Skip to main content

Advertisement

Log in

Ability of Eelgrass to Alter Oyster Growth and Physiology Is Spatially Limited and Offset by Increasing Predation Risk

  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

Marine foundation species have strong effects on sympatric species, but the strength may vary along environmental gradients. Climate change is shifting the distribution and magnitude of environmental gradients, making identification of when and where foundation species effects occur necessary for effective management. We reviewed existing work to identify expected mechanisms by which seagrass affect suspension feeding bivalves, then tested whether these effects shifted across estuarine conditions for two species of oysters (native Ostrea lurida and non-native Crassostrea gigas) grown in and out of eelgrass (Zostera marina) at six estuarine sites in Washington state. Hypothesized mechanisms of eelgrass influence include reduced predation pressure, reduced or altered food availability, and amelioration of environmental (pH) stress. We analyzed oyster survival, shell and tissue growth, shell strength, and stable isotope (SI) and fatty acid (FA) biomarkers. Oyster survival was > 20% lower in eelgrass at lower-estuary sites, but not up-estuary sites. Both species grew faster in eelgrass at one low-estuary (higher pH) site, but not elsewhere. Shell strength in eelgrass increased by 21.1% for native but decreased by 12.6% for non-native oysters. FA and SI biomarkers only differed in eelgrass at one site but correlated significantly to growth among individuals. No measurement showed a consistent response to eelgrass across estuarine conditions and taxa, and responses were often opposite of expectations based on published literature. These results have important implications for management and restoration of oysters in areas with eelgrass.

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

Similar content being viewed by others

References

  • Allen, B.J., and S.L. Williams. 2003. Native eelgrass Zostera marina controls growth and reproduction of an invasive mussel through food limitation. Marine Ecology Progress Series 254: 57–67.

    Article  Google Scholar 

  • Altieri, A.H., B.R. Silliman, M.D. Bertness, and Associate Editor: Marcel Holyoak, and Editor: Donald L. DeAngelis. 2007. Hierarchical organization via a facilitation cascade in intertidal cordgrass bed communities. The American Naturalist 169: 195–206.

    Article  Google Scholar 

  • Attrill, M.J. 2002. A testable linear model for diversity trends in estuaries. Journal of Animal Ecology 71 (2): 262–269.

    Article  Google Scholar 

  • Bates, D., M. Maechler, B. Bolker, and S. Walker. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1–48.

    Article  Google Scholar 

  • Baumann, H., and E.M. Smith. 2017. Quantifying metabolically driven pH and oxygen fluctuations in US nearshore habitats at diel to interannual time scales. Estuaries and Coasts.

  • Bible, J., K.R. Griffith, and E. Sanford. 2017. Inducible defenses in Olympia oysters in response to an invasive predator. Oecologia 183 (3): 809–819.

    Article  Google Scholar 

  • Bologna, P.A.X., and K.L. Heck. 1999. Differential predation and growth rates of bay scallops within a seagrass habitat. Journal of Experimental Marine Biology and Ecology 239 (2): 299–314.

    Article  Google Scholar 

  • Borges, A., and G. Abril. 2011. Carbon dioxide and methane dynamics in estuaries. Treatise on estuarine and coastal science. Biogeochemistry 5: 119–161.

  • Budge, S.M., E. Devred, M.-H. Forget, V. Stuart, M.K. Trzcinski, S. Sathyendranath, and T. Platt. 2014. Estimating concentrations of essential omega-3 fatty acids in the ocean: Supply and demand. ICES Journal of Marine Science 71 (7): 1885–1893. https://doi.org/10.1093/icesjms/fsu003.

    Article  Google Scholar 

  • Buhle, E.R., and J.L. Ruesink. 2009. Impacts of invasive oyster drills on Olympia oyster (Ostrea lurida Carpenter 1864) recovery in Willapa Bay, Washington, United States. Journal of Shellfish Research 28 (1): 87–96.

    Article  Google Scholar 

  • Callaway, R.M., R.W. Brooker, P. Choler, Z. Kikvidze, C.J. Lortie, R. Michalet, L. Paolini, F.I. Pugnaire, B. Newingham, E.T. Aschehoug, C. Armas, D. Kikodze, and B.J. Cook. 2002. Positive interactions among alpine plants increase with stress. Nature 417 (6891): 844–848.

    Article  CAS  Google Scholar 

  • Carroll, J.M., and B.J. Peterson. 2013. Ecological trade-offs in seascape ecology: Bay scallop survival and growth across a seagrass seascape. Landscape Ecology 28 (7): 1401–1413.

    Article  Google Scholar 

  • Chamberlain, S.A., J.L. Bronstein, and J.A. Rudgers. 2014. How context dependent are species interactions? Ecology Letters 17 (7): 881–890.

    Article  Google Scholar 

  • Cloern, J.E., A.D. Jassby, T.S. Schraga, E. Nejad, and C. Martin. 2017. Ecosystem variability along the estuarine salinity gradient: Examples from long-term study of San Francisco Bay. Limnology and Oceanography 62 (S1): S272–S291.

    Article  CAS  Google Scholar 

  • Dayton, P. K. 1972. Toward an understanding of community resilience and the potential effects of enrichments to the benthos at McMurdo Sound, Antarctica. Proceedings of the Colloquium on Conservation Problems in Antarctica, 81–95.

  • de Boer, W.F. 2007. Seagrass–sediment interactions, positive feedbacks and critical thresholds for occurrence: A review. Hydrobiologia 591 (1): 5–24.

    Article  CAS  Google Scholar 

  • Doi, H., F. Akamatsu, and A.L. González. 2017. Starvation effects on nitrogen and carbon stable isotopes of animals: An insight from meta-analysis of fasting experiments. Royal Society Open Science 4: 170633.

    Article  CAS  Google Scholar 

  • Duarte, C.M., Esther Benavent, and Maria del Carmen Sanchez. 1999. The microcosm of particles within seagrass Posidonia oceanica canopies. Marine Ecology Progress Series 181: 289–295.

    Article  Google Scholar 

  • Ellison, A.M., M.S. Bank, B.D. Clinton, E.A. Colburn, K. Elliott, C.R. Ford, D.R. Foster, B.D. Kloeppel, J.D. Knoepp, G.M. Lovett, J. Mohan, D.A. Orwig, N.L. Rodenhouse, W.V. Sobczak, K.A. Stinson, J.K. Stone, C.M. Swan, J. Thompson, B. Von Holle, and J.R. Webster. 2005. Loss of foundation species: Consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and the Environment 3: 479–486.

    Article  Google Scholar 

  • Galloway, A.W.., M.E. Eisenlord, M.N. Dethier, G.W. Holtgrieve, and M.T. Brett. 2014. Quantitative estimates of isopod resource utilization using a Bayesian fatty acid mixing model. Marine Ecology Progress Series 507: 219–232.

    Article  Google Scholar 

  • González-Ortiz, V., L.G. Egea, R. Jiménez-Ramos, F. Moreno-Marín, J.L. Pérez-Lloréns, T.J. Bouma, and F.G. Brun. 2014. Interactions between seagrass complexity, hydrodynamic flow and biomixing alter food availability for associated filter-feeding organisms. PLoS One 9: e104949.

    Article  CAS  Google Scholar 

  • Granata, T.C., T. Serra, J. Colomer, X. Casamitjana, C.M. Duarte, and E. Gacia. 2001. Flow and particle distributions in a nearshore seagrass meadow before and after a storm. Marine Ecology Progress Series 218: 95–106.

    Article  Google Scholar 

  • Grason, E.W., and E.R. Buhle. 2016. Comparing the influence of native and invasive intraguild predators on a rare native oyster. Journal of Experimental Marine Biology and Ecology 479: 1–8.

    Article  Google Scholar 

  • Gray, M. W., and C. J. Langdon. 2018. Ecophysiology of the Olympia oyster, Ostrea lurida, and Pacific oyster, Crassostrea gigas. Estuaries and Coasts 41: 521–535.

  • Hasegawa, N., M. Hori, and H. Mukai. 2008. Seasonal changes in eelgrass functions: Current velocity reduction, prevention of sediment resuspension, and control of sediment-water column nutrient flux in relation to eelgrass dynamics. Hydrobiologia 596: 387–399.

    Article  CAS  Google Scholar 

  • He, Q., and M.D. Bertness. 2014. Extreme stresses, niches, and positive species interactions along stress gradients. Ecology 95: 1437–1444.

    Article  Google Scholar 

  • He, Q., M.D. Bertness, and A.H. Altieri. 2013. Global shifts towards positive species interactions with increasing environmental stress. Ecology Letters 16: 695–706.

    Article  Google Scholar 

  • Hettinger, A., E. Sanford, T.M. Hill, A.D. Russell, K.N.S. Sato, J. Hoey, M. Forsch, H.N. Page, and B. Gaylord. 2012. Persistent carry-over effects of planktonic exposure to ocean acidification in the Olympia oyster. Ecology 93: 2758–2768.

    Article  Google Scholar 

  • Holsman, K.K., P.S. McDonald, and D.A. Armstrong. 2006. Intertidal migration and habitat use by subadult Dungeness crab Cancer magister in a NE Pacific estuary. Marine Ecology Progress Series 308: 183–195.

    Article  Google Scholar 

  • Irlandi, E.A., and C.H. Peterson. 1991. Modification of animal habitat by large plants: Mechanisms by which seagrasses influence clam growth. Oecologia 87: 307–318.

    Article  CAS  Google Scholar 

  • Jones, C.G., J.H. Lawton, and M. Shachak. 1997. Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78: 1946–1957.

    Article  Google Scholar 

  • Judge, M.L., L.D. Coen, and K.L. Heck. 1993. Does Mercenaria mercenaria encounter elevated food levels in seagrass beds? Results from a novel technique to collect suspended food resources. Marine Ecology Progress Series 92: 141–150.

    Article  Google Scholar 

  • Ko, G.W.K., R. Dineshram, C. Campanati, V.B.S. Chan, J. Havenhand, and V. Thiyagarajan. 2014. Interactive effects of ocean acidification, elevated temperature, and reduced salinity on early-life stages of the Pacific oyster. Environmental Science & Technology 48: 10079–10088.

    Article  CAS  Google Scholar 

  • Koweek, D.A., R.C. Zimmerman, K.M. Hewett, B. Gaylord, S.N. Giddings, K.J. Nickols, J.L. Ruesink, J.J. Stachowicz, Y. Takeshita, and K. Caldeira. 2018. Expected limits on the ocean acidification buffering potential of a temperate seagrass meadow. Ecological Applications 28: 1694–1714.

    Article  Google Scholar 

  • Langdon, C.J., and R.I.E. Newell. 1990. Utilization of detritus and bacteria as food sources by two bivalve suspension-feeders, the oyster Crassostrea virginica and the mussel Geukensia demissa. Marine Ecology Progress Series 58: 299–310.

    Article  Google Scholar 

  • Lebreton, B., P. Richard, R. Galois, G. Radenac, C. Pfléger, G. Guillou, F. Mornet, and G. Blanchard. 2011. Trophic importance of diatoms in an intertidal Zostera noltii seagrass bed: Evidence from stable isotope and fatty acid analysis. Estuarine, Coastal and Shelf Science 92: 140–153.

    Article  CAS  Google Scholar 

  • Lowe, A.T., A.W.E. Galloway, J.S. Yeung, M.N. Dethier, and D.O. Duggins. 2014. Broad sampling and diverse biomarkers allow characterization of nearshore particulate organic matter. Oikos 123: 1341–1354.

    Article  CAS  Google Scholar 

  • MacArthur, R.H. 1964. Environmental factors affecting bird diversity. American Naturalist 98: 387–397.

    Article  Google Scholar 

  • McDevitt-Irwin, J., J.C. Iacarella, and J.K. Baum. 2016. Reassessing the nursery role of seagrass habitats from temperate to tropical regions: A meta-analysis. Marine Ecology Progress Series 557: 133–143.

    Article  Google Scholar 

  • Muller-Navarra, D.C., M.T. Brett, A.M. Liston, and C.R. Goldman. 2000. A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature 403: 74–77.

    Article  CAS  Google Scholar 

  • Nakaoka, M. 2000. Nonlethal effects of predators on prey populations: Predator-mediated change in bivalve growth. Ecology 81: 1031–1045.

    Article  Google Scholar 

  • Nelson, T.A., and J.R. Waaland. 1997. Seasonality of eelgrass, epiphyte, and grazer biomass and productivity in subtidal eelgrass meadows subjected to moderate tidal amplitude. Aquatic Botany 56: 51–74.

    Article  Google Scholar 

  • Newton, J.A., and R.A. Horner. 2003. Use of phytoplankton species indicators to track the origin of phytoplankton blooms in Willapa Bay, Washington. Estuaries 26: 1071.

    Article  Google Scholar 

  • Nielsen, K., J. Stachowicz, H. Carter, K. Boyer, M. Bracken, F. Chan, F. Chavez, K. Hovel, M. Kent, K. Nickols, J. Ruesink, J. Tyburczy, and S. Wheeler. 2018. Emerging understanding of the potential role of seagrass and kelp as an ocean acidification management tool in California. Oakland: California Ocean Science Trust.

    Google Scholar 

  • Odum, W.E. 1984. Dual-gradient concept of detritus transport and processing in estuaries. Bulletin of Marine Science 35: 510–521.

    Google Scholar 

  • Oksanen, J., F. Guillaume Blanchet, R. Kindt, P. Legendre, P.R. Minchin, R.B. O’Hara, G.L. Simpson, P. Solymos, M.H.H. Stevens, and H. Wagner. 2013. R package version 2.0–8. Page Vegan: Community Ecology Package.

    Google Scholar 

  • Orth, R.J., K.L. Heck, and J. van Montfrans. 1984. Faunal communities in seagrass beds: A review of the influence of plant structure and prey characteristics on predator: Prey relationships. Estuaries 7: 339–350.

    Article  Google Scholar 

  • Pernet, F., R. Tremblay, L. Comeau, and H. Guderley. 2007. Temperature adaptation in two bivalve species from different thermal habitats: Energetics and remodelling of membrane lipids. Journal of Experimental Biology 210: 2999–3014.

    Article  Google Scholar 

  • Peterson, B.J., and B. Fry. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18 (1): 293–320.

    Article  Google Scholar 

  • Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar, and R Core Team. 2017. nlme: Linear and Nonlinear mixed effects models. R package version 3.1-137.

  • R Core Team. 2013. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

    Google Scholar 

  • Reusch, T.B.H. 1998. Differing effects of eelgrass Zostera marina on recruitment and growth of associated blue mussels Mytilus edulis. Marine Ecology Progress Series 167: 149–153.

    Article  Google Scholar 

  • Reusch, T.B.H., and S.L. Williams. 1999. Macrophyte canopy structure and the success of an invasive marine bivalve. Oikos 84: 398–416.

    Article  Google Scholar 

  • Richards, M.G., M. Huxham, and A. Bryant. 1999. Predation: A causal mechanism for variability in intertidal bivalve populations. Journal of Experimental Marine Biology and Ecology 241: 159–177.

    Article  Google Scholar 

  • Richoux, N.B., and R.T. Ndhlovu. 2015. Temporal variability in the isotopic niches of rocky shore grazers and suspension-feeders. Marine Ecology 36: 1045–1059.

    Article  CAS  Google Scholar 

  • Ruesink, J.L. 2016. Epiphyte load and seagrass performance are decoupled in an estuary with low eutrophication risk. Journal of Experimental Marine Biology and Ecology 481: 1–8.

    Article  Google Scholar 

  • Ruesink, J.L., G.C. Roegner, B.R. Dumbauld, J.A. Newton, and D.A. Armstrong. 2003. Contributions of coastal and watershed energy sources to secondary production in a Northeastern Pacific estuary. Estuaries 26: 1079–1093.

    Article  Google Scholar 

  • Ruesink, J., S. Yang, and Alan C. Trimble. 2015. Variability in carbon availability and eelgrass (Zostera marina) biometrics along an estuarine gradient in Willapa Bay, WA, USA. Estuaries and Coasts: 1–10.

  • Taipale, S.J., M.J. Kainz, and M.T. Brett. 2011. Diet-switching experiments show rapid accumulation and preferential retention of highly unsaturated fatty acids in Daphnia. Oikos 120: 1674–1682.

    Article  Google Scholar 

  • Timmins-Schiffman, E., W.D. Coffey, W. Hua, B.L. Nunn, G.H. Dickinson, and S.B. Roberts. 2014. Shotgun proteomics reveals physiological response to ocean acidification in Crassostrea gigas. BMC Genomics 15: 951.

    Article  CAS  Google Scholar 

  • Valdez, S.R., B. Peabody, B. Allen, B. Blake, and J.L. Ruesink. 2017. Experimental test of oyster restoration within eelgrass. Aquatic Conservation: Marine and Freshwater Ecosystems 27: 578–587.

    Article  Google Scholar 

  • Wahl, M., S. Schneider Covachã, V. Saderne, C. Hiebenthal, J.D. Müller, C. Pansch, and Y. Sawall. 2018. Macroalgae may mitigate ocean acidification effects on mussel calcification by increasing pH and its fluctuations. Limnology and Oceanography 63: 3–21.

    Article  CAS  Google Scholar 

  • Waldbusser, G.G., B. Hales, C.J. Langdon, B.A. Haley, P. Schrader, E.L. Brunner, M.W. Gray, C.A. Miller, and I. Gimenez. 2015. Saturation-state sensitivity of marine bivalve larvae to ocean acidification. Nature Climate Change 5: 273–280.

    Article  CAS  Google Scholar 

  • Waldbusser, G.G., M.W. Gray, B. Hales, C.J. Langdon, B.A. Haley, I. Gimenez, S.R. Smith, E.L. Brunner, and G. Hutchinson. 2016. Slow shell building, a possible trait for resistance to the effects of acute ocean acidification. Limnology and Oceanography. 61 (6): 1969–1983.

    Article  CAS  Google Scholar 

  • Wilkie, E.M., and M.J. Bishop. 2012. Differences in shell strength of native and non-native oysters do not extend to size classes that are susceptible to a generalist predator. Marine and Freshwater Research 63: 1201–1205.

    Article  Google Scholar 

  • Winder, M., J. Carstensen, A.W.E. Galloway, H.H. Jakobsen, and J.E. Cloern. 2017. The land–sea interface: A source of high-quality phytoplankton to support secondary production. Limnology and Oceanography 62: S258–S271.

    Article  Google Scholar 

  • Wright, J.M., L.M. Parker, W.A. O’Connor, M. Williams, P. Kube, and P.M. Ross. 2014. Populations of Pacific oysters Crassostrea gigas respond variably to elevated CO2 and predation by Morula marginalba. The Biological Bulletin 226: 269–281.

    Article  Google Scholar 

  • Zuur, A.F., E.N. Ieno, N. Walker, A.A. Saveliev, and G.M. Smith. 2009. Mixed effects models and extensions in ecology with R. New York: Springer.

    Book  Google Scholar 

Download references

Acknowledgments

This work could not have been completed without the field and lab assistance of A. Lee, M. Payne, J. Aspée, H. Hayford, S. Von Reis, P. Stamp, and A. Trimble. We thank B. Taylor and Taylor Shellfish for providing oysters and the Padilla Bay National Estuarine Research Reserve (NERR) staff for field and logistical support. M. Dethier, C. Gross, and M. Turner provided valuable feedback on the manuscript. This work was authorized by Washington Fish and Wildlife Shellfish transfer permit no. 15-1105.

Funding

Funding for this research was provided by the Padilla Bay NERR Assistantship and Washington Department of Natural Resources.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alexander T. Lowe.

Additional information

Communicated by Henrique Cabral

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lowe, A.T., Kobelt, J., Horwith, M. et al. Ability of Eelgrass to Alter Oyster Growth and Physiology Is Spatially Limited and Offset by Increasing Predation Risk. Estuaries and Coasts 42, 743–754 (2019). https://doi.org/10.1007/s12237-018-00488-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-018-00488-9

Keywords

Navigation