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Pacific walrus diet across 4000 years of changing sea ice conditions

Published online by Cambridge University Press:  14 March 2019

Casey T. Clark*
Affiliation:
Water and Environmental Research Center, University of Alaska Fairbanks, 1764 Tanana Loop, Fairbanks, Alaska 99775-5860, USA College of Fisheries and Ocean Sciences, University of Alaska Fairbanks, 2150 Koyukuk Drive, Fairbanks, Alaska 99775-7220, USA
Lara Horstmann
Affiliation:
College of Fisheries and Ocean Sciences, University of Alaska Fairbanks, 2150 Koyukuk Drive, Fairbanks, Alaska 99775-7220, USA
Anne de Vernal
Affiliation:
Centre de Recherché en Géochimie et Géodynamique (Geotop), Université du Québec à Montréal, P.O. Box 8888, Succursale Centre-Ville, Montréal, Québec H3C 3P8, Canada
Anne M. Jensen
Affiliation:
UIC Science LLC, P.O. Box 577, Utqiaġvik, Alaska 99723, USA University of Alaska Museum, University of Alaska Fairbanks, 1962 Yukon Drive, Fairbanks, Alaska 99775, USA
Nicole Misarti
Affiliation:
Water and Environmental Research Center, University of Alaska Fairbanks, 1764 Tanana Loop, Fairbanks, Alaska 99775-5860, USA
*
*Corresponding author e-mail address: [email protected]

Abstract

Declining sea ice is expected to change the Arctic's physical and biological systems in ways that are difficult to predict. This study used stable isotope compositions (δ13C and δ15N) of archaeological, historic, and modern Pacific walrus (Odobenus rosmarus divergens) bone collagen to investigate the impacts of changing sea ice conditions on walrus diet during the last ~4000 yr. An index of past sea ice conditions was generated using dinocyst-based reconstructions from three locations in the northeastern Chukchi Sea. Archaeological walrus samples were assigned to intervals of high and low sea ice, and δ13C and δ15N were compared across ice states. Mean δ13C and δ15N values were similar for archaeological walruses from intervals of high and low sea ice; however, variability among walruses was greater during low-ice intervals, possibly indicating decreased availability of preferred prey. Overall, sea ice conditions were not a primary driver of changes in walrus diet. The diet of modern walruses was not consistent with archaeological low sea ice intervals. Rather, the low average trophic position of modern walruses (primarily driven by males), with little variability among individuals, suggests that trophic changes to this Arctic ecosystem are still underway or are unprecedented in the last ~4000 yr.

Type
Research Article
Copyright
Copyright © University of Washington. Published by Cambridge University Press, 2019

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References

REFERENCES

Alter, S.E., Newsome, S.D., Palumbi, S.R., 2012. Pre-whaling genetic diversity and population ecology in eastern pacific gray whales: insights from ancient DNA and stable isotopes. PLoS ONE 7, 112.CrossRefGoogle ScholarPubMed
Arrigo, K.R., Perovich, D.K., Pickart, R.S., Brown, Z.W., van Dijken, G.L., Lowry, K.E., Mills, M.M., et al. , 2012. Massive phytoplankton blooms under Arctic sea ice. Science 336, 14081408.CrossRefGoogle ScholarPubMed
Arrigo, K.R., van Dijken, G.L., 2015. Continued increases in Arctic Ocean primary production. Progress in Oceanography 136, 6070.CrossRefGoogle Scholar
Beatty, W.S., Jay, C.V., Fischbach, A.S., Grebmeier, J.M., Taylor, R.L., Blanchard, A.L., Jewett, S.C., 2016. Space use of a dominant Arctic vertebrate: effects of prey, sea ice, and land on Pacific walrus resource selection. Biological Conservation 203, 2532.CrossRefGoogle Scholar
Blaauw, M., Christen, J.A., 2011. Flexible paleoclimate age-depth models using an autoregressive gamma process. Bayesian Analysis 6, 457474.CrossRefGoogle Scholar
Blanca, M.J., Alarcón, R., Arnau, J., Bono, R., Bendayan, R., 2017. Non-normal data: is ANOVA still a valid option? Psicothema 29, 552557.Google ScholarPubMed
Bolnick, D.I., Svanbäck, R., Fordyce, J.A., Yang, L.H., Davis, J.M., Hulsey, C.D., Forister, M.L., 2003. The ecology of individuals: incidence and implications of individual specialization. American Naturalist 161, 128.CrossRefGoogle ScholarPubMed
Broecker, W.S., 2001. Was the Medieval Warm Period global? Science 291, 14971499.CrossRefGoogle ScholarPubMed
Casey, M.M., Post, D.M., 2011. The problem of isotopic baseline: reconstructing the diet and trophic position of fossil animals. Earth-Science Reviews 106, 131148.CrossRefGoogle Scholar
Castellini, M.A., Rea, L.D., 1992. The biochemistry of natural fasting at its limits. Experientia 48, 575582.CrossRefGoogle ScholarPubMed
Chikaraishi, Y., Ogawa, N.O., Kashiyama, Y., Takano, Y., Suga, H., Tomitani, A., Miyashita, H., Kitazato, H., Ohkouchi, N., 2009. Determination of aquatic food-web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnology and Oceanography: Methods 7, 740750.Google Scholar
Clark, C.T., Horstmann, L., Misarti, N., 2017. Quantifying variability in stable carbon and nitrogen isotope ratios within the skeletons of marine mammals of the suborder Caniformia. Journal of Archaeological Science: Reports 15, 393400.Google Scholar
Conners, M.E., Hollowed, A.B., Brown, E., 2002. Retrospective analysis of Bering Sea bottom trawl surveys: regime shift and ocean reorganization. Progress in Oceanography 55, 209222.CrossRefGoogle Scholar
Coyle, K.O., Konar, B., Blanchard, A., Highsmith, R.C., Carroll, J., Carroll, M., Denisenko, S.G., Sirenko, B.I., 2007. Potential effects of temperature on the benthic infaunal community on the southeastern Bering Sea shelf: possible impacts of climate change. Deep-Sea Research Part II: Topical Studies in Oceanography 54, 28852905.CrossRefGoogle Scholar
Cronin, M.A., Hills, S., Born, E.W., Patton, J.C., 1994. Mitochondrial DNA variation in Atlantic and Pacific walruses. Canadian Journal of Zoology 72, 10351043.CrossRefGoogle Scholar
Danielson, S.L., Weingartner, T.J., Hedstrom, K.S., Aagaard, K., Woodgate, R., Curchitser, E., Stabeno, P.J., 2014. Coupled wind-forced controls of the Bering-Chukchi shelf circulation and the Bering Strait throughflow: Ekman transport, continental shelf waves, and variations of the Pacific-Arctic sea surface height gradient. Progress in Oceanography 125, 4061.CrossRefGoogle Scholar
Dehn, L.A., Sheffield, G.G., Follmann, E.H., Duffy, L.K., Thomas, D.L., O'Hara, T.M., 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 Biology 30, 167181.CrossRefGoogle Scholar
de Vernal, A., Hillaire-Marcel, C., Darby, D.A., 2005. Variability of sea ice cover in the Chukchi Sea (western Arctic Ocean) during the Holocene. Paleoceanography 20, PA4018.CrossRefGoogle Scholar
de Vernal, A., Rochon, A., Fréchette, B., Henry, M., Radi, T., Solignac, S., 2013. Reconstructing past sea ice cover of the Northern Hemisphere from dinocyst assemblages: status of the approach. Quaternary Science Reviews 79, 122134.CrossRefGoogle Scholar
Dickson, R.R., Osborn, T.J., Hurrell, J.W., Meincke, J., Blindheim, J., Adlandsvik, B., Vinje, T., Alekseev, G., Maslowski, W., 2000. The Arctic Ocean response to the North Atlantic Oscillation. Journal of Climate 13, 26712696.2.0.CO;2>CrossRefGoogle Scholar
Dunnett, C., 1980. Pairwise multiple comparisons in the unequal variance case. Journal of the American Statistical Association 75, 796800.CrossRefGoogle Scholar
Dyke, A.S., Savelle, J.M., 2001. Holocene history of the Bering Sea bowhead whale (Balaena mysticetus) in its Beaufort Sea summer grounds off southwestern Victoria Island, western Canadian Arctic. Quaternary Research 55, 371379.CrossRefGoogle Scholar
Ebbesmeyer, C.C., Cayan, D.R., McLain, D.R., Nichols, F.H., Peterson, D.H., Redmond, K.T., 1991. 1976 Step in the Pacific climate: forty environmental changes between 1968–1975 and 1977–1984. In: Betancourt, J.L., Tharp, V.L. (Eds.), Proceedings of the Seventh Annual Pacific Climate (PACLIM) Workshop: Asilomar, California – April 1990. Technical Report 26 of the Interagency Ecological Studies Program for the Sacramento–San Joaquin Estuary. California Department of Water Resources, Sacramento, CA, pp. 115126.Google Scholar
Fabry, V., McClintock, J., Mathis, J., Grebmeier, J., 2009. Ocean acidification at high latitudes: the bellwether. Oceanography 22, 160171.CrossRefGoogle Scholar
Farmer, J.R., Cronin, T.M., De Vernal, A., Dwyer, G.S., Keigwin, L.D., Thunell, R.C., 2011. Western Arctic Ocean temperature variability during the last 8000 years. Geophysical Research Letters 38, 49.CrossRefGoogle Scholar
Fay, F.H. 1982. Ecology and biology of the Pacific walrus, Odobenus rosmarus divergens Illiger. North American Fauna 74, 1279.CrossRefGoogle Scholar
Fay, F.H., Kelly, B.P., Sease, J.L., 1989. Managing the exploitation of Pacific walruses: a tragedy of delayed response and poor communication. Marine Mammal Science 5, 116.CrossRefGoogle Scholar
Fogel, M.L., Cifuentes, L.A., 1993. Isotope fractionation during primary production. In: Engel, M.H., Macko, S.A. (Eds.), Organic Geochemistry. Springer, Boston, MA, pp. 7398.CrossRefGoogle Scholar
Fry, B., 2006. Stable Isotope Ecology. Springer, New York.CrossRefGoogle Scholar
Garlich-Miller, J., MacCracken, J.G., Snyder, J., Meehan, R., Myers, M., Wilder, J.M., Lance, E., Matz, A., 2011. Status Review of the Pacific Walrus (Odobenus rosmarus divergens). U.S. Fish and Wildlife Service, Anchorage, AK.Google Scholar
Garlich-Miller, J.L., Stewart, R.E.A., Stewart, B.E., Hiltz, E.A., 1993. Comparison of mandibular with cemental growth-layer counts for ageing Atlantic walrus (Odobenus rosmarus rosmarus). Canadian Journal of Zoology 71, 163167.CrossRefGoogle Scholar
Goericke, R., Fry, B., 1994. Variations of marine plankton δ13C with latitude, temperature, and dissolved CO2 in the world ocean. Global Biogeochemical Cycles 8, 8590.CrossRefGoogle Scholar
Grebmeier, J.M., 2012. Shifting patterns of life in the Pacific Arctic and sub-Arctic seas. Annual Review of Marine Science 4, 6378.CrossRefGoogle ScholarPubMed
Grebmeier, J.M., Bluhm, B.A., Cooper, L.W., Danielson, S.L., Arrigo, K.R., Blanchard, A.L., Clarke, J.T., et al. , 2015a. Ecosystem characteristics and processes facilitating persistent macrobenthic biomass hotspots and associated benthivory in the Pacific Arctic. Progress in Oceanography 136, 92114.CrossRefGoogle Scholar
Grebmeier, J.M., Bluhm, B.A., Cooper, L.W., Denisenko, S.G., Iken, K., Kedra, M., Serratos, C., 2015b. Time-series benthic community composition and biomass and associated environmental characteristics in the Chukchi Sea during the RUSALCA 2004–2012 Program. Oceanography 28, 116133.CrossRefGoogle Scholar
Grebmeier, J.M., Cooper, L.W., Feder, H.M., Sirenko, B.I., 2006. Ecosystem dynamics of the Pacific-influenced northern Bering and Chukchi Seas in the Amerasian Arctic. Progress in Oceanography 71, 331361.CrossRefGoogle Scholar
Grove, J.M., 1988. The Little Ice Age. Methuen, London.CrossRefGoogle Scholar
Hedges, J.E.M., Stevens, R.E., Koch, P.L., 2006. Isotopes in bones and teeth. In: Leng, M.J. (Ed.), Isotopes in Palaeoenvironmental Research. Springer, Dordrecht, the Netherlands, pp. 117145.CrossRefGoogle Scholar
Heusser, C.J., Heusser, L.E., Peteet, D.M., 1985. Late-Quaternary climatic change on the American North Pacific Coast. Letters to Nature 315, 485487.CrossRefGoogle Scholar
Hobson, K.A., Alisauskas, R.A.Y.T., Clark, R.G., 1993. Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. Condor 95, 388394.CrossRefGoogle Scholar
Hobson, K.A., Welch, H.E., 1992. Determination of trophic relationships within a high Arctic marine food web using δ13C and δ15N analysis. Marine Ecology Progress Series 84, 918.CrossRefGoogle Scholar
Horstmann, L., Stimmelmayr, R., McCarthy, M., 2017. Eating seal or hungry like a wolf? Polar bear use of terrestrial resources revealed by compound-specific stable isotopes. In: 22nd Biennial Conference on the Biology of Marine Mammals, 70. Society for Marine Mammalogy, Lawrence, KS.Google Scholar
Huang, B., Banzon, V.F., Freeman, E., Lawrimore, J., Liu, W., Peterson, T.C., Smith, T.M., Thorne, P.W., Woodruff, S.D., Zhang, H.-M., 2015. Extended reconstructed sea surface temperature version 4 (ERSST.v4). Part I: upgrades and intercomparisons. Journal of Climate 28, 911930.CrossRefGoogle Scholar
Huntington, H.P., Quakenbush, L.T., Nelson, M., Huntington, H.P., 2016. Effects of changing sea ice on marine mammals and subsistence hunters in northern Alaska from traditional knowledge interviews. Biology Letters 12, 47.CrossRefGoogle ScholarPubMed
Jackson, A.L., Inger, R., Parnell, A.C., Bearhop, S., 2011. Comparing isotopic niche widths among and within communities: SIBER – Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80, 595602.CrossRefGoogle ScholarPubMed
Jay, C.V., Fischbach, A.S., Kochnev, A.A., 2012. Walrus areas of use in the Chukchi Sea during sparse sea ice cover. Marine Ecology Progress Series 468, 113.CrossRefGoogle Scholar
Jay, C.V., Grebmeier, J.M., Fischbach, A.S., McDonald, T.L., Cooper, L.W., Hornsby, F., 2014. Pacific walrus (Odobenus rosmarus divergens) resource selection in the northern Bering Sea. PLoS ONE 9, e93035.CrossRefGoogle ScholarPubMed
Jay, C.V., Marcot, B.G., Douglas, D.C., 2011. Projected status of the Pacific walrus (Odobenus rosmarus divergens) in the twenty-first century. Polar Biology 34, 10651084.CrossRefGoogle Scholar
Jay, C.V., Outridge, P.M., Garlich-Miller, J.L., 2008. Indication of two Pacific walrus stocks from whole tooth elemental analysis. Polar Biology 31, 933943.CrossRefGoogle Scholar
Kaufman, D.S., Axford, Y.L., Henderson, A.C.G., McKay, N.P., Oswald, W.W., Saenger, C., Anderson, R.S., et al. , 2016. Holocene climate changes in eastern Beringia (NW North America) – a systematic review of multi-proxy evidence. Quaternary Science Reviews 147, 312339.CrossRefGoogle Scholar
Kȩdra, M., Moritz, C., Choy, E.S., David, C., Degen, R., Duerksen, S., Ellingsen, I., et al. , 2015. Status and trends in the structure of Arctic benthic food webs. Polar Research 34, 123.CrossRefGoogle Scholar
Keeling, C.D., Piper, S.C., Bacastow, R.B., Wahlen, M., Whorf, T.P., Heimann, M., Meijer, H.A., 2005. Atmospheric CO2 and 13CO2 exchange with the terrestrial biosphere and oceans from 1978 to 2000: observations and carbon cycle implications. In: Baldwin, I.T., Caldwell, M.M., Heldmaier, G., Jackson, R.B., Lange, O.L., Mooney, H.A., Schulze, E.-D., et al. (Eds.), A History of Atmospheric CO2 and Its Effects on Plants, Animals, and Ecosystems. Springer, New York, pp. 83113.Google Scholar
Koch, P.L., Fogel, M.L., Tuross, N., 1994. Tracing the diets of fossil animals using stable isotopes. In: Lajtha, K., Michener, B. (Eds.), Stable Isotopes in Ecology and Environmental Science. Blackwell Scientific, Boston, MA, pp. 6392.Google Scholar
Kutzbach, J.E., 1970. Large-scale features of monthly mean Northern Hemisphere anomaly maps of sea-level pressure. Monthly Weather Review 98, 708716.2.3.CO;2>CrossRefGoogle Scholar
Laws, E.A., Popp, B.N., Bidigare, J.R.R., Kennicutt, M.C., Macko, S.A., 1995. Dependence of phytoplankton carbon isotopic composition on growth rate and [CO2]aq: theoretical considerations and experimental results. Geochimica et Cosmochimica Acta 59, 11311138.CrossRefGoogle Scholar
Laws, E.A., Popp, B.N., Cassas, N., Tanimoto, J., 2002. 13C discrimination patterns in oceanic phytoplankton: likely influence of CO2 concentrating mechanisms, and implications for palaeoreconstructions. Functional Plant Biology 29, 323333.CrossRefGoogle ScholarPubMed
Li, W.K.W., McLaughlin, F.A., Lovejoy, C., Carmack, E.C., 2009. Smallest algae thrive as the Arctic Ocean freshens. Science 326, 539.CrossRefGoogle ScholarPubMed
Lindqvist, C., Bachmann, L., Andersen, L.W., Born, E.W., Arnason, U., Kovacs, K.M., Lydersen, D., Abramov, A.V., Wiig, Ø., 2009. The Laptev Sea walrus Odobenus rosmarus laptevi: an enigma revisited. Zoologica Scripta 38, 113127.CrossRefGoogle Scholar
Ljungqvist, F.C., 2010. A regional approach to the Medieval Warm Period and the Little Ice Age. In: Simard, S., Austin, M. (Eds.), Climate Change and Variability. Sciyo, Rijek, Croatia, pp. 126.Google Scholar
Long, J.S., Ervin, L.H., 2000. Using heteroscedasticity consistent standard errors in the linear regression model. American Statistician 54, 217224.Google Scholar
Lotze, H.K., Worm, B., 2009. Historical baselines for large marine animals. Trends in Ecology and Evolution 24, 254262.CrossRefGoogle ScholarPubMed
MacCracken, J.G., 2012. Pacific Walrus and climate change: observations and predictions. Ecology and Evolution 2, 20722090.CrossRefGoogle ScholarPubMed
MacCracken, J.G., Beatty, W.S., Garlich-Miller, J.L., Kissling, M.L., Snyder, J.A., 2017. Final Species Status Assessment for the Pacific Walrus. U.S. Fish and Wildlife, Anchorage, AK.Google Scholar
Mahoney, A.R., Bockstoce, J.R., Botkin, D.B., Eicken, H., Nisbet, R.A., 2011. Sea-ice distribution in the Bering and Chukchi seas: information from historical whaleships' logbooks and journals. Arctic 64, 465477.CrossRefGoogle Scholar
Manolagas, S.C., 2000. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocrine Reviews 21, 115137.Google ScholarPubMed
Matheus, P.E., 1995. Diet and co-ecology of Pleistocene short-faced bears and brown bears in eastern Beringia. Quaternary Research 44, 447453.CrossRefGoogle Scholar
Matthews, J.A., Dresser, P.Q., 2008. Holocene glacier variation chronology of the Smørstabbtindan massif, Jotunheimen, southern Norway, and the recognition of century- to millennial-scale European Neoglacial Events. Holocene 18, 181201.CrossRefGoogle Scholar
McClelland, J.W., Montoya, J.P., 2017. Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83, 21732180.CrossRefGoogle Scholar
McKay, J.L., de Vernal, A., Hillaire-Marcel, C., Not, C., Polyak, L., Darby, D., 2008. Holocene fluctuations in Arctic sea-ice cover: dinocyst-based reconstructions for the eastern Chukchi Sea. Canadian Journal of Earth Sciences 45, 13771397.CrossRefGoogle Scholar
McNeely, R., Dyke, A.S., Southon, J.R., 2006. Canadian Marine Reservoir Ages, Preliminary Data Assessment. Open File 5094. Geological Survey of Canada, Calgary, AB, Canada.Google Scholar
Misarti, N., Finney, B., Maschner, H., Wooller, M.J., 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, 11391151.CrossRefGoogle Scholar
Misarti, N., Gier, E., Finney, B., Barnes, K., McCarthy, M., 2017. Compound-specific amino acid δ15N values in archaeological shell: assessing diagenetic integrity and potential for isotopic baseline reconstruction. Rapid Communications in Mass Spectrometry 31, 18811891.CrossRefGoogle Scholar
Newsome, S.D., Clementz, M.T., Koch, P.L., 2010. Using stable isotope biogeochemistry to study marine mammal ecology. Marine Mammal Science 26, 509572.Google Scholar
Newsome, S.D., Etnier, M.A., Kurle, C.M., Waldbauer, J.R., Chamberlain, C.P., Koch, P.L., 2007. Historic decline in primary productivity in western Gulf of Alaska and eastern Bering Sea: isotopic analysis of northern fur seal teeth. Marine Ecology Progress Series 332, 211224.CrossRefGoogle Scholar
Niebauer, H.J., 1998. Variability in Bering Sea ice cover as affected by a regime shift in the North Pacific in the period 1947–1996. Journal of Geophysical Research: Oceans 103, 2771727737.CrossRefGoogle Scholar
Noren, S.R., Udevitz, M.S., Jay, C.V., 2012. Bioenergetics model for estimating food requirements of female Pacific walruses Odobenus rosmarus divergens. Marine Ecology Progress Series 460, 261275.CrossRefGoogle Scholar
Noren, S.R., Udevitz, M.S., Jay, C.V., 2016. Sex-specific energetics of Pacific walruses (Odobenus rosmarus divergens) during the nursing interval. Physiological and Biochemical Zoology 89, 93109.CrossRefGoogle ScholarPubMed
Ostrom, P.H., Wiley, A.E., James, H.F., Rossman, S., Walker, W.A., Zipkin, E.F., Chikaraishi, Y., 2017. Broad-scale trophic shift in the pelagic North Pacific revealed by an oceanic seabird. Proceedings of the Royal Society B: Biological Sciences 284, 20162436.CrossRefGoogle ScholarPubMed
Oxtoby, L.E., Mathis, J.T., Juranek, L.W., Wooller, M.J., 2016. Estimating stable carbon isotope values of microphytobenthos in the Arctic for application to food web studies. Polar Biology 39, 473483.CrossRefGoogle Scholar
Porter, S.C., Denton, G.H., 1967. Chronology of neoglaciation in the North American Cordillera. American Journal of Science 265, 177210.CrossRefGoogle Scholar
Reimer, P.J., Bard, E., Bayliss, A., Beck, J.W., Blackwell, P.G., Bronk Ramsey, C., Buck, C.E., et al. , 2013. Intcal13 and Marine13 radiocarbon age calibration curves 0–50,000 years cal BP. Radiocarbon 55, 18691887.CrossRefGoogle Scholar
Rick, T.C., Lockwood, R., 2013. Integrating paleobiology, archeology, and history to inform biological conservation. Conservation Biology 27, 4554.CrossRefGoogle ScholarPubMed
Rodionov, S.N., Bond, N.A., Overland, J.E., 2007. The Aleutian Low, storm tracks, and winter climate variability in the Bering Sea. Deep Sea Research Part II: Topical Studies in Oceanography 54, 25602577.CrossRefGoogle Scholar
Schoener, T.W., 1971. Theory of feeding strategies. Annual Review of Ecology and Systematics 2, 369404.CrossRefGoogle Scholar
Scribner, K.T., Hills, S., Fain, S.R., Cronin, M.A., 1997. Population genetics studies of the walrus (Odobenus rosmarus): a summary and interpretation of results and research needed. In: Dizon, A.E., Chivers, S.J., Perrin, W.F. (Eds.), Molecular Genetics of Marine Mammals. Society for Marine Mammalogy, Lawrence, KS, pp. 173184.Google Scholar
Seymour, J., Horstmann-Dehn, L., Wooller, M.J., 2014a. Inter-annual variability in the proportional contribution of higher trophic levels to the diet of Pacific walruses. Polar Biology 37, 597609.CrossRefGoogle Scholar
Seymour, J., Horstmann-Dehn, L., Wooller, M.J., 2014b. Proportion of higher trophic-level prey in the diet of Pacific walruses (Odobenus rosmarus divergens). Polar Biology 37, 941952.CrossRefGoogle Scholar
Sheffield, G., Grebmeier, J.M., 2009. Pacific walrus (Odobenus rosmarus divergens): differential prey digestion and diet. Marine Mammal Science 25, 761777.CrossRefGoogle Scholar
Sherwood, O.A., Guilderson, T.P., Batista, F.C., Schiff, J.T., McCarthy, M.D., 2014. Increasing subtropical North Pacific Ocean nitrogen fixation since the Little Ice Age. Nature 505, 7881.CrossRefGoogle ScholarPubMed
Shitova, M.V., Kochnev, A.A., Dolnikova, O.G., Kryukova, N.V., Malinina, T.V., Pereverzev, A.A., 2017. Genetic diversity of the Pacific walrus (Odobenus rosmarus divergens) in the western part of the Chukchi Sea. Russian Journal of Genetics 53, 242251.CrossRefGoogle ScholarPubMed
Sol, D., Elie, M., Marcoux, M., Chrostovsky, E., Porcher, C., Lefebvre, L., 2005. Ecological mechanisms of a resource polymorphism in Zenaida Doves of Barbados. Ecology 86, 23972407.CrossRefGoogle Scholar
Sonsthagen, S.A., Jay, C.V., Fischbach, A.S., Sage, G.K., Talbot, S.L., 2012. Spatial genetic structure and asymmetrical gene flow within the Pacific walrus. Journal of Mammalogy 93, 15121524.CrossRefGoogle Scholar
Springer, A.M., Estes, J.A., van Vliet, G.B., Williams, T.M., Doak, D.F., Danner, E.M., Forney, K.A., Pfister, B., 2003. Sequential megafaunal collapse in the North Pacific Ocean: an ongoing legacy of industrial whaling? Proceedings of the National Academy of Sciences of the United States of America 100, 1222312228.CrossRefGoogle ScholarPubMed
Stephens, D.W., Krebs, J.R., 1986. Foraging Theory. Princeton University Press, Princeton, NJ.Google Scholar
Stuiver, M., Pearson, G.W., Braziunas, T., 1986. Radiocarbon age calibration of marine samples back to 9000 cal yr BP. Radiocarbon 28, 9801021.CrossRefGoogle Scholar
Sun, J., Wang, H., 2006. Relationship between Arctic Oscillation and Pacific Decadal Oscillation on decadal timescale. Chinese Science Bulletin 51, 7579.CrossRefGoogle Scholar
Svanbäck, R., Bolnick, D.I., 2007. Intraspecific competition drives increased resource use diversity within a natural population. Proceedings of the Royal Society B: Biological Sciences 274, 839844.CrossRefGoogle ScholarPubMed
Swetnam, T.W., Allen, C.D., Betancourt, J.L., Applications, E., Nov, N., 1999. Applied historical ecology: using the past to manage for the future. Ecological Applications 9, 11891206.CrossRefGoogle Scholar
Szpak, P., Buckley, M., Darwent, C.M., Richards, M.P., 2018. Long-term ecological changes in marine mammals driven by recent warming in northwestern Alaska. Global Change Biology 24, 490503.CrossRefGoogle ScholarPubMed
Szpak, P., Metcalfe, J.Z., Macdonald, R.A., 2017. Best practices for calibrating and reporting stable isotope measurements in archaeology. Journal of Archaeological Science: Reports 13, 609616.Google Scholar
Thompson, D.W.J., Wallace, J.M., 1998. The Arctic Oscillation signature in the wintertime geopotential height and temperature fields. Geophysical Research Letters 25, 12971300.CrossRefGoogle Scholar
Tinker, M.T., Bentall, G., Estes, J.A., 2008. Food limitation leads to behavioral diversification and dietary specialization in sea otters. Proceedings of the National Academy of Sciences of the United States of America 105, 560565.CrossRefGoogle ScholarPubMed
Tu, K.L., Blanchard, A.L., Iken, K., Horstmann-Dehn, L., 2015. Small-scale spatial variability in benthic food webs in the northeastern Chukchi Sea. Marine Ecology Progress Series 528, 1937.CrossRefGoogle Scholar
Tuross, N., Fogel, M.L., Hare, P.E., 1988. Variability in the preservation of the isotopic composition of collagen from fossil bone. Geochimica et Cosmochimica Acta 52, 929935.CrossRefGoogle Scholar
Viau, A. E., Gajewski, K., Sawada, M. C., & Fines, P. (2006). Millennial-scale temperature variations in North America during the Holocene. Journal of Geophysical Research: Atmospheres, 111(D9).CrossRefGoogle Scholar
Walsh, J.E., Fetterer, F., Scott Stewart, J., Chapman, W.L., 2017. A database for depicting Arctic sea ice variations back to 1850. Geographical Review 107, 89107.CrossRefGoogle Scholar
Wang, T., Surge, D., Mithen, S., 2012. Seasonal temperature variability of the Neoglacial (3300–2500 BP) and Roman Warm Period (2500–1600 BP) reconstructed from oxygen isotope ratios of limpet shells (Patella vulgata), northwest Scotland. Palaeogeography, Palaeoclimatology, Palaeoecology 317–318, 104113.CrossRefGoogle Scholar
Wassmann, P., Reigstad, M., 2011. Future Arctic Ocean seasonal ice zones and implications for pelagic-benthic coupling. Oceanography 24, 220231.CrossRefGoogle Scholar
White, H., 1980. A heteroskedasticity-consistent covariance matrix estimator and a direct test for heteroskedasticity. Econometrica 48, 817838.CrossRefGoogle Scholar
Wiley, A.E., Ostrom, P.H., Welch, A.J., Fleischer, R.C., Gandhi, H., Southon, J.R., Stafford, T.W. Jr., et al. , 2013. Millennial-scale isotope records from a wide-ranging predator show evidence of recent human impact to oceanic food webs. Proceedings of the National Academy of Sciences of the United States of America 110, 89728977.CrossRefGoogle ScholarPubMed
Woodgate, R.A., Weingartner, T.J., Lindsay, R., 2012. Observed increases in Bering Strait oceanic fluxes from the Pacific to the Arctic from 2001 to 2011 and their impacts on the Arctic Ocean water column. Geophysical Research Letters 39, 27.CrossRefGoogle Scholar
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