Part 4

Body temperature, evaporative water loss, and metabolic data indicated that, in winter, T_{uc} was very close to 35 deg.C. In winter, the lowest level of oxygen consumption was recorded during the first hour after the chamber had reached T_{a} = 35 deg.C. Unlike summer, animals became restless after the first hour at 35 deg.C, at which point their oxygen consumption increased and showed a high degree of variability. Body temperature responses at 35 deg.C were recorded from both females that had implanted radio transmitters. In one case, T_{b} rose from 37.9 deg.C at the end of the first hour to 40.5 deg.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 T_{a} = 35 deg.C one other time during winter. In that instance, its T_{b} rose to 40.0 deg.C during the first 30 minutes and was maintained at that level for three hours with no apparent distress. The other female elevated its T_{b} from 37.3 deg.C to 39.0 deg.C during the second hour at T_{a} = 35 deg.C and maintained its T_{b} at that level for two hours. Thus, during winter, prolonged exposure to T_{a} = 35 deg.C stimulated more of an increase in T_{b} than it did in summer. During winter, both males and females increased evaporative water loss at T_{a} = 35 deg.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 T_{b}'s during summer and winter are presented in Figure 7. In general, T_{b}'s showed a marked circadian cycle in phase with photoperiod. T_{b}'s rose above 38 deg.C for several hours each night but remained below 38 deg.C during daytime. During summer, with the exception of one female whose record was not typical (Figure 7), T_{b}'s rose above 38 deg.C shortly after sunset, whereas in winter T_{b}'s did not rise above 38 deg.C until several hours after sunset. Once T_{b} was elevated it usually remained so until just before or after sunrise (Figure 7). During summer, T_{b} was above 38 deg.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, T_{b} would oscillate between 38 deg.C and about 39 deg.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 T_{b} of the day for both sexes was near 37 deg.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 [.H]_{b} maintain 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 [.H]_{b} appears 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' [.H]_{b} evolves 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 [.H]_{b}'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 for _Procyon lotor_ in 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, [.H]_{b} is 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 [.H]_{b} has 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 [.H]_{b} (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.

+------------------------------------------------ |Body Basal[a] Minimum[b] Species |mass metabolism conductance T_{b}[c] |(g) ------------ ------------- ------------- | Meas H_{br} Meas C_{mwr} [alpha] [rho] ---------------------+------------------------------------------------ _Bassariscus astutus_| 865 0.43 0.68 0.0288[e] 0.85 37.6 23 _Procyon cancrivorus_|1160 0.40 0.69 0.0368[e] 1.25 _Potos flavus_ |2030 0.36 0.51 _Potos flavus_ |2400 0.32 0.65 38.1 36.0 _Potos flavus_ |2600 0.34 0.71 0.0200[f] 1.02 _Nasua nasua_ |3850 0.26 0.60 0.0200[f] 1.24 38.3 36.4 _Nasua nasua_ |4847 0.33 0.79 0.0238[e] 1.65 39.1 37.9 _Nasua narica_ |5554 0.25 0.62 0.0208[e] 1.55 38.9 37.4 _Nasua narica_ |4150 0.42 1.20 0.0341[e] 2.20 | 0.0224[g] 1.45 _Procyon lotor_ | Summer | Trapped male |4400 0.54 1.28 Captive male |4790 0.46 1.07 0.0256[f] 1.77 38.4 37.5 Captive female |4670 0.42 1.02 0.0256[f] 1.79 38.2 37.6 Winter | Captive male |5340 0.47 1.17 38.6 37.6 Captive female |4490 0.46 1.10 0.0172[f] 1.15 38.3 37.3 ---------------------+------------------------------------------------

+----------------------------------------------- | Species | T_{n}[d] |--------------- | T_{lc} T_{uc} References ---------------------+----------------------------------------------- _Bassariscus astutus_| 35.5 Chevalier (1985) _Procyon cancrivorus_| 26 Scholander et al. (1950b, c) _Potos flavus_ | McNab (1978a) _Potos flavus_ | 23 30 Mueller and Kulzer (1977) _Potos flavus_ | 23 33 Mueller and Rost (1983) _Nasua nasua_ | 25 33 Chevillard-Hugot et al. (1980) _Nasua nasua_ | 30 35 Mugaas et al. (in prep.) _Nasua narica_ | 25 35 _Nasua narica_ | Scholander et al. (1950b, c) | _Procyon lotor_ | This study Summer | Trapped male | 20 Captive male | 20 Captive female | 25 Winter | Captive male | 11 Captive female | 11 ---------------------+-----------------------------------------------

[a] Meas is measured basal metabolism (mL O_{2}.g^{-1}.h^{-1}). H_{br} is the ratio of measured to predicted basal metabolism where the predicted value is calculated from [.H]_{b} = 3.42.m^{-.25} (Kleiber, 1932, 1961:206) and m is body mass in grams.

[b] Meas is measured minimum thermal conductance (mL O_{2}.g^{-1}.h^{-1}. deg.C^{-1}). C_{mwr} is the ratio of measured to predicted minimum thermal conductance where the predicted value is calculated from C_{m} = 1.0.m^{-0.5} (McNab and Morrison, 1963; Herreid and Kessel, 1967), and m is body mass in grams.

[c] T_{b} is body temperature during the active ([alpha]) and rest ([rho]) phases of the daily cycle ( deg.C).

[d] T_{n} is the thermoneutral zone as defined by the lower (T_{lc}) and upper (T_{uc}) critical temperatures ( deg.C).

[e] Conductance calculated as the slope of the line describing oxygen consumption at temperatures below the lower critical temperature.

[f] Conductance calculated from C_{mw} = [.H]_{r}/(T_{b} - T_{a}), where [.H]_{r} is resting metabolic rate at temperatures below T_{lc}, 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 lotor_ has a much higher mass-specific [.H]_{b} than other procyonids (Table 7). To quantify the magnitude of this difference, we compared the measured value for _Procyon lotor_ with one calculated for it from a mass-specific least-squares regression equation (Eq. 6; R squared = 0.78) derived from data for those procyonids with lower than predicted [.H]_{b}: _Potos flavus_, _Procyon cancrivorus_, _Nasua nasua_, _Nasua narica_, and _Bassariscus astutus_ (Table 7).

[.H]_{b} = 2.39.m^{-0.25} Eq. 6

[.H]_{b} in Eq. 6 is basal metabolism (mL O_{2}.g^{-1}.h^{-1}) and m is body mass (g). Measured values of [.H]_{b} for _Procyon lotor_ were 1.45 to 1.86 times greater than those predicted for it by Eq. 6 (Table 8).

TABLE 8.--Basal metabolism (mL O_{2}.g^{-1}.h^{-1}) of _Procyon lotor_ as predicted by Eq. 6 ([.H]_{b} = 2.39.m^{-0.25}). Body masses, used to calculate predicted values, and measured values were taken from Table 7.

+-------------------------------- Season and sex | Predicted Measured/Predicted ----------------+-------------------------------- Summer | Trapped male | 0.29 1.86 Captive male | 0.29 1.59 Captive female| 0.29 1.45 Winter | Captive male | 0.28 1.68 Captive female| 0.29 1.59 ----------------+--------------------------------

_Influence of Diet on Basal Metabolism_

BACKGROUND.--With respect to [.H]_{b}, 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 [.H]_{b}. For example, terrestrial frugivores have [.H]_{b}'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_, and _Nasua nasua_ taken from Bisbal (1986); _Nasua narica_ taken from Kaufmann (1962:182-198); _Bassariscus astutus_ taken from Martin et al. (1951), Taylor (1954), Wood (1954), Toweill and Teer (1977), and Trapp (1978); _Procyon lotor_ taken 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.

+ <20% by volume when found. | 1%-19% frequency of occurrence. ++ >20% by volume when found. || 20%-50% frequency of occurrence. ||| >50% frequency of occurrence.

+-------------------------------------------------------------- |_Potos_ _Procyon_ _Nasua_ _Nasua_ _Bassariscus_ _Procyon_ Food |_flavus_ _cancrivorus_ _nasua_ _narica_ _astutus_ _lotor_ -----------+-------------------------------------------------------------- Mammalia | + | # ++ ||| ++ || Aves | ++ | + || Birds' eggs| ||| Reptilia | + | + ||| # + | + | Amphibia | + | # + | Pices | ++ || ++ || Insecta |++ | + ||| ++ ||| # + || ++ || Arachnida | ++ ||| # + | + | Chilopoda | ++ ||| Diplopoda | # + | Crustacea | ++ ||| # ++ ||| Mollusca | + || # + || Annelida | # + | Nuts | ++ || Grains | ++ || Buds | + | Fruit |++ ||| ++ # || ++ ||| Leaves | + | Grass | + | -----------+--------------------------------------------------------------

FOOD HABITS OF PROCYONIDS.--Food habits of six procyonids for which metabolic data are available are presented in Table 9. All six species clearly have mixed diets. Compared to other species, _Procyon lotor_ is highly catholic in its diet, taking food from almost twice as many categories as _Nasua narica_, three times as many as _Procyon cancrivorus_, _Nasua nasua_, and _Bassariscus astutus_, and nine times as many as _Potos flavus_.

For those species for which food habit data are quantified, we used Eisenberg's (1981:247-251) substrate/feeding matrix method, where "substrate" is analogous to McNab's (1986a) "behavior," to construct the following feeding categories that are based on the major food groups utilized by each species (Table 9).

1. _Potos flavus:_ (1) arboreal/frugivore, insectivore.

2. _Procyon cancrivorus:_ (1) semiaquatic/crustacivore, molluscivore, insectivore, piscivore, carnivore.

3. _Nasua nasua:_ (1) terrestrial/insectivore, arachnidivore, carnivore, frugivore.

4. _Bassariscus astutus:_ (1) terrestrial/carnivore, insectivore, frugivore.

5. _Procyon lotor:_ (1) terrestrial/carnivore, granivore, frugivore, insectivore; and (2) semiaquatic/crustacivore, molluscivore, insectivore, piscivore, carnivore.

FOOD HABITS AND BASAL METABOLISM.--The most important foods in the diet of _Procyon lotor_ are vertebrates, nuts, seeds, and fruits (Table 9). These are the same foods that are eaten by those dietary specialists that have [.H]_{b}'s equivalent to, or higher than, values predicted for them by the Kleiber equation (McNab, 1986a). The most important foods in the diets of _Potos flavus_, _Procyon cancrivorus_, and _Nasua nasua_ are invertebrates and fruit (Table 9), and these foods are eaten by dietary specialists that have lower than predicted [.H]_{b}'s (McNab, 1986a). Major foods in the diet of _Bassariscus astutus_ are terrestrial vertebrates, insects, and fruit (Table 9). Dietary specialists that eat terrestrial vertebrates have higher than predicted [.H]_{b}'s, whereas those that feed on insects have [.H]_{b}'s that are lower than predicted (McNab, 1986a). Year-round utilization of vertebrates by _Bassariscus astutus_ suggests that it also should have a metabolic rate that is equivalent to or higher than predicted, rather than lower (McNab, 1986a). However, perhaps year-round inclusion of insects in its diet (Martin et al., 1951; Taylor, 1954; Wood, 1954; Toweill and Teer, 1977; Trapp, 1978), plus water- and energy-conserving advantages of a low metabolic rate, each exert a stronger selective influence on [.H]_{b} than do vertebrates in its diet.

SUMMARY.--The basal metabolic rate of these procyonids does appear to be influenced by diet. But, it is apparent from this family's evolutionary history and tropical origins that climate also has had a profound influence on its member's metabolism. The history of the family and the data presented here (Table 7) suggest that lower than predicted [.H]_{b} is a feature that evolved very early as the primary metabolic adjustment to a tropical climate. From this perspective, it could be argued that climate would have been the major selective force determining [.H]_{b}, whereas food habits would have had a secondary influence.

_Basal Metabolism and Intrinsic Rate of Natural Increase_

BACKGROUND.--McNab (1980a) suggested that if food is not restricted during an animal's reproductive period, the factor that will limit growth and reproduction will be the rate at which energy can be used in growth and development. Under these conditions, an increase in [.H]_{b} would actually increase r_{max} because it would provide a higher rate of biosynthesis, a faster growth rate, and a shorter generation time. Hennemann (1983) tested McNab's (1980a) premise and found a significant correlation between r_{max} and metabolic rate, independent of body size, for 44 mammal species. A low correlation coefficient for this relationship, however, indicated to him (Hennemann, 1983) that factors such as (1) food supply, (2) thermal characteristics of the environment, and (3) brain size also contribute toward shaping a species' reproductive potential, particularly when these factors strongly influence rates of biosynthesis or growth or for some reason alter generation time. Results of our estimates of r_{max} for procyonids are presented in Table 10.

_Procyon lotor._--This species had the highest [.H]_{b} and D_{d}, and also had the highest r_{max} (1.34; Table 10). Such a high r_{max} may infer that this trait evolved under conditions where food and temperature were not limiting to reproduction. Under these conditions selection could have favored those reproductive characteristics sensitive to a higher [.H]_{b} (biosynthesis, growth, and generation time; McNab, 1980a). _Procyon lotor_'s high reproductive potential is due to its early age of first female reproduction and its large litter size, characteristics that may reflect metabolically driven increases in both biosynthesis and growth.

_Bassariscus astutus._--This species has a low [.H]_{b} but an r_{max} that was 124% of expected (Table 10). This suggests that r_{max} evolved under conditions where food and temperature were not limiting to reproduction. Reduced litter size should restrict this species' reproductive potential and may be a reflection of its low [.H]_{b}. The factor that is responsible for increasing its reproductive potential, however, is its early age of first female reproduction. _Bassariscus astutus_ is the smallest of these procyonids, and even though it has a low [.H]_{b}, its small mass may contribute to its ability to reach adult size and sexual maturity in its first year. The high quality of its diet (a high proportion of small vertebrates; Table 9) also may be a factor that is permissive to early female reproduction. Thus, small body size and diet may be factors that have allowed this species to evolve a higher than expected reproductive potential in spite of its low [.H]_{b}.

_Nasua narica._--This species is one of the largest procyonids (Table 7), and it possesses characteristics that should limit its reproductive potential: lower than predicted [.H]_{b} (Table 7), a relatively low-quality diet (Kaufmann, 1962:182-198; Table 9), and delayed time of first reproduction (Table 10). In spite of this, _Nasua narica_ has a higher than expected r_{max} (111% of predicted; Table 10). The life history feature that enhances _Nasua narica_'s reproductive potential, and increases r_{max} beyond expected, is its large litter size. In this species females live in bands. Each year just before their young are born these bands break up, and each female seeks out a den for herself and her litter. Once the young are able to leave the den (approximately five weeks), bands reform. In this situation, females not only care for their own young but also for those of other females in the band (Kaufmann, 1962:157-159, 1982, 1987; Russell, 1983). This social structure may contribute to this species' ability to produce large litters and in this way increase its reproductive potential.

TABLE 10.--Intrinsic rate of natural increase (r_{max}) of several procyonids. (a = potential age of females producing first young; b = potential annual birth rate of female young (= average litter size/2; average litter size was calculated from the published range of litter sizes for each species); n = potential age of females producing their final young; r_{maxe} = intrinsic rate of natural increase expected from body mass (Hennemann, 1983); r_{maxr} = ratio of calculated to expected intrinsic rate of natural increase (r_{max}/r_{maxe}).)

+------------------------------------------------ | Species |Body mass a b n r r [a] r [b] | (g) max maxe maxr ---------------------+------------------------------------------------ _Procyon lotor_ | 4940 0.83 2.25 16 1.34 0.53 2.52 | | | _Bassariscus astutus_| 900 0.83 1.50 14 1.02 0.82 1.24 | | | _Nasua narica_ | 3900 2.50 2.25 14 0.62 0.56 1.11 | _Nasua nasua_ | 3850 _Procyon cancrivorus_| 1160 0.83 1.50 15 1.02[c] 0.77 1.32 | 1.75 0.65[c] 0.84 _Potos flavus_ | 2490 1.75 0.50 12 0.30 0.63 0.48 | _Bassaricyon gabbii_ | 1600 1.75 0.50 15 0.32 0.71 0.45 | ---------------------+------------------------------------------------