Comprehensive Physiology Wiley Online Library
For Librarians For Authors Editors About

Behavioral Thermoregulation in the Cold

Evelyn Satinoff

10.1002/cphy.cp040121

Source: Supplement 14: Handbook of Physiology, Environmental Physiology

Originally published: 1996

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 The Concept of Thermoneutrality
1.1 The Thermoneutral Zone
1.2 The Thermal Comfort Zone
2 Forced Movements
3 What Affects the Thermal Comfort Zone?
3.1 The Concept of Setpoint
3.2 Hypoxia
3.3 Fever
3.4 Circadian Rhythms
4 Examples of Behavioral Thermoregulation
4.1 Constructing a Microenvironment
4.2 Social Aggregation
4.3 Postural Changes
4.4 Preening
4.5 Alterations in Food Intake
5 Parental Thermoregulation for Offspring
6 Summary
Figure 1.

Control diagram for behavioral thermoregulation. The learned response (e.g., pressing a bar to turn on a heat lamp) occurs when there is a discrepancy (an error signal) between the ideal body temperature (setpoint) and the actual body temperature. The error arises from a disturbance. The actual body temperature is monitored and the feedback loops maintain the response at a level appropriate to the existing discrepancy. The lower feedback path carries information about actual body temperature that is compared with the set temperature at the comparator. The upper pathways adjust the parameters of the response mechanisms in terms of response cost and response effectiveness and optimize the effectiveness of the system. Low effectiveness or high response cost might be expected to lower the slope of the function relating error to response.
Figure 2.

Positions of 1‐day‐old rat pups in a thermal gradient at 10 min intervals for 120 min.

From ref. 126
Figure 3.

Thermal gradient response of Rana pipiens larvae. Each point represents the number of animals found at a given temperature during a succession of 10 min intervals. Note preference for warmer temperatures as the season progressed. Almost identical results were found in Rana catesbeiana larvae. From ref. 95
Figure 4.

Top: Effects of gradient PO2 on selected temperature (Ts). Values are means ± SEM. Numbers in parentheses = number of animals observed in determining Ts at each PO2. The filled circle represents Ts at a PO2 of 127 torr after N2 exposure. *: mean Ts is significantly different from mean Ts at PO2 of 127 torr (P < 0.05). **: mean Ts is significantly different from all other values (p < 0.01). Bottom: Effects of temperature on paramecia survival at 3 ambient PO2s. From ref. 100
Figure 5.

Closed circles: Esophageal temperature measured every 6 h for 24 h while the subjects were resting, showing the circadian cyclicity of body temperature. Open circles: Set temperature estimated from behavioral results. Subjects were asked to choose the most pleasurable temperature in a glove through which water was circulating. These results imply that set and body temperatures vary in the same direction in normal male subjects over 24 h. From ref. 26
Figure 6.

Operant responding and telemetered body temperature (Tb) of a normal rat. The rat was in either a cold or a hot environment. A single bar press rotated a valve so that the “drive” air was shunted away from the chamber and “reinforcement air” entered the chamber for 15 ss. Four sessions are shown. Sessions conducted when the rat's Tb was high are shown at the top. Those conducted when the rat's Tb was low are at the bottom. For cold‐escape sessions, ambient temperature (Ta) is indicated by solid lines and Tb by solid squares. For heat‐escape sessions, Ta is shown as dashed lines and Tb as open squares. Note that Tb at the end of the 90 min test is within 0.5°C of Tb at the beginning, except for the condition of escaping heat when Tb was low (in the morning), where the rat allowed its Tb to rise to nighttime levels.

From ref. 146
Figure 7.

Burrows of prairie voles showing simple (a), average (b), and complex (c) systems.

From ref. 46
Figure 8.

Nest‐building of adult male rat during 5 periods of ambient‐temperature changes. Breaks in baseline indicate transition from one period to the next. Ordinate: size of nest in strips of nesting material. Six hundred strips were offered every day.

From ref. 80
Figure 9.

Abandoned emperor penguin chicks usually huddle together for warmth while awaiting the presumed return of a parent.

From ref. 90
Figure 10.

Examples of close (A) and loose (B) aggregation responses of muskrats exposed to 5°C in the laboratory. There was no consistency between conformation pattern and air temperature, although there was a greater tendency for horizontal rather than vertical displacement at warmer temperatures.

From ref. 11
Figure 11.

Left: Four views of the flow of pups (6-10‐day‐old siblings) through a huddle. The arrows show the movements of individual pups, both downward into the clump and upward away from it, as they periodically appear and disappear in the huddle. Right: Time spent exposed by individual pups on the surface of the huddle during successive 7.5 min intervals of 2 h observations. The graphs depict the cyclic pattern of appearance and disappearance of pups on the huddle surface. (Pups in panels a and c were littermates. Their patterns of movement can be compared by superimposing those panels.)

From ref. 3
Figure 12.

Group of piglets in cool (top) and warm (bottom) conditions.

From ref. 106
Figure 13.

Mean percentages of body temperatures greater than the daily mean temperatures that occur in the light (open bar) and the dark (solid bar) period of a 12:12 light/dark cycle in 20-60‐day‐old rats in 5‐day blocks. N = 13 or 14 up to day 40 and 6-10 at older ages.

From ref. 81
Figure 14.

Characteristic heating posture often displayed when whiptail lizards were placed in a thermal gradient on the sand floor directly under a heat lamp. The lizard flattened its body on the substrate, arching its tail off the ground with only the tip touching. The palms were elevated perpendicular to the ground, the wrists were on the ground, and the hind feet were raised off the ground. This posture never lasted more than 4 min and stopped when the lizard was near its mean body temperature. Body temperature always rose when the lizard was in this posture.

From ref. 19
Figure 15.

Effect of changes in orientation to the sun on the radiant heat load. The model cows have been illuminated by a lamp set at an angle of 30° to represent the sun. The area of the shadow cast indicates the area of the body receiving radiation. The greater the area of shadow, the greater the surface that is directly illuminated (except, of course, when the sun, or lamp, is directly overhead).

From ref. 75
Figure 16.

Diagrammatic sectional view of the nests of two hummingbird species showing the differences in the quantity and arrangement of nest material. (a) Nest of the mountain species Selasphorus platycercus. (b) nest of the lowland species Amazilis violiceps.

From ref. 63, adapted from ref. 155


Figure 1.

Control diagram for behavioral thermoregulation. The learned response (e.g., pressing a bar to turn on a heat lamp) occurs when there is a discrepancy (an error signal) between the ideal body temperature (setpoint) and the actual body temperature. The error arises from a disturbance. The actual body temperature is monitored and the feedback loops maintain the response at a level appropriate to the existing discrepancy. The lower feedback path carries information about actual body temperature that is compared with the set temperature at the comparator. The upper pathways adjust the parameters of the response mechanisms in terms of response cost and response effectiveness and optimize the effectiveness of the system. Low effectiveness or high response cost might be expected to lower the slope of the function relating error to response.



Figure 2.

Positions of 1‐day‐old rat pups in a thermal gradient at 10 min intervals for 120 min.

From ref. 126


Figure 3.

Thermal gradient response of Rana pipiens larvae. Each point represents the number of animals found at a given temperature during a succession of 10 min intervals. Note preference for warmer temperatures as the season progressed. Almost identical results were found in Rana catesbeiana larvae. From ref. 95



Figure 4.

Top: Effects of gradient PO2 on selected temperature (Ts). Values are means ± SEM. Numbers in parentheses = number of animals observed in determining Ts at each PO2. The filled circle represents Ts at a PO2 of 127 torr after N2 exposure. *: mean Ts is significantly different from mean Ts at PO2 of 127 torr (P < 0.05). **: mean Ts is significantly different from all other values (p < 0.01). Bottom: Effects of temperature on paramecia survival at 3 ambient PO2s. From ref. 100



Figure 5.

Closed circles: Esophageal temperature measured every 6 h for 24 h while the subjects were resting, showing the circadian cyclicity of body temperature. Open circles: Set temperature estimated from behavioral results. Subjects were asked to choose the most pleasurable temperature in a glove through which water was circulating. These results imply that set and body temperatures vary in the same direction in normal male subjects over 24 h. From ref. 26



Figure 6.

Operant responding and telemetered body temperature (Tb) of a normal rat. The rat was in either a cold or a hot environment. A single bar press rotated a valve so that the “drive” air was shunted away from the chamber and “reinforcement air” entered the chamber for 15 ss. Four sessions are shown. Sessions conducted when the rat's Tb was high are shown at the top. Those conducted when the rat's Tb was low are at the bottom. For cold‐escape sessions, ambient temperature (Ta) is indicated by solid lines and Tb by solid squares. For heat‐escape sessions, Ta is shown as dashed lines and Tb as open squares. Note that Tb at the end of the 90 min test is within 0.5°C of Tb at the beginning, except for the condition of escaping heat when Tb was low (in the morning), where the rat allowed its Tb to rise to nighttime levels.

From ref. 146


Figure 7.

Burrows of prairie voles showing simple (a), average (b), and complex (c) systems.

From ref. 46


Figure 8.

Nest‐building of adult male rat during 5 periods of ambient‐temperature changes. Breaks in baseline indicate transition from one period to the next. Ordinate: size of nest in strips of nesting material. Six hundred strips were offered every day.

From ref. 80


Figure 9.

Abandoned emperor penguin chicks usually huddle together for warmth while awaiting the presumed return of a parent.

From ref. 90


Figure 10.

Examples of close (A) and loose (B) aggregation responses of muskrats exposed to 5°C in the laboratory. There was no consistency between conformation pattern and air temperature, although there was a greater tendency for horizontal rather than vertical displacement at warmer temperatures.

From ref. 11


Figure 11.

Left: Four views of the flow of pups (6-10‐day‐old siblings) through a huddle. The arrows show the movements of individual pups, both downward into the clump and upward away from it, as they periodically appear and disappear in the huddle. Right: Time spent exposed by individual pups on the surface of the huddle during successive 7.5 min intervals of 2 h observations. The graphs depict the cyclic pattern of appearance and disappearance of pups on the huddle surface. (Pups in panels a and c were littermates. Their patterns of movement can be compared by superimposing those panels.)

From ref. 3


Figure 12.

Group of piglets in cool (top) and warm (bottom) conditions.

From ref. 106


Figure 13.

Mean percentages of body temperatures greater than the daily mean temperatures that occur in the light (open bar) and the dark (solid bar) period of a 12:12 light/dark cycle in 20-60‐day‐old rats in 5‐day blocks. N = 13 or 14 up to day 40 and 6-10 at older ages.

From ref. 81


Figure 14.

Characteristic heating posture often displayed when whiptail lizards were placed in a thermal gradient on the sand floor directly under a heat lamp. The lizard flattened its body on the substrate, arching its tail off the ground with only the tip touching. The palms were elevated perpendicular to the ground, the wrists were on the ground, and the hind feet were raised off the ground. This posture never lasted more than 4 min and stopped when the lizard was near its mean body temperature. Body temperature always rose when the lizard was in this posture.

From ref. 19


Figure 15.

Effect of changes in orientation to the sun on the radiant heat load. The model cows have been illuminated by a lamp set at an angle of 30° to represent the sun. The area of the shadow cast indicates the area of the body receiving radiation. The greater the area of shadow, the greater the surface that is directly illuminated (except, of course, when the sun, or lamp, is directly overhead).

From ref. 75


Figure 16.

Diagrammatic sectional view of the nests of two hummingbird species showing the differences in the quantity and arrangement of nest material. (a) Nest of the mountain species Selasphorus platycercus. (b) nest of the lowland species Amazilis violiceps.

From ref. 63, adapted from ref. 155
References
 1. Adair, E. R., and B. A. Wright. Behavioral thermoregulation in the squirrel monkey when response effort is varied. J. Comp. Physiol. Psychol. 90: 179-184.
 2. Adler, J. The sensing of chemicals by bacteria. Sci. Amer. 234: 40-47, 1976.
 3. Alberts, J. R., Huddling by rat pups: Group behavioral mechanisms of temperature regulation and energy consumption. J. Comp. Physiol. Psychol. 92: 231-235, 1978.
 4. Alberts, J. R., and P. C. Brunjes. Ontogeny of thermal and olfactory determinants of huddling in the rat. J. Comp. Physiol. Psychol. 92: 897-906, 1978.
 5. Ankney, C. D., and C. D. MacInnes. Nutrient reserves and reproductive performance of female lesser snow geese. Auk 95: 459-471, 1978.
 6. Baldwin, B. A., and D. L. Ingram. The effects of food intake and acclimatization to temperature on behavioral thermoregulation in pigs and mice. Physiol. Behav. 3: 395-400, 1968.
 7. Baldwin, B. A., and D. L. Ingram. Factors influencing behavioral thermoregulation in the pig. Physiol. Behav. 3: 400-415, 1968.
 8. Baldwin, B. A., and G. B. Meese. Sensory reinforcement and illumination preference in the domesticated pig. Anim. Behav. 25: 497-507, 1977.
 9. Barber, B. J., and E. C. Crawford, Jr, Dual threshold control of peripheral temperature in the lizard Dipsosaurus dorsalis. Physiol. Zool. 52: 250-263, 1979.
 10. Bartholomew, G. A field study of the temperature relations in the Galápagos marine iguanas. Copeia, 241-250, 1966.
 11. Bazin, R. C., and R. A. MacArthur. Thermal benefits of huddling in the muskrat (Ondatra zibethicus). J Mamm. 73: 559-564, 1992.
 12. Benzinger, T. H., Peripheral cold reception and central warm reception, sensory mechanisms of behavioral and autonomic homeostasis. In: Physiological and Behavioral Temperature Regulation, edited by J. D. Hardy, A. P. Gagge, and J. A. J. Stolwijk. Springfield, IL: C. C. Thomas, 1970, p. 831-855.
 13. Berk, M. L., and J. E. Heath. Effects of preoptic, hypothalamic and telencephalic lesions on thermoregulation in the lizard Dipsosaurus dorsalis. J. Therm. Biol. 1: 65-78, 1976.
 14. Bernheim, H. A., and M. J. Kluger. Fever: effect of drug‐induced antipyresis on survival. Science 193: 237-239, 1976.
 15. Beutow, K. C., and S. W. Klein. Effect of maintenance of “normal” skin temperature on survival of infants of low birth weight. Pediatrics 34: 163-170, 1964.
 16. Biere, J. M., and G. W. Uetz. Web orientation in the spider Micrathena gracilis (Araneae: Araneidae). Ecology 62: 336-344, 1967.
 17. Bignall, K. E., F. W. Heggeness, and J. E. Palmer. Effects of acute starvation on cold‐induced thermogenesis in the preweanling rat. Am. J. Physiol. 227: 1088-1093, 1974.
 18. Boorstein, S. M., and P. W. Ewald. Costs and benefits of behavioral fever in Melanoplus sanguinipes infected by Nosema acri‐dophagus. Physiol. Zool. 60: 586-595, 1987.
 19. Bowker, R. G., and O. W. Johnson. Thermoregulatory precision in three species of whiptail lizards (Lacertilia: Teiidae). Physiol. Zool. 53: 176-185, 1980.
 20. Brauer, R. W., E. D. Johnson, C. G. Miller, M. I. Sanchez‐Griana, M. G. Shelton, and E. E. Williams. Modification of temperature preference behavior by hypoxia and metabolic inhibitors. In: Homeostasis and Thermal Stress. Sixth International Symposium on Pharmacology of Thermoregulation, edited by K. E. Cooper, P. Lomax, E. Schönbaum, and W. L. Veale. Basel: Karger, 1986, p. 27-29.
 21. Briese, E., Rats prefer ambient temperatures out of phase with their body temperature circadian rhythm. Br. Res. 345: 389-393, 1985.
 22. Briese, E., Circadian body temperature rhythm and behavior of rats in thermoclines. Physiol. Behav. 37: 839-847, 1986.
 23. Brooke, O. G., M. Harris, and C. B. Salvosa. The response of malnourished babies to cold. J. Physiol. (Lond.), 223: 75-91, 1973.
 24. Butler, C. G., The World of the Honey Bee (2nd ed.). London: Collins, 1962.
 25. Cabanac, M., and B. Drolet. Absence of fever in planarian: Turbellaria: Phogocata gracilis. Comp. Biochem. Physiol. 98A: 417-420, 1991.
 26. Cabanac, M., G. Hildebrandt, B. Massonet, and H. Strempel. A study of the nycthemeral cycle of behavioural temperature regulation in man. J. Physiol. 257: 275-291, 1976.
 27. Cabanac, M. and L. Le Guelte. Temperature regulation and prostaglandin E1 fever in scorpions. J. Physiol. 303: 365-370, 1980.
 28. Canals, M., M. Rosenmann, and F. Bozinovic. Energetics and geometry of huddling in small mammals. J. Theor. Biol. 141: 181-189, 1089.
 29. Carlisle, H. J., Thermal reinforcement and temperature regulation. In: Animal Psychophysics: The Design and Conduct of Sensory Experiments, edited by W. C. Stebbins. Englewood Cliffs, NJ: Prentice‐Hall, 1970, p. 211-229.
 30. Carmichael, L. E., F. D. Barnes, and D. H. Percy. Temperature as a factor in resistance of young puppies. J. Infec. Dis. 120: 669-678, 1969.
 31. Chappell, M. A., Thermal limitations to escape responses in desert grasshoppers. Anim. Behav. 31: 1088-1093, 1983.
 32. Cloudsley‐Thompson, J. L., Terrestrial invertebrates. In: Comparative Physiology of Thermoregulation, vol. I. Invertebrates and Nonmammalian Vertebrates, edited by G. C. Whittow. New York: Academic Press, 1970, p. 15-77.
 33. Cogger, H. G., and A. Holmes. Thermoregulatory behaviour in a specimen of Morelia spilotes variegata Gray (Serpentaes: Boidae). Proc. Linnean Soc. New South Wales 85: 328-333, 1960.
 34. Collier, G. H., Body weight loss as a measure of motivation in hunger and thirst. Ann. N.Y. Acad. Sci. 157: 594-609, 1969.
 35. Collier, G. H., D. F. Johnson, J. Naveira, and K. A. Cybulski. Ambient temperature and food costs: effects on behavior patterns in rats. Am. J. Physiol. 257 (Regulatory Integrative Comp. Physiol. 26): R1328-R1334, 1989.
 36. Covert, J. B., and W. W. Reynolds. Survival value of fever in fish. Nature 267: 43-45, 1977.
 37. Cowgell, J., and H. Underwood. Behavioral thermoregulation in lizards: a circadian rhythm. J. Exp. Zool. 210: 189-194, 1979.
 38. Cowles, R. B., and C. M. Bogert. A preliminary study of the thermal requirements of desert reptiles. Bull. Amer. Museum Nat. Hist. 83: 265-296, 1944.
 39. Crawshaw, L. I., and H. T. Hammel. Behavioral thermoregulation in two species of antarctic fish. Life Sci. 10: 1009-1020, 1971.
 40. Crawshaw, L. I., and Stitt, J. T., Behavioural and autonomic induction of prostaglandin E1 fever in squirrel monkeys. J. Physiol. 244: 197-206, 1975.
 41. Curtis, S. E., Perception of thermal comfort by farm animals. In: Farm Animal Housing and Welfare, edited by S. H. Baxter, M. R. Baxter, and J. A. D. MacCormack. Boston: Martinus Nijhoff, 1983, p. 59-66.
 42. Dahl, J. F., and E. O. Smith. Assessing variation in the social behavior of stumptail macaques using thermal criteria. Am. J. Phys. Anthropol. 68: 467-477, 1985.
 43. Davenport, J., Cold resistance in Gammarus duebeni Liljeborg. Astarte 12: 21-26, 1979.
 44. Davenport, J., Environmental Stress and Behavioural Adaptation, London: Croom Helm, 1985.
 45. Davis, W. H., Hibernation: ecology and physiological ecology. In: Biology of Bats, vol. 1, edited by W. A. Wimsatt. New York: Academic Press, 1970, p. 265-300.
 46. Davis, W. H., and P. J. Kalisz. Burrow systems of the prairie vole, Microtus ochrogaster, in central Kentucky. J. Mamm. 73: 582-585, 1992.
 47. Dawson, W. R., and J. W. Hudson. Birds, In: Comparative Physiology of Thermoregulation, vol. 1, Invertebrates and Nonmammalian Vertebrates, edited by G. C. Whittow. New York: Academic Press, 1970, p. 223-310.
 48. De Witt, C. B., Behavioral thermoregulation in the desert iguana. Science 158: 809-810, 1967.
 49. Dupré, R. K., and T. L. Owen. Behavioral thermoregulation by hypoxic rats. J. Exp. Zool. 262: 230-235, 1992.
 50. Dupré, R. K., and S. C. Wood. Behavioral temperature regulation by aquatic ectotherms during hypoxia. Can. J. Zool. 66: 2649-2652, 1988.
 51. Esch, H., F. Goller, and B. Heinrich. How do bees shiver? Naturwissenschaften 78: 325-328, 1991.
 52. Fantino, M., and M. Cabanac. Effect of a cold ambient temperature on the rat's food hoarding behavior. Physiol. Behav. 32: 183-190, 1984.
 53. Fraenkel, G. S., and D. L. Gunn. The Orientation of Animals: Kineses, Taxes and Compass Reactions. New York: Dover, 1961. (Originally published in 1940.)
 54. Furuuchi, S., and Y. Shimizu. Effect of ambient temperature on multiplication of attenuated transmissible gastroenteritis virus in the bodies of newborn piglets. Infec. Immun. 13: 990-992, 1976.
 55. Gatten, R. E., Jr, Effect of nutritional status on the preferred body temperature of the turtles Pseudemys scripta and Terrapene ornata. Copeia 1974: 912-917, 1974.
 56. Gordon, C. J., Twenty‐four‐hour rhythms of selected ambient temperature in rat and hamster. Physiol. Behav. 53: 257-263, 1993.
 57. Gordon, C. J., and L. Fogelson. Comparative effects of hypoxia on behavioral thermoregulation in rats, hamsters, and mice. Am. J. Physiol. 260 (Regulatory Integrative Comp. Physiol. 29): R120-R125, 1991.
 58. Guenaire, C., J. C. Costa, and J. Delacour. Conditionnement opérant avec renforcement thermique chez le rat nouveauné. Physiol. Behav. 29: 419-424, 1982.
 59. Gundlach, H., Brutfürsorge, Brutpflege, Verhaltensontegenese und Tagesperiodik beim Europäischen Wildschwein (Sus scrofa L.). Zeit. Tierpsychol. 25: 955-995, 1967.
 60. Hamilton, C. L., Effect of food deprivation on thermal behavior of the rat. Proc. Soc. Exp. Biol. Med. 100: 354-356, 1959.
 61. Hamilton, C. L., Interactions of food intake and temperature regulation in the rat. J. Comp. Physiol. Psychol. 56: 476-488, 1963.
 62. Hammerson, G. A., Thermal ecology of the striped racer, Masticophis lateralis. Herpetologica 35: 267-273, 1979.
 63. Hansell, M. H., Animal Architecture and Building Behaviour. London: Longman, 1984.
 64. Hayward, J. S., Microclimate temperature and its adaptive significance in six geographic races of Peromyscus. Canad. J. Zool. 43: 341-350, 1965.
 65. Heath, J. E., Temperature fluctuation in the turkey vulture. Condor 64: 234-235, 1962.
 66. Heath, J. E., Temperature‐independent morning emergence in lizards of the genus Phrynosoma. Science 138: 891-892, 1962.
 67. Heath, J. E., Behavioral regulation of body temperature in poikilotherms. Physiologist 13: 399-410, 1970.
 68. Heim, T. and Z. Szelényi. Temperature regulation in rats semistarved since birth. Acta Physiol. Acad. Sci. Hung. 27: 247-255, 1965.
 69. Henderson, S., M. M. Fort, M. E. Rashotte, and R. P. Henderson. Ingestive behavior and body temperature of pigeons during long‐term cold exposure. Physiol. Behav. 52: 455-469, 1992.
 70. Hensel, H., and M. Banet. Adaptive changes in cats after long‐term exposure to various temperatures. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 52: 1008-1012, 1982.
 71. Hensel, H., K. Brück, and P. Raths. Homeothermic organisms. In: Temperature and Life, edited by H. Precht, J. Christophersen, H. Hensel, and W. Larcher. New York: Springer‐Verlag, 1973, p. 505-732.
 72. Hicks, J. W., and S. C. Wood. Temperature regulation in lizards: the role of oxygen. Am. J. Physiol. 248 (Regulatory Integrative Comp. Physiol. 17): R595-R600, 1985.
 73. Hocking, B., and C. D. Sharplin. Flower basking by Arctic insects. Nature 206: 215, 1965.
 74. Huey, R. B., and M. Slatkin. Costs and benefits of lizard thermoregulation. Quart. Rev. Biol. 51: 363-384, 1976.
 75. Ingram, D. L., and L. E. Mount. Man and Animals in Hot Environments. New York: Springer‐Verlag, 1975.
 76. IUPS Thermal Commission. Glossary of terms for thermal physiology, 2nd ed. Pflugers Arch. 410: 567-587, 1987.
 77. Jans, J. E., and M. Leon. Determinants of mother‐young contact in Norway rats. Physiol. Behav. 30: 919-935, 1982.
 78. Jouventin, P., Mortality parameters in emperor penguins Aptenodytes. In: The Biology of Penguins, edited by B. Stonehouse. London: MacMillan, 1975, p. 435-446.
 79. Kavaliers, M., Opioid systems, behavioral thermoregulation and shell polymorphism in the land snail Cepaea nemoralis. J. Comp. Physiol. B. 162: 172-178, 1992.
 80. Kinder, E. F., A study of the nest‐building activity of the albino rat. J. Exp. Zool. 47: 117-161, 1927.
 81. Kittrell, E. M. W., and E. Satinoff. Development of the circadian rhythm of body temperature in rats. Physiol. Behav. 38: 99-104, 1986.
 82. Kittrell, E. M. W., and E. Satinoff. Diurnal rhythms of body temperature, drinking and activity over reproductive cycles. Physiol. Behav. 42: 477-484, 1988.
 83. Kivivuori, L., and K. Y. H. Lagerspetz. Temperature selection behaviour of the isopod Saduria entomon (L.). J. Therm. Biol. 15: 83-86, 1990.
 84. Kleitman, N., and E. Satinoff. Behavioral responses to pyrogen in cold‐stressed and starved newborn rabbits. Am. J. Physiol. 241 (Regulatory Integrative Comp. Physiol. 10) R167-R171, 1981.
 85. Kleitman, N., and E. Satinoff. Thermoregulatory behavior in rat pups from birth to weaning. Physiol. Behav. 29: 537-541, 1982.
 86. Kluger, M., Fever: role of pyrogens and cryogens. Physiol. Rev. 71: 1-35, 1991.
 87. Kluger, M. J., D. H. Ringler, and M. R. Anver. Fever and survival. Science 188: 166-168, 1975.
 88. Kluger, M. J., R. S. Tarr, and J. E. Heath. Posterior hypothalamic lesions and disturbances in behavioral thermoregulation. Physiol. Zool. 46: 79-84, 1973.
 89. Kraly, F. S., and Blass, E. M., Increased feeding in rats in a low temperature. In: Hunger: Basic Mechanisms and Clinical Implications, edited by D. Novin, W. Wyrwicka, and G. Bray. New York: Raven Press, 1976, p. 77-87.
 90. Le Maho, E. Y., The emperor penguin: a strategy to live and breed in the cold. Am. Sci. 65: 680-693, 1977.
 91. Leonard, C. M., Thermotaxis in golden hamster pups. J. Comp. Physiol. Psychol. 86: 458-469, 1974.
 92. Lillywhite, H. B., P. Licht, and P. Chelgren. The role of behavioral thermoregulation in the growth energetics of the toad Bufo boreas. Ecology 54: 375-383, 1973.
 93. Loeb, J., Forced Movements, Tropisms, and Animal Conduct. New York: Dover, 1973. (Originally published in 1918.)
 94. Louis, C., M. Jourdan, and M. Cabanac. Behavioral fever and therapy in a rickettsia‐infected Orthoptera. Am. J. Physiol. 250 (Regulatory Integrative Comp. Physiol. 19) R991-R995, 1986.
 95. Lucas, E. A., and W. A. Reynolds. Temperature selection by amphibian larvae. Physiol. Zool. 40: 159-171, 1967.
 96. Lynch, C. B., Environmental modification of nest‐building in the white‐footed mouse, Peromyscus leucopus. Anim. Behav. 22: 405-409, 1974.
 97. Macari, M., D. L. Ingram, and M. J. Dauncey. Influence of thermal and nutritional acclimation on body temperatures and metabolic rate. Comp. Biochem. Physiol. 74A: 549-553, 1983.
 98. MacArthur, R. A., Daily and seasonal activity patterns of the muskrat Ondatra zibethicus as revealed by radiotelemetry. Holarctic Ecol. 3: 1-9, 1980.
 99. MacMillen, R. E., and C. H. Trost. Nocturnal hypothermia in the inca dove, Scardafella inca. Comp. Biochem. Physiol. 23: 243-253, 1967.
 100. Malvin, G. M., and S. C. Wood. Behavioral hypothermia and survival of hypoxic protozoans Paramecium caudatum. Science 255: 1423-1425, 1992.
 101. Marquez, P. R., R. L. Spencer, T. F. Burks, and J. N. McDougal. Behavioral thermoregulation, core temperature, and motor activity: Simultaneous quantitative assessment in rats after dopamine and prostaglandin E1. Behav. Neurosci. 98: 858-867, 1984.
 102. Marx, J., R. Hilbig, and H. Rahmann. Endotoxin and prostaglandin E1 fail to induce fever in a teleost fish. Comp. Biochem. Physiol. 77A: 483-487, 1984.
 103. McFarland, D. J., editor Oxford Companion to Animal Behavior. London: Oxford University Press, 1982.
 104. Midgley, M., Beast and Man: The Roots of Human Nature. Brighton, UK: Harvester Press, 1979.
 105. Mitchell, D., H. P. Laburn, M. Matter, and E. McClain. Fever in Namib and other ectotherms. In: Namib Ecology: 25 Years of Namib Research, edited by M. K. Seely. Transvaal Museum Monograph #7. Pretoria, South Africa: Transvaal Museum, 1990, p. 179-192.
 106. Mount, L. E., The Climatic Physiology of the Pig. London: Edward Arnold, 1968.
 107. Mount, L. E., The concept of thermal neutrality. In: Heat Loss From Animals and Man, edited by J. L. Monteith and L. E. Mount. London: Butterworths, 1974, p. 425-439.
 108. Mower, G. D., Perceived intensity of peripheral thermal stimuli is independent of internal body temperature. J. Comp. Physiol. Psychol. 90: 1152-1155, 1976.
 109. Mrosovsky, N., Rheostasis. New York: Oxford University Press, 1990.
 110. Mullens, D. P., and V. H. Hutchinson. Diel, seasonal, postprandial and food‐deprived thermoregulatory behaviour in tropical toads (Bufo marinus). J. Therm. Biol. 17: 63-67, 1992.
 111. Mumm, B., R. Kaul, and I. Schmidt. Endogenous circadian core temperature rhythm in artifically reared week‐old Wistar rats. In: Chronobiology and Chronomedicine, edited by E. Morgan. Frankfurt, FRG: Land, 1990, p. 92-101.
 112. Murray, M. D., Marine Insects, edited by L. Cheng. Amsterdam: North‐Holland, 1976, p. 79-96.
 113. Myhre, K., and H. T. Hammel. Behavioral thermoregulation of internal temperature in the lizard Teliqua scincoides. Am. J. Physiol. 217: 1490-1495, 1969.
 114. Myres, B. C., and H. M. Eells. Thermal aggregation in Boa constrictor. Herpetologica 24: 61-66, 1968.
 115. Nuesslein, B., and I. Schmidt. Development of circadian cycle of core temperature in juvenile rats. Am. J. Physiol. 259 (Regulatory Integrative Comp. Physiol. 28) R270-R276, 1990.
 116. Redlin, U., B. Nuesslein, and I. Schmidt. Circadian changes of brown adipose tissue thermogenesis in juvenile rats. Am. J. Physiol. 262 (Regulatory Integrative Comp. Physiol. 31) R504-R508, 1992.
 117. Refinetti, R., and M. Menaker. The circadian rhythm of body temperature. Physiol. Behav. 51: 613-637, 1992.
 118. Regal, P. J., Thermophilic response following feeding in certain reptiles. Copeia 3: 588-590, 1966.
 119. Regal, P. J., Voluntary hypothermia in reptiles. Science 155: 1551-1553, 1967.
 120. Reynolds, W. W., M. E. Casterlin, J. K. Matthey, S. T. Millington, and A. C. Ostrowski. Diel patterns of preferred temperature and locomotor activity in the goldfish Carassius auratus. Comp. Biochem. Physiol. 59A: 225-227, 1978.
 121. Richards, S. A., Temperature Regulation. London: Wykeham, 1973.
 122. Ritter, W., Experimenteller Beitrag zur Thermoregulation des Bienenvolks (Apis mellifera L.). Apidologie 13: 169-195, 1982.
 123. Ruttner, F., Biogeography and Taxonomy of Honeybees. Berlin: Springer‐Verlag, 1987.
 124. Saint Girons, H., Thermoregulation in reptiles with special reference to the tuatara and its ecophysiology. Tuatara 24: 59-80, 1980.
 125. Satinoff, E., Neural organization and evolution of thermal regulation in mammals. Science 201: 16-22, 1978.
 126. Satinoff, E., Developmental aspects of behavioral and reflexive thermoregulation. In: Developmental Psychobiology: New Methods and Changing Concepts, edited by H. N. Shair, G. A. Barr, and M. A. Hofer. New York: Oxford University Press, 1991, p. 169-188.
 127. Satinoff, E., Temperature effects on sleep. In: Encyclopedia of Sleep and Dreaming, edited by M. Carskadon. New York: Macmillan, 1993, p. 113-114.
 128. Satinoff, E., G. N. McEwen, and B. A. Williams. Behavioral fever in newborn rabbits. Science 193: 1139-1140, 1976.
 129. Schmidt, I., R. Kaul, and G. Heldmaier. Thermoregulation and diurnal rhythms in 1‐week‐old rat pups. Canad. J. Physiol. Pharmacol. 65: 1355-1364, 1986.
 130. Schmidt, I., B. Markewicz, and B. Nuesslein. Endogenous circadian rhythm of metabolic rate in periodically cold‐exposed week‐old rat pups. J. Interdiscip. Cycle Res. 21: 241-243, 1990.
 131. Seelye, T. D., Honeybee Ecology: A Study of Adaptation in Social Life. Princeton, NJ: Princeton University Press, 1985.
 132. Sherry, D. F., N. Mrosovksy, and J. A. Hogan. Weight loss and anorexia during incubation in birds. J. Comp. Physiol. Psychol. 94: 89-98, 1980.
 133. Silverman, W. A., The physical environment and the premature infant. Paediatrics 23: 166-171, 1959.
 134. Southwick, E. E., Bee hair structure and effect of hair on metabolism at cool temperature. J. Apicult. Res. 24: 144-149, 1985.
 135. Southwick, E. E., The colony as a thermoregulating superorganism. In: The Behaviour and Physiology of Bees, edited by L. J. Goodman and R. C. Fisher. Oxon, UK: CAB International, 1991, p. 28-47.
 136. Southwick, E. E., Overwintering in honeybees: Implications for apiculture. In: Insects at Low Temperature, edited by R. E. Lee, Jr., and D. L. Denlinger. London: Chapman and Hall, 1991, p. 446-459.
 137. Spiers, D. E., Nocturnal shifts in thermal and metabolic responses of the immature rat. J. Appl. Physiol., 64: 2119-2124, 1988.
 138. Stanier, M. W., Effect of body weight, ambient temperature and huddling on oxygen consumption and body temperature of young mice. Comp. Biochem. Physiol. 51A: 79-82, 1975.
 139. Steen, J., Food intake and oxygen consumption in pigeons at low temperatures. Acta Physiol. Scand. 39: 22-26, 1957.
 140. Stelzner, J. K., and G. Hausfater. Posture, microclimate, and thermoregulation in yellow baboons. Primates 27: 449-463, 1986.
 141. Stone, E. A., K. A. Bonnet, and M. A. Hofer. Survival and development of maternally deprived rats: Role of body temperature. Psychosom. Med. 38: 242-249, 1976.
 142. Stower, W. J., and J. F. Griffiths. The body temperature of the desert locust (Schistocerca gregaria). Entomol. Exp. Appl. 9: 127-178, 1966.
 143. Sugano, Y., and T. Nagasaka. Effect of huddling on heat losses in infant dogs. J. Physiol. Soc. (Japan) 41: 145-147, 1979.
 144. Swiergiel, A. H., Decrease in body temperature and locomotor activity as an adaptational response in piglets exposed to cold on restricted feeding. Physiol. Behav. 40: 117-125, 1987.
 145. Swiergiel, A. H., and D. L. Ingram. Effect of diet and temperature acclimation on thermoregulatory behaviour in piglets. Physiol. Behav. 36: 637-642, 1986.
 146. Szymusiak, R., A. DeMory, E. M. W. Kittrell, and E. Satinoff. Diurnal changes in thermoregulatory behavior in rats with medial preoptic lesions. Am. J. Physiol. (Regulatory Integrative Comp. Physiol. 18): R219-R227, 1985.
 147. Szymusiak, R., Satinoff, E., Schallert, T. and Whishaw, I., Brief skin temperature changes towards thermoneutrality trigger REM sleep in rats. Physiol. Behav., 25: 305-311, 1980.
 148. Taylor, R. C., Thermal preference and temporal distribution in three crayfish species. Comp. Biochem. Physiol. 77A: 513-517, 1984.
 149. Teisner, B., and S. Haahr. Poikilothermia and susceptibility of suckling mice to Coxsackie B1 virus. Nature 247: 568, 1974.
 150. Templeton, J. R. Reptiles, In: Comparative Physiology of Thermoregulation, vol. 1, edited by G. C. Whittow. New York: Academic Press, p. 167-221. 1970.
 151. Terai, Y., M. Asayama, T. Ogawa, J. Sugenoya, and T. Miyagawa. Circadian variation of preferred environmental temperature and body temperature. J. Therm. Biol. 10: 151-156, 1985.
 152. Trojan, P., and B. Wojciechowska. The effect of huddling on the resting metabolic rate of the European common vole Microtus arvallis (Pall). Bul. Polish Acad. Sci., Biol. Series 16: 107-109, 1968.
 153. Vaughn, L. K., H. A. Bernheim, and M. J. Kluger. Fever in the lizard Dipsosaurus dorsalis. Nature 252: 473-474.
 154. Vogt, F. D., and G. R. Lynch. Influence of ambient temperature, nest availability, huddling, and daily torpor on energy expenditure in the white‐footed mouse Peromyscus leucopus. Physiol. Zool. 55: 56-63, 1982.
 155. Wagner, H. O., Einfluss der poikilothermie bei kolibris auf ihre Brutbiologie. J. Ornithol. 96: 361-368, 1955.
 156. Walker, L. E., J. M. Walker, J. W. Palca, and R. J. Berger. A continuum of sleep and shallow torpor in fasting doves. Science 221: 194-195, 1983.
 157. Weiss, B., Thermal behavior of the subnourished and pantothenic‐acid‐deprived rat. J. Comp. Physiol. Psychol. 59: 481-485, 1957.
 158. Weitzman, E., M. Moline, C. Czeisler, and J. Zimmerman. Chronobiology of aging: Temperature, sleep‐wake rhythms and entrainment. Neurobiol. Aging 3: 299-309, 1982.
 159. West, S. D., and H. T. Dublin. Behavioral strategies of small mammals under winter conditions. In: Winter Ecology of Small Mammals, edited by J. F. Merritt. Special Publication of Carnegie Museum of Natural History 10: 293-299, 1984.
 160. Wever, R. A., The Circadian System of Man. New York: Springer‐Verlag, 1979.
 161. Williams, E. H., Thermal influences on oviposition in the montane butterfly Euphydryas gilletti. Oecologia 50: 342-346, 1981.

Contact Editor

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

* Required Field

Article Title: Behavioral Thermoregulation in the Cold
 

How to Cite

Evelyn Satinoff. Behavioral Thermoregulation in the Cold. Compr Physiol 2011, Supplement 14: Handbook of Physiology, Environmental Physiology: 481-505. First published in print 1996. doi: 10.1002/cphy.cp040121