Metabolic Adaptation to Climate and Distribution of the Raccoon Procyon Lotor and Other Procyonidae

Mugaas, J. N., J. Seidensticker, and K. Mahlke-Johnson. Metabolic Adaptation to Climate and Distribution of the Raccoon Procyon lotor and Other Procyonidae. Smithsonian Contributions to Zoology, number 542, 34 pages, 8 figures, 12 tables, 1993.—Although the family Procyonidae is largely a Neotropical group, the North American raccoon, Procyon lotor, is more versatile in its use of climate, and it is found in nearly every habitat from Panama to 60°N in Canada. We hypothesized that most contemporary procyonids have remained in tropic and subtropic climates because they have retained the metabolic characteristics of their warm-adapted ancestors, whereas Procyon lotor evolved a different set of adaptations that have enabled it to generalize its use of habitats and climates. To test this hypothesis we compared Procyon lotor with several other procyonids (Bassariscus astutus, Nasua nasua, Nasua narica, Procyon cancrivorus, and Potos flavus) with respect to (1) basal metabolic rate (Ḣb), (2) minimum wet thermal conductance (Cmw), (3) diversity of diet (Dd), (4) intrinsic rate of natural increase (rmax), and, where possible, (5) capacity for evaporative cooling (Ec). We measured basal and thermoregulatory metabolism, evaporative water loss, and body temperature of both sexes of Procyon lotor from north central Virginia, in summer and winter. Metabolic data for other procyonids were from literature, as were dietary and reproductive data for all species.

Procyon lotor differed from other procyonids in all five variables. (1) Procyon lotor's mass specific Ḣb (0.46 mL O2·g-1·h-1) was 1.45 to 1.86 times greater than values for other procyonids. (2) Because of its annual molt, Procyon lotor's Cmw was about 49% higher in summer than winter, 0.0256 and 0.0172 mL O2·g-1·h-1·°C-1, respectively. The ratio of measured to predicted Cmw for Procyon lotor in winter (1.15) was similar to values calculated for Potos flavus (1.02) and Procyon cancrivorus (1.25). Values for other procyonids were higher than this, but less than the value for Procyon lotor (1.76) in summer. On a mass specific basis, Bassariscus astutus had the lowest Cmw with a ratio of 0.85. (3) Procyon lotor utilized three times as many food categories as Procyon cancrivorus, Nasua nasua, and Bassariscus astutus; about two times as many as Nasua narica; and nine times as many as Potos flavus. (4) Intrinsic rate of natural increase correlated positively with Ḣb. Procyon lotor had the highest rmax (2.52 of expected) and Potos flavus the lowest (0.48 of expected). The other procyonids examined also had low Ḣb, but their rmax's were higher than predicted (1.11-1.32 of expected). Early age of first female reproduction, fairly large litter size, long life span, high-quality diet, and, in one case, female social organization all compensated for low Ḣb and elevated rmax. (5) Although data on the capacity for evaporative cooling were incomplete, this variable appeared to be best developed in Procyon lotor and Bassariscus astutus, the two species that have been most successful at including temperate climates in their distributions.

These five variables are functionally interrelated, and have co-evolved in each species to form a unique adaptive unit that regulates body temperature and energy balance throughout each annual cycle. The first four variables were converted into normalized dimensionless numbers, which were used to derive a composite score that represented each species' adaptive unit. Procyon lotor had the highest composite score (1.47) and Potos flavus the lowest (0.39). Scores for the other procyonids were intermediate to these extremes (0.64-0.79). There was a positive correlation between the number of climates a species occupies and the magnitude of its composite score. Linear regression of this relationship indicated that 89% of the variance in climatic distribution was attributed to the composite scores. Differences in metabolic adaptation, therefore, have played a role in delimiting climatic distribution of these species.

It was clear that Procyon lotor differed from the other procyonids with respect to thermoregulatory ability, diet, and reproductive potential. These differences have enabled it to become a highly successful climate generalist, and its evolution of an Ḣb that is higher than the procyonid norm appears to be the cornerstone of its success.

Official publication date is handstamped in a limited number of initial copies and is recorded in the Institution's annual report, Smithsonian Year. Series cover design: The coral Montastrea cavernosa (Linnaeus).

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Library of Congress Cataloging-in-Publication Data
Mugaas, John N.
Metabolic adaptation to climate and distribution of the raccoon Procyon lotor and other Procyonidae / John N. Mugaas, John Seidensticker, and Kathleen P. Mahlke-Johnson.
p. cm.—(Smithsonian contributions to zoology; no. 542)
Includes bibliographical references (p.       )
1. Raccoons-Metabolism-Climatic factors. 2. Procyonidae-Metabolism-Climatic factors. 3. Raccoons-Geographical distribution. 4. Procyonidae-Geographical distribution. I. Seidensticker, John. II. Mahlke-Johnson, Kathleen. III. Title. IV. Series.
QL1.S54 no. 542 [QL737.C26] 591 s-dc20 [599.74´443´04542] 93-3119

The paper used in this publication meets the minimum requirements of the American National Standard for Permanence of Paper for Printed Library Materials z39.48—1984.

  Page Introduction 1     Defining the Problem 1         Procyonid Origins 1        

href="@public@vhost@g@gutenberg@html@files@36036@[email protected]#Typical_Procyonids" class="pginternal" tag="{http://www.w3.org/1999/xhtml}a">Typical Procyonids 2         The Atypical Procyonid 3         The Hypothesis 4         Hypothesis Testing 4     Adaptive Significance of the Variables 4         Basal Metabolic Rate and Intrinsic Rate of Natural Increase 4         Minimum Thermal Conductance 4         Capacity for Evaporative Cooling 5         Diet 5     Experimental Design and Summary 5     Acknowledgments 5 Materials and Methods 6     Live-trapping 6     Metabolic Studies 6         Basal and Thermoregulatory Metabolism 6         Evaporative Water Loss 7         Body Temperature 7     Calibrations 7         Calorimeter 7         Body Temperature Transmitters 8     Statistical Methods 8     Estimating Intrinsic Rate of Natural Increase 8     Comparison of Adaptive Units 8 Results 8     Body Mass 8     Basal Metabolic Rate 9     Minimum Thermal Conductance 9     Evaporative Water Loss 11     Thermoregulation at Low Temperatures 12         Body Temperature 12         Summer 14         Winter 14     Thermoregulation at High Temperatures 16         Body Temperature 16  

      Summer 16         Winter 16     Daily Cycle of Body Temperature 16 Discussion 16     Basal Metabolic Rate 16         Background 16         Captive versus Wild Raccoons 17         Seasonal Metabolism of Raccoons 17         Comparison of Procyon lotor with Other Procyonids 17         Influence of Diet on Basal Metabolism 18                 Background 18                 Food Habits of Procyonids 18                 Food Habits and Basal Metabolism 19                 Summary 19         Basal Metabolism and Intrinsic Rate of Natural Increase 19                 Background 19                 Procyon lotor 19                 Bassariscus astutus 19                 Nasua narica 19                 Nasua nasua 20                 Procyon cancrivorus 20                 Potos flavus 20                 Summary 20         Basal Metabolism and Climatic Distribution 21                 Procyon lotor 21                 Other Procyonids 21     Minimum Thermal Conductance 21         Background 21         Effect of Molt on Thermal Conductance 21         Comparison of Thermal Conductances 22                 Procyon lotor versus Tropical Procyonids 22                 Bassariscus astutus 22    

tag="{http://www.w3.org/1999/xhtml}a">Thermoregulation and Use of Stored Fat at Low Temperatures 22         Background 22                 Thermoregulation 22                 Stored Fat 23         Thermal Model of the Raccoon and Its Den 23         Metabolic Advantage of the Den 23     Thermoregulation at High Temperatures 24         Background 24         Comparison of Procyonid Responses to Heat Stress 24                 Potos flavus 24                 Nasua nasua and Nasua narica 24                 Bassariscus astutus 24                 Procyon lotor 24                 Procyon cancrivorus 24                 Summary 24     Composite Scores of Adaptive Units and Geographic Distribution 25     Evolution of Metabolic Adaptations 26         Evolution of Low Basal Metabolic Rate 26         Evolution of High Basal Metabolic Rate 27     Summary 28 Appendix: List of Symbols 29 Literature Cited 30

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).

class="pginternal" tag="{http://www.w3.org/1999/xhtml}a">[C] 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).

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 Ḣb. 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 Ḣb's that are 40%-80% of the values predicted for them by the Kleiber (1961:206) equation. Lower than predicted Ḣb 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 Ḣb 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.

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.