Ontogenetic dietary information of the California sea lion (Zalophus californianus) assessed using stable isotope analysis

Marine Mammal Science

Volumn 28, Issue 4, 2012, Pages 714-732

  Orr, Anthony J ^a,b   Newsome, Seth D ^c   Laake, Jeffrey L ^a   Vanblaricom, Glenn R ^b   Delong, Robert L ^a  

^a NOAA EARTH SYSTEM RESEARCH LABORATORY   (United States)

^b UNIVERSITY OF WYOMING   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Diet shift; Otariids; Stable isotopes; Zalophus californianus

Indexed keywords

CARBON ISOTOPE; DEVELOPMENTAL BIOLOGY; DIETARY SHIFT; FORAGING BEHAVIOR; MORPHOLOGY; NITROGEN ISOTOPE; ONTOGENY; PINNIPED; STABLE ISOTOPE;

CALIFORNIA; CHANNEL ISLANDS [CALIFORNIA]; SAN MIGUEL ISLAND [CHANNEL ISLANDS]; UNITED STATES;

ANIMALIA; OTARIIDAE; RODENTIA; ZALOPHUS; ZALOPHUS CALIFORNIANUS;

EID: 84867232945     PISSN: 08240469     EISSN: 17487692     Source Type: Journal    
DOI: 10.1111/j.1748-7692.2011.00522.x     Document Type: Article

References (74)

1. Antonelis, G. A., C. H. Fiscus and R. L. DeLong. 1984. Spring and summer prey of California sea lions, Zalophus californianus, at San Miguel Island, California, 1978-79. Fishery Bulletin 82:67-76.
2. Antonelis, G. A., B. S. Stewart and W. F. Perryman. 1990. Foraging characteristics of female northern fur seals (Callorhinus ursinus) and California sea lions (Zalophus californianus). Canadian Journal of Zoology 68:150-158.
3. Aurioles-Gamboa, D. 1988. Behavioral ecology of California sea lions in the Gulf of California. Ph.D. dissertation, University of California at Santa Cruz, Santa Cruz, CA. 174 pp.
4. Aurioles-Gamboa, D., and A. Zavala. 1994. Ecological factors that determine distribution and abundance of the California sea lion Zalophus californianus in the Gulf of California. Ciencias Marinas 20:535-553.
5. Aurioles-Gamboa, D., P. L. Koch and B. J. Le Boeuf. 2006. Differences in foraging location of Mexican and California elephant seals: Evidence from stable isotopes in pups. Marine Mammal Science 22:326-338.
6. Aurioles-Gamboa, D., S. D. Newsome, S. Salazar-Pico and P. L. Koch. 2009. Stable isotope differences between sea lions (Zalophus) from the Gulf of California and Galápagos Islands. Journal of Mammalogy 90:1410-1420.
7. Baker, J. D. and M. J. Donohue. 2000. Ontogeny of swimming and diving in northern fur seal (Callorhinus ursinus) pups. Canadian Journal of Zoology 78:100-109.
8. Burns, J. M. 1999. The development of diving behavior in juvenile Weddell seals: Pushing physiological limits in order to survive. Canadian Journal of Zoology 77:737-747.
9. Burton, R. K. and P. L. Koch. 1999. Isotopic tracking of foraging and long-distance migration in northeastern Pacific pinnipeds. Oecologia 119:578-585.
10. DeLong, R. L., G. A. Antonelis, C. W. Oliver, B. S. Stewart, M. C. Lowry and P. K. Yochem. 1991. Effects of the 1982-83 El Niño on several population parameters and diet of California sea lions on the California Channel Islands. Pages 166-172 in F. Trillmich and K. A. Ono, eds. Pinnipeds and El Niño: Responses to environmental stress. Springer-Verlag, New York, NY.
11. DeNiro, M. J., and S. Epstein. 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42:495-506.
12. De Smet, S., A. Balcaen, E. Claeys, P. Boeckx and O. Van Cleemput. 2004. Stable carbon isotope analysis of different tissues of beef animals in relation to their diet. Rapid Communications in Mass Spectrometry 18:1227-1232.
13. Drago, M., L. Cardona, E. A. Crespo and A. Aguilar. 2009. Ontogenic dietary changes in South American sea lions. Journal of Zoology 279:251-261.
14. Feldkamp, S. D., R. L. DeLong and G. A. Antonelis. 1989. Diving patterns of California sea lions, Zalophus californianus. Canadian Journal of Zoology 67:872-883.
15. Fiscus, C. H., and G. A. Baines. 1966. Food and feeding behavior of Steller and California sea lions. Journal of Mammalogy 47:195-200.
16. Fogel, M. L., N. Tuross and D. W. Owsley. 1989. Nitrogen isotope tracers of human lactation in modern and archaeological populations. Pages 111-117. Annual Report of the Director, Geophysical Laboratory, Carnegie Institution of Washington 1988-1989.
17. Fogel, M. L., N. Tuross, B. J. Johnson and G. H. Miller. 1997. Biogeochemical record of ancient humans. Organic Geochemistry 27:275-287.
18. Fowler, S. L., D. P. Costa, J. P. Y. Arnould, N. J. Gales and J. M. Burns. 2007a. Ontogeny of oxygen stores and physiological diving capacity in Australian sea lion. Functional Ecology 21:922-935.
19. Fowler, S. L., D. P. Costa and J. P. Y. Arnould. 2007b. Ontogeny of movements and foraging ranges in the Australian sea lion. Marine Mammal Science 23:598-614.
20. France, R. L. 1995. Carbon-13 enrichment in benthic compared to planktonic algae: Foodweb implications. Marine Ecology Progress Series 124:307-312.
21. Fuller, B. T., M. P. Richards and S. A. Mays. 2003. Stable carbon and nitrogen isotope variations in tooth dentine serial sections from Wharram Percy. Journal of Archaeological Science 30:1673-1684.
22. 13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Smithsonain Contributions to the Marine Sciences 27:13-47.
23. Hernández-Camacho, C. J., D. Aurioles-Gamboa and L. R. Gerber. 2008. Age-specific birth rates of California sea lion (Zalophus californianus californianus) in the Gulf of California, Mexico. Marine Mammal Science 24:664-676.
24. 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.
25. Hobson, K. A. 2005. Using stable isotopes to trace long-distance dispersal in birds and other taxa. Diversity and Distributions 11:157-164.
26. 13C in cellular and plasma factors of blood: Implications for non-destructive sampling in avian dietary studies. Auk 110:638-641.
27. Hobson, K. A., and J. L. Sease. 1998. Stable isotope analyses of tooth annuli reveal temporal dietary records: An example using Steller sea lions. Marine Mammal Science 14:116-129.
28. Hobson, K. A., D. M. Schell, D. Renouf and E. Noseworthy. 1996. Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: Implications for dietary reconstructions involving marine mammals. Canadian Journal of Fisheries and Aquatic Sciences 53:528-533.
29. Hobson, K. A., J. L. Sease, R. L. Merrick and J. F. Piatt. 1997. Investigating trophic relationships of pinnipeds in Alaska and Washington using stable isotope ratios of nitrogen and carbon. Marine Mammal Science 13:114-132.
30. Horning, M., and F. Trillmich. 1997a. Ontogeny of diving behavior in the Galapagos fur seal. Behaviour 134:1211-1257.
31. Horning, M., and F. Trillmich. 1997b. Development of hemoglobin, hematocrit, and erthyrocyte values in Galapagos fur seals. Marine Mammal Science 13:100-113.
32. Jenkins, S. G., S. T. Partridge, T. R. Stephenson, S. D. Farley and C. T. Robbins. 2001. Nitrogen and carbon isotope fractionation between mothers, neonates, and nursing offspring. Oecologia 129:336-341.
33. Jennings, S., J. K. Pinnegar, N. V. C. Polunin and T. W. Boon. 2001. Weak cross-species relationships between body size and trophic level belie powerful size-based trophic structuring in fish communities. Journal of Animal Ecology 70:934-944.
34. Johnson, D. S., J. M. London, M.-A. Lea and J. W. Durban. 2008. Continuous-time correlated random walk model for animal telemetry data. Ecology 89:1208-1215.
35. Kelly, J. F. 2000. Stable isotopes of nitrogen and carbon in the study of avian and mammalian trophic ecology. Canadian Journal of Zoology 78:1-27.
36. Klaassen, M., M. Thums and I. D. Hume. 2004. Effects of diet change on carbon and nitrogen stable-isotope ratios in blood cells and plasma of the long-nosed bandicoot (Perameles nasuta). Australian Journal of Zoology 52:635-647.
37. Kleiber, M. 1975. The fire of life. Robert Krieger, New York, NY.
38. Knoff, A., A. Hohn, and S. Macko. 2008. Ontogenetic diet changes in bottlenose dolphins (Tursiops truncates) reflected through stable isotopes. Marine Mammal Science 24:128-137.
39. Kooyman, G. L. 1989. Diverse divers: Physiology and behavior. Springer-Verlag, New York, NY.
40. Kurle, C. M. 2002. 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. Canadian Journal of Zoology 80:902-909.
41. Kurle, C. M., and G. A. J. Worthy. 2001. Stable isotope assessment of temporal and geographic differences in feeding ecology of northern fur seals (Callorhinus ursinus) and their prey. Oecologia 126:254-265.
42. Kurle, C. M., and G. A. J. Worthy. 2002. Variation in stable carbon and nitrogen isotope ratios in northern fur seal (Callorhinus ursinus) tissues: Implications for dietary and migratory reconstructions. Marine Ecology Progress Series 236:289-300.
43. Martínez del Rio, C., N. Wolf, S. A. Carleton and L. Z. Gannes. 2009. Isotopic ecology ten years after a call for more laboratory experiments. Biological Reviews 84:91-111.
44. McConnell, B. J., C. Chambers and M. A. Fedak. 1992. Foraging ecology of southern elephant seals in relation to the bathymetry and productivity of the Southern Ocean. Antarctic Science 4:393-398.
45. McConnaughey, T., and C. McRoy. 1979. Food-web structure and the fractionation of carbon isotopes in the Bering Sea. Marine Biology 53:257-262.
46. Melin, S. R. 1995. Winter and spring attendance patterns of California sea lion (Zalophus californianus) females and pups at San Miguel Island, 1991-1994. M.S. thesis, University of Washington, Seattle, WA. 67 pp.
47. Melin, S. R. 2002. The foraging ecology and reproduction of the California sea lion (Zalophus californianus californianus). Ph.D. thesis, Univeristy of Minnesota, Twin Cities, MN. 150 pp.
48. Melin, S. R., R. L. DeLong, J. R. Thomason and G. R. VanBlaricom. 2000. Attendance patterns of California sea lion (Zalophus californianus) females and pups during the non-breeding season at San Miguel Island. Marine Mammal Science 16:169-185.
49. Melin, S. R., R. L. DeLong and D. B. Siniff. 2008. The effects of El Niño on the foraging behavior of lactating California sea lions (Zalophus californianus californianus) during the nonbreeding season. Canadian Journal of Zoology 86:192-206.
50. Nelson, G. 1970. The lipid composition of the blood of marine mammals. I. Young elephant seals (Mirounga angustirostris) and harp seals (Pagophilus groenlandicus). Comparative Biochemistry and Physiology 34:109-116.
51. Newsome, S. D., M. A. Etnier and D. Aurioles-Gamboa. 2006. Using carbon and nitrogen isotope values to investigate maternal strategies in northeast pacific otariids. Marine Mammal Science 22:556-572.
52. Newsome, S. D., M. T. Clementz and P. L. Koch. 2010. Using stable isotope biogeochemistry to study marine mammal ecology. Marine Mammal Science 26:509-572.
53. Odell, D. K. 1975. Abundance of California sea lions on San Nicolas Island, California. Wildlife Management 39:729-736.
54. Orr, A. J., G. R. VanBlaricom, R. L. DeLong, V. H. Cruz-Escalona and S. D. Newsome. 2011. Intraspecific comparison of California sea lion (Zalophus californianus) diet assessed using fecal and stable isotope analyses. Canadian Journal of Zoology 89:109-122.
55. 15N in the marine environment. Advances in Marine Biology 24:389-451.
56. Peterson, B. J., and B. Fry. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18:293-320.
57. Phillips, D. L., and P. M. Eldridge. 2006. Estimating the timing of diet shifts using stable isotopes. Oecologia 147:195-203.
58. Polischuk, S. C., K. A. Hobson and M. A. Ramsay. 2001. Use of stable-carbon and -nitrogen isotopes to assess weaning and fasting in female polar bears and their cubs. Canadian Journal of Zoology 79:499-2001.
59. Porras-Peters, H., D. Aurioles-Gamboa, V. H. Cruz-Escalona and P. L. Koch. 2008. Trophic level and overlap of sea lions (Zalophus californianus) in the Gulf of California, Mexico. Marine Mammal Science 24:554-576.
60. R Development Core Team. 2006. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
61. 12C ratio changes with latitude: Differences between northern and southern oceans. Deep Sea Research 29:1035-1039.
62. Schell, D. M., S. M. Saupe and N. Haubenstock. 1989. Natural isotope abundances in bowhead whale (Balaena mysticetus) baleen: Markers of aging and habitat use. Ecological Studies 68:260-269.
63. Schier, D., J. Butler and R. Lewis. 1996. Human anatomy and physiology. McGraw-Hill Companies, Boston, MA.
64. Schmidt-Nielsen, K. 1984. Scaling: Why is body size so important? Cambridge University Press, Cambridge, UK.
65. 2 of alpacas (Lama pacos). Rapid Communications in Mass Spectrometry 20:1395-1399.
66. Thorson, P. H., and B. J. Le Boeuf. 1994. Developmental aspects of diving in northern elephant seal pups. Pages 271-289 in B. J. Le Boeuf and R. M. Laws, eds. Elephant seals: Population ecology, behavior, and physiology. University of California Press, Berkley, CA.
67. Tieszen, L. L., and T. W. Boutton. 1988. Stable carbon isotopes in terrestrial ecosystems research. Pages 167-195 in P. W. Rundel, J. R. Ehleringer, and K. A. Nagy, eds. Stable isotopes in ecological research. Springer-Verlag, Berlin, Germany.
68. 13C analysis of diet. Oecologia 57:32-37.
69. 15N enrichment: A meta-analysis. Oecologia 136:169-182.
70. Wada, E., H. Mizutani and M. Minagawa. 1991. The use of stable isotopes for food web analysis. Critical Reviews in Food Science and Nutrition 30:361-371.
71. Wood, S. N. 2006. Generalized additive models: An introduction with R. Chapman & Hall/CRC, Boca Raton, FL.
72. Wright, L. E., and H. P. Schwarcz. 1999. Correspondence between stable carbon, oxygen and nitrogen isotopes in human tooth enamel and dentine: Infant diets at Kaminaljuyu. Journal of Archaeological Science 26:1159-1170.
73. Zar, J. H. 1999. Biostatistical analysis. Prentice-Hall, Inc., Upper Saddle River, NJ.
74. 15N signatures of pinnipeds: Captive feeding studies with harbor seals (Phoca vitulina). Comparative Biochemistry and Physiology, Part A 143:469-478.