Investigating the use of stable isotope analysis of milk to infer seasonal trends in the diets and foraging habitats of female Antarctic fur seals

Journal of Experimental Marine Biology and Ecology

Volumn 395, Issue 1-2, 2010, Pages 1-9

  Polito, Michael J ^a   Goebel, Michael E ^b  

^a UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

^b SOUTHWEST FISHERIES SCIENCE CENTER   (United States)

Author keywords

Antarctic fur seal; Arctocephalus gazella; Diets; Milk; Stable isotopes

Indexed keywords

BIOMARKER; DIET; FORAGING BEHAVIOR; ISOTOPIC ANALYSIS; LACTATION; MILK; PINNIPED; SEASONAL VARIATION; STABLE ISOTOPE;

ANTARCTICA; CAPE SHIRREFF; LIVINGSTON ISLAND; SCOTLAND; SHETLAND; SOUTH SHETLAND ISLANDS; UNITED KINGDOM;

ARCTOCEPHALUS GAZELLA; CEPHALOPODA; DECAPODA (CRUSTACEA); EUPHAUSIA SUPERBA; EUPHAUSIACEA;

EID: 77957891299     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2010.08.015     Document Type: Article

References (68)

1. Akaike H. Information theory and an extension of the maximum likelihood principle. Second International Symposium on Information Theory 1973, 267-281. Akademini Kindo, Budapest. B.N. Petrov, F. Czaki (Eds.).
2. Arnould J.P.Y. Indices of body condition and body composition in female Antarctic fur seals (Arctocephalus gazella). Mar. Mamm. Sci. 1995, 11:301-313.
3. Arnould J.P.Y., Boyd I.L. Temporal patterns of milk production in Antarctic fur seals (Arctocephalus gazella). J. Zool. Lond. 1995, 237:1-12.
4. Ashmole N.P. The regulation of numbers of tropical oceanic birds. Ibis 1963, 103(b):458-473.
5. Bearhop S., Waldron S., Votier S.C., Furness R.W. Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol. Biochem. Zool. 2002, 75:451-458.
6. Biuw M., Krafft B.A., Hofmeyr G.J.G., Lydersen C., Kovacs K.M. Time budgets and at-sea behaviour of lactating female Antarctic fur seals Arctocephalus gazella at Bouvetøya. Mar. Ecol. Prog. Ser. 2009, 385:271-284.
7. Bost C.A., Cotte C., Bailleul F., Cherel Y., Charrassin J.B., Guinet C., Ainley D.G., Weimerskirch H. The importance of oceanographic fronts to marine birds and mammals of the southern oceans. J. Mar. Syst. 2009, 78:363-376.
8. Boyd I.L., Staniland I.J., Martin A.R. Distribution of foraging by female Antarctic fur seals. Mar. Ecol. Prog. Ser. 2002, 242:258-294.
9. Top Predators in Marine Ecosystems: Their role in Monitoring and Management 2006, Cambridge University Press, Cambridge. I.L. Boyd, S. Wanless, C.J. Camphuysen (Eds.).
10. Brown D.J., Boyd I.L., Cripps G.C., Butler P.J. Fatty acid signature analysis from the milk of Antarctic fur seals and southern elephant seals from South Georgia: implications for diet determination. Mar. Ecol. Prog. Ser. 1999, 187:251-263.
11. Burns J.M., Trumble S.J., Castellini M.A., Testa J.W. The diet of Weddell seals in McMurdo Sound, Antarctica as determined from scat collections and stable isotope analysis. Polar Biol. 1998, 19:272-282.
12. CCAMLR CCAMLR ecosystem monitoring program standard methods 2004, CCAMLR, Hobart, Australia.
13. Cherel Y., Hobson K.A. Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Mar. Ecol. Prog. Ser. 2007, 329:281-287.
14. Cherel Y., Ducatez S., Fontaine C., Richard P., Guinet C. Stable isotopes reveal the trophic position and mesopelagic fish diet of female southern elephant seals breeding on the Kerguelen Islands. Mar. Ecol. Prog. Ser. 2008, 370:239-247.
15. Cherel Y., Kernaléguen L., Richard P., Guinet C. Whisker isotopic signature depicts migration patterns and multi-year intra- and inter-individual foraging strategies in fur seals. Biol. Lett. 2009, 5(6):830-832.
16. Ciaputa P., Sicinski J. Seasonal and annual changes in Antarctic fur seal (Arctocephalus gazella) diet in the area of Admiralty Bay, King George Island, South Shetland Islands. Pol. Polar Res. 2006, 27:181-184.
17. Cossio A.M., Reiss C.R. Bioacoustic survey. AMLR 2006/07 Field Season Report. NOAA-TM-NMFS-SWFSC-409 2007, 44-53. J.D. Lipsky (Ed.).
18. Cossio A.M., Reiss C.R. Bioacoustic survey. AMLR 2007/08 Field Season Report. NOAA-TM-NMFS-SWFSC-427 2008, 49-58. J.D. Lipsky (Ed.).
19. Crawford K., McDonald R.A., Bearhop S. Applications of stable isotopes to the ecology of mammals. Mamm. Rev. 2008, 38:87-107.
20. Daneri G.A., Piatkowski U., Coria N.R., Carlini A.R. Predation on cephalopods by Antarctic fur seals, Arctocephalus gazella, at two localities of the Scotia Arc, Antarctica. Polar Biol. 1999, 21:59-63.
21. DeNiro M.J., Epstein S. Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Acta 1978, 42:495-506.
22. DeNiro M.J., Epstein S. Influence of diet on the distribution of nitrogen isotopes in animals. Geochim. Cosmochim. Acta 1981, 45:341-351.
23. 13C measurements of Antarctic Peninsula fauna: trophic relationships and assimilation of benthic seaweeds. Am. Zool. 2001, 41:99-112.
24. Ferreira S.M., Bester M.N. Chemical immobilization, physical restraint, and stomach lavaging of fur seals (Arctocephalus spp.) at Marion Island. S. Afr. J. Wildl. Res. 1999, 29:55-61.
25. Folch J., Lees M., Sloane-Stanly G.H. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 1957, 226:497-509.
26. France R.L. Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar. Ecol. Prog. Ser. 1995, 124:307-312.
27. Gales N.J., Mattlin R.H. Fast, safe, field-portable gas anesthesia for otariids. Mar. Mamm. Sci. 1998, 14:355-361.
28. Glorioso P.D., Flarther R.A. A barotropic model of the currents off SE South America. J. Geophys. Res. Oceans 1995, 100:13427-13440.
29. Goebel M.E., McDonald B.I., Haner R.G., Champagne C.D., Lipsky J.D., Driscoll R., Sexton S.N., Holt R.S. Pinniped research at Cape Shirreff Island, Antarctica 2006/07. AMLR 2006/07 Field Season Report. NOAA-TM-NMFS-SWFSC-409 2007, 122-143. J.D. Lipsky (Ed.).
30. Goebel M.E., McDonald B.I., Freeman S., Haner R.G., Spear N.B., Sexton S.N. Pinniped research at Cape Shirreff Island, Antarctica 2007/08. AMLR 2007/08 Field Season Report. NOAA-TM-NMFS-SWFSC-427 2008, 120-132. J.D. Lipsky (Ed.).
31. Goldsworthy S.D. Maternal attendance behaviour of sympatrically breeding Antarctic and subantarctic fur seals, Arctocephalus spp., at Macquarie Island. Polar Biol. 1999, 21:316-325.
32. Green K., Burton H.R., Williams R. The diet of Antarctic fur seals Arctocephalus gazella (Peters) during the breeding season at Heard Island. Antarct. Sci. 1989, 1:317-324.
33. Helm R.C. Rate of digestion in 3 species of pinnipeds. Can. J. Zool. 1984, 62:1751-1756.
34. 13C in tissues. Condor 1992, 94:181-188.
35. Hobson K.A., Alisauskas R.T., Clark R.G. Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. Condor 1993, 95:388-394.
36. Hobson K.A., Schell D.M., Renouf D., Noseworthy E. 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. 1996, 53:528-533.
37. Ichii T., Bengtson J.L., Boveng P.L., Takao Y., Jansen J.K., Hiruki-Raring L.M., Cameron M.F., Okamura H., Hayashi T., Naganobu M. Provisioning strategies of Antarctic fur seals and chinstrap penguins produce different responses to distribution of common prey and habitat. Mar. Ecol. Prog. Ser. 2007, 344:277-297.
38. Iverson S.J. Tracing aquatic food webs using fatty acids: from qualitative indicators to quantitative determination. Lipids in Aquatic Ecosystems 2009, 281-307. Springer-Verlag, New York. M.T. Arts, M.T. Brett, M. Kainz (Eds.).
39. Iverson S.J., Arnould J.P.Y., Boyd I.L. Milk fatty acid signatures indicate both major and minor shifts in the diet of lactating Antarctic fur seals. Can. J. Zool. 1997, 75:188-197.
40. Iverson S.J., Lang S.L.C., Cooper M.C. Comparison of the Bligh and Dyer and Folch methods for total lipid determination in a broad range of marine tissue. Lipids 2001, 36:123-1287.
41. Kurle C.M. Stable isotope ratios of blood components from captive northern fur seals (Callorhinus ursinus) and their diet: applications for studying the foraging ecology of wild otariids. Can. J. Zool. 2002, 80:902-909.
42. Lea M.-A., Cherel Y., Guinet C., Nichols P.D. Antarctic fur seals foraging in the Polar Frontal Zone: inter-annual shifts in diet as shown from fecal and fatty acid analyses. Mar. Ecol. Prog. Ser. 2002, 245:281-297.
43. Lesage V., Hammill M.O., Kovacs K.M. Diet-tissue fractionation of stable carbon and nitrogen isotopes in phocid seals. Mar. Mamm. Sci. 2002, 18:182-193.
44. MacAvoy S.E., Arneson L.S., Bassett E. Correlation of metabolism with tissue carbon and nitrogen turnover rate in small mammals. Oecologia 2006, 150:190-201.
45. McDonald B.I., Goebel M.E., Crocker D.E., Tremblay Y., Costa D.P. Effects of maternal traits and individual behavior on the foraging strategies and provisioning rates of an income breeder, the Antarctic fur seal. Mar. Ecol. Prog. Ser. 2009, 394:277-288.
46. Miller A.K., Trivelpiece W.Z. Chinstrap penguins alter foraging and diving behavior in response to the size of their principle prey, Antarctic krill. Mar. Biol. 2008, 154:201-208.
47. 15N and animal age. Geochim. Cosmochim. Acta 1984, 48:1135-1140.
48. Mori M., Butterworth D.S. A first step towards modeling the krill-predator dynamics of the Antarctic ecosystem. CCAMLR Sci. 2006, 13:217-277.
49. Newsome S.D., Etnier M.A., Aurioles-Gamboa D., Koch P.L. Using carbon and nitrogen isotope values to investigate maternal strategies in northeast Pacific otariids. Mar. Mamm. Sci. 2006, 22:1-18.
50. Newsome S.D., Etnier M.A., Kurle C.M., Waldbauer J.R., Chamberlain C.P., Koch P.L. Historic decline in primary productivity in western Gulf of Alaska and eastern Bering Sea: isotopic analysis of northern fur seal teeth. Mar. Ecol. Prog. Ser. 2007, 332:211-224.
51. North A.W. Fish in the diet of Antarctic fur seals (Arctocephalus gazella) at South Georgia during winter and spring. Antarct. Sci. 1996, 8:155-160.
52. Osman L.P., Hucke-Gaete R., Moreno C.A., Torres D. Feeding ecology of Antarctic fur seals at Cape Shirreff, South Shetlands, Antarctica. Polar Biol. 2004, 27:92-98.
53. Polito M., Emslie S.D., Walker W. A 1,000-year record of Adélie penguin diets in the southern Ross Sea. Antarct. Sci. 2002, 14:327-332.
54. Quillfeldt P., McGill R.A.R., Furness R.W. Diet and foraging areas of Southern Ocean seabirds and their prey inferred from stable isotopes: review and case study of Wilson's storm-petrel. Mar. Ecol. Prog. Ser. 2005, 295:295-304.
55. 2 and productivity in past oceans. Nature 1989, 341:516-518.
56. Reid K. The diet of Antarctic fur seals (Arctocephalus gazella Peters 1875) during winter at South Georgia. Antarct. Sci. 1995, 7:241-249.
57. Reid K., Arnould P.Y. The diet of Antarctic fur seals Arctocephalus gazella during the breeding season at South Georgia. Polar Biol. 1996, 16:105-114.
58. Reid K., Croxall J.P. Environmental response of upper trophic level predators reveals a system change in an Antarctic marine ecosystem. Proc. R. Soc. Lond. B 2001, 268:377-384.
59. Reid K., Davis D., Staniland I.J. Spatial and temporal variability in the fish diet of Antarctic fur seal (Arctocephalus gazella) in the Atlantic sector of the Southern Ocean. Can. J. Zool. 2006, 84:1025-1037.
60. Sears J., Hatch S.A., O'Brien D.M. Disentangling effects of growth and nutritional status on seabird stable isotope ratios. Oecologia 2009, 159:41-48.
61. Staniland I.J. Investigating the biases in the use of hard prey remains to identify diet composition using Antarctic fur seals (Arctocephalus gazella) in captive feeding trials. Mar. Mamm. Sci. 2002, 18:223-243.
62. Staniland I.J., Pond D. Variability in milk fatty acids: recreating a foraging trip to test dietary predictions in Antarctic fur seals. Can. J. Zool. 2004, 82:1099-1107.
63. Staniland I.J., Pond D.W. Investigating the use of milk fatty acids to detect dietary changes: a comparison with faecal analysis in Antarctic fur seals. Mar. Ecol. Prog. Ser. 2005, 294:283-294.
64. Staniland I.J., Taylor R.I., Boyd I.L. An enema method for obtaining fecal material from known individual seals on land. Mar. Mamm. Sci. 2003, 19:363-370.
65. Staniland I.J., Boyd I.L., Reid K. An energy-distance trade-off in a central-place forager, the Antarctic fur seal (Arctocephalus gazella). Mar. Biol. 2007, 152:233-241.
66. Sullivan C.W., McClain C.R., Comiso J.C., Smith W.O. Phytoplankton standing crops within an Antarctic ice edge assessed by satellite remote-sensing. J. Geophys. Res. Oceans 1988, 93:12487-12498.
67. Williams R., McEldowney A. ANARE research notes 75: a guide to the fish otoliths from waters of the Australian Antarctic Territory, Heard and Macquarie Islands. ANARE Res. Notes 1990, 75:1-169.
68. Williams C.T., Buck C.L., Sears J., Kitaysky A.S. Effects of nutritional restriction on nitrogen and carbon stable isotopes in growing seabirds. Oecologia 2007, 153(1):11-18.