Skip to main content
SpringerLink
Log in

Relative Impacts of Natural Stressors on Life History Traits Underlying Resilience of Intertidal Eelgrass (Zostera marina L.)

  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

Seagrasses are a critical marine habitat and are in decline worldwide. Previous studies have demonstrated that factors such as sediment conditions, resource availability, and desiccation can influence life history transitions and morphology in intertidal eelgrass (Zostera marina L.) and therefore potential for recovery after a disturbance. We combined these factors in an exploratory path model linking environmental conditions to eelgrass vegetative (shoot size and density) and reproductive traits (branching, flowering, seedling recruitment). In this construction, significant path coefficients reveal factors influencing recovery potential. To test the path model, we collected abiotic and eelgrass data at 17 sites in the southern Salish Sea (Washington, USA) and assessed model fit with structural equation modeling. Significant path coefficients linked sediment organic content to shoot size and seedling recruitment, tidal amplitude to reduced flowering, and shoot size and density were inversely correlated. We found no significant links between any morphological or life history trait and nutrient availability, possibly reflecting consistently high nutrients across sites. Variable rates of asexual reproduction and a trade-off between shoot size and density may reflect light limitation in eelgrass’ intertidal range, where light is not expected to be strongly limiting. Overall, structural equation modeling identified organic-rich sediments as relatively more important than desiccation and nutrient conditions for resilience potential of intertidal eelgrass populations in this region. Life history and morphological traits provide eelgrass with recovery mechanisms from disturbance where sediments are muddy, which has implications for both conservation and restoration.

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

Similar content being viewed by others

References

  • Backman, T.W.H. 1991. Genotypic and phenotypic variability of Zostera marina on the west coast of North America. Canadian Journal of Botany 69: 1361–1371.

    Article  Google Scholar 

  • Baden, S.P., and C. Boström. 2001. The leaf canopy of seagrass beds: faunal community structure and function in a salinity gradient along the Swedish coast. In Ecological Comparisons of Sedimentary Shores, ed. K. Reise. Ecological Studies 151: 213–236.

  • Barko, J.W., and R.M. Smart. 1983. Effects of organic matter additions to sediment on the growth of aquatic plants. Journal of Ecology 71: 161–175.

    Article  CAS  Google Scholar 

  • Berry, H.D., A.T. Sewell, S. Wyllie-Echeverria, B.R. Reeves, T.F. Mumford, Jr., J.R. Skalski, R.C. Zimmerman, and J. Archer. 2003. Puget sound submerged vegetation monitoring project: 2000-2002 monitoring report. Nearshore Habitat Program, Washington State Department of Resources. Olympia, WA. 60 pp. plus appendices.

  • Boese, B.L., and B.D. Robbins. 2008. Effects of erosion and macroalgae on intertidal eelgrass (Zostera marina) in a northeastern Pacific estuary (USA). Botanica Marina 51: 247–257.

    Article  Google Scholar 

  • Boese, B.L., J.E. Kaldy, P.J. Clinton, P.M. Eldridge, and C.L. Folger. 2009. Recolonization of intertidal Zostera marina L. (eelgrass) following experimental shoot removal. Journal of Experimental Marine Biology and Ecology 374(1): 69–77.

    Article  Google Scholar 

  • Burkholder, J.M., D.A. Tomasko, and B.W. Touchette. 2007. Seagrasses and eutrophication. Journal of Experimental Marine Biology and Ecology 350(1–2): 46–72.

    Article  Google Scholar 

  • Dennison, W.C., and R.S. Alberte. 1985. Role of daily light period in the depth distribution of Zostera marina (eelgrass). Marine Ecology Progress Series 25: 51–61.

    Article  Google Scholar 

  • Duarte, C.M. 1990. Seagrass nutrient content. Marine Ecology Progress Series 67: 201–207.

    Article  Google Scholar 

  • Duarte, C.M. 1991. Allometric scaling of seagrass form and productivity. Marine Ecology Progress Series 77: 289–300.

    Article  Google Scholar 

  • Duffy, J.E. 2006. Biodiversity and functioning of seagrass ecosystems. Marine Ecology Progress Series 311: 233–250.

    Article  Google Scholar 

  • Ferdie, M., and J.W. Fourqurean. 2004. Responses of seagrass communities to fertilization along a gradient of relative availability of nitrogen and phosphorus in a carbonate environment. Limnology and Oceanography 49: 2082–2094.

    Article  Google Scholar 

  • Gaeckle, J., P. Dowty, H. Berry, and L. Ferrier. 2011. Puget Sound Submerged Vegetation Monitoring Project 2009 Monitoring Report. Nearshore Habitat Program, Washington State Department of Natural Resources. Olympia, WA. 56 pp. plus appendices.

  • Grace, J.B. 2006. Structural equation modeling and natural systems. New York: Cambridge University Press.

    Book  Google Scholar 

  • Gray, J.S., and M. Elliott. 2009. Ecology of marine sediments: from science to management, 2nd ed, 22–27. New York: Oxford University Press.

    Google Scholar 

  • Greve, T.M., D. Krause-Jensen, M.B. Rasmusson, and P.B. Christensen. 2005. Means of rapid eelgrass (Zostera marina L.) recolonisation in former dieback areas. Aquatic Botany 82: 143–156.

    Article  Google Scholar 

  • Harrison, P.G. 1993. Variations in demography of Zostera marina and Z. noltii on an intertidal gradient. Aquatic Botany 45: 63–77.

    Article  Google Scholar 

  • Harwell, M.C., and R.J. Orth. 1999. Eelgrass (Zostera marina L.) seed protection for field experiments and implications for large-scale restoration. Aquatic Botany 64: 51–61.

    Article  Google Scholar 

  • Hauxwell, J., J. Cebrian, and I. Valiela. 2006. Light dependence of Zostera marina annual growth dynamics in estuaries subject to different degrees of eutrophication. Aquatic Botany 84(1): 17–25.

    Article  Google Scholar 

  • Hessing-Lewis, M.L., S.D. Hacker, B.A. Menge, and S.S. Rumrill. 2011. Context-dependent eelgrass-macroalgae interactions along an estuarine gradient in the Pacific Northwest, USA. Estuar. Coast. 34: 1169–1181.

    Article  Google Scholar 

  • Hooper, D., J. Coughlan, and M.R. Mullen. 2008. Structural equation modelling: guidelines for determining model fit. The Electronic Journal of Business Research Methods. 6(1): 53–60.

    Google Scholar 

  • Hu, L., and P.M. Bentler. 1999. Cutoff criteria for fit indexes in covariance structure analysis: conventional criteria versus new alternatives. Structural Equation Modeling: A Multidisciplinary Journal. 6(1): 1–55.

    Article  Google Scholar 

  • Hughes, A.R., S.L. Williams, C.M. Duarte, K.L. Heck Jr., and M. Waycott. 2009. Associations of concern: declining seagrasses and threatened dependent species. Frontiers in Ecology and the Environment 7: 242–246.

    Article  Google Scholar 

  • Jarvis, J.C., and K.A. Moore. 2010. The role of seedlings and seed bank viability in the recovery of Chesapeake Bay, USA, Zostera marina populations following a large-scale decline. Hydrobiologia 649: 55–68.

    Article  Google Scholar 

  • Kaldy, J. 2009. Water column and sediment nutrients as limits to growth of Zostera marina and Thalassia testudinum. In Seagrasses and protective criteria: A review and assessment of research status, ed. W.G. Nelson. Washington, D.C: Office of Research and Development, National Health and Environmental Effects Research Laboratory, EPA/600/R-09/050.

    Google Scholar 

  • Kentula, M.E., and C.D. McIntire. 1986. The autecology and production dynamics of eelgrass (Zostera marina L) in Netarts Bay, Oregon. Estuaries 9(3): 188–199.

    Article  Google Scholar 

  • Koch, E.W. 2001. Beyond light: physical, geological, and geochemical parameters as possible submersed aquatic vegetation habitat requirements. Estuaries 24: 1–17.

    Article  Google Scholar 

  • Koch, E.W., J.D. Ackerman, J. Verduin, and M. van Keulen. 2006. Fluid dynamics in seagrass ecology—from molecules to ecosystems. In Seagrasses: Biology, ecology and conservation, ed. A.W.D. Larkum, R.J. Orth, and C.M. Duarte, 193–225. Dordrecht: Springer.

    Chapter  Google Scholar 

  • Marion, S.R., and R.J. Orth. 2012. Seedling establishment in eelgrass: seed burial effects on winter losses of developing seedlings. Marine Ecology Progress Series 448: 197–207.

    Article  Google Scholar 

  • Marbà, N., and C.M. Duarte. 1998. Rhizome elongation and seagrass clonal growth. Marine Ecology Progress Series 174: 269–280.

    Article  Google Scholar 

  • Marbà, N., M. Holmer, E. Gacia, and C. Barròn. 2006. Seagrass beds and coastal biogeochemistry. In Seagrasses: Biology, ecology and conservation, ed. A.W.D. Larkum, R.J. Orth, and C.M. Duarte, 135–157. Dordrecht: Springer.

    Chapter  Google Scholar 

  • Moore, K.A., R.J. Orth, and J.F. Nowak. 1993. Environmental regulation of seed germination in Zostera marina L. (eelgrass) in Chesapeake Bay: effects of light, oxygen and sediment burial. Aquatic Botany 45: 79–91.

    Article  Google Scholar 

  • Moore, K.A., and F.T. Short. 2006. Zostera: Biology, ecology, and management. In Seagrasses: Biology, ecology and conservation, ed. A.W.D. Larkum, R.J. Orth, and C.M. Duarte, 361–386. Dordrecht: Springer.

    Chapter  Google Scholar 

  • Nixon, S., B. Buckley, S. Granger, and J. Bintz. 2001. Responses of very shallow marine ecosystems to nutrient enrichment. Human Ecological Risk Assessment 7(5): 1457–1481.

    Article  Google Scholar 

  • Olesen, B., and K. Sand-Jensen. 1994. Biomass-density patterns in the temperate seagrass Zostera marina. Marine Ecology Progress Series 109: 283–291.

    Article  Google Scholar 

  • Olesen, B. 1999. Reproduction in Danish eelgrass (Zostera marina L.) stands: size-dependence and biomass partitioning. Aquatic Botany 65: 209–219.

    Article  Google Scholar 

  • Olesen, B., N. Marbà, C.M. Duarte, R.S. Savela, and M.D. Fortes. 2004. Recolonization dynamics in a mixed seagrass meadow: the role of clonal versus sexual processes. Estuaries 27: 770–780.

    Article  Google Scholar 

  • Orth, R.J., T.J.B. Carruthers, W.C. Dennison, C.M. Duarte, J.W. Fourqurean, K.L. Heck Jr., A.R. Hughes, G.A. Kendrick, W.J. Kenworthy, S. Olyarnik, F.T. Short, M. Waycott, and S.L. Williams. 2006. A global crisis for seagrass ecosystems. BioScience 56: 987–996.

    Article  Google Scholar 

  • Orth, R.J., K.A. Moore, S.R. Marion, D.J. Wilcox, and D.B. Parrish. 2012. Seed addition facilitates eelgrass recovery in a coastal bay system. Marine Ecology Progress Series 448: 177–195.

    Article  Google Scholar 

  • Phillips, R.C., W.E. Grant, and C.P. McRoy. 1983. Reproductive strategies of eelgrass (Zostera marina L.). Aquatic Botany 16: 1–20.

    Article  Google Scholar 

  • Phillips, R.C., and E.G. Meñez. 1988. Seagrasses. Smithsonian contributions to the marine science series, no. 34. Washington, D.C.: Smithsonian Institution Press.

    Google Scholar 

  • Plus, M., J.M. Deslous-Paoli, and F. Dagault. 2003. Seagrass (Zostera marina L.) bed recolonisation after anoxia-induced full mortality. Aquatic Botany 77: 121–134.

    Article  Google Scholar 

  • R Development Core Team. 2011. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.

  • Roberts Jr., M.H., R.J. Orth, and K.A. Moore. 1984. Growth of Zostera marina L. seedlings under laboratory conditions of nutrient enrichment. Aquatic Botany 20: 321–328.

    Article  Google Scholar 

  • Rosseel, Y., D. Oberski, and J. Byrnes. 2011. lavaan: Latent variable analysis. R package version 0.4-10. http://CRAN.R-project.org/package=lavaan.

  • Ruesink, J.L., J.S. Hong, L. Wisehart, S.D. Hacker, B.R. Dumbauld, M. Hessing-Lewis, and A.C. Trimble. 2010. Congener comparison of native (Zostera marina) and introduced (Z. japonica) eelgrass at multiple scales within a Pacific Northwest estuary. Biological Invasions 12: 1773–1789.

    Article  Google Scholar 

  • Ruesink, J.L., J.P. Fitzpatrick, B.R. Dumbauld, S.D. Hacker, A.C. Trimble, E.L. Wagner, and L.M. Wisehart. 2012. Life history and morphological shifts in an intertidal seagrass following multiple disturbances. Journal of Experimental Marine Biology and Ecology 424–425: 25–31.

    Article  Google Scholar 

  • Schanz, A., H. Julich, L. Ferrier, and H. Berry. 2010. Eelgrass stressor-response report 2007–2008: Zostera marina L. (eelgrass) transplant growth and survival along a spatial and tidal gradient in Westcott Bay. Olympia, WA: Washington State Department of Natural Resources.

    Google Scholar 

  • Short, F.T., and S. Wyllie-Echeverria. 1996. Natural and human-induced disturbance of seagrasses. Environmental Conservation 23: 17–27.

    Article  Google Scholar 

  • Specht, D.T., and B.L. Boese. 2009. The effects of temperature and desiccation on the seagrasses Zostera marina and Thalassia testudinum. In Seagrasses and protective criteria: A review and assessment of research status, ed. W.G. Nelson. Newport, OR: Western Ecology Division, National Health and Environmental Effects Research Laboratory, U.S. Environmental Protection Agency, EPA/600/R-09/050.

    Google Scholar 

  • Thom, R.M., H.L. Diefenderfer, J. Vavrinec, and A.B. Borde. 2012. Restoring resiliency: case studies from Pacific Northwest estuarine eelgrass (Zostera marina L.) ecosystems. Estuaries and Coasts 35: 78–91.

    Article  Google Scholar 

  • Valdemarsen, T., P. Canal-Vergés, E. Kristensen, M. Holmer, M.D. Kristiansen, and M.R. Flindt. 2010. Vulnerability of Zostera marina seedlings to physical stress. Marine Ecology Progress Series 418: 119–130.

    Article  Google Scholar 

  • van Katwijk, M.M., and L.J.M. Wijgergangs. 2004. Effects of locally varying exposure, sediment type and low-tide water cover on Zostera marina recruitment from seed. Aquatic Botany 80: 1–12.

    Article  Google Scholar 

  • Vermaat, J.E. 2009. Linking clonal growth patterns and ecophysiology allows the prediction of meadow-scale dynamics of seagrass beds. Perspectives in Plant Ecology 11: 137–155.

    Article  Google Scholar 

  • Waycott, M., C.M. Duarte, T.J.B. Carruthers, R.J. Orth, W.C. Dennison, S. Olyarnike, A. Calladine, J.W. Fourqurean, K.L. Heck Jr., A.R. Hughes, G.A. Kendrick, W.J. Kenworthy, F.T. Short, and S.L. Williams. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences 106: 12377–12381.

    Article  CAS  Google Scholar 

  • Wicks, E.C., E.W. Koch, J.M. O’Neil, and K. Elliston. 2009. Effects of sediment organic content and hydrodynamic conditions on the growth and distribution of Zostera marina. Marine Ecology Progress Series 378: 71–80.

    Article  CAS  Google Scholar 

  • Wisehart, L.M., B.R. Dumbauld, J.L. Ruesink, and S.D. Hacker. 2007. Importance of eelgrass early life history stages in response to oyster aquaculture disturbance. Marine Ecology Progress Series 344: 71–80.

    Article  Google Scholar 

Download references

Acknowledgments

We sincerely thank everyone who made this huge field effort possible: Amy Glaub, Michael Hannam, Kevin See, Lauren Sullenberger, Ginger Tennant, and students in the Spring 2007 Marine Ecology course at University of Washington: Demian Bailey, Sean Cappello, Matt Chin, Anna Choi, Nhuchi Dao, Heather Deboli, Greg Dunster, Anna Grishchenko, Ken Hamel, Tenecia Harris, Michael Klaczynski, Kelsea Laegreid, Justin Neste, Natalee Nusslock, Cody Nutsch, Stephanie Raghubeer, Jennifer Reitz, Elizabeth Suguira, Chaochung Tsai, and Pamela Williams. We appreciate the guidance we received from Helen Berry, Pete Dowty, Jeffrey Gaeckle, Thomas Mumford, Anja Schanz, Ron Thom, Sandy Wyllie-Echeverria, Laura Feinstein, and the insightful editorial comments provided by Janneke HilleRisLambers, and two anonymous reviewers. Thanks also to the following for access to private tidelands: Paul Blau (Blau Oyster Company), Doug Bulthuis (Padilla Bay National Estuarine Research Reserve), Betty Carteret, Bill Dewey (Taylor Shellfish Farms), Harry Eiesland, John and Brit Glomset, Mike MacKay (Lummi Tribe), and Eric Shen. This study was supported by funds from the Environmental Protection Agency Science to Achieve Results, Achievement Rewards for College Scientists fellowships, and National Science Foundation GK-12 Ocean and Coastal Interdisciplinary Science Program Fellowship (to S. Yang), Washington State Department of Natural Resources and Department of Ecology (to E. Wheat), and the Western Regional Aquaculture Center through grant no. 2004-38500-14698 from the United States Department of Agriculture, Cooperative State Research, Education, and Extension Service (to J. Ruesink).

Author information

Authors and Affiliations

  1. Shannon Point Marine Center, Western Washington University, 1900 Shannon Point Road, Anacortes, WA, 98221, USA

    Sylvia Yang

  2. Program on the Environment, University of Washington, Box 355679, Seattle, WA, 98195-5679, USA

    Elizabeth E. Wheat

  3. Department of Biology, University of Washington, Box 351800, Seattle, WA, 98195-1800, USA

    Micah J. Horwith & Jennifer L. Ruesink

Authors
  1. Sylvia Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elizabeth E. Wheat
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Micah J. Horwith
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jennifer L. Ruesink
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sylvia Yang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 99 kb)

Appendix: Methods to Cull Correlated Metrics of Desiccation Stress and Sediment Conditions

Appendix: Methods to Cull Correlated Metrics of Desiccation Stress and Sediment Conditions

We explored the following metrics relevant to desiccation stress before settling on tidal amplitude and elevation: (1) tidal elevation, (2) estimated hours inundated in the previous year (2006) using tidal elevation and predicted water levels by hour (http://tbone.biol.sc.edu/tide/), (3) relative tidal amplitude (the difference between mean lower low water and mean higher high water on May 18, 2007), and (4) relative time of day at low tide during summer using tidal predictions (as a proxy for air temperature). Tidal elevation and inundation time were correlated (r(29) = −0.95, p < 0.0001), and tidal amplitude and time at low tide were correlated (r(32) = 0.34, p = 0.046).

We explored the following metrics of sediment conditions before settling on sediment organic content: (1) beach slope, in two categories: extensive broad shallows in embayments or pocket beaches (“flats”) versus narrow, sloping shorelines (“fringes”) (Berry et al. 2003), (2) silt to sand ratio, and (3) sediment organic matter. Categorical beach slope (r(29) = −0.53, p = 0.002) and silt to sand ratio (r(29) = 0.85, p < < 0.0001) were highly correlated with sediment organic matter. Sediment organic content is controlled by biological processes, including heterotrophic assimilation and autochthonous production, as well as physical processes. Thus, we used it to indicate relative differences in biologically relevant sediment conditions among our sites.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yang, S., Wheat, E.E., Horwith, M.J. et al. Relative Impacts of Natural Stressors on Life History Traits Underlying Resilience of Intertidal Eelgrass (Zostera marina L.). Estuaries and Coasts 36, 1006–1013 (2013). https://doi.org/10.1007/s12237-013-9609-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-013-9609-0

Keywords

Search

Navigation