Part 1

Produced by Colin Bell, Tom Cosmas, Joseph Cooper and the Online Distributed Proofreading Team at http://www.pgdp.net

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY . NUMBER 542

Metabolic Adaptation to Climate and Distribution of the Raccoon _Procyon lotor_ and Other Procyonidae

_John N. Mugaas, John Seidensticker, and Kathleen P. Mahlke-Johnson_

[Smithsonian Institution logo]

SMITHSONIAN INSTITUTION PRESS Washington, D.C. 1993

ABSTRACT

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 deg.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 ([.H]_{b}), (2) minimum wet thermal conductance (C_{mw}), (3) diversity of diet (D_{d}), (4) intrinsic rate of natural increase (r_{max}), and, where possible, (5) capacity for evaporative cooling (E_{c}). 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 [.H]_{b} (0.46 mL O_{2}.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 C_{mw} was about 49% higher in summer than winter, 0.0256 and 0.0172 mL O_{2}.g^{-1}.h^{-1}. deg.C^{-1}, respectively. The ratio of measured to predicted C_{mw} 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 C_{mw} 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 [.H]_{b}. _Procyon lotor_ had the highest r_{max} (2.52 of expected) and _Potos flavus_ the lowest (0.48 of expected). The other procyonids examined also had low [.H]_{b}, but their r_{max}'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 [.H]_{b} and elevated r_{max}. (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 [.H]_{b} 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).

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

[permanent paper symbol] 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.

Contents

_Page_ Introduction 1 Defining the Problem 1 Procyonid Origins 1 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 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

Metabolic Adaptation to Climate and Distribution of the Raccoon _Procyon lotor_ and Other Procyonidae

_John N. Mugaas, John Seidensticker, and Kathleen P. Mahlke-Johnson_

_John N. Mugaas, Department of Physiology, Division of Functional Biology, West Virginia School of Osteopathic Medicine, Lewisburg, West Virginia 24901. John Seidensticker and Kathleen P. Mahlke-Johnson, National Zoological Park, Smithsonian Institution, Washington, D.C. 20008._

$Introduction$

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_[a] (S.A.) _B. beddardi_[a] (S.A.) _B. gabbii_[a] (nS.A., C.A.) _B. lasius_[a] (C.A.) _B. pauli_[a] (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_[b] (nS.A., C.A., M., swU.S.) _N. nasua_[b] (S.A., sC.A.) Genus _Nasuella_ Hollister, 1915 _N. olivacea_ (S.A.) Genus _Procyon_ Storr, 1780 _P. cancrivorus_ (S.A., sC.A.) _P. gloveralleni_[c] (Barbados) _P. insularis_[c] (Maria Madre Is., Maria Magdalene Is.) _P. lotor_[c] (C.A., M., U.S., sC.) _P. maynardi_[c] (Bahamas, New Providence Is.) _P. minor_[c] (Guadeloupe Is.) _P. pygmaeus_[c] (M., Quintana Roo, Cozumel Is.)

[a] The several named forms of _Bassaricyon_ are a single species, _Bassaricyon gabbii_ (Wozencraft, 1989a).

[b] 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).

[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).

_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_ (Mueller and Kulzer, 1977; McNab, 1978a; Mueller 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 (Mueller and Kulzer, 1977; Chevillard-Hugot et al., 1980; Mueller 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 deg.N) to southern Canada. In Alberta, Canada, its range reaches the edge of the Hudsonian Life Zone at 60 deg.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_