ECOTOXICOLOGY: A Comprehensive Treatment - Chapter 33 docx

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33
Patterns and Processes:
The Relationship
between Species
Diversity and Ecosystem
Function
The economies of the Earth would grind to a halt without the services of ecological life-support
systems
(Costanza et al. 1997)
The biodiversity–ecosystem function linkage appears to be another concept for which enthusiasm
outweighs supportive evidence.
(Schwartz et al. 2000)
33.1 INTRODUCTION
Afundamental characteristic of most biological systems is their remarkable diversity. Our accounting
of global diversity should not be restricted to the large number of species inhabiting the biosphere,
estimated to be between 10 and 100 million (Wilson 1999), but should also include the genetic
variation residing within each species as well as the functional diversity of processes for which they
are responsible. The rapid loss of genetic, species, and functional diversity resulting from habitat
destruction, exotic species, climate change, overharvesting, chemical stressors, and other sources of
anthropogenic disturbance is a significant environmental concern with global consequences. Argu-
ments for the protection of biological diversity have traditionally been based on moral or aesthetic
perspectives. However, researchers and policymakers are becoming increasingly aware that species
also provide ecological goods and services that are essential for human welfare. In this chapter,
we describe theoretical and empirical evidence that supports the hypothesis that species diversity
controls ecosystem function, describe the limitations in our understanding of this relationship, and
discuss theimplications for ecotoxicology. Becauseof the controversysurrounding thesignificance of
the diversity–ecosystem function relationship and its practical importance in managing ecosystems,
the topic has received considerable attention in the ecological literature. The recent comprehensive
review published by Hooper et al. (2005) is especially noteworthy because coauthors included both
proponents and critics of the diversity–ecosystem function relationship. This review, which charac-

terizes major points of agreement and uncertainty, represents a broad consensus within the scientific
community (Table 33.1).
Because reduced genetic, species, and functional diversity resulting from contaminants
has important consequences for the services provided by ecosystems, we believe that the
diversity–ecosystem function relationship has significant implications for ecotoxicology. We first
review the observational and experimental studies that support the theoretical relationship between
715
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716 Ecotoxicology: A Comprehensive Treatment
TABLE 33.1
Major Points of Agreement and Remaining Uncertainty within the Ecological Community
Regarding the Relationship between Species Diversity and Ecosystem Function
Points of certainty:
1. Species and functional diversities influence ecosystem function.
2. Anthropogenic alteration of ecosystem function and related services has been well documented.
3. The relationship between species diversity and ecosystem processes is context-dependent and varies among ecosystem
properties and types.
4. The relative insensitivity of some ecosystem processes to loss of species or changes in composition results from the
redundancy of some species, the fact that some species contribute relatively little to ecosystem function, and the dominant
influence of abiotic environmental factors.
5. As spatial and temporal variability increases, more species are required to maintain the stability of ecosystem processes
and services.
Points of high confidence:
1. Although some combinations of species are complementary and can increase ecosystem function, environmental factors
can influence the importance of complementarity.
2. The effects of exotic species are determined by community composition and are generally lower in communities with high
species richness.
3. Variation in the sensitivity and susceptibility of species to anthropogenic stressors within a community can provide stability
to ecosystem processes.

Points of uncertainty and the need for future research:
1. Additional research is necessary to understand the mechanisms responsible for the relationship between species diversity,
functional diversity, and ecosystem function.
2. Because most studies have focused on the relationship between diversity of primary producers and ecosystem function,
effects of diversity across trophic levels are poorly understood.
3. Although there is broad theoretical support for the relationship between species diversity and stability, long-term field
experiments are necessary to determine the importance of this relationship in natural ecosystems.
4. Because ecosystem function simultaneously influences and responds to biological diversity, understanding the feedback
between these variables is critical.
5. Because the focus of diversity–ecosystem function research has been in terrestrial ecosystems and to a limited extent in
freshwater ecosystems, little is known about this relationship in marine ecosystems.
Source: From Table 1 in Hooper et al. 2005.
species diversity and ecosystem processes. We then discuss the practical implications of this relation-
ship and argue that, in addition to the direct effects of pollutants on energy flow and biogeochemical
cycles describedin previouschapters, contaminant-induced changein diversitycan negatively impact
ecosystem processes and services. We also review the evidence supporting the hypothesis that
ecosystems with lower biological diversity have lower resistance and resilience to natural and anthro-
pogenic stressors compared to species-rich ecosystems. Finally, we demonstrate that recent studies
investigating the concept of ecological thresholds have important implications for understanding the
diversity–ecosystem function relationship. We suggest that quantifying the level of perturbation (or
species loss) where ecosystem function is significantly impaired will improve our ability to predict
effects of anthropogenic perturbations.
Many of the important ecosystem processes we have discussed in the preceding chapters, includ-
ing primary productivity, nutrient dynamics, decomposition, and energy flow respond directly to
anthropogenic perturbations. We also know that changes in abundance of keystone species and other
ecologically important taxa as a result of physical and chemical stressors affect ecosystem function at
local and global scales (Chapin et al. 1997). In this chapter, we consider the implications of reduced
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Diversity–Ecosystem Function Relationship 717

species richness and diversity on ecosystem processes. The fundamental argument supporting this
relationship is quite simple. From a probabilistic perspective, greater species richness increases
the likelihood that functionally important species will be present in an ecosystem. Elimination of
species in ecosystems with lower species diversity increases the likelihood that critical ecosystem
processes will be affected. As described previously (Chapter 25), greater species diversity provides
functional redundancy and increases the resistance and resilience of ecosystems to anthropogenic
perturbations. For example, Frost et al. (1999) attributed the functional redundancy and increased
resilience of acidified lakes to high zooplankton diversity.
Although our understanding of the mechanistic linkages between community structure and eco-
system function remains limited, it is becoming increasingly apparent that alterations in ecosystem
processes as a result of species loss have important implications for ecosystem services provided
to humans. Species loss within functionally related assemblages, such as pollinators and flowering
plants, may impact ecosystem services at very large spatial scales (Biesmeijer et al. 2006). The
unprecedented rate of species extinction occurring at a global scale requires that ecologists and
ecotoxicologists develop a better appreciation of the relationship between patterns and processes.
Despite the recent interest in this relationship within the basic ecological literature, surprisingly few
studies have examined the consequences of contaminant-induced species loss on ecosystem function
and services. In addition to measuring the direct effects of chemical stressors on ecosystems, we
believe that it is important that ecotoxicologists recognize the indirect effects on ecosystem processes
owing to loss of species. The goal of this chapter is to provide an ecotoxicological perspective on
the critical relationship between community patterns and ecosystem processes.
33.2 SPECIES DIVERSITY AND ECOSYSTEM FUNCTION
Although biologists have hypothesized about the relationship between species diversity and eco-
system function for over a century, the topic remains controversial in the contemporary ecological
literature (Grime 1997, Hooper and Vitousek 1997, Huston 1997). There is general agreement that
high species diversity provides benefits to ecosystems beyond simple aesthetics. In a review of evid-
ence supporting the diversity–ecosystem function relationship, Chapin et al. (1998) concluded that
high species diversity maximizes resource acquisition across trophic levels, reduces the risk associ-
ated with stochastic changes in environmental conditions, and protects communities from exposure
to pathogens or exotic species. Because diversity’s relationship with ecosystem goods and services

has important socioeconomic implications, this debate has also generated significant attention among
policymakers.
A key issue in the diversity–ecosystem function debate is that many of the ecosystem processes
that have been linked directly to species diversity, such as the primary productivity of tropical
rainforests, are clearly influenced by other environmental factors in addition to the number of species
(Figure 33.1). Second, while most research has investigated the influence of diversity on ecosystem
function, ecosystem processes such as primary productivity also regulate species diversity. The
influence of ecosystem processes on species diversity may be very complex. For example, Chase
and Leibold (2002) reported that the shape of the relationship between productivity and species
diversity was scale dependent. At a local scale, the relationship was hump shaped, with diversity
increasing up to a certain level of productivity and then declining at higher levels. In contrast,
species diversity increased linearly with productivity at the regional scale. As a consequence of these
complex, scale-dependent relationships, an understanding of potential feedbacks between diversity
and ecosystem processes is critical. The relationships between species diversity, ecosystem function,
and ecosystem services also must be interpreted within the context of changing global climate. The
most contentious debates within the ecological community pertain to the mechanisms by which
species diversity controls ecosystem function. It is possible that the positive relationship is simply
a sampling artifact, by which greater species richness increases ecosystem function by increasing
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718 Ecotoxicology: A Comprehensive Treatment
Local chemical
and
physical stressors
Species diversity
and community
structure
Ecosystem
processes
Ecosystem

services
Human
health
Global atmospheric
stressors
FIGURE 33.1 The influence of anthropogenic stressors and species diversity on ecosystem processes and
services. Because ecosystem processes also influence species diversity, an understanding of the potential feed-
back is necessary for characterizing these relationships. All of these interactions must be interpreted within the
context of global atmospheric stressors such as climate change, N deposition, and increased UV-B radiation.
the likelihood that functionally important species are present. Alternatively, increased ecosystem
function at higher species richness could be a result of positive interactions among species, described
as complementarity or facilitation effects. Thus, while many researchers accept the existence of a
relationship between species diversity and ecosystem function, the mechanisms responsible for this
relationship remain a significant source of controversy.
33.2.1 EXPERIMENTAL SUPPORT FOR THE SPECIES
DIVERSITY–ECOSYSTEM FUNCTION RELATIONSHIP
Large-scale field experiments conducted in grasslands by Tilman and colleagues have contributed
significantly toour understandingof therelationship betweendiversity andplant productivity(Tilman
et al. 1997). By adding a known number of species (0–32) orfunctional groups (0–5) tolarge (169 m
2
)
grassland plots, these researchers foundthat both speciesdiversity and functional diversityinfluenced
plant productivity (Figure 33.2). When results were analyzed based on functional composition, the
relationships were stronger, suggesting that composition of the community was more important than
the number of species. Similarly, Hooper and Vitousek (1997) reported that the composition of plant
functional groups was more closely related to ecosystem processes than functional group richness.
These results demonstrate that the different functional roles of species may be more important
predictors of ecosystem integrity than the actual identity of those species.
A large-scale experimental test of the relationship between grassland plant diversity and pro-
ductivity was conducted at eight European field sites (Hector et al. 1999). Five levels of species

richness were established at each site across a broad geographic region (Germany, Portugal, Switzer-
land, Greece, Ireland, Sweden, and two sites in the United Kingdom). Productivity (measured
as aboveground biomass) varied among locations, but the overall pattern at all sites was greater
productivity with higher species richness. The mechanisms proposed to account for this pattern
included positive mutualistic interactions among species and niche complementarity, whereby vari-
ation among species resulted in more complete utilization of resources. Although distinguishing
between these alternative explanations will not be simple, the results demonstrate that loss of species
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Diversity–Ecosystem Function Relationship 719
*
*
*
*
*
*
*
*
*
*
*
*
*
010203035
0
50
100
150
200
Species diversity

012345
0
50
100
150
200
Functional diversity
Plant biomass (g/m
2
)
FIGURE 33.2 The influence of species diversity and functional diversity on productivity (measured as above-
ground biomass) in grassland plots. Species diversity and functional diversity were manipulated by adding a
known number of species or functional groups to experimental plots. (Modified from Figure 1 in Tilman et al.
(1997).)
and the alteration in community composition will significantly alter ecosystem processes. Consistent
with predictions of the drivers and passengers model described in Chapter 25 (Figure 25.2d), the loss
of some functionally important species will have greater impacts on ecosystem function than the loss
of other species. Taylor et al. (2006) reported that removal of a single detritivorous fish species from a
species-rich tropical river had large effects on carbon flow and ecosystem metabolism. These results
were contrary to the theoretical prediction that high species diversity at lower trophic levels provides
insurance against changes in ecosystem function. If one of the key goals of basic ecology is to
identify these functionally important species, we believe that one of the challenges in ecotoxicology
is to predict the consequences of their local extinction owing to the presence of chemical stressors.
33.2.2 FUNCTIONAL REDUNDANCY AND SPECIES SATURATION IN
ECOSYSTEMS
The positiveinfluence of speciesrichness on ecosystem function reportedin many studieshas attained
greater significance as conservation biologists have used this relationship to argue for species protec-
tion. The accelerating loss of biodiversity has intensified efforts to clarify the diversity–productivity
relationship and to identify mechanistic explanations. From a species conservation perspective, the
shape of the relationship between richness and ecosystem processes may be at least as import-

ant as the actual existence of this relationship. A linear relationship between ecosystem processes
and richness implies that all species in a community are important and contribute to ecosystem
function (Figure 33.3). However, if the relationship is curvilinear and ecosystem processes can be
supported by a relatively small number of species, then ecosystems could potentially lose a signi-
ficant number of species without affecting function. Schwartz et al. (2000) reviewed observational,
experimental, and theoretical studies and found relatively little support for the linear dependence of
ecosystem processes on species richness. These researchers recommended caution when using the
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720 Ecotoxicology: A Comprehensive Treatment
Species richness
Ecosystem process
A
B
C
FIGURE 33.3 Three hypothetical relationships between species richness and ecosystem processes. TypeA is
an example of where ecosystem processes are saturated at a relatively low number of species. This response also
shows an abrupt threshold response when species richness is reduced below a certain critical number. Type B
shows an intermediate relationship between species richness and ecosystem function. The linear relationship
between species richness and ecosystem function depicted by Type C implies that all species contribute equally
to ecosystem function. (Modified from Figure 1 in Schwartz et al. (2000).)
diversity–ecosystem function relationship as an argument to support species conservation. Although
a saturating response of ecosystem processes to increasing species richness is the most commonly
observed pattern (Hooper et al. 2005), in a global analysis of marine ecosystems Worm et al. (2006)
found no evidence of functional redundancy and reported a linear relationship between richness and
ecosystem processes.
33.2.3 INCREASED STABILITY IN SPECIES-RICH ECOSYSTEMS
In many respects, the relationship between species richness and ecosystem function is closely related
to the diversity–stability relationship described in Chapter 25. Indeed, one of the responses frequently
cited to support the existence of a positive diversity–ecosystem function relationship is greater sta-

bility in species-rich ecosystems. This relationship is supported by mathematical models that predict
that, if species abundances vary randomly or are negatively correlated, ecosystem processes will be
more stable in diverse communities than in species-poor communities. This statistical averaging phe-
nomenon, which has been termed the “portfolio” effect, provides a type of insurance for ecosystems
where species have varying sensitivities to environmental conditions. Despite its broad theoretical
support and intuitive appeal, there have been few long-term experiments testing the relationship
between species diversity and ecosystem stability in nature. We agree with Hooper et al. (2005) that
linking results of long-term experiments with theoretical and mathematical models will improve our
understanding of the role that biological diversity plays in stabilizing ecosystem function.
33.2.4 C
RITICISMS OF THE DIVERSITY–ECOSYSTEM FUNCTION
RELATIONSHIP
Critics of the diversity–ecosystem function relationship argue that ecosystem properties are not a
direct consequence of species richness or diversity per se, but simply an outcome of the functional
composition of dominant species. Experimental studies conducted in grasslands, greenhouses, and
growth chambers that controlled for potential confounding variables have demonstrated a strong
positive relationship between species diversity and plant productivity. However, large-scale com-
parative field studies showed that this relationship was not consistent, suggesting that factors other
than species diversity determined ecosystem processes (Chapin et al. 1997). Wardle et al. (1997)
took advantage of natural variation in community composition of an island archipelago to examine
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Diversity–Ecosystem Function Relationship 721
the relationship between island size and ecosystem processes. In contrast to predictions based on
many studies, ecosystem processes were inversely related to species diversity.
Another legitimate criticism of studies reporting a relationship between community structure
and ecosystem processes is that biological diversity within a community is frequently reduced to a
single number (e.g., species richness). However, there are other important community characteristics
that are equally likely to respond to anthropogenic stressors and influence ecosystem processes. For
example, in addition to reduced species richness and alterations in community composition, one of

the mostconsistent responses tomany chemical stressors is increaseddominance of pollution-tolerant
species. Dangles and Malmqvist (2004) reported that the relationship between species richness and
leaf breakdownrates in 36European streams was determined bydominance of invertebrateshredders.
Detrital processing rates were higher and showed an asymptotically increasing relationship with
species richness in streams with high dominance, indicating considerable functional redundancy.
In contrast, the relationship between species richness and detrital processing in streams with an
even distribution of individuals was linear, indicating that all shredder species were important and
contributed to ecosystem function.
33.2.5 MECHANISMS RESPONSIBLE FOR THE SPECIES
DIVERSITY–ECOSYSTEM FUNCTION RELATIONSHIP
Sacrificing those aspects of ecosystems that are difficult or impossible to reconstruct, such as diversity,
simply because we are not yet certain about the extent and mechanisms by which they affect ecosystem
properties, will restrict future management options even further.
(Hooper et al. 2005)
If we assume that different species in a community have different functional roles and that the
functions performed by individual species are limited, it follows that alterations in community
composition resulting from anthropogenic disturbance will affect ecosystem processes. However,
identifying the specific mechanistic explanations for the diversity–ecosystem function relationship
and characterizing its form (e.g., linear vs. curvilinear) have been challenging. Some ecologists
suggest that this relationship is inconsistent among communities because the relative contributions
of individual species to ecosystem function are context dependent and vary with environmental
conditions (Cardinale et al. 2000). Others argue that the observed pattern is a sampling artifact
resulting from inappropriate experimental designs and hidden treatment effects (Grime 1997, Huston
1997). An important research challenge will be to distinguish among these alternatives and to identify
the specific mechanisms responsible for the diversity–ecosystem function relationship. Fox (2006)
developed a framework to partition effects of species loss on ecosystem function. Effects were
partitioned into those resulting from random loss of species, nonrandom loss of species, and changes
in functioning of remaining species.
Much of the debate about the relationship between biodiversity and ecosystem function centers
on the hypothesis that ecosystem integrity is dependent on the number of species and that loss of

species will affect critical ecosystem services. In addition, there is an obvious inconsistency between
the hypothesis that all species in an ecosystem are important and the alternative that ecosystems with
a large number of species have significant functional redundancy (Figure 33.3). Chapin et al. (1997)
argue that this issue can be resolved by considering functional traits of species instead of simple
measures of species richness and diversity. Species richness is predicted to influence ecosystem
function in several fundamental ways. First, ecosystems with a large number of species have a
greater probability of containing taxa with important functional roles. Second, ecosystems with
more species will likely use available resources more efficiently, resulting in greater productivity.
Finally, a large number of species provide functional redundancy in an ecosystem and a buffer
against species loss owing to anthropogenic disturbance. Yachi and Loreau (1999) developed a
stochastic dynamic model to test this “insurance hypothesis” and concluded that greater species
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722 Ecotoxicology: A Comprehensive Treatment
richness had both a buffering effect on temporal variance and a performance-enhancing effect on
productivity.
As described above, ecosystem processes are more likely to respond to the functional diversity
of a community rather than the total number of species. Heemsbergen et al. (2004) measured the
effects of species richness and functional dissimilarity (defined as the range of species traits that
determine their functional role) on soil processes (leaf litter mass loss, nitrification, and respiration).
Although the number of species had relatively little impacton soil processes, leaf litter decomposition
and soil respiration significantly increased with functional dissimilarity. Finally, while the focus of
the biodiversity–ecosystem function debate has been primarily on the role of species diversity, we
should remember that genetic diversity within populations may also influence ecosystem processes.
Crutsinger et al. (2006) reported that genotypic diversity in a population of plant species increased
aboveground net primary productivity and species richness of arthropod herbivores and predators.
This increase in consumer species richness was a result of both greater resource productivity and
greater diversity of these resources.
33.3 THE RELATIONSHIP BETWEEN ECOSYSTEM
FUNCTION AND ECOSYSTEM SERVICES

Although a number of uncertainties remain, the importance of ecosystem services to human welfare
requires that we adopt the prudent strategy of preserving biodiversity in order to safeguard ecosystem
processes vital to society.
(Naeem et al. 1999)
The practical significance of understanding the relationship between community patterns and ecosys-
tem processes is best illustrated by considering the services provided by ecosystems. We know that
natural ecosystems supply irreplaceable benefits to society, and that many of these benefits are crit-
ical for the health and survival of humanity. Some ecosystem services, such as removal of nutrients
and other wastes, soil stabilization, pollination, and regulation of climate and atmospheric gasses,
contribute directly to human welfare. The ecosystem service most familiar to ecotoxicologists is the
biotic and abiotic attenuation of contaminants, often referred to as the assimilative capacity of an
ecosystem. The purifying function of ecosystems has been widely reported in the literature (Havens
and James 2005, Ng et al. 2006, Richardson and Qian 1999), but only recently have research-
ers considered specific management practices that facilitate assimilative capacity (Vorenhout et al.
2000). Although researchers and policymakers have long recognized the qualitative importance of
ecosystem services, collaboration between ecologists and economists has improved our ability to
estimate their total economic value. Costanza et al. (1997) estimated that the global economic value
of 17 ecosystem services across a range of aquatic and terrestrial biomes was US$ 16–54 trillion
(average = US$ 33 trillion) per year, which was approximately 1.8 times the global gross domestic
product (Table 33.2). These researchers also note that as ecosystems providing services become
increasingly stressed, it is likely that their economic value will significantly increase.
Disruption of ecosystem services is a result of alterations in ecosystem processes that are linked
either directly or indirectly to physical, chemical and biological stressors (Figure 33.1). These
linkages all occur within the context of global climate change, which operates at a much larger spa-
tiotemporal scale. The dependence of ecosystem processes on community characteristics described
in this chapter provides additional justification for the protection of biological diversity. Identifying
quantitative relationships among community patterns, processes, and ecosystem services should be
a research priority in ecotoxicology. Many ecologists now recognize that research conducted exclus-
ively inundisturbed ecosystems providesan important but somewhat biasedperspective of ecosystem
processes (Palmer et al. 2004). Although the inclusion of humans and associated anthropogenic

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Diversity–Ecosystem Function Relationship 723
TABLE 33.2
Ecosystem Function, Services, and Annual Economic Global Value
Ecosystem Function Ecosystem Services Examples Value (US$ 10
9
)
Regulation of atmospheric chemical
composition
Gas regulation CO
2
/O
2
balance; O
3
for UV-B
protection
1,341
Regulation of global temperature Climate regulation Greenhouse gas regulation 684
Damping ecosystem response to
environmental fluctuations
Disturbance
regulation
Storm protection, flood control, and
other response to environmental
variability
1,779
Regulation of hydrological flows Water regulation Provision of water for agricultural
and industrial processes

1,115
Storage and retention of water Water supply Provision of water by watersheds,
reservoirs, and aquifers
1,692
Soil retention Erosion control Prevention of soil loss by wind and
runoff
576
Soil formation processes Soil formation Geological weathering and
accumulation of organic material
53
Nutrient storage, cycling and
processing
Nutrient cycling N fixation; N and P cycling 17,075
Retention of nutrients and
immobilization of toxic chemicals
Waste treatment Pollution control and detoxification 2,277
Movement of floral gametes Pollination Providing pollinators for plant
reproduction
117
Trophodynamic regulation of
populations
Biological control Keystone predator control of prey
species; herbivore control by top
predators
417
Habitat for resident and transient
populations
Refugia Nurseries and habitat for migratory
and commercially important
species

124
Portion of GPP used as food Food production Production of fish, game, fruits,
nuts, and crops
1,386
Portion of GPP used as raw materials Raw materials Production of lumber, fuel, or fodder 721
Sources of unique biological materials
and products
Genetic resources Medicine, products for materials
science, and genes for resistance to
plant pathogens
79
Opportunities for recreational activities Recreation Ecotourism, sport fishing, and other
outdoor activities
815
Opportunities for noncommercial uses Cultural Aesthetic, artistic, educational, and
spiritual value
3,015
Source: From Table 2 in Costanza et al. (1997).
disturbances into the study of basic ecosystem processes is controversial, we believe this step is
fundamental to understanding the complex relationship between ecosystems and the services they
provide. Because there will likely be variation in the sensitivity among ecosystem processes to
chemical stressors, quantifying stressor–response relationships should be a research priority. The
lack of a consensus on which ecosystem services are critical and therefore should be protected also
impedes our ability to make policy decisions based on the diversity–ecosystem function relationship
(Schwartz et al. 2000). A critical step will be to prioritize the importance of ecosystem services
and to determine which are irreplaceable and which can be maintained with technological advances
(Palmer et al. 2004).
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724 Ecotoxicology: A Comprehensive Treatment

33.4 FUTURE RESEARCH DIRECTIONS AND
IMPLICATIONS OF THE DIVERSITY–ECOSYSTEM
FUNCTION RELATIONSHIP FOR
ECOTOXICOLOGY
33.4.1 E
FFECTS OF RANDOM AND NONRANDOM SPECIES LOSS ON
ECOSYSTEM PROCESSES
Because most experimental investigations of the diversity–productivity relationship have focused
on terrestrial primary producers, the widespread generality of these patterns in other ecosystems is
uncertain. In addition, most studies investigating this relationship have assumed that elimination of
species is a random process. However, the susceptibility of a species to anthropogenic disturbance
in natural systems will be influenced by a wide range of life history features, including mobility,
longevity, reproductive rates, and body size (Bunker et al. 2005, Raffaelli 2004, Solan et al. 2004).
For example, specialized species are likely to be more sensitive to stressors than generalized species
that rely on a broader range of resources. Our understanding of the diversity–ecosystem function
relationship is also limited because species removals are generally restricted to a single trophic
level. We can be confident that the relationship between species diversity and ecosystem processes
is considerably more complex in natural systems with multiple trophic levels than what is predicted
based on single-trophic models. The oft-cited metaphor that keystone species represent a critical
supporting stone in an arch of subordinate species has recently been modified to account for the
dynamic nature of food webs (de Ruiter et al. 2005). The potentially complex functional interactions
among trophic groups require that ecologists adopt a multitrophic approach to predict ecosystem
responses to changes in species diversity. For example, loss of species occupying higher trophic
levels will likely have very different consequences for energy flow and other ecosystem processes
compared to the loss of primary producers and herbivores. Furthermore, because species richness
generally decreases at higher trophic levels and because species at higher trophic levels are often
more susceptible to anthropogenic disturbances, an understanding of food web structure is necessary
to predict the consequences of local species extinctions on ecosystem function (Petchey et al. 2004).
In addition to the cascading effects through food webs, species occupying higher trophic levels
may also have direct effects on ecosystem processes. Ngai and Srivastava (2006) reported that con-

sumption of detritivores by damselfly predators reduced the export of N and increased N cycling.
In systems regulated by top–down trophic interactions, we would expect that removal of species at
higher trophic levels will have greater effects (Downing and Leibold 2002). However, the relation-
ship between species richness and ecosystem processes is context dependent and will be influenced
by many environmental factors (de Ruiter et al. 2005). For example, major changes in community
composition of Tuesday Lake (Michigan, USA) resulting from removal of three planktivorous fish
species and addition of one piscivorous fish species had remarkably little effect on trophic dynamics
(Jonsson et al. 2005). Naeem et al. (2000) also reported that increased producer or decomposer
diversity could not account for greater algal production observed in freshwater microcosms. Duffy
et al. (2001) observed that species composition of grazers in marine seagrass beds strongly influ-
enced productivity and was more important than species richness. These results indicate that studies
focusing on a single trophic level may underestimate ecosystem effects of anthropogenic disturbance
on biodiversity.
Failure toconsider the consequencesof ordered versusrandom species lossesmay cause research-
ers to underestimate the effects of species extinction on ecosystem function (Zavaleta and Hulvey
2004). Assuming that the loss of species from ecosystems will likely be nonrandom, understanding
factors that influence the susceptibility of species to local extinction will improve our ability to
predict ecosystem consequences. Solan et al. (2004) compared effects of species loss on ecosystem
processes in marine sediments under random and nonrandom species extinction models. Removal
of abundant, large, and highly mobile marine invertebrates had much greater effect on ecosystem
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Diversity–Ecosystem Function Relationship 725
To p
carnivore
Carnivores
Traits that
increase up
the food chain
Traits that

increase down
the food chain
Herbivores
Primary
producers
Body size
Home range
Longevity
Vulnerability
to contaminants
Adaptability
Species
richness
FIGURE 33.4 The effect of species loss on ecosystem function depends on life history traits (body size,
susceptibility to stress), trophic level, and stressor type. Large individuals at higher trophic levels are predicted
to be more susceptible to habitat loss whereas small individuals at lower trophic levels are predicted to be more
sensitive to contaminants. Predictingthe effects of speciesremoval onecosystem function ischallenging because
some species traits increase with trophic level whereas others decrease. (Modified from Raffaelli (2004).)
processes than removal of smaller, less abundant species. Bunker et al. (2005) performed model
simulations based on random and nonrandom extinction scenarios and showed that effects of species
extinction on carbon storage were strongly influenced by which species were removed first. Results
of these studies also suggested that the consequences of species loss on ecosystem processes were
determined by the particular stressors responsible. Raffaelli (2004) provides a conceptual model
to show how life history traits that determine vulnerability to anthropogenic stressors vary among
trophic levels (Figure 33.4). Because the effects of physical (e.g., habitat loss) and chemical stressors
vary among trophic levels, this model could be used to predict which species are most likely to be
eliminated from an ecosystem and the potential effects on ecosystem processes.
Contaminants often reduce abundance of sensitive species and alter evenness of communities,
but may not result in the complete elimination of a species from an ecosystem. Consequently,
relationships between community structure and ecosystem processes should account for changes

in relative abundance of important species. The relative contribution of a species to ecosystem
processes is a function of both its relative abundance and functional importance. Balvanera et al.
(2005) developed a model analogous to the dominance–diversity curves described in Chapter 22
to quantify the relative contribution of a species to ecosystem processes. In addition to expanding
our understanding of diversity–ecosystem function relationships beyond simple measures of species
richness, this model allows researchers to quantify the relative contributions of each species to
ecosystem processes.
33.4.2 THE NEED TO CONSIDER BELOWGROUND PROCESSES
Most research investigating the relationship between species diversity and ecosystem function in
terrestrial ecosystems has focused on aboveground processes. Because of the intimate connection
between plants and soil microbial communities, some researchers have argued that plant diversity
will directly influence microbial communities in soils and thereby affect belowground ecosys-
tem processes such as decomposition and nutrient cycling (Heemsbergen et al. 2004, Zak et al.
2003). In terrestrial ecosystems, complex positive and negative feedbacks between aboveground
plant communities and belowground microbial communities ultimately determine the nature of the
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726 Ecotoxicology: A Comprehensive Treatment
Plant
productivity
Plant species
diversity
Soil microbial
communities
Soil
ecosystem
processes
Chemical
stressors
Aboveground components

Belowground components
FIGURE 33.5 The influence of chemical stressors on the relationship between above- and belowground
components in soil ecosystems. Complex positive and negative feedback determines the relationship between
species diversity and ecosystem processes.
relationship between biodiversity and ecosystem function (Figure 33.5). For example, if increased
plant diversity affects resource availability and community composition of soil communities, we
would expect changes in rates of C and N cycling. Zak et al. (2003) reported that increased plant
diversity altered community composition and increased soil microbial biomass, resulting in greater
rates of N mineralization. It is important to note that these linkages between above- and below-
ground communities are not unidirectional. Alterations in microbial community composition and
biogeochemical cycles within soil communities resulting from greater plant diversity will also affect
aboveground productivity; however, these relationships may be either positive or negative (Wardle
et al. 2004). These linkages between above- and belowground communities and the processes they
control also have important implications for distinguishing between direct and indirect effects of
chemical stressors in terrestrial ecosystems. We agree with Wardle et al. (2004) that a combined
aboveground–belowground approach may be necessary to understand the effects of global change
and other anthropogenic stressors on the relationship between biodiversity and ecosystem function.
33.4.3 THE INFLUENCE OF SCALE ON THE RELATIONSHIP BETWEEN
DIVERSITY AND ECOSYSTEM PROCESSES
Most research supporting the relationship between species diversity and ecosystem function has been
conducted at relatively small to moderate spatial scales. Because species loss is a regional and global
phenomenon, an understanding of the consequences of reduced biological diversity at larger spati-
otemporal scales is essential. Schroter et al. (2005) quantified the vulnerability of ecosystem services
to climate and land use changes across broad geographic regions in Europe. Significant species loss
and increased vulnerability were observed in all regions, but effects were greatest in Mediterranean
and mountainous areas. Lotze et al. (2006) reconstructed historical baselines (300–1000 years bp)
of species richness and ecosystem processes for 12 temperate estuaries and coastal ecosystems in
Europe, North America, and Australia. Patterns were remarkably consistent among these diverse
geographic regions, showing gradual declines immediately after human settlement followed by
accelerating degradation during the past 150–300 years. These long-term, global declines in abund-

ance, diversity, and ecosystem function were attributed to several causes, including overexploitation,
habitat degradation, pollution, and disturbance.
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Diversity–Ecosystem Function Relationship 727
Worm et al. (2006) conducted one of the most spatially extensive investigations of the rela-
tionship between biodiversity and ecosystem processes in marine ecosystems. Meta-analysis of 32
controlled experiments showed consistent positive relationships between biodiversity (both genetic
and speciesdiversity) and primaryproductivity, secondary productivity, and stability. Resultsof these
experiments scaled up regionally and globally, also demonstrating a positive relationship between
biodiversity and recovery potential, stability and water quality. Worm et al. (2006) conclude that
reduced biodiversity in marine ecosystems has significantly impaired stability and productivity of
the world’s oceans. More importantly, at the current rate of diversity loss their model projects a
complete collapse of all marine fisheries by the year 2048.
33.4.4 HOW WILL THE STRUCTURE–FUNCTION RELATIONSHIP
BE INFLUENCED BY GLOBAL CHANGE?
Descriptive and observational studies conducted to quantify the influence of species diversity on
ecosystem processes have generally not considered the effects of climate change and other global
atmospheric stressors. If the nature of the relationship between diversity and ecosystem function is
context dependent as some researchers have suggested (de Ruiter 2005, Wardle 2004), then consid-
eration of how elevated CO
2
, UV-B radiation, NO
x
, and other global stressors will influence this
relationship is necessary (Figure 33.1). For example, ecosystem processes associated with C sequest-
ration will be directly influenced by elevated CO
2
and NO
x

and indirectly influenced by effects of
these stressors on species diversity (Aber et al. 2001). Similarly, UV-B radiation simultaneously
eliminates sensitive phytoplankton species and reduces primary productivity in marine ecosystems
(Day and Neale 2002). Separating the relative importance of these direct and indirect effects will
require that researchers move away from relatively small-scale, closed experimental systems to
larger and more ecologically realistic outdoor systems.
33.4.5 BIODIVERSITY–ECOSYSTEM FUNCTION IN AQUATIC
ECOSYSTEMS
A key limitation to our understanding of the diversity–ecosystem function relationship is the lack
of research conducted in aquatic ecosystems. Because diversity in aquatic ecosystems is particu-
larly susceptible to anthropogenic disturbance and declining rapidly, we believe that quantifying
diversity–ecosystem function relationships in lentic, lotic, and marine aquatic ecosystems should
be a research priority. Covich et al. (2004) reviewed the role of biodiversity in the functioning of
freshwater and marine benthic communities and describe some of the unique features of aquatic eco-
systems that affect this relationship. Approximately one half of the 32 diversity–ecosystem function
relationships were significantly positive, and most of the remaining relationships either showed no
effect or were positive but not statistically significant. Variability in the magnitude and direction
of the diversity–ecosystem function relationship among aquatic ecosystems was partially attributed
to spatiotemporal variation and the dependency of these relationships on environmental conditions
(Covich et al. 2004).
33.5 ECOLOGICAL THRESHOLDS AND
THE DIVERSITY–ECOSYSTEM FUNCTION
RELATIONSHIP
One of the fundamental issues that must be resolved before we can fully understand the influence
of species diversity and richness on ecosystem function is the shape of these relationships. As
explained above, linear and curvilinear increases in ecosystem processes as a function of species
diversity have very different implications. A linear relationship between ecosystem function and
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728 Ecotoxicology: A Comprehensive Treatment

species diversity implies that all species contribute equally to ecosystem processes. In contrast,
a decrease in ecosystem function at some threshold of species richness (Figure 33.3) implies inherent
redundancy and that ecosystem processes are saturated until species richness is reduced to a critical
level. Characterizing the nature of the relationship between diversity and ecosystem function and
identifying the existence and location of any threshold would be useful for predicting ecosystem
responses to species loss. The existence of ecological thresholds and the statistical techniques used
to identify their location along stressor gradients have recently received attention in the literature. We
believe that quantifying the relationship between stressors and ecosystem responses and identifying
potential ecological thresholds is fundamental to understanding the influence of species richness and
has important implications for ecosystem ecotoxicology.
33.5.1 THEORETICAL AND EMPIRICAL SUPPORT FOR ECOLOGICAL
THRESHOLDS
Theoretical and empirical studies suggest that some ecosystems show abrupt, nonlinear changes in
structure and function in response to perturbations (e.g., Connell and Sousa 1983, Estes and Duggins
1995, May 1977). While gradients of nutrient or toxic chemical concentrations may be gradual,
responses to these changes can occur rapidly and without warning (Figure 33.6). Catastrophic shifts
to alternative stable states have been reported in a variety of ecosystems including lakes, coral
reefs, deserts, and oceans (Scheffer et al. 2001). Shifts to alternative stable states can be triggered
by natural disturbance, such as fire or flooding, or anthropogenic factors such as climate change,
nutrient accumulation, exotic species, and toxic chemicals. The loss of natural resistance caused by
long-term exposure to a chronic stressor may increase the likelihood that an ecosystem will shift
to an alternative stable state. Although most ecosystems recover from natural disturbance through
successional processes, human-induced disturbances are often unique and may move ecological
Ecosystem response
Stressor level
A
B
C
S
1

S
2
FIGURE 33.6 Hypothetical responses of ecosystems to stressors. A. Gradual response to increased stressor
levels where a distinct threshold does not occur. B. Threshold response to increased stressor level. C. Threshold
response to increased stressor level showing two alternative stable states, S
1
and S
2
. Note that for ecosystem C
to recover and return to the initial stable state, stressor levels must be reduced below those causing the initial
shift. (Modified from Figure 1 in Scheffer et al. (2001).)
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Diversity–Ecosystem Function Relationship 729
systems to novel, alternative states (Holling 1973). If ecosystems are chronically stressed owing to
natural or anthropogenic disturbances, these alternative states may remain stable even when stressors
are removed (Paine et al. 1998, Scheffer et al. 2001).
Thresholds, or ecological discontinuities, represent significant changes in an ecological state
variable as a consequence of continuous changes in an independent (stressor) variable (Muradian
2001). The point at which rapid change initially occurs defines the threshold. Near this point, small
changes in stressor intensity may produce large effects on response variables. Given this, it is
possible to interpret ecological thresholds within the context of theoretical relationships between
biodiversity and resistance stability. Both the diversity–stability hypothesis (Johnson et al. 1996)
and the rivet hypothesis (Walker 1995) predict that ecosystem-level functions should decline with
declining biodiversity. The diversity–stability hypothesis predicts that the decline should be smooth
and linear. In contrast, the rivet hypothesis predicts that the decline will be nonlinear, showing a
steep threshold at a critical level of diversity loss.
Unfortunately, there is an inherent arbitrariness to the above definition of ecological threshold
because of uncertainty in determining if the magnitude of change in the response variable at the
threshold is ecologically relevant. Nevertheless, numerous statistical models have been developed

to detect these thresholds. For example, consider a nonlinear relationship between aresponse variable
and a stressor variable. If this functionshows a dramatic change in slopeat some point along a stressor
gradient, then a threshold point has been defined. However, this does not necessarily imply that the
system has been shifted to an alternative stable state. One important challenge in the evaluation of
data used to estimate these functions is to distinguish true thresholds from background variation in a
response variable. It is also important to identify changes in slope of the function owing to external
or internal factors that affect the response variable but act independently of the stressor. Because of
the uncertainties associated with quantifying a precise ecological threshold, some researchers have
suggested that we identify a range of stressor values where threshold responses may occur instead
of a specific stressor level (Figure 33.7) (Muradian 2001).
The ecological threshold concept is closely related to other ecosystem properties such as resist-
ance and resilience that we have discussed previously; however, there remains confusion over the
use of these terms in the ecological literature describing thresholds. We have previously defined res-
istance stability as the ability of a community (or an ecosystem) to maintain equilibrium conditions
following a disturbance. In contrast, we defined resilience stability as the ability of the system to
return to predisturbance conditions following a disturbance. One way to distinguish between these
concepts is to note that resistance is estimated from the relationship between an ecosystem response
variable and stressor level. In contrast, resilience is measured as the relationship between an eco-
system response variable and the length of time since stressor removal (Figure 33.8). Just as the
catastrophic response to a stressor may shift an ecosystem to an alternative stable state, the recovery
Stressor level
Ecosystem process
Threshold
zone
FIGURE 33.7 A hypothetical relationship between stressors and ecosystem processes. Because of inherent
uncertainty in quantifying the precise location of an ecological threshold, a threshold zone is identified where
the system is most likely to move to an alternative stable state. (Modified from Figure 1 in Muradian (2001).)
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730 Ecotoxicology: A Comprehensive Treatment

Time
t
1
t
2
Ecosystem response
Stressor
removal
Recovery
Reference conditions
Stressor gradient
Threshold
Reference conditions
Stressor resilience
(= elasticity)
Stressor resistance
(= persistence)
FIGURE 33.8 Resistance, resilience, and ecological thresholds. Resistance (ecosystem persistence) is estim-
ated from the relationship between an ecosystem response and stressor level. The threshold is the point where
we see an abrupt change in the ecosystem response. Resilience (elasticity) is measured as the relationship
between an ecosystem response and the length of time since stressor removal. The threshold is the point where
the ecosystem response returns to background conditions.
“Healthy”
reference
state
Macroalgal
state
Sea urchin
barren
state

Bare
rock
Increasing stressor level
FIGURE 33.9 Ecosystem shifts between alternative steady states in coral reefs as a result of anthropogenic
disturbance. The figure depicts a decline in ecosystem characteristics as a result of increasing stressor level.
Returning to a previous steady state requires that stressors be reduced below levels that initially triggered the
transition. (Modified from Figure 2 in Bellwood et al. (2004).)
after a stressor is removed may require that conditions improve beyond where the initial switch
occurred (Scheffer et al. 2001). For example, many lakes are resistant to increases in nutrient con-
centrations up to a critical threshold, after which the system quickly shifts from clear to turbid water
conditions. Restoring clear water conditions may require that nutrient levels be reduced well below
the initial threshold concentration (Carpenter et al. 1999). Similarly, recovery of coral reef ecosys-
tems following exposure to elevated nutrients, temperature, or siltation may require that stressor
levels be reduced below those that initially caused shifts to alternative stable states (Figure 33.9)
(Bellwood et al. 2004). The need to reduce stressor levels below those that initially caused the shift
to an alternative stable state clearly has important implications for the restoration and recovery of
damaged ecosystems.
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Diversity–Ecosystem Function Relationship 731
33.5.2 E
COLOGICAL THRESHOLDS IN STREAMS
Despite evidence that some lotic ecosystems may show abrupt responses to disturbance, few stud-
ies have examined threshold responses in streams. This is surprising given that streams are highly
susceptible to anthropogenic disturbance, but also may recover rapidly when stressors are removed
(Clements 2004, Lake 2000, Yount and Niemi 1990). Lotic organisms may respond to these dis-
turbances such that community structure is continually maintained in a nonequilibrium state (Reice
1994). Given this momentum of community change, lotic communities may quickly shift between
alternate states in response to natural or anthropogenic disturbance (Strange et al. 1993). Anthro-
pogenic disturbances (i.e., contamination, habitat restructuring, exotic species, or climate change)

can dramatically alter lotic communities (Yount and Niemi 1990) and hold the greatest potential for
eliciting threshold responses. For instance, thresholds have been observed in fish communities in
urban streams where 10–20% of the watershed consisted of impervious surfaces (Paul and Meyer
2001). Similarly, Wang et al. (1997) found that nonlinear declines in fish communities occurred
once >20% of a watershed was urbanized, or after 50% of a watershed was converted to agriculture.
Others have found that catastrophic wildfires, and the flooding and sediment scouring that follow,
can result in relatively permanent shifts in community composition (Minshall et al. 1997, 2001;
Vieira et al. 2004).
33.6 SUMMARY
The relationship between species diversity and ecosystem function is well established in the ecolo-
gical literature. Although uncertainties regarding specific mechanisms and appropriate experimental
designs remain, the fundamental relationship and its practical importance for protecting biological
diversity are well supported. We agree with Hooper et al. (2005) that we should not restrict manage-
ment options for protecting important ecosystem processes and services simply because of debate
over these details. One of the greatest challenges in quantifying the potential effects of species
loss on ecosystem function is to identify the important species traits that are most likely to alter
processes. Because species loss from ecosystems will likely be nonrandom, models that estimate
consequences based on removal of species from a single trophic level are unrealistic. Chapin et al.
(1997) argue that species traits that modify resource dynamics, trophic structure and disturbance
regimes have the greatest potential to affect ecosystem processes. Because species at higher trophic
levels are more susceptible to extinction, understanding the relationship between top predators and
ecosystem function should be a research priority. From an ecotoxicological perspective, we believe
that alterations in trophic structure are most likely to impact contaminant transfer through ecosys-
tems. For example, introduction of exotic fish species into food chains can significantly increase the
transfer of contaminants to higher trophic levels (Johnston et al. 2003, Kidd et al. 1995).
33.6.1 SUMMARY OF FOUNDATION CONCEPTS AND PARADIGMS
• Reduced genetic, species, and functional diversity resulting from contaminants and other
stressors has important consequences for the services provided by ecosystems.
• Although many ecologists acknowledge the relationship between species diversity and
ecosystem function, the mechanisms responsible for this relationship remain a significant

source of controversy.
• We should not restrict management options for protecting important ecosystem processes
and services simply because of debate over details of the underlying mechanisms.
• Many of the ecosystem processes that have been linked directly to species diversity are
influenced by other environmental factors in addition to the number of species.
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732 Ecotoxicology: A Comprehensive Treatment
• Large-scale field experiments conducted in grasslands have contributed significantly to
our understanding of the relationship between diversity and plant productivity.
• From a species conservation perspective, the shape of the diversity–ecosystem function
relationship (e.g., linear, curvilinear) may be at least as important as the actual existence
of this relationship.
• There is an obvious inconsistency between the hypothesis that all species in an ecosystem
are important and the alternative that ecosystems with a large number of species have
inherent functional redundancy.
• Failure to consider the consequences of ordered versus random species losses may cause
researchers to underestimate the effects of species extinction on ecosystem function.
• Because species loss is a regional and global phenomenon, an understanding of
the consequences of reduced biological diversity at larger spatiotemporal scales is
necessary.
• Ecological thresholds represent significant changes in an ecological state variable as a
consequence of continuous changes in an independent (stressor) variable.
• Quantifying the existence and location of ecological thresholds is fundamental to
understanding the influence of species richness on ecosystem function.
• Ecosystem recovery after a stressor is removed may require that conditions improve
beyond where the initial state transition occurred.
• Natural ecosystems supply irreplaceable benefits to society, some of which are essential
for human welfare.
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