Estuaries and Coasts

, Volume 36, Issue 1, pp 28–35 | Cite as

Chronic Nutrient Enrichment Increases the Density and Biomass of the Mudsnail, Nassarius obsoletus

Article

Abstract

In summer 2009, the effects of 6 years of landscape-level experimental nutrient enrichment on the eastern mudsnail, Nassarius obsoletus (formerly Ilyanassa obsoleta), were examined. The experiment was conducted in five tidal creeks (two nutrient-enriched, three reference creeks) in the Plum Island Estuary, Massachusetts, USA. (42°44′ N, 70°52′ W). After 6 years of enrichment, N. obsoletus size structure differed between treatment creeks with adult snails on average 14 % larger in enriched creeks. N. obsoletus densities (in individuals per square meter) and biomass (in grams dry weight per square meter) were four times higher in nutrient-enriched versus reference creeks. Nutrient enrichment did not significantly affect the biomass of benthic microalgae (a N. obsoletus food resource), but snail density was significantly correlated with benthic microalgal biomass, suggesting bottom–up control of snails. N. obsoletus is abundant on the east and west coast of North America; thus, N. obsoletus density and biomass may be useful variables for monitoring eutrophication effects on North American estuaries.

Keywords

Biomonitoring Bioindicator Eutrophication Ilyanassa obsoleta Estuarine management Bottom–up 

Notes

Acknowledgments

We thank C. Haight, K. Lockfield, K. Mullin, M. Poole, T. Richards, and S. Wilkins for field and laboratory assistance. We thank A. Giblin, H. Garrit, L. Deegan, and research assistants on the Plum Island Estuary Long Term Ecological Research program for providing pre-treatment snail density data. Comments from J.W. Fleeger, P. Pascal, A. Ritter, and three anonymous reviewers greatly improved this manuscript. The National Science Foundation funded this work under grants Nos. 9726921, 0213767, 0816963, 1058747, and 0423565.

References

  1. Allen, E.A., P.E. Fell, M.A. Peck, J.A. Gieg, C.R. Guthke, and M.D. Newkirk. 1994. Gut contents of common mummichogs, Fundulus heteroclitus L., in a restored impounded marsh and in natural reference marshes. Estuaries 17: 462–471.CrossRefGoogle Scholar
  2. Bertness, M.D., C. Crain, C. Holdredge, and N. Sala. 2008. Eutrophication and consumer control of New England salt marsh primary productivity. Conservation Biology 22: 131–139.CrossRefGoogle Scholar
  3. Bianchi, T.S., and J.S. Levinton. 1981. Nutrition and food limitation of deposit-feeders. II. Differential effects of Hydrobia totteni and Ilyanassa obsoleta on the microbial community. Journal of Marine Research 39: 547–556.Google Scholar
  4. Brenchley, G.A. 1987. Herbivory in juvenile Ilyanassa obsoleta (Neogastropoda). Veliger 30: 167–172.Google Scholar
  5. Brown, C.L., and S.N. Luoma. 1995. Use of the euryhaline bivalve Potamocorbula amurensis as a biosentinel species to assess trace metal contamination in San Francisco Bay. Marine Ecology Progress Series 124: 129–142.CrossRefGoogle Scholar
  6. Bryan, G.W., P.E. Gibbs, R.J. Huggett, L.A. Curtis, D.S. Bailey, and D.M. Dauer. 1989. Effects of tributyltin pollution on the mud snail, Ilyanassa obsoleta, from the York River and Sarah Creek, Chesapeake Bay. Marine Pollution Bulletin 20: 458–462.CrossRefGoogle Scholar
  7. Carlton, J.T. 1992. Introduced marine and estuarine mollusks of North America: an end-of-the-20th century perspective. Journal of Shellfish Research 11: 489–505.Google Scholar
  8. Carpenter, S.R., S.W. Chisholm, C.J. Krebs, D.W. Schindler, and R.F. Wright. 1995. Ecosystem experiments. Science 26: 324–326.CrossRefGoogle Scholar
  9. Cloern, J.E. 2001. Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series 210: 223–253.CrossRefGoogle Scholar
  10. Connor, M.S., and R.K. Edgar. 1982. Selective grazing by the mud snail Ilyanassa obsoleta. Oecologia 53: 271–275.CrossRefGoogle Scholar
  11. Curtis, L.A. 1994. A decade-long perspective on a bioindicator of pollution—imposex in Ilyanassa obsoleta on Cape Henlopen, Delaware Bay. Marine Environmental Research 38: 291–302.CrossRefGoogle Scholar
  12. Curtis, L.A., and L.E. Hurd. 1979. On the broad nutritional requirements of the mud snail, Ilyanassa (Nassarius) obsoleta (Say), and its polytrophic role in the food web. Journal of Experimental Marine Biology and Ecology 41: 289–297.CrossRefGoogle Scholar
  13. Curtis, L.A., and L.E. Hurd. 1983. Age, sex, and parasites—spatial heterogeneity in a sandflat population of Ilyanassa obsoleta. Ecology 64: 819–828.CrossRefGoogle Scholar
  14. Curtis, L.A., J.L. Kinley, and N.L. Tanner. 2000. Longevity of oversized individuals: growth, parasitism, and history in an estuarine snail population. Journal of the Marine Biological Association of the United Kingdom 80: 811–820.CrossRefGoogle Scholar
  15. Deegan, L.A., J.L. Bowen, D. Drake, J.W. Fleeger, C.T. Friedrichs, K.A. Galván, J.E. Hobbie, C. Hopkinson, J.M. Johnson, D.S. Johnson, L.E. Lemay, E. Miller, B.J. Peterson, C. Picard, S. Sheldon, J. Vallino, and R.S. Warren. 2007. Susceptibility of salt marshes to nutrient enrichment and predator removal. Ecological Applications 17: S42–S63.CrossRefGoogle Scholar
  16. Deegan, L.A., D.S. Johnson, R.S. Warren, B.J. Peterson, J.F. Fleeger, S. Fagherazzi, and W.M. Wollheim. 2012. Coastal eutrophication as a driver of saltmarsh loss. Nature. Google Scholar
  17. DeWitt, T.H., and J.S. Levinton. 1985. Disturbance, emigration, and refugia: how the mud snail, Ilyanassa obsoleta (Say), affects the habitat distribution of an epifunal ampipod, Microdeutopus gryllotalpa (Costa). Journal of Experimental Marine Biology and Ecology 92: 97–113.CrossRefGoogle Scholar
  18. Diaz, R.J., and R. Rosenberg. 2008. Spreading dead zones and consequences for marine ecosystems. Science 321: 926–929.CrossRefGoogle Scholar
  19. Drolet, D., M.A. Barbeau, M.R.S. Coffin, and D. Hamilton. 2009. Effect of the snail Ilyanassa obsoleta (Say) on dynamics of the amphipod Corophium volutator (Pallas) on an intertidal mudflat. Journal of Experimental Marine Biology and Ecology 368: 189–195.CrossRefGoogle Scholar
  20. Dunn, R., L.S. Mullineaux, and S.W. Mills. 1999. Resuspension of postlarval soft-shell clams Mya arenaria through disturbance by the mud snail Ilyanassa obsoleta. Marine Ecology Progress Series 180: 223–232.CrossRefGoogle Scholar
  21. Environmental Protection Agency. 2002. Mid-Atlantic integrated assessment (MAIA) estuaries 1997–1998. Summary report. Narragansett: U.S. Environmental Protection Agency, Office of Research and Development, National Health and Environ Mental Effects Research Laboratory, Atlantic Ecology Division.Google Scholar
  22. 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
  23. Fox, S.E., M. Teichberg, Y.S. Olsen, L. Heffner, and I. Valiela. 2009. Restructuring of benthic communities in eutrophic estuaries: lower abundance of prey leads to trophic shifts from omnivory to grazing. Marine Ecology Progress Series 380: 43–57.CrossRefGoogle Scholar
  24. Galván, K.A., 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
  25. Green, P.A., C.J. Vörösmarty, M. Meybeck, J.N. Galloway, B.J. Peterson, and E.W. Boyer. 2004. Pre-industrial and contemporary fluxes of nitrogen through rivers: a global assessment based on typology. Biogeochemistry 68: 71–105.CrossRefGoogle Scholar
  26. Hamilton, D.J., A.W. Diamond, and P.G. Wells. 2006. Shorebirds, snails, and the amphipod (Corophium volutator) in the upper Bay of Fundy: top–down vs. bottom–up factors, and the influence of compensatory interactions on mudflat ecology. Hydrobiologia 567: 285–306.CrossRefGoogle Scholar
  27. Hunt, J.H., W.G. Ambrose Jr., and C.H. Peterson. 1987. Effects of the gastropod, Ilyanassa obsoleta (Say), and the bivalve, Mercenaria mercenaria (L.), on larval settlement and juvenile recruitment of infauna. Journal of Experimental Biology and Ecology 108: 229–240.CrossRefGoogle Scholar
  28. Johnson, D.S. 2011. High-marsh invertebrates are susceptible to eutrophication. Marine Ecology Progress Series 438: 143–152.CrossRefGoogle Scholar
  29. 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.Google Scholar
  30. 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. Estuaries and Coasts 30: 226–237.Google Scholar
  31. Johnson, D.S., J.W. Fleeger, and L.A. Deegan. 2009. Large-scale manipulations reveal that top-down and bottom-up controls interact to alter habitat utilization by saltmarsh fauna. Marine Ecology Progress Series 377: 33–41.CrossRefGoogle Scholar
  32. Kelaher, B., J.S. Levinton, and J.M. Hoch. 2003. Foraging by the mud snail, Ilyanassa obsoleta (Say), modulates spatial variation in benthic community structure. Journal of Experimental Marine Biology and Ecology 292: 139–157.CrossRefGoogle Scholar
  33. Kneib, R.T. 1986. The role of Fundulus heteroclitus in salt marsh trophic dynamics. American Zoologist 26: 259–269.Google Scholar
  34. Legendre, P. 1998. Model II regression user's guide, R edition. R Vignette.Google Scholar
  35. Leise, E.M., S.J. Froggett, J.E. Nearhoff, and L.B. Cahoon. 2009. Diatom cultures exhibit differential effects on larval metamorphosis in the marine gastropod Ilyanassa obsoleta (Say). Journal of Experimental Marine Biology and Ecology 379: 51–59.CrossRefGoogle Scholar
  36. Levine, J.M., J.S. Brewer, and M.D. Bertness. 1998. Nutrients, competition and plant zonation in a New England salt marsh. Journal of Ecology 86: 285–292.CrossRefGoogle Scholar
  37. Levinton, J.S., D.E. Martinez, M.M. McCartney, and M.L. Judge. 1995. The effect of water flow on movement, burrowing, and distributions of the gastropod Ilyanassa obsoleta in a tidal creek. Marine Biology 122: 417–424.CrossRefGoogle Scholar
  38. Lockfield, K. 2011. Population-level responses of the mummichog,Fundulus heteroclitus, to chronic nutrient enrichment in a New England salt marsh. Master’s Thesis. Louisiana State University, Baton Rouge, LA.Google Scholar
  39. Lorenzen, G.L. 1967. Determination of chlorophyll and phaeopigments; spectrophotometric equations. Limnology and Oceanography 12: 343–346.CrossRefGoogle Scholar
  40. Nixon, S.W. 1995. Coastal marine eutrophication—a definition, social causes, and future concerns. Ophelia 41: 199–219.Google Scholar
  41. Novak, M., M. Lever, and I. Valiela. 2001. Top–down vs. bottom–up controls of microphytobenthic standing crop: role of mud snails and nitrogen supply in the littoral of Waquoit Bay estuaries. The Biological Bulletin 201: 292–294.CrossRefGoogle Scholar
  42. Pascal, P-Y, J.W. Fleeger, H.T.S. Boshker, H. Mitwally, and D.S. Johnson. 2012. Chronic nutrient-enrichment influence on mudflat food web in a New England (USA) estuary. Marine Ecology Progress Series. Google Scholar
  43. Recher, H.F. 1966. Some aspects of the ecology of migrant shorebirds. Ecology 47: 393–407.Google Scholar
  44. R Development Core Team. 2009. 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.
  45. Say, T. 1822. An account of some of the marine shells of the United States. Journal of the Academy of Natural Sciences of Philadelphia 2:221–248, 257–276, 302–325.Google Scholar
  46. Scheltema, R.S. 1961. Metamorphosis of the veliger larvae of Nassarius obsoletus (Gastropoda) in response to bottom sediment. The Biological Bulletin 120: 92–109.CrossRefGoogle Scholar
  47. Scheltema, R.S. 1964. Feeding habits and growth in the mud-snail Nassarius obsoletus. Chesapeake Science 5: 161–166.CrossRefGoogle Scholar
  48. Schindler, D.W. 1998. Replication versus realism: the need for ecosystem-scale experiments. Ecosystems 4: 323–334.CrossRefGoogle Scholar
  49. Sun, B., and J.W. Fleeger. 1994. Field experiments on the colonization of meiofauna into sediment depressions. Marine Ecology Progress Series 110: 167–175.CrossRefGoogle Scholar
  50. Turgeon, D.D., J.F. Quinn, Jr., A.E. Bogan, E.V. Coan, F.G. Hochberg, W.G. Lyons, P. M. Mikkelsen, R.J. Neves, C.F.E. Roper, G. Rosenberg, B. Roth, A. Scheltema, F.G. Thompson, M. Vecchione, and J.D. Williams. 1998. Common and scientific names of aquatic invertebrates from the United States and Canada: Mollusks, 2nd ed. In American Fisheries Society Special Publication 26. 526.Google Scholar
  51. Wigand, C., R.A. McKinney, M.A. Charpentier, M.M. Chintala, and G.B. Thursby. 2003. Relationships of nitrogen loadings, residential development, and physical characteristics with plant structure in New England salt marshes. Estuaries 26: 1494–1504.CrossRefGoogle Scholar
  52. Young, T., S. Komarow, L. Deegan, and R. Garritt. 1999. Population size and summer home range of the green crab, Carcinus maenas, in salt marsh tidal creeks. Biological Bulletin 197: 297–299.Google Scholar

Copyright information

© Coastal and Estuarine Research Federation 2012

Authors and Affiliations

  1. 1.Marine Biological LaboratoryWoods HoleUSA
  2. 2.Brown UniversityProvidenceUSA

Personalised recommendations