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Species traits and environmental conditions govern the relationship between biodiversity effects across trophic levels

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Abstract

Changing environments can have divergent effects on biodiversity–ecosystem function relationships at alternating trophic levels. Freshwater mussels fertilize stream foodwebs through nutrient excretion, and mussel species-specific excretion rates depend on environmental conditions. We asked how differences in mussel diversity in varying environments influence the dynamics between primary producers and consumers. We conducted field experiments manipulating mussel richness under summer (low flow, high temperature) and fall (moderate flow and temperature) conditions, measured nutrient limitation, algal biomass and grazing chironomid abundance, and analyzed the data with non-transgressive overyielding and tripartite biodiversity partitioning analyses. Algal biomass and chironomid abundance were best explained by trait-independent complementarity among mussel species, but the relationship between biodiversity effects across trophic levels (algae and grazers) depended on seasonal differences in mussel species’ trait expression (nutrient excretion and activity level). Both species identity and overall diversity effects were related to the magnitude of nutrient limitation. Our results demonstrate that biodiversity of a resource-provisioning (nutrients and habitat) group of species influences foodweb dynamics and that understanding species traits and environmental context are important for interpreting biodiversity experiments.

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References

  • Ackerly DD, Cornwell WK (2007) A trait-based approach to community assembly: partitioning of species trait values into within- and among-community components. Ecol Lett 10:135–145

    Article  PubMed  CAS  Google Scholar 

  • Allen DC, Vaughn CC (2009) Burrowing behavior of freshwater mussels in experimentally manipulated communities. J North Am Benthol Soc 28:93–100

    Article  Google Scholar 

  • ASTM (1995) Standard methods for the examination of water and wastewater. American Public Health Association/American Water Works Association/Water Environment Federation, Alexandria

  • Borer ET, Seabloom EW, Shurin JB, Anderson KE, Blanchette CA, Broitman B, Cooper SD, Halper BS (2005) What determines the strength of a trophic cascade? Ecology 86:528–537

    Article  Google Scholar 

  • Canuel EA, Spivak AC, Waterson EJ, Duffy JE (2007) Biodiversity and food web structure influence short-term accumulation of sediment organic matter in an experimental seagrass system. Limnol Oceanogr 52:590–602

    Article  CAS  Google Scholar 

  • Cardinale BJ, Nelson K, Palmer MA (2000) Linking species diversity to the functioning of ecosystems: on the importance of environmental context. Oikos 9:175–183

    Article  Google Scholar 

  • Cardinale BJ (2011) Biodiversity improves water quality through niche partitioning. Nature 472:86–89

    Article  PubMed  CAS  Google Scholar 

  • Cardinale BJ, Palmer MA, Collins SL (2002) Species diversity enhances ecosystem functioning through interspecific facilitation. Nature 414:427–429

    Google Scholar 

  • Cardinale BJ, Svristava DS, Duffy JE, Wright JP, Downing AL, Sankaran M, Jouseau JC (2006) Effects of diversity on the functioning of trophic groups and ecosystems. Nature 443:991–992

    Article  Google Scholar 

  • Diaz S, Boy-Meir I, Cabido M (2001) Can grazing response of herbaceous plants be predicted from simple vegetative traits? J Appl Ecol 38:497–508

    Article  Google Scholar 

  • Douglass JG, Duffy JE, Bruno JF (2008) Herbivore and predator diversity interactively affect ecosystem properties in an experimental marine community. Ecol Lett 11:598–608

    Article  PubMed  Google Scholar 

  • Duffy JE (2003) Biodiversity loss, trophic skew and ecosystem functioning. Ecol Lett 6:680–687

    Article  Google Scholar 

  • Duffy JE, Cardinale BJ, France KE, McIntyre PB, Thebault E, Loreau M (2007) The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol Lett 10:522–538

    Article  PubMed  Google Scholar 

  • Duffy JE, Richardson PJ, Canuel EA (2003) Grazer diversity effects on ecosystem functioning in seagrass beds. Ecol Lett 6:637–645

    Article  Google Scholar 

  • Dyer LA, Letourneau D (2003) Top-down and bottom-up diversity cascades in detrital vs. living food webs. Ecol Lett 6:60–68

    Article  Google Scholar 

  • Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine, and terrestrial ecosystems. Ecol Lett 10:1–8

    Article  Google Scholar 

  • Evans-White MA, Lamberti GA (2005) Grazer species effects on epilithon nutrient composition. Freshw Biol 50:1853–1863

    Article  CAS  Google Scholar 

  • Finke DL, Denno RF (2005) Predator diversity and the functioning of ecosystems: the role of intraguild predation in dampening trophic cascades. Ecol Lett 8:1299–1306

    Article  Google Scholar 

  • Fox JW (2005) Interpreting the selection effect of biodiversity on ecosystem function. Ecol Lett 8:846–856

    Article  Google Scholar 

  • Galbraith HS, Spooner DE, Vaughn CC (2008) Status of rare and endangered freshwater mussels in southeastern Oklahoma rivers. Southwest Nat 5:45–50

    Article  Google Scholar 

  • Galbraith HS, Spooner DE, Vaughn CC (2010) Synergistic effects of regional climate patterns and local water management on freshwater mussel communities. Biol Conserv 143:1175–1183

    Article  Google Scholar 

  • Gessner MO, Swan CM, McKie BG, Bardgett RD, Wall DH, Hättenschwiler S (2010) Diversity meets decomposition. Trends Ecol Evol 25:372–380

    Article  PubMed  Google Scholar 

  • Gresens SE (1995) Grazer diversity, competition and the response of the periphyton community. Oikos 73:336–346

    Article  Google Scholar 

  • Griffin JN, De La Haye KL, Hawkins SJ, Thompson RC, Jenkins SR (2008) Predator diversity and ecosystem functioning: density modifies the effect of resource partitioning. Ecology 89:298–305

    Article  PubMed  Google Scholar 

  • Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94:421–425

    Article  Google Scholar 

  • Hillebrand H, Cardinale BJ (2004) Consumer effects decline with prey diversity. Ecol Lett 7:192–201

    Article  Google Scholar 

  • Hillebrand H, de Montpellier G, Liess A (2004) Effects of macrograzers and light on periphyton stoichiometry. Oikos 106:93–104

    Article  Google Scholar 

  • Hillebrand H, Matthiessen B (2009) Biodiversity in a complex world: consolidation and progress in functional biodiversity research. Ecol Lett 12:1405–1419

    Article  PubMed  Google Scholar 

  • Hillebrand H, Shurin JB (2005) Biodiversity and aquatic food webs. In: Belgrano A, Scharler UM, Dunne J, Ulanowicz RE (eds) Aquatic food webs–an ecosystem approach. Oxford University Press, Oxford, pp 184–197

  • Hillebrand H, Gruner DS, Borer ET, Bracken MES, Cleland EE, Elser JJ, Harpole WS, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Consumer versus resource control of producer diversity depends on ecosystem type and producer community structure. Proc Natl Acad Sci USA 104:10904–10909

    Article  PubMed  CAS  Google Scholar 

  • Hooper DU (1998) The role of complementarity and competition in ecosystem responses to variation in plant diversity. Ecology 79:704–719

    Article  Google Scholar 

  • Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom–up and top–down forces in natural communities. Ecology 73:724–732

    Google Scholar 

  • Kahmen A, Renker C, Unsicker SB, Buchmann N (2006) Niche complementarity for nitrogen: an explanation for the biodiversity and ecosystem function relationship. Ecology 87:1244–1255

    Article  PubMed  Google Scholar 

  • Kominoski JS, Hoellin TJ, Leroy CJ, Pringle CM, Swan CM (2010) Beyond species richness: expanding biodiversity-ecosystem functioning theory in detritus-based streams. Rivers Res Appl 26:67–75

    Article  Google Scholar 

  • Leibold MA, Chase JM, Shurin JB, Downing AL (1997) Species turnover and the regulation of trophic structure. Annu Rev Ecol Syst 28:467–494

    Article  Google Scholar 

  • Loreau M (1998) Separating sampling and other effects in biodiversity experiments. Oikos 82:600–602

    Article  Google Scholar 

  • Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76

    Article  PubMed  CAS  Google Scholar 

  • Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli D, Schmid B, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808

    Article  PubMed  CAS  Google Scholar 

  • Matthews WJ, Vaughn CC, Gido KB, Marsh-Matthews E (2005) Southern Plains Rivers. In: Benke AC, Cushing CE (eds) Rivers of North America. Elsevier, London, pp 283–325

    Google Scholar 

  • McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185

    Article  PubMed  Google Scholar 

  • McIntyre PB, Flecker AS, Vanni MJ, Hood JM, Taylor BW, Thomas SA (2008) Fish distributions and nutrient cycling in streams: can fish create biogeochemical hotspots? Ecology 89:2335–2346

    Article  PubMed  Google Scholar 

  • Naeem S, Wright JP (2003) Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecol Lett 6:567–579

    Article  Google Scholar 

  • Naeem S, Thompson LJ, Lawton JH, Woodfin RM (1994) Declining biodiversity can alter the performance of ecosystems. Nature 368:734–736

    Article  Google Scholar 

  • Poff NL (1997) Landscape filters and species traits: towards mechanistic understanding and prediction in stream ecology. J North Am Benthol Soc 16:391–409

    Article  Google Scholar 

  • Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147:813–845

    Article  Google Scholar 

  • Pringle CM, Triska FJ (1996) Effects of nutrient enrichment on periphyton. In: Hauer FR, Lamberti GA (eds) Methods in stream ecology. Academic Press, San Diego, pp 607–623

  • Rosemond AD, Pringle CM, Ramirez A, Paul MJ (2001) A test of top–down and bottom–up control in a detritus-based food web. Ecology 82:2279–2293

    Article  Google Scholar 

  • Schmid B, Hector A, Huston MA, Inchausti P, Nijs I, Leadley PW, Tilman D (2002) The design and analysis of biodiversity experiments. In: Loreau N, Naeem NS, Inchausti P (eds) Biodiversity and ecosystem functioning: synthesis and perspectives. Oxford University Press, Oxford, pp 61–75

    Google Scholar 

  • Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163

    Article  Google Scholar 

  • Spivak AC, Canuel EA, Duffy JE, Richardson JP (2007) Top–down and bottom–up controls on sediment organic matter composition in an experimental seagrass ecosystem. Limnol Oceanogr 52:2595–2607

    Article  CAS  Google Scholar 

  • Spooner DE, Vaughn CC (2006) Context-dependent effects of freshwater mussels on the benthic community. Freshw Biol 5:1016–1024 Corrigendum 1188

    Article  Google Scholar 

  • Spooner DE, Vaughn CC (2008) A trait-based approach to species’ roles in stream ecosystems: climate change, community structure, and material cycling. Oecologia 158:307–317

    Article  PubMed  Google Scholar 

  • Spooner DE, Vaughn CC (2011) Species’ traits, dominance, and environmental gradients interact to govern primary production in freshwater mussel communities. Oikos (in press). doi:10.1111/j.1600-0706.2011.19380.x

  • Srivastava DS, Bell T (2009) Reducing horizontal and vertical diversity in a foodweb triggers extinctions and impacts functions. Ecol Lett 12:1016–1028

    Article  PubMed  Google Scholar 

  • Srivastava DS, Cardinale BJ, Downing AL, Duffy JE, Jouseau C, Sankaran M, Wright JP (2009) Diversity has stronger top–down than bottom–up effects on decomposition. Ecology 90:1073–1083

    Article  PubMed  Google Scholar 

  • Symstad AJ, Tilman D, Wilson J, Knops JMH (1998) Species loss and ecosystem functioning: effects of species identity and community composition. Oikos 81:389–397

    Article  Google Scholar 

  • Tilman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75:2–16

    Article  Google Scholar 

  • Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and productivity in a long-term grassland experiment. Science 294:843–845

    Article  PubMed  CAS  Google Scholar 

  • Vaughn CC, Spooner DE, Galbraith HS (2007) Context-dependent species identity effects within a functional group of filter-feeding bivalves. Ecology 88:1654–1662

    Article  PubMed  Google Scholar 

  • Vaughn CC, Nichols SJ, Spooner DE (2008) Community and foodweb ecology of freshwater mussels. J North Am Benthol Soc 27:41–55

    Article  Google Scholar 

  • Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of earth’s ecosystems. Science 277:494–499

    Article  CAS  Google Scholar 

  • Walker BH (1992) Biodiversity and ecological redundancy. Conserv Biol 6:18–23

    Article  Google Scholar 

  • Worm B, Duffy JE (2003) Biodiversity, productivity and stability in real food webs. Trends Ecol Evol 18:629–632

    Article  Google Scholar 

  • Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Selkow KA, Stachowicz JJ, Watson R (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314:787–790

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank T. Garrett for allowing access to the field site, R. Deaton, S. and B. Dengler, D. Fenolio, S. Frazier, P. Jeyasingh, M. Jones, S. Jones, F. March, K. Reagan, R. Remington, and E. Webber for field and/or laboratory assistance, and D. Allen for comments on the manuscript. This study was funded by the National Science Foundation (DEB-0211010) and is a contribution to the program of the Oklahoma Biological Survey.

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  1. Daniel E. Spooner & Heather S. Galbraith

    Present address: Northern Appalachian Research Laboratory, United States Geological Survey, Wellsboro, PA, 16901, USA

Authors and Affiliations

  1. Oklahoma Biological Survey and Department of Zoology, University of Oklahoma, Norman, OK, 73019, USA

    Daniel E. Spooner, Caryn C. Vaughn & Heather S. Galbraith

  2. Graduate Program in Ecology and Evolutionary Biology, University of Oklahoma, Norman, OK, 73019, USA

    Caryn C. Vaughn

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  1. Daniel E. Spooner
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Correspondence to Daniel E. Spooner.

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Communicated by Jonathan Shurin.

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Spooner, D.E., Vaughn, C.C. & Galbraith, H.S. Species traits and environmental conditions govern the relationship between biodiversity effects across trophic levels. Oecologia 168, 533–548 (2012). https://doi.org/10.1007/s00442-011-2110-1

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