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Comparative Mammalian Respiratory Control

S. M. Tenney, D. F. Boggs

10.1002/cphy.cp030227

Source: Supplement 11: Handbook of Physiology, The Respiratory System, Control of Breathing

Originally published: 1986

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Problems of Size
1.1 Metabolic Rate and Controller Gain
1.2 Scaling of Hemoglobin (Hb)‐O2 Affinity and Threshold of Hypoxic Ventilatory Response
1.3 Oscillations of Blood‐Borne Chemical Signals
1.4 Relative Influences of Various Arterial Chemoreceptors
2 Normal Variations of Body Temperature
2.1 Questions About Homeostasis
2.2 Panting and Nonpanting Responses
3 Activity Pattern
3.1 Exercise
3.2 Synchrony of Limb and Respiratory Movements
4 Mechanical Considerations: Optimization of Respiratory Frequency
5 Special Behavioral Features
5.1 Hibernation, Estivation, and Torpor
5.2 Sham Death
6 Variations of Habitat
6.1 High Altitude
6.2 Burrowing
6.3 Diving
6.4 Flying
6.5 Cave Dwelling
7 Unique Problems
7.1 Air Breathing With Very Immature Control Systems
7.2 Sluggish Motor Systems
7.3 Purring
8 Conclusion
Figure 1. Figure 1.

Comparison of mammalian and Poikilothermie blood pH values as function of body temperature. Upper shaded area represents region of constant pH‐pOH values in which all cold‐blooded vertebrate values fall; lower shaded area represents values characteristic of mammals.

From Reeves 143
Figure 2. Figure 2.

Relationship between ventilation () and O2 consumption (). A: during deep hibernation (○) and early arousal (•) in marmot.

Adapted from Malan et al. 110.] B: during entry into (○) and arousal from (•) torpor in pocket mouse. □, Mean euthermic and torpid values. BTPS, body temperature, ambient pressure, saturated with water vapor; STPD, standard temperature and pressure, dry; Tb body temperature. [Adapted from Withers 195
Figure 3. Figure 3.

Comparative ventilatory responses () to inspired CO2 for mole rat and white rat 11, hamster 30, human 20,38, dog 5, echidna 20,130, pocket gopher 38, and chipmunk 109.
Figure 4. Figure 4.

Ventilatory response to CO2 of some diving mammals. , minute ventilation; , alveolar partial pressure of CO2.

Adapted from refs. 15 (▪), 132 (Δ, □, •), and 149 (○, X)
Figure 5. Figure 5.

Arterial lactate concentrations during (solid line) and immediately after (dashed line) forced dives in beaver (•) 34 and harbor seal (Δ) 88 and immediately after free dives of various durations in Weddell seal (○) 94.


Figure 1.

Comparison of mammalian and Poikilothermie blood pH values as function of body temperature. Upper shaded area represents region of constant pH‐pOH values in which all cold‐blooded vertebrate values fall; lower shaded area represents values characteristic of mammals.

From Reeves 143


Figure 2.

Relationship between ventilation () and O2 consumption (). A: during deep hibernation (○) and early arousal (•) in marmot.

Adapted from Malan et al. 110.] B: during entry into (○) and arousal from (•) torpor in pocket mouse. □, Mean euthermic and torpid values. BTPS, body temperature, ambient pressure, saturated with water vapor; STPD, standard temperature and pressure, dry; Tb body temperature. [Adapted from Withers 195


Figure 3.

Comparative ventilatory responses () to inspired CO2 for mole rat and white rat 11, hamster 30, human 20,38, dog 5, echidna 20,130, pocket gopher 38, and chipmunk 109.



Figure 4.

Ventilatory response to CO2 of some diving mammals. , minute ventilation; , alveolar partial pressure of CO2.

Adapted from refs. 15 (▪), 132 (Δ, □, •), and 149 (○, X)


Figure 5.

Arterial lactate concentrations during (solid line) and immediately after (dashed line) forced dives in beaver (•) 34 and harbor seal (Δ) 88 and immediately after free dives of various durations in Weddell seal (○) 94.

References
 1. Adams, W. E. The Comparative Morphology of the Carotid Body and Carotid Sinus. Springfieid, IL: Thomas, 1958.
 2. Adolph, E. F. Quantitative relations in the physiological constituents of mammals. Science 109: 579‐585, 1949.
 3. Agostoni, E., and E. D'Angelo. Comparative features of the transpulmonary pressure. Respir. Physiol. 11: 76‐83, 1970‐71.
 4. Agostoni, E., F. F. Thimm, and W. O. Fenn. Comparative features of the mechanics of breathing. J. Appl. Physiol. 14: 679‐683, 1959.
 5. Albers, C. Der Mechanismus des Wärmehecheins beim Hund. III. Die CO2‐Empfindlichkeit des Atemzentrums während des Wärmehecheins. Pfluegers Arch. 274: 166‐183, 1961.
 6. Albers, C., W. Usinger, and C. Scholand. Intracellular pH in unanesthetized dogs during panting. Respir. Physiol. 23: 59‐70, 1975.
 7. Andrews, W. H. H., B. M. Deane, A. Howe, and J. Orbach. Abdominal chemoreceptors in the rat (Abstract). J. Physiol. London 222: 84P‐85P, 1972.
 8. Angell‐James, J. E., and M. de B. Daly. The interaction of reflexes elicited by stimulation of carotid body chemoreceptors and receptors in the nasal mucosa affecting respiration and pulse interval in the dog. J. Physiol. London 229: 133‐149, 1973.
 9. Ar, A., R. Arieli, and A. Shkolnik. Blood‐gas properties and function in the fossorial mole rat under normal and hypoxic‐hypercapnic atmospheric conditions. Respir. Physiol. 30: 201‐218, 1977.
 10. Arieli, R. The atmospheric environment of the fossorial mole rat (Spalax ehrenbergi): effects of season, soil texture, rain, temperature and activity. Comp. Biochem. Physiol. A 63: 569‐575, 1979.
 11. Arieli, R., and A. Ar. Ventilation of a fossorial mammal (Spalax ehrenbergi) in hypoxic and hypercapnic conditions. J. Appl. Physiol: Respirat. Environ. Exercise Physiol. 47: 1011‐1017, 1979.
 12. Arieli, R., A. Ar, and A. Shkolnik. Metabolic responses of a fossorial rodent (Spalax ehrenbergi) to simulated burrow conditions. Physiol Zool. 50: 61‐75, 1977.
 13. Asmussen, R. Exercise and the regulation of ventilation. Circ. Res. 20, Suppl. 1: 1132‐1145, 1967.
 14. Augee, M. L., R. W. Elsner, B. A. Gooden, and P. R. Wilson. Respiratory and cardiac responses of a burrowing animal, the echidna. Respir. Physiol. 11: 327‐334, 1971.
 15. Bainton, C. R., R. Elsner, and R. C. Matthews. Inhaled CO2 and progressive hypoxia: ventilatory response in a yearling and a newborn harbor seal. Life Sci. 12: 527‐533, 1973.
 16. Bartels, H., P. Hilpert, K. Barbey, K. Betke, K. Riegel, E. M. Lang, and J. Metcalfe. Respiratory functions of blood of the yak, llama, camel, Dybowski deer, and African elephant. Am. J. Physiol. 205: 331‐336, 1963.
 17. Baudinette, R. V. Physiological correlates of burrow gas conditions in the California ground squirrel. Comp. Biochem. Physiol. A 48: 733‐743, 1974.
 18. Bechbache, R. R., and J. Duffin. The entrainment of breathing frequency by exercise rhythm. J. Physiol. London 272: 553‐561, 1977.
 19. Bennett, F. M., and S. M. Tenney. Comparative mechanics of mammalian respiratory system. Respir. Physiol. 49: 131‐140, 1982.
 20. Bentley, P. J., C. F. Herreid II, and K. Schmidt‐Nielsen. Respiration of a monotreme, the echidna, Tachyglossus aculeatus. Am. J. Physiol. 212: 957‐961, 1967.
 21. Berger, M., O. Z. Roy, and J. S. Hart. The coordination between respiration and wing beats in birds. Z. Vgl. Physiol. 66: 190‐200, 1970.
 22. Biscoe, T. J. Carotid body: structure and function. Physiol. Rev. 51: 437‐495, 1971.
 23. Biscoe, T. J., and M. J. Purves. Observations on the rhythmic variation in the cat carotid body chemoreceptor activity which has the same period as respiration. J. Physiol. London 190: 389‐412, 1967.
 24. Black, A. M. S., and R. W. Torrance. Respiratory oscillations in chemoreceptor discharge in the control of breathing. Respir. Physiol. 13: 221‐237, 1971.
 25. Black, C. P., and S. M. Tenney. Oxygen transport during progressive hypoxia in high‐altitude and sea‐level waterfowl. Respir. Physiol 39: 217‐239, 1980.
 26. Bouverot, P., Rate of ventilatory acclimatization to altitude and strength of the O2‐chemoreflex drive. In: Respiratory Centres and Afferent Systems, edited by B. Duron. Amiens, France: INSERM, 1976, p. 213‐220.
 27. Bouverot, P., and M. Bureau. Ventilatory acclimatization and CSF acid‐base balance in carotid chemodenervated dogs at 3550 m. Pfluegers Arch. 361: 17‐23, 1975.
 28. Bouverot, P., V. Candas, and J. P. Libert. Role of the arterial chemoreceptors in ventilatory adaptation to hypoxia of awake dogs and rabbits. Respir. Physiol. 17: 209‐219, 1973.
 29. Brooks, J. G., III, and S. M. Tenney. Ventilatory response of llama to hypoxia at sea level and high altitude. Respir. Physiol 5: 269‐278, 1968.
 30. Chapin, J. L. Ventilatory response of the unrestrained and unanesthetized hamster to CO2. Am. J. Physiol. 179: 146‐148, 1954.
 31. Chapman, R. C., and A. F. Bennet. Physiological correlates of burrowing in rodents. Comp. Biochem. Physiol. A 51: 599‐603, 1975.
 32. Chapot, G. Action de la temperature et de Faco2 sur les décharges du nerf phrenique. Polypnée thermique. Pfluegers Arch. 296: 196‐201, 1967.
 33. Clausen, G., and A. Ersland. The respiratory properties of the blood of two diving rodents, the beaver and the water vole. Respir. Physiol. 5: 350‐359, 1968.
 34. Clausen, G., and A. Ersland. Blood O2 and acid‐base changes in the beaver during submersion. Respir. Physiol. 11: 104‐112, 1970.
 35. Cohen, M. I. Respiratory periodicity in the paralyzed, vagotomized cat: hypocapnic polypnea. Am. J. Physiol. 206: 845‐854, 1964.
 36. Crosfill, M. L., and J. G. Widdicombe. Physical characteristics of the chest and lungs and the work of breathing in different mammalian species. J. Physiol. London 158: 1‐14, 1961.
 37. Daly, M. de B., R. Elsner, and J. E. Angell‐James. Cardiorespiratory control by carotid chemoreceptors during experimental dives in the seal. Am. J. Physiol. 232 (Heart Circ. Physiol. 1): H508‐H516, 1977.
 38. Darden, T. R. Respiratory adaptations of a fossorial mammal, the pocket gopher (Thomomys bottae). J. Comp. Physiol. 78: 121‐137, 1972.
 39. Dawson, T. J., and R. W. Rose. Influence of the respiratory response to moderate and severe heat on the blood gas values of a macropodid marsupial. Comp. Biochem. Physiol. 37: 59‐66, 1970.
 40. Dejours, P. Control of respiration by arterial chemoreceptors. Ann. NY Acad. Sci. 109: 682‐695, 1963.
 41. Dejours, P. Comparison of gas transport by convection among animals. Respir. Physiol. 14: 96‐104, 1972.
 42. Eldridge, F. L. The importance of timing on the respiratory effects of intermittent carotid body chemoreceptor stimulation. J. Physiol. London 222: 319‐333, 1972.
 43. Elsner, R., Cardiovascular adjustments to diving. In: Biology of Marine Mammals, edited by H. T. Andersen. New York: Academic, 1968, p. 117‐145.
 44. Elsner, R., J. E. Angell‐James, and M. de B. Daly. Carotid body chemoreceptor reflexes and their interactions in the seal. Am. J. Physiol. 232 (Heart Circ. Physiol. 1): H517‐H525, 1977.
 45. Farber, J. P. Development of pulmonary reflexes and pattern of breathing in the Virginia opossum. Respir. Physiol. 14: 278‐286, 1972.
 46. Farber, J. P., H. N. Hultgren, and S. M. Tenney. Development of the chemical control of breathing in the Virginia opossum. Respir. Physiol. 14: 267‐277, 1972.
 47. Farber, J. P., and S. M. Tenney. The pouch gas of the Virginia opossum (Didelphis virginiana). Respir. Physiol. 11: 335‐345, 1971.
 48. Favier, R., and A. Lacaisse. Stimulus oxygène de la ventilation chez le rat eveillé (Eng. Abstract). J. Physiol. Paris 74: 411‐417, 1978.
 49. Gallivan, G. J. Hypoxia and hypercapnia in the respiratory control of the Amazonian manatee (Trichechus inunguis). Physiol. Zool. 53: 254‐261, 1980.
 50. Gallivan, G. J., and R. C. Best. Metabolism and respiration of the Amazonian manatee (Trichechus inunguis). Physiol. Zool. 53: 245‐253, 1980.
 51. Gibbs, E. L., and F. A. Gibbs. A purring center in the brain of the cat. J. Comp. Neurol. 64: 209‐211, 1936.
 52. Godfrey, S., and E. J. M. Campbell. The control of breath holding. Respir. Physiol. 5: 385‐400, 1968.
 53. Goffart, M. Function and Form in the Sloth. Oxford, UK: Pergamon, 1971.
 54. Goodrich, C. A. Acid‐base balance in euthermic and hibernating marmots. Am. J. Physiol. 224: 1185‐1189, 1973.
 55. Goodrich, C., and C. P. Lyman. Blood acid‐base balance in hibernating marmots (Abstract). Federation Proc. 30: 483, 1971.
 56. Grover, R. F., J. T. Reeves, D. H. Will, and S. G. Blount, Jr.. Pulmonary vasoconstriction in steers at high altitude. J. Appl. Physiol. 18: 567‐574, 1963.
 57. Günther, B., and B. L. De la Barra. Comparative physiometry of the mechanics of breathing in mammals. Respir. Physiol. 2: 129‐134, 1967.
 58. Guyton, A. C. Measurement of the respiratory volumes of laboratory animals. Am. J. Physiol. 150: 70‐77, 1947.
 59. Hales, J. R. S., J. Bligh, and M. Maskrey. Cerebrospinal fluid acid‐base balance during respiratory alkalosis in the panting animal. Am. J. Physiol. 219: 469‐473, 1970.
 60. Hales, J. R. S., and J. D. Findlay. Respiration of the ox: normal values and the effects of exposure to hot environments. Respir. Physiol. 4: 333‐352, 1968.
 61. Hales, J. R. S., J. D. Findlay, and R. M. Mabon. Tissue hypoxia in oxen exposed to severe heat. Respir. Physiol. 3: 43‐46, 1967.
 62. Hales, J. R. S., and M. E. D. Webster. Respiratory function during thermal tachypnoea in sheep. J. Physiol. London 190: 241‐260, 1967.
 63. Hall, F. G. Hemoglobin and oxygen: affinities in seven species of Sciuridae. Science 148: 1350‐1351, 1965.
 64. Hall, F. G., D. B. Dill, and E. S. G. Barron. Comparative physiology in high altitude. J. Cell Comp. Physiol. 8: 301‐313, 1936.
 65. Hayward, J. S. Abnormal concentrations of respiratory gases in rabbit burrows. J. Mammal. 47: 723‐724, 1966.
 66. Heisey, S. R., T. Adams, W. Hofman, and G. Riegle. Thermally induced respiratory responses of the unanesthetized goat. Respir. Physiol 11: 145‐151, 1971.
 67. Hill, A. V. Dimensions of animals and their muscular dynamics. Sci. Prog. 38: 209‐230, 1950.
 68. Hill, N., and S. M. Tenney. Ventilatory responses to CO2 and hypoxia in the two‐toed sloth (Choloepus hoffmanni). Respir. Physiol. 22: 311‐323, 1974.
 69. Hochachka, P. W. Brain, lung and heart functions during diving and recovery. Science 212: 509‐514, 1981.
 70. Hofer, M. A. Cardiac and respiratory function during sudden prolonged immobility in wild rodents. Psychosom. Med. 32: 633‐647, 1970.
 71. Hornbein, T. F., and J. W. Severinghaus. Carotid chemoreceptor response to hypoxia and acidosis in cats living at high altitude. J. Appl. Physiol. 27: 837‐839, 1969.
 72. Horvath, S. M., H. Chiodi, S. H. Ridgway, and S. Azar, Jr.. Respiratory and electrophoretic characteristics of hemoglobin of porpoises and sea lions. Comp. Biochem. Physiol. 24: 1027‐1033, 1968.
 73. Iampietro, P. F., V. Fiorica, E. A. Higgins, M. Mager, and R. F. Goldman. Exposure to heat: comparison of responses of dog and man. Int. J. Bioclimatol. Biometeorol. 10: 175‐185, 1966.
 74. Irving, L. Respiration of the beaver. J. Cell. Comp. Physiol. 9: 437‐451, 1937.
 75. Irving, L. The insensitivity of diving animals to CO2. Am. J. Physiol 124: 729‐734, 1938.
 76. Irving, L. Respiration in diving mammals. Physiol. Rev. 19: 112‐134, 1939.
 77. Irving, L., P. F. Scholander, and S. W. Grinnell. The respiration of the porpoise, Tursiops truncatus. J. Cell Comp. Physiol. 17: 145‐168, 1941.
 78. Irving, L., P. F. Scholander, and S. W. Grinnell. Experimental studies of the respiration of sloths. J. Cell Comp. Physiol. 20: 189‐210, 1942.
 79. Irving, L., O. M. Solandt, D. Y. Solandt, and K. C. Fisher. Respiratory characteristics of the blood of the seal. J. Cell. Comp. Physiol. 6: 393‐404, 1935.
 80. Jasinskas, C. L., B. A. Wilson, and J. Hoare. Entrainment of breathing rate to movement frequency during work at two intensities. Respir. Physiol. 42: 199‐209, 1980.
 81. Johansen, K., C. Lenfant, and G. C. Grigg. Respiratory properties of blood and responses to diving of the platypus, Ornithorhynchus anatinus (Shaw). Comp. Biochem. Physiol. 18: 597‐608, 1966.
 82. Johansen, K., G. Lykkeboe, R. E. Weber, and G. M. O. Maloiy. Blood respiratory properties in the naked mole rat Heterocephalus glaber, a mammal of low body temperature. Respir. Physiol. 28: 303‐314, 1976.
 83. Jurgens, K. D., H. Bartels, and R. Bartels. Blood oxygen transport and organ weights of small bats and small non‐flying mammals. Respir. Physiol. 45: 243‐260, 1981.
 84. Kappey, F., C. Albers, and R. Schmidt. Die ventilatorische CO2‐Reaktion des Hundes während der Wärmetachypnoea. Pfluegers Arch. 275: 312‐326, 1962.
 85. Kay, F. R. Influence of the Burrow Environment on Body Temperature, Oxygen Consumption and Water Loss in the Banner‐Tailed Kangaroo Rat, Dipodomys spectabilis. Las Cruces: New Mexico State Univ., 1974. Dissertation.
 86. Kennerly, T. E. Microenvironmental conditions of the pocket gopher burrow. Tex. J. Sci. 16: 395‐441, 1964.
 87. Kent, K. M., and E. C. Peirce II.. Acid‐base characteristics of hibernating animals. J. Appl. Physiol 23: 336‐340, 1967.
 88. Kerem, D., and R. Elsner. Cerebral tolerance to asphyxial hypoxia in the harbor seal. Respir. Physiol 19: 188‐200, 1973.
 89. King, C. E., E. A. Blair, and W. E. Garrey. The inspiratory augmentation of proprioceptive reflexes. Am. J. Physiol. 97: 329‐342, 1931.
 90. Kitts, W. D., M. C. Robertson, B. Stephenson, and I. McT. Cowan. The normal blood chemistry of the beaver (Castor canadensis). Am. J. Zool 36: 279‐283, 1958.
 91. Kleiber, M. The Fire of Life. An Introduction to Animal Energetics. New York: Wiley, 1961.
 92. Klemm, W. R. Neurophysiologic studies of the immobility reflex (“animal hypnosis”). Neurosci. Res. 4: 165‐212, 1971.
 93. Kooyman, G. L. Respiratory adaptations in marine mammals. Am. Zool 13: 457‐468, 1973.
 94. Kooyman, G. L., M. A. Castellini, and R. W. Davis. Physiology of diving in marine mammals. Annu. Rev. Physiol 43: 343‐356, 1981.
 95. Kooyman, G. L., D. H. Kerem, W. B. Campbell, and J. J. Wright. Pulmonary function in freely diving Weddell seals (Leptonychotes weddelli). Respir. Physiol. 12: 271‐282, 1971.
 96. Kooyman, G. L., and E. E. Sinnett. Mechanical properties of the harbor porpoise lung, Phocoena phocoena. Respir. Physiol. 36: 287‐300, 1979.
 97. Kristoffersson, R., and A. Sorvio. Hibernation in the hedgehog (Erinaceus europaeus L.). Changes of respiratory pattern, heart rate, and body temperature in response to gradually decreasing or increasing ambient temperature. Ann. Acad. Sci. Fenn. 82: 1‐17, 1964.
 98. Lahiri, S. Unattenuated ventilatory hypoxic drive in ovine and bovine species native to high altitude. J. Appl. Physiol. 32: 95‐102, 1972.
 99. Lahiri, S. Blood oxygen affinity and alveolar ventilation in relation to body weight in mammals. Am. J. Physiol. 229: 529‐536, 1975.
 100. Lechner, A. J. Respiratory adaptations in burrowing pocket gophers from sea level and high altitude. J. Appl. Physiol 41: 168‐173, 1976.
 101. Lechner, A. J. The scaling of maximal oxygen consumption and pulmonary dimensions in small mammals. Respir. Physiol. 34: 29‐44, 1978.
 102. Leivestad, H., D. Richardson, and P. G. Wright. The respiratory properties of the blood of the hippopotamus. Respir. Physiol. 19: 19‐25, 1973.
 103. Lenfant, C., Physiological properties of blood of marine mammals. In: Biology of Marine Mammals, edited by H. T. Andersen. New York: Academic, 1968, p. 95‐116.
 104. Lenfant C. R. Elsner, G. L. Kooyman, and C. M. Drabek. Respiratory function of blood of the adult and fetus Weddell seal Leptonychotes weddelli. Am. J. Physiol. 216: 1595‐1597, 1969.
 105. Lenfant, C., K. Johansen, and J. D. Torrance. Gas transport and oxygen storage capacity in some pinnipeds and the sea otter. Respir. Physiol. 9: 277‐286, 1970.
 106. Loring, S., P. Gulesian, M. Goldman, and J. Mead. Entrainment of respiratory frequency to stepping rate during walking (Abstract). Physiologist 19: 276, 1976.
 107. Lyman, C. P. Effect of increased CO2 on respiration and heart rate of hibernating hamsters and ground squirrels. Am. J. Physiol. 167: 638‐643, 1951.
 108. Lyman, C. P., and A. B. Hastings. Total CO2, plasma pH and pCO2 of hamsters and ground squirrels during hibernation. Am. J. Physiol. 167: 633‐637, 1951.
 109. Maclean, G. S. Respiratory physiology of a semifossorial mammal, Tamias striatus (Abstract). Physiologist 21: 75, 1978.
 110. Malan, A., H. Arens, and A. Waechter. Pulmonary respiration and acid‐base state in hibernating marmots and hamsters. Respir. Physiol. 17: 45‐61, 1973.
 111. Maréchal, G., M. Goffart, and Z. Aubert. Nouvelles recherches sur les propriétés du muscle squelletique de pares‐seux (Choelopus hoffmanni Peters). Arch. Int. Physiol. Biochim. 71: 236‐240, 1963.
 112. Maskrey, M., P. P. Hoppe, and O. S. Bamford. Blood gas changes during panting in a small East African antelope, the dik‐dik. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 44: 534‐537, 1978.
 113. McCormick, J. G. Relationship of sleep, respiration, and anesthesia in the porpoise: a preliminary report. Proc. Natl. Acad. Sci. USA 62: 697‐703, 1969.
 114. McMahon, T. Size and shape in biology. Science 179: 1201‐1204, 1973.
 115. McNab, B. K. The metabolism of fossorial rodents: a study in convergence. Ecology 47: 712‐733, 1966.
 116. Mead, J. Control of respiratory frequency. J. Appl. Physiol. 15: 325‐336, 1960.
 117. Mitchell, H. A. Ammonia tolerance of the California leaf‐nosed bat. J. Mammal. 44: 543‐551, 1963.
 118. Mithoefer, J. C., Breath holding. In: Handbook of Physiology. Respiration, edited by W. O. Fenn and H. Rahn. Washington, DC: Am. Physiol. Soc., 1965, sect. 3, vol. II, chapt. 38, p. 1011‐1025.
 119. Morgan, M. L., and T. Adams. Respiratory acid‐base balance in the unanesthetized cat during acute heat stress (Abstract). Physiologist 15: 221, 1972.
 120. Musacchia, X. J., and W. A. Volkert. Blood gases in hibernating and active ground squirrels: HbO2 affinity at 6 and 38 C. Am. J. Physiol. 221: 128‐130, 1971.
 121. Natsui, T. Respiratory response to hypoxia with hypocapnia or normocapnia and to CO2 in hypothermic dogs. Respir. Physiol. 7: 188‐202, 1969.
 122. Natsui, T. Threshold Pco2 as a chemical stimulus for ventilation during acute hypoxia in dogs. Pfluegers Arch. 339: 217‐224, 1973.
 123. norton, A. C., A. V. beran, and G. A. Misrahy. Electroencephalograph during “feigned” sleep in the opossum. Nature London 204: 162‐163, 1964.
 124. Orr, J. A., G. F. Bisgard, H. V. Forster, D. D. Buss, J. A. Dempsey, and J. A. Will. Cerebrospinal fluid alkalosis during high‐altitude sojourn in unanesthetized ponies. Respir. Physiol. 25: 23‐37, 1975.
 125. Oruç, T., and M. Terzioglu. The sensitivity to hypoxia of peripheral and central respiratory control mechanisms under normo‐ and hypothermic conditions. Bull. Eur. Physiopathol. Respir. 15: 1117‐1128, 1979.
 126. Otis, A. B., W. O. Fenn, and H. Rahn. Mechanics of breathing in man. J. Appl. Physiol. 2: 592‐607, 1950.
 127. Ou, L. C., and S. M. Tenney. Post‐prandial rise in alveolar CO2 and ventilatory response in cats. Respir. Physiol. 22: 263‐268, 1974.
 128. Ou, L. C., and S. M. Tenney. The role of brief hypocapnia in the ventilatory response to CO2 with hypoxia. Respir. Physiol. 28: 333‐346, 1976.
 129. Ozorio De Almeida, M. Sur la régulation chimique de la respiration chez le paresseux (Bradypus tridactylus). C. R. Soc. Biol. 98: 1576‐1578, 1928.
 130. Parer, J. T., and W. A. Hodson. Respiratory studies of monotremes. IV. Normal respiratory functions of echnidnas and ventilatory response to inspired oxygen and carbon dioxide. Respir. Physiol. 21: 307‐316, 1974.
 131. Parer, J. T., and J. Metcalfe. Respiratory studies of monotremes. II. Blood of the echidna (Tachyglossus setosus). Respir. Physiol. 3: 143‐150, 1967.
 132. Påsche, A. The effect of hypercapnia on respiratory characteristics and diving behavior of freely diving seals. Respir. Physiol. 26: 183‐194, 1976.
 133. Påsche, A. Hypoxia in freely diving hooded seal, Cystophora cristata. Comp. Biochem. Physiol. A 55: 319‐322, 1976.
 134. Pasquis, P., A. Lacaisse, and P. Dejours. Maximal oxygen uptake in four species of small mammals. Respir. Physiol. 9: 298‐309, 1970.
 135. Pembrey, M. S. Observations on respiration and temperature of the marmot. J. Physiol. London 27: 66‐84, 1901.
 136. Pleschka, K. The effect of temperature on phrenic nerve activity. Pfluegers Arch. 308: 357‐381, 1969.
 137. Pleschka, K. Interaction of CO2 and thermal stimuli in panting. J. Physiol. Paris 63: 383‐386, 1970.
 138. Pleschka, K., and W. Usinger. Cerebrospinal fluid pH, Pco2 and bicarbonate of the conscious dog, under exposure to high ambient temperature (Abstract). Experientia 25: 1266, 1969.
 139. Quilliam, T. A., J. A. Clarke, and A. J. Salsbury. The ecological significance of certain new haematological findings in the mole and hedgehog. Comp. Biochem. Physiol. A 40: 89‐102, 1971.
 140. Rahn, H., R. B. Reeves, and B. J. Howell. Hydrogen ion regulation, temperature and evolution. Am. Rev. Respir. Dis. 112: 165‐172, 1975.
 141. Raths, P., and E. Julzer. Physiology of hibernation and related lethargic states in mammals and birds. Bonn. Zool. Monogr. 9: 1976.
 142. Rayner, J. M. V., Flight adaptations in vertebrates. In: Vertebrate Locomotion, edited by M. H. Day. London: Academic, 1981, p. 137‐172. (Symp. Zool. Soc. London 48.).
 143. Reeves, R. B. Role of body temperature in determining the acid‐base state in vertebrates. Federation Proc. 28: 1204‐1208, 1969.
 144. Reeves, R. B. An imidazole alphastat hypothesis for vertebrate acid‐base regulation: tissue carbon dioxide content and body temperature in bullfrogs. Respir. Physiol. 14: 219‐236, 1972.
 145. Reeves, R. B., and W. A. Wimsatt. Blood pH and body temperature in the heterothermic mammal Myotis lucifugus (Abstract). Physiologist 9: 274, 1966.
 146. Remmers, J. E., and H. Gautier. Neural and mechanical mechanisms of feline purring. Respir. Physiol. 16: 351‐361, 1972.
 147. Richards, S. A. The biology and comparative physiology of thermal panting. Biol. Rev. 45: 223‐264, 1970.
 148. Ridgway, S. H., B. L. Scronce, and J. Kanwisher. Respiration and deep diving in the bottlenose porpoise. Science 166: 1651‐1654, 1969.
 149. Robin, E. D., H. V. Murdaugh, Jr., W. Pyron, E. Weiss, and P. Soteres. Adaptations to diving in the harbor seal—gas exchange and ventilatory response to CO2. Am. J. Physiol. 205: 1175‐1177, 1963.
 150. Robinson, S., Physiological adjustments to heat. In: The Physiology of Heat Regulation and the Science of Clothing, edited by L. H. Newburgh. Philadelphia, PA: Saunders, 1949, p. 193‐231.
 151. Ruiz, A. V. Carbon dioxide response curves during hypothermia. Pfluegers Arch. 358: 125‐133, 1975.
 152. Sant'Ambrogio, G., and F. Saibene. Contractile properties of the diaphragm in some mammals. Respir. Physiol. 10: 349‐357, 1970.
 153. Sapru, H. N., and A. J. Krieger. Carotid and aortic chemoreceptor function in the rat. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 42: 344‐348, 1977.
 154. Schaefer, V. H., and R. M. F. S. Sadleir. Concentrations of carbon dioxide and oxygen in mole tunnels. Acta Theriol. 24: 267‐276, 1979.
 155. Schmidt, C. F., and J. H. Comroe, Jr.. Functions of the carotid and aortic bodies. Physiol. Rev. 20: 115‐157, 1940.
 156. Schmidt‐Nielsen, K., E. C. Crawford, Jr., A. E. Newsome, K. S. Rawson, and H. T. Hammel. Metabolic rate of camels: effect of body temperature and dehydration. Am. J. Physiol. 212: 341‐346, 1967.
 157. Schmidt‐Nielsen, K., and J. L. Larimer. Oxygen dissociation curves of mammalian blood in relation to body size. Am. J. Physiol. 195: 424‐428, 1958.
 158. Schmidt‐Vanderheyden, W., L. Heinrich, and H. P. Koepchen. Investigations into the fluctuations of proprioceptive reflexes in man. I. Fluctuations of the patellar tendon reflex and their relation to the vegetative rhythms during spontaneous respiration. Pfluegers Arch. 317: 56‐71, 1970.
 159. Schoener, E. P., and H. M. Frankel. Effect of hyperthermia and Paco2 on the slowly adapting pulmonary stretch receptor. Am. J. Physiol. 222: 68‐72, 1972.
 160. Scholander, P. F. Experimental investigations on the respiratory function in diving mammals and birds. Hvalradets Skr. 22: 1‐120, 1940.
 161. Scholander, P. F., and L. Irving. Experimental investigations on respiration and diving of the Florida manatee. J. Cell. Comp. Physiol. 17: 169‐191, 1941.
 162. Severinghaus, J. W., C. R. Bainton, and A. Carcelen. Respiratory insensitivity to hypoxia in chronically hypoxic man. Respir. Physiol. 1: 308‐334, 1966.
 163. Snyder, G. K. Respiratory characteristics of whole blood and selected aspects of circulatory physiology in the common short‐nosed fruit bat, Cynopterus brachyotis. Respir. Physiol. 28: 239‐247, 1976.
 164. Soholt, L. F. Environmental conditions in an artificial burrow occupied by Merriam's kangaroo rat, Dipodomys merriami. J. Mammal. 55: 859‐864, 1974.
 165. Soholt, L. F., M. K. Yousef, and D. B. Dill. Responses of Merriam's kangaroo rats, Dipodomys merriami, to various levels of carbon dioxide concentration. Comp. Biochem. Physiol. A 45: 455‐462, 1973.
 166. Spells, K. E. Comparative studies in lung mechanics based on a survey of literature data. Respir. Physiol. 8: 37‐57, 1969‐70.
 167. Stahl, W. R. Scaling of respiratory variables in mammals. J. Appl. Physiol. 22: 453‐460, 1967.
 168. Struhsaker, T. T. Morphological factors regulating flight in bats. J. Mammal. 42: 152‐159, 1961.
 169. Studier, E. H. Studies in the mechanisms of ammonia tolerance of the guano bat. J. Exp. Zool. 163: 79‐85, 1966.
 170. Studier, E. H., L. R. Beck, and R. G. Lindeborg. Tolerance and initial metabolic response to ammonia intoxication in selected bats and rodents. J. Mammal. 48: 564‐572, 1967.
 171. Studier, E. H., and A. A. Fresquez. Carbon dioxide retention: a mechanism of ammonia tolerance in mammals. Ecology 50: 492‐494, 1969.
 172. Studier, E. H., and J. W. Procter. Respiratory gases in burrows of Spermophilus tridecemlineatus. J. Mammal 52: 631‐633, 1971.
 173. Suthers, R. A., S. P. Thomas, and B. S. Suthers. Respiration, wing‐beat and ultrasonic pulse emission in an echo locating bat. J. Exp. Biol. 56: 37‐48, 1972.
 174. Tähti, H. Effects of changes in CO2 and O2 concentrations in the inspired gas on respiration in the hibernating hedgehog (Erinaceus europaeus L.). Ann. Zool Fenn. 12: 183‐187, 1975.
 175. Tähti, H., and A. Soivio. Blood gas concentrations, acid‐base balance and blood pressure in hedgehogs in the active state and in hibernation with periodic respiration. Ann. Zool Fenn. 12: 188‐192, 1975.
 176. Tanner, J. M. Fallacy of per‐weight and per‐surface area standards, and their relation to spurious correlation. J. Appl. Physiol. 2: 1‐15, 1949.
 177. Taylor, C. R., G. M. O. Maloiy, E. R. Weibel, V. A. Langman, J. M. Z. Kamau, H. J. Seeherman, and N. C. Heglund. Design of the mammalian respiratory system. III. Scaling maximum aerobic capacity to body mass: wild and domestic animals. Respir. Physiol. 44: 25‐37, 1981.
 178. Taylor, C. R., D. Robertshaw, and R. Hofmann. Thermal panting: a comparison of wildebeest and zebu cattle. Am. J. Physiol. 217: 907‐910, 1969.
 179. Taylor, C. R., K. Schmidt‐Nielsen, and J. L. Raab. Scaling of energetic cost of running to body size in mammals. Am. J. Physiol. 219: 1104‐1107, 1970.
 180. Tenney, S. M. Some aspects of the comparative physiology of muscular exercise in mammals. Circ. Res. 20, Suppl. 1: 7‐14, 1967.
 181. Tenney, S. M., and D. Bartlett, Jr.. Comparative quantitative morphology of the mammalian lung: trachea. Respir. Physiol. 3: 130‐135, 1967.
 182. Tenney, S. M., and D. H. Morrison. Tissue gas tensions in small wild mammals. Respir. Physiol. 3: 160‐165, 1967.
 183. Tenney, S. M., and L. C. Ou. Hypoxic ventilatory response of cats at high altitude: an interpretation of “blunting.” Respir. Physiol. 30: 185‐199, 1977.
 184. Tenney, S. M., and J. E. Remmers. Comparative quantitative morphology of the mammalian lung: diffusing area. Nature London 197: 54‐56, 1963.
 185. Thomas, S. P. The physiology and energetics of bat flight. Proc. Int. Bat Res. Conf., 5th, Lubbock, Texas, 1980. Lubbuck: Texas Tech. Univ. Press, p. 393‐402.
 186. Thomas, S. P. Ventilation and oxygen extraction in the bat Pteropus gouldii during rest and steady flight. J. Exp. Biol 63: 1‐9, 1981.
 187. Thomas, S. P., and R. A. Suthers. The physiology and energetics of bat flight. J. Exp. Biol 57: 317‐335, 1972.
 188. Twente, J. A., and J. W. Twente. Concentrations of l‐lactate in the tissues of Citellus lateralis after known intervals of hibernating periods. J. Mammal 49: 541‐544, 1968.
 189. Van Nice, P., C. P. Black, and S. M. Tenney. A comparative study of ventilatory responses to hypoxia with reference to hemoglobin O2 affinity in llama, cat, rat, duck, and goose. Comp. Biochem. Physiol. A 66: 347‐350, 1980.
 190. Vaughan, T. A., The skeletal system. In: Biology of Bats, edited by W. A. Wimsatt. New York: Academic, 1970, vol. 1, p. 98‐138.
 191. Vaughan, T. A., The muscular system. In: Biology of Bats, edited by W. A. Wimsatt. New York: Academic, 1970, vol. 1, p. 140‐194.
 192. Vaughan, T. A., Flight patterns and aerodynamics. In: Biology of Bats, edited by W. A. Wimsatt New York: Academic, 1970, vol. 1, p. 195‐216.
 193. Wichser, J., and H. Kazemi. Ammonia and ventilation: site and mechanism of action. Respir. Physiol 20: 393‐406, 1974.
 194. Williams, D. D., and R. L. Rausch. Seasonal carbon dioxide and oxygen concentrations in the dens of hibernating mammals (Sciuridae). Comp. Biochem Physiol. A 44: 1227‐1235, 1973.
 195. Withers, P. C. Metabolic, respiratory and haematological adjustments of the little pocket mouse to circadian torpor cycles. Respir. Physiol 31: 295‐307, 1977.
 196. Withers, P. C. Acid base regulation as a function of body temperature in ectothermic toads, a heliothermic lizard, and a heterothermic mammal. J. Therm. Biol 3: 163‐171, 1978.

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Article Title: Comparative Mammalian Respiratory Control
 

How to Cite

S. M. Tenney, D. F. Boggs. Comparative Mammalian Respiratory Control. Compr Physiol 2011, Supplement 11: Handbook of Physiology, The Respiratory System, Control of Breathing: 833-855. First published in print 1986. doi: 10.1002/cphy.cp030227