Download Review Paper Biodiversity Effects on Aquatic Ecosystem Functioning

Internat. Rev. Hydrobiol.
93
2008
4–5
550–564
DOI: 10.1002/iroh.200711022
LARS GAMFELDT *, 1, 2 and HELMUT HILLEBRAND 1
1
Institute for Botany, University of Cologne, Gyrhofstraße 15, D-50931 Köln,
Germany; e-mail: [email protected], [email protected]
2
Marine Biological Association of the United Kingdom, The Laboratory,
Citadel Hill, Plymouth PL1 2PB, UK
Review Paper
Biodiversity Effects on Aquatic Ecosystem Functioning –
Maturation of a New Paradigm
key words: paradigm shift, functions, freshwater, marine
Abstract
Starting with the publication of some influential studies in the early 1990’s, the topic of biodiversity
and ecosystem functioning has emerged as a major field within ecological research. Within this framework, the diversity of genotypes, species and functional groups are considered as explanatory variables
of ecosystem functions rather than response variables of factors such as productivity and disturbance.
Biodiversity-ecosystem functioning research has received considerable attention, and new publications
are emerging at a high pace. Both the validity of experimental approaches and the way the results may
be extrapolated to natural systems have, however, been widely discussed. The width of the debate
regarding whether or not biodiversity is important for ecosystem functioning have encouraged many
scientists to refine both experiments and theory, as well as develop novel methods to analyse the relationship between diversity and functioning. Aquatic ecologists have contributed greatly to the evolution
of ideas and concepts within the field. In this review, we discuss how the paradigm that biodiversity is an
important factor for the functioning of aquatic ecosystems is currently maturing with more realistic studies embracing both new and innovative approaches. We also suggest fruitful areas for future research.
Each of us is trapped in a place, a time, and a circumstance, and our attempts to use our minds to
transcend those boundaries are, more often than not, ineffective.
From the book “Stumbling on happiness” by DANIEL GILBERT
1. Introduction
The ability of scientists in general to think outside the box, to transcend traditional boundaries, is often limited. This holds true for ecologists and their fascination in the tremendous
diversity of life inhabiting our globe. With a few exceptions, people have often been so mesmerized by the causes of biological diversity, that they have forgotten to ask themselves in
what ways biodiversity might itself be important. Indeed, some of the most important issues
within the field of ecology has been to describe the “when, where, and how” of biological
diversity. Historically, the dominant puzzling question has been which factors are driving the
striking and diverse patterns of species abundances observed in nature (HUTCHINSON, 1959).
Classic examples of explored factors include competition (GAUSE, 1934), disturbance (DAYTON, 1971), environmental fluctuations (HUTCHINSON, 1961), and predation (PAINE, 1966).
* Corresponding author
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The role of diversity of organisms for ecosystem processes such as biomass accumulation
(e.g., CARLANDER, 1955), and stability (e.g., MACARTHUR, 1955) has attracted the attention
of scientists for a long time. DARWIN (1859) discussed that “… where they [animals and
plants] come into the closest competition with each other, the advantages of diversification
of structure, with the accompanying differences of habit and constitution, determine that the
inhabitants, which thus jostle each other most closely, shall, as a general rule, belong to what
we call different genera and orders.” (brackets inserted by the authors), and that “… if a plot
of ground be sown with several distinct genera of grasses, a greater number of plants and
a greater weight of dry herbage can (thus) be raised” (DARWIN, 1859). GAUSE (1934) used
experiments to show that species with similar requirements tend not to co-exist because one
species will be better at using the available resources than the other one. Following this principle, HARPER (1967) concluded that natural assemblages of mixed species should occupy
different niches, and that complex ecosystems would be more efficient than simple ones in
using environmental resources. In a book about the causes and consequences of species loss
(EHRLICH and EHRLICH, 1982), the authors discussed that disappearing species may be much
like losing the rivets of an aeroplane, because species have unique roles. When too many
rivets are lost, the plane (or the ecosystem) will stop functioning.
Numerous researchers have over the years addressed the relationship between single species or whole assemblages on ecosystem processes. Most have not, however, considered
the role of biological diversity per se (RAFFAELLI et al., 2005). Mainly motivated by global
change and rapid expansion of the human population (PIMM et al., 1995; VITOUSEK et al.,
1997), the last two decades have seen an increasing interest in the consequences of biodiversity loss. A book summarising data and theory that could lend support to the hypothesis that
biodiversity may be important to ecosystem functioning was published in 1993 (SCHULZE
and MOONEY, 1993). Since then, ecologists have broadened their horizon to explicitly consider the functional consequences of biodiversity by viewing diversity as the independent
variable. They have, if you will, transcended traditional boundaries to also include the functional consequences of altered levels of biodiversity. When, where, and how is biodiversity
driving processes in nature?
2. The New Paradigm
Most early work focused on the effects of biodiversity loss within one trophic level, and
the bulk of these studies concerned terrestrial plants (TILMAN et al., 1996; HOOPER and
VITOUSEK, 1997; HECTOR et al., 1999; MULDER et al., 2001). The conclusion from these
experiments was that species and functional richness affect biomass accumulation, used as a
proxy for productivity, and stability of the examined communities. Other studies inferred the
same using multitrophic protist microcosms (MCGRADY-STEED et al., 1997; NAEEM and LI,
1997; PETCHEY et al., 1999). Another set of experiments considered the role of biodiversity
in mediating invasion by alien species. By doing so, they revisited the classic hypothesis
that more species-rich communities should also be more resistant to invasion (ELTON, 1958).
STACHOWICZ et al. (1999) found that more diverse assemblages of sessile marine invertebrates were less invaded than were poorer counterparts. The authors contributed this to
more complete use of settling space (a limiting resource in this system) over time in diverse
assemblages. On the other hand, although diverse assembled plant communities appeared
to be resistant to invasion in a riparian system, naturally diverse communities were the
ones with the highest rate of invaders (LEVINE, 2000). It was concluded that other factors
co-varying with diversity change in nature (e.g., propagule supply) may override the effects
of diversity.
Even though the biodiversity-ecosystem functioning experiments have provided new
insights into community and ecosystem ecology, the new approach has not come without
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L. GAMFELDT and H. HILLEBRAND
friction. Many have questioned the validity of the biodiversity ecosystem function experiments (e.g., HUSTON and MCBRIDE, 2002), and have claimed that although biodiversity can
be shown experimentally to be important for various processes (SPEHN et al., 2005), such
patterns remain elusive in the real world (GRIME, 1997; GRACE et al., 2007). The tremendous
debate concerning issues of biodiversity effects on functioning (KAISER, 2000), the attention
the early studies received, and the number of studies emerging at an increasing pace suggests that biodiversity and ecosystem functioning is a rapidly evolving paradigm (Fig. 1)
(NAEEM, 2002; but see PAINE, 2002). The paradigm of diversity and functioning challenges
the idea (or central tenet if you will) that diversity is merely a function of extrinsic structuring forces (Fig. 1a). In doing so, it has stirred up conflicts about many fundamental issues in
ecology: the relative strength of abiotic and biotic factors, the strength of observational vs.
experimental approaches, the relative importance of taxonomic vs. functional diversity, and
the question whether diversity begets stability or not. It has also forced scientists to integrate
two previously largely separated subfields of ecology: community (studying the biotic components of ecosystems and their interactions) and ecosystem (taking a more holistic approach
including material and energy flow) ecology. Obviously, biodiversity is neither a passive
result of other structuring agents nor the sole vector explaining ecosystem processes. As is
often the case, the truth lies somewhere in between with feedback loops between abiotic and
biotic factors (Fig. 1b). All the same, if the paradigm of biodiversity and functioning receives
a)
Ecosystem properties
and processes
Diversity
Regional species pool
b)
Metacommunity dynamics
3
Coexistence mechanisms
6
Multifunctionality
Evenness
1
More
ecosystem
types
Ecosystem properties
and processes
Species
richness
Landscape structure
Trophic structure
Habitat diversity
Multitrophic assemblages
4
5
2
Genotypic,
species, and
functional
diversity
More
functions
Figure 1. Diagram representing the causality between ecosystem processes and biodiversity in the
classical paradigm (a), and the paradigm shift of including species richness as a driver (as well as a
consequence) of ecosystem properties and processes (b). Numbered points (1–6) refer to aspects representing the maturation of this paradigm shift towards higher generality and realism. Each point is
further explained in the text.
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Biodiversity Effects on Ecosystem Functioning
enough support from scientists as well as from experiments and observational studies, it has
the potential to evolve into a new central tenet in ecology.
A common criticism of biodiversity-ecosystem functioning experiments has been that
most of them have used artificially assembled communities with random species loss. The
results from such studies, it has been argued, are unlikely to provide us with any useful information about the functioning of real ecosystems (HUSTON and MCBRIDE, 2002). Such claims
seem to get good support from observations that many of the world’s aquatic ecosystems
that are dominated by one or a few species (e.g., salt marshes, seagrass beds, kelp forests)
still experience high standing biomass and/or high productivity. They are also supported by
recent meta-analyses that find that individual species are as important for ecosystem processes as are mixtures of species (CARDINALE et al., 2006; GRACE et al., 2007). Another metaanalysis, however, shows that positive effects of biodiversity such as niche partitioning and
positive interactions seem to dominate over sampling effects, i.e., the effects of individual
species or combinations (CARDINALE et al., 2007), and that these effects grow stronger with
time. Furthermore, analyses of data on marine biodiversity on both regional and global
scales reveal that large-scale patterns of changes in biodiversity and ecosystem services correspond to those of experiments on a small temporal and spatial scale (WORM et al., 2006;
DANOVARO et al., 2008). Even though conclusions from these broad-scale studies are based
on correlations from which it is difficult to infer causation, it seems that biodiversity has a
role to play on both local and regional scales in the marine realm.
We focus on aquatic ecosystems in this review as the effects of biodiversity on ecosystem
functioning may differ between aquatic and terrestrial environments (COVICH et al., 2004;
GILLER et al., 2004). Recent reviews have highlighted important differences in trophic structure (SHURIN et al., 2006) including the importance of herbivory (CEBRIAN and LARTIGUE,
2004) and trophic cascades and top-down control (SHURIN et al., 2002). The response of
plant diversity to consumer presence and fertilization also differs between aquatic and terrestrial systems (HILLEBRAND et al., 2007). Even diversity itself differs between the realms,
as marine systems may harbour less species, but much higher phylogenetic diversity than terrestrial systems (GILLER et al., 2004). Though diversity-functioning research lagged behind
in aquatic systems in the beginning, considerable progress has been made over the last few
years. The effects of plant diversity may be common and similar to those of terrestrial systems (DUARTE, 2000; BRUNO et al., 2005), and generally weaker than the effects of consumers (DUFFY, 2002). Enough evidence currently exists to suggest that the new paradigm is
maturing with more realistic scenarios and experiments providing mechanistic understanding
about the relationship between diversity and the functioning of aquatic ecosystems.
3. Maturation of the Biodiversity-Functioning Paradigm
3.1. Expanding the Scales of Inference: More Systems and Functions
As in many emerging paradigms, the scope of studies on the effects of biodiversity on ecosystem functioning has been narrow, very much focused on few aspects of biodiversity and
few ecosystem functions. Most studies used either species richness or a measure of functional richness (NAEEM et al., 1994; HOOPER and VITOUSEK, 1997; TILMAN et al., 1997) and the
response variables were mostly either productivity and nutrient uptake (NAEEM et al., 1994;
TILMAN et al., 1996) or a measure of stability (TILMAN and DOWNING, 1994; MCGRADYSTEED et al., 1997). This scope has become more general and more comprising through the
evolution of the paradigm (Fig. 1b). Other aspects of biodiversity, e.g., evenness, have been
incorporated (DANGLES and MALMQVIST, 2004; MULDER et al., 2004; HILLEBRAND et al.,
2008), and studies have started to investigate how the diversity within species (genotypic
variation) affects ecosystem processes (HUGHES and STACHOWICZ, 2004; GAMFELDT et al.,
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L. GAMFELDT and H. HILLEBRAND
2005a; REUSCH et al., 2005; GAMFELDT and KÄLLSTRÖM, 2007) (Fig. 1b, point 1). Most of
all, the definition of ecosystem function have started to include other important ecosystem
processes, acknowledging the complexity of ecosystem functioning (Fig. 1b, point 2). In
addition to the one-trophic level approach of many early studies, aquatic ecologists proposed
the importance of looking at multitrophic assemblages (DUFFY, 2002; GILLER et al., 2004)
and analyzed diversity effects on consumption rates (transfer between trophic levels) (JONSSON and MALMQVIST, 2000; CARDINALE et al., 2002; DUFFY et al., 2003). Other ecosystem
processes, which are now considered, comprise predation (BYRNES et al., 2006), rates of
bioturbation (EMMERSON et al., 2001), or – in terrestrial systems-pollination (FONTAINE et al.,
2006). For aquatic ecosystems, GILLER et al., (2004) listed more than 20 processes of relevance in ecosystems, which potentially are affected by diversity loss.
3.2. Spatial Scale, Coexistence and Metacommunities
Most experiments and models founding the biodiversity-ecosystem functioning paradigm
considered only local scales and local interactions of communities. However, there are good
reasons to include a broader approach including the regional species pool and dispersal
processes (GILLER et al., 2004). First, regional diversity is supposed to affect local diversity by altering the number of species potentially colonizing a certain site (RICKLEFS 1987;
SHURIN et al., 2000; HILLEBRAND and BLENCKNER, 2002). Second, the loss of species in a
local habitat may be transient and the ability of a system to persist may be more dependent on the rate of (re-)colonization rather than the number of species present. This includes
also the notion that the community composition may be constrained by dispersal limitation
(SHURIN et al., 2000; CACERES and SOLUK, 2002). Third, experiments with local manipulations of species richness, as they have been conducted in the biodiversity-ecosystem functioning framework, did not provide a stable coexistence mechanism for the high number
of species involved. Thus, these experiments would have lost many, if not most, of the
species over time. For these reasons, GILLER et al. (2004) proposed to conduct experiments
manipulating both local and regional richness as well as the dispersal rate in order to add
more realism to biodiversity-functioning research.
The importance of regional processes has been embedded in the concept of metacommunities (LEIBOLD et al., 2004; HOLYOAK et al., 2005), which represent local communities
connected via dispersal, e.g., lakes and ponds in a landscape or rock pools along the coast.
Metacommunity dynamics can lead to stable coexistence by a variety of mechanisms, among
these patch dynamics (coexistence along a colonization-competition trade-off), source-sink
dynamics (coexistence by high reproduction in one habitat and mass effect of propagules in
other locales of the metacommunity) or species sorting across a heterogeneous metacommunity (LEIBOLD et al., 2004).
The role of dispersal and propagule supply is becoming an important part of biodiversityfunctioning research (FRANCE and DUFFY, 2006; NAESLUND and NORBERG, 2006; MATTHIESSEN et al., 2007; Fig. 1b, point 3). Two models have analyzed how metacommunity dynamics
may change our understanding of the effects biodiversity loss. LOREAU et al. (2003) showed
that dispersal rates controlled the number of coexisting species in a metacommunity, which
then transfered into higher biomass production. Thus, they found higher richness in intermediate dispersal scenarios and a positive correlation between diversity and productivity. Also
a second model concluded that an extension of scale may alter the outcome of biodiversityecosystem functioning studies and suggested to acknowledge the importance of the regional
scale (CARDINALE et al., 2004).
Whereas a number of studies have analyzed the importance of metacommunity dynamics
for species coexistence (COTTENIE et al., 2003; KNEITEL and MILLER, 2003; CADOTTE and
FUKAMI, 2005), few actually transferred this to biodiversity-ecosystem functioning research.
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Biodiversity Effects on Ecosystem Functioning
For rock pool systems, communities arising from a regional species pool had higher abundances of zooplankton compared to communities stemming from local pools, with cascading effects on the primary producer level (NAESLUND and NORBERG, 2006). MATTHIESSEN
and HILLEBRAND (2006) showed that local diversity is maximized at intermediate dispersal
rate, which leads to higher resource use efficiency and primary production. Although their
experimental setup with marine microcosms differed from the model concepts of metacommunities, it seemed that providing a stable coexistence mechanism actually strengthened the
main hypothesis of the new paradigm that ecosystem process rates increase with increasing
diversity.
Regional aspects may affect biodiversity-ecosystem functioning relationships not only by
dispersal, but also by the structure of the landscape and the connectivity between different
habitats (Fig. 1b, point 4). GILLER et al. (2004) suggested that certain processes may be
enhanced rather by the diversity of habitats involved than by species richness. This may
be especially true for aquatic ecosystems with strong exchange of organisms, material and
energy across boundaries (benthic-pelagic coupling, riparian-zone – river).
3.3. Roles of Consumers and Interactions among Trophic Levels
Aquatic research has played an important role in elucidating the potential importance of
consumer diversity for ecosystem functioning. While documented extinctions of primary
producers are rare, they appear to be more common for consumer species (DUFFY, 2003).
For example, overexploitation of fish and shellfish in the oceans has resulted in dramatic
shifts in many ocean ecosystems (DAYTON et al., 1998; PAULY et al., 1998; JACKSON et al.,
2001; BELLWOOD et al., 2004), often with significant effects on vital ecosystem processes
(BELLWOOD et al., 2003; WORM et al., 2006; MYERS et al., 2007).
Accumulating evidence from aquatic studies suggest that the diversity of consumer species is indeed an important feature of aquatic ecosystems (Fig. 1b, point 5). A series of
experiments on fresh-water insects showed that the richness and evenness of these insect
larvae can determine process rates of leaf consumption (e.g., JONSSON and MALMQVIST, 2000;
JONSSON et al., 2001; DANGLES and MALMQVIST, 2004; JONSSON, 2006), and that these rates
may depend on a few dominant species and per capita responses by non-manipulated species
(RUESINK and SRIVASTAVA, 2001). For another set of aquatic insect larvae, resource consumption of filter feeders increased more than expected based on single species performances due
to interspecific facilitation (CARDINALE et al., 2002). WOJDAK and MITTELBACH (2007) took
the innovative approach to include habitat use of pond grazers as the predictor of ecosystem
properties. The explicit inclusion of habitat preference of organisms is likely to contribute
significantly to our knowledge about effects of diversity (SCHMITZ, 2007). Results from
seagrass systems indicate that a richness of marine herbivore mesograzers is important for
a range of processes such as epiphyte overgrowth and secondary production (DUFFY et al.,
2003). Similar results have been obtained for rocky shore communities where herbivore
and predator complementarity in feeding strategies appears to be important for community
structure (LOTZE and WORM, 2000; RÅBERG and KAUTSKY, 2007; GRIFFIN et al., 2008).
Food chain length can have profound effects on the importance of grazer diversity. For
example, in a seagrass system, grazer richness had effects on system processes only with
a predator present (DUFFY et al., 2005). Indeed, three manipulations of predator richness
suggest that losing predator diversity from marine systems can have cascading effects on
the algal communities (BYRNES et al., 2006; BRUNO and O’CONNOR, 2005; ELLIS et al.,
2007). The results of these experiments parallel those of observational studies on functional diversity and predator extinctions. In coastal marine systems, functional diversity
may be strongly correlated with species diversity, suggesting that functional redundancy is
low (MICHELI and HALPERN, 2005). This indicates that coastal habitats may be sensitive to
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species loss. Concordantly, kelp forests of the Californian coast were found to be strongly
top-down controlled rather than bottom-up (HALPERN et al., 2006, but see FOSTER et al.,
2006). It should be noted that simultaneous diversity changes at multiple trophic levels can
have interactive effects that may not be predicted by studying each trophic level in isolation
(GAMFELDT et al., 2005b). Using the framework of DUFFY et al. (2007), both horizontal (e.g.,
among species diversity) and vertical (e.g., number of trophic levels) components must be
considered simultaneously for a comprehensive picture of the effects biodiversity loss.
In addition to rates of consumption, consumers indirectly affect ecosystem processes
by altering nutrient cycling. Since species differ in habitat use and their requirements for
nutrients, species loss can affect nutrient recycling as shown for both tropical fresh-water
fish communities (MCINTYRE et al., 2007) and assemblages of sediment bioturbating invertebrates (EMMERSON et al., 2001; CALIMAN et al., 2007).
3.4. Multiple and Parallel Functions
Within the extensive biodiversity-ecosystem functioning research over the past decade,
most studies have used a single-function perspective, i.e., addressed the consequence of
species loss on single process rates or properties. The use of single response variables as
proxies for ecosystem functioning may ignore other important ecosystem processes (ROSENFELD, 2002; DUFFY et al., 2003). Equating single functions with overall functioning can be
highly misleading, especially if research ultimately aims to provide knowledge and advice
to management and conservation. Rather, individual functions and processes may be better
viewed as components of overall ecosystem functioning writ large (Fig. 1b, point 6).
The effect of multiple ecosystem functions on joint ecosystem functioning has been
explicitly examined quantitatively in four studies. There are indeed more studies that have
measured multiple functions (e.g., TILMAN et al., 1997; DUFFY et al., 2003; SPEHN et al.,
2005) but they have not been considered jointly. Using plants and an index of relative
resource use, HOOPER and VITOUSEK (1998) showed that the diversity of functional groups
was important for the total depletion of soil nutrients over time, and HECTOR and BAGCHI
(2007) found that plant species richness is more important for multifunctionality than for
single functions. GAMFELDT (2006) and GAMFELDT et al. (2008) examined a broader range
of systems and organisms that included marine seagrass and grazers, and reached similar
conclusions: as more functions are considered, the importance of biodiversity for ecosystem
functioning becomes more apparent. The combined results from these studies suggest that
focusing on individual functions can often be highly misleading, because a high level of
a single function does not equal overall ecosystem functioning. In contrast, it is possible
that mixtures perform worse than the best constituting species for each individual function
considered (unifunctional underyielding), but still experience multifunctional overyielding
because the identity of the best monoculture species switches between functions. In many
cases, only one ecosystem function is of interest and biodiversity may, or may not, be important for this function. Nonetheless, the more functions considered, the closer we get to an
approximation of overall ecosystem functioning.
3.5. Complementary Approaches and Experimental Design
Due to logistical constraints, experimental work has been limited in both space and time,
and this limits the possibility to extrapolate results to the real world. There is thus a need
to complement experiments and theoretical models with observational data on larger scales
(NAEEM, 2006), as in WORM et al. (2006). New approaches must also embrace the fact that
species loss is not random in response to stressors and exploitation. SOLAN et al. (2004)
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modelled a set of extinction scenarios for soft-bottom invertebrates and showed that the
magnitude of reduction in bioturbation depended on the covariation between species functional traits and their risk of extinction. Similar results were found for alternative extinction
scenarios of fresh-water fishes and their effects on nutrient recycling (MCINTYRE et al.,
2007). Combining field observations with experiments and modelling, BRACKEN et al. (2008)
showed that realistic scenarios of species loss in a macroalgal community resulted in declines
in nutrient uptake whereas random loss had no effect. Modelling the effects of biodiversity
loss using existing data from observational studies together with scenarios of global change
will be an important part of biodiversity-functioning research.
In terms of experimental design, there is an increased awareness within the field that
the design of most experiments to date have been such that it is hard to separate effects
of diversity and density of species. This is not surprising news to people well acquainted
with the literature on experimental design and the replacement series (JOLLIFFE, 2000). The
majority of studies have used a replacement design to examine the role of biodiversity.
This means that they have used the same total density (dtot) of organisms across diversity
treatments so that n number of species within species mixtures have a density of dtot/n. This
obviously confounds density with diversity, and it is hard to tell if observed effects are due
to increased diversity or decreased intraspecific competition. An alternative approach, the
additive design (e.g., CARDINALE et al., 2003), keeps the density of each species (dmono) constant so that species mixtures have a density of dmono · n. For a thorough understanding of
the ways in which both density and diversity affect functions, a combination of substitutive
and additive designs may be necessary (FIRBANK and WATKINSON, 1985; WEIS et al., 2007).
Furthermore, the number of possible unique species (or functional group) combinations,
and thus also the similarity among replicates, varies with diversity. This produces inherent
variance reduction effects, and the possibility to interpret uncontrolled error effects as true
diversity effects (HUSTON and MCBRIDE, 2002). BENEDETTI-CECCHI (2006) has proposed a
design that disentangles the effects of density and diversity. Furthermore, in order to detect
effects of consumer diversity on consumer production it is important that experiments are
run long enough for competition among species to occur, so that realised densities are
reached. Actual starting densities should then be less important for the outcome. The role of
functional diversity is also an important aspect of biodiversity that deserves more attention
(PETCHEY and GASTON, 2006).
4. Future Outlook
Current evidence from experimental studies generally shows that ecosystem functioning
can often be sustained by only a few species (CARDINALE et al., 2006). In many cases, a
small subset of species may be sufficient, and the loss of a large fraction of biodiversity from
systems may often have little effect on the magnitude of ecosystem functions (SOLAN et al.,
2004). Furthermore, the effects of biodiversity may interact with, or be much weaker than,
other factors such as disturbance, flow conditions and nutrient availability (CARDINALE et al.,
2000; BILES et al., 2003; DZIALOWSKI and SMITH, 2008). Manipulating both biodiversity and
other factors such as propagule and resource supply in a factorial design to evaluate the relative importance of these factors will be an important feature of future experiments.
Nonetheless, as the paradigm that biodiversity affects aquatic ecosystem performance
matures, we are receiving information from more realistic studies. Experiments are run over
larger scales spanning longer time periods, include more complex food webs, and are complemented by a wider set of approaches. These include the study of relationships between
species abundances and ecosystem processes over large scales in nature (NAEEM, 2006), the
exploration of the consequences of non-random species extinctions (e.g., JONSSON et al.,
2002; SOLAN et al., 2004; MCINTYRE et al., 2007), and meta-analyses of published experi© 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
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ments to gain new insights about the role of different mechanisms (CARDINALE et al., 2007).
Additionally, by re-examining data from studies that were not initially designed to address
the effect of biodiversity on functions (as in EMMERSON and HUXHAM, 2002), we can learn
from the vast literature that already exist on e.g., the roles of different species in succession
(PEARSON and ROSENBERG, 1978), nutrient cycling (SNELGROVE et al., 1997), and tolerance to
changing water temperatures (SOUTHWARD et al., 1995). For a thorough understanding about
how and when biodiversity can influence ecosystem functioning, however, future experimental studies must be designed to evaluate specific mechanisms, something that microcosm
systems are well suited to do (CADOTTE et al., 2005). Another set of informative experiments
involves removing one or a few target species from otherwise intact communities, and track
the effects on ecosystem functioning (SCHIEL, 2006). Removal experiments are unfortunately
still not widely used in biodiversity-ecosystem functioning studies.
Even though the term biodiversity refers to the diversity at any hierarchical level (genes,
species, ecosystems), studies addressing the importance of diversity at the higher levels of
organization are still missing. This is unfortunate, since human activity and global change are
likely to have large effects at the landscape level. Modelling approaches (e.g., SOLAN et al.,
2004) should be used on existing data on whole ecosystems to evaluate the importance of
landscape heterogeneity to overall ecosystem functioning.
One pressing question relates to the role of consumer diversity in ecosystems. The exact
roles of consumers in general, and predators in particular, are hard to predict as a consequence of indirect interactions, omnivory and cascading effects (DUFFY et al., 2007). Furthermore, the primary focus of consumer diversity has been on the effects of lower trophic
levels, whereas there is good reason to expect that it will also affect the production of the
consumers themselves (IVES et al., 2005; GAMFELDT et al., 2005b; WORM et al., 2006). It
is more difficult to examine consumer production because experiments have to run long
enough for consumers to grow and reproduce. A fruitful approach would be to remove consumer species in different combinations from natural systems and study if the lost biomass is
replaced by other complementary species. The role of consumer diversity at multiple trophic
levels and its influence on secondary production is an interesting area for future research.
In species-poor systems, or environments dominated by one or a few species, it would
be especially interesting to explore the relative importance and interaction of intra- and
interspecific diversity. For example, the genetic diversity of habitat-forming seagrass may
govern resistance to disturbance and disease, whereas the total diversity of associated primary producers and consumers is important for processes such as productivity and nutrient
recycling. To the best of our knowledge, there is to date no study that has addressed the
interaction between intra- and interspecific diversity and the effect on ecosystem functions.
Another challenge is to map and characterise the range of relevant functions of notable
importance in aquatic systems. Which functions are considered most important, how are
functions correlated across organisms and ecosystems, and how are multiple functions (overall functioning) affected by species loss (GAMFELDT et al., 2008)? This is important if we
are to be able to provide society and conservation management with guidance of why and
when biodiversity may matter for the functioning of natural ecosystems (SRIVASTAVA and
VELLEND, 2005; STACHOWICZ et al., 2007). Only by combining efforts on different scales
and with different methods can we start to fully understand the consequences of biodiversity
loss in real ecosystems.
5. Acknowledgements
LG was supported by a postdoc grant (2006-1173) from the Swedish research council Formas, and
we would like to thank RITA ADRIAN for inviting us to write this paper. The article benefited from comments by two anonymous reviewers.
© 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
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6. References
BELLWOOD, D. R., A. S. HOEY and J. H. CHOAT, 2003: Limited functional redundancy in high diversity
systems: resilience and ecosystem function on coral reefs. – Ecol. Lett. 6: 281–285.
BELLWOOD, D. R., T. P. HUGHES, C. FOLKE and M. NYSTRÖM, 2004: Confronting the coral reef crisis. –
Nature 429: 827–833.
BENEDETTI-CECCHI, L., 2006: Understanding the consequences of changing biodiversity on rocky shores:
How much have we learned from past experiments? – J. Exp. Mar. Biol. Ecol. 338: 193.
BILES, C. L., M. SOLAN, I. ISAKSSON, D. M. PATERSON, C. EMES and D. G. RAFFAELLI, 2003: Flow
modifies the effect of biodiversity on ecosystem functioning: an in situ study of estuarine sediments. –
J. Exp. Mar. Biol. Ecol. 285–286: 165–177.
BRACKEN, M. E. S., S. E. FRIBERG, C. A. GONZALEZ-DORANTES and S. L. WILLIAMS, 2008: Functional
consequences of realistic biodiversity changes in a marine ecosystem. – Proc. Natl. Acad. Sci. USA.
105: 924–928.
BRUNO, J. F. and M. I. O’CONNOR, 2005: Cascading effects of predator diversity and omnivory in a
marine food web. – Ecol. Lett. 8: 1048–1056.
BRUNO, J. F., K. E. BOYER, J. E. DUFFY, S. C. LEE and J. S. KERTESZ, 2005: Effects of macroalgal
species identity and richness on primary production in benthic marine communities. – Ecol. Lett. 8:
1165–1174.
BYRNES, J., J. J. STACHOWICZ, K. M. HULTGREN, A. RANDALL HUGHES, S. V. OLYARNIK and C. S. THORNBER, 2006: Predator diversity strengthens trophic cascades in kelp forests by modifying herbivore
behaviour. – Ecol. Lett. 9: 61–71.
CACERES, C. E. and D. A. SOLUK, 2002: Blowing in the wind: a field test of overland dispersal and
colonization by aquatic invertebrates. – Oecologia 131: 402–408.
CADOTTE, M. W. and T. FUKAMI, 2005: Dispersal, spatial scale, and species diversity in a hierarchically
structured experimental landscape. – Ecol. Lett. 8: 548–557.
CADOTTE, M. W., J. A. DRAKE and T. FUKAMI, 2005: Constructing nature: Laboratory models as necessary tools for investigating complex ecological communities. – Adv. Ecol. Res. 37: 333–353.
CALIMAN, A., J. J. F. LEAL, F. A. ESTEVES, L. S. CARNEIRO, R. L. BOZELLI and V. F. FARJALLA, 2007:
Functional bioturbator diversity enhances benthic-pelagic processes and properties in experimental
microcosms. – J. North Am. Benth. Soc. 26: 450–459.
CARDINALE, B. J., K. NELSON and M. A. PALMER, 2000: Linking species diversity to the functioning of
ecosystems: on the importance of environmental context. – Oikos 91: 175–183.
CARDINALE, B. J., M. A. PALMER and S. L. COLLINS, 2002: Species diversity enhances ecosystem functioning through interspecific facilitation. – Nature 415: 426–429.
CARDINALE, B. J., C. T. HARVEY, K. GROSS and A. R. IVES, 2003: Biodiversity and biocontrol: emergent
impacts of a multi-enemy assemblage on pest suppression and crop yield in an agroecosystem. –
Ecol. Lett. 6: 857–865.
CARDINALE, B. J., A. R. IVES and P. INCHAUSTI, 2004: Effects of species diversity on the primary productivity of ecosystems: extending our spatial and temporal scales of inference. – Oikos 104: 437–450.
CARDINALE, B. J., D. S. SRIVASTAVA, J. EMMETT DUFFY, J. P. WRIGHT, A. L. DOWNING, M. SANKARAN
and C. JOUSEAU, 2006: Effects of biodiversity on the functioning of trophic groups and ecosystems. –
Nature 443: 989–992.
CARDINALE, B. J., J. P. WRIGHT, M. W. CADOTTE, I. T. CARROLL, A. HECTOR, D. S. SRIVASTAVA, M. LOREAU
and J. J. WEIS, 2007: Impacts of plant diversity on biomass production increase through time because
of species complementarity. – Proc. Natl. Acad. Sci. USA. 104: 18123–18128.
CARLANDER, K. D., 1955: The standing crop of fish in lakes. – J. Fish. Res. Board Can. 12: 543–570.
CEBRIAN, J. and J. LARTIGUE, 2004: Patterns of herbivory and decomposition in aquatic and terrestrial
ecosystems. – Ecol. Monogr. 74: 237–259.
COTTENIE, K., E. MICHELS, N. NUYTTEN and L. DE MEESTER, 2003: Zooplankton metacommunity structure: Regional vs. local processes in highly interconnected ponds. – Ecology 84: 991–1000.
COVICH, A. P., M. C. AUSTEN, F. BÄRLOCHER, E. CHAUVET, B. J. CARDINALE, C. L. BILES, P. INCHAUSTI,
O. DANGLES, M. SOLAN, M. O. GESSNER, B. STATZNER and B. MOSS, 2004: The role of Biodiversity
in the functioning of freshwater and marine benthic ecosystems. – Bioscience 54: 767–775.
DANGLES, O. and B. MALMQVIST, 2004: Species richness-decomposition relationships depend on species
dominance. – Ecol. Lett. 7: 395–402.
© 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.revhydro.com
560
L. GAMFELDT and H. HILLEBRAND
DANOVARO, R., C. GAMBI, A. DELL’ANNO, C. CORINALDESI, S. FRASCHETTI, A. VANREUSEL, M. VINCX
and A. J. GOODAY, 2008: Exponential decline of deep-sea ecosystem functioning linked to benthic
biodiversity loss. – Current Biology 18: 1–8.
DARWIN, C., 1859: On the origin of species by means of natural selection. John Murray, London.
DAYTON, P. K., 1971: Competition, disturbance, and community organization – provision and subsequent
utilization of space in a rocky intertidal community. – Ecol. Monogr. 41: 351–389.
DAYTON, P. K., M. J. TEGNER, P. B. EDWARDS and K. L. RISER, 1998: Sliding baselines, ghosts, and
reduced expectations in kelp forest communities. – Ecol. Appl. 8: 309–322.
DUARTE, C. M., 2000: Marine biodiversity and ecosystem services: an elusive link. – J. Exp. Mar. Biol.
Ecol. 250: 117–131.
DUFFY, J. E., 2002: Biodiversity and ecosystem function: the consumer connection. – Oikos 99:
201–219.
DUFFY, J. E., 2003: Biodiversity loss, trophic skew and ecosystem functioning. – Ecol. Lett. 6:
680–687.
DUFFY, J. E., J. P. RICHARDSON and E. A. CANUEL, 2003: Grazer diversity effects on ecosystem functioning in seagrass beds. – Ecol. Lett. 6: 637–645.
DUFFY, J. E., J. P. RICHARDSON and K. E. FRANCE, 2005: Ecosystem consequences of diversity depend
on food chain length in estuarine vegetation. – Ecol. Lett. 8: 301–309.
DUFFY, J. E., B. J. CARDINALE, K. E. FRANCE, P. B. MCINTYRE, E. THEBAULT and M. LOREAU, 2007:
The functional role of biodiversity in ecosystems: incorporating trophic complexity. – Ecol. Lett. 10:
522–538.
DZIALOWSKI, A. R. and V. H. SMITH, 2008: Nutrient dependent effects of consumer identity and diversity
on freshwater ecosystem function. – Freshw. Biol. 53: 148–158.
EHRLICH, P. R. and A. H. EHRLICH, 1982: Extinction: the causes and consequences of the disappearance
of species. Random House, New York.
ELLIS, J. C., M. J. SHULMAN, M. WOOD, J. D. WITMAN and S. LOZYNIAK, 2007: Regulation of intertidal
food webs by avian predators on New England rocky shores. – Ecology 88: 853–863.
ELTON, C. S., 1958: The ecology of invasions by animals and plants. Methuen and Co Ltd, London.
EMMERSON, M. M. SOLAN, C. EMES, D. M. PATERSON and D. RAFFAELLI, 2001: Consistent patterns and
the idiosyncratic effects of biodiversity in marine ecosystems. – Nature 411: 73–77.
EMMERSON, M. and M. HUXHAM, 2002: How can marine ecology contribute to the biodiversity – ecosystem functioning debate?– In: M. LOREAU, S. NAEEM and P. INCHAUSTI (eds.), Biodiversity and
ecosystem functioning synthesis and perspectives. Oxford University Press, pp. 139–146.
FIRBANK, L. G. and A. R. WATKINSON, 1985: On the analysis of competition within 2-species mixtures
of plants. – J. Appl. Ecol. 22: 503–517.
FONTAINE, C., I. DAJOZ, J. MERIGUET and M. LOREAU, 2006: Functional diversity of plant – pollinator
interaction webs enhances the persistence of plant communities. – PLoS Biol. 4: 129–135.
FOSTER, M. S., M. S. EDWARDS, D. C. REED, D. R. SCHIEL, ZIMMERMAN, R. C., M. A. STEELE,
S. C. SCHROETER, R. C. CARPENTER, D. J. KUSHNER, B. S. HALPERN, K. COTTENIE and B. R. BROITMAN, 2006: Top-down vs. bottom-up effects in kelp forests. – Science 313: 1737–1739.
FRANCE, K. E. and J. E. DUFFY, 2006: Diversity and dispersal interactively affect predictability of ecosystem function. – Nature 441: 1139–1143.
GAMFELDT, L., J. WALLÉN, P. R. JONSSON, K. BERNTSSON and J. HAVENHAND, 2005a: Intraspecific diversity enhances settling success in a marine invertebrate. – Ecology 86: 3219–3224.
GAMFELDT, L., H. HILLEBRAND and P. R. JONSSON, 2005b: Species richness changes across two trophic
levels simultaneously affect prey and consumer biomass. – Ecol. Lett. 8: 696–703.
GAMFELDT, L., 2006: Biodiversity and ecosystem functions – the importance of marine biodiversity for
ecosystem functioning. PhD thesis, Department of Marine Ecology. Göteborg University.
GAMFELDT, L. and B. KÄLLSTRÖM, 2007: Increasing intraspecific diversity increases predictability in
population survival in the face of perturbations. – Oikos 116: 700–705.
GAMFELDT, L., H. HILLEBRAND and P. R. JONSSON, 2008: Multiple functions increase the importance of
biodiversity for overall ecosystem functioning. – Ecology 89: 1223–1231.
GAUSE, G. F., 1934: The struggle for existence. The Williams and Wilkins Company, Baltimore.
GILLER, P. S., H. HILLEBRAND, U.-G. BERNINGER, M. O. GESSNER, S. HAWKINS, P. INCHAUSTI, C. INGLIS,
H. LESLIE, B. MALMQVIST, M. T. MONAGHAN, P. J. MORIN and G. O’MULLAN, 2004: Biodiversity
effects on ecosystem functioning: emerging issues and their experimental test in aquatic environments. – Oikos 104: 423–436.
© 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.revhydro.com
Biodiversity Effects on Ecosystem Functioning
561
GRACE, J. B., T. MICHAEL ANDERSON, M. D. SMITH, E. SEABLOOM, S. J. ANDELMAN, G. MECHE, E. WEIHER,
L. K. ALLAIN, H. JUTILA, M. SANKARAN, J. KNOPS, M. RITCHIE and M. R. WILLIG, 2007: Does species
diversity limit productivity in natural grassland communities? – Ecol. Lett. 10: 680–689.
GRIFFIN, J. N., K. DE LA HAYE, S. HAWKINS, R. THOMPSON and S. JENKINS, 2008: Predator diversity
effects and ecosystem functioning: density modifies the effect of resource partitioning. – Ecology
89: 298–305.
GRIME, J. P., 1997: Biodiversity and ecosystem function: the debate deepens. – Science 277: 1260–
1261.
HALPERN, B. S., K. COTTENIE and B. R. BROITMAN, 2006: Strong top-down control in Southern California kelp forest ecosystems. – Science 312: 1230–1232.
HARPER, J. L., 1967: A Darwinian Approach to Plant Ecology. – J. Ecology 55: 247–270.
HECTOR, A., B. SCHMID, C. BEIERKUHNLEIN, M. C. CALDEIRA, M. DIEMER, P. G. DIMITRAKOPOULOS,
J. A. FINN, H. FREITAS, P. S. GILLER, J. GOOD, R. HARRIS, P. HÖGBERG, K. HUSS-DANELL, J. JOSHI,
A. JUMPPONEN, C. KÖRNER, P. W. LEADLEY, M. LOREAU, A. MINNS, C. P. H. MULDER, G. O’DONOVAN,
S. J. OTWAY, J. S. PEREIRA, A. PRINZ, D. J. READ, M. SCHERER-LORENZEN, E. D. SCHULZE, A. S. D. SIAMANTZIOURAS, E. M. SPEHN, A. C. TERRY, A. Y. TROUMBIS, F. I. WOODWARD, S. YACHI and J. H. LAWTON, 1999: Plant diversity and productivity experiments in European grasslands. – Science 286:
1123–1127.
HECTOR, A. and R. BAGCHI, 2007: Biodiversity and ecosystem multifunctionality. – Nature 448:
188–190.
HILLEBRAND, H. and T. BLENCKNER, 2002: Regional and local impact on species diversity – from pattern
to processes. – Oecologia 132: 479–491.
HILLEBRAND, H., D. S. GRUNER, E. T. BORER, M. E. S. BRACKEN, E. E. CLELAND, J. J. ELSER, W. S. HARPOLE, J. T. NGAI, E. W. SEABLOOM, J. B. SHURIN and J. E. SMITH, 2007: Consumer versus resource
control of producer diversity depends on ecosystem type and producer community structure. – Proc.
Natl. Acad. Sci. USA. 104: 10904–10909.
HILLEBRAND, H., D. M. BENNETT and M. W. CADOTTE, 2008: The consequences of dominance: A review
of the effects of evenness on local and regional ecosystem processes. – Ecology 89: 1510–1520.
HOLYOAK, M., M. A. LEIBOLD, N. M. MOUQUET, R. D. HOLT and M. F. HOOPES. 2005. Metacommunities: A framework for large-scale community ecology. – In: M. HOLYOAK, M. A. LEIBOLD and
R. D. HOLT (eds), Metacommunities – Spatial dynamics and ecological communities. University of
Chicago Press, Chicago, 31 pp.
HOOPER, D. U. and P. M. VITOUSEK, 1997: The effects of plant composition and diversity on ecosystem
processes. – Science 277: 1302–1305.
HOOPER, D. U. and P. M. VITOUSEK, 1998: Effects of plant composition and diversity on nutrient
cycling. – Ecol. Monogr. 68: 121–149.
HUGHES, A. R. and J. J. STACHOWICZ, 2004: Genetic diversity enhances the resistance of a seagrass
ecosystem to disturbance. – Proc. Natl. Acad Sci. USA. 101: 8998–9002.
HUSTON, M. A. and A. C. MCBRIDE, 2002: Evaluating the relative strengths of biotic versus abiotic
controls on ecosystem processes. – In: M. LOREAU, S. NAEEM and P. INCHAUSTI (eds.), Biodiversity
and ecosystem functioning, synthesis and perspectives. Oxford University Press, pp. 47–60.
HUTCHINSON, G. E., 1959: Homage to Santa Rosalia or why are there so many kinds of animals? –
Am. Nat. 93: 145–159.
HUTCHINSON, G. E., 1961: The Paradox of the Plankton. – Am. Nat. 95: 137.
IVES, A. R., B. J. CARDINALE and W. E. SNYDER, 2005: A synthesis of subdisciplines: predator-prey
interactions, and biodiversity and ecosystem functioning. – Ecol. Lett. 8: 102–116.
JACKSON, J. B. C., M. X. KIRBY, W. H. BERGER, K. A. BJORNDAL, L. W. BOTSFORD, B. J. BOURQUE,
R. H. BRADBURY, R. COOKE, J. ERLANDSON, J. A. ESTES, T. P. HUGHES, S. KIDWELL, C. B. LANGE,
H. S. LENIHAN, J. M. PANDOLFI, C. H. PETERSON, R. S. STENECK, M. J. TEGNER and R. R. WARNER,
2001: Historical overfishing and the recent collapse of coastal ecosystems. – Science 293: 629–638.
JOLLIFFE, P. A., 2000: The replacement series. – J. Ecology 88: 371–385.
JONSSON, M. and B. MALMQVIST, 2000: Ecosystem process rate increases with animal species richness:
evidence from leaf-eating, aquatic insects. – Oikos 89: 519–523.
JONSSON, M., B. MALMQVIST and P. O. HOFFSTEN, 2001: Leaf litter breakdown rates in boreal streams:
does shredder species richness matter? – Freshw. Biol. 46: 161–171.
© 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.revhydro.com
562
L. GAMFELDT and H. HILLEBRAND
JONSSON, M., O. DANGLES, B. MALMQVIST and F. GUÉROLD, 2002: Simulating species loss
following perturbation: assessing the effects on process rate. – Proc. R. Soc. London, Ser. B 269:
1047–1052.
JONSSON, M., 2006: Species richness effects on ecosystem functioning increase with time in an ephemeral resource system. – Acta Oecol. 29: 72–77.
KAISER, J., 2000: Rift over biodiversity divides ecologists. – Science 289: 1282–1283.
KNEITEL, J. M. and T. E. MILLER, 2003: Dispersal rates affect species composition in metacommunities
of Sarracenia purpurea inquilines. – Am. Nat. 162: 165–171.
LEIBOLD, M. A., M. HOLYOAK, N. MOUQUET, P. AMARASEKARE, J. M. CHASE, M. F. HOOPES, R. D. HOLT,
J. B. SHURIN, R. LAW, D. TILMAN, M. LOREAU and A. GONZALEZ, 2004: The metacommunity concept:
a framework for multi-scale community ecology. – Ecol. Lett. 7: 601–613.
LEVINE, J. M., 2000: Species diversity and biological invasions: relating local process to community
pattern. – Science 288: 852–854.
LOREAU, M., N. MOUQUET and A. GONZALEZ, 2003: Biodiversity as spatial insurance in heterogenous
landscapes. – Proc. Natl. Acad. Sci. USA. 100: 12765–12770.
LOTZE, H. K. and B. WORM, 2000: Variable and complementary effects of herbivores on different life
stages of bloom-forming macroalgae. – Mar. Ecol. Pro. Ser. 200: 167–175.
MACARTHUR, R., 1955: Fluctuations of animal populations, and a measure of community stability. –
Ecology 36: 533–536.
MATTHIESSEN, B. and H. HILLEBRAND, 2006: Dispersal frequency affects local biomass production by
controlling local diversity. – Ecol. Lett. 9: 652–662.
MATTHIESSEN, B., L. GAMFELDT, P. R. JONSSON and H. HILLEBRAND, 2007: Effects of grazer richness and
composition on algal biomass in a closed and open marine system. – Ecology 88: 178–187.
MAY, R. M., 1972: Will a large complex system be stable? – Nature 238: 413–414.
MCGRADY-STEED, J., P. M. HARRIS and P. J. MORIN, 1997: Biodiversity regulates ecosystem predictability. – Nature 390: 162–165.
MCINTYRE, P. B., L. E. JONES, A. S. FLECKER and M. J. VANNI, 2007: Fish extinctions alter nutrient
recycling in tropical freshwaters. – Proc. Natl. Acad. Sci. USA. 104: 4461–4466.
MICHELI, F. and B. S. HALPERN, 2005: Low functional redundancy in coastal marine assemblages. –
Ecol. Lett. 8: 391–400.
MULDER, C. P. H., D. D. ULIASSI and D. F. DOAK, 2001: Physical stress and diversity-productivity relationships: the role of positive interactions. – Proc. Natl. Acad. Sci. USA. 98: 6704–6708.
MULDER, C. P. H., E. BAZELEY-WHITE, P. G. DIMITRAKOPOULOS, A. HECTOR, M. SCHERER-LORENZEN
and B. SCHMID, 2004: Species evenness and productivity in experimental plant communities. – Oikos
107: 50–63.
MYERS, R. A., J. K. BAUM, T. D. SHEPHERD, S. P. POWERS and C. H. PETERSON, 2007: Cascading effects
of the loss of apex predatory sharks from a coastal ocean. – Science 315: 1846–1850.
NAEEM, S., L. J. THOMPSON, S. P. LAWLER, J. H. LAWTON and R. M. WOODFIN, 1994: Declining biodiversity can alter the performance of ecosystems. – Nature 368: 734–737.
NAEEM, S. and S. LI, 1997: Biodiversity enhances ecosystem reliability. – Nature 390: 507–509.
NAEEM, S., 2002: Ecosystem consequences of biodiversity loss: the evolution of a paradigm. – Ecology
83: 1537–1552.
NAEEM, S., 2006: Expanding scales in biodiversity-based research: challenges and solutions for marine
systems. – Mar. Ecol. Pro. Ser. 311: 273–283.
NAESLUND, B. and J. NORBERG, 2006: Ecosystem consequences of the regional species pool. – Oikos
115: 504–512
PAINE, R. T., 1966: Food web complexity and species diversity. – Am. Nat. 100: 65–75.
PAINE, R. T., 2002: Advances in ecological understanding: By Kuhnian revolution or conceptual evolution? – Ecology 83: 1553–1559.
PAULY, D., V. CHRISTENSEN, J. DALSGAARD, R. FROESE and F. TORRES, JR., 1998: Fishing Down Marine
Food Webs. – Science 279: 860–863.
PEARSON, T. H. and R. ROSENBERG, 1978: Macrobenthic succession in relation to organic enrichment
and pollution of the marine environment. – Oceanogr. Mar. Biol. Ann. Rev. 16: 229–311.
PETCHEY, O. L., P. T. MCPHEARSON, T. M. CASEY and P. J. MORIN, 1999: Environmental warming alters
food-web structure and ecosystem function. – Nature 402: 69–72.
© 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.revhydro.com
Biodiversity Effects on Ecosystem Functioning
563
PETCHEY, O. L., A. L. DOWNING, G. G. MITTELBACH, L. PERSSON, C. F. STEINER, P. H. WARREN and
G. WOODWARD, 2004: Species loss and the structure and functioning of multitrophic aquatic systems. – Oikos 104: 467–478.
PETCHEY, O. L. and K. J. GASTON, 2006: Functional diversity: back to basics and looking forward. –
Ecol. Lett. 9: 741–758.
PIMM, S. L., G. J. RUSSELL, J. L. GITTLEMAN and T. M. BROOKS, 1995: The future of biodiversity. –
Nature 269: 347–350.
RÅBERG, S. and L. KAUTSKY, 2007: Consumers affect prey biomass and diversity through resource
partitioning. – Ecology 88: 2468–2473.
RAFFAELLI, D., B. J. CARDINALE, A. L. DOWNING, K. A. M. ENGELHARDT, J. L. RUESINK, M. SOLAN and
D. S. SRIVASTAVA, 2005: Reinventing the wheel in ecology research? – Science 307: 1875–1876.
REUSCH, T. B. H., A. EHLERS, A. HAMMERLI and B. WORM, 2005: Ecosystem recovery after climatic
extremes enhanced by genotypic diversity. – Proc. Natl. Acad. Sci. USA. 102: 2826–2831.
RICKLEFS, R. E., 1987: Community diversity: Relative roles of local and regional processes. – Science
235:167–171.
ROSENFELD, J. S., 2002: Logical fallacies in the assessment of functional redundancy. – Cons. Biol. 16:
837–839.
RUESINK, J. L. and D. S. SRIVASTAVA, 2001: Numerical and per capita responses to species loss: mechanisms maintaining ecosystem function in a community of stream insect detritivores. – Oikos 93:
221–234.
SCHIEL, D. R., 2006: Rivets or bolts? When single species count in the function of temperate rocky reef
communities. – J. Exp. Mar. Biol. Ecol. 338: 233.
SCHMITZ, O. J., 2007: Predator diversity and trophic interactions. – Ecology 88: 2415–2426.
SCHULZE, E.-D. and H. A. MOONEY, 1993: Biodiversity and ecosystem function. Springer Verlag, Berlin.
SHURIN, J. B., J. E. HAVEL, M. A. LEIBOLD and B. PINEL ALLOUL, 2000: Local and regional zooplankton
species richness: A scale-independent test for saturation. – Ecology 81: 3062–3073.
SHURIN, J. B., E. T. BORER, E. W. SEABLOOM, K. ANDERSON, C. A. BLANCHETTE, B. BROITMAN,
S. D. COOPER and B. S. HALPERN, 2002: A cross-ecosystem comparison of the strength of trophic
cascades. – Ecol. Lett. 5: 785–791.
SHURIN, J. B., D. S. GRUNER and H. HILLEBRAND, 2006: All wet or dried up? Real differences between
aquatic and terrestrial food webs. – Proc. R. Soc. London, Ser. B 273: 1–9.
SNELGROVE, P., T. H. BLACKBURN, P. A. HUTCHINGS, D. M. ALONGI, J. F. GRASSLE, H. HUMMEL, G. KING,
I. KOIKE, P. J. D. LAMBSHEAD, N. B. RAMSING and V. SOLIS-WEISS, 1997: The importance of marine
sediment biodiversity in ecosystem processes. – Ambio 26: 578–583.
SOLAN, M., B. J. CARDINALE, A. L. DOWNING, K. A. M. ENGELHARDT, J. L. RUESINK and D. S. SRIVASTAVA, 2004: Extinction and Ecosystem Function in the Marine Benthos. – Science 306: 1177–1180.
SOUTHWARD, A. J., S. J. HAWKINS and M. T. BURROWS, 1995: 70 Years observations of changes in distribution and abundance of zooplankton and intertidal organisms in the Western English-channel in
relation to rising sea temperature. – J. Therm. Biol. 20: 127–155.
SPEHN, E. M., A. HECTOR, J. JOSHI, M. SCHERER-LORENZEN, B. SCHMID, E. BAZELEY-WHITE, C. BEIERKUHNLEIN, M. C. CALDEIRA, M. DIEMER, P. G. DIMITRAKOPOULOS, J. A. FINN, H. FREITAS, P. S. GILLER,
J. GOOD, R. HARRIS, P. HOGBERG, K. HUSS-DANELL, A. JUMPPONEN, J. KORICHEVA, P. W. LEADLEY,
M. LOREAU, A. MINNS, C. P. H. MULDER, G. O’DONOVAN, S. J. OTWAY, C. PALMBORG, J. S. PEREIRA,
A. B. PFISTERER, A. PRINZ, D. J. READ, E. D. SCHULZE, A. S. D. SIAMANTZIOURAS, A. C. TERRY,
A. Y. TROUMBIS, F. I. WOODWARD, S. YACHI and J. H. LAWTON, 2005: Ecosystem effects of biodiversity manipulations in European grasslands. – Ecol. Monogr. 75: 37–63.
SRIVASTAVA, D. S. and M. VELLEND, 2005: Biodiversity-ecosystem function research: is it relevant to
conservation? – Ann. Rev. Ecol. Evol. Syst. 36: 267–294.
STACHOWICZ, J. J., R. B. WHITLATCH and R. W. OSMAN, 1999: Species diversity and invasion resistance
in a marine ecosystem. – Science 286: 1577–1579.
STACHOWICZ, J. J., J. F. BRUNO and J. E. DUFFY, 2007: Understanding the effects of marine biodiversity
on communities and ecosystems. – Ann. Rev. Ecol. Evol. Syst. 38: 739–766.
TILMAN, D. and J. A. DOWNING, 1994: Biodiversity and Stability in Grasslands. – Nature 367: 363–
365.
TILMAN, D., D. WEDIN and J. KNOPS, 1996: Productivity and sustainability influenced by biodiversity
in grassland ecosystems. – Nature 379: 718–720.
© 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.revhydro.com
564
L. GAMFELDT and H. HILLEBRAND
TILMAN, D., J. KNOPS, D. WEDIN, P. REICH, M. RITCHIE and E. SIEMANN, 1997: The influence of functional diversity and composition on ecosystem processes. – Science 277: 1300–1302.
VITOUSEK, P. M., H. A. MOONEY, J. LUBCHENCO and J. M. MELILLO, 1997: Human domination of earth’s
ecosystems. – Science 277: 494–499.
WEIS, J. J., B. J. CARDINALE, K. J. FORSHAY and A. R. IVES, 2007: Effects of species diversity on community biomass production change over the course of succession. – Ecology 88: 929–939.
WHITTAKER, R. H., 1960: Vegetation of the Siskiyou Mountains, Oregon and California. – Ecol. Monogr. –
30: 279–338.
WOJDAK, J. M. and G. G. MITTELBACH, 2007: Consequences of niche overlap for ecosystem functioning:
An experimental test with pond grazers. – Ecology 88: 2072–2083.
WORM, B., E. B. BARBIER, N. BEAUMONT, J. E. DUFFY, C. FOLKE, B. S. HALPERN, J. B. C. JACKSON,
H. K. LOTZE, F. MICHELI, S. R. PALUMBI, E. SALA, K. A. SELKOE, J. J. STACHOWICZ and R. WATSON,
2006: Impacts of biodiversity loss on ocean ecosystem services. – Science 314: 787–790.
Manuscript received October 22nd, 2007; revised February 7th, 2008; accepted February 27th, 2008
© 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.revhydro.com