Abstract
Pacific walruses (Odobenus rosmarus divergens) depend on Arctic sea ice as a resting and foraging platform; however, recent years have seen unprecedented seasonal reductions in ice extent. Previous researchers proposed that during unfavorable ice conditions, walruses might prey on other pinnipeds. To examine this hypothesis, we analyzed carbon and nitrogen stable isotope ratios of muscle from walruses (n = 155) sampled from the Bering and Chukchi seas during 2001–2010. We used a Bayesian stable isotope mixing model to examine the proportional contribution of higher trophic level prey (HTLP) (e.g., seals, seabirds) to walrus diets and extrapolated a tissue-specific turnover rate to compare diet of individuals over time. Mode HTLP across years was 19 % ± 8. Results indicate a significant decrease (P < 0.05) in the reliance on HTLP during 2008–2009 (mode HTLP 13 %), one of two sampling periods that experienced great seasonal loss of pan-Arctic sea ice (the other being 2007–2008 with mode HTLP of 23 %). We also reveal intra-annual fluctuations in the contribution of HTLP to the diet of a walrus sampled in 2011 with seal remains in its stomach through high-resolution sectioning along a whisker length. Our findings suggest that walruses forage opportunistically as a result of multiple environmental factors and that sea ice extent alone does not drive consumption of HTLP.
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References
Atwell L, Hobson KA, Welch HE (1998) Biomagnifications and bioaccumulation of mercury in an arctic marine food web: insights from stable nitrogen isotope analysis. Can J Fish Aquat Sci 55:1114–1121
Bahar B, Moloney AP, Monahan FJ, Harrison SM, Zazzo A, Scrimgeour CM, Begley IS, Schmidt O (2009) Turnover of carbon, nitrogen, and sulfur in bovine longissimus dorsi and psoas major muscles: implications for isotopic authentication of meat. J Anim Sci 87(3):905–913
Barboza PS, Parker KL, Hume ID (2009) Integrative wildlife nutrition. Springer, Berlin
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
Bluhm BA, Gebruk AV, Gradinger R, Hopcroft RR, Huettmann F, Kosobokova KN, Sirenko BI, Weslawski JM (2011) Arctic marine biodiversity: an update of species richness and examples of biodiversity change. Oceanography 24:232–248
Bond AL, Diamond AW (2011) Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecol Appl 21:1017–1023
Born EW, Rysgaard S, Ehlmé G, Sejr M, Acquarone M, Leverman N (2003) Underwater observations of foraging free-living Atlantic walruses (Odobenus rosmarus rosmarus) and estimates of their food consumption. Polar Biol 26:348–357
Burek KA, Gulland FMD, O’Hara TM (2008) Effects of climate change on Arctic marine mammal health. Ecol Appl 18:S126–S134
Burns JJ (1970) Remarks on the distribution and natural history of pagophilic pinnipeds in the Bering and Chukchi Seas. J Mammal 51:445–454
Carbone C, Teacher A, Rowcliffe JM (2007) The costs of carnivory. PLoS Biol 5:363–368
Carroll SS (2012) Insight into the diet history of ice seals using isotopic signatures of muscle tissue and claws. M.S. thesis, School of Fisheries and Ocean Sciences, University of Alaska Fairbanks, Fairbanks, AK
Carroll SS, Horstmann-Dehn L-A, Norcross BL (2013) Diet history of ice seals using stable isotope ratios in claw growth bands. Can J Zool 91:191–202
Cherel Y, Kernaléguen L, Richard P, Guinet C (2009) Whisker isotopic signature depicts migration patterns and multi-year intra- and inter-individual foraging strategies in fur seals. Biol Lett 5:830–832
Coyle KO, Bluhm B, Konar B, Blanchard A, Highsmith RC (2007) Amphipod prey of gray whales in the Northern Bering Sea: comparison of biomass and distribution between the 1980s and 2002–2003. Deep Sea Res Pt II 54:2906–2918
Dehn L-A, Sheffield G, Follman EH, Duffy LK, Thomas DL (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 30:167–181
Deniro MJ, Epstein S (1977) Influence of diet on the distribution of carbon isotopes in animals. Geochima et Cosmochimica Acta 42:495–506
Fay FH (1960) Carnivorous walruses and some arctic zoonoses. Arctic 13:111–122
Fay FH (1982) Ecology and biology of the Pacific walrus, Odobenus rosmarus divergens Illiger. U.S. Department of the Interior, Fish and Wildlife Service, Washington, DC
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, Nelson RR, Sease JL (1983) Trip report: Walrus research cruise of the ZRS Zykovo, Chukchi Sea, 24 July–22 August 1983. Project V. 6: Marine Mammals, US-USSR Environmental Protection Agreement. 14 pp
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
Fischbach AS, Amstrup SC, Douglas DC (2007) Landward and eastward shift of Alaskan polar bear denning associated with recent sea ice changes. Polar Biol 30:1395–1405
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
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 (1993) Studies of pelagic-benthic coupling extended onto the Soviet continental shelf in the northern Bering and Chukchi seas. Cont Shelf Res 13:653–668
Grebmeier JM (2012) Shifting patterns of life in the Pacific Arctic and sub-arctic seas. Annu Rev Mar Sci 4:63–78
Grebmeier JM, Cooper LW (1995) Influence of the St. Lawrence Island Polynya upon the Bering Sea benthos. J Geophys Res 100:4439–4460
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 311:1461–1464
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. Global Biogeochem Cycles 1:307–335
Harington CR (2008) The evolution of Arctic marine mammals. Ecol Appl 18(2):S38–S40
Herreman JK, Blundell GM, Ben-David M (2008) Evidence of bottom-up control of diet driven by top-down processes in a declining harbor seal Phoca vitulina richardsi population. Mar Ecol Prog Ser 374:287–300
Hindell MA, Lydersen C, Hop H, Kovacs K (2012) Pre-partum diet of adult female bearded seals in years of contrasting ice conditions. PLoS ONE 7(5):e38307
Hirons AC, Schell DM, St. Aubin DJ (2001) Growth rates of vibrissae of harbor seals (Phoca vitulina) and Steller sea lions (Eumetopias jubatus). Can J Zool 79:1053–1061
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
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
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
Hückstädt LA, Koch PL, McDonald BI, Goebel ME, Crocker DE, Costa DP (2011) Stable isotope analyses reveal individual variability in the trophic ecology of a top marine predator, the southern elephant seal. Oecologia 169:395–406
Iman RL, Conover WJ (1979) The use of the rank transform in regression. Technometrics 21:499–509
Jay CV, Fischbach AS (2008) Pacific Walrus Response to Arctic Sea Ice Losses. U.S. Geological Survey Fact Sheet 2008–3041
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
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
Jorde DG, Owen RB Jr (1988) Efficiency of nutrient use by American black ducks wintering in Maine. J Wildl Manage 52:209–214
Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78:1–27
Knutsen LØ, Born EW (1994) Body growth in Atlantic walruses (Odobenus rosmarus rosmarus). J Zool 234:371–385
Kolokotrones T, Savage V, Deeds EJ, Fontana W (2010) Curvature in metabolic scaling. Nature 464:753–756
Krebs CJ, Boonstra R, Boutin S, Sinclair ARE (2001) What drives the 10-year cycle of snowshoe hares? Bioscience 51:25–35
Kuhnlein HV, Soueida R (1992) Use and nutrient composition of traditional Baffin Inuit foods. J Food Compos Anal 5:112–126
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
Kutz SJ, Hoberg EP, Polley L, Jenkins EJ (2005) Global warming is changing the dynamics of Arctic host-parasite systems. Proc Biol Sci 272:2571–2576
Liedberg P, Garlich-Miller J, Meehan R (2009) Walrus mortality event Cape Peirce, Alaska-October 2009. News Release
Lowry LF, Fay FH (1984) Seal eating by walruses in the Bering and Chukchi Seas. Polar Biol 3:11–18
MacAvoy SE, Macko SA, Arneson LS (2005) Growth versus metabolic tissue replacement in mouse tissues determined by stable carbon and nitrogen isotope analysis. Can J Zool 83:631–641
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 23:111–114
McCauly E, Murdoch WM (1987) Cyclic and stable populations: plankton as paradigm. Am Nat 129:97–121
Misarti N, Finney B, Maschner H, Wooller MJ (2009) Changes in northeast Pacific marine ecosystems over the last 4,500 years: evidence from stable isotope analysis of bone collagen from archeological middens. Holocene 19(8):1139–1151
Monson DH, Udevitz MS, Jay CV (2013) Estimating age ratios and size of Pacific walrus herds on coastal haulouts using video imaging. PLoS ONE 8:1–12
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 90:335–348
Newsome SD, Tinker MT, Monson DH, Oftedal OT, Ralls K, Staedler MM, Fogel ML, Estes JA (2009) Using stable isotopes to investigate individuals diet specialization in California sea otters (Enhydra lutris nereis). Ecology 90:961–974
Newsome SD, Clementz MT, Koch PL (2010) Using stable isotope biogeochemistry to study marine mammal ecology. Mar Mamm Sci 26(3):509–572
NMFS (2012a) Endangered and threatened species: threaded status for the Arctic, Okhotsk, and Baltic subspecies of the ringed seal and endangered status for the Ladoga subspecies of ringed seal; Final Rule 77(249). December 28 2012. http://www.alaskafisheries.noaa.gov/frules/77fr76740.pdf. Accessed 2 January 2013
NMFS (2012b) Endangered and threatened species: Threaded status for the Beringia and Okhotsk District Distinct Population Segments of the Erignathus barbatus nauticus subspecies of the bearded seal; Final Rule. 77(249). December 28 2012. http://www.alaskafisheries.noaa.gov/frules/77fr76706.pdf. Accessed 2 January 2013
Norrdahl K (1995) Population cycles in northern small mammals. Biol Rev 70:621–637
NSIDC (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 August 2012
Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS One 5:e9672
Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320
Phillips DL, Gregg JW (2001) Uncertainty in source partitioning using stable isotopes. Oecologia 127:171–179
Phillips DL, Newsome SD, Gregg JW (2005) Combining sources in stable isotope mixing models. Oecologia 44:520–527
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 January 2004
Quakenbush L, Citta J, Crawford J (2011a) Biology of the ringed seal (Phoca hispida) in Alaska, 1960–2010. Final report to: National Marine Fisheries Service. Alaska Department of Fish and Game Arctic Marine Mammal Program. March 2011
Quakenbush L, Citta J, Crawford J (2011b) Biology of the bearded seal (Erignathus barbatus) in Alaska, 1961–2009. Final report to: National Marine Fisheries Service. Alaska Department of Fish and Game Arctic Marine Mammal Program. March 2011
Quay PD, Tilbrook B, Wong CS (1992) Oceanic uptake of fossil fuel CO2: carbon-13 evidence. Science 256:74–79
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 93:1247–1251
Ray GC, McCormick-Ray J, Berg P, Epstein HE (2006) Pacific walrus: benthic bioturbator of Beringia. J Exp Mar Biol Ecol 330:403–419
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 362:2151–2168
Schell DM, Saupe SM, Haubenstock N (1989) Bowhead whale (Balaena mysticetus) growth and feeding as estimated by δ13C techniques. Mar Biol 103:433–443
Sheffield G, Grebmeier JM (2009) Pacific walrus (Odobenus rosmarus divergens): differential prey digestion and diet. Mar Mamm Sci 25:761–777
Sheffield G, Fay FH, Feder H, Kelly BP (2001) Laboratory digestion of prey and interpretation of walrus stomach contents. Mar Mamm Sci 17:310–330
Søreide JE, Hop H, Carroll ML, Falk-Petersen S, Hegset EN (2006) Seasonal food web structures and sympagic-pelagic coupling in the European Arctic revealed by stable isotopes and a two-source food web model. Prog Oceanogr 71:59–87
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 20:1395–1399
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
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 57:32–37
USFWS (2011) 12-month finding on a petition to list the Pacific walrus as endangered or threatened; Proposed Rule. Federal Register 75(28). February 10 2011. http://www.gpo.gov/fdsys/pkg/FR-2011-02-10/pdf/2011-2400.pdf. Accessed 2 January 2012
Weslawski JM, Kendall MA, Wlodarska-Kowalczuk M, Iken K, Kedra M, Legezynska J, Seir MK (2011) Climate change effects on Arctic fjord and coastal macrobenthic biodiversity-observations and predictions. Mar Biodivers 41:71–85
Wolkers H, van Bavel B, Ericson I, Skoglund E, Kovacs KM, Lydersen C (2006) Congener-specific accumulation and patters of chlorinated and brominated contaminants in adult male walruses from Svalbard, Norway: indications for individual-specific prey selection. Sci Total Environ 370:70–79
Woodroffe R, Lindsey PA, Romanach SS, Ole Ranah SMK (2007) African wild dogs (Lycaon pictus) can subsist on small prey: implications for conservation. J Mammal 88:181–193
Zhao L, Schell DM (2004) Stable isotope ratios in harbor seal Phoca vitulina vibrissae: effects of growth patterns on ecological records. Mar Ecol Prog Ser 281:267–273
Acknowledgments
The authors 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. They gratefully acknowledge the U.S. Fish and Wildlife Service, and North Slope Borough Department of Wildlife Management for logistical coordination, particularly B. Adams, J. Garlich-Miller, C. George, C. Hanns, G. Krafsur, C. Nayakik, Sr., T. Sformo and J. Snyder. The authors further thank the University of Alaska Fairbanks Museum of the North for providing archived walrus tissue (Loan #2010.006.Mamm), the Togiak National Wildlife Refuge for sharing samples from the 2009 Cape Peirce mortality event, Dr. K. Iken for providing Serripes spp. stable isotope ratios utilized in the mixing model, and the staff of the Alaska Stable Isotope Facility, particularly T. Howe and N. Haubenstock. They are indebted to B. Gaglioti for many hours spent preparing whisker samples for isotope analysis. Statistical analyses were guided by the suggestions of A. Blanchard, UAF. 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). The authors are appreciative of the comments by G. Sheffield, Dr. S. Atkinson, Dr. P. Barboza, Dr. D. Piepenburg, and two anonymous reviewers, which greatly improved this manuscript.
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Seymour, J., Horstmann-Dehn, L. & Wooller, M.J. Inter-annual variability in the proportional contribution of higher trophic levels to the diet of Pacific walruses. Polar Biol 37, 597–609 (2014). https://doi.org/10.1007/s00300-014-1460-7
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DOI: https://doi.org/10.1007/s00300-014-1460-7