Importance of terrestrial subsidies for estuarine food webs in contrasting East African catchments

Ecosphere

Volumn 4, Issue 1, 2013, Pages

  Abrantes, Kátya G ^a,d   Barnett, Adam ^b,c   Marwick, Trent R ^a   Bouillon, Steven ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEAKIN UNIVERSITY   (Australia)

^c UNIVERSITY OF TASMANIA   (Australia)

^d JAMES COOK UNIVERSITY   (Australia)

Author keywords

Africa; Bayesian mixing models; Catchment; Estuaries; Stable isotopes; Terrestrial subsidies

Indexed keywords

EID: 84884518547     PISSN: None     EISSN: 21508925     Source Type: Journal    
DOI: 10.1890/ES12-00322.1     Document Type: Article

References (98)

1. Abrantes, K., and M. Sheaves. 2008. Incorporation of terrestrial wetland material into aquatic food webs in a tropical estuarine wetland. Estuarine, Coastal and Shelf Science 80:401-412.
2. Abrantes, K. G., and M. Sheaves. 2010. Importance of freshwater flow in terrestrial-aquatic energetic connectivity in intermittently connected estuaries of tropical Australia. Marine Biology 157:2071-2086.
3. Admiraal, W. 1984. The ecology of estuarine sedimentinhabiting diatoms. Pages 269-323 in F. E. Round and D. J. Chapman, editors. Progress in Phycological Research. Biopress, Bristol, UK.
4. Aldegheri, M. 1972. Rivers and streams on Madagascar. Pages 261-310 in R. Battistini and G. Richard- Vindard, editors. Biogeography and ecology in Madagascar. Dr. W Junk, The Hague, The Netherlands.
5. Anderson, C., and G. Cabana. 2005. d15N in riverine food webs: effects of N inputs from agricultural watersheds. Canadian Journal of Fisheries and Aquatic Sciences 62:333-340.
6. Balcombe, S. R., S. E. Bunn, F. J. M. Smith, and P. M. Davies. 2005. Variability of fish diets between dry and flood periods in an arid zone floodplain river. Journal of Fish Biology 67:1552-1567.
7. Bartels, P., J. Cucherousset, C. Gudasz, M. Jansson, J. Karlsson, L. Persson, K. Premke, A. Rubach, K. Steger, L. J. Tranvik, and P. Eklov. 2012. Terrestrial subsidies to lake food webs: an experimental approach. Oecologia 168:807-818.
8. Bateman, A. S., and S. D. Kelly. 2007. Fertilizer nitrogen isotope signatures. Isotopes in Environmental and Health Studies 43:237-247.
9. Beilfuss, R. D., and B. R. Davies. 1998. Prescribed flooding and wetland rehabilitation in the Zambezi Delta, Mozambique. In W. Streever, editor. An international perspective on wetland rehabilitation. Kluwer, Dordrecht, The Netherlands.
10. Bernardes, M. C., L. A. Martinelli, A. V. Krusche, J. Gudeman, M. Moreira, R. L. Victoria, J. P. H. B. Ometto, M. V. R. Ballester, A. K. Aufdenkampe, J. E. Richey, and J. I. Hedges. 2004. Riverine organic matter composition as a function of land use changes, southwest Amazon. Ecological Applications 14:263-279.
11. Boston, H. L., and W. R. Hill. 1991. Photosynthesislight relations of stream periphyton communities. Limnology and Oceanography 36:644-656.
12. Bouillon, S., G. Abril, A. V. Borges, F. Dehairs, G. Govers, H. J. Hughes, R. Merckx, F. J. R. Meysman, J. Nyunja, C. Osburn, and J. J. Middelburg. 2009. Distribution, origin and cycling of carbon in the Tana River (Kenya): a dry season basin-scale survey from headwaters to the delta. Biogeosciences 6:2475-2493.
13. Bouillon, S., R. Connolly, and S. Y. Lee. 2008. Organic matter exchange and cycling in mangrove ecosystems: Recent insights from stable isotope studies. Journal of Sea Research 59:44-58.
14. Bouillon, S., F. Dehairs, L.-S. Schiettecatte, and A. V. Borges. 2007. Biogeochemistry of the Tana estuary and delta (northern Kenya). Limnology and Oceanography 52:46-59.
15. Bouillon, S., T. Moens, I. Overmeer, N. Koedam, and F. Dehairs. 2004. Resource utilization patterns of epifauna from mangrove forests with contrasting inputs of local versus imported organic matter. Marine Ecology Progress Series 278:77-88.
16. Bouillon, S., P. C. Mohan, N. Sreenivas, and 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.
17. Buchheister, A., and R. J. Latour. 2010. Turnover and fractionation of carbon and nitrogen stable isotopes in tissues of a migratory coastal predator, summer flounder (Paralichthys dentatus). Canadian Journal of Fisheries and Aquatic Sciences 67:445-461.
18. Cadenasso, M. L., S. T. A. Pickett, K. C. Weathers, and C. G. Jones. 2003. A framework for a theory of ecological boundaries. BioScience 53:750-758.
19. Chanton, J., and 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.
20. Chanton, J. P., and F. G. Lewis. 1999. Plankton and dissolved inorganic carbon isotopic composition in a river-dominated estuary: Apalachicola Bay, Florida. Estuaries 22:575-583.
21. Clementz, M. T., and P. L. Koch. 2001. Differentiating aquatic mammal habitat and foraging ecology with stable isotopes in tooth enamel. Oecologia 129:461-472.
22. Cloern, J. E., E. A. Canuel, and D. Harris. 2002. Stable carbon and nitrogen isotope composition of aquatic and terrestrial plants of the San Francisco Bay estuarine system. Limnology and Oceanography 47:713-729.
23. Cole, J. J., S. R. Carpenter, M. L. Pace, M. C. Van de Bogert, J. L. Kitchell, and J. R. Hodgson. 2006. Differential support of lake food webs by three types of terrestrial organic carbon. Ecology Letters 9:558-568.
24. Couch, C. A. 1989. Carbon and nitrogen stable isotopes of meiobenthos and their food resources. Estuarine, Coastal and Shelf Science 28:433-441.
25. Craine, J. M., A. J. Elmore, M. P. M. Aidar, M. Bustamante, T. E. Dawson, E. A. Hobbie, A. Kahmen, M. C. Mack, K. K. McLauchlan, A. Michelsen, G. B. Nardoto, L. H. Pardo, J. Peñuelas, P. B. Reich, E. A. G. Schuur, W. D. Stock, P. H. Templer, R. A. Virginia, J. M. Welker, and I. J. Wright. 2009. Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytologist 183:980-992.
26. D'Avanzo, C., and I. Valiela. 1990. Use of detrital foods and assimilation of nitrogen by coastal detritivores. Estuaries 13:20-24.
27. Davies, B. R. 1986. The Zambezi River system. In B. R. Davies and K. F. Walker, editors. The ecology of river systems. Dr. W. Junk, Dordrecht, The Netherlands.
28. Deegan, L. A., and R. H. Garritt. 1997. Evidence for spatial variability in estuarine food webs. Marine Ecology Progress Series 147:31-47.
29. del Giorgio, P. A., and R. L. France. 1996. Ecosystemspecific patterns in the relationship between zooplankton and POM or microplankton d13C. Limnology and Oceanography 41:359-365.
30. DeNiro, M. J., and S. Epstein. 1977. A mechanism of carbon isotope fractionation associated with lipid synthesis. Science 197:261-263.
31. DeNiro, M. J., and S. Epstein. 1978. Influence of diet in the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42:495-506.
32. Dittmar, T., R. J. Lara, and G. Kattner. 2001. River or mangrove? Tracing major organic matter sources in tropical Brazilian coastal waters. Marine Chemistry 73:253-271.
33. Dubois, S., B. Jean-Louis, B. Bertrand, and S. Lefebvre. 2007. Isotope trophic-step fractionation of suspension- feeding species: Implications for food partitioning in coastal ecosystems. Journal of Experimental Marine Biology and Ecology 351:121-128.
34. FAO. 2002. Hydrological Basins in Africa database. www.fao.org/ geonetwork/srv/en/metadata.show? Id=296&currTab=simple
35. Flindt, M. R., M. A. Pardal, A. I. Lillebo, I. Martins, and J. C. Marques. 1999. Nutrient cycling and plant dynamics in estuaries: a brief review. Acta Oecologica 20:237-248.
36. France, R. L. 1996. Scope for use of stable carbon isotopes in discerning the incorporation of forest detritus into aquatic foodwebs. Hydrobiologia 325:219-222.
37. Fry, B. 2002. Stable isotopic indicators of habitat use by Mississippi River fish. Journal of the North American Benthological Society 21:676-685.
38. Gillikin, D. P., and S. Bouillon. 2007. Determination of d18O of water and d13C of dissolved inorganic carbon using a simple modification of an elemental analyzer-isotope ratio mass spectrometer: an evaluation. Rapid Communications in Mass Spectrometry 21:1475-1478.
39. Guelinckx, J., J. Maes, P. van den Driessche, B. Geysen, F. Dehairs, and F. Ollevier. 2007. Changes in d13C and d15N in different tissues of juvenile sand goby Pomatoschistus minutus: a laboratory diet-switch experiment. Marine Ecology Progress Series 341:205-215.
40. Heck, K. L., T. J. B. Carruthers, C. M. Duarte, A. R. Hughes, G. Kendrick, R. J. Orth, and S. W. Williams. 2008. Trophic transfers from seagrass meadows subsidize diverse marine and terrestrial consumers. Ecosystems 11:1198-1210.
41. Hesslein, R. H., K. A. Halard, and P. Ramlal. 1993. Replacement of sulfur, carbon and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by d34S, d13C, and d15N. Canadian Journal of Fisheries and Aquatic Sciences 50:2071-2076.
42. 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.
43. Hoover, R. S., D. Hoover, M. Miller, M. R. Landry, E. H. DeCarlo, and F. T. Mackenzie. 2006. Zooplankton response to storm runoff in a tropical estuary: bottom-up and top-down controls. Marine Ecology Progess Series 318:187-201.
44. Jaschinski, S., T. Hansen, and U. Sommer. 2008. Effects of acidification in multiple stable isotope analyses. Limnology and Oceanography: Methods 6:12-15.
45. Junk, W. J. 2002. Long-term environmental trends and the future of tropical wetlands. Environmental Conservation 29:414-435.
46. Kaldy, J. E., L. A. Cifuentes, and D. Brock. 2005. Using stable isotope analyses to assess carbon dynamics in a shallow subtropical estuary. Estuaries 28:86-95.
47. Kendall, C., S. R. Silva, and V. J. Kelly. 2001. Carbon and nitrogen isotopic compositions of particulate organic matter in four large river systems across the United States. Hydrological Processes 15:1301-1346.
48. Kitheka, J. U., M. Obiero, and P. Nthenge. 2005. River discharge, sediment transport and exchange in the Tana Estuary, Kenya. Estuarine, Coastal and Shelf Science 63:455-468.
49. Koch, P. L., A. K. Behrensmeyer, and M. Fogel. 1991. The isotopic ecology of plants and animals in Amboseli National Park, Kenya. Pages 163-171 in Annual Report of the Director of the Geophysical Laboratory, Carnegie Institution of Washington, 1990-1991. Carnegie Institution, Washington, D.C., USA.
50. Kolasinski, J., K. Rogers, and P. Frouin. 2008. Effects of acidification on carbon and nitrogen stable isotopes of benthic macrofauna from a tropical coral reef. Rapid Communications in Mass Spectrometry 22:2955-2960.
51. Krause-Jensen, D., and K. Sand-Jensen. 1998. Light attenuation and photosynthesis of aquatic plant communities. Limnology and Oceanography 43:396-407.
52. Lin, G., T. Banks, and L. S. L. O. Sternberg. 1991. Variation in d13C values for the seagrass Thalassia testudinum and its relations to mangrove carbon. Aquatic Botany 40:333-341.
53. Logan, J. M., T. D. Jardine, T. J. Miller, S. E. Bunn, R. A. Cunjak, and M. E. Lutcavage. 2008. Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. Journal of Animal Ecology 77:838-846.
54. Lowe-McConnell. 2000. The role of tilapias in ecosystems. In M. C. M. Beveridge and B. J. McAndrew, editors. Tilapias: biology and exploitation. Fish and Fisheries Series 25. Kluwer, Dordrecht, The Netherlands.
55. MacIntyre, H. L., R. J. Geider, and D. C. Miller. 1996. Microphytobenthos: the ecological role of the ''secret garden'' of unvegetated, shallow-water marine habitats. I. Distribution, abundance and primary production. Estuaries 19:186-201.
56. Maingi, J. K., and S. E. Marsh. 2002. Quantifying hydrologic impacts following dam construction along the Tana River, Kenya. Journal of Arid Environments 50:53-79.
57. Mateo, M. A., O. Serrano, L. Serrano, and R. H. Michener. 2008. Effects of sample preparation on stable isotope ratios of carbon and nitrogen in marine invertebrates: implications for food web studies using stable isotopes. Oecologia 157:105-115.
58. May, C. L., J. R. Koseff, L. V. Lucas, J. E. Cloern, and D. H. Schoellhamer. 2003. Effects of spatial and temporal variability of turbidity on phytoplankton blooms. Marine Ecology Progress Series 254:111-128.
59. McClelland, J. W., and I. Valiela. 1997. Nitrogen-stable isotope signatures in estuarine food webs: a record of increasing urbanization in coastal watersheds. Limnology and Oceanography 42:930-937.
60. McConnaughey, T., and C. P. McRoy. 1979. Food-web structure and the fractionation of carbon isotopes in the Bering Sea. Marine Biology 53:257-262.
61. McCutchan, J. H., W. M. Lewis, Jr, C. Kendall, and C. C. McGrath. 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen and sulfur. Oikos 102:378-390.
62. McIntyre, P. B., and A. S. Flecker. 2006. Rapid turnover of tissue nitrogen of primary consumers in tropical freshwaters. Oecologia 148:12-21.
63. Mead, L. H., and T. N. Wiegner. 2010. Surface water metabolism in a tropical estuary, Hilo Bay, Hawaii, USA, during storm and non-storm conditions. Estuaries and Coasts 33:1099-1112.
64. Meybeck, M. 1982. Carbon, nitrogen, and phosphorus transport by world rivers. American Journal of Science 282:401-450.
65. Mortazavi, B., R. L. Iverson, W. M. Landing, F. G. Lewis, and W. Huang. 2000. Control of phytoplankton production and biomass in a riverdominated estuary: Apalachicola Bay, Florida, USA. Marine Ecology Progress Series 198:19-31.
66. Muzuka, A. N. N. 1999. Isotopic compositions of tropical East African flora and their potential as source indicators of organic matter in coastal marine sediments. Journal of African Earth Sciences 28:757-766.
67. Nakano, S., and M. Murakami. 2001. Reciprocal subsidies: Dynamic interdependence between terrestrial and aquatic food webs. Proceedings of the National Academy of Sciences 98:166-170.
68. Pardo, L. H., and K. J. Nadelhoffer. 2010. Using nitrogen isotope ratios to assess terrestrial ecosystems at regional and global scales. Pages 221-249 in J. B. West, G. J. Bowen, T. E. Dawson, and K. P. Tu, editors. Isoscapes: Understanding movement, pattern, and process on earth through isotope mapping. Springer, London, UK.
69. Parnell, A., R. Inger, S. Bearhop, and A. L. Jackson. 2008. SIAR: Stable isotope analysis in R. http://cran. r-project.org/web/packages/siar
70. Parnell, A. C., R. Inger, S. Bearhop, and A. L. Jackson. 2010. Source partitioning using stable isotopes: coping with too much variation. PlosOne 5:9672.
71. Peterson, B. J., and B. Fry. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18:293-320.
72. Polis, G. A., W. B. Anderson, and R. D. Holt. 1997. Towards an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annual Review of Ecology and Systematics 28:289-316.
73. Polis, G. A., and S. D. Hurd. 1996. Linking marine and terrestrial food webs: allochthonous input from the ocean supports high secondary productivity on small islands and coastal land communities. American Naturalist 147:396-423.
74. Polis, G. A., and D. R. Strong. 1996. Food web complexity and community dynamics. American Naturalist 147:813-846.
75. Post, D. M., C. A. Layman, D. A. Arrington, G. Takimoto, J. Quattrochi, and C. G. Montaña. 2007. Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179-189.
76. Raharimahefa, T., and T. M. Kusky. 2010. Environmental monitoring of Bombetoka Bay and the Betsiboka Estuary, Madagascar, using multi-temporal satellite data. Journal of Earth Science 21:210-226.
77. Ralison, O. H., A. V. Borges, F. Dehairs, J. J. Middelburg, and S. Bouillon. 2008. Carbon biogeochemistry of the Betsiboka estuary (north-western Madagascar). Organic Geochemistry 39:1649-1658.
78. Randrianarijaona, P. 1983. The erosion of Madagascar. Ambio 12:308-311.
79. Rizzo, W. M., and R. L. Wetze. 1985. Intertidal and shoal benthic community metabolism in a temperate estuary: studies of spatial and temporal scales of variability. Estuaries 8:342-351.
80. Robertson, A. I., and S. J. M. Blaber. 1992. Plankton, epibenthos and fish communities. Pages 173-224 in A. I. Robertson and D. M. Alongi, editors. Tropical mangrove ecosystems. American Geophysical Union, Washington, D.C., USA.
81. Sakamaki, T., J. Y. T. Shum, and J. S. Richardson. 2010. Watershed effects on chemical properties of sediment and primary consumption in estuarine tidal flats: Importance of watershed size and food selectivity by macrobenthos. Ecosystems 11:328-337.
82. Schlacher, T. A., and R. M. Connolly. 2007. Estuarine fish health assessment: Evidence of wastewater impacts based on nitrogen isotopes and histopathology. Marine Pollution Bulletin 54:1762-1776.
83. Schlacher, T. A., R. M. Connolly, A. J. Skillington, and T. F. Gaston. 2009. Can export of organic matter from estuaries support zooplankton in nearshore, marine plumes? Aquatic Ecology 43:383-393.
84. Schlacher, T. A., B. Liddell, T. F. Gaston, and M. Schlacher-Hoenlinger. 2005. Fish track wastewater pollution to estuaries. Oecologia 144:570-584.
85. Smyntek, P. M., M. A. Teece, K. L. Schulz, and S. J. Thackeray. 2007. A standard protocol for stable isotope analysis of zooplankton in aquatic food web research using mass balance correction models. Limnology and Oceanography 52:2135-2146.
86. Still, C. J., and R. L. Powell. 2010. Continental-scale distributions of vegetation stable carbon isotope ratios. Pages 179-193 in J. B.West, G. J. Bowen, T. E. Dawson, and K. P. Tu, editors. Isoscapes: Understanding movement, pattern, and process on earth through isotope mapping. Springer, London, UK.
87. Sullivan, M. L., Y. Zhang, and T. H. Bonner. 2012. Terrestrial subsidies in the diets of stream fishes of the USA: comparisons among taxa and morphology. Marine and Freshwater Research 63:409-414.
88. Syvitski, J. P. M., C. J. Vörösmarty, A. J. Kettner, and P. Green. 2005. Impact of humans on the flux of terrestrial sediment to the global coastal ocean. Science 308:376-380.
89. Tamooh, F., K. V. d. Meersche, F. Meysman, T. R. Marwick, A. V. Borges, R. Merckx, F. Dehairs, S. Schmidt, J. Nyunja, and S. Bouillon. 2012. Distribution and origin of suspended sediments and organic carbon pools in the Tana River Basin, Kenya. Biogeosciences Discussions 9:1-44.
90. Turpie, J., B. Smith, L. Emerton, and J. Barnes. 1999. Economic value of the Zambezi Basin wetlands. University of Cape Town Press, Cape Town, South Africa.
91. Underwood, G. J. C., and J. Kromkamp. 1999. Primary production by phytoplankton and microphytobenthos in estuaries. Advances in Ecological Research 29:93-152.
92. Van den Meersche, K., P. V. Rijswijk, K. Soetaert, and J. J. Middelburg. 2009. Autochthonous and allochthonous contributions to mesozooplankton diet in a tidal river and estuary: Integrating carbon isotope and fatty acid constraints. Limnology and Oceanography 54:62-74.
93. Vanderklift, M. A., and S. Ponsard. 2003. Sources of variation in consumer-diet d15N enrichment: a meta-analysis. Oecologia 136:169-182.
94. Vörösmarty, C. J., B. Fekete, and B. A. Tucker. 1998. River discharge database. http://www.sage.wisc. edu/riverdata/
95. Wai, T.-C., K. M. Y. Leung, S. Y. T. Sin, A. Cornish, D. Dudgeon, and G. A. Williamsa. 2011. Spatial, seasonal, and ontogenetic variations in the significance of detrital pathways and terrestrial carbon for a benthic shark, Chiloscyllium plagiosum (Hemiscylliidae), in a tropical estuary. Limnology and Oceanography 56:1035-1053.
96. Wantzen, K. M., F. A. Machado, M. Voss, H. Boriss, and W. J. Junk. 2002. Seasonal isotopic shifts in fish of the Pantanal wetland, Brazil. Aquatic Sciences 64:239-251.
97. Weidel, B. C., S. R. Carpenter, J. F. Kitchell, and M. J. Vander Zanden. 2011. Rates and components of carbon turnover in fish muscle: insights from bioenergetics models and a whole-lake 13C addition. Canadian Journal of Fisheries and Aquatic Sciences 68:387-399.
98. Wiegner, T. N., R. L. Tubal, and R. A. MacKenzie. 2009. Bioavailability and export of dissolved organic matter from a tropical river during base- and stormflow conditions. Limnology and Oceanography 54:1233-1242.