Quantitative fatty acid signature analysis: A new method of estimating predator diets

Ecological Monographs

Volumn 74, Issue 2, 2004, Pages 211-235

  Iverson, Sara J ^a   Field, Chris ^a   Bowen, W Don ^b   Blanchard, Wade ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b BEDFORD INSTITUTE OF OCEANOGRAPHY   (Canada)

Author keywords

Feeding ecology; Food webs; Marine carnivores; Pinnipeds; Predator diets; Predator prey relationships; Prey fatty acid composition and signatures; Statistical model

Indexed keywords

DIET; ESTIMATION METHOD; FATTY ACID; FEEDING ECOLOGY; PINNIPED; QUANTITATIVE ANALYSIS;

ATLANTIC OCEAN; SCOTIA SHELF;

ANIMALIA; CLUPEA HARENGUS; GRYPUS; HALICHOERUS GRYPUS; MALLOTUS VILLOSUS; MAMMALIA; MUSTELA; MUSTELA VISON; PHOCA; PHOCA GROENLANDICA; PHOCA VITULINA; PHOCIDAE; PINNIPEDIA; PLEURONECTIFORMES; PLEURONECTOIDEI;

EID: 4444263352     PISSN: 00129615     EISSN: None     Source Type: Journal    
DOI: 10.1890/02-4105     Document Type: Article

References (85)

1. Ackman, R. G. 1980. Fish lipids, part 1. Pages 86-103 in J. J. Connell, editor. Advances in fish science and technology. Fishing News Books, Surrey, UK.
2. 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.
3. Ackman, R. G., C. A. Eaton, J. Kinneman, and C. Litchfield. 1975. Lipids of freshwater dolphin Sotalia fluviatilis: comparison of odontocete bioacoustic lipids and habitat. Lipids 10:44-49.
4. Ackman, R. G., W. M. N. Ratnayake, and B. Olsson. 1988. The 'basic' fatty acid composition of Atlantic fish oils: potential similarities useful for enrichment of polyunsaturated fatty acids by urea complexation. Journal of the American Oil Chemist's Society 65:136-138.
5. Bowen, W. D. 2000. Reconstruction of pinniped diets: accounting for complete digestion of otoliths and cephalopod beaks. Canadian Journal of Fisheries and Aquatic Science 57:898-905.
6. Bowen, W. D., and G. D. Harrison. 1994. Offshore diet of grey seals Halichoerus grypus near Sable Island, Canada. Marine Ecology Progress Series 112:1-11.
7. Bowen, W. D., and S. J. Iverson. 1998. Estimation of total body water in pinnipeds using hydrogen-isotope dilution. Physiological Zoology 71:329-332.
8. Bowen, W. D., S. J. Iverson, D. J. Boness, and O. T. Oftedal. 2001. Foraging effort, food intake and lactation performance depend on maternal mass in a small phocid seal. Functional Ecology 15:325-334.
9. Bowen, W. D., D. Tully, D. J. Boness, B. Bulhier, and G. Marshall. 2002. Prey-dependent foraging tactics and prey profitability in a marine mammal. Marine Ecology Progress Series 244:235-245.
10. Boyle, P. R., G. J. Pierce, and J. S. W. Diack. 1990. Sources of evidence for salmon in the diet of seals. Fisheries Research 10:137-150.
11. Bremer, J., and K. R. Norum. 1982. Metabolism of very long-chain monounsaturated fatty acids (22:1) and the adaptation to their presence in diet. Journal of Lipid Research 23:243-256.
12. Budge, S. M., S. J. Iverson, W. D. Bowen, and R. G. Ackman. 2002. Among- and within-species variation in fatty acid signatures of marine fish and invertebrates on the Scotian Shelf, Georges Bank and southern Gulf of St. Lawrence. Canadian Journal of Fisheries and Aquatic Sciences 59:886-898.
13. Carss, D. N., and S. G. Parkinson. 1996. Errors associated with otter Lutra lutra faecal analysis. I. Assessing general diet from spraints. Journal of Zoology (London) 238:301-317.
14. Colby, R. H., C. A. Mattacks, and C. M. Pond. 1993. The gross anatomy, cellular structure and fatty acid composition of adipose tissue in captive polar bears (Ursus maritimus). Zoo Biology 12:267-275.
15. Coltman, D., W. D. Bowen, D. J. Boness, and S. J. Iverson. 1997. Balancing foraging and reproduction in the male harbour seal: an aquatically mating pinniped. Animal Behaviour 54:663-678.
16. Cook, H. W. 1991. Fatty acid desaturation and chain elongation in eucaryotes. Pages 141-169 in D. E. Vance and J. E. Vance, editors. Biochemistry of lipids and membranes. Elsevier Science, Amsterdam, The Netherlands.
17. Cooper, M. H., S. J. Iverson, and W. D. Bowen. 2001. Direct and quantitative effects on blubber fatty acids of homogenous diets fed to grey seals. Fourteenth Biennial Conference on the Biology of Marine Mammals, Vancouver. Society for Marine Mammalogy, Miami, Florida, USA.
18. DiCiccio, T., and J. Romano. 1989. Nonparametric confidence limits by resampling methods and least favorable families. International Statistical Review 58:59-76.
19. Encyclopedia of Statistics. 1983. The Kulback distance. Pages 421-425 in S. Kotz and N. L. Johnson, editors. Encyclopedia of Statistics. John Wiley and Sons, New York, New York, USA.
20. Folch, J., M. Lees, and G. H. Sloane-Stanly. 1957. A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 226:497-509.
21. Fraser, A. J., J. R. Sargent, J. C. Gamble, and D. D. Seaton. 1989. Formation and transfer of fatty acids in an enclosed marine food chain comprising phytoplankton, zooplankton and herring (Clupea harengus L.) larvae. Marine Chemistry 27:1-18.
22. Gannes, L. Z., D. M. O'Brien, and C. Martinez del Rio. 1997. Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78:1271-1276.
23. Gaston, A. J., and D. G. Noble. 1985. The diet of Thick-billed Murres (Uria lomvia) in west Hudson Strait and northeast Hudson Bay. Canadian Journal of Zoology 93:1148-1160.
24. Gilmore, I., M. A. Johnston, C. T. Pillinger, C. M. Pond, C. A. Mattacks, and P. Prestrud. 1995. The carbon isotopic composition of individual fatty acids as indicators of dietary history in arctic foxes on Svalbard. Philosophical Transactions of the Royal Society of London B 349:135-142.
25. 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.
26. Gurr, M. I., and A. T. James. 1980. Lipid biochemistry: an introduction. Chapman and Hall, London, UK.
27. Hobson, K. A. 1993. Trophic relationships among high Arctic seabirds: insights from tissue-dependent stable-isotope models. Marine Ecology Progress Series 95:7-18.
28. Hooper, S. N., M. Paradis, and R. G. Ackman. 1973. Distribution of trans-6-hexadecanoic acid, 7-methyl-7-hexadecanoic acid and common fatty acids in lipids of the ocean sunfish Mola mola. Lipids 8:509-516.
29. Iverson, S. J. 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.
30. Iverson, S. J. 2002. Blubber. Pages 107-112 in W. F. Perrin, B. Wursig, and H. G. Thewissen, editors. Encyclopedia of marine mammals. Academic Press, San Diego, California, USA.
31. Iverson, S. J., J. P. Y. Arnould, and I. L. Boyd. 1997a. Milk fatty acid signatures indicate both major and minor shifts in diet of lactating Antarctic fur seals. Canadian Journal of Zoology 75:188-197.
32. Iverson, S. J., W. D. Bowen, D. J. Boness, and O. T. Oftedal. 1993. The effect of maternal size and milk energy output on pup growth in grey seals (Halichoerus grypus). Physiological Zoology 66:61-88.
33. Iverson, S. J., K. J. Frost, and S. Lang. 2002. Fat content and fatty acid composition of forage fish and invertebrates in Prince William Sound, Alaska: factors contributing to among and within species variability. Marine Ecology Progress Series 241:161-181.
34. Iverson, S. J., K. J. Frost, and L. L. Lowry. 1997b. 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.
35. Iverson, S. J., S. Lang, and M. Cooper. 2001a. Comparison of the Bligh and Dyer and Folch methods for total lipid determination in a broad range of marine tissue. Lipids 36:1283-1287.
36. Iverson, S. J., J. E. McDonald, and L. H. Smith. 2001b. Changes in diet of free-ranging black bears in years of contrasting food availability revealed through milk fatty acids. Canadian Journal of Zoology 79:2268-2279.
37. Iverson, S. J., and O. T. Oftedal. 1992. Fatty acid composition of black bear (Ursus americanus) milk during and after the period of winter dormancy. Lipids 27:940-943.
38. Iverson, S. J., and O. T. Oftedal: 1995. Phylogenetic and ecological variation in the fatty acid composition of milks. Pages 789-827 in R. G. Jensen, editor. The handbook of milk composition. Academic Press, Orlando, Florida, USA.
39. Iverson, S. J., 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 165:1-12.
40. Iverson, S. J., and A. M. Springer. 2002. Estimating seabird diets using fatty acids: protocol development and testing of ReFER hypotheses. Report to the National Pacific Marine Research Program. University of Alaska, Fairbanks, Alaska, USA.
41. Jackson, M. J. 1974. Transport of short chain fatty acids. Pages 673-709 in D. H. Smyth, editor. Biomembranes. Volume 4B. Plenum, New York, New York, USA.
42. Jandacek, R. J., E. J. Hollenbach, B. N. Holcombe, C. M. Kuehlthau, J. C. Peters, and J. D. Taulbee. 1991. Reduced storage of dietary eicosapentaeonic and docosahexaenoic acids in the weanling rat. Journal of Nutritional Biochemistry 2:142-149.
43. Jobling, M. 1987. Marine mammal faecal samples as indicators of prey importance - a source of error in bioenergetics studies. Sarsia 72:255-260.
44. Jobling, M., and A. Breiby. 1986. The use and abuse of fish otoliths in studies of feeding habits of marine piscivores. Sarsia 71:265-274.
45. Johnson, S. R., and G. C. West. 1973. Fat content, fatty acid composition and estimates of energy metabolism of Adelie Penguins (Pygoscelis adeliae) during the early breeding season fast. Comparative Biochemistry and Physiology B 45:709-719.
46. Kakela, R., H. Hyvarinen, and P. Vainiotalo. 1993. Fatty acid composition in liver and blubber of the Saimaa ringed seal (Phoca hispida saimensis) compared to that of the ringed seal (Phoca hispida botanica) and grey seal (Halichoerus grypus) from the Baltic. Comparative Biochemistry and Physiology B 105:553-565.
47. Kelly, J. F. 1999. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Canadian Journal of Zoology 78:1-27.
48. Kirsch, P. E. 1997. Dietary effects on fatty acid signatures in marine species: five captive animal studies. Thesis. Dalhousie University, Halifax, Nova Scotia, Canada.
49. Kirsch, P. E., S. J. Iverson, and W. D. Bowen. 2000. Effect of a low-fat diet on body composition and blubber fatty acids in captive harp seals (Phoca groenlandica). Physiological and Biochemical Zoology 73:45-59.
50. Kirsch, P. E., S. J. Iverson, W. D. Bowen, S. Kerr, and R. G. Ackman. 1998. Dietary effects on the fatty acid signatures of whole Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 55:1378-1386.
51. Klem, A. 1935. Studies in the biochemistry of whale oils. Hvalradets Skrifter 11:49-108.
52. Koch, P. L., J. Heisinger, C. Moss, R. W. Carlson, M. L. Fogel, and A. K. Behrensmeyer. 1995. Isotopic tracking of change in diet and habitat use in African elephants. Science 267:1340-1343.
53. Koopman, H. N., S. J. Iverson, and D. E. Gaskin. 1996. Stratification and age-related differences in blubber fatty acids of the male harbour porpoise (Phocoena phocoena). Journal of Comparative Physiology 165:628-639.
54. Koopman, H. N., S. J. Iverson, and A. J. Read. 2003. High concentrations of isovaleric acid in the fats of odontocetes: variation and patterns of accumulation in blubber vs. stability in the melon. Journal of Comparative Physiology 173:247-261.
55. Koopman, H. N., D. A. Pabst, W. A. McLellan, R. M. Dillaman, and A. J. Read. 2002. Changes in blubber distribution and morphology associated with starvation in the harbour porpoise (Phocoena phocoena): evidence for regional variation in blubber structure and function. Physiological and Biochemical Zoology 75:498-512.
56. Layton, H. 1998. Development of digestive capabilities and improvement of diet utilization by mink pre- and post-weaning with emphasis on gastric lipase. Thesis. Nova Scotia Agricultural College, Truro, Nova Scotia, Canada.
57. Layton, H., K. Rouvinen, and S. J. Iverson. 2000. Body composition in mink (Mustela vison) kits during 21-42 days postpartum using estimates of hydrogen isotope dilution and direct carcass analysis. Comparative Biochemistry and Physiology A 126:295-303.
58. Lin, D. S., and W. E. Connor. 1990. Are the n-3 fatty acids from dietary fish oil deposited in the triglyceride stores of adipose tissue? American Journal of Clinical Nutrition 51: 535-539.
59. Marshall, G. J. 1998. Crittercam: an animal-borne imaging and data logging system. Marine Technology Society Journal 32:11-17.
60. Morii, H., and T. Kaneda. 1982. Biosynthesis of branched-chain fatty acids from branched-chain amino acids in subcutaneous tissue of the marine little toothed whale, Stenella caeruleo-alba. Comparative Biochemistry and Physiology 718:357-365.
61. Nelson, G. J. 1992. Dietary fatty acids and lipid metabolism. Pages 437-471 in C. K. Chow, editor. Fatty acids in foods and their health implications. Marcel Dekker, New York, New York, USA.
62. Navarro, J. C., L. A. McEvoy, F. Amat, and J. R. Sargent. 1995. Effects of diet on fatty acid composition of body zones in larvae of the sea bass Dicentrarchus labrax: a chemometric study. Marine Biology 124:177-183.
63. Oftedal, O. T., and S. J. Iverson. 1987. Hydrogen isotope methodology for measurement of milk intake and energetics of growth in suckling pinnipeds. Pages 67-96 in A. C. Huntley, D. P. Costa, G. A. J. Worthy, and M. A. Castellini, editors. Approaches to marine mammal energetics. Society for Marine Mammalogy Special Publication Number 1. Alien Press, Lawrence, Kansas, USA.
64. Paine, R. T. 1980. Food webs: linkage, interaction strength and community infrastructure. Journal of Animal Ecology 49:667-685.
65. Pierce, G. J., and P. R. Boyle. 1991. A review of methods for diet analysis in piscivorous marine mammals. Oceanography and Marine Biology 29:409-486.
66. Pimm, S. L., J. H. Lawton, and J. E. Cohen. 1991. Food web patterns and their consequences. Nature 350:669-674.
67. Pond, C. M. 1998. The fats of life. Cambridge University Press, Cambridge, UK.
68. Pond, C. M. 2000. Adipose tissue: quartermaster to the lymph node garrisons. Biologist 47:147-150.
69. Pond, C. M., C. A. Mattacks, I. Gilmore, M. A. Johnson, and C. T. Pillinger. 1995. Chemical and carbon isotopic composition of fatty acids in adipose tissue as indicators of dietary history in wild foxes (Alopex lagopus) on Svalbard. Journal of Zoology (London) 236:611-623.
70. Raclot, T., and R. Groscolas. 1995. Selective mobilization of adipose tissue fatty acids during energy depletion in the rat. Journal of Lipid Research 36:2164-2173.
71. Raclot, T., R. Groscolas, and Y. Cherel. 1998. Fatty acid evidence for the importance of myctophid fishes in the diet of king penguins, Aptenodytes patagonicus. Marine Biology 132:523-533.
72. Rau, G. H., D. G. Ainley, J. L. Bengtson, J. J. Torres, and T. L. Hopkins. 1992. 15N/14N and 13C/12C in Weddell Sea birds, seals, and fish: implications for diet and trophic structure. Marine Ecology Progress Series 84:1-8.
73. 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.
74. Sargent, J. R., R. J. Parkes, I. Mueller-Harvey, and R. J. Henderson. 1988. Lipid biomarkers in marine ecology. Pages 119-138 in M. A. Sleigh, editor. Microbes in the sea. Ellis Horwood, Chichester, UK.
75. Schoener, T. W. 1971. Theory of feeding strategies. Annual Review of Ecological Systems 2:369-404.
76. Sih, A., G. Englund, and D. Wooster. 1998. Emergent impacts of multiple predators on prey. Trends in Ecology and Evolution 13:350-355.
77. 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.
78. Smith, S., S. J. Iverson, and W. D. Bowen. 1997. Fatty acid signatures and classification trees: new tools for investigating the foraging ecology of seals. Canadian Journal of Fisheries and Aquatic Sciences 54:1377-1386.
79. S-Plus. 2000. S-Plus 2000. Mathsoft, Seattle, Washington, USA.
80. Stephens, D. W., and J. R. Krebs. 1986. Foraging theory. Princeton University Press, Princeton, New Jersey, USA.
81. St. John, M. A., and T. Lund. 1996. Lipid biomarkers: linking the utilization of frontal plankton biomass to enhanced condition of juvenile North Sea cod. Marine Ecology Progress Series 131:75-85.
82. Volpe, J. J., and P. R. Vagelos. 1973. Saturated fatty acid biosynthesis and its regulation. Annual Review of Biochemistry 42:21-60.
83. Wakil, S. J., J. K. Stoops, and V. C. Joshi. 1983. Fatty acid synthesis and its regulation. Annual Review of Biochemistry 52:537-579.
84. Walker, B. G., and W. D. Bowen. 1993. Changes in body mass and feeding behaviour in male harbour seals, Phoca vitulina, in relation to female reproductive status. Journal of Zoology (London) 231:423-436.
85. Wamberg, S., C. R. Olesen, and H. O. Hansen. 1992. Influence of dietary sources of fat on lipid synthesis in mink (Mustela vison) mammary tissue. Comparative Biochemistry and Physiology A 103:199-204.