Foraging ecology of ringed seals (Pusa hispida), beluga whales (Delphinapterus leucas) and narwhals (Monodon monoceros) in the Canadian High Arctic determined by stomach content and stable isotope analysis

References

• Aubail A., Dietz R., Rigét F., Simon-Bouhet B., Caurant F. An evaluation of teeth of ringed seals (Phoca hispida) from Greenland as a matrix to monitor spatial and temporal trends of mercury and stable isotopes. Science of the Total Environment. 2010; 408: 5137–5146.
   Web of Science ®Google Scholar
• Bluhm B.A., Gradinger R. Regional variability in food availability for Arctic marine mammals. Ecological Applications. 2008; 18: S77–S96.
   PubMed Web of Science ®Google Scholar
• Bradstreet M.S.W., Cross W.E. Trophic relationships at High Arctic ice edges. Arctic. 1982; 35: 1–12.
   Web of Science ®Google Scholar
• Bradstreet M.S.W., Finley K.J., Sekerak A.D., Griffiths W.B., Evans C.R., Fabijan M.F., Stallard H.E. Aspects of the biology of cod (Boreogadus saida) and its importance in Arctic marine food chains. Canadian Technical Report of Fisheries and Aquatic Sciences 1491. 1986; Winnipeg: Fisheries and Oceans, Canada.
   Google Scholar
• Caut S., Laran S., Garcia-Hartmann E., Das K. Stable isotopes of captive cetaceans (killer whales and bottlenose dolphins). The Journal of Experimental Biology. 2011; 214: 538–545.
   Web of Science ®Google Scholar
• Chouvelon T., Spitz J., Caurant F., Chappuis A., Laugier F., Le Goff E., Bustamante P. Revisiting the use of δ15N in meso-scale studies of marine food webs by considering spatio-temporal variations in stable isotopic signatures—the case of an open ecosystem: the Bay of Biscay (north-east Atlantic). Progress in Oceanography. 2012; 101: 95–102.
   Web of Science ®Google Scholar
• Christiansen J.S., Gamst Moen A-G., Hansen T.H., Nilssen K.T. Digestion of capelin, Mallotus villosus (Müller), herring, Clupea harengus L., and polar cod, Boreogadus saida (Lepechin), otoliths in a simulated seal stomach. ICES Journal of Marine Science. 2005; 62: 86–92.
   Web of Science ®Google Scholar
• Crawford R.E., Jorgenson J.K. Quantitative studies of cod (Boreogadus saida) schools: important energy stores in the Arctic food webs. Arctic. 1996; 49: 181–193.
   Web of Science ®Google Scholar
• Dalerum F., Angerbjörn A. Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia. 2005; 144: 647–658.
   PubMed Web of Science ®Google Scholar
• Dehn L.A., Sheffield G.G., Follmann E.H., Duffy L.K., Thomas D.L., O'Hara T.M. Feeding ecology of phocid seals and some walrus in the Alaskan and Canadian Arctic as determined by stomach contents and stable isotope analysis. Polar Biology. 2007; 30: 167–181.
   Web of Science ®Google Scholar
• Dennard S.T., McMeans B.C., Fisk A.T. Preliminary assessment of Greenland halibut diet in Cumberland Sound using stable isotopes. Polar Biology. 2009; 32: 941–945.
   Web of Science ®Google Scholar
• Finley K.J., Gibb E.J. Summer diet of the narwhal (Monodon monoceros) in Pond Inlet, northern Baffin Island. Canadian Journal of Zoology. 1982; 60: 3353–3363.
   Web of Science ®Google Scholar
• France R.L. Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Marine Ecology Progress Series. 1995; 124: 307–312.
   Web of Science ®Google Scholar
• Gardiner K., Dick T.A. Arctic cephalopod distributions and their associated predators. Polar Research. 2010; 29: 209–227.
   Web of Science ®Google Scholar
• Heide-Jørgensen M.P., Stewart B.S., Leatherwood S. Satellite tracking of ringed seals Phoca hispida off northwest Greenland. Ecography. 1992; 15: 56–61.
   Web of Science ®Google Scholar
• Heide-Jørgensen M.P., Teilmann J. Growth, reproduction, age structure and feeding habits of white whales (Delphinapterus leucas) in west Greenland waters. Bioscience. 1994; 39: 195–212.
   Google Scholar
• Hobson K.A., Ambrose W.G. Jr., Renaud P.E. Sources of primary production, benthic–pelagic coupling, and trophic relationships with the Northeast Water Polynya: insights from 13C and 15N analysis. Marine Ecology Progress Series. 1995; 128: 1–10.
   Web of Science ®Google Scholar
• Hobson K.A., Clark R.G. Assessing avian diets using stable isotopes II: factors influencing diet–tissues fractionation. Condor. 1992; 94: 189–197.
   Web of Science ®Google Scholar
• Hobson K.A., Schell D.M., Renouf D., Noseworthy E. 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. 1996; 53: 528–533.
   Web of Science ®Google Scholar
• Hobson K.A., Welch H.E. Determination of trophic relationships within a High Arctic marine food web using δ13C and δ15N analysis. Marine Ecology Progress Series. 1992; 84: 9–18.
   Web of Science ®Google Scholar
• Holst M., Stirling I., Hobson K.A. Diet of ringed seals (Phoca hispida) on the east and west sides of the North Water Polynya, northern Baffin Bay. Marine Mammal Science. 2001; 17: 888–908.
   Web of Science ®Google Scholar
• Hop H., Welch H.E., Crawford R.E. Reynolds J. Population structure and feeding ecology of cod (Boreogadus saida) schools in the Canadian High Arctic. Fish ecology in Arctic North America. 1997; Bethesda: American Fisheries Society. 68–80.
   Google Scholar
• Hunt J.J. Morphological characteristics of otoliths for selected fish in the northwest Atlantic. Journal of Northwest Atlantic Fishery Science. 1992; 13: 63–75.
   Google Scholar
• Hussey N.E., MacNeil M.A., McMeans B.C., Olin J.A., Dudley S.F.J., Cliff G., Wintner S.P., Fennessy S.T., Fisk A.T. Rescaling the trophic structure of marine food webs. Ecology Letters. 2013; 17: 239–50.
   Web of Science ®Google Scholar
• Hyslop E.J. Stomach contents analysis—a review of methods and their application. Journal of Fish Biology. 1980; 17: 411–429.
   Web of Science ®Google Scholar
• Innes S., Heide-Jørgensen M.P., Laake J.L., Laidre K.L., Cleator H.J., Richard P., Stewart R.E.A. Surveys of belugas and narwhals in the Canadian High Arctic in 1996. NAMMCO Scientific Publications. 1996; 4: 169–190.
   Google Scholar
• Labansen A.L., Lydersen C., Levermann N., Haug T., Kovacs K.M. Diet of ringed seals (Pusa hispida) from northeast Greenland. Polar Biology. 2011; 34: 227–234.
   Web of Science ®Google Scholar
• Laidre K., Heide-Jørgensen M.P. Winter feeding intensity of narwhals (Monodon monoceros). Marine Mammal Science. 2005; 21: 45–57.
   Web of Science ®Google Scholar
• Layman C.A., Araujo M.S., Boucek R., Hammerschlag-Peyer C.M., Harrison E., Jud Z.R., Matich P., Rosenblatt A.E., Vaudo J.J., Yeager L.A., Post D.M., Bearhop S. Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biological Reviews. 2012; 87: 545–562.
   PubMed Web of Science ®Google Scholar
• Loseto L., Stern G., Connelly T., Deibel D., Gemmill B., Prokopowicz A. Summer diet of beluga whales inferred by fatty acid analysis of the eastern Beaufort Sea food web. Journal of Experimental Marine Biology and Ecology. 2009; 374: 12–18.
   Web of Science ®Google Scholar
• Luque S.P., Ferguson S.H. Age structure, growth, mortality, and density of belugas (Delphinapterus leucas) in the Canadian Arctic: responses to environment?. Polar Biology. 2010; 33: 163–178.
   Web of Science ®Google Scholar
• Mansfield A.W., Smith T.G., Beck B. Narwhal, Monodon monoceros, in eastern Canadian waters. Journal of the Fisheries Research Board of Canada. 1975; 32: 1041–1046.
   Web of Science ®Google Scholar
• Marcin W.J. Diet of ringed seals (Phoca hispida) in a fjord of West Svalbard. Arctic. 1994; 47: 109–114.
   Web of Science ®Google Scholar
• Marcoux M., McMeans B.C., Fisk A.T., Ferguson S.H. Composition and temporal variation in the diet of beluga whales, derived from stable isotopes. Marine Ecology Progress Series. 2012; 47: 283–291.
   Web of Science ®Google Scholar
• Matley J.K., Fisk A.T., Dick T.A. Seabird predation on Arctic cod during summer in the Canadian Arctic. Marine Ecology Progress Series. 2012; 450: 219–228.
   Web of Science ®Google Scholar
• Matley J.K., Fisk A.T., Dick T.A. The foraging ecology of Arctic cod (Boreogadus saida) during open water (July–August) in Allen Bay, Arctic Canada. Marine Biology. 2013; 160: 2993–3004.
   Web of Science ®Google Scholar
• McLaren I.A. Growth in pinnipeds. Biological Reviews of the Cambridge Philosophical Society. 1993; 68: 1–79.
   PubMed Web of Science ®Google Scholar
• McMeans B.C., Olin J.A., Benz G.W. Stable-isotope comparisons between embryos and mothers of a placentatrophic shark species. Journal of Fish Biology. 2009; 75: 2464–2474.
   PubMed Web of Science ®Google Scholar
• Moore J.W., Semmens B.X. Incorporating uncertainty and prior information in stable isotope mixing models. Ecological Letters. 2008; 11: 470–480.
   PubMed Web of Science ®Google Scholar
• Montoya J.P. Michener R., Lajtha K. Natural abundance of ¹⁵N in marine planktonic ecosystems, Stable isotopes in ecology and environmental science. 2007; 2nd edn, Malden, MA: Blackwell. 176–201.
   Google Scholar
• Newsome S.D., Clementz M.T., Koch P.L. Using stable isotope biogeochemistry to study marine mammal ecology. Marine Mammal Science. 2010; 26: 509–572.
   Web of Science ®Google Scholar
• Parnell A.C., Inger R., Bearhop S., Jackson A.L. Source partitioning using stable isotopes: coping with too much variation. PLoS One. 2010; 5: e9672.
   PubMed Web of Science ®Google Scholar
• Pierce G.J., Boyle P.R. A review of methods for diet analysis in piscivorous marine mammals. Oceanography and Marine Biology: Annual Review. 1991; 29: 409–486.
   Web of Science ®Google Scholar
• Pomerleau C., Lesage V., Ferguson S.H., Winkler G., Petersen S.D., Higdon J.W. Prey assemblage isotopic variability as a tool for assessing diet and the spatial distribution of bowhead whale Balaena mysticetus foraging in the Canadian eastern Arctic. Marine Ecology Progress Series. 2012; 469: 161–174.
   Web of Science ®Google Scholar
• Post D.M. Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology. 2002; 83: 703–718.
   Web of Science ®Google Scholar
• R Core Team. R: a language and environment for statistical computing. 2013; Vienna, Austria: R Foundation for Statistical Computing.
   Google Scholar
• Richard P.R., Heide-Jørgensen M.P., Orr J.R., Dietz R., Smith T.G. Summer and autumn movements and habitat use by belugas in the Canadian High Arctic and adjacent areas. Arctic. 2001; 54: 207–222.
   Web of Science ®Google Scholar
• Ruiz-Cooley R.I., Engelhaupt D.T., Ortega-Ortiz J.G. Contrasting C and N isotope ratios from sperm whale skin and squid between the Gulf of Mexico and Gulf of California: effect of habitat. Marine Biology. 2012; 159: 151–164.
   Web of Science ®Google Scholar
• Shaw C.N., Wilson P.J., White B.N. A reliable method of gender determination for mammals. Journal of Mammalogy. 2003; 84: 123–128.
   Web of Science ®Google Scholar
• Sheffield G., Fay F.H., Feder H., Kelly B.P. Laboratory digestion of prey and interpretation of walrus stomach contents. Marine Mammal Science. 2001; 17: 310–330.
   Web of Science ®Google Scholar
• Stewart B.E. A technical report on methods for tooth preparation and age estimates of beluga (Delphinapterus leucas). Canadian Technical Report of Fisheries and Aquatic Sciences 3020. 2012; Winnipeg: Fisheries and Oceans Canada.
   Google Scholar
• Stewart R.E.A. Size-at-age relationships as discriminators of white whale (Delphinapterus leucas) stocks in the eastern Canadian Arctic. Bioscience. 1994; 39: 217–225.
   Google Scholar
• Stewart R.E.A., Campana S.E., Jones C.M., Stewart B.E. Bomb radiocarbon dating calibrates beluga (Delphinapterus leucas) age estimates. Canadian Journal of Zoology. 2006; 84: 1840–1852.
   Web of Science ®Google Scholar
• Stewart R.E.A., Stewart B.E., Stirling I., Street E. Counts of growth layer groups in cementum and dentine in ringed seals (Phoca hispida). Marine Mammal Science. 1996; 12: 383–401.
   Web of Science ®Google Scholar
• Teilmann J., Born E.W., Acquarone M. Behaviour of ringed seals tagged with satellite transmitters in the North Water polynya during fast-ice formation. Canadian Journal of Zoology. 1999; 77: 1934–1946.
   Google Scholar
• Tieszen L.L., Boutton T.W., Tesdahl K.G., Slade N.A. Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia. 1983; 57: 32–37.
   PubMed Web of Science ®Google Scholar
• Vander Zanden M.J., Rasmussen J.B. Primary consumer δ13C and δ15N and the trophic position of aquatic consumers. Ecology. 1999; 80: 1395–1404.
   Web of Science ®Google Scholar
• Vander Zanden M.J., Rasmussen J.B. Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography. 2001; 48: 2061–2066.
   Google Scholar
• Venables W.N., Dichmont C.M. GLMs, GAMs and GLMMs: an overview of theory for applications in fisheries research. Fisheries Research. 2004; 70: 319–337.
   Web of Science ®Google Scholar
• Watt C.A., Ferguson S.H. Fatty acids and stable isotopes (δ13C and δ15N) reveal temporal changes in narwhal (Monodon monoceros) diet linked to migration patterns. Marine Mammal Science. 2015; 31: 21–44.
   Web of Science ®Google Scholar
• Welch H.E., Bergmann M.A., Siferd T.D., Martin K.A., Curtis M.F., Crawford R.E., Canover R.J., Hop H. Energy flow through the marine ecosystem of the Lancaster Sound region, Arctic Canada. Arctic. 1992; 45: 343–357.
   Web of Science ®Google Scholar
• Welch H.E., Crawford R.E., Hop H. Occurrence of cod (Boreogadus saida) schools and their vulnerability to predation in the Canadian High Arctic. Arctic. 1993; 46: 331–339.
   Web of Science ®Google Scholar
• Wood S.N. Modelling and smoothing parameter estimation with multiple quadratic penalties. Journal of the Royal Statistical Society Series B. 2000; 62: 413–428.
   Google Scholar