (2006). Long-distance dispersal of plants. Science, 313, 786–788.
Lawton, J.H. (1999). Are there general laws in ecology? Oikos, 84, 177–192. Niklas, K.J. (1994). Plant Allometry. University of Chicago, Chicago, IL.
Le Qu
er
e, C., Sandy P. Harrison, S.P., Prentice, I.C., Buitenhuis, E.T., Aumont, Oberhardt, M.A., Palsson, B.Ø. & Papin, J.A. (2009). Applications of genome-
O., Bopp, L. et al. (2005). Ecosystem dynamics based on plankton functional scale metabolic reconstructions. Mol. Syst. Biol., 5, 320.
types for global ocean biogeochemistry models. Glob. Change Biol., 11, 2016– Ostrom, E. (2005). Understanding Institutional Diversity. Princeton University Press,
2040. Princeton, NJ, 376 pp.
Le Qu
er
e, C., Raupach, M.R., Canadell, J.P., Marland, G., Bopp, L., Ciais, P. Ostrom, E., Burger, J., Field, C.B., Norgaard, N.B. & Policansky, D. (1999).
et al. (2009). Trends in the sources and sinks of carbon dioxide. Nat. Geosci., 2, Revisiting the commons: local lessons, global challenges. Science, 284, 278–282.
831–836. Pace, N.R. (1997). A molecular view of microbial diversity and the biosphere.
Leibold, M.A., Holyoak, M., Mouquet, N., Amarasekare, P., Chase, J.M., Science, 276, 734–740.
Hoopes, M.F. et al. (2004). The metacommunity concept: a framework for Paine, R.T. (1980). Linkage, interaction strength and community infrastructure. J.
multi-scale community ecology. Ecol. Lett., 7, 601–613. Anim. Ecol., 49, 666–685.
Leroi, A.M., Kofoupanou, V. & Burt, A. (2003). Cancer selection. Nat. Rev. Palkovacs, E.P., Marshall, M.C., Lamphere, B.A., Lynch, B.R., Weese, D.J.,
Cancer, 3, 226–231. Fraser, D.F. et al. (2009). Experimental evaluation of evolution and
Levin, S.A. (1992). The problem of pattern and scale in ecology. Ecology, 73, coevolution as agents of ecosystem change in Trinidadian streams. Philos.
1943–1967. Trans. R. Soc. Lond., B, Biol. Sci., 364, 1617–1628.
Lloyd, J. & Taylor, J.A. (1994). On the temperature dependence of soil Parmesan, C. (2006). Ecological and evolutionary responses to recent climate
respiration. Funct. Ecol., 8, 315–323. change. Annu. Rev. Ecol. Evol. Syst.., 37, 637–669.
L

opez-Urrutia, A., San Martin, E., Harris, R.P. & Irigoien, X. (2006). Scaling the Parter, M., Kashtan, N. & Alon, U. (2007). Environmental variability and
metabolic balance of the oceans. Proc. Natl. Acad. Sci. U.S.A., 103, 202–213. modularity of bacterial metabolic networks. BMC Evol. Biol., 7, 169.
Losos, J.B. (2008). Phylogenetic niche conservatism, phylogenetic signal and the Peregr
ın-Alvarez, J., Sanford, C. & Parkinson, J. (2009). The conservation and
relationship between phylogenetic relatedness and ecological similarity among evolutionary modularity of metabolism. Genome Biol., 63, R63.
species. Ecol. Lett., 11, 995–1007. Plotkin, J., Chave, J. & Ashton, P.S. (2002). Cluster analysis of spatial patterns in
Luyssaert, S., Inglima, I., Jung, M., Richardson, A.D., Reichstein, M., Papale, D. Malaysian tree species. Am. Nat., 160, 629–644.
et al. (2007). CO2 balance of boreal, temperate, and tropical forests derived Polis, G.A. (1991). Complex trophic interactions in deserts: an empirical critique
from a global database. Glob. Change Biol., 13, 2509–2537. of food web theory. Am. Nat., 138, 123–155.
MacArthur, R.H. (1972). Geographical Ecology. Patterns in the Distribution of Species. Rabosky, D.L. & Lovette, I.J. (2008). Explosive evolutionary radiations:
Harper and Row, New York, NY. decreasing speciation or increasing extinction through time? Evolution, 62,
Malhi, Y., Baldocchi, D.D. & Jarvis, P.G. (1999). The carbon balance of tropical, 1866–1875.
temperate and boreal forests. Plant Cell Env., 22, 715–740. Reznick, D.N., Shaw, F.H., Rodd, F.H. & Shaw, R.G. (1997). Evaluation of the
Mallarino, R., Grant, P.R., Grant, B.R., Herrel, A., Kuo, W.P. & Abzhanov, A. rate of evolution in natural populations of guppies (Poecilia reticulata). Science,
(2011). Two developmental modules establish 3D beak-shape variation in 275, 1934–1937.
Darwin’s finches. Proc. Natl. Acad. Sci. U.S.A., 108, 4057–4062. Ricklefs, R.E. (1987). Community diversity: relative roles of local and regional
Maynard-Smith, J. & Szathm
ary, E. (1995). The Major Transitions in Evolution. WH processes. Science, 235, 167–171.
Freeman, New York, 346 pp. Running, S.W., Nemani, R.R., Heinsch, F.A., Zhao, M., Reeves, M. &
McCann, K.S. & Rooney, N. (2009). The more food webs change, the more Hashimoto, H. (2004). A continuous satellite-derived measure of global
they stay the same. Philos. Trans. R. Soc. Lond., B, Biol. Sci., 364, 1789–1801. terrestrial primary production. Bioscience, 54, 547–560.
McClain, C.R. (2009). A decade of satellite ocean color observations. Ann. Rev. Salath
e, M. & Jones, J.H. (2010). Dynamics and control of diseases in networks
Mar. Sci., 1, 19–42. with community structure. PLoS Comput. Biol., 6, e1000736.
Medvigy, D., Wofsy, S.C., Munger, J.W. & Moorcroft, P.R. (2010). Responses of Savage, V.M., Deeds, E.J. & Fontana, W. (2008). Sizing up allometric scaling
terrestrial ecosystems and carbon budgets to current and future environmental theory. PLoS Comput. Biol., 4, 17.
variability. Proc. Natl. Acad. Sci. U.S.A., 107, 8275–8280. Savolainen, O., Pyh€aj€arvi, T. & Kn€urr, T. (2007). Gene flow and local adaptation
Meli
an, C.J. & Bascompte, J. (2004). Food web cohesion. Ecology, 85, 352–358. in trees. Annu. Rev. Ecol. Evol. Syst., 38, 595–619.
Meli
an, C.J., Vilas, C., Bald
o, F., Gonz
alez-Orteg
on, E., Drake, P. & Williams, Schoener, T.W. (2011). The newest synthesis: understanding the interplay of
R.J. (2011). Eco-evolutionary dynamics of individual-based food webs. Adv. evolutionary and ecological dynamics. Science, 331, 426–429.
Ecol. Res., 45, 225–268. Silvertown, J. (2009). A new dawn for citizen science. Trends Ecol. Evol., 24, 467–
Merlo, L.M.F., Pepper, J.W., Reid, B.J. & Maley, C.C. (2006). Cancer as an 471.
evolutionary and ecological process. Nat. Rev. Cancer, 6, 924–935. Simberloff, D. (2004). Community ecology: is it time to move on? Am. Nat.,
Mil
a, B., Tavares, E.S., Salda~ na, A.M., Karubian, J., Smith, T.B. & Baker, A.J. 163, 787–799.
(2012). A trans-Amazonian screening of mtDNA reveals deep intraspecific Simon, H.A. (1962). The architecture of complexity. Proc. Amer. Phil. Soc., 106,
divergence in forest birds and suggests a vast underestimation of species 467–482.
diversity. PLoS ONE, 7, e40541. Stolyar, S., van Dien, S., Hillesland, K.L., Pinel, N., Lie, T.J., Leigh, J.A. et al.
Mittelbach, G.G., Schemske, D.W., Cornell, H.V., Allen, A.P., Brown, J.M., (2007). Metabolic modeling of a mutualistic microbial community. Mol. Syst.
Bush, M.B. et al. (2007). Evolution and the latitudinal diversity gradient: Biol., 3, 92.
speciation, extinction and biogeography. Ecol. Lett., 10, 315–331. Sugihara, G., Schoenly, K. & Trombla, A. (1989). Scale invariance in food web
Moorcroft, P.R., Hurtt, G.C. & Pacala, S.W. (2001). A method for scaling properties. Science, 245, 48–52.
vegetation dynamics: the Ecosystem Demography model (ED). Ecol. Monogr., Taberlet, P., Coissac, E., Pompanon, F., Brochmann, C. & Willerslev, E. (2012).
71, 557–586. Towards next-generation biodiversity assessment using DNA metabarcoding.
Mori, S., Yamaji, K., Ishida, A., Prokushin, S.G., Masyagina, O.V., Hagihara, A. Mol. Ecol., 21, 2045–2050.
et al. (2010). Mixed-power scaling of whole plant respiration from seedlings to Tans, P. P., Fung, I.Y. & Takahashi, T. (1990). Observational constraints on the
giant trees. Proc. Natl. Acad. Sci. U.S.A., 107, 1447–1451. global atmospheric CO2 budget. Science, 247, 1431–1438.

© 2013 John Wiley & Sons Ltd/CNRS

16 J. Chave Review and Synthesis

Tylianakis, J.M., Tscharntke, T. & Lewis, O.T. (2007). Habitat modification alters West, G.B., Brown, J.H. & Enquist, B.J. (1997). A general model for the origin
the structure of tropical host-parasitoid food webs. Nature, 445, 202–205. of allometric scaling laws in biology. Science, 276, 122–126.
Tyrrell, T. & Merico, A. (2004). Emiliania huxleyi: bloom observations and the Wheatley, M. & Johnson, C. (2009). Factors limiting our understanding of
conditions that induce them. In: Coccolithophores. From Molecular Processes to ecological scale. Ecol. Complex., 6, 151–159.
Global Impact (eds Thierstein, H.R. & Young, J.R.). Springer, Berlin, Wiens, J.J. & Donoghue, M.J. (2004). Historical biogeography, ecology and
Heidelberg, Germany, pp. 75–97. species richness. Trends Ecol. Evol., 19, 639–644.
Uitz, J., Claustre, H., Gentili, B. & Stramski, D. (2010). Phytoplankton class- Wortmann, U.G. & Paytan, A. (2004). Rapid variability of seawater chemistry
specific primary production in the world’s oceans: Seasonal and interannual over the past 130 million years. Science, 337, 334–336.
variability from satellite observations. Glob. Biogeochem. Cycles, 24, GB3016. Yoshida, T., Jones, L.E., Ellner, S.P., Fussman, G.F. & Hairston, N.G. Jr (2003).
Unsicker, S.B., Kunert, G. & Gershenzon, J. (2009). Protective perfumes: the Rapid evolution drives ecological dynamics in a predator-prey system. Nature,
role of vegetative volatiles in plant defense against herbivores. Curr. Opin. 424, 303–306.
Plant Biol., 12, 479–485. Yvon-Durocher, G., Caffrey, J.M., Cescatti, A., Dossena, M., del Giorgio, P.,
Vanderklift, M.A. & Ponsard, S. (2003). Sources of variation in consumer-diet Gasol, J.M. et al. (2012). Reconciling the temperature dependence of
d15N enrichment: a meta-analysis. Oecologia, 136, 169–182. respiration across timescales and ecosystem types. Nature, 487, 472–476.
Vargas, R., Detto, M., Baldocchi, D.D. & Allen, M.F. (2010). Multiscale analysis
of temporal variability of soil CO2 production as influenced by weather and
vegetation. Glob. Change Biol., 16, 1589–1605. SUPPORTING INFORMATION
Vaulot, D., Eikrem, W., Viprey, M. & Moreau, H. (2008). The diversity of small
eukaryotic phytoplankton (< 3lm) in marine ecosystems. FEMS Microbiol. Rev.,
Additional Supporting Information may be downloaded via the online
32, 795–820. version of this article at Wiley Online Library(www.ecologyletters.com).
Velicer, G.J. & Yu, Y.N. (2003). Evolution of novel cooperative swarming in the
bacterium Myxococcus xanthus. Nature, 425, 75–78.
Wagner, G.P., Pavlicev, M. & Cheverud, J.M. (2007). The road to modularity. Editor, Jordi Bascompte
Nat. Rev. Genet, 8, 921–931.
Manuscript received 22 September 2012
Webb, C.O. (2000). Exploring the phylogenetic structure of ecological
communities: an example for rain forest trees. Am. Nat., 156, 145–155.
First decision made 29 October 2012
Weir, J.T. & Schluter, D. (2007). The latitudinal gradient in recent speciation and Manuscript accepted 9 November 2012
extinction rates of birds and mammals. Science, 315, 1574–1576.

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