summer - evap water loss vs tempFigure 4.—Relationship between evaporative water loss and chamber air temperature for raccoons in summer: captive females, open circles; captive males, closed circles; trapped males, open squares. Lines represent polynomial regressions of evaporative water loss on chamber air temperature.
Figure 4.—Relationship between evaporative water loss and chamber air temperature for raccoons in summer: captive females, open circles; captive males, closed circles; trapped males, open squares. Lines represent polynomial regressions of evaporative water loss on chamber air temperature.
winter - evap water loss vs tempFigure 5.—Relationship between evaporative water loss and chamber air temperature for raccoons in winter: captive females, open circles; captive males, closed circles. Lines represent polynomial regressions of evaporative water loss on chamber air temperature.
Figure 5.—Relationship between evaporative water loss and chamber air temperature for raccoons in winter: captive females, open circles; captive males, closed circles. Lines represent polynomial regressions of evaporative water loss on chamber air temperature.
Table 4.—Polynomial regression equations describing evaporative water loss (mg·g-1·h-1) ofProcyon lotorin summer and winter (X = chamber temperature (°C), Y = evaporative water loss, n = number of observations, R2= coefficient of determination, and SEE = standard error of estimate).
Thermoregulation at Low Temperatures
Body Temperature
Body temperatures inFigure 6are those recorded during metabolic measurements from animals equipped with surgically implanted, temperature-sensitive radio transmitters. Each point was recorded during the lowest level of oxygen consumption at each Ta. In both summer and winter, Tb's were lowest during metabolic measurements at Ta's around Tlc. At Ta's below Tlc, Tb's increased (Figure 6), which is an unusualresponse. Under similar conditions, other procyonids either maintain a nearly constant Tbor allow it to fall slightly (Müller and Kulzer, 1977; Chevillard-Hugot et al., 1980; Müller and Rost, 1983; Chevalier, 1985). For our raccoons, confinement in the metabolism chamber at low temperatures must have stimulated a greater than necessary increase in metabolic rate such that heat production exceeded heat loss, which caused Tbto become elevated.
body temp vs air tempFigure 6.—Relationship between body temperature and chamber air temperature in summer (panel A), and winter (panel B): captive females, open circles and solid lines; captive males, solid circles and dashed lines. Solid vertical lines represent lower critical temperatures.
Figure 6.—Relationship between body temperature and chamber air temperature in summer (panel A), and winter (panel B): captive females, open circles and solid lines; captive males, solid circles and dashed lines. Solid vertical lines represent lower critical temperatures.
Table 5.—Regression equations describing oxygen consumption(mL O2·g-1·h-1)ofProcyon lotorat temperatures below their lower critical temperature (I = x-intercept (°C), n = number of observations, R2= coefficient of determination, SEE = standard error of estimate for the y-intercept (a) and slope (b), X = chamber temperature (°C), and Y = oxygen consumption).
Summer
During summer, Tlcfor male raccoons was 20°C, whereas for females it was 25°C (Figure 2). Regression equations calculated to describe oxygen consumption at Ta's below Tlcare presented inTable 5. For three groups of summer animals, slopes of regressions are identical. This indicates that minimum conductances of these three groups were equivalent. Intercepts of these equations are different, which suggests a difference in metabolic cost of thermoregulation between these groups (Figure 2); captive males had a lower intercept than either trapped males (p<0.005) or captive females (p<0.05), but there was no difference in intercepts of captive females and trapped males. These regression equations, therefore, also were derived using values of oxygen consumption expressed in terms of metabolic body mass (Mellen, 1963). Relationships between intercepts of these equations are different than those for regressions inTable 5. Intercept for females was intermediate to, and not different from, those of the two groups of males. However, captive males still had a lower intercept than trapped males (p<0.025). Thus, in summer, thermoregulatory metabolism was less expensive for captive than for trapped males, and in spite of a 5°C difference in their Tlc's (Figure 2), captive males and females had similar thermoregulatory costs.
Regression lines for three groups of animals in summer extrapolate to zero metabolism at values equivalent to, or greater than, normal Tb; 38.8°C for trapped males, 37.6°C for captive males, and 41.1°C for captive females (Table 5). Thus, all three groups had minimized thermal conductance at Ta's below Tlc(Scholander et al., 1950b; McNab, 1980b). Minimum wet thermal conductance calculated for raccoons in summer withEq. 4(Table 3) is numerically similar to these "slope" values (Table 5), and it was, therefore, considered to be the best estimate of CmwforProcyon lotorduring that season(0.0256 mL O2·g-1·h-1·°C-1).
Winter
During winter Tlcfor both sexes decreased to 11°C (Figure 3). Regression equations of thermoregulatory metabolism for males and females in winter are not different from each other in either slope or intercept. These data, therefore, were combined into a single equation (Table 5). Slope and intercept of this equation are both lower (p<0.005 and p<0.05, respectively) than those for summer animals (Table 5). Identical results were obtained from comparisons using regressions derived from oxygen consumption expressed in terms of metabolic body mass (Mellen, 1963). Thermoregulatory costs at any temperature below 20°C were lower for winter than summer animals (Figures 2,3).
Table 6.—Regression equations describing oxygen consumption(mL O2·g-1·h-1)ofProcyon lotorat temperatures below their lower critical temperature in winter (A = females with radio transmitters, B = females without radio transmitters, C = males, I = x-intercept (°C), n = number of observations, R2= coefficient of determination, X = chamber temperature (°C), and Y = oxygen consumption).
body temp vs time of dayFigure 7.—Relationship between body temperature and time of day at various months of the year: captive females, open circles; captive males, closed circles. Vertical cross-hatched areas represent civil twilight.
Figure 7.—Relationship between body temperature and time of day at various months of the year: captive females, open circles; captive males, closed circles. Vertical cross-hatched areas represent civil twilight.
The regression line forProcyon lotorin winter (Table 5) extrapolates to zero metabolism at 35.2°C, which is below normal Tb(Figures 6,7). This suggests that not all raccoons measured in winter minimized thermoregulatory metabolism or conductances at Ta's below Tlc(Scholander et al., 1950b; McNab, 1980b). To assess this possibility, data for these animals were divided into three groups: (A) females with radio transmitters, (B) females without radio transmitters, and (C) males (Table 6). Regression equations of metabolism below Tlcwere derived for each group, and based on extrapolated Tb's at zero metabolism, only the two females with implanted radio transmitters (group A) minimized thermoregulatory metabolism and conductance. Had animals in groups B and C also minimized their thermal conductances, while retaining their measured metabolic rates, their rates of heat production would have been disproportionately higher than their rates of heat loss. Equation 4 predicts that under these conditions their body temperatures would have been elevated to 42.0°C and 40.4°C, respectively. Thus, in order to avoid such a large increase in body temperature, animals in groups B and C increased their thermal conductances in preference to lowering their metabolicrates. The regression equation of thermoregulatory metabolism for all winter animals (Table 5), therefore, overestimates minimum metabolic cost of temperature regulation below Tlc, and its slope underestimates Cmw. Consequently, the best estimate of CmwforProcyon lotorin winter is the value calculated for group A animals withEq. 4(0.0172 mL O2·g-1·h-1·°C-1;Table 3), and the minimum cost of thermoregulatory metabolism at any Tabelow Tlcis best estimated by substituting this value intoEq. 4and solving for Ḣr.
Thermoregulation at High Temperatures
Body Temperature
In both summer and winter, Tb's increased during metabolic measurements at Ta's above Tlc(Figure 6). This response also was seen during metabolic measurements conducted on other procyonids (Müller and Kulzer, 1977; Chevillard-Hugot et al., 1980; Müller and Rost, 1983; Chevalier, 1985).
Summer
During summer our data suggested that the upper critical temperature (Tuc) was higher than 35°C. The lowest rates of oxygen consumption at Ta= 35°C occurred after 1.5 to 2.5 hours of exposure to that temperature. Prolonged exposure to this temperature in summer did not make animals restless, and their rate of oxygen consumption was very stable throughout each measurement. Body temperature responses at Ta= 35°C were recorded from two males and two females that had implanted radio transmitters. With the exception of one male, Tb's were maintained near 38°C (Figure 6). The one exception (a male) maintained its Tbat 39.3°C. At Ta= 35°C, summer males had rates of evaporative water loss that were lower than those of summer females (Figure 4). At this temperature, males dissipated 35% ± 6% and females 56% ± 18% of their metabolic heat via evaporative water loss. Thus, at Ta= 35°C, males must have utilized modes of heat transfer other than evaporative cooling (convective and conductive heat transfer) to a greater extent than females.
Winter
Body temperature, evaporative water loss, and metabolic data indicated that, in winter, Tucwas very close to 35°C. In winter, the lowest level of oxygen consumption was recorded during the first hour after the chamber had reached Ta= 35°C. Unlike summer, animals became restless after the first hour at 35°C, at which point their oxygen consumption increased and showed a high degree of variability. Body temperature responses at 35°C were recorded from both females that had implanted radio transmitters. In one case, Tbrose from 37.9°C at the end of the first hour to 40.5°C by the end of the second hour, and as it did not show signs of leveling off, we terminated the experiment. We exposed that same animal to Ta= 35°C one other time during winter. In that instance, its Tbrose to 40.0°C during the first 30 minutes and was maintained at that level for three hours with no apparent distress. The other female elevated its Tbfrom 37.3°C to 39.0°C during the second hour at Ta= 35°C and maintained its Tbat that level for two hours. Thus, during winter, prolonged exposure to Ta= 35°C stimulated more of an increase in Tbthan it did in summer. During winter, both males and females increased evaporative water loss at Ta= 35°C (Figure 5) but only to the extent that they dissipated 35% ± 10% of their metabolic heat production. Thus, even in winter, convective and conductive heat transfers were still the most important modes of heat loss at this temperature.
Daily Cycle of Body Temperature
The daily cycle of raccoon Tb's during summer and winter are presented inFigure 7. In general, Tb's showed a marked circadian cycle in phase with photoperiod. Tb's rose above 38°C for several hours each night but remained below 38°C during daytime. During summer, with the exception of one female whose record was not typical (Figure 7), Tb's rose above 38°C shortly after sunset, whereas in winter Tb's did not rise above 38°C until several hours after sunset. Once Tbwas elevated it usually remained so until just before or after sunrise (Figure 7). During summer, Tbwas above 38°C for 85% or more of the time between sunset and sunrise (87% for the female with the typical body temperature pattern, and 85% and 98% for males), whereas in winter it was elevated for only 47%-78% of the time between sunset and sunrise (47% and 61% for females, and 67% and 78% for males). During night, Tbwould oscillate between 38°C and about 39°C, such that two peak values occurred. These peak values presumably corresponded to two periods of heightened nighttime activity. During summer, one of these peaks occurred before and the other after 24:00 hours, whereas in winter both peaks occurred after 24:00 hours. With the exception of one female in winter (Figure 7), the lowest Tbof the day for both sexes was near 37°C, and this typically occurred during daytime (Figure 7).
Discussion
Basal Metabolic Rate
Background
Basal metabolism represents the minimum energy required by a mammal to maintain endothermy and basic homeostasis (Lusk, 1917:141; Kleiber, 1932, 1961:251; Benedict, 1938:191-215; Brody, 1945:59; Robbins, 1983:105-111). Mammals with lower than predicted Ḣbmaintain endothermy and enjoy its attendant advantages at a discount, whereas others, with rates that are higher than predicted, pay a premium(Calder, 1987). Such variation in Ḣbappears to be tied to ecological circumstances rather than taxonomic affinities (Vogel, 1980; McNab, 1986a, 1988a, 1989), and depending on environmental conditions, each rate provides an individual with various advantages and limitations. During the course of evolution, therefore, each species' Ḣbevolves to provide it with the best match between its energy requirements for continuous endothermy, its food supply, and the thermal characteristics of its environment.
Captive versus Wild Raccoons
Male raccoons trapped in summer had higher Ḣb's than our captive animals in any season (Table 2). The higher rate of metabolism of these trapped males could have been due to the stress of captivity or to the fact that "wild" animals actually may have higher metabolic rates than those that have adjusted to captivity. If the latter is true, then our data for captive animals underestimated the actual energy cost of maintenance metabolism forProcyon lotorin the wild. At present, we have no way of determining which of these alternatives is true.
Seasonal Metabolism of Raccoons
In some temperate-zone mammals, Ḣbis elevated in winter, which presumably increases their "cold-hardiness." Conversely, lower summer metabolism is considered to be a mechanism that reduces the potential for heat stress. Such seasonal variation in Ḣbhas been found in several species: collard peccary,Tayassu tajacu(Zervanos, 1975); antelope jackrabbit,Lepus alleni(Hinds, 1977); desert cottontail,Sylvilagus audubonii(Hinds, 1973); and, perhaps, cold-acclimatized rat,Rattus norvegicus(Hart and Heroux, 1963). Unlike these species, our captive raccoons showed no seasonal variation in Ḣb(Table 2). Instead, raccoons achieved "cold-hardiness" in winter and reduced their potential for heat stress in summer with a large seasonal change in thermal conductance (Table 3).
Table 7.—Metabolic characteristics of several procyonid species.
[a]Meas is measured basal metabolism(mL O2·g-1·h-1).Hbris the ratio of measured to predicted basal metabolism where the predicted value is calculated from Ḣb= 3.42·m-.25(Kleiber, 1932, 1961:206) and m is body mass in grams.[b]Meas is measured minimum thermal conductance(mL O2·g-1·h-1·°C-1).Cmwris the ratio of measured to predicted minimum thermal conductance where the predicted value is calculated from Cm= 1.0·m-0.5(McNab and Morrison, 1963; Herreid and Kessel, 1967), and m is body mass in grams.[c]Tbis body temperature during the active (α) and rest (ρ) phases of the daily cycle (°C).[d]Tnis the thermoneutral zone as defined by the lower (Tlc) and upper (Tuc) critical temperatures (°C).[e]Conductance calculated as the slope of the line describing oxygen consumption at temperatures below the lower critical temperature.[f]Conductance calculated from Cmw= Ḣr/(Tb- Ta), where Ḣris resting metabolic rate at temperatures below Tlc, and other symbols are as described elsewhere.[g]Inactive-phase thermal conductance: estimated from Scholander et al. (1950b), assuming that active-phase thermal conductance is 52% higher than values determined during the inactive phase (Aschoff, 1981).
Comparison of Procyon lotor with Other Procyonids
Procyon lotorhas a much higher mass-specific Ḣbthan other procyonids (Table 7). To quantify the magnitude of this difference, we compared the measured value forProcyon lotorwith one calculated for it from a mass-specific least-squares regression equation (Eq. 6; R2= 0.78) derived from data for those procyonids with lower than predicted Ḣb:Potos flavus,Procyon cancrivorus,Nasua nasua,Nasua narica, andBassariscus astutus(Table 7).
Ḣbin Eq. 6 is basal metabolism(mL O2·g-1·h-1)and m is body mass (g). Measured values of ḢbforProcyon lotorwere 1.45 to 1.86 times greater than those predicted for it by Eq. 6 (Table 8).
Table 8.—Basal metabolism(mL O2·g-1·h-1)ofProcyon lotoras predicted byEq. 6(Ḣb= 2.39·m-0.25). Body masses, used to calculate predicted values, and measured values were taken fromTable 7.
Season and sexPredictedMeasured/PredictedSummerTrapped male0.291.86Captive male0.291.59Captive female0.291.45WinterCaptive male0.281.68Captive female0.291.59
Influence of Diet on Basal Metabolism
Background.—With respect to Ḣb, McNab (1986a:1) maintains that "the influence of climate is confounded with the influence of food habits," and that departures from the Kleiber (1961) "norm" are best correlated with diet. Although this does appear to be the case for diet specialists, the analysis is not so clear-cut for omnivorous species (McNab, 1986a). His analysis also indicates that an animal's "behavior" (i.e., whether it is terrestrial, arboreal, subterranean, aquatic, etc.), secondarily modifies the influence of food habits on Ḣb. For example, terrestrial frugivores have Ḣb's that are very near predicted values, whereas arboreal frugivores have rates that are much lower than predicted (McNab, 1986a).
Table 9.—Food habits of some Procyonids. References for foods were as follows:Potos flavus,Procyon cancrivorus, andNasua nasuataken from Bisbal (1986);Nasua naricataken from Kaufmann (1962:182-198);Bassariscus astutustaken from Martin et al. (1951), Taylor (1954), Wood (1954), Toweill and Teer (1977), and Trapp (1978);Procyon lotortaken from Hamilton (1936), Stuewer (1943:218-220), Stains (1956:39-51), and Greenwood (1981). Symbols represent either qualitative (#) or quantitative (+, †) assessments of feeding habits: # indicates that the animal was observed eating the food; + and † represent volume and frequency, respectively, of food utilization. No attempt was made to account for seasonal variation in the use of these foods.