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Estuaries and Coasts

, Volume 39, Issue 4, pp 1221–1233 | Cite as

Trophic Dynamics of the Cape Stumpnose (Rhabdosargus holubi, Sparidae) Across Three Adjacent Aquatic Habitats

  • L. Carassou
  • A. K. Whitfield
  • L. Bergamino
  • S. Moyo
  • N. B. Richoux
Article

Abstract

Migratory fish species are major vectors of connectivity among aquatic habitats. In this study, conventional stomach contents and stable isotope methods (δ13C and δ15N) were combined to understand how fish of different sizes feed across contrasting aquatic habitats. The Cape stumpnose Rhabdosargus holubi (Sparidae, Perciformes) was selected as an abundant estuarine-dependent species in the permanently open Kowie system, South Africa. Three different habitats were sampled in the region, namely, river, estuary, and sea. Fish entered the estuary as post-larvae from the marine environment, resided in the estuary and lower part of the river as juveniles, and then returned to the sea as sub-adults. The diet varied among habitats, seasons, and fish sizes. “Stable Isotope Analysis with R” (SIAR) Bayesian mixing models mostly supported the results from the stomach content analyses, but also revealed the importance of some prey (e.g., insects) that were underestimated in the consumed diet. Rhabdosargus holubi δ13C values indicated a clear spatial gradient in the origin of food sources assimilated across the habitats, with increasing δ13C along the freshwater-marine continuum. The δ13C ranges of sources and fish also overlapped within each habitat along this continuum, thus illustrating the fidelity of R. holubi to specific habitats at different life stages. By consuming prey in a particular habitat before migrating, either permanently or temporarily to another habitat, R. holubi participates in allochthonous fluxes among riverine, estuarine, and coastal marine environments, with approximately 7 tonnes of Cape stumpnose productivity being exported from the 142-ha Kowie Estuary to the sea each year.

Keywords

Stomach contents Stable isotopes Connectivity SIAR Fish 

Notes

Acknowledgments

This study was funded by the Water Research Commission (WRC) of South Africa, the National Research Foundation (NRF) of South Africa, Rhodes University’s Sandisa Imbewu Initiative, and the South African Institute for Aquatic Biodiversity (SAIAB). This project received ethics clearance from Rhodes University (RU Ethics Clearance ZOOL-02-2012) and the South African Institute for Aquatic Biodiversity (SAIAB Ethics Clearance 2012/04). We thank Dr. Angus Paterson, Professor Paul Cowley, Mandla Magoro, Dr. Tatenda Dalu, and Bernadette Hubbart for their help with field and laboratory work. Dr. Bergamino is grateful to the CSIC-program “Contratación de Cientificos Provenientes del Exterior” for financial support.

Supplementary material

12237_2016_75_MOESM1_ESM.docx (26 kb)
ESM 1 (DOCX 25 kb)

References

  1. Allan, L.E., S.T. Ambrose, N.B. Richoux, and P.W. Froneman. 2010. Determining spatial changes in the diet of nearshore suspension-feeders along the South African coastline: stable isotopes and fatty acid signatures. Estuarine, Coastal and Shelf Science 87: 463–471.CrossRefGoogle Scholar
  2. Antonio, E.S., A. Kasai, M. Ueno, N. Won, Y. Ishibi, H. Yokohama, and Y. Yamashita. 2010. Spatial variation in organic matter utilization by benthic communities from Yura river-estuary to offshore of Tango Sea, Japan. Estuarine, Coastal and Shelf Science 86: 107–117.CrossRefGoogle Scholar
  3. Baxter, C.V., K.D. Fausch, and W.C. Saunders. 2005. Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshwater Biology 50: 201–220.CrossRefGoogle Scholar
  4. Bergamino, L., and N.B. Richoux. 2015. Spatial and temporal changes in estuarine food web structure: differential contributions of marsh grass detritus. Estuaries and Coasts 38: 367–382.CrossRefGoogle Scholar
  5. Bergamino, L., T. Dalu, and N.B. Richoux. 2014. Evidence of spatial and temporal changes in sources of organic matter in estuarine sediments: stable isotope and fatty acid analyses. Hydrobiologia 732: 133–145.CrossRefGoogle Scholar
  6. Bertrand, M., G. Cabana, D.J. Marcogliese, and P. Magna. 2011. Estimating the feeding range of a mobile consumer in a river-flood plain system using δ13C gradients and parasites. Journal of Animal Ecology 80: 1313–1323.CrossRefGoogle Scholar
  7. Blaber, S.J.M. 1973a. Population size and mortality of the marine teleost Rhabdosargus holubi (Pisces: Sparidae) in a closed estuary. Marine Biology 21: 219–225.CrossRefGoogle Scholar
  8. Blaber, S.J.M. 1973b. Temperature and salinity tolerance of juvenile Rhabdosargus holubi (Steindachner) (Teleostei: Sparidae). Journal of Fish Biology 5: 593–598.CrossRefGoogle Scholar
  9. Blaber, S.J.M. 1974a. The population structure and growth of juvenile Rhabdosargus holubi (Steindachner) (Teleostei: Sparidae) in a closed estuary. Journal of Fish Biology 6: 455–460.CrossRefGoogle Scholar
  10. Blaber, S.J.M. 1974b. Field studies of the diet of Rhabdosargus holubi (Pisces: Teleostei: Sparidae). Journal of Zoology (London) 173: 407–417.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. Buchheister, A., and R.J. Latour. 2011. Trophic ecology of summer flounder in lower Chesapeake Bay inferred from stomach content and stable isotope analyses. Transactions of the American Fisheries Society 140: 1240–1254.CrossRefGoogle Scholar
  13. Buxton, C.D., and H.M. Kok. 1983. Notes on the diet of Rhabdosargus holubi (Steindachner) and Rhabdosargus globiceps (Cuvier) in the marine environment. South African Journal of Zoology 18: 406–408.CrossRefGoogle Scholar
  14. Caut, S., E. Angelo, and F. Courchamp. 2009. Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic value and applications for diet reconstruction. Journal of Applied Ecology 46: 443–453.CrossRefGoogle Scholar
  15. Cortés, E. 1997. A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fished. Canadian Journal of Fisheries and Aquatic Sciences 54: 726–738.CrossRefGoogle Scholar
  16. Cowley, P.D., and A.K. Whitfield. 2002. Biomass and production estimates of a fish community in a small South African estuary. Journal of Fish Biology 61(Supplement A): 74–89.CrossRefGoogle Scholar
  17. Cremona, F., D. Planas, and M. Lucotte. 2010. Influence of functional feeding groups and spatiotemporal variables on the δ15N signature of littoral macroinvertebrates. Hydrobiologia 647: 51–61.CrossRefGoogle Scholar
  18. Dalu, T., N.B. Richoux, and P.W. Froneman. 2016. Nature and source of suspended particulate matter and detritus along an austral temperate river-estuary continuum, assessed using stable isotope analysis. Hydrobiologia http://link.springer.com/article/10.1007/s10750-015-2480-1.
  19. De Wet, P.S., and J.F.K. Marais. 1990. Stomach content analysis of juvenile Cape stumpnose Rhabdosargus holubi in the Swartkops Estuary, South Africa. South African Journal of Marine Science 9: 127–133.CrossRefGoogle Scholar
  20. 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.CrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. Fry, B. 2013. Alternative approaches for solving underdetermined isotope mixing problems. Marine Ecology Progress Series 472: 1–13.CrossRefGoogle Scholar
  23. Gillanders, B.M., K.W. Able, J.A. Brown, D.B. Eggleston, and P.F. Sheridan. 2003. Evidence of connectivity between juvenile and adult habitats for mobile marine fauna: an important component of nurseries. Marine Ecology Progress Series 247: 281–295.CrossRefGoogle Scholar
  24. Herzka, S.Z. 2005. Assessing connectivity of estuarine fishes based on stable isotope ratio analysis. Estuarine, Coastal and Shelf Science 64: 58–69.CrossRefGoogle Scholar
  25. Hobson, K.A. 1999. Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120: 314–326.CrossRefGoogle Scholar
  26. Hyslop, E.J. 1980. Stomach contents analysis—a review of methods and their application. Journal of Fish Biology 17: 411–429.CrossRefGoogle Scholar
  27. Jardine, T., B. Pusey, S. Hamilton, N. Pettit, P. Davies, M. Douglas, V. Sinnamon, I. Halliday, and S. Bunn. 2012. Fish mediate high food web connectivity in the lower reaches of a tropical floodplain river. Oecologia 168: 829–838.CrossRefGoogle Scholar
  28. Kelly, L.J., and C. Martínez del Rio. 2010. The fate of carbon in growing fish: an experimental study of isotopic routing. Physiological and Biochemical Zoology 83: 473–480.CrossRefGoogle Scholar
  29. Lugendo, B.R., I. Nagelkerken, G. Van der Velde, and Y.D. Mgaya. 2006. The importance of mangroves, mud and sand flats, and seagrass beds as feeding areas for juvenile fishes in Chwaka Bay, Zanzibar: gut content and stable isotope analyses. Journal of Fish Biology 69: 1639–1661.CrossRefGoogle Scholar
  30. Marcarelli, A.M., C.V. Baxter, M.M. Mineau, and R.O. Hall. 2011. Quantity and quality: unifying food web and ecosystem perspectives on the role of resource subsidies in freshwaters. Ecology 92(6): 1215–1225.CrossRefGoogle Scholar
  31. Martínez 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.CrossRefGoogle Scholar
  32. McCann, K.S., J.B. Rasmussen, and J. Umbanhowar. 2005. The dynamics of spatially coupled food webs. Ecology Letters 8: 513–523.CrossRefGoogle Scholar
  33. McCutchan, J.H.J., W.M.J. 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.CrossRefGoogle Scholar
  34. Miller, T.W., K.L. Bosley, J. Shibata, R.D. Brodeur, K. Omori, and R. Emmett. 2013. Contribution of prey to Humboldt squid Dosidicus gigas in the northern California Current, revealed by stable isotope analyses. Marine Ecology Progress Series 477: 123–134.CrossRefGoogle Scholar
  35. Moore, J.W., and B.X. Semmens. 2008. Incorporating uncertainty and prior knowledge into stable isotope mixing models. Ecology Letters 11: 470–480.CrossRefGoogle Scholar
  36. Moyo, S. 2016. Aquatic-terrestrial trophic linkages via riverine invertebrates in a South African catchment. PhD dissertation, Rhodes University, Grahamstown, under review.Google Scholar
  37. Nelson, J., R. Wilson, F. Coleman, C. Koenig, D. DeVries, C. Gardner, and J. Chanton. 2012. Flux by fin: fish-mediated carbon and nutrient flux in the northeastern Gulf of Mexico. Marine Biology 159: 365–372.CrossRefGoogle Scholar
  38. 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.CrossRefGoogle Scholar
  39. Paterson, A.W., and A.K. Whitfield. 1997. A stable carbon isotope study of the food-web in a freshwater-deprived South African estuary, with particular emphasis on the ichthyofauna. Estuarine, Coastal and Shelf Science 45: 705–715.CrossRefGoogle Scholar
  40. Peterson, M.S. 2003. A conceptual view of environment-habitat-production linkages in tidal river estuaries. Reviews in Fisheries Science 11: 291–313.CrossRefGoogle Scholar
  41. Phillips, D., S. Newsome, and J. Gregg. 2005. Combining sources in stable isotope mixing models: alternative methods. Oecologia 144(4): 520–527.CrossRefGoogle Scholar
  42. Phillips, D.L., R. Inger, S. Bearshop, A.L. Jackson, J.W. Moore, A. Parnell, B.X. Semmens, and E.J. Ward. 2014. Best practices for use of stable isotope mixing models in food-web studies. Canadian Journal of Zoology 92: 823–835.CrossRefGoogle Scholar
  43. Platell, M.E., and P. Freewater. 2009. Importance of saltmarsh to fish species of a large south-eastern Australian estuary during a spring tide cycle. Marine and Freshwater Research 60: 936–941.CrossRefGoogle Scholar
  44. Polis, G.A., W.B. Anderson, and R.D. Holt. 1997. Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annual Review of Ecology and Systematics 28: 289–316.CrossRefGoogle Scholar
  45. Post, D.M. 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83: 703–718.CrossRefGoogle Scholar
  46. Ray, G.C. 2005. Connectivities of estuarine fishes to the coastal realm. Estuarine and Coastal Marine Science 64: 18–32.CrossRefGoogle Scholar
  47. Richardson, J.S., Y. Zhang, and L.B. Marczak. 2010. Resource subsidies across the land–freshwater interface and responses in recipient communities. River Research and Applications 26(1): 55–66.CrossRefGoogle Scholar
  48. Rooker, J.R., and J.T. Turner. 2006. Trophic ecology of Sargassum-associated fishes in the Gulf of Mexico determined from stable isotopes and fatty acids. Marine Ecology Progress Series 313: 249–259.CrossRefGoogle Scholar
  49. Secor, D.H., and J.R. Hooker. 2005. Connectivity in life histories of fishes that use estuaries. Estuarine, Coastal and Shelf Science 64: 1–3.CrossRefGoogle Scholar
  50. Semmens, B.X., E.J. Ward, A.C. Parnell, D.L. Phillips, S. Bearhop, R. Inger, A. Jackson, and J.W. Moore. 2013. Statistical basis and outputs of stable isotope mixing models: comment on Fry (2013). Marine Ecology Progress Series 490: 285–289.CrossRefGoogle Scholar
  51. Sheppard, J.N., A.K. Whitfield, P.D. Cowley, and J.M. Hill. 2012. Effects of altered estuarine submerged macrophyte bed cover on the omnivorous Cape stumpnose Rhabdosargus holubi. Journal of Fish Biology 80: 705–712.CrossRefGoogle Scholar
  52. Vanderklift, M.A., and S. Ponsard. 2003. Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136: 169–182.CrossRefGoogle Scholar
  53. Wasserman, R.J., and N.A. Strydom. 2011. The importance of estuary head waters as nursery areas for young estuary- and marine-spawned fishes in temperate South Africa. Estuarine, Coastal and Shelf Science 94: 56–67.CrossRefGoogle Scholar
  54. Wasserman, R.J., N.A. Strydom, and O. Weyl. 2011. Diet of largemouth bass, Micropterus salmoides (Centrarchidae), an invasive alien in the lower reaches of an Eastern Cape river, South Africa. African Zoology 46: 378–386.CrossRefGoogle Scholar
  55. Whitfield, A.K. 1984. The effects of prolonged aquatic macrophyte senescence on the biology of the dominant fish species in a southern African coastal lake. Estuarine, Coastal and Shelf Science 18: 315–329.CrossRefGoogle Scholar
  56. Whitfield, A.K. 1998. Biology and ecology of fishes in southern African estuaries. Ichthyological Monographs of the J.L.B. Smith Institute of Ichthyology 2: 1–223.Google Scholar
  57. Whitfield, A.K., and S.J.M. Blaber. 1978. Feeding ecology of piscivorous birds at Lake St Lucia. Part I: Diving birds. Ostrich 49: 185–198.CrossRefGoogle Scholar
  58. 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.CrossRefGoogle Scholar
  59. Zar, J.H. 1999. Biostatistical Analysis, 4th ed. Upper Saddle River, NJ: Prentice-Hall.Google Scholar

Copyright information

© Coastal and Estuarine Research Federation 2016

Authors and Affiliations

  • L. Carassou
    • 1
    • 2
    • 3
  • A. K. Whitfield
    • 2
  • L. Bergamino
    • 1
    • 4
  • S. Moyo
    • 1
  • N. B. Richoux
    • 1
  1. 1.Department of Zoology and EntomologyRhodes UniversityGrahamstownSouth Africa
  2. 2.South African Institute for Aquatic BiodiversityGrahamstownSouth Africa
  3. 3.Labex COTE, Integrative and Theoretical Integrative Ecology ChairUniversity of BordeauxBordeauxFrance
  4. 4.Centro Universitario Regional Este (CURE)Universidad de la RepúblicaRochaUruguay

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