, Volume 799, Issue 1, pp 327–348 | Cite as

Dietary tracers and stomach contents reveal pronounced alimentary flexibility in the freshwater mullet (Myxus capensis, Mugilidae) concomitant with ontogenetic shifts in habitat use and seasonal food availability

  • Laure Carassou
  • Alan K. Whitfield
  • Sydney Moyo
  • Nicole B. Richoux
Primary Research Paper


We investigated ontogenetic and seasonal variations in the diet of the freshwater mullet (Myxus capensis) across a river–estuary interface using dietary tracer (stable isotopes and fatty acids) and stomach content analyses. Two hypotheses were tested: (A) the freshwater mullet diet shifts as individuals grow and migrate from the estuary to the river, and (B) the dominant food resources utilized by freshwater mullet vary through time, mainly as a function of the seasonal changes in the availability of preferred food items in each habitat. Both hypotheses were supported, as our results indicated broad dietary flexibility by M. capensis, with utilized food items ranging from benthic microalgae to insects depending on habitat and seasonal patterns in availability of resources. Given the unexpected importance of invertebrate-derived prey, including some of terrestrial origin (i.e. aerial or semi-aquatic insects), during the freshwater phase of the M. capensis life cycle, we also emphasize a need for a re-assessment of the trophic designation of this species (previously designated as a strict detritivore).


Fish trophic ecology Insects Allochthony Detritivory Ontogeny Riparian zone 



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 Paul Cowley, Mandla Magoro, Tatenda Dalu, Leandro Bergamino and Bernadette Hubbart for their assistance with field and/or laboratory work.

Supplementary material

10750_2017_3230_MOESM1_ESM.pdf (20 kb)
Supplementary material 1 (PDF 20 kb)


  1. Abrantes, K. G. & M. Sheaves, 2010. Importance of freshwater flow in terrestrial-aquatic energetic connectivity in intermittently connected estuaries of tropical Australia. Marine Biology 157: 2071–2086.CrossRefGoogle Scholar
  2. Antonio, E. S. & N. B. Richoux, 2014. Trophodynamics of three decapod crustaceans in a temperate estuary using stable isotope and fatty acid analyses. Marine Ecology Progress Series 504: 193–205.CrossRefGoogle Scholar
  3. Babler, A. L., A. Pilati & M. J. Vanni, 2010. Terrestrial support of detritivorous fish populations decreases with watershed size. Ecosphere 2: 1–23.Google Scholar
  4. Baxter, C. V., K. D. Fausch & W. C. Saunders, 2005. Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshwater Biology 50: 201–220.CrossRefGoogle Scholar
  5. Bergamino, L. & 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
  6. Bergamino, L., T. Dalu & N. B. Richoux, 2014. Spatial and temporal patterns in sediment organic matter composition within an estuarine environment: stable isotope and fatty acid signatures. Hydrobiologia 732: 133–145.CrossRefGoogle Scholar
  7. Blaber, S. J. M., 1976. The food and feeding ecology of Mugilidae in the St Lucia lake system. Biological Journal of the Linnean Society 8: 267–277.CrossRefGoogle Scholar
  8. Blaber, S. J. M., 1977. The feeding ecology and relative abundance of mullet (Mugilidae) in Natal and Pondoland estuaries. Biological Journal of the Linnean Society 9: 259–275.CrossRefGoogle Scholar
  9. Blaber, S. J. M. & A. K. Whitfield, 1977. The feeding ecology of juvenile mullet (Mugilidae) in south-east African estuaries. Biological Journal of the Linnean Society 9: 277–284.CrossRefGoogle Scholar
  10. Bok, A. H., 1979. The distribution and ecology of two mullet species in some freshwater rivers in the eastern Cape, South Africa. Journal of the Limnology Society of South Africa 5: 97–102.CrossRefGoogle Scholar
  11. Brett, M. T., M. J. Kainz, S. J. Taipale & H. Seshan, 2009. Phytoplankton, not allochthonous carbon, sustains herbivorous zooplankton production. Proceedings of the National Academy of Science 106: 21197–21201.CrossRefGoogle Scholar
  12. Brett, M. T., G. B. Arhonditsis, S. Chandra & M. Z. Kainz, 2012. Mass flux calculations show strong allochthonous support of freshwater zooplankton in unlikely. PLoS ONE 7: e39508.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Buchleister, A. & 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
  14. Budge, S. M., C. C. Parrish & C. H. Mckenzie, 2001. Fatty acid composition of phytoplankton, settling particulate matter and sediments at a sheltered bivalve aquaculture site. Marine Chemistry 2001: 285–303.CrossRefGoogle Scholar
  15. Budge, S. M., S. A. Iverson & H. N. Koopman, 2006. Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Marine Mammal Science 22: 759–801.CrossRefGoogle Scholar
  16. Carassou, L., A. K. Whitfield, L. Bergamino, S. Moyo & N. B. Richoux, 2016. Trophic dynamics of the Cape stumpnose (Rhabdosargus holubi, Sparidae) across three adjacent aquatic habitats. Estuaries and Coasts 39: 1221–1233.CrossRefGoogle Scholar
  17. Cardona, L., 2016. Food and feeding of Mugilidae. Chapter 9 pp. In Crosetti, D. & S. J. M. Blaber (eds), Biology, Ecology and Culture of Grey Mullets (Mugilidae). CRC Press, Boca Raton: 165–195.CrossRefGoogle Scholar
  18. Carpenter, S. R., J. J. Cole, M. L. Pace, M. Van de Bogert, D. L. Bade, D. Bastviken, C. M. Gille, J. R. Hodgson, J. F. Kitchell & E. Kritzberg, 2005. Ecosystem subsidies: terrestrial support of aquatic food webs from 13C addition to contrasting lakes. Ecology 86: 2737–2750.CrossRefGoogle Scholar
  19. Caut, S., E. Angelo & 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
  20. Cole, J. J., S. R. Carpenter, J. Kitchell, M. L. Pace, C. T. Solomon & B. Weidel, 2011. Strong evidence for terrestrial support of zooplankton in small lakes based on stable isotopes of carbon, nitrogen, and hydrogen. Proceedings of the National Academy of Sciences 108: 1975–1980.CrossRefGoogle Scholar
  21. Cortés, E., 1997. A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Sciences 54: 726–738.CrossRefGoogle Scholar
  22. Crosetti, D. & S. J. M. Blaber (eds), 2016. Biology, Ecology and Culture of Grey Mullets (Mugilidae). CRC Press, Boca Raton.Google Scholar
  23. Dalsgaard, J., M. St John, G. Kattner, D. Müller-Navarra & W. Hagen, 2003. Fatty acid trophic markers in the pelagic marine environment. Advances in Marine Biology 46: 225–340.CrossRefPubMedGoogle Scholar
  24. Dalu, T., P. W. Froneman & N. B. Richoux, 2014. Using multivariate analysis and stable isotopes to assess the effects of substrate type on phytobenthos communities. Inland Waters 4: 397–412.CrossRefGoogle Scholar
  25. Dalu, T., N. B. Richoux & P. W. Froneman, 2016. Nature and source of suspended particulate organic matter and detritus along an austral temperate river-estuary continuum assessed using stable isotope analysis. Hydrobiologia 767: 95–110.CrossRefGoogle Scholar
  26. Elsdon, T. S., 2010. Unraveling diet and feeding histories of fish using fatty acids as natural tracers. Journal of Experimental Marine Biology and Ecology 386: 61–68.CrossRefGoogle Scholar
  27. Folch, J., M. Lees & G. H. Sloane Stanley, 1957. A simple method for the isolation and purification of total lipids from animal tissues. The Journal of Biological Chemistry 226: 497–509.PubMedGoogle Scholar
  28. Franco, A., M. Elliott, P. Franzoi & P. Torricelli, 2008. Life strategies of fishes in European estuaries: the functional guild approach. Marine Ecology Progress Series 354: 219–228.CrossRefGoogle Scholar
  29. Froese, R. & D. Pauly, 2016. Fishbase. World Wide Web electronic publication [available on internet at www.fishbase.org]. Accessed July 2016
  30. Fry, B., 2013. Alternative approaches for solving underdetermined isotope mixing problems. Marine Ecology Progress Series 472: 1–13.CrossRefGoogle Scholar
  31. Fry, B. & E. B. Sherr, 1989. δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. In Rundel, P. W., J. R. Ehleringer & K. A. Nagy (eds), Stable Isotopes in Ecological Research. Springer, New York: 196–229.CrossRefGoogle Scholar
  32. Harrison, T. D. & A. K. Whitfield, 2006. Estuarine typology and the structuring of fish communities in South Africa. Environmental Biology of Fishes 75: 269–293.CrossRefGoogle Scholar
  33. Hobson, K. A., 1999. Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120: 314–326.CrossRefPubMedGoogle Scholar
  34. Hyslop, E. J., 1980. Stomach contents analysis – a review of methods and their application. Journal of Fish Biology 17: 411–429.CrossRefGoogle Scholar
  35. Iitembu, J. A. & N. B. Richoux, 2016. Characterisation of the dietary relationships of two sympatric hake species, Merluccius capensis and M. paradoxus, in the northern Benguela region using fatty acid profiles. African Journal of Marine Science 38: 39–48.CrossRefGoogle Scholar
  36. Indarti, E., M. I. A. Majid, R. Hashim & 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.CrossRefGoogle Scholar
  37. Izquierdo, M., 2005. Essential fatty acid requirements in Mediterranean fish species. Cahiers Options Méditerranéennes 63: 91–102.Google Scholar
  38. Jaschinski, S., D. C. Brepoll & U. Sommer, 2011. The trophic importance of epiphytic algae in a freshwater macrophyte system (Potamogeton perfoliatus L.): stable isotope and fatty acid analyses. Aquatic Sciences 73: 91–101.CrossRefGoogle Scholar
  39. Kelly, J. R. & R. E. Scheibling, 2012. Fatty acids as dietary tracers in benthic food webs. Marine Ecology Progress Series 446: 1–22.CrossRefGoogle Scholar
  40. Koch, P. L. & D. L. Phillips, 2002. Incorporating concentration dependence in stable isotope mixing models: a reply to Robbins, Hilderbrand and Farley (2002). Oecologia 133: 14–18.CrossRefPubMedGoogle Scholar
  41. Lebreton, B. P., P. Richard, E. P. Parlier, G. Guillou & G. F. Blanchard, 2011. Trophic ecology of mullets during their spring migration in a European saltmarsh: a stable isotope study. Estuarine Coastal and Shelf Science 91: 502–510.CrossRefGoogle Scholar
  42. Le Loc’h, F., J.-D. Durand, K. Diop & J. Panfili, 2015. Spatio-temporal isotopic signatures (δ13C and δ15N) reveal that two sympatric West African mullet species do not feed on the same basal production sources. Journal of fish Biology 86: 1444–1453.CrossRefPubMedGoogle Scholar
  43. Lin, H.-J., W.-Y. Kao & Y.-T. Wang, 2007. Analyses of stomach contents and stable isotopes reveal food sources of estuarine detritivorous fish in tropical/subtropical Taiwan. Estuarine Coastal and Shelf Science 73: 527–537.CrossRefGoogle Scholar
  44. Lopes, C. A., E. Benedito-Cecilio & L. A. Martinelli, 2007. Variability in the carbon isotope signature of Prochilodus lineatus (Prochilodontidae, Characiformes) a bottom-feeding fish of the Neotropical region. Journal of Fish Biology 70: 1649–1659.CrossRefGoogle Scholar
  45. Magoro, M. L., A. K. Whitfield & L. Carassou, 2015. Predation by introduced largemouth bass, Micropterus salmoides on indigenous marine fish in the lower Kowie River, South Africa. African Journal of Aquatic Science 40: 81–88.CrossRefGoogle Scholar
  46. Marais, J. F. K., 1980. Aspects of food intake, food selection, and alimentary canal morphology of Mugil cephalus (Linnaeus, 1958), Liza tricuspidens (Smith, 1935), L. richardsoni (Smith, 1846), and L. dumerili (Steindachner, 1869). Journal of Experimental Marine Biology and Ecology 44: 193–209.CrossRefGoogle Scholar
  47. Marcarelli, A. M., C. V. Baxter, M. M. Mineau & R. O. Hall, 2011. Quantity and quality: unifying food web and ecosystem perspectives on the role of resource subsidies in freshwaters. Ecology 92: 1215–1225.CrossRefPubMedGoogle Scholar
  48. Martínez del Rio, C., N. Wolf, S. A. Carleton & L. Z. Gannes, 2009. Isotopic ecology ten years after a call for more laboratory experiments. Biological Reviews 84: 91–111.CrossRefGoogle Scholar
  49. McCutchan, J. H. J., W. M. J. Lewis, C. Kendall & C. C. McGrath, 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen and sulfur. Oikos 102: 378–390.CrossRefGoogle Scholar
  50. Moore, J. W. & B. X. Semmens, 2008. Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters 11: 470–480.CrossRefPubMedGoogle Scholar
  51. Moyo, S., 2016. Aquatic-terrestrial linkages via riverine invertebrates in a South African catchment. Ph.D. Dissertation, Department of Zoology and Entomology, Rhodes University, Grahamstown. Available at Rhodes University eRepository [ available on internet at http://contentpro.seals.ac.za/iii/cpro/]. Accessed on March 18th 2017.
  52. Moyo, S., L. D. Chari, M. H. Villet & N. B. Richoux, 2017. Decoupled reciprocal subsidies of biomass and fatty acids in fluxes of invertebrates between a temperate river and the adjacent riparian land. Aquatic Sciences: in press. doi: 10.1007/s00027-017-0529-0.Google Scholar
  53. Nakano, S. & M. Murakami, 2001. Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proceedings of the National Academy of Science 98: 166–170.CrossRefGoogle Scholar
  54. Nakano, S., H. Miyasaka & N. Kuhara, 1999. Terrestrial-aquatic linkages: riparian arthropod inputs alter trophic cascades in a stream food web. Ecology 80: 2435–2441.Google Scholar
  55. Osman, H., A. R. Suriah & E. C. Law, 2001. Fatty acid composition and cholesterol content of selected marine fish in Malaysian waters. Food Chemistry 73: 55–60.CrossRefGoogle Scholar
  56. Parnell, A., D. L. Phillips, S. Bearshop, B. X. Semmens, E. J. Ward, J. W. Moore, A. L. Jackson, J. Grey, D. J. Kelly & R. Inger, 2013. Bayesian stable isotope mixing models. Environmetrics 24: 387–399.Google Scholar
  57. Parrish, C. C., T. A. Abrajano, S. M. Budge, R. J. Helleur, E. D. Hudson, K. Pulchan & C. Ramos, 2000. Lipid and phenolic biomarkers in marine ecosystems: analysis and interpretation. In Wangersky, P. (ed.), The Handbook of Environmental Chemistry Part D Marine Chemistry, Chapter 8, Vol. 5. Springer-Verlag, Berlin: 193–223.Google Scholar
  58. Phillips, D. L. & P. L. Koch, 2002. Incorporating concentration dependence in stable isotope mixing models. Oecologia 130: 114–125.CrossRefPubMedGoogle Scholar
  59. Philipps, D. L., R. Inger, S. Bearshop, A. L. Jackson, J. W. Moore, A. Parnell, B. X. Semmens & 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
  60. Polis, G. A., W. B. Anderson & R. D. Holt, 1997. Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annual Review of Ecology, Evolution and Systematics 28: 289–316.CrossRefGoogle Scholar
  61. Post, D. M., 2002. Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83: 703–718.CrossRefGoogle Scholar
  62. Pusey, B. J. & A. H. Arthington, 2003. Importance of the riparian zone to the conservation and management of freshwater fish: a review. Marine and Freshwater Research 54: 1–16.CrossRefGoogle Scholar
  63. Richardson, J. S. & T. Sato, 2015. Resource subsidy flows across freshwater-terrestrial boundaries and influence on processes linking adjacent ecosystems. Ecohydrology 8: 406–415.CrossRefGoogle Scholar
  64. Richardson, J. S., Y. Zhang & L. B. Marczak, 2010. Resource subsidies across the land-freshwater interface and responses in recipient communities. River Research and Applications 26: 55–66.CrossRefGoogle Scholar
  65. 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.CrossRefGoogle Scholar
  66. Richoux, N. B. & P. W. Froneman, 2008. Trophic ecology of dominant zooplankton and macrofauna in a temperate and oligotrophic South African estuary: a fatty acid approach. Marine Ecology Progress Series 357: 121–137.CrossRefGoogle Scholar
  67. Richoux, N. B. & R. T. Ndhlovu, 2014. Temporal shifts in the fatty acid profiles of rocky intertidal invertebrates. Marine Biology 161: 2199–2211.CrossRefGoogle Scholar
  68. Robbins, C. T., G. V. Hilderbrand & S. D. Farley, 2002. Incorporating concentration dependence in stable isotope mixing models: a response to Phillips and Koch (2002). Oecologia 133: 10–13.CrossRefPubMedGoogle Scholar
  69. Robin, J. H., C. Regost, J. Arzel & S. J. Kaushik, 2003. Fatty acid profile of fish following a change in dietary fatty acids source: model of fatty acid composition with a dilution hypothesis. Aquaculture 225: 283–293.CrossRefGoogle Scholar
  70. Skadullah, A. & M. Tsuchiya, 2009. The origin of particulate organic matter and the diet of tilapia from an estuarine ecosystem subjected to domestic wastewater discharge: fatty acid analysis approach. Aquatic Ecology 43: 577–589.CrossRefGoogle Scholar
  71. Stock, B.C. & B.X. Semmens, 2013. MixSIAR GUI User Manual. Version 3.1.Google Scholar
  72. Taipale, S., U. Strandberg, E. Peltomaa, A. W. E. Galloway, A. Ojala & M. T. Brett, 2013. Fatty acid composition as biomarkers of freshwater microalgae: analysis of 37 strains of microalgae in 22 genera and in seven classes. Aquatic Microbial Ecology 71: 165–178.CrossRefGoogle Scholar
  73. Takeuchi, T., 1997. Essential fatty acid requirements of aquatic animals with emphasis on fish larvae and fingerlings. Reviews in Fisheries Science 5: 1–25.CrossRefGoogle Scholar
  74. Tocher, D. R., 2010. Fatty acid requirements in ontogeny of marine and freshwater fish. Aquaculture Research 41: 717–732.CrossRefGoogle Scholar
  75. Turner, J. P. & J. R. Rooker, 2005. Effects of dietary fatty acids on the body tissues of larval and juvenile cobia and their prey. Journal of Experimental Marine Biology and Ecology 322: 13–27.CrossRefGoogle Scholar
  76. Turner, J. P. & J. R. Rooker, 2006. Effect of diet on fatty acid compositions in Sciaenops ocellatus. Journal of Fish Biology 67: 1119–1138.CrossRefGoogle Scholar
  77. Van der Bank, M. G., A. C. Utne-Palme, K. Pittman, A. K. Sweetman, N. B. Richoux, V. Brüchert & M. J. Gibbons, 2011. Dietary success of a ‘new’ key fish in an overfished ecosystem: evidence from fatty acid and stable isotope signatures. Marine Ecology Progress Series 428: 219–233.CrossRefGoogle Scholar
  78. Vanderklift, M. A. & S. Ponsard, 2003. Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136: 169–182.CrossRefPubMedGoogle Scholar
  79. Vaz, M. M., M. Jr, L. A. Partinelli Petrere & A. A. Moreto, 1999. The dietary regime of detritivorous fish from the River Jacaré, Brazil. Fisheries Management and Ecology 6: 121–132.CrossRefGoogle Scholar
  80. Wang, L., J. Lyons, P. Rasmussen, P. Seelbach, T. Simon, M. Wiley, P. Kanehl, E. Baker, S. Niemela & P. W. Stewart, 2003. Watershed, reach, and riparian influences on stream fish assemblages in the Northern Lakes and Forest Ecoregion, USA. Canadian Journal of Fisheries and Aquatic Sciences 60: 491–505.CrossRefGoogle Scholar
  81. Wang, C.-H., C.-C. Hsu, W.-N. Tzeng, C.-F. You & C.-W. Chang, 2011. Origin of the mass mortality of the flathead grey mullet (Mugil cephalus) in the Tanshui River, northern Taiwan, as indicated by otolith elemental signatures. Marine Pollution Bulletin 62: 1809–1813.CrossRefPubMedGoogle Scholar
  82. Wantzen, K. M., F. de Arruda Machado, M. Voss, H. Boriss & W. J. Junk, 2002. Seasonal isotopic shifts in fish of the Pantanal wetland, Brazil. Aquatic Sciences 64: 239–251.CrossRefGoogle Scholar
  83. Whitfield, A. K., 1998. Biology and Ecology of Fishes in southern African estuaries. JLB Institute of Ichthyology, South Africa.Google Scholar
  84. Whitfield, A. K., 2016. Ecological role of Mugilidae in the coastal zone. In Crosetti, D. & S. J. M. Blaber (eds), Biology, Ecology and Culture of Grey Mullets (Mugilidae), Chapter 14. CRC Press, Boca Raton: 324–348.CrossRefGoogle Scholar
  85. Zar, J. H., 1999. Biostatistical Analysis, 4th ed. Prentice Hall, Upper Saddle River, NJ.Google Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.Department of Zoology and EntomologyRhodes UniversityGrahamstownSouth Africa
  2. 2.South African Institute for Aquatic BiodiversityGrahamstownSouth Africa
  3. 3.Aquatic Ecology and Global Change (EABX) Research UnitNational Institute of Science and Technology for Environment and Agriculture (Irstea), Bordeaux CenterCestasFrance

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