Using fatty acid signatures to study bear foraging: Technical considerations and future applications

Ursus

Volumn 19, Issue 1, 2008, Pages 59-72

  Thiemann, Gregory W ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Diet; Fatty acid; Food webs; Foraging ecology; Grizzly bear; Nutrition; Physiology; Polar bear; Ursus

Indexed keywords

CETACEA; URSUS; URSUS ARCTOS; URSUS MARITIMUS;

EID: 45149118588     PISSN: 15376176     EISSN: None     Source Type: Journal    
DOI: 10.2192/08PER001R.1     Document Type: Article

References (94)

1. ACKMAN, R.G., AND C.A. EATON. 1966. Lipids of the fin whale (Balaenoptera physalus) from North Atlantic waters. III. Occurrence of eicosenoic and docosenoic fatty acids in the Zooplankton Meganyctiphanes norvegica (M. Sars) and their effect on whale oil composition. Canadian Journal of Biochemistry 44:1561-1566.
2. S.N. HOOPER. 1973. Non-methylene-interrupted fatty acids in lipids of shallow-water marine invertebrates: a comparison of two molluscs (Littorina littorea and Lunatia triseriata) with the sand shrimp (Crangon septemspinosus). Comparative Biochemistry and Physiology 46B:153-165.
3. 1989. Fatty acids. Pages 103-137 in R.G. Ackman, editor. Marine biogenic lipids, fats, and oils. CRC Press, Boca Raton, Florida, USA.
4. AITCHISON, J. 1986. The statistical analysis of compositional data. Chapman and Hall, New York, New York, USA.
5. BECK, C.A., S.J. IVERSON, W.D. BOWEN, AND W. BLANCHARD. 2007. Sex differences in grey seal diet reflect seasonal variation in foraging behaviour and reproductive expenditure: evidence from quantitative fatty acid signature analysis. Journal of Animal Ecology 76:490-502.
6. BEEMAN, L.E., AND M.R. PELTON. 1980. Seasonal foods and feeding ecology of black bears in the Smoky Mountains. International Conference on Bear Research and Management 4:141-147.
7. BELLEMAIN, E., J.E. SWENSON, D. TALLMON, S. BRUNBERG, AND P. TABERLET. 2005. Estimating population size of elusive animals with DNA from hunter-collected feces: four methods for brown bears. Conservation Biology 19:150-161.
8. BEN-DAVID, M., K. TITUS, AND L.R. BEIER. 2004. Consumption of salmon by Alaskan brown bears: a trade-off between nutritional requirements and the risk of infanticide? Oecologia 138:465-474.
9. BENTZEN, T.W., E.H. FOLLMANN, S.C. AMSTRUP, G.S. YORK, M.J. WOOLLER, AND T.M. O'HARA. 2007. Variation in winter diet of southern Beaufort Sea polar bears inferred from stable isotope analysis. Canadian Journal of Zoology 85:596-608.
10. 15N). Canadian Journal of Zoology 82:576-586.
11. BOYCE, M.S., AND L.L. MCDONALD. 1999. Relating populations to habitats using resource selection functions. Trends in Ecology & Evolution 14:268-272.
12. BUDGE, S.M., M.H. COOPER, AND S.J. IVERSON. 2004. Demonstration of the deposition and modification of dietary fatty acids in pinniped blubber using radiolabelled precursors. Physiological and Biochemical Zoology 77:682-687.
13. S.J. IVERSON, AND H.N. KOOPMAN. 2006. Studying trophic ecology in marine ecosystems using fatty acids: A primer on analysis and interpretation. Marine Mammal Science 22:759-801.
14. A.M. SPRINGER, S.J. IVERSON, AND G. SHEFFIELD. 2007. Fatty acid biomarkers reveal niche separation in an Arctic benthic food web. Marine Ecology Progress Series 336:305-309.
15. CHRISTIE, W.W. 1973. Lipid analysis: isolation, separation, identification, and structural analysis of lipids. Pergamon Press, Toronto, Ontario, Canada.
16. COOK, H.W. 1991. Fatty acid desaturation and chain elongation in eucaryotes. Pages 141-169 in D.E. Vance and J. Vance, editors. Biochemistry of lipids, lipoproteins and membranes. Elsevier Science Publishers B.V., New York, New York, USA.
17. COOPER, M.H., S.J. IVERSON, AND H. HERAS. 2005. Dynamics of blood chylomicron fatty acids in a marine carnivore: implications for lipid metabolism and quantitative estimation of predator diets. Journal of Comparative Physiology 1756:133-145.
18. DA SILVA, J., AND J.D. NEILSON. 1985. Limitations of using otoliths recovered in scats to estimate prey consumption in seals. Canadian Journal of Fisheries and Aquatic Sciences 42:1439-1442.
19. DEROCHER, A.E., Ø. WIIG, AND M. ANDERSEN. 2002. Diet composition of polar bears in Svalbard and the western Barents Sea. Polar Biology 25:448-452.
20. DOREAU, M., AND A. FERLAY. 1994. Digestion and utilisation of fatty acids by ruminants. Animal Feed Science and Technology 45:379-396.
21. FLORANT, G.L., L.C. NUTTLE, D.E. MULLINEX, AND D.A. RINTOUL. 1990. Plasma and white adipose tissue lipid composition in marmots. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 258:1123-1131.
22. 1998. Lipid metabolism in hibernators: the importance of essential fatty acids. American Zoologist 38:331-340.
23. FOLCH, J., M. LEES, AND G.H. SLOANE STANLEY. 1957. A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry 226:497-509.
24. FORTIN, J.K., S.D. FARLEY, K.D. RODE, AND C.T. ROBBINS. 2007. Dietary and spatial overlap between sympatric ursids relative to salmon use. Ursus 18:19-29.
25. GALLI, C., AND P. RISÉ. 2006. Origin of fatty acids in the body: endogenous synthesis versus dietary intakes. European Journal of Lipid Science and Technology 108:521-525.
26. CANNES, L.Z., D.M. O'BRIEN, AND C.M. DEL RIO. 1997. Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78:1271-1276.
27. GAU, R.J., R. CASE, D.F. PENNER, AND P.D. MCLOUGHLIN. 2002. Feeding patterns of barren-ground grizzly bears in the central Canadian Arctic. Arctic 55:339-344.
28. GENDE, S.M., T.P. QUINN, AND M.F. WILLSON. 2001. Consumption choice by bears feeding on salmon. Oecologia 127:372-382.
29. T.P. QUINN. 2004. The relative importance of prey density and social dominance in determining energy intake by bears feeding on Pacific salmon. Canadian Journal of Zoology 82:75-85.
30. GRAEVE, M., G. KATTNER, AND W. HAGEN. 1994. Diet-induced changes in the fatty acid composition of Arctic herbivorous copepods: Experimental evidence of trophic markers. Journal of Experimental Marine Biology and Ecology 182:97-110.
31. GUNN, A., AND F.L. MILLER. 1982. Muskox bull killed by a barren-ground grizzly bear, Thelon Game Sanctuary, N.W.T. Arctic 35:545-546.
32. HILDERBRAND, G.V., S.D. FARLEY, C.T. ROBBINS, T.A. HANLEY, K. TITUS, AND C. SERVHEEN. 1996. Use of stable isotopes to determine diets of living and extinct bears. Canadian Journal of Zoology 74:2080-2088.
33. T.A. HANLEY, C.T. ROBBINS, AND C.C. SCHWARTZ. 1999a. Role of brown bears (Ursus arctos) in the flow of marine nitrogen into a terrestral ecosystem. Oecologia 121:546-550.
34. S.G. JENKINS, C.C. SCHWARTZ, T.A. HANLEY, AND C.T. ROBBINS. 1999b. Effect of seasonal differences in dietary meat intake on changes in body mass and composition in wild and captive brown bears. Canadian Journal of Zoology 77:1623-1630.
35. HOBSON, K.A., AND I. STIRLING. 1997. Low variation in blood 513C among Hudson Bay polar bears: implications for metabolism and tracing terrestrial foraging. Marine Mammal Science 13:359-367.
36. 15N) isotopes to infer trophic relationships among black and grizzly bears in the upper Columbia River basin, British Columbia. Canadian Journal of Zoology 78:1332-1339.
37. HOLLAND, D.L., J. DAVENPORT, AND J. EAST. 1990. The fatty acid composition of the leatherback turtle Dermochelys coriacea and its jellyfish prey. Journal of the Marine Biological Association of the United Kingdom 70:761-770.
38. IUPAC-IUB COMMISSION ON BIOCHEMICAL NOMENCLATURE. 1967. The nomenclature of lipids. European Journal of Biochemistry 2:127-131.
39. IVERSON, S.J. 1988. Composition, intake and gastric digestion of milk lipids in pinnipeds. Dissertation, University of Maryland, College Park, Maryland, USA.
40. 1993. Milk secretion in marine mammals in relation to foraging: can milk fatty acids predict diet? Symposium of the Zoological Society of London 66:263-291.
41. O.T. OFTEDAL, W.D. BOWEN, D.J. BONESS, AND J. SAMPUGNA. 1995. Prenatal and postnatal transfer of fatty acids from mother to pup in the hooded seal. Journal of Comparative Physiology 165B:1-12.
42. K.J. FROST, AND L.F. LOWRY. 1997. Fatty acid signatures reveal fine scale structure of foraging distribution of harbor seals and their prey in Prince William Sound, Alaska. Marine Ecology Progress Series 151:255-271.
43. S.L.C. LANG, AND M.H. COOPER. 2001b. Comparison of the Bligh and Dyer and Folch methods for total lipid determination in a broad range of marine tissue. Lipids 36:1283-1287.
44. J.E. MCDONALD, AND L.K. SMITH. 2001a. Changes in the diet of free-ranging black bears in years of contrasting food availability revealed through milk fatty acids. Canadian Journal of Zoology 79:2268-2279.
45. C. FIELD, W.D. BOWEN, AND W. BLANCHARD. 2004. Quantitative fatty acid signature analysis: a new method of estimating predator diets. Ecological Monographs 74:211-235.
46. I. STIRLING, AND S.L.C. LANG. 2006. Spatial and temporal variation in the diets of polar bears across the Canadian Arctic: indicators of changes in prey populations and environment. Pages 98-117 in I.L. Boyd, S. Wanless, and C.J. Camphuysen, editors. Top predators in marine ecosystems. Cambridge University Press, New York, New York, USA.
47. A.M. SPRINGER, AND A.S. KITAYSKY. 2007. Seabirds as indicators of food web structure and ecosystem variability: qualitative and quantitative diet analyses using fatty acids. Marine Ecology Progress Series 352:235-244.
48. JACOBY, M.E., G.V. HILDERBRAND, C. SERVHEEN, C.C. SCHWARTZ, S.M. ARTHUR, T.A. HANLEY, C.T. ROBBINS, AND R. MICHENER. 1999. Trophic relations of brown and black bears in several western North American ecosystems. Journal of Wildlife Management 63:921-929.
49. JENKINS, T.C. 1993. Lipid metabolism in the rumen. Journal of Dairy Science 76:3851-3863.
50. JOSEPH, J.D. 1982. Lipid composition of marine and estuarine invertebrates. Part II: Mollusca. Progress in Lipid Research 21:109-153.
51. KÄKELÄ, R., H. HYVÄRINEN, AND P. VAINIOTALO. 1993. Fatty acid composition in liver and blubber of the Saimaa ringed seal (Phoca hispida saimensis) compared with that of the ringed seal (Phoca hispida botnica) and grey seal (Halichorus grypus) from the Baltic. Comparative Biochemistry and Physiology 105B:553-565.
52. KEELING, C.I., AND D.E. NELSON. 2001. Changes in the intramolecular stable carbon isotope ratios with age of the European cave bear (Ursus spelaeus). Oecologia 127:495-500.
53. KIRSCH, P.E., S.J. IVERSON, AND W.D. BOWEN. 2000. Effect of a low-fat diet on body composition and blubber fatty acids of captive juvenile harp seals (Phoca groenlandica). Physiological and Biochemical Zoology 73:45-59.
54. KLINGENSMITH, J.S. 1982. Distribution of methylene and nonmethylene-interrupted dienoic fatty acids in polar lipids and triacylglycerols of selected tissues of the hardshell clam (Mercenaria mercenaria). Lipids 17:976-981.
55. MATTSON, D.J., B.M. BLANCHARD, AND R.R. KNIGHT. 1991. Food habits of Yellowstone grizzly bears, 1977-1987. Canadian Journal of Zoology 69:1619-1629.
56. MIZUKAMI, R.N., M. GOTO, S. IZUMIYAMA, H. HAYASHI, AND M. YOH. 2005. Estimation of feeding history by measuring carbon and nitrogen stable isotope ratios in hair of Asiatic black bears. Ursus 16:93-101.
57. MOWAT, G., AND D.C. HEARD. 2006. Major components of grizzly bear diet across North America. Canadian Journal of Zoology 84:473-489.
58. MUNRO, R.H.M., S.E. NIELSEN, M.H. PRICE, G.B. STENHOUSE, AND M.S. BOYCE. 2006. Seasonal and diel patterns of grizzly bear diet and activity in west-central Alberta. Journal of Mammalogy 87:1112-1121.
59. NARITA, R., A. SUGIMOTO, AND A. TAKAYANAGI. 2006. Animal components in the diet of Japanese black bears Ursus thibetanus japonicus in the Kyoto area, Japan. Wildlife Biology 12:375-384.
60. NELSON, G.J. 1992. Dietary fatty acids and lipid metabolism. Pages 437-411 in C.K. Chow, editor. Fatty acids in foods and their health implications. Marcel Drekker, Inc., New York, New York, USA.
61. NOYCE, K.V., P.B. KANNOWSKI, AND M.R. RIGGS. 1997. Black bears as ant-eaters: Seasonal associations between bear myrmecophagy and ant ecology in north-central Minnesota. Canadian Journal of Zoology 75:1671-1686.
62. PARADIS, M., AND R.G. ACKMAN. 1977. Potential for employing the distribution of anomalous non-methylene-interrupted dienoic fatty acids in several marine invertebrates as part of food web studies. Lipids 12: 170-176.
63. PELTON, M.R. 2003. Black bear. Pages 547-555 in G.A. Feldhamer, B.C. Thompson, and J.A. Chapman, editors. Wild mammals of North America. Johns Hopkins University Press, Baltimore, Maryland, USA.
64. POND, C.M., C.A. MATTACKS, R.H. COLBY, AND M.A. RAMSAY. 1992. The anatomy, chemical composition, and metabolism of adipose tissue in wild polar bears (Ursus maritimus). Canadian Journal of Zoology 70:326-341.
65. I. GILMOUR, M.A. JOHNSTON, C.T. PILLINGER, AND P. PRESTRUD. 1995. Chemical and carbon isotopic composition of fatty acids in adipose tissue as indicators of dietary history in wild arctic foxes (Alopex lagopus) on Svalbard. Journal of Zoology 236:611-623.
66. RAMSAY, M.A., AND K.A. HOBSON. 1991. Polar bears make little use of terrestrial food webs: evidence from stablecarbon isotope analysis. Oecologia 86:598-600.
67. C.A. MATTACKS, AND C.M. POND. 1992. Seasonal and sex differences in the structure and chemical composition of adipose tissue in wild polar bears (Ursus maritimus). Journal of Zoology 228:533-544.
68. REIDINGER, R.F., J.N. LABOWS, D.P. FELLOWS, AND J.R. MASON. 1985. Fatty acid composition of adipose tissue as an indicator of diet: a preliminary assessment. Journal of Wildlife Management 49:170-177.
69. ROBBINS, C.T., C.C. SCHWARTZ, AND L.A. FELICETTI. 2004. Nutritional ecology of ursids: a review of newer methods and management implications. Ursus 15:161-171.
70. RODE, K.D., AND C.T. ROBBINS. 2000. Why bears consume mixed diets during fruit abundance. Canadian Journal of Zoology 78:1640-1645.
71. L.A. SHIPLEY. 2001. Constraints on herbivory by grizzly bears. Oecologia 128:62-71.
72. ROUVINEN, K., AND T. KIISKINEN. 1989. Influence of dietary fat source on the body fat composition of mink (Mustela vison) and blue fox (Alopex lagopus). Acta Agriculturae Scandinavica 39:279-288.
73. RUGGERONE, G.T., R. HANSON, AND D.E. ROGERS. 2000. Selective predation by brown bears (Ursus arctos) foraging on spawning sockeye salmon (Oncorhynchus nerka). Canadian Journal of Zoology 78:974-981.
74. RULE, D.C., K.S. BROUGHTON, S.M. SHELLITO, AND G. MAIORANO. 2002. Comparison of muscle fatty acid profiles and cholesterol concentrations of bison, beef cattle, elk, and chicken. Journal of Animal Science 80:1202-1211.
75. SARGENT, J.R., J.G. BELL, M.V. BELL, R.J. HENDERSON, AND D.R. TOCHER. 1995. Requirement criteria for essential fatty acids. Journal of Applied Ichthyology 11:183-198.
76. SCHEMMEL, R. 1976. Physiological consideration of lipid storage and utilization. American Zoologist 16:661-670.
77. SCHWALME, K. 1992. A quantitative comparison between diet and body fatty acid composition in wild northern pike (Esox lucius L.). Fish Physiology and Biochemistry 10:91-98.
78. SMITH, R.J., K.A. HOBSON, H.N. KOOPMAN, AND D.M. LAVIGNE. 1996. Distinguishing between populations of fresh- and salt-water harbour seals (Phoca vitulina) using stable-isotope ratios and fatty acid profiles. Canadian Journal of Fisheries and Aquatic Sciences 53:272-279.
79. SMITH, T.G. 1980. Polar bear predation of ringed and bearded seals in the land-fast sea ice habitat. Canadian Journal of Zoology 58:2201-2209.
80. SMITH, T.S., AND S.T. PARTRIDGE. 2004. Dynamics of intertidal foraging by coastal brown bears in southwestern Alaska. Journal of Wildlife Management 68:233-240.
81. STEVENS, J. 1986. Applied multivariate statistics for the social sciences. Lawrence Erlbaum Associates, Mahwah, New Jersey, USA.
82. STIRLING, I. 1974. Midsummer observations on the behavior of wild polar bears (Ursus maritimus). Canadian Journal of Zoology 52:1191-1198.
83. W.R. ARCHIBALD. 1977. Aspects of predation of seals by polar bears. Journal of the Fisheries Research Board of Canada 34:1126-1129.
84. G.W. THIEMANN, AND E. RICHARDSON. 2008. Quantitative support for a subjective fatness index for immobilized polar bears. Journal of Wildlife Management 72:568-574.
85. SUAREZ, L. 1988. Seasonal distribution and food habits of spectacled bears Tremarctos ornatus in the highlands of Ecuador. Studies on Neotropical Fauna & Environment 23:133-136.
86. THIEMANN, G.W., S.M. BUDGE, AND S.J. IVERSON. 2004. Determining blubber fatty acid composition: a comparison of in situ direct and traditional methods. Marine Mammal Science 20:284-295.
87. 2006. Continental scale variation in polar bear (Ursus maritimus) diets and the fatty acid signatures of their marine mammal prey. Dissertation, Dalhousie University, Halifax, Nova Scotia, Canada.
88. S.J. IVERSON, AND I. STIRLING. 2006. Seasonal, sexual and anatomical variability in the adipose tissue of polar bears (Ursus maritimus). Journal of Zoology 269:65-76.
89. S.M. BUDGE, S.J. IVERSON, AND I. STIRLING. 2007. Unusual fatty acid biomarkers reveal age- and sex-specific foraging in polar bears (Ursus maritimus). Canadian Journal of Zoology 85:505-517.
90. S.J. IVERSON, AND I. STIRLING. In press. Polar bear (Ursus maritimus) diet composition and the structure of arctic marine food webs: insights from quantitative fatty acid signature analysis. Ecological Monographs.
91. VAN VLIET, T., AND M.B. KATAN. 1990. Lower ratio of n-3 to n-6 fatty acids in cultured than in wild fish. American Journal of Clinical Nutrition 51:1-2.
92. WASSER, S.K., B. DAVENPORT, E.R. RAMAGE, K.E. HUNT, M. PARKER, C. CLARKE, AND G. STENHOUSE. 2004. Scat detection dogs in wildlife research and management: application to grizzly and black bears in the Yellowhead Ecosystem, Alberta, Canada. Canadian Journal of Zoology 82:475-492.
93. WATANABE, T., AND R.G. ACKMAN. 1972. Effect of unicellular algal lipids on oyster lipids and their fatty acid compositions. Fisheries Research Board of Canada, Technical Report 334.
94. WELCH, C.A., J. KEAY, K.C. KENDALL, AND C.T. ROBBINS. 1997. Constraints on frugivory by bears. Ecology 78:1105-1119.