Part 8

MINIMUM THERMAL CONDUCTANCE

Background

Thermal conductance is a measure of the ease with which heat is passively transferred to or from a body through its tissues and pelt. Within T{n}, a mammal is able to vary its thermal conductance over a wide range of values by changing heat transfer characteristics of both of these layers. Minimum thermal conductance occurs when total heat transfer through these layers is reduced to its lowest possible rate. This minimum value, which is the reciprocal of maximum resistance, occurs, theoretically, but not always practically (see McNab, 1988b), at the animal's T{lc} and is best estimated under standard conditions in a metabolism chamber (McNab, 1980b; Aschoff, 1981). Minimum thermal conductance scales to body mass (McNab and Morrison, 1963; Herreid and Kessel, 1967; McNab, 1970, 1979b; Bradley and Deavers, 1980; Aschoff, 1981). Therefore, to make comparisons between species of various sizes, we scaled out body mass by expressing C{mw} as the ratio of measured to predicted values (C{mwr}; Table 7). These ratios were used to make comparisons of heat-transfer characteristics between species that occupy different habitats or climates.

Effect of Molt on Thermal Conductance

In summer, T{lc}'s of male and female Procyon lotor (Figure 2) were very similar to those of other procyonids (22°C-26°C; Table 7). In winter, T{lc} of both sexes shifted downward to 11°C (Figure 3). This seasonal shift in T_{lc} occurred as the result of a seasonal change in minimum thermal conductance (Table 3). For many northern mammals, a seasonal change in thermal conductance is partly mediated via cyclic changes in the insulative quality of their pelt (Scholander et al., 1950a; Irving et al., 1955; Hart, 1956, 1957; Irving, 1972:165).

Procyon lotor begins to shed its heavy winter coat about the time its young are born. Molt progresses through summer and by late August the new coat is complete (Stuewer, 1942). During its summer molt, Procyon lotor's C{mw} increased by about 49% over the value for female raccoons in winter (Table 3). In summer, therefore, it had the highest mass specific C{mw} of those procyonids considered (C{mwr} = 1.77 and 1.79; Table 7). An increase in thermal conductance facilitates passive heat loss for temperate and arctic species, and this serves as an important thermoregulatory adaptation during warm summer months (Scholander et al., 1950c; Irving et al., 1955; Hart, 1956, 1957; Irving, 1972:165). This adaptation is particularly important to those temperate- and arctic-zone species (including raccoons) whose [.H]{b}'s do not decrease during summer (Irving et al., 1955). From August on, the fur of Procyon lotor becomes increasingly longer and heavier, with peak, or prime, condition occurring in late fall and early winter (Stuewer, 1942). Minimum conductance of our captive raccoons was lowest in winter (C{mwr} = 1.15) when their pelts were in prime condition (Tables 3, 7). Because "primeness" of raccoon pelts varies geographically, thicker pelts being associated with colder climates (Goldman, 1950:21; Whitney and Underwood, 1952:24-41), the degree of seasonal change in C{mw} must also vary geographically.

The only other procyonid for which a seasonal molt has been described is Bassariscus astutus. Molt in this species extends from late summer to late fall (Toweill and Toweill, 1978). How molt effects thermal conductance in Bassariscus astutus is not known because metabolic data for this species (Table 7) apparently were collected only when their pelts were in prime condition (Chevalier, 1985).

Goldman (1950:20) reports that Procyon cancrivorus does not have a seasonal molt. Like other tropical procyonids, Procyon cancrivorus lives in an environment that has the following characteristics: high even temperatures throughout the year (1°C-13°C difference in monthly mean temperature), a greater range in temperature between day and night than in mean monthly temperature throughout the year, uniform lengths of day and night, seasonal variation in rainfall, and lowest temperatures during the rainy season(s) (Kendeigh, 1961:340). In such a stable environment there would be no advantage to a sharply defined seasonal molt cycle that could place an animal in thermoregulatory jeopardy by increasing its thermal conductance. This would be particularly true for animals like tropical procyonids that have lower than predicted [.H]_{b}'s but that maintain typical eutherian body temperatures (Table 7). Consequently, molt in all tropical procyonids may either be prolonged or continuous. This is a feature of their biology that needs to be examined in more detail.

Comparison of Thermal Conductances

Procyon lotor VERSUS TROPICAL PROCYONIDS.--C{mwr} for Procyon lotor in winter was 1.15, which is similar to the values for Potos flavus and Procyon cancrivorus, 1.02 and 1.25, respectively (Table 7). These two tropical species, therefore, have C{mw}'s that are similar on a mass specific basis to the value for Procyon lotor in winter. However, at their T{lc}'s, the thermal gradient sustained by these tropical animals is only about 11°C, whereas for Procyon lotor in winter it was 26.5°C. Examination of Eq. 4 with respect to these thermal gradients suggests that tropical procyonids achieve such low C{mw}'s by virtue of their lower than predicted [.H]{b}'s rather than by having pelts that are exceptionally good insulators. In fact, the insulation afforded by the pelts of these tropical procyonids is about the same as that of the 50 g arctic lemming, Dicrostonyx groenlandicus rubricatus, whose coat has an insulative value that is about half that of the hare, Lepus americanus, red fox, Vulpes fulva alascensis, and pine martin, Martes americana, animals comparable in size to these procyonids (Scholander et al., 1950a). Therefore, pelts of these tropical procyonids do not have the same insulative value as the prime winter coat of Procyon lotor_.

Nasua narica and Nasua nasua have tropical and subtropical distributions and they are the only procyonids that are diurnal (Kaufmann, 1962:103-105, 1982, 1987). Because they are active during the day they experience a more extreme thermal environment (higher T{a}'s and solar radiation) than their nocturnal cousins. Values of C{mwr} for Nasua narica (1.45 and 1.55) and Nasua nasua (1.24 and 1.65) are higher than those for Procyon cancrivorus or Potos flavus (Table 7). Thus, these coatis have higher mass specific C{mw}'s than their nocturnal tropical cousins. A high C{mw} reduces the cost of thermoregulation in hot environments because it increases an animal's ability to lose excess heat passively. The higher C_{mw}'s of these coatis serve as an adaptation that contributes to the success of their diurnal life style as well as their ability to expand their habitat use to areas with less thermal stability, such as oak and pine woodlands and deserts.

Bassariscus astutus.--This species has the lowest mass specific C{mw} of these procyonids (C{mwr} = 0.85; Table 7), which indicates that its pelt has a greater insulative value than the coats of Potos flavus, Procyon cancrivorus, Nasua nasua, or Nasua narica. This, coupled with a lower than predicted [.H]{b}, allows Bassariscus astutus to maintain T{b} with less energy expenditure than is possible for any other procyonid of comparable size; and this combination of adaptations provides Bassariscus astutus with a distinct energy advantage in environments that have low productivity (Wang et al., 1973). The evolution of a pelt that provides better insulation must be considered an important contributing factor for the spread of this species into desert regions of the western United States.

THERMOREGULATION AND USE OF STORED FAT AT LOW TEMPERATURES

Background

THERMOREGULATION.--At temperatures below a mammal's T{n}, heat loss exceeds [.H]{b}. To maintain T{b} under these conditions, metabolic rate must be increased (Eq. 4). Procyon lotor in summer during its annual molt (Table 5; Figure 2), Bassariscus astutus (Chevalier, 1985), Nasua nasua (Chevillard-Hugot et al., 1980; Mugaas et al., in prep.), Nasua narica (Scholander et al., 1950b; Mugaas et al., in prep.), and Potos flavus (Müller and Kulzer, 1977; Müller and Rost, 1983) all are able to elevate their metabolic rates by 130% above basal when they are exposed to T{a} = 0°C. Procyon cancrivorus responds to 0°C with an increase in metabolic rate of 257% above basal (Scholander et al., 1950b). All animals listed have about the same T{lc} and T{b}, so the temperature differential producing this response is about the same for each species. Metabolic ability to defend body temperature against low ambient temperatures, therefore, is well developed in these procyonids. Such large increases in metabolic rate are energetically expensive, and if these animals were routinely exposed to T{a} = 0°C, it would be difficult for them to acquire enough food each day to maintain endothermy. Raccoons in winter pelage, however, need only elevate their metabolic rate by 47% above basal to maintain endothermy at T{a} = 0°C (Table 5; Figure 3). Each year at the completion of its molt, the raccoon's highly insulative pelt is renewed. This lowers their T{lc} by 9°C to 15°C below that measured for them in summer (Figure 3) and decreases their cost of thermoregulation at low temperatures. The increased insulative capacity of their pelt is one of the primary adaptations that has allowed Procyon lotor_ to extend its distribution into cold climates.

STORED FAT.--Cyclic fattening is an integral and important part of a raccoon's annual cycle (Mugaas and Seidensticker, ms); however, it has not been reported for other procyonids. During winter in parts of the United States and Canada, raccoons are confined to their dens for variable periods of time (days to months) depending on the severity of the weather (Stuewer, 1943:223-225; Whitney and Underwood, 1952:108-116; Sharp and Sharp, 1956; Mech et al., 1968; Schneider et al., 1971). During this confinement, they do not hibernate but rather enter a state of "dormancy" and become inactive. While dormant they remain endothermic (T_{b} > 35°C; Thorkelson, 1972:87-90) and derive most of their energy requirement from fat reserves accumulated during fall. The rate at which fat stores are consumed during winter dormancy depends on the thermoregulatory requirement imposed on them by local weather conditions, the insulative quality of their pelt, and any advantage they may gain by seeking shelter in a den.

Thermal Model of the Raccoon and Its Den

Heat transfer between an animal and its environment is a function of the interaction of its body temperature and thermal conductance with various environmental variables (air temperature, wind speed, vapor pressure, and thermal radiation). When a raccoon is outside its den, its thermal conductance (C{mw}) is the only barrier to heat transfer with the external environment. However, when it enters a tree den, a raccoon imposes two other thermal barriers between itself and the external environment: (1) conductance of the air space between its fur and the den's walls (C{a}) and (2) conductance of the den's walls (C{d}; Thorkelson, 1972:59-63; Thorkelson and Maxwell, 1974). Thorkelson and Maxwell (1974) modeled heat transfer of a simulated raccoon (a water-filled aluminum cylinder equipped with a heater and covered with a raccoon pelt) in a closed tree den. In their system, 65% of resistance to heat flux was attributable to the pelt, whereas the remainder (35%) was due to C{a} and C{d}. Because resistance is the inverse of conductance, and resistances for the raccoon and its den are arranged in series, we can estimate total conductance (C{t}) of this system with Eq. 7.

1/C{t} = 1/C{mw} + 1/C{a} + 1/C{d} Eq. 7

Minimum thermal conductance C{mw} for raccoons in winter was 0.0172 mL O{2}·g^{-1}·h^{-1}·°C^{-1} (Table 3). Based on Thorkelson and Maxwell's (1974) model we let 1/C{mw} = 0.65(1/C{t}) = 1/0.0172 mL O{2}·g^{-1}·h^{-1}·°C^{-1}, and 1/C{a} + 1/C{d} = 0.35(1/C{t}). Substituting these values into Eq. 7 and solving for C{t} yields 0.0112 mL O{2}·g^{-1}·h^{-1}·°C^{-1}, a value that is 35% lower than that of the animal alone. Substituting this value and the value for basal metabolism of winter raccoons (0.47 mL O{2}·g^{-1}·h^{-1}; Table 7) into Eq. 4 and solving for (T{b} - T{a}) yields a new temperature differential of 42°C. Therefore, by using tree dens, raccoons in north central Virginia, with T{b} = 37°C (Figure 7), could effectively reduce their T_{lc} from 11°C to -5°C and markedly reduce their metabolic cost of thermoregulation.

Metabolic Advantage of the Den

Given prevailing winter temperatures in north central Virginia (see "Materials and Methods"), adult raccoons in that area should be able to sustain endothermy most of the time they are in their dens by simply maintaining [.H]{b}. Depending on the mass of their stored fat, they could remain in their dens for several weeks without eating (Mugaas and Seidensticker, ms). The thermal advantage of a den could be further enhanced during colder temperatures if two or more raccoons occupied it at the same time and huddled together, and/or if these animals could reduce C{mw} even more by lowering T{b} and cooling their extremities. Although we do not have any data to verify the second mechanism, there are many accounts in natural history literature that document raccoons occupying dens together (Lotze and Anderson, 1979). This habit could be particularly important for the young of the year and may be one reason why they often continue to den with their mothers during winter (Lotze and Anderson, 1979; Seidensticker et al., 1988). Raccoons that live in colder climates, such as Minnesota, undoubtedly obtain the same advantage from a den as Virginia animals, but because of their greater body mass, longer fur, and potentially lower C{mw}, T_{lc} of a Minnesota raccoon in a den could be even lower than what we calculated for Virginia raccoons. Therefore, when they are in their dens, raccoons living in very cold climates also may be able to maintain homeothermy with a basal level of metabolism.

THERMOREGULATION AT HIGH TEMPERATURES

Background

In hot environments mammals depend on behavior to minimize their thermal load (escape to shaded or cooler microclimates, use posture and orientation to wind and sun, restrict activity, become nocturnal, etc.) and on evaporative water loss to rid themselves of excess heat. With regard to evaporative heat loss, Calder and King (1974:326) arbitrarily subdivided the response to various T_{a}'s as follows: "(1) cool temperatures at which water loss should be minimized, both to reduce heat loss and as an adaptation to terrestriality; (2) an intermediate temperature range wherein evaporation is gradually increased as dry heat losses are proportionately reduced with smaller thermal gradients; and (3) warm to hot temperatures at which evaporation must be actively increased to dispose of metabolic and exogenous heat loads." Some mammals are able to thermoregulate very well at high ambient temperatures via panting or sweating, whereas others have a very limited capacity. Hence, there is no general approach to calculating evaporative water loss under these conditions (Campbell, 1977:85). However, the ratio of evaporative heat lost to metabolic heat produced can be used to quantify a species' capacity for evaporative cooling and to make comparisons between species.

Comparison of Procyonid Responses to Heat Stress

Potos flavus.--This species lives in Neotropical forests of Central and South America. It is nocturnal, arboreal in habit, and appears to be the most heat-sensitive of these procyonids. Its T{uc} is at 30°C to 33°C (Table 7; Müller and Kulzer, 1977; Müller and Rost, 1983). It begins to pant at about 30°C, but its efforts at evaporative cooling are very ineffective. At 33°C Potos flavus can dissipate 33% of its metabolic heat via evaporative water loss, but at 35°C the efficiency of this mechanism falls to 20% (Müller and Rost, 1983). Consequently, when exposed to T{a}'s above 33°C, any kind of excitement causes its T_{b} to rise rapidly in an uncontrolled manner (Müller and Kulzer, 1977; Müller and Rost, 1983). These animals rely on their nocturnal and arboreal habits to keep them out of situations that could lead to hyperthermia (Müller and Kulzer, 1977; Müller and Rost, 1983).

Nasua nasua and Nasua narica.--Nasua nasua is abundant in tropical and subtropical South America, whereas Nasua narica occupies the same climates in North America from southern Arizona and New Mexico south through Panama and on into Colombia and Ecuador (Hall and Kelson, 1959:892; Ewer, 1973:391, 392; Poglayen-Neuwall, 1975). Both coatis are diurnal and forage primarily on the ground (Kaufmann, 1962:185-188, 1987; Poglayen-Neuwall, 1975; Nowak and Paradiso, 1983:982), consequently they are exposed to a more severe thermal environment while active (higher T{a}'s and solar radiation) than are nocturnal procyonids. Both coatis are more heat-tolerant than Potos flavus; their T{uc}'s are higher (33°C-35°C; Table 7), they can tolerate T{a}'s of 35°C without raising their T{b}'s (Chevillard-Hugot et al., 1980; Mugaas et al., in prep.), and they have a greater capacity for evaporative cooling than Potos flavus (Mugaas et al., in prep.). The greater heat tolerance of these coatis is compatible with their diurnal habits and widespread distribution in a variety of forest habitats in both tropical and subtropical areas of the western hemisphere.