Estuaries and Coasts

, Volume 34, Issue 6, pp 1169–1181 | Cite as

Context-Dependent Eelgrass–Macroalgae Interactions Along an Estuarine Gradient in the Pacific Northwest, USA

  • Margot L. Hessing-Lewis
  • Sally D. Hacker
  • Bruce A. Menge
  • Steve S. Rumrill
Article

Abstract

Land-based eutrophication is often associated with blooms of green macroalgae, resulting in negative impacts on seagrasses. The generality of this interaction has not been studied in upwelling-influenced estuaries where oceanic nutrients dominate seasonally. We conducted an observational and experimental study with Zostera marina L. and ulvoid macroalgae across an estuarine gradient in Coos Bay, Oregon. We found a gradient in mean summer macroalgal biomass from 56.1 g dw 0.25 m−2 at the marine site to 0.3 g dw 0.25 m−2 at the riverine site. Despite large macroalgal blooms at the marine site, eelgrass biomass exhibited no seasonal or interannual declines. Through experimental manipulations, we found that pulsed additions of macroalgae biomass (+4,000 mL) did not affect eelgrass in marine areas, but it had negative effects in riverine areas. In upwelling-influenced estuaries, the negative effects of macroalgal blooms are context dependent, affecting the management of seagrass habitats subject to nutrient inputs from both land and sea.

Keywords

Zostera marina Ulva Species interactions Estuarine gradient Oceanic upwelling Oregon 

Notes

Acknowledgments

Thanks to all the supportive field and lab help associated with this research: at Oregon State University—O. Moulton, P. Zarnetske, J. Henderson, L. Wisehart, D. Eerkes-Medrano, S. McConville, W. Rice-Narusch, H. Bailey, J. Schaefers, M. Rogers, B. Dumbauld, and L. McCoy; SS NERR—A. Helms and A. DeMarzo; and R advice—T. Gouhier. This manuscript was greatly improved by reviewer comments. Research was funded from an award from the National Estuarine Reserve System, Estuarine Reserves Division, Office of Ocean and Coastal Resource Management, National Ocean Service, NOAA. Additional financial support for this research was provided by Oregon State University Department of Zoology and the Hacker and Menge Labs.

References

  1. Armitage, A., T. Frankovich, K. Heck, and J. Fourqurean. 2005. Experimental nutrient enrichment causes complex changes in seagrass, microalgae, and macroalgae community structure in Florida Bay. Estuaries and Coasts 28(3): 422–434.CrossRefGoogle Scholar
  2. Barbier, E.B., S.D. Hacker, C. Kennedy, E.W. Koch, A.D. Stier, and B.R. Silliman. 2011. The value of estuarine and coastal ecosystem services. Ecological Monographs 81: 169–193.CrossRefGoogle Scholar
  3. Berlow, E.L., S.A. Navarrete, C.J. Briggs, M.E. Power, and B.A. Menge. 1999. Quantifying variation in the strengths of species interactions. Ecology 80(7): 2206–2224.CrossRefGoogle Scholar
  4. Boese, B.L., K.E. Alayan, E.F. Gooch, and B.D. Robbins. 2003. Desiccation index: a measure of damage caused by adverse aerial exposure on intertidal eelgrass (Zostera marina) in an Oregon (USA) estuary. Aquatic Botany 76(4): 329–337.CrossRefGoogle Scholar
  5. Boese, B.L., B.D. Robbins, and G. Thursby. 2005. Desiccation is a limiting factor for eelgrass (Zostera marina L.) distribution in the intertidal zone of a northeastern Pacific (USA) estuary. Botanica Marina 48(4): 274–283.CrossRefGoogle Scholar
  6. Bricker, S., J. Ferreira, and T. Simas. 2003. An integrated methodology for assessment of estuarine trophic status. Ecological Modelling 169: 39–60.CrossRefGoogle Scholar
  7. Bronstein, J.L. 1994. Conditional outcomes in mutualistic interactions. Trends in Ecology & Evolution 9(6): 214–217.CrossRefGoogle Scholar
  8. Brown, C., and R. Ozretich. 2009. Coupling between the coastal ocean and Yaquina Bay, Oregon: Importance of oceanic inputs relative to other nitrogen sources. Estuaries and Coasts 32(2): 219–237.CrossRefGoogle Scholar
  9. Brown, C., W.G. Nelson, B.L. Boese, T.H. DeWitt, P.M. Eldridge, J.E. Kaldy, H. Lee, J.H. Power, and D.R. Young. 2007. An approach to developing nutrient criteria for Pacific Northwest estuaries: A case study of Yaquina Estuary, Oregon, 146. Durham: USEPA Office of Research and Development, National Health and Environmental Effects Laboratory, Western Ecology Division.Google Scholar
  10. Brun, F.G., J.J. Vergara, G. Navarro, I. Hernandez, and J.L. Perez-Llorens. 2003. Effect of shading by Ulva rigida canopies on growth and carbon balance of the seagrass Zostera noltii. Marine Ecology Progress Series 265: 85–96.CrossRefGoogle Scholar
  11. Burkholder, J., D. Tomasko, and B. Touchette. 2007. Seagrasses and eutrophication. Journal of Experimental Marine Biology and Ecology 350: 46–72.CrossRefGoogle Scholar
  12. Burkholder, J., K.M. Mason, H.B. Jr. Glasgow. 1992. Water-column nitrate enrichment promotes decline of eelgrass Zostera manna: evidence from seasonal mesocosm experiments. Marine Ecology Progress Series 81: 163–178Google Scholar
  13. Carr, J., P. D’Odorico, K. McGlathery and P. Wiberg. 2010. Stability and bistability of seagrass ecosystems in shallow coastal lagoons: Role of feedbacks with sediment resuspension and light attenuation. Journal of Geophysical Research 115. doi: 10.1029/2009JG001103.
  14. Cohen, R.A., and P. Fong. 2004. Physiological responses of a bloom-forming green macroalga to short-term change in salinity, nutrients, and light help explain its ecological success. Estuaries 27(2): 209–216.CrossRefGoogle Scholar
  15. Crain, C.M., and M.D. Bertness. 2006. Ecosystem engineering across environmental gradients: Implications for conservation and management. Bioscience 56(3): 211–218.CrossRefGoogle Scholar
  16. Dayton, P.K. 1971. Competition, disturbance, and community organization: The provision and subsequent utilization of space in a rocky intertidal community. Ecological Monographs 41: 351–389.CrossRefGoogle Scholar
  17. Duarte, C.M. 2000. Marine biodiversity and ecosystem services: An elusive link. Journal of Experimental Marine Biology and Ecology 250(1–2): 117–131.CrossRefGoogle Scholar
  18. Eriksson, B.K., A. Rubach, and H. Hillebrand. 2007. Dominance by a canopy forming seaweed modifies resource and consumer control of bloom-forming macroalgae. Oikos 11(7): 1211–1219.CrossRefGoogle Scholar
  19. Fry, B., A. Gace, and J.W. McClelland. 2003. Chemical indicators of anthropogenic nutrient loading in four Pacific estuaries. Pacific Science 57(1): 77–101.CrossRefGoogle Scholar
  20. Gabrielson, P., T. Widdowson, and S. Lindstrom. 2006. Keys to the seaweeds and seagrasses of Southeast Alaska, British Columbia, Washington and Oregon, phycological contribution 7. Hillsborough: PhycoID.Google Scholar
  21. Hacker, S.D., and M.N. Dethier. 2006. Community modifications by a grass invader has differing impacts for marine habitats. Oikos 113: 279–286.CrossRefGoogle Scholar
  22. Hacker, S.D., P. Zarnetske, E. Seabloom, P. Ruggiero, J. Mull, S. Gerrity, and C. Jones. 2011. Subtle differences in two non-native congeneric beach grasses significantly affect their colonization, spread, and impact. Oikos. doi: 10.1111/j.1600-0706.2011.18887.x
  23. Hacker, S.D., S. Gaines. 1997. Some implications of direct positive interactions for community species diversity. Ecology 78: 1990–2003Google Scholar
  24. Harris, D., W.G. McDougal, W.A. Patton, and N. Talebbeydokhpi. 1979. Hydrologic study for South Slough Estuarine Sanctuary. Corvallis: Oregon State University, Water Resources Research Institute.Google Scholar
  25. Hauxwell, J., J. McClelland, P.J. Behr, and I. Valiela. 1998. Relative importance of grazing and nutrient controls of macroalgal biomass in three temperate shallow estuaries. Estuaries 21(2): 347–360.CrossRefGoogle Scholar
  26. Hauxwell, J., J. Cebrian, C. Furlong, and I. Valiela. 2001. Macroalgal canopies contribute to eelgrass (Zostera marina) decline in temperate estuarine ecosystems. Ecology 82(4): 1007–1022.Google Scholar
  27. Havens, K.E., J. Hauxwell, A.C. Tyler, S. Thomas, K.J. McGlathery, J. Cebrian, I. Valiela, A.D. Steinman, and S. Hwang. 2001. Complex interactions between autotrophs in shallow marine and freshwater ecosystems: Implications for community responses to nutrient stress. Environmental Pollution 113(1): 95–107.CrossRefGoogle Scholar
  28. Hemminga, M. 1998. The root/rhizome system of seagrasses: An asset and a burden. Journal of Sea Research 39: 183–196.CrossRefGoogle Scholar
  29. Hickey, B.M., and N. Banas. 2003. Oceanography of the U.S. Pacific Northwest coastal ocean and estuaries with application to coastal ecology. Estuaries 26: 1010–1031.CrossRefGoogle Scholar
  30. Jorgensen, P., S.E. Ibarra-Obando, and J.D. Carriquiry. 2007. Top-down and bottom-up stabilizing mechanisms in eelgrass meadows differentially affected by coastal upwelling. Marine Ecology Progress Series 333: 81–93.CrossRefGoogle Scholar
  31. Jorgensen, P., S.E. Ibarra-Obando, and J.D. Carriquiry. 2010. Management of natural Ulva spp. blooms in San Quintin Bay, Baja California: Is it justified? Journal of Applied Phycology 22(5): 549–558.CrossRefGoogle Scholar
  32. Kamer, K., P. Fong, R. Kennison, and K. Schiff. 2004. Nutrient limitation of the macroalga Enteromorpha intestinalis collected along a resource gradient in a highly eutrophic estuary. Estuaries 27(2): 201–208.CrossRefGoogle Scholar
  33. Kentula, M., and T. DeWitt. 2003. Abundance of seagrass (Zostera marina L.) and macroalgae in relation to the salinity–temperature gradient in Yaquina Bay, Oregon, USA. Estuaries and Coasts 26(2): 1130–1141.CrossRefGoogle Scholar
  34. Krause-Jensen, D., K. Glathery, S. Rysgaard, and P.B. Christensen. 1996. Production within dense mats of the filamentous macroalga Chaetomorpha linum in relation to light and nutrient availability. Marine Ecology Progress Series 134: 207–216.CrossRefGoogle Scholar
  35. Kuhn, M., S. Weston, J. Wing and J. Forester. 2010. Contrast: A collection of contrast methods. http://CRAN.R-project.org/package=contrast. Accessed 29 Aug 2010.
  36. McGlathery, K. 2001. Macroalgal blooms contribute to the decline of seagrass in nutrient-enriched coastal waters. Journal of Phycology 35: 1–4.Google Scholar
  37. Menge, B.A., and J.P. Sutherland. 1987. Community regulation: Variation in disturbance, competition, and predation in relation to environmental stress and recruitment. The American Naturalist 130(5): 730–757.CrossRefGoogle Scholar
  38. Menge, B.A., C. Blanchette, P. Raimondi, T. Freidenburg, S. Gaines, J. Lubchenco, D. Lohse, G. Hudson, M. Foley, and J. Pamplin. 2004. Species interaction strength: Testing model predictions along an upwelling gradient. Ecological Monographs 74(4): 663–684.CrossRefGoogle Scholar
  39. Moore, K.A., R.L. Wetzel, and R.J. Orth. 1997. Seasonal pulses of turbidity and their relations to eelgrass (Zostera marina L.) survival in an estuary. Journal of Experimental Marine Biology and Ecology 21(1): 115–134.CrossRefGoogle Scholar
  40. Nejrup, L., and M. Pedersen. 2008. Effects of salinity and water temperature on the ecological performance of Zostera marina. Aquatic Botany 88: 239–246.Google Scholar
  41. Nelson, T.A., K. Haberlin, A.V. Nelson, H. Ribarich, R. Hotcchkiss, K.L. Van Alstyne, L. Buckingham, D.J. Simunds, and K. Fredrickson. 2008. Ecological and physiological controls of species composition in green macroalgal blooms. Ecology 89(5): 1287–1298.CrossRefGoogle Scholar
  42. O'Higgins, T. and S. Rumrill. 2007. Tidal and watershed forcing of nutrients and dissolved oxygen stress within four pacific coast estuaries: Analysis of time-series data collected by the National Estuarine Research Reserve System-Wide Monitoring Program (2000–2006) within Padilla Bay (WA), South Slough (OR), Elkhorn Slough (CA) and the Tijuana River estuary (CA). Report for the NOAA/UNH Cooperative Institute for Coastal and Estuarine Environmental Technology (CICEET), 58.Google Scholar
  43. Orth, R.J., T.J.B. Carruthers, W. Dennison, C.M. Duarte, J. Fourqurean, K.L. Heck, 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(12): 987–996.CrossRefGoogle Scholar
  44. Pacific Fisheries Environmental Laboratory. 2011. http://www.pfeg.noaa.gov. Accessed 14 Jan 2010.
  45. Peralta, G., J.L. Perez-Llorens, I. Hernandez, and J.J. Vergara. 2002. Effects of light availability on growth, architecture and nutrient content of the seagrass Zostera noltii Hornem. Journal of Experimental Marine Biology and Ecology 269: 9–26.CrossRefGoogle Scholar
  46. Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar and the R Core Team .2009. nlme: Linear and nonlinear mixed effects models. http://cran.r-project.org/web/packages/nlme/index.html. Accessed 29 Aug 2010
  47. Pregnall, A., and P. Rudy. 1985. Contribution of green macroalgal mats (Enteromorpha spp.) to seasonal production in an estuary. Marine Ecology Progress Series 24: 167–176.CrossRefGoogle Scholar
  48. R Development Core Team. 2009. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. http://www.R.project.org. Accessed Aug 29 2010.
  49. Ralph, P.J., D. Tomasko, K. Moore, S. Seddon, and C.M.O. Macinnis-Ng. 2006. Human impacts on seagrasses: Eutrophication, sedimentation, and contamination. In Seagrasses: Biology, ecology and conservation, ed. A.W.D. Larkum, R.J. Orth, and C.M. Duarte, 567–593. the Netherlands: Springer.CrossRefGoogle Scholar
  50. Rivers, J., and P. Peckol. 1995. Summer deline of Ulva lactuca (Chlorophyta) in a eutrophic embayment: Interactive effects of temperature and nitrogen availability. Journal of Phycology 31(2): 223–228.CrossRefGoogle Scholar
  51. Robbins, B.D., and B.L. Boese. 2002. Macroalgal volume: A surrogate for biomass in some green algae. Botanica Marina 45(6): 586–588.CrossRefGoogle Scholar
  52. Roegner, G.C., and A.L. Shanks. 2001. Import of coastally-derived chlorophyll a to South Slough, Oregon. Estuaries 24(2): 244–256.CrossRefGoogle Scholar
  53. Rumrill, S. 2006. The ecology of the South Slough Estuary: Site profile of the South Slough National Estuarine Research Reserve. Salem: NOAA.Google Scholar
  54. Salomon, A.K., S.K. Gaichas, N.T. Shears, J.E. Smith, E. Madin, and S.D. Gaines. 2010. Key features and context-dependence of fishery-induced trophic cascades. Conservation Biology 24(2): 382–394.CrossRefGoogle Scholar
  55. Sfriso, A., B. Pavoni, A. Marcomini, and A. Orio. 1992. Macroalgae, nutrient cycles, and pollutants in the Lagoon of Venice. Estuaries and Coasts 15(4): 517–528.CrossRefGoogle Scholar
  56. Teichberg, M., S.E. Fox, Y.S. Olsen, I. Valiela, P. Martinettos, O. Iribarnes, E.Y. Muto, M.A.V. Petti, T.N. Corbisier, M. Soto-Jimenez, F. Paez-Osuna, P. Castro, H. Freitas, A. Zitelli, M. Cardinaletti, and D. Tagliapietrass. 2010. Eutrophication and macroalgal blooms in temperate and tropical coastal waters: nutrient enrichment experiments with Ulva spp. Global Change Biology 16: 2624–2637.Google Scholar
  57. Terrados, J., C.M. Duarte, L. Kemp-Nielsen, N.S.R. Agawin, E. Gacia, D. Lacap, M.D. Fortes, J. Borum, M. Lubanski, and T. Greve. 1999. Are seagrass growth and survival constrained by the reducing conditions of the sediment? Aquatic Botany 65: 175–197.CrossRefGoogle Scholar
  58. Thom, R., A. Borde, S. Rumrill, D. Woodruff, G. Williams, J. Southard, and S. Sargeant. 2003. Factors influencing spatial and annual variability in eelgrass (Zostera marina L.) meadows in Willapa Bay, Washington, and Coos Bay, Oregon, estuaries. Estuaries and Coasts 26(4): 1117–1129.CrossRefGoogle Scholar
  59. Thom, R.M., S.L. Southard, A.B. Borde, and P. Stoltz. 2008. Light requirements for growth and survival of eelgrass (Zostera marina L.) in Pacific Northwest (USA) estuaries. Estuaries and Coasts 31(5): 969–980.CrossRefGoogle Scholar
  60. Underwood, A. 1997. Experiments in ecology; their logical design and interpretation using analysis of variance. Cambridge: Cambridge University Press.Google Scholar
  61. Valiela, I., J. McClelland, J. Hauxwell, P.J. Behr, D. Hersh, and K. Foreman. 1997. Macroalgal blooms in shallow estuaries: Controls and ecophysiological ecosystem consequences. Limnology and Oceanography 42(5): 1105–1118.CrossRefGoogle Scholar
  62. Waycott, M., C.M. Duarte, T.J.B. Carruthers, R.J. Orth, W. Dennison, S. Olyarnik, A. Calladine, J. Fourqurean, K.L. Heck, A.R. Hughes, F.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(30): 12377–12381.CrossRefGoogle Scholar
  63. Wickham, H. 2009. ggplot2: Elegant graphics for data analysis. http://had.co.nz/ggplot2/. Accessed Aug 29 2010
  64. Zimmerman, R.C., J.L. Reguzzoni, and R.S. Alberte. 1995. Eelgrass (Zostera marina L.) transplants in San Francisco Bay: Role of light availability on metabolism, growth and survival. Aquatic Botany 51(1–2): 67–86.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2011

Authors and Affiliations

  • Margot L. Hessing-Lewis
    • 1
  • Sally D. Hacker
    • 1
  • Bruce A. Menge
    • 1
  • Steve S. Rumrill
    • 2
  1. 1.Department of ZoologyOregon State UniversityCorvallisUSA
  2. 2.South Slough National Estuarine Research ReserveCharlestonUSA

Personalised recommendations