A model for energetics and bioaccumulation in marine mammals with applications to the right whale

Ecological Applications

Volumn 17, Issue 8, 2007, Pages 2233-2250

  Klanjscek, Tin ^a,c   Nisbet, Roger M ^b   Caswell, Hal ^a   Neubert, Michael G ^a  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c RUDER BO KOVI INSTITUTE   (Croatia)

Author keywords

Bioaccumulation; Dynamic energy budget (DEB) model; Energy intake and utilization; Eubalaena glacialis; Lipophilic; Marine mammal; North Atlantic right whale growth and reproduction; PCB; Toxicant transfer

Indexed keywords

BIOACCUMULATION; BIOENERGETICS; CLIMATE CHANGE; ENERGY BUDGET; FOOD CHAIN; LIPID; MARINE POLLUTION; PARTURITION; PCB; POLLUTANT TRANSPORT; POPULATION MODELING; REPRODUCTION; SEASONAL VARIATION; TOXIC SUBSTANCE; WHALE;

ATLANTIC OCEAN; ATLANTIC OCEAN (NORTH);

BALAENIDAE; CETACEA; EUBALAENA AUSTRALIS; EUBALAENA GLACIALIS; MAMMALIA;

POLYCHLORINATED BIPHENYL;

AGING; ANIMAL; ARTICLE; BIOLOGICAL MODEL; ENERGY METABOLISM; FEMALE; FOOD CHAIN; GREENHOUSE EFFECT; MALE; PHYSIOLOGY; REPRODUCTION; WATER POLLUTANT; WHALE;

AGING; ANIMALS; ENERGY METABOLISM; FEMALE; FOOD CHAIN; GREENHOUSE EFFECT; MALE; MODELS, BIOLOGICAL; POLYCHLORINATED BIPHENYLS; REPRODUCTION; WATER POLLUTANTS, CHEMICAL; WHALES;

EID: 39349095078     PISSN: 10510761     EISSN: None     Source Type: Journal    
DOI: 10.1890/06-0426.1     Document Type: Article

References (82)

1. Aguilar, A., and A. Borrell. 1990. Patterns of lipid content and stratification in the blubber of fin whales (Balaenoptera physalus). Journal of Mammalogy 71:544-554.
2. Aguilar, A., and A. Borrell. 1994. Reproductive transfer and variation of body load of organochlorine pollutants with age in fin whales (Balaenoptera physalus). Archives of Environmental Contamination and Toxicology 27:546-554.
3. Aguilar, A., A. Borrell, and T. Pastor. 1999. Biological factors affecting variability of persistent pollutant levels in cetaceans. Journal of Cetacean Research and Management Special Issue 1:83-116.
4. Angell, C. 2005. Body fat condition of right whales, Eubalaena glacialis and Eubalaena australis. Dissertation. Boston University, Boston, Massachusetts, USA.
5. Baumgartner, M. F., T. V. N. Cole, R. G. Campbell, G. J. Teegarden, and E. G. Durbin. 2003. Associations between north Atlantic right whales and their prey, Calanus finmarchicus, over diel and tidal time scales. Marine Ecological Progress Series 264:155-166.
6. Beardsley, R. C., A. W. Epstein, C. Chen, K. F. Wishner, M. C. Macaulay, and R. D. Kenney. 1996. Spatial variability in zooplankton abundance near feeding right whales in the great south channel. Deep-Sea Research Part II, Topical Studies in Oceanography 43:1601-1625.
7. Best, P. B., A. Brandao, and D. S. Butterworth. 2001. Demographic parameters of southern right whales off south Africa. Journal of Cetacean Research and Management, Special Issue 2:161-169.
8. Best, P. B., and D. M. Schell. 1996. Stable isotopes in southern right whale (Eubalaena australis) baleen as indicators of seasonal movements, feeding and growth. Marine Biology 124:483-494.
9. Boon, J., I. Oostingh, J. van der Meer, and T. Hillebrand. 1994. A model for the bioaccumulation of chlorobiphenyl congeners in marine mammals. European Journal of Pharmacology: Environmental Toxicology and Pharmacology 270:237-251.
10. Boon, J. P., E. van Arnhem, S. Jansen, N. Kannan, G. Petrick, D. Schulz, J. Duinker, P. Reijnders, and A. Goksoyr. 1992. The toxicokinetics of PCBs in marine mammals with special reference to possible interactions of individual congeners with the cytochrome P450-dependent monooxygenase system: an overview. Pages 119-160 in C. H. Walker and D. R. Livingstone, editors. Persistent pollutants in marine ecosystems. Pergamon Press, Oxford, UK.
11. Borga, K., A. Fisk, P. Hoekstra, and D. Muir. 2004. Biological and chemical factors of importance in the bioaccumulation and trophic transfer of persistent organochlorine contaminants in Arctic marine food webs. Environmental Toxicology and Chemistry 23:2367-2385.
12. Bronson, F., and J. Manning. 1991. The energetic regulation of ovulation: a realistic role for body fat. Biology of Reproduction 44:945-950.
13. Brownell, R. L., Jr., P. J. Clapham, T. Miyashita, and T. Kasuya. 2001. Conservation status of North Pacific right whales. Journal of Cetacean Research and Management, Special Issue 2:269-286.
14. Brunell, S. R. 2001. Aspects of the reproductive biology, movement and site fidelity of right whales off Australia. Journal of Cetacean Research and Management, Special Issue 2:89-99.
15. Convention, W. 1931. Convention for the regulation of whaling, Geneva. League of Nations Treaty Series 155:349-365.
16. Crank, J. 2004. The mathematics of diffusion. Second edition. Oxford University Press, Oxford, UK.
17. deBruyn, A. M., M. G. Ikonomou, and F. A. Gobas. 2005. Magnification and toxicity of PCBs, PCDDs, and PCDFs in upriver-migrating Pacific Salmon. Environmental Science and Technology 38:6217-6224.
18. de Swart, R. L., P. S. Ross, L. J. Vedder, H. H. Timmerman, S. Heisterkamp, H. Van Loveren, J. G. Vos, P. J. H. Reijnders, and A. D. M. E. Osterhaus. 1994. Impairment of immune function in harbour seals (Phoca vitulina) feeding on fish from polluted waters. Ambio 23:155-159.
19. Frisch, R. 1978. Population, food intake, and fertility. Science 199:22-30.
20. Frisch, R. 1990. The right weight: body fat, menarche and ovulation. Bailliere's Clinical Obstetrics and Gynaecology 4:419-439.
21. Frisch, R., D. Hegsted, and K. Yoshinaga. 1975. Body weight and food intake at early estrus of rats on a high-fat diet. Proceedings of the National Academy of Sciences (USA) 72:4172-4176.
22. Fujiwara, M., and H. Caswell. 2001. Demography of the endangered North Atlantic right whale. Nature 414:537-541.
23. Gopalan, C., and A. Naidu. 1972. Nutrition and fertility. Lancet 2:1077-1079.
24. Greene, C., A. Pershing, R. Kenney, and J. Jossi. 2003. Impact of climate variability on the recovery of endangered North Atlantic right whales. Oceanography 16:98-103.
25. Guo, Y., G. Lambert, C. C. Hsu, and M. M. Hsu. 2004. Yucheng: health effects of prenatal exposure to polychlorinated biphenyls and dibenzofurans. International Archives of Occupational and Environmental Health 77:153-158.
26. Gurney, W. S. C., E. McCauley, R. M. Nisbet, and W. W. Murdoch. 1990. The physiological ecology of daphnia: a dynamic model of growth and reproduction. Ecology 71:716-732.
27. Gurney, W. S. C., and R. M. Nisbet. 1998. Ecological dynamics. Oxford University Press, New York, New York, USA.
28. Gurney, W. S. C., and R. M. Nisbet. 2004. Resource allocation, hyperphagia and compensatory growth. Bulletin of Mathematical Biology 66:1731-1753.
29. Hallam, T. G., R. R. Lassiter, J. Li, and L. A. Suarez. 1990. Modelling individuals employing an integrated energy response: application to daphnia. Ecology 71:938-954.
30. Hickie, B. E., M. C. S. Kingsley, P. V. Hodson, D. C. G. Muir, P. Beland, and D. Mackay. 2000. A modelling-based perspective on the past, present, and future polychlorinated biphenyl contamination of the St. Lawrence 800 beluga whale (Delphinapterus leucas) population. Canadian Journal of Fisheries and Aquatic Sciences 57:101-112.
31. Hickie, B. E., D. Mackay, and J. De Koning. 1999. Lifetime pharmacokinetic model for hydrophobic contaminants in marine mammals. Environmental Toxicology and Chemistry 18:2622-2633.
32. Hickie, B., D. Mackay, and D. Muir. 1997. Use of novel pharmacokinetic models to estimate contaminant elimination rates in marine mammals. 18th Annual Meeting of the Society of Environmental Toxicology and Chemistry, San Francisco, California. SETAC Press, Pensacola, Florida, USA.
33. Iverson, S. 2002. Blubber. Pages 107-112 in W. F. Perrin, B. G. Wuersig, and J. G. M. Thewissen, editors. Encyclopedia of marine mammals. Academic Press, San Diego, California, USA.
34. Jørgensen, E., B. Bye, and M. Jobling. 1999. Influence of nutritional status on biomarker responses to PCB in the arctic charr (Salvelinus alpinus). Aquatic Toxicology 44:233-244.
35. Kenney, R. D., C. A. Mayo, and H. E. Winn. 2001. Migration and foraging strategies at varying spatial scales in western North Atlantic right whales: a review of hypotheses. Journal of Cetacean Research and Management, Special Issue 2:251-260.
36. Klanjscek, T., H. Caswell, M. G. Neubert, and R. M. Nisbet. 2006. Integrating dynamic energy budgets into matrix population models. Ecological Modelling 196:407-420.
37. Knowlton, A. R., S. D. Kraus, and R. D. Kenney. 1994. Reproduction in North-Atlantic right whales (Eubalaena glacialis). Canadian Journal of Zoology 72:1297-1305.
38. Kooijman, S. A. L. M. 2000. Dynamic energy and mass budgets in biological systems. Second edition. Cambridge University Press, Cambridge, UK.
39. Koopman, H. N., D. A. Pabst, W. A. McLellan, R. M. Dillaman, and A. J. Read. 2002. Changes in blubber distribution and morphology associated with starvation in the harbor porpoise (Phocoena phocoena): evidence for regional differences in blubber structure and function. Physiological and Biochemical Zoology 75:498-512.
40. Kraus, S. D., P. K. Hamilton, R. D. Kenney, A. R. Knowlton, and C. K. Slay. 2001. Reproductive parameters of the North Atlantic right whale. Journal of Cetacean Research and Management, Special Issue 2:231-236.
41. Lee, J. S., S. Tanabe, H. Umino, R. Tatsukawa, D. C. Loughlin, and T. R. Calkins. 1996. Persistent organochlorines in Steller sea lion (Eumetopias jubatus) from the bulk of Alaska and the Bering Sea, 1976-1981. Marine Pollution Bulletin 32:535-544.
42. Lee, P. 1987. Nutrition, fertility and maternal investment in primates. Journal of Zoology (London) 213:409-422.
43. Leung, H., D. Paustenbach, F. Murray, and M. Andersen. 1990a. A physiological pharmacokinetic description of the tissue distribution and enzyme-inducing properties of 2,3,7,8-tetrachlorodibenzo-p-dioxin in the rat. Toxicology and Applied Pharmacology 103:399-410.
44. Leung, H., A. Poland, D. Paustenbach, F. Murray, and M. Andersen. 1990b. Pharmacokinetics of [125i]-2-iodo-3,7,8-trichlorodibenzo-p-dioxin in mice: analysis with a physiological modeling approach. Toxicology and Applied Pharmacology 103:411-419.
45. Lika, K., and R. M. Nisbet. 2000. A dynamic energy budget model based on partitioning of net production. Journal of Mathematical Biology 41:361-386.
46. Lockyer, C. 1976. Body weights of some species of large whales. Journal du Conseil International pour l'Exploration de la Mer 36:259-273.
47. Lockyer, C. 1986. Body fat condition in northeast Atlantic fin whales, Balaenoptera physalus, and its relationship with reproduction and food resource. Canadian Journal of Fisheries and Aquatic Sciences 43:142-147.
48. Martin, R. D., and A. M. MacLarnon. 1985. Gestation period, neonatal size and maternal investment in placental mammals. Nature 313:220-223.
49. Martineau, D., K. Lemberger, A. Dallaire, P. Labelle, T. P. Lipscomb, P. Michel, and I. Mikaelian. 2002. Cancer in wildlife, a case study: beluga from the St. Lawrence estuary, Quebec, Canada. Environmental Health Perspectives 110:285-292.
50. Mayo, C. A., and M. K. Marx. 1990. Surface foraging behaviour of the North Atlantic right whale, Eubalaena glacialis, and associated zooplankton characteristics. Canadian Journal of Zoology 68:2214-2220.
51. McCauley, E., W. Murdoch, R. Nisbet, and W. Gurney. 1990. The physiological ecology of daphnia I: development of a model of growth and reproduction. Ecology 71:703-715.
52. Moore, J., A. Knowlton, S. Kraus, W. McLellan, and R. Bonde. 2005. Morphometry, gross morphology and available histopathology in North Atlantic right whale (Eubalaena glacialis) mortalities (1980-2002). Journal of Cetacean Research and Management 6:199-214.
53. Muller, E. B., and R. M. Nisbet. 1997. Modeling the effect of toxicants on the parameters of dynamic energy budget models, in ASTM Special Technical Publication. ASTM, Conshohocken, Pennsylvania, USA.
54. Nisbet, R. M., S. Diehl, W. G. Wilson, S. D. Cooper, D. D. Donalson, and K. Kratz. 1997. Primary-productivity gradients and short-term population dynamics in open systems. Ecological Monographs 67:535-553.
55. Nisbet, R. M., E. B. Muller, K. Lika, and S. A. L. M. Kooijman. 2000. From molecules to ecosystems through dynamic energy budget models. Journal of Animal Ecology 69:913-926.
56. Noonburg, E. G., R. M. Nisbet, E. McCauley, W. S. C. Gurney, W. W. Murdoch, and A. M. De Roos. 1998. Experimental testing of dynamic energy budget models. Functional Ecology 12:211-222.
57. Nordoy, E. S., and A. S. Blix. 1985. Energy sources in fasting grey seal pups evaluated with computed tomography. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 249:471-476.
58. North Atlantic Right Whale Recovery Team. 2000. Canadian recovery plan for the North Atlantic right whale. World Wildlife Fund Canada and the Department of Fisheries and Oceans, Toronto, Ontario, Canada.
59. Nowacek, D., M. Johnson, and P. Tyack. 2004. North Atlantic right whales (Eubalaena glacialis) ignore ships but respond to alerting stimuli. Proceedings of the Royal Society of London, Series B 271:227-231.
60. Phillips, D. L., A. B. Smith, V. W. Burse, G. K. Steele, L. L. Needham, and W. H. Hannon. 1989. Half-life of polychlorinated biphenyls in occupationally exposed workers. Archives of Environmental Health 44:351-354.
61. Pond, C. M. 1987. Some conceptual and comparative aspects of body composition analysis. Pages 499-529 in F. M. Toates and N. Rowland, editors. Methods and techniques to study feeding and drinking behaviour. Elsevier, Amsterdam, The Netherlands.
62. Porter, W. P., S. Budaraju, W. E. Stewart, and N. Ramankutty. 2000. Calculating climate effects on birds and mammals: Impacts on biodiversity, conservation, population parameters, and global community structure. American Zoologist 40:597-630.
63. Porter, W., J. Sabo, C. Tracy, O. Reichman, and N. Ramankutty. 2002. Physiology on a landscape scale: plant-animal interactions. Integrative and Comparative Biology 42:431-453.
64. Reeves, R. R., J. M. Breiwick, and E. Mitchell. 1992. Pre-exploitation abundance of right whales off the eastern United States. Pages 5-7 in J. Hain, editor. Right whales in the western North Atlantic: a management workshop. Northeast Fisheries Science Center Reference Document No. 92-05. NEFSC/NMFS, Woods Hole, Massachusetts, USA.
65. Reijnders, P. J. H. 1986. Reproductive failure in common seals feeding on fish from polluted coastal waters. Nature 324:456-457.
66. Reilly, J. J. 1991. Adaptations to prolonged fasting in free-living weaned gray seal pups. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 260:267-272.
67. Restum, J., S. Bursian, J. Giesy, J. Render, W. Helferich, E. Shipp, D. Verbrugge, and R. Aulerich. 1998. Multigenerational study of the effects of consumption of PCB-contaminated carp from Saginaw Bay, Lake Huron, on mink. 1. Effects on mink reproduction, kit growth and survival, and selected biological parameters. Journal of Toxicology and Environmental Health A 54:343-375.
68. Rosenbaum, H. C., et al. 2000. World-wide genetic differentiation of Eubalaena: questioning the number of right whale species. Molecular Ecology 9:1793-1802.
69. Ross, A. H., and R. M. Nisbet. 1990. Dynamic models of growth and reproduction of the mussel Mytilus edulis l. Functional Ecology 4:777-787.
70. Ross, P. S., R. L. De Swart, R. F. Addison, H. Van Loveren, J. Vos, and A. Osterhaus. 1996. Contaminant-induced immunotoxicity in harbour seals: wildlife at risk? Toxicology 112(2):157-169.
71. Ross, P. S., G. M. Ellis, M. G. Ikonomou, L. G. Barrett-Lennard, and R. F. Addison. 2000. High PCB concentrations in freeranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference. Marine Pollution Bulletin 40:504-515.
72. Schwacke, L. H., E. O. Voit, L. J. Hansen, R. S. Wells, G. B. Mitchum, A. A. Hohn, and P. A. Fair. 2002. Probabilistic risk assessment of reproductive effects of polychlorinated biphenyls on bottlenose dolphins (Tursiops truncatus) from the southeast United States coast. Environmental Toxicology and Chemistry 21:2752-2764.
73. Struntz, D. J., W. A. McLellan, R. M. Dillaman, J. E. Blum, J. R. Kucklick, and D. Pabst. 2004. Blubber development in bottlenose dolphins (Tursiops truncatus). Journal Morphology 259:7-20.
74. Thomas, P. O., and S. M. Taber. 1984. Mother-infant interaction and behavioral development in southern right whales, Eubalaena australis. Behaviour 88:42-46.
75. Thomas, P. T., and R. D. Hinsdill. 1980. Perinatal PCB exposure and its effect on the immune system of young rabbits. Drug and Chemical Toxicology 3:173-184.
76. Van der Spuy, Z. 1985. Nutrition and reproduction. Bailliere's Clinical Obstetrics and Gynaecology 12:579-604.
77. von Bertalanffy, L. 1957. Quantitative laws in metabolism and growth. Quarterly Review of Biology 32:217-231.
78. Weisbrod, A. V., D. Shea, M. J. Moore, and J. J. Stegeman. 2000. Organochlorine exposure and bioaccumulation in the endangered northwest Atlantic right whale (Eubalaena glacialis) population. Environmental Toxicology and Chemistry 19:654-666.
79. Wells, R., V. Tornero, A. Borrell, A. Aguilar, T. Rowles, H. Rhinehart, S. Hofmann, W. Jarman, A. Hohn, and J. Sweeney. 2005. Integrating life-history and reproductive success data to examine potential relationships with organochlorine compounds for bottlenose dolphins (Tursiops truncatus) in Sarasota Bay, Florida. Science of the Total Environment. 349:106-119.
80. Winn, H. E., C. A. Price, and P. W. Sorensen. 1986. The distributional biology of the right whale (Eubalaena glacialis) in the western North Atlantic. Report of the International Whaling Commission, Special Issue 10:129-138.
81. Wishner, K., E. Durbin, A. Durbin, M. Macaulay, H. Winn, and R. Kenney. 1988. Copepod patches and right whales in the great south channel off New England. Bulletin of Marine Science 43:825-844.
82. Young, R. 1976. Fat, energy and mammalian survival. American Zoologist 16:699-710