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Proportion of higher trophic-level prey in the diet of Pacific walruses (Odobenus rosmarus divergens)

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Abstract

During nutritionally stressful situations, Pacific walruses (Odobenus rosmarus divergens) may switch from preying on benthic invertebrates to higher trophic-level prey (HTLP) (e.g., pinnipeds and/or seabirds). We applied a Bayesian mixing model to stable isotope (C and N) data from analyses of various tissues (tongue and lumbar muscle, skin, and liver) to quantify the proportional contribution of HTLP to walruses (n = 293 individuals). The mode contribution of HTLP to walrus diet was ~22 % (±10 %) based on muscle mixing models, which is consistent with results from contaminant studies of Atlantic walruses (Odobenus rosmarus rosmarus), but higher than estimates based on historical stomach content analyses of Pacific walruses. A broader range in the proportion of HTLP (0–60 %) shown by mixing models using stable isotope data from liver and skin of walruses indicated they pursue an opportunistic foraging strategy. Data from the HTLP-consuming walruses were comparable with our stable isotope data of a known “seal-eating” walrus. No significant difference was evident between the estimated contributions of HTLP to the diet of male versus female walruses (P > 0.01). This finding suggests that changes in diet base for walruses are not influenced by the sex of the predator.

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References

  • Barboza PS, Parker KL, Hume ID (2009) Integrative wildlife nutrition. Springer, Berlin

    Book  Google Scholar 

  • Beaulieu M, Dervaux A, Thierry AM, Lazin D, Le Maho Y, Ropert-Coudert Y, Spée M, Raclot T, Ancel A (2009) When sea-ice clock is ahead of Adélie penguins’ clock. Funct Ecol 24:93–102

    Article  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37(8):911–917

    Article  CAS  PubMed  Google Scholar 

  • Bond AL, Diamond AW (2011) Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecol Appl 21:1017–1023

    Google Scholar 

  • Born EW, Rysgaard S, Ehlmé G, Sejr M, Acquarone M, Levermann N (2003) Underwater observations of foraging free-living Atlantic walruses (Odobenus rosmarus rosmarus) and estimates of their food consumption. Polar Biol 26:348–357

    Google Scholar 

  • Bowen WD, Oftedal OT, Boness DJ (1992) Mass and energy transfer during lactation in a small phocid, the harbor seal (Phoca vitulina). Physiol Zool 65(4):844–866

    Google Scholar 

  • Bowen WD, Beck CA, Iverson SJ, Austin D, McMillan JI (2006) Top predators in marine ecosystems. Cambridge University Press, Cambridge

    Google Scholar 

  • Burek KA, Gulland FMD, O’Hara TM (2008) Effects of climate change on Arctic marine mammal health. Ecol Appl 18:S126–S134

    Article  PubMed  Google Scholar 

  • Burns JJ (1970) Remarks on the distribution and natural history of pagophilic pinnipeds in the Bering and Chukchi Seas. J Mammal 51(3):445–454

    Article  Google Scholar 

  • Burns JM, Trumble SJ, Castellini MA, Testa JW (1998) The diet of Weddell seals in McMurdo Sound, Antarctica as determined from scat collections and stable isotope analysis. Polar Biol 19:272–282

    Google Scholar 

  • Crawford K, MacDonald RA, Bearhop S (2008) Applications of stable isotope techniques to the ecology of mammals. Mamm Rev 38(1):87–107

    Article  Google Scholar 

  • Dehn L-A, Sheffield G, Follman EH, Duffy LK, Thomas DL, O’Hara TM (2007) Feeding ecology of phocid seals and some walrus in the Alaskan and Canadian Arctic as determined by stomach contents and stable isotope analysis. Polar Biol 30(2):167–181

    Article  Google Scholar 

  • Deniro MJ, Epstein S (1977) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506

    Article  Google Scholar 

  • Fay FH (1960) Carnivorous walruses and some arctic zoonoses. Arctic 13:111–122

    Article  Google Scholar 

  • Fay FH (1982) Ecology and biology of the Pacific walrus, Odobenus rosmarus divergens Illiger. N Am Fauna 74:1–279

    Article  Google Scholar 

  • Fay FH, Feder H, Stoker SW (1977) An estimation of the impact of the Pacific walrus population on its food resources in the Bering Sea. U.S. Marine Mammal Commission, MMC-75/06, Washington, DC

  • Fay FH, Sease JL, Merrick RL (1990) Predation on a ringed seal, Phoca hispida, and a black guillemot, Cepphus grylle, by a Pacific walrus, Odobenus rosmarus divergens. Mar Mamm Sci 6(3):348–350

    Article  Google Scholar 

  • Feder HM, Iken K, Blanchard AL, Jewett SC, Schonberg S (2011) Benthic food web structure in the southeastern Chukchi Sea: an assessment using δ13C and δ15N analyses. Polar Biol 34(4):521–532

    Article  Google Scholar 

  • Fischbach AS, Amstrup SC, Douglas DC (2007) Landward and eastward shift of Alaskan polar bear denning associated with recent sea ice changes. Polar Biol 30(11):1395–1405

    Article  Google Scholar 

  • Fox AD, Fox GF, Liaklev A, Gerhardsson N (2010) Predation of flightless pink-footed geese (Anser brachyrhynchus) by Atlantic walruses (Odobenus rosmarus rosmarus) in southern Edgeøya, Svalbard. Polar Res 29:455–457

    Article  Google Scholar 

  • Garlich-Miller J, Quakenbush LT, Bromaghin JF (2006) Trends in age structure and productivity of Pacific walruses harvested in the Bering Strait region of Alaska, 1952–2002. Mar Mamm Sci 22(4):880–896

    Article  Google Scholar 

  • Garlich-Miller J, MacCracken JG, Snyder J, Meehan R, Myers M, Wilder JM, Lance E, Matz A (2011) Status review of the Pacific walrus (Odobenus rosmarus divergens) report. U.S. Fish and Wildlife Service Report, pp 2–52

  • Grebmeier JM (2012) Shifting patterns of life in the Pacific Arctic and Sub-Arctic seas. Annu Rev Mar Sci 4:63–78

    Article  Google Scholar 

  • Grebmeier JM, Overland JE, Moore SE, Farley EV, Carmack EC, Cooper LW, Frey KE, Helle JH, McLaughlin FA, McNutt SL (2006) A major ecosystem shift in the northern Bering Sea. Science 311(5766):1461–1464

    Article  CAS  PubMed  Google Scholar 

  • Gruber N, Keeling CD, Bacastow RB, Guenther PR, Lueker TJ, Wahlen M, Meijer HA, Mook WG, Stocker TF (1999) Spatiotemporal patterns of carbon-13 in the global surface oceans and the oceanic Suess effect. Glob Biogeochem Cycles 13(2):307–335

    Article  CAS  Google Scholar 

  • Hilton GM, Thompson DR, Sagar PM, Cuthbert RJ, Cherel Y, Bury SJ (2006) A stable isotopic investigation into the causes of decline in a sub-Antarctic predator, the rockhopper penguin Eudyptes chrysocome. Glob Change Biol 12(4):611–625

    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 

  • Hoekstra PF, Dehn LA, George JC, Solomon KR, Muir DC, O’Hara TM (2002) Trophic ecology of bowhead whales (Balaena mysticetus) compared with that of other arctic marine biota as interpreted from carbon-, nitrogen-, and sulfur-isotope signatures. Can J Zool 80:223–231

    Article  Google Scholar 

  • Hondolero D, Bluhm BA, Iken K (2012) Caloric content of dominant benthic species from the northern Bering and Chukchi Seas: historical comparisons and the effects of preservation. Polar Biol 35(4):637–644

    Article  Google Scholar 

  • Iman RL, Conover WJ (1979) The use of the rank transform in regression. Technometrics 21:499–509

    Article  Google Scholar 

  • Inger R, Jackson A, Parnell A, Bearhop S (2010) SIAR v4 (Stable Isotope Analysis in R): an ecologist’s guide. http://www.tcd.ie/Zoology/research/research/theoretical/siar/SIAR_For_Ecologists.pdf

  • Jay CV, Fischbach AS (2008) Pacific walrus response to Arctic sea ice losses. U.S. Geological Survey Fact Sheet 2008-3041

  • Jay CV, Outridge PM, Garlich-Miller JL (2008) Indication of two Pacific walrus stocks from whole tooth elemental analysis. Polar Biol 31(8):933–943

    Article  Google Scholar 

  • Jay CV, Fischbach AS, Kochnev AA (2012) Walrus areas of use in the Chukchi Sea during sparse sea ice cover. Mar Ecol Prog Ser 468:1–13

    Article  Google Scholar 

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

    Google Scholar 

  • Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78(1):1–27

    Article  Google Scholar 

  • Kuhnlein HV, Soueida R (1992) Use and nutrient composition of traditional Baffin Inuit foods. J Food Compos Anal 5(2):112–126

    Article  CAS  Google Scholar 

  • Kurle CM, Worthy GAJ (2002) Stable nitrogen and carbon isotope ratios in multiple tissues of the northern fur seal Callorhinus ursinus: implications for dietary and migratory reconstructions. Mar Ecol Prog Ser 236:289–300

    Article  Google Scholar 

  • Kutz SJ, Hoberg EP, Polley L, Jenkins EJ (2005) Global warming is changing the dynamics of Arctic host-parasite systems. Proc Biol Sci 272(1581):2571–2576

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liedberg P, Garlich-Miller J, Meehan R (2009) Walrus mortality event Cape Peirce, Alaska-October 2009. News Release

  • Lovvorn JR, Wilson JJ, McKay D, Bump JK, Cooper LW, Grebmeier JM (2010) Walruses attack spectacled eiders wintering in pack ice of the Bering Sea. Arctic 63(1):53–56

    Article  Google Scholar 

  • Lowry LF, Fay FH (1984) Seal eating by walruses in the Bering and Chukchi Seas. Polar Biol 3:11–18

    Article  Google Scholar 

  • Mallory ML, Woo K, Gaston AJ, Davies WE, Mineau P (2004) Walrus (Odobenus rosmarus) predation on adult thick-billed murres (Uria lomvia) at Coats Island, Nunavut, Canada. Polar Res 23(1):111–114

    Article  Google Scholar 

  • Metcalf V, Robards M (2008) Sustaining a healthy human–walrus relationship in a dynamic environment: challenges for comanagement. Ecol Appl 18(2 Suppl):S148–S156

    Article  PubMed  Google Scholar 

  • Misarti N, Finney B, Maschner H, Wooller MJ (2009) Changes in northeast Pacific marine ecosystems over the last 4500 years: evidence from stable isotope analysis of bone collagen from archeological middens. Holocene 19(8):1139–1151

    Article  Google Scholar 

  • Muir DCG, Segstro MD, Hobson KA, Ford CA, Stewart REA, Olpinski S (1995) Can seal eating explain elevated levels of PCBs and organochlorine pesticides in walrus blubber from eastern Hudson Bay (Canada)? Environ Pollut 90(3):335–348

    Article  CAS  PubMed  Google Scholar 

  • National Snow and Ice Data Center (2012) A summer storm in the Arctic. Arctic Sea Ice News & Analysis. http://nsidc.org/arcticseaicenews/2012/08/a-summer-storm-in-the-arctic/. Accessed 14 Aug 2012

  • Newsome SD, Clementz MT, Koch PL (2010) Using stable isotope biogeochemistry to study marine mammal ecology. Mar Mamm Sci 26(3):509–572

    CAS  Google Scholar 

  • Oftedal OT (2000) Use of maternal reserves as a lactation strategy in large mammals. Proc Nutr Soc 59(1):99–106

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Phillips DL, Newsome SD, Gregg JW (2005) Combining sources in stable isotope mixing models. Oecologia 44:520–527

    Article  Google Scholar 

  • Pierce GJ, Santos MB, Learmonth JA, Mente E, Stowasser G (2004) Methods for dietary studies on marine mammals. The Mediterranean science commission: investigating the roles of cetaceans in marine ecosystems. Venice, Italy. 28–31 Jan 2004

  • Quay PD, Tilbrook B, Wong CS (1992) Oceanic uptake of fossil fuel CO2: carbon-13 evidence. Science 256(5053):74–79

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org/

  • Rausch R, George JC, Brower HK (2007) Effect of climatic warming on the Pacific walrus and potential modification of its helminth fauna. J Parasitol 93(5):1247–1251

    Article  PubMed  Google Scholar 

  • Ray GC, McCormick-Ray J, Berg P, Epstein HE (2006) Pacific walrus: benthic bioturbator of Beringia. J Exp Mar Biol Ecol 330(1):403–419

    Article  Google Scholar 

  • Reeves R, Stewart B, Leatherwood S (1992) The Sierra Club handbook of seals and sirenians. Sierra Club Books, San Francisco

    Google Scholar 

  • Ricciardi A, Bourget E (1998) Weight-to-weight conversion factors for marine benthic macroinvertebrates. Mar Ecol Prog Ser 163:245–251

    Article  Google Scholar 

  • Rosen DAS, Winship AJ, Hoopes LA (2007) Thermal and digestive constraints to foraging behaviour in marine mammals. Philos Trans R Soc Lond B Biol Sci 362(1487):2151–2168

    Article  PubMed Central  PubMed  Google Scholar 

  • Ryg M, Lydersen C, Markussen NH, Smith TG, Øritsland NA (1990) Estimating the blubber content of phocid seals. Can J Fish Aquat Sci 47(6):1223–1227

    Article  Google Scholar 

  • Seymour J, Horstmann-Dehn L, Wooller MJ (2014) Inter-annual variability in the proportional contribution of higher trophic levels to the diet of Pacific walruses. Polar Biol. doi:10.1007/s00300-014-1460-7

    Google Scholar 

  • Sheffield G, Grebmeier JM (2009) Pacific walrus (Odobenus rosmarus divergens): differential prey digestion and diet. Mar Mamm Sci 25(4):761–777

    Article  Google Scholar 

  • Sheffield G, Fay FH, Feder H, Kelly BP (2001) Laboratory digestion of prey and interpretation of walrus stomach contents. Mar Mamm Sci 17(2):310–330

    Article  Google Scholar 

  • Sponheimer M, Robinson TF, Cerling TE, Tegland L, Roeder BL, Ayliffe L, Dearing MD, Ehleringer JR (2006) Turnover of stable carbon isotopes in the muscle, liver, and breath CO2 of alpacas (Lama pacos). Rapid Commun Mass Spectrom 20(9):1395–1399

    Article  CAS  PubMed  Google Scholar 

  • Stroeve JC, Serreze MC, Holland MM, Kay JE, Malanik J, Barrett AP (2012) The Arctic’s rapidly shrinking sea ice cover: a research synthesis. Clim Change 110:1005–1027

    Article  Google Scholar 

  • Sweeting CJ, Polunin NVC, Jennings S (2006) Effects of chemical lipid extraction and arithmetic lipid correction on stable isotope ratios of fish tissues. Rapid Commun Mass Spectrom 20(1):595–601

    Article  CAS  PubMed  Google Scholar 

  • TE Sub Systems Inc. and Sax Software (2006) SigmaPlot for Windows®. Version 10.0. Germany

  • Tiezsen LL, Boutton TW, Tesdahl KG, Slade NA (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57(1–2):32–37

    Article  Google Scholar 

  • Todd SK, Holm B, Rosen DAS, Tollit DJ (2010) Stable isotope signal homogeneity and differences between and within pinniped muscle and skin. Mar Mamm Sci 26(1):176–185

    Article  Google Scholar 

  • Usher PJ, Church M (1969) On the relationship of weight, length, and girth of the ringed seal (Pusa hispida) of the Canadian Arctic. Arctic 22(2):120–129

    Article  Google Scholar 

  • Wang SW, Budge SM, Gradinger RR, Iken K, Wooller MJ (2013) Fatty acid and stable isotope characteristics of sea ice and pelagic particulate matter in the Bering Sea: tools for estimating sea ice algal contribution to Arctic food web production. Oecologia. doi:10.1007/s00442-013-2832-3

    Google Scholar 

  • Welle S (1999) Human protein metabolism. Springer, Berlin

    Book  Google Scholar 

  • Wolkers H, van Bavel B, Ericson I, Skoglund E, Kovacs KM, Lydersen C (2006) Congener-specific accumulation and patterns of chlorinated and brominated contaminants in adult male walruses from Svalbard, Norway: indications for individual-specific prey selection. Sci Total Environ 370(1):70–79

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank the Eskimo Walrus Commission and the Alaskan coastal communities of Barrow, Diomede, Gambell, Savoonga, and Wainwright for providing walrus tissue samples from their subsistence harvests. We gratefully acknowledge the Alaska Department of Fish and Game, U.S. Fish and Wildlife Service, and North Slope Borough Department of Wildlife Management for logistical coordination, particularly B. Adams, A. Bryan, J. Garlich-Miller, C. George, C. Hanns, G. Krafsur, C. Nayakik, Sr., L. Quakenbush, T. Sformo, and J. Snyder. We further thank U.S. Geological Survey, particularly A. Fischbach and C. Jay, for providing skin samples from their ongoing biopsy program, the University of Alaska Museum of the North for providing archived walrus tissue (Loan # 2010.006.Mamm, samples UAM 24069, 36307, 36308, 36312, 36313, 36317, 36322, 36324, 36325, 36339, 36342, 36349, 36355, 49575, 54001, 60205, 60206, 60211, 60212, 60346, 60352, 60383, 60410, 83321, 85027, 85036, 85043, 88474, 88491, 88493, 88514, 97916, 97932, 98208, 98209, 98210, 99576, 99579, 99594, 99595, 99599, 99600, 99951, 99972), and Togiak National Wildlife Refuge for sharing samples from the 2009 Cape Peirce mortality event, K. Iken for providing Serripes spp. stable isotope values, J. Lovvorn for providing spectacled eider stable isotope values, and to the staff of the Alaska Stable Isotope Facility, particularly T. Howe and N. Haubenstock. Funding was provided by University of Alaska Fairbanks through Dr. Horstmann-Dehn, the North Pacific Research Board (Project #901), and the Cooperative Institute for Alaska Research (GC 10-04). K. Seymour provided thoughtful insight on early drafts of this manuscript. The content of this manuscript was greatly improved by the comments of S. Atkinson, C. Rosa, G. Sheffield, P. Barboza, D. Piepenburg, and three anonymous reviewers.

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Authors and Affiliations

  1. School of Fisheries and Ocean Sciences, University of Alaska Fairbanks, P.O. Box 755220, Fairbanks, AK, 99775-7220, USA

    J. Seymour

  2. School of Fisheries and Ocean Sciences, Institute of Marine Science, University of Alaska Fairbanks, P.O. Box 757220, Fairbanks, AK, 99775-7220, USA

    L. Horstmann-Dehn

  3. School of Fisheries and Ocean Sciences, Institute of Marine Science, University of Alaska Fairbanks, P.O. Box 755860, Fairbanks, AK, 99775-5860, USA

    M. J. Wooller

  4. Alaska Stable Isotope Facility, Water and Environmental Research Center, University of Alaska Fairbanks, P.O. Box 755860, Fairbanks, AK, 99775-5860, USA

    M. J. Wooller

  5. Alaska Quaternary Center, University of Alaska Fairbanks, P.O. Box 755860, Fairbanks, AK, 99775-5860, USA

    M. J. Wooller

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Seymour, J., Horstmann-Dehn, L. & Wooller, M.J. Proportion of higher trophic-level prey in the diet of Pacific walruses (Odobenus rosmarus divergens). Polar Biol 37, 941–952 (2014). https://doi.org/10.1007/s00300-014-1492-z

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