The diving response mechanism and its surprising evolutionary path in seals and sea lions

American Zoologist

Volumn 39, Issue 2, 1999, Pages 434-450

  Mottishaw, Petra D ^a   Thornton, Sheila J ^a   Hochachka, Peter W ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 33746023034     PISSN: 00031569     EISSN: None     Source Type: Journal    
DOI: 10.1093/icb/39.2.434     Document Type: Article

References (78)

1. Allen, P. S., G. O. Matheson, G. Zhu, D. Gheorgiu, R. S. Dunlop, T. Falconer, C. Stanley, and P. W. Ho-
2. chachka. 1997. Simultaneous 31P magnetic resource spectroscopy of the soleus and gastrocnemius in sherpas during graded calf muscle exercise and recovery. Amer. J. Physiol. 273:R999R1007.
3. Andrews, R. D., D. R. Jones, J. D. Williams, D. E. Crocker, D. P. Costa, and B. J. LeBeouf. 1994. Thermorégulation and metabolism in freely diving northern elephant seals. FASEB J. 8:A2.
4. Andrews, R. D., D. R. Jones, J. D. Williams, P. H. Thorson, G. W. Oliver, D. P. Costa, and B. J. LeBoeuf. 1997. Heart rates of northern elephant seals diving at sea and resting on the beach. J. Exp. Biol. 200:2083-2095.
5. Arnason, U., K. Bodin, A. Gullberg, C. Ledje, and S. Mouchaty. 1995. A molecular view of pinniped relationships with particular emphasis on the true seals. J. Mol. Evol. 40:78-85.
6. Arnold, R. W. 1985. Extremes in human breath hold, facial immersion bradycardia. Undersea Biomed. Res. 12:183-190.
7. Berta, A. and T. A. Demere. 1986. Callorliinus gilmorei n. sp., (Camivora: Otariidae) from the San Diego formation (Blancan) and its implications for Otariid phylogeny. Trans. San Diego Soc. Nat. Hist. 21:111-126.
8. Berta, A. and A. R. Wyss. 1994. Pinniped phylogeny. Proc. San Diego Soc. Nat. Hist. 29:33-56.
9. Blix, A. S. 1988. Cardiovascular responses to diving. Acta Physiol. Scand. 571:561-68.
10. Boyd, I. L., A. J. Woakes, P. J. Butler, R. W. Davis, and T. M. Williams. 1995. Validation of heart rate and doubly labelled water as measures of metabolic rate during swimming in California sea lions. Funct. Ecol. 9:151-160.
11. Burns, J. J. and F. H. Fay. 1970. Comparative methodology of the skull of the Ribbon seal, Histriophoca fasciata, with remarks on the systematics of Phocidae. J. Zool. (Lond) 161:363-394.
12. Butler, P. J., R. M. Bevan, A. J. Woakes, J. P. Croxall, and I. L. Boyd. 1995. The use of data loggers to determine the energetics and physiology of aquatic birds and mammals. Brazil J. Med. Biol. Res. 28:1307-1317.
13. Butler, P. J. and D. R. Jones. 1982. The comparative physiology of diving in vertebrates. Adv. Comp. Physiol. Biochem. 8:179-368.
14. Castellini, M. A., G. L. Kooyman, and P. J. Ponganis. 1992. Metabolic rates of freely diving Weddell seals. J. Exp. Biol. 165:181-194.
15. Costa, D. P. 1991. Reproductive and foraging energetics of pinnipeds: Implications for life history patterns. In D. Renouf (ed.), The behaviour of Pinnipeds, pp. 300-344. Chapman and Hall, London.
16. Costa, D. P. 1993. The relationship between reproductive and foraging energetics and the evolution of the Pinnipedia. In I. L. Boyd (ed.). Marine mammals: Advances in behavioural and population biology, Symposia of the Zoological Society of London, No. 66, pp. 293-314. Oxford University Press, Oxford.
17. Craig, A. B., Jr. and A. Pasche. 1980. Respiratory physiology of freely diving harbor seals (Phoca vitulina). Physiol. Zool. 53:419-432.
18. De Muizon, C. 1976. Pinniped phylogeny and dispersai. Ann. South Afr. Mus. 89:175-213.
19. Delong, R. L. and B. S. Stewart. 1991. Diving patterns of northern elephant seal bulls. Mar. Mammal Sei. 7:369-384.
20. Delong, R. L., B. S. Stewart, and R. D. Hill. 1992. Documenting migrations of northern elephant seals using day length. Mar. Mammal Sei. 8:155159.
21. Doughty, P. 1996. Statistical analysis of natural experiments in evolutionary biology: Comments on recent criticisms of the use of comparative methods to study adaptation. Am. Nat. 148:943-956.
22. Elsner, R. and B. Gooden. 1983. Diving and asphyxia-a comparative study of animals and man. Cambridge Univ. Press, Cambridge.
23. Fedak, M. 1986. Diving and exercise in seals-a benthic perspective. In A. Brubaklc, J. W. Kanwisher, and G. Sundnes (eds.), Diving in animals and man, pp. 11-32. Tapir Publ., Trondheim.
24. Fedak, M. A., M. R. Pullen, and J. Kanwisher. 1988. Circulatory responses of seals to periodic breathing: Heart rate and breathing during exercise and diving in the laboratory and open sea. Can. J. Zool. 66:53-60.
25. Felsenstein, J. 1985. Phylogenies and the comparative method. Am. Nat. 125:1-15.
26. Gallivan, G. J. 1981. Ventilation and gas exchange in unrestrained harp seals (Phoca groenlandica). Comp. Biochem. Physiol. 69A:809-813.
27. Garland, T. Jr., and S. C. Adolph. 1994. Why not to do two species comparative studies: Limitations on inferring adaptation. Physiol. Zool. 67:797828.
28. Garland, T. Jr., A. W. Dickerman, C. M. Janis, and J. A. Jones. 1993. Phylogenetic analysis of covariance by computer simulation. Systematic Biology. 42:265-292.
29. Garland, T. Jr., P. H. Harvey, and A. R. Ives. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology. 41:18-32.
30. Gentry, R. L. and G. L. Kooyman. 1986. Fur seals. Princeton Univ. Press, Princeton, NJ.
31. Golding, G. B. 1994. Using maximum likelihood to infer selection from phylogenies. In B. Golding (ed.), Non-neutral evolution. Theories and molecular data, pp. 126-138. Chapman and Hall, London.
32. Guppy, M., R. D. Hill, R. C. Schneider, J. Qvist, G. C. Liggins, \V. M. Zapol, and P. W. Hochachka. 1986. Microcomputer assisted metabolic studies of voluntary diving of Weddell seals. Am. J. Physiol. 250:R175-R187.
33. Guyton, G. P., K. S. Stanek, R. C. Schneider, P. W. Hochachka, W. E. Hurford, D. G. Zapol, and W. M. Zapol. 1995. Myoglobin saturation in free diving Weddell seals. J. Appl. Physiol. 79:11481155.
34. Hill, R. D., R. C. Schneider, G. C. Liggins, A. H. Schuette, R. L. Elliott, M. Guppy, P. W. Hochachka, J. Qvist, K. J. Falke, and W. M. Zapol. 1987. Heart rate and body temperature during free div-
35. ing of Weddell seals. Am. J. Physiol. 253:R344R351.
36. Hille, B. 1992. Ionic channels of excitable membranes. Sinauer Assoc. Inc., Sunderland, Massachusetts.
37. Hindell, M. A., D. J. Slip, H. R. Burton, and M. M. Bryden. 1992. Physiological implications of continuous and deep dives of the southern elephant seal (Mirounga leonina). Can. J. Zool. 70:370379.
38. Hochachka, P. W. 1986. Balancing the conflicting demands of diving and exercise. Federation Proceedings 45:2949-2954.
39. Hochachka, P. \V. 1992. Metabolic biochemistry and the making of a mesopelagic mammal. Experientia. 48:570-575.
40. Hochachka, P. W. and R. A. Foreman, III. 1993. Phocid and cetacean blueprints of muscle metabolism. Can. J. Zool. 71:2089-2098.
41. Hochachka, P. W. and M. Guppy. 1987. Metabolic arrest and the control of biological time. Harvard University Press, Cambridge.
42. Hochachka, P. W., H. C. Gunga, and K. Kirsch. 1998. Our ancestral physiological phenotype. An adaptation for hypobaric hypoxia and for endurance performance? Proc. Natl. Acad. Sei. 95:19151920.
43. Hochachka, P. W., G. C. Liggins, G. P. Guyton, R. C. Schneider, K. S. Stanek, W. E. Hurford, R. K. Creasy, D. G. Zapol, and W. M. Zapol. 1995. Hormonal regulatory adjustments during voluntary diving in Weddell seals. Comp. Biochem. Physiol. 1128:361-375.
44. Hochachka, P. W. and G. B. McClelland. 1997. Cellular metabolic homeostasis during large scale change in ATP turnover rates in muscles. J. Exp. Biol. 200:381-386.
45. Hochachka, P. W. and P. D. Mottishaw. 1998. Evolution and adaptation of the diving response: Phocids and otariids. In H. O. Portner, and R. C. Playle (eds.), Cold Ocean Symposia, pp. 391-431. Cambridge University Press, Cambridge, UK..
46. Hochachka, P. W. and G. N. Somero. 1984. Biochemical adaptation. Princeton University Press, Princeton.
47. Hurford, W. E., P. W. Hochachka, R. C. Schneider, G. P. Guyton, K. S. Stanek, D. G. Zapol, G. C. Liggins, and W. M. Zapol. 1995. Splenic contraction, catecholamine release and blood volume redistribution during voluntary diving in the Weddell seal. J. Appl. Physiol. 80:298-306.
48. Hurley, J. A. 1996. Metabolic rate and heart rate during trained dives in adult California sea lions. Ph.D. Diss., Univ. of California, Santa Cruz.
49. Kirkpatrick, M. 1996. Genes and adaptation: A pocket guide to the theory. In M. R. Rose and G. V. Lauder (eds.). Adaptation, pp. 125-146. Academic Press, San Diego.
50. Kooyman, G. L. 1985. Physiology without restraint in diving mammals. Mar. Mammal Sei. 1:166-178.
51. Kooyman, G. L., E. H. Wahrenbrock, M. A. Castellini, R. W. Davis, and E. E. Sinnett. 1980. Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: Evidence of preferred pathways
52. from blood chemistry and behaviour. J. Comp. Physiol. 138:335-346.
53. Lacombe, A. M. and D. R. Jones. 1991. Role of adrenal catecholamines during forced submergence in ducks. Am. J. Physiol. 261:R1364-R1372.
54. Le Boeuf, B. J., D. E. Crocker, D. P. Costa, S. B. Blackwell, P. M. Webb, and D. S. Houser. 1999. Foraging ecology of northern elephant seals. Ecol. Monographs. (In press)
55. Le Boeuf, B. J., Y. Naito, T. Asaga, D. Crocker, and D. Costa. 1992. Swim velocity and dive patterns in a northern elephant seal, Mirounga angustirostris. Can. J. Zool. 70:786-795.
56. Le Boeuf, B. J., Y. Naito, A. C. Huntley, and T. Asaga. 1989. Prolonged, continuous, deep diving by northern elephant seals. Can. J. Zool. 67:25142519.
57. Lenfant, C., K. Johansen, and J. D. Torrance. 1970. Gas transport and oxygen storage capacity in some pinnipeds and the sea otter. Resp. Physiol. 9:277-286.
58. Lento, G. M., R. E. Hickson, G. K. Chambers, and D. Penny. 1995. Use of spectral analysis to test hypotheses on the origin of pinnipeds. Mol. Biol. Evol. 12:28-52.
59. Leroi, A. M., M. R. Rose, and G. V. Lauder. 1994. What does the comparative method reveal about adaptation? Am. Nat. 143:381-402.
60. Li, K. C., R. L. Dalman, I. Y. Chen, L. R. Pelc. C. K. Song, W. K. Moon, M. I. Kang, and G. A. Wright. 1997. Chronic mesenteric ischemia: Use of in vivo MR imaging measurements of blood oxygen saturation in the superior mesenteric vein for diagnosis. Radiology. 204:71-77.
61. McConnell, D. 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.
62. Mottishaw, P. D. 1997. The diving physiology of pinnipeds: An evolutionary enquiry. M.Sc. Thesis, Univ. of British Columbia, Vancouver.
63. Ponganis, P., E. P. Ponganis, R. L. Gentry, and F. Trillmich. 1990. Swimming velocities in otariids. Can. J. Zool. 68:2105-2112.
64. Purvis, A. and A. Rambaut. 1995. Comparative analysis by independent contrasts (CAIC): An Apple Macintosh application for analyzing comparative data. CABIOS. 11:247-251.
65. Qvist, J., R. D. Hill, R. C. Schneider, K. J. Falke, G. C. Liggins, M. Guppy, R. L. Elliott, and P. W. Hochachka. 1986. Hemoglobin concentrations and
66. blood gas tensions of free diving Weddell seals. J. Appl. Physiol. 61:1560-1569.
67. Reed, J. Z., C. Chambers, M. A. Fedak, and P. J. Butler. 1994. Gas exchange of captive freely diving grey seals (Halichoerus grypus). J. Exp. Biol. 191: 1-18.
68. Repenning, C. A., R. S. Peterson, and C. L. Hubbs. 1971. Contributions to the systematics of the southern fur seals, with particular reference to the Juan Fernandez and Guadalupe species. Antarctic Research 18:1-34.
69. Scholander, P. F. 1940. Experimental investigations in diving animals and birds. Hvalradets Skrifter. 22: 1-131.
70. Scholander, P. F. 1963. The master switch of life. Sei. Amer. 209:92-106.
71. Thompson, D. and M. A. Fedak. 1989. Comparison of dive behaviour and cardiac responses of free ranging harbor and grey seals. Tenth Biennial Conf. Biol. Marine Mammals. A106.
72. Thompson, D. and M. A. Fedak. 1993. Cardiac responses of grey seals during diving at sea. J. Exp. Biol. 174:139-164.
73. Thormon, S. J., N. J. Pelc, D. M. Spielman, J. R. Liao, D. P. Costa, D. E. Crocker, D. Houser, S. Kohin, B. J. LeBoeuf, L. R. Pelc, and P. W. Hochachka. \991b. Vascular flow dynamics in a diving elephant seal (Alirounga angustrirostris). Intl. Soc. Magn. Res. Med. 2:823.
74. Thornton, S. J., D. M. Spielman, \V. F. Block, P. W. Hochachka, D. E. Crocker, B. J. LeBoeuf, D. P. Costa, D. Houser, S. Kohin, L. R. Pelc, and N. J. Pelc. \991a. MR. Imaging in a Diving Seal. Proc. Intl. Soc. Magn. Res. Med. 2:822.
75. Williams, T. M., G. L. Kooyman, and D. A. Croll. 1991. The effect of submergence of heart rate and oxygen consumption of swimming seals and sea lions. J. Comp. Physiol. B, 160:637-644.
76. Winslow, R. M. and C. C. Monge. 1987. Hypo.xia, polycythemia and chronic mountain sickness. Johns Hopkins University Press, Baltimore.
77. Worthy, G. A. J., P. A. Morris, D. P. Costa, and B. J. LeBeouf. 1992. Moult energetics of the northern elephant seal (Alirounga angastirostris). }. Zool. Lond. 227:257-265.
78. Zapol, W. M., G. C. Liggins, R. C. Schneider, J. Qvist, M. T. Snider, R. K. Creasy, and P. W. Hochachka. 1979. Regional blood flow during simulated diving in the conscious Weddell seal. J. Appl. Physiol. 47:968-973.