Part 6

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 deg.C to 33 deg.C (Table 7; Mueller and Kulzer, 1977; Mueller and Rost, 1983). It begins to pant at about 30 deg.C, but its efforts at evaporative cooling are very ineffective. At 33 deg.C _Potos flavus_ can dissipate 33% of its metabolic heat via evaporative water loss, but at 35 deg.C the efficiency of this mechanism falls to 20% (Mueller and Rost, 1983). Consequently, when exposed to T_{a}'s above 33 deg.C, any kind of excitement causes its T_{b} to rise rapidly in an uncontrolled manner (Mueller and Kulzer, 1977; Mueller and Rost, 1983). These animals rely on their nocturnal and arboreal habits to keep them out of situations that could lead to hyperthermia (Mueller and Kulzer, 1977; Mueller 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 deg.C-35 deg.C; Table 7), they can tolerate T_{a}'s of 35 deg.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.

_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 deg.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 deg.C _Bassariscus astutus_ is able to dissipate 100% of its resting metabolic heat via evaporative water loss, and at 45 deg.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 deg.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[a] Cold[b] Species | Tropics Subtropics temperate temperate -----------------------+--------------------------------------------- _Procyon lotor_ | + + + + _Bassariscus astutus_ | + + + _Nasua nasua_ | + + _Nasua narica_ | + + _Procyon cancrivorus_ | + + _Potos flavus_ | + -----------------------+---------------------------------------------

[a] Extends from the subtropics north to the northern limit of _Bassariscus astutus_' distribution (Hall and Kelson, 1959:881), which approximates the 10 deg.C isotherm for average annual temperature in the United States (Kincer, 1941).

[b] Extends northward from the 10 deg.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[a] |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[b] 0.64 _Nasua nasua_ | 0.48 0.33 1.11[b] 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 ----------------------+----------------------------------------------

[a] Composite score = [(H_{br}/C_{mwr}) + D_{dr} + r_{maxr}]/3.

[b] 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.