Diet of the brown bear in Himalaya: Combining classical and molecular genetic techniques

Autoři: Muhammad Ali Nawaz aff001;  Alice Valentini aff005;  Noor Kamal Khan aff003;  Christian Miquel aff005;  Pierre Taberlet aff005;  Jon E. Swenson aff002
Působiště autorů: Department of Animal Sciences, Quaid-i-Azam University, Islamabad, Pakistan aff001;  Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, Norway aff002;  Himalayan Wildlife Foundation, Islamabad, Pakistan aff003;  Norwegian Institute for Nature Research, Trondheim, Norway aff004;  Laboratoire d'Ecologie Alpine, Université Joseph Fourier, France aff005;  Dipartimento di Ecologia e Sviluppo Economico Sostenibile, Università degli Studi della Tuscia, Viterbo, Italy aff006
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article


The ecological requirements of brown bears are poorly known in the Himalaya region, which complicates conservation efforts. We documented the diet of the Himalayan brown bear (Ursus arctos isabellinus) by combining classical scat analysis and a newly developed molecular genetic technique (the trnL approach), in Deosai National Park, Pakistan. Brown bears consumed over 50 plant species, invertebrates, ungulates, and several rodents. Eight plant families; Poaceae, Polygonaceae, Cyperaceae, Apiaceae, Asteraceae, Caryophyllaceae, Lamiaceae, and Rubiaceae were commonly eaten with graminoids comprising the bulk of the diet. Golden marmots comprised the major mammalian biomass in the park, and were also the main meat source for bears. Animal matter, making 36% of dietary content, contributed half of the digestible energy, due to its higher nutritious value. We did not find a significant temporal pattern in diet, perhaps because the availability of the major diet (graminoids) did not change over the foraging period. Male brown bears were more carnivorous than females, probably because of their larger size, which requires higher energy and also makes them more efficient in capturing marmots. Frequencies of three plant species were also significantly higher in male brown bears; Bistorta affinis, Carex diluta, and Carex sp. Diet of the brown bear differed significantly between the park and surrounding valleys. In valleys, diet consisted predominantly of graminoids and crops, whereas the park provided more nutritious and diverse foodThe estimated digestible energy available to brown bears in Deosai was the lowest documented among brown bear populations, due to the lack of fruits and a relatively lower meat content. The low nutritious diet and high cost of metabolism in a high-altitude environment, probably explains the very low reproductive potential of this population.

Klíčová slova:

Bears – Diet – Plants – Poaceae – Rodents – Sequence databases – Trophic interactions – Valleys


1. Robbins CT. Wildlife feeding and nutrition. Academic Press; 1993.

2. Sih A. Effects of ecological interaction on forager diets: competition, predation risk, parasitism, and prey behavior., Pp. 182–211 in Diet selection an interdisplinary approach to foraging behavior. John Wiley & Sons; 2009.

3. Robbins CT, Schwartz CC, Felicetti LA. Nutritional ecology of ursids: a review of newer methods and management implications. Ursus. 2004;15: 161–171. doi: 10.2192/1537-6176(2004)015<0161:neouar>;2

4. Hamer D, Herrero S. Grizzly Bear Food and Habitat in the Front Ranges of Banff National Park, Alberta. Bears Their Biol Manag. 1987;7: 199. doi: 10.2307/3872626

5. McLellan BN, Hovey FW. The diet of grizzly bears in the Flathead River drainage of southeastern British Columbia. Can J Zool. 1995;73: 704–712. doi: 10.1139/z95-082

6. Mealey SP. The natural food habits of grizzly bears in Yellowstone National Park, 1973–74. 1980. pp. 281–292.

7. Clevenger AP, Purroy FJ, Pelton MR. Food Habits of Brown Bears (Ursus arctos) in the Cantabrian Mountains, Spain. J Mammal. 1992;73: 415–421. doi: 10.2307/1382077

8. Dahle B, Sørensen OJ, Wedul EH, Swenson JE, Sandegren F. The diet of brown bears (Ursus arctos) in central Scandinavia: effect of access to free-ranging domestic sheep Ovis aries. Wildlife Biol. 1998;4: 147–158. doi: 10.2981/wlb.1998.017

9. Schwartz C, Miller S, Haroldson M. Grizzly bear, Pp. 556–586 in Wild mammals of North America: biology, management, and conservation. ( Feldamer GA, Thompson BC and Chapman JA., eds.). Johns Hopkins University Press; 2003.

10. Craighead JJ, Sumner JS, Mitchell JA. The Grizzly bears of Yellowstone: their ecology in the yellowstone ecosystem 1959–1992. Washington, D.C.: Island Press; 1995.

11. Lefranc MNJ, Moss MB, Patnode KA, Sugg WCI. Grizzly bear compendium. Washington, D.C.; 1987.

12. Nomura F, Higashi S. Effects of food distribution on the habitat usage of a female brown bear Ursus arctos yesoensis in a beech-forest zone of northernmost Japan. Ecol Res. 2000;15: 209–217. doi: 10.1046/j.1440-1703.2000.00342.x

13. Ohdachi SAT. Food habits of brown bears in Hokkaido, Japan. 7th International Conference on Bear Research and Management. International Bear Association; 1987. pp. 215–220.

14. Xu A, Jiang Z., Li C, Guo J, Wu G., Cai P. Summer food habits of brown bears in Kekexili Nature Reserve. Ursus. 2006;17: 132–137.

15. Robbins CT, Fortin JK, Rode KD, Farley SD, Shipley LA, Felicetti LA. Optimizing protein intake as a foraging strategy to maximize mass gain in an omnivore. Oikos. 2007;116: 1675–1682. doi: 10.1111/j.0030-1299.2007.16140.x

16. Nawaz MA. Status of the brown bear in Pakistan. Ursus. 2007;18: 89–100.

17. Bunnell FL, Tait DEN. Population dynamics of bears __ implications. In: Fowler CW, Smith TD, editors. Dynamics of large mammal populations. New York: John Wiley and Sons; 1981. pp. 75–98.

18. Nawaz MA, Swenson JE, Zakaria V. Pragmatic management increases a flagship species, the Himalayan brown bears, in Pakistan’s Deosai National Park. Biol Conserv. 2008;141: 2230–2241. doi: 10.1016/j.biocon.2008.06.012

19. Hilderbrand G V, Jacoby ME, Schwartz CC, Arthur SM, Robbins CT, Hanley TA, et al. The importance of meat, particularly salmon, to body size, population productivity, and conservation of North American brown bears. Can J Zool. 1999;77: 132–138.

20. Jonkel CJ, Cowan IM. The Black Bear in the Spruce-Fir Forest. Wildlife Monographs. WileyWildlife Society; pp. 3–57. doi: 10.2307/3830521

21. Rogers LL. Effects of food supply and kinship on social behavior, movements, and population growth of black bears in northeastern Minnesota. Wildl Monogr. 1987;97: 1–72. doi: 10.2307/3830545

22. Schwartz CC, Franzmann AW. Interrelationship of Black Bears to Moose and Forest Succession in the Northern Coniferous Forest. Wildlife Monographs. WileyWildlife Society; pp. 3–58. doi: 10.2307/3830725

23. Stringham SF. Grizzly Bear Reproductive Rate Relative to Body Size. Bears Their Biol Manag. 1990;8: 433. doi: 10.2307/3872948

24. Ferguson SH, McLoughlin PD. Effect of Energy Availability, Seasonality, and Geographic Range on Brown Bear Life History. Ecography. WileyNordic Society Oikos; pp. 193–200. doi: 10.2307/3683021

25. MacHutchon AG, Wellwood DW. Grizzly bear food habits in the northern Yukon, Canada. Ursus. 2003;14: 225–235. doi: 10.2307/3873022

26. Welch CA, Keay J, Kendall KC, Robbins CT. Constraints on frugivory by bears. Ecology. 1997;78: 1105–1119. doi: 10.1890/0012-9658(1997)078[1105:COFBB]2.0.CO;2

27. Mattson DJ. Causes and consequences of dietary differences among Yellowstone grizzly bears (Ursus arctos). University of Idaho. 2000.

28. Case RL, Buckland L. Reproductive characteristics of grizzly bears in the Kugluktuk area, northwest territories, Canada. Ursus. 1998;10: 41–47. doi: 10.2307/3873107

29. Powell RA, Zimmerman JW, Seaman DE ( David E. Ecology and behaviour of North American black bears: home ranges, habitat, and social organization. Chapman & Hall; 1997.

30. Boertje RD, Gasaway WC, Grangaard D V., Kelleyhouse DG. Predation on moose and caribou by radio-collared grizzly bears in east central Alaska. Can J Zool. 1988;66: 2492–2499. doi: 10.1139/z88-369

31. Garshelis DL, Gibeau ML, Herrero S. Grizzly Bear Demographics in and around Banff National Park and Kananaskis Country, Alberta. The Journal of Wildlife Management. WileyWildlife Society; pp. 277–297. doi: 10.2307/3803605

32. Hobson KA, McLellan BN, Woods JG. Using stable carbon (δ 13 C) and nitrogen (δ 15 N) isotopes to infer trophic relationships among black and grizzly bears in the upper Columbia River basin, British Columbia. Can J Zool. 2000;78: 1332–1339. doi: 10.1139/z00-069

33. Jacoby ME, Hilderbrand G V., Servheen C, Schwartz CC, Arthur SM, Hanley TA, et al. Trophic Relations of Brown and Black Bears in Several Western North American Ecosystems. J Wildl Manage. 1999;63: 921. doi: 10.2307/3802806

34. Mattson DJ. Use of ungulates by yellowstone grizzly bears Ursus arctos. Biol Conserv. 1997;81: 161–177. doi: 10.1016/S0006-3207(96)00142-5

35. Nawaz MA, Martin J, Swenson JE. Identifying key habitats to conserve the threatened brown bear in the Himalaya. Biol Conserv. 2014;170: 198–206. doi: 10.1016/j.biocon.2013.12.031

36. Bellemain E, Nawaz MA, Valentini A, Swenson JE, Taberlet P. Genetic tracking of the brown bear in northern Pakistan and implications for conservation. Biol Conserv. 2007;134: 537–547. doi: 10.1016/j.biocon.2006.09.004

37. Nawaz MA, Shah M, Zakaria V. Environmental baseline of Deosai National Park. Draft Report. Islamabad: Himalayan Wildlife Foundation; 2006.

38. Taberlet P, Coissac E, Pompanon F, Gielly L, Miquel C, Valentini A, et al. Power and limitations of the chloroplast trnL (UAA) intron for plant DNA barcoding. Nucleic Acids Res. 2007;35. doi: 10.1093/nar/gkl987

39. Nawaz MA. Ecology, genetics and conservation of Himalayan brown bears. Ecology and Natural Resource Management. Norwegian University of Life Sciences. 2008.

40. Woods C. Biodiversity and conservation of the Deosai Plateau, Northern areas, Pakistan. In Biodiversity of Pakistan. Proceedings of International symposium, Pakistan Museum of Natural History and Florida Museum of Natural History (Gainesville), Islamabad, Pakistan. 1997.

41. Kok OB, Haddad CR, Niekerk VDJ, Butler HJB, Nawaz MA. Invertebrates as a Potential Food Source of Brown Bears on the Deosai Plateau, Northern Pakistan. Pakistan J Biol Sci. 2005;8: 13–19. doi: 10.3923/pjbs.2005.13.19

42. Blumstein DT, Arnold W. Ecology and Social Behavior of Golden Marmots (Marmota caudata aurea). J Mammal. 1998;79: 873. doi: 10.2307/1383095

43. Nawaz MA, Kok OB. Activity patterns of brown bears (Ursus arctos) on the Deosai Plateau, northern Pakistan. Suid-Afrikaanse Tydskr vir Natuurwetenskap en Tegnol. 2004;23: 61–67. doi: 10.4102/satnt.v23i3.194

44. Valentini A, Miquel C, Nawaz MA, Bellemain E, Coissac E, Pompanon F, et al. New perspectives in diet analysis based on DNA barcoding and parallel pyrosequencing: the trnL approach. Mol Ecol Resour. 2009;9: 51–60. doi: 10.1111/j.1755-0998.2008.02352.x 21564566

45. Mattson DJ, Blanchard BM, Knight RR. Food habits of Yellowstone grizzly bears, 1977–1987. Can J Zool. 1991;69: 1619–1629. doi: 10.1139/z91-226

46. Brownstein MJ, Carpten JD, Smith JR. Modulation of non-templated nucleotide addition by Taq DNA polymerase: Primer modifications that facilitate genotyping. Biotechniques. 1996;20: 1004–1010. doi: 10.2144/96206st01 8780871

47. Magnuson VL, Ally DS, Nylund SJ, Karanjawala ZE, Rayman JB, Knapp JI, et al. Substrate nucleotide-determined non-templated addition of adenine by Taq DNA polymerase: Implications for PCR-based genotyping and cloning. Biotechniques. 1996;21: 700–709. doi: 10.2144/96214rr03 8891224

48. Zhang Z, Schwartz S, Wagner L, Miller W. A greedy algorithm for aligning DNA sequences. Journal of Computational Biology. 2000. pp. 203–214. doi: 10.1089/10665270050081478 10890397

49. Hewitt DG, Robbins CT. Estimating Grizzly Bear Food Habits from Fecal Analysis. Wildlife Society Bulletin (1973–2006). WileyWildlife Society; pp. 547–550. doi: 10.2307/3783342

50. Pritchard GT, Robbins CT. Digestive and metabolic efficiencies of grizzly and black bears. Can J Zool. 1990;68: 1645–1651. doi: 10.1139/z90-244

51. Johansen T. The diet of the brown bear (Ursus arctos) in central Sweden. MSc thesis at Norwegian University of Science and Technology, Trondheim,36pp. 1997.

52. Agresti A. Categorical data analysis. Wiley-Interscience; 1996.

53. Krebs JR, McCleery RH. Optimization in Behavioural Ecology. In: Behavioural ecology: an evolutionary approach. Blackwell Scientific Publications; 1991.

54. Manly BFJ, McDonald LL, Thomas DL, McDonald TL, Erickson WP. Resource Selection by Animals: Statistical Design and Analysis for Field Studies. Second. London: Kluwer Academic Publishers; 2002.

55. Deosai Brown Bear Project Final Report. Himalayan Wildlife Foundation Islamabad Pakistan. 1999.

56. Swenson JE, Jansson A, Riig R, Sandegren F. Bears and ants: myrmecophagy by brown bears in central Scandinavia. Can J Zool. 1999;77: 551–561. doi: 10.1139/z99-004

57. White D Jr., Kendall KC, Picton HD. Potential Energetic Effects of Mountain Climbers on Foraging Grizzly Bears. Wildlife Society Bulletin (1973–2006). WileyWildlife Society; pp. 146–151. doi: 10.2307/3783951

58. Cicnjak L, Huber D, Roth HU, Ruff RL, Vinovrski Z. Food Habits of Brown Bears in Plitvice Lakes National Park, Yugoslavia. Bears Their Biol Manag. 1987;7: 221. doi: 10.2307/3872628

59. Clark JD, Clapp DL, Smith KG, Ederington B. Black bear habitat use in relation to food availability in the interior highlands of Arkansas. NCASI Tech Bull. 1999; 89–90. doi: 10.2307/3872716

60. Costello CM, Sage RW. Predicting black bear habitat selection from food abundance under 3 forest management systems. NCASI Tech Bull. 1999; 106. doi: 10.2307/3872724

61. Atwell G, Boone DL, Gustafson J, Berns VD. Brown Bear Summer Use of Alpine Habitat on the Kodiak National Wildlife Refuge. Bears Their Biol Manag. 1980;4: 297. doi: 10.2307/3872884

62. Stevens CE, Hume ID. Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiological Reviews. American Physiological Society; 1998. pp. 393–427. doi: 10.1152/physrev.1998.78.2.393 9562034

63. Van Soest PJ. Nutritional ecology of the ruminant. Ithaca, NY (USA) Cornell Univ. Press; 1994.

64. Davis DD. The giant panda: a morphological study of evolutionary mechanisms / Davis D. Dwight. Chicago, U.S.A.: Chicago Natural History Museum,; 1964. doi: 10.5962/bhl.title.5133

65. Clemens ET, Stevens CE. A comparison of gastrointestinal transit time in ten species of mammal. J Agric Sci. 1980;94: 735–737. doi: 10.1017/S0021859600028732

66. Dierenfeld ES, Hintz HF, Robertson JB, Van Soest PJ, Oftedal OT. Utilization of bamboo by the giant panda. J Nutr. 1982;112: 636–641. doi: 10.1093/jn/112.4.636 6279804

67. Koike S, Kasai S, Yamazaki K, Furubayashi K. Fruit phenology of Prunus jamasakura and the feeding habit of the Asiatic black bear as a seed disperser. Ecol Res. 2008;23: 385–392. doi: 10.1007/s11284-007-0399-3

68. Udén P, Rounsaville TR, Wiggans GR, Van Soest PJ. The measurement of liquid and solid digesta retention in ruminants, equines and rabbits given timothy (Phleum pratense) hay. Br J Nutr. 1982;48: 329–339. doi: 10.1079/bjn19820117 6810917

69. Schenk A, Kovacs KM. Multiple mating between black bears revealed by DNA fingerprinting. Anim Behav. 1995;50: 1483–1490. doi: 10.1016/0003-3472(95)80005-0

70. Steyaert SMJG, Endrestøl A, Hackländer K, Swenson JE, Zedrosser A. The mating system of the brown bear Ursus arctos. Mammal Review. Blackwell Publishing Ltd; 2012. pp. 12–34. doi: 10.1111/j.1365-2907.2011.00184.x

71. Erickson AW, Mossman H.W., Hensel R.J., Troyer W.A. The breeding biology of the male brown bear (Ursus arctos). Zoologica. 1968;53: 85–105.

72. Hamilton AN, Bunnell FL. Foraging Strategies of Coastal Grizzly Bears in the Kimsquit River Valley, British Columbia. Bears Their Biol Manag. 1987;7: 187. doi: 10.2307/3872625

73. Graham DC. Grizzly bear distribution, use of habitats, food habits and habitat characterization in Pelican and Hayden Valleys, Yellowstone National Park (Doctoral dissertation, Montana State University-Bozeman, College of Letters & Science).

74. Nelson RA, Folk GE, Pfeiffer EW, Craighead JJ, Jonkel CJ, Steiger DL. Behavior, Biochemistry, and Hibernation in Black, Grizzly, and Polar Bears. Bears Their Biol Manag. 1983;5: 284. doi: 10.2307/3872551

75. Arnold W. Energetics of Social Hibernation. 1993. pp. 65–80. doi: 10.1201/9780429040931-7

76. Arnold W, Heldmaier G, Ortmann S, Pohl H, Ruf T, Steinlechner S. Ambient temperatures in hibernacula and their energetic consequences for alpine marmots Marmota marmota. J Therm Biol. 1991;16: 223–226. doi: 10.1016/0306-4565(91)90029-2

77. Westerterp KR, Kayser B. Body mass regulation at altitude. European Journal of Gastroenterology and Hepatology. 2006. pp. 1–3. doi: 10.1097/00042737-200601000-00001 16357611

78. Hamad N, Travis SPL. Weight loss at high altitude: Pathophysiology and practical implications. Eur J Gastroenterol Hepatol. 2006;18: 5–10. doi: 10.1097/00042737-200601000-00002 16357612

79. Reynolds H V., Garner GW, Reynolds H V. Patterns of Grizzly Bear Predation on Caribou in Northern Alaska. Bears Their Biol Manag. 1987;7: 59. doi: 10.2307/3872608

80. Kendall KC. Use of Pine Nuts by Grizzly and Black Bears in the Yellowstone Area. Bears Their Biol Manag. 1983;5: 166. doi: 10.2307/3872534

81. Fortin JK, Farley SD, Rode KD, Robbins CT. Dietary and spatial overlap between sympatric ursids relative to salmon use. Ursus. 2007;18: 19–29. doi: 10.2192/1537-6176(2007)18[19:dasobs];2

82. Schaller GB. Wildlife of the Tibetan steppe. University of Chicago Press; 1998.

83. Galbreath GJ, Groves CP, Waits LP. Genetic resolution of composition and phylogenetic placement of the Isabelline Bear. Available:

84. Schaller GB. Mountain Monarchs. Wild sheep and goats of the Himalaya. Chicago and London: The University of Chicago Press; 1977.

85. Vaisfeld MA, Chestin IE. Bears: distribution, ecology, use and protection. in Game animals of Russia and adjacent countries and their environment. Russ Acad Sci World Soc Prot Anim Moscow; 1993.

86. Sæther BE, Engen S, Swenson JE, Bakke Ø, Sandegren F, Saether B-E, et al. Assessing the Viability of Scandinavian Brown Bear, Ursus arctos, Populations: The Effects of Uncertain Parameter Estimates. Oikos. 1998;83: 403. doi: 10.2307/3546856

87. Persson IL, Wikan S, Swenson JE, Mysterud I. The diet of the brown bear Ursus arctos in the Pasvik Valley, northeastern Norway. Wildlife Biol. 2001;7: 27–37. doi: 10.2981/wlb.2001.006

88. Elgmork K, Kaasa J. Food Habits and Foraging of the Brown Bear Ursus arctos in Central South Norway. Ecography. WileyNordic Society Oikos; pp. 101–110. doi: 10.2307/3682968

89. Naves J, Ferna A, Rodri C, Delibes M, Uría R. Brown bear food habits at the border of its range: a long-term study. J Mammal. 2006;87: 899–908. Available:

90. Mclellan B. Density-dependent population regulation in brown bears. in Density dependant population regulation of black, brown and Polar bears ( Taylor M., ed.). International Association for Bear Research and Management, Missoula, Montana, USA; 1994.

91. Munro RHM, Nielsen SE, Price MH, Stenhouse GB, Boyce MS. Seasonal and diel patterns of grizzly bear diet and activity in west-central alberta. J Mammal. 2006;87: 1112–1121. doi: 10.1644/05-mamm-a-410r3.1

92. McLellan BN. Dynamics of a grizzly bear population during a period of industrial resource extraction. I. Density and age-sex composition. Can J Zool. 1989;67: 1856–1860. doi: 10.1139/z89-264

93. Schwartz CC, Haroldson MA, White GC, Harris RB, Cherry S, Keating KA, et al. Temporal, spatial, and environmental influences on the demographics of grizzly bears in the Greater Yellowstone Ecosystem. Wildl Monogr. 2006;161.

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