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

Volumn 367, Issue 1, 2008, Pages 1-10

  Jeanniard du Dot, Tiphaine ^a   Rosen, David A S ^a   Trites, Andrew W ^a  

^a Fisheries Center   (Canada)

Author keywords

Body composition; Compensatory growth; Diet; Nutritional stress; Sea lion

Indexed keywords

BODY CONDITION; CLUPEOID; COMPENSATION; DIET; ENVIRONMENTAL STRESS; FEEDING BEHAVIOR; FOOD AVAILABILITY; FOOD QUALITY; GADOID; NUTRIENT LIMITATION; PHYSIOLOGICAL RESPONSE; PINNIPED; SEASONAL VARIATION; WINTER;

ANIMALIA; CLUPEA PALLASI; CLUPEIDAE; EUMETOPIAS JUBATUS; OTARIIDAE; POLLACHIUS; THERAGRA CHALCOGRAMMA;

EID: 54349103198     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2008.08.005     Document Type: Article

References (103)

1. Adams S.H., and Costa D.P. Water conservation and protein metabolism in northern elephant seal pups during the postweaning fast. J. Comp. Physiol. B 163 (1993) 367-373
2. Ali M., Nicieza A., and Wootton R.J. Compensatory growth in fishes: a response to growth depression. Fish. Fish. 4 (2003) 147-190
3. Alvarez D., and Nicieza A.G. Compensatory response 'defends' energy levels but not growth trajectories in brown trout, Salmo trutta L. P. Roy. Soc. Lond. B Bio. 272 (2005) 601-607
4. Anderson S.S., and Fedak M.A. Grey seal males: Energetic and behavioural links between size and sexual success. Anim. Behav. 33 (1985) 829-838
5. Anthony J.A., Roby D.D., and Turco K.R. Lipid content and energy density of forage fishes from the northern Gulf of Alaska. J. Exp. Mar. Biol. Ecol. 248 (2000) 53-78
6. Arendt J.D. Adaptive intrinsic growth rates: an integration across taxa. Q. Rev. Biol. 72 (1997) 149-177
7. Arnould J.P.Y., Boyd I.L., and Speakman J.R. Measuring the body composition of Antarctic fur seals (Arctocephalus gazella): validation of hydrogen isotope dilution. Physiol. Zool. 69 (1996) 93-116
8. Baker J.D., Fowler C.W., and Antonelis G.A. Body weight and growth of juvenile male northern fur seals, Callorhinus ursinus. Mar. Mamm. Sci. 10 (1994) 151-162
9. Bjorndal K.A., Bolten A.B., Dellinger T., Delgado C., and Martins H.R. Compensatory growth in oceanic loggerhead sea turtles: Response to a stochastic environment. Ecology 84 (2003) 1237-1249
10. Boersma B., and Wit J.M. Catch-up growth. Endocr. Rev. 18 (1997) 646-661
11. Boltnev A.I., York A.E., and Antonelis G.A. Northern fur seal young: interrelationships among birth size, growth, and survival. Can. J. Zool. 76 (1998) 843-854
12. Boness D.J., Clapham P.J., and Mesnick S.L. Life history and reproductive strategies. In: Hoelzel A.R. (Ed). Marine mammal biology: an evolutionary approach (2002), Blackwell Science Publishing, Oxford 278-324
13. Bowen W.D., and Iverson S.J. Estimation of total body water in pinnipeds using hydrogen-isotope dilution. Physiol. Zool. 71 (1998) 329-332
14. Boyd I.L. Energetics: consequences for fitness. In: Hoelzel A.R. (Ed). Marine mammal biology: an evolutionary approach (2002), Blackwell Sciences Publishing, Oxford 247-277
15. Boyle P.C., Storlien L.H., Harper A.E., and Keesey R.E. Oxygen consumption and locomotor activity during restricted feeding and realimentation. Am. J. Physiol. 241 (1981) R392-397
16. Brosnan J.T., and Young V.R. Integration of metabolism 2: proteins and amino acids. In: Gibney M.J., Macdonald I., and Roche H.M. (Eds). Nutrition and Metabolism (2003), Blackwell Publishing, Oxford 43-73
17. Bryden M.M. Growth of the southern elephant seal, Mirounga leonina (Linn.). Growth 33 (1969) 69-82
18. Cahill G.F., Herrera M.G., Morgan A.P., Soeldner J.S., Steinke J., Levy P.L., Reichard G.A., and Kipins D.M. Hormone-fuel interrelationships during fasting. J. Clin. Invest. 45 (1966) 1751-1769
19. Castellini M.A., and Rea L.D. The biochemistry of natural fasting at its limits. Experientia 48 (1992) 575-582
20. Chambellant M., Beauplet G., Guinet C., and Georges J.Y. Long-term evaluation of pup growth and preweaning survival rates in subantarctic fur seals, Arctocephalus tropicalis, on Amsterdam Island. Can. J. Zool. 81 (2003) 1222-1232
21. Cherel Y., Robin J.P., Heitz A., Calgari C., and Le Maho Y. Relationships between lipid availability and protein utilization during prolonged fasting. J. Comp. Physiol. B 162 (1992) 305-313
22. Costa, D.P.,, 1987. Isotopic method for quantifying material and energy intake of free-ranging marine mammals. In: Huntley, A.C., Costa, D.P., Worthy, G.A.J., Castellini, M.A. (Eds.), Approaches to marine mammal energetics. Society for Marine Mammalogy. Allen Press, Lawrence, pp. 43-66.
23. Cummings D.E., and Overduin J. Gastrointestinal regulation of food intake. J. Clin. Invest. 117 (2007) 13-23
24. Cupples W.A. Physiological regulation of food intake. Am. J. Phys. 288 (2005) R1438-R1443
25. Depocas F., and Hart J.S. Use of the Pauling oxygen analyzer for measurement of oxygen consumption of animals in open-circuit systems and in a short-lag, closed-circuit apparatus. J. Appl. Physiol. 10 (1957) 388-392
26. Donnelly C.P., Trites A.W., and Kitts D.D. Possible effects of pollock and herring on the growth and reproductive success of Steller sea lions (Eumetopias jubatus): insights from feeding experiments using an alternative animal model, Rattus norvegicus. Br. J. Nutr. 89 (2003) 71-82
27. Fujita Y., Yamamoto T., Rikimaru T., Ebisawa H., and Inoue G. Effect of quality and quantity of dietary protein on free amino-acids in plasma and tissues of adult rats. J. Nutr. Sci. Vitaminol. 27 (1981) 129-147
28. Gibney M.J., Macdonald I., and Roche H.M. Nutrition and metabolism (2003), Blackwell Publishing, Oxford xiv, 385 pp.
29. Gòmez F., Galvan R.R., Frenk S., Muñoz J.C., Chavez R., and Vasquez J. Mortality in second and third degree malnutrition. Bull. World Health Organ. 78 (2000) 1275-1280
30. Gotthard K. Increased risk of predation as a cost of high growth rate: an experimental test in a butterfly. J. Anim. Ecol. 69 (2000) 896-902
31. Hales C.N., and Ozanne S.E. The dangerous road of catch-up growth. J. Physiol. 547 (2003) 5-10
32. Hall A., McConnell B.J., and Barker R.J. Factors affecting first-year survival in grey seals and their implications for life history strategy. J. Anim. Ecol. 70 (2001) 138-149
33. Harding K.C., Fujiwara M., Axberg Y., and Harkonen T. Mass-dependent energetics and survival in harbour seal pups. Funct. Ecol. 19 (2005) 129-135
34. Heath R.G.M., and Randall R.M. Growth of jackass penguin chicks (Spheniscus demersus) hand reared on different diets. J. Zool. 205 (1985) 91-105
35. Jespersen L.B., and Toft S. Compensatory growth following early nutritional stress in the wolf spider Pardosa prativaga. Funct. Ecol. 17 (2003) 737-746
36. Jodice P.G.R., Roby D.D., Turco K.R., Suryan R.M., Irons D.B., Piatt J.F., Shultz M.T., Roseneau D.G., Kettle A.B., and Anthony J.A. Assessing the nutritional stress hypothesis: relative influence of diet quantity and quality on seabird productivity. Mar. Ecol.-Prog. Ser. 325 (2006) 267-279
37. Johnsson J.I., and Bohlin T. Compensatory growth for free? A field experiment on brown trout, Salmo trutta. Oikos 111 (2005) 31-38
38. Johnsson J.I., and Bohlin T. The cost of catching up: increased winter mortality following structural growth compensation in the wild. P. Roy. Soc. Lond. B Bio. 273 (2006) 1281-1286
39. Jonsson E., Johnsson J.I., and Bjornsson B.T. Growth hormone increases predation exposure of rainbow trout. P. Roy. Soc. Lond. B Bio. 263 (1996) 647-651
40. Kastelein R.A., Vaughan N., and Wiepkema P.R. The food consumption of Steller sea lions (Eumetopias jubatus). Aquat. Mamm. 15 (1990) 137-144
41. Kastelein R., Schooneman N.M., Vaughan N., and Wiepkema P.R. Food consumption and growth of California sea lions (Zalophus californianus californianus). Zoo Biol. 19 (2000) 143-159
42. Keiver K.M., Ronald K., and Beamish F.W.H. Metabolizable energy requirements for maintenance and fecal and urinary losses of juvenile harp seals (Phoca groenlandica). Can. J. Zool. 62 (1984) 769-776
43. Kerr B.J., and Easter R.A. Effects of feeding reduced protein, amino acid supplemented diets on nitrogen and energy balance in grower pigs. J. Anim. Sci. 73 (1995) 3000-3008
44. Kirsch P.E., Iverson S.J., and Bowen W.D. Effect of a low-fat diet on body composition and blubber fatty acids of captive juvenile harp seals (Phoca groenlandica). Physiol. Biochem. Zool. 73 (2000) 45-59
45. Kitts D.D., Huynh M.D., Hu C., and Trites A.W. Seasonal variation in nutrient composition of Alaskan walleye pollock. Can. J. Zool. 82 (2004) 1408-1415
46. Klasing K.C. Influence of stress on protein metabolism. In: Moberg G.P. (Ed). Animal stress (1985), American Physiological Society, Bethesda, Maryland 269-280
47. Kleiber M. The fire of life: an introduction to animal energetics (1975), R. E. Krieger Pub. Co., Huntington, N.Y. xxii, 453 pp
48. Konarzewski M., Kowalczyk J., Swierubska T., and Lewonczuk B. Effects of long-term feed restriction, realimentation and overfeeding on growth of song thrush (Turdus philomelos) nestlings. Funct. Ecol. 10 (1996) 97-105
49. Kumagai S. Seasonal differences in physiology of captive Steller sea lions (Eumetopias jubatus) in response to short term low energy intake. Faculty of Graduate studies- Zoology (2004), University of British Columbia, Vancouver 95
50. Kumagai S., Rosen D.A.S., and Trites A.W. Body mass and composition responses to short-term low energy intake are seasonally dependent in Steller sea lions (Eumetopias jubatus). J. Comp. Physiol. B 176 (2006) 589-598
51. Le Boeuf B.J. Variation in the diving pattern of northern elephant seals with age, mass, sex, and reproductive condition. In: Le Boeuf B.J., and Laws R.M. (Eds). Elephant seals (1994), University of California Press, Berkeley 237-252
52. Markussen N.H., Ryg M., and Øritsland N.A. Metabolic rate and body composition of harbour seals, Phoca vitulina, during starvation and refeeding. Can. J. Zool. 70 (1992) 220-224
53. McNab B.K. The physiological ecology of vertebrates: a view from energetics (2002), Cornell University Press, Ithaca xxvii, 576 p. pp.
54. McNamara J.M., and Houston A.I. The value of fat reserves and the tradeoff between starvation and predation. Acta Biotheor. 38 (1990) 37-61
55. Merrick R.L., Chumbley M.K., and Byrd G.V. Diet diversity of Steller sea lions (Eumetopias jubatus) and their population decline in Alaska: a potential relationship. Can. J. Fish. Aquat. Sci. 54 (1997) 1342-1348
56. Metcalfe N.B., and Monaghan P. Compensation for a bad start: grow now, pay later?. Trends Ecol. Evol. 16 (2001) 254-260
57. Miglavs I., and Jobling M. The effects of feeding regime on proximate body composition and patterns of energy deposition in juvenile Arctic charr, Salvelinus alpinus. J. Fish. Biol. 35 (1989) 1-11
58. Millward D.J., Garlick P.J., and Reeds P.J. Energy cost of growth. Proc. Nutr. Soc. 35 (1976) 339-349
59. Moundras C., Remesy C., and Demigne C. Dietary protein paradox- decrease of amino-acid availability induced by high protein diets. Am. J. Phys. 264 (1993) G1057-G1065
60. Muelbert M.M., Bowen W.D., and Iverson S.J. Weaning mass affects changes in body composition and food intake in harbour seal pups during the first month of independence. Physiol. Biochem. Zool. 76 (2003) 418-427
61. Nicieza A.G., and Metcalfe N.B. Growth compensation in juvenile Atlantic salmon: Responses to depressed temperature and food availability. Ecology 78 (1997) 2385-2400
62. Oftedal O.T., and Iverson S.J. Hydrogen isotope methodology for measurement of milk intake and energetics of growth in suckling young. In: Huntley A.D., Costa D.P., Worthy G.A.J., and Castellini M.A. (Eds). Approaches to Marine Mammal Energetics (1987), Society for Marine Mammalogy, Lawrence, Kansas 67-96
63. Ortiz C.L., Costa D.P., and Le Boeuf B.J. Water and energy flux in elephant seal pups fasting under natural conditions. Physiol. Zool. 51 (1978) 166-178
64. Peters J.C., and Harper A.E. Adaptation of rats to diets containing different levels of protein- effects of food intake, plasma and brain amino acid concentrations and brain neurotransmitter metabolism. J. Nutr. 115 (1985) 382-398
65. Pinheiro J.C., and Bates D.M. Mixed-Effects Models in S and S-PLUS (2000), Springer-Verlag, New York
66. Pinheiro J., Bates D., DebRoy S., and Sarkar D. nlme: Linear and nonlinear mixed effects models (2006)
67. Pitcher K.W., Calkins D.G., and Pendleton G.W. Reproductive performance of female Steller sea lions: an energetics-based reproductive strategy?. Can. J. Zool. 76 (1998) 2075-2083
68. Pitts G.C. Cellular aspects of growth and catch-up growth in the rat : a reevaluation. Growth 50 (1986) 419-436
69. Pullar J.D., and Webster A.J.F. Energy cost of fat and protein deposition in rat. Br. J. Nutr. 37 (1977) 355-363
70. Qian X., Cui Y., Xiong B., and Yang Y. Compensatory growth, feed utilization and activity in gibel carp, following food deprivation. J. Fish. Biol. 56 (2000) 228-232
71. Rea L.D., Rosen D.A.S., and Trites A.W. Metabolic response to fasting in 6-week-old Steller sea lion pups (Eumetopias jubatus). Can. J. Zool. 78 (2000) 890-894
72. Rea L.D., Rosen D.A.S., and Trites A.W. Utilization of stored energy reserves during fasting varies by age and season in Steller sea lions. Can. J. Zool. 85 (2007) 190-200
73. Reilly J.J., and Fedak M.A. Measurement of the body composition of living gray seals by hydrogen isotope dilution. J. Appl. Physiol. 69 (1990) 885-891
74. Reimers E., Kjorrefjord A.G., and Stavostrand S.M. Compensatory growth and reduced maturation in second sea winter farmed Atlantic salmon following starvation in February and March. J. Fish. Biol. 43 (1993) 805-810
75. Renouf D., and Noseworthy E. Changes in food intake, mass, and fat accumulation in association with variations in thyroid hormone levels of harbour seals (Phoca vitulina). Can. J. Zool. 69 (1991) 2470-2479
76. Ridgway S.H. Homeostasis in the aquatic environment. In: Ridgway S.H. (Ed). Mammals of the sea: Biology and medicine (1972), Charles C. Thomas, Springfield, Ill 590-747
77. Roach J.O., Benyon S., and Dominiczak M. Metabolism and nutrition. 2d ed. (2003), Elsevier Science Ltd, London 263 pp.
78. Romano M.D., Piatt J.F., and Roby D.D. Testing the junk-food hypothesis on marine birds: effects of prey type on growth and development. Waterbirds 29 (2006) 407-414
79. Rosen D.A.S., and Renouf D. Seasonal changes in blubber distribution in Atlantic harbor seals: indications of thermodynamic considerations. Mar. Mamm. Sci. 13 (1997) 229-240
80. Rosen D.A.S., and Renouf D. Correlates of seasonal changes in metabolism in Atlantic harbour seals (Phoca vitulina concolor). Can. J. Zool. 76 (1998) 1520-1528
81. Rosen D.A.S., and Trites A.W. Pollock and the decline of Steller sea lions: testing the junk-food hypothesis. Can. J. Zool. 78 (2000) 1243-1250
82. Rosen D.A.S., and Trites A.W. Satiation and compensation for short-term changes in food quality and availability in young Steller sea lions (Eumetopias jubatus). Can. J. Zool. 82 (2004) 1061-1069
83. Rosen D.A., and Trites A.W. Examining the potential for nutritional stress in young Steller sea lions: physiological effects of prey composition. J. Comp. Physiol. B 175 (2005) 265-273
84. Rosen D.A., Winship A.J., and Hoopes L.A. Thermal and digestive constraints to foraging behavior in marine mammals. Philos. Trans. R. Soc. Lond. [Biol] 362 (2007) 2451-2168
85. Royle N. Overproduction in the lesser black-backed gull- can marginal chicks overcome the initial handicap of hatching asynchrony?. J. Avian Biol. 31 (2000) 335-344
86. Russell N.G., and Wootton R.J. Appetite and growth compensation in the European minnow, Phoxinus phoxinus (Cyprinidae), following short periods of food restriction. Environ. Biol. Fishes 34 (1992) 277-285
87. Schmidt-Nielsen K. Animal physiology: adaptation and environment (1997), Cambridge University Press, Cambridge, England viii, 607 p. pp.
88. Sigler M.F., Womble J.N., and Vollenweider J.J. Availability to Steller sea lions (Eumetopias jubatus) of a seasonal prey resource: a prespawning aggregation of eulachon (Thaleichthys pacificus). Can. J. Fish. Aquat. Sci. 61 (2004) 1475-1484
89. Trites A.W., and Donnelly C.P. The decline of Steller sea lions Eumetopias jubatus in Alaska: a review of the nutritional stress hypothesis. Mamm. Rev. 33 (2003) 3-28
90. Vaz M. Undernutrition. In: Gibney M.J., Macdonald I., and Roche H.M. (Eds). Nutrition and Metabolism (2003), Blackwell Publishing, Oxford 341-348
91. Victora C.G., Barros F.C., Horta B.L., and Martorell R. Short-term benefits of catch-up growth for small-for-gestational-age infants. Int. J. Epidemiol. 30 (2001) 1325-1330
92. Waterlow J.C. Metabolic adaptation to low intakes of energy and protein. Annu. Rev. Nutr. 6 (1986) 495-526
93. Waterlow J.C. Whole body protein turnover in humans- past, present, and future. Annu. Rev. Nutr. 15 (1995) 57-92
94. Webster A.J.F. The energetic efficiency of metabolism. Proceedings, the Nutrition Society vol. 40 (1981) 121-128
95. Whang K.Y., Kim S.W., Donovan S.M., McKeith F.K., and Easter R.A. Effects of protein deprivation on subsequent growth performance, gain of body components, and protein requirements in growing pigs. J. Anim. Sci. 81 (2003) 705-716
96. Wilson P.N., and Osbourn D.F. Compensatory growth after undernutrition in mammals and birds. Biol. Rev. Camb. Philos. Soc. 35 (1960) 324-363
97. Winship A.J., Trites A.W., and Rosen D.A.S. A bioenergetic model for estimating the food requirements of Steller sea lions Eumetopias jubatus in Alaska, USA. Mar. Ecol.-Prog. Ser. 229 (2002) 291-312
98. Womble J.N., Willson M.F., Sigler M.F., Kelly B.P., and VanBlaricom G.R. Distribution of Steller sea lions Eumetopias jubatus in relation to spring-spawning fish in SE Alaska. Mar. Ecol.-Prog. Ser. 294 (2005) 271-282
99. Worthy G.A.J. Nutrition and energetics. In: Dierauf L.A., and Gulland F.M.D. (Eds). CRC Handbook of Marine Mammal Medicine (2001), CRC Press, London 791-827
100. Xie S., Zhu X., Cui Y., Wootton R.J., Lei W., and Yang Y. Compensatory growth in the gibel carp following feed deprivation: temporal patterns in growth, nutrient deposition, feed intake and body composition. J. Fish. Biol. 58 (2001) 999-1009
101. Yambayamba E.S., Price M.A., and Foxcroft G.R. Hormonal status, metabolic changes, and resting metabolic rate in beef heifers undergoing compensatory growth. J. Anim. Sci. 74 (1996) 57-69
102. Zhao L., Castellini M.A., and Schell D.M. Metabolic adjustments to varying protein intake in harbor seals (Phoca vitulina): evidence from serum free amino acids. Physiol. Biochem. Zool. 79 (2006) 965-976
103. Zubair A.K., and Leeson S. Compensatory growth in broiler chicken: a review. World Poult. Sci. J. 52 (1996) 189-201