Skip to main content

Advertisement

SpringerLink
Log in

Species effects on ecosystem processes are modified by faunal responses to habitat composition

  • Ecosystem Ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Heterogeneity is a well-recognized feature of natural environments, and the spatial distribution and movement of individual species is primarily driven by resource requirements. In laboratory experiments designed to explore how different species drive ecosystem processes, such as nutrient release, habitat heterogeneity is often seen as something which must be rigorously controlled for. Most small experimental systems are therefore spatially homogeneous, and the link between environmental heterogeneity and its effects on the redistribution of individuals and species, and on ecosystem processes, has not been fully explored. In this paper, we used a mesocosm system to investigate the relationship between habitat composition, species movement and sediment nutrient release for each of four functionally contrasting species of marine benthic invertebrate macrofauna. For each species, various habitat configurations were generated by selectively enriching patches of sediment with macroalgae, a natural source of spatial variability in intertidal mudflats. We found that the direction and extent of faunal movement between patches differs with species identity, density and habitat composition. Combinations of these factors lead to concomitant changes in nutrient release, such that habitat composition effects are modified by species identity (in the case of NH4–N) and by species density (in the case of PO4–P). It is clear that failure to accommodate natural patterns of spatial heterogeneity in such studies may result in an incomplete understanding of system behaviour. This will be particularly important for future experiments designed to explore the effects of species richness on ecosystem processes, where the complex interactions reported here for single species may be compounded when species are brought together in multi-species combinations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Balvanera P, Pfisterer AB, Buchman N, He J-H, Nakashizuka T, Raffaelli D, Schmid B (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156

    Article  PubMed  Google Scholar 

  • Benedetti-Cecchi L, Vaselli S, Maggi E, Bertocci I (2005) Interactive effects of spatial variance and mean intensity of grazing on algal cover in rock pools. Ecology 86:2212–2222

    Article  Google Scholar 

  • Benton TG, Solan M, Travis J, Sait SM (2007) Microcosm experiments can inform global ecological problems. Trends Ecol Evol 22:516–521

    Article  PubMed  Google Scholar 

  • Biles CL, Solan M, Isaksson I, Paterson DM, Emes C, Raffaelli DG (2003) Flow modifies the effect of biodiversity on ecosystem functioning: an in situ study of estuarine sediments. J Exp Mar Biol Ecol 285:165–177

    Article  Google Scholar 

  • Bracken MES, Stachowicz JJ (2006) Seaweed diversity enhances nitrogen uptake via complementary use of nitrate and ammonium. Ecology 87:2397–2403

    Article  PubMed  Google Scholar 

  • Bracken MES, Friberg SE, Gonzalez-Dorantes CA, Williams SL (2008) Functional consequences of realistic biodiversity changes in a marine ecosystem. Proc Natl Acad Sci USA 105:924–928

    Article  PubMed  CAS  Google Scholar 

  • Bulling MT, White PCL, Raffaelli DG, Pierce GJ (2006) Using model systems to address the biodiversity-ecosystem functioning process. Mar Ecol Prog Ser 311:295–309

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Cadée GC (2000) Sediment dynamics by bioturbating organisms. In: Reise K (ed) Ecological comparisons of sedimentary shores. Springer, Berlin, pp 127–143

    Google Scholar 

  • Cardinale BJ, Ives AR, Inchausti P (2004) Effects of species diversity on the primary productivity of ecosystems: extending our spatial and temporal scales of inference. Oikos 104:437–450

    Article  Google Scholar 

  • Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, Sankaran M, Jouseau C (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–992

    Article  PubMed  CAS  Google Scholar 

  • Covich AP, Austen M, Bärlocher F, Chauvet E, Biles CL, Inchausti P, Dangles O, Statzner B, Solan M, Moss BR, Asmus H (2004) The role of biodiversity in the functioning of freshwater and marine benthic ecosystems. Bioscience 54:767–775

    Article  Google Scholar 

  • Diggle PJ, Heagerty P, Liang K-Y, Zeger SL (2002) Analysis of longitudinal data. Oxford University Press, New York

    Google Scholar 

  • Duffy JE, MacDonald KS, Rhode JM, Parker JD (2001) Grazer diversity, functional redundancy, and productivity in seagrass beds: an experimental test. Ecology 82:2417–2434

    Article  Google Scholar 

  • Dyson KE, Bulling MT, Solan M, Hernandez-Milian G, Raffaelli DG, White PC, Paterson DM (2007) Influence of macrofaunal assemblages and environmental heterogeneity on microphytobenthic production in experimental systems. Proc Biol Sci 274:2547–2554

    Article  PubMed  Google Scholar 

  • Ellingsen KE, Gray JS (2002) Spatial patterns of benthic diversity: is there a latitudinal gradient along the Norwegian continental shelf? J Anim Ecol 71:373–389

    Article  Google Scholar 

  • Emmerson MC, Solan M, Emes C, Paterson DM, Raffaelli D (2001) Consistent patterns and the idiosyncratic effects of biodiversity in marine ecosystems. Nature 411:73–77

    Article  PubMed  CAS  Google Scholar 

  • Faraway JJ (2006) Extending the linear model with R: generalized linear, mixed effects and non-parametric regression models. Chapman & Hall/CRC, Boca Raton

  • Giller PS, Hillebrand H, Berninger UG, Gressner MO, Hawkins S, Inchausti P, Inglis C, Leslie H, Malmqvist B, Monaghan MT, Morin PJ, O’Mullan G (2004) Biodiversity effects on ecosystem functioning: emerging issues and their experimental test in aquatic environments. Oikos 104:423–436

    Article  Google Scholar 

  • Goodsell PJ, Connell SD (2002) Can habitat loss be treated independently of habitat configuration? Implications for rare and common taxa in fragmented landscapes. Mar Ecol Prog Ser 239:37–44

    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 

  • Hall SJ, Raffaelli D, Thrush SF (1994) Patchiness and disturbance in shallow water benthic assemblages. In: Giller PS, Hildrew AG, Raffaelli DG (eds) Aquatic ecology: scale, pattern and process. Blackwell, Oxford, pp 333–375

    Google Scholar 

  • Hewitt JE, Thrush SF, Legendre P, Cummings VJ, Norkko A (2002) Integrating heterogeneity across spatial scales: interactions between Atrina zelandica and benthic macrofauna. Mar Ecol Prog Ser 239:115–128

    Article  Google Scholar 

  • Hovel KA, Lipcius RN (2001) Habitat fragmentation in a seagrass landscape: patch size and complexity control blue crab survival. Ecology 82:1814–1829

    Google Scholar 

  • Hull SC (1987) Macroalgal mats and species abundance: a field experiment. Estuar Coast Shelf Sci 25:519–532

    Article  Google Scholar 

  • Ieno EN, Solan M, Batty P, Pierce GJ (2006) How biodiversity affects ecosystem functioning: roles of infaunal species richness, identity and density in the marine benthos. Mar Ecol Prog Ser 311:263–271

    Article  Google Scholar 

  • Jahn A, Janas U, Theede H, Szaniawska A (1997) Significance of body size in sulphide detoxification in the Baltic clam Macoma balthica (Bivalvia, Tellinidae) in the Gulf of Gdansk. Mar Ecol Prog Ser 154:175–183

    Article  CAS  Google Scholar 

  • Johnson RG (1972) Conceptual models of benthic marine communities. In: Schopf TJM (ed) Models in paleobiology. Freeman Cooper, San Francisco, pp 148–159

  • Kelaher BP, Levinton JS (2003) Variation in detrital enrichment causes spatio-temporal variation in soft-sediment assemblages. Mar Ecol Prog Ser 261:85–97

    Article  Google Scholar 

  • Lawrie SM (1996) Spatial patterns of the amphipod Corophium volutator on the Ythan estuary. Unpublished Ph.D. thesis, University of Aberdeen, p 204

  • Levinton J, Kelaher B (2004) Opposing organising forces of deposit-feeding marine communities. J Exp Mar Biol Ecol 300:65–82

    Article  Google Scholar 

  • Mermillod-Blondin F, Francois-Carcaillet F, Rosenberg R (2005) Biodiversity of benthic invertebrates and organic matter processing in shallow marine sediments: an experimental study. J Exp Mar Biol Ecol 315:187–209

    Article  Google Scholar 

  • Millennium Ecosystem Assessment (2005) Ecosystems and human well-being: biodiversity synthesis. World Resources Institute, Washington, DC

    Google Scholar 

  • Nogaro G, Charles F, de Mendonça Jr JB, Mermillod-Blondin F, Stora G, François-Carcaillet F (2008) Food supply impacts sediment reworking by Nereis diversicolor. Hydrobiologia 598:403–408

    Article  Google Scholar 

  • Noren K, Lindegarth M (2005) Spatial, temporal and interactive variability of infauna in Swedish coastal sediments. J Exp Mar Biol Ecol 317:53–68

    Article  Google Scholar 

  • Norkko A (1998) The impact of loose-lying algal mats and predation by the brown shrimp Crangon crangon (L.) on infaunal prey dispersal and survival. J Exp Mar Biol Ecol 221:99–116

    Article  Google Scholar 

  • Norkko A, Bonsdorff E (1996a) Population responses of coastal zoobenthos to stress induced by drifting algal mats. Mar Ecol Prog Ser 141:141–151

    Article  Google Scholar 

  • Norkko A, Bonsdorff E (1996b) Altered benthic prey-availability due to episodic oxygen deficiency caused by drifting algal mats. Mar Ecol 17:355–372

    Article  CAS  Google Scholar 

  • Parry DM, Kendall MA, Pilgrim DA, Jones MB (2003) Identification of patch structure within marine benthic landscapes using a remotely operated vehicle. J Exp Mar Biol Ecol 285:497–511

    Article  Google Scholar 

  • Pearson TH, Rosenberg R (1978) Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanogr Mar Biol Ann Rev 16:229–311

    Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-plus. Springer, New York

    Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D (2006) nlme: an R package for fitting and comparing Gaussian linear and nonlinear mixed-effects models. Available at http://www.stats.bris.ac.uk/R/. Last accessed 22 Sept 2008

  • Quinn QP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Google Scholar 

  • R Development Core Team (2005) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Raffaelli D (1999) Nutrient enrichment and trophic organisation in an estuarine food web. Acta Oecol 20:449–461

    Article  Google Scholar 

  • Raffaelli D (2000) Interactions between macro-algal mats and invertebrates in the Ythan estuary, Aberdeenshire, Scotland. Helgol Mar Res 54:71–79

    Article  Google Scholar 

  • Raffaelli D, Limia J, Hull S, Pont S (1991) Interactions between the amphipod Corophium volutator and macroalgal mats on estuarine mudflats. J Mar Biol Assoc UK 71:899–908

    Article  Google Scholar 

  • Raffaelli D, Emmerson M, Solan M, Biles C, Paterson D (2003) Biodiversity and ecosystem processes in shallow coastal waters: an experimental approach. J Sea Res 49:133–141

    Article  Google Scholar 

  • Rhoads DC, McCall PL, Yingst JY (1978) Disturbance and production on the estuarine seafloor. Am Sci 66:577–586

    Google Scholar 

  • Sakamoto Y, Ishiguro M, Kitagawa G (1986) Akaike information criterion statistics. Reidel, Dordrecht

    Google Scholar 

  • Sanvicente-Anorve L, Lepretre A, Davoult D (2002) Diversity of benthic macrofauna in the eastern English Channel: comparison among and within communities. Biodivers Conserv 11:265–282

    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 M, Naeem S, Inchausti P (eds) Biodiversity and ecosystem functioning: synthesis and perspectives. Oxford University Press, Oxford, pp 61–75

    Google Scholar 

  • Teixido N, Garrabou J, Arntz WE (2002) Spatial pattern quantification of Antarctic benthic communities using landscape indices. Mar Ecol Prog Ser 242:1–14

    Article  Google Scholar 

  • Underwood AJ (1998) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge

    Google Scholar 

  • Verbeke G, Molenberghs G (2000) Linear mixed models for longitudinal data. Springer, New York

    Google Scholar 

  • Waldbusser GG, Marinelli RL, Whitlatch RB, Visscher PT (2004) The effects of infaunal biodiversity on biogeochemistry of coastal marine sediments. Limnol Oceanogr 49:1482–1492

    CAS  Google Scholar 

  • West BT, Welch KB, Gatecki AT (2007) Linear mixed models: a practical guide using statistical software. Chapman & Hall/CRC, Boca Raton

  • Zajac RN (2001) Organism–sediment relations at multiple spatial scales: implications for community structure and successional dynamics. In: Aller JY, Woodin SA, Aller RC (eds) Organism–sediment interactions. University of South Carolina Press, USA

  • Zuur AF, Ieno EN, Smith GM (2007) Analysing ecological data. Springer, New York

    Google Scholar 

Download references

Acknowledgments

We thank three anonymous reviewers for their helpful and constructive comments, O. McPherson, A. Holford and D. Mackinnon for technical assistance, and M. Feilen, T. Fujii, A. Goyal, L. Murray, M. Shepherd, R. Sutton, E. Walpersdorff for support in the field. Graphical representations of fauna were designed by L. Murray. Statistical advice from Highland Statistics Ltd is gratefully acknowledged. We confirm that the experiments comply with the current laws of the country in which they were performed. The research was supported by NERC under grant NER/A/S/2003/00577.

Author information

Authors and Affiliations

  1. Environment Department, University of York, Heslington, York, YO10 5DD, UK

    Mark T. Bulling, Dave Raffaelli & Piran C. L. White

  2. Oceanlab, University of Aberdeen, Main Street, Newburgh, Aberdeenshire, AB41 6AA, UK

    Martin Solan, Gema Hernandez-Milian, Patricia Luque & Graham J. Pierce

  3. Gatty Marine Laboratory, University of St Andrews, East Sands, St Andrews, Fife, KY16 8LB, UK

    Kirstie E. Dyson & David M. Paterson

Authors
  1. Mark T. Bulling
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martin Solan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kirstie E. Dyson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gema Hernandez-Milian
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Patricia Luque
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Graham J. Pierce
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Dave Raffaelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. David M. Paterson
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Piran C. L. White
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark T. Bulling.

Additional information

Communicated by Ulrich Sommer.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Tables and Models (DOC 210 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bulling, M.T., Solan, M., Dyson, K.E. et al. Species effects on ecosystem processes are modified by faunal responses to habitat composition. Oecologia 158, 511–520 (2008). https://doi.org/10.1007/s00442-008-1160-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-008-1160-5

Keywords

Search

Navigation