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Coping with Thermal Challenges: Physiological Adaptations to Environmental Temperatures

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Abstract

Temperature profoundly influences physiological responses in animals, primarily due to the effects on biochemical reaction rates. Since physiological responses are often exemplified by their rate dependency (e.g., rate of blood flow, rate of metabolism, rate of heat production, and rate of ion pumping), the study of temperature adaptations has a long history in comparative and evolutionary physiology. Animals may either defend a fairly constant temperature by recruiting biochemical mechanisms of heat production and utilizing physiological responses geared toward modifying heat loss and heat gain from the environment, or utilize biochemical modifications to allow for physiological adjustments to temperature. Biochemical adaptations to temperature involve alterations in protein structure that compromise the effects of increased temperatures on improving catalytic enzyme function with the detrimental influences of higher temperature on protein stability. Temperature has acted to shape the responses of animal proteins in manners that generally preserve turnover rates at animals' normal, or optimal, body temperatures. Physiological responses to cold and warmth differ depending on whether animals maintain elevated body temperatures (endothermic) or exhibit minimal internal heat production (ectothermic). In both cases, however, these mechanisms involve regulated neural and hormonal over heat flow to the body or heat flow within the body. Examples of biochemical responses to temperature in endotherms involve metabolic uncoupling mechanisms that decrease metabolic efficiency with the outcome of producing heat, whereas ectothermic adaptations to temperature are best exemplified by the numerous mechanisms that allow for the tolerance or avoidance of ice crystal formation at temperatures below 0°C. © 2012 American Physiological Society. Compr Physiol 2:2151‐2202, 2012.

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Figure 1. Figure 1.

Thermal image depicting an ectotherm (South American rattlesnake, Crotalus durissus) and an endotherm (mouse, Mus musculus). The ambient temperature is 30°C.

Images courtesy G.J. Tattersall.
Figure 2. Figure 2.

Schematic representation of the Maxwell‐Boltzmann distribution () for the kinetic energy of molecules, and the effect of temperature on the number of molecules (gray shading) that exceed low and high activation energies (Ea).

Figure 3. Figure 3.

Influence of temperature on Q10 values for processes of different activation energies, ranging from 2.5 kJ·mol−1(diffusion) to 100 kJ·mol−1. Hatched area represents “typical” Q10 values (between 2 and 3, usually with Ea ∼50‐75 kJ·mol−1) for enzymes at physiological body temperatures.

Figure 4. Figure 4.

Schematic representation of a species performance curve () for a thermal generalist (dark curve), showing the critical thermal minimum CTmin), optimal performance temperature (Topt), critical thermal maximum (CTmax) and the performance breadth, and performance curves for low‐temperature and high‐temperature specialists (light curves).

Figure 5. Figure 5.

Critical maximum (CTmax) and critical minimum (CTmin) temperatures from stingrays acclimated to a range of temperatures (Adapted, with permission, from reference ).

Figure 6. Figure 6.

Effect of temperature on the binding of acetylcholine to acetylecholine esterases of several marine fishes. Shaded area indicates the relatively preserved Km value for the species at their respective habitat temperature. (Adapted, with permission, from reference ).

Figure 7. Figure 7.

Pattern of change with Ta for body temperature, metabolic rate, evaporative water loss, and wet (solid symbols) and dry (open symbols) thermal conductance for a typical endotherm, a small marsupial, the dibbler Parantechinus apicalis (modified, with permission, from reference ).

Figure 8. Figure 8.

Effect of insulation thickness on thermal conductance of still air, feathers, fur, and fat. Modified, with permission, from references and .

Figure 9. Figure 9.

Schematic representation of the difference between an endotherm thermoconforming to keep the thermal differential (ΔT) constant at elevated Ta compared to thermoregulating at a constant Ta. Examples of birds (see reference ) thermoconforming (starling) and thermoregulating (Monk parakeet) are also shown.

Figure 10. Figure 10.

(A) Antelope ground squirrel (Ammospermophilus leucurus) dissipating heat in the shade (photo C.E. Cooper). (B) Red kangaroo (Macropus rufa) licking its forearms for evaporative heat dissipation (photo A. Lothian). (C) Facial view of eland showing engorged nasal veins returning blood to the angularis oculi and facial veins (photo A. Fuller).

Figure 11. Figure 11.

Toco toucan (A) (live image) utilizes the underlying vasculature within its bill (B) (live image) as a thermal window to lose heat (C) (thermal image).

Photos courtesy of G.J. Tattersall.
Figure 12. Figure 12.

Body (arterial blood and brain) temperatures of four free‐ranging Southern oryx measured every 5 minutes for 3 months. The top panel (A) shows the mean ± SD, with the lines denoting maximum and minimum, brain temperature at each 0.1°C category of arterial blood temperature measured in the carotid artery. The lower panel (B) shows the frequency of occurrence of each arterial blood temperature category. The diagonal line in the top panel is the line of identity; points above the line indicate the brain was hotter than the blood, points below the line denote selective brain cooling.

Figure 13. Figure 13.

Body temperature profile of an insect undergoing freezing, demonstrating the minimum supercooling point (−26°C) where ice nucleation occurs, the heat released (shaded area) from the latent fusion of water, and the background cooling rate (2.5°C·h−1). (Unpublished Data, G.J. Tattersall.)

Figure 14. Figure 14.

Thermal hysteresis (°C difference between melting and freezing temperatures) as a function of antifreeze protein concentration (A) for synthetic Type I AFP and variants with Ala residues replaced with Leu. (B) The morphology of the ice crystals for four of the different variants. Adapted, with permission, from reference .

Figure 15. Figure 15.

Behavioral thermoregulation in ectotherms, demonstrated by basking. (A) Trachemys scripta with outstretched limbs (inset diagram is a thermal image showing two individuals of the same species). (B) Caiman latirostris exposed to full sun reaches temperatures well above ambient temperature (inset diagram is a thermal image showing two individuals of the same species).

Images courtesy of G.J. Tattersall.
Figure 16. Figure 16.

Representative schematic of the asymmetry in heating and cooling rates (thermal hysteresis) in many reptiles (A) manifests from a differential distribution of blood flow to the periphery during heating compared to cooling, resulting in a hysteresis in the heart rate (B) response to changes in body temperature.

Figure 17. Figure 17.

Temperature‐related skin reflectance changes in the Brazilian frog (Bokermannohyla alvarengai) at 20 (A) and 30°C (B) Corresponding changes in skin reflectance are shown in (C) (data adapted, with permission, from reference ).

Figure 18. Figure 18.

Thermal images demonstrating extensive evaporative heat loss in an amphibian (A) (Bokermannohyla alvarengai) and evaporative cooling localized to the mouth during gaping in the bearded dragon (B) (Pogona vitticeps).

Images courtesy of G.J. Tattersall.
Figure 19. Figure 19.

Bill size in birds demonstrates a strong dependency on habitat temperature, with small bills observed in cold climates, and large bills in warmer climates (data derived, with permission, from reference ).



Figure 1.

Thermal image depicting an ectotherm (South American rattlesnake, Crotalus durissus) and an endotherm (mouse, Mus musculus). The ambient temperature is 30°C.

Images courtesy G.J. Tattersall.


Figure 2.

Schematic representation of the Maxwell‐Boltzmann distribution () for the kinetic energy of molecules, and the effect of temperature on the number of molecules (gray shading) that exceed low and high activation energies (Ea).



Figure 3.

Influence of temperature on Q10 values for processes of different activation energies, ranging from 2.5 kJ·mol−1(diffusion) to 100 kJ·mol−1. Hatched area represents “typical” Q10 values (between 2 and 3, usually with Ea ∼50‐75 kJ·mol−1) for enzymes at physiological body temperatures.



Figure 4.

Schematic representation of a species performance curve () for a thermal generalist (dark curve), showing the critical thermal minimum CTmin), optimal performance temperature (Topt), critical thermal maximum (CTmax) and the performance breadth, and performance curves for low‐temperature and high‐temperature specialists (light curves).



Figure 5.

Critical maximum (CTmax) and critical minimum (CTmin) temperatures from stingrays acclimated to a range of temperatures (Adapted, with permission, from reference ).



Figure 6.

Effect of temperature on the binding of acetylcholine to acetylecholine esterases of several marine fishes. Shaded area indicates the relatively preserved Km value for the species at their respective habitat temperature. (Adapted, with permission, from reference ).



Figure 7.

Pattern of change with Ta for body temperature, metabolic rate, evaporative water loss, and wet (solid symbols) and dry (open symbols) thermal conductance for a typical endotherm, a small marsupial, the dibbler Parantechinus apicalis (modified, with permission, from reference ).



Figure 8.

Effect of insulation thickness on thermal conductance of still air, feathers, fur, and fat. Modified, with permission, from references and .



Figure 9.

Schematic representation of the difference between an endotherm thermoconforming to keep the thermal differential (ΔT) constant at elevated Ta compared to thermoregulating at a constant Ta. Examples of birds (see reference ) thermoconforming (starling) and thermoregulating (Monk parakeet) are also shown.



Figure 10.

(A) Antelope ground squirrel (Ammospermophilus leucurus) dissipating heat in the shade (photo C.E. Cooper). (B) Red kangaroo (Macropus rufa) licking its forearms for evaporative heat dissipation (photo A. Lothian). (C) Facial view of eland showing engorged nasal veins returning blood to the angularis oculi and facial veins (photo A. Fuller).



Figure 11.

Toco toucan (A) (live image) utilizes the underlying vasculature within its bill (B) (live image) as a thermal window to lose heat (C) (thermal image).

Photos courtesy of G.J. Tattersall.


Figure 12.

Body (arterial blood and brain) temperatures of four free‐ranging Southern oryx measured every 5 minutes for 3 months. The top panel (A) shows the mean ± SD, with the lines denoting maximum and minimum, brain temperature at each 0.1°C category of arterial blood temperature measured in the carotid artery. The lower panel (B) shows the frequency of occurrence of each arterial blood temperature category. The diagonal line in the top panel is the line of identity; points above the line indicate the brain was hotter than the blood, points below the line denote selective brain cooling.



Figure 13.

Body temperature profile of an insect undergoing freezing, demonstrating the minimum supercooling point (−26°C) where ice nucleation occurs, the heat released (shaded area) from the latent fusion of water, and the background cooling rate (2.5°C·h−1). (Unpublished Data, G.J. Tattersall.)



Figure 14.

Thermal hysteresis (°C difference between melting and freezing temperatures) as a function of antifreeze protein concentration (A) for synthetic Type I AFP and variants with Ala residues replaced with Leu. (B) The morphology of the ice crystals for four of the different variants. Adapted, with permission, from reference .



Figure 15.

Behavioral thermoregulation in ectotherms, demonstrated by basking. (A) Trachemys scripta with outstretched limbs (inset diagram is a thermal image showing two individuals of the same species). (B) Caiman latirostris exposed to full sun reaches temperatures well above ambient temperature (inset diagram is a thermal image showing two individuals of the same species).

Images courtesy of G.J. Tattersall.


Figure 16.

Representative schematic of the asymmetry in heating and cooling rates (thermal hysteresis) in many reptiles (A) manifests from a differential distribution of blood flow to the periphery during heating compared to cooling, resulting in a hysteresis in the heart rate (B) response to changes in body temperature.



Figure 17.

Temperature‐related skin reflectance changes in the Brazilian frog (Bokermannohyla alvarengai) at 20 (A) and 30°C (B) Corresponding changes in skin reflectance are shown in (C) (data adapted, with permission, from reference ).



Figure 18.

Thermal images demonstrating extensive evaporative heat loss in an amphibian (A) (Bokermannohyla alvarengai) and evaporative cooling localized to the mouth during gaping in the bearded dragon (B) (Pogona vitticeps).

Images courtesy of G.J. Tattersall.


Figure 19.

Bill size in birds demonstrates a strong dependency on habitat temperature, with small bills observed in cold climates, and large bills in warmer climates (data derived, with permission, from reference ).

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Further Reading
 1.Angilletta MJ. Thermal Adaptation: A Theoretical and Empirical Synthesis. Oxford, UK: Oxford University Press, 2009.
 2.Bennett AF, Johnston IA. Animals and Temperature: Phenotypic and Evolutionary Adaptation. Cambridge [England]; New York: Cambridge University Press, 1996.
 3.Blumberg MS. Body Heat: Temperature and Life on Earth. Cambridge, MA: Harvard University Press, 2002.
 4.Davenport J. Animal Life at Low Temperature. London; New York: Chapman & Hall, 1992.
 5.Jessen C. Temperature Regulation in Humans and Other Mammals. Berlin: Springer, 2001.

Further Reading

Angilletta MJ. Thermal Adaptation: A Theoretical and Empirical Synthesis. Oxford, UK: Oxford University Press, 2009.

Bennett AF and Johnston IA. Animals and Temperature: Phenotypic and Evolutionary Adaptation. Cambridge [England]; New York: Cambridge University Press, 1996.

Blumberg MS. Body Heat: Temperature and Life on Earth. Cambridge, MA: Harvard University Press, 2002.

Davenport J. Animal Life at Low Temperature. London ; New York: Chapman & Hall, 1992.

Jessen C. Temperature Regulation in Humans and Other Mammals. Berlin: Springer, 2001.

 


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Glenn J. Tattersall, Brent J. Sinclair, Philip C. Withers, Peter A. Fields, Frank Seebacher, Christine E. Cooper, Shane K. Maloney. Coping with Thermal Challenges: Physiological Adaptations to Environmental Temperatures. Compr Physiol 2012, 2: 2151-2202. doi: 10.1002/cphy.c110055