Comprehensive Physiology Wiley Online Library

Life Under Water: Physiological Adaptations to Diving and Living at Sea

Full Article on Wiley Online Library



Abstract

This review covers the field of diving physiology by following a chronological approach and focusing heavily on marine mammals. Because the study of modern diving physiology can be traced almost entirely to the work of Laurence Irving in the 1930s, this particular field of physiology is different than most in that it did not derive from multiple laboratories working at many locations or on different aspects of a similar problem. Because most of the physiology principles still used today were first formulated by Irving, it is important to the study of this field that the sequence of thought is examined as a progression of theory. The review covers the field in roughly decadal blocks and traces ideas as they were first suggested, tested, modified and in some cases, abandoned. Because diving physiology has also been extremely dependent on new technologies used in the development of diving recorders, a chronological approach fits well with advances in electronics and mechanical innovation. There are many species that dive underwater as part of their natural behavior, but it is mainly the marine mammals (seals, sea lions, and whales) that demonstrate both long duration and dives to great depth. There have been many studies on other diving species including birds, snakes, small aquatic mammals, and humans. This work examines these other diving species as appropriate and a listing of reviews and relevant literature on these groups is included at the end. © 2012 American Physiological Society. Compr Physiol 2:1889‐1919, 2012.

Comprehensive Physiology offers downloadable PowerPoint presentations of figures for non-profit, educational use, provided the content is not modified and full credit is given to the author and publication.

Download a PowerPoint presentation of all images


Figure 1. Figure 1.

Arterial blood and muscle lactate concentrations during forced submersion in harbor seals. Adapted, with permission, from ().

Figure 2. Figure 2.

Diagram of the general arrangement of the isolated‐hole diving hut for Weddell seals on the Antarctic sea ice. Adapted, with permission, from ().

Figure 3. Figure 3.

Relationship of heart rate to dive duration in adult Weddell seals. Adapted, with permission, from ().

Figure 4. Figure 4.

Percent change of organ blood flow, mL/(min · kg) during simulated diving in Weddell seal. Asterisk beneath bar denotes probability dive value different from control (P < 0.005). Adapted, with permission, from ().

Figure 5. Figure 5.

A summary of the peak arterial lactic acid concentrations obtained during recovery from various dive durations in Weddell seals. The diamond at the abscissa zero is the average resting lactic acid concentration. Adapted, with permission, from ().

Figure 6. Figure 6.

Postdive circulating lactate concentrations and diving duration of emperor penguin, Baikal seal, and Weddell seal. Adapted, with permission, from ().



Figure 1.

Arterial blood and muscle lactate concentrations during forced submersion in harbor seals. Adapted, with permission, from ().



Figure 2.

Diagram of the general arrangement of the isolated‐hole diving hut for Weddell seals on the Antarctic sea ice. Adapted, with permission, from ().



Figure 3.

Relationship of heart rate to dive duration in adult Weddell seals. Adapted, with permission, from ().



Figure 4.

Percent change of organ blood flow, mL/(min · kg) during simulated diving in Weddell seal. Asterisk beneath bar denotes probability dive value different from control (P < 0.005). Adapted, with permission, from ().



Figure 5.

A summary of the peak arterial lactic acid concentrations obtained during recovery from various dive durations in Weddell seals. The diamond at the abscissa zero is the average resting lactic acid concentration. Adapted, with permission, from ().



Figure 6.

Postdive circulating lactate concentrations and diving duration of emperor penguin, Baikal seal, and Weddell seal. Adapted, with permission, from ().

References
 1. Andersen HT. Factors determining the circulatory adjustments to diving: I. Water immersion. Acta Physiol Scand 58: 173‐185, 1963.
 2. Andersen HT. The reflex nature of the physiological adjustments to diving and their afferent pathway. Acta Physiol Scand 58: 263‐273, 1963.
 3. Andersen HT. Physiological adaptations in diving vertebrates. Physiol Rev 46: 212‐243, 1966.
 4. Andrews RD, Costa DP, Le Boeuf BJ, Jones DR. Breathing frequencies of northern elephant seals at sea and on land revealed by heart rate spectral analysis. Respir Physiol 123: 71‐85, 2000.
 5. Andrews RD, Williams JD, Jones DR. Heart rate responses to apnea on land and at sea in northern elephant seals (Mirounga angustirostris). Am Zool 32: 31A, 1992.
 6. Angell‐James JE, de Burgh Daly M. Some mechanisms involved in the cardiovascular adaptations to diving. Symp Soc Exp Biol 26: 313‐341, 1972.
 7. Angell‐James JE, Elsner R, Daly MD. Lung inflation: Effects on heart rate, respiration, and vagal afferent activity in seals. Am J Physiol 240: H190‐H198, 1981.
 8. Bailleul F, Authier M, Ducatez S, Roquet F, Charrassin JB, Cherel Y, Guinet C. Looking at the unseen: Combining animal bio‐logging and stable isotopes to reveal a shift in the ecological niche of a deep‐diving predator. Ecography 33: 709‐719, 2010.
 9. Bailleul F, Cotte C, Guinet C. Mesoscale eddies as foraging area of a deep‐diving predator, the southern elephant seal. Mar Ecol Prog Ser 408: 251‐264, 2010.
 10. Baker DA, Gough Da. A continuous, implantable lactate sensor. Anal Chem 67: 1536‐1540, 1995.
 11. Barnett CH, Harrison RJ, Tomlinson JDW. Variations in the venous systems of mammals. Biol Rev Camb Philos Soc 33: 442‐487, 1958.
 12. Bartholomew GA. Body temperature and respiratory and heart rates in the northern elephant seal. J Mammal 35: 211‐218, 1954.
 13. Belkin DA. Variations in heart rate during voluntary diving in the turtle Pseudemys concinna. Copeia 2: 321‐330, 1964.
 14. Bengtson J, Stewart B. Diving and haulout behavior of crabeater seals in the Weddell Sea, Antarctica, during March 1986. Pol Biol 12: 635‐644, 1992.
 15. Bennett KA, McConnell BJ, Moss SEW, Speakman JR, Pomeroy PP, Fedak MA. Effects of age and body mass on development of diving capabilities of gray seal pups: Costs and benefits of the postweaning fast. Physiol Biochem Zool 83: 911‐923, 2010.
 16. Bennett PB, Coggin R, McLeod M. Effect of compression rate on use of trimix to ameliorate HPNS in man to 686 m (2250 ft). Undersea Biomed Res 9: 335‐351, 1982.
 17. Bennett PB, McLeod M. Probing the limits of human deep diving. Philos Trans R Soc Lond B Biol Sci 304: 105‐117, 1984.
 18. Bert P. Lecons Sur La Physiologie Comparee De La Respiration. In: Bailliere JB et Fils, editor. Paris. 1870, p. 526‐553.
 19. Blackwell SB, Le Boeuf BJ. Developmental aspects of sleep‐apnea in northern elephant seals, Mirounga‐angustirostris. J Zool 231: 437‐447, 1993.
 20. Blix AS, Berg T, Fyhn HJ. Lactate dehydrogenase in a diving mammal, the common seal (Phoca vitulina vitulina L.). Int J Biochem 1: 292‐294, 1970.
 21. Blix AS, Kjekshus JK, Enge I, Bergan A. Myocardial blood flow in the diving seal. Acta Physiol Scand 96: 277‐280, 1976.
 22. Blix AS, Elsner RW, Kjekshus JK. Cardiac output and its distribution through capillaries and A‐V shunts in diving seals. Acta Physiol Scand 118: 109‐116, 1983.
 23. Blix AS, Folkow B. Cardiovascular adjustments to diving in mammals and birds. In: Shepherd JT, Abboud FM, editors. Handbook of Physiology: The Cardiovascular System, Section 2. Bethesda, MD: Am Physiol Soc, 1983, p. 917‐945.
 24. Blix AS. Diving responses: Fact or fiction. News Physiol Sci 2: 64‐66, 1987.
 25. Bograd SJ, Block BA, Costa DP, Godley BJ. Biologging technologies: New tools for conservation. Introduction. Endang Spec Res 10: 1‐7, 2010.
 26. Bornemann H, Mohr E, Plotz J. Monitoring the feeding‐behavior on freely diving Weddell seals (Leptonychotes weddellii). J Vet Med 39: 228‐235, 1992.
 27. Boutilier RG, Reed JZ, Fedak MA. Unsteady‐state gas exchange and storage in diving marine mammals: The harbor porpoise and gray seal. Am J Physiol 281: R490‐R494, 2001.
 28. Boyd IL, Croxall JP. Diving behaviour of lactating Antarctic fur seals. Can J Zool 70: 919‐928, 1992.
 29. Bradley SE, Bing RS. Renal function in the Harbor seal (Phoca vitulina) during asphyxial ischemia and pyrogenic hyperemia. J Cell Comp Physiol 19: 229‐237, 1942.
 30. Bradley SE, Mudge GH, Blake WD. The renal excretion of sodium, potassium, and water by the harbor seal (Phoca vitulina): Effect of apnea; sodium, potassium, and water loading; pitressin; and mercurial diuresis. J Cell Comp Physiol 43: 1‐22, 1954.
 31. Brauer RW, Bennett PB, Elliot DH. The high pressure nervous syndrome: animals. In: Bennett PB, Elliott DH, editros. The Physiology and Medicine of Diving, and Compressed Air Work. Baltimore: Williams and Wilkins Co, 1975, p. 231‐247.
 32. Bron KM, Murdaugh HV, Millen JE, Lenthall R, Raskin P, Robin ED. Arterial constrictor response in a diving mammal. Science 152: 540‐543, 1966.
 33. Burns JM. The development of diving behavior in juvenile Weddell seals: Pushing physiological limits in order to survive. Can J Zool 77: 737‐747, 1999.
 34. Burns JM, Castellini MA, Testa JW. Movements and diving behavior of weaned Weddell seal (Leptonychotes weddellii) pups. Pol Biol 21: 23‐36, 1999.
 35. Burns JM, Lestyk KC, Folkow LP, Hammill MO, Blix AS. Size and distribution of oxygen stores in harp and hooded seals from birth to maturity. J Comp Physiol B 177: 687‐700, 2007.
 36. Burns JM, Schreer JF, Castellini MA. Physiological effects on dive patterns and foraging strategies in yearling Weddell seals (Leptonychotes weddellii). Can J Zool 75: 1796‐1810, 1997.
 37. Burns JM, Testa JW, Battaglia B, Valencia J, Walton DWH. Developmental changes and diurnal and seasonal influences on the diving behavior of Weddell seal (Leptonychotes weddellii) pups. In: Battaglia B, Valencia J, Walton DWH, editors. Antarctic Communities. Cambridge: Cambridge University Press, 1997, p. 328‐334.
 38. Butler P, Jones DR. Onset and recovery from diving bradycardia in ducks. J Physiol (Lond) 196: 225‐272, 1968.
 39. Butler PJ. Respiratory and cardiovascular control during diving in birds and mammals. J Exp Biol 100: 195‐221, 1982.
 40. Butler PJ. The exercise response and the “classical” diving response during natural submersion in birds and mammals. Can J Zool 66(1): 29‐39, 1988.
 41. Butler PJ. Aerobic dive limit. What is it and is it always used appropriately? Comp Biochem Physiol A 145: 1‐6, 2006.
 42. Butler PJ, Amlaner JCJ, MacDonald DW. The use of radio telemetry in the studies of diving and flying of birds. In: Amlaner CJ, Macdonald DW, editors. A Handbook on Biotelemetry and Radio Tracking. Oxford: Pergamon Press, 1979, p. 569‐577.
 43. Butler PJ, Jones DR. The comparative physiology of diving in vertebrates. Adv Comp Physiol Biochem 8: 179‐364, 1982.
 44. Butler PJ, Woakes AJ. Changes in heart rate and respiratory frequency during natural behavior of ducks with particular reference to diving. J Exp Biol 79: 283‐300, 1979.
 45. Cantu‐Medellin N, Byrd B, Hohn A, Vazquez‐Medina JP, Zenteno‐Savin T. Differential antioxidant protection in tissues from marine mammals with distinct diving capacities. Shallow/short vs. deep/long divers. Comp Biochem Physiol A Mol Integr Physiol 158: 438‐443, 2011.
 46. Carbone C, Houston AI. The optimal allocation of time over the dive cycle: An approach based on aerobic and anaerobic respiration. Anim Behav 51: 1247‐1255, 1996.
 47. Castellini M. History of polar whaling: insights into the physiology of the great whales. Comp Biochem Physiol A 126: 153‐159, 2000.
 48. Castellini M. Pressure tolerance in diving birds and mammals. In: Sebert P, editor. Comparative High Pressure Biology. Enfield, NH: Science Publishers, 2010, p. 373‐392.
 49. Castellini M, Baskurt O, Castellini JM, Meiselman HJ. Blood rheology in marine mammals. Front Physiol 2: 1‐8, 2010.
 50. Castellini MA. Closed systems: Resolving potentially conflicting demands of diving and exercise in marine mammals. In: Gilles R, editor. Circulation, Respiration and Metabolism Current Comparative Approaches. Berlin: Springer‐Verlag, 1985, p. 219‐226.
 51. Castellini MA. The biology of diving mammals: Behavioral, physiological and biochemical limits. In: Gilles R, editor. Advances in Comparative and Environmental Physiology. Berlin: Springer‐Verlag, 1991, p. 105‐134.
 52. Castellini MA. Apnea tolerance in the elephant seal during sleeping and diving: Physiological mechanisms and correlations. In: Le Boeuf BJ, Laws RM, editors. Elephant Seals. Berkeley, CA: University of California Press, 1993, p. 343‐353.
 53. Castellini MA. Dreaming about diving: Sleep apnea in seals. News Physiol Sci 11: 208‐214, 1996.
 54. Castellini MA, Castellini JM. Influence of hematocrit on whole blood glucose levels: new evidence from marine mammals. Am J Physiol 256: R1220‐R1224, 1989.
 55. Castellini MA, Castellini JM. Defining the limits of diving biochemistry in marine mammals. Comp Biochem Physiol 139: 509‐518, 2004.
 56. Castellini MA, Castellini JM, Kirby VL. Effects of standard anticoagulants and storage procedures on plasma glucose values in seals. J Am Vet Med Assoc 201: 145‐148, 1992.
 57. Castellini MA, Costa DP, Huntley AC. Hematocrit variation during sleep apnea in elephant seal pups. Am J Physiol 251: R429‐R431, 1986.
 58. Castellini MA, Davis RW, Kooyman GL. Blood chemistry regulation during repetitive diving in Weddell seals. Physiol Zool 61: 379‐386, 1988.
 59. Castellini MA. Fuel homeostasis and organ function using single injection tracer techniques in marine mammals. In: Castellini MA, Huntley AC, Costa DP, Worthy GAJ, editors. Approaches to Marine Mammal Energetics. Society for Marine Mammalogy, 1987, p. 1‐13.
 60. Castellini MA, Kooyman GL. Behavior of freely diving animals. Undersea Biomed Res 16: 355‐362, 1989.
 61. Castellini MA, Kooyman GL, Ponganis PJ. Metabolic rates of freely diving Weddell seals: Correlations with oxygen stores, swim velocity and diving duration. J Exp Biol 165: 181‐194, 1992.
 62. Castellini MA, Milsom W, Berger R, Costa D, Jones D, Castellini J, Rea L, Bharma S, Harris M. Patterns of respiration and heart rate during wakefulness and sleep in elephant seal pups. Am J Physiol 266: R863‐R869, 1994.
 63. Castellini MA, Murphy BJ, Fedak M, Ronald K, Gofton N, Hochachka PW. Potentially conflicting metabolic demands of diving and exercise in seals. J Appl Physiol 58(2): 392‐399, 1985.
 64. Castellini MA, Rea LD, Sanders JL, Castellini JM, Zenteno‐Savin T. Developmental changes in cardiorespiratory patterns of sleep‐associated apnea in northern elephant seals. Am J Physiol 267: R1294‐R1301, 1994.
 65. Castellini MA, Rivera PM, Castellini JM. Adaptations to pressure in the RBC metabolism of diving mammals. Comp Biochem Physiol 129(A): 751‐757, 2001.
 66. Castellini MA, Rivera PM, Castellini JM. Biochemical aspects of pressure tolerance in marine mammals. Comp Biochem Physiol 133: 893‐899, 2002.
 67. Castellini MA, Somero GN. Buffering capacity of vertebrate muscle: Correlations with potential for anaerobic function. J Comp Physiol 143: 191‐198, 1981.
 68. Castellini MA, Somero GN, Kooyman GL. Glycolytic enzyme activities in tissues of marine and terrestrial mammals. Physiol Zool 54(2): 242‐252, 1981.
 69. Clark CA, Burns JM, Schreer JF, Hammill MO. Erythropoietin concentration in developing harbor seals (Phoca vitulina). Gen Comp Endocrinol 147: 262‐267, 2006.
 70. Clark CA, Burns JM, Schreer JF, Hammill MO. A longitudinal and cross‐sectional analysis of total body oxygen store development in nursing harbor seals Phoca vitulina. J Comp Physiol B 177: 217‐227, 2007.
 71. Costa D. The secret life of marine mammals. Oceanography 6: 120‐128, 1993.
 72. Costa DP. Reproductive and foraging energetics of high‐latitude penguins, albatrosses and pinnipeds ‐ implications for life‐history patterns. Am Zool 31: 111‐130, 1991.
 73. Costa DP, Sinervo B. Field physiology: Physiological insights from animals in nature. Annu Rev Physiol 66: 209‐238, 2004.
 74. Costa DP, Huckstadt LA, Crocker DE, McDonald BI, Goebel ME, Fedak MA. Approaches to studying climatic change and its role on the habitat selection of Antarctic pinnipeds. Integ Comp Biol 50: 1018‐1030, 2010.
 75. Cox TM, Ragen TJ, Read AJ, Vos E, Baird RW, Balcomb K, Barlow J, Caldwell J, Cranford T, Crum L, D'Amico A, D'Spain G, Fernández A, Finneran J, Gentry R, Gerth W, Gulland F, Hildebrand J, Houser D, Hullar T, Jepson PD, Ketten D, Macleod CD, Miller P, Moore S, Mountain DC, Palka D, Ponganis P, Rommel S, Rowles T, Taylor B, Tyack P, Wartzok D, Gisiner R, Mead J, Benner L. Understanding the impacts of anthropogenic sound on beaked whales. J Cet Res Manag 7: 177‐187, 2006.
 76. Craig AB, Pasche A. Respiratory physiology of freely diving harbor seals (Phoca vitulina). Physiol Zool 53: 419‐432, 1980.
 77. Croll DA, Nishiguchi MK, Kaupp S. Pressure and lactate dehydrogenase function in diving mammals and birds. Physiol Zool 65(5): 1022‐1027, 1992.
 78. Daly MD. Interactions between respiration and circulation. In: Cherniack NS, Widdicombe JG, editors. Handbook of Physiology: The Respiratory System II, Section 3. Bethesda, MD: American Physiological Society, 1986, p. 529‐594.
 79. Daly MD, Elsner R, Angell‐James JE. Cardiorespiratory control by carotid chemoreceptors during experimental dives in the seal. Am J Physiol 232: H508‐H516, 1977.
 80. Davis RW. Lactate and glucose metabolism in resting and diving harbor seals (Phoca vitulina). J Comp Physiol 153: 275‐288, 1983.
 81. Davis RW, Castellini MA, Kooyman GL, Maue RA. Renal glomerular filtration rate and hepatic blood flow during voluntary diving in Weddell seals. Am J Physiol 245: R743‐R748, 1983.
 82. Davis RW, Castellini MA, Williams TM, Kooyman GL. Fuel homeostasis in the harbor seal during submerged swimming. J Comp Physiol 160B: 627‐635, 1992.
 83. Davis RW, Kanatous SB. Convective oxygen transport and tissue oxygen consumption in Weddell seals during aerobic dives. J Exp Biol 202: 1091‐1113, 1999.
 84. Davis RW, Polasek L, Watson R, Fuson A, Williams TM, Kanatous SB. The diving paradox: New insights into the role of the dive response in air‐breathing vertebrates. Comp Biochem Physiol A 138: 263‐268, 2004.
 85. Davydov AF, Makarova AR. Changes in heat regulation and circulation in newborn seals on transition to aquatic form of life. Fiziologicheskii Zhurnal SSSR imeni Schenova 50: T563‐T566, 1964.
 86. Dawson RW. Laurence Irving: An appreciation. Physiol Biochem Zool 80: 9‐24, 2007.
 87. de Bruijn R, Richardson M, Schagatay E. Oxygen‐conserving effect of the diving response in the immersed human. Div Hyperb Med 39: 193‐199, 2009.
 88. Delong RL, Stewart BS, Hill RD. Documenting migrations of northern elephant seals using day length. Mar Mamm Sci 8: 155‐159, 1992.
 89. Dormer KJ, Denn MJ, Stone HL. Cerebral blood flow in the sea lion (Zalophus californianus) during voluntary dives. Comp Biochem Physiol 58: 11‐18, 1977.
 90. Dragon AC, Monestiez P, Bar‐Hen A, Guinet C. Linking foraging behaviour to physical oceanographic structures: Southern elephant seals and mesoscale eddies east of Kerguelen Islands. Prog Ocean 87: 61‐71, 2010.
 91. DuBois KP, Geiling EMK, McBride AF, Thomson JF. Studies on the intermediary carbohydrate metabolism of aquatic animals. J Gen Physiol 31: 347‐359, 1948.
 92. Dunn JF, Hochachka PW, Davison W, Guppy M. Metabolic adjustments to diving and recovery in the African lungfish. Am J Physiol 245: R651‐R657, 1983.
 93. Dykes RW. Factors related to the dive reflex in harbor seals: Respiration, immersion, bradycardia and lability of the heart rate. Can J Physiol Pharmacol 52: 248‐258, 1974.
 94. Dykes RW. Factors related to the dive reflex in harbor seals: Sensory contributions from the trigeminal region. Can J Physiol Pharmacol 52: 259‐265, 1974.
 95. Eguchi T, Harvey JT. Diving behavior of the Pacific harbor seal (Phoca vitulina richardii) in Monterey Bay, California. Mar Mamm Sci 21: 283‐295, 2005.
 96. Eliassen E. Cardiovascular Responses to Submersion Asphyxia in Avian Divers. Bergen: Norwegian Universities Press, 1960, pp.
 97. Elsner R, Angell‐James JE, de Burgh Daly M. Carotid body chemoreceptor reflexes and their interactions in the seal. Am J Physiol 1: H517‐H525, 1977.
 98. Elsner R, Franklin L, Van Citters RL, Kenney DW. Cardiovascular defenses against asphyxia. Science 153: 941‐949, 1966.
 99. Elsner RW. Diving bradycardia in the unrestrained hippopotamus. Nature 212: 408‐408, 1966.
 100. Elsner RW. Diving mammals. Sci J 6: 68‐74, 1970.
 101. Elsner RW, Hammond DD, Parker HR. Circulatory responses to asphyxia in pregnant and fetal animals: A comparative study of Weddell seals and sheep. Yale J Biol Med 42: 202‐217, 1970.
 102. Elsner RW, Scholander PF. Circulatory adaptations to diving in animals and man. In: Rahn H, editor. Physiology of Breath‐hold Diving and the Ama of Japan. Washington, D.C.: National Academy of Sciences, National Research Council, 1965, p. 281‐294.
 103. Elsner RW, Shurley JT, Hammond DD, Brooks RE. Cerebral tolerance to hypoxemia in asphyxiated Weddell seals. Respir Physiol 9: 287‐297, 1970.
 104. Elsner RW, Gooden B. Diving and Asphyxia: A Comparative Study of Animals and Man. Cambridge: Physiological Society Monograph 40. Cambridge University Press, 1983, 168 pp.
 105. Fahlman A, Hooker SK, Szowka A, Bostrom BL, Jones DR. 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, 2009.
 106. Fairbanks ES, Kilgore JDL. Post‐dive oxygen consumption of restrained and unrestrained muskrats (Ondatra zibethica). Comp Biochem Physiol 59A: 113‐117, 1978.
 107. Falabella V, Campagna C, Lewis M. Electrocardiography of southern elephant seal (Mirounga leonina) weanlings. J Zoo Wildl Med 30: 526‐531, 1999.
 108. Falabella V, Lewis M, Campagna C. Development of cardiorespiratory patterns associated with terrestrial apneas in free‐ranging southern elephant seals. Physiol Biochem Zool 72: 64‐70, 1999.
 109. Falke KJ, Hill RD, Qvist J, Schneider RC, Guppy M, Liggins GC, Hochachka PW, Elliott RE, Zapol WM. Seal lungs collapse during free diving: Evidence from arterial nitrogen tensions. Science 229: 556‐558, 1985.
 110. Fernandez A, Edwards JF, Rodriguez F, de los Monteros AE, Herraez P, Castro P, Jaber JR, Martin V, Arbelo M. “Gas and fat embolic syndrome” involving a mass stranding of beaked whales (Family Ziphiidae) exposed to anthropogenic sonar signals. Vet Pathol 42: 446‐457, 2005.
 111. Ferrante FL. Oxygen conservation during submergence apnea in a diving mammal, the nutria. Am J Physiol 218: 363‐371, 1970.
 112. Field CL, Walker NJ, Tablin F. Northern elephant seal platelets: Analysis of shape change and response to platelet agonists. Thromb Res 101: 267‐277, 2001.
 113. Fitz‐Clarke JR. Mechanics of airway and alveolar collapse in human breath‐hold diving. Respir Physiol Neurobiol 159: 202‐210, 2007.
 114. Foster GE, Sheel AW. The human diving response, its function, and its control. Scand J Med Sci Sports 15: 3‐12, 2005.
 115. Fowler SL, Costa DP, Arnould JPY, Gales NJ, Burns JM. Ontogeny of oxygen stores and physiological diving capability in Australian sea lions. Func Ecol 21: 922‐935, 2007.
 116. Fuiman LA, Madden KM, Williams TM, Davis RW. Structure of foraging dives by Weddell seals at an offshore isolated hole in the Antarctic fast‐ice environment. Deep Sea Res II: Top Stud Oceano 54: 270‐289, 2007.
 117. Gabrielsen G. Free and forced diving in ducks: Habituation of the initial dive response. Acta Physiol Scand 123: 67‐72, 1985.
 118. Gallivan GJ. Hypoxia and hypercapnia in the respiratory control of the Amazonian manatee (Trichechus inunguis). Physiol Zool 53: 254‐261, 1980.
 119. Gallivan GJ, Kanwisher JW, Best RC. Heart rates and gas exchange in the Amazonian manatee (Trichechus inunguis). J Comp Physiol 156: 415‐423, 1986.
 120. Gentry RL, Kooyman GL. Fur Seals: Maternal Strategies on Land and at Sea. Princeton, NJ: Princeton University Press, 1986, p. 291.
 121. Gooden BA, Stone HL, Young S. Cardiac responses to snout immersion in trained dogs. J Physiol (Lond) 242: 405‐414, 1974.
 122. Gooden BA. Why some people do not drown ‐ hypothermia versus the diving response. Med J Aust 157: 629‐632, 1992.
 123. Goodyear JD. A sonic/radio tag for monitoring dive depths and underwater movements of whales. J Wildl Manag 57: 503‐513, 1993.
 124. Grinnell SW, Irving L, Scholander PF. Experiments on the relation between blood flow and heart rate in the diving seal. J Cell Comp Physiol 19: 341‐350, 1942.
 125. Guppy M, Hill RD, Schneider RC, Qvist J, Liggins GC, Zapol WM, Hochachka PW. Microcomputer‐assisted metabolic studies of voluntary diving of Weddell seals. Am J Physiol 250: R175‐R187, 1986.
 126. Guyton GP, Stanek KS, Schneider RC, Hochachka PW, Hurford WE, Zapol DG, Liggins GC, Zapol WM. Myoglobin saturation in free‐diving Weddell seals. J Appl Physiol 79: 1148‐1155, 1995.
 127. Haddad GG, Jeng HJ, Lai TL. Heart rate variability during respiratory pauses in puppies and dogs. Pediatr Res 22: 306‐311, 1987.
 128. Hagihara R, Jones RE, Sheppard JK, Hodgson AJ, Marsh H. Minimizing errors in the analysis of dive recordings from shallow‐diving animals. J Exp Mar Biol Ecol 399: 173‐181, 2011.
 129. Halsey MJ. Effects of high pressure on the central nervous system. Physiol Rev 62: 1341‐1377, 1982.
 130. Harrison RJ, Tomlinson JDW. Observations on the venous system in certain pinnipedia and cetacea. Proc Zool Soc London 126: 205‐231, 1956.
 131. Harrison RJ, Tomlinson JDW. Normal and experimental diving in the common seal (Phoca vitulina). Mammalia 24: 386‐399, 1960.
 132. Harrison RJ, Kooyman GL. General physiology of the pinnipedia. In: Harrison RJ, Hubbard RC, Petersen RS, Rice C, Schusterman RJ, editors. The Behavior and Physiology of Pinnipeds. New York: Appleton‐Century‐Crofts, 1968, p. 211‐296.
 133. Harrison RJ, Ridgway S. Restrained and unrestrained diving in seals. Rapp P‐v Reun Cons Int Explor Mer 169: 76‐80, 1975.
 134. Harrison RJ, Ridgway S, Joyce PL. Telemetry of heart rate in diving seals. Nature 238: 280‐281, 1972.
 135. Hayward JS, Hay C, Matthews BR, Overweel CH, Radford DD. Temperature effect on the human dive response in relation to cold water near‐drowning. J Appl Physiol 56: 202‐206, 1984.
 136. Heath AG. Cardiac responses of larval and adult tiger salamanders to submergence and emergence. Comp Biochem Physiol 65A: 439‐444, 1980.
 137. Hempleman HV, Lockwood APM. The Physiology of Diving in Man and Other Animals. London: Edward Arnold, 1978, 58 pp.
 138. Hill RD. Microcomputer monitor and blood sampler for free‐diving Weddell seals. J Appl Physiol 61: 1570‐1576, 1986.
 139. Hindell MA, Slip DJ, Burton HR. The diving behaviour of adult male and female Southern elephant seals, Mirounga leonina (Pinnipedia: Phocidae). Aust J Zool 39: 595‐619, 1991.
 140. Hindell MA, Slip DJ, Burton HR, Bryden MM. Physiological implications of continuous, prolonged, and deep dives of the southern elephant seal (Mirounga leonina). Can J Zool 70: 370‐379, 1992.
 141. Hindle AG, Horning M. Energetics of breath‐hold hunting: Modeling the effects of aging on foraging success in the Weddell seal. J Theor Biol 264: 673‐682, 2010.
 142. Hindle AG, Horning M, Mellish JAE, Lawler JM. Diving into old age: Muscular senescence in a large‐bodied, long‐lived mammal, the Weddell seal (Leptonychotes weddellii). J Exp Biol 212: 790‐796, 2009.
 143. Hochachka PW. How animal anaerobes do it without oxygen: A summary of enzyme and metabolic mechanisms. Proceedings of the Canadian Society of Zoologists Annual Meeting, June 2‐5, p. 35‐46, 1974.
 144. Hochachka PW. Living Without Oxygen: Closed Systems in Hypoxia Tolerance. Cambridge: Harvard University Press, 1980, 181 pp.
 145. Hochachka PW. Brain, lung and heart function during diving and recovery. Science 212: 509‐514, 1981.
 146. Hochachka PW, Castellini JM, Hill RD, Schneider RC, Bengtson JL, Hill SE, Liggins GC, Zapol WM. Protective metabolic mechanisms during liver ischemia: Transferable lessons from long‐diving animals. Mol Cell Biochem 84: 77‐85, 1988.
 147. Hochachka PW, Dunn JF. Metabolic arrest: The most effective means of protecting tissues against hypoxia. Prog Clin Biol Res 136: 297‐309, 1983.
 148. Hochachka PW, Guppy M. Metabolic Arrest and the Control of Biological Time. Cambridge: Harvard University Press, 1987, 227 pp.
 149. Hochachka PW, Liggins GC, Qvist J, Schneider R, Snider MY, Wonders TR, Zapol WM. Pulmonary metabolism during diving: Conditioning blood for the brain. Science 198: 831‐834, 1977.
 150. Hochachka PW, Murphy B. Metabolic status during diving and recovery in marine mammals. In: Robertshaw D, editor. International Review of Physiology, Environmental Physiology III. Baltimore: Park Press, 1979, p. 253‐287.
 151. Hochachka PW, Owen TG, Allen JF, Whittow GC. Multiple end products of anaerobiosis in diving vertebrates. Comp Biochem Physiol 50B: 17‐22, 1975.
 152. Hochachka PW, Somero GN. Strategies of Biochemical Adaptation. Philadelphia: W.B. Saunders Company, 1973, 358 pp.
 153. Hochachka PW, Taylor CR, Johansen K. Anaerobic metabolism: Living without oxygen. In: Taylor CR, editor. A Companion to Animal Physiology. London: Cambridge University Press, 1982, p. 138‐150.
 154. Hooker SK, Heaslip SG, Matthiopoulos J, Cox O, Boyd IL. Data sampling options for animal‐borne video cameras: Considerations based on deployments with Antarctic fur seals. Mar Tech Soc J 42: 65‐75, 2008.
 155. Houston AI, Carbone C. The optimal allocation of time during the diving cycle. Behav Ecol 3: 255‐265, 1992.
 156. Huang TF, Peng YI. Role of chemoreceptor in diving bradycardia in rat. Jpn J Physiol 26: 395‐401, 1976.
 157. Hudson DM, Jones DR. Remarkable blood catecholamine levels in forced dived ducks. J Exp Zool 224: 451‐456, 1982.
 158. Hurford WE, Hochachka PW, Schneider RC, Guyton GP, Stanek KS, Zapol DG, Liggins GC, Zapol WM. Splenic contraction, catecholamine release, and blood volume redistribution during diving in the Weddell seal. J Appl Physiol 80: 298‐306, 1996.
 159. Huxley FM. On the reflex nature of apnoea in the duck in diving: The reflex nature of submersion apnoea. Acta Physiol Scand 101: 148‐157, 1913.
 160. Irving L. On the ability of mammals to survive without breathing. The Collecting Net 8: 138‐141, 1933.
 161. Irving L. On the ability of warm‐blooded animals to survive without breathing. Sci Month 38: 422‐428, 1934.
 162. Irving L. The protection of whales from the danger of caisson disease. Science 81: 560‐561, 1935.
 163. Irving L. A demonstration of the respiratory control of seals. The Collecting Net 11: 204, 1936.
 164. Irving L. Respiration of beaver. J Cell Comp Physiol 9: 437‐451, 1937.
 165. Irving L. Changes in the blood flow through the brain and muscles during the arrest of breathing. Am J Physiol 122: 207‐214, 1938.
 166. Irving L. Respiration in diving mammals. Physiol Rev 19: 112‐134, 1939.
 167. Irving L. Elective regulation of the circulation in diving animals. In: Norris KS, editor. Whales, Dolphins and Porpoises. Los Angeles: University of California Press, 1966, p. 381‐396.
 168. Irving L. Temperature regulation in marine mammals. In: Anderson HT, editor. The Biology of Marine Mammals. New York and London: Academic Press, 1969, p. 147‐174.
 169. Irving L, Scholander PF, Grinnell SW. Significance of the heart rate to the diving ability of seals. J Cell Comp Physiol 18: 283‐297, 1941.
 170. Irving L, Scholander PF, Grinnell SW. The respiration of the porpoise, Tursiops truncatus. J Cell Comp Physiol 17: 145‐168, 1941.
 171. Irving L, Scholander PF, Grinnell SW. The regulation of arterial blood pressure in the seal during diving. Am J Physiol 135: 557‐566, 1942.
 172. Irving L, Solandt OM, Solandt DY, Fisher DJ. Respiratory characteristics of the blood of the seal. J Cell Comp Physiol 6: 393‐403, 1935.
 173. Irving L, Solandt OM, Solandt DY, Fisher KC. The respiratory metabolism of the seal and its adjustments to diving. J Cell Comp Physiol 7: 137‐151, 1935.
 174. Irving L, Welch HG. The effect of the composition of the inspired air on the circulation through the brain. Q J Exp Physiol 25: 121‐129, 1935.
 175. Jacob JS, McDonald HS. Diving bradycardia in four species of North American aquatic snakes. Comp Biochem Physiol 53A: 69‐72, 1976.
 176. Johansen K. Heart activity during experimental diving of snakes. Am J Physiol 197: 604‐606, 1959.
 177. Johansen K, Lenfant C, Grigg GC. Respiratory properties of blood and responses to diving of the platypus, Ornithorhynchus anatinus (Shaw). Comp Biochem Physiol 18: 597‐608, 1966.
 178. Jones DR, Fisher HD, McTaggart S, West NH. Heart rate during breath‐holding and diving in the unrestrained harbor seal (Phoca vitulina richardi). Can J Zool 51: 671‐680, 1973.
 179. Jones DR, West NH, Bamford OS, Drummond PC, Lord RA. The effect of the stress of forcible submergence on the diving response in muskrats (Ondatra zibethica). Can J Zool 60: 187‐193, 1982.
 180. Kanatous SB, DiMichele LV, Cowan DF, Davis RW. High aerobic capacities in the skeletal muscles of pinnipeds: Adaptations to diving hypoxia. J Appl Physiol 86: 1247‐1256, 1999.
 181. Kanatous SB, Garry DJ. Gene deletional strategies reveal novel physiological roles for myoglobin in striated muscle. Respir Physiol Neurobiol 151: 151‐158, 2006.
 182. Kanatous SB, Hawke TJ, Trumble SJ, Pearson LE, Watson RR, Garry DJ, Williams TM, Davis RW. The ontogeny of aerobic and diving capacity in the skeletal muscles of Weddell seals. J Exp Biol 211: 2559‐2565, 2008.
 183. Kanwisher JW, Gabrielsen G, Kanwisher N. Free and forced diving habits in birds. Science 211: 717‐719, 1981.
 184. Kayar SR, Fahlman A, Lin WC, Whitman WB. Increasing activity of H‐2‐metabolizing microbes lowers decompression sickness risk in pigs during H‐2 dives. J Appl Physiol 91: 2713‐2719, 2001.
 185. Kerem D, Elsner R. Cerebral tolerance to asphyxial hypoxia in the harbor seal. Respir Physiol 19: 188‐200, 1973.
 186. Kerem DH, Hammond DD, Elsner RW. Tissue glycogen levels in the Weddell seal (Leptonychotes weddelli): A possible adaptation to asphyxial hypoxia. Comp Biochem Physiol 45: 731‐736, 1973.
 187. Kjekshus JK, Blix AS, Elsner R, Millard R, Hol R. The multifactorial approach to myocardial salvage. The experience from diving seals. Acta Med Scand Suppl 651: 49‐57, 1981.
 188. Kjekshus JK, Blix AS, Elsner RW, Hol R, Amundsen E. Myocardial blood flow and metabolism in the diving seal. Am J Physiol 242: R97‐R104, 1982.
 189. Kooyman GL. Techniques used in measuring diving capacities of Weddell seals. Polar Rec 12: 391‐394, 1965.
 190. Kooyman GL. Maximum diving capacities of the Weddell seal, (Leptonychotes weddelli). Science 151: 1553‐1554, 1966.
 191. Kooyman GL. An analysis of some behavioral and physiological characteristics related to diving in the Weddell seal. In: Schmitt WL, Llano GA, editors. Antarctic Research Series Biology of the Antarctic Seals III, Vol. 11. Washington, DC: American Geophysical Union, 1968, 227‐261.
 192. Kooyman GL. The Weddell seal. Sci Am 221: 3‐8, 1969.
 193. Kooyman GL, Kerem DH, Campbell WB, Wright JJ. Pulmonary function in freely diving Weddell seals, Leptonychotes weddelli. Respir Physiol 12: 271‐282, 1971.
 194. Kooyman GL. Deep diving behaviour and effects of pressure in reptiles, birds, and mammals. In: Sleigh MA, Macdonald AG, editors. The Effects of Pressure on Organisms: Symposia of the Society for Experimental Biology. Cambridge: Cambridge University Press, 1972, p. 295‐311.
 195. Kooyman GL. Respiratory adaptations in marine mammals. Am Zool 13: 457‐478, 1973.
 196. Kooyman GL. Weddell seal: Consummate Diver. Cambridge: Cambridge University Press, 1981, 135 pp.
 197. Kooyman GL. Physiology without restraint in diving mammals. Mar Mamm Sci 1(2): 166‐178, 1985.
 198. Kooyman GL. Pressure and the diver. Can J Zool 66: 84‐88, 1988.
 199. Kooyman GL. Diverse Divers: Physiology and Behavior. Berlin: Springer‐Verlag, 1989, 216 pp.
 200. Kooyman GL. Mysteries of adaptation to hypoxia and pressure in marine mammals ‐ The Kenneth S. Norris lifetime achievement award lecture ‐ Presented on 12 December 2005 ‐ San Diego, California. Mar Mamm Sci 22: 507‐526, 2006.
 201. Kooyman GL, Campbell WB. Heart rate in freely diving Weddell seals, Leptonychotes weddelli. Comp Biochem Physiol 43A: 31‐36, 1972.
 202. Kooyman GL, Castellini MA, Davis RW. Physiology of diving in marine mammals. Annu Rev Physiol 43: 343‐356, 1981.
 203. Kooyman GL, Castellini MA, Davis RW, Maue RA. Aerobic diving limits of immature Weddell seals. J Comp Physiol 151: 171‐174, 1983.
 204. Kooyman GL. A reappraisal of diving physiology: Seals and penguins. In: Dejours P, Bolis L, Taylor CR, Weibel ER, editors. Comparative Physiology: Life in Water and on Land. Berlin: Springer‐Verlag, 1987, p. 459‐469.
 205. Kooyman GL, Gentry RL, Urquhart DL. Northern fur seal diving behavior: A new approach to its study. Science 193: 411‐412, 1976.
 206. Kooyman GL, Kerem DH, Campbell WB, Wright JJ. Pulmonary gas exchange in freely diving Weddell seals, Leptonychotes weddelli. Respir Physiol 17: 283‐290, 1973.
 207. Kooyman GL, Ponganis PJ. The physiological basis of diving to depth: Birds and mammals. Annu Rev Physiol 60: 19‐32, 1998.
 208. Kooyman GL, Ronald KW, Mansfield AW. Physiology of freely diving Weddell seals. In: Ronald K, Mansfield AW, editors. Rapp P v Reun Cons int Explor Mer Denmark: Host and Son, Charlottenlund Slot, 1975, p. 441‐444.
 209. Kooyman GL, Schroeder JP, Denison DM, Hammond DD, Wright JJ, Bergman WP. Blood nitrogen tensions of seals during simulated deep dives. Am J Physiol 223: 1016‐1020, 1972.
 210. Kooyman GL. Behavior and physiology of diving. In: Stonehouse B, editor. The Biology of Penguins. London: MacMillan Press, 1974, p. 115‐137.
 211. Kooyman GL, Wahrenbrock EA, Castellini MA, Davis RW, Sinnett EE. Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: Evidence of preferred pathways from blood chemistry and behavior. J Comp Physiol 138: 335‐346, 1980.
 212. Kooyman GL. Diving physiology. Marine Mammals. In: Wood SF, editor. Comparative Pulmonary Physiology: Current Concepts. New York: Marcel Dekker, Inc, 1988, p. 721‐734.
 213. Krogh A. The comparative physiology of respiratory organs. Cell Mol Life Sci 2: 431‐438, 1946.
 214. Kuhn CE, McDonald BI, Shaffer SA, Barnes J, Crocker DE, Burns J, Costa DP. Diving physiology and winter foraging behavior of a juvenile leopard seal (Hydrurga leptonyx). Pol Biol 29: 303‐307, 2006.
 215. Ladd M, Raisz L, Crowder CH, Page LB. Filtration rate and water diuresis in the seal, Phoca vitulina. J Cell Comp Physiol 38: 157‐164, 1951.
 216. Le Boeuf BJ. Incredible diving machines. Natural History 89: 35‐40, 1989.
 217. Le Boeuf BJ, Costa DP, Huntley AC, Feldkamp SD. Continuous, deep diving in female northern elephant seals, Mirounga angustirostris. Can J Zool 66: 446‐4580, 1988.
 218. Le Boeuf BJ, Costa DP, Huntley AC, Kooyman GL, Davis RW. Pattern and depth of dives in northern elephant seal, Mirounga angustirostris. J Zool 208: 1‐7, 1986.
 219. Le Boeuf BJ. Variation in the diving pattern of Northern Elephant seals with age, mass, sex, and reproductive condition. In: Le Boeuf BJ, Laws RM, editors. Elephant Seals: Population Ecology, Behavior, and Physiology. Berkeley: University of California Press, 1994, p. 237‐252.
 220. Le Boeuf BJ, Naito Y, Huntley AC, Asaga T. Prolonged, continuous, deep diving by northern elephant seals. Can J Zool 67: 2514‐2519, 1989.
 221. Lea MA, Johnson D, Melin S, Ream R, Gelatt T. Diving ontogeny and lunar responses in a highly migratory mammal, the northern fur seal Callorhinus ursinus. Mar Ecol Prog Ser 419: 233‐247, 2010.
 222. Lenfant C. Physiological properties of blood of marine mammals. In: Andersen HT, editor. The Biology of Marine Mammals. New York: Academic Press, 1969, p. 95‐116.
 223. Lenfant C, Elsner R, Kooyman GL, Drabek CM. Respiratory function of the blood of the adult and fetus Weddell seal, Leptonychotes weddelli. Am J Physiol 216: 1595‐1597, 1969.
 224. Lenfant C, Johansen K, Torrance JD. Gas transport and oxygen storage capacity in some pinnipeds and the sea otter. Respir Physiol 9: 277‐286, 1970.
 225. Liamin OI, Mukhametov LM, Poliakova IG. Features of sleep in the water by the northern fur seal Callorhinus ursinus. Zh Vyssh Nerv Deiat Im I P Pavlova 36: 1039‐1044, 1986.
 226. Liamin OI, Oleksenko AI, Poliakova IG. Sleep and wakefulness in Greenland seal pups. Zhurnal Vysshei Nervnoi Deiatelnosti Imeni I‐P‐Pavlova 39: 1061‐1069, 1989.
 227. Lin YC, Matsuura DT, Whittow GC. Respiratory variation of heart rate in the California sea lion. Am J Physiol 222: 260‐264, 1972.
 228. Lin YC. Autonomic nervous control of cardiovascular response during diving in the rat. Am J Physiol 227: 601‐605, 1974.
 229. Lin YC. Breath‐hold diving in terrestrial mammals. Exerc Sport Sci Rev 10: 270‐307, 1982.
 230. Lowrance PB, Nickel JF, Smythe CM, Bradely SE. Comparison of the effects of anoxic anoxia and apnea on renal function in the harbor seal (Phoca vitulina, L.). J Cell Comp Physiol 48: 35‐49, 1956.
 231. Lyamin OI, Chetybrok IS. Unilateral EEG activation during sleep in the cape fur seal, Arctocephalus pusillus. Neurosci Lett 143: 263‐266, 1992.
 232. Lyamin OI, Oleksenko AI, Polyakova IG. Sleep in the harp seal (Pagophilus groenlandica) ‐ peculiarities of sleep in pups during the 1st month of their lives. J Sleep Res 2: 163‐169, 1993.
 233. Lyamin OI, Manger PR, Mukhametov LM, Siegel JM, Shpak OV. Rest and activity states in a gray whale. J Sleep Res 9: 261‐267, 2000.
 234. Lyamin OI, Lapierre JL, Kosenko PO, Mukhametov LM, Siegel JM. Electroencephalogram asymmetry and spectral power during sleep in the northern fur seal. J Sleep Res 17: 154‐165, 2008.
 235. Lydersen C, Hammill MO. Diving in ringed seal (Phoca hispida) pups during the nursing period. Can J Zool 71: 985‐996, 1993.
 236. Madden KM, Fuiman LA, William TM, Davis RW. Identification of foraging dives in free‐ranging Weddell seals Leptonychotes weddellii: confirmation using video records. Mar Ecol Prog Ser 365: 263‐275, 2008.
 237. Mate B, Mesecar R, Lagerquist B. The evolution of satellite‐monitored radio tags for large whales: One laboratory's experience. Deep‐Sea Res II, Top Stud Oceanogr 54: 224‐247, 2007.
 238. McConnell BJ, Chambers C, Fedak MA. Foraging ecology of southern elephant seals in relation to the bathymetry and productivity of the Southern ocean. Ant Sci 4(4): 393‐398, 1992.
 239. McIntyre T, de Bruyn P, Ansorge I, Bester M, Bornemann H, Plötz J, Tosh C. A lifetime at depth: Vertical distribution of southern elephant seals in the water column. Pol Biol 33: 1037‐1048, 2010.
 240. McKean TA. Cardiovascular adjustments to laboratory diving in beavers and nutria. Am J Physiol 11: R434‐R440, 1982.
 241. Meir JU, Champagne CD, Costa DP, Williams CL, Ponganis PJ. Extreme hypoxemic tolerance and blood oxygen depletion in diving elephant seals. Am J Physiol 297: R927‐R939, 2009.
 242. Meir JU, Ponganis PJ. High‐affinity hemoglobin and blood oxygen saturation in diving emperor penguins. J Exp Biol 212: 3330‐3338, 2009.
 243. Meir JU, Ponganis PJ. Blood temperature profiles of diving elephant seals. Physiol Biochem Zool 83: 531‐540, 2010.
 244. Millard RW, Johansen K, Milsom WK. Radiotelemetry of cardiovascular responses to exercise and diving in penguins. Comp Biochem Physiol 46: 227‐240, 1973.
 245. Miller NJ, Daniels CB, Costa DP, Orgeig S. Control of pulmonary surfactant secretion in adult California sea lions. Biochem Biophys Res Commun 313: 727‐732, 2004.
 246. Miller NJ, Postle AD, Schurch S, Schoel WM, Daniels CB, Orgeig S. The development of the pulmonary surfactant system in California sea lions. Comp Biochem Physiol A Mol Integr Physiol 141: 191‐199, 2005.
 247. Miller NJ, Daniels CB, Schurch S, Schoel WM, Orgeig S. The surface activity of pulmonary surfactant from diving mammals. Respir Physiol Neurobiol 150: 220‐232, 2006.
 248. Miller NJ, Postle AD, Orgeig S, Koster G, Daniels CB. The composition of pulmonary surfactant from diving mammals. Respir Physiol Neurobiol 152: 152‐168, 2006.
 249. Milsom W, Castellini M, Harris M, Castellini J, Jones D, Berger R, Bahrma S, Rea L, Costa D. Effects of hypoxia and hypercapnia on patterns of sleep‐associated apnea in elephant seal pups. Am J Physiol 40: R1017‐R1024, 1996.
 250. Mitani Y, Andrews RD, Sato K, Kato A, Naito Y, Costa DP. Three‐dimensional resting behaviour of northern elephant seals: drifting like a falling leaf. Biol Lett 6: 163‐166, 2010.
 251. Mitz SA, Reuss S, Folkow LP, Blix AS, Ramirez JM, Hankeln T, Burmester T. When the brain goes diving: Glial oxidative metabolism may confer hypoxia tolerance to the seal brain. Neuroscience 163: 552‐560, 2009.
 252. Mukhametov LM. Sleep in marine mammals. Exp Brain Res 8: 227‐238, 1988.
 253. Mukhametov LM, Lyamin OI, Chetyrbok IS, Vassilyev AA, Diaz RP. Sleep in an Amazonian manatee, Trichechus inunguis. Experientia 48: 417‐419, 1992.
 254. Murdaugh HV, Cross CE, Millen JE, Gee JBL, Robin ED. Dissociation of bradycardia and arterial constriction during diving in the seal, phoca vitulina. Science 162: 364‐365, 1968.
 255. Murdaugh HV, Jackson JE. Heart rate and blood lactic acid concentration during experimental diving of water snakes. Am J Physiol 202: 1163‐1165, 1962.
 256. Murphy B, Zapol WM, Hochachka PW. Metabolic activities of heart, lung, and brain during diving and recovery in the Weddell seal. J Appl Physiol 48: 596‐605, 1980.
 257. Murphy BJ, Hochachka PW. Free amino acid profiles in blood during diving and recovery in the Antarctic Weddell seal. Can J Zool 59: 455‐459, 1981.
 258. Nagel EL, Morgane PJ, McFarland WL, Galliano RE. Rete mirabile of dolphins: Its pressure damping effect on cerebral circulation. Science 161: 898‐899, 1968.
 259. Naito Y. What is “Bio‐Logging”? Aquatic Mammals 36: 308‐322, 2010.
 260. Olsen CR, Fanestil DD, Scholander PF. Some effects of breath holding and apneic underwater diving on cardiac rhythm in man. J Appl Physiol 17: 461‐466, 1962.
 261. Olsen CR, Fanestil DD, Scholander PF. Some effects of apneic underwater diving on blood gases, lactate, and pressure in man. J Appl Physiol 17: 938‐942, 1962.
 262. Padman L, Costa DP, Bolmer ST, Goebel ME, Huckstadt LA, Jenkins A, McDonald BI, Shoosmith DR. Seals map bathymetry of the Antarctic continental shelf. Geophys Res Lett 37: 1‐5, 2010.
 263. Page LB, Scott‐Baker JC, Zak GA, Becker EL, Baxter CF. The effect of variation in filtration rate on the urinary concentrating mechanism in the seal, Phoca vitulina L. J Cell Comp Physiol 43: 257‐269, 1954.
 264. Panneton WM, Gan Q, Juric R. The rat: A laboratory model for studies of the diving response. J Appl Physiol 108: 811‐820, 2010.
 265. Pasche A, Krog J. Heart rate in resting seals on land and in water. Comp Biochem Physiol 67A: 77‐83, 1980.
 266. Påsche A. The effect of hypercapnia on respiratory characteristics and diving behaviour of freely diving seals. Respir Physiol 26: 183‐193, 1976.
 267. Ponganis PJ, Kooyman GL. Diving physiology of penguins. In: Buter PJ, Jones DR, editors. Acta XX Congressus Internationalis Ornithologici. Wellington: New Zealand Ornithological Congress Trust Board, 1991, p. 1887‐1892.
 268. Ponganis PJ, Kooyman GL. Diving physiology of birds: A history of studies on polar species. Comp Biochem Physiol 126: 143‐151, 2000.
 269. Ponganis PJ, Kooyman GL, Baranov EA, Thorson PH, Stewart BS. The aerobic submersion limit of Baikal seals, Phoca sibirica. Can J Zool 75: 1323‐1327, 1997.
 270. Ponganis PJ, Kooyman GL, Winter LM, Starke LN. Heart rate and plasma lactate responses during submerged swimming and trained diving in California sea lions, Zalophus californianus. J Comp Physiol [B] 167: 9‐16, 1997.
 271. Ponganis PJ, Kreutzer U, Sailasuta N, Knower T, Hurd R, Jue T. Detection of myoglobin desaturation in Mirounga angustirostris during apnea. Am J Physiol 282: R267‐R272, 2002.
 272. Ponganis PJ, Kreutzer U, Stockard TK, Lin PC, Sailasuta N, Tran TK, Hurd R, Jue T. Blood flow and metabolic regulation in seal muscle during apnea. J Exp Biol 211: 3323‐3332, 2008.
 273. Ponganis PJ, Meir JU, Williams CL. Oxygen store depletion and the aerobic dive limit in emperor penguins. Aq Biol 8: 237‐245, 2010.
 274. Ponganis PJ, Ponganis EP, Ponganis KV, Kooyman GL, Gentry RL, Trillmich F. Swimming velocities in otariids. Can J Zool 68: 2105‐2112, 1990.
 275. Pough FH. Heart rate, breathing and voluntary diving of the elephant trunk snake, acrochordus javanicus. Comp Biochem Physiol 44A: 183‐189, 1973.
 276. Prewitt JS, Freistroffer DV, Schreer JF, Hammill MO, Burns JM. Postnatal development of muscle biochemistry in nursing harbor seal (Phoca vitulina) pups: Limitations to diving behavior? J Comp Physiol B 180: 757‐766, 2010.
 277. Qvist J, Hill RD, Schneider RC, Falke KJ, Liggins GC, Guppy M, Elliot RL, Hochachka PW, Zapol WM. Hemoglobin concentrations and blood gas tensions of free‐diving Weddell seals. J Appl Physiol 61: 1560‐1569, 1986.
 278. Qvist J, Hurford WE, Park YS, Radermacher P, Falke KJ, Ahn DW, Guyton GP, Stanek KS, Hong SK, Weber RE, Zapol WM. Arterial blood‐gas tensions during breath‐hold diving in the Korean alma. J Appl Physiol 75: 285‐293, 1993.
 279. Reed JZ, Chambers C, Fedak MA, Butler PJ. Gas‐exchange of captive freely diving grey seals (Halichoerus grypus). J Exp Biol 191: 1‐18, 1994.
 280. Richet C. De la resistance des canards a l'asphyxie. J Physiol Pathol Gen 1: 641‐650, 1899.
 281. Richmond JP, Burns JM, Rea LD, Mashburn KL. Postnatal ontogeny of erythropoietin and hematology in free‐ranging Steller sea lions (Eumetopias jubatus). Gen Comp Endocrinol 141: 240‐247, 2005.
 282. Richmond JP, Burns JM, Rea LD. Ontogeny of total body oxygen stores and aerobic dive potential in Steller sea lions (Eumetopias jubatus). J Comp Physiol B 176: 535‐545, 2006.
 283. Ridgway SH. Homeostasis in the aquatic environment. In: Ridgway SH, editor. Mammals of the Sea Biology and Medicine. Springfield: Charles C. Thomas, 1972, p. 590‐748.
 284. Ridgway SH, Harrison RJ, Joyce PL. Sleep and cardiac rhythm in the gray seal. Science 187: 553‐555, 1975.
 285. Ridgway SH, Howard R. Dolphin lung collapse and intramuscular circulation during free diving: Evidence from nitrogen washout. Science 206: 1182‐1183, 1979.
 286. Robin ED. Of seals and mitochondria. N Engl J Med 275: 646‐652, 1966.
 287. Robin ED, Ensinck J, Hance AJ, Newman A, Lewiston N, Cornell L, Davis RW, Theodore J. Glucoregulation and simulated diving in the harbor seal, Phoca vitulina. Am J Physiol 241: R293‐R300, 1981.
 288. Robin ED, Murdaugh JV, Pyron W, Weiss E, Soteres P. Adaptations to diving in the harbor seal ‐ gas exchange and ventilatory response to CO2. Am J Physiol 205: 1175‐1177, 1963.
 289. Robinson PW, Simmons SE, Crocker DE, Costa DP. Measurements of foraging success in a highly pelagic marine predator, the northern elephant seal. J Anim Ecol 79: 1146‐1156, 2010.
 290. Schaefer KE, Allison RD, Dougherty JH Jr, Carey CR, Walker R, Yost F, Parker D. Pulmonary and circulatory adjustments determining the limits of depths in breathhold diving. Science 162: 1020‐1023, 1968.
 291. Schagatay E, Andersson J. Diving response and apneic time in humans. Undersea Hyperb Med 25: 13‐19, 1998.
 292. Schagatay E, Holm B. Effects of water and ambient air temperatures on human diving bradycardia. Eur J Appl Physiol 73: 1‐6, 1996.
 293. Schmidt‐Nielsen B, Murdaugh HV, O'Dell R, Bacsanyi J. Urea excretion and diving in the seal (Phoca vitulina). J Cell Comp Physiol 53: 393‐411, 1959.
 294. Scholander PF. Experimental investigations on the respiratory function in diving mammals and birds. Hvalradets Skrifter, Norske Videnskamp‐Akad, Oslo 22: 1‐131, 1940.
 295. Scholander PF. The Master Switch of Life. Sci Am 209: 92‐106, 1963.
 296. Scholander PF. Animals in aquatic environments: Diving mammals and birds. In: Dill DB, Adolph E, Wiber CG, editors. Handbook of Physiology: Adaptation to the Environment, Section 4. Bethesda, MD: Am Physiol Soc, 1964, p. 729‐740.
 297. Scholander PF. Enjoying a Life in Science: The Autobiography of P.F. Scholander. Fairbanks: University of Alaska Press, 1990, 226 pp.
 298. Scholander PF, Hammel HT, Lemessurier H, Hemmingsen E, Garey W. Circulatory adjustment in pearl divers. J Appl Physiol 17: 184‐190, 1962.
 299. Scholander PF, Irving L, Grinnell SW. On the temperature and metabolism of the seal during diving. J Cell Comp Physiol 19: 67‐78, 1942.
 300. Scholander PF, Irving L, Grinnell SW. Aerobic and anaerobic changes in seal muscle during diving. J Biol Chem 142: 431‐440, 1942.
 301. Seymour RS. Blood lactate in free‐diving sea snakes. Copeia 1979 (3): 494‐497, 1979.
 302. Shaffer SA, Costa DP, Williams TM, Ridgway SH. 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, 1997.
 303. Simmons SE, Tremblay Y, Costa DP. Pinnipeds as ocean‐temperature samplers: Calibrations, validations, and data quality. Limnol Ocean Meth 7: 648‐656, 2009.
 304. Simon LM, Robin ED, Elsner R, Van Kessel ALGJ, Theodore J. A biochemical basis for differences in maximal diving time in aquatic mammals. Comp Biochem Physiol 47B: 209‐215, 1974.
 305. Sinnett EE, Kooyman GL, Wahrenbrock EA. Pulmonary circulation of the harbor seal. J Appl Physiol 45: 718‐727, 1978.
 306. Slip DJ, Hindell MA, Burton HR. Diving behavior of Southern Elephant seals from Macquarie Island: An overview. In: Le Boeuf BJ, Laws RM, editors. Elephant Seals: Population Ecology, Behavior, and Physiology. Berkeley: University of California Press, 1994, p. 253‐270.
 307. Snyder GK. Respiratory adaptations in diving mammals. Respir Physiol 54: 269‐294, 1983.
 308. Spragg RG, Ponganis PJ, Marsh JJ, Rau GA, Bernhard W. Surfactant from diving aquatic mammals. J Appl Physiol 96: 1626‐1632, 2004.
 309. Stephens PA, Carbone C, Boyd IL, McNamara JM, Harding KC, Houston AI. The scaling of diving time budgets: Insights from an optimality approach. Am Nat 171: 305‐314, 2008.
 310. Stockard TK, Levenson DH, Berg L, Fransioli JR, Baranov EA, Ponganis PJ. Blood oxygen depletion during rest‐associated apneas of northern elephant seals (Mirounga angustirostris). J Exp Biol 210: 2607‐2617, 2007.
 311. Storey KB, Hochachka PW. Glycolytic enzymes in muscle of the Pacific dolphin: Role of pyruvate kinase in aerobic‐anaerobic transition during diving. Comp Biochem Physiol 49B: 119‐128, 1974.
 312. Tanji DG, Weste J, Dykes RW. Interactions of respiration and the bradycardia of submersion in harbor seals. Can J Physiol Pharmacol 53: 555‐559, 1975.
 313. Taylor WF, Chen S, Barshtein G, Hyde DE, Yedgar S. Enhanced aggregability of human red blood cells by diving. Undersea Hyperb Med 25: 167‐170, 1998.
 314. Tenney SM, Boggs DF. Comparative mammalian respiratory control. In: Fishman AP, editor. Handbook of Physiology: The Respiratory System II, Section 3. Bethesda, MA: American Physiological Society, 1986, p. 833‐855.
 315. Testa JW, Kovacs K, Francis J, York A, Hindell M. Analysis of Data from Time‐Depth Recorders and Satellite‐Linked Time‐Depth Recorders: Report of a Technical Workshop. Document # ADA327488. http://handle.dtic.mil/100.2/ADA327488. 1993, Fairbanks: University of Alaska Fairbanks, p. 31.
 316. Thorson PH, Le Boeuf BJ. Developmental aspects of diving in northern elephant seal pups. In: Le Boeuf BJ, Laws RM, editors. Elephant Seals: Population Ecology, Behavior, and Physiology. Berkeley: University of California Press, 1994, p. 271‐289.
 317. Tomkiewicz SM, Fuller MR, Kie JG, Bates KK. Global positioning system and associated technologies in animal behaviour and ecological research. Philos Trans R Soc Lond B Biol Sci 365: 2163‐2176, 2010.
 318. Trillmich F. The behavioral ecology of maternal effort in fur seals and sea lions. Behaviour 114: 3‐20, 1990.
 319. Trumble SJ, Noren SR, Cornick LA, Hawke TJ, Kanatous SB. Age‐related differences in skeletal muscle lipid profiles of Weddell seals: Clues to developmental changes. J Exp Biol 213: 1676‐1684, 2010.
 320. Valladares BK, Lemberg L. Use of the “diving reflex” in paroxysmal atrial tachycardia. Heart Lung 12: 202‐205, 1983.
 321. Van Citters RL, Franklin DL, Smith OA, Watson NW, Elsner RW. Cardiovascular adaptations to diving in the northern elephant seal Mirounga angustirostris. Comp Biochem Physiol 16: 267‐276, 1965.
 322. Vazquez‐Medina JP, Olguin‐Monroy NO, Maldonado PD, Santamaria A, Konigsberg M, Elsner R, Hammill MO, Burns JM, Zenteno‐Savin T. Maturation increases superoxide radical production without increasing oxidative damage in the skeletal muscle of hooded seals (Cystophora cristata). Can J Zool 89: 206‐212, 2011.
 323. Vazquez‐Medina JP, Zenteno‐Savin T, Elsner R. Antioxidant enzymes in ringed seal tissues: Potential protection against dive‐associated ischemia/reperfusion. Comp Biochem Physiol C 142: 198‐204, 2006.
 324. Vazquez‐Medina JP, Zenteno‐Savin T, Elsner R. Glutathione protection against dive‐associated ischemia/reperfusion in ringed seal tissues. J Exp Mar Biol Ecol 345: 110‐118, 2007.
 325. Vazquez‐Medina JP, Zenteno‐Savin T, Forman HJ, Crocker DE, Ortiz RM. Sleep‐ and diving‐associated apneas do not induce oxidative damage in northern elephant seals. Free Radic Biol Med 49: S30‐S31, 2010.
 326. Viamonte M, Morgane PJ, Galliano RE, Nagel EL, McFarland WL. Angiography in the living dolphin and observations on blood supply to the brain. Am J Physiol 214: 1225‐1249, 1968.
 327. Watkins WA, Daher MA, Fristrup KM, Howald TJ, Di Sciara GN. Sperm whales tagged with transponders and tracked underwater by sonar. Mar Mamm Sci 9: 55‐67, 1993.
 328. Watson RR, Kanatous SB, Cowan DF, Wen JW, Han VC, Davis RW. Volume density and distribution of mitochondria in harbor seal (Phoca vitulina) skeletal muscle. J Comp Physiol B 177: 89‐98, 2007.
 329. White FN, Ikeda M, Elsner RW. Adrenergic innervation of large arteries in the seal. Comp Gen Physiol 4: 271‐276, 1973.
 330. Wiig Ø, Gjertz I, Griffiths D, Lydersen C. Diving patterns of an Atlantic walrus, Odobenus rosmarus rosmarus,near Svalbard. Pol Biol 13: 71‐72, 1993.
 331. Williams CL, Ponganis PJ. Muscle oxygen depletion in diving emperor penguins. J Physiol Sci 59: 115‐115, 2009.
 332. Williams CL, Meir JU, Ponganis PJ. What triggers the aerobic dive limit? Patterns of muscle oxygen depletion during dives of emperor penguins. J Exp Biol 214: 1802‐1812, 2011.
 333. Williams EE, Stewart BS, Beuchat CA, Somero GN, Hazel JR. Hydrostatic‐pressure and temperature effects on the molecular order of erythrocyte membranes from deep‐, shallow‐, and non‐diving mammals. Can J Zool 79: 888‐894, 2001.
 334. Williams R, Noren DP. Swimming speed, respiration rate, and estimated cost of transport in adult killer whales. Mar Mamm Sci 25: 327‐350, 2009.
 335. Williams TM, Haun JE, Friedl WA. 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, 1999.
 336. Zapol WM, Liggins GC, Schneider RC, Qvist J, Snider MT, Creasy RK, Hochachka PW. Regional blood flow during simulated diving in the conscious Weddell seal. J Appl Physiol 47: 968‐973, 1979.
 337. Zapol WM. Diving adaptations of the Weddell seal. Sci Am 256: 100‐107, 1987.
 338. Zapol WM, Hill RD, Qvist J, Falke K, Schneider RC, Liggins GC, Hochachka PW. Arterial gas tensions and hemoglobin concentrations of the freely diving Weddell seal. Undersea Biomed Res 16: 363‐373, 1989.
 339. Zenteno‐Savin T, Clayton‐Hernandez E, Elsner R. Diving seals: Are they a model for coping with oxidative stress? Comp Biochem Physiol C 133: 527‐536, 2002.
 340. Zenteno‐Savin T, Leger JS, Ponganis PJ. Hypoxemic and ischemic tolerance in emperor penguins. Comp Biochem Physiol C 152: 18‐23, 2010.

Related Articles:

Cardiovascular Adjustments to Diving in Mammals and Birds
Comparative Mammalian Respiratory Control
Diving Mammals
Diving physiology of the Weddell seal

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite

Michael Castellini. Life Under Water: Physiological Adaptations to Diving and Living at Sea. Compr Physiol 2012, 2: 1889-1919. doi: 10.1002/cphy.c110013