Skip to main content

Advertisement

Log in

Upstream—Downstream Shifts in Peak Recruitment of the Native Olympia Oyster in San Francisco Bay During Wet and Dry Years

  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

Understanding the conditions that drive variation in recruitment of key estuarine species can be important for effective conservation and management of their populations. The Olympia oyster (Ostrea lurida) is native to the Pacific coast of North America and has been a target of conservation efforts, though relatively little information on larval recruitment exists across much of its range. This study examined the recruitment of Olympia oysters at biweekly to monthly intervals at four sites in northern San Francisco Bay from 2010 to 2015 (except 2013). Mean monthly temperatures warmed at all sites during the study, while winter (January–April) mean monthly salinity decreased significantly during a wet year (2011), but otherwise remained high as a result of a drought. A recurring peak in oyster recruitment was identified in mid-estuary, in conditions corresponding to a salinity range of 25–30 and >16 °C at the time of settlement (April–November). Higher average salinities and temperatures were positively correlated with greater peak recruitment. Interannual variation in the timing of favorable conditions for recruitment at each site appears to explain geographic and temporal variation in recruitment onset. Higher winter/spring salinities and warmer temperatures at the time of recruitment corresponded with earlier recruitment onset within individual sites. Across all sites, higher winter/spring salinities were also correlated with earlier onset and earlier peak recruitment. Lower winter salinities during 2011 also resulted in a downstream shift in the location of peak recruitment.

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
Fig. 7
Fig. 8

Similar content being viewed by others

References

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

    Article  Google Scholar 

  • Baker, P. 1995. Review of ecology and fishery of the Olympia oyster, Ostrea lurida with annotated bibliography. Journal of Shellfish Research 14: 501–518.

    Google Scholar 

  • Bates, D., Maechler, M., Bolker, B., and S. Walker. 2015. lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-8. Available at: http://CRAN.R-project.org/package=lme4>.

  • Bennett, W.A., W.J. Kimmerer, and J.R. Burau. 2002. Plasticity in vertical migration by native and exotic estuarine fishes in a dynamic low-salinity zone. Limnology and Oceanography 47: 1496–1507.

    Article  Google Scholar 

  • Berg, N., and A. Hall. 2015. Increased interannual precipitation extremes over California under climate change. Journal of Climate 28: 6324–6334.

    Article  Google Scholar 

  • Bolker, B.M., B. Gardner, M. Maunder, C.W. Berg, M. Brooks, L. Comita, E. Crone, S. Cubaynes, T. Davies, P. de Valpine, J. Ford, O. Gimenez, M. Kéry, E.J. Kim, C. Lennert-Cody, A. Magnusson, S. Martell, J. Nash, A. Nielsen, J. Regetz, H. Skaug, and E. Zipkin. 2013. Strategies for fitting nonlinear ecological models in R, AD model builder, and BUGS. Methods in Ecology and Evolution 4: 501–512.

    Article  Google Scholar 

  • Bonnot, P. 1937. Report on the California oyster industry for 1937. California Fish and Game, 42.

  • Bousfield, E.L. 1955. Ecological control of the occurrence of barnacles in the Miramichi estuary. Bulletin of the National Museum of Canada 137: 1–69.

    Google Scholar 

  • Broitman, B.R., C.A. Blanchette, B.A. Menge, J. Lubchenco, C. Krenz, M. Foley, P.T. Raimondi, D. Lohse, and S.D. Gaines. 2008. Spatial and temporal patterns of invertebrate recruitment along the west coast of the United States. Ecological Monographs 78: 403–421.

    Article  Google Scholar 

  • Buskey, E.J., M. Bundy, M. Ferner, D. Porter, W. Reay, E. Smith, and D. Trueblood. 2015. System-wide monitoring program of the National Estuarine Research Reserve system: research and monitoring to address coastal management issues. In Coastal Ocean observing systems: advances and syntheses, ed. Y. Liu, H. Kerkering, and R.H. Weisberg, 392–414. The Netherlands: Elsevier.

    Chapter  Google Scholar 

  • Carriker, M.R. 1951. Ecological observations on the distribution of oyster larvae in New Jersey estuaries. Ecological Monographs 21: 19–38.

    Article  Google Scholar 

  • Carson, H.S. 2010. Population connectivity of the Olympia oyster in southern California. Limnology and Oceanography 55: 134–148.

    Article  CAS  Google Scholar 

  • Cloern, J.E., and A.D. Jassby. 2012. Drivers of change in estuarine-coastal ecosystems: discoveries from four decades of study in San Francisco Bay. Reviews in Geophysics 50: RG4001.

    Article  Google Scholar 

  • Cloern, J.E., N. Knowles, L.R. Brown, D. Cayan, M.D. Dettinger, T.L. Morgan, D.H. Schoellhamer, M.T. Stacey, M. van der Wegen, R.W. Wagner, and A.D. Jassby. 2011. Projected evolution of California’s San Francisco Bay-Delta-river system in a century of climate change. PloS One 6: e24465.

    Article  CAS  Google Scholar 

  • Coe, W.R. 1931. Development of the organs and the sequence of the sexual phases in the California oyster (Ostrea lurida). Bulletin of Shellfish 3: 119–139.

    Google Scholar 

  • Conomos, T.J. 1979. Properties and circulation of San Francisco Bay waters. In San Francisco Bay: the urbanized estuary, ed. T.J. Conomos, 47–84. San Francisco, California: Pacific Division of the American Association for the Advancement of Science.

    Google Scholar 

  • Conomos, T.J., R.E. Smith, and J.W. Gartner. 1985. Environmental setting of San Francisco Bay. Hydrobiologia 129: 1–12.

    Article  Google Scholar 

  • Crisp, D.J. 1976. Settlement responses in marine organisms. In Adaptation to environment: essays on the physiology of marine animals, ed. R.C. Newell, 83–124. London: Butterworths.

    Chapter  Google Scholar 

  • Das, T., E.P. Maurer, D.W. Pierce, M.D. Dettinger, and D.R. Cayan. 2013. Increases in flood magnitudes in California under warming climates. Journal of Hydrology 501: 101–110.

    Article  Google Scholar 

  • Diffenbaugh, N.S., D.L. Swain, and D. Touma. 2015. Anthropogenic warming has increased drought risk in California. Proceedings of the National Academy of Sciences of the United States of America 112: 3931–3936.

    Article  CAS  Google Scholar 

  • Forward, R.B. Jr., and R.A. Tankersley. 2001. Selective tidal-stream transport of marine animals. In Oceanography and marine biology, ed. R.B. Gibson, M. Barnes, and R.J.A. Atkinson, 305–353. London: Taylor & Francis.

    Google Scholar 

  • Fournier, D.A., H.J. Skaug, J. Ancheta, J. Ianelli, A. Magnusson, M.N. Maunder, A. Nielsen, and J. Sibert. 2012. AD model builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optimization Methods and Software 27: 233–249.

    Article  Google Scholar 

  • Fuchs, H.L., and M.A. Reidenbach. 2013. Biophysical constraints on optimal patch lengths for settlement of a reef-building bivalve. PloS One 8: e71506. doi:10.1371/journal.pone.0071506.

    Article  CAS  Google Scholar 

  • Gaines, S.D., and M.D. Bertness. 1992. Dispersal of juveniles and variable recruitment in sessile marine species. Nature 360: 579–580.

    Article  Google Scholar 

  • Gilman, S.E., C.D. Harley, D.C. Strickland, O. Vanderstraeten, M.J. O'Donnell, and B. Helmuth. 2006. Evaluation of effective shore level as a method of characterizing intertidal wave exposure regimes. Limnology and Oceanography: Methods 4: 448–457.

    Article  Google Scholar 

  • Graham, W.M., and J. Largier. 1997. Upwelling shadows as nearshore retention sites: the example of northern Monterey Bay. Continental Shelf Research 17: 509–532.

    Article  Google Scholar 

  • Grosholz, E., Moore, J., Zabin, C., Attoe, S. and Obernolte, R. 2007. Planning for native oyster restoration in San Francisco Bay. Final Report to California Coastal Conservancy. 40 pp.

  • Gyory, J., J. Pineda, and A. Solow. 2013. Turbidity triggers larval release by the intertidal barnacle Semibalanus balanoides. Marine Ecology Progress Series 476: 141–151.

    Article  Google Scholar 

  • Harley, C.D., A. Randall Hughes, K.M. Hultgren, B.G. Miner, C.J. Sorte, C.S. Thornber, L.F. Rodriguez, L. Tomanek, and S.L. Williams. 2006. The impacts of climate change in coastal marine systems. Ecology Letters 9: 228–241.

    Article  Google Scholar 

  • Hopkins, A.E. 1935. Attachment of larvae of the Olympia oyster, Ostrea lurida, to plane surfaces. Ecology 16: 82–87.

    Article  Google Scholar 

  • Hopkins, A.E. 1936. Ecological observations on spawning and early larval development in the Olympia oyster (Ostrea lurida). Ecology 17: 551–566.

    Article  Google Scholar 

  • Hopkins, A.E. 1937. Experimental observations on spawning, larval development, and setting in the Olympia oyster Ostrea lurida. Bulletin of the U.S. Bureau of Fisheries 48: 438–503.

    Google Scholar 

  • Ketchum, B.H. 1954. Relation between circulation and planktonic populations in estuaries. Ecology 35: 191–200.

    Article  Google Scholar 

  • Kimbro, D.L., and E.D. Grosholz. 2006. Disturbance influences oyster community richness and evenness, but not diversity. Ecology 87: 2378–2388.

    Article  Google Scholar 

  • Koehl, M.A., and M.G. Hadfield. 2010. Hydrodynamics of larval settlement from a larva's point of view. Integrative and Comparative Biology 50: 539–551.

    Article  CAS  Google Scholar 

  • Kunze, H.B., S.G. Morgan, and K.M.M. Lwiza. 2013. A field test of the behavioral regulation of larval transport. Marine Ecology Progress Series 487: 71–87.

    Article  Google Scholar 

  • Leslie, H.M., E.N. Breck, F. Chan, J. Lubchenco, and B.A. Menge. 2005. Barnacle reproductive hotspots linked to nearshore ocean conditions. Proceedings of the National Academy of Sciences of the United States of America 102: 10534–10539.

    Article  CAS  Google Scholar 

  • Mace, A.J., and S.G. Morgan. 2006. Larval accumulation in the lee of a small headland: implications for the design of marine reserves. Marine Ecology Progress Series 318: 19–29.

    Article  Google Scholar 

  • Morgan, S.G., J.L. Fisher, and J.L. Largier. 2011. Larval retention, entrainment, and accumulation in the lee of a small headland: recruitment hotspots along windy coasts. Limnology and Oceanography 56: 161–178.

    Article  Google Scholar 

  • Morgan, S.G., J.L. Fisher, S.T. McAfee, J.L. Largier, and C.M. Halle. 2012. Limited recruitment during relaxation events: larval advection and behavior in an upwelling system. Limnology and Oceanography 57: 457–470.

    Article  Google Scholar 

  • National Estuarine Research Reserve System. 2015. System-wide monitoring program. Available at: http://www.nerrsdata.org/. Accessed 1 Dec 2015.

  • Neelin, J.D., B. Langenbrunner, J.E. Meyerson, A. Hall, and N. Berg. 2013. California winter precipitation change under global warming in the coupled model Intercomparison project phase 5 ensemble. Journal of Climate 26: 6238–6256.

    Article  Google Scholar 

  • Newman, W.A. 1953. Some ecological considerations on Barnacles of the San Francisco Bay Estuarine System. MA Thesis. University of California, Berkeley, California.

  • Nichols, F.H., J.E. Cloern, S.N. Luoma, and D.H. Peterson. 1986. The modification of an estuary. Science 231: 567–573.

    Article  CAS  Google Scholar 

  • Pawlik, J.R. 1992. Chemical ecology of the settlement of benthic marine invertebrates. Oceanography and Marine Biology: An Annual Review 30: 273–335.

    Google Scholar 

  • Peteiro, L., and A. Shanks. 2015. Up and down or how to stay in the bay: retentive strategies of Olympia oyster larvae in a shallow estuary. Marine Ecology Progress Series 530: 103–117.

    Article  Google Scholar 

  • Polson, M.P., and D.C. Zacherl. 2009. Geographic distribution and intertidal population status for the Olympia oyster, Ostrea lurida carpenter 1864, from Alaska to Baja. Journal of Shellfish Research 28: 69–77.

    Article  Google Scholar 

  • Prairie, J.C., K.R. Sutherland, K.J. Nickols, and A.M. Kaltenberg. 2012. Biophysical interactions in the plankton: a cross-scale review. Limnology and Oceanography: Fluids and Environments 2: 121–145.

    Google Scholar 

  • Pritchard, C., A. Shanks, R. Rimler, M. Oates, and S. Rumrill. 2015. The Olympia oyster Ostrea lurida: recent advances in natural history, ecology, and restoration. Journal of Shellfish Research 34: 259–271.

    Article  Google Scholar 

  • R Core Team. 2015. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Available at: http://www.r-project.org/.

  • Raith, M., D.C. Zacherl, E.M. Pilgrim, and D.J. Eernisse. 2016. Phylogeny and species diversity of gulf of California oysters (Ostreidae) inferred from mitochondrial DNA. American Malacological Bulletin 33: 263–283.

    Article  Google Scholar 

  • Remane, A., and C. Schlieper. 1971. Biology of brackish water. Stuttgart: Schweizerbart'sche Verlagsbuchhandlung.

    Google Scholar 

  • Roughan, M., A.J. Mace, J.L. Largier, S.G. Morgan, J.L. Fisher, and M.L. Carter. 2005. Subsurface recirculation and larval retention in the lee of a small headland: a variation on the upwelling shadow theme. Journal of Geophysical Research 110: C10027. doi:10.1029/2005JC002898.

    Article  Google Scholar 

  • Seager, R., M. Hoerling, S. Schubert, H. Wang, B. Lyon, A. Kumar, J. Nakamura, and N. Henderson. 2015. Causes of the 2011–14 California drought. Journal of Climate 28: 6997–7024.

    Article  Google Scholar 

  • Seale, E.M., and D.C. Zacherl. 2009. Seasonal settlement of Olympia oyster larvae, Ostrea lurida carpenter 1864 and its relationship to seawater temperature in two southern California estuaries. Journal of Shellfish Research 28: 113–120.

    Article  Google Scholar 

  • Skaug, H., Fournier, D., Bolker, B., Magnusson, A. and A. Nielsen. 2015. Generalized Linear Mixed Models using AD Model Builder. R package version 0.8.0. Available at: http://CRAN.R-project.org/package=vegan.

  • Southward, A.J., S.J. Hawkins, and M.T. Burrows. 1995. Seventy years' observations of changes in distribution and abundance of zooplankton and intertidal organisms in the western English Channel in relation to rising sea temperature. Journal of Thermal Biology 20: 127–155.

    Article  Google Scholar 

  • Starr, M., J.H. Himmelman, and J.C. Therriault. 1990. Direct coupling of marine invertebrate spawning with phytoplankton blooms. Science 247: 1071–1074.

    Article  CAS  Google Scholar 

  • Strathmann, M.F. 1987. Reproduction and development of marine invertebrates of the northern Pacific coast: data and methods for the study of eggs, embryos, and larvae. University of Washington Press.

  • Swain, D.L. 2015. A tale of two California droughts: lessons amidst record warmth and dryness in a region of complex physical and human geography. Geophysical Research Letters 42. doi:10.1002/2015GL066628.

  • Trimble, A.C., J.L. Ruesink, and B.R. Dumbauld. 2009. Factors preventing the recovery of a historically overexploited shellfish species, Ostrea lurida carpenter 1864. Journal of Shellfish Research 28: 97–106.

    Article  Google Scholar 

  • United States Geological Survey. 2015. Water quality data for San Francisco Bay. Available at: http://waterdata.usgs.gov/. Accessed 1 Dec 2015.

  • Wasson, K., Zabin, C., Bible, J., Ceballos, E., Chang, A., Cheng, B., Deck, A., Grosholz, E., Latta, M. and M. Ferner. 2014. A guide to Olympia oyster restoration and conservation: environmental conditions and sites that support sustainable populations in Central California. San Francisco Bay National Estuarine Research Reserve.

  • Wing, S.R., L. Botsford, L.E. Morgan, J.M. Diehl, and C.J. Lundquist. 2003. Inter-annual variability in larval supply to populations of three invertebrate taxa in the northern California current. Estuarine, Coastal and Shelf Science 57: 859–872.

    Article  Google Scholar 

  • Yoon, J.H., S.Y. Wang, R.R. Gillies, B. Kravitz, L. Hipps, and P.J. Rasch. 2015. Increasing water cycle extremes in California and in relation to ENSO cycle under global warming. Nature Communications 6: 8657.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by postdoctoral fellowships to ALC from the CALFED Bay-Delta Authority (R/SF-33) and the Smithsonian Institution, the National Estuarine Research Reserve System Science Collaborative (NOAA grant no. NA09NOS4190153 to MCF), and an award under the Federal Coastal Zone Management Act, administered by the National Oceanic and Atmospheric Administration’s Office for Coastal Management to San Francisco State University for operation of the San Francisco Bay National Estuarine Research Reserve. The authors would like to express sincere gratitude to the Dominican University of California (San Rafael, CA) Invertebrate Zoology (BIO3150, Fall 2011) and Aquatic Ecosystems (HONO3200, Spring 2012, 2013, 2014, and 2016) classes taught by LJS for their devoted counting of oyster recruitment tiles.

Author Contributions

ALC, SGM, and MCF obtained funding; ALC, AKD, SGM, and MCF designed the research; ALC, AKD, LJS, and MCF performed the work; ALC analyzed the data; and ALC, AKD, LJS, SGM, and MCF wrote the paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrew L. Chang.

Additional information

Communicated by Judy Grassle

Electronic Supplementary Material

ESM 1

(DOCX 567 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chang, A.L., Deck, A.K., Sullivan, L.J. et al. Upstream—Downstream Shifts in Peak Recruitment of the Native Olympia Oyster in San Francisco Bay During Wet and Dry Years. Estuaries and Coasts 41, 65–78 (2018). https://doi.org/10.1007/s12237-016-0182-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-016-0182-1

Keywords

Navigation