**3.1 Ratio of surface area to volume**

Organisms with a large ratio of surface area to volume such as small passerines and mammals must be careful to maintain heat balance, as they are prone to rapid heat exchange. They require a large amount of energy intake to aid in heat balance; birds and bats even more so due to the high metabolic cost of flight. Treecreepers, a type of bird found in forests of Spain, selectively forage on certain areas of trees depending on the TA. In warm temperatures the birds tend to forage on shaded areas whereas they prefer areas exposed to sunlight in cooler temperatures (Carrascal et al., 2001). By maintaining TB using behavioral thermoregulation the birds are able to save energy that can be allotted to other expenses such as predator avoidance, especially since foraging in sunlit patches increases their predation risk. In fact, the overall abundance and species richness of birds in a montane forest was calculated to be mainly a function of solar radiation (Huertas & Diaz, 2001). By choosing areas higher in available sunlight, small birds can lower their metabolic cost of thermoregulation and improve survival in cold temperatures. In warm environments small birds are able to balance thermoregulation by avoiding sunlit areas. Verdins are able to reduce their metabolic rates by shifting to wind and solar-shielded microsites, allowing for a highly reduced rate of evaporative water loss. In order to maintain efficient use of energy and water, verdins must actively select thermoregulatory beneficial areas within their habitat (Wolf & Walsburg, 1996).

#### **3.1.1 Torpor**

Small mammals often use torpor as a thermoregulatory strategy. By decreasing TB and metabolic rate, small animals can substantially reduce energy expenditure. Though it requires energy to arouse from torpor, some mammals can choose sites exposed to solar radiation during the day and are able to bask in sunlight, using the passive absorption of radiant heat to rewarm their body and profit from the energy saved while torpid (Warnecke et al., 2008).

#### **3.2 Birds**

Birds lack sweat glands so they must rely on other mechanisms of heat reduction. Even something as simple as changing orientation in relation to the sun can have a large effect in reducing heat gain. Flying is an energetically expensive mode of locomotion that can generate high heat loads. Herring gulls, for example, are able to lessen heat gained by reducing exposed surface area and orienting their bodies in a way that presents only the white-feathered surface, allowing for a greater degree of reflection rather than absorption of solar energy (Lustwick et al., 1978). The Great Knot, a shorebird from Australia, raises its back feathers to initiate a possible increase in convective or cutaneous cooling (Battley et al., 2003). Cormorants often spread their wings on land; most likely a wing-drying strategy but also a mechanism used to dissipate heat. During periods of low wind these cormorants rely on the sun to dry their plumage. This behavior saves cormorants the large energetic cost it would take to dry their feathers using metabolic heat to evaporate the water (Sellers, 1995).

Depending on the environment, many incubating birds that are restricted to their nest site must tolerate direct solar radiation. For example, the Heermann gull resorts to ptilomotor responses, posture changes, and increased respiration through a gaping mouth, employing several mechanisms of heat dissipation to offset heat gain from direct radiation as well as conduction from the nest substrate (Figure 3) (Bartholomew & Dawson, 1979).

in forests of Spain, selectively forage on certain areas of trees depending on the TA. In warm temperatures the birds tend to forage on shaded areas whereas they prefer areas exposed to sunlight in cooler temperatures (Carrascal et al., 2001). By maintaining TB using behavioral thermoregulation the birds are able to save energy that can be allotted to other expenses such as predator avoidance, especially since foraging in sunlit patches increases their predation risk. In fact, the overall abundance and species richness of birds in a montane forest was calculated to be mainly a function of solar radiation (Huertas & Diaz, 2001). By choosing areas higher in available sunlight, small birds can lower their metabolic cost of thermoregulation and improve survival in cold temperatures. In warm environments small birds are able to balance thermoregulation by avoiding sunlit areas. Verdins are able to reduce their metabolic rates by shifting to wind and solar-shielded microsites, allowing for a highly reduced rate of evaporative water loss. In order to maintain efficient use of energy and water, verdins must actively select thermoregulatory beneficial areas within their

Small mammals often use torpor as a thermoregulatory strategy. By decreasing TB and metabolic rate, small animals can substantially reduce energy expenditure. Though it requires energy to arouse from torpor, some mammals can choose sites exposed to solar radiation during the day and are able to bask in sunlight, using the passive absorption of radiant heat to rewarm their body and profit from the energy saved while torpid (Warnecke

Birds lack sweat glands so they must rely on other mechanisms of heat reduction. Even something as simple as changing orientation in relation to the sun can have a large effect in reducing heat gain. Flying is an energetically expensive mode of locomotion that can generate high heat loads. Herring gulls, for example, are able to lessen heat gained by reducing exposed surface area and orienting their bodies in a way that presents only the white-feathered surface, allowing for a greater degree of reflection rather than absorption of solar energy (Lustwick et al., 1978). The Great Knot, a shorebird from Australia, raises its back feathers to initiate a possible increase in convective or cutaneous cooling (Battley et al., 2003). Cormorants often spread their wings on land; most likely a wing-drying strategy but also a mechanism used to dissipate heat. During periods of low wind these cormorants rely on the sun to dry their plumage. This behavior saves cormorants the large energetic cost it would take to dry their feathers using metabolic heat to evaporate the

Depending on the environment, many incubating birds that are restricted to their nest site must tolerate direct solar radiation. For example, the Heermann gull resorts to ptilomotor responses, posture changes, and increased respiration through a gaping mouth, employing several mechanisms of heat dissipation to offset heat gain from direct radiation as well as conduction from the nest substrate (Figure 3) (Bartholomew &

habitat (Wolf & Walsburg, 1996).

**3.1.1 Torpor** 

et al., 2008).

**3.2 Birds** 

water (Sellers, 1995).

Dawson, 1979).

Fig. 3. Thermoregulatory posture changes in the Heerman gull. Source: Bartholomew & Dawson, 1979.

Kentish plovers abandon their nests when exposed to high TA and solar intensity. This species rushes to a nearby water source to soak their ventral surface, quickly reducing their TB by convection. Although this raises the possibility that egg temperature will increase to dangerous levels in the absence of the individuals that are incubating the egg, overall this behavior allows the plovers to stay at their nests for longer periods (Amat & Masero, 2009). Adult birds and their chicks nesting in extreme environments such as the arctic tundra are exposed to long periods of sunlight along with low TA, low sun angles and unobstructed wind. By exposing more surface area (i.e. facing away from the sun), Greater Snow goose chicks, which have yellow down in comparison to the grey down and white feathers of older chicks and adults, are able to increase the amount of radiative heat gain. The plumage of younger goslings may even absorb solar radiation at a higher rate than adult plumage (Fortin et al., 2000). Grackle chicks exhibit shade seeking behavior, moving around the edges of the nest in attempts to keep their highly vascularized heads shaded. These chicks also orient their bodies toward the sun to diminish absorptive surface area which is a behavior also seen in chicks of Ferruginous hawks, gulls, and adult titmice and chickadees (Glassey & Amos, 2009; Tomback & Murphy, 1981 Bartholomew & Dawson, 1954 Wood & Lustick, 1989 in Glassey & Amos 2009 ). Moderating heat load is extremely important, especially by nestlings and small passerines, for without such behavior or access to shade in high TAs small birds can succumb to heat stress within 20 min (Glassey & Amos, 2009).

#### **3.3 Mammals**

Most species of mammals, particularly larger ones, are well insulated with fur, fat, or a combination of both. Often this creates conflicting thermoregulatory demands depending on the gradient between body and ambient temperature as well as environmental variables such as solar radiation, wind speed, humidity etc. A variety of behavioral responses to solar radiation exposure have evolved in mammals.

#### **3.3.1 Behavioral**

Many mammals use simple methods such as body orientation or posture changes to balance radiant heat gain from solar radiation. The black wildebeest, which inhabits the savannah, a habitat that has little natural shade, orients itself either parallel or perpendicular to the sun depending largely upon skin temperature. As the intensity of solar radiation increases, wildebeests are more likely to change their position when standing so their bodies are parallel to the sun's rays. By minimizing the surface area exposed to solar radiation in a parallel orientation, wildebeests absorb 30% less radiant heat than if they stood in a perpendicular stance (Maloney et al., 2005). The angle of the sun, both daily and seasonal, also affects wildebeest body orientation. During the cooler season, when solar angle and intensity is reduced, the preference of body orientation decreases. By reducing heat gain these large mammals are able to lessen the energy needed for evaporative cooling. However, this orientation behavior decreases when there is a reliable source of water available (Maloney et al., 2005). Other African species, such as the eland, blue wildebeest, and impala also use preferential body orientations, positioning their bodies parallel to the sun in summer and perpendicular in winter (Figure 4) (Hetem et al., 2011). Once again, energetic demands drive these behaviors relative to the amount of direct solar radiation.

Fig. 4 Proportion of observations (mean7SD) in which eland (open bars), blue wildebeest (hatched bars) and impala (black bars) orientated parallel, perpendicular and oblique to incident solar radiation in winter (left panels) and summer (right panels). The dotted line represents the proportion expected if orientation was random (0.25); significant differences between orientations indicated by \*P<0.05, \*\*P<0.01, \*\*\*P<0.001. Source: Hetem et al., 2011

nestlings and small passerines, for without such behavior or access to shade in high TAs

Most species of mammals, particularly larger ones, are well insulated with fur, fat, or a combination of both. Often this creates conflicting thermoregulatory demands depending on the gradient between body and ambient temperature as well as environmental variables such as solar radiation, wind speed, humidity etc. A variety of behavioral responses to solar

Many mammals use simple methods such as body orientation or posture changes to balance radiant heat gain from solar radiation. The black wildebeest, which inhabits the savannah, a habitat that has little natural shade, orients itself either parallel or perpendicular to the sun depending largely upon skin temperature. As the intensity of solar radiation increases, wildebeests are more likely to change their position when standing so their bodies are parallel to the sun's rays. By minimizing the surface area exposed to solar radiation in a parallel orientation, wildebeests absorb 30% less radiant heat than if they stood in a perpendicular stance (Maloney et al., 2005). The angle of the sun, both daily and seasonal, also affects wildebeest body orientation. During the cooler season, when solar angle and intensity is reduced, the preference of body orientation decreases. By reducing heat gain these large mammals are able to lessen the energy needed for evaporative cooling. However, this orientation behavior decreases when there is a reliable source of water available (Maloney et al., 2005). Other African species, such as the eland, blue wildebeest, and impala also use preferential body orientations, positioning their bodies parallel to the sun in summer and perpendicular in winter (Figure 4) (Hetem et al., 2011). Once again, energetic demands drive these behaviors relative to the amount of direct solar radiation.

Fig. 4 Proportion of observations (mean7SD) in which eland (open bars), blue wildebeest (hatched bars) and impala (black bars) orientated parallel, perpendicular and oblique to incident solar radiation in winter (left panels) and summer (right panels). The dotted line represents the proportion expected if orientation was random (0.25); significant differences between orientations indicated by \*P<0.05, \*\*P<0.01, \*\*\*P<0.001. Source: Hetem et al., 2011

small birds can succumb to heat stress within 20 min (Glassey & Amos, 2009).

**3.3 Mammals** 

**3.3.1 Behavioral** 

radiation exposure have evolved in mammals.

Marine mammals that haul out on land, such as the pinnipeds, face a thermoregulatory challenge when it comes to reproductive or molting periods. Developed for efficient locomotion and thermoregulation in an aquatic environment they often have thick fur, blubber, or a combination of both to protect them from frigid temperatures beneath the ocean surface. On land, however, these insulative properties, along with a low ratio of surface area to volume, become a hindrance to heat transfer across the body surface. The flippers of sea lions are long, hairless, and often thought to have a thermoregulatory function. South Australian fur seals, New Zealand and California sea lions respond to solar radiation by regulating the amount of flipper surface area that is exposed to solar radiation (Beentjes, 2006; Gentry, 1973). As temperature and solar intensity increases, sea lions unfold from a prone position with flippers tucked beneath their body to a dorsal up position with all four flippers laid out on the sand and exposed to the air for conductive and convective heat transfer (Figure 5) (Beentjes, 2006; Gentry, 1973).

Of course, the best method to inhibit solar radiation is to block or avoid it. Cape ground squirrels use their own tails to shade their bodies as well as orient themselves so that their backs are oriented toward the sun when the TA exceeds 40°C. TB is actually reduced over 5°C, allowing these squirrels to continue foraging for longer periods when exposed to direct solar radiation (Bennett et al., 1984). Male South Australian fur seals exhibit shade seeking behavior, not only blocking solar radiation but also transferring heat via conduction to a cool rocky substrate (Gentry, 1973). Marine mammals as large as the northern elephant seal, which periodically haul out on land, are able to use sand to block some of the solar radiation they would otherwise be subjected to during breeding or molting periods. This behavior known as sand-flipping, observed in some species of pinnipeds that use their fore-flippers to scoop sand up onto their backs, increases in New Zealand sea lions as solar radiation increases (Beentjes, 2006). The layer of moist and/or cooler sand facilitates heat transfer through conduction as well as creates a barrier against direct solar radiation. Southern sea lions have been observed to dig their foreflippers into the cool substrate to shield themselves from the sun's rays (Campagna & Le Boeuf, 1998). Flipper waving is another behavior often seen in several species of pinnipeds, exhibited by seals lying on their side, raising a flipper and sometimes moving it back and forth, using convection to diffuse heat from the body before letting it rest again. As solar radiation warms the substrate, heat gain increases through conduction and reflection, making behaviors such as posture changes, sandflipping, and flipper waving by hauled-out pinnipeds increasingly beneficial to their overall energy balance. For some pinnipeds, solar radiation is often an indirect or combined stressor when associated with TA and/or wind speed. Intense solar radiation, such as the levels recorded near the equator and other tropical regions, may only be tolerated if evaporative cooling is used, which may partially explain why tropical pinnipeds are often found near upwellings of cold water rather than in warm ocean currents.

Daily and seasonal migrations are often a result, at least in part, of solar radiation intensity. The marked ibex, which lives in arctic environments, has a low tolerance for heat gain. During the summer, males change their behavior, feeding mainly in the early morning rather than midday or evening. As solar radiation increases throughout the day, the marked ibex migrate to higher elevations, thus using the cooler air to reduce heat gain. Throughout the afternoon and evening, this species feeds in the cooler hours of the day before moving to higher altitude as TA increases (Aublet et al, 2009).

Fig. 5. Postures (prone, curled, oblique, ventral-up, and dorsal-up) used by New Zealand sea lions as solar radiation and ambient temperature increase. Source: Beentjes, 2006.

Seasonal migration can also be affected by solar radiation. Models using data collected over long periods or seasons are created to calculate the range of intensities of solar radiation over a large area such as a nature reserve or park. Collared pandas within Foping Nature Reserve, China have been radio tracked and their distributions in the park were overlaid with a map of 12 months of solar radiation data. During the warm months pandas moved to areas with lower solar radiation, whereas during the colder months they were recorded in areas of higher radiation. The model suggested that solar radiation does affect the distribution of giant pandas (Liu et al., 2011).

Smaller mammals are prone to losing heat rapidly due to their high ratio of surface area to volume but they are also susceptible to losing water through evaporation at a rapid rate. Degus, a species of rodent found in arid and semiarid environments, minimize the distances

Fig. 5. Postures (prone, curled, oblique, ventral-up, and dorsal-up) used by New Zealand sea

Seasonal migration can also be affected by solar radiation. Models using data collected over long periods or seasons are created to calculate the range of intensities of solar radiation over a large area such as a nature reserve or park. Collared pandas within Foping Nature Reserve, China have been radio tracked and their distributions in the park were overlaid with a map of 12 months of solar radiation data. During the warm months pandas moved to areas with lower solar radiation, whereas during the colder months they were recorded in areas of higher radiation. The model suggested that solar radiation does affect the

Smaller mammals are prone to losing heat rapidly due to their high ratio of surface area to volume but they are also susceptible to losing water through evaporation at a rapid rate. Degus, a species of rodent found in arid and semiarid environments, minimize the distances

lions as solar radiation and ambient temperature increase. Source: Beentjes, 2006.

distribution of giant pandas (Liu et al., 2011).

they travel out in the open, away from the shelter of scrub brush. One hypothesis for this behavior is predator avoidance, but another possibility is to avoid heat gain in areas subjected to direct solar radiation. Degus also exhibit seasonal changes in behavior, reducing activity near midday in summer while remaining steadily active during winter. Temperatures ≥30°C have not been measured in the microhabitat beneath the shrubs, preventing degus from reaching hyperthermic body temperatures while they remain sheltered from solar radiation. In order to both avoid predation and maintain efficient heat balance degus use the microhabitats underneath shrubs, especially during periods of high ambient temperature (Lagos et al., 1995).

Various species of bats roost in trees, exposed to sunlight and other environmental variables during day, unlike cave dwelling bats who are contained in a relatively stable microclimate and shielded from solar radiation. The wing membranes of bats, like sea lion flippers, are naked and incorporate a large amount of overall body surface area. This makes bat wings a likely tool for thermoregulation. Flying foxes, found mainly in the tropics, likely lack sweat glands and are exposed to the high temperatures and humidity of the forests they inhabit. These bats exhibit wing fanning and body licking, incorporating evaporation and convection to facilitate heat loss (Ochoa-Acuña & Kunz, 1999). Through exposure of greater amounts of wing surface, flying foxes can increase the area available for heat transfer as required during periods of increasing body and ambient temperature. Other species have special adaptations to aid them in releasing excess heat. The Brazilian free-tailed bat is known to fly during periods of daylight in the warmer environments it inhabits as well as taking part in long migrations. These bats have a unique vascular radiator lacking any insulative fur along their flanks (Reichard et al., 2010a). By flushing the area with warmed blood Brazilian free-tailed bats are able to efficiently dump heat when necessary while conserving body heat in the high altitudes they forage in by shunting blood away from the radiators (Reichard et al., 2010; Reichard et al., 2010b).

#### **3.3.2 Physiological**

Solar radiation is not only important when researching wild mammals but domesticated animals as well, especially livestock left out in large pastures with little to no shade. When cattle, goats, and sheep are exposed to the sun, they experience greater heat loads than those present in enclosed shelters or in shaded areas (Al-Tamimi, 2007; Brosh et al., 1998; Sevi et al., 2001). For some species of cattle, a high heat load during the summer results in reduced growth and reproductive rates, causing a decrease in overall productivity (Brosh et al., 1998). Dairy cows experience a decrease in fertility when under severe heat stress, more so in the summer than the winter (De Rensis & Scaramuzzi, 2003; Schütz et al., 2009). In addition to behaviors like shade-seeking, physiological responses such as increased respiration rate, heart rate, skin temperature, and of course high TB are often the first signs of heat stress resulting from direct solar radiation. Above the UCT, evaporation through respiratory and cutaneous water loss can aid in reducing TB. Blood vessels dilate near the skin surface allowing increased blood flow to areas that facilitate heat loss through multiple modes of heat transfer. This response is only efficient as long as blood temperature is less than TA; because it is the thermal gradient that drives heat loss across the skin barrier. Heat loss can be supplemented by behavioral changes such as feeding in the late afternoon or even at night so that the heat increment of feeding is produced during cooler periods, allowing heat loss through both conduction and radiation. Increased rates and total intake of water is often observed in livestock, compensating for the water lost through evaporation. Some species of goats and cattle are able to reduce their TBs in the early morning as a preparatory strategy for the increased amount of solar radiation they will be exposed to during the warmer parts of the day (Al-Tamimi, 2007; Brosh et al., 1998).

#### **3.3.2.1 Evaporation**

Many animals are able to use their own body parts, fluids, or environment to reduce heat absorption or expedite heat loss. Since water transfers heat 25X faster than air, metabolic as well as environmental water is used in evaporative cooling. It is beneficial to have an external water source nearby as the rate of body water turnover increases with solar radiation in most species, though at different levels depending on body mass and other characteristics (Figure 6) (King et al., 1975). Environmental water is an excellent source if available and many animals, including humans, use rivers, lakes, ponds, and the ocean to transfer excess heat. South Australian, Northern fur seals and Stellar sea lion females are able to tolerate solar radiation by keeping themselves wet, via mass movements to the shoreline while New Zealand sea lions immerse their hind flippers in tide pools or stay within the splash zone (Beentjes, 2006). Humans and other organisms that have sweat glands secrete the plasma portion of their blood onto the surface of their skin where it evaporates, the heat energy being used to transform liquid to gas. Organisms lacking sweat glands must devise other means of cooling their TB effectively. Dogs, cats, even sea lions, pant when they become overheated, using the evaporation of their saliva and moist tissue to dump heat. Kangaroos lick their own wrists where the skin is thinner and blood vessels are closer to the surface, aiding heat balance in the high solar and arid regions of Australia (Dawson et al., 2000). South Australian fur seal males unable to gain access to water due to territorial defense use their own urine for evaporatory cooling. After urinating on the rocks, males wet their ventral side and rear flippers, then lie on their side and raise a hindflipper into the air to enable convective heat loss. Female Stellar sea lions are often seen to huddle around small tidepools with increasing temperatures (Gentry, 1973).

Fig. 6. Relation between daily total body water turnover and solar radiation in domestic Eland and oryx under African ranching conditions. Source: King et al., 1975.
