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Spatial segregation and similar trophic-level diet among eastern Canadian Arctic/north-west Atlantic killer whales inferred from bulk and compound specific isotopic analysis

Published online by Cambridge University Press:  13 November 2013

Cory J.D. Matthews  and
Steven H. Ferguson
Cory J.D. Matthews*
Affiliation:
Department of Biological Sciences, University of Manitoba, Winnipeg, MB, CanadaR3T 2N2
Steven H. Ferguson
Affiliation:
Department of Biological Sciences, University of Manitoba, Winnipeg, MB, CanadaR3T 2N2 Fisheries and Oceans Canada, 501 University Crescent, Winnipeg MB, CanadaR3T 2N6
*
Correspondence should be addressed to: C. Matthews, Department of Biological Sciences, University of Manitoba, Winnipeg, MB, CanadaR3T 2N2 email: cory_matthews@umanitoba.ca
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Abstract

Killer whales in the Eastern Canadian Arctic (ECA) prey on narwhal, beluga, bowhead whales and seals, while further south in the north-west Atlantic (NWA), killer whales off the coast of Newfoundland and Labrador prey on both marine mammals and fish. Bulk and amino acid (AA) specific isotopic composition of dentinal collagen in teeth of 13 ECA/NWA killer whales were analysed to assess the degree, if any, of dietary specialization of killer whales across the region. Dentine was sampled from within annual growth layer groups (GLGs) to construct chronological profiles of stable nitrogen (δ15N) and carbon (δ13C) isotopic compositions for individual whales spanning 3–25 years. Interannual isotopic variation across GLGs was less than that among individuals, and median bulk δ15N values differed by up to 5‰ among individuals. Significant correlation between bulk δ15N values and baseline (source AA) δ15N values indicates much of the observed isotopic variation among individuals reflects foraging within isotopically distinct food webs, rather than diet differences. This interpretation is supported by consistent differences in bulk δ13C values between the two individuals with lowest source AA δ15N values and the remaining whales. After accounting for baseline isotopic variation, comparable δ15N values among individuals indicates similar trophic-level diet, although uncertainties in relative trophic 15N enrichment of individual AAs currently limits trophic position estimates for top consumers. Further research is required to clarify seasonal movement patterns and possible diet shifts of ECA/NWA killer whales to better define their role in marine ecosystems across the region.

Keywords

Orcinus orcadentinegrowth layer groupsstable isotope analysisnitrogencarbonamino acidsmarine mammalsdistribution
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 94 , Issue 6 , September 2014 , pp. 1343 - 1355
Copyright
Copyright © Marine Biological Association of the United Kingdom 2013 

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References

REFERENCES

Amano, M., Yamada, T.K., Brownell, R.L. and Uni, Y. (2011) Age determination and reproductive traits of killer whales entrapped in ice off Aidomari, Hokkaido, Japan. Journal of Mammalogy 92, 275–282.CrossRefGoogle Scholar
Baird, R.W. and Dill, L.M. (1995) Occurrence and behaviour of transient killer whales: seasonal and pod-specific variability, foraging behaviour, and prey handling. Canadian Journal of Zoology 73, 1300–1311.CrossRefGoogle Scholar
Baird, R.W., McSweeney, D.J., Bane, C., Barlow, J., Salden, D.R., Antoine, L.K., LeDuc, R.G. and Webster, D.L. (2006) Killer whales in Hawaiian waters: information on population identity and feeding habits. Pacific Science 60, 523–530.CrossRefGoogle Scholar
Best, P.B., Meÿer, M.A. and Lockyer, C. (2010) Killer whales in South African water—a review of their biology. African Journal of Marine Science 32, 171–186.CrossRefGoogle Scholar
Bloom, W. and Fawcett, D.W. (1975) A textbook of histology. 3rd edition.Philadelphia, PA: W.B. Saunders.Google Scholar
Burdin, A.M., Hoyt, E., Sato, H., Tarasyan, K. and Filatova, O.A. (2004) Resident and transient-type killer whales, Orcinus orca, in southeast Kamchatka, Russia. IWC Report SC/56/SM15.Google Scholar
Cherel, Y. and Hobson, K.A. (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.CrossRefGoogle Scholar
Chikaraishi, Y., Ogawa, N.O., Kashiyama, Y., Takano, Y., Suga, H., Tomitani, A., Miyashita, H., Kitazato, H. and Ohkouchi, N. (2009) Determination of aquatic food-web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnology and Oceanography: Methods 7, 740–750.Google Scholar
Chikaraishi, Y., Kashiyama, Y., Ogawa, N.O., Kitazato, H. and Ohkouchi, N. (2007) Biosynthetic and metabolic controls of nitrogen isotopic composition of amino acids in marine macroalgae and gastropods: implications for aquatic food web studies. Marine Ecology Progress Series 342, 85–90.CrossRefGoogle Scholar
Choy, C.A., Davison, P.C., Drazen, J.C., Flynn, A., Gier, E.J., Hoffman, J.C., McClain-Counts, J.P., Miller, T.W., Popp, B.N., Ross, S.W. and Sutton, T.T. (2012) Global trophic position comparison of two dominant mesopelagic fish families (Myctophidae, Stomiidae) using amino acid nitrogen isotopic analysis. PLOS ONE 7, e50133. doi: 10.1371/journal.pone.0050133.CrossRefGoogle Scholar
Conover, W.J. and Iman, R.L. (1981) Rank transformation as a bridge between parametric and nonparametric statistics. American Statistician 35, 124–129.Google Scholar
Cortés, E. (1999) Standardized diet compositions and trophic levels of sharks. ICES Journal of Marine Science 56, 707–717.CrossRefGoogle Scholar
Dale, J.J., Wallsgrove, N.J., Popp, B.N. and Holland, K.N. (2011) Nursery habitat use and foraging ecology of the brown stingray Dasyatis lata determined from stomach contents, bulk and amino acid stable isotopes. Marine Ecology Progress Series 433, 221–236.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
DeNiro, M.J. (1985) Postmortem preservation and alteration of in vivo bone collagen isotope ratios in relation to paleodietary reconstruction. Nature 317, 806–809.CrossRefGoogle Scholar
Eastoe, J.E. (1963) The amino acid composition of proteins from the oral tissues—II. The matrix proteins in dentine and enamel from developing human deciduous teeth. Archives of Oral Biology 8, 633–652.CrossRefGoogle ScholarPubMed
Estes, J.A., Tinker, M.T., Williams, T.M. and Doak, D.F. (1998) Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282, 473–476.CrossRefGoogle ScholarPubMed
Estrada, J.A., Rice, A.N., Lutcavage, M.E. and Skomal, G.B. (2003) Predicting trophic position in sharks of the north-west Atlantic Ocean using stable isotope analysis. Journal of the Marine Biological Association of the United Kingdom 83, 1347–1350.CrossRefGoogle Scholar
Ferguson, S.H., Higdon, J.W. and Westdal, K.H. (2012a) Prey items and predation behavior of killer whales (Orcinus orca) in Nunavut, Canada based on Inuit hunter interviews. Aquatic Biosystems 8:3.CrossRefGoogle ScholarPubMed
Ferguson, S.H., Kingsley, C.S. and Higdon, J.W. (2012b) Killer whale (Orcinus orca) predation in a multi-prey system. Population Ecology 54, 31–41.CrossRefGoogle Scholar
France, R.L. (1995) Carbon-13 enrichment in benthic compared to planktonic algae: food web implications. Marine Ecology Progress Series 124, 307–312.CrossRefGoogle Scholar
Foote, A.D., Newton, J., Piertney, S.B., Willerslev, E. and Gilbert, M.T.P. (2009) Ecological, morphological and genetic divergence of sympatric North Atlantic killer whale populations. Molecular Ecology 18, 5207–5217.CrossRefGoogle ScholarPubMed
Ford, J.K.B., Ellis, G.M., Barrett-Lennard, L.G., Morton, A.B., Palm, R.S. and Balcomb, K.C. (1998) Dietary specialization in two sympatric populations of killer whales (Orcinus orca) in coastal British Columbia and adjacent waters. Canadian Journal of Zoology 76, 1456–1471.CrossRefGoogle Scholar
Ford, J.K.B., Ellis, G.M., Olesiuk, P.F. and Balcomb, K.C. (2010) Linking killer whale survival and prey abundance: food limitation in the oceans' apex predator? Biology Letters 6, 139–142.CrossRefGoogle ScholarPubMed
Ford, J.K.B., Ellis, G.M., Matkin, C.O., Wetklo, M.H., Barrett-Lennard, L.G. and Withler, R.E. (2011) Shark predation and tooth wear in a population of northeastern Pacific killer whales. Aquatic Biology 11, 213–224.CrossRefGoogle Scholar
Forney, K.A. and Wade, P.R. (2006) Worldwide distribution and abundance of killer whales. In Estes, J.A., Demaster, D.P., Doak, D.F., Williams, T.E. and Brownell, R.L. Jr. (eds) Whales, whaling, and ocean ecosystems. Berkeley, CA: University of California Press, pp. 145–162.Google Scholar
Gaebler, O.H., Vitti, T.G. and Vukmirovich, R. (1966) Isotope effects in metabolism of 14N and 15N from unlabeled dietary proteins. Canadian Journal of Biochemistry 44, 1249–1257.CrossRefGoogle ScholarPubMed
Germain, L.R., Koch, P.L., Harvey, J. and McCarthy, M.D. (2013) Nitrogen isotope fractionation in amino acids from harbor seals: implications for compound-specific trophic position calculations. Marine Ecology Progress Series 482, 265–277.CrossRefGoogle Scholar
Graham, B.S., Koch, P.L., Newsome, S.D., McMahon, K.W. and Aurioles, D. (2010) Using isoscapes to trace the movements and foraging behaviour of top predators in oceanic ecosystems. In West, J.B., Bowen, G.J., Dawson, T.E. and Tu, K.P. (eds) Isoscapes: understanding movement, pattern, and process on Earth through isotope mapping. Dordrecht, Heidelberg, London, New York: Springer, pp. 299–318.CrossRefGoogle Scholar
Hannides, C.C.S., Popp, B.N., Landry, M.R. and Graham, B.S. (2009) Quantification of zooplankton trophic position in the North Pacific subtropical gyre using stable nitrogen isotopes. Limnology and Oceanography 54, 50–61.CrossRefGoogle Scholar
Heide-Jørgensen, M.P. (1988) Occurrence and hunting of killer whales in Greenland. Rit Fiskideildar 11, 115–135.Google Scholar
Higdon, J.W. (2007) Status of knowledge on killer whales (Orcinus orca) in the Canadian Arctic. Fisheries and Oceans Canada. Canadian Science Advisory Secretariat Research Document 2007/048.Google Scholar
Higdon, J.W. and Ferguson, S.H. (2009) Sea ice declines causing punctuated change as observed with killer whale (Orcinus orca) sightings in the Hudson Bay region over the past century. Ecological Applications 19, 1365–1375CrossRefGoogle Scholar
Higdon, J.W., Hauser, D.D.W. and Ferguson, S.H. (2011) Killer whales (Orcinus orca) in the Canadian Arctic: distribution, prey items, group sizes, and seasonality. Marine Mammal Science 28, E93–E109.Google Scholar
Hobson, K.A. and Welch, H.E. (1992) Determination of trophic relationships with a high Arctic marine food web using δ13C and δ15N analysis. Marine Ecology Progress Series 84, 9–18.CrossRefGoogle Scholar
Hobson, K.A. and Sease, J.L. (1998) Stable isotope analyses of tooth annuli reveal temporal dietary records: an example using stellar sea lions. Marine Mammal Science 14, 116–129.CrossRefGoogle Scholar
Hobson, K.A., Fisk, A., Karnovsky, N., Holst, M., Gagnon, J.-M. and Fortier, M. (2002) A stable isotope (δ13C, δ15N) model for the North Water food web: implications for evaluating trophodynamics and the flow of energy and contaminants. Deep-Sea Research II 49, 5131–5150.CrossRefGoogle Scholar
Hothorn, T., Bretz, F. and Westfall, P. (2008) Simultaneous inference in general parametric models. Biometrical Journal 50, 346–363.CrossRefGoogle ScholarPubMed
Jefferson, T.A., Stacey, P.J. and Baird, R.W. (1991) A review of killer whale interactions with other marine mammals: predation to co-existence. Mammal Review 21, 151–180.CrossRefGoogle Scholar
Kuker, K. and Barrett-Lennard, L. (2010) A re-evaluation of the role of killer whales Orcinus orca in a population decline of sea otters Enhydra lutris in the Aleutian islands and review of alternative hypotheses. Mammal Review 40, 103–124.CrossRefGoogle Scholar
Laidre, K.L., Heide-Jorgensen, M.P. and Orr, J.R. (2006) Reactions of narwhals, Monodon monoceros, to killer whale, Orcinus orca, attacks in the eastern Canadian Arctic. Canadian Field Naturalist 120, 457–465.CrossRefGoogle Scholar
Lawson, J.W. and Hobson, K.A. (2000) Diet of harp seals (Pagophilus groenlandicus) in nearshore northeast Newfoundland: inferences from stable carbon (δ13C) and nitrogen (δ15N) isotope analyses. Marine Mammal Science 16, 578–591.CrossRefGoogle Scholar
Lawson, J.W. and Stevens, T.S. (2013) Historic and seasonal distribution patterns and abundance of killer whales (Orcinus orca) in the northwest Atlantic. Journal of the Marine Biological Association of the United Kingdom.Google Scholar
Lawson, J., Stevens, T. and Snow, D. (2008) Killer whales of Atlantic Canada, with particular reference to the Newfoundland and Labrador Region. Fisheries and Oceans Canada. Canadian Science Advisory Secretariat Research Document 2007/062.Google Scholar
Lien, J., Stenson, G.B. and Jones, P.W. (1988) Killer whales (Orcinus orca) in waters off Newfoundland and Labrador, 1978–1986. Rit Fiskideildar 11, 194–201.Google Scholar
Lorrain, A., Graham, B., Ménard, F., Popp, B., Bouillon, S., van Breuel, P. and Cherel, Y. (2009) Nitrogen and carbon isotope values of individual amino acids: a tool to study foraging ecology of penguins in the Southern Ocean. Marine Ecology Progress Series 391, 293–306.CrossRefGoogle Scholar
Martin, C., Bentaleb, I., Steelandt, S. and Guinet, C. (2011) Stable carbon and nitrogen isotope variations in canine dentine growth layers of Kerguelen southern elephant seals. Marine Ecology Progress Series 439, 295–305.CrossRefGoogle Scholar
Matthews, C.J.D., Luque, S.L., Petersen, S.D., Andrews, R.D. and Ferguson, S.H. (2011) Satellite tracking of a killer whale (Orcinus orca) in the eastern Canadian Arctic documents ice avoidance and rapid, long-distance movement into the North Atlantic. Polar Biology 34, 1091–1096.CrossRefGoogle Scholar
McCarthy, M.D., Benner, R., Lee, C. and Fogel, M.L. (2007) Amino acid nitrogen isotopic fractionation patterns as indicators of heterotrophy in plankton, particulate, and dissolved organic matter. Geochimica et Cosmochimica Acta 71, 4727–4744.CrossRefGoogle Scholar
McClelland, J.W. and Montoya, J.P. (2002) Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83, 2173–2180.CrossRefGoogle Scholar
McCutchan, J.H. Jr, Lewis, W.M. Jr, Kendall, C. and McGrath, C.C. (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102, 378–390.CrossRefGoogle Scholar
Mendes, S., Newton, J., Reid, R.J., Zuur, A.F. and Pierce, G.J. (2007a) Stable carbon and nitrogen isotope ratio profiling of sperm whale teeth reveals ontogenetic movements and trophic ecology. Oecologia 151, 605–615.CrossRefGoogle ScholarPubMed
Mendes, S., Newton, J., Reid, R.J., Frantzis, A. and Pierce, G.J. (2007b) Stable isotope profiles in sperm whale teeth: variations between areas and sexes. Journal of the Marine Biological Association of the United Kingdom 87, 621–627.CrossRefGoogle Scholar
Minagawa, 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
Mitchell, E. and Baker, A.N. (1980) Age of reputedly old killer whale, Orcinus orca, ‘Old Tom’ from Eden, Twofold Bay, Australia. Reports of the International Whaling Commission Special Issue 3, 143–154.Google Scholar
Montoya, J.P, Carpenter, E.J. and Capone, D.G. (2002) Nitrogen fixation and nitrogen isotope abundances in zooplankton of the oligotrophic North Atlantic. Limnology and Oceanography 47, 1617–1628.CrossRefGoogle Scholar
Morin, P.A., Archer, F.I., Foote, A.D., Vilstrup, J., Allen, E.E., Wade, P., Durban, J., Parsons, K., Pitman, R., Li, L., Bouffard, P., Nielsen, S.C.A., Rasmussen, M., Willerslev, E., Gilbert, M.T.P. and Harkins, T. (2010) Complete mitochondrial genome phylogeographic analysis of killer whales (Orcinus orca) indicates multiple species. Genome Research 20, 908–916.CrossRefGoogle ScholarPubMed
Myrick, A.C., Yochem, P.K. and Cornell, L.H. (1988) Toward calibrating dentinal layers in captive killer whales by use of tetracycline labels. Rit Fiskideildar 11, 285–296.Google Scholar
Naito, Y.I., Honch, N.V., Chikaraishi, Y., Ohkouchi, N. and Yoneda, M. (2010) Quantitative evaluation of marine protein contribution in ancient diets based on nitrogen isotope ratios of individual amino acids in bone collagen: an investigation at the Kitakogane Jomon site. American Journal of Physical Anthropology 143, 31–40.CrossRefGoogle ScholarPubMed
Newsome, S.D., Etnier, M.A., Monson, D.H. and Fogel, M.L. (2009) Retrospective characterization of ontogenetic shifts in killer whale diets via δ13C and δ15N analysis of teeth. Marine Ecology Progress Series 374, 229–242.CrossRefGoogle Scholar
O'Malley, J.M., Drazen, J.C., Popp, B.N., Gier, E. and Toonen, R.J. (2012) Spatial variability in growth and prey availability of lobsters in the northwestern Hawaiian Islands. Marine Ecology Progress Series 449, 211–220.CrossRefGoogle Scholar
Ostrom, P.H., Lien, J. and Macko, S.A. (1993) Evaluation of the diet of Sowerby's beaked whale, Mesoplodon bidens, based on isotopic comparisons among northwestern Atlantic cetaceans. Canadian Journal of Zoology 71, 858–861.CrossRefGoogle Scholar
Pauly, D., Trites, A.W., Capuli, E. and Christensen, V. (1998) Diet composition and trophic levels of marine mammals. ICES Journal of Marine Science 55, 467–481.CrossRefGoogle Scholar
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. and the R Development Core Team (2012) nlme: Linear and Nonlinear Mixed Effects Models. R package v.3.1-104.Google Scholar
Pitman, R.L. and Ensor, P. (2003) Three forms of killer whales (Orcinus orca) in Antarctic waters. Journal of Cetacean Research and Management 5, 131–139.CrossRefGoogle Scholar
Popp, B.N., Graham, B.S., Olson, R.J., Hannides, C.C.S., Lott, M.J., López-Ibarra, G.A., Galván-Magaña, F. and Fry, B. (2007) Insight into the trophic ecology of yellowfin tuna, Thunnus albacares, from compound-specific nitrogen isotope analysis of proteinaceous amino acids. In Dawson, T.E. and Siegwolf, R.T.W. (eds) Stable isotopes as indicators of ecological change. London: Academic Press, pp. 173–190.Google Scholar
Quay, P., Sonnerup, R., Westsby, T., Stutsman, J. and McNichol, A. (2003) Changes in the 13C/12C of dissolved inorganic carbon in the ocean as a tracer of anthropogenic CO2 uptake. Global Biogeochemical Cycles 17, 1004.CrossRefGoogle Scholar
R Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: http://www.R-project.org/ (accessed 7 October 2013).Google Scholar
Rau, G.H., Sweeney, R.E. and Kaplan, I.R. (1982) Plankton 13C:12C ratio changes with latitude: differences between northern and southern oceans. Deep-Sea Research 29, 1035–1039.CrossRefGoogle Scholar
Reeves, R.R. and Mitchell, E. (1988) Distribution and seasonality of killer whales in the eastern Canadian Arctic. Rit Fiskideildar 11, 136–160.Google Scholar
Reinhart, N.R., Ferguson, S.H., Koski, W.R., Higdon, J.W., LeBlanc, B., Tervo, O. and Jepson, P.D. (2013) Occurrence of killer whale Orcinus orca rake marks on Eastern Canada–West Greenland bowhead whales Balaena mysticetus. Polar Biology 36, 1133–1146.CrossRefGoogle Scholar
Riofrío-Lazo, M., Aurioles-Gamboa, D. and Le Boeuf, B.J. (2012) Ontogenetic changes in feeding habits of northern elephant seals revealed by δ15N and δ13C analysis of growth layers in teeth. Marine Ecology Progress Series 450, 229–241.CrossRefGoogle Scholar
Saulitis, E., Matkin, C., Barrett-Lennard, L., Heise, K. and Ellis, G. (2000) Foraging strategies of sympatric killer whale (Orcinus orca) populations in Prince William Sound, Alaska. Marine Mammal Science 16, 94–109.CrossRefGoogle Scholar
Seminoff, J.A., Benson, S.R., Arthur, K.E., Eguchi, T., Dutton, P.H., Tapilatu, R.F. and Popp, B.N. (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.CrossRefGoogle ScholarPubMed
Sergeant, D.E. and Fisher, H.D. (1957) The smaller cetacea of eastern Canadian waters. Journal of the Fisheries Research Board of Canada 14, 83–115.CrossRefGoogle Scholar
Styring, A.K., Sealy, J.C. and Evershed, R.P. (2010) Resolving the bulk δ15N values of ancient human and animal bone collagen via compound-specific nitrogen isotope analysis of constituent amino acids. Geochimica et Cosmochimica Acta 74, 241–251.CrossRefGoogle Scholar
Trueman, C.N., McGill, R.A.R. and Guyard, P.H. (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.CrossRefGoogle ScholarPubMed
Visser, I.N. (2000) Orca (Orcinus orca) in New Zealand waters. PhD dissertation. University of Auckland, New Zealand.CrossRefGoogle Scholar
Walker, J.L. and Macko, S.A. (1999) Dietary studies of marine mammals using stable carbon and nitrogen isotopic ratios of teeth. Marine Mammal Science 15, 314–334.CrossRefGoogle Scholar
Walker, J.L., Potter, C.W. and Macko, S.A. (1999) The diets of modern and historic bottlenose dolphin populations reflected through stable isotopes. Marine Mammal Science 15, 335–350.CrossRefGoogle Scholar
Waser, A.D., Harrison, W.G., Head, E.J., Nielsen, B., Lutz, V.A. and Calvert, S.E. (2000) Geographic variations in the nitrogen isotope composition of surface particulate nitrogen and new production across the North Atlantic Ocean. Deep-Sea Research I 47, 1207–1226.CrossRefGoogle Scholar
Whitehead, H. and Glass, C. (1985) Orcas (killer whales) attack humpback whales. Journal of Mammalogy 66, 183–185.CrossRefGoogle Scholar
Young, B.G., Higdon, J.W. and Ferguson, S.H. (2011) Killer whale (Orcinus orca) photo-identification in the eastern Canadian Arctic. Polar Research 30, 7203. doi: 10.3402/polar.v30i0.7203.CrossRefGoogle Scholar