Steller sea lions Eumetopias jubatus and nutritional stress: Evidence from captive studies

Mammal Review

Volumn 39, Issue 4, 2009, Pages 284-306

  Rosen, David A S ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Conservation; Diet; Metabolism; Nutrition; Pinnipeds

Indexed keywords

DIET; FEEDING BEHAVIOR; FOOD AVAILABILITY; FOOD CONSUMPTION; FOOD INTAKE; HYPOTHESIS TESTING; LABORATORY METHOD; METABOLISM; NUTRITIONAL REQUIREMENT; NUTRITIONAL STATUS; PINNIPED; POPULATION DECLINE; STRESS;

PACIFIC OCEAN; PACIFIC OCEAN (NORTH);

ANIMALIA; EUMETOPIAS JUBATUS; OTARIIDAE; PINNIPEDIA;

EID: 74049104558     PISSN: 03051838     EISSN: 13652907     Source Type: Journal    
DOI: 10.1111/j.1365-2907.2009.00150.x     Document Type: Review

References (79)

1. Allen, P.C. (2009) Seasonal oscillations in the mass and food intake of Steller sea lions. MSc Thesis, University of British Columbia, Vancouver, BC, Canada.
2. Alverson, D.L. (1992) A review of commercial fisheries and the Steller sea lion (Eumetopias jubatus): the conflict arena. Reviews in Aquatic Science, 6, 203-256.
3. Anonymous (1981) Nutritional Energetics of Domestic Animals & Glossary of Energy Terms. National Research Council (US) National Academy Press, Washington, DC, USA.
4. Anonymous (1993) Is It Food? Addressing Marine Mammal and Sea Bird Declines. Alaska Sea Grant Report 93-01, Fairbanks, AK, USA.
5. Anonymous (2003) Decline of the Steller Sea Lion in Alaskan Waters: Untangling Food Webs and Fishing Nets. National Research Council (US) Committee on the Alaska Groundfish Fishery and Steller Sea Lions National Academies Press, Washington, DC, USA.
6. Anonymous (2008) Recovery plan for the Steller sea lion (Eumetopias jubatus). Revision. National Marine Fisheries Service, Silver Spring. Maryland, USA.
7. Ashwell-Erickson, S. & Elsner, R. (1981) The energy cost of free existence for Bering Sea harbor and spotted seals. In: The Eastern Bering Sea Shelf: Oceanography and Resources (Ed. by D.W. Hood & J.A. Calder), pp. 869-899. University of Washington Press, Seattle, WA, USA.
8. Atkinson, S., Calkins, D.G., Burkanov, V., Castellini, M.A., Hennen, D.R. & Inglis, S. (2008a) Impact of changing diet regimes on Steller sea lion body condition. Marine Mammal Science, 24, 276-289.
9. Atkinson, S., DeMaster, D.P. & Calkins, D.G. (2008b) Anthropogenic causes of the western Steller sea lion Eumetopias jubatus population decline and their threat to recovery. Mammal Review, 38, 1-18.
10. Barbour, A.S. (1993) Heat increment of feeding in juvenile northern elephant seals. MSc Thesis, University of California, Santa Cruz, California, USA.
11. Blaxter, K. (1989) Energy Metabolism in Animals and Man. Cambridge University Press, Cambridge, UK.
12. Blaxter, K.L. & Boyne, A.W. (1978) The estimation of the nutritive value of feeds as energy sources for ruminants and the derivation of feeding systems. Journal of Agricultural Science (Cambridge), 90, 47-68.
13. Calder, W.A. (1984) Size, Function and Life History. Harvard University Press, Cambridge, MA, USA.
14. Calkins, D. & Goodwin, E. (1988) Investigation of the declining sea lion population in the Gulf of Alaska. Unpublished report to Alaska Dept of Fish and Game, 333 Raspberry Road, Anchorage, AK, 99518.
15. Castellini, M.A. & Calkins, D.G. (1993) Mass estimates using body morphology in Steller sea lions. Marine Mammal Science, 9, 48-54.
16. Castellini, M.A. & Rea, L.D. (1992) The biochemistry of natural fasting at its limits. Experientia, 48, 575-582.
17. Fadely, B.S., Worthy, G.A.J. & Costa, D.P. (1990) Assimilation efficiency of northern fur seals determined using dietary manganese. Journal of Wildlife Management, 54, 246-251.
18. Fadely, B.S., Zeligs, J.A. & Costa, D.P. (1994) Assimilation efficiencies and maintenance requirements of California sea lions (Zalophus californianus) fed walleye pollock (Theragra chalcogramma) and herring (Clupea harengus). Final report to National Marine Mammal Laboratory, National Marine Fisheries Service, 7600 Sand Point Way, Seattle, WA, USA.
19. Fritz, L. & Hinckley, S. (2005) A critical review of the regime shift - 'junk food' - nutritional stress hypothesis for the decline of the western stock of Steller sea lion. Marine Mammal Science, 21, 476-518.
20. Gende, S.M. & Sigler, M.F. (2006) Persistence of forage fish 'hot spots' and its association with foraging Steller sea lions (Eumetopias jubatus) in southeast Alaska. Deep Sea Research Part II, 53, 432-441.
21. Goodman-Lowe, G.D., Atkinson, S. & Carpenter, J.R. (1997) Initial defecation time and rate of passage of digesta in adult Hawaiian monk seals, Monachus schauinslandi. Canadian Journal of Zoology, 75, 433-438.
22. Guenette, S., Heymans, S.J.J., Christensen, V. & Trites, A.W. (2006) Ecosystem models show combined effects of fishing, predation, competition, and ocean productivity on Steller sea lions (Eumetopias jubatus)in Alaska. Canadian Journal of Fisheries and Aquatic Sciences, 63, 2495-2517.
23. Guppy, M. & Withers, P. (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biological Review, 74, 1-40.
24. Harris, L.E. (1966) Biological energy interrelationships and glossary of energy terms. Publication of the National Academy of Science, National Research Council U.S., 1411, 1-35.
25. Helm, R.C. (1984) Rate of digestion in three species of pinnipeds. Canadian Journal of Zoology, 62, 1751-1756.
26. Hilton, G.M., Houston, D.C., Barton, N.W.H., Furness, R.W. & Ruxton, G.D. (1999) Ecological constraints on digestive physiology in carnivorous and piscivorous birds. Journal of Experimental Zoology, 283, 365-376.
27. Holmes, E.E., Fritz, L.W., York, A.E. & Sweeney, K. (2007) Age-structured modeling reveals long-term declines in the natality of western Steller sea lions. Ecological Applications, 17, 2214-2232.
28. Jeanniard du Dot, T. (2007) Diet quality and season affect physiology and energetic priorities of captive Steller sea lions during and after periods of nutritional stress. MSc Thesis, University of British Columbia, Vancouver, BC, Canada.
29. Jeanniard du Dot, T., Rosen, D.A.S. & Trites, A.W. (2008) Steller sea lions show diet-dependent changes in body composition during nutritional stress and recover more easily from mass loss in winter than in summer. Journal of Experimental Marine Biology and Ecology, 377, 1-10.
30. Jeanniard du Dot, T., Rosen, D.A.S., Richmond, J.P., Kitaysky, A.S., Zinn, S.A. & Trites, A.W. (2009a) Changes in glucocorticoids, IGF-1 and thyroid hormones as indicators of nutritional stress and subsequent refeeding in Steller sea lions (Eumetopias jubatus). Comparative Biochemistry and Physiology A, 152, 524-534.
31. Jeanniard du Dot, T., Rosen, D.A.S. & Trites, A.W. (2009b) Energy reallocation during and after periods of nutritional stress in Steller sea lions: low-quality diet reduces capacity for physiological adjustments. Physiological and Biochemical Zoology, 82, 516-530.
32. Karasov, W.H. & Diamond, J. (1988) Interplay between physiology and ecology in digestion. Bioscience, 38, 602-611.
33. King, J.R. & Murphy, M.E. (1985) Periods of nutritional stress in the annual cycles of endotherms: fact or fiction? American Zoologist, 25, 955-964.
34. Kirsch, P.E., Iverson, S.J. & Bowen, W.D. (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.
35. Kleiber, M. (1975) The Fire of Life: an Introduction to Animal Energetics. Robert E. Krieger Publ. Co., New York, USA.
36. Krockenberger, M.B. & Bryden, M.M. (1994) Rate of passage through the alimentary tract of southern elephant seals (Mirounga leonina) (Carnovira: Phocidae). Journal of Zoology, London, 234, 229-237.
37. Kumagai, S., Rosen, D.A.S. & Trites, A.W. (2006) Body mass and composition responses to short-term low energy intake are seasonally dependent in Steller sea lions (Eumetopias jubatus). Journal of Comparative Physiology B, 176, 589-598.
38. Lavigne, D.M., Barchard, W., Innes, S. & Øritsland, N.A. (1982) Pinniped bioenergetics. In: Mammals in the Seas: Small Cetaceans, Seals, Sirenians and Otters. Food and Agriculture Organization, United Nations Working Party on Marine Mammals. FAO (Rome) Fisheries Series, Vol. 4, pp. 191-235. FAO, Rome, Italy.
39. Lawson, J.W., Miller, E.H. & Noseworthy, E. (1997) Variation in assimilation efficiency and digestive efficiency of captive harp seals (Phoca groenlandica) on different diets. Canadian Journal of Zoology, 75, 1285-1291.
40. Logerwell, E.A. & Schaufler, L.E. (2005) New data on proximate composition and energy density of Steller sea lion (Eumetopias jubatus) prey fills seasonal and geographic gaps in existing information. Aquatic Mammals, 31, 62-82.
41. Loughlin, T.R. & York, A.E. (2000) An accounting of the sources of Steller sea lion, Eumetopias jubatus, mortality. Marine Fisheries Review, 62, 40-45.
42. Malavear, M.Y. (2002) Modelling the energetics of Steller sea lions (Eumetopias jubatus) along the Oregon coast. MSc Thesis, Oregon State University, Corvallis, Oregon, USA.
43. Mazzaro, L.M., Dunn, J.L., Furr, H.C. & Clark, R.M. (2003) Serum retinol, alpha-tocopherol, and lipids in four species of adult captive pinnipeds. Zoo Biology, 22, 83-96.
44. Merrick, R.L., Chumbley, M.K. & Byrd, G.V. (1997) Diet diversity of Steller sea lions (Eumetopias jubatus) and their population decline in Alaska: a potential relationship. Canadian Journal of Fisheries and Aquatic Sciences, 54, 1342-1348.
45. Morell, V. (2008) Puzzling over a Steller whodunit. Science, 320, 44-45.
46. Pitcher, K.W. & Calkins, D.G. (1981) Reproductive biology of Steller sea lions in the Gulf of Alaska. Journal of Mammology, 62, 599-605.
47. Pitcher, K.W., Calkins, D.G. & Pendleton, G. (1998) Reproductive performance of female Steller sea lions: an energetics-based reproductive strategy? Canadian Journal of Zoology, 76, 2075-2083.
48. Rea, L.D., Rosen, D.A.S. & Trites, A.W. (2000) Metabolic response to fasting in 6-week-old Steller sea lion pups (Eumetopias jubatus). Canadian Journal of Zoology, 78, 890-894.
49. Rea, L.D., Rosen, D.A.S. & Trites, A.W. (2007) Utilization of stored energy reserves during fasting varies by age and season in Steller sea lions. Canadian Journal of Zoology, 85, 190-200.
50. Rea, L.D., Berman-Kowalewski, M., Rosen, D.A.S. & Trites, A.W. (2009) Seasonal differences in biochemical adaptation to fasting in juvenile and subadult Steller sea lions (Eumetopias jubatus). Physiological and Biochemical Zoology, 82, 236-247.
51. Richmond, J.P., Burns, J.M. & Rea, L. (2006) Ontogeny of total body oxygen stores and aerobic dive potential in Steller sea lions (Eumetopias jubatus). Journal of Comparative Physiology B, 176, 535-545.
52. Rosen, D.A.S. & Kumagai, S. (2008) Hormone changes indicate that winter is a critical period for food shortages in Steller sea lions. Journal of Comparative Physiology B, 178, 573-583.
53. Rosen, D.A.S. & Renouf, D. (1998) Correlates to seasonal changes in metabolism in Atlantic harbour seals (Phoca vitulina concolor). Canadian Journal of Zoology, 76, 1520-1528.
54. Rosen, D.A.S. & Trites, A.W. (1997) Heat increment of feeding in Steller sea lions, Eumetopias jubatus. Comparative Biochemistry and Physiology A, 118, 877-881.
55. Rosen, D.A.S. & Trites, A.W. (1999) Metabolic effects of low-energy diet on Steller sea lions, Eumetopias jubatus. Physiological and Biochemical Zoology, 72, 723-731.
56. Rosen, D.A.S. & Trites, A.W. (2000a) Digestive efficiency and dry-matter digestibility of Steller sea lions fed herring, pollock, squid, and salmon. Canadian Journal of Zoology, 78, 234-239.
57. Rosen, D.A.S. & Trites, A.W. (2000b) Pollock and the decline of Steller sea lions: testing the junk food hypothesis. Canadian Journal of Zoology, 78, 1243-1250.
58. Rosen, D.A.S. & Trites, A.W. (2002) Changes in metabolism in response to fasting and food restriction in the Steller sea lion. Comparative Biochemistry and Physiology B, 132, 389-399.
59. Rosen, D.A.S. & Trites, A.W. (2004) Satiation and compensation for short-term changes in food quality and availability in young Steller sea lions (Eumetopias jubatus). Canadian Journal of Zoology, 82, 1061-1069.
60. Rosen, D.A.S. & Trites, A.W. (2005) Examining the potential for nutritional stress in Steller sea lions: physiological effects of prey composition. Journal of Comparative Physiology B, 175, 265-273.
61. Rosen, D.A.S., Winship, A.J. & Hoopes, L.A. (2007) Thermal and digestive constraints to foraging behavior in marine mammals. Philosophical Transactions, Royal Society of London B, 362, 2151-2168.
62. Schmidt-Nielsen, K. (1984) Scaling: Why is Animal Size so Important? Cambridge University Press, Cambridge, UK.
63. Sinclair, E.H. & Zeppelin, T.K. (2002) Seasonal and spatial differences in diet in the western stock of Steller sea lions (Eumetopias jubatus). Journal of Mammology, 83, 973-990.
64. Stanberry, K. (2003) The effect of changes in dietary fat level on body composition, blood metabolites and hormones, rate of passage, and nutrient assimilation efficiency in harbor seals. MSc Thesis, University of Hawaii, Honolulu, Hawaii, USA.
65. Stansby, M.E. (1976) Proximate composition of fish and shellfish. Marine Fisheries Review, 1198, 3-4.
66. Thompson, P.M., Tollit, D.J., Corpe, H.M., Reid, R.J. & Ross, H.M. (1997) Changes in haemotological parameters in relation to prey switching in a wild population of harbour seals. Functional Ecology, 11, 743-750.
67. Trites, A.W., Porter, B.P., Deecke, V.B., Coombs, A.P. & Rosen, D.A.S. (2006) Insights into the timing of weaning and the attendance patterns of lactating Steller sea lions (Eumetopias jubatus) in Alaska during winter, spring and summer. Aquatic Mammals, 323, 85-97.
68. Trites, A.W., Calkins, D.G. & Winship, A.J. (2007) Diets of Steller sea lions (Eumetopias jubatus) in Southeast Alaska, 1993-1999. Fishery Bulletin, 105, 234-248.
69. Trumble, S.J. & Castellini, M.A. (2005) Diet mixing in an aquatic carnivore, the harbour seal. Canadian Journal of Zoology, 83, 851-859.
70. Trumble, S.J., Barboza, P.S. & Castellini, M.A. (2003) Digestive constraints on an aquatic carnivore: effects of feeding frequency and prey composition on harbor seals. Journal of Comparative Physiology B, 173, 501-509.
71. Trumble, S.J., Castellini, M.A., Mau, T.L. & Castellini, J.M. (2006) Dietary and seasonal influences on blood chemistry and hematology in captive harbor seals. Marine Mammal Science, 22, 104-123.
72. Vollenweider, J.J. (2004) Variability in Steller sea lion (Eumetopias jubatus) prey quality in southeastern Alaska. MSc Thesis, University of Alaska, Fairbanks, USA.
73. Webster, A.J.F. (1981) The energetic efficiency of metabolism. Proceedings, the Nutrition Society, 40, 121-128.
74. Weiner, J. (1992) Physiological limits to sustainable energy budgets in birds and mammals: ecological implications. Trends in Ecology and Evolution, 7, 384-388.
75. Winship, A.J. & Trites, A.W. (2003) Prey consumption of Steller sea lions (Eumetopias jubatus) off Alaska: how much prey do they require? Fisheries Bulletin United States, 101, 147-163.
76. Winship, A.J., Trites, A.W. & Rosen, D.A.S. (2002) A bioenergetic model for estimating the food requirements of Steller sea lions (Eumetopias jubatus) in Alaska. Marine Ecology Progress Series, 229, 291-312.
77. York, A.E. (1994) The population dynamics of Northern sea lions, 1975-1985. Marine Mammal Science, 10, 38-51.
78. Zeppelin, T.K., Tollit, D.J., Call, K.A., Orchard, T.J. & Gudmundson, C.J. (2004) Sizes of walleye pollock (Theragra chalcogramma) and Atka mackerel (Pleurogrammus monopterygius) consumed by the western stock of Steller sea lions (Eumetopias jubatus) in Alaska from 1998 to 2000. Fishery Bulletin, 102, 509-521.
79. Zhao, L., Castellini, J.M. & Schell, D.M. (2006) Metabolic adjustments to varying protein intake in harbor seals (Phoca vitulina): evidence from serum free amino acids. Physiological and Biochemical Zoology, 79, 965-976.