Part 9

Bassariscus astutus.--In addition to living in Neotropical forests of Mexico, Bassariscus astutus also flourishes in hot arid climates, and it has extended its range much farther north than Nasua narica (Hall and Kelson, 1959:881,892; Poglayen-Neuwall, 1975; Kaufmann, 1982). Its T{uc} is higher (35.5°C; Table 7) than that of Potos flavus, but it is comparable to those of Nasua nasua and Nasua narica. Its capacity for evaporative cooling is well developed; at 40°C Bassariscus astutus is 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 [.H]{b}, should allow it to keep thermoregulatory water requirements to a minimum.

Procyon lotor.--Our data suggested that T{uc} for Procyon lotor in winter was comparable to that for Bassariscus astutus (35°C), and that in summer it was even higher. When exposed to temperatures near the upper end of its T{n}, Procyon lotor increased the gradient for passive heat loss with a controlled rise in T{b} (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 lotor is nocturnal, and this may allow it to eliminate, or at least reduce, the need for evaporative cooling, even in hot climates. Thus, Procyon lotor_ appears 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 T{b} to enhance passive heat loss, and behavioral avoidance of thermal stress are the primary methods used by procyonids to thermoregulate at high temperatures. Procyon lotor and Bassariscus 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 nasua and Nasua narica appear to have thermoregulatory abilities that are intermediate to those of Bassariscus astutus and Potos flavus_. This suggests that ancestral procyonids may 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.

-----------------------+--------------------------------------------- | Mild Cold Species | Tropics Subtropics temperate temperate -----------------------+--------------------------------------------- Procyon lotor | + + + + Bassariscus astutus | + + + Nasua nasua | + + Nasua narica | + + Procyon cancrivorus | + + Potos flavus | + -----------------------+---------------------------------------------

Extends from the subtropics north to the northern limit of Bassariscus astutus' distribution (Hall and Kelson, 1959:881), which approximates the 10°C isotherm for average annual temperature in the United States (Kincer, 1941).

Extends northward from the 10°C isotherm for average annual temperature in the United States.

COMPOSITE SCORES OF ADAPTIVE UNITS AND GEOGRAPHIC DISTRIBUTION

In Table 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 for Procyon lotor to a low of 0.39 for Potos flavus, whereas Nasua nasua, Nasua narica, Procyon cancrivorus, and Bassariscus astutus had intermediate values ranging from 0.64 to 0.79 (Table 12). Figure 8 demonstrates 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's normalized 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 provide Procyon lotor with 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 lotor is, 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 of Procyon lotor's biology needs to be further examined.

TABLE 12.--Normalized and composite scores for selected procyonids. (H{br} = ratio of measured to predicted basal metabolism (Table 7), C{mwr} = ratio of measured to predicted minimum thermal conductance (Table 7), D{dr} = ratio of food categories actually utilized by each species to total food categories eaten by all six species (calculated from Table 9), r{maxr} = ratio of calculated to expected r_{max} (Table 10).)

----------------------+---------------------------------------------- | Normalized scores Species |---------------------------- Composite |H{br}/C{mwr} D{dr} r{maxr} score ----------------------+---------------------------------------------- Procyon lotor | 0.95 0.95 2.52 1.47 Bassariscus astutus | 0.80 0.33 1.24 0.79 Nasua nasua | 0.48 0.33 1.11 0.64 Nasua nasua | 0.48 0.33 1.11 0.64 Nasua narica | 0.40 0.53 1.11 0.68 Procyon cancrivorus | 0.55 0.33 1.32 0.73 Potos flavus | 0.60 0.11 0.48 0.39 ----------------------+----------------------------------------------

Composite score = [(H{br}/C{mwr}) + D{dr} + r{maxr}]/3.

Value calculated for Nasua narica (Table 10) and used with the assumption that it must be similar to the value for Nasua nasua.

All five species with low [.H]{b}'s have composite scores less than 1.0 (Table 12; Figure 8). Four of these five, Nasua nasua, Nasua narica, Procyon cancrivorus, and Potos flavus, have H{br}/C{mwr} ratios 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 at temperatures below their T{lc}, 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 D{dr} and r{maxr} values than on differences in their H{br}/C{mwr} ratios. This is supported by the fact that Potos flavus, which has the lowest D{dr} and r{maxr} values, is confined to a single climate, whereas Nasua nasua, Nasua narica, and Procyon cancrivorus each possess larger D{dr} and r{maxr} values 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, and Procyon cancrivorus are less specialized and thus show more ecological flexibility in their distributions.

Bassariscus astutus, the other species with low [.H]{b}, is found in three climates, which indicates that it has greater ecological flexibility than Nasua nasua, Nasua narica, or Procyon cancrivorus. D{dr} and r{maxr} are comparable for these four species (Table 12). This suggests that the greater ecological flexibility of Bassariscus astutus is derived largely from its greater cold tolerance. Bassariscus astutus has a more insulative pelt than these other procyonids (C{mwr} = 0.85; Table 7), so its H{br}/C{mwr} ratio is higher (0.80; Table 12). This, and its greater capacity for evaporative cooling (Chevalier, 1985), allows Bassariscus astutus to take advantage of a wider range of thermal environments than these other species. However, even with its higher H{br}/C{mwr} ratio, the composite score for Bassariscus astutus is not much different than those for Nasua nasua, Nasua narica, and Procyon cancrivorus (Table 12). Consequently, Bassariscus astutus is found in more climates than would be predicted for it on the basis of its composite score (Figure 8). This suggests that either the H{br}/C{mwr} ratio 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 astutus may extend its distribution farther than expected via use of its behavior. In either case, for procyonids with low [.H]{b}, Bassariscus astutus_ represents 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 as Cyonasua, Nasua, and Procyon (Webb, 1985b). The earliest procyonid genus to find its way to South America was Cyonasua, an omnivorous carnivore that presumably split, along with its sister genus Arctonasua, 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 American Arctonasua was about the same size as Cyonasua (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 forms Potos and Bassaricyon (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 reproductive potential, 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 [.H]{b} to 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 T{b}, 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 r_{max}.

Bassariscus astutus is the only species with low [.H]{b} that has all these characteristics, and it is the only one of them that has added temperate climate to its distribution (Table 11). This suggests that Bassariscus astutus is a species that evolved away from the norm for procyonids with low [.H]{b}, 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 to Potos flavus in this respect (see also Table 10). This suggests that of the extant procyonids, Nasua nasua, Nasua narica, and Procyon cancrivorus have retained metabolic and behavioral characteristics that are closest to those of their Miocene ancestors.

Evolution of High Basal Metabolic Rate

Between the time that Cyonasua appeared 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 [.H]{b}, improved insulative quality of pelt, a more sharply defined molt cycle, improved capacity for evaporative cooling, greater D{d}, and higher r{max}. Consequently, by the upper Pliocene, two metabolically distinct groups of procyonids could have been established: those species with low [.H]{b} living in climatically stable forests and those with higher [.H]_{b} living in unstable tropical, subtropical, and perhaps temperate climates.

Procyon lotor is the only extant procyonid with high [.H]{b}. Procyon cancrivorus is 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, r{max}, and climatic distribution, Procyon cancrivorus shares more in common with other procyonids than it does with Procyon lotor (Tables 7, 11, 12; Figure 8). This suggests that metabolically Procyon lotor portrays 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 genus Procyon to 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.

Genus Procyon appears 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 genus Procyon caught 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 lotor is 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 [.H]{b}, which provides it with advantages not shared with other procyonids (see earlier discussion). Three other adaptations also have had a profound influence on Procyon 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 adaptations required 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