Advertisement

Polar Biology

, Volume 42, Issue 8, pp 1581–1593 | Cite as

Space use patterns affect stable isotopes of polar bears (Ursus maritimus) in the Beaufort Sea

  • Nicole P. BoucherEmail author
  • Andrew E. Derocher
  • Evan S. Richardson
Original Paper

Abstract

Space use patterns vary within a population and can influence diet composition of individuals. Within the Beaufort Sea, polar bears (Ursus maritimus) either use offshore areas and follow sea ice retreat (pelagic) or utilize nearshore areas (coastal), exposing individuals to different food sources. We examine the relationship between coastal and pelagic space use patterns and diet quantified by stable isotopes (δ15N and δ13C) of polar bears in the Beaufort Sea between 2007 and 2011. We examined spatial fidelity using home range overlap and assigned bears to one of two space use patterns (coastal or pelagic) based on proximity of home ranges to the coast. We estimated diet composition using inter- and intratissue variability in stable isotopes from hair and claws to examine seasonal shifts in diet. Sectioning of claws provided additional insights on diet, but guard hair sections did not. Polar bears showed spatial fidelity between years. Nitrogen stable isotopes were related to space use patterns. Coastal bears were 15N-depleted compared to pelagic bears due to coastal bears being enriched in 15N possibly from either scavenging on bowhead whale carcasses (Balaena mysticetus) killed during subsistence hunts or pelagic bears being nutritionally stressed. Although upper trophic level predators can provide insight into trophic dynamics and changes in ecosystem function, knowledge of space use patterns and foraging behavior is an important aspect of diet interpretation.

Keywords

Space use Stable isotopes Beaufort sea Polar bears Ursus maritimus 

Notes

Acknowledgements

We gratefully acknowledge support from Banrock Station Environmental Fund, Canadian Association of Zoos and Aquariums, Canadian Wildlife Federation, Environment and Climate Change Canada, Hauser Bears, Natural Sciences and Engineering Research Council of Canada, Polar Bears International, Polar Continental Shelf Project of Natural Resources Canada, Quark Expeditions Ltd., United States Department of the Interior (Bureau of Ocean Energy Management), Kansas City Zoo, and World Wildlife Fund Canada.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest to disclose.

Human and animal rights

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

References

  1. Amstrup SC (2003) Polar bear, Ursus maritimus. In: Feldhamer GA, Thompson BC, Chapman JA (eds) Wild mammals of North America: biology, management, and conservation. John Hopkins University Press, Baltimore, pp 587–610, pp 587–610Google Scholar
  2. Arrigo KR, van Dijken GL (2004) Annual cycles of sea ice and phytoplankton in Cape Bathurst polynya, southeastern Beaufort Sea. Canadian Arctic. Geophys Res Lett 31:L08304Google Scholar
  3. Atwood TC, Peacock E, McKinney MA, Lillie K, Wilson R, Douglas DC, Miller S, Terletzky P (2016) Rapid environmental change drives increased land use by an Arctic marine predator. PLoS ONE 11:e0155932Google Scholar
  4. Bauchinger U, Keil J, McKinney RA, Starck JM, McWilliams SR (2010) Exposure to cold but not exercise increases carbon turnover rates in specific tissues of a passerine. J Exp Biol 213:526–534Google Scholar
  5. Belant JL, Kielland K, Follmann EH, Adam LG (2006) Interspecific resource partitioning in sympatric ursids. Ecol Appl 16:2333–2343Google Scholar
  6. Bentzen TW (2006) Winter feeding ecology and biomagnification of organochlorine contaminants in Alaskan polar bears. Dissertation, University of Alaska FairbanksGoogle Scholar
  7. Bentzen TW, Follmann EH, Amstrup SC, York GS, Wooller MJ, O’Hara TM (2007) Variation in winter diet of southern Beaufort Sea polar bears inferred from stable isotope analysis. Can J Zool 85:596–608Google Scholar
  8. Blix AS, Lentfer JW (1979) Modes of thermal protection in polar bear cubs–at birth and on emergence from the den. Am J Physiol 236:R67–74Google Scholar
  9. Bluhm BA, Gradinger R (2008) Regional variability in food availability for Arctic marine mammals. Ecol Appl 18:S77–S96Google Scholar
  10. Bond AL, Diamond AW (2011) Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecol Appl 21:1017–1023Google Scholar
  11. Braham HW, Fraker MA, Krogman BD (1980) Spring migration of the western Arctic population of bowhead whales. Mar Fish Rev 42:36–46Google Scholar
  12. Bromaghin JF, McDonald TL, Stirling I, Derocher AE, Richardson ES, Regehr EV, Douglas DC, Durner GM, Atwood T, Amstrup SC (2015) Polar bear population dynamics in the southern Beaufort Sea during a period of sea ice decline. Ecol Appl 25:634–651Google Scholar
  13. Brown DR, Sherry TW (2008) Alternative strategies of space use and response to resource change in a wintering migrant songbird. Behav Ecol 19:1314–1325Google Scholar
  14. Burton RK, Koch PL (1999) Isotopic tracking of foraging and long-distance migration in northeastern Pacific pinnipeds. Oecologia 119:578–585Google Scholar
  15. Calenge C (2006) The package “adehabitat” for the R software: atool for the analysis of space and habitat use by animals. Ecol Modell 197:516–519Google Scholar
  16. Cardona-Marek T, Knott KK, Meyer BE, O'Hara TM (2009) Mercury concentrations in southern Beaufort Sea polar bears: variation based on stable isotopes of carbon and nitrogen. Environ Toxicol Chem 28:1416–1424Google Scholar
  17. Carleton SA, Kelly L, Anderson-Sprecher R, del Rio CM (2008) Should we use one-, or multi-compartment models to describe 13C incorporation into animal tissues? Rapid Commun Mass Spectrom 22:3008–3014Google Scholar
  18. Carroll SS, Horstmann-Dehn L, Norcross BL (2013) Diet history of ice seals using stable isotope ratios in claw growth bands. Can J Zool 91:191–202Google Scholar
  19. Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443–453Google Scholar
  20. 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 Let 5:830Google Scholar
  21. Cherry SG, Derocher AE, Stirling I, Richardson ES (2009) Fasting physiology of polar bears in relation to environmental change and breeding behavior in the Beaufort Sea. Polar Biol 32:383–391Google Scholar
  22. Cherry SG, Derocher AE, Hobson KA, Stirling I, Thiemann GW (2011) Quantifying dietary pathways of proteins and lipids to tissues of a marine predator. J Appl Ecol 48:373–381Google Scholar
  23. Crawford JA, Quakenbush LT, Citta JJ (2015) A comparison of ringed and bearded seal diet, condition and productivity between historical (1975–1984) and recent (2003–2012) periods in the Alaskan Bering and Chukchi seas. Prog Oceanogr 136:133–150Google Scholar
  24. Dalerum F, Angerbjorn A (2005) Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144:647–658Google Scholar
  25. Dehn LA, Follmann EH, Rosa C, Duffy LK, Thomas DL, Bratton GR, Taylor RJ, O’Hara TM (2006) Stable isotope and trace element status of subsistence-hunted bowhead and beluga whales in Alaska and gray whales in Chukotka. Mar Pollut Bull 52:301–319Google Scholar
  26. Derocher A (2019) Stable isotope values for sectioned claw and guard hair samples from polar bears in the Beaufort Sea, 2007 to 2011. https://doi.org/10.7939/DVN/XBIZIB, UAL Dataverse, DRAFT VERSION
  27. Derocher AE, Stirling I (1990) Distribution of polar bears (Ursus maritimus) during the ice-free period in western Hudson Bay. Can J Zool 68:1395–1403Google Scholar
  28. Derocher AE, Andriashek D, Stirling I (1993) Terrestrial foraging by polar bears during the ice-free period in western Hudson Bay. Arctic 46:251–254Google Scholar
  29. Dunton KH, Schell DM (1987) Dependence of consumers on macroalgal (Laminaria solidungula) carbon in an arctic kelp community: δ13C evidence. Mar Biol 93:615–625Google Scholar
  30. Durner GM, Douglas DC, Nielson RM, Amstrup SC, McDonald TL, Stirling I, Mauritzen M, Born EW, Wiig O, DeWeaver E, Serreze MC, Belikov SE, Holland MM, Maslanik J, Aars J, Bailey DA, Derocher AE (2009) Predicting 21st-century polar bear habitat distribution from global climate models. Ecol Monogr 79:25–58Google Scholar
  31. Durner GM, Douglas DC, Albeke SE, Whiteman JP, Amstrup SC, Richardson E, Wilson RR, Ben-David M (2017) Increased Arctic sea ice drift alters adult female polar bear movements and energetics. Glob Change Biol 23:3460–3473Google Scholar
  32. Edwards MA, Derocher AE, Hobson KA, Branigan M, Nagy JA (2011) Fast carnivores and slow herbivores: differential foraging strategies among grizzly bears in the Canadian Arctic. Oecologia 165:877–889Google Scholar
  33. Ethier DM, Kyle CJ, Kyser TK, Nocera JJ (2010) Variability in the growth patterns of the cornified claw sheath among vertebrates: implications for using biogeochemistry to study animal movement. Can J Zool 88:1043–1051Google Scholar
  34. Ferguson SH, Taylor MK, Born EW, Rosing-Asvid A, Messier F (1999) Determinants of home range size for polar bears (Ursus maritimus). Ecol Lett 2:311–318Google Scholar
  35. Ferreira EO, Loseto LL, Ferguson SH (2011) Assessment of claw growth-layer groups from ringed seals (Pusa hispida) as biomonitors of inter- and intra-annual Hg, δ15N, and δ13C variation. Can J Zool 89:774–784Google Scholar
  36. France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar Ecol Prog Ser 124:307–312Google Scholar
  37. Freitas C, Kovacs KM, Ims RA, Fedak MA, Lydersen C (2008) Ringed seal post-moulting movement tactics and habitat selection. Oecol 155:193–204Google Scholar
  38. Frost KJ, Lowry LF, Pendleton G, Nute HR (2004) Factors affecting the observed densities of ringed seals, Phoca hispida, in the Alaskan Beaufort Sea, 1996–99. Arctic 57:115–128Google Scholar
  39. Galley RJ, Key E, Barber DG, Hwang BJ, Ehn JK (2008) Spatial and temporal variability of sea ice in the southern Beaufort Sea and Amundsen Gulf: 1980–2004. J Geophys Res Oceans 113:C05S95Google Scholar
  40. Galley RJ, Babb D, Ogi M, Else BGT, Geilfus NX, Crabeck O, Barber DG, Rysgaard S (2016) Replacement of multiyear sea ice and changes in the open water season duration in the Beaufort Sea since 2004. J Geophys Res Oceans 121:1806–1823Google Scholar
  41. Goericke R, Fry B (1994) Variations of marine plankton δ13C with latitude, temperature, and dissolved CO2 in the world ocean. Glob Biogeochem Cycles 8:85–90Google Scholar
  42. Goering J, Alexander V, Haubenstock N (1990) Seasonal variability of stable carbon and nitrogen isotope ratios of organisms in a North Pacific Bay. Estuar Coast Shelf Sci 30:239–260Google Scholar
  43. Hansen DJ (2004) Observations of habitat use by polar bears, Ursus maritimus, in the Alaskan Beaufort, Chukchi, and northern Bering Seas. Can Field-Nat 118:395–399Google Scholar
  44. Harwood LA, Stirling I (1992) Distribution of ringed seals in the southeastern Beaufort Sea during late summer. Can J Zool 70:891–900Google Scholar
  45. Hénaux V, Powell LA, Hobson KA, Nielsen CK, LaRue MA (2011) Tracking large carnivore dispersal using isotopic clues in claws: an application to cougars across the Great Plains. Methods Ecol Evol 2:489–499Google Scholar
  46. Herreman J, Peacock E (2013) Polar bear use of a persistent food subsidy: insights from non-invasive genetic sampling in Alaska. Ursus 24:148–163Google Scholar
  47. Hertz E, Trudel M, Cox MK, Mazumder A (2015) Effects of fasting and nutritional restriction on the isotopic ratios of nitrogen and carbon: a meta-analysis. Ecol Evol 5:4829–4839Google Scholar
  48. Hilderbrand GV, Farley SD, Robbins CT, Hanley TA, Titus K, Servheen C (1996) Use of stable isotopes to determine diets of living and extinct bears. Can J Zool 74:2080–2088Google Scholar
  49. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94:181–188Google Scholar
  50. Hobson KA, Alisauskas RT, Clark RG (1993) Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. Condor 95:388–394Google Scholar
  51. 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 53:528–533Google Scholar
  52. Hobson KA, Stirling I, Andriashek DS (2009) Isotopic homogeneity of breath CO2 from fasting and berry-eating polar bears: implications for tracing reliance on terrestrial foods in a changing Arctic. Can J Zool 87:50–55Google Scholar
  53. 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 80:223–231Google Scholar
  54. Holladay BA (1988) Identification of polar bear stocks in the Chukchi and Beaufort Seas through the use of carbon isotope ratios. Dissertation, University of Alaska FairbanksGoogle Scholar
  55. Ji R, Jin M, Varpe Ø (2013) Sea ice phenology and timing of primary production pulses in the Arctic Ocean. Glob Change Biol 19:734–741Google Scholar
  56. Kingsley MCS, Stirling I, Calvert W (1985) The distribution and abundance of seals in the Canadian High Arctic, 1980–82. Can J Fish Aquat Sci 42:1189–1210Google Scholar
  57. Kolts JM, Lovvorn JR, North CA, Grebmeier JM, Cooper LW (2013) Relative value of stomach contents, stable isotopes, and fatty acids as diet indicators for a dominant invertebrate predator (Chionoecetes opilio) in the northern Bering Sea. J Exp Mar Biol Ecol 449:274–283Google Scholar
  58. Kotler BP, Blaustein L (1995) Titrating food and safety in a heterogeneous environment: when are the risky and safe patches of equal value? Oikos 74:251–258Google Scholar
  59. Laidre KL, Stirling I, Lowry LF, Wiig O, Heide-Jorgensen MP, Ferguson SH (2008) Quantifying the sensitivity of Arctic marine mammals to climate-induced habitat change. Ecol Appl 18:S97–125Google Scholar
  60. Laidre KL, Stirling I, Estes JA, Kochnev A, Roberts J (2018) Historical and potential future importance of large whales as food for polar bears. Front Ecol Environ 16:515–524Google Scholar
  61. Latour PB (1981) Spatial relationships and behavior of polar bears (Ursus maritimus Phipps) concentrated on land during the ice-free season of Hudson Bay. Can J Zool 59:1763–1774Google Scholar
  62. Lowry LF, Frost KJ, Burns JJ (1980) Variability in the diet of ringed seals, Phoca hispida, in Alaska. Can J Fish Aquat Sci 37:2254–2261Google Scholar
  63. Lowry LF, Frost KJ, Davis R, DeMaster DP, Suydam RS (1998) Movements and behavior of satellite-tagged spotted seals (Phoca largha) in the Bering and Chukchi Seas. Polar Biol 19:221–230Google Scholar
  64. Lowry LF, Sheffield G, George JC (2004) Bowhead whale feeding in the Alaskan Beaufort Sea, based on stomach contents analyses. J Cetacean Res Manag 6:215–223Google Scholar
  65. Lunn NJ, Stirling I (1985) The significance of supplemental food to polar bears during the ice-free period of Hudson Bay. Can J Zool 63:2291–2297Google Scholar
  66. Marshall JD, Brooks JR, Lajtha K (2007) Sources of variation in the stable isotopic composition of plants. In: Michener RH, Lajtha K (eds) Stable isotopes in ecology and environmental science. Blackwell Publishing Ltd, Malden, MA, pp 22–60Google Scholar
  67. Mauchly JW (1940) Significance test for sphericity of a normal n-variate distribution. Ann Math Statist 11:204–209Google Scholar
  68. Mauritzen M, Derocher AE, Wiig O (2001) Space-use strategies of female polar bears in a dynamic sea ice habitat. Can J Zool 79:1704–1713Google Scholar
  69. Mauritzen M, Belikov SE, Boltunov AN, Derocher AE, Hansen E, Ims RA, Wiig Ø, Yoccoz N (2003a) Functional responses in polar bear habitat selection. Oikos 100:112–124Google Scholar
  70. Mauritzen M, Derocher AE, Pavlova O, Wiig O (2003b) Female polar bears, Ursus maritimus, on the Barents Sea drift ice: walking the treadmill. Anim Behav 66:107–113Google Scholar
  71. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140Google Scholar
  72. Monnett C, Gleason JS (2006) Observations of mortality associated with extended open-water swimming by polar bears in the Alaskan Beaufort Sea. Polar Biol 29:681–687Google Scholar
  73. Pilfold NW, Derocher AE, Richardson E (2014a) Influence of intraspecific competition on the distribution of a wide-ranging, non-territorial carnivore. Glob Ecol Biogeogr 23:425–435Google Scholar
  74. Pilfold NW, Derocher AE, Stirling I, Richardson E (2014b) Polar bear predatory behaviour reveals seascape distribution of ringed seal lairs. Popul Ecol 56:129–138Google Scholar
  75. Pilfold NW, Derocher AE, Stirling I, Richardson E (2015) Multi-temporal factors influence predation for polar bears in a changing climate. Oikos 124:1098–1107Google Scholar
  76. Pilfold NW, McCall A, Derocher AE, Lunn NJ, Richardson E (2017) Migratory response of polar bears to sea ice loss: to swim or not to swim. Ecography 40:189–199Google Scholar
  77. Pongracz JD, Derocher AE (2017) Summer refugia of polar bears (Ursus maritimus) in the southern Beaufort Sea. Polar Biol 40:1–11Google Scholar
  78. Pyke GH, Pulliam HR, Charnov EL (1977) Optimal foraging: a selective review of theory and tests. Q Rev Biol 52:137–154Google Scholar
  79. R Core Development Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  80. Ramsay MA, Hobson KA (1991) Polar bears make little use of terrestrial food webs - evidence from stable-carbon isotope analysis. Oecol 86:598–600Google Scholar
  81. Robbins CT, Lopez-Alfaro C, Rode KD, Toien O, Nelson OL (2012) Hibernation and seasonal fasting in bears: the energetic costs and consequences for polar bears. J Mammal 93:1493–1503Google Scholar
  82. Rode KD, Robbins CT, Nelson L, Amstrup SC (2015) Can polar bears use terrestrial foods to offset lost ice-based hunting opportunities? Front Ecol Environ 13:138–145Google Scholar
  83. Rode KD, Wilson RR, Douglas DC, Muhlenbruch V, Atwood TC, Regehr EV, Richardson ES, Pilfold NW, Derocher AE, Durner GM, Stirling I, Amstrup SC, St. Martin M, Pagano AM, Simac K, (2018) Spring fasting behavior in a marine apex predator provides an index of ecosystem productivity. Glob Change Biol 24:410–423Google Scholar
  84. Rogers MC, Peacock E, Simac K, O’Dell MB, Welker JM (2015) Diet of female polar bears in the southern Beaufort Sea of Alaska: evidence for an emerging alternative foraging strategy in response to environmental change. Polar Biol 38:1035–1047Google Scholar
  85. Rubenstein DR, Hobson KA (2004) From birds to butterflies: animal movement patterns and stable isotopes. Trends Ecol Evol 19:256–263Google Scholar
  86. Russell RH (1975) The food habits of polar bears of James Bay and Southwest Hudson Bay in summer and autumn. Arctic 28:117–129Google Scholar
  87. Saupe SM, Schell DM, Griffiths WB (1989) Carbon-isotope ratio gradients in western arctic zooplankton. Mar Biol 103:427–432Google Scholar
  88. Schell DM, Saupe SM, Haubenstock N (1989) Bowhead whale (Balaena mysticetus) growth and feeding as estimated by δ13C techniques. Mar Biol 103:433–443Google Scholar
  89. Schliebe S, Rode KD, Gleason JS, Wilder J, Proffitt K, Evans TJ, Miller S (2008) Effects of sea ice extent and food availability on spatial and temporal distribution of polar bears during the fall open-water period in the Southern Beaufort Sea. Polar Biol 31:999–1010Google Scholar
  90. Schwertl M, Auerswald K, Schnyder H (2003) Reconstruction of the isotopic history of animal diets by hair segmental analysis. Rapid Commun Mass Spectrom 17:1312–1318Google Scholar
  91. Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611Google Scholar
  92. Smith TG (1980) Polar bear predation of ringed and bearded seals in the land-fast sea ice habitat. Can J Zool 58:2201–2209Google Scholar
  93. Smith AE, Hill MRJ (1996) Polar bear, Ursus maritimus, depredation of Canada goose, Branta canadensis, nests. Can Field-Nat 110:339–340Google Scholar
  94. Stempniewicz L (2006) Polar bear predatory behaviour toward molting barnacle geese and nesting glaucous gulls on Spitsbergen. Arctic 59:247–251Google Scholar
  95. Stern HL, Laidre KL (2016) Sea-ice indicators of polar bear habitat. Cryosphere 10:2027Google Scholar
  96. Stirling I, Archibald WR (1977) Aspects of predation of seals by polar bears. J Fish Res Board Can 34:1126–1129Google Scholar
  97. Stirling I, Archibald WR, DeMaster D (1977) Distribution and abundance of seals in the eastern Beaufort Sea. J Fish Res Board Can 34:976–988Google Scholar
  98. Stirling I, Spencer C, Andriashek D (1989) Immobilization of polar bears (Ursus maritimus) with Telazol in the Canadian Arctic. J Wildl Dis 25:159–168Google Scholar
  99. Stirling I, Andriashek D, Calvert W (1993) Habitat preferences of polar bears in the western Canadian Arctic in late winter and spring. Polar Rec 29:13–24Google Scholar
  100. Stirling I, Øritsland NA (1995) Relationships between estimates of ringed seal (Phoca hispida) and polar bear (Ursus maritimus) populations in the Canadian Arctic. Can J Fish Aquat Sci 52:2594–2612Google Scholar
  101. Stock BC, Semmens BX (2016) MixSIAR GUI user manual. Version 3.1. https://github.com/brianstock/MixSIAR. Accessed 21 Sep, 2018
  102. Sullivan JC, Buscetta KJ, Michener RH, Whitaker JO, Finnerty JR, Kunz TH (2006) Models developed from δ13C and δ15N of skin tissue indicate non-specific habitat use by the big brown bat (Eptesicus fuscus). Ecoscience 13:11–22Google Scholar
  103. Thiemann GW, Iverson SJ, Stirling I (2008) Polar bear diets and arctic marine food webs: insights from fatty acid analysis. Ecol Monogr 78:591–613Google Scholar
  104. Toscano BJ, Gownaris NJ, Heerhartz SM, Monaco CJ (2016) Personality, foraging behavior and specialization: integrating behavioral and food web ecology at the individual level. Oecol 182:55–69Google Scholar
  105. Verde M (2005) Canine and feline nail diseases. In: Proceeding of the NAVC North American Veterinary Conference, Orlando, Fla., 8–12 June 2005. North American Veterinary Conference, Gainesville, Fla. Available online from www.ivis.org
  106. Wassmann P, Duarte CM, Agusti S, Sejr MK (2011) Footprints of climate change in the Arctic marine ecosystem. Glob Change Biol 17:1235–1249Google Scholar
  107. Whiteman JP, Harlow HJ, Durner GM, Anderson-Sprecher R, Albeke SE, Regehr EV, Amstrup SC, Ben-David M (2015) Summer declines in activity and body temperature offer polar bears limited energy savings. Science 349:295–298Google Scholar
  108. Whiteman JP, Harlow HJ, Durner GM, Regehr EV, Rourke BC, Robles M, Amstrup SC, Ben-David M (2017) Polar bears experience skeletal muscle atrophy in response to food deprivation and reduced activity in winter and summer. Conserv Physiol 5:cox049Google Scholar
  109. Whiteman JP, Harlow HJ, Durner GM, Regehr EV, Amstrup SC, Ben-David M (2018) Phenotypic plasticity and climate change: can polar bears respond to longer Arctic summers with an adaptive fast? Oecol 186:369–381Google Scholar
  110. Wilson RR, Regehr EV, St. Martin M, Atwood TC, Peacock E, Miller S, Divoky G, (2017) Relative influences of climate change and human activity on the onshore distribution of polar bears. Biol Conserv 214:288–294Google Scholar
  111. Zeppelin TK, Johnson DS, Kuhn CE, Iverson SJ, Ream RR (2015) Stable isotope models predict foraging habitat of northern fur seals (Callorhinus ursinus) in Alaska. PLoS ONE 10:e0127615Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of AlbertaEdmontonCanada
  2. 2.Wildlife Research Division, Science and Technology BranchEnvironment and Climate Change CanadaWinnipegCanada

Personalised recommendations