Marine Biology

, Volume 158, Issue 5, pp 1043–1055 | Cite as

Stable isotope analysis in two sympatric populations of bottlenose dolphins Tursiops truncatus: evidence of resource partitioning?

  • Ruth Fernández
  • Susana García-Tiscar
  • M. Begoña Santos
  • Alfredo López
  • Jose A. Martínez-Cedeira
  • Jason Newton
  • Graham J. Pierce
Original Paper


Skin and muscle from 43 bottlenose dolphins (38 juveniles/adults, 5 calves) stranded in NW Spain were analysed to determine whether stable isotope ratios (δ13C and δ15N) could be used to assess dietary variation, habitat segregation and population substructure. Results were compared with published stomach contents data. Stable isotope ratios from 17 known prey species were also determined. Isotope ratios of the main prey (blue whiting, hake) varied significantly in relation to fish body size. Dolphin calves showed significant heavy isotope enrichments compared to adult females. Excluding calves, δ15N decreased with increasing dolphin body size, probably related to an ontogenetic shift in diet towards species at lower trophic levels, e.g. on blue whiting as suggested by stomach content results. Bottlenose dolphins were divided into two putative populations (North, South) based on previous genetic studies, and values of δ13C and δ15N differed significantly between these two groups, confirming the existence of population structuring.


Trophic Level Enrichment Factor Stable Isotope Ratio Bottlenose Dolphin Lower Trophic Level 
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We thank Ester Molina at the Universidad Autónoma de Madrid and Rona McGill at SUERC (Scottish Universities Environmental Research Centre) for their help with sample preparation. The authors gratefully acknowledge the assistance of volunteers from the Galician strandings network (CEMMA) and the collaboration of Jorge Millos, Jesús Estévez and Antonio Palanca from the University of Vigo. We also thank Antonio González and Lorena Rodríguez from the IEO (Instituto Español de Oceanografía), María del Carmen García, José Luís Fernández and Alfonso Fernández for providing fish and cephalopod samples. Thanks to Colin MacLeod and Stuart Piertney at the University of Aberdeen for useful comments during data analysis and discussion. R.F. was supported during the research period through a Postgraduate grant by Fundación La Caixa and a Marie Curie Early-Stage Research Grant (ECOSUMMER project. 020501-2). The stable isotope analyses were carried out in the NERC (Natural Environment Research Council) Life Sciences Mass Spectrometry Facility (Award number. EK115-10/07). G.J.P. was supported by the ANIMATE project (MEXC-CT-2006-042337).


  1. Abend AG, Smith TD (1995) Differences in ratios of stable isotopes of nitrogen in long-finned pilot whales (Globicephala melas) in the western and eastern North Atlantic. ICES J Mar Sci 52:837–841CrossRefGoogle Scholar
  2. Aguilar A (1997) Inventario de los cetáceos de las aguas atlánticas peninsulares: aplicación de la directiva 92/43/CEE. Memoria Final. Departamento de Biología Animal (Vert.), Facultad de Biología, Universitat de Barcelona, BarcelonaGoogle Scholar
  3. Barros NB, Ostrom PH, Stricker CA, Wells RS (2009) Stable isotopes differentiate bottlenose dolphins off west-central Florida. Mar Mamm Sci 26:324–336CrossRefGoogle Scholar
  4. Bas C, Morales E (1966) Crecimiento y desarrollo en Micromesistius (Gadus, Merlangus) poutassou. Investigación Pesquera 30:179–195Google Scholar
  5. Ben-Tuvia A (1986) Mugilidae. In: Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of the north-eastern Atlantic and the Mediterranean vol. 3. UNESCO, Paris, pp 1197–1204Google Scholar
  6. Bode A, Carrera P, Lens S (2003) The pelagic foodweb in the upwelling ecosystem of Galicia (NW Spain) during spring: natural abundance of stable carbon and nitrogen isotopes. ICES J Mar Sci 60:11–22CrossRefGoogle Scholar
  7. Borrell A, Aguilar A, Tornero V, Sequeira M, Fernández G, Alıs S (2006) Organochlorine compounds and stable isotopes indicate bottlenose dolphin subpopulation structure around the Iberian Peninsula. Environ Int 32:516–523CrossRefGoogle Scholar
  8. Boyle PR (1983) Cephalopod life cycles. Volume I. Species accounts. Academic press, LondonGoogle Scholar
  9. Bozzano A, Recasens L, Sartor P (1997) Diet of the European hake Merluccius merluccius (Pisces: Merluccidae) in the Western Mediterranean (Gulf of Lions). Sci Mar 61(1):1–8Google Scholar
  10. CODA (2009) Cetacean offshore distribution and abundance. Final report. available from SMRU, Gatty Marine Laboratory, University of St Andrews, St Andrews, Fife, KY16 8LB, UKGoogle Scholar
  11. Cohen DM, Inada T, Iwamoto T and Scialabba N (1990) Gadiform fishes of the world (Order Gadiformes). An annotated and illustrated catalogue of cods, hakes, grenadiers and other gadiform fishes known to date. FAO species catalogue. Vol 10, FAOGoogle Scholar
  12. Connor RC, Wells RS, Mann J, Read AJ (2000) The bottlenose dolphin. In: Mann J, Connor RC, Tyack PL, Whitehead H (eds) Cetacean societies. University of Chicago Press, London, pp 19–125Google Scholar
  13. Das K, Lepoint G, Leroy Y, Bouquegneau JM (2003) Marine mammals from the southern North Sea: feeding ecology data from δ13C and δ15N measurements. Mar Ecol Prog Ser 263:287–298CrossRefGoogle Scholar
  14. de Niro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506CrossRefGoogle Scholar
  15. de Niro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351CrossRefGoogle Scholar
  16. de Stephanis R, García-Tiscar S, Verborgh P, Esteban-Pavo R, Pérez S, Minvielle-Sebastia L, Guinet C (2008) Diet of the social groups of long-finned pilot whales (Globicephala melas) in the Strait of Gibraltar. Mar Biol 154:603–612CrossRefGoogle Scholar
  17. Dos Santos ME, Lacerda M (1987) Preliminary observations of the bottlenose dolphin (Tursiops truncatus) in the Sado estuary (Portugal). Aquat Mamm 13:65–80Google Scholar
  18. Evans PGH (1980) Cetaceans in British waters. Mamm Rev 10:1–52CrossRefGoogle Scholar
  19. Fernández R (2010) Ecology of the bottlenose dolphin, Tursiops truncatus (Montagu 1821), in Galician waters, NW Spain. PhD thesis, Universidade de Vigo, SpainGoogle Scholar
  20. Fernández R, Santos MB, Pierce GJ, Llavona A, López A, Silva MA, Ferreira M, Carrillo M, Cermeño P, Lens S and Piertney S (in press) Fine scale genetic structure of bottlenose dolphins (Tursiops truncatus) off Atlantic waters of the Iberian Peninsula. Hydrobiologia Google Scholar
  21. France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: food web implications. Mar Ecol Prog Ser 124:207–312CrossRefGoogle Scholar
  22. Guichet R (1995) The diet of European hake (Merluccius merluccius) in the northern part of the Bay of Biscay. ICES J Mar Sci 52:21–31CrossRefGoogle Scholar
  23. Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326CrossRefGoogle Scholar
  24. Hobson KA, Piatt JF, Pitochelli J (1994) Using stable isotopes to determine seabird trophic relationships. Jour Anim Ecol 63(4):786–798CrossRefGoogle Scholar
  25. Hobson KA, Schell DM, Renouf D, Noseworthy E (1996) Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals. Can J Fish Aquat Sci 53:528–533CrossRefGoogle Scholar
  26. Hooker SK, Iverson SJ, Ostrom P, Smith SC (2001) Diet of northern bottlenose whales inferred from fatty-acid and stable-isotope analysis of biopsy samples. Can J Zool 79:1442–1454CrossRefGoogle Scholar
  27. Ingram SN, Rogan E (2002) Identifying critical areas and habitat preferences of bottlenose dolphins Tursiops truncatus. Mar Ecol Prog Ser 244:247–255CrossRefGoogle Scholar
  28. Jenkins S, Partridge ST, Stephenson TR, Farley SD, Robins TC (2001) Nitrogen and carbon isotope fractionation between mothers, neonates and nursing offspring. Oecologia 129:336–341Google Scholar
  29. Knoff A, Hohn A, Macko S (2008) Ontogenetic diet changes in bottlenose dolphins (Tursiops truncatus) reflected through stable isotopes. Mar Mamm Sci 24:128–137CrossRefGoogle Scholar
  30. Kuiken T (1996) Review of the criteria for the diagnosis of by-catch in cetaceans. In: Kuiken T (ed) Newsletter 26 (special Issue): diagnosis of by-catch in cetaceans, Proceedings of the Second ECS workshop on Cetacean pathology. European Cetacean Society, Saskatoon, Saskatchewan, Canada, pp 38–43Google Scholar
  31. Lesage V, Hammill M, Kovacs KM (2001) Marine mammals and the community structure of the Estuary and Gulf of St Lawrence, Canada: evidence from stable isotope analysis. Mar Ecol Prog Ser 210:203–221CrossRefGoogle Scholar
  32. López A (2003) Estatus dos pequenos cetáceos da plataforma de Galicia. PhD Thesis. Universidade de Santiago de Compostela, SpainGoogle Scholar
  33. López A, Santos MB, Pierce GJ, González AF, Valeiras X, Guerra A (2002) Trends in strandings and by-catch of marine mammals in northwest Spain during the 1990s. J mar biol Ass UK 82:513–521CrossRefGoogle Scholar
  34. López A, Pierce GJ, Valeiras X, Santos MB, Guerra A (2004) Distribution patters of small cetaceans in Galician waters. J mar biol Ass UK 84:283–294CrossRefGoogle Scholar
  35. López A, Ferreira M, Guyomard S, Méndez P, Caldas M, Covelo P (2009) Follow up of a solitary dolphin in three European countries: the case of Jean Floc’h/Gaspar. 23th Conference of the European Cetacean Society, 2–4 March 2009, Istambul, TurkeyGoogle Scholar
  36. McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulphur. Oikos 102:378–390CrossRefGoogle Scholar
  37. McKinney CR, McCrea JM, Epstein S, Allen HA, Urey HC (1950) Improvements in mass spectrometers for the measurement of small differences in isotope abundance ratios. Rev Sci Instrum 21(8):724–730CrossRefGoogle Scholar
  38. Mead JG, Potter CW (1990) Natural history of bottlenose dolphins along the central Atlantic coast of the United States. In: Leatherwood S, Reeves RR (eds) The bottlenose dolphin. Academic Press, San Diego, USA, pp 165–195Google Scholar
  39. Mendes S, Newton J, Reid RJ, Zuur AF, Pierce GJ (2007) Stable carbon and nitrogen isotope ratio profiling of sperm whale teeth reveals ontogenetic movements and trophic ecology. Oecologia 151:605–615CrossRefGoogle Scholar
  40. Morin Y, Lesage V (2003) Effects of dimethyl sulfoxide (DMSO) and lipid extraction methods on stable carbon and nitrogen isotope ratios in the skin of odontocetes and mysticetes. In: 15th Conference of the Society for Marine Mammalogy. Greensboro, NC. EEUU. December 2003Google Scholar
  41. Mouat B, Collins MA, Pompert J (2001) Patterns in the diet of Illex argentinus (Cephalopoda: Ommastrephidae) from the Falkland Islands jigging fishery. Fish Res 52:41–49CrossRefGoogle Scholar
  42. Natoli A, Birkun A, Aguilar A, Lopez A, Hoelzel AR (2005) Habitat structure and the dispersal of male and female bottlenose dolphins (Tursiops truncatus). Proc R Soc Lond B Biol Sci 272:1217–1226CrossRefGoogle Scholar
  43. Olaso I, Rodriguez-Marin E (1995) Alimentacion de veinte especies de peces demersales pertenecientes a la division VIIIc del ICES. Otoño 1991. Inf Tec IEO 157:56Google Scholar
  44. Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLOS ONE 5(3):e9672CrossRefGoogle Scholar
  45. Pierce GJ, Boyle PR (1991) A review of methods for diet analysis in piscivorous marine mammals. Oceanogr Mar Biol Annu Rev 29:409–486Google Scholar
  46. Pierce GJ, Caldas M, Cedeira J, Santos MB, Llavona A, Covelo P, Martínez G, Torres J, Sacau M, López A (2010) Trends in cetacean sightings along the Galician coast, north-western Spain, 2003–2007, and inferences about cetacean habitat preferences. J mar biol Ass UK. doi: 10.1017/S0025315410000664
  47. Quesada A (2005) Estudio de las redes tróficas de ecosistemas acuáticos mediante δ13C y δ15N. In: Alcorlo P, Redondo R, Toledo J (eds) Libro de resúmenes de las jornadas técnicas Nuevas técnicas metodológicas aplicadas al estudio de los ecosistemas: los isótopos estables. Madrid, Spain, 21–25 November 2005 Univerisdad Autónoma de Madrid, Madrid, pp 259–270Google Scholar
  48. Quignard JP, Pras A (1986) Atherinidae. In: Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of the north-eastern Atlantic and the Mediterranean, vol 3. UNESCO, Paris, pp 1207–1210Google Scholar
  49. Raitt DFS (1968) Synopsis of biological data on the blue whiting Micromesistius poutassou (Risso, 1810). FAO Fisheries Synopsis, 34Google Scholar
  50. Santos MB, Fernández R, López A, Martínez JA, Pierce GJ (2007) Variability in the diet of bottlenose dolphin, Tursiops truncatus, in Galician waters, North-Western Spain, 1990–2005. J mar biol Ass UK 87:231–241CrossRefGoogle Scholar
  51. SCANS-II (2008) Small Cetaceans in the European Atlantic and North Sea. Final Report to the European Commission under project LIFE04NAT/GB/000245. Available from SMRU, Gatty Marine Laboratory, University of St Andrews, St Andrews, Fife, KY16 8LB, UKGoogle Scholar
  52. Segura I, Rocha-Olivares A, Flores-Ramírez S, Rojas-Bracho L (2006) Conservation implications of the genetic and ecological distinction of Tursiops truncatus ecotypes in the Gulf of California. Biol Cons 133:336–346CrossRefGoogle Scholar
  53. Sorbe, JC (1980) Regime alimentaire de Micromesistius poutassou (Risso, 1826) dans le sud du Golfe de Gascogne. Ifremer. Available via Archimer. Accessed 22 Nov 2009
  54. Svetovidov AN (1986) Gadidae. In: Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of the North-Eastern Atlantic and the Mediterranean, vol 2. UNESCO, Paris, pp 680–710Google Scholar
  55. Vanderklift M, Ponsard S (2003) Sources of variation in consumer-diet d15 N enrichment: a meta analysis. Oecologia 136:169–182CrossRefGoogle Scholar
  56. VVAA (2007) Bases para la conservación y la gestiόn de las especies de cetaceos amenazadas en las aguas atlánticas y cantábricas. Memoria Final Proyecto Fundaciόn Biodiversidad. CEMMA, Gondomar, SpainGoogle Scholar
  57. Wells RS, Scott MD (2002) Bottlenose dolphins, Tursiops truncatus and Tursiops aduncus. In: Perrin WF, Würsic B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, London, pp 122–128Google Scholar
  58. Wilson B, Thompson P, Hammond PS (1997) Habitat use by Bottlenose dolphins: seasonal distribution and stratified movement patterns in the Moray Firth, Scotland. J App Ecol 34:1365–1374CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Ruth Fernández
    • 1
    • 2
  • Susana García-Tiscar
    • 3
  • M. Begoña Santos
    • 4
  • Alfredo López
    • 2
  • Jose A. Martínez-Cedeira
    • 2
  • Jason Newton
    • 5
  • Graham J. Pierce
    • 1
    • 4
  1. 1.School of Biological SciencesUniversity of AberdeenAberdeenScotland, UK
  2. 2.CEMMAGondomarSpain
  3. 3.Ecology DepartmentUniversidad Autónoma de MadridMadridSpain
  4. 4.Instituto Español de OceanografíaCanido, VigoSpain
  5. 5.NERC Life Sciences Mass Spectrometry FacilitySUERCEast KilbrideScotland, UK

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