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Spatial and Temporal Changes in Estuarine Food Web Structure: Differential Contributions of Marsh Grass Detritus

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Abstract

We measured stable isotope signatures and fatty acid profiles in dominant consumers and basal food sources to assess spatial and temporal changes in the trophic structure within an estuarine ecosystem. The consumers analyzed included zooplankton, benthic invertebrates and fishes from the upper, middle and lower reaches of the estuary collected over four seasons. The contributions of different food sources to the consumers were assessed using the isotopic mixing model stable isotope analysis in R (SIAR). Our stable isotope and fatty acid data indicated that the food webs differed significantly among reaches and seasons within the estuary. Benthic invertebrates exhibited lower carbon isotopic (δ13C) values in the upper reaches of the estuary during all seasons, with lowest values occurring during autumn. In contrast, nitrogen isotopic (δ15N) values of consumers were higher in the upper reaches of the estuary and were highest during summer and spring. SIAR models and fatty acid compositional data both indicated greater utilization of marsh grass by consumers inhabiting the lower reaches of the estuary, particularly during autumn and winter. Our data indicated that differential inputs of detritus contributed to spatial changes in the benthic estuarine food web structure and that the trends changed throughout the year.

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References

  • Akin, S., K.O. Winemiller, and F.P. Gelwick. 2003. Seasonal and spatial variation in fish and macrocrustacean assemblage structure in Mad Island Marsh estuary, Texas. Estuarine Coastal and Shelf Science 57: 269–282.

    Google Scholar 

  • Alfaro, A.C., F. Thomas, L. Sergent, and M. Duxbury. 2006. Identification of trophic interactions within an estuarine food web (northern New Zealand) using fatty acid biomarkers and stable isotopes. Estuarine, Coastal and Shelf Science 70: 271–286.

    Article  Google Scholar 

  • Antonio, E.S., A. Kasai, M. Ueno, Y. Ishihi, H. Yokoyama, and Y. Yamashita. 2012. Spatial-temporal feeding dynamics of benthic communities in an estuary-marine gradient. Estuarine, Coastal and Shelf Science 112: 86–97.

    Article  CAS  Google Scholar 

  • Arts, M.T., R.G. Ackman, and B.J. Holub. 2001. “Essential fatty acids” in aquatic ecosystems: a crucial link between diet and human health and evolution. Canadian Journal of Fisheries and Aquatic Sciences 58: 122–137.

    Article  CAS  Google Scholar 

  • Attrill, M.J. 2002. A testable linear model for diversity trends in estuaries. Journal of Animal Ecology 71: 262–269.

    Article  Google Scholar 

  • Baeta, A., R. Pinto, I. Valiela, P. Richard, N. Niquil, and J.C. Marques. 2009. δ15N and δ13C in the Mondego estuary food web: seasonal variation in producers and consumers. Marine Environmental Research 67: 109–116.

    Article  CAS  Google Scholar 

  • Bergamino, L., T. Dalu, and N.B. Richoux. 2014. Spatial and temporal changes in sediment organic matter composition within an estuarine environment: stable isotope and fatty acid analyses. Hydrobiologia. doi:10.1007/s10750-014-1853-1.

    Google Scholar 

  • Boecklen, W.J., T.C. Yarnes, B.A. Cook, and A.C. James. 2011. On the use of stable isotopes in trophic ecology. Annual Review of Ecology, Evolution, and Systematics 42: 411–440.

    Article  Google Scholar 

  • Bok, A. 1983. The demography, breeding biology and management of two mullet species (Pisces: Mugilidae) in the Eastern Cape, South Africa.

  • Bouillon, S., N. Koedam, W. Baeyens, B. Satyanarayana, and F. Dehairs. 2004. Selectivity of subtidal benthic invertebrate communities for local microalgal production in an estuarine mangrove ecosystem during the post-monsoon period. Journal of Sea Research 51: 133–144.

    Article  Google Scholar 

  • Bouma, T.J., M.B. De Vries, E. Low, L. Kusters, P.M.J. Herman, I.C. Tanczos, S. Temmerman, A. Hesselink, P. Meire, and S. van Regenmortel. 2005. Flow hydrodynamics on a mudflat and in salt marsh vegetation: identifying general relationships for habitat characterizations. Hydrobiologia 540: 259–274.

    Article  Google Scholar 

  • Claudino, M.C., P.C. Abreu, and A.M. Garcia. 2013. Stable isotopes reveal temporal and between-habitat changes in trophic pathways in a southwestern Atlantic estuary. Marine Ecology Progress Series 489: 29–42.

    Article  CAS  Google Scholar 

  • Connolly, R.M., D. Gorman, and M.A. Guest. 2005. Movement of carbon among estuarine habitats and its assimilation by invertebrates. Oecologia 144: 684–691.

    Article  Google Scholar 

  • Currin, C.A., S.Y. Newell, and H.W. Paerl. 1995. The role of standing dead Spartina alterniflora and benthic microalgae in salt marsh food webs: considerations based on multiple stable isotope analysis. Marine Ecology Progress Series 121: 99–116.

    Article  Google Scholar 

  • Cyrus, D.P. 1988. Episodic events and estuaries: effects of cyclonic flushing on the benthic fauna and diet of Solea bleekeri (Teleostei) in Lake St Lucia on the south-eastern coast of Africa. Journal of Fish Biology 33(Supplement A): 1–7.

    Article  Google Scholar 

  • Dalsgaard, J., M. St. John, G. Kattner, D. Müller-Navarra, and W. Hagen. 2003. Fatty acid trophic markers in the pelagic marine environment. Advances in Marine Biology 46: 225–340.

    Article  Google Scholar 

  • Day, J.H. 1969. A guide to marine life on South African shores. Cape Town: A.A. Balkema.

    Google Scholar 

  • Deegan, L.A., and R.H. Garritt. 1997. Evidence for spatial variability in estuarine food webs. Marine Ecology Progress Series 147: 31–47.

    Article  Google Scholar 

  • Deegan, L.A., D.S. Johnson, R.S. Warren, B.J. Peterson, J.W. Fleeger, S. Fagherazzi, and W.M. Wollheim. 2012. Coastal eutrophication as a driver of salt marsh loss. Nature 490: 388–392.

    Article  CAS  Google Scholar 

  • Dubois, S., H. Blanchet, A. Garcia, M. Massé, R. Galois, A. Grémare, K. Charlier, G. Guillou, P. Richard, and N. Savoye. 2014. Trophic resource use by macrozoobenthic primary consumers within a semi-enclosed coastal ecosystem: stable isotope and fatty acid assessment. Journal of Sea Research 88: 87–99.

    Article  Google Scholar 

  • Dunstan, G.A., J.K. Volkman, and S.M. Barrett. 1993. Essential polyunsaturated fatty acids from 14 species of diatom (Bacillariophyceae). Phytochemistry 35: 155–161.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Froneman, P.W. 2001. Seasonal changes in zooplankton biomass and grazing in a temperate estuary, South Africa. Estuarine, Coastal and Shelf Science 52: 543–553.

    Article  CAS  Google Scholar 

  • Froneman, P.W., and T.O. Henninger. 2009. The influence of prolonged mouth closure on selected components of the hyperbenthos in the littoral zone of the temporarily open/closed Kasouga Estuary, South Africa. Estuarine, Coastal and Shelf Science 83: 326–332.

    Article  Google Scholar 

  • Fry, B. 2006. Stable isotope ecology. New York: Springer.

    Book  Google Scholar 

  • Fry, B., and E.B. Sherr. 1984. δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contributions in Marine Science 27: 13–47.

    CAS  Google Scholar 

  • Gning, N., F. Le Loc’h, O.T. Thiaw, C. Aliaume, and G. Vidy. 2010. Estuarine resources use by juvenile Flagfin mojarra (Eucinostomus melanopterus) in an inverse tropical estuary (Sine Saloum, Senegal). Estuarine, Coastal and Shelf Science 86: 683–691.

    Article  CAS  Google Scholar 

  • Guest, M.A., and R.M. Connolly. 2006. Movement of carbon among estuarine habitats: the influence of saltmarsh patch size. Marine Ecology Progress Series 310: 15–24.

    Article  CAS  Google Scholar 

  • Guest, M.A., R.M. Connolly, and N.R. Loneragan. 2004. Carbon movement and assimilation by invertebrates in estuarine habitats at a scale of meters. Marine Ecology Progress Series 278: 27–34.

    Article  CAS  Google Scholar 

  • Hammer, Ø., D.A.T. Harper, and P.D. Ryan. 2001. PAST: palaeontological statistics software package for education and data analysis. Palaeontologia Electronica 4: p 9. Available at: palaeo-electronica.org/2001_1/past/issue1_01.htm.

  • Heinecken, TJ.E., and J.R. Grindley. 1982. Estuaries of the Cape Part II: synopses of available information on individual systems. Report No. 10: Kowie. CSIR Research Report 409.

  • Herman, P.M.J., J.J. Middelburg, J. Van De Kopple, and C.H.R. Heip. 1999. Ecology of estuarine macrobenthos. Advances in Ecological Research 29: 195–240.

    Article  Google Scholar 

  • Hoeinghaus, D.J., and S.E. Davis III. 2007. Size-based trophic shifts of salt-marsh dwelling blue crabs elucidated by dual stable C and N isotope analyses. Marine Ecology Progress Series 334: 199–204.

    Article  CAS  Google Scholar 

  • Hoeinghaus, D.J., J.P. Vieira, C.S. Costa, C.E. Bemvenuti, K.O. Winemiller, and A.M. Garcia. 2011. Estuary hydrogeomorphology affects carbon sources supporting aquatic consumers within and among ecological guilds. Hydrobiologia 673: 79–92.

    Article  CAS  Google Scholar 

  • Indarti, E., M.I.A. Majid, R. Hashim, and A. Chong. 2005. Direct FAME synthesis for rapid total lipid analysis from fish oil and cod liver oil. Journal of Food Composition and Analysis 18: 161–170.

    Article  CAS  Google Scholar 

  • James, N.C., and T.D. Harrison. 2010. A preliminary survey of the estuaries on the southeast coast of South Africa, Cape Padrone—Great Fish River, with particular reference to the fish fauna. Transactions of the Royal Society of South Africa 90: 411–417.

    Google Scholar 

  • Kang, C.K., J.B. Kim, K.S. Lee, P.Y. Lee, and J.S. Hong. 2003. Trophic importance of benthic microalgae to macrozoobenthos in coastal bay systems in Korea: dual stable C and N isotope analyses. Marine Ecology Progress Series 259: 79–92.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Kruskal, J.B., and M. Wish. 1978. Multidimensional scaling. Beverly Hills: Sage Publications.

    Google Scholar 

  • Kwak, T.J., and J.B. Zedler. 1997. Food web analysis of southern California coastal wetlands using multiple stable isotopes. Oecologia 110: 262–277.

    Article  Google Scholar 

  • Lucas, J.S. 1980. Australian species: systematics and biology 33: 148–247.

  • Martinez del Rio, C., N. Wolf, S.A. Carleton, and L.Z. Gannes. 2009. Isotopic ecology ten years after a call for more laboratory experiments. Biological Reviews 84: 91–111.

    Article  Google Scholar 

  • McClelland, J.W., and I. Valiela. 1998. Changes in food web structure under the influence of increased anthropogenic nitrogen inputs to estuaries. Marine Ecology Progress Series 168: 259–271.

    Article  CAS  Google Scholar 

  • McCutchan, J.H., W.M. Lewis, C. Kendall, and C.C. McGrath. 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102: 378–390.

    Article  CAS  Google Scholar 

  • McLeod, R.J., S.R. Wing, and J.P. Davis. 2010. Habitat conversion and species loss alters the composition of carbon sources to benthic communities. Marine Ecology Progress Series 411: 127–136.

    Article  CAS  Google Scholar 

  • McLusky, D.S., and M. Elliott. 2004. The estuarine ecosystem: ecology, threats and management, third ed. Oxford: Oxford University Press.

    Book  Google Scholar 

  • Odum, W.E., and E.J. Heald. 1972. Trophic analyses of an estuarine mangrove community. Bulletin of Marine Science 22: 671–738.

    Google Scholar 

  • Olin, J., N. Hussey, S. Rush, G. Poulakis, C. Simpfendorfer, M. Heupel, and A. Fisk. 2013. Seasonal variability in stable isotopes of estuarine consumers under different freshwater flow regimes. Marine Ecology Progress Series 487: 55–69.

    Article  CAS  Google Scholar 

  • Olsen, Y.S., S.E. Fox, M. Teichberg, M. Otter, and I. Valiela. 2011. δ15N and δ13C reveal differences in carbon flow through estuarine benthic food webs in response to the relative availability of macroalgae and eelgrass. Marine Ecology Progress Series 421: 83–96.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Parrish, C.C., T.A. Abrajano, S.M. Budge, R.J. Helleur, E.D. Hudson, K. Pulchan, and C. Ramos. 2000. Lipid and phenolic biomarkers in marine ecosystems: analysis and applications. In The handbook of environmental chemistry, vol. 5, 193–223. Berlin: Springer.

    Google Scholar 

  • Peterson, B.J., and B. Fry. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18: 293–320.

    Google Scholar 

  • Peterson, B.J., R.W. Howarth, and R.H. Garritt. 1985. Multiple stable isotopes used to trace the flow of organic matter in estuarine food webs. Science 227: 1361–1363.

    Article  CAS  Google Scholar 

  • Pimm, S.L. 2002. Food webs. New York: Chapman and Hall.

    Google Scholar 

  • Post, D.M. 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83: 703–718.

    Article  Google Scholar 

  • Post, D.M., C.A. Layman, D.A. Arrington, G. Takimoto, J. Quattrochi, and C.J. Montana. 2007. Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152: 179–189.

    Article  Google Scholar 

  • Power, M., K. Guiguer, and D.R. Barton. 2003. Effects of temperature on isotopic enrichment in Daphnia magna: implications for aquatic food-web studies. Rapid Communications in Mass Spectrometry 17: 1619–1625.

    Article  CAS  Google Scholar 

  • Richoux, N.B., and P.W. Froneman. 2007. Assessment of spatial variation in carbon utilization by benthic and pelagic invertebrates in a temperate South African estuary using stable isotope signatures. Estuarine, Coastal and Shelf Science 71: 545–558.

    Article  Google Scholar 

  • Richoux, N.B., and P.W. Froneman. 2008. Trophic ecology of dominant zooplankton and macrofauna in a temperate, oligotrophic South African estuary: a fatty acid approach. Marine Ecology Progress Series 357: 121–137.

    Article  Google Scholar 

  • Riera, P., and P. Richard. 1997. Temporal variation of δ13C in particulate organic matter and oyster Crassostrea gigas in Marennes-Oleron Bay (France): effect of freshwater inflow. Marine Ecology Progress Series 147: 105–115.

    Article  Google Scholar 

  • Riera, P., L.J. Stal, J. Nieuwenhuize, P. Richard, G. Blanchard, and F. Gentil. 1999. Determination of food sources for benthic invertebrates in a salt marsh (Aiguillon Bay, France) by carbon and nitrogen stable isotopes: importance of locally produced sources. Marine Ecology Progress Series 187: 301–307.

    Article  CAS  Google Scholar 

  • Schindler, D.E., and M.D. Scheuerell. 2002. Habitat coupling in lake ecosystems. Oikos 98: 177–189.

    Article  Google Scholar 

  • Schumann, E.H., R.R.W. Gray, and R.W. Shone. 2001. Tidal flow structures and sedimentation in the lower Kowie estuary, Port Alfred, South Africa. Transactions of the Royal Society of South Africa 56: 11–24.

    Article  Google Scholar 

  • Serrano, O., L. Serrano, M.A. Mateo, I. Colombini, L. Chelazzi, E. Gagnarli, and M. Fallaci. 2008. Acid washing effect on elemental and isotopic composition of whole beach arthropods: implications for food web studies using stable isotopes. Acta Oecologica 34: 89–96.

    Article  Google Scholar 

  • Volkman, J.K., S.M. Barrett, S.I. Blackburn, M.P. Mansour, E.L. Sikes, and F. Gelin. 1998. Microalgal biomarkers: a review of recent research developments. Organic Geochemistry 29: 1163–1179.

    Article  CAS  Google Scholar 

  • Vorsatz, J.P. 2009. Ecological role of estuarine brachyuran crabs in mangrove and salt marsh estuaries, Eastern Cape, South Africa. PhD thesis, University of Port Elizabeth, South Africa.

  • Wasserman, R.J. 2012. Feeding ecology of the early life-history stages of two dominant gobiid species in the headwaters of a warm-temperate estuary. Estuarine, Coastal and Shelf Science 109: 11–19.

    Article  Google Scholar 

  • Whitfield, A.K. 1988. The fish community of the Swartvlei Estuary and the influence of food availability on resource utilisation. Estuaries 11: 160–170.

    Article  Google Scholar 

  • Whitfield, A.K. 1989. The benthic invertebrate community of a southern cape estuary: structure and possible food sources. Transactions of the Royal Society of South Africa 47: 159–179.

    Article  Google Scholar 

  • Whitfield, A.K. 1998. Biology and ecology of fishes in South African estuaries. Ichthyological monographs of the J.L.B. Smith Institute of Ichthyology 2: 1–223.

    Google Scholar 

  • Whitfield, A.K., A.W. Paterson, A.H. Bok, and H.M. Kok. 1994. A comparison of the ichthyofaunas in two permanently open eastern Cape estuaries. South African Journal of Zoology 29: 175–185.

    Google Scholar 

  • Whitfield, A.K., M. Elliott, A. Basset, S.J.M. Blaber, and R.J. West. 2012. Paradigms in estuarine ecology—a review of the Remane diagram with a suggested revised model for estuaries. Estuarine, Coastal and Shelf Science 97: 78–90.

    Article  Google Scholar 

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Acknowledgements

This research was funded by the Sandisa Imbewu Initiative at Rhodes University, the Water Research Commission of South Africa, and the National Research Foundation of South Africa. We thank Tatenda Dalu for sharing the stable isotope data of some food sources, and Katherina Schoo, Matthew Parkinson, and Mandla Magoro for field assistance. In addition, one anonymous referee provided valuable comments that helped us significantly improve the quality of our manuscript.

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  1. Department of Zoology and Entomology, Rhodes University, P.O. Box 94, Grahamstown, 6140, South Africa

    Leandro Bergamino & Nicole B. Richoux

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Correspondence to Leandro Bergamino.

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Bergamino, L., Richoux, N.B. Spatial and Temporal Changes in Estuarine Food Web Structure: Differential Contributions of Marsh Grass Detritus. Estuaries and Coasts 38, 367–382 (2015). https://doi.org/10.1007/s12237-014-9814-5

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