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

Volumn 469, Issue , 2012, Pages 161-174

  Pomerleau, C ^a,f   Lesage, V ^b   Ferguson, S H ^c   Winkler, G ^a   Petersen, S D ^d   Higdon, J W ^e  

^a INSTITUT DES SCIENCES DE LA MER DE RIMOUSKI   (Canada)

^b MAURICE LAMONTAGNE INSTITUTE   (Canada)

^c FRESHWATER INSTITUTE   (Canada)

^d Assiniboine Park Zoo   (Canada)

^e Higdon Wildlife Consulting   (Canada)

^f INSTITUTE OF OCEAN SCIENCES   (Canada)

Author keywords

Bayesian mixing model; Bowhead whale; Canadian Arctic; Diet; Foraging behaviour; Marine mammal; SIAR; Stable isotopes; Trophic ecology; Zooplankton

Indexed keywords

AGE CLASS; ANNUAL VARIATION; BAYESIAN ANALYSIS; CARBON ISOTOPE; CLIMATE CHANGE; CRUSTACEAN; DIET; ENDEMIC SPECIES; FEEDING GROUND; FISHING; ISOTOPIC COMPOSITION; LATITUDINAL GRADIENT; NITROGEN ISOTOPE; PREY AVAILABILITY; SEA ICE; SPATIAL DISTRIBUTION; TROPHIC INTERACTION; VULNERABILITY; WARMING; WHALE; ZOOPLANKTON;

ARCTIC; CANADA; CANADIAN ARCTIC; DAVIS STRAIT; DISKO BAY; GREENLAND;

BALAENA MYSTICETUS; BALAENIDAE; CALANOIDA; CALANUS HYPERBOREUS; COPEPODA; EUPHAUSIACEA; EUPHAUSIIDAE; MAMMALIA; METRIDIA LONGA; MYSIDA; PARAEUCHAETA;

EID: 84870179304     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps10004     Document Type: Article

References (99)

1. ACIA (Arctic Climate Impact Assessment) (2004) Impacts of a warming Arctic. Cambridge University Press, New York, NY
2. Aurioles-Gamboa D, Newsome SD, Salazar-Pico S, Koch PL (2009) Stable isotope difference betwen sea lions (Zalophus) from the Gulf of California and Galapagos Islands. J Mammal 90: 1410-1420
3. Bearhop S, Adam CE, Waldron S, Fuller RA, MacLeod H (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 73: 1007-1012 (Pubitemid 39123240)
4. Beaugrand G (2009) Decadal changes in climate ecosystems in the North Atlantic Ocean and adjacent seas. Deep-Sea Res II 56: 656-673
5. Beaugrand G, Reid PC, Ibañez F, Lindley JA, Edwards M (2002) Reorganization of North Atlantic marine copepod biodiversity and climate. Science 296: 1692-1694 (Pubitemid 34579168)
6. Bolnick DI, Svanback R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161: 1-28 (Pubitemid 36144810)
7. Bonin W, Vladykov VD (1940) Étude sur les mammifères aquatiques. La peau du marsouin blanc ou beluga. Nat Can 67: 253-287
8. Brown MW, Kraus SD, Gaskin DE (1991) Reaction of North Atlantic right whales (Eubalaena glacialis) to skin biopsy sampling for genetic and pollutant analysis. Rep Int Whal Comm Spec Issue 13: 81-89
9. Budge SM, Springer AM, Iverson SJ, Sheffield G, Rosa C (2008) Blubber fatty acid composition of bowhead whales, Balaena mysticetus: implications for diet assessment and ecosystem monitoring. J Exp Mar Biol Ecol 359: 40-46
10. Calinski T, Harabasz J (1974) A dendrite method for cluster analysis. Commun Stat 3: 1-27
11. 13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46: 443-453
12. Caut S, Laran S, Garcia-Hartmann E, Das K (2011) Stable isotopes of captive cetaceans (killer whales and bottlenose dolphins). J Exp Biol 214: 538-545
13. Comeau S, Gattuso JP, Nisumaa AM, Orr J (2011) Impact of aragonite saturation state changes on migratory ptero - pods. Proc R Soc Lond B Biol Sci 279: 732-738
14. Cosens SE, Blouw A (2003) Size and age class segregation of bowhead whales summering in northern Foxe Basin: a photogrammetric analysis. Mar Mamm Sci 19: 284-296 (Pubitemid 36333427)
15. Cosens SE, Innes S (2000) Distribution and numbers of bowhead whales (Balaena mysticetus) in northwestern Hudson Bay in August 1995. Arctic 53: 36-41 (Pubitemid 30244476)
16. Cosens SE, Qamukaq T, Parker B, Dueck LP, Anardjuak B (1997) The distribution and numbers of bowhead whales, Balaena mysticetus, in northern Foxe Basin in 1994. Can Field Nat 111: 381-388
17. Cubbage JC, Calambokidis J (1987) Size-class segregation of bowhead whales discerned through aerial stereophotogrammetry. Mar Mamm Sci 3: 179-185 (Pubitemid 17274930)
18. Dalerum F, Angerbjörn A (2005) Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144: 647-658 (Pubitemid 41218815)
19. Drago M, Cardona L, Crespo EA, Aguilar A (2009) Ontogenic dietary changes in South American sea lions. J Zool (Lond) 279: 251-261
20. Duda RO, Hart PE (1973) Pattern classification and scene analysis. John Wiley & Sons, New York, NY
21. Dueck L, Ferguson SH (2009) Habitat use by bowhead whales (Balaena mysticetus) of the eastern Canadian Arctic. Canadian Science Advisory Secretariat Research Document, 2008/082, Fisheries and Oceans Canada, Winnipeg
22. Dyke AS, Hooper J, Savelle JM (1996) A history of sea ice in the Canadian Arctic Archipelago based on postglacial remains of the bowhead whale (Balaena mysticetus). Arctic 49: 235-255
23. Estes JA, Riedman ML, Staedler MM, Tinker MT, Lyon BT (2003) Individual variation in prey selection by sea otters: patterns, causes and implications. J Anim Ecol 72: 144-155 (Pubitemid 36251181)
24. Falk-Petersen S, Timofeev S, Pavlov V, Sargent JR (eds) (2007) Climate variability and the effect on Arctic food chains. The role of Calanus. Springer-Verlag, Berlin
25. Ferguson SH, Dueck L, Loseto LL, Luque SP (2010a) Bowhead whale Balaena mysticetus seasonal selection of sea ice. Mar Ecol Prog Ser 411: 285-297
26. Ferguson SH, Higdon JW, Chmelnitsky EG (2010b) The rise of killer whales as a major Arctic predator. In: Ferguson SH, Loseto LL, Mallory ML (eds) A little less Arctic: top predators in the world's largest northern inland sea, Hudson Bay. Springer, New York, NY, p 117-136
27. Fetzer I, Hirche HJ, Kolosova EG (2002) The influence of freshwater discharge on the distribution of zooplankton in the southern Kara Sea. Polar Biol 25: 404-415 (Pubitemid 36058863)
28. Finley KJ (2001) Natural history and conservation of the Greenland whale, or bowhead, in the northwest Atlantic. Arctic 54: 55-76 (Pubitemid 32442561)
29. Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226: 497-509
30. George JC, Zeh J, Suydam R, Clark C (2004) Abundance and population trend (1978-2001) of western Arctic bowhead whales surveyed near Barrow, Alaska. Mar Mamm Sci 20: 755-773 (Pubitemid 39384945)
31. Gosselin M, Levasseur M, Wheeler PA, Horner RA, Booth BC (1997) New measurements of phytoplankton and ice algal production in the Arctic Ocean. Deep-Sea Res II 44: 1623-1644 (Pubitemid 28159080)
32. Greene CH, Pershing AJ (2007) Climate drives sea change. Science 315: 1084-1085 (Pubitemid 46328009)
33. Hagen W, Auel H (2001) Seasonal adaptations and the role of lipids in oceanic zooplankton. Zoology 104: 313-326
34. Hair JF, Tatham RL, Anderson RE, Black W (1995) Multivariate data analysis, 5th edn. Prentice-Hall, Upper Saddle River, NJ
35. Haldiman JT, Henk WG, Henry RW, Albert TF, Abdelbaki YZ, Duffield DW (1985) Epidermal and papillary dermal characteristics of the bowhead whale (Balaena mysticetus). Anat Rec 211: 391-402 (Pubitemid 15081132)
36. Heide-Jørgensen MP, Laidre KL, Wiig Ø, Jensen MV, and others (2003) From Greenland to Canada in ten days: tracks of bowhead whales, Balaena mysticetus, across Baffin Bay. Arctic 56: 21-31 (Pubitemid 36646967)
37. Heide-Jørgensen MP, Laidre KL, Jensen MV, Dueck L, Postma LD (2006) Dissolving stock discreteness with satellite tracking: bowhead whales in Baffin Bay. Mar Mamm Sci 22: 34-45 (Pubitemid 43201808)
38. Heide-Jørgensen MP, Laidre KL, Wiig Ø, Postma L, Dueck L, Bachman L (2010) Large-scale sexual segregation of bowhead whales. Endang Species Res 13: 73-78
39. Hicks BD, St Aubin DJ, Geraci JR, Brown WR (1985) Epidermal growth in the bottlenose dolphin, Tursiops truncatus. J Invest Dermatol 85: 60-63 (Pubitemid 15069716)
40. Higdon JW, Ferguson SH (2010) Past, present, and future for bowhead whales (Balaena mysticetus) in northwest Hudson Bay. In: Ferguson SH, Loseto LL, ML Mallory (eds) A little less Arctic: top predators in the world's largest northern inland sea, Hudson Bay. Springer, New York, NY, p 159-177
41. Hobson KA (1993) Trophic relationships among high Arctic seabirds: insights from tissue-dependant stable isotope models. Mar Ecol Prog Ser 95: 7-18 (Pubitemid 24411913)
42. Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120: 314-326 (Pubitemid 29429051)
43. Hobson KA, Sease JL (1998) Stable isotope analyses of tooth annuli reveal temporal dietary records: an example using stellar sea lions. Mar Mamm Sci 14: 116-129 (Pubitemid 28051994)
44. Hobson KA, Schell DM, Renouf D, Noseworthy E (1996) Stable carbon and nitrogen fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals. Can J Fish Aquat Sci 53: 528-533 (Pubitemid 26310269)
45. Hobson KA, Fisk A, Karnovsky N, Holst M, Gagnon JM, Fortier M (2002) A stable isotope model for the North Water food web: implications for evaluating trophodynamics and the flow of energy and contaminants. Deep- Sea Res II 49: 5131-5150 (Pubitemid 35241036)
46. ICES (International Council for the Exploration of the Sea) (2008) An assessment of the changes in the distribution and abundance of marine species in the OSPAR maritime area in relation to changes in hydrodynamics and sea temperature. ICES Advice 2008, Book 1, section 1.5.5.1. ICES, Copenhagen
47. Jackson AC, Rundle SD, Attrill MJ, Cotton PA (2004) Ontogenic changes in metabolism may determine diet shifts for a sit-and-wait predator. J Anim Ecol 73: 536-545
48. Jones FM, Pfeiffer CJ (1994) Morphometric comparison of the epidermis in several cetacean species. Aquat Mamm 20: 29-34
49. Kattner G, Hagen W (2009) Lipids in marine copepods: latitudinal characteristics and perspective to global warming. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, Dordrecht, p 257-280
50. Knoff A, Hohn A, Macko SA (2008) Ontogenetic diet changes in bottlenose dolphins (Tursiops truncatus) reflected through stable isotopes. Mar Mamm Sci 24: 128-137 (Pubitemid 351239279)
51. Koski WR, Davis RA, Miller GW, Withrow DE (1993) Reproduction. In: JJ Burns, JJ Montague, CJ Cowles (eds) The bowhead whale. Society for Marine Mammalogy, Spec Publ No. 2, Allen Press, Lawrence, KS, p 239-274
52. Koski WR, Heide-Jørgensen MP, Laidre KL (2006) Winter abundance of bowhead whales, Balaena mysticetus, in the Hudson Strait, March 1981. J Cetacean Res Manag 8: 139-144
53. Laidre K, Heide-Jørgensen MP, Nielsen TG (2007) Role of the bowhead whale as a predator in West Greenland. Mar Ecol Prog Ser 346: 285-297 (Pubitemid 350043225)
54. Laidre KL, Stirling I, Lowry LF, Wiig Ø, Heide-Jørgensen MP, Ferguson SH (2008) Quantifying the sensitivity of Arctic marine mammals to climate-induced habitat change. Ecol Appl 18: S97-S125
55. 15N) isotope analyses. Mar Mamm Sci 16: 578-591 (Pubitemid 30438042)
56. Lee SH, Schell DM, McDonald TL, Richardson WJ (2005) Regional and seasonal feeding by bowhead whales Balaena mysticetus as indicated by stable isotope ratios. Mar Ecol Prog Ser 285: 271-287 (Pubitemid 40263264)
57. Lowry LF, Sheffield G, George JC (2004) Bowhead whale feeding in the Alaskan Beaufort Sea, based on stomach contents analyses. J Cetacean Res Manag 6: 215-223
58. MacLeod CD (2009) Global climate change, range changes and potential implications for the conservation of marine cetaceans: a review and synthesis. Endang Species Res 7: 125-136
59. MacLeod CD, Santos MB, López A, Pierce GJ (2006) Relative prey size consumption in toothed whales: implications for prey selection and level of specialization. Mar Ecol Prog Ser 326: 295-307 (Pubitemid 46026144)
60. 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 (Pubitemid 46440149)
61. Michaud R (2005) Sociality and ecology of the odontocetes. In: Ruckstuhl KE, Neuhaus P (eds) Sexual segregation in vertebrates: ecology of the two sexes. Cambridge University Press, Cambridge, p 303-326
62. 13C): sample treatment effects and model bias. J Fish Biol 72: 815-830 (Pubitemid 351300951)
63. Møller P (2006) Lipids and stable isotopes in marine food webs in West Greenland. Trophic relations and health implications. PhD thesis, Technical University of Denmark, Kongens Lyngby
64. 15N in marine planktonic ecosystems. In: Michener R, Lajtha K (eds) Stable isotope in ecology and environmental science. Blackwell Publishing, Oxford, p 176-201
65. Moore SE, Reeves RR (1993) Distribution and movement. In: Burns JJ, Montague JJ, Cowles CJ (eds) The bowhead whale. Society for Marine Mammalogy Spec Publ No. 2, Allen Press, Lawrence, KS, p 313-386
66. Moore JW, Semmens BX (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecol Lett 11: 470-480 (Pubitemid 351499224)
67. Neibauer HJ, Schell DM (1993) Physical environment of the Bering Sea population. In: Burns JJ, Montague JJ, Cowles CJ (eds) The bowhead whale. Society for Marine Mammalogy Spec Publ No. 2, Allen Press, Lawrence, KS, p 23-44
68. 15N analysis of teeth. Mar Ecol Prog Ser 374: 229-242
69. Newsome SD, Clementz MT, Koch PL (2010) Using stable isotope biogeochemistry to study marine mammal ecology. Mar Mamm Sci 26: 509-572
70. NWMB (Nunavut Wildlife Management Board) (2000) Final report of the Inuit bowhead knowledge study, Nunavut, Canada. NWMB, Iqaluit
71. Orr AJ, Newsome SD, Laake JL, VanBlaricom GR, DeLong RL (2011) Ontogenetic dietary information of the Cali - fornia sea lion (Zalophus californianus) assessed using stable isotope analysis. Mar Mamm Sci 28: 714-732
72. Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with variation. PLoS ONE 5: e9672
73. Perovich DK, Richter-Menge JA (2009) Loss of ice in the Arctic. Ann Rev Mar Sci 1: 417-441
74. Peters RH (1983) The ecological implications of body size. Cambridge University Press, Cambridge
75. Petersen SD, Tenkula D, Ferguson SH (2011) Population genetic structure of narwhal (Monodon monoceros). DFO Can Sci Advis Sec Res Doc 2011/021. Fisheries and Oceans Canada, Ottawa
76. Peterson AT (2006) Uses and requirements of ecological niche models and related distributional models. Biodiversity Informatics 3: 59-72
77. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Ann Rev Ecol Syst 18: 293-320
78. Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136: 261-269 (Pubitemid 36933259)
79. Pomerleau C, Patterson TA, Luque S, Lesage V, Heide-Jørgensen MP, Dueck LL, Ferguson SH (2011a) Bowhead whale Balaena mysticetus diving and movement patterns in the eastern Canadian Arctic: implications for foraging ecology. Endang Species Res 15: 167-177
80. Pomerleau C, Ferguson SH, Walkutz W (2011b) Stomach contents of bowhead whales (Balaena mysticetus) from four locations in the Canadian Arctic. Polar Biol 34: 615-620
81. 15N) isotope ratios. J Plankton Res 33: 1779-1792
82. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83: 703-718 (Pubitemid 36524158)
83. Postma LD, Dueck LL, Heide-Jørgensen MP, Cosens SE (2006) Molecular genetic support of a single population of bowhead whales (Balaena mysticetus) in western Canadian Arctic and western Greenland waters. DFO Can Sci Advis Sec Res Doc 2006/051. Fisheries and Oceans Canada, Ottawa
84. R Development Core Team (2010) R: a language and en - vironment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at www.Rproject.org
85. Reeves RR, Heide-Jørgenson MP (1996) Recent status of bowhead whales, Balaena mysticetus, in the wintering grounds off West Greenland. Polar Res 15: 115-125
86. Reeves RR, Mansfield A, McLaughlin M (1983) Distribution and migration of the bowhead whale (Balaena mysticetus) in the eastern North American Arctic. Arctic 36: 5-64
87. Roughgarden J (1972) Evolution of niche width. Am Nat 106: 683-718
88. Ruckstuhl KE, Neuhaus P (2005) Sexual segregation in vertebrates: ecology of the two sexes. Cambridge University Press, Cambridge
89. Rugh D, DeMaster D, Rooney A, Breiwick J, Shelden K, Moore S (2003) A review of bowhead whale (Balaena mysticetus) stock identity. J Cetacean Res Manag 5: 267-279
90. Ruiz-Cooley RI, Gendron D, Aguiñiga S, Mesnick S, Carriquiry JD (2004) Trophic relationships between sperm whales and jumbo squid using stable isotopes of C and N. Mar Ecol Prog Ser 277: 275-283 (Pubitemid 39225198)
91. Runge JA, Ingram RG (1991) Under-ice feeding and diel migration by the planktonic copepods Calanus glacialis and Pseudocalanus minutus in relation to the ice algal production cycle in southeastern Hudson Bay, Canada. Mar Biol 108: 217-225
92. Sarle W (1983) Cubic clustering criterion. SAS Technical report A-108. SAS Institute, Cary, NC
93. Shaw CN, Wilson PJ, White BN (2003) A reliable molecular method of gender determination for mammals. J Mammal 84: 123-128 (Pubitemid 36280756)
94. St. Aubin DJ, Smith TG, Geraci JR (1990) Seasonal epidermal moult in beluga whales, Delphinapterus leucas. Can J Zool 68: 359-367
95. 13C analysis of diet. Oecologia 57: 32-37 (Pubitemid 15275016)
96. 13C) determination. J Northwest Atl Fish Sci 22: 71-76 (Pubitemid 28424446)
97. Werner EE, Hall DJ (1988) Ontogenetic habitat shifts in bluegill: the foraging-rate predation risk trade-off. Ecology 69: 1352-1366 (Pubitemid 19323788)
98. Wiig Ø, Heide-Jørgensen MP, Lindqvist C, Laidre KL and others (2011) Recaptures of genotyped bowhead whales Balaena mysticetus in eastern Canada and West Greenland. Endang Species Res 14: 235-242
99. Witteveen BH, Worthy GAJ, Wynne KM, Roth JD (2009) Population structure of North Pacific humpback whales on their feeding grounds revealed by stable carbon and nitrogen isotope ratios. Mar Ecol Prog Ser 379: 299-310