Thermoregulation in Vertebrates: Acclimation, Acclimatization and Adaptation

John R Speakman, University of Aberdeen, Scotland, UK

Environments vary enormously in the thermal challenge they impose on the organisms that live in them. Some of these changes occur over very small temporal and spatial scales, and animals respond to these changes by acute modulations of their behaviour and physiology. More chronic changes in thermal environments, such as seasonal changes and latitudinal changes across the globe, require different responses. Three types of response have been recognized in both exothermic and endothermic vertebrates. These are termed acclimation, acclimatization and adaptive responses.

Introductory article
Article Contents
. Environmental Variation . Acclimatory Responses . Acclimatization Responses . Adaptative Responses

Environmental Variation
Environments vary tremendously in the thermal challenges that they pose to the organisms that inhabit them. Some of these changes can be extremely rapid and can occur over very short distances. For example, studies of temperature proles surrounding small bushes in hot deserts have shown that during the early part of the afternoon the ambient temperatures in the shadows of such bushes can be up to 208C lower than the ambient temperatures out on the open sand only 12 m away. Clearly, animals moving between these two microclimates must experience massive shifts in the thermal demands that are placed on them over very short timescales. Another example is the fact that every night the rotation of the earth deprives us of the heat input of the sun for a variable period during which thermal regimes are considerably dierent than during the day. Over these spatial and temporal scales animals respond to the thermal environment by acute modulations of their behaviour and physiology. These changes serve to sustain homeostasis of their internal body temperatures. The mechanisms include modulation of heat ow into and out of the animals by behavioural mechanisms (for example, shade seeking, burrowing, orientation behaviour and nest building), and in endothermic animals these behavioural changes are supplemented by the generation of heat internally by elevated rates of metabolism. Animals must not only face the challenges of altered thermal demands over very short temporal and spatial scales, but must also contend with modulations of their environment that occur over much more protracted periods and distances. In particular, two types of change in the environment are of critical importance. The rst is the seasonal change in temperature that occurs in all

habitats that exist more than 308 north or south of the equator. These changes tend to become more profound at greater latitudes and in terrestrial habitats that are farthest from the sea because they are less buered by the thermal inertia of the oceans. Although greater latitudes tend to have more divergent contrasts between summer and winter, they are also on average colder than the tropical regions. Hence, in addition to the seasonal dierences that all animals outside the tropics must contend with, there is also a spatial latitudinal eect on ambient temperature to which animals must respond. These dierences are apparent both in the oceans and in terrestrial habitats, but the extent of dierences in terrestrial habitats tends to be approximately an order of magnitude greater than in the marine habitat, again because of the thermal inertia of large water masses. The responses of animals to the thermal challenges of the environment over these much greater temporal and spatial scales cannot be the same as their acute responses. This is because acute responses over much longer durations would be unsustainable. Many endothermic animals, for example, would probably not be able to sustain elevated generation of internal heat in response to seasonal reductions in ambient temperature because the consequences of this response for their total daily energy, and hence food, demands would be impossible to meet by foraging eort. This might be particularly the case in winter, when for many species cold ambient temperatures coincide with periods of low environmental productivity and hence sparse food resources. Three dierent types of response have been recognized by researchers in this eld and they have been given dierent names to distinguish them. The rst type of response is the phenotypic modulation of behaviour and
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Thermoregulation in Vertebrates: Acclimation, Acclimatization and Adaptation

physiology that occurs when animals are exposed to changes in ambient temperature (or thermal stress) in a laboratory setting, with all other environmental changes controlled. These responses are called acclimatory responses or acclimation. Such responses can be contrasted to the phenotypic responses of animals in the wild to seasonal changes in their thermal environment. By denition these changes involve not only aspects of the thermal demands placed on the animals but also other changes in the environment. Two of the most important factors correlated to seasonal changes in thermal stress are changes in the daylength and changes in the levels of food availability. Phenotypic responses in the environment are called acclimatization responses. Both acclimation and acclimatization are characterized by the fact they occur within individuals and that the eects are generally reversible once the period of thermal stress is alleviated. These two responses can be contrasted with the dierences that are observed between populations of single species, or between dierent species that perpetually inhabit dierent regions of the globe that have dierent thermal characteristics. These dierences are generally genotypic in nature and are not lost when animals from dierent populations or species are brought into a neutral environment. These irreversible genotypic changes are adaptive responses. It is important to note that for a long time the use of these terms has been confused in the literature particularly prior to the 1990s. A case in point is the classic book on these responses by Hochachka and Somero published in 1973 called Strategies of biochemical adaptation, which in fact concentrates on acclimation and acclimatization. It is therefore incumbent on readers to establish the true nature of historical pieces of work as to whether they reect studies of acclimation, acclimatization or adaptation, independently of what the papers actually claim to be addressing.

Log (rate of reaction)

Cold-acclimated

Warm-acclimated

Temperature (a)

Cold-acclimated Log (rate of reaction)

Translation

Warm-acclimated

Temperature (b)

Cold-acclimated Log (rate of reaction)

Rotation

Warm-acclimated

Acclimatory Responses
Exotherms
During exposure to cold temperatures, and with deprivation of an external heat source, the body temperatures and metabolic rates of exothermic animals decline and they lose biological functionality. A familiar example of this is the eect of body temperature on the locomotory behaviour of exotherms. The maximal running speeds of reptiles, for example, and the maximal swimming speeds of sh are both strongly dependent on body temperature. During thermal acclimation, animals respond to the cold by compensating the activities of their physiological systems so that the temperature eect is ameliorated. If the absence of thermal acclimation is as illustrated by Figure 1a then there are two basic mechanisms by which animals may modulate their systems to acclimate to the temperature
2

Temperature (c)

Figure 1 Schematic diagrams illustrating (a) the lack of a compensatory response to thermal acclimation in an exothermic animal, (b) a translational compensation and (c) a rotational compensation.

change. The entire thermal response curve may be shifted, but retain its shape (Figure 1b), generally called a translational modication, or the shape of the response to temperature may be modied (Figure 1c), generally known as a rotational modication. A third possibility is to combine the rotational and translational eects (not illustrated). The scientic literature is replete with examples of changes in enzyme activities, whole-animal and tissue-level physiological responses, such as changes in oxygen consumption rate, and behavioural changes in exothermic animals that follow either the translational or

Thermoregulation in Vertebrates: Acclimation, Acclimatization and Adaptation

rotational patterns of response during acclimation. Two examples may serve to illustrate the general point. In the frog, the short-circuit current across the epithelium (which is a measure of the rate of sodium transport across the tissue) shows a translational compensation in animals that have been acclimated at dierent temperatures (Figure 2a). An example of a rotational change is the oxygen consumption of liver slices taken from cold-acclimated and warm-acclimated striped bass (Figure 2b). In this example, cold-acclimated animals have a negative relationship between oxygen consumption and temperature, compared with a positive relation in warm-acclimated
Acclimated at 6C 30 Short-circuit current (A cm2)

20

Acclimated at 12C

Acclimated at 23C 10

animals. The net result is that at their respective acclimation temperatures the rates of metabolism are very similar. These changes are mirrored by alterations in activities of the main enzymes involved in aerobic metabolism. It has been recognized that, to generate the commonly observed acclimatory changes in enzyme activities, exothermic animals may respond in three dierent ways. These three mechanisms may be combined to dierent extents in dierent species under varying acclimation regimes and with respect to dierent enzymes. Enzyme activities may be sustained in response to declines mediated by temperature changes by elevating the amount of enzyme present either by retarding its degradation or, more commonly, by elevating gene expression rates so that more of the enzyme is produced. This is normally called the quantitative response. An alternative mechanism is not to alter the amount of enzyme present but to modify the nature of the enzymes either by changing them from inactive to active forms (for example by phosphorylation), or by the synthesis of dierent isozymes that vary in their temperature sensitivity. A good example of these latter alterations is the responses to acclimation in the isozymes of trout acetylcholinesterase (Figure 3). Finally, the eects of temperature on enzyme function may in part be the result of the eects of temperature on the tertiary and quaternary structure of enzymes. To an extent, these changes can be resisted by altering in an opposing direction
Low-temperature acclimated individuals

10 Temperature (C) (a)

20

0.8

0.6
Rate of oxygen consumption of liver slices (mg O2 kg1h1) Warmacclimated

Km

2.0

0.4

1.5 Coldacclimated

Hightemperature acclimated individuals

1.0

0.2

0.5

10 20 Temperature (C)
5 15 Temperature (C) 25
Figure 3 Activity as a function of temperature of two isozymes of acetylcholinesterase from trout brains. The two forms of the enzyme have different sensitivities to temperature (minima in the Michaelis constant Km), with one form showing peak activity at 208C and the other peak activity at 28C. When fish were acclimated at high temperature they produced only the isoform active at high temperature; when acclimated at low temperature they produced only the isoform active at low temperature. At intermediate temperatures they produced a mix of both forms, allowing them to overcome the disruptive effects of temperature on substrate binding. Redrawn from original study by Baldwin J and Hochachka PW (1970) Journal of Biochemistry 116: 883 887.

(b)
Figure 2 Actual examples of (a) a translational response to thermal acclimation in an exotherm (short-circuit current across frog epithelium) and (b) a rotational change (oxygen consumption rates of liver slices from striped bass acclimated to cold and warm temperatures). Redrawn from Stone BB and Siddell BD (1981) Journal of Experimental Zoology 218: 371 379.

Thermoregulation in Vertebrates: Acclimation, Acclimatization and Adaptation

other aspects of the milieu in which the enzymes operate. The most common response in this respect is to modulate the pH buering of the enzyme environment. This response during acclimation has been termed the modulatory response. A major consequence of changes in body temperature due to changes in environmental temperatures is the physical nature of the body constituents. Most readers will be familiar with the fact that the physical nature of butter changes as its temperature is altered. Taken fresh from the refrigerator, butter can be extremely hard; at room temperature, it is much more uid; and at even higher temperatures, it becomes a clear liquid. Fats in the body behave in similar ways, with their uidity being critically dependent on the body temperature. Such alterations in membrane lipids may have a dramatic eect on membrane uidity and function. Although butter is still solid at room temperature, other fats, such as olive oil, are not. This dierence in physical state of fats at a given temperature depends on whether the fat molecules are saturated, as in butter, or unsaturated, as in olive oil. This is because saturated fat molecules are straight and therefore line up more readily to form a solid as they are cooled, whereas unsaturated molecules have kinks in their tails, which prevent them lining up so easily. During periods of low-temperature acclimation, exothermic animals shift the proportion of unsaturated fats in their membranes to avoid the problems of reductions in membrane uidity. This type of response has been called homeoviscous adaptation, reecting the fact it is a response designed to sustain membrane uid viscosity constant.

Endotherms
When endothermic animals are placed into the cold, their immediate responses are to conserve heat by vasoconstricting blood vessels in their peripheral tissues, allowing their surface temperatures to decline and retard heat loss. This cannot be a long-term strategy for coping with cold ambient temperatures, however, because the absence of blood ow in peripheral tissues would ultimately lead to oxygen decits and tissue necrosis (frostbite). As the period of exposure increases, therefore, animals respond by pumping blood into their peripheral tissues, and over a period of several days or weeks of cold exposure there are generally large increases observed in the degree of vascularization of such peripheral tissues. One example is in the ears of rabbits, where vascularization of the tissue increased almost 4-fold during a 2-week period of cold acclimation at 58C. This is a seemingly paradoxical response to cold exposure, when one might anticipate that the animals would be attempting to minimize heat loss, but in these experi-

mental acclimation treatments where the exposure could not be anticipated in advance by the animals the response serves to protect the extremities from tissue damage. Increased vascularization has the eect that heat loss via these extremities is increased and hence the total burden of energy demand on the animals increases. This has two immediate consequences. The animal must elevate its food intake to cover the increased energy demands and it must increase its ability to generate heat internally to supply the required heat to oset the increased losses. Changes in food intake are often also accompanied by hypertrophic and hyperplastic alterations in the alimentary tract that allow the animals to sustain digestive eciency at the elevated rates of food intake. Small mammals elevate their ability to generate heat mostly by changes in the levels of production of a specialized protein called uncoupling protein 1 (UCP-1), which is located exclusively in the mitochondria of brown adipose tissue. Another name for UCP-1 is thermogenin. UCP-1 decouples the movement of hydrogen ions across the inner mitochondrial membrane from the production of adenosine triphosphate (ATP) (oxidative phosphorylation), thus allowing the potential energy in the hydrogen ions to be released directly as heat. During acclimation in small mammals, the brown adipose tissue undergoes marked growth and an increase in the amount of UCP-1 on its mitochondria. This enables the animals to generate substantially more heat when placed under a thermal stress than they are capable of doing prior to cold exposure. In parallel with the changes in UCP-1, there are often also increases in lipoprotein lipase that allow for faster mobilization of lipids to fuel the increases in metabolic rate. Brown adipose tissue is supplied by a rich innervation from the autonomic nervous system. It is activated by noradrenaline (norepinephrine). Injections of noradrenaline into coldacclimated small mammals stimulate considerably more heat than the same injections into warm-acclimated animals, demonstrating the large contribution to their thermogenic capacity that is mediated via brown adipose tissue. It has been estimated that following cold acclimation brown adipose tissue may contribute up to 60% of the total thermoregulatory requirement. Overall, then, the cold-acclimated endotherm is morphologically and physiologically a substantially dierent animal from the control animal that remains in the warm. These dierences mean that, even after the cold-acclimated animal is returned to thermoneutral conditions, it still retains a much higher metabolic rate than its nonacclimated counterpart. This elevation has been interpreted as mostly a consequence of the energy costs of sustaining the increased masses of the very metabolically active tissues such as the alimentary tract, and in mammals the brown adipose tissue.

Thermoregulation in Vertebrates: Acclimation, Acclimatization and Adaptation

Acclimatization Responses
Exotherms
During winter, most terrestrial vertebrate exotherms that inhabit temperate regions enter states of torpor or quiescence and hence do not show patterns of thermal acclimatization to compensate the temperature changes in the same way as occurs during acclimation. For these animals, changes in their physiology mostly reect attempts to avoid their bodies freezing when they cool to very low temperatures. Nevertheless, some species, notably sh, do show patterns of change in their responses to temperature that are similar to the patterns observed during acclimation (i.e. translational and rotational changes in their thermal response curves). These changes appear to be mostly triggered by photoperiod, rather than in direct response to alterations in ambient temperature, although the numbers of studies is small relative to studies of acclimation.

Endotherms
The main dierences between acclimatization responses to seasonal changes in temperature in the wild and acclimatory responses in the laboratory are twofold. First, in the wild there is generally an option open to the animals that researchers do not allow in the laboratory: that is, the animals can simply run away from the problem in the wild by migrating. Indeed, global environmental thermoselection behaviour is a dominant feature of the lives of about 30% of the birds that inhabit temperate and arctic regions. Some birds routinely travel for several thousand miles to avoid the low ambient temperatures and poor food supplies that characterize the temperate and arctic winter. In terrestrial mammals, however, seasonal migration over such distances is far less common, but it is known, for example, in caribou and polar bears in northern Canada. The reasons why birds have a much greater proclivity to migrate relates principally to their dominant mode of locomotion ight. Flight allows birds to cross natural environmental barriers such as lakes, rivers and even the open ocean. Moreover it is rapid even small birds are able to sustain speeds of 1215 m s 2 1 for many hours on end and the costs of transport are relatively low (despite the absolute rates of energy demand during ight being quite high). By contrast, terrestrial locomotion is costly (on a joule per kilometre basis) and slow, and does not aord an easy method of avoiding environmental barriers. An alternative response that has evolved in mammals to cope with seasonal reductions in temperature and food supply is hibernation. This is eectively running away physiologically from the problem of sustaining heat balance, by relaxing endothermy. The second major dierence between seasonal acclimatization in the wild and thermal acclimation in the

laboratory is that generally, in the wild, animals have a whole range of cues but most critically alterations in photoperiod that alert them to the impending reduction in temperatures. This capability is closely linked to the ability to run away from the problem by migrating or hibernating, because both these responses require some preparation before they can be executed. Migrating animals and hibernators need to store energy (either as fat in the case of migrants and some hibernators or as a food hoard in some hibernators) and to prepare themselves physiologically for the tasks confronting them. In contrast, the laboratory animal spends its time under constant environmental conditions, completely unable to anticipate the fact that one day it will suddenly experience a large drop in the ambient temperature. Even if researchers aorded animals the opportunity to respond to acclimatory cold exposures by migration or hibernation, it is doubtful that they would have the physiological capacities to do so. The ability to anticipate the change is absolutely critical because it means that animals during acclimatization can prepare for the cold, rather than having to respond to it post hoc, which is what occurs in acclimatory responses. When endothermic animals can anticipate the cold, using the decline in photoperiod as a trigger, a dominant response is to increase the amount and quality of their external insulation by moulting into a winter plumage or pelage. These winter coats are generally substantially thicker (i.e. deeper) than during the summer, thereby retarding heat ow from the body (Figure 4). The extent to which dierent species utilize this strategy is strongly dependent on body mass (Figure 4), because the quality of

1.2 Insulation value (W1 m2 C)

Wolf Wolverine

Polar bear

0.9

0.6

Red squirrel

0.3

20 40 Fur thickness (mm)

Figure 4 Insulative value of the fur as a function of fur thickness for four species of arctic mammals in both summer and winter. Summer values are shaded in lilac and winter values are shaded in pink. In all cases there was an increase in fur thickness between summer and winter, but the smaller animals had thinner coats and the extent of increase between summer and winter was also lower in the smaller species. Redrawn from original study by Hart JS (1956) Canadian Journal of Zoology 34: 53 57.

Thermoregulation in Vertebrates: Acclimation, Acclimatization and Adaptation

insulation is dependent mostly on the absolute thickness of the plumage or pelage. It is far easier for an animal weighing 100 kg with a body length of over a metre to increase the thickness of its coat by 5 cm, without there being negative consequences for mobility, than it is for a 10 g animal with a body length of less than 10 cm. This does not mean that changes in pelage and plumage are unimportant for smaller animals but simply that their scope to oset the cold using this strategy is much lower than in larger animals, and consequently they are also more dependent on other responses. Another response that is mostly employed by larger endothermic animals is to deposit a subcutaneous fat store. Since fat tissue has a lower conductance than lean tissue, such subcutaneous deposits may also act as a barrier to heat ow. As with the external insulation provided by fur, the increase in insulation provided by subcutaneous fat is a direct function of its thickness. Larger animals can deposit such stores without impeding their mobility. Many small mammals and birds do increase their fat contents during winter; however, these increases in fat generally are not located subcutaneously and appear to act mostly as an insurance against shortfalls of food intake during periods of inclement weather. Because of their size, small animals generally are unable to modify the insulation provided by both fat and their pelage/plumage suciently to oset completely the change in temperature during winter. Consequently, smaller animals that remain active through the winter have a series of other responses. Probably the most important of these is the increase in thermogenic capacity: that is, the animals are capable of generating substantially more heat when they are cold-acclimatized than they can during the period prior to acclimatizon. In small mammals the changes in thermogenic capacity are predominantly mediated by changes in brown adipose tissue. These include growth of the tissue and increases in the activities of UCP-1 and lipoprotein lipase, stimulated by the declining photoperiod as winter approaches. Similar acclimatization responses in capability to generate heat are observed in birds and in marsupials. In these groups, however, the mechanism must be dierent since the changes do not appear to involve either brown adipose tissue or UCP-1. Several other uncoupling proteins have been isolated and they nd widespread expression in the body. The roles of these UCPs in the generation of heat and acclimatization responses remains uncertain. In addition to changes in the capacity to generate heat, small animals also tend to show profound dierences in body mass between summer and winter that develop during acclimatization. Some species increases and others decrease in total body mass and the causes of such opposite eects are dierent. Where animals increase in body mass during winter, this is often the consequence of deposition of substantial fat stores that serve as insurance for severe periods of energy shortage. In contrast, when animals
6

decrease in mass, this is generally because they have shed lean tissue. Reducing the amount of lean tissue is a useful strategy because lean tissue has a much greater metabolic rate than fat tissue. Overall energy requirements can therefore be reduced by reductions in body mass. Probably the most extreme examples of such reductions in mass occur in shrews, where there appears to be skeletal remodelling so that the animals not only shed lean tissue but actually get physically smaller as well. This latter eect is sometimes called Dehels phenomenon after the Polish biologist who rst discovered it. In addition to these morphological and physiological changes during acclimatization, animals also generally exhibit behavioural changes during the winter months that combine to oset the low-temperature eects. In particular, animals that are often solitary during the summer and may react aggressively to conspecics may become gregarious in winter and huddle together in shared nests to conserve heat. Because animals during thermal acclimatization are able to anticipate the exposure to cold temperatures, their reactions to the cold are generally very dierent from those of animals in the laboratory during cold acclimation, where they have little or no time to prepare for the period of cold exposure. During cold acclimation, the animal can be considered to be in a state of crisis management of its heat budget. It responds to protect its peripheral tissues from frostbite, and the consequences include substantial elevations of thermogenic capacity and total daily energy expenditures and food requirements. Changes observed during cold acclimatization, however, generally ameliorate the eects of lowered temperature, and in consequence total daily energy demands and food requirements may be little altered or even reduced when compared to those in the summer.

Adaptative Responses
Exotherms
As with the acclimation and acclimatization responses, the adaptive responses of exotherms can be characterized as translational or rotational modications in their acute responses to temperature change that serve to oset the eects of declining temperatures. There are many examples of thermal adaptive responses in the metabolism of vertebrate exotherms that inhabit dierent latitudes. A typical example is the thermal response behaviour of natracine snakes from Spain and the United Kingdom (Figure 5). When raised in a common environment, natracine snakes from the United Kingdom generally sustain metabolic rates about two to three times greater than their Spanish counterparts, which inhabit a climatic zone that is routinely 5158C warmer throughout the year. Comparing the metabolic rates of the two species at the

Thermoregulation in Vertebrates: Acclimation, Acclimatization and Adaptation

0.9 Oxygen consumption (mL O2 g1 h1) 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0 0 10 20 Temperature (C) 30 UK

Spain

Figure 5 Metabolic rates (oxygen consumption) of natracine snakes from the United Kingdom (458N) and Spain (308N), raised in a common environment, as a function of ambient temperature. Redrawn from original study by Davies PMC and Bennett EL (1981) Journal of Comparative Physiology 142: 489 494.

temperatures they normally inhabit yields very similar levels of expenditure, indicating almost complete translational compensation. Early studies of marine sh drawn from dierent latitudes pointed to very similar patterns of translational compensation in their metabolic rates. In consequence, sh taken from the seas around Antarctica appeared to sustain metabolic rates in cold temperatures that were almost ten times greater than those of their temperate counterparts. Studies in the 1970s, however, revealed that much of this eect could be attributed to the dierent stress responses to capture and handling of animals from the two environments. Once activity levels following capture had subsided, the dierence between Antarctic sh and temperate-zone sh was considerably reduced but still approximately twofold. This is nowhere near the level required to equal perfect compensation. Indeed, it has been suggested that these animals exhibit very little thermal adaptation but rather a suite of adaptations that enable them to survive in the cold Antarctic waters without using up the considerable amounts of energy that perfect compensation would entail. These adaptations include slow growth, slow reproductive rates and deferred maturity.

Endotherms
Probably the best-known adaptive response of vertebrate endotherms to the thermal environment is Bergmanns law, named after the nineteenth-century German zoologist who rst observed it and proposed a mechanism to explain it. Bergmann noted that populations of a species drawn from higher latitudes tended to have larger body sizes than populations drawn from lower latitudes. There are many common examples of the phenomenon. An interesting one

is the body sizes of European house sparrows in North America. These show a clear trend for individuals to be larger the farther north they are found. Since this is an introduced species, these dierences reect a natural experimental demonstration that the same trend observed in Europe is not due to an artefact of drift eects but is due to some selective advantage linking larger body sizes with colder conditions. Many other examples have been reported. Bergmann suggested the reason for the eect was that larger animals have greater surface-to-volume ratios and thus have proportionately lower heat loss across their body surfaces, giving them a selective advantage in cold conditions because of their reduced heat losses. Discussion of Bergmanns law can be divided into two separate problems. First, whether the observed changes in body size with latitude do follow the trend he originally reported, i.e. getting larger as one moves farther north. The second issue is whether his explanation of the eect is valid. During the 1970s it was noted that in fact, although many species do conform with Bergmanns law, a great many other species do not. Indeed, there appear to be as many species with opposite trends in their body sizes getting smaller as one moves farther north. The suggestion, therefore, that a phenomenon existed that was in need of explanation was called into question. Only very recently has reanalysis of the accumulated data provided some support for the original proposition, because trends in which animals get larger substantially outnumber the opposite trends in which species get smaller combined with species where no trend is observed. It would appear, therefore, that clines in body size are a valid adaptive phenomenon in need of explanation. Although there may be a phenomenon requiring explanation, it has been known since the 1950s that Bergmanns own explanation for the eect is fundamentally awed. The aw is to consider that heat ow per unit tissue mass is important for selection. In fact, animals must balance their energy budgets not on a per gram basis but as entire animals, and it is very clear that while heat losses per gram of tissue are lower in larger animals, total heat losses are inevitably increased. Larger animals actually require more heat (and thus food intake) in the cold than do smaller animals. Bergmanns explanation that being larger conserves energy cannot be correct. Indeed, a primary response of many small animals during acclimatization is to reduce body mass to conserve energy (see above). It would appear the most likely explanation for the phenomenon revolves around the scaling of the capability of dierent-sized animals to deposit fat stores. Although larger animals require more energy, they are able to store fat at a much greater rate. Hence, when food becomes unavailable these animals have much greater fasting endurance. Another aspect of thermal adaptation in endotherms is the profound dierences that are observed in insulative properties of their pelage or plumage. Endotherms
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Thermoregulation in Vertebrates: Acclimation, Acclimatization and Adaptation

inhabiting more northern climes have much thicker and denser coats that allow them to minimize heat losses under cold conditions. These dierences result in very wide thermoneutral zones for the animals from high latitudes, which enable them to live in very cold conditions without elevating their metabolism above basal levels to keep warm. Typical examples are Arctic gulls and Arctic foxes, both of which expend energy at basal levels down to 2 308C.

Further Reading
Cossins A and Bowler K (1980) Temperature and Life. London: Chapman and Hall. Davenport C (1996) Low Temperature Adaptations of Animals. Cambridge, UK: Cambridge University Press. Schmidt Nielsen K (1998) Environmental Physiology of Animals: Adaptation and Environment. Cambridge, UK: Cambridge University Press.