In pursuit of Irving and Scholander: A review of oxygen store management in seals and penguins

Journal of Experimental Biology

Volumn 214, Issue 20, 2011, Pages 3325-3339

  Ponganis, Paul J ^a   Meir, Jessica U ^b   Williams, Cassondra L ^a,c  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aerobic dive limit; Blood flow; Heart rate; Hemoglobin; Hypoxemia; Marine mammals; Metabolic rate; Myoglobin; Oxygen stores; Penguins; Re perfusion injury; Seals

Indexed keywords

OXYGEN;

AIR SAC; ANIMAL; BLOOD; DIVING; METABOLISM; MUSCLE; PENGUIN; PHOCA; PHYSIOLOGY; REVIEW;

AIR SACS; ANIMALS; DIVING; MUSCLES; OXYGEN; SEALS, EARLESS; SPHENISCIDAE;

ANIMALIA; APTENODYTES FORSTERI; AVES; MAMMALIA; MIROUNGA; MIROUNGA ANGUSTIROSTRIS; SPHENISCIDAE;

EID: 80053928369     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.031252     Document Type: Review

References (156)

1. Andersson, J. P. A., Liner, M. H. and Jonsson, H. (2009a). Asystole and increased serum myoglobin levels associated with 'packing blackout' in a competitive breathhold diver. Clin. Physiol. Funct. Imaging 29, 458-461.
2. Andersson, J. P. A., Liner, M. H. and Jonsson, H. (2009b). Increased serum levels of the brain damage marker S100B after apnea in trained breath-hold divers: a study including respiratory and cardiovascular observations. J. Appl. Physiol. 107, 809-815.
3. Andrews, R. D., Jones, D. R., Williams, J. D., Thorson, P. H., Oliver, G. W., Costa, D. P. and Le Boeuf, B. J. (1997). Heart rates of northern elephant seals diving at sea and resting on the beach. J. Exp. Biol. 200, 2083-2095.
4. Baldwin, J. (1988). Prediciting the swimming and diving behavior of penguins from muscle biochemistry. Hydrobiologia 165, 255-261.
5. Bayly, W. M., Hodgson, D. R., Schulz, D. A., Dempsey, J. A. and Gollnick, P. D. (1989). Exercise-induced hypercapnia in the horse. J. Appl. Physiol. 67, 1958-1966.
6. Black, C. P. and Tenney, S. M. (1980). Oxygen transport during progressive hypoxia in high-altitude and sea-level waterfowl. Respir. Physiol. 39, 217-239.
7. Blei, M. L., Conley, K. E. and Kushmerick, M. J. (1993). Separate measures of ATP utilization and recovery in human skeletal muscle. J. Physiol. 465, 203-222.
8. Blessing, M. H. (1972). Studies on the concentration of myoglobin in the sea-cow and porpoise. Comp. Physiol. Biochem. 41A, 475-480.
9. Blix, A. S., Elsner, R. W. and Kjekhus, J. K. (1983). Cardiac output and its distribution through capillaries and A-V shunts in diving seals. Acta Physiol. Scand. 118, 109-116.
10. Blix, A. S., Walloe, L., Messelt, E. B. and Folkow, L. P. (2010). Selective brain cooling and its vascular basis in diving seals. J. Exp. Biol. 213, 2610-2616.
11. Bryden, M. M. (1972). Body size and composition of elephant seals (Mirounga leonina): absolute measurements and estimates from bone dimensions. J. Zool. 167, 265-276.
12. Burns, J. M., Costa, D. P., Frost, K. and Harvey, J. T. (2005). Physiological development in juvenile harbor seals. Physiol. Biochem. Zool. 78, 1057-1068.
13. Burns, J. M., Skomp, N., Bishop, N., Lestyk, K. and Hammill, M. (2010). Development of aerobic and anaerobic metabolism in cardiac and skeletal muscles from harp and hooded seals. J. Exp. Biol. 213, 740-748.
14. Butler, P. J. (2000). Energetic costs of surface swimming and diving of birds. Physiol. Biochem. Zool. 73, 699-705.
15. Butler, P. J. (2004). Metabolic regulation in diving birds and mammals. Respir. Physiol. Neurobiol. 141, 297-315.
16. Butler, P. J. and Jones, D. R. (1997). The physiology of diving of birds and mammals. Physiol. Rev. 77, 837-899.
17. Castellini, M. A. and Somero, G. N. (1981). Buffering capacity of vertebrate muscle: correlations with potentials for anaerobic function. J. Comp. Physiol. B 143, 191-198.
18. Castellini, M. A., Costa, D. P. and Huntley, A. (1986). Hematocrit variation during sleep apnea in elephant seal pups. Am. J. Physiol. 251, R429-R431.
19. Cherel, Y., Charassin, J.-B. and Handrich, Y. (1993). Comparison of body reserve buildup in prefasting chicks and adults of king penguins (Aptenodytes patagonicus). Physiol. Zool. 66, 750-770.
20. Croll, D. A., Gaston, A. J., Burger, A. E. and Konnoff, D. (1992). Foraging behavior and physiological adaptation for diving in thick-billed murres. Ecology 73, 344-356.
21. Davis, R. W. and Kanatous, S. B. (1999). Convective oxygen transport and tissue oxygen consumption in Weddell seals during aerobic dives. J. Exp. Biol. 202, 1091-1113.
22. Davis, R. W., Castellini, M. A., Kooyman, G. L. and Maue, R. (1983). Renal GFR and hepatic blood flow during voluntary diving in Weddell seals. Am. J. Physiol. 245, 743-748.
23. Dempsey, J. A., Veasey, S. C., Morgan, B. J. and O'Donnell, C. P. (2010). Pathophysiology of sleep apnea. Physiol. Rev. 90, 47-112.
24. Elsner, R. (1969). Cardiovascular adjustments to diving. In The Biology of Marine Mammals (ed. H. T. Andersen), pp. 117-145. New York: Academic Press.
25. Elsner, R., Franklin, D. L., Van Citters, R. L. and Kenney, D. W. (1966). Cardiovascular defense against asphyxia. Science 153, 941-949.
26. Elsner, R., Shurley, J. T., Hammond, D. D. and Brooks, R. E. (1970). Cerebral tolerance to hypoxemia in asphyxiated Weddell seals. Respir. Physiol. 9, 287-297.
27. Elsner, R., Oyasaetr, S., Almaas, R. and Sauagstad, O. D. (1998). Diving seals, ischemia-reperfusion, and oxygen radicals. Comp. Biochem. Physiol. 119A, 975-980.
28. Elsner, R. W., Scholander, P. F., Craig, A. B., Dimond, E. G., Irving, L., Pilson, M., Johansen, K. and Bradstreet, E. (1964). A venous blood oxygen reservoir in the diving elephant seal. Physiologist 7, 124.
29. Fahlman, A., Hooker, S. K., Olszowka, A., Bostrom, B. L. and Jones, D. R. (2009). Estimating the effect of lung collapse and pulmonary shunt on gas exchange during breath-hold diving: the Scholander and Kooyman legacy. Respir. Physiol. Neurobiol. 165, 28-39.
30. Fedak, M. A., Pullen, M. R. and Kanwisher, J. (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.
31. Ferretti, G., Costa, M., Ferrigno, M., Grassi, B., Marconi, C., Lundgren, C. E. G. and Cerretelli, P. (1991). Alveolar gas composition and exchange during deep breath-hold diving and dry breath holds in elite divers. J. Appl. Physiol. 70, 794-802.
32. Ferrigno, M. and Lundgren, C. E. (2003). Breath-hold diving. In Physiology and Medicine of Diving (ed. A. O. Brubakk and T. S. Neuman), pp. 153-180. Edinburgh: Saunders.
33. Folkow, L. P., Ramirez, J.-M., Ludvigsen, S., Ramirez, N. and Blix, A. S. (2008). Remarkable neuronal hypoxia tolerance in the deep-diving adult hooded seal (Cystophora cristata). Neurosci. Lett. 446, 147-150.
34. Fujise, Y., Hidaka, H., Tatsukawa, R. and Miyazaki, N. (1985). External measurements and organ weights of five Weddell seals (Leptonychotes weddelli) caught near Syowa Station. Antarct. Rec. 85, 96-101.
35. Fuson, A. L., Cowan, D. F., Kanatous, S. B., Polasek, L. K. and Davis, R. W. (2003). Adaptations to hypoxia in the heart, kidneys, and splanchnic organs of harbor seals (Phoca vitulina). J. Exp. Biol. 206, 4139-4154.
36. Green, J. A., Halsey, L. G. and Butler, P. J. (2005). To what extent is the foraging behaviour of aquatic birds constrained by their physiology? Physiol. Biochem. Zool. 78, 766-781.
37. Grocott, M. P. W., Martin, D. S., Levett, D. Z. H., McMorrow, R., Windsor, J. and Montgomery, H. E. (2009). Arterial blood gases and oxygen content in climbers on Mount Everest. N. Engl. J. Med. 360, 140-149.
38. Gros, G., Wittenberg, B. A. and Jue, T. (2010). Myoglobin's old and new clothes: from molecular structure to function in living cells. J. Exp. Biol. 213, 2713-2725.
39. Grubb, B. R. (1981). Blood flow and oxygen consumption in avian skeletal muscle during hypoxia. J. Appl. Physiol. 50, 450-455.
40. Guppy, M., Hill, R. D., Liggins, G. C., Zapol, W. M. and Hochachka, P. W. (1986). Micro-computer assisted metabolic studies of voluntary diving of Weddell seals. Am. J. Physiol. 250, 175-187.
41. Guyton, G. P., Stanek, K. S., Schneider, R. C., Hochachka, P. W., Hurford, W. E., Zapol, D. G. and Zapol, W. M. (1995). Myoglobin-saturation in free-diving Weddell seals. J. Appl. Physiol. 79, 1148-1155.
42. Halasz, N. A., Elsner, R. and Garvie, R. S. (1974). Renal recovery from ischemia: a comparative study of harbor seal and dog kidneys. Am. J. Physiol. 227, 1331-1335.
43. Hassrick, J. L., Crocker, D. E., Teutschel, N. M., McDonald, B. I., Robinson, P. W., Simmons, S. E. and Costa, D. P. (2010). Condition and mass impact oxygen stores and dive duration in adult female northern elephant seals. J. Exp. Biol. 213, 585-592.
44. Hill, R. D., Schneider, R. C., Liggins, G. C., Schuette, A. H., Elliott, R. L., Guppy, M., Hochachka, P. W. and Zapol, W. M. (1987). Heart rate and body temperature during free diving of Weddell seals. Am. J. Physiol. 253, R344-R351.
45. Hindle, A. G., Young, B. L., Rosen, D. A. S., Haulena, M. and Trites, A. W. (2010). Dive response differs between shallow- and deep-diving Steller sea lions. J. Exp. Mar. Biol. Ecol. 394, 141-148.
46. Hochachka, P. W., Liggins, G. C., Qvist, J., Schneider, R. C., Snider, M. T., Wonders, T. R. and Zapol, W. M. (1977). Pulmonary metabolism for diving: conditioning blood for the brain. Science 198, 831-834.
47. Howell, A. B. (1930). Aquatic Mammals. New York: Dover.
48. Hudson, D. M. and Jones, D. R. (1986). The influence of body mass on the endurance to restrained submersion in the Pekin duck. J. Exp. Biol. 120, 351-367.
49. Hurford, W. E., Hochachka, P. W., Schneider, R. C., Guyton, G. P., Stanek, K. S., Zapol, D. G., Liggins, G. C. and Zapol, W. M. (1996). Splenic contraction, catecholamine release, and blood volume redistribution during diving in the Weddell seal. J. Appl. Physiol. 80, 298-306.
50. Irving, L. (1934). On the ability of warm-blooded animals to survive without breathing. Sci. Mon. 38, 422-428.
51. Irving, L. (1939). Respiration in diving mammals. Physiol. Rev. 19, 112-134.
52. Irving, L., Scholander, P. F. and Grinnell, S. W. (1941). Significance of the heart rate to the diving ability of seals. J. Cell. Comp. Physiol. 18, 283-297.
53. Jobsis, P. D., Ponganis, P. J. and Kooyman, G. L. (2001). Effects of training on forced submersion responses in harbor seals. J. Exp. Biol. 204, 3877-3885.
54. Kanatous, S. B., DiMichele, L. V., Cowan, D. F. and Davis, R. W. (1999). High aerobic capacities in the skeletal muscles of pinnipeds: adaptations to diving hypoxia. J. Appl. Physiol. 86, 1247-1256.
55. Kanatous, S. B., Davis, R. W., Watson, R., Polasek, L., Willliams, T. M. and Mathieu-Costello, O. (2002). Aerobic capacities in the skeletal muscles of Weddell seals: key to longer dive durations? J. Exp. Biol. 205, 3601-3608.
56. Keijer, E. and Butler, P. J. (1982). Volumes of the respiratory and circulatory systems in tufted and mallard ducks. J. Exp. Biol. 101, 213-220.
57. Kerem, D. and Elsner, R. (1973). Cerebral tolerance to asphyxial hypoxia in the harbor seal. Respir. Physiol. 19, 188-200.
58. Kerem, D. H., Hammond, D. D. and Elsner, R. (1973). Tissue glycogen levels in the Weddell seals (Leptonychotes weddelli): a possible adaptation to asphyxial hypoxia. Comp. Biochem. Physiol. 45, 731-736.
59. Kleiber, M. (1975). The Fire of Life. New York: Wiley and Sons.
60. Kooyman, G. L. (1968). An analysis of some behavioral and physiological characteristics related to diving in the Weddell seal. Antarct. Res. Ser. 11, 227-261.
61. Kooyman, G. L. (1985). Physiology without restraint in diving mammals. Mar. Mamm. Sci. 1, 166-178.
62. Kooyman, G. L. (1989). Diverse Divers Physiology and Behavior. Berlin: Springer-Verlag.
63. Kooyman, G. L. (2006). Mysteries of adaptation to hypoxia and pressure in marine mammals. The Kenneth S. Norris lifetime achievement award lecture. Mari. Mamm. Sci. 22, 507-526.
64. Kooyman, G. L. and Kooyman, T. G. (1995). Diving behavior of emperor penguins nurturing chicks at Coulman Island, Antarctica. Condor 97, 536-549.
65. Kooyman, G. L. and Ponganis, P. J. (1994). Emperor penguin oxygen consumption, heart rate and plasma lactate levels during graded swimming exercise. J. Exp. Biol. 195, 199-209.
66. Kooyman, G. L. and Ponganis, P. J. (1998). The physiological basis of diving to depth: birds and mammals. Annu. Rev. Physiol. 60, 19-32.
67. Kooyman, G. L. and Sinnett, E. E. (1982). Pulmonary shunts in harbor seals and sea lions during simulated dives to depth. Physiol. Zool. 55, 105-111.
68. Kooyman, G. L., Drabek, C. M., Elsner, R. and Campbell, W. B. (1971). Diving behavior of the emperor penguin, Aptenodytes forsteri. Auk 88, 775-795.
69. Kooyman, G. L., Kerem, D. H., Campbell, W. B. and Wright, J. J. (1973a). Pulmonary gas exchange in freely diving Weddell seals (Leptonychotes weddelli). Respir. Physiol. 17, 283-290.
70. 2 tensions of seals during simulated deep dives. Am. J. Physiol. 223, 1016-1020.
71. Kooyman, G. L., Schroeder, J. P., Greene, D. G. and Smith, V. A. (1973c). Gas exchange in penguins during simulated dives to 30 and 68?m. Am. J. Physiol. 225, 1467-1471.
72. Kooyman, G. L., Wahrenbrock, E. A., Castellini, M. A., Davis, R. W. and Sinnett, E. E. (1980). Aerobic and anaerobic metabolism during diving in Weddell seals: evidence of preferred pathways from blood chemistry and behavior. J. Comp. Physiol. 138, 335-346.
73. Kooyman, G. L., Castellini, M. A., Davis, R. W. and Maue, R. A. (1983). Aerobic dive limits in immature Weddell seals. J. Comp. Physiol. 151, 171-174.
74. Kooyman, G. L., Ponganis, P. J., Castellini, M. A., Ponganis, E. P., Ponganis, K. V., Thorson, P. H., Eckert, S. A. and LeMaho, Y. (1992). Heart rates and swim speeds of emperor penguins diving under sea ice. J. Exp. Biol. 165, 161-180.
75. Kooyman, G. L., Ponganis, P. J. and Howard, R. S. (1999). Diving animals. In The Lung at Depth (ed. C. Lundgren and J. Miller), pp. 587-620. New York: Marcel Dekker.
76. Kooyman, M. M. and Kooyman, G. L. (2009). Historical perspectives. Aquat. Mamm. 35, 523-556.
77. Lasiewski, R. C. and Calder, W. A. (1971). A preliminary allometric analysis of respiratory variables in resting birds. Respir. Physiol. 11, 152-166.
78. LeBoeuf, B. J., Costa, D. P., Huntley, A. C. and Feldkamp, S. D. (1988). Continuous, deep diving in female northern elephant seals, Mirounga angustirostris. Can. J. Zool. 66, 446-458.
79. Lenfant, C., Kooyman, G. L., Elsner, R. and Drabek, C. M. (1969). Respiratory function of the blood of the Adelie penguins (Pygoscelis adleiae). Am. J. Physiol. 216, 1598-1600.
80. Lenfant, C., Johansen, K. and Torrance, J. D. (1970). Gas transport and oxygen storage capacity in some pinnipeds and the sea otter. Respir. Physiol. 9, 277-286.
81. Lindholm, P. and Lundgren, C. E. G. (2009). The physiology and pathophysiology of human breath-hold diving. J. Appl. Physiol. 106, 284-292.
82. Liner, M. H. and Andersson, J. P. A. (2009). Hypoxic syncope in a competitive breath-hold diver with elevation of the brain damage marker S100B. Aviat. Space Environ. Med. 80, 1066-1068.
83. Lockyer, C. (1976). Body weights of some species of large whales. J. Cons. Int. Explor. Mer 36, 259-273.
84. Manohar, M., Goetz, T. E. and Hassan, A. S. (2001). Effect of prior high-intensity exercise on exercise-induced arterial hypoxemia in thoroughbred horses. J. Appl. Physiol. 90, 2371-2377.
85. Mason, R. J., Murray, J. F., Broaddus, V. C. and Nadel, T. A. (2005). Murray and Nadel's Textbook of Respiratory Medicine. Philadelphia: Elsevier Saunders.
86. Meir, J. U. and Ponganis, P. J. (2009). High-affinity hemoglobin and blood oxygen saturation in diving emperor penguins. J. Exp. Biol. 212, 3330-3338.
87. Meir, J. U. and Ponganis, P. J. (2010). Blood temperature profiles of diving elephant seals. Physiol. Biochem. Zool. 83, 531-540.
88. Meir, J. U., Stockard, T. K., Williams, C. L., Ponganis, K. V. and Ponganis, P. J. (2008). Heart rate regulation and extreme bradycardia in diving emperor penguins. J. Exp. Biol. 211, 1169-1179.
89. Meir, J. U., Champagne, C. D., Costa, D. P., Williams, C. L. and Ponganis, P. J. (2009). Extreme hypoxemic tolerance and blood oxygen depletion in diving elephant seals. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R927-R939.
90. Miller, P. J., Johnson, M. P., Tyack, P. L. and Terray, E. A. (2004). Swimming gait, passive drag and buoyancy of diving sperm whales. J. Exp. Biol. 207, 1953-1967.
91. Nakaoa, A., Netoa, J. S., Kannob, S., Stolzc, D. B., Kimizuka, K., Liud, F., Bache, F. H., Billarb, T. R., Choid, A. M., Otterbeind, L. E. et al. (2005). Protection against ischemia/reperfusion injury in cardicac and renal transplantation with carbon monoxide, bilverdin, and both. Am. J. Transplant. 5, 282-291.
92. Nunn, J. F. (1977). Applied Respiratory Physiology. London: Butterworths.
93. Odden, A., Folkow, L. P., Caputa, M., Hotvedt, R. and Blix, A. S. (1999). Brain cooling in seals. Acta Physiol. Scand. 166, 77-78.
94. Oliver, G. W., Morris, P. A., Thorson, P. H. and Le Boeuf, B. J. (1998). Homing behavior of juvenile northern elephant seals. Mar. Mamm. Sci. 14, 245-256.
95. Persson, S. G. B., Ekman, L., Lyden, G. and Tufvesson, G. (1973). Circulation effects of splenectomy in the horse I-IV. II. Effect on plasma volume and total and circulating red cell volume. Zentrabl. Veterinaermed. 20, 456-468.
96. Ponganis, P. J. (2011). Diving mammals. In Comprehensive Physiology (ed. R. Terjung), pp. 447-465. Hoboken, NJ: John Wiley & Sons, Inc.
97. Ponganis, P. J., Kooyman, G. L. and Castellini, M. A. (1993a). Determinants of the aerobic dive limit of Weddell seals: analysis of diving metabolic rates, post-dive end tidal PO2's, and blood and muscle oxygen stores. Physiol. Zool. 66, 732-749.
98. Ponganis, P. J., Kooyman, G. L., Castellini, M. A., Ponganis, E. P. and Ponganis, K. V. (1993b). Muscle temperature and swim velocity profiles during diving in a Weddell seal, Leptonychotes weddellii. J. Exp. Biol. 183, 341-348.
99. Ponganis, P. J., Costello, M. L., Starke, L. N., Mathieu-Costello, O. and Kooyman, G. L. (1997a). Structural and biochemical characteristics of locomotory muscles of emperor penguins, Aptenodytes forsteri. Respir. Physiol. 109, 73-80.
100. Ponganis, P. J., Kooyman, G. L., Starke, L. N., Kooyman, C. A. and Kooyman, T. G. (1997b). Post-dive blood lactate concentrations in emperor penguins, Aptenodytes forsteri. J. Exp. Biol. 200, 1623-1626.
101. Ponganis, P. J., Kooyman, G. L., Winter, L. M. and Starke, L. N. (1997c). Heart rate and plasma lactate responses during submerged swimming and diving in California sea lions (Zalophus californianus). J. Comp. Physiol. B 167, 9-16.
102. Ponganis, P. J., Kooyman, G. L., Van Dam, R. and Le Maho, Y. (1999). Physiological responses of king penguins during simulated diving to 136?m depth. J. Exp. Biol. 202, 2819-2822.
103. Ponganis, P. J., Van Dam, R. P., Marshall, G., Knower, T. and Levenson, D. H. (2000). Sub-ice foraging behavior of emperor penguins. J. Exp. Biol. 203, 3275-3278.
104. Ponganis, P. J., Van Dam, R. P., Knower, T. and Levenson, D. H. (2001). Temperature regulation in emperor penguins foraging under sea ice. Comp. Biochem. Physiol. 129A, 811-820.
105. Ponganis, P. J., Kreutzer, U., Sailasuta, N., Knower, T., Hurd, R. and Jue, T. (2002). Detection of myoglobin desaturation in Mirounga angustirostris during apnea. Am. J. Physiol. 282, R267-R272.
106. Ponganis, P. J., Kooyman, G. L. and Ridgway, S. H. (2003a). Comparative diving physiology. In Bennett and Elliott's Physiology and Medicine of Diving (ed. A. O. Brubakk and T. S. Neuman), pp. 211-226. Edinburgh: Saunders.
107. Ponganis, P. J., Van Dam, R. P., Levenson, D. H., Knower, T., Ponganis, K. V. and Marshall, G. (2003b). Regional heterothermy and conservation of core temperature in emperor penguins diving under sea ice. Comp. Biochem. Physiol. 135A, 477-487.
108. Ponganis, P. J., van Dam, R. P., Knower, T., Levenson, D. H. and Ponganis, K. V. (2004). Deep dives and aortic temperatures of emperor penguins: new directions for bio-logging at the isolated dive hole. Mem. Natl. Inst. Polar Res. Special Issue 58, 155-161.
109. Ponganis, P. J., Stockard, T., Levenson, D. H., Berg, L. and Barnov, E. A. (2006). Cardiac output and muscle blood flow during rest-associated apneas in elephant seals. Comp. Biochem. Physiol. 144A, 105-111.
110. 2 depletion underlies dive capacity of emperor penguins. J. Exp. Biol. 210, 4279-4285.
111. Ponganis, P. J., Kreutzer, U., Stockard, T. K., Lin, P. C., Sailasuta, N., Tran, T.-K., Hurd, R. and Jue, T. (2008). Blood flow and metabolic regulation in seal muscle during apnea. J. Exp. Biol. 211, 3323-3332.
112. 2 store management in diving emperor penguins. J. Exp. Biol. 212, 217-224.
113. Ponganis, P. J., Meir, J. U. and Williams, C. L. (2010). Oxygen store depletion and the aerobic dive limit in emperor penguins. Aquat. Biol. 8, 237-245.
114. Pugh, L. G. C. E. (1959). Carbon monoxide content of the blood and other observations on Weddell seals. Nature 183, 74-76.
115. Qvist, J., Hill, R. D., Schneider, R. C., Falke, K. J., Liggins, G. C., Guppy, M., Elliott, R. L., Hochachka, P. W. and Zapol, W. M. (1986). Hemoglobin concentrations and blood gas tensions of free-diving Weddell seals. J. Appl. Physiol. 61, 1560-1569.
116. Qvist, J., Hurford, W. E., Park, Y. S., Radermacher, P., Falke, K. J., Ahn, D. W., Guyton, G. P., Stanek, K. S., Hong, S. K., Weber, R. E. et al. (1993). Arterial blood gas tensions during breath-hold diving in the Korean ama. J. Appl. Physiol. 75, 285-293.
117. Ramirez, J.-M., Folkow, L. P. and Blix, A. S. (2007). Hypoxia tolerance in mammals and birds: from the wilderness to the clinic. Annu. Rev. Physiol. 69, 113-143.
118. 2 transport. J. Clin. Invest. 96, 1916-1926.
119. Ridgway, S. H. (1986). Diving by cetaceans. In Diving in Animals and Man (ed. A. O. Brubakk, J. W. Kanwisher and G. Sundnes), pp. 33-62. Trondheim: Royal Norwegian Society of Science and Letters.
120. Ridgway, S. H. and Johnston, D. G. (1966). Blood oxygen and ecology of porpoises of three genera. Science 151, 456-458.
121. Ridgway, S. H., Scronce, B. L. and Kanwisher, J. (1969). Respiration and deep diving in the bottlenose porpoise. Science 166, 1651-1654.
122. Sato, K., Naito, Y., Kato, A., Niizuma, Y., Watanuki, Y., Charassin, J. B., Bost, C.- A., Handrich, Y. and Le Maho, Y. (2002). Buoyancy and maximal diving depth in penguins: do they control inhaling air volume? J. Exp. Biol. 205, 1189-1197.
123. Sato, K., Mitani, Y., Camerson, M. F., Siniff, D. B. and Naito, Y. (2003). Factors affecting stroking patterns and body angle in diving Weddell seals under natural conditions. J. Exp. Biol. 206, 1461-1470.
124. Sato, K., Shiomi, K., Marshall, G., Kooyman, G. L. and Ponganis, P. J. (2011). Stroke rates and diving air volumes of emperor penguins: implications for dive performance. J. Exp. Biol. 214, 2854-2863.
125. Schmidt-Nielsen, K. (1997). Animal Physiology: Adaptation and Environment. Cambridge: Cambridge University Press.
126. Scholander, P. F. (1940). Experimental investigations on the respiratory function in diving mammals and birds. Hvalradets Skrifter 22, 1-131.
127. Scholander, P. F., Irving, L. and Grinnell, S. W. (1942). Aerobic and anaerobic changes in seal muscle during diving. J. Biol. Chem. 142, 431-440.
128. Shaffer, S. A., Costa, D. P., Williams, T. M. and Ridgway, S. H. (1997). Diving and swimming performance of white whales, Delphinapterus leucas: an assessment of plasma lactate and blood gas levels and respiratory rates. J. Exp. Biol. 200, 3091-3099.
129. Shiomi, K., Sato, K., Mitamura, H., Arai, N., Naito, Y. and Ponganis, P. J. (2008). Effect of ocean current on the dead-reckoning estimation of 3D dive paths of emperor penguins. Aquat. Biol. 3, 265-270.
130. Simpson, J. G., Gilmartin, W. G. and Ridgway, S. H. (1970). Blood volume and other hematologic values in young elephant seals (Mirounga angustirostris). Am. J. Vet. Res. 31, 1449-1452.
131. Skrovan, R. C., Williams, T. M., Berry, P. S., Moore, P. W. and Davis, R. W. (1999). The diving physiology of bottlenose dolphins (Tursiops truncatus). II. Biomechanics and changes in buoyancy at depth. J. Exp. Biol. 202, 2749-2761.
132. Sleet, R. B., Sumich, J. L. and Weber, L. J. (1981). Estimates of total blood volume and total body weight of sperm whale (Physeter catodon). Can. J. Zool. 59, 567-570.
133. Snyder, G. K. (1983). Respiratory adaptations in diving mammals. Respir. Physiol. 54, 269-294.
134. Stephenson, R. (1995). Respiratory and plumage gas volumes in unrestrained diving ducks (Aythya affinis). Respir. Physiol. 100, 129-137.
135. Stephenson, R. and Jones, D. R. (1992). Metabolic responses to forced dives in Pekin duck measured by indirect calorimetry and 31P-MRS. Am. J. Physiol. 263, R1309-R1317.
136. 2 and oxygen depletion during dives of emperor penguins. J. Exp. Biol. 208, 2973-2981.
137. Stockard, T. K., Levenson, D. H., Berg, L., Fransioli, J. R., Baranov, E. A. and Ponganis, P. J. (2007). Blood oxygen depletion during rest-associated apneas of northern elephant seals (Mirounga angustirostris). J. Exp. Biol. 210, 2607-2617.
138. Thompson, D. and Fedak, M. A. (1993). Cardiac responses of grey seals during diving at sea. J. Exp. Biol. 174, 139-164.
139. Thorson, P. H. and Le Boeuf, B. J. (1994). Developmental aspects of diving in northern elephant seal pups. In Elephant Seals: Population Ecology, Behavior, and Physiology (ed. B. J. Le Boeuf and R. M. Laws), pp. 271-289. Berkeley: University of California Press.
140. 2 in human skeletal muscle. Am. J. Physiol. 276, R1682-R1690.
141. van Dam, R. P., Ponganis, P. J., Ponganis, K. V., Levenson, D. H. and Marshall, G. (2002). Stroke frequencies of emperor penguins diving under sea ice. J. Exp. Biol. 205, 3769-3774.
142. Vázquez-Medina, J. P., Zenteno-Savín, T. and Elsner, R. (2006). Antioxidant enzymes in ringed seal tissues: potential protection against dive-associated ischemia/reperfusion. Comp. Biochem. Physiol. 142C, 198-204.
143. Vázquez-Medina, J. P., Zenteno-Savín, T. and Elsner, R. (2007). Glutathione protection against dive-associated ischemia/reperfusion in ringed seal tissues. J. Exp. Mar. Biol. Ecol. 345, 110-118.
144. Weber, R. E., Hemmingsen, E. A. and Johansen, K. (1974). Functional and biochemical studies of penguin myoglobin. Comp. Biochem. Physiol. 49B, 197-214.
145. Weise, M. J. and Costa, D. P. (2007). Total body oxygen stores and physiological diving capacity of California sea lions as a function of sex and age. J. Exp. Biol. 210, 278-289.
146. West, J. B., Hackett, P. H., Maret, K. H., Milledge, J. S., Peters, R. M., Jr, Pizzo, C. J. and Winslow, R. M. (1983). Pulmonary gas exchange on the summit of Mt. Everest. J. Appl. Physiol. 55, 678-687.
147. Wienecke, B., Robertson, G., Kirkwood, R. and Lawton, K. (2007). Extreme dives by free-ranging emperor penguins. Polar Biol. 30, 133-142.
148. Williams, C. L., Meir, J. U. and Ponganis, P. J. (2011). What triggers the aerobic dive limit? Muscle oxygen depletion during dives of emperor penguins. J. Exp. Biol. 214, 1801-1812.
149. Williams, T. M., Kooyman, G. L. and Croll, D. A. (1991). The effects of submergence on heart rate and oxygen consumption of swimming seals and sea lions. J. Comp. Physiol. B 160, 637-644.
150. Williams, T. M., Haun, J. E. and Friedl, W. A. (1999). The diving physiology of bottlenose dolphins (Tursiops truncatus). I. Balancing the demands of exercise for energy conservation at depth. J. Exp. Biol. 202, 2739-2748.
151. Williams, T. M., Davis, R. W., Fuiman, L. A., Francis, J., Le Boeuf, B. J., Horning, M., Calambokidis, J. and Croll, D. A. (2000). Sink or swim: strategies for costefficient diving by marine mammals. Science 288, 133-136.
152. Williams, T. M., Fuiman, L. A., Horning, M. and Davis, R. W. (2004). The cost of foraging by a marine predator, the Weddell seal Leptonychotes weddellii: pricing by the stroke. J. Exp. Biol. 207, 973-982.
153. Williams, T. M., Zavanelli, M., Miller, M. A., Goldbeck, R. A., Morledge, M., Casper, D., Pabst, D. A., McClellan, W., Cantin, L. P. and Kliger, D. S. (2008). Running, swimming, and diving modifies neuroprotecting globins in the mammalian brain. Proc. R. Soc. B 275, 751-758.
154. Yumino, D. and Bradley, T. D. (2008). Central sleep apnea and Cheyne-Stokes respiration. Proc. Am. Thorac. Soc. 5, 226-236.
155. Zapol, W. M., Liggins, G. C., Schneider, R. C., Qvist, J., Snider, M. T., Creasy, R. K. and Hochachka, P. W. (1979). Regional blood flow during simulated diving in the conscious Weddell seal. J. Appl. Physiol. 47, 968-973.
156. Zenteno-Savin, T., St. Leger, J. and Ponganis, P. J. (2010). Hypoxemic and ischemic tolerance in emperor penguins. Comp. Biochem. Physiol. 152C, 18-23.