Abstract
The relative importance of carbon sources supporting aquatic food webs within and among estuaries may be influenced by factors that affect relative availability of autotrophic carbon sources, as well as movement of individuals among marine, estuarine and freshwater zones. We used stable isotopes of carbon and nitrogen to examine (1) the relative importance of carbon sources supporting estuarine consumers among estuaries with different hydrogeomorphic characteristics, (2) stable isotope signatures of consumer ecological guilds defined by dependence on estuarine habitats and residence time, and (3) if patterns in stable isotope signatures of ecological guilds repeat across estuaries with distinct hydrogeomorphological features. At the assemblage level, consumer carbon isotope signatures reflected the consumption of locally abundant primary production sources and differed across estuary types (choked lagoon, coastal river). Consumer ecological guilds differed in δ13C within sites, and the same trend repeated across sites but with differing magnitudes. This variation is attributed to movement and residence patterns in addition to differences in the relative abundances of autotrophic sources across sites. Although within-estuary variation in consumer resource use is to be expected, estuarine food webs may be broadly classified according to landscape-scale hydrogeomorphic factors that allow an initial prediction of the relative importance of carbon sources to secondary production. Predictions may be refined at the species level using knowledge of habitat use and residence time. Such predictions are useful as a starting point for poorly studied regions such as ours in southern Brazil, as well as for global-scale analyses of patterns in estuarine food webs.
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References
Abreu, P. A., A. M. Anésio, C. Costa, C. Bemvenuti, C. Odebrecht & W. Granéli, 2006. Eutrophication processes and trophic interactions in a shallow estuary: preliminary results based on stable isotope analysis (δ13C and δ15N). Estuaries 29: 277–285.
Alfaro, A. C., F. Thomas, L. Sergent & 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.
Bardonnet, A. & P. Riera, 2005. Feeding of glass eels (Anguilla anguilla) in the course of their estuarine migration: new insights from stable isotope analysis. Estuarine Coastal and Shelf Science 63: 201–209.
Bouillon, S., P. Chandra Mohan, N. Sreenivas & F. Dehairs, 2000. Sources of suspended organic matter and selective feeding by zooplankton in an estuarine mangrove ecosystem as traced by stable isotopes. Marine Ecology Progress Series 208: 79–92.
Camara, G., R. C. M. Souza, U. M. Freitas & J. Garrido, 1996. SPRING: integrating remote sensing and GIS by object-oriented data modelling. Computer & Graphics 20: 395–403.
Canuel, E. A., J. E. Cloern, D. B. Ringelberg, J. B. Guckert & G. H. Rau, 1995. Molecular and isotopic tracers used to examine sources of organic matter and its incorporation into the food webs of San Francisco Bay. Limnology and Oceanography 40: 67–81.
Chanton, J. & F. G. Lewis, 2002. Examination of coupling between primary and secondary production in a river-dominated estuary: Apalachicola Bay, Florida. U.S.A. Limnology and Oceanography 47: 683–697.
Connolly, R. M., M. A. Guest, A. J. Melville & J. M. Oakes, 2004. Sulfur stable isotopes separate producers in marine food-web analysis. Oecologia 138: 161–167.
Connolly, R. M., D. Gorman & M. A. Guest, 2005. Movement of carbon among estuarine habitats and its assimilation by invertebrates. Oecologia 144: 684–691.
Costa, C. S. B., U. Seeliger, C. P. L. Oliveira & A. M. M. Mazo, 1997. Distribuição, funções e valores das marismas e pradarias submersas no estuário da Lagoa dos Patos (RS, Brasil). Atlântica 19: 65–83.
Day, J. W., C. A. S. Hall, W. M. Kemp & A. Yanez-Arancibia, 1989. Estuarine Ecology. Wiley, New York.
Deegan, L. A., 1993. Nutrient and energy transport between estuaries and coastal marine ecosystems by fish migration. Canadian Journal of Fisheries and Aquatic Sciences 50: 74–79.
Deegan, L. A. & R. H. Garritt, 1997. Evidence for spatial variability in estuarine food webs. Marine Ecology Progress Series 147: 31–47.
Fry, B., 2002. Conservative mixing of stable isotopes across estuarine salinity gradients: a conceptual framework for monitoring watershed influences on downstream fisheries production. Estuaries 25: 264–271.
Garcia, A. M. & J. P. Vieira, 1997. Abundância e diversidade da assembléia de peixes dentro e fora de uma pradaria de Ruppia maritima L., no estuário da Lagoa dos Patos (RS-Brasil). Atlântica 19: 161–181.
Garcia, A. M., J. P. Vieira, C. E. Bemvenuti & R. M. Geraldi, 1996. Abundância e diversidade da assembléia de crustáceos decápodes dentro e fora de uma pradaria de Ruppia maritima L., no estuário da Lagoa dos Patos (RS-Brasil). Náuplius 4: 113–128.
Garcia, A. M., J. P. Vieira & K. O. Winemiller, 2003. Effects of 1997–1998 El Niño on the dynamics of the shallow-water fish assemblage of the Patos Lagoon estuary (Brazil). Estuarine Coastal and Shelf Science 57: 489–500.
Garcia, A. M., J. P. Vieira, K. O. Winemiller & A. M. Grimm, 2004. Comparison of the 1982–1983 and 1997–1998 El Nino effects on the shallow-water fish assemblage of the Patos Lagoon estuary (Brazil). Estuaries 27: 905–914.
Garcia, A. M., D. J. Hoeinghaus, J. P. Vieira & K. O. Winemiller, 2007. Isotopic variation of fishes in freshwater and estuarine zones of a large subtropical coastal lagoon. Estuarine Coastal and Shelf Science 73: 399–408.
Garman, G. C. & S. A. Macko, 1998. Contribution of marine-derived organic matter to an Atlantic coast, freshwater, tidal stream by anadromous clupeid fish. Journal of the North American Benthological Society 17: 277–285.
Gauch, H. G. Jr., 1984. Multivariate Analysis in Community Ecology. Cambridge University Press, Cambridge.
Guest, M. A. & R. M. Connolly, 2006. Movement of carbon among estuarine habitats: the influence of saltmarsh patch size. Marine Ecology Progress Series 310: 15–24.
Herzka, S. Z., 2005. Assessing connectivity of estuarine fishes based on stable isotope ratio analysis. Estuarine, Coastal and Shelf Science 64: 58–69.
Hoeinghaus, D. J. & 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.
Hoeinghaus, D. J., K. O. Winemiller & A. A. Agostinho, 2007. Landscape-scale hydrologic characteristics differentiate patterns of carbon flow in large-river food webs. Ecosystems 10: 1019–1033.
Hoeinghaus, D. J., K. O. Winemiller & A. A. Agostinho, 2008. Hydrogeomorphology and river impoundment affect food-chain length of diverse neotropical food webs. Oikos 117: 984–995.
Hsieh, H. L., C. P. Chen, Y. G. Chen & H. H. Yang, 2002. Diversity of benthic organic matter flows through polychaetes and crabs in a mangrove estuary: δ13C and δ34S signals. Marine Ecology Progress Series 227: 145–155.
Isacch, J. P., C. S. B. Costa, L. Rodríguez-Gallego, D. Conde, M. Escapa, D. A. Gagliardini & O. O. Iribarne, 2006. Distribution of saltmarsh plat communities associated with environmental factors along a latitudinal gradient on the south-west Atlantic coast. Journal of Biogeography 33: 888–900.
Kaldy, J. E., L. A. Cifuentes & D. Brock, 2005. Using stable isotope analyses to assess carbon dynamics in a shallow subtropical estuary. Estuaries 28: 86–95.
Kanaya, G., S. Takagi, E. Nobata & E. Kikuchi, 2007. Spatial dietary shift of macrozoobenthos in a brackish lagoon revealed by carbon and nitrogen stable isotope ratios. Marine Ecology Progress Series 345: 117–127.
Kang, C. K., J. B. Kim, K. S. Lee, J. B. Kim, P. Y. Lee & 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.
Kennish, M. J., 1990. Ecology of Estuaries, Vol. 1. Physical and Chemical Aspects. CRC Press, Boca Raton.
Kjerfve, B., 1986. Comparative oceanography of coastal lagoons. In Wolfe, D. A. (ed.), Estuarine Variability. Academic Press, Orlando: 63–81.
MacAvoy, S. E., S. A. Macko, S. P. McIninch & G. C. Garman, 2000. Marine nutrient contributions to freshwater apex predators. Oecologia 122: 568–573.
Moller, O. O. J., P. Casting, J.-C. Salomon & P. Lazure, 2001. The influence of local and non-local forcing effects on the subtidal circulation of Patos Lagoon. Estuaries 24: 297–311.
Pereira, L. E., L. A. Ramos & S. X. Pontes, 1998. Lista comentada dos peixes e crustáceos decápodas do estuário do Arroio Chuí e região costeira adjacente, RS. Atlântica 20: 165–172.
Peterson, B. J. & B. Fry, 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18: 293–320.
Peterson, B. J., R. W. Howarth & R. H. Garritt, 1985. Multiple stable isotopes used to trace the flow of organic matter in estuarine food webs. Science 227: 1361–1363.
Peterson, B. J., B. Fry, M. A. Hullar, S. Saupe & R. Wright, 1994. The distribution and stable carbon isotopic composition of dissolved organic carbon in estuaries. Estuaries 17: 111–121.
Post, D. M., 2002. Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83: 703–718.
Reis, E. G. & F. D’incao, 2000. The present status of artisanal fisheries of extreme Southern Brazil: an effort towards community-based management. Ocean & Coastal Management 43: 585–595.
Richoux, N. B. & 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.
Riera, P. & C. Hubas, 2003. Trophic ecology of nematodes from various microhabitats of the Roscoff Aber Bay (France): importance of stranded macroalgae evidenced through delta C-13 and delta N-15. Marine Ecology Progress Series 260: 151–159.
Rodriguez-Grana, L., D. Calliari, D. Conde, J. Sellanes & R. Urrutia, 2008. Food web of a SW Atlantic shallow coastal lagoon: spatial environmental variability does not impose substantial changes in the trophic structure. Marine Ecology Progress Series 362: 69–83.
Rosa-Filho, J. S., C. E. Bemvenuti & M. Elliott, 2004. Predicting biological parameters of estuarine benthic communities using models based on environmental data. Brazilian Archives of Biology and Technology 47: 613–627.
Rubenstein, D. R. & K. A. Hobson, 2004. From birds to butterflies: animal movement patterns and stable isotopes. Trends in Ecology and Evolution 19: 256–263.
Schwarzbold, A. & A. Schäfer, 1984. Gênese e morfologia das lagoas costeiras do Rio Grande do Sul, Brasil. Amazoniana 9: 87–104.
Seeliger, U., 2001. The Patos Lagoon Estuary, Brazil. In Seeliger, U. & B. Kjerfve (eds), Coastal Marine Ecosystems of Latin America. Springer Verlag, Berlin: 167–182.
Seeliger, U., C. Odebrecht & J. P. Castello, 1996. Subtropical Convergence Environments: The Coast and Sea in the Southwestern Atlantic. Springer Verlag, Berlin.
Vanderklift, M. A. & S. Ponsard, 2003. Sources of variation in consumer-diet d15N enrichment: a meta-analysis. Oecologia 136: 169–182.
Vieira, J. P. & J. P. Castello, 1996. Fish fauna. In Seeliger, U., C. Odebrecht & J. P. Castello (eds), Subtropical Convergence Environments: The Coast and Sea in the Southwestern Atlantic. Springer Verlag, Berlin: 56–61.
Wainright, S. C., M. P. Weinstein, K. W. Able & C. A. Currin, 2000. Relative importance of benthic microalgae, phytoplankton and the detritus of smooth cordgrass Spartina alterniflora and the common reed Phragmites australis to brackish-marsh food webs. Marine Ecology Progress Series 200: 77–91.
Winemiller, K. O., S. Akin & S. C. Zeug, 2007. Production sources and food web structure of a temperate tidal estuary: integration of dietary and stable isotope data. Marine Ecology Progress Series 343: 63–76.
Winemiller, K. O., D. J. Hoeinghaus, A. A. Pease, P. E. Esselman, R. L. Honeycutt, D. Gbanaador, E. Carrera & J. Payne, in press. Stable isotope analysis reveals food web structure and watershed impacts along the fluvial gradient of a Mesoamerican coastal river. River Research and Applications.
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Thanks to the numerous colleagues and technicians that assisted in the field and laboratory work, especially A. C. Mai, F. Roselet and V. Condini. D.J.H. was supported in part by research scholarships from the Society of Wetland Scientists during field collection. A.M.G. acknowledges fellowship support provided by CNPq (Grant 150868/2003-0). K.O.W. and D.J.H. acknowledge financial support from the International Sportfish Fund.
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Hoeinghaus, D.J., Vieira, J.P., Costa, C.S. et al. Estuary hydrogeomorphology affects carbon sources supporting aquatic consumers within and among ecological guilds. Hydrobiologia 673, 79–92 (2011). https://doi.org/10.1007/s10750-011-0751-z
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DOI: https://doi.org/10.1007/s10750-011-0751-z