, Volume 713, Issue 1, pp 97–114 | Cite as

Long-term nutrient enrichment elicits a weak density response by saltmarsh meiofauna

  • Hanan M. Mitwally
  • John W. Fleeger
Primary Research Paper


The effect of chronic nutrient enrichment on benthic meiofauna was examined in a whole-ecosystem experiment conducted in salt marshes in the Plum Island watershed of northeastern Massachusetts, USA. We compared abundances of total meiofauna, nematodes, copepods, ostracods, and annelids including Manayunkia aestuarina, in fertilized (where N and P was increased 15× in incoming tidal water throughout each growing season for 6 years) and reference marsh creeks to test for bottom-up responses. Although some responses to nutrient enrichment were evident, results did not match our expectations of strong increases in abundance. Variation in abundance between nutrient-enriched and reference creeks was detected in all three subhabitats but responses were inconsistent and variable over time, suggesting that natural variability was greater than variation induced by fertilization. Our results showed an overall weak negative correlation between meiofauna abundance and benthic microalgae (BMA) biomass partly because the BMA response to nutrient enrichment was relatively small and perhaps limited by grazing macrofauna and nekton. Our results suggest a better mechanistic understanding of the relationship between BMA and meiofaunal abundance is needed to fully understand how nutrient enrichment affects meiofauna.


Bottom-up effects Meiofauna Natural variability Benthic microalgae Manayunkia aestuarina 



We thank Dr. J. Geagan for his statistical consultations and we also thank Ms. S. Terrebonne for help with SAS programming. We greatly appreciate Dr. Linda Deegan and Dr. David Johnson for making data from the TIDE project available for us. The first author expresses her deep gratitude to the Fulbright Commission for support that allowed her to do this research at the USA. This material is based upon work supported by the National Science Foundation under Grant Nos. 0213767 and 9726921. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.


  1. Anderson, M. J., 2005. Permanova: a FORTRAN computer program for Permutational multivariate analysis of Variance. Department of Statistics, University of Auckland, New Zealand: 24 pp.Google Scholar
  2. Armitage, A. R. & P. Fong, 2004. Upward cascading effects of nutrients: shifts in a benthic microalgal community and a negative herbivore response. Oecologia 139: 560–567.PubMedCrossRefGoogle Scholar
  3. Austen, M. C. & S. Widdicombe, 1998. Experimental evidence of effects of the heart Urchin Brissopsis lyrifera on associated subtidal meiobenthic nematode communities. Journal of Experimental Marine Biology and Ecology 222: 219–238.CrossRefGoogle Scholar
  4. Austen, M. C., R. M. Warwick & M. C. Rosado, 1989. Meiobenthic and macrobenthic community structure along putative pollution gradient in southern Portugal. Marine Pollution Bulletin 20: 398–404.CrossRefGoogle Scholar
  5. Austen, M. C., S. Widdicombe & N. Villano-Pitacco, 1998. Effects of biological disturbance on diversity and structure of meiobenthic nematode communities. Marine Ecology Progress Series 174: 233–246.CrossRefGoogle Scholar
  6. Bianchi, T. S. & J. S. Levinton, 1981. Nutrition and food limitation of deposit feeders. II. Differential effects of Hydobia totteni and Ilyanassa obsoleta on the microbial community. Journal of Marine Research 39: 547–556.Google Scholar
  7. Bowen, J. L., B. C. Crump, L. A. Deegan & J. E. Hobbie, 2009a. Increased supply of ambient nitrogen has minimal effect on salt marsh bacterial production. Limnology and Oceanography 54(3): 713–722.CrossRefGoogle Scholar
  8. Bowen, J. L., B. C. Crump, L. A. Deegan & J. E. Hobbie, 2009b. Salt marsh sediment bacteria: their distribution and response to external nutrient inputs. International Society for Microbial Ecology 3: 924–934.Google Scholar
  9. Braeckman, U., P. Provoost, T. Moens, K. Soetaert, J. J. Middelburg, M. Vincx & J. Vanaverbeke, 2011a. Biological vs. physical mixing effects on benthic food web dynamics. PLoS ONE 6(3): 1:12 e18078.Google Scholar
  10. Braeckman, U., C. V. Colen, K. soetaert, M. Vincx & J. Vanaverbeke, 2011b. Contrasting macrobenthic activities differentially affect nematode density and diversity in a shallow subtidal marine sediment. Marine Ecology Progress Series 422: 179–191.CrossRefGoogle Scholar
  11. Carman, K. R., J. W. Fleeger & S. M. Pomarico, 1997. Response of a benthic food web to hydrocarbon contamination. Limnology and Oceanography 42: 561–571.CrossRefGoogle Scholar
  12. Chandler, G. T. & J. W. Fleeger, 1983. Meiofaunal colonization of azoic estuarine sediment in Louisiana: mechanisms of dispersal. Journal of Experimental Marine Biology and Ecology 69: 175–188.CrossRefGoogle Scholar
  13. Cloern, J. E., 2001. Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series 210: 223–253.CrossRefGoogle Scholar
  14. Connor, M. S. & J. M. Teal, 1981. The effect of feeding by mud snails, Ilyanassa obsoleta (say), on the structure and metabolism of a laboratory benthic algal community. Journal of Experimental Marine Biology and Ecology 65: 29–45.CrossRefGoogle Scholar
  15. Coull, B. C., 1985. Long term variability of estuarine meiobenthose: an 11 year study. Marine Ecology Progress Series 24: 205–218.CrossRefGoogle Scholar
  16. Coull, B. C., 1986. Long term variability of meiobenthos: value, synopsis, hypothesis generation and predictive modeling. Hydrobiologia 142: 271–279.CrossRefGoogle Scholar
  17. Danovaro, R., M. Fabiano & M. Vincx, 1995. Meiofauna response to the Agip Abruzzo Oil spill in subtidal sediments of the Ligurian Sea. Marine Pollution Bulletin 30(2): 133–145.CrossRefGoogle Scholar
  18. Deegan, L. A. & R. H. Garritt, 1997. Evidence for spatial variability in estuarine food webs. Marine Ecology Progress Series 147: 31–47.CrossRefGoogle Scholar
  19. Deegan, L. A., J. L. Bowen, D. Drake, J. W. Fleeger, C. T. Friedeichs, K. A. Galván, J. E. Hobbie, C. Hopkinson, D. S. Johnson, J. M. Johnson, L. E. May, E. Miller, B. J. Peterson, C. Picard, S. Sheldon, M. Sutherland, J. Vallino & R. S. Warren, 2007. Susceptibility of salt marshes to nutrient enrichment and predator removal. Ecological Applications 17: S42–S63.CrossRefGoogle Scholar
  20. Deegan, L. A., D. S. Johnson, R. S. Warren, B. J. Peterson, J. W. Fleeger, S. Fagherazzi & W. M. Wollheim, 2012. Coastal eutrophication as a driver of saltmarsh loss. Nature 490: 388–394.PubMedCrossRefGoogle Scholar
  21. Delaune, R. D., C. J. Smith, W. H. Patrick, J. W. Fleeger & M. D. Tolley, 1984. Effect of oil on salt marsh biota: methods for restoration. Environment Pollution 36: 207–227.Google Scholar
  22. Diaz, D. & Rj. J. Rosenberg, 2008. Spreading dead zones and consequences for marine ecosystems. Science 321: 926–929.Google Scholar
  23. Edwards, D. & B. C. Coull, 1987. Autoregressive trend analysis: an example using long term ecological data. Oikos 50: 95–102.CrossRefGoogle Scholar
  24. Emberton Jr., K., 1981. Season-depth relations in subtidal meiofauna of Cape Cod Bay. Estuaries 4: 121–126.CrossRefGoogle Scholar
  25. Findlay, S. E. G., 1982. Effect of detrital nutritional quality on population dynamics of a marine nematode (Diplolaimella chitwoodi). Marine Biology 68: 223–227.CrossRefGoogle Scholar
  26. Fleeger, J. W. & K. R. Carman, 2011. Experimental and genetic studies of meiofauna assess environmental quality and reveal mechanisms of toxicity. Vie et Milieu 61: 1–26.Google Scholar
  27. Fleeger, J. W. & G. T. Chandler, 1983. Meiofauna responses to an experimental oil spill in a Louisiana Saltmarsh. Marine Ecology Progress Series 11: 257–264.CrossRefGoogle Scholar
  28. Fleeger, J. W., S. A. Whipple & L. L. Cook, 1982. Field manipulations of tidal flushing, light exposure and natant macrofauna in a Louisiana Salt marsh; effects on meiofauna. Journal of Experimental Marine Biology and Ecology 56: 87–100.CrossRefGoogle Scholar
  29. Fleeger, J. W., T. C. Shirley & D. A. Ziemann, 1989. Meiofaunal response to sedimentation from an Alaskan spring bloom. I. Major taxa. Marine Ecology Progress Series 57: 137–145.Google Scholar
  30. Fleeger, J. W., G. Tita, K. R. Carman, R. N. Millward, E. B. Moser & R. P. Gambrell, 2006. Does bioturbation by a benthic fish modify the effects of sediment contamination on saltmarsh microalgae and meiofauna? Journal of Experimental Marine Biology and Ecology 330: 180–194.CrossRefGoogle Scholar
  31. Fleeger, J. W., D. S. Johnson, K. A. Galván & L. A. Deegan, 2008. Top-down and bottom-up control of infauna varies across the salt marsh landscape. Journal of Experimental Marine Biology and Ecology 357: 20–34.CrossRefGoogle Scholar
  32. Foreman, K. H., 1989. Regulation of benthic microalgal and meiofaunal productivity and standing stock in a salt marsh ecosystem: the relative importance of resources and predation. Ph.D. Boston University, Massachusetts, USA: 235 pp.Google Scholar
  33. Foreman, K., I. Valiela & R. Sardà’, 1995. Controls of benthic marine food webs. Scientia Marina 59: 119–128.Google Scholar
  34. Galván, K. A., J. W. Fleeger & B. Fry, 2008. Stable isotope addition reveals dietary importance of phytoplankton and microphytobenthos to salt marsh infauna. Marine Ecology Progress Series 359: 37–49.CrossRefGoogle Scholar
  35. Giere, O., 1993. Meiobenthology. The Microscopic in Aquatic Sediments. Springer, Berlin: 300 pp.CrossRefGoogle Scholar
  36. Gourbault, N. E., 1987. Long term monitoring of marine nematode assemblages in the Morlaix Estuary (France) following the Amoco Cadiz Oil Spill. Estuarine Coastal and Shelf Sciences 24: 657–670.CrossRefGoogle Scholar
  37. Gregg, C. S. & J. W. Fleeger, 1998. Grass shrimp Palaemonetes pugio predation on sediment and stem dwelling meiofauna: field and laboratory experiments. Marine Ecology Progress Series 175: 77–86.CrossRefGoogle Scholar
  38. Hicks, G. R. F., 1980. Structure of phytal hapacticoida copepod assemblages and the influence of habitat complexity and turbidity. Journal Experimental of Marine Biology and Ecology 44: 157–192.CrossRefGoogle Scholar
  39. Hillebrand, H., M. Kahlert, A. L. Haglund, U. G. Berninger, S. Nagel & S. Wickham, 2002. Control of microbenthic communities by grazing and nutrient supply. Ecology 83(8): 2205–2219.CrossRefGoogle Scholar
  40. Huys, R., M. Gee, C. G. Moore & R. Hamond, 1996. Marine and brackish water harpacticoid copepods. Part 1. In Barnes, R. S. K. & J. H. Crothers (eds), Synopses of the British fauna (New Series). London: 350 pp.Google Scholar
  41. Jakobsen, K. K. & A. E. Giblin, 2010. The effect of increased nitrate loading on nitrate reduction via dentrification and DNRA in salt marsh sediment. Limnology and Oceanography 55(2): 789–802.CrossRefGoogle Scholar
  42. Johnson, D. S., 2011. High-marsh invertebrates are susceptible to eutrophication. Marine Ecology Progress Series 438: 143–152.CrossRefGoogle Scholar
  43. Johnson, D. S. & J. W. Fleeger, 2009. Weak response of salt marsh 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
  44. Johnson, D. S. & M. I. Short, 2013. Chronic nutrient enrichment increases the density and biomass of the mudsnail, Nassarius obsoletus. Estuaries and Coasts 36: 28–35.CrossRefGoogle Scholar
  45. Johnson, D. S., J. W. Fleeger, K. A. Galván & 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
  46. Johnson, D. S., J. W. Fleeger & 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
  47. Kelaher, B. P., A. J. underwood & M. G. Chapman, 2003. Experimental transplantations of Coralline algal truf to demonstrate causes of differences in macrofauna at different tidal height. Journal of Marine Biology and Ecology 282(1–2): 23–41.CrossRefGoogle Scholar
  48. Lei, Y., K. Stumm, N. Volkenborn, S. A. Wickham & U. G. Berninger, 2010. Impact of Arenicola marina (Polychaeta) on the microbial assemblages and meiobenthos in a marine intertidal flat. Marine Biology 157: 1271–1282.CrossRefGoogle Scholar
  49. Levin, L. A. & T. S. Talley, 2002. Natural and manipulated sources of heterogeneity controlling early faunal development of a salt marsh. Ecological Applications, Special Issue 12: 1785–1802.CrossRefGoogle Scholar
  50. Lockfield, K., 2011. Chronic nutrient enrichment effects on mummichog, Fundulus heteroclitus in a northeastern Massachusetts salt marsh. Master thesis, Louisiana State University, Baton Rouge, USA: 80 pp.Google Scholar
  51. Lorenzen, G. L., 1967. Determination of chlorophyll and phaeopigments; spectrophotometric equations. Limnology and Oceanography 12: 343–346.CrossRefGoogle Scholar
  52. McCormick, P. V., 1991. Lotic protistan herbivore selectivity and its potential impact on benthic algal assemblages. Journal of North American Benthological Society 10: 238–250.CrossRefGoogle Scholar
  53. Modig, H., W. J. Van de Bund & E. Ólafsson, 2000. Uptake of phytodetritus by three ostracod species from the Baltic Sea: effects of amphipod disturbance and ostracod density. Marine Ecology Progress Series 202: 125–134.CrossRefGoogle Scholar
  54. Moens, T., L. Verbeeck & M. Vincx, 1999. Feeding biology of a predatory and a facultatively predatory nematode (Enoploides longispiculosus and Adoncholaimus fuscus). Marine Biology 134: 585–593.CrossRefGoogle Scholar
  55. Moens, T., P. Herman, I. Verbeeck, M. Steyaert & M. Vincx, 2000. Predation rates and prey selectivity in two predacious estuarine nematode species. Marine Ecology Progress Series 205: 185–193.CrossRefGoogle Scholar
  56. Montagna, P. A., 1995. Rates of metazoan meiofaunal microbivory: a review. Vie et Milieu 45: 1–10.Google Scholar
  57. Nascimento, F. J. A., 2010. Trophic ecology of meiofauna. Responses to sedimentation of phytoplankton blooms in the Baltic Sea. PhD in Marine Ecology, Stockholm, Sweden. ISBN: 978-91-7447-083-3.Google Scholar
  58. Nichols, J. A. & J. R. Robertson, 1979. Field evidence that the eastern mud snail Ilyanassa obsoleta, influences nematode community structure. The Nautilus 93: 44–46.Google Scholar
  59. Nixon, S. W., 1995. Coastal marine eutrophication: a definition, social causes and future concerns. Ophelia 41: 199–219.Google Scholar
  60. Ólafsson, E., J. Ullberg & N. L. Arroyo, 2005. The clam Macoma balthica prevents in situ growth of microalgal mats: implications for meiofaunal assemblages. Marine Ecology Progress Series 298: 179–188.CrossRefGoogle Scholar
  61. Pace, M. L., S. Shimmel & W. M. Darley, 1979. The effect of grazing by a gastropod Nassarius obsoletus on the benthic microbial community of a salt marsh mudflat. Estuarine and Coastal Marine Science 9: 121–134.CrossRefGoogle Scholar
  62. Pascal, Y. P., J. W. Fleeger, H. T. S. Boschker, H. M. Mitwally & D. S. Johnson, 2013. Top-down control may mask the bottom up effects of nutrient enrichment on benthic microalgae in estuarine mudflats. Marine Ecology Progress series in print.Google Scholar
  63. Piereira, T. J., A. Martinez-Arce, R. Gingold, & A. R. Olivares, 2008. Direct nematode predation in the marine nematode Synonchiella spiculara (Selachinematidae:nematode). Journal of Marine Biological Association JMBA2-Biodiversity records-published on line-1:3.Google Scholar
  64. Posey, M., C. Power, L. Cahoon & D. Lindquist, 1995. Top down vs. bottom up control of benthic community composition on an intertidal tide flat. Journal of Experimental Marine Biology and Ecology 185: 19–31.CrossRefGoogle Scholar
  65. Posey, M. H., T. D. Alphin, L. Cahoon, D. G. Lindquiest, M. A. Mallin & M. B. Nevers, 2002. Top-down versus bottom up limitation in benthic infaunal communities: direct and indirect effects. Estuaries 25: 99–1014.CrossRefGoogle Scholar
  66. Power, M. E., 1992. Top-down and bottom up forces in food webs: do plants have primacy? Ecology 73: 733–746.CrossRefGoogle Scholar
  67. Santos, P. J. P., M. L. Botter-Carvalho, A. B. Nascimento-Junior, R. G. C. Marinho, P. V. C. Carvalho & P.C. Valenca, 2009. Response of estuarine meiofauna assemblage to effects of fertilizer enrichment used in the sugar cane monoculture. Pernambuco, Brazil. Brazalian Journal of Oceanography 57(1): 43–55.Google Scholar
  68. Sardá, R., I. Valiela & 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
  69. SAS Institute Inc., 1991. SAS User’s Guide: Statistics. SAS Institute Inc, Cary, North Carolina.Google Scholar
  70. Schratzberger, M. & R. M. Warwick, 1999. Impact of predation and sediment disturbance by Carcinus maenas (L.) on free-living nematode community structure. Journal of Experimental Marine Biology and Ecology 235: 255–271.CrossRefGoogle Scholar
  71. Schratzberger, M., F. Daniel, C. M. Wall, R. Kilbride, S. J. Macnaughton, S. E. Boyed, H. L. Rees, K. Lee & R. P. J. Swannell, 2003. Response of estuarine meio-and macrofauna to in situ bioremediation of oil contaminated sediment. Marine Pollution Bulletin 46: 430–443.PubMedCrossRefGoogle Scholar
  72. Somerfield, P. J. & R. M. Warwick, 1996. Meiofauna in marine pollution monitoring programmes: a laboratory Manual. Ministry of Agriculture, Fisheries and Food, Directorate of Fisheries, Lowestoft.Google Scholar
  73. Sommer, U., 2001. Reversal of density dependence of juvenile Littorina littorea (Gastropoda) growth in response to periphyton nutrient status. Journal of Sea Research 45: 95–103.CrossRefGoogle Scholar
  74. SYSTAT, 1998. Computer Software for Statistics. Copyright @1998 by SPSS Inc. ISBNI-56827-222-7, USA.Google Scholar
  75. Valiela, I., J. McClelland, J. Hauxwell, P. J. Behr, D. Hersh & K. Foreman, 1997. Macroalgal blooms in shallow estuaries: controls and eco-physiological and ecosystem consequences. Limnology and Oceanography 42: 1105–1118.CrossRefGoogle Scholar
  76. Valiela, I., D. Rutecki & S. Fox, 2004. Salt marshes: biological controls of food webs in a diminishing environment. Journal of Experimental Marine Biology and Ecology 300: 131–159.CrossRefGoogle Scholar
  77. Warwick, R. M., 1981. The nematode copepod ratio and its use in pollution ecology. Marine Pollution Bulletin 12: 329–333.CrossRefGoogle Scholar
  78. Warwick, R. M., H. M. Platt, K. R. Clarke, J. Agard & J. Gobin, 1990. Analysis of macrobenthic and meiobenthic community structure in relation to pollution and disturbance in Hamilton Harbour, Bermuda. Journal of Experimental Marine Biology and Ecology 138: 119–142.CrossRefGoogle Scholar
  79. Wynberg, R. P. & G. M. Branch, 1994. Disturbance associated with bait- collection for sand prawns (Callianassa Kraussi) and mud prawns (Upogebia Africana): long-term effects on the biota of intertidal sand flats. Journal of Marine Research 52: 523–558.CrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of Biological SciencesLouisiana State UniversityBaton RougeUSA
  2. 2.Oceanography Department, Faculty of ScienceUniversity of AlexandriaAlexandriaEgypt

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