Estuaries and Coasts

, Volume 36, Issue 6, pp 1115–1124 | Cite as

Diverse Dietary Responses by Saltmarsh Consumers to Chronic Nutrient Enrichment



We examined the effect of whole-ecosystem nutrient enrichment on herbivory in saltmarsh creek-wall habitats in the Plum Island Estuary (Massachusetts, USA). Located between the macrophyte-dominated high marsh and adjoining mudflats, creek walls are steep vertical habitats vegetated with productive filamentous algae and associated epiphytes. Annual nitrate and phosphate loading rates were increased approximately ×10–15 in creeks mimicking short-term (2-month) and chronic (6-year) eutrophication. We assessed the diets of epifaunal invertebrates (three gastropods and one amphipod species) that potentially graze on benthic algae using natural isotope abundance data and per capita grazing rate measurements derived from 13C prelabeled algae. Substantial dietary contributions from benthic algae were observed in all consumers even though previous research has indicated most rely on Spartina detritus as the principal food resource. The amphipod Orchestia grillus and the snail Melampus bidentatus grazed benthic algae in excess of 500 μg algal C g C−1 h−1, whereas the snail Nassarius obsoletus and hydrobiid snails grazed at lower rates. Few dietary changes were detected with short-term enrichment. Algal grazing rates of N. obsoletus and M. bidentatus increased with chronic enrichment probably as a functional response to increased algal productivity. O. grillus grazed at a high rate and parasitic infection did not affect its consumption of benthic algae. The abundance and frequency of occurrence of O. grillus on creek-wall habitats increased with chronic nutrient enrichment suggesting amphipods contribute to top–down control on benthic algae and slow algal growth as nutrient enrichment occurs.


Nutrient enrichment Food web Epiphytes Filamentous algae Estuary Creek-wall habitat 


  1. APHA (1992) Standard methods for the examination of water and wastewater, 18th ed. American Waterworks Association and Water Pollution Control Federation, Washington.Google Scholar
  2. Armitage, A.R., and J.W. Fourqurean. 2009. Stable isotope reveal complex changes in trophic relationships following nutrient addition in a coastal marine ecosystem. Estuar Coast 32: 1152–1164.CrossRefGoogle Scholar
  3. Bertness, M.D., P.J. Ewanchug, and B.R. Silliman. 2002. Anthropogenic modification of New England salt marsh landscapes. Proc Natl Acad Sci USA 99: 1395–1398.CrossRefGoogle Scholar
  4. Bousfield, E.L., and R.W. Heard. 1986. Systematics distributional ecology and some host–parasite relationships of Uhlorchestia uhleri (Shoemaker) and U spartinophila new species (Crustacea: Amphipoda) endemic to salt marshes of the Atlantic Coast of North America. J Crustacean Biol 6: 264–274.CrossRefGoogle Scholar
  5. Canfield, D.E., A.N. Glazer, and P.G. Falkowski. 2010. The evolution of Earth’s nitrogen cycle. Science 330: 192–196.CrossRefGoogle Scholar
  6. Carpenter, S.R. 1989. Replication and treatment strenght in whole-lake experiments. Ecology 70: 453–463.CrossRefGoogle Scholar
  7. Carpenter, S.R., S.W. Chrisholm, C.J. Krebs, D.W. Schlinder, and R.F. Wright. 1995. Ecosystem experiments. Science 269: 324–327.CrossRefGoogle Scholar
  8. Costanza, R., R. d’Arge, R. de Groot, S. Farber, M. Grasso, B. Hannon, K. Limburg, S. Naeem, R.V. O’Neil, J. Paruelo, R.G. Raskin, P. Sutton, and M. van den Belt. 1997. The value of the world’s ecosystem services and natural capital. Nature 387: 253–260.CrossRefGoogle Scholar
  9. Crompton, D.W.T. (1970) An ecological approach to acanthocephalan physiology. Cambridge University Press, Cambridge.Google Scholar
  10. Curtis, L.A., and L.E. Hurd. 1979. On the broad nutritional requirements of the mudsnail, Ilyanassa (Nassarius) obsoleta (Say) and its polytrophic role in the food web. Journal of Experimental Marine Biology and Ecology 41: 289–297.CrossRefGoogle Scholar
  11. Darby, F.A., and R.E. Turner. 2008. Consequences of eutrophication to salt marsh roots, rhizomes, and soils. Marine Ecology Progress Series 363: 63–70.CrossRefGoogle Scholar
  12. Deegan, L.A., J.L. Bowen, D. Drake, J.W. Fleeger, C.T. Fiedrichs, K.A. Galván, J.E. Hobbie, C.S. Hopkinson, D.S. Johnson, J.M. Johnson, L.E. LeMay, E. Miller, B.J. Peterson, C. Picard, S. Sheldom, M. Sutherland, J. Vallino, and R.S. Warren. 2007. Susceptiblity of salt-marshes to nutrient enrichment and predator removal. Ecological Applications 17: S42–S63.CrossRefGoogle Scholar
  13. Deegan, L.A., D.S. Johnson, R.S. Warren, B. Peterson, J.W. Fleeger, S. Fagherazzi, and W.M. Wollheim. 2012. Coastal eutrophication as a driver of saltmarsh loss. Nature 490: 388–392.CrossRefGoogle Scholar
  14. DeNiro, M.J., and S. Epstein. 1981. Influence of the diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45: 341–351.CrossRefGoogle Scholar
  15. Diaz, R.J., and R. Rosenberg. 2008. Spreading dead zones and consequences for marine ecosystems. Science 321: 926–929.CrossRefGoogle Scholar
  16. Drake, D.C., B.J. Peterson, K.A. Galván, L.A. Deegan, C.S. Hopkinson, J.M. Johnson, K. Koop-Jakobsen, L.E. LeMay, and C. Picard. 2009. Salt marsh ecosystem biogeochemical responses to nutrient enrichment: a paired 15N tracer study. Ecology 90: 2535–2546.CrossRefGoogle Scholar
  17. Duffy, E.J., and M.E. Hay. 2000. Strong impacts of grazing amphipods on the organization of a benthic community. Ecological Monographs 70: 237–263.CrossRefGoogle Scholar
  18. E.P.A. (2002) In, Book 2002 EPA/620/R-02/003. US Environmental Protection Agency, Office of Research and Development, National Health and Research Laboratory, Atlantic Ecology Divisioni, Narangasett.Google Scholar
  19. Ferreira, J.G., J.H. Andersen, A. Borja, S.B. Bricker, J. Camp, M.C. de Silva, E. Garces, A.S. Heiskanen, C. Humborg, L. Ignatiades, C. Lancelot, A. Menesguen, P. Tett, N. Hoepffner, and U. Claussen. 2011. Overview of eutrophication indicators to assess environmental status within the European Marine Framework Strategy Framework Directive. Est Coast Shelf Sci 93: 117–131.CrossRefGoogle Scholar
  20. Fielding, N.J., C. MacNeil, J.T.A. Dick, R.W. Elwood, G.E. Riddell, and A.M. Dunn. 2003. Effects of the acanthocephlan parasite Echinorhynchus truttae on the feeding ecology of Gammarus pulex (Crustacea: Amphipoda). J Zool Lond 261: 321–325.CrossRefGoogle Scholar
  21. Fleeger, J.W., D.S. Johnson, K.A. Galván, and L.A. Deegan. 2008. Top–down and bottom–up control of infauna varies across the saltmarsh landscape. Journal of Experimental Marine Biology and Ecology 357: 20–34.CrossRefGoogle Scholar
  22. Fox, S.E., M. Teichberg, Y. Olsen, L. Heffner, and I. Valiela. 2009. Restructuring of benthic communities in eutrophic estuaries: lower abundance of preys leads to trophic shifts from omnivory to grazing. Marine Ecology Progress Series 380: 43–57.CrossRefGoogle Scholar
  23. Fry B (2006) Stable isotope ecology. Springer, New York.Google Scholar
  24. Galloway, J.N., A.R. Townsend, J.W. Erisman, M. Bekunda, Z. Cai, J. Freney, L.A. Martinelli, S.P. Seitzinger, and M.A. Sutton. 2008. Transformation of the nitrogen cycle: recent trends, questions and potential solutions. Science 320: 889–892.CrossRefGoogle Scholar
  25. Galván, K. 2008. The diet of saltmarsh consumers. Baton Rouge: Louisiana State University.Google Scholar
  26. Galván, K., J.W. Fleeger, and B. Fry. 2008. Stable isotope addition reveals dietary importance of phytoplankton and microphytobenthos to saltmarsh infauna. Marine Ecology Progress Series 359: 37–49.CrossRefGoogle Scholar
  27. Galván, K.A., J.W. Fleeger, B. Peterson, D. Drake, L.A. Deegan, and D.S. Johnson. 2011. Natural abundance stable isotopes and dual isotope tracer additions help to resolve resources supporting saltmarsh food web. Journal of Experimental Marine Biology and Ecology 410: 1–11.CrossRefGoogle Scholar
  28. Giordani, G., J.M. Zaldivar, and P. Viaroli. 2009. Simple tools for assessing water quality and trophic status in transitional water ecosystems. Ecological Indicators 9: 982–991.CrossRefGoogle Scholar
  29. Gruber, N., and J.N. Galloway. 2008. An earth-system perspective of the global nitrogen cycle. Nature 451: 293–296.CrossRefGoogle Scholar
  30. Hillebrand, H., B. Worm, and H.K. Lotze. 2000. Marine microbenthic community structure regulated by nitrogen loading and grazing pressure. Marine Ecology Progress Series 204: 27–38.CrossRefGoogle Scholar
  31. Hillebrand, H., M. Kahlert, A.L. Haglund, U.G. Berninger, S. Nagel, and S. Wickham. 2002. Control of microbenthic communities by grazing and nutrient supply. Ecology 83: 2205–2219.CrossRefGoogle Scholar
  32. Hurd, L.E. 1985. On the importance of carrion to reproduction in an omnivorous estuarine neogasteropode, Ilyanassa obsoleta (Say). Oecologia 65: 513–515.CrossRefGoogle Scholar
  33. Jaschinski, S., and C. Sommer. 2010. Positive effects of mesograzers on epiphytes in an eelgrass system. Marine Ecology Progress Series 401: 77–85.Google Scholar
  34. Johnson, D.S. 2011. High-marsh invertebrates are susceptible to eutrophication. Marine Ecology Progress Series 438: 143–152.CrossRefGoogle Scholar
  35. Johnson, D.S., and J.W. Fleeger. 2009. Weak response of saltmarsh infauna to ecosystem-wide nutrient enrichment and fish predator reduction: a four-year study. Journal of Experimental Marine Biology and Ecology 373: 35–44.CrossRefGoogle Scholar
  36. Johnson, D.S., and M. Short. 2013. Chronic nutrient enrichment increase the density and biomass of the mudsnail, Nassarius obsoletus. Estuar Coast 36: 28–35.CrossRefGoogle Scholar
  37. Johnson, D.S., J.W. Fleeger, K.A. Galván, and E.B. Moser. 2007. Worm holes and their space-time continuum: spatial and temporal variability of macroinfaunal annelids in a northern New England salt marsh. Estuar Coast 30: 226–237.CrossRefGoogle Scholar
  38. Johnson, D.S., J.W. Fleeger, and L.A. Deegan. 2009. Large-scale manipulation reveal top–down and bottom–up controls interact to alter habitat utilization by saltmarsh fauna. Marine Ecology Progress Series 377: 33–41.CrossRefGoogle Scholar
  39. Jonge, V.N.D. 1980. Fluctuations in the organic carbon to chlorophyll-a ratios in estuarine benthic diatom populations. Marine Ecology Progress Series 2: 345–353.CrossRefGoogle Scholar
  40. Juanes, J.A., X. Guinda, A. Puente, and J.A. Revilla. 2008. Macroalgae, a suitable indicator of the ecological status of coastal rocky communities in the NE Atlantic. Ecological Indicators 8: 351–359.CrossRefGoogle Scholar
  41. Keats, R.A., L.J. Osher, and H.A. Neckles. 2004. The effect of nitrogen loading on a brackish estuarine faunal community: a stable isotope approach. Estuaries 27: 460–471.CrossRefGoogle Scholar
  42. Lee, S.C., and B.R. Silliman. 2006. Competitive displacement of a detritivorous salt marsh snail. Journal of Experimental Marine Biology and Ecology 339: 75–85.CrossRefGoogle Scholar
  43. Lockfield, K. 2011. Chronic nutrient enrichment effects on mummichog, Fundulus heteroclitus in a northeastern Massachusetts salt marsh. Masters, Louisiana State University, Baton Rouge.Google Scholar
  44. Lopez, G.R., J.S. Levinton, and L.B. Slobodkin. 1977. The effect of grazing by the detritivore Orchestia grillus on Spartina litter and its associated microbial community. Oecologia 30: 111–127.CrossRefGoogle Scholar
  45. McCahon, C.P., A.F. Brown, and D. Pascoe. 1988. The effect of acanthocephalan Pomphorhynchus laevis (Muller 1776) on the acute toxicity of cadmium to its intermediate host, the amphipod Gammarus pulex (L.). Archives of Environmental Contamination and Toxicology 17: 239–243.CrossRefGoogle Scholar
  46. Middelburg, J.J., C. Barranguet, H.T.S. Boschker, P.M.J. Herman, T. Moens, and C.H.R. Heip. 2000. The fate of intertidal microphytobenthos carbon. An in situ 13C labelling study. Limnology and Oceanography 45: 1224–1234.CrossRefGoogle Scholar
  47. Minagawa, M., and E. Wada. 1984. Stepwise enrichment of 15N along food chain: further evidence and the δ15N and animal age. Geochimica et Cosmochimica Acta 48: 1135–1140.CrossRefGoogle Scholar
  48. Mitwally, H.M., Fleeger, J.W. (2013) Long-term nutrient fertilization effects on salt marsh meiofauna. Hydrobiologia. doi:10.1007/s10750-013-1496-7
  49. Parnell, A.C., R. Inger, S. Bearhop, and A.L. Jackson. 2010. Source partitioning using stable isotopes: coping with too much variation. PloS One 5: e9672.CrossRefGoogle Scholar
  50. Pascal, P.Y., J.W. Fleeger, H.T.S. Boschker, H.M. Mitwally, and D.S. Johnson. 2013. Response of the benthic food web to short- and long-term nutrient enrichment in saltmarsh mudflats. Marine Ecology Progress Series 474: 27–41.CrossRefGoogle Scholar
  51. Pascoe, D., T.J. Kedwards, S.J. Blockwell, and E.J. Taylor. 1995. Gammarus pulex (L.) feeding bioassay—effects of parasitism. Bulletin of Environmental Contamination and Toxicology 55: 629–632.CrossRefGoogle Scholar
  52. Peterson, B.J., L.A. Deegan, J. Helfrich, J.E. Hobbie, M. Hullar, B. Moller, T.E. Ford, A. Hershey, A. Hiltner, G. Kipphut, M.A. Lock, D.M. Fiebig, V. McKinley, M.C. Miller, J.R. Vestal, R. Ventullo, and G. Volk. 1993. Biological response of a tundra river to fertilization. Ecology 74: 653–672.CrossRefGoogle Scholar
  53. Posey, M., C. Powell, L. Cahoon, and D. Lindquist. 1995. Top down vs. bottom up control of benthic community composition on an intertdal tideflat. Journal of Experimental Marine Biology and Ecology 185: 19–31.CrossRefGoogle Scholar
  54. Rosemond, A.D., C.M. Pringle, and A. Ramirez. 2001. A test of top–down and bottom–up control in a detritus-based food web. Ecology 82: 2279–2293.CrossRefGoogle Scholar
  55. Sardá, R., I. Valiela, and K. Foreman. 1996. Decadal shifts in a salt marsh macroinfaunal community in response to sustained long-term experimental nutrient enrichment. Journal of Experimental Marine Biology and Ecology 205: 63–81.CrossRefGoogle Scholar
  56. Taylor, A.C., S.W. Nixon, S.L. Granger, J.P. Buckley, J.P. McMahon, and H.J. Lin. 1995. Responses of coastal lagoon plant comminuties to different forms of nutrient enrichment—a mesocosm experiment. Aquatic Botany 52: 19–34.CrossRefGoogle Scholar
  57. Thompson, L.S. 1984. Comparison of the diets of the tidal marsh snail, Melampus bidentatus and the amphipod, Orchestia grillus. Nautilus 98: 44–53.Google Scholar
  58. Valiela, I., and M.L. Cole. 2002. Comparative evidence that salt marshes and mangrove may protect seagrass meadows from land-derived nitrogen loads. Ecosystems 5: 92–102.CrossRefGoogle Scholar
  59. Vermeulen, S., S. Sturaro, S. Goberts, J.M. Bouquegneau, and G. Lepoint. 2011. Potential early indicators of anthropogenically derived nutrients: a mutiscale stable isotope analysis. Marine Ecology Progress Series 422: 9–22.CrossRefGoogle Scholar
  60. Wear, D.J., M.J. Sullivan, A.D. Moore, and D.F. Millie. 1999. Effects of water-column enrichment on the production dynamics of three seagrass species and their epiphytic algae. Marine Ecology Progress Series 179: 201–213.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2013

Authors and Affiliations

  1. 1.UMR 7138, Equipe Biologie de la Mangrove, Laboratoire de Biologie MarineUniversité des Antilles et de la GuyaneGuadeloupeFrance
  2. 2.Department of Biological SciencesLouisiana State UniversityBaton RougeUSA

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