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 Ḣb. 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 Cmweven more by lowering Tband 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 Cmw, Tlcof 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 Ta'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 Tucis 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°CPotos flavuscan 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 Ta's above 33°C, any kind of excitement causes its Tbto 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 nasuaandNasua narica.—Nasua nasuais abundant in tropical and subtropical South America, whereasNasua naricaoccupies 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 Ta's and solar radiation) than are nocturnal procyonids. Both coatis are more heat-tolerant thanPotos flavus; their Tuc's are higher (33°C-35°C;Table 7), they can tolerate Ta's of 35°C without raising their Tb's (Chevillard-Hugot et al., 1980; Mugaas et al., in prep.), and they have a greater capacity for evaporative cooling thanPotos 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.
Bassariscus astutus.—In addition to living in Neotropical forests of Mexico,Bassariscus astutusalso flourishes in hot arid climates, and it has extended its range much farther north thanNasua narica(Hall and Kelson, 1959:881,892; Poglayen-Neuwall, 1975; Kaufmann, 1982). Its Tucis higher (35.5°C;Table 7) than that ofPotos flavus, but it is comparable to those ofNasua nasuaandNasua narica. Its capacity for evaporative cooling is well developed; at 40°CBassariscus astutusis able to dissipate 100% of its resting metabolic heat via evaporative water loss, and at 45°C it is able to dissipate 172% (Chevalier, 1985). In spite of its great capacity for evaporative cooling, this species is nocturnal, a habit that, along with its low Ḣb, should allow it to keep thermoregulatory water requirements to a minimum.
Procyon lotor.—Our data suggested that TucforProcyon lotorin winter was comparable to that forBassariscus astutus(35°C), and that in summer it was even higher. When exposed to temperatures near the upper end of its Tn,Procyon lotorincreased the gradient for passive heat loss with a controlled rise in Tb(Figure 6). In summer its capacity for passive heat loss was enhanced by the molt of its heavy winter fur.Procyon lotor's capacity for evaporative cooling also appeared to be well developed, although our animals were not heated to the point that evaporative cooling was fully expressed (Figures 4,5). However,Procyon lotoris nocturnal, and this may allow it to eliminate, or at least reduce, the need for evaporative cooling, even in hot climates. Thus,Procyon lotorappears to be well equipped physiologically and behaviorally to cope with thermal demands of hot environments in its distribution.
Procyon cancrivorus.—Unfortunately, data for the crab-eating raccoon are not complete enough at high temperatures to include it in this survey.
Summary.—This comparison demonstrates that capacity for evaporative cooling, tolerance of an elevated Tbto enhance passive heat loss, and behavioral avoidance of thermal stress are the primary methods used by procyonids to thermoregulate at high temperatures.Procyon lotorandBassariscus astutus, whose distributions extend into temperate regions, have developed these abilities to a greater extent than other procyonids.Potos flavus, whose distribution is confined to lowland tropical forests, has the least ability in this regard.Nasua nasuaandNasua naricaappear to have thermoregulatory abilities that are intermediate to those ofBassariscus astutusandPotos flavus. This suggests that ancestral procyonidsmay have had poor to modest ability to thermoregulate at high temperatures, a condition that would have limited their ability to leave the thermal stability afforded by tropical forests. Dispersal into temperate climates, therefore, required not only increased cold tolerance but also selective enhancement of those mechanisms used in thermoregulation at high temperatures.
Table 11.—Distribution by climate of selected procyonid species.
[a]Extends from the subtropics north to the northern limit ofBassariscus astutus' distribution (Hall and Kelson, 1959:881), which approximates the 10°C isotherm for average annual temperature in the United States (Kincer, 1941).[b]Extends northward from the 10°C isotherm for average annual temperature in the United States.
Composite Scores of Adaptive Units and Geographic Distribution
InTable 11, procyonid species are arranged in descending order with respect to the number of major climates that are included in their geographic distributions (Hall and Kelson, 1959:878-897; Poglayen-Neuwall, 1975; Kortlucke and Ramirez-Pulido, 1982; Nowak and Paradiso, 1983:977-985). Composite scores ranged from a high of 1.47 forProcyon lotorto a low of 0.39 forPotos flavus, whereasNasua nasua,Nasua narica,Procyon cancrivorus, andBassariscus astutushad intermediate values ranging from 0.64 to 0.79 (Table 12).Figure 8demonstrates that there is a direct relationship between the number of climates these species occupy and their composite scores. Regression analysis (Y = 2.68·X + 0.24; where Y is number of climates, and X is composite score) demonstrates a high degree of correlation between these variables (R = 0.94) and indicates that 89% of the variance in distribution can be explained by composite scores. The various combinations of adaptations expressed by these species do, therefore, play a role in delimiting their climatic (latitudinal) distributions.
Procyon lotor'snormalized scores were higher in all categories than those of other procyonids.Procyon lotor, therefore, possesses those traits that have allowed it to become the premier climate generalist of the procyonid family. As an adaptive unit, these traits provideProcyon lotorwith the physiological and behavioral flexibility required to take full advantage of a wide range of climates and habitats, and its distribution verifies that it has done so. Even so, it is probably not fair to assume that this species represents a perfect physiological match with climate over its entire distribution.Procyon lotoris, in many respects, still a forest-dwelling species, and its ability to expand its distribution into other habitats such as prairie and desert may well be due, in part, to its use of behavior to take advantage of favorable microclimates in otherwise hostile environments (Bartholomew, 1958, 1987). This feature ofProcyon lotor'sbiology needs to be further examined.
Table 12.—Normalized and composite scores for selected procyonids. (Hbr= ratio of measured to predicted basal metabolism (Table 7), Cmwr= ratio of measured to predicted minimum thermal conductance (Table 7), Ddr= ratio of food categories actually utilized by each species to total food categories eaten by all six species (calculated fromTable 9), rmaxr= ratio of calculated to expected rmax(Table 10).)
[a]Composite score = [(Hbr/Cmwr) + Ddr+ rmaxr]/3.[b]Value calculated forNasua narica(Table 10) and used with the assumption that it must be similar to the value forNasua nasua.
All five species with low Ḣb's have composite scores less than 1.0 (Table 12;Figure 8). Four of these five,Nasua nasua,Nasua narica,Procyon cancrivorus, andPotos flavus, have Hbr/Cmwrratios that are 0.6 or less, which indicates they are the least cold-tolerant procyonids (McNab, 1966). These four species also are confined to either tropic, or tropic and subtropic climates (Table 11). This suggests that these species share a common thermoregulatory adaptation that represents a specialization to these climates. Attendant with this adaptation, however, is a high cost of thermoregulation attemperatures below their Tlc, and this must be an important factor in limiting their distributions to tropic and subtropic climates. Differences in their distributions within these climates, therefore, must hinge more on differences in their Ddrand rmaxrvalues than on differences in their Hbr/Cmwrratios. This is supported by the fact thatPotos flavus, which has the lowest Ddrand rmaxrvalues, is confined to a single climate, whereasNasua nasua,Nasua narica, andProcyon cancrivoruseach possess larger Ddrand rmaxrvalues and are found in two climates. Thus,Potos flavus, with its highly specialized diet and low reproductive potential, is the most ecologically specialized of these procyonids, and its distribution is limited to the single climate that can provide its requirements.Nasua nasua,Nasua narica, andProcyon cancrivorusare less specialized and thus show more ecological flexibility in their distributions.
number of climates vs composite scoreFigure 8.—Relationship between number of climates in which a species is found and its composite score. Symbols forNasua nasuaoverlap at coordinates (0.64, 2). Solid line represents linear regression of climates (Y) on composite scores (X): Y = 2.68·X + 0.24; R = 0.94.
Figure 8.—Relationship between number of climates in which a species is found and its composite score. Symbols forNasua nasuaoverlap at coordinates (0.64, 2). Solid line represents linear regression of climates (Y) on composite scores (X): Y = 2.68·X + 0.24; R = 0.94.
Bassariscus astutus, the other species with low Ḣb, is found in three climates, which indicates that it has greater ecological flexibility thanNasua nasua,Nasua narica, orProcyon cancrivorus. Ddrand rmaxrare comparable for these four species (Table 12). This suggests that the greater ecological flexibility ofBassariscus astutusis derived largely from its greater cold tolerance.Bassariscus astutushas a more insulative pelt than these other procyonids (Cmwr= 0.85;Table 7), so its Hbr/Cmwrratio is higher (0.80;Table 12). This, and its greater capacity for evaporative cooling (Chevalier, 1985), allowsBassariscus astutusto take advantage of a wider range of thermal environments than these other species. However, even with its higher Hbr/Cmwrratio, the composite score forBassariscus astutusis not much different than those forNasua nasua,Nasua narica, andProcyon cancrivorus(Table 12). Consequently,Bassariscus astutusis found in more climates than would be predicted for it on the basis of its composite score (Figure 8). This suggests that either the Hbr/Cmwrratio carries greater weight in determining distribution than is reflected in this analysis, or as has been described for some other species (Bartholomew, 1958, 1987),Bassariscus astutusmay extend its distribution farther than expected via use of its behavior. In either case, for procyonids with low Ḣb,Bassariscus astutusrepresents the pinnacle of adaptation for climate generalization.
Evolution of Metabolic Adaptations
Evolution of Low Basal Metabolic Rate
A radiation of frugivorous and omnivorous Procyoninae (Table 1) occurred in the middle and late Miocene of North America. It included origins of such terrestrial genera asCyonasua,Nasua, andProcyon(Webb, 1985b). The earliest procyonid genus to find its way to South America wasCyonasua, an omnivorous carnivore that presumably split, along with its sister genusArctonasua, from a common North American ancestor (Baskin, 1982; Webb, 1985b).Cyonasua, about the size of present-day raccoons, was adapted to a wide range of habitats and was probably comparable to modern raccoons with respect to the breadth of its feeding habits (Webb, 1985b; Marshall, 1988). Because North AmericanArctonasuawas about the same size asCyonasua(Webb, 1985b) and shared a number of characters with it (Baskin, 1982), we speculate that it also may have had similar habits and occupied similar climates and habitats.Bassariscus, another member of Procyoninae, had an even earlier origin in tropical North America (Webb, 1985b). The origin of the small arboreal formsPotosandBassaricyon(subfamily Potosinae) is obscure but is thought to have occurred in the rainforests of Central America (Webb, 1985b). What were the metabolic capabilities of these early procyonids? We do not know, but for several million years, from middle to late Miocene, procyonids lived in tropical and subtropical forests of Central and North America (Webb, 1985b; Marshall, 1988). Then, in the Pleistocene, several modern forms crossed the Panamanian land bridge into similar habitats and climates in South America; but none of them appear to have spread far enough northward to have crossed the Bering land bridge.
Several million years exposure to a tropical environment, with its continuous high temperatures and modest range of thermal extremes, would have favored selection of metabolic and thermoregulatory traits that would minimize energy requirements: a lower than predicted basal metabolic rate, a prolonged or continuous molt resulting in very little annual change in minimum thermal conductance, and a modest capacity for evaporative cooling. In addition, we would expect selection to have favored a diverse diet, good reproductivepotential, and behavioral flexibility to utilize a variety of habitats within these climates. Our analysis has shown that such characteristics are the norm for extant members of this family living in tropical and subtropical climates, and we speculate that these traits also were common to early procyonids and served to restrict them to these climates. Our speculation is supported by the fact that their known fossil history from the Miocene is confined to geographic areas that had tropical and subtropical climates.
Later on, during Pleistocene glaciations, tropical and subtropical forests shrank, savannas expanded, and temperate climate was pushed toward equatorial regions. The opposite occurred during interglacial periods (Raven and Axelrod, 1975; Webb, 1977, 1978; Marshall, 1988). Consequently, mid-latitudes experienced alternating periods of temperate and tropical, or at least subtropical, climate change. Selection of characteristics that would have adapted a species with low Ḣbto temperate as well as tropic or subtropic climates could have occurred in mid-latitudes at the temperate edge of these tropical advances and retreats. Our analysis indicates that, for this purpose, selection would have favored lower than predicted thermal conductance, seasonal molt, increased capacity for evaporative cooling, increased tolerance of elevated Tb, increased flexibility of thermoregulatory behavior, food habits that provided for year-round access to a high-quality diet in all three climates, and a higher than predicted rmax.
Bassariscus astutusis the only species with low Ḣbthat has all these characteristics, and it is the only one of them that has added temperate climate to its distribution (Table 11). This suggests thatBassariscus astutusis a species that evolved away from the norm for procyonids with low Ḣb, toward characteristics that allowed it to become more of a climate generalist.Potos flavus, with its dietary specialization, low tolerance to high temperatures, and arboreal mode of existence, has become a highly specialized species totally dependent on tropical forests for its survival. As such, it also represents a species that has evolved away from the procyonid norm and portrays the extreme in climate specialization. Olingos,Bassaricyon gabbii(Table 1), may be similar toPotos flavusin this respect (see alsoTable 10). This suggests that of the extant procyonids,Nasua nasua,Nasua narica, andProcyon cancrivorushave retained metabolic and behavioral characteristics that are closest to those of their Miocene ancestors.
Evolution of High Basal Metabolic Rate
Between the time thatCyonasuaappeared and the Panamanian land bridge was established in the upper Pliocene (4 to 5 million years ago), northern climates continued their gradual cooling. This, along with ongoing elevation of the continents and continuous modification of their mountain ranges, served to shrink the tropical forest and create pockets of climatic instability within it and on its edges (Darlington, 1963:578-596; Marshall, 1988). In areas of instability, selection would have favored traits that provided for a broader range of thermal tolerance: higher Ḣb, improved insulative quality of pelt, a more sharply defined molt cycle, improved capacity for evaporative cooling, greater Dd, and higher rmax. Consequently, by the upper Pliocene, two metabolically distinct groups of procyonids could have been established: those species with low Ḣbliving in climatically stable forests and those with higher Ḣbliving in unstable tropical, subtropical, and perhaps temperate climates.
Procyon lotoris the only extant procyonid with high Ḣb.Procyon cancrivorusis its congeneric counterpart in Central and South America (Table 1), and the two species are sympatric in Panama and Costa Rica. However, in terms of its metabolism, thermal conductance, molt, diversity of diet, rmax, and climatic distribution,Procyon cancrivorusshares more in common with other procyonids than it does withProcyon lotor(Tables 7,11,12;Figure 8). This suggests that metabolicallyProcyon lotorportrays a divergent line of this genus that arose as the result of a series of mutations that gave rise to different metabolic characteristics. This view is in keeping with a recent phylogenetic analysis of this family that shows the genusProcyonto be highly derived (Decker and Wozencraft, 1991). Consequently, it would be instructive and would add to our knowledge of the evolution of climatic adaptation to know more about the genetic relatedness of these two species as well as their historical relationship.
GenusProcyonappears in the fossil record (Hemphillian and Blancan ages; Baskin, 1982) prior to Pleistocene glaciations. During the Pleistocene, there were four different glacial advances and retreats in a relatively short time period (the first appearing little more than a million years ago; Darlington, 1963:578-596; Webb, 1985a; Marshall, 1988). Glacial retreats created pulses of time during which subtropic and temperate climates advanced toward the poles into areas with large seasonal differences in light/dark cycles, whereas glacial advances pushed these climates southward into areas having smaller seasonal differences in light/dark cycles (Raven and Axelrod, 1975; Webb, 1977, 1978; Marshall, 1988). Those members of the genusProcyoncaught in these wide latitudinal fluctuations would have experienced conditions favorable to continued selection for characteristics conducive to physiologic adaptation to a wide range of climatic conditions.Procyon lotoris the only member of its genus to have survived this selective process, and as we have seen, it does possess traits that adapt it to a wide range of climatic conditions. Primary among these is its higher Ḣb, which provides it with advantages not shared with other procyonids (see earlier discussion). Three other adaptations also have had a profound influence onProcyon lotor's ability to generalize its use of climate: (1) the increased insulative quality of its pelt coupled with its sharply defined molt cycle, which allows for a large annual change in thermal conductance; (2) its annual cycle of fat storage; and (3) a diverse high-quality diet. The first two of these adaptationsrequired evolution of neuroendocrine pathways capable of responding to time-dependent environmental cues such as changing day length, changing temperature, etc. Such conditions would have been available as selective stimuli in high-latitude forests and savannas of interglacial periods.Procyon lotor's elevated basal metabolic rate would have increased its overall energy requirement, and it makes good intuitive sense, therefore, that evolution during the Pleistocene also would have favored selection of a diverse diet containing many items of high nutritive value.
Summary
Our analysis has illustrated that within Procyonidae there are two distinct modes of metabolic adaptation to climate. One is typified by those species with low Ḣb's (Bassariscus astutus,Nasua nasua,Nasua narica,Procyon cancrivorus, andPotos flavus), and the other byProcyon lotorwith its higher Ḣb. Those with low Ḣb's have more restricted geographic distributions, and, with the exception ofBassariscus astutus, they are all confined to tropical and subtropical areas. The fossil history of this family indicates that it had its origins in tropical forests of North and Central America. This indicates that those procyonids whose distributions are still primarily restricted to tropical forests share many of the metabolic adaptations characteristic of their ancestors. We speculate, therefore, that ancestral procyonids had a lower than predicted Ḣb, a pelt with modest to poor insulative quality, good thermogenic ability but poor heat tolerance, modest to poor capacity for evaporative cooling, no well-defined molt cycle, no cyclic period of fattening, nocturnal habits, and a modestly diverse diet of high-enough quality to provide for an average reproductive potential. Although this pedigree contributed to the success of this family in tropical and subtropical forests, it limited the ability of its members to expand their distributions into cooler, less stable climates. Viewed in this perspective,Procyon lotor's high basal metabolic rate, extraordinarily diverse diet, well-defined cyclic changes in fat content and thermal conductance, high level of heat tolerance, high capacity for evaporative cooling, and high reproductive potential all stand out in sharp contrast to the condition described for other procyonids. This suggests that the North American raccoon represents culmination of a divergent evolutionary event that has given this species the ability to break out of the old procyonid mold and carry the family into new habitats and climates.
Appendix: List of Symbols
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