Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-24T03:14:10.010Z Has data issue: false hasContentIssue false
  • English
  • Français

Feeding ecology of striped dolphins, Stenella coeruleoalba, in the north-western Mediterranean Sea based on stable isotope analyses

Published online by Cambridge University Press:  13 September 2011

A.M. Meissner ,
C.D. MacLeod ,
P. Richard ,
V. Ridoux  and
G. Pierce
A.M. Meissner*
Affiliation:
Institute of Biological and Environmental Sciences (IBES), University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen, AB24 3JG, UK Littoral, Envinnement et Sociétés, UMR 6250 CNRS-Université de La Rochelle, 17000 La Rochelle, France Centre de Recherche sur les Cétacés-Marineland, 306 Avenue Mozart, 06600 Antibes, France
C.D. MacLeod
Affiliation:
Institute of Biological and Environmental Sciences (IBES), University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen, AB24 3JG, UK
P. Richard
Affiliation:
Littoral, Envinnement et Sociétés, UMR 6250 CNRS-Université de La Rochelle, 17000 La Rochelle, France
V. Ridoux
Affiliation:
Littoral, Envinnement et Sociétés, UMR 6250 CNRS-Université de La Rochelle, 17000 La Rochelle, France
G. Pierce
Affiliation:
Instituto Español de Oceanografía, Centro Oceanográfico de Vigo, PO Box 1552, 36200, Vigo, Spain Oceanlab, University of Aberdeen, Main Street, Newburgh, Aberdeenshire, AB41 6AAUK
*
Correspondence should be addressed to: A.M. Meissner, Coastal-Marine Research Group, Institute of Natural Sciences, Massey University, Private Bag 102-904, North Shore City 0745, Auckland, New Zealand email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The feeding ecology of striped dolphin, Stenella coeruleoalba, in the north-western Mediterranean Sea was studied using stable isotope analyses. Carbon and nitrogen stable isotope ratios were measured in skin and muscle tissues of stranded and by-caught dolphins from six geographical areas in the Mediterranean Sea and Atlantic Ocean. Variation in δ15N in relation to dolphin size is attributed to changes in diet. Nursing calves have a higher trophic level than weaned animals and their δ15N values decrease progressively until weaning, estimated to be at a body length of around 155 cm. δ15N values then increased for larger individuals which suggests changes in diet for mature dolphins. Geographical differences in diet were apparent between the Atlantic and the Mediterranean, although no clear differences were apparent between the five Mediterranean areas. Comparisons of the nitrogen isotope ratios of skin and muscle highlighted a higher fractionation in skin compared to the muscle tissue. Values of δ13C also increased with body length although it appears that this is not only driven by trophic level enrichment. δ13C increases before weaning and the difference in trophic level between newly-weaned and mature dolphins was twice as high for carbon as for nitrogen. Ontogenetic changes in carbon isotope composition may therefore be driven by feeding on deep water prey and dolphin movements outside the coastal feeding grounds. Indeed, seasonal variations in δ13C are suspected to be driven by migration within the Mediterranean basin.

Keywords

striped dolphinStenella coeruleoalbafeeding ecologynitrogen and carbon stable isotopesskinmusclenorth-western Mediterranean Sea
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 92 , Issue 8: Marine Mammals , December 2012 , pp. 1677 - 1687
Copyright
Copyright © Marine Biological Association of the United Kingdom 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abend, A.G. and Smith, T.D. (1997) Differences in stable isotope ratios of carbon and nitrogen between long-finned pilot whales (Globicephala melas) and their primary prey in the western north Atlantic. ICES Journal of Marine Science 54, 500–503.CrossRefGoogle Scholar
Aguiar dos Santos, R. and Haimovici, M. (2001) Cephalopods in the diet of marine mammals stranded or incidentally caught along southeastern and southern Brazil (21–24°S). Fisheries Research 52, 99–112.CrossRefGoogle Scholar
Aguilar, A. (2000) Population biology, conservation threats and status of Mediterranean striped dolphins (Stenella coeruleoalba). Journal of Cetacean Research and Management 2, 17–26.Google Scholar
Anderson, D.R., Burnham, K.P. and Thompson, W.L. (2000) Null hypothesis testing: problems, prevalence, and an alternative. Journal of Wildlife Management 64, 912–923.CrossRefGoogle Scholar
Archer, F.I. (1996) Morphological and genetic variation of striped dolphins (Stenella coeruleoalba, Meyen,1833). PhD thesis. University of California.Google Scholar
Archer, F.I. (2000) Striped dolphin (Stenella coeruleoalba). In Perrin, N., Würsig, B. and Thewissen, H.G.M. (eds) Encyclopedia of marine mammals. San Diego, CA: Academic Press, pp. 1201–1203.Google Scholar
Archer, F.I. and Perrin, W.F. (1999) Stenella coeruleoalba. Mammalian Species 603, 1–9.Google Scholar
Azzelino, A., Gaspari, S., Airoldi, S. and Nani, B. (2008) Habitat use and preferences of cetaceans along the continental slope and the adjacent pelagic waters in the western Ligurian Sea. Deep-Sea Research I 55, 296–323.CrossRefGoogle Scholar
Bode, A., Alvarez-Ossorio, M.T. and Varela, M. (2006) Phytoplankton and macrophyte contributions to littoral food webs in the Galician upwelling estimated from stable isotopes. Marine Ecology Progress Series 318, 89–102.CrossRefGoogle Scholar
Boily, P. and Lavigne, D.M. (1997) Developmental and seasonal changes in resting metabolic rates of captive female grey seals. Canadian Journal of Zoology 75, 1781–1798.CrossRefGoogle Scholar
Burns, J.M., Trumble, S.J., Castellini, M.A. and Testa, J.W. (1998) The diet of Weddell seals in McMurdo Sound, Antarctica as determined from scat collections and stable isotope analysis. Polar Biology 19, 272–282.CrossRefGoogle Scholar
Calzada, N. and Aguilar, A. (1995) Geographical variation of body size in western Mediterranean striped dolphins (Stenella coeruleoalba). Zeitschrift für Säugetierkunde 60, 257–264.Google Scholar
Calzada, N., Aguilar, A., Lockyer, C.H. and Grau, E. (1997) Pattern of growth and physical maturity in the western Mediterranean striped dolphin, Stenella coerueloalba (Cetacea: Odontoceti). Canadian Journal of Zoology 75, 632–637.CrossRefGoogle Scholar
Cañadas, A., Sagarminaga, R. and Garcia-Tiscar, S. (2002) Cetacean distribution related with depth and slope in the Mediterranean waters off southern Spain. Deep-Sea Research I 1, 2053–2073.CrossRefGoogle Scholar
Cherel, Y., Fontaine, C., Richard, P. and Labat, J.-P. (2010) Isotopic niches and trophic levels of myctophid fishes and their predators in the Southern Ocean. Limnology and Oceanography 55, 324–332.CrossRefGoogle Scholar
Das, K., Lepoint, G., Loizeau, V., Debacker, V., Dauby, P. and Bouquegneau, J.M. (2000) Tuna and dolphin association in the north-east Atlantic: evidence of different ecological niches from stable isotope and heavy metal measurements. Marine Pollution Bulletin 40, 102–109.CrossRefGoogle Scholar
Das, K., Beans, C., Holsbeek, L., Mauger, G., Berrow, S.D., Rogan, E. and Bouquegneau, J.M. (2003a) Marine mammals from northeast Atlantic: relationship between their trophic status as determined by δ13C and δ15N measurements and their trace metal concentrations. Marine Environmental Research 56, 349–365.CrossRefGoogle ScholarPubMed
Das, K., Lepoint, G., Leroy, Y. and Bouquegneau, J.M. (2003b) Marine mammals from the southern North Sea: feeding ecology data from δ13C and δ15N measurements. Marine Ecology Progress Series 263, 287–298.CrossRefGoogle Scholar
DeNiro, M.J. and Epstein, S. (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, 495–506.CrossRefGoogle Scholar
DeNiro, M.J. and Epstein, S. (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341–351.CrossRefGoogle Scholar
Desportes, G. (1985) La nutrition des Odontocètes en Atlantique nord-est (côtes françaises—Iles Feroë). PhD thesis. Université de Poitiers.Google Scholar
Fernandez, R., Garcia-Tiscar, S., Santos, M.B., Lopez, A., Martinez-Cedeira, J.A., Newton, J. and Pierce, G.J. (2011) Stable isotope analysis in two sympatric populations of bottlenose dolphins Tursiops truncatus: evidence of resource partitioning? Marine Biology 158, 1043–1055.CrossRefGoogle Scholar
Forcada, J., Aguilar, A., Hammond, P.S., Pastor, X. and Aguilar, R. (1994) Distribution and numbers of striped dolphins in the Western Mediterranean Sea after the 1990 epizootic outbreak. Marine Mammal Science 10, 137–150.CrossRefGoogle Scholar
France, R.L. (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Marine Ecology Progress Series 124, 307–312.CrossRefGoogle Scholar
Fry, B. (1988) Food web structure on Georges Bank from stable C, N and S isotopic compositions. Limnology and Oceanography 33, 1182–1190.CrossRefGoogle Scholar
Fry, B. and Sherr, E.B. (1984) δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contributions in Marine Science 27, 13–47.Google Scholar
Gannes, L.Z., Martinez del Rio, C. and Koch, P. (1998) Natural abundance variations in stable isotopes and their potential uses in animal physiological ecology. Comparative Biochemistry and Physiology—Part A: Molecular and Integrative Physiology 119, 725–737.CrossRefGoogle ScholarPubMed
Gannier, A. (1998) Variation saisonnière de l'affinité bathymétrique des cétacés dans le bassin Liguro-Provençal (Méditerranée occidentale). Vie et Milieu 48, 25–34.Google Scholar
Gannier, A. (1999) Les cétacés de Méditerranée: nouveaux résultats sur leur distribution, la structure de leur peuplement et l'abondance relative des différentes espèces. Mésogée 56, 3–19.Google Scholar
Gannier, A. (2005) Summer distribution and relative abundance of delphinids in the Mediterranean Sea. Revue d'Ecologie (Terre et Vie) 60, 223–238.Google Scholar
Garcia-Martinez, J., Moya, A., Raga, J.A. and Latorre, A. (1999) Genetic differentiation of striped dolphin Stenella coeruleoalba from European waters according to mitochondrial DNA (mtDNA) restriction analysis. Molecular Ecology 8, 1069–1073.CrossRefGoogle ScholarPubMed
Gaspari, S. (2004) Social and population structure of striped and Risso's dolphins in the Mediterranean Sea. PhD thesis. University of Durham.Google Scholar
Gordon, J.C.D., Matthews, J.N., Panigada, S., Gannier, A., Borsani, F.J. and Notarbartolo di Sciara, G. (2000) Distribution and relative abundance of striped dolphins, and distribution of sperm whales in the Ligurian Sea cetacean sanctuary. Journal of Cetacean Research and Management 2, 27–36.Google Scholar
Hastie, T.J. and Tibshirani, R.J. (1990) Generalized additive models. New York: Chapman and Hall.Google Scholar
Hicks, B.D., St Aubin, D.J., Geraci, J.R. and Brown, W.R. (1985) Epidermal growth in the bottlenose dophin, Tursiops truncatus. Journal of Investigative Dermatology 85, 60–63.CrossRefGoogle Scholar
Hobson, K.A. and Clark, R.G. (1992) Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation. Condor 94, 189–197.CrossRefGoogle Scholar
Hobson, K.A. and Welch, H.E. (1992) Determination of trophic relationships within a high Arctic marine food web using δ13C and δ13N analysis. Marine Ecology Progress Series 84, 9–18.CrossRefGoogle Scholar
Hobson, K.A., Piatt, J.F. and Pitocchelli, J. (1994) Using stable isotopes to determine seabird trophic relationships. Journal of Animal Ecology 63, 786–798.CrossRefGoogle Scholar
Hobson, K.A., Schell, D.M., Renouf, D. and Noseworthy, E. (1996) Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals. Canadian Journal of Fisheries and Aquatic Sciences 53, 528–533.CrossRefGoogle Scholar
Hobson, K.A., Sease, J.L., Merrick, R.L. and Piatt, J.F. (1997) Investigating trophic relationships of pinnipeds in Alaska and Washington using stable isotope ratios of nitrogen and carbon. Marine Mammal Science 13, 114–132.CrossRefGoogle Scholar
Hooker, S.K., Iverson, S.J., Ostrom, P. and Smith, S. (2001) Diet of northern bottlenose whales inferred from fatty-acid and stable-isotope analyses of biopsy samples. Canadian Journal of Zoology 79, 1442–1454.CrossRefGoogle Scholar
Jennings, S., Pinnegar, J.K., Polunin, N.V.C. and Warr, K.J. (2002) Linking size-based and trophic analyses of benthic community structure. Marine Ecology Progress Series 226, 77–85.CrossRefGoogle Scholar
Knoff, A., Hohn, A. and Macko, S. (2008) Ontogenic diet changes in bottlenose dolphins (Tursiops truncatus) reflected through stable isotopes. Marine Mammal Science 24, 128–137.CrossRefGoogle Scholar
Laran, S. and Drouot-Dulau, V. (2007) Seasonal variation of striped dolphins, fin- and sperm whales' abundance in the Ligurian Sea (Mediterranean Sea). Journal of the Marine Biological Association of the United Kingdom 87, 345–352.CrossRefGoogle Scholar
Marcoux, M., Whitehead, H. and Rendell, L. (2007) Sperm whale feeding variation by location, year, social group and clan: evidence from stable isotopes. Marine Ecology Progress Series 333, 309–314.CrossRefGoogle Scholar
Marini, L., Consiglio, C., Angradi, A.M., Catalano, B., Sanna, A., Valentini, T., Finoia, M.G. and Villetti, G. (1996) Distribution, abundance and seasonality of cetaceans sighted during scheduled ferry crossing in the Central Tyrrhenian Sea: 1989–1992. Italian Journal of Zoology 63, 381–388.CrossRefGoogle Scholar
Markussen, N.H. (1995) Changes in metabolic rate and body composition during starvation and semistarvation in harbour seals. In Blix, A.S., Walloe, L. and Ulltang, O. (eds) Developments in marine biology 4: whales, seals, fish and man. Amsterdam: Elsevier, pp. 383–391.Google Scholar
Minawaga, M. and Wada, E. (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.CrossRefGoogle Scholar
Miyazaki, N., Kusaka, T. and Nishiwaki, M. (1973) Food of Stenella caeruleoalba. Scientific Reports of the Whales Research Institute 25, 265–275.Google Scholar
Monaci, F., Borrell, A., Leonzio, C., Marsili, L. and Calzada, N. (1998) Trace elements in striped dolphins (Stenella coeruleoalba) from the western Mediterranean. Environmental Pollution 99, 61–68.CrossRefGoogle ScholarPubMed
Mook, W.G. and de Vries, J.J. (1989) Volume I: Introduction—theory, methods, review. In Mook, W.G. (ed.) Environmental isotopes in the hydrological cycle. Principles and applications. Paris: UNESCO/IAEA, 271 pp.Google Scholar
Mundry, R. and Nunn, C.L. (2009) Stepwise model fitting and statistical inference: turning noise into signal pollution. American Naturalist 173, 119–123.CrossRefGoogle ScholarPubMed
Murtaugh, P.A. (2009) Performance of several variable-selection methods applied to real ecological data. Ecology Letters 12, 1061–1068.CrossRefGoogle ScholarPubMed
Noren, S.R. and Edwards, E.F. (2007) Physiological and behavioral developement in delphinid calves: implications for calf separation and mortality due to tuna purse-seine sets. Marine Mammal Science 23, 15–29.CrossRefGoogle Scholar
Noren, S.R., Lacave, G., Wells, R.S. and Williams, T.M. (2002) The development of blood oxygen stores in bottlenose dolphins (Tursiops truncatus): implications for diving capacity. Journal of Zoology 258, 105–113.CrossRefGoogle Scholar
Notarbartolo di Sciara, G., Venturino, M.C., Zanardelli, M., Bearzi, G., Borsani, F.J. and Cavalloni, B. (1993) Cetaceans in the central Mediterranean Sea: distribution and sightings frequencies. Bollettino di Zoologia 60, 131–138.CrossRefGoogle Scholar
Ostrom, P.H., Lien, J. and Macko, S.A. (1993) Evaluation of diet of Sowersby's beaked whale, Mesoplodon bidens, based on isotopic comparisons among northwestern Atlantic cetaceans. Canadian Journal of Zoology 71, 858–861.CrossRefGoogle Scholar
Perrin, W.F., Wilson, C.E. and Archer, F.I. (1994) Striped dolphin Stenella coeruleoalba (Meyen, 1833). In Ridgway, S.H. and Harrison, R. (eds) Handbook of marine mammals. Volume 5. The first book of dolphins. London: Academic Press, pp. 129–159.Google Scholar
Peterson, B.J. and Fry, B. (1987) Stable isotopes in ecosystem studies. Annual Review in Ecology and Systematics 18, 293–320.CrossRefGoogle Scholar
Pinnegar, J.K. and Polunin, N.V.C. (1999) Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Functional Ecology 13, 225–231.CrossRefGoogle Scholar
Pinnegar, J.K., Polunin, N.V.C. and Badalamenti, F. (2003) Long-term changes in the trophic level of western Mediterranean fishery and aquaculture landings. Canadian Journal of Fisheries and Aquatic Sciences 60, 222–235.CrossRefGoogle Scholar
Polunin, N.V.C., Morales-Nin, B., Pawsey, W.E., Cartes, J.E., Pinnegar, J.K. and Moranta, J. (2001) Feeding relationships in Mediterranean bathyal assemblages elucidated by stable nitrogen and carbon isotope data. Marine Ecology Progress Series 220, 13–23.CrossRefGoogle Scholar
R Development Core Team (2008) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. ISBN 3-900051-07-0, URL http://www.R-project.orgGoogle Scholar
Rau, G.H., Mearns, A.J., Young, D.R., Olson, R.J., Scheafer, H.A. and Kaplan, I.R. (1983) Animal 13C/12C correlates with trophic level in pelagic food webs. Ecology 64, 1314–1318.CrossRefGoogle Scholar
Reeves, R.R. and Notarbartolo di Sciara, G. (2006) The status and distribution of cetaceans in the Black Sea and Mediterranean Sea. Malaga: IUCN Centre for Mediterranean Cooperation, 137 pp.Google Scholar
Ringelstein, J., Pusinieri, C., Hassani, S., Meynier, L., Nicolas, R. and Ridoux, V. (2006) Food and feeding ecology of the striped dolphin, Stenella coeruleoalba, in the oceanic waters of the north-east Atlantic. Journal of the Marine Biological Association of the United Kingdom 86, 909–918.CrossRefGoogle Scholar
Ruiz-Cooley, R.I., Gendron, D., Aguiniga, S., Mesnick, S. and Carriquiry, J.D. (2004) Trophic relationships between sperm whales and jumbo squid using stable isotopes of C and N. Marine Ecology Progress Series 277, 275–283.CrossRefGoogle Scholar
Ruiz-Cooley, R.I., Villa, E.C. and Gould, W.R. (2010) Ontogenetic variation of δ13C and δ15N recorded in the gladius of the jumbo squid Dosidicus gigas: geographic differences. Marine Ecology Progress Series 399, 187–198.CrossRefGoogle Scholar
Santos, M.B., Clarke, M.R. and Pierce, G.J. (2001) Assessing the importance of cephalopods in the diet of marine mammals and other top predators: problems and solutions. Fisheries Research 52, 121–139.CrossRefGoogle Scholar
Schell, D.M., Saupe, S.M. and Haubenstock, N. (1989) Bowhead whale (Balaena mysticetus) growth and feeding as estimated by δ13C techniques. Marine Biology 103, 433–443.CrossRefGoogle Scholar
Slip, D.J. (1995) The diet of southern elephant seals (Mirounga leonina) from Heard Island. Canadian Journal of Zoology 73, 1519–1528.CrossRefGoogle Scholar
Smith, R.J., Hobson, K.A., Koopman, H.N. and Lavigne, D.M. (1996) Distinguishing between populations of fresh- and salt-water harbour seals (Phoca vitulina) using stable-isotope ratios and fatty acid profiles. Canadian Journal of Fisheries and Aquatic Sciences 53, 272–279.CrossRefGoogle Scholar
Spitz, J., Richard, E., Meynier, L., Pusinieri, C. and Ridoux, V. (2006) Dietary plasticity of the oceanic striped dolphin, Stenella coeruleoalba, in the neritic waters of the Bay of Biscay. Journal of Sea Research 55, 309–320.CrossRefGoogle Scholar
Sponheimer, M., Robinson, T.F., Cerling, T.E., Tegland, L., Roeder, B.L., Ayliffe, L., Dearing, M.D. and Ehlinger, J.R. (2006) Turnover of stable carbon isotopes in the muscle, liver, and breath CO2 of alpacas (Lama pacos). Rapid Communications in Mass Spectrometry 20, 1395–1399.CrossRefGoogle ScholarPubMed
St Aubin, D.J., Smith, T.G. and Geraci, J. (1990) Seasonal epidermal molt in beluga, Delphinapterus leucas. Canadian Journal of Zoology 68, 359–367.CrossRefGoogle Scholar
Steele, K.W. and Daniel, R.M. (1978) Fractionation of nitrogen isotopes by animals: a further complication to the use of variations in the natural abundance of 15N for tracer studies. Journal of Agricultural Science 90, 7–9.CrossRefGoogle Scholar
Takai, N., Onaka, S., Ikeda, Y., Yatsu, A., Kidokoro, H. and Sakamoto, W. (2000) Geographical variations in carbon and nitrogen stable isotope ratios in squid. Journal of the Marine Biological Association of the United Kingdom 80, 675–684.CrossRefGoogle Scholar
Tieszen, L.L., Boutton, T.W., Tesdahl, K.G. and Slade, N.A. (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57, 32–37.CrossRefGoogle ScholarPubMed
Vander Zanden, M.J., Cabana, G. and Rasmussen, J.B. (1997) Comparing trophic position of freshwater fish calculated using stable isotope ratios (δ15N) and literature dietary data. Canadian Journal of Fisheries and Aquatic Sciences 54, 1142–1158.CrossRefGoogle Scholar
Vander Zanden, M.J. and Rasmussen, J.B. (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography 46, 2061–2066.CrossRefGoogle Scholar
Wada, E., Terazaki, M., Kabaya, Y. and Nemoto, T. (1987) 15N and 13C abundances in the Antarctic Ocean with emphasis on the biogeochemical structure of the food web. Deep-Sea Research Part A 34, 829–841.CrossRefGoogle Scholar
Walker, J.L., Potter, C.W. and Macko, S.A. (1999) The diet of modern and historic bottlenose dolphin populations reflected through stable isotopes. Marine Mammal Science 15, 335–350.CrossRefGoogle Scholar
Whittingham, M.J., Stephens, P.A., Bradbury, R.B. and Freckleton, R.P. (2006) Why do we still use stepwise modelling in ecology and behaviour? Journal of Animal Ecology 75, 1182–1189.CrossRefGoogle ScholarPubMed
Witteveen, B.H., Worthy, G.A.J., Wynne, K.M., Hirons, A.C., Andrews III, A.G. and Markel, R.W. (2011) Trophic levels of north Pacific humpback whales (Megaptera novaeangliae) through analysis of stable isotopes: implications on prey and resource quality. Aquatic Mammals 37, 101–110.CrossRefGoogle Scholar
Würsig, B. and Clark, C. (1993) Behavior. In Burns, J.J., Montague, J.J. and Cowles, C.J. (eds) The bowhead whale. Society for Marine Mammalogy, Special Publication No. 2. Lawrence, KS: Allen Press, pp. 157–199.Google Scholar
Würtz, M. and Marrale, D. (1993) Food of striped dolphin, Stenella coeruleoalba, in the Ligurian Sea. Journal of the Marine Biological Association of the United Kingdom 73, 571–578.CrossRefGoogle Scholar
Zuur, A.F., Ieno, E.N. and Smith, G.M. (2007) Analysing ecological data. New York: Springer Science.CrossRefGoogle Scholar
Zuur, A.F., Ieno, E.N. and Elphick, S. (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1, 3–14.CrossRefGoogle Scholar