Ability of Eelgrass to Alter Oyster Growth and Physiology Is Spatially Limited and Offset by Increasing Predation Risk
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.
KeywordsFoundation species Habitat modification Food availability Ocean acidification Stable isotopes Fatty acids Ostrea lurida Crassostrea gigas Oysters
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 for this research was provided by the Padilla Bay NERR Assistantship and Washington Department of Natural Resources.
- 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. 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.Google Scholar
- 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.CrossRefGoogle 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.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.CrossRefGoogle 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.CrossRefGoogle 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.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.CrossRefGoogle 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.CrossRefGoogle 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
- 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.Google Scholar
- R Core Team. 2013. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.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.Google Scholar