Advertisement

Plasticity and specialisation in the isotopic niche of African clawless otters foraging in marine and freshwater habitats

Abstract

Individual-level behavioural plasticity resulting from differences in environmental conditions is prevalent in many organisms and may result in phenomena such as dietary- or habitat specialisation. The isotopic niche of African clawless otters, Aonyx capensis, occupying different habitats was investigated with the use of stable isotope techniques. Stable isotope analyses revealed that African clawless otter isotopic niche varied between, as well as within, individuals and varied when compared to conspecifics occupying different habitats. Some otters varied their isotopic niche and foraging areas temporally, whilst others did not. The isotopic niche of African clawless otters in a coastal habitat overlapped substantially with previous reports on otter diet, but illustrated that otters eat more shark and molluscs than previously estimated. In freshwater habitats, not all otters had trout in their isotopic niche, although this prey item was abundantly available in the study area. Our results suggest that the African clawless otters can exhibit substantial behavioural plasticity. Such evident adaptability is likely to benefit otters and allow for extended use of non-pristine environments affected by human disturbance when sufficient quantities of prey remain available.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

References

  1. Angerbjörn, A., Hersteinsson, P., Lidén, K., Nelson, E., 1994. Dietary variation inarctic foxes (Alopex lagopus) — an analysis of stable carbon isotopes. Oecologia 99, 226–232.

  2. Arden-Clarke, C.H.G., 1986. Population density, home range size and spatial organization of the Cape clawless otter, Aonyx capensis, in a marine habitat. J.Zool. (Lond.) 209, 201–221.

  3. Badyaev, A.V., 2005. Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation. Proc. R. Soc. Brit. 272, 877–886.

  4. Bateson, P., Gluckman, P., 2011. Plasticity, Robustness, Development and Evolution. Cambridge University Press, Cambridge.

  5. Bojarska, K., Selva, N., 2012. Spatial patterns in brown bear Ursus arctos diet: the role of geographical and environmental factors. Mamm. Rev. 42 (2), 120–143.

  6. Bolnick, D.I., Svanback, R., Fordyce, J.A., Yang, L.H., Davis, J.M., Hulsey, C.D., Forister, M.L., 2003. The ecology of individuals: incidence and implications of individual specialization. Am. Nat. 161, 1–28.

  7. Bownes, S.J., McQuaid, C.D., 2006. Will the invasive mussel Mytilus galloprovincialis Lamarck replace the indigenous Perna perna L. On the southcoast of South Africa? J. Exp. Mar. Biol. Ecol. 338, 140–151.

  8. Boyer, B., Grue, C.E., 1995. The need for water quality criteria for frogs. Environ. Health Perspect. 103, 352–357.

  9. Branch, G.M., Steffani, C.N., 2004. Can we predict the effects of alien species? Acase-history of the invasion of South Africa by Mytilus galloprovincialis (Lamarck). J. Exp. Mar. Biol. Ecol. 300, 189–215.

  10. Brown, A.C., 1996. Behavioural plasticity is a key factor in the survival and evolution of the macrofauna on exposed sandy beaches. Rev. Chil. Hist. Nat. 69, 469–474.

  11. Butler, J.R.A., Du Toit, J.T., 1994. Diet and conservation of Cape clawless otters in eastern Zimbabwe. S. Afr. J. Wildl. Res. 24, 41–47.

  12. Carrasco, T.S., Botta, S., Machado, R., Simões-Lopes, P.C., Carvalho-Junior, O., Ott, P.H., Colares, E.P., Secchi, E.R., 2019. Isotopic niche of the Neotropical otter, Lontra longicaudis (Carnivora, Mustelidae), in different coastal aquatic systems in southern Brazil. Hydrobiologia 835, 83–100.

  13. Carss, D.N., Parkinson, S.G., 1996. Errors associated with otter Lutra lutra faecalanalysis in assessing general diet from spraints. J. Zool. (Lond.) 238, 301–307.

  14. Clavero, M., Prenda, J., Delibes, M., 2003. Trophic diversity of the otter (Lutra lutraL.) in temperate and Mediterranean freshwater habitats. J. Biogeogr. 30, 761–769.

  15. Clementz, M.T., Koch, P.L., 2001. Differentiating aquatic mammal habitat and foraging ecology with stable isotopes in tooth enamel. Oecologia 129, 461–472.

  16. Coplen, T.B., 1994. Reporting of stable hydrogen, carbon, and oxygen isotopic abundances. Pure Appl. Chem. 66, 273–276.

  17. Day, C.C., Westover, M.D., McMillan, B.R., 2015. Seasonal diet of the northern river otter (Lontra canadensis): what drives prey selection? Can. J. Zool. 93, 197–205.

  18. de Vos, M., 2018. Human-predator Conflict in the South African Fly-fishing Industry: Fish Survival Probabilities and Stakeholder Perceptions. Unpublished MSc Dissertation. University of Pretoria, South Africa.

  19. Emmerson, W., Philip, S., 2004. Diets of Cape clawless otters at two South African coastal localities. Afr. Zool. 39, 201–210.

  20. Englund, J., 1965. Studies on the food ecology of the Red fox (Vulpes vulpes) in Sweden. Viltrevy 3, 377–484.

  21. Estes, J.A., Riedman, M.L., Staedler, M.M., Tinker, M.T., Lyon, B.E., 2003. Individual variation in prey selection by sea otters: patterns, causes and implications. J. Anim. Ecol. 72, 144–155.

  22. Farquhar, G.D., Ehleringer, J.R., Hubick, K.T., 1989. Carbon isotope discrimination and photosynthesis. In: Briggs, W.R. (Ed.), Annual Review of Plant Physiology and Plant Molecular Biology Vol 40. Annual Reviews. Palo Alto, pp. 503–538.

  23. Ford, J.K.B., Ellis, G.M., Barrett-Lennard, L.G., Morton, A.B., Palm, R.S., Balcomb, K.C., 1998. Dietary specialization in two sympatric populations of killer whales (Orcinus orca) in coastal British Columbia and adjacent waters. Can. J. Zool. 76, 1456–1471.

  24. Fry, B., Wainright, S.C., 1991. Diatom sources of carbon-13 rich carbon in marine food webs. Mar. Ecol. Prog. Ser. 76, 149–157.

  25. Ghalambor, C.K., Angeloni, L.M., Carroll, S.P., 2010. Behavior as phenotypic plasticity. In: D.F, Fox, C.W. (Eds.), Westneatv, Evolutionary Behavioral Ecology. Oxford University Press, New York, pp. 90–107.

  26. Glasser, J.W., 1982. A theory of trophic strategies: the evolution of facultative specialists. Am. Nat. 119, 250–262.

  27. Gorgadze, G., 2013. Seasonal diet of the otter (Lutra lutra) on the Alazani River(Georgia). Hystrix 24, 157–160.

  28. Grey, J., 2001. Ontogeny and dietary specialization in brown trout (Salmo trutta L.) from Loch Ness, Scotland, examined using stable isotopes of carbon and nitrogen. Ecol. Freshw. Fish 10, 168–176.

  29. Hanekom, N., Southwood, A., Ferguson, M., 1989. A vegetation survey of the Tsitsikamma Coastal National Park. Koedoe 32, 47–67.

  30. Hemminga, M.A., Mateo, M.A., 1996. Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies. Mar. Ecol. Prog. Ser. 140, 285–298.

  31. Hilderbrand, G.V., Farley, S.D., Robbins, C.T., Hanley, T.A., Titus, K., Servheen, C., 1996. Use of stable isotopes to determine diets of living and extinct bears. Can. J. Zool. 74, 2080–2088.

  32. Hobson, K.A., Welch, H.E., 1992. Determination of trophic relationships within a high Arctic marine food web using δ13C and δ15N analysis. Mar. Ecol. Prog. Ser. 84, 9–18.

  33. Hoffmann, A.A., Parsons, P.A., 1997. Extreme Environmental Change and Evolution. Cambridge University Press.

  34. Hooker, S.K., Iverson, S.J., Ostrom, P., Smith, S.C., 2001. Diet of northern bottlenose whales inferred from fatty-acid and stable isotope analyses of biopsy samples. Can. J. Zool. 79, 1442–1454.

  35. Iriarte, J.A., Franklin, W.L., Johnson, W.E., Redford, K.H., 1990. Biogeographic variation of food habits and body size of the America puma. Oecologia 85, 185–190.

  36. Iverson, S.J., Frost, K.J., Lowry, L.F., 1997. Fatty acid signatures reveal fine scales tructure of foraging distribution of harbor seals and their prey in Prince William Sound. Alaska. Mar. Ecol. Prog. Ser. 151, 255–271.

  37. Jenkins, D., Walker, J.G.W., McCowan, D., 1979. Analysis of otter (Lurra lutra) faeces from Deeside, N.E. Scotland. J. Zool. (Lond.) 187, 235–244.

  38. Jonsson, B., Jonsson, N., 2009. A review of the likely effects of climate change on anadromous Atlantic salmon Salmo salar and brown trout Salmo trutta, with particular reference to water temperature and flow. J. Fish Biol. 75, 2381–2447.

  39. Jordaan, R.K., McIntyre, T., Somers, M.J., Bester, M.N., 2015. An assessment of spatial and temporal variation in the diet of Cape clawless otters (Aonyx capensis) in marine environments. Afr. J. Wildl. Res. 45, 342–353.

  40. Klare, U., Kamler, J.F., McDonald, D.W., 2011. A comparison and critique of different scat-analysis methods for determining carnivore diet. Mam. Rev. 41, 294–312.

  41. KPMG, 1999. Mpumalanga Tourism Growth Plan. Unpublished Report. Nelspruit: Mpumalanga Tourism Authority.

  42. Kruuk, H., Goudswaard, P.C., 1990. Effects of changes in fish populations in Lake Victoria on the food of otters (Lutra maculicollis Schinz and Aonyx capensis Lichtenstein). Afr. J. Ecol. 28, 322–329.

  43. Lerner, J.E., Ono, K., Hernandez, K.M., Runstadler, J.A., Puryear, W.B., Polito, M.J., 2018. Evaluating the use of stable isotope analysis to infer the feeding ecology of a growing US gray seal (Halichoerus grypus) population. PLoS One 13, e0192241.

  44. Lübcker, N., Condit, R., Beltran, R.S., de Bruyn, P.J.N., Bester, M.N., 2016. Vibrissal growth parameters of southern elephant seals Mirounga leonina: obtaining fine-scale, time-based stable isotope data. Mar. Ecol. Prog. Ser. 559, 243–255.

  45. Meynier, L., Pusineri, C., Spitz, J., Santos, M.B., Pierce, G.J., Ridoux, V., 2008. Intraspecific dietary variation in the short-beaked common dolphin Delphinus delphis in the Bay of Biscay: importance of fat fish. Mar. Ecol. Prog. Ser. 354, 277–287.

  46. Minagawa, M., Wada, E., 1984. Stepwise enrichment of 15N along food chains: further evidence and the relation between 15N and animal age. Geochim. Cosmochim. Acta 48, 1135–1140.

  47. Moore, J.W., Semmens, B.X., 2008. Incorporating uncertainty and prior information into stable isotope mixing models. Ecol. Lett. 11, 470–480.

  48. Newsome, S.D., Tinker, M.T., Monson, D.H., Oftedal, O.T., Ralls, K., Staedler, M.M., Fogel, M.L., Estes, J.A., 2009. Using stable isotopes to investigate individual diet specialization in California sea otters (Enhydra lutris nereis). Ecology 90, 961–974.

  49. Newsome, S.D., Bentall, G.B., Tinker, M.T., Oftedal, O.T., Ralls, K., Estes, J.A., Fogel, M.L., 2010. Variation in δ13C and δ15N diet-vibrissae trophic discrimination factors in a wild population of California sea otters. Ecol. Appl. 20, 1744–1752.

  50. Norbury, G.L., Sanson, G.D., 1992. Problems with measuring diet selection of terrestrial, mammalian herbivores. Aust. J. Ecol. 17, 1–7.

  51. Nussey, D.H., Wilson, A.J., Brommer, J.E., 2007. The evolutionary ecology of individual phenotypic plasticity in wild populations. J. Evol. Biol. 20, 831–844.

  52. O’Leary, M.H., 1981. Carbon isotope fractionation in plants. Phytochemistry 20, 553–567.

  53. Parnell, A.C., Inger, R., Bearhop, S., Jackson, A.L., 2010. Source partitioning using stable isotopes: coping with too much variation. PLoS One 5, e9672.

  54. Parnell, A., R package version 0.3 2016. SIMMR: A Stable Isotope Mixing Model.

  55. Phillips, D.L., Gregg, J.W., 2003. Source partitioning using stable isotopes: coping with too many sources. Oecologia 136, 261–269.

  56. Piersma, T., Drent, J., 2003. Phenotypic flexibility and the evolution of organismal design. Trends Ecol. Evol. (Amst.) 18, 228–233.

  57. Ponsonby, D.W., Schwaibold, U., 2018. Country otter, city otter: the distribution patterns of two otter species in an urbanized area of Gauteng, South Africa. Afr. J. Ecol., 1–7.

  58. R Core Team, 2018. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.

  59. Rheingantz, M.L., Santiago-Plata, V.M., Trinca, C.S., 2017. The Neotropical otter Lontra longicaudis: a comprehensive update on the current knowledge and conservation status of this semiaquatic carnivore. Mamm. Rev. 47, 291–305.

  60. Reznick, D.N., Endler, J.A., 1982. The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution 36, 160–177.

  61. Reznick, D., Yang, A.P., 1993. The influence of fluctuating resources on life history: patterns of allocation and plasticity in female guppies. Ecology 74, 2011–2019.

  62. Rowe-Rowe, D.T., 1977a. Variation in the predatory behaviour of the clawless otter. Lammergeyer 23, 22–27.

  63. Rowe-Rowe, D.T., 1977b. Food ecology of otters in Natal, South Africa. Oikos 28, 210–219.

  64. Rowe-Rowe, D.T., 1991. Status of otters in Africa. Habitat 6, 15–20.

  65. Rowe-Rowe, D.T., Somers, M.J., 1998. Diet, foraging behaviour and coexistence of African otters and the water mongoose. Symp. Zool. Soc. Lond. 71, 215–227.

  66. Schumann, E.H., Cohen, A.L., Jury, M.R., 1995. Coastal sea surface temperature variability along the south coast of South Africa and the relationship to regional and global climate. J. Mar. Res. 53, 231–248.

  67. Smith, D.C., van Buskirk, J., 1995. Phenotypic design, plasticity, and ecological performance in two tadpole species. Am. Nat. 145, 211–233.

  68. Snell-Rood, E.C., 2013. An overview of the evolutionary causes and consequences of behavioural plasticity. Anim. Behav. 85, 1004–1011.

  69. Somers, M.J., 2000. Seasonal variation in the diet of Cape clawless otters (Aonyxcapensis) in a marine habitat. Afr. Zool. 35, 261–268.

  70. Somers, M.J., Purves, M.G., 1996. Trophic overlap between three semi-aquatic carnivores: Cape clawless otter, spotted-necked otter and water mongoose. Afr. J. Ecol. 34, 158–166.

  71. Somers, M.J., Nel, J.A.J., 2003. Diet in relation to prey of Cape clawless otters in two South African rivers. Afr. Zool. 38, 317–326.

  72. Tinker, M.T., Costa, D.P., Estes, J.A., Wieringa, N., 2007. Individual dietary specialization and dive behaviour in the California sea otter: using archivaltime-depth data to detect alternative foraging strategies. Deep Sea Res. Part II Top. Stud. Oceanogr. 54, 330–342.

  73. Tinker, M.T., Estes, J.A., Bentall, G., 2008. Food limitation leads to behavioral diversification and dietary specialization in sea otters. Proc. Nat. Acad. Sci. USA 105, 560–565.

  74. van der Zee, D., 1979. Food and Status of the Cape Clawless Otter, Aonyx capensis Schinz, in the Tsitsikamma Coastal National Park, South Africa. M. SC. Thesis. University of Pretoria, South Africa.

  75. van der Zee, D., 1981. Prey of the Cape clawless otter (Aonyx capensis) in the Tsitsikamma Coastal National Park, South Africa. J. Zool. (Lond.) 194, 467–483.

  76. Walton, M.J., Henderson, R.J., Pomeroy, P.P., 2000. Use of blubber fatty acid profiles to distinguish dietary differences between grey seals Halichoerus grypus from two UK breeding colonies. Mar. Ecol. Prog. Ser. 193, 201–208.

  77. West-Eberhard, M.J., 2003. Developmental Plasticity and Evolution. Oxford University Press, New York.

  78. Watson, L.H., Lang, A.J., 2003. Diet of Cape clawless otters in Groenvlei Lake, South Africa. S. Afr. J. Wildl. Res. 33, 135–137.

  79. Zhou, Y.B., Newman, C., Xu, W.T., Buesching, C.D., Zalewski, A., Kaneko, Y., Macdonald, D.W., Xie, Z.Q., 2011. Biogeographical variation in the diet of Holarctic martens (genus Martes, Mammalia: carnivora: mustelidae): adaptive foraging in generalists. J. Biogogr. 38, 137–147.

Download references

Author information

Correspondence to Rowan K. Jordaan.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Jordaan, R.K., Somers, M.J., Hall, G. et al. Plasticity and specialisation in the isotopic niche of African clawless otters foraging in marine and freshwater habitats. Mamm Biol 98, 61–72 (2019). https://doi.org/10.1016/j.mambio.2019.07.006

Download citation

Keywords

  • Behavioural plasticity
  • Diet
  • Isotope analysis
  • Trout
  • Conflict
  • Africa