Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

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.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • 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 52:837–841

    Article  Google Scholar 

  • 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, Barcelona

  • Barros NB, Ostrom PH, Stricker CA, Wells RS (2009) Stable isotopes differentiate bottlenose dolphins off west-central Florida. Mar Mamm Sci 26:324–336

    Article  Google Scholar 

  • Bas C, Morales E (1966) Crecimiento y desarrollo en Micromesistius (Gadus, Merlangus) poutassou. Investigación Pesquera 30:179–195

    Google Scholar 

  • 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 1197–1204

    Google Scholar 

  • 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 60:11–22

    Article  CAS  Google Scholar 

  • 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 32:516–523

    Article  CAS  Google Scholar 

  • Boyle PR (1983) Cephalopod life cycles. Volume I. Species accounts. Academic press, London

    Google Scholar 

  • 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):1–8

    Google Scholar 

  • CODA (2009) Cetacean offshore distribution and abundance. Final report. available from SMRU, Gatty Marine Laboratory, University of St Andrews, St Andrews, Fife, KY16 8LB, UK

  • 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, FAO

  • 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 19–125

    Google Scholar 

  • 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 263:287–298

    Article  Google Scholar 

  • de Niro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506

    Article  Google Scholar 

  • de Niro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351

    Article  Google Scholar 

  • 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 154:603–612

    Article  Google Scholar 

  • Dos Santos ME, Lacerda M (1987) Preliminary observations of the bottlenose dolphin (Tursiops truncatus) in the Sado estuary (Portugal). Aquat Mamm 13:65–80

    Google Scholar 

  • Evans PGH (1980) Cetaceans in British waters. Mamm Rev 10:1–52

    Article  Google Scholar 

  • Fernández R (2010) Ecology of the bottlenose dolphin, Tursiops truncatus (Montagu 1821), in Galician waters, NW Spain. PhD thesis, Universidade de Vigo, Spain

  • 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

  • France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: food web implications. Mar Ecol Prog Ser 124:207–312

    Article  Google Scholar 

  • Guichet R (1995) The diet of European hake (Merluccius merluccius) in the northern part of the Bay of Biscay. ICES J Mar Sci 52:21–31

    Article  Google Scholar 

  • Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326

    Article  Google Scholar 

  • Hobson KA, Piatt JF, Pitochelli J (1994) Using stable isotopes to determine seabird trophic relationships. Jour Anim Ecol 63(4):786–798

    Article  Google Scholar 

  • 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 53:528–533

    Article  Google Scholar 

  • 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 79:1442–1454

    Article  Google Scholar 

  • Ingram SN, Rogan E (2002) Identifying critical areas and habitat preferences of bottlenose dolphins Tursiops truncatus. Mar Ecol Prog Ser 244:247–255

    Article  Google Scholar 

  • Jenkins S, Partridge ST, Stephenson TR, Farley SD, Robins TC (2001) Nitrogen and carbon isotope fractionation between mothers, neonates and nursing offspring. Oecologia 129:336–341

    Google Scholar 

  • Knoff A, Hohn A, Macko S (2008) Ontogenetic diet changes in bottlenose dolphins (Tursiops truncatus) reflected through stable isotopes. Mar Mamm Sci 24:128–137

    Article  Google Scholar 

  • 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 38–43

  • 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 210:203–221

    Article  CAS  Google Scholar 

  • López A (2003) Estatus dos pequenos cetáceos da plataforma de Galicia. PhD Thesis. Universidade de Santiago de Compostela, Spain

  • 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 82:513–521

    Article  Google Scholar 

  • López A, Pierce GJ, Valeiras X, Santos MB, Guerra A (2004) Distribution patters of small cetaceans in Galician waters. J mar biol Ass UK 84:283–294

    Article  Google Scholar 

  • 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, Turkey

  • McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulphur. Oikos 102:378–390

    Article  CAS  Google Scholar 

  • 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):724–730

    Article  CAS  Google Scholar 

  • 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 165–195

    Google Scholar 

  • 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 151:605–615

    Article  Google Scholar 

  • 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 2003

  • Mouat B, Collins MA, Pompert J (2001) Patterns in the diet of Illex argentinus (Cephalopoda: Ommastrephidae) from the Falkland Islands jigging fishery. Fish Res 52:41–49

    Article  Google Scholar 

  • 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 272:1217–1226

    Article  CAS  Google Scholar 

  • 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 157:56

    Google Scholar 

  • Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLOS ONE 5(3):e9672

    Article  Google Scholar 

  • Pierce GJ, Boyle PR (1991) A review of methods for diet analysis in piscivorous marine mammals. Oceanogr Mar Biol Annu Rev 29:409–486

    Google Scholar 

  • 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

  • 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 259–270

  • 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 1207–1210

    Google Scholar 

  • Raitt DFS (1968) Synopsis of biological data on the blue whiting Micromesistius poutassou (Risso, 1810). FAO Fisheries Synopsis, 34

  • 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 87:231–241

    Article  Google Scholar 

  • 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, UK

  • 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 133:336–346

    Article  Google Scholar 

  • Sorbe, JC (1980) Regime alimentaire de Micromesistius poutassou (Risso, 1826) dans le sud du Golfe de Gascogne. Ifremer. Available via Archimer. http://www.ifremer.fr/docelec/doc/1980/publication-4469.pdf. Accessed 22 Nov 2009

  • 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 680–710

    Google Scholar 

  • Vanderklift M, Ponsard S (2003) Sources of variation in consumer-diet d15 N enrichment: a meta analysis. Oecologia 136:169–182

    Article  Google Scholar 

  • 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, Spain

  • 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 122–128

    Google Scholar 

  • 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 34:1365–1374

    Article  Google Scholar 

Download references

Acknowledgments

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).

Author information

Authors and Affiliations

  1. School of Biological Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen, AB24 2TZ, Scotland, UK

    Ruth Fernández & Graham J. Pierce

  2. CEMMA, Ap. 15, 36380, Gondomar, Spain

    Ruth Fernández, Alfredo López & Jose A. Martínez-Cedeira

  3. Ecology Department, Universidad Autónoma de Madrid, 28049, Madrid, Spain

    Susana García-Tiscar

  4. Instituto Español de Oceanografía, Cabo Estay, P.O. Box 1552, 36200, Canido, Vigo, Spain

    M. Begoña Santos & Graham J. Pierce

  5. NERC Life Sciences Mass Spectrometry Facility, SUERC, Rankine Avenue, East Kilbride, G75 0QF, Scotland, UK

    Jason Newton

Authors
  1. Ruth Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Susana García-Tiscar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Begoña Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alfredo López
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jose A. Martínez-Cedeira
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jason Newton
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Graham J. Pierce
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ruth Fernández.

Additional information

Communicated by C. Harrod.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fernández, R., García-Tiscar, S., Begoña Santos, M. et al. Stable isotope analysis in two sympatric populations of bottlenose dolphins Tursiops truncatus: evidence of resource partitioning?. Mar Biol 158, 1043–1055 (2011). https://doi.org/10.1007/s00227-011-1629-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-011-1629-3

Keywords

Search

Navigation