Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-15T21:18:36.489Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  09 March 2007

Carolyn P. Donnelly
Affiliation:
Marine Mammal Research Unit, The University of British Columbia, Room 18, Hut B-3, 6248 Biological Sciences Road, Vancouver, British Columbia, V6T 1Z4, Canada
A. W. Trites*
Affiliation:
Marine Mammal Research Unit, The University of British Columbia, Room 18, Hut B-3, 6248 Biological Sciences Road, Vancouver, British Columbia, V6T 1Z4, Canada
D. D. Kitts
Affiliation:
Food Nutrition and Health, The University of British Columbia, 6650 NW Marine Drive, Vancouver, British Columbia, V6T 1Z4, Canada
*
*Corresponding Author: Dr Andrew W. Trites, fax +1 604 822 8180, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The decline of Steller sea lions (Eumetopias jubatus) in the Gulf of Alaska appears to have been associated with a switch of diet from one dominated by fatty forage fishes (such as herring; Clupea pallasi) to one dominated by low-fat fish (such as pollock; Theragra chalcogramma). Observations made during the decline include reduced body size of sea lions, low pregnancy rates, and high mortality. We used the general mammalian model, the laboratory rat (Rattus norvegicus), to test whether changing the quality of prey consumed could cause changes in size and reproductive performance. Five groups of twelve female, weanling rats were fed diets composed of herring (H), pollock (P), pollock supplemented with herring oil (PH), pollock supplemented with pollock oil (PP), or a semi-purified diet (ICN). Mean body weights were greatest for H, followed by PH, P, PP and finally ICN, although ICN was the only group significantly different from the others (P<0·05). Food intakes before mating were 10 % higher for groups on the lower-fat diets (P and ICN), resulting in similar energy intakes in all groups. The protein efficiency ratio was highest for the H diet, slightly lower for all pollock diets, and significantly lower for ICN (P<0·05). The fetal weights for mothers fed P were significantly reduced (P<0·05). The present study shows that the energy content was a major limiting factor in the nutritional quality of pollock. When food intake was adjusted to meet energetic requirements, there were no detrimental consequences from eating pollock. However, supplementation of pollock meal with additional pollock oil may reduce growth and reproductive performance, although the reasons for this were not apparent.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2003

References

Abel, EL (1990) Effects of paternal and maternal undernutrition on growth of offspring in rats. Growth, Development and Aging 54, 125129.Google Scholar
Ackroff, K & Sclafani, A (1996) Rats integrate meal cost and postoral changes in caloric density. Physiology and Behavior 60, 927932.CrossRefGoogle ScholarPubMed
Alaska Sea Grant, (1993) Is it Food? Addressing Marine Mammal and Seabird Declines, pp. 59. Fairbanks, AK: Alaska Sea Grant College Program.Google Scholar
Alverson, DL (1992) A review of commercial fisheries and the Steller sea lion (Eumetopias jubatus): the conflict arena. Reviews in Aquatic Sciences 6, 203256.Google Scholar
AOAC (2000) Official Method 965·33. Official Methods of Analysis of the Association of Official Analytical Chemists. Washington DC: AOAC.Google Scholar
Arrington, LR (1978) Introductory Laboratory Animal Science; The Breeding, Care and Management of Experimental Animals, 2nd ed, Danville, IL: The Interstate Printers and Publishers, Inc.Google Scholar
Arts, MT, Ackman, RG & Holub, BJ (2001) "Essential fatty acids" in aquatic ecosystems: a crucial link between diet and human health and evolution. Canadian Journal of Fisheries and Aquatic Science 58, 122137.CrossRefGoogle Scholar
Beck, B, Strickler-Krongrad, A, Burlet, A, Nicolas, J-P & Burlet, C (1990) Influence of diet composition on food intake and hypothalamic neuropeptide Y (NPY) in the rat. Neuropeptides 17, 197203.CrossRefGoogle ScholarPubMed
Bennet, JP & Vichery, BH (1970) Rats and mice. In Reproduction and Breeding Techniques for Laboratory Animals, pp. 299315 [Hafez, ESE, editor]. Philadelphia: Lea & Febiger.Google Scholar
Benson, AJ & Trites, AW (2002) A review of the effects of regime shifts on the production domains in the eastern North Pacific Ocean. Fish and Fisheries 3, 95113.CrossRefGoogle Scholar
Blank, JL & Desgardins, C (1984) Spermatogenesis is modified by food intake in mice. Biology of Reproduction 30, 410415.Google Scholar
Bronson, FH (1988) Effect of food manipulation on the GnRH-LH-estradiol axis of young female rats. American Journal of Physiology 254, R616R621.Google Scholar
Bulik, CM, Sullivan, PF, Fear, JL, Pickering, A, Dawn, A & McCullin, M (1999) Fertility and reproduction in women with anorexia nervosa: a controlled study. Journal of Clinical Psychiatry 60, 130135.CrossRefGoogle ScholarPubMed
Burton-Freeman, B, Gietzen, DW & Schneeman, BO (1999) Cholecystokinin and serotonin receptors in the regulation of fat-induced satiety in rats. American Journal of Physiology 276, R429R434.Google Scholar
Calkins, DG, Becker, EF & Pitcher, KW (1998) Reduced body size of female Steller sea lions from a declining population in the Gulf of Alaska. Marine Mammal Science 14, 232244.Google Scholar
Calkins, DG, McAllister, DC & Pitcher, KW (1999) Steller sea lions status and trend in southeast Alaska: 1979–1997. Marine Mammal Science 15, 462477.Google Scholar
Calkins, DG & Pitcher, KW (1982) Population Assessment, Ecology, and Trophic Relationships of Steller Sea Lions in the Gulf of Alaska, pp. 546. Anchorage, AK: Alaska Department of Fish and Game.Google Scholar
Calkins, P & Goodwin, E (1988) Investigation of the Declining Sea Lion Population in the Gulf of Alaska, pp. 76. Anchorage, AK: Alaska Department of Fish and Game.Google Scholar
Carlsson, B, Ankarberg, C, Rosberg, S, Norjavaara, E, Albertsson-Wikland, K & Carlsson, LMS (1997) Serum leptin concentrations in relation to pubertal development. Archives of Disease in Children 77, 396400.Google Scholar
Castellini, MA, Davis, RW, Loughlin, TR & Williams, TM (1993) Blood chemistries and body condition of Steller sea lion pups at Marmot Island, Alaska. Marine Mammal Science 9, 202208.CrossRefGoogle Scholar
Chehab, FF, Mounzih, K, Lu, R & Lim, ME (1997) Early onset of reproductive function in normal female mice treated with leptin. Science 275, 8890.CrossRefGoogle ScholarPubMed
Cheung, CC, Thornton, JE, Kuijper, JL, Weigle, DS, Clifton, DK & Steiner, RA (1997) Leptin is a metabolic gate for the onset of puberty in the female rat. Endocrinology 138, 855858.CrossRefGoogle ScholarPubMed
de Mello, MAR & Cury, L (1989) Influence of protein-calorie malnutrition on reproductive performance of young and mature rats. Growth, Development and Aging 53, 141144.Google Scholar
Dratz, EA & Deese, AJ (1986) The role of docosahexaenoic acid (22: 6n-3) in biological membranes: examples from photoreceptors and model membrane bilayers. In Health Effects of Polyunsaturated Fatty Acids in Seafoods, [Simopoulos, AP, Kifer, RR and Martin, RE, editors]. Orlando, FL: Academic Press.Google Scholar
Folch, J, Lees, M & Sloane-Stanley, GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry 226, 497509.Google Scholar
Follett, BK (1982) The environment and reproduction. In Reproductive Fitness, pp. 103132 [Austin, CR and Short, RV, editors]. Cambridge: Cambridge University Press.Google Scholar
Harris, RBS (1991) Growth measurements in Sprague–Dawley rats fed diets of very low fat concentration. Journal of Nutrition 121, 10751080.Google Scholar
Holman, RT (1997) ω3 and ω6 essential fatty acid status in human health and disease. In Handbook of Essential Fatty Acid Biology: Biochemistry, Physiology, and Behavioral Neurobiology, pp. 139181 [Yehuda, S and Mostofsky, DI, editors]. Totowa, NJ: Humana Press Inc.Google Scholar
Iossa, S, Mollica, MP, Lionetti, L, Barletta, A & Liverini, G (1997) Energy balance and liver respiratory activity in rats fed on an energy-dense diet. British Journal of Nutrition 77, 99105.Google Scholar
Jacquot, R (1961) Organic constituents of fish and other aquatic animal foods. In Fish as Food: Production, Biochemistry, and Microbiology, pp. 145209 [Borgstrom, G, editor]. New York: Academic Press.Google Scholar
Johnson, DR, Ackroff, K, Peters, J & Collier, GH (1986) Changes in rats' meal patterns as a function of the caloric density of the diet. Physiology and Behavior 36, 929936.Google Scholar
Kirsch, PE, Iverson, SJ & Bowen, WD (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, 4549.CrossRefGoogle ScholarPubMed
Krajcivicova-Kudlackova, M & Dibak, O (1991) Utilization of qualitatively different proteins in relation to age and high fat intake under experimental conditions. Ceskslovenska Gastroenterologie a Vyziva 45, 2734.Google Scholar
Lands, WEM (1986) The fate of polyunsaturated fatty acids. In Health Effects of Polyunsaturated Fatty Acids in Seafoods, pp. 3348 [Simopoulos, AP, Kifer, RR and Martin, RE, editors]. Orlando, FL: Academic Press.Google Scholar
Larsen, FM, Wilson, MN & Moughan, PJ (1994) Dietary fiber viscosity and amino acid digestibility, proteolytic digestive enzyme and digestive organ weight in growing rats. Journal of Nutrition 124, 833841.Google Scholar
Leoschke, WL (1961) Fish in the raising of mink. In Fish as Food, pp. 435441 [Borgstrom, G, editor]. New York: Academic Press.Google Scholar
McGuire, MK, Littleton, AW, Schulze, KJ & Rasmussen, KM (1995) Pre- and postweaning food restrictions interact to determine reproductive success and milk volume in rats. Journal of Nutrition 125, 24002406.Google Scholar
Mehta, RS, Gunnett, CA, Harris, SR, Bunce, OR & Hartle, DK (1994) High fish oil diet increases oxidative stress potential in mammary gland of spontaneously hypertensive rats. Clinical and Experimental Pharmacology and Physiology 21, 881889.Google Scholar
Merrick, RL, Brown, R, Calkins, DG & Loughlin, TR (1995) A comparison of Steller sea lion, Eumetopias jubatus, pup masses between rookeries with increasing and decreasing populations. Fisheries Bulletin 93, 738758.Google Scholar
Merrick, RL & Calkins, DG (1996) Importance of juvenile walleye pollock, Theragra chalcogramma, in the diet of Gulf of Alaska Steller sea lions, Eumetopias jubatus. pp. 153166. Seattle: National Marine Fisheries Service, NOAA.Google Scholar
Merrick, RL, Chumbley, MK & Byrd, GV (1997) Diet diversity of Steller sea lions (Eumetopias jubatus) and their population decline in Alaska: a potential relationship. Canadian Journal of Fisheries and Aquatic Science 54, 13421348.CrossRefGoogle Scholar
Mitchell, HH (1955) Some species and age differences in amino acid requirements. In Protein and Amino Acid Requirements of Mammals, [Albanese, AA, editor]. New York: Academic Press.Google Scholar
Muller, HG & Tobin, G (1980) Nutrition and Food Processing. Westport, CT: The AVI Publishing Company, Inc.Google Scholar
Nilson, HW, Martinek, WA & Jacobs, B (1947) Nutritive value for growth of some fish proteins. Commercial Fisheries Review 9, 17.Google Scholar
Nwokolo, E & Kitts, DD (1988) Growth parameters and plasma and tissue fatty acid profiles in rats fed rubber seed oil. Food Chemistry 30, 219229.Google Scholar
Ohlsson, T & Smith, HG (2001) Early nutrition causes persistent effects on pheasant morphology. Physiological and Biochemical Zoology 74, 212218.Google Scholar
Olsen, SF, Hansen, HS & Jensen, B (1990) Fish oil versus arachis oil food supplementation in relation to pregnancy duration in rats. Prostaglandins, Leukotrienes and Essential Fatty Acids 40, 255260.Google Scholar
Pitcher, KW (1981) Prey of the Steller sea lion, Eumetopias jubatus, in the Gulf of Alaska. Fishery Bulletin 79, 467472.Google Scholar
Pitcher, KW, Calkins, DG & Pendleton, GW (1998) Reproductive performance of female Steller sea lions: an energetics-based reproductive strategy? Canadian Journal of Zoology 76, 20752083.Google Scholar
Privett, OS, Pusch, FJ, Holman, RT & Lundberg, WO (1960) Essential fatty acid properties of tuna, herring and menhaden oils. Journal of Nutrition 71, 6669.CrossRefGoogle ScholarPubMed
Rea, L (1995) Prolonged fasting in pinnipeds, PhD thesis, University of Alaska at Fairbanks.Google Scholar
Rosen, DAS & Trites, AW (1997) Heat increment of feeding in Steller sea lions, Eumetopias jubatus. Comparative Biochemistry and Physiology 118A, 877881.CrossRefGoogle Scholar
Rosen, DAS & Trites, AW (2000a) Digestive efficiency and dry-matter digestibility in Steller sea lions fed herring, pollock, squid, and salmon. Canadian Journal of Zoology 78, 16.Google Scholar
Rosen, DAS & Trites, AW (2000b) Pollock and the decline of Steller sea lions: testing the junk food hypothesis. Canadian Journal of Zoology 78, 12431250.Google Scholar
Ross, PS, de Swart, RL, van der Vliet, H, Willemsen, L, de Klerk, A, van Amerongen, G, Groen, J, Brouwer, A, Schipholt, I, Morse, DC, van Loveren, H, Osterhaus, ADME & Vos, JG (1997) Impaired cellular immune response in rats exposed perinatally to Baltic Sea herring oil or 2,3,7,8-TCDD. Archives of Toxicology 17, 563574.CrossRefGoogle Scholar
Ross, PS, Van Loveren, H, de Swart, RL, van der Vliet, H, de Klerk, A, Timmerman, JJ, van Binnendijk, R, Brouwer, A, Vos, JG & Osterhaus, ADME (1996) Host resistance to rat cytomegalorvirus (RCMV) and immune function in adult PVG rats fed herring from the contaminated Baltic Sea. Archives of Toxicology 70, 661671.Google Scholar
Rowlands, IW & Weir, BJ (1984) Mammals: non-primate eutherians. In Marshall's Physiology of Reproduction, pp. 455658 [Lamming, GE, editor]. New York, NY: Churchill Livingstone.Google Scholar
Schwartz, MW, Baskin, DG, Kaiyala, KJ & Woods, SC (1999) Model for the regulation of energy balance and adiposity by the central nervous system. American Journal of Clinical Nutrition 69, 584596.Google Scholar
Shaw, MA, Rasmussen, KM & Myers, TR (1997) Consumption of a high fat diet impairs reproductive performance in Sprague–Dawley rats. Journal of Nutrition 187, 6469.CrossRefGoogle Scholar
Short, RV (1982) Species differences in reproductive mechanisms. In Reproductive Fitness, pp. 2461 [Austin, CR and Short, RV, editors]. Cambridge: Cambridge University Press.Google Scholar
Sohlstrom, A, Kabir, N, Sadurskis, A & Forsum, E (1994) Body composition and fat distribution during the first 2 weeks of gestation in ad lib.-fed and energy-restricted rats. British Journal of Nutrition 71, 317333.Google Scholar
Stansby, ME (1969) Nutritional properties of fish oils. World Review of Nutrition and Dietetics 11, 46105.Google Scholar
Stansby, ME (1986) Fatty acids in fish. In Health Effects of Polyunsaturated Fatty Acids in Seafoods, pp. 389401 [Simopoulos, AP, Kifer, RR and Martin, RE, editors]. Orlando, FL: Academic Press.Google Scholar
Trites, AW & Larkin, PA (1996) Changes in the abundance of Steller sea lions (Eumetopias jubatus) in Alaska from 1956 to 1992: how many were there? Aquatic Mammals 22, 153166.Google Scholar
Trites, AW, Livingston, PA, Vasconcellos, MC, Mackinson, S, Springer, AM & Pauly, D (1999) Ecosystem change and the decline of marine mammals in the Eastern Bering Sea: testing the ecosystem shift and commercial whaling hypotheses. 7(1) pp. 106. Vancouver: Fisheries Center, UBC.Google Scholar
Veloso, C & Bozinovic, F (2000) Effect of food quality on the energetics of reproduction in a precocial rodent, Octodon degus. Journal of Mammalogy 81, 971978.2.0.CO;2>CrossRefGoogle Scholar
Warner, RG & Breuer, JH Jr (1972) Nutrient requirements of the laboratory rat. In Nutrient Requirements of Laboratory Animals, pp. 5693. Washington, DC: National Academy of Sciences.Google Scholar
Weber, PC, Fischer, S, von Schacky, C, Lorenz, R & Strasser, T (1986) Dietary omega-3 polyunsaturated fatty acids and eicosanoid formation in man. In Health Effects of Polyunsaturated Fatty Acids in Seafoods. Orlando, FL: Academic Press.Google Scholar
Widdowson, EM (1981) The role of nutrition in mammalian reproduction. In Environmental Factors in Mammal Reproduction, pp. 143159 [Gilmore, D and Cook, B, editors]. Baltimore: University Park Press.Google Scholar
Winship, AJ, Trites, AW & Rosen, DAS (2002) A bioenergetics model for estimating the food requirements of Steller sea lions (Eumetopias jubatus) in Alaska. Marine Ecology Progress Series 229, 291312.Google Scholar
Yonekubo, A, Honda, S, Okano, M, Takahashi, K & Yamamoto, Y (1993) Dietary fish oil alters rat milk composition and liver and brain fatty acid composition of fetal and neonatal rats. Journal of Nutrition 123, 17031708.CrossRefGoogle ScholarPubMed
Zhang, Z, Benson, B & Logan, JL (1992) Dietary fish oil delays puberty in female rats. Biology of Reproduction 47, 9981003.Google Scholar