High-energy, high-fat lifestyle challenges an Arctic apex predator, the polar bear
A demanding lifestyle
Polar bears appear to be well adapted to the extreme conditions of their Arctic habitat. Pagano et al., however, show that the energy balance in this harsh environment is narrower than we might expect (see the Perspective by Whiteman). They monitored the behavior and metabolic rates of nine free-ranging polar bears over 2 years. They found that high energy demands required consumption of high-fat prey, such as seals, which are easy to come by on sea ice but nearly unavailable in ice-free conditions. Thus, as sea ice becomes increasingly short-lived annually, polar bears are likely to experience increasingly stressful conditions and higher mortality rates.
Abstract
Regional declines in polar bear (Ursus maritimus) populations have been attributed to changing sea ice conditions, but with limited information on the causative mechanisms. By simultaneously measuring field metabolic rates, daily activity patterns, body condition, and foraging success of polar bears moving on the spring sea ice, we found that high metabolic rates (1.6 times greater than previously assumed) coupled with low intake of fat-rich marine mammal prey resulted in an energy deficit for more than half of the bears examined. Activity and movement on the sea ice strongly influenced metabolic demands. Consequently, increases in mobility resulting from ongoing and forecasted declines in and fragmentation of sea ice are likely to increase energy demands and may be an important factor explaining observed declines in body condition and survival.
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References and Notes
1
A. Berta, Return to the Sea: The Life and Evolutionary Times of Marine Mammals (University of California Press, 2012).
2
K. L. Laidre, I. Stirling, L. F. Lowry, O. Wiig, M. P. Heide-Jørgensen, S. H. Ferguson, Quantifying the sensitivity of Arctic marine mammals to climate-induced habitat change. Ecol. Appl. 18, S97–S125 (2008).
3
I. Stirling, A. E. Derocher, Factors affecting the evolution and behavioral ecology of the modern bears. Int. Conf. Bear Res. Manag. 8, 189–204 (1990).
4
S. H. Ferguson, M. K. Taylor, E. W. Born, A. Rosing-Asvid, F. Messier, Determinants of home range size for polar bears (Ursus maritimus). Ecol. Lett. 2, 311–318 (1999).
5
A. M. Pagano, G. M. Durner, S. C. Amstrup, K. S. Simac, G. S. York, Long-distance swimming by polar bears (Ursus maritimus) of the southern Beaufort Sea during years of extensive open water. Can. J. Zool. 90, 663–676 (2012).
6
R. J. Hurst, N. A. Øritsland, P. D. Watts, Body mass, temperature and cost of walking in polar bears. Acta Physiol. Scand. 115, 391–395 (1982).
7
B. D. Griffen, Modeling the metabolic costs of swimming in polar bears (Ursus maritimus). Polar Biol. 10.1007/s00300-017-2209-x (2017).
8
I. Stirling, Midsummer observations on the behavior of wild polar bears (Ursus maritimus). Can. J. Zool. 52, 1191–1198 (1974).
9
J. C. Stroeve, T. Markus, L. Boisvert, J. Miller, A. Barrett, Changes in Arctic melt season and implications for sea ice loss. Geophys. Res. Lett. 41, 1216–1225 (2014).
10
I. Stirling, A. E. Derocher, Possible impacts of climatic warming on polar bears. Arctic 46, 240–245 (1993).
11
J. H. Brown, J. F. Gillooly, A. P. Allen, V. M. Savage, G. B. West, Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).
12
R. J. Hurst, M. L. Leonard, P. D. Watts, P. Beckerton, N. A. Øritsland, Polar bear locomotion: Body temperature and energetic cost. Can. J. Zool. 60, 40–44 (1982).
13
I. Stirling, N. A. Øritsland, Relationships between estimates of ringed seal (Phoca hispida) and polar bear (Ursus maritimus) populations in the Canadian Arctic. Can. J. Fish. Aquat. Sci. 52, 2594–2612 (1995).
14
M. C. S. Kingsley, in Ringed Seals in the North Atlantic, M.-P. Heide-Jorgensen, C. Lydersen, Eds. (The North Atlantic Marine Mammal Commission, 1998), vol. 1, pp. 181–196.
15
R. A. Nelson et al., Behavior, biochemistry, and hibernation in black, grizzly, and polar bears. Int. Conf. Bear Res. Manag. 5, 284–290 (1983).
16
S. N. Atkinson, R. A. Nelson, M. A. Ramsay, Changes in the body composition of fasting polar bears (Ursus maritimus): The effect of relative fatness on protein conservation. Physiol. Zool. 69, 304–316 (1996).
17
C. T. Robbins, C. Lopez-Alfaro, K. D. Rode, Ø. Tøien, O. L. Nelson, Hibernation and seasonal fasting in bears: The energetic costs and consequences for polar bears. J. Mammal. 93, 1493–1503 (2012).
18
J. P. Whiteman, H. J. Harlow, G. M. Durner, R. Anderson-Sprecher, S. E. Albeke, E. V. Regehr, S. C. Amstrup, M. Ben-David, Summer declines in activity and body temperature offer polar bears limited energy savings. Science 349, 295–298 (2015).
19
Materials and methods are available as supplementary materials.
20
B. K. McNab, Complications inherent in scaling the basal rate of metabolism in mammals. Q. Rev. Biol. 63, 25–54 (1988).
21
M. Kleiber, The Fire of Life: An Introduction to Animal Energetics (John Wiley & Sons, 1975).
22
R. J. Hurst, thesis, University of Ottawa (1981).
23
P. D. Watts, K. L. Ferguson, B. A. Draper, Energetic output of subadult polar bears (Ursus maritimus): Resting, disturbance and locomotion. Comp. Biochem. Physiol. A. Comp. Physiol. 98, 191–193 (1991).
24
P. D. Watts, N. A. Øritsland, R. J. Hurst, Standard metabolic rate of polar bears under simulated denning conditions. Physiol. Zool. 60, 687–691 (1987).
25
K. A. Nagy, Field metabolic rate and body size. J. Exp. Biol. 208, 1621–1625 (2005).
26
K. A. Nagy, I. A. Girard, T. K. Brown, Energetics of free-ranging mammals, reptiles, and birds. Annu. Rev. Nutr. 19, 247–277 (1999).
27
P. K. Molnár, T. Klanjscek, A. E. Derocher, M. E. Obbard, M. A. Lewis, A body composition model to estimate mammalian energy stores and metabolic rates from body mass and body length, with application to polar bears. J. Exp. Biol. 212, 2313–2323 (2009).
28
S. N. Atkinson, M. A. Ramsay, The effects of prolonged fasting on the body composition and reproductive success of female polar bears (Ursus maritimus). Funct. Ecol. 9, 559–567 (1995).
29
E. Geffen, A. A. Degen, M. Kam, R. Hefner, K. A. Nagy, Daily energy expediture and water flux of free-living Blandford’s foxes (Vulpes cana), a small desert carnivore. J. Anim. Ecol. 61, 611–617 (1992).
30
J. B. Williams, M. D. Anderson, P. R. K. Richardson, Seasonal differences in field-metabolism, water requirements, and foraging behavior of free-living aardwolves. Ecology 78, 2588–2602 (1997).
31
A. E. Derocher, R. A. Nelson, I. Stirling, M. A. Ramsay, Effects of fasting and feeding on serum urea and serum creatinine levels in polar bears. Mar. Mamm. Sci. 6, 196–203 (1990).
32
I. Stirling, C. Spencer, D. Andriashek, Behavior and activity budgets of wild breeding polar bears (Ursus maritimus). Mar. Mamm. Sci. 32, 13–37 (2016).
33
F. Messier, M. K. Taylor, M. A. Ramsay, Seasonal activity patterns of female polar bears (Ursus maritimus) in the Canadian Arctic as revealed by satellite telemetry. J. Zool. (Lond.) 226, 219–229 (1992).
34
S. Paisley, D. L. Garshelis, Activity patterns and time budgets of Andean bears (Tremarctos ornatus) in the Apolobamba Range of Bolivia. J. Zool. (Lond.) 268, 25–34 (2006).
35
D. P. Costa, T. M. Williams, in Biology of Marine Mammals, J. E. Reynolds, S. A. Rommel, Eds. (Smithsonian Institution Press, 1999), pp. 176–217.
36
K. D. Rode, A. M. Pagano, J. F. Bromaghin, T. C. Atwood, G. M. Durner, K. S. Simac, S. C. Amstrup, Effects of capturing and collaring on polar bears: Findings from long-term research on the southern Beaufort Sea population. Wildl. Res. 41, 311–322 (2014).
37
T. M. Williams, J. Haun, R. W. Davis, L. A. Fuiman, S. Kohin, A killer appetite: Metabolic consequences of carnivory in marine mammals. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 129, 785–796 (2001).
38
K. D. Rode, A. M. Pagano, J. F. Bromaghin, T. C. Atwood, G. M. Durner, K. S. Simac, S. C. Amstrup, Spring fasting behavior in a marine apex predator provides an index of ecosystem productivity. Glob. Chang. Biol. 24, 410–423 (2018).
39
G. M. Durner, D. C. Douglas, R. M. Nielson, S. C. Amstrup, T. L. McDonald, I. Stirling, M. Mauritzen, E. W. Born, Ø. Wiig, E. DeWeaver, M. C. Serreze, S. E. Belikov, M. M. Holland, J. Maslanik, J. Aars, D. A. Bailey, A. E. Derocher, Predicting 21st-century polar bear habitat distribution from global climate models. Ecol. Monogr. 79, 25–58 (2009).
40
J. V. Ware, K. D. Rode, J. F. Bromaghin, D. C. Douglas, R. R. Wilson, E. V. Regehr, S. C. Amstrup, G. M. Durner, A. M. Pagano, J. Olson, C. T. Robbins, H. T. Jansen, Habitat degradation affects the summer activity of polar bears. Oecologia 184, 87–99 (2017).
41
I. Stirling, N. J. Lunn, J. Iacozza, Long-term trends in the population ecology of polar bears in western Hudson Bay in relation to climatic change. Arctic 52, 294–306 (1999).
42
J. F. Bromaghin, T. L. Mcdonald, I. Stirling, A. E. Derocher, E. S. Richardson, E. V. Regehr, D. C. Douglas, G. M. Durner, T. Atwood, S. C. Amstrup, Polar bear population dynamics in the southern Beaufort Sea during a period of sea ice decline. Ecol. Appl. 25, 634–651 (2015).
43
G. M. Durner et al., Increased Arctic sea ice drift alters adult female polar bear movements and energetics. Glob. Chang. Biol. 23, 3460–3473 (2017).
44
V. Sahanatien, A. E. Derocher, Monitoring sea ice habitat fragmentation for polar bear conservation. Anim. Conserv. 15, 397–406 (2012).
45
I. Stirling, C. Spencer, D. Andriashek, Immobilization of polar bears (Ursus maritimus) with Telazol in the Canadian Arctic. J. Wildl. Dis. 25, 159–168 (1989).
46
W. Calvert, M. A. Ramsay, Evaluation of age determination of polar bears by counts of cementum growth layer groups. Ursus 10, 449–453 (1998).
47
J. P. Y. Arnould, thesis, University of Saskatchewan (1990).
48
D. Farley, T. Robbins, Development of two methods to estimate body composition of bears. Can. J. Zool. 72, 220–226 (1994).
49
J. R. Speakman, Doubly Labelled Water: Theory and Practice (Chapman and Hall, 1997).
50
G. V. Hilderbrand, S. D. Farley, C. T. Robbins, Predicting body condition of bears via two field methods. J. Wildl. Manage. 62, 406–409 (1998).
51
J. R. Speakman, G. Perez-Camargo, T. McCappin, T. Frankel, P. Thomson, V. Legrand-Defretin, Validation of the doubly-labelled water technique in the domestic dog (Canis familiaris). Br. J. Nutr. 85, 75–87 (2001).
52
C. E. Sparling, D. Thompson, M. A. Fedak, S. L. Gallon, J. R. Speakman, Estimating field metabolic rates of pinnipeds: Doubly labelled water gets the seal of approval. Funct. Ecol. 22, 245–254 (2008).
53
A. J. M. Dalton, D. A. S. Rosen, A. W. Trites, Season and time of day affect the ability of accelerometry and the doubly labeled water methods to measure energy expenditure in northern fur seals (Callorhinus ursinus). J. Exp. Mar. Biol. Ecol. 452, 125–136 (2014).
54
J. P. Whiteman, thesis, University of Wyoming (2014).
55
I. Stirling, E. H. McEwan, The caloric value of whole ringed seals (Phoca hispida) in relation to polar bear (Ursus maritimus) ecology and hunting behavior. Can. J. Zool. 53, 1021–1027 (1975).
56
R. C. Best, Digestibility of ringed seals by the polar bear. Can. J. Zool. 63, 1033–1036 (1985).
57
G. W. Thiemann, S. J. Iverson, I. Stirling, Polar bear diets and arctic marine food webs: Insights from fatty acid analysis. Ecol. Monogr. 78, 591–613 (2008).
58
M. C. Rogers, E. Peacock, K. Simac, M. B. O’Dell, J. M. Welker, 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, 1035–1047 (2015).
59
M. A. McKinney, T. C. Atwood, S. J. Iverson, E. Peacock, Temporal complexity of southern Beaufort Sea polar bear diets during a period of increasing land use. Ecosphere 8, e01633 (2017).
60
R. A. Nelson, T. D. I. Beck, D. L. Steiger, Ratio of serum urea to serum creatinine in wild black bears. Science 226, 841–842 (1984).
61
D. S. Johnson, J. M. London, M.-A. Lea, J. W. Durban, Continuous-time correlated random walk model for animal telemetry data. Ecology 89, 1208–1215 (2008).
62
D. S. Johnson, Crawl: Fit continuous-time correlated random walk models to animal movement data (2016).
63
R Core Team, R: A language and environment for statistical computing (2014); www.r-project.org.
64
J. L. Frair, J. Fieberg, M. Hebblewhite, F. Cagnacci, N. J. DeCesare, L. Pedrotti, Resolving issues of imprecise and habitat-biased locations in ecological analyses using GPS telemetry data. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 2187–2200 (2010).
65
A. M. Pagano, K. D. Rode, A. Cutting, M. A. Owen, S. Jensen, J. V. Ware, C. T. Robbins, G. M. Durner, T. C. Atwood, M. E. Obbard, K. R. Middel, G. W. Thiemann, T. M. Williams, Using tri-axial accelerometers to identify wild polar bear behaviors. Endanger. Species Res. 32, 19–33 (2017).
66
L. Breiman, Random forests. Mach. Learn. 45, 5–32 (2001).
67
H. Wickham, ggplot2: Elegant Graphics for Data Analysis (Springer-Verlag, 2009).
68
D. Kahle, H. Wickham, ggmap: Spatial Visualization with ggplot2. R J. 5, 144–161 (2013).
69
M. W. Hayward, G. J. Hayward, Activity patterns of reintroduced lion Panthera leo and spotted hyaena Crocuta crocuta in the Addo Elephant National Park, South Africa. Afr. J. Ecol. 45, 135–141 (2007).
70
N. L. Mogensen, J. O. Ogutu, T. Dabelsteen, The effects of pastoralism and protection on lion behaviour, demography and space use in the Mara Region of Kenya. Afr. Zool. 46, 78–87 (2011).
71
E. M. Gese, R. L. Ruff, R. L. Crabtree, Foraging ecology of coyotes (Canis latrans): The influence of extrinsic factors and a dominance hierarchy. Can. J. Zool. 74, 769–783 (1996).
72
J. Theuerkauf, W. Jędrzejewski, K. Schmidt, H. Okarma, I. Ruczyński, S. Śnieżko, R. Gula, Daily patterns and duration of wolf activity in the Białowieża forest, Poland. J. Mammal. 84, 243–253 (2003).
73
C. M. Bryce, thesis, University of California, Santa Cruz (2017).
74
J. C. Seidensticker, M. G. Hornocker, W. V. Wiles, J. P. Messick, Mountain lion social organization in the Idaho primitive area. Wildl. Monogr. 35, 3–60 (1973).
75
J. M. Kolowski, D. Katan, K. R. Theis, K. E. Holekamp, Daily patterns of activity in the spotted hyena. J. Mammal. 88, 1017–1028 (2007).
76
P. C. Withers, Measurement of VO2, VCO2, and evaporative water loss with a flow-through mask. J. Appl. Physiol. 42, 120–123 (1977).
77
M. A. Fedak, L. Rome, H. J. Seeherman, One-step N2-dilution technique for calibrating open-circuit VO2 measuring systems. J. Appl. Physiol. 51, 772–776 (1981).
78
P. D. Watts, C. Jonkel, Energetic cost of winter dormancy in grizzly bear. J. Wildl. Manage. 52, 654–656 (1988).
79
Ø. Tøien, J. Blake, D. M. Edgar, D. A. Grahn, H. C. Heller, B. M. Barnes, Hibernation in black bears: Independence of metabolic suppression from body temperature. Science 331, 906–909 (2011).
80
P. Watts, C. Cuyler, Metabolism of the black bear under simulated denning conditions. Acta Physiol. Scand. 134, 149–152 (1988).
81
Y. Fei, R. Hou, J. R. Spotila, F. V. Paladino, D. Qi, Z. Zhang, Metabolic rates of giant pandas inform conservation strategies. Sci. Rep. 6, 27248 (2016).
82
B. K. McNab, Rate of metabolism in the termite-eating sloth bear (Ursus ursinus). J. Mammal. 73, 168–172 (1992).
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Volume 359 | Issue 6375
2 February 2018
2 February 2018
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Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.
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Received: 31 May 2017
Accepted: 19 December 2017
Published in print: 2 February 2018
Acknowledgments
This work was supported by the U.S. Geological Survey’s Changing Arctic Ecosystems Initiative. Additional support was provided by Polar Bears International; the North Pacific Research Board; Washington State University; World Wildlife Fund (Canada); San Diego Zoo Global; SeaWorld and Busch Gardens Conservation Fund; University of California, Santa Cruz; and the International Association for Bear Research and Management. Funding for the resting metabolic study was also provided by a NSF Instrument Development for Biological Research grant 1255913-015 (to T.M.W.). We thank M. Bakhtiari (Exeye) for developing the video collars used in this study. We thank T. Donnelly, K. Simac, and M. Spriggs for assistance in the field. We thank helicopter pilot F. Ross (Soloy Helicopters) for field support. We thank San Diego Zoo polar bear trainers T. Batson, N. Wagner, B. Wolf, and P. O’Neill. We thank members of the T.M.W. laboratory, D. Rizzolo, and B. Lyon for comments on previous drafts of the manuscript. This research used resources of the Core Science Analytics and Synthesis Applied Research Computing program at the U.S. Geological Survey. Data reported in this paper are archived at https://doi.org/10.5066/F7XW4H0P. The authors declare no competing financial interests. Any use of trade, firm, or product names is for descriptive purposes only and does not reflect endorsement by the U.S. government.
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Funding Information
National Science Foundation: 1255913-015
Polar Bears International:
San Diego Zoo Global:
International Association for Bear Research and Management:
North Pacific Research Board:
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