Skip to main content

Advertisement

Log in

The mechanisms by which oysters facilitate invertebrates vary across environmental gradients

  • Ecosystem ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The effective use of ecosystem engineers to conserve biodiversity requires an understanding of the types of resources an engineer modifies, and how these modifications vary with biotic and abiotic context. In the intertidal zone, oysters engineer ecological communities by reducing temperature and desiccation stress, enhancing the availability of hard substrate for attachment, and by ameliorating biological interactions such as competition and predation. Using a field experiment manipulating shading, predator access and availability of shell substrate at four sites distributed over 900 km of east Australian coastline, we investigated how the relative importance of these mechanisms of facilitation vary spatially. At all sites, and irrespective of environmental conditions, the provision of hard substrate by oysters enhanced the abundance and richness of invertebrates, in particular epibionts (barnacles and oyster spat) and grazing gastropods. Mobile arthropods utilised the habitat provided by disarticulated dead oysters more than live oyster habitat, whereas the abundance of polychaetes and bivalves were much greater in live oysters, suggesting the oyster filter-feeding activity is important for these groups. In warmer estuaries, shading by oysters had a larger effect on biodiversity, whereas in cooler estuaries, the provision of a predation refuge by oysters played a more important role. Such knowledge of how ecosystem engineering effects vary across environmental gradients can help inform management strategies targeting ecosystem resilience via the amelioration of specific environmental stressors, or conservation of specific community assemblages.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Bateman DC, Bishop MJ (2017) The environmental context and traits of habitat-forming bivalves influence the magnitude of their ecosystem engineering. Mar Ecol Prog Ser 563:95–110

    Article  Google Scholar 

  • Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193

    Article  CAS  PubMed  Google Scholar 

  • Bishop MJ, Byers JE, Marcek BJ, Gribben PE (2012) Density-dependent facilitation cascades determine epifaunal community structure in temperate Australian mangroves. Ecology 93:1388–1401

    Article  PubMed  Google Scholar 

  • Branch GM, Branch ML (1980) Competition in Bembicium auratum (Gastropoda) and its effect on microalgal standing stock in mangrove muds. Oecologia 46:106–114

    Article  CAS  PubMed  Google Scholar 

  • Bulleri F, Bruno JF, Silliman BR, Stachowicz JJ (2016) Facilitation and the niche: implications for coexistence, range shifts and ecosystem functioning. Funct Ecol 30:70–78

    Article  Google Scholar 

  • Byers JE, Cuddington K, Jones CG, Talley TS, Hastings A, Lambrinos JG, Crooks JA, Wilson WG (2006) Using ecosystem engineers to restore ecological systems. Trends Ecol Evol 21:493–500

    Article  PubMed  Google Scholar 

  • Callaway RM (2007) Positive interactions and interdependence in plant communities. Springer, Dordrecth

    Google Scholar 

  • Crain CM, Bertness MD (2006) Ecosystem engineering across environmental gradients: implications for conservation and management. Bioscience 56:211–218

    Article  Google Scholar 

  • Freestone AL, Osman RW, Ruiz GM, Torchin ME (2011) Stronger predation in the tropics shapes species richness patterns in marine communities. Ecology 92:983–993

    Article  PubMed  Google Scholar 

  • Gómez-Aparicio L, Zamora R, Gómez JM, Hódar JA, Castro J, Baraza E (2004) Applying plant facilitation to forest restoration: a meta-analysis of the use of shrubs as nurse plants. Ecol Appl 14:1128–1138

    Article  Google Scholar 

  • Grabowski JH (2004) Habitat complexity disrupts predator–prey interactions but not the trophic cascade on oyster reefs. Ecology 85:995–1004

    Article  Google Scholar 

  • Grabowski JH, Powers SP (2004) Habitat complexity mitigates trophic transfer on oyster reefs. Mar Ecol Prog Ser 277:291–295

    Article  Google Scholar 

  • Grabowski JH, Hughes AR, Kimbro DL (2008) Habitat complexity influences cascading effects of multiple predators. Ecology 89:3413–3422

    Article  PubMed  Google Scholar 

  • Grabowski JH, Brumbaugh RD, Conrad RF, Keeler AG, Opaluch JJ, Peterson CH, Piehler MF, Powers SP, Smyth AR (2012) Economic valuation of ecosystem services provided by oyster reefs. Bioscience 62:900–909

    Article  Google Scholar 

  • Gutiérrez JL, Jones CG, Strayer DL, Iribarne OO (2003) Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101:79–90

    Article  Google Scholar 

  • Hastings A, Byers JE, Crooks JA, Cuddington K, Jones CG, Lambrinos JG, Talley TS, Wilson WG (2007) Ecosystem engineering in space and time. Ecol Lett 10:153–164

    Article  PubMed  Google Scholar 

  • Helmuth B, Mieszkowska N, Moore P, Hawkins SJ (2006) Living on the edge of two changing worlds: forecasting the responses of rocky intertidal ecosystems to climate change. Annu Rev Ecol Evol Syst 37:373–404

    Article  Google Scholar 

  • Hughes AR, Gribben PE, Kimbro DL, Bishop MJ (2014) Additive and site-specific effects of two foundation species on invertebrate community structure. Mar Ecol Prog Ser 508:129–138

    Article  Google Scholar 

  • IBM Corp. (2016) IBM SPSS Statistics for windows, Version 24.0. Armonk, New York, The United States of America

  • Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 78:1946–1957

    Google Scholar 

  • Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957

    Article  Google Scholar 

  • Jones CG, Gutiérrez JL, Byers JE, Crooks JA, Lambrinos JG, Talley TS (2010) A framework for understanding physical ecosystem engineering by organisms. Oikos 119:1862–1869

    Article  Google Scholar 

  • Keppel G, Van Niel KP, Wardell-Johnson GW, Yates CJ, Byrne M, Mucina L, Schut AG, Hopper SD, Franklin SE (2012) Refugia: identifying and understanding safe havens for biodiversity under climate change. Glob Ecol Biogeogr 21:393–404

    Article  Google Scholar 

  • La Peyre MK, Gossman B, La Peyre JF (2009) Defining optimal freshwater flow for oyster production: effects of freshet rate and magnitude of change and duration on eastern oysters and Perkinsus marinus infection. Estuar Coast 32:522–534

    Article  Google Scholar 

  • Lavender JT, Dafforn KA, Bishop MJ, Johnston EL (2017) An empirical examination of consumer effects across twenty degrees of latitude. Ecology 98:2391–2400

    Article  PubMed  Google Scholar 

  • Maestre FT, Callaway RM, Valladares F, Lortie CJ (2009) Refining the stress-gradient hypothesis for competition and facilitation in plant communities. J Ecol 97:199–205

    Article  Google Scholar 

  • McAfee D, Cole VJ, Bishop MJ (2016) Latitudinal gradients in ecosystem engineering by oysters vary across habitats. Ecology 97:929–939

    PubMed  Google Scholar 

  • McAfee D, O’Connor WA, Bishop MJ (2017) Fast-growing oysters show reduced capacity to provide a thermal refuge to intertidal biodiversity at high temperatures. J Anim Ecol 86:1352–1362

    Article  PubMed  Google Scholar 

  • McAfee D, Bishop MJ, Yu TN, Williams GA (2018) Structural traits dictate abiotic stress amelioration by intertidal oysters. Funct Ecol 32:2666–2677

    Article  Google Scholar 

  • McMahon RF (1990) Thermal tolerance, evaporative water loss, air-water oxygen consumption and zonation of intertidal prosobranchs: a new synthesis. Hydrobiologia 193:241–260

    Article  Google Scholar 

  • Michalet R, Brooker RW, Cavieres LA, Kikvidze Z, Lortie CJ, Pugnaire FI, Valiente-Banuet A, Callaway RM (2006) Do biotic interactions shape both sides of the humped-back model of species richness in plant communities? Ecol Lett 9:767–773

    Article  PubMed  Google Scholar 

  • Minchinton TE, Ross PM (1999) Oysters as habitat for limpets in a temperate mangrove forest. Aust J Ecol 24:157–170

    Article  Google Scholar 

  • Mittelbach GG, Schemske DW, Cornell HV, Allen AP, Brown JM, Bush MB, Harrison SP, Hurlbert AH, Knowlton N, Lessios HA, McCain CM (2007) Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol Lett 10:315–331

    Article  PubMed  Google Scholar 

  • Nelson KA, Leonard LA, Posey MH, Alphin TD, Mallin MA (2004) Using transplanted oyster (Crassostrea virginica) beds to improve water quality in small tidal creeks: a pilot study. J Exp Mar Biol Ecol 298:347–368

    Article  Google Scholar 

  • Newell RIE (2004) Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. J Shellfish Res 23:51–61

    Google Scholar 

  • Padilla DK (2010) Context-dependent impacts of a non-native ecosystem engineer, the Pacific oyster Crassostrea gigas. Integr Comp Biol 50:213–225

    Article  PubMed  Google Scholar 

  • Reid DG (1988) The genera Bembicium and Risellopsis (Gastropoda: littorinidae) in Australia and New Zealand. Rec Aust Mus 40:91–150

    Article  Google Scholar 

  • Ridge JT, Rodriguez AB, Fodrie FJ, Lindquist NL, Brodeur MC, Coleman SE, Grabowski JH, Theuerkauf EJ (2015) Maximizing oyster-reef growth supports green infrastructure with accelerating sea-level rise. Sci Rep 5:14785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seed R (1996) Patterns of biodiversity in the macro-invertebrate fauna associated with mussel patches on rocky shores. J Mar Biol Assoc UK 76:203–210

    Article  Google Scholar 

  • Silliman BR, Bertness MD, Altieri AH, Griffin JN, Bazterrica MC, Hidalgo FJ, Crain CM, Reyna MV (2011) Whole-community facilitation regulates biodiversity on Patagonian rocky shores. PLoS One 6:e24502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Summerhayes SA, Bishop MJ, Leigh A, Kelaher BP (2009) Effects of oyster death and shell disarticulation on associated communities of epibiota. J Exp Mar Biol Ecol 379:60–67

    Article  Google Scholar 

  • Wells HW (1961) The fauna of oyster beds, with special reference to the salinity factor. Ecol Monogr 31:239–266

    Article  Google Scholar 

  • Wilkie EM, Bishop MJ, O’Connor WA (2013) The density and spatial arrangement of the invasive oyster Crassostrea gigas determines its impact on settlement of native oyster larvae. Ecol Evol 3:4851–4860

    Article  PubMed  PubMed Central  Google Scholar 

  • Wright JP, Jones CG (2006) The concept of organisms as ecosystem engineers 10 years on: progress, limitations, and challenges. Bioscience 56:203–209

    Article  Google Scholar 

Download references

Acknowledgements

We thank A. McAfee, M. Vozzo, L. Ainley, L. Burn, P. Vine and J. Davey for assistance with fieldwork, and are grateful to J. Long and two anonymous reviewers for improving the quality of the manuscript.

Funding

This research was funded by an Australian Research Council Discovery Grant DP150101363 to M. Bishop. D. McAfee was supported by an Australian Postgraduate Award and the Department of Biological Sciences, Macquarie University.

Author information

Authors and Affiliations

Authors

Contributions

DM and MB conceived and designed the experiments. DM performed the experiments. DM and MB analysed the data and wrote the manuscript.

Corresponding author

Correspondence to Dominic McAfee.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest. All applicable institutional and/or national guidelines for the care and use of animals were followed.

Additional information

Communicated by Jeremy Long.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 845 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

McAfee, D., Bishop, M.J. The mechanisms by which oysters facilitate invertebrates vary across environmental gradients. Oecologia 189, 1095–1106 (2019). https://doi.org/10.1007/s00442-019-04359-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-019-04359-3

Keywords

Navigation