Animal thermoregulation: a review of insulation, physiology and behaviour relevant to temperature control in buildings

The skin and associated tissues (integument) provide multiple functions in vertebrates, principally providing a barrier to water diffusion and physical protection of underlying tissues. It also determines thermal properties and is covered by numerous nerve endings and an extensive network of blood vessels. The vertebrate integument consists of epithelial cells attached to an underlying fibrous and vascular dermis. Localized cellular growth and differentiation give rise to appendages such as claws, glands, hair or feathers, and patterned folds or scales formed from keratin, a family of fibrous structural proteins. Keratin is a common and important structural feature formed in the epidermis [11]. Amphibian skin is relatively permeable to water (see below) and gas exchange can take place through the skin (cutaneous respiration). Secretion of mucus from glands in the dermis keeps skin moist, and in some species mucosubstances and lipid compounds form an extra-epidermal layer, reducing water loss. Reptilian skin has a thickened epidermis with a relatively thin dermal layer in comparison to that of birds or mammals (see figure 1 in [11]). This provides a more effective barrier to water and gas exchange compared to most amphibians. Reptile skin is mechanically protected by scales or scutes, and in lizards and snakes the entire skin is covered by scales. However, avian and mammalian integuments have a thickened outer layer of the skin (stratum corneum) which can be highly keratinized to provide a strong mechanical barrier. Specialized epithelial cells form feather and hair follicles in these skins.

Water loss through the integument occurs by the passive diffusion of water across cell membranes (not requiring metabolic energy) and also by active secretion in mucus (in amphibians) or from sweat (mammals). Water loss is therefore largely determined by the skin's resistance to water passage. For comparative purposes, skin resistance to evaporative loss may be negligible (~ 0 s cm⁻¹) in many aquatic and terrestrial amphibians, 100–200+  s cm⁻¹ in some frogs adapted to low moisture environments, and very high at over 1000 s cm⁻¹ in desert reptiles, while most birds and mammals have skin resistances of 10–300 s cm⁻¹ [11]. Only mammals may lose considerable quantities of water through sweating. Sweat is secreted to the skin's surface through pores from specialized glands, allowing cooling of the surface through latent heat transfer. Humans, horses and patas monkeys (Erythrocebus patas) are the only mammals reported to sweat profusely for thermoregulation. The compositions of their sweat fluids differ markedly; humans have high-salt, low-protein sweat, whereas horses have high-protein, low-salt sweat [12]. Sweating may appear to be maladaptive for species such as horses with a thick and waterproof pelt that would slow down the transfer of sweat from the skin to the outer hair surface for evaporative cooling. However, horses have evolved a surface-active detergent-like protein (latherin) that they secrete in their sweat. Latherin reduces water surface tension at low concentrations and most likely acts as a wetting agent to allow evaporative cooling through an existing waterproof coat [13]. Sweating is a unique physiological mechanism to only maximize latent heat loss, in comparison to other bi-directional heat transfer processes through adjustments to conduction, radiation and convection across the integument. Heat transfer occurs by a combination of conduction through the epidermis to the skin surface and latent heat transfer from passive diffusion of water and by evaporation of water on the skin surface. Conduction and latent heat transfer are strongly influenced by dilation and constriction of capillary networks through the epidermis that can bring about rapid changes in skin temperature [7].

Thermal insulation in animals is provided by layers of lipid-filled cells with low thermal conductivity (fat and blubber) or by a keratin matrix that traps still air (feathers and hair) (table 1). The thermal characteristics of different types of insulation are derived by a combination of physical structure and dynamic properties controlled by an animal's physiology and behaviour. Feathers and hair are hierarchical materials that derive their mechanical characteristics from the basic keratin unit (helical proteins), to individual element composition and their arrangement in plumage and fur [14].

3.2.1. Fat and blubber

3.2.2. Feathers and plumage

3.2.3. Hair, fur and wool

Heat transfer through an animal's coat occurs by a number of processes, either by: (i) conduction, through trapped air and along feather or hair fibres; (ii) radiation from these fibres; (iii) free convection, and; (iv) forced convection when wind penetrates the coat [10]. Conduction along feather elements is the predominant mechanism of heat transfer, accounting for around 50% of heat flow through plumage [44]. Conversely, conduction in fur has been considered negligible as the cross-sectional area of hair represents approximately 0.01% of the skin's surface area [45]. Radiative heat transfer within bird and mammal coats is relatively small and represents around 4–10% of total heat flux due to efficient interception of radiation within the coat matrix [44, 46]. Free convection through plumage represents less than 15% of total heat transfer in still air but may be around twice this in fur because of its more open structure [44, 47]. In contrast, at high wind speeds, forced convection leads to the penetration of air inside the coat, decreasing coat conductance [18].

Wind penetration of the coat is influenced by wind direction relative to the coat axis, and there are large differences between species in the ability of wind to penetrate the coat [48]. Particularly wind-resistant plumages are found in penguins, where the thickened rachis (feather shaft) provides an effective barrier to wind, as well as providing hydrodynamic properties [36]. In Arctic mammals such as reindeer, stiff guard hairs and dense packing of hair elements prevents wind penetration [41]. In the rain, penetration of water into the coat also increases conduction or decreases insulation by displacing trapped air and mechanically disrupting the coat structure [49]. For diving animals, the pressure increase at depth compresses the coat's air layer and may allow water to penetrate and displace this air layer [27]. However, the coats of aquatic animals with stiffened rachis of contour feathers or primary guard hairs, combined with densely-packed coat elements, are especially efficient in reducing water penetration. This is further aided by the micro-structural topography of the coat and surface coatings of hydrophobic molecules that increase water shedding [50]. These lipids and waxes are produced by the uropygial (preen) gland and are coated onto feathers by preening. In mammals, lipids (sebum) secreted from the sebaceous gland at the base of the hair follicle provide the water-repellent coating [51]. Penguin body feathers also have air-infused micro- and nanoscale rough structures, giving hydrophobic and anti-adhesion properties that may prevent ice formation at the surface [52].

Diving animals such as otters show specialized morphology of the fur that reduces penetration by water. The cuticles of the thin under-hairs have sharply sculpted fins with deep grooves between them that provide an interlocking structure [53]. However, in contrast to the hydrophobic properties of many avian plumages, including most diving birds, the feathers of cormorants are partially wettable, allowing some reduction in buoyancy while retaining the insulative air layer. This is achieved by a loose outer section of the feather that is instantaneously wettable, with an inner section that remains dry. Microscopic examination indicates that this is due to regular and close interlocking feather elements that are resistant to water pressure [54].

Latent heat transfer is also an important heat transfer mechanism within animal coats. Water vapour transfer is influenced by feather or hair characteristics, particularly their hydrophilic properties, and by the humidity of air within the coat. Wool is highly hydrophilic, and in a sheep's fleece heat is released by condensation (equal to latent heat of vaporization) as water condenses on fibres and when water vapour is absorbed by the wool. Overall, these transient heating effects are trivial (typically less than 10 W m⁻²) because relative humidity changes slowly in the fleece and any increase in humidity near the skin is balanced by a decrease in humidity in the outer fleece [55]. Rain may increase relative humidity in the outer fleece, resulting in transient heat production, but prolonged rain will also increase heat loss by decreased insulation of the fleece and by evaporation.

Animal insulation changes with time, responding to variation in the environment and longer-term seasonal climate patterns. Piloerection (mammals) and ptiloerection (birds) elevate hair or feather elements instantaneously to modify heat exchange. For example, contraction of muscles at the base of the hair raises the effective coat depth in horses by 16–32% or by a depth of 0.4–1.4 cm in new-born foals [56]. In birds, ptiloerection is controlled by muscles that result in fluffing or flattening of the plumage in response to air temperature or wind and may be responsible for increases in depth and insulation of 50% or more [57].

Species living in seasonal environments change their coat insulation in response to day length. Unlike the rapid change in insulation occurring over a few minutes with pilomotion, seasonal adjustments to insulation occur over a time scale of weeks to months. Many birds and mammals become obese before intense periods of fast (when migrating, breeding, or moulting) or in anticipation of the harsh season (combining food shortages and air temperatures far below body temperature). This will increase thermal inertia and will often be beneficial during the start of winter. For example, increases in fat stores have been attributed to increases in whole animal insulation in Arctic birds such as the rock ptarmigan [58]. As winter progresses, however, fat will be metabolised and any small benefit from this insulation will be lost. In contrast, the plumage will continue to provide effective insulation throughout this period.

Changes in coat insulation are controlled by the process of moult that brings about complete replacement of hair or feathers. This may occur as a gradual process over several months or relatively rapidly [33, 59, 60]. For example, Arctic foxes (Alopex lagopus), and Arctic hares (Lepus arcticus) undergo seasonal moults involving both colour change for camouflage and alterations to thickness and quality of insulation [61, 62]. The autumn moult replaces the thin summer coat with a thick, well-insulated coat that reduces heat loss [59]. Typically, changes to the density, diameter and/or length of hair result in higher insulation in the winter [63]. For example, in three species of sub-Arctic mammals, coat thermal resistance was greater in winter by as much as 27–87% compared to summer [64].

Similarly in birds, major differences in plumage thickness and insulation occur due to seasonal moult prior to the cold season. For example, the whole-body insulation of a small shorebird, the knot (Calidris canutus) was 35% lower in full breeding plumage compared to birds in winter plumage, due to a 37% reduction in feather mass [65]. A multi-species comparison of mostly passerine birds shows that larger species have fewer and heavier feathers, and the rate of feather loss is less in autumn and winter. During spring and summer the rate of feather loss remains constant, with a minimum number of feathers in summer prior to the start of moult [30].

In contrast to solid surfaces, animal coats are not simple surfaces with respect to radiative transfer. Coat reflectivity determines solar radiative gain, but how this contributes to overall heat transfer depends on how well radiation penetrates and is absorbed over a range of coat depths. These properties depend on the micro-optics and structure of the coat [66]. Light-coloured coats have a higher albedo, but solar radiation penetrates deeper into light coats as a result of forward radiative scattering. Animals with dark coats receive a greater heat load at the skin surface when wind speed is low, but at high wind speeds the heat load is less than for similar white-coated animals due to a decrease in conductance at the outer coat surface where radiation has not penetrated further [42, 67]. The polar bear remains white throughout the year but many Arctic species moult into cryptic white fur or feathers in winter. Any radiative advantages from a white coat are however offset by a combination of low winter solar radiation and thicker winter coats that prevent radiative penetration to the skin surface [42, 64]. There has been considerable interest in the radiative properties of polar bear fur, after it was reported that their fur has low UV reflectance. It was suggested that their hollow hairs facilitated internal reflection to their dark skin, thereby providing a thermal gain [68]. However, further evaluation of this model of fibre-optic transmission demonstrated that low UV reflectance could be attributed to the absorption of radiation by keratin that makes up hair [69]. Nevertheless, polar bear fur is extremely thick and has a high density of hairs that effectively intercept most radiation from the skin surface [70].

Colour change is common in animals for communication, camouflage, thermoregulation and protection from UV. In contrast to birds and mammals which moult at most twice a year, amphibians and reptiles have the ability to reversibly adjust skin colour over short periods of time, thanks to chromatophores within the integument. Morphological colour change over days or months occur due to changes in the amount of pigment and/or number of chromatophores, whereas rapid changes over seconds to hours occur by pigment migration within the chromatophores [71]. In some species of amphibians, colour change from dark to light is stimulated by increases in solar energy and anticipated changes in body temperature [72]. The ability to change colour is linked to the organisation of chromatophores in the dermis of the dorsal skin. Pale colouration is due to light-reflecting organelles (iridophores) comprising stacks of purine-containing reflecting platelets (a heterocyclic aromatic organic compound). However, the melanophores darken the skin by rearrangement of melanin in the cytoplasm [73]. Darkening melanosomes migrate from a basal position into cellular processes of the iridophores and obscure the reflective properties of the brightly coloured pigments they contain. When basking, however, melanosomes are found in the cell body below the iridiphores, allowing the light to be reflected by the crystals within the iridiphore and causing the skin to whiten. Recent studies on the bearded dragon lizard (Pogona vitticeps) showed that it exhibited an endogenous circadian rhythm in pigmentation that was entrained by light/dark cycle, decreasing reflectance in both the ultraviolet visible and near-infrared spectra (300–2100 nm) during the early part of the day to match solar input [71].

The complex structural and optical properties of avian and mammalian coats in comparison to skin surface (above) provides a counter-intuitive selective advantage to dark-coloured birds and mammals in hot environments where heat transfer may also be modified by wind. This, combined with a thick and dense covering of fur or feathers, leads to relatively small heat loads at the skin surface [42]. To provide an extreme example, the fur surface temperatures of cape fur seal (Arctocephalus pusillus) pups were recorded reaching as much as 79.6 °C, while skin and rectal temperature were only 42.1 °C and 36.1 °C, respectively [74].

Studies into the thermal significance of colouration have generally focused on dark or light colouration, perhaps neglecting the thermal properties of animals with distinctive markings or stripes.

The adaptive significance of stripes in zebras may originate from social cohesion, predation evasion, avoidance of biting flies and/or thermoregulation [75, 76]. Black and white stripes have even been predicted to enhance heat loss through the formation of convection eddies under sun exposure, but this has yet to be investigated.

Vertebrate physiology can be broadly classified by stability in body temperature and source of body heat (figure 1). Ectotherms are thermo-conformers, i.e. their body temperature changes with environmental temperature. Ectotherm implies a reduced level of thermoregulation, as metabolism is driven by the thermal environment, whereby animals passively acquire their heat from the environment (e.g. by basking). It is only when they are warm enough that they can begin to undertake biological functions, such as foraging or mating. Actually, ectothermy is an ancestral state, and is still the prevailing thermoregulation system in invertebrates and the earliest evolved classes of vertebrates, including fish, amphibians and reptiles [77, 78].

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Endotherms are thermo-regulators: they produce heat (through their metabolism) to maintain a high and relatively constant (homeothermic) body temperature. Normal core temperature ranges from 34–44 °C in birds, depending on species. Core temperature in mammals is usually maintained around 36–38 °C but can be as low as 30 °C in the monotremes (platypus and echidnas) and as high as 40 °C in some groups. However, many endotherms are regionally or temporally heterothermic, with variable endothermic heat production and body temperature [79]. The major benefit of endothermy is that it allows the uncoupling of internal thermal needs for maximal biological performance from external constraints, and particularly thermal constraints. It also permits permanent maintenance of high brain temperature for maximal cognitive performance (and therefore, integrated control of homeostasis) year-round.

One important challenge in applying animal models to the human environment is addressing the concept of 'thermal comfort', described as 'the condition of mind that expresses satisfaction with the thermal environment (ANSI/ASHRAE Standard 55)' [80]. This is based on the thermal aspects of a building that determine the physical and psychological perception of temperature and energy exchange, and which are influenced by metabolic rate, clothing insulation, air temperature, radiant temperature, air speed and relative humidity [81, 82]. For ectotherms, this could be equated with preferred body temperature, which is generally close to the 'optimal' temperature for many physiological processes, but this preferred temperature may vary for different activities. Thermo-preferences have been reported for endotherms, largely in the context of laboratory studies [83]. Often, 'thermal comfort' for endotherms is regarded as synonymous with 'thermal neutrality': the range of environmental temperatures over which metabolic rate and therefore heat production does not change [84]. An alternative approach is to derive a thermal index, the operative environmental temperature that combines microclimate (temperature, radiation, wind) with properties of an organism (size, shape, posture). This index indicates if the organism, given its current temperature, will gain or lose heat in that microenvironment [85].

Control theory as used in engineering provides a framework for understanding temperature regulation in animals [86, 87]. On this basis, the regulated variable is body temperature, and temperature sensors throughout the body generate neural signals to a controller which is then compared to a reference signal or set-point (figure 2). The difference between body temperature and the set-point represents a load error which drives effector mechanisms for heat production or heat loss. Effector responses act in a direction opposite to the load error and therefore control it, typically by negative feedback. In this way, changes in heat production and heat loss are also proportional to the load error generated.

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Endotherms generally have a relatively stable internal or core temperature in comparison with variable skin temperature [88]. The regulated body temperature is therefore an internal temperature but it may also be an integrated temperature from different body regions. The function of the controller is to link afferent signals from temperature sensors with efferent drives to multiple effector mechanisms through the central nervous system (CNS). The preoptic anterior hypothalamus (POAH) of the brain appears to function as the main controller, in addition to some other CNS regions. Temperature sensors are not restricted to the CNS. They are found in the intestine, abdomen, skeletal muscles and trunk [87]. However, all thermoregulatory effector mechanisms may be activated or inhibited by skin temperature changes. Cold and warm thermoreceptors are found in the skin corresponding to the sensation of cooling or heating. These have different dynamic properties: cold receptors respond to rapid drops in skin temperature with a short-duration rise in activity, while warm receptors overshoot during warming and demonstrate transient inhibition while cooling quickly [86].

Sensation of temperature is dependent on both the absolute level of skin temperature and the extent and rate of change of temperature. For animals with fur and feather insulation, behavioural changes may be determined by the rate of change in skin temperature of bare skin areas. For skin temperature to activate or deactivate effector mechanisms, skin temperature must exceed an effector specific threshold. These thresholds are strongly defined by the extent of external insulation, such that for well-insulated animals a drop in skin temperature of 1 °C may initiate shivering, while for a bare-skinned animal such as a pig, shivering still does not occur even when absolute skin temperature is as low as 10 °C [89, 90]. Temperature changes of localised and small skin regions can activate effector mechanisms. For example, in humans, changes in face temperature produce a three-fold difference in sweating rate compared to a similar-sized region of the thigh [91]. However, small changes of body core temperature can produce large effector responses that are independent of skin temperature. For most free-living animals, core and skin temperature interact to influence effector mechanisms such as heat production, evaporative water loss and behavioural thermoregulation (figure 2).

Heat produced within the body is distributed by blood flow and through conduction from core to shell. In the cold, there is minimal flow of blood to the skin surface. Vertebrates have direct connections between arteries and veins controlled by valves (known as arteriovenous anastomoses, AVAs) that prevent blood from flowing to the fine blood vessels (capillaries) close to the skin surface [7]. In contrast, in the heat or when animals are active, peripheral blood vessels (arterioles) dilate, and AVAs allow blood to flow to the periphery. This system is particularly important in marine mammals, where the heat exchange shunt vessels are located beneath the blubber layer, allowing blood to bypass insulation when heat dissipation is required, or to restrict blood flow to the surface for heat conservation [28]. Heat distribution within the body is also facilitated by counter-current heat exchangers that are found in body extremities that are particularly well developed among cold-adapted species [92]. In this case, warm arterial blood runs parallel to venous returning blood to the core. This system may function together with vasomotor control, resulting in regional heterothermy of the body. Species such as antelope and deer have effective heat exchange systems to regulate brain temperature when excessive heat is produced during exercise [7]. However, more recent measurements on free-living animals have questioned the accepted view that brain cooling is a response to high body temperature, at least under moderate heat loads [93].

Vertebrates have the ability to precisely regulate skin surface temperature by vasoconstriction and dilation of peripheral blood vessels. However, certain regions of the body have particularly well-developed capillary networks, often on bare skin. These act as highly efficient 'thermal windows': when 'open' (vasodilated) they are used to dissipate excessive heat, and when 'closed' (vasoconstricted) they minimize heat loss. Their main function maximizes dissipation of excessive heat, e.g. the large external ears (pinnae) of elephants [94]. However, these are not necessarily confined to particular appendages but may also occur as isolated 'hot spots' across the body (e.g. in seals) that increase heat loss by convection or evaporation from a wet pelage [95]. Heat exchangers may potentially function to maximize solar heat gain. However, the extent to which 'thermal windows' are used by endotherms for heat gain is less well known than for ectotherms, where rewarming by basking is common [96].

Heat exchange occurs by passive latent heat loss through skin and by respiratory latent heat loss from lungs, which may be increased by panting in mammals or vibration of the throat (gular flutter) in birds. Evaporative water loss at high temperatures occurs from sweating or may be enhanced by the wetting of fur or feathers from bathing, etc. In cold climates, water can be replenished only by drinking cold water or ingesting snow, which costs energy along with the latent heat loss from the respiratory tract. For example, in reindeer, both latent heat and water losses are minimized by counter-current heat exchange in the nasal cavity [92]. The cavity contains an elaborate system of scrolled structures (conchae) which have a highly vascularized mucosal layer. Inhaled air becomes warmed and saturated en route to the lungs. This process cools the mucosa, and when air is returned from the lungs the warm humid air flows down a temperature gradient, allowing cooling and water condensation and resulting in the expiration of cold and dry air. This system is also seen in seals, with previous studies on grey seals (Halichoerus grypus) showing that more than 60% of heat and 80% of water added to inspired air is recovered at  −20 °C, saving 10–30% of total water flux for the animal [97, 98].

Most environments do not remain constant over time and therefore animals must cope with a range of conditions that vary across days, months and years. Thermal acclimation in an endotherm is a response to compensate for changes in resource availability and the thermal environment. Many of these may be gradual and involve daily, monthly or annual adjustments to behaviour, morphology, physiology or biochemistry [7].

Endotherms respond to changes in the thermal environment in multiple ways, involving initial behavioural (e.g. posture, activity or migration) and physical adjustments to alter their energy balance (insulation and energy storage). However, many vertebrates also respond to seasonal changes in climate or food availability by decreasing their metabolic rate (energy use) and down-regulating their body temperature. Metabolic rate and body temperature are controlled by endogenous signals entrained to the photoperiod (day length) and fine-tuned according to climatic conditions [99, 100]. Most endotherms show daily changes in body temperature, with diurnally active species generally having a lower body temperature at night and nocturnal species having a lower body temperature during the day.

There are generally four recognisable temperature control patterns in endotherms with progressively greater decreases in body temperature between activity and rest: strict homeothermy, daily heterothermy, daily torpor, and hibernation. Many species, including humans, show small decreases in body temperature related to rest/sleep-activity patterns. This confers only small energy savings when animals are inactive. However, some species use shallow heterothermia to cope with cold winter conditions. Large endotherms use hypometabolism as a strategy over the winter, and peripheral cooling may be the mechanism by which the down regulation of the resting metabolic rate occurs. For example, in red deer (Cervus elaphus), heart rate (as a measure of metabolic rate) has been shown to be endogenously lowered in winter. Rumen temperature (as a measure of core temperature) on average decreased by 0.5 °C in winter and was correlated with seasonal and periodic variation in heart rate, supporting the hypothesis that lowered body temperature controlled by peripheral cooling is also an important mechanism by which large mammals achieve hypometabolism during food shortage [101]. It appears that a reduction in BMR and the set-point of core body temperature are both required in order to achieve an overall decrease in thermoregulatory costs in cold temperatures [99].

Pronounced patterns of heterothermy in endotherms are characterized traditionally as two different types of hypometabolic states associated with low body temperature: daily torpor lasting less than 24 h and followed by foraging activity, and hibernation with periods of torpor occurring over consecutive days to several weeks, where animals do not usually forage but rely on food caches or body energy stores. Heterothermic birds and mammals are small (<1 kg; apart from bears) and hibernators are larger and found at higher latitudes (or altitudes) compared to most daily heterotherms. Basically, it seems that heterotherms are endotherms that evolved in environments where energetic constraints are too strong to be compensated by usual adaptations; they are too small to store internally a sufficient amount of energy, and their small size (high surface/volume ratio) means that they passively lose considerable amounts of heat. Heterothermic bouts are on average more than 25 times longer, and minimum body temperatures ~ 13 °C lower in hibernators [102]. In energy saving terms, the minimum torpor metabolic rate of ~ 35% of BMR in daily heterotherms compares with only 6% of BMR in hibernators, indicating the much greater energetic efficiency of hibernation over daily torpor. Daily heterotherms use a circadian system to control the timing of torpor, which allows foraging to continue following torpor bouts. In contrast, hibernators are 'uncoupled' from circadian control so as to facilitate long-duration periods of low metabolism; but they maintain a circa-annual clock that is necessary in order to time the termination of the hibernation period, and emergence from the winter burrow (or den), in the absence of direct cues about exterior environmental conditions. Interestingly, in the transition between summer and winter, hibernators have a period when they are daily heterotherms: they use torpor facultatively, flexibly, on a daily basis, depending on current needs and environmental constraints. It also seems that there is a need for a period of acclimation of the organism, when torpor is progressively used for longer periods of time, and increasingly lower body temperature [103].

Hibernation is an obvious seasonal adaptation of small mammals and birds to cold (or dry) climates, with predictable, long periods of low temperatures and/or drought. It is characterized by prolonged periods of inactivity and down-regulation of metabolism and body temperature. Therefore, suitable animal models for seasonal cold temperate climates may be better found amongst species that remain active during winter and are able to maintain energy use and control body temperature within set limits. Studies of species that are adapted to cold winter conditions may reveal obvious annual patterns in body temperature and energy use that provide a basis for seasonal adaptive control of temperature and energy use in buildings. New technology that records body temperature and energy expenditure has provided an annual picture of the dynamics of thermoregulation [79]. In cold environments, small diurnally active birds exhibiting rest-phase hypothermia during winter indicate an energy-saving strategy for animals that are inactive at night [104]. Nocturnal body temperature reaches a minimum in midwinter corresponding to the reduced period of daylight. However, body temperature also varies according to air temperature, suggesting that environmental stochasticity fine-tunes energy use. Daily heterothermia and torpor are physiological mechanisms that provide considerable energy savings for animals in cold climates. This combination of thermal adaptations may therefore be a useful model to explore energy savings for cold seasonal climates.

Applicable animal models that may provide insights into thermal aspects of building design for warm climates may come from large desert-dwelling mammals that tolerate extreme heat during the day and cool conditions at night. The key adaptive feature of these species is a thermoregulatory system based on dry (non-evaporative) heat exchange facilitated by daily heterothermia. For example, in the Arabian camel (Camelus dromedaries) during dehydration and heat stress, the amplitude of the daily body temperature rhythm in rectal temperature exceeded 6 °C [6]. More recent studies have shown that after a prolonged period of dehydration, when exposed to air temperatures of 38–46 °C in the day and 20–25 °C at night, the amplitude of the core body temperature rhythm averaged 3.8 °C (average minimum 35.4 °C in the morning and maximum 39.2 °C in the evening) [105]. By allowing body temperature to rise during the day, the gradient in temperature between body and environment is minimized, reducing thermal gain. The 'stored' heat offsets nocturnal heat loss, resulting in a minimum body temperature in the early morning. Camels also show morphological adaptations to cope with high solar gains. They possess thick fur on their dorsal surfaces and most adipose stores are distributed, particularly in the dorsal hump [24]. Fur is less thick on flanks and legs, which may enhance heat loss from these regions. The overall body shape may also be an adaption that minimizes solar gain. Small nocturnal heterotherms living in the tropics may also be useful models for understanding how patterns of heterothermia result in reduced energy costs during the dry season. There is considerable variation in the patterns of heterothermia between and within species. For example, in grey mouse lemurs (Microcebus murinus), energy savings (decreased metabolic rate) resulting from torpor are proportional to torpor depth (minimum temperature) and torpor duration. These savings increase with decreasing air temperature, indicating that these facultative thermoconformers can save more energy in colder conditions [106].

Behavioural and ecological factors allow endotherms to adapt to different climates, and these factors are actually more important than an animal's metabolic characteristics [107]. For species that are unable to avoid unfavourable thermal conditions by migration, there is a great diversity of behavioural adaptations for thermoregulation that reduce energy costs (see detailed review in [83]). These may be best described broadly as 'individual' or 'group' strategies. Individually, animals may change their posture to reduce their surface to volume ratio, and increase their effective insulative layer by adopting hunched or 'ball-like' postures such as those seen in small birds and rodents. Similarly, animals may bask to allow passive warming, or change posture or position to facilitate convective cooling from wind, or seek water to cool by evaporation. Group behaviours such as huddling and/or nest-sharing are principally used to reduce heat loss and decrease individual costs of heat production [108]. These behaviours function by reducing the surface area exposed to the environment, modifying the microclimate and sharing metabolic heat. Examples are common amongst species adapted to cold. The huddling behaviour of emperor penguins during the Antarctic winter is particularly effective in providing shelter from extreme winds, modifying the microclimate of the huddle and minimising exposed surface area. In contrast, huddling is highly beneficial for young birds and mammals before insulation has developed, allowing them to minimize surface area and increase the temperature of the sheltered and well insulated nest environment.

Animals have the ability to construct structures that enhance the thermal and ventilation properties of their nests. The most well-known nests in bioinspiration studies are termite mounds, which appear to promote cooling and gas exchange by some combination of enhanced convection due to heat derived from metabolism (termites and fungal colonies) and ventilation driven by vertical wind speed profiles (Bernoulli's principle) [109]. Magnetic or compass termites (Amitermes meridionalis) endemic to northern Australia build wedge-shaped mounds many metres in height. They are composed of a hard outer shell (with connections between chambers) that is aligned with the north–south axis. This has been interpreted to provide a thermal function, allowing the early morning sun to warm the nest while its narrow width minimizes solar gain when the sun is overhead. Such explanations have however been questioned, and there may be multiple environmental factors influencing mound shape and structure [110–112]. Indeed, recent measurements of air flow within mounds of the species (Odontotermes obesus) in south Asia show that 'a simple combination of geometry, heterogeneous thermal mass and porosity allows the mounds to use diurnal temperature oscillations for ventilation' [112]. The outer structure of the mound containing 'flutelike conduits' rapidly heats up during the day relative to the internal 'chimneys', forcing air to move down the chimneys in a closed convection cell. The direction of flow is reversed at night as the exterior of the mound cools, and these cyclic flows allow CO₂ to be flushed out and air to be replenished to the termite colony. Construction is also widespread amongst many ectotherms to maintain humidity within nests and cocoons. Silk produced by the hornet (Vespa orientalis) and several similar species also has thermoelectric properties [113]. Measurements taken on strips of hornet silk showed rises in electric charge when temperature increased from 20 °C to 33 °C and at more than 90% relative humidity [114]. In the warm daytime hours, hornet silk transports water, raising relative humidity, thus providing the evaporation needed for nest thermoregulation, and at night electric current and heat flows along the silk.

Amongst vertebrates, a variety of nests and dens are constructed underground to avoid either excessive heat or cold (as well as to provide a hiding-place from predators). These provide favourable microclimates and are insulated by collected material [115] or from snow [62, 116]. Maximising insulation has the potential to compromise ventilation. The paired and elevated entrances to burrows constructed by prairie dogs (Cynomys sp.) in arid zones of North America facilitate wind-induced ventilation [117]. Measurement of air flow and temperature within the burrow systems of small rodents shows that even at low wind speeds, the unpredictable penetration of eddies into a burrow through its openings can maintain CO₂ concentration within physiologically appropriate limits [118].

Avian nest construction is highly specialized, providing enhanced insulation in cold environments and protection from wind and rain. Successful nests are often associated with the choice of suitable microclimates with regard to orientation to the sun and shelter from wind and precipitation [119]. Nesting materials vary but feather down provides the best insulation while some grasses are relatively poor insulators [120]. In general, the insulation properties of nests are poorer in warmer low latitudes and this may involve changes in morphology (wall thickness) and composition (dry grasses) [121]. Many nests incorporate a variety of materials including mud, plant stems and branches to provide additional structural support. However, there are direct thermal benefits from the choice of nest material. For example, in Australia, the malleefowl (Leipoa ocellata) constructs a large nest mound containing buried plant material that maintains incubation temperature from the heat of decomposing vegetation [122]. Many birds also occupy man-made structures, including customised nest boxes or buildings that provide favourable microclimates for nesting or roosting [123].