Part 2

$Introduction$

DEFINING THE PROBLEM

Procyonid Origins

The major carnivore radiations took place about 40 million years before present (MYBP) in the late Eocene and early Oligocene (Ewer, 1973:363; Wayne et al., 1989). Between 30 and 40 MYBP, a progenitor split into the ursid and procyonid lineages, which evolved into present-day bears, pandas, and raccoons (Wayne et al., 1989). The taxonomic relatedness of pandas to bears and raccoons has been tested extensively and a number of authors have summarized current thinking on the problem (Martin, 1989; Wayne et al., 1989; Wozencraft, 1989a, 1989b; Decker and Wozencraft, 1991). Davis (1964:322-327) and others (Leone and Wiens, 1956; Todd and Pressman, 1968; Sarich, 1976; O'Brien et al., 1985) place the giant panda, Ailuropoda melanoleuca, with the ursids. The taxonomic status of the red panda, Ailurus fulgens, appears to be less certain. Some current investigations align the red panda with bears (Segall, 1943; Todd and Pressman, 1968; Hunt, 1974; Ginsburg, 1982; Wozencraft, 1984:56-110; 1989a), whereas others place them intermediate to procyonids and bears (Wurster and Benirschke, 1968; Sarich, 1976; O'Brien et al., 1985), or in close relationship to the giant panda (Tagle et al., 1986).

The procyonid radiation took place in North America and produced forms that were mostly arboreal and omnivorous (Eisenberg, 1981:122; Martin, 1989). The center of this diversification occurred in Middle America (Baskin, 1982; Webb, 1985b) during the Miocene (Darlington, 1963:367; Webb, 1985b). Fossil procyonids from the late Miocene are represented in Florida, California, Texas, Nebraska, Kansas, and South Dakota (Baskin, 1982; Martin, 1989) and include such genera as Bassariscus, Arctonasua, Cyonasua, Paranasua, Nasua, and Procyon (Baskin, 1982; Webb, 1985b). During the Miocene procyonids underwent a modest radiation within tropical and subtropical climates of North America's central and middle latitudes. Cyonasua, which has close affinities to Arctonasua (Baskin, 1982), appears in tropical South America in the late Miocene and immigrated there either by rafting across the Bolivar Trough or by island-hopping through the Antilles archipelagoes (Marshall et al., 1982; Marshall, 1988). Thus, procyonids were found on both continents prior to formation of the Panamanian land bridge (Darlington, 1963:367, 395; Marshall et al., 1982; Marshall, 1988). Origins of Bassaricyon and Potos are obscure but probably occurred in tropical rainforests of Middle America (Baskin, 1982; Webb, 1985b). A subsequent Pleistocene dispersal carried several modern genera (Table 1) across the Panamanian land bridge into South America (Webb, 1985b). Bassariscus and Bassaricyon represent the most primitive genera in Procyoninae and Potosinae subfamilies, respectively (Table 1; Wozencraft, 1989a; Decker and Wozencraft, 1991).

In the early Tertiary, mid-latitudes of North America were much warmer than they are now, but not fully tropical, and temperate deciduous forests, associated with strongly seasonal climates, occurred only in the far north (Barghoorn, 1953; Colbert, 1953; Darlington, 1963:589, 590). Major climatic deteriorations, with their attendant cooling of northern continents, occurred during the Eo-Oligocene transition, in the middle Miocene, at the end of the Miocene, and at about 3 MYBP (late Pliocene). This last deterioration corresponds with closure of the Panamanian isthmus (Berggren, 1982; Webb, 1985a). Climatic deterioration went on at an accelerating rate during the late Tertiary, with glacial conditions developing at the poles by the mid-Pliocene (Barghoorn, 1953). Therefore, throughout the Tertiary, as continents cooled, northern climate zones moved toward the tropics (Barghoorn, 1953; Colbert, 1953; Darlington, 1963:589, 590, 594, 595; Webb, 1985a).

TABLE 1.--Classification of recent Procyonidae after Wozencraft (1989a) and Decker and Wozencraft (1991). Information in parenthesis indicates general geographic distribution (modified from Kortlucke and Ramirez-Pulido (1982) and Poglayen-Neuwall (1975)): S.A. = South America; C.A. = Central America; M. = Mexico; U.S. = United States; C. = Canada. Lower case letters preceding geographic areas signify north (n), south (s), and west (w).

Order CARNIVORA Bowdich, 1821 Suborder CANIFORMIA Kretzoi, 1945 Family PROCYONIDAE Gray, 1825 Subfamily POTOSINAE Trouessart, 1904 Genus Potos E. Geoffroy and G. Cuvier, 1795 P. flavus (S.A., C.A., M.) Genus Bassaricyon Allen, 1876 B. alleni (S.A.) B. beddardi (S.A.) B. gabbii (nS.A., C.A.) B. lasius (C.A.) B. pauli (C.A.) Subfamily PROCYONINAE Gray, 1825 Genus Bassariscus Coues, 1887 B. astutus (M., wU.S.) B. sumichrasti (C.A., M.) Genus Nasua Storr, 1780 N. narica (nS.A., C.A., M., swU.S.) N. nasua (S.A., sC.A.) Genus Nasuella Hollister, 1915 N. olivacea (S.A.) Genus Procyon Storr, 1780 P. cancrivorus (S.A., sC.A.) P. gloveralleni (Barbados) P. insularis (Maria Madre Is., Maria Magdalene Is.) P. lotor (C.A., M., U.S., sC.) P. maynardi (Bahamas, New Providence Is.) P. minor (Guadeloupe Is.) P. pygmaeus (M., Quintana Roo, Cozumel Is.)

The several named forms of Bassaricyon are a single species, Bassaricyon gabbii (Wozencraft, 1989a).

These are considered conspecific in some current taxonomies (Kortlucke and Ramirez-Pulido, 1982); however, the scheme followed here maintains them as separate species (Decker, 1991).

Several named forms of Procyon are a single species, Procyon lotor (Wozencraft, 1989a).

During the late Miocene, late Pliocene, and Pleistocene, the Bering land bridge between North America and Asia formed periodically, offering an avenue for dispersal between northern continents (Darlington, 1963:366; Webb, 1985a). However, by the late Tertiary, northern continents had cooled to the extent that climate, with its attendant sharply defined vegetative zones, became the major factor limiting dispersal by this route (Darlington, 1963:366; Webb, 1985a). Those Holarctic mammals that did cross the Bering land bridge in the late Tertiary were "cold-adapted" species associated with relatively cool, but not alpine, climates (Darlington, 1963:366; Ewer, 1973:369). Among carnivores this included some canids, ursids, mustelids, and felids (Darlington, 1963:393-395, 397; Webb, 1985a). Procyonids, however, did not cross the Bering land bridge into Asia, and Ewer (1973:369) ascribes this to their being an "essentially tropical group." Miocene radiation of procyonids occurred at a time when two of the four major climatic deteriorations (middle and late Miocene) were taking place (Webb, 1985a, 1985b). These deteriorations had the effect of cooling the middle latitudes to the extent that temperate forest forms began to appear in mid-latitude floras, along with a rapid influx of herbaceous plants (Barghoorn, 1953). The procyonid radiation did not penetrate beyond these climatically changing middle latitudes, which implies that these animals were "warm-adapted," and were, therefore, physiologically excluded from reaching the Bering land bridge. Today, three of the six genera and over half of the 18 species that comprise Procyonidae (Table 1; Wozencraft, 1989b) remain confined to tropical regions of North and South America (Hall and Kelson, 1959:878-897; Poglayen-Neuwall, 1975; Kortlucke and Ramirez-Pulido, 1982; Nowak and Paradiso, 1983:977-985).

Typical Procyonids

McNab (1988a) contends that basal metabolism is a highly plastic character in evolution, and he has amply shown that ecologically uniform species are more apt to share common metabolic rates than taxonomically allied species from drastically different environments (McNab, 1984a, 1986a, 1986b, 1988a). Procyonids represent a taxonomically allied group that shared a common ecological situation for millions of years; consequently, members of this family might be expected to show some uniformity in their [.H]{b}. Basal and thermoregulatory metabolism of several procyonids have been measured: kinkajou, Potos flavus (Müller and Kulzer, 1977; McNab, 1978a; Müller and Rost, 1983), coatis, Nasua nasua (Chevillard-Hugot et al., 1980; Mugaas et al., in prep.), and Nasua narica (Scholander et al., 1950c; Mugaas et al., in prep.), ringtail, Bassariscus astutus (Chevalier, 1985), and crab-eating raccoon, Procyon cancrivorus (Scholander et al., 1950c). In general, these species have [.H]{b}'s that are 40%-80% of the values predicted for them by the Kleiber (1961:206) equation. Lower than predicted [.H]{b} is viewed as an energy-saving adaptation for procyonids living in relatively stable tropical climates (Müller and Kulzer, 1977; Chevillard-Hugot et al., 1980; Müller and Rost, 1983). This implies that lower than predicted [.H]{b} is a general procyonid condition and that it represents a characteristic that evolved in response to the family's long association with tropical and subtropical forest environments.

The Atypical Procyonid

Although most procyonids are found in only tropical to subtropical climates, the North American raccoon, Procyon lotor, (Figure 1) has a much broader distribution that extends from tropical Panama (8°N) to southern Canada. In Alberta, Canada, its range reaches the edge of the Hudsonian Life Zone at 60°N (for distribution maps see Hall and Kelson, 1959:878-897, and Poglayen-Neuwall, 1975). Range extensions and an increase in numbers have been noted in Canada and in parts of the United States since the 19th century (Lotze and Anderson, 1979; Kaufmann, 1982; Nowak and Paradiso, 1983:977-985). Thus, Procyon lotor is more complex ecologically than other procyonids, particularly when one takes into account its highly generalized food habits (Hamilton, 1936; Stuewer, 1943; Stains, 1956:39-51; Greenwood, 1981) and the wide range of habitat types (forest, prairie, desert, mountain, coastal marsh, freshwater marsh) and climates (tropical to north temperate) in which it is successful (Whitney and Underwood, 1952:1; Hall and Kelson, 1959:885; Lotze and Anderson, 1979; Kaufmann, 1982). On this basis it is clear that Procyon lotor has deviated from the typical procyonid portrait and has become the consummate generalist of the Procyonidae.

The Hypothesis

Our general hypothesis was that whereas most contemporary procyonids have retained the metabolic characteristics of their warm-adapted ancestors, Procyon lotor possesses a different set of adaptations, which either evolved as characteristics unique to this species or were acquired from its ancestral stock. In either case, its unique adaptations have given Procyon lotor the physiological flexibility to generalize its use of habitats and climates and expand its geographic distribution to a much greater extent than other procyonids.

Hypothesis Testing

We tested our hypothesis by comparing Procyon lotor with several other procyonids (Bassariscus astutus, Nasua nasua, Nasua narica, Procyon cancrivorus, and Potos flavus) on the basis of their (1) basal metabolic rate ([.H]{b}), (2) minimum wet thermal conductance (C{mw}), (3) diversity of diet (D{d}), (4) intrinsic rate of natural increase (r{max}), and, when data were available, (5) capacity for evaporative cooling (E_{c}). In a genetic sense each one of these variables is a complex adaptive characteristic, expression of which is determined by the interaction of several genes (Prosser, 1986:110-165). Experience has shown that a given species will express each one of these variables in a specific manner that is relevant to its mass, physiology, behavior, and environmental circumstance. Thus, different expressions of these variables may represent specific climatic adaptations (Prosser, 1986:16) that have been selected-for by evolutionary process. Because these variables are interrelated with respect to regulation of body temperature and energy balance, they have co-evolved in each species to form an adaptive unit. For each species, measured and calculated values for the first four variables were converted into dimensionless numbers and used to derive a composite score that represented its adaptive unit. Climatic distributions of these species were then compared relative to their composite scores.

ADAPTIVE SIGNIFICANCE OF THE VARIABLES

Basal Metabolic Rate and Intrinsic Rate of Natural Increase

Basal metabolic rate represents the minimum energy required by an animal to maintain basic homeostasis (Lusk, 1917:141; Kleiber, 1932, 1961:251; Benedict, 1938; Brody, 1945:59; Robbins, 1983:105-111). For mammals, [.H]b appears to be determined by complex interactions between their body size (Kleiber, 1932, 1961:206; Benedict, 1938; Brody, 1945:368-374; Hemmingsen, 1960:15-36; McNab, 1983b; Calder, 1987), the climate in which they live (Scholander et al., 1950c; McNab and Morrison, 1963; Hulbert and Dawson, 1974; Shkolnik and Schmidt-Nielsen, 1976; McNab, 1979a; Vogel, 1980), their food habits (McNab, 1978a, 1978b, 1980a, 1983a, 1984a, 1986a, 1986b, 1988a, 1989), and their circadian period (Aschoff and Pohl, 1970; Prothero, 1984). Some species have higher mass-specific [.H]{b} than others, and this variation appears to be tied to ecological circumstances rather than taxonomic affinities (McNab, 1988a, 1989). Basal metabolic rate is important ecologically because it serves as a measure of a species' minimum "obligatory" energy requirement, and under many circumstances, it represents the largest energy demand associated with a daily energy budget (King, 1974:38-55; McNab, 1980a; Mugaas and King, 1981:37-40). Recently it also has been implicated as a permissive factor with respect to r{max} of mammals (Hennemann, 1983; Lillegraven et al., 1987; Nicoll and Thompson, 1987; Thompson, 1987) via its direct effect on their rates of development and fecundity (McNab, 1980a, 1983a, 1986b; Hennemann, 1983; Schmitz and Lavigne, 1984; Glazier, 1985a, 1985b). The implication of this latter point is that those species with higher [.H]{b}'s also have faster rates of development and greater fecundity and hence enjoy the competitive advantage of a higher r_{max}. Basal metabolism is, therefore, "a highly plastic character in the course of evolution" (McNab, 1988a:25) that has a profound influence on each species' life history.

Minimum Thermal Conductance

Whole-body resistance to passive heat transfer is equal to tissue resistance plus coat resistance. Within limits, these resistances can be altered; tissue resistance can be varied by changes in blood flow, whereas coat resistance can be changed by piloerection, molt, and behavior. When whole-body resistance is maximized (maximum tissue and coat resistances), passive heat transfer is minimized. The inverse of resistance is conductance; therefore, maximum whole-body resistance is the inverse of minimum thermal conductance (C{m}). Minimum thermal conductance is readily derived from metabolic chamber data, and it is commonly used to describe an animal's capacity to minimize passive heat transfer. Minimum thermal conductance interacts with [.H]{b} and body mass to set the maximum temperature differential a mammal can maintain without increasing its basal level of heat production. The low temperature in this differential is the lower critical temperature (T_{lc}).

Mass-specific C{m} for mammals is negatively correlated with body mass (McNab and Morrison, 1963; Herreid and Kessel, 1967; McNab, 1970, 1979b; Bradley and Deavers, 1980; Aschoff, 1981), and for any given mass its magnitude is 52% higher during the active, rather than the inactive, phase of the daily cycle (Aschoff, 1981). However, some mammals have C{m}'s that are higher or lower than would be predicted for them on the basis of body mass and circadian phase. Seasonal variation in C{m} (higher values during summer than winter) has been reported for many northern mammals that experience large annual variations in air temperature (Scholander et al., 1950a; Irving et al., 1955; Hart, 1956, 1957; Irving, 1972:165). Some tropical mammals with very thin fur coats, and others with nearly hairless bodies, have high C{m}'s (McNab, 1984a), as do burrowing mammals (McNab, 1966, 1979b, 1984a) and the kit fox, Vulpes macrotis (Golightly and Ohmart, 1983). Some small mammals with low basal metabolic rates tend to have lower than predicted C{m}'s: small marsupials (McNab, 1978a), heteromyid rodents (McNab, 1979a), several ant eaters (McNab, 1984a), the arctic hare, Lepus arcticus (Wang et al., 1973), the ringtail, Bassariscus astutus (Chevalier, 1985), and the fennec, Fennecus zerda (Noll-Banholzer, 1979). Thus, in spite of its mass dependence, C{m} also has been modified during the course of evolution by selective factors in the environment and by the animal's own metabolic characteristics.

Capacity for Evaporative Cooling

Latent heat loss occurs as a result of evaporation from the respiratory tract and through the skin, and except under conditions of heat stress, it "is a liability in thermal and osmotic homeostasis" (Calder and King, 1974:302). E{c}, defined as the ratio of evaporative heat lost to metabolic heat produced, can be used to quantify thermoregulatory effectiveness of evaporative cooling and to make comparisons of heat tolerance between species. Thermoregulatory effectiveness of latent heat loss is not just a function of the rate of evaporative water loss but also of the rate of metabolic heat production (Lasiewski and Seymour, 1972). For example, a low metabolic rate minimizes endogenous heat load and thus conserves water, whereas the opposite is true of high metabolic rates (Lasiewski and Seymour, 1972). Some mammals that live in arid regions have evolved low metabolic rates and thus capitalize on this relationship to reduce their thermoregulatory water requirement (McNab and Morrison, 1963; McNab, 1966; MacMillen and Lee, 1970; Noll-Banholzer, 1979). What is evident, therefore, is that an animal's capacity for increasing latent heat loss must evolve together with its [.H]{b} and C_{m} in response to specific environmental demands.