Difference between revisions of "Biodiversity and Ecosystem function"

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== ''' A review of biodiversity-ecosystem function research ''' ==
 
  
  
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Human needs and actions have, and will continue to, extensively alter ecosystems and biodiversity on a global scale <ref name = "Vitousek"> Vitousek, P.M., Mooney, H.A., Lubchenco, J. and Melillo, J.M. (1997). Human domination of earth’s ecosystems. ''Science'' 277: 494-499</ref>. Predictions of changes in biodiversity, not only in marine, but also terrestrial and freshwater ecosystems <ref name = "Sala"> Sala, O.E., Chapin, F.S., Armesto, J.J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, E., Huenneke, L.F., Jackson, R.B., Kinzig, A., Leemans, R., Lodge, D.M., Mooney, H.A., Oesterheld, M., Poff, N.L., Sykes, M.T., Walker, B.H., Walker, M. and Wall, D.H. (2000). Biodiversity - Global biodiversity scenarios for the year 2100. ''Science'' 287: 1770-1774. </ref>, have raised substantial concern over the consequences of biodiversity loss on ecosystem processes and function, which subsequently affect the provision of ecosystem goods and services, and ultimately affect human well-being <ref name = "Diaz"> Diaz, D., Fargione, J., Chapin, F.S. III and Tilman, D. (2006). Biodiversity loss threatens human well-being. ''PLOS Biology'' 4: 1300-1305.</ref>.
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== Introduction ==
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Since the early 1990’s a portfolio of evidence obtained from the development of theory, laboratory experiments, field experiments and observational studies has shown that, irrespective of the system under study, increasing biodiversity tends to have positive effects on ecosystem properties, although the pattern of response may vary depending on the ecosystem and species investigated.
 
  
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The recognition that species interactions may play important roles in ecosystems and the rapidly emerging interest in the biodiversity conservation have prompted ecologists to ask new questions on the relationships between '[[biodiversity]]' and '[[ecosystem function]]' (for example, Walker, 1992<ref>Walker, B.H., 1992. Biodiversity and ecological redundancy. Conserv. Biol. 6: 18-23.</ref>; Schultze and Mooney, 1993<ref>Schulze, E.-D. and Mooney, H. A. (eds). 1993. Biodiversity and ecosystem function. Springer Verlag.</ref>; Jones and Lawton, 1995<ref>Jones, C. G., and Lawton, J. H. editors. 1995. Linking species and ecosystems. Chapman and Hall, New York, New York, USA.</ref>; Johnson et al., 1996<ref>Johnson, K.H., Vogt, K.A., Clark, H., Schmitz, O. and Vogt, D. 1996.  Biodiversity and the productivity and stability of ecosystems. Trends in Ecology & Evolution 11: 372-377</ref>).
  
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[[Image:Flow diagramm.jpg|thumb|right|450px|Figure 1: Summary of research approaches adopted to address the relationship between biodiversity and ecosystem function in the peer-reviewed scientific literature. Yellow boxes represent theoretical studies, green boxes represent experimental manipulations of species diversity, red boxes represent the observational studies and the purple boxes represent those studies in which BEF concepts are linked to, or applied, in the real world. Modified from Godbold, J.A. (2008). Marine benthic biodiversity-ecosystem function relations in complex systems. Ph.D. Thesis, University of Aberdeen.]]
 
  
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== Emergence of a new paradigm ==
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== Importance of ecosystem function ==
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The central thesis that guided early community ecology saw patterns in the distribution and abundance of species merely as an expression of the abiotic (chemical and physical) and biotic (species interactions) components of the environment, giving a predictive understanding of species distribution and abundance within ecosystems <ref name="Pearson"> Pearson, T.H. and Rosenberg, R. (1978). Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. ''Oceanography and Marine Biology: An Annual Review'' 16: 229-311</ref>. In the early 1990’s, however, an increasing number of ecologists began to challenge this view and, instead, started to examine, how ecosystem properties are mediated by the biota <ref name="Schulze"> Schulze, E.D. and Mooney, J.A. (1993). Biodiversity and ecosystem function. Springer-Verlag, Berlin</ref>. A wide range of hypotheses were developed describing the form of the biodiversity-ecosystem function relationship and which collectively formed a framework within which this relationship could be tested experimentally <ref name="Schmid 2002"> Schmid, B., Hector, A. and Huston, M.A. (2002). The design and anlalysis of biodiversity experiments. In Loreau, M., Naeem, S. and Inchausti, P. (eds) Biodiversity and ecosystem functioning: Synthesis and perspectives. Oxford University Press. pp. 61-75.</ref>.
 
  
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In a series of phases, biodiversity-ecosystem function research has steadily improved to make experimental designs and model predictions more realistic (Figure 1). The timing of publications from each phase shows that, although different approaches have been used within the biodiversity-ecosystem function framework almost since the first influential paper was published in 1994 <ref name="Naeem 1994"> Naeem, S., Thompson, L.J., Lawler, S.P., Lawton, J.H. and Woodfin, R.M. (1994). Declining biodiversity can alter the performance of ecosystems. ''Nature'' 368: 734-736.</ref>, there has been a general trend for experimental and theoretical studies to incorporate more natural environmental complexities (Reality filter, Figure 1).
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One reason for the interest in the functional role of biodiversity (rather than structural) in ecosystems is that society might be more likely to take action to preserve biodiversity if it could be shown that there was some direct economic gain by doing it (Bengtsson, 1998<ref name=Beng>Bengtsson, J. 1998. Which species? What kind of diversity? Which ecosystem function? Some problems in studies of relations between biodiversity and ecosystem function. Applied Soil Ecology 10: 191-199</ref>).
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Over the last fifteen years, an increasing number of studies have focused on biodiversity. This is principally because the world’s flora and fauna are disappearing at rates greater than during historical mass extinction events (Chapin et al, 2001<ref>Chapin, F. S., III, Sala, O. E. and Huber-Sannwald, E. editors. 2001. Global biodiversity in a changing environment: scenarios for the 21st century. Springer-Verlag, New York, New York, USA.</ref>). As suggested by Thomas et al. (2004<ref>Thomas, C.D., Cameron, A., Green, R.E., Bakkenes, M., Beaumont, L.J., Collingham, Y.C., Erasmus, B.F.N., de Siqueira, M.F., Grainger, A., Hannah, L., Hughes, L., Huntley, B., van Jaarsveld, A.S., Midgley, G.F., Miles, L., Ortega-Huerta, M.A., Townsend, P.A., Phillips, O.L. and Williams, S.E. 2004. Extinction risk from climate change. Nature 427: 145–148</ref>), there is an 18 to 35% risk of species-level extinction resulting from climate changes by the year 2050. Moreover, other processes, for example, agricultural expansion in response to an increasing demand for food, have a negative impact on biodiversity as a result of habitat destruction (Tilman et al., 2001<ref>Tilman, D., Reich, P. B., Knops, J., Wedin, D., Mielke, T. and Lehman C. 2001. Diversity and productivity in a longterm grassland experiment. Science 294: 843–845</ref>; Humbert and Dorigo, 2005<ref name=HD>Humbert, J.F. and Dorigo, U. 2005  Biodiversity and aquatic ecosystem functioning: A mini-review. Ecosystem Health and Management 8: 367-374</ref>).
  
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== Phase 1 - Laboratory experiments ==
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Biodiversity and Ecosystem function are central to both community and ecosystems ecology and need to be understood to predict, for example, how communities and ecosystems respond to environmental change (Bengtsson, 1998<ref name=Beng/>) and on understanding how declining diversity influences ecosystem services on which humans depend (Duffy, 2003<ref name=Duf>Duffy, J.E. 2003. Biodiversity loss, trophic skew and ecosystem functioning. Ecol. Lett. 6: 680–687</ref>).  
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Initially, biodiversity-ecosystem function relationships were investigated by manipulating biodiversity under controlled conditions in the laboratory (Figure 2a, b) <ref name = "Covich"> Covich, A.P., Austen, M.C., Barlöcher, F., Chauvet, E., Cardinale, B.J., Biles, C.L., Inchausti, P., Dangles, O., Solan, M., Gessner, M.O., Statzner, B. and Moss, B. (2004). The role of Biodiversity in the functioning of freshwater and marine benthic ecosystems. ''BioScience'' 54: 767-775.>/ref>,<ref name = "Hooper"> Hooper, D.U., Chapin, F.S. III, Ewel, J.J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J.H., Lodge, D.M., Loreau, M., Naeem, S., Schmid, B., Setala, H., Symstad, A.J., Vandermeer, J., Wardle, D.A. (2005). Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. ''Ecological Monographs'' 75: 3 - 35.>/ref>. In such studies, simple, single species communities are randomly assembled and their effects on ecosystem function determined. Then diversity is increased by constructing multi-species assemblages comprising the single species that have already been characterised and the effects of these multi-species assemblages on ecosystem function is determined (Figure 2c). If the observed response of the multi-specific assemblages differs from the response predicted by summation of the single species responses, then it is concluded that diversity has had an effect.
 
  
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[[Image:Figure 2a.jpg|thumb|left|300px|Figure 2a: Mesocosms used to investigate the effect of invertebrate biodiversity loss on sediment nutrient release, e.g. 9.]]
 
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[[Image:Figure 2b.jpg|thumb|300px|none|Figure 2b: Mesocosms used to investigate the effect of biodiversity loss on bioturbation and nutrient release, e.g. 10, 36.]] 
 
  
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== Research on Ecosystem Function ==
  
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Although these experiments successfully articulated biodiversity-ecosystem function hypotheses and allowed for the unambiguous interpretation of cause-effect relationships, critics were quick to assert that such studies lack realism because they tend to only include a few species (representing only a subset of the total community), often only from one trophic level, and they invariably assume that species loss is random. In addition, these types of experiments attracted further criticism because ecosystem function is measured infrequently and in the absence of the appropriate environmental context, thus making applicability to the real world questionable <ref name = "Srivastava"> Srivastava, D.S. and Vellend, M. (2005). Biodiervsity-ecosystem function research: is it relevant to conservation? Annual review of Ecology, Evolution and Systematics 36: 267-294.>/ref>.
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[[A review of biodiversity-ecosystem function research|Research on Biodiversity - Ecosystem Function]] (the BEF agenda) has stimulated a new and highly productive intercourse between population, community, ecosystem, and conservation ecology (Kinzig et al. 2002<ref>Kinzig, A. P., Pacala, S. W. and Tilman, D. (eds). 2002. The functional consequences of biodiversity. Princeton Univ. Press. </ref>; Loreau et al. 2002<ref name=Lo2>Loreau, M., Naeem, S. and Inchausti, P. 2002. Biodiversity and Ecosystem Function – Synthesis and Perspectives. Oxford University Press</ref>; Duffy, 2003<ref name=Duf/>).
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Most experimental evidence for biodiversity effects on ecosystem function has come from terrestrial ecosystems, particularly grasslands (Naeem et al. 1994<ref name=Na94>Naeem, S., Thompson, L. J., Lawler, S. P. et al. 1994. Declining biodiversity can alter the performance of ecosystems. Nature 368: 734-737</ref>, Tilmann et al. 1997<ref name=Til97>Tilman, D., Knops, J. M. H., Wedin, D. et al. 1997. The influence of functional diversity and composition on ecosystem processes. / Science 277: 1300-1302</ref>, Hector et al. 1999<ref name=Hec99>Hector, A., Schmid, B., Beierkuhnlein, C. et al. 1999. Plant diversity and productivity experiments in European grasslands. Science 286: 1123-1127</ref>, Schmid et al. 2001<ref>Schmid, B., Joshi, J. and Schlaepfer, F. 2001. Empirical evidence for biodiversity-ecosystem function relationships. In: Kinzig, A. P., Pacala, S. W. and Tilman, D. (eds), The functional consequences of biodiversity. Princeton Univ. Press, pp. 120-150.</ref>; Giller et al., 2004<ref name=Gil>Giller, P. S., Hillebrand, H., Berninger, U. G., Gessner, M. O., Hawkins, S. J., Inchausti, P., Inglis, C., Leslie, H. A., Malmqvist, B., Monaghan, M. T., Morin, P. J. and O'Mullan, G. 2004. Biodiversity effects on ecosystem functioning: emerging issues and their experimental test in aquatic environments. Oikos 104: 423-436</ref>). These studies have shown that changing biodiversity in natural ecosystems is likely to have far more complicated impacts on ecosystem function than predicted from changes in plant diversity alone (Duffy, 2003<ref name=Duf/>). For example in trophic levels of plant communities, as diversity is lost from a system, impacts will also depend from the loss of predators which will evoke change in the structure of all trophic levels (Hairston et al. 1960<ref>Hairston, N. G., Smith, F. E. and Slobodkin, L. G. 1960. Community structure, population control, and competition. Am. Nat. 94: 421–425</ref>; Power 1990<ref>Power, M. E. 1990. Effects of fish in river food webs. Science 250: 411–415</ref>; Estes et al. 1998<ref>Estes, J. A., Tinker, M. T., Williams, T. M. and Doak, D. F. 1998. Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282:473–476</ref>; Duffy, 2003<ref name=Duf/>).  
  
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[[Image:Figure 2c.jpg|thumb|right|450px|Figure 2c: Experimental design commonly adopted in biodiversity-ecosystem function experiments. Red boxes indicate treatments with one species (Single species), two species and three species (Species mixtures). Total biomass between treatments is kept constant.]]
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The mosaic of habitat patches in aquatic systems often is more spatially compact than in terrestrial environments, presenting more tractable experimental systems at the landscape scale (Schindler and Scheuerell 2002<ref>Schindler, D. E. and Scheuerell, M. D. 2002. Habitat coupling in lake ecosystems. Oikos 98: 177-189</ref>). Because each aquatic ecosystem is composed of multiple habitat types, assessing the effects of biodiversity changes on the function of aquatic ecosystems requires experimental designs that allow a scaling up from individual homogenous patches to large scale, often highly heterogeneous areas (Giller et al. 2004<ref Name=Gil/>).
  
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Despite debates over experimental designs and applicability, syntheses of the available evidence suggest that, irrespective of the system studied, increased biodiversity tends to have a positive effect on ecosystem properties, such as primary productivity, nutrient flux and decomposition, but the pattern of response varies depending on the ecosystem and species investigated [15, 16]. This variability between results suggests that ecosystems respond differently to biodiversity loss, as natural ecosystems are complex, open systems that are composed of interconnected gradients, patches and networks between, and within which, organisms move and interact [17]. The high degree of control required in experiments and the short time periods under which they are conducted means, however, that the environmental variation and biological interactions that occur in natural systems are largely controlled for. The inherent complexity of environmental systems resulted in increasing calls to incorporate more environmental realism into experimental designs [13, 18] as it is still unclear whether the currently observed patterns in the biodiversity-ecosystem function relationship will hold, for example, for realistic extinction scenarios, in multi-trophic communities, and over larger spatial and temporal scales (14, 19).
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The most influential empirical research on biodiversity-ecosystem function linkages has been the series of experiments manipulating diversity in grasslands (reviewed by Tilman et al. 2002<ref>Tilman, D., Knops, J., Wedin, D. and Reich P. 2002. Experimental and observational studies of diversity, productivity, and stability. Pages 42–70 in A. Kinzig, S. Pacala, and D. Tilman, editors. Functional consequences of biodiversity: Ecological Monographs Vol. 75, No. 1 Empirical progress and theoretical extensions. Princeton University Press, Princeton, New Jersey, USA.</ref>) and in aquatic microbial microcosms (reviewed by Petchey et al. 2002<ref name=PG>Petchey, O. L. and Gaston, K. J. 2002. Functional diversity (FD), species richness and community composition. Ecol. Lett. 5: 402-411</ref>). Typically these have tested how ecosystem-wide biomass accumulation or metabolic rates change along gradients of species richness achieved by randomly assembling experimental communities from a pool of species. The grassland experiments have manipulated plant species richness, and sometimes also functional group richness. These studies have demonstrated significant positive correlations between species richness and plant biomass. Loreau et al. (2002<ref name=Lo2/>) provide a global overview of concepts and debates concerning the relationships between biodiversity and ecosystem function (Humbert and Dorigo, 2005<ref name=HD/>).
  
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== Phase 2 – Inclusion of a subset of environmental variation ==
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It has been clearly established that ecosystem function depends both on biotic factors and/or processes (such as the diversity and functions of the species, and interactions between species) and abiotic factors (such as climate or geology). However, what relative contribution these factors make is still a central question in the debate about diversity and ecosystem function (Huston and McBride, 2002<ref>Huston, M. A., and McBride, A. C.. 2002. Evaluating the relative strengths of biotic versus abiotic controls on ecosystem processes. Pages 47–60 in M. Loreau, S. Naeem, and P. Inchausti, editors. Biodiversity and ecosystem functioning: synthesis and perspectives. Oxford University Press, Oxford, UK.</ref>; Humbert and Dorigo, 2005<ref name=HD/>).
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[[Image: BEF_Seagrass.jpg|thumb|left|250px| Figure 3: Outdoor mesocosms used in experiments investigating the effects of gazer diversity on ecosystem fucntioning in seagrass beds, [20].]]
 
  
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Diversity manipulations in outdoor mesocosms [Figure 3, 20] are subjected to natural fluctuations in light, temperature and rainfall and thus represent better analogues of natural systems than more controlled laboratory conditions.  
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Species deletion stability can also be linked easily to removal experiments that address the consequences of species loss for ecosystem function (Thebault, et al. 2007<ref>Thebault, E., Huber, V., Loreau, M. 2007  Cascading extinctions and ecosystem functioning: contrasting effects of diversity depending on food web structure. Oikos 116: 163-173</ref>). With a few exceptions, theoretical work on the direct impact of species loss has focused on the study of secondary extinctions but has not considered associated changes in ecosystem properties (see King and Pimm 1983<ref>King, A.W. and Pimm, S.L. 1983. Complexity, diversity and stability: a reconciliation of theoretical and empirical results. The American Naturalist 122: 229–239</ref>, Petchey et al. 2004<ref>Petchey, O. L, Downing, A. L., Mittelbach, G. G. et al. 2004. Species loss and the structure and functioning of multitrophic aquatic systems. Oikos 104: 467-478</ref>).  
  
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In-situ experiments or species addition/removal field experiments have been particularly valuable for determining biodiversity effects under naturally fluctuating environmental conditions (Figure 1)[21-23]. These experiments largely involve synthetically assembled communities in plots, mesocosms (Figure 4) or mesh-bags, in which biodiversity is controlled, but natural fluctuations in, for example, tidal cycles, rainfall or temperature, occur (Figure 4c). Although such studies incorporate more environmental variation, the spatial and temporal scales of the experimental designs largely do not relate to the dynamics of the study organisms, particularly in terms of their size or generation time. One way to incorporate such population dynamics at small and large scales is to adapt elements of meta-population theory [24]. In such studies, the importance of dispersal, the mechanism that regulates and maintains species coexistence (especially in fragmented habitats), in mediating the biodiversity-ecosystem function relationship, is recognised. At the same time, theoretical models have been extended to include environmental fluctuations [25].
 
  
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[[Image: Figure 4a.jpg|thumb|left|150px|Figure 4a: Mesocosm design to hold invertebrate communities and algal resources. Blue grids represent fine mesh, allowing tidally associated environmental fluctutations in the mesocosms, [23]]]
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Many of the studies that dealt specifically with the mechanisms involved in the relationships between biodiversity and ecosystem function investigated the niche complementarity mechanism, stimulating both theoretical and experimental approaches (e.g., Naeem et al., 1994<ref name=Na94/>; Loreau, 1998<ref>Loreau, M. 1998. Biodiversity and ecosystem functioning: a mechanistic model. Proceedings of the National Academy of Sciences (USA) 95: 5632–5636</ref>). The sampling effect, difficult to distinguish from the niche complementarity, is defined as the greater likelihood of finding species with a strong impact on ecosystem function in highly diversified communities (e.g., Huston, 1997<ref>Huston, M. A. 1997. Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110: 449-460</ref>; Hector et al., 1999<ref name=Hec99/>; Wardle, 1999<ref>Wardle, D. A. 1999. Is ‘‘sampling effect’’ a problem for experiments investigating biodiversity–ecosystem function relationships? Oikos 87: 403–407</ref>). These are not either-or mechanisms, but may be viewed as concomitant processes (Naeem, 2002<ref name=Na2>Naeem, S. 2002. Disentangling the impacts of diversity on ecosystem functioning in combinatorial experiments. Ecology 83: 2925–2935</ref>). Sampling effects are involved in community assembly, and thus in determining the number of phenotypic traits present in the community. Subsequently, this phenotypic diversity influences ecosystem processes through mechanisms that can be viewed as a continuum ranging from the selection of species with particular traits to complementarity among species with different traits (Loreau et al., 2001<ref>Loreau, M., Naeem, S., Inchausti, P. et al. 2001. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294: 804-808</ref>).
  
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[[Image: Figure 4c.jpg|thumb|right|350px|Figure 4b: Mesocosms containing invertebrate communities and algal resources pushed 10 cm into the mud, [23].]]
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Mathematical modelling has also been used recently, to investigate the relationships between biodiversity and ecosystem stability. For example, McCann et al. (1998<ref>McCann, K., Hastings, A. and Huxel, G.R. 1998. Weak trophic interactions and the balance of nature. Nature 395: 794–798. https://doi.org/10.1038/27427</ref>) have shown that weak to intermediate interaction strengths within food webs are important in promoting community persistence and stability (Humbert and Dorigo, 2005<ref name=HD/>).  
  
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Most biodiversity-ecosystem function studies, use only a subset of the natural community to construct gradients of diversity, often selectively choosing those species that are either highly abundant or that may give the greatest response [18]. A move away from random extinction scenarios has relied primarily on modelling approaches to predict the consequences of diversity loss [26, 27]. The derived scenarios use extinction drivers that are explicitly associated with trait-based extinction probabilities and thereby provide a more direct way of assessing the possibilities of ecosystem responses to biodiversity loss. Such modelling approaches have the potential for exploring the consequences of biodiversity loss at greater spatial and temporal scales by making use of large data sets which are already available for many marine and terrestrial areas [19].
 
  
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== Theories and Hypothesis ==
  
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== Phase 3 – Incorporating environmental variation ==
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In a review of the topic, Naeem et al. (2002<ref name=Na2/>) proposed three hypotheses to account for linking biodiversity and ecosystem function:
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Despite the fact that there has been a steady increase in complexity of experimental and theoretical investigations of the biodiversity-ecosystem function relationship, it is still not clear whether the same patterns observed in experimental systems are just as strong and clear in natural systems. Studies based on field observations (Figure 4), have given some insight into the biodiversity-ecosystem function relationship in natural systems [28-30], however such studies are generally correlative in nature, lack direct experimental control and do not allow for replication. In addition, the inability to control confounding factors restricts the determination of cause-effect relationships between biodiversity loss and ecosystem function [28-30]. Despite efforts to overcome such problems (e.g. selecting sites of similar abiotic conditions, 28; or collecting data on additional environmental variables, 29), results are still open to alternative interpretations and have subsequently not shown any consistent results.
 
  
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[[Image:SPI images.jpg|thumb|centre|500px|Figure 4: Sediment profile images used to investigate the effects of biodiversity loss on sediment mixing in natural systems [7].]]
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*The first hypothesis is that species are primarily redundant, which means that one species can partially replace another. Many species have the same function, and the loss of one species can therefore be offset by some other species.
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*The second hypothesis is that species are essentially singular, and make unique contributions to the ecosystem function. The loss or gain of species (generally referred to as Keystone or Key species) therefore has a measurable impact on the ecosystem function.
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*The third hypothesis is that species impacts are context dependent such that the impact of the loss or gain of a species on ecosystem function is idiosyncratic and unpredictable.
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What happens, will depend on the local conditions under which the species extinction or addition occurs (Humbert and Dorigo, 2005<ref name=HD/>)
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For further details on this topic, see the article [[Disturbances, biodiversity changes and ecosystem stability]].
  
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This third phase (Figure 1) is currently in its infancy, however it heralds a point in biodiversity-ecosystem function research history where the discipline has matured and a full suite of evidence (i.e. theory, methodology, laboratory and field experiments, or field observations) exists, providing insight into the likely ecosystem consequences of biodiversity loss. The biodiversity-ecosystem function relationship has been found to vary depending on the relative contribution of dominant and minor species [9], environmental context [31, 32], density dependence and species interactions [21, 23, 33], but few studies have explicitly incorporated those structuring abiotic (environmental heterogeneity) and biotic (movement, dispersal) features that are key to species co-existence and vital for the maintenance of species diversity [34]. In addition, biodiversity effects on ecosystem properties are significantly weaker under less-well controlled conditions [15], suggesting that the effect of biodiversity on ecosystem properties may be masked by abiotic factors in natural systems [35]. At present there is insufficient empirical evidence to determine the modifying effects of environmental factors, such as nutrient concentration, heterogeneity or elevated CO<sub>2</sub> on biodiversity and community dynamics and, subsequently, ecosystem properties [15]. Even fewer attempts have been made, however, to establish and distinguish the relative importance of biodiversity and environmental factors in modifying ecosystem properties. Thus, a main challenge for the biodiversity-ecosystem function community is to demonstrate whether the observed importance of biodiversity in controlled experimental systems also persists in natural systems.
 
  
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== See also ==
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== How do we measure Ecosystem Function? ==
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Further detailed reviews on the relationship between biodiversity and ecosystem function include:
 
  
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Balvanera, P., Pfisterer, A.B., Buchmann, N., He, J.S., Nakashizuka, T., Raffaelli, D. & Schmid, B. (2006). Quantifying the evidence for biodiversity effects on ecosystem functioning and services. ''Ecology Letters'' 9: 1146-1156.
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Describing or measuring ecosystem function is difficult, as it encompasses a number of phenomena (Hooper et al., 2005<ref>Hooper, D.U., Chapin, F.S., III, Ewel, J.J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J.H., Lodge, D.M., Loreau, M., Naeem, S., et al. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 75: 3–35 </ref>). The overall function of an ecosystem is complex and involves many factors relating to the chemical, physical and biological components of the system. The way in which differences between species affect diversity-function relationships can be very complex (Lawton et al., 1998<ref>Lawton, J. H., Naeem, S., Thompson, L. J., Hector, A. and Crawley, M. J. 1998;  Biodiversity and Ecosystem Function: Getting the Ecotron Experiment in its Correct Context Functional Ecology 12: 848-852</ref>; Ricotta, 2005<ref name=Ric5>Ricotta, C. 2005. Through the jungle of biological diversity. Acta Biotheoretica 53: 29–38</ref>).  
  
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Cardinale, B.J., Srivastava, D.S., Duffy, J.E., Wright, J.P., Downing, A.L., Sankaran, M., & Jouseau, C. (2006). Effects of biodiversity on the functioning of trophic groups and ecosystems. ''Nature'' 443: 989-992.
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[[Functional diversity]] (FD), i.e. the diversity and range of functional traits possessed by the biota of an ecosystem (Wright et al., 2006<ref>Wright, J. P., Naeem, S., Hector, A., Lehman, C., Reich, P. B., Schmid, B. and Tilman, D. 2006. Conventional functional classification schemes underestimate the relationship with ecosystem functioning. Ecology Letters, 9: 111 –120</ref>) or else defined by Tilman (2001<ref>Tilman, D. 2001. Effects of diversity and composition on grassland stability and productivity. Pages 183–207 in M.C. Press, N. J. Huntley, and S. Levin, editors. Ecology: achievement and challenge. Blackwell Science, Oxford, UK</ref>) as "those components of biodiversity that influence how an ecosystem operates or functions" (Ricotta, 2005<ref name=Ric5/>), is likely to be the component of biodiversity most relevant to the function of the ecosystems (Hooper et al., 2002<ref>Hooper, D. U., Solan, M., Symstad, A., Diaz, S., Gessner, M. A., Buchmann, N., Degrange, V., et al. 2002. Species diversity, functional diversity, and ecosystem functioning. In Biodiversity and Ecosystem Functioning: Synthesis and Perspectives, pp. 195 –208. Ed. by M. Loreau, S. Naeem, and P. Inchausti. Oxford University Press, Oxford.</ref>; 2005<ref>Hooper, D. U., Chapin, F. S., Ewel, J. J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J. H., et al. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs, 75: 3 –35</ref>; Heemsbergen et al., 2004<ref>Heemsbergen, D. A., Berg, M. P., Loreau, M., van Hal, J. R., Faber, J.H., and Verhoef, H. A. 2004. Biodiversity effects on soil processes explained by interspecific functional dissimilarity. Science, 306: 1019–1020</ref>), even though, there is no clear relationship demonstrated between species diversity and ecosystem function (Somerfield et al., 2008<ref name=So8> Somerfield, P. J., Clarke, K. R., Warwick, R. M., and Dulvy, N. K. 2008. Average functional distinctness as a measure of the composition of assemblages. – ICES Journal of Marine Science, 65: 1462–1468</ref>).
  
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Covich, A.P., Austen, M.C., Barlöcher, F., Chauvet, E., Cardinale, B.J., Biles, C.L., Inchausti, P., Dangles, O., Solan, M., Gessner, M.O., Statzner, B. & Moss, B. (2004). The role of Biodiversity in the functioning of freshwater and marine benthic ecosystems. ''BioScience'' 54: 767-775.  
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Whereas traditional diversity indices focus on species richness, rarity (Schmera 2003<ref>Schmera, D. 2003. Assessing stream dwelling caddis fly assemblages (Insecta: Trichoptera) collected by light traps in Hungary. Biodivers Conserv 12: 1175–119</ref>) or the uncertainty of predicting species identity from abundance data (Magurran 1988<ref>Magurran, A. (1988) Ecological Diversity and its Measurement. Princeton University Press, Princeton, NJ.</ref>), functional diversity formulae are used to measure ‘‘those components of biodiversity that influence how an ecosystem operates or functions’’ (Tilman et al. 1997<ref name=Til97/>; Schmera, Erös  and Podani, 2009<ref>Schmera, D., Eros, T. and Podani, J. 2009. A measure for assessing functional diversity in ecological communities. Aquatic Ecology, 2009 – Springer</ref>). Functional Diversity relates the number, type and distribution of functions performed by organisms within an ecosystem (Diaz & Cabido, 2001<ref>Diaz, S. and Cabido, M. 2001. Vive la difference: plant functional diversity matters to ecosystem processes. Trends in Ecology and Evolution 16: 646-655</ref>). It incorporates interactions between organisms and their environment into a concept that can portray ecosystem level structure in marine environments (Bremner et al., 2003<ref>Bremner J. Rogers, S. I and Frid, C. L. J. 2003. Assessing functional diversity in marine benthic ecosystems: a comparison of approaches. Mar. Ecol. Prog. Ser. 254: 11–25</ref>) and conjectures to be useful in predicting the consequences of changes in species richness and composition, or biodiversity in general, on ecosystem properties (Somerfield et al., 2008<ref name=So8).
  
−
Hooper, D.U., Chapin, F.S. III, Ewel, J.J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J.H., Lodge, D.M., Loreau, M., Naeem, S., Schmid, B., Setala, H., Symstad, A.J., Vandermeer, J. & Wardle, D.A. (2005). Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. ''Ecological Monographs'' 75: 3 - 35.
+
Biodiversity can influence ecosystem function through changes in the amount of resource use complementary among species. [[Functional diversity]] is a measure of biodiversity that aims to quantify resource use complementarity and thereby explain and predict ecosystem function (Petchey, Hector and Gaston, 2004<ref>Petchey, O.L., Hector, A. and Gaston, K.J. 2004. How do different measures of functional diversity perform? Ecology 85: 847– 857</ref>). Many studies have focused on calculating Functional Diversity, in order to measure the Ecosystem Function. Methods and indices have been applied and tested on a long series of data concerning abiotic and biotic measures of fresh and sea water.  
  
−
Hughes, J.B. & Petchey, O.L. (2001). Merging perspectives on biodiversity and ecosystem functioning. ''Trends in Ecology and Evolution'' 16: 222-223.
+
Recent methods for calculating [[functional diversity]] of a community, include Functional Attribute Diversity (FAD), as used in a study of Australian rangelands by Walker et al. (1999<ref>Walker, B., Kinzig, A. and Langridge, J. 1999. Plant attribute diversity, resilience, and ecosystem function: the nature and significance of dominant and minor species. Ecosystems 2: 95– 113</ref>), and Functional Diversity (FD) proposed more recently by Petchey and Gaston (2002<ref name=PG/>) which is computed as the total branch length of the functional dendrogram that results from clustering the species in trait space (Ricotta, 2005<ref name=Ric5/>). Trait variance, measured as the width of a trait distribution, has been proposed by Norberg (2004<ref>Norberg, J. 2004. Biodiversity and ecosystem functioning: A complex adaptive systems approach. Limnology and Oceanography 49: 1269-1277</ref>). Beyond the simple measurement of diversity, Mason et al. (2005<ref>Mason, N. W. H., Mouillot, D., Lee, W. G. and Wilson, J. B. 2005. 2005. Functional richness, functional evenness and functional divergence: the primary components of functional diversity. Oikos 111: 112–118</ref>) proposed also estimating functional richness, functional evenness and functional divergence, to enable descriptions of niche use and competitive interactions in communities. In order to take a functional approach and to use these new measures, however, we must have descriptors of the functional groups present in a community.
  
−
Loreau, M, Naeem, S., Inchausti, P., Bengtsson, J, Grime, J.P., Hector, A., Hooper, D.U., Huston, M.A., Raffaelli, D., Schmid, B., Tilman, D. & Wardle, D.A. (2001). Biodiversity and ecosystem functioning: Current knowledge and future challenges. ''Science'' 294: 804-808.
+
Most recently, based on the methodology proposed by the formers, Somerfield et al. (2008<ref name=So8/>) defined average functional distinctness (X+, from χαρακτηριστικό, meaning a trait) simply as the average resemblance among species in a sample.  
 +
Incidentally, the same logic may be applied to Δ+ (Clarke and Warwick, 1998<ref>Clarke, K. R., and Warwick, R. M. 1998. A taxonomic distinctness index and its statistical properties. Journal of Applied Ecology, 35: 523–531</ref>). Once branch lengths are defined between taxonomic levels, a matrix of resemblances (Euclidean distances) between species becomes implicit, and the index is the average resemblance between species. In the same study, the authors concluded that the type of information we get from the functional level is complementary to the information we take from the taxonomic level.  
  
−
Solan, M., Godbold, J.A., Symstad, A., Flynn, D.F.B. & Bunker, D. (2009). Biodiversity-ecosystem function research and biodiversity futures: early bird catches the worm or a day late and a dollar short? In: Biodiversity and human impacts. Ecological and societal implications. Naeem, S., Bunker, D.E., Hector, A., Loreau, M. & Perrings, C. (Eds.). Oxford University Press.
 
  
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Stachowicz, J.J., Bruno, J.F. & Duffy, J.E. (2007). Understanding the effects of marine biodiversity on communities and ecosystems. ''Annual Review of Ecology, Evolution and Systematics'' 38: 739-766.
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== How do we calculate Ecosystem Function in practice? ==
  
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The influence of the lugworm (''Arenicola marina'') on biodiversity and ecosystem functioning in an intertidal mudflat [http://www.marbef.org/outreach/newsletter.php]<p>
+
The categorization of species into [[functional groups]] can be done by simply assigning each species found in the assemblage to a given a priori defined functional group (Hector et al., 1999<ref name=Hec99/>), or by standard multivariate clustering methods (Gitay & Noble, 1997<ref>Gitay, H. and Noble, I.R. 1997. What are functional types and how should we seek them? In: Smith, T.M., Shugart, H.H. and Woodward, F.I. (eds.). Plant Functional Types. Their Relavance to Ecosystem Properties and Global Change, pp. 3–19. Cambridge University Press, Cambridge.</ref>; Deckers, Verheyen, Hermy, & Muys, 2004<ref>Deckers, B., Verheyen, K., Hermy, M. and Muys, B. 2004. Differential environmental response of plant functional types in hedgerow habitats. Basic and Applied Ecology 5: 551-566</ref>; Roscher et al., 2004<ref>Roscher, C., Schumacher, J. and Baade, J. 2004. The role of biodiversity for element cycling and trophic interactions: an experimental approach in a grassland community. Basic Appl. Ecol. 121: 107–121</ref>) - see also [[Biological Trait Analysis]] (BTA).
 +
To cluster species into functional groups, first, a set of [[functional traits]] thought to be of significance for ecosystem function is measured for each species obtaining an <math>S \times \tau</math> matrix of <math>\tau</math> functional traits measured on <math>S</math> species (Petchey & Gaston, 2002<ref name=PG/>). Next, the trait matrix is converted into a distance matrix <math>\Delta</math> of which the elements <math>\Delta_{i,j}</math> embody the functional distances between the <math>i</math>-th and the <math>j</math>-th species such that <math>\Delta_{i,i}=0</math> and <math>\Delta_{i,j}=\Delta_{j,i}</math> for any <math>i \neq j</math>. Finally, the distance matrix is clustered with standard multivariate methods to separate species from different functional groups (Ricotta, 2005<ref name=Ric5/>).  
 +
Generally, regardless of the proposed index, in most cases the information available for computing the FD of a given species assemblage is the set of pair wise species functional distances <math>\Delta_{i,j}</math> (Ricotta, 2005<ref name=Ric5/>). For further details and explanations, see the article [[Measurements of biodiversity]].
  
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==References==
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==Related articles==
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:[[Ecosystem function]]
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:[[Measurements of biodiversity]]
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:[[Biological Trait Analysis]]
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:[[Biodiversity]]
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Latest revision as of 15:25, 1 November 2020


Introduction

The recognition that species interactions may play important roles in ecosystems and the rapidly emerging interest in the biodiversity conservation have prompted ecologists to ask new questions on the relationships between 'biodiversity' and 'ecosystem function' (for example, Walker, 1992[1]; Schultze and Mooney, 1993[2]; Jones and Lawton, 1995[3]; Johnson et al., 1996[4]).


Importance of ecosystem function

One reason for the interest in the functional role of biodiversity (rather than structural) in ecosystems is that society might be more likely to take action to preserve biodiversity if it could be shown that there was some direct economic gain by doing it (Bengtsson, 1998[5]). Over the last fifteen years, an increasing number of studies have focused on biodiversity. This is principally because the world’s flora and fauna are disappearing at rates greater than during historical mass extinction events (Chapin et al, 2001[6]). As suggested by Thomas et al. (2004[7]), there is an 18 to 35% risk of species-level extinction resulting from climate changes by the year 2050. Moreover, other processes, for example, agricultural expansion in response to an increasing demand for food, have a negative impact on biodiversity as a result of habitat destruction (Tilman et al., 2001[8]; Humbert and Dorigo, 2005[9]).

Biodiversity and Ecosystem function are central to both community and ecosystems ecology and need to be understood to predict, for example, how communities and ecosystems respond to environmental change (Bengtsson, 1998[5]) and on understanding how declining diversity influences ecosystem services on which humans depend (Duffy, 2003[10]).


Research on Ecosystem Function

Research on Biodiversity - Ecosystem Function (the BEF agenda) has stimulated a new and highly productive intercourse between population, community, ecosystem, and conservation ecology (Kinzig et al. 2002[11]; Loreau et al. 2002[12]; Duffy, 2003[10]). Most experimental evidence for biodiversity effects on ecosystem function has come from terrestrial ecosystems, particularly grasslands (Naeem et al. 1994[13], Tilmann et al. 1997[14], Hector et al. 1999[15], Schmid et al. 2001[16]; Giller et al., 2004[17]). These studies have shown that changing biodiversity in natural ecosystems is likely to have far more complicated impacts on ecosystem function than predicted from changes in plant diversity alone (Duffy, 2003[10]). For example in trophic levels of plant communities, as diversity is lost from a system, impacts will also depend from the loss of predators which will evoke change in the structure of all trophic levels (Hairston et al. 1960[18]; Power 1990[19]; Estes et al. 1998[20]; Duffy, 2003[10]).

The mosaic of habitat patches in aquatic systems often is more spatially compact than in terrestrial environments, presenting more tractable experimental systems at the landscape scale (Schindler and Scheuerell 2002[21]). Because each aquatic ecosystem is composed of multiple habitat types, assessing the effects of biodiversity changes on the function of aquatic ecosystems requires experimental designs that allow a scaling up from individual homogenous patches to large scale, often highly heterogeneous areas (Giller et al. 2004[17]).

The most influential empirical research on biodiversity-ecosystem function linkages has been the series of experiments manipulating diversity in grasslands (reviewed by Tilman et al. 2002[22]) and in aquatic microbial microcosms (reviewed by Petchey et al. 2002[23]). Typically these have tested how ecosystem-wide biomass accumulation or metabolic rates change along gradients of species richness achieved by randomly assembling experimental communities from a pool of species. The grassland experiments have manipulated plant species richness, and sometimes also functional group richness. These studies have demonstrated significant positive correlations between species richness and plant biomass. Loreau et al. (2002[12]) provide a global overview of concepts and debates concerning the relationships between biodiversity and ecosystem function (Humbert and Dorigo, 2005[9]).

It has been clearly established that ecosystem function depends both on biotic factors and/or processes (such as the diversity and functions of the species, and interactions between species) and abiotic factors (such as climate or geology). However, what relative contribution these factors make is still a central question in the debate about diversity and ecosystem function (Huston and McBride, 2002[24]; Humbert and Dorigo, 2005[9]).

Species deletion stability can also be linked easily to removal experiments that address the consequences of species loss for ecosystem function (Thebault, et al. 2007[25]). With a few exceptions, theoretical work on the direct impact of species loss has focused on the study of secondary extinctions but has not considered associated changes in ecosystem properties (see King and Pimm 1983[26], Petchey et al. 2004[27]).


Many of the studies that dealt specifically with the mechanisms involved in the relationships between biodiversity and ecosystem function investigated the niche complementarity mechanism, stimulating both theoretical and experimental approaches (e.g., Naeem et al., 1994[13]; Loreau, 1998[28]). The sampling effect, difficult to distinguish from the niche complementarity, is defined as the greater likelihood of finding species with a strong impact on ecosystem function in highly diversified communities (e.g., Huston, 1997[29]; Hector et al., 1999[15]; Wardle, 1999[30]). These are not either-or mechanisms, but may be viewed as concomitant processes (Naeem, 2002[31]). Sampling effects are involved in community assembly, and thus in determining the number of phenotypic traits present in the community. Subsequently, this phenotypic diversity influences ecosystem processes through mechanisms that can be viewed as a continuum ranging from the selection of species with particular traits to complementarity among species with different traits (Loreau et al., 2001[32]).

Mathematical modelling has also been used recently, to investigate the relationships between biodiversity and ecosystem stability. For example, McCann et al. (1998[33]) have shown that weak to intermediate interaction strengths within food webs are important in promoting community persistence and stability (Humbert and Dorigo, 2005[9]).


Theories and Hypothesis

In a review of the topic, Naeem et al. (2002[31]) proposed three hypotheses to account for linking biodiversity and ecosystem function:

  • The first hypothesis is that species are primarily redundant, which means that one species can partially replace another. Many species have the same function, and the loss of one species can therefore be offset by some other species.
  • The second hypothesis is that species are essentially singular, and make unique contributions to the ecosystem function. The loss or gain of species (generally referred to as Keystone or Key species) therefore has a measurable impact on the ecosystem function.
  • The third hypothesis is that species impacts are context dependent such that the impact of the loss or gain of a species on ecosystem function is idiosyncratic and unpredictable.

What happens, will depend on the local conditions under which the species extinction or addition occurs (Humbert and Dorigo, 2005[9]) For further details on this topic, see the article Disturbances, biodiversity changes and ecosystem stability.


How do we measure Ecosystem Function?

Describing or measuring ecosystem function is difficult, as it encompasses a number of phenomena (Hooper et al., 2005[34]). The overall function of an ecosystem is complex and involves many factors relating to the chemical, physical and biological components of the system. The way in which differences between species affect diversity-function relationships can be very complex (Lawton et al., 1998[35]; Ricotta, 2005[36]).

Functional diversity (FD), i.e. the diversity and range of functional traits possessed by the biota of an ecosystem (Wright et al., 2006[37]) or else defined by Tilman (2001[38]) as "those components of biodiversity that influence how an ecosystem operates or functions" (Ricotta, 2005[36]), is likely to be the component of biodiversity most relevant to the function of the ecosystems (Hooper et al., 2002[39]; 2005[40]; Heemsbergen et al., 2004[41]), even though, there is no clear relationship demonstrated between species diversity and ecosystem function (Somerfield et al., 2008[42]).

Whereas traditional diversity indices focus on species richness, rarity (Schmera 2003[43]) or the uncertainty of predicting species identity from abundance data (Magurran 1988[44]), functional diversity formulae are used to measure ‘‘those components of biodiversity that influence how an ecosystem operates or functions’’ (Tilman et al. 1997[14]; Schmera, Erös and Podani, 2009[45]). Functional Diversity relates the number, type and distribution of functions performed by organisms within an ecosystem (Diaz & Cabido, 2001[46]). It incorporates interactions between organisms and their environment into a concept that can portray ecosystem level structure in marine environments (Bremner et al., 2003[47]) and conjectures to be useful in predicting the consequences of changes in species richness and composition, or biodiversity in general, on ecosystem properties (Somerfield et al., 2008[48]). Many studies have focused on calculating Functional Diversity, in order to measure the Ecosystem Function. Methods and indices have been applied and tested on a long series of data concerning abiotic and biotic measures of fresh and sea water.

Recent methods for calculating functional diversity of a community, include Functional Attribute Diversity (FAD), as used in a study of Australian rangelands by Walker et al. (1999[49]), and Functional Diversity (FD) proposed more recently by Petchey and Gaston (2002[23]) which is computed as the total branch length of the functional dendrogram that results from clustering the species in trait space (Ricotta, 2005[36]). Trait variance, measured as the width of a trait distribution, has been proposed by Norberg (2004[50]). Beyond the simple measurement of diversity, Mason et al. (2005[51]) proposed also estimating functional richness, functional evenness and functional divergence, to enable descriptions of niche use and competitive interactions in communities. In order to take a functional approach and to use these new measures, however, we must have descriptors of the functional groups present in a community.

Most recently, based on the methodology proposed by the formers, Somerfield et al. (2008[42]) defined average functional distinctness (X+, from χαρακτηριστικό, meaning a trait) simply as the average resemblance among species in a sample. Incidentally, the same logic may be applied to Δ+ (Clarke and Warwick, 1998[52]). Once branch lengths are defined between taxonomic levels, a matrix of resemblances (Euclidean distances) between species becomes implicit, and the index is the average resemblance between species. In the same study, the authors concluded that the type of information we get from the functional level is complementary to the information we take from the taxonomic level.


How do we calculate Ecosystem Function in practice?

The categorization of species into functional groups can be done by simply assigning each species found in the assemblage to a given a priori defined functional group (Hector et al., 1999[15]), or by standard multivariate clustering methods (Gitay & Noble, 1997[53]; Deckers, Verheyen, Hermy, & Muys, 2004[54]; Roscher et al., 2004[55]) - see also Biological Trait Analysis (BTA). To cluster species into functional groups, first, a set of functional traits thought to be of significance for ecosystem function is measured for each species obtaining an [math]S \times \tau[/math] matrix of [math]\tau[/math] functional traits measured on [math]S[/math] species (Petchey & Gaston, 2002[23]). Next, the trait matrix is converted into a distance matrix [math]\Delta[/math] of which the elements [math]\Delta_{i,j}[/math] embody the functional distances between the [math]i[/math]-th and the [math]j[/math]-th species such that [math]\Delta_{i,i}=0[/math] and [math]\Delta_{i,j}=\Delta_{j,i}[/math] for any [math]i \neq j[/math]. Finally, the distance matrix is clustered with standard multivariate methods to separate species from different functional groups (Ricotta, 2005[36]). Generally, regardless of the proposed index, in most cases the information available for computing the FD of a given species assemblage is the set of pair wise species functional distances [math]\Delta_{i,j}[/math] (Ricotta, 2005[36]). For further details and explanations, see the article Measurements of biodiversity.


Related articles

Ecosystem function
Measurements of biodiversity
Biological Trait Analysis
Biodiversity


References

  1. ↑ Walker, B.H., 1992. Biodiversity and ecological redundancy. Conserv. Biol. 6: 18-23.
  2. ↑ Schulze, E.-D. and Mooney, H. A. (eds). 1993. Biodiversity and ecosystem function. Springer Verlag.
  3. ↑ Jones, C. G., and Lawton, J. H. editors. 1995. Linking species and ecosystems. Chapman and Hall, New York, New York, USA.
  4. ↑ Johnson, K.H., Vogt, K.A., Clark, H., Schmitz, O. and Vogt, D. 1996. Biodiversity and the productivity and stability of ecosystems. Trends in Ecology & Evolution 11: 372-377
  5. ↑ 5.0 5.1 Bengtsson, J. 1998. Which species? What kind of diversity? Which ecosystem function? Some problems in studies of relations between biodiversity and ecosystem function. Applied Soil Ecology 10: 191-199
  6. ↑ Chapin, F. S., III, Sala, O. E. and Huber-Sannwald, E. editors. 2001. Global biodiversity in a changing environment: scenarios for the 21st century. Springer-Verlag, New York, New York, USA.
  7. ↑ Thomas, C.D., Cameron, A., Green, R.E., Bakkenes, M., Beaumont, L.J., Collingham, Y.C., Erasmus, B.F.N., de Siqueira, M.F., Grainger, A., Hannah, L., Hughes, L., Huntley, B., van Jaarsveld, A.S., Midgley, G.F., Miles, L., Ortega-Huerta, M.A., Townsend, P.A., Phillips, O.L. and Williams, S.E. 2004. Extinction risk from climate change. Nature 427: 145–148
  8. ↑ Tilman, D., Reich, P. B., Knops, J., Wedin, D., Mielke, T. and Lehman C. 2001. Diversity and productivity in a longterm grassland experiment. Science 294: 843–845
  9. ↑ 9.0 9.1 9.2 9.3 9.4 Humbert, J.F. and Dorigo, U. 2005 Biodiversity and aquatic ecosystem functioning: A mini-review. Ecosystem Health and Management 8: 367-374
  10. ↑ 10.0 10.1 10.2 10.3 Duffy, J.E. 2003. Biodiversity loss, trophic skew and ecosystem functioning. Ecol. Lett. 6: 680–687
  11. ↑ Kinzig, A. P., Pacala, S. W. and Tilman, D. (eds). 2002. The functional consequences of biodiversity. Princeton Univ. Press.
  12. ↑ 12.0 12.1 Loreau, M., Naeem, S. and Inchausti, P. 2002. Biodiversity and Ecosystem Function – Synthesis and Perspectives. Oxford University Press
  13. ↑ 13.0 13.1 Naeem, S., Thompson, L. J., Lawler, S. P. et al. 1994. Declining biodiversity can alter the performance of ecosystems. Nature 368: 734-737
  14. ↑ 14.0 14.1 Tilman, D., Knops, J. M. H., Wedin, D. et al. 1997. The influence of functional diversity and composition on ecosystem processes. / Science 277: 1300-1302
  15. ↑ 15.0 15.1 15.2 Hector, A., Schmid, B., Beierkuhnlein, C. et al. 1999. Plant diversity and productivity experiments in European grasslands. Science 286: 1123-1127
  16. ↑ Schmid, B., Joshi, J. and Schlaepfer, F. 2001. Empirical evidence for biodiversity-ecosystem function relationships. In: Kinzig, A. P., Pacala, S. W. and Tilman, D. (eds), The functional consequences of biodiversity. Princeton Univ. Press, pp. 120-150.
  17. ↑ 17.0 17.1 Giller, P. S., Hillebrand, H., Berninger, U. G., Gessner, M. O., Hawkins, S. J., Inchausti, P., Inglis, C., Leslie, H. A., Malmqvist, B., Monaghan, M. T., Morin, P. J. and O'Mullan, G. 2004. Biodiversity effects on ecosystem functioning: emerging issues and their experimental test in aquatic environments. Oikos 104: 423-436
  18. ↑ Hairston, N. G., Smith, F. E. and Slobodkin, L. G. 1960. Community structure, population control, and competition. Am. Nat. 94: 421–425
  19. ↑ Power, M. E. 1990. Effects of fish in river food webs. Science 250: 411–415
  20. ↑ Estes, J. A., Tinker, M. T., Williams, T. M. and Doak, D. F. 1998. Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282:473–476
  21. ↑ Schindler, D. E. and Scheuerell, M. D. 2002. Habitat coupling in lake ecosystems. Oikos 98: 177-189
  22. ↑ Tilman, D., Knops, J., Wedin, D. and Reich P. 2002. Experimental and observational studies of diversity, productivity, and stability. Pages 42–70 in A. Kinzig, S. Pacala, and D. Tilman, editors. Functional consequences of biodiversity: Ecological Monographs Vol. 75, No. 1 Empirical progress and theoretical extensions. Princeton University Press, Princeton, New Jersey, USA.
  23. ↑ 23.0 23.1 23.2 Petchey, O. L. and Gaston, K. J. 2002. Functional diversity (FD), species richness and community composition. Ecol. Lett. 5: 402-411
  24. ↑ Huston, M. A., and McBride, A. C.. 2002. Evaluating the relative strengths of biotic versus abiotic controls on ecosystem processes. Pages 47–60 in M. Loreau, S. Naeem, and P. Inchausti, editors. Biodiversity and ecosystem functioning: synthesis and perspectives. Oxford University Press, Oxford, UK.
  25. ↑ Thebault, E., Huber, V., Loreau, M. 2007 Cascading extinctions and ecosystem functioning: contrasting effects of diversity depending on food web structure. Oikos 116: 163-173
  26. ↑ King, A.W. and Pimm, S.L. 1983. Complexity, diversity and stability: a reconciliation of theoretical and empirical results. The American Naturalist 122: 229–239
  27. ↑ Petchey, O. L, Downing, A. L., Mittelbach, G. G. et al. 2004. Species loss and the structure and functioning of multitrophic aquatic systems. Oikos 104: 467-478
  28. ↑ Loreau, M. 1998. Biodiversity and ecosystem functioning: a mechanistic model. Proceedings of the National Academy of Sciences (USA) 95: 5632–5636
  29. ↑ Huston, M. A. 1997. Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110: 449-460
  30. ↑ Wardle, D. A. 1999. Is ‘‘sampling effect’’ a problem for experiments investigating biodiversity–ecosystem function relationships? Oikos 87: 403–407
  31. ↑ 31.0 31.1 Naeem, S. 2002. Disentangling the impacts of diversity on ecosystem functioning in combinatorial experiments. Ecology 83: 2925–2935
  32. ↑ Loreau, M., Naeem, S., Inchausti, P. et al. 2001. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294: 804-808
  33. ↑ McCann, K., Hastings, A. and Huxel, G.R. 1998. Weak trophic interactions and the balance of nature. Nature 395: 794–798. https://doi.org/10.1038/27427
  34. ↑ Hooper, D.U., Chapin, F.S., III, Ewel, J.J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J.H., Lodge, D.M., Loreau, M., Naeem, S., et al. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 75: 3–35
  35. ↑ Lawton, J. H., Naeem, S., Thompson, L. J., Hector, A. and Crawley, M. J. 1998; Biodiversity and Ecosystem Function: Getting the Ecotron Experiment in its Correct Context Functional Ecology 12: 848-852
  36. ↑ 36.0 36.1 36.2 36.3 36.4 Ricotta, C. 2005. Through the jungle of biological diversity. Acta Biotheoretica 53: 29–38
  37. ↑ Wright, J. P., Naeem, S., Hector, A., Lehman, C., Reich, P. B., Schmid, B. and Tilman, D. 2006. Conventional functional classification schemes underestimate the relationship with ecosystem functioning. Ecology Letters, 9: 111 –120
  38. ↑ Tilman, D. 2001. Effects of diversity and composition on grassland stability and productivity. Pages 183–207 in M.C. Press, N. J. Huntley, and S. Levin, editors. Ecology: achievement and challenge. Blackwell Science, Oxford, UK
  39. ↑ Hooper, D. U., Solan, M., Symstad, A., Diaz, S., Gessner, M. A., Buchmann, N., Degrange, V., et al. 2002. Species diversity, functional diversity, and ecosystem functioning. In Biodiversity and Ecosystem Functioning: Synthesis and Perspectives, pp. 195 –208. Ed. by M. Loreau, S. Naeem, and P. Inchausti. Oxford University Press, Oxford.
  40. ↑ Hooper, D. U., Chapin, F. S., Ewel, J. J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J. H., et al. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs, 75: 3 –35
  41. ↑ Heemsbergen, D. A., Berg, M. P., Loreau, M., van Hal, J. R., Faber, J.H., and Verhoef, H. A. 2004. Biodiversity effects on soil processes explained by interspecific functional dissimilarity. Science, 306: 1019–1020
  42. ↑ 42.0 42.1 Somerfield, P. J., Clarke, K. R., Warwick, R. M., and Dulvy, N. K. 2008. Average functional distinctness as a measure of the composition of assemblages. – ICES Journal of Marine Science, 65: 1462–1468
  43. ↑ Schmera, D. 2003. Assessing stream dwelling caddis fly assemblages (Insecta: Trichoptera) collected by light traps in Hungary. Biodivers Conserv 12: 1175–119
  44. ↑ Magurran, A. (1988) Ecological Diversity and its Measurement. Princeton University Press, Princeton, NJ.
  45. ↑ Schmera, D., Eros, T. and Podani, J. 2009. A measure for assessing functional diversity in ecological communities. Aquatic Ecology, 2009 – Springer
  46. ↑ Diaz, S. and Cabido, M. 2001. Vive la difference: plant functional diversity matters to ecosystem processes. Trends in Ecology and Evolution 16: 646-655
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