Incorporating stable isotopes into a multidisciplinary framework to improve data inference and their conservation and management application

African Journal of Marine Science

Volumn 37, Issue 2, 2015, Pages 189-197

  Christiansen, H M ^a   Fisk, A T ^a   Hussey, N E ^a  

^a UNIVERSITY OF WINDSOR   (Canada)

Author keywords

carbon isotopes; individualisation; maternal influence; nitrogen isotopes; physiological effects; spatial variation

Indexed keywords

CONSERVATION MANAGEMENT; DATA SET; INDIVIDUALISM; ISOTOPIC ANALYSIS; NITROGEN ISOTOPE; POPULATION STRUCTURE; SHARK; SPATIAL VARIATION; SPECIES CONSERVATION; STABLE ISOTOPE;

CARCHARODON CARCHARIAS;

EID: 84938838289     PISSN: 1814232X     EISSN: 18142338     Source Type: Journal    
DOI: 10.2989/1814232X.2015.1039583     Document Type: Article

References (88)

1. M.K.Alonso, E.A.Crespo, N.A.García, S.N.Pedraza, P.A.Mariottie, N.J.Mora 2002. Fishery and ontogenetic driven changes in the diet of the spiny dogfish, Squalus acanthias, in Patagonian waters, Argentina. Environmental Biology of Fishes 63: 193–202. doi: 10.1023/A:1014229432375
2. D.Aurioles, P.L.Koch, B.J.Le Boeuf 2006. Differences in foraging location of Mexican and California elephant seals: evidence from stable isotopes in pups. Marine Mammal Science 22: 326–338. doi: 10.1111/j.1748-7692.2006.00023.x
3. P.B.Best, D.M.Schell 1996. Stable isotopes in southern right whale (Eubalaena australis) baleen as indicators of seasonal movements, feeding and growth. Marine Biology 124: 483–494. doi: 10.1007/BF00351030
4. D.C.Blower, J.M.Pandolfi, B.D.Bruce, M.D.C.Gomez-Cabrera, J.R.Ovenden 2012. Population genetics of Australian white sharks reveals fine-scale spatial structure, transoceanic dispersal events and low effective population sizes. Marine Ecology Progress Series 455: 229–244. doi: 10.3354/meps09659
5. D.I.Bolnick, R.Svanbäck, J.A.Fordyce, L.H.Yang, J.M.Davis, C.D.Hulsey, M.L.Forister 2003. The ecology of individuals: incidence and implications of individual specialization. The American Naturalist 161: 1–28. doi: 10.1086/343878
6. D.I.Bolnick, L.H.Yang, J.A.Fordyce, J.M.Davis, R.Svanbäck 2002. Measuring individual-level resource specialization. Ecology 83: 2936–2941. doi: 10.1890/0012-9658(2002)083[2936:MILRS]2.0.CO;2
7. A.L.Bond, A.W.Diamond 2011. Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecological Applications 21: 1017–1023. doi: 10.1890/09-2409.1
8. R.Bonfil, M.Meÿer, M.C.Scholl, R.Johnson, S.O'Brien, H.Oosthuizen 2005. Transoceanic migration, spatial dynamics, and population linkages of white sharks. Science 310: 100–103. doi: 10.1126/science.1114898
9. H.T.S.Boschker, J.J.Middelburg 2002. Stable isotopes and biomarkers in microbial ecology. FEMS Microbiology Ecology 40: 85–95. doi: 10.1111/j.1574-6941.2002.tb00940.x
10. B.D.Bruce, R.W.Bradford 2008. Spatial dynamics and habitat preferences of juvenile white sharks—identifying critical habitat and options for monitoring recruitment. Final report to Department of Environment, Water, Heritage and the Arts. CSIRO, Hobart.
11. B.D.Bruce, R.W.Bradford 2012. Habitat use and spatial dynamics of juvenile white sharks, Carcharodon carcharias, in eastern Australia. In: M.L.Domeier (ed.), Global perspectives on the biology and life history of the white shark. Boca Raton: CRC Press. pp 225–253.
12. S.E.Campana, L.J.Natanson, S.Myklevoll 2002. Bomb dating and age determination of large pelagic sharks. Canadian Journal of Fisheries and Aquatic Sciences 59: 450–455. doi: 10.1139/f02-027
13. A.B.Carlisle, K.J.Goldman, S.Y.Litvin, D.J.Madigan, J.S.Bigman, A.M.Swithenbank 2014. Stable isotope analysis of vertebrae reveals ontogenetic changes in habitat in an endothermic pelagic shark. Proceedings of the Royal Society B 282: 20141446. doi: 10.1098/rspb.2014.1446
14. A.B.Carlisle, S.L.Kim, B.X.Semmens, D.J.Madigan, S.J.Jorgensen, C.R.Perle 2012. Using stable isotope analysis to understand the migration and trophic ecology of northeastern Pacific white sharks (Carcharodon carcharias). PLoS ONE 7: e30492. doi: 10.1371/journal.pone.0030492
15. S.Caut, E.Guirlet, E.Angulo, K.Das, M.Girondot 2008. Isotope analysis reveals foraging area dichotomy for Atlantic leatherback turtles. PLoS ONE 3: e1845. doi: 10.1371/journal.pone.0001845
16. S.A.Ceriani, J.D.Roth, D.R.Evans, J.F.Weishampel, L.M.Ehrhart 2012. Inferring foraging areas of nesting loggerhead turtles using satellite telemetry and stable isotopes. PLoS ONE 7: e45335. doi: 10.1371/journal.pone.0045335
17. T.K.Chapple, S.J.Jorgensen, S.D.Anderson, P.E.Kanive, A.P.Klimley, L.W.Botsford, B.A.Block 2011. A first estimate of white shark, Carcharodon carcharias, abundance off Central California. Biology Letters 7: 581–583.
18. Y.Cherel, K.A.Hobson 2007. Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Marine Ecology Progress Series 329: 281–287. doi: 10.3354/meps329281
19. Y.Cherel, K.A.Hobson, F.Bailleul, R.Groscolas 2005. Nutrition, physiology and stable isotopes: new information from fasting and molting penguins. Ecology 86: 2881–2888. doi: 10.1890/05-0562
20. C.A.Choy, P.C.Davison, J.C.Drazen, A.Flynn, E.J.Gier, J.C.Hoffman 2012. Global trophic position comparison of two dominant mesopelagic fish families (Myctophidae, Stomiidae) using amino acid nitrogen isotopic analyses. PLoS ONE 7: e50133. doi: 10.1371/journal.pone.0050133
21. H.M.Christiansen, N.E.Hussey, S.P.Wintner, G.Cliff, S.F.J.Dudley, A.T.Fisk 2014a. Effect of sample preparation techniques for carbon and nitrogen stable isotope analysis of hydroxyapatite structures in the form of elasmobranch vertebral central. Rapid Communications in Mass Spectrometry 28: 448–456. doi: 10.1002/rcm.6801
22. H.M.Christiansen, V.Lin, S.Tanaka, A.Velikanov, H.F.Mollet, S.P.Wintner 2014b. The last frontier: catch records of white sharks (Carcharodon carcharias) in the northwest Pacific Ocean. PLoS ONE 9: e94407.
23. S.M.Clegg, J.F.Kelly, M.Kimura, T.B.Smith 2003. Combining genetic markers and stable isotopes to reveal population connectivity and migration patterns in a Neotropical migrant, Wilson's warbler (Wilsonia pusilla). Molecular Ecology 12: 819–830. doi: 10.1046/j.1365-294X.2003.01757.x
24. G.Cliff, L.J.V.Compagno, M.J.Smale, R.P.van der Elst, S.P.Wintner 2000. First records of white sharks, Carcharodon carcharias, from Mauritius, Zanzibar, Madagascar and Kenya. South African Journal of Science 96: 365–367.
25. L.I.E.Couturier, C.A.Rohner, A.J.Richardson, A.D.Marshall, F.R.A.Jaine, M.B.Bennett 2013. Stable isotope and signature fatty acid analyses suggest reef manta rays feed on demersal zooplankton. PLoS ONE 8: e77152. doi: 10.1371/journal.pone.0077152
26. R.A.Cunjak, J.M.Roussel, M.A.Gray, J.P.Dietrich, D.F.Cartwright, K.R.Munkittrick, T.D.Jardine 2005. Using stable isotope analysis with telemetry or mark-recapture data to identify fish movement and foraging. Oecologia 144: 636–646. doi: 10.1007/s00442-005-0101-9
27. M.J.DeNiro, S.Epstein 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42: 495–506. doi: 10.1016/0016-7037(78)90199-0
28. M.J.DeNiro, S.Epstein 1981. Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45: 341–351. doi: 10.1016/0016-7037(81)90244-1
29. M.L.Domeier, N.Nasby-Lucas 2013. Two-year migration of adult female white sharks (Carcharodon carcharias) reveals widely separated nursery areas and conservation concerns. Animal Biotelemetry 1: 2–9. doi: 10.1186/2050-3385-1-2
30. N.K.Dulvy, S.L.Fowler, J.A.Musick, R.D.Cavanagh, P.M.Kyne, L.R.Harrison 2014. Extinction risk and conservation of the world's sharks and rays. eLife 3: e00590. doi: 10.7554/eLife.00590
31. J.A.Estrada, M.Lutcavage, S.R.Thorrold 2005. Diet and trophic position of Atlantic Bluefin tuna (Thunnus thynnus) inferred from stable carbon and nitrogen isotope analysis. Marine Biology 147: 37–45. doi: 10.1007/s00227-004-1541-1
32. R.L.France 1995. Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Marine Ecology Progress Series 124: 307–312. doi: 10.3354/meps124307
33. M.P.Francis 1996. Observations on a pregnant white shark with a review of reproductive biology. In: A.P.Klimley, D.G.Ainley (eds), Great white sharks: the biology of Carcharodon carcharias. San Diego: Academic Press. pp 157–172.
34. L.Z.Gannes, C.Martínez del Rio, P.Koch 1998. Natural abundance variations in stable isotopes and their potential uses in animal physiological ecology. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 119: 725–737. doi: 10.1016/S1095-6433(98)01016-2
35. L.Z.Gannes, D.M.O'Brien, C.Martinez del Rio 1997. Stable isotopes in animal ecology: assumptions, caveats and a call for more laboratory experiments. Ecology 78: 1271–1276. doi: 10.1890/0012-9658(1997)078[1271:SIIAEA]2.0.CO;2
36. M.R.Heithaus, J.J.Vaudo, S.Kreicker, C.A.Layman, M.Krützen, D.A.Burkholder 2013. Apparent resource partitioning and trophic structure of large-bodied marine predators in a relatively pristine seagrass ecosystem. Marine Ecology Progress Series 481: 225–237. doi: 10.3354/meps10235
37. D.P.Herman, D.G.Burrow, P.R.Wade, J.W.Durban, C.O.Matkin, R.G.LeDuc 2005. Feeding ecology of eastern North Pacific killer whales Orcinus orca from fatty acid, stable isotope, and organochlorine analyses of blubber biopsies. Marine Ecology Progress Series 302: 275–291. doi: 10.3354/meps302275
38. G.V.Hilderbrand, S.D.Farley, C.T.Robbins, T.A.Hanley, K.Titus, C.Servheen 1996. Use of stable isotopes to determine diets of living and extinct bears. Canadian Journal of Zoology 74: 2080–2088. doi: 10.1139/z96-236
39. J.M.Hill, C.D.McQuaid, S.Kaehler 2006. Biogeographic and nearshore-offshore trends in isotope ratios of intertidal mussels and their food sources around the coast of southern Africa. Marine Ecology Progress Series 318: 63–73. doi: 10.3354/meps318063
40. K.A.Hobson 1999. Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120: 314–326. doi: 10.1007/s004420050865
41. K.A.Hobson, R.T.Alisauskas, R.G.Clark 1993. Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. The Condor 95: 388–394. doi: 10.2307/1369361
42. K.A.Hobson, R.G.Clark 1993. Turnover of 13C in cellular and plasma fractions of blood: implications for non-destructive sampling in avian dietary studies. The Auk 110: 638–641. doi: 10.2307/4088430
43. K.A.Hobson, H.E.Welch 1992. Determination of trophic relationships within a high Arctic marine food web using δ13C and δ15N analysis. Marine Ecology Progress Series 84: 9–18. doi: 10.3354/meps084009
44. K.Honda, H.Kagiwada, N.Takahashi, K.Miyashita 2012. Seasonal stream habitat of adult Sakhalin taimen, Parahucho perryi, in the Bekanbeushi River system, eastern Hokkaido, Japan. Ecology of Freshwater Fish 21: 640–657. doi: 10.1111/j.1600-0633.2012.00585.x
45. L.A.Hückstädt, P.L.Koch, B.I.McDonald, M.E.Goebel, D.E.Crocker, D.P.Costa 2012. Stable isotope analyses reveal individual variability in the trophic ecology of a top marine predator, the southern elephant seal. Oecologia 169: 395–406. doi: 10.1007/s00442-011-2202-y
46. N.E.Hussey, S.F.J.Dudley, I.D.McCarthy, G.Cliff, A.T.Fisk 2011. Stable isotope profiles of large marine predators: viable indicators of trophic position, diet, and movement in sharks? Canadian Journal of Fisheries and Aquatic Sciences 68: 2029–2045. doi: 10.1139/f2011-115
47. N.E.Hussey, S.T.Kessel, K.Aarestrup, S.J.Cooke, P.D.Cowley, A.T.Fisk 2015b. Aquatic animal telemetry: a panoramic window into the underwater world. Science 348: 1255642. doi: 10.1126/science.1255642
48. N.E.Hussey, M.A.MacNeil, B.McMeans, J.Olin, S.F.J.Dudley, G.Cliff 2014. Rescaling the trophic structure of marine food webs. Ecology Letters 17: 239–250. doi: 10.1111/ele.12226
49. N.E.Hussey, M.A.MacNeil, M.C.Siple, B.N.Popp, S.F.J.Dudley, A.T.Fisk 2015a. Expanded trophic complexity among large sharks. Food Webs 4: 1–7. doi: 10.1016/j.fooweb.2015.04.002
50. N.E.Hussey, H.M.McCann, G.Cliff, S.F.J.Dudley, S.P.Wintner, A.T.Fisk 2012. Size-based analysis of diet and trophic position of the white shark (Carcharodon carcharias) in South African waters. In: M.L.Domeier (ed.), Global perspectives on the biology and life history of the great white shark. Boca Raton: CRC Press. pp 27–49.
51. S.P.Johnson, D.E.Schindler 2009. Trophic ecology of Pacific salmon (Oncorhynchus spp.) in the ocean: a synthesis of stable isotope research. Ecological Research 24: 855–863. doi: 10.1007/s11284-008-0559-0
52. V.I.Kharlamenko, S.I.Kiyashko, A.B.Imbs, D.I.Vyshkvartzev 2001. Identification of food sources of invertebrates from the seagrass Zostera marina community using carbon and sulfur stable isotope ratio and fatty acid analyses. Marine Ecology Progress Series 220: 103–117. doi: 10.3354/meps220103
53. S.L.Kim, M.T.Tinker, J.A.Estes, P.L.Koch 2012. Ontogenetic and among-individual variation in foraging strategies of northeast Pacific white sharks based on stable isotope analysis. PLoS ONE 7: e45068. doi: 10.1371/journal.pone.0045068
54. J.J.Kiszka, A.Aubail, N.E.Hussey, M.R.Heithaus, F.Caurant, P.Bustamante 2015. Plasticity of trophic interactions among sharks from the oceanic south-western Indian Ocean revealed by stable isotope and mercury analyses. Deep-Sea Research I 96: 49–58. doi: 10.1016/j.dsr.2014.11.006
55. C.G.Lowe, B.M.Wetherbee, G.L.Crow, A.L.Tester 1996. Ontogenetic dietary shifts and feeding behaviour of the tiger shark, Galeocerdo cuvier, in Hawaiian waters. Environmental Biology of Fishes 47: 203–211. doi: 10.1007/BF00005044
56. C.Martínez del Rio, 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. doi: 10.1111/j.1469-185X.2008.00064.x
57. P.Matich, M.R.Heithaus 2013. Multi-tissue stable isotope analysis and acoustic telemetry reveal seasonal variability in the trophic interactions of juvenile bull sharks in a coastal estuary. Journal of Animal Ecology 83: 199–213. doi: 10.1111/1365-2656.12106
58. P.Matich, M.R.Heithaus, C.A.Layman 2010. Size-based variation in intertissue comparisons of stable carbon and nitrogen isotopic signatures of bull sharks (Carcharhinus leucas) and tiger sharks (Galeocerdo cuvier). Canadian Journal of Fisheries and Aquatic Sciences 67: 877–885. doi: 10.1139/F10-037
59. P.Matich, M.R.Heithaus, C.A.Layman 2011. Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. Journal of Animal Ecology 80: 294–305. doi: 10.1111/j.1365-2656.2010.01753.x
60. J.W.McClelland, J.P.Montoya 2002. Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83: 2173–2180. doi: 10.1890/0012-9658(2002)083[2173:TRATNI]2.0.CO;2
61. B.C.McMeans, J.A.Olin, G.W.Benz 2009. Stable-isotope comparisons between embryos and mothers of a placentatrophic shark species. Journal of Fish Biology 75: 2464–2474. doi: 10.1111/j.1095-8649.2009.02402.x
62. F.Ménard, A.Lorrain, M.Potier, F.Marsac 2007. Isotopic evidence of distinct feeding ecologies and movement patterns in two migratory predators (yellowfin tuna and swordfish) of the western Indian Ocean. Marine Biology 153: 141–152. doi: 10.1007/s00227-007-0789-7
63. M.Minagawa, E.Wada 1984. Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48: 1135–1140. doi: 10.1016/0016-7037(84)90204-7
64. J.W.Moore, B.X.Semmens 2008. Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters 11: 470–480. doi: 10.1111/j.1461-0248.2008.01163.x
65. J.Navarro, L.López, M.Coll, C.Barría, R.Sáez-Liante 2014. Short- and long-term importance of small sharks in the diet of the rare deep-sea shark Dalatias licha. Marine Biology 161: 1697–1707.
66. J.Navarro, M.Louzao, J.M.Igual, D.Oro, A.Delgado, J.M.Arcos 2009. Seasonal changes in the diet of a critically endangered seabird and the importance of trawling discards. Marine Biology 156: 2571–2578. doi: 10.1007/s00227-009-1281-3
67. S.D.Newsome, M.T.Tinker, D.H.Monson, O.T.Oftedal, K.Ralls, M.M.Staedler 2009. Using stable isotopes to investigate individual diet specialization in California sea otters (Enhydra lutris nereis). Ecology 90: 961–974. doi: 10.1890/07-1812.1
68. J.A.Olin, N.E.Hussey, M.Fritts, M.R.Heupel, C.A.Simpfendorfer, G.R.Poulakis, A.T.Fisk 2011. Maternal meddling in neonatal sharks: implications for interpreting stable isotopes in young animals. Rapid Communications in Mass Spectrometry 25: 1008–1016. doi: 10.1002/rcm.4946
69. A.T.Pardini, C.S.Jones, L.R.Noble, B.Kreiser, H.Malcolm, B.D.Bruce 2001. Sex-biased dispersal of great white sharks. Nature 412: 139–140. doi: 10.1038/35084125
70. A.C.Parnell, R.Inger, S.Bearhop, A.L.Jackson 2010. Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5: e9672. doi: 10.1371/journal.pone.0009672
71. B.J.Peterson, B.Fry 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18: 293–320. doi: 10.1146/annurev.es.18.110187.001453
72. D.L.Phillips, J.W.Gregg 2003. Source partitioning using stable isotopes: coping with too many sources. Oecologia 136: 261–269. doi: 10.1007/s00442-003-1218-3
73. D.L.Phillips, R.Inger, S.Bearhop, A.L.Jackson, J.W.Moore, A.C.Parnell 2014. Best practices for use of stable isotope mixing models in food web studies. Canadian Journal of Zoology 92: 823–835. doi: 10.1139/cjz-2014-0127
74. R.A.Phillips, S.Bearhop, R.A.R.Mcgill, D.A.Dawson 2009. Stable isotopes reveal individual variation in migration strategies and habitat preferences in a suite of seabirds during the nonbreeding period. Oecologia 160: 795–806. doi: 10.1007/s00442-009-1342-9
75. R.Ramos, F.Ramírez, J.L.Carrasco, L.Jover 2011. Insights into the spatiotemporal component of feeding ecology: an isotopic approach for conservation management sciences. Diversity and Distributions 17: 338–349. doi: 10.1111/j.1472-4642.2010.00736.x
76. A.E.Rosenblatt, J.C.Nifong, M.R.Heithaus, F.J.Mazzotti, M.S.Cherkiss, B.M.Jeffery 2015. Factors affecting individual foraging specialization and temporal diet stability across the range of a large “generalist” apex predator. Oecologia 178: 5–16. doi: 10.1007/s00442-014-3201-6
77. D.R.Rubenstein, K.A.Hobson 2004. From birds to butterflies: animal movement patterns and stable isotopes. Trends in Ecology and Evolution 19: 256–263. doi: 10.1016/j.tree.2004.03.017
78. J.A.Seminoff, S.R.Benson, K.E.Arthur, T.Eguchi, P.H.Dutton, R.F.Tapilatu, B.N.Popp 2012. Stable isotope tracking of endangered sea turtles: validation with satellite telemetry and δ15N analysis of amino acids. PLoS ONE 7: e37403. doi: 10.1371/journal.pone.0037403
79. M.J.Smale 2008. Pelagic shark fisheries in the Indian Ocean. In: M.D.Camhi, E.K.Pikitch, E.A.Babcock (eds), Sharks of the open ocean. Oxford: Blackwell Publishing. pp 247–259.
80. C.N.Trueman, R.A.R.McGill, P.H.Guyard 2005. The effect of growth rate on tissue-diet isotopic spacing in rapidly growing animals. An experimental study with Atlantic salmon (Salmo salar). Rapid Communications in Mass Spectrometry 19: 3239–3247. doi: 10.1002/rcm.2199
81. S.Uchida, M.Todo, K.Teshima, K.Yano 1996. Pregnant white sharks and full-term embryos from Japan. In: A.P.Klimley, D.G.Ainley (eds), Great white sharks: the biology of Carcharodon carcharias. San Diego: Academic Press. pp 139–155.
82. L.O.Valenzuela, M.Sironi, V.J.Rowntree, J.Seger 2009. Isotopic and genetic evidence for culturally inherited site fidelity to feeding grounds in southern right whales (Eubalaena australis). Molecular Ecology 18: 782–791. doi: 10.1111/j.1365-294X.2008.04069.x
83. H.B.Vander Zanden, K.E.Arthur, A.B.Bolten, B.N.Popp, C.J.Lagueux, E.Harrison 2013. Trophic ecology of a green turtle breeding population. Marine Ecology Progress Series 476: 237–249. doi: 10.3354/meps10185
84. H.B.Vander Zanden, K.A.Bjorndal, K.J.Reich, A.B.Bolten 2010. Individual specialists in a generalist population: results from a long-term stable isotope series. Biology Letters 6: 711–714. doi: 10.1098/rsbl.2010.0124
85. J.J.Vaudo, P.Matich, M.R.Heithaus 2010. Mother-offspring isotope fractionation in two species of placentatrophic sharks. Journal of Fish Biology 77: 1724–1727. doi: 10.1111/j.1095-8649.2010.02813.x
86. J.M.Werry, S.Y.Lee, N.M.Otway, Y.Hu, W.Sumpton 2011. A multi-faceted approach for quantifying the estuarine-nearshore transition in the life cycle of the bull shark, Carcharhinus leucas. Marine and Freshwater Research 62: 1421–1431. doi: 10.1071/MF11136
87. C.T.Williams, C.L.Buck, J.Sears, A.S.Kitaysky 2007. Effects of nutritional restriction on nitrogen and carbon stable isotopes in growing seabirds. Oecologia 153: 11–18. doi: 10.1007/s00442-007-0717-z
88. N.Wolf, S.A.Carleton, C.Martínez del Rio 2009. Ten years of experimental animal isotopic ecology. Functional Ecology 23: 17–26. doi: 10.1111/j.1365-2435.2009.01529.x