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diff --git a/36036.txt b/36036.txt new file mode 100644 index 0000000..0f517b8 --- /dev/null +++ b/36036.txt @@ -0,0 +1,4264 @@ +The Project Gutenberg EBook of Metabolic Adaptation to Climate and +Distribution of the Raccoon Procyon Lotor and Other Procyonidae, by John N. Mugaas and John Seidensticker and Kathleen P. Mahlke-Johnson + +This eBook is for the use of anyone anywhere at no cost and with +almost no restrictions whatsoever. You may copy it, give it away or +re-use it under the terms of the Project Gutenberg License included +with this eBook or online at www.gutenberg.org + + +Title: Metabolic Adaptation to Climate and Distribution of the Raccoon Procyon Lotor and Other Procyonidae + +Author: John N. Mugaas + John Seidensticker + Kathleen P. Mahlke-Johnson + +Release Date: May 5, 2011 [EBook #36036] + +Language: English + +Character set encoding: ASCII + +*** START OF THIS PROJECT GUTENBERG EBOOK THE RACCOON PROCYON LOTOR *** + + + + +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. + + [Illustration: FIGURE 1.--North American raccoon, _Procyon lotor_.] + + +_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. + + +_Diet_ + +McNab (1986a, 1988a, 1989) demonstrated that, for mammals, departures +of [.H]_{b} from the Kleiber (1961:206) "norm" are highly correlated +with diet and independent of phylogenetic relationships. McNab's +analysis indicates that for mammals that feed on invertebrates, those +species with body mass less than 100 g have [.H]_{b}'s that are equal +to or greater than values predicted by the Kleiber equation, whereas +those with body mass greater than 100 g have metabolic rates that are +lower than predicted. Grazers, vertebrate eaters, nut eaters, and +terrestrial frugivores also have [.H]_{b}'s that are equal to or +greater than predicted, whereas insectivorous bats, arboreal +folivores, arboreal frugivores, and terrestrial folivores all have +rates that are lower than predicted. McNab (1986a) found animals with +mixed diets harder to categorize, but in general he predicted that +their [.H]_{b}'s would be related to (1) a food item that is +constantly available throughout the year, (2) a food item that is most +available during the worst conditions of the year, or (3) a mix of +foods available during the worst time of the year. Although these +correlations do not establish cause and effect between food habits and +[.H]_{b}, McNab's analysis does make it clear that the relationship +between these variables has very real consequences for an animal's +physiology, ecology, and evolution. + + + +EXPERIMENTAL DESIGN AND SUMMARY + + +In this investigation we measured basal and thermoregulatory +metabolism, evaporative water loss, and body temperature of raccoons +from north central Virginia. Measurements were conducted on both sexes +in summer and winter to determine how season and sex influenced these +variables. We then compared the data for this widely distributed +generalist with data from literature for its ecologically more +restricted relatives. Dietary data for all species were taken from +literature, as were reproductive data for calculation of r_{max}. + +Our analysis demonstrated clear differences between _Procyon lotor_ +and other procyonids with respect to [.H]_{b}, C_{mw}, D_{d}, and +r_{max}. The composite score calculated from these variables for +_Procyon lotor_ was much higher than those derived for other species, +and there was a positive correlation between the number of climates a +species occupies and the magnitude of its composite score. Data on +evaporative water loss, although not complete for all species, +suggested that tropical and subtropical procyonids have less capacity +for evaporative cooling than _Procyon lotor_ or _Bassariscus astutus_. +It was clear, therefore, that with respect to its thermal physiology, +_Procyon lotor_ differed markedly from other procyonids, and we +contend that these differences have allowed this species to become a +highly successful climate generalist and to expand its distribution +into many different habitats and climates. Our analysis also suggested +that the cornerstone of _Procyon lotor_'s success as a climate +generalist is its [.H]_{b}, which is higher than the procyonid norm. + + + +ACKNOWLEDGMENTS + + +The authors would like to thank John Eisenberg and Devra Kleiman for +their support and encouragement throughout the study. This +investigation was supported by research grants from the West Virginia +School of Osteopathic Medicine (WVSOM), and Friends of the National +Zoo (FONZ). Logistic support was provided by the National Zoological +Park's Conservation and Research Center (CRC), and the departments of +Mammalogy and Zoological Research. Our ability to conduct +physiological research at CRC was made possible by the thoughtful +support and encouragement provided by Chris Wemmer. His excellent +staff at CRC, especially Jack Williams, Junior Allison, and Red +McDaniel, were very helpful in providing hospitality and logistical +support to the senior author and his family during their various +visits to the Center. The assistance of several people at the National +Zoo also is gratefully acknowledged: Mitch Bush and Lyndsay Phillips +not only provided veterinary support throughout the investigation, +but also performed surgical procedures required to implant +temperature-sensitive radio transmitters in several raccoons; Olav +Oftedal made his laboratory available to us at various times and +loaned us equipment to use at CRC; Miles Roberts and his staff +provided care for our captive raccoons in the Department of Zoological +Research during various parts of the investigation. Greg Sanders and +Ken Halama, supported by FONZ assistantships, cared for our captive +raccoons at CRC, provided assistance in the laboratory whenever +needed, and were an invaluable source of aid. Their friendship and +help is gratefully acknowledged. Ellen Broudy and Andy Meyer, +supported by WVSOM and a student work study grant, respectively, +provided assistance in the laboratory. David Brown, John Eisenberg, +Mary Etta Hight, Brian McNab, Steve Thompson, and W. Chris Wozencraft +critically reviewed various phases of the manuscript and provided many +helpful suggestions. We deeply appreciate the work of Jean B. +McConville, whose beneficial editorial suggestions helped us improve +several early versions of the manuscript. We also gratefully +acknowledge Diane M. Tyler, our editor at the Smithsonian Institution +Press, whose expertise helped us mold the manuscript into its final +form. Jill Mellon and Sriyanie Miththalapa, supported by FONZ +traineeships, assisted in measuring the daily cycle of body +temperature in raccoons. The Virginia Commission of Game and Inland +Fisheries gave us permission to use wild-caught raccoons in this +project. + + + + +$Materials and Methods$ + + + +LIVE-TRAPPING + + +Raccoons were caught from May 1980 through December 1984 on a trapping +grid of 30 to 35 stations (one or two "live traps" per station) that +covered about one-third of the National Zoological Park's Conservation +and Research Center (CRC) near Front Royal, Virginia (Seidensticker et +al., 1988; Hallett et al., 1991). Animals were trapped during 10 +consecutive days each month, and in this five-year interval 407 +raccoons were captured and marked with tattoos and ear tags. All +captured animals were individualized with respect to age, reproductive +status, physical condition, parasite load, and mass and body +dimensions. These data characterized the structure and dynamics of the +raccoon population at CRC and provided information on the annual +cycle of fattening for raccoons in north central Virginia. + +Animals used for metabolic measurements were captured at CRC about +1.5 km south of the trapping grid and thus were genetically +representative of the area. Six males were captured and measured during +the summer of 1983. These animals were kept isolated for a week before +being measured and were released later that summer at the site of their +capture. The other seven animals used in our study were from the +collection of the National Zoological Park and all of them had their +origins at CRC. + + + +METABOLIC STUDIES + + +_Basal and Thermoregulatory Metabolism_ + +Metabolic measurements, conducted at CRC, were carried out on eight +males during July and August 1983, on four females and three males +from November 1983 through March 1984, and on four females during June +and July 1984. + +Raccoons were housed throughout the study such that they were +constantly exposed to a natural cycle of temperature and photoperiod. +Weather records for the Front Royal area indicate that average +temperatures are around -0.5 deg.C in January and 23.3 deg.C in July +(Crockett, 1972). Light:dark (L:D) periods for the latitude of CRC +(48 deg.55'N; United States Department of the Interior Geological Survey, +1972), calculated from duration of daylight tables (List, 1971:506-512), +were 14.9:9.1 and 9.4:14.6 hours L:D for summer and winter solstices, +respectively, and 12.2:11.8 hours L:D for vernal and autumnal equinoxes. + +Our animals were fed a measured amount of food daily, and they usually +ate most of what was provided. Occasionally these animals would eat +very little or none of their ration, and on some days they would eat +all that was given to them. We fed them either feline diet (ground +horse meat) or canned mackerel (Star-kist(R)[1]) along with +high-protein dog chow (Purina(R)). When available, fresh fruit also +was added to their diet. Water was always provided ad libitum. + + [1] _The use of product brand names in this publication is + not intended as an endorsement of the products by the + Smithsonian Institution._ + +Measurements were conducted during the raccoons' daily inactive period +(sunrise to sunset) in both summer and winter. Oxygen consumption was +measured in a flow-through metabolism chamber at 5 deg.C intervals from +-10 deg.C to 35 deg.C. Animals were held at each temperature until the lowest +rate of oxygen consumption had been obtained and maintained for at +least 15 minutes. During each determination, oxygen consumption was +monitored for 30 minutes to one hour beyond a suspected minimum value +to see if an even lower reading could be obtained. Raccoons attained +minimum levels of oxygen consumption more quickly at warm (>10 deg.C) than +at cold temperatures. Depending on the temperature, therefore, each +measurement took from two to five hours to complete. On days when two +measurements could be completed, the second trial was always at a +temperature 10 deg.C warmer than the first. + +The metabolism chamber was constructed from galvanized sheet metal +(77.5 x 45.5 x 51.0 cm = 180 liters) and was painted black inside. +Within the chamber, the animal was held in a cage (71 x 39 x 33 cm) +constructed from turkey wire that also was painted black. This cage +prevented the raccoons from coming into contact with the walls of the +chamber, yet it was large enough to allow them to stand and freely +move about. The bottom of the cage was 11 cm above the chamber floor, +which was covered to a depth of one cm with mineral oil to trap urine +and feces. + +During measurements, the metabolism chamber was placed in a +controlled-temperature cabinet (modified Montgomery Ward model 8969 +freezer). Air temperature (T_{a}) in the metabolism chamber was +regulated with a Yellow Springs Instrument model 74 temperature +controller. T_{a} was controlled to +-1.0 deg.C at temperatures below +freezing, and to +-0.5 deg.C at temperatures above freezing. The chamber +air and wall temperatures were recorded continuously (Linseis model +LS-64 recorder) during each experiment, and, except during temperature +changes, they were always within 0.5 deg.C of each other. + +Columns of Drierite(R) and Ascarite(R) removed water vapor and carbon +dioxide, respectively, from air entering and leaving the chamber. Dry +carbon-dioxide-free room air was pumped into the chamber (Gilman model +13152 pressure/vacuum pump) at a rate of 3.0 L/min (Gilmont model +K3203-20 flow meter). Downstream from the chemical absorbents, an +aliquot (0.1 L/min) of dry carbon-dioxide-free air was drawn off the +chamber exhaust line and analyzed for oxygen content (Applied +Electrochemistry model S-3A oxygen analyzer, model 22M analysis cell, +and model R-1 flow control). All gas values were corrected to standard +temperature and pressure for dry gas. Oxygen consumption was +calculated from the difference in oxygen content between inlet and +outlet air using Eq. 8 of Depocas and Hart (1957). + +Each raccoon was fasted for at least 12 hours before oxygen +consumption measurements began. At the start and end of each metabolic +trial the animal was weighed to the nearest 10 g (Doctors Infant +Scale, Detecto Scales, Inc., Brooklyn, N.Y., U.S.A.). The body mass +used in calculating minimum oxygen consumption and evaporative water +loss was estimated from timed extrapolations of the difference between +starting and ending weights, and the time at which these variables +were measured. + + +_Evaporative Water Loss_ + +During metabolic measurements at temperatures above freezing, +evaporative water loss was determined gravimetrically. Upstream from +the chemical columns, an aliquot of air (0.1 L/min) was drawn off the +exhaust line and diverted for a timed interval through a series of +preweighed (0.1 mg) U-tubes containing Drierite(R). The aliquot then +passed through a second series of U-tubes containing Ascarite(R) +before entering the oxygen analysis system. Evaporative water loss was +calculated using Eq. 1 + + [.E] = (m_{w}.[.V]_{e})/([.V]_{a}.t.m) Eq. 1 + +where [.E] is evaporative water loss (mg.g^{-1}.h^{-1}), m_{w} is mass +of water collected (mg), [.V]_{e} is rate of air flow into the chamber +(3.0 L/min), [.V]_{a} is rate of air flow through the U-tubes +(0.1 L/min), t is length of the timed interval (h), and m is the +estimated mass of the raccoon at the time of sampling (g). + + +_Body Temperature_ + +Veterinarians at the National Zoological Park surgically implanted +calibrated temperature-sensitive radio transmitters (Telonics, Inc., +Mesa, AZ, U.S.A.) into abdominal cavities of two female and two male +raccoons. Transmitter pulse periods were monitored with a digital +processor (Telonics TDP-2) coupled to a receiver (Telonics +TR-2-164/166). During some metabolic measurements, body temperatures +of these animals were recorded to the nearest 0.1 deg.C at 30-minute +intervals. The daily cycle of body temperature of these raccoons also +was measured once a month. + + + +CALIBRATIONS + + +_Calorimeter_ + +At the conclusion of these experiments, the accuracy of our +calorimetry apparatus was tested by burning an ethanol lamp in the +metabolism chamber. During these tests a CO_{2} analyzer was +incorporated into the system (Beckman, LB-2). Results demonstrated +that we measured 84% of the oxygen consumed by the lamp as well as 84% +of the water and CO_{2} it produced; standard deviation = +-2.6, +-5.0, +and +-3.6, respectively (n = 27). Average respiratory quotient (RQ) +calculated from these data was O.657 +-0.008 (n = 27), which is 99.5% +of that predicted (0.66). McNab (1988b) reports that the accuracy of +open-flow indirect calorimetry systems, such as ours, depends on the +rate of air flow through the animal chamber. If flow rates are too +low, there is inadequate mixing of air within the chamber, and the +rate of oxygen consumption, as calculated from the difference in +oxygen content of air flowing into and out of the chamber (Depocas and +Hart, 1957), is underestimated. At some critical rate of air flow, +which is unique to each combination of chamber and animal, this +situation changes such that measured rates of oxygen consumption +become independent of any further increase in flow rate (McNab, +1988b). In recent tests of our system, where we burned the ethanol +lamp at a variety of chamber flow rates, the efficiency of +measurement increased linearly as flow rate increased, and the +critical rate of air flow was about 6.7 L/min. This appeared to +explain why a flow rate of 3.0 L/min underestimated oxygen consumption +of the ethanol lamp. + +Our earlier tests of the efficiency of our system indicated that +although we underestimated actual oxygen consumption of the ethanol +lamp, we did so with a fair degree of precision; probably because flow +rates were closely controlled. During our metabolic measurements, +chamber flow rates also were closely controlled at 3.0 L/min, and we +believe, therefore, that these measurements also were carried out with +a high degree of precision. Consequently, all measured values of +oxygen consumption and water production were considered to be 84% of +their actual value and were adjusted to 100% before being included in +this report. + + +_Body Temperature Transmitters_ + +The calibration of all temperature-sensitive radio transmitters +drifted over time. Transmitters were calibrated before they were +surgically implanted and again after they were removed from the +animals. Although the drift of each transmitter was unique, it was +also linear (S. Tomkiewicz, Telonics, Inc., pers. com.). All body +temperature measurements were corrected from timed extrapolations of +the difference between starting and ending calibrations. + + + +STATISTICAL METHODS + + +Values of oxygen consumption, evaporative water loss, and body +temperature were plotted as a function of chamber air temperature. +Linear regressions of oxygen consumption at temperatures below the +thermoneutral zone (T_{n}), and evaporative water loss at temperatures +above freezing, were determined with the SAS (1982) GLM procedure. +Lower critical temperature (T_{lc}) was determined graphically from +intersection of the line representing [.H]_{b} and the regression line +representing oxygen consumption below T_{n}. Slopes and intercepts of +regression lines, as well as other mean values, were compared with +_t_-tests (Statistical Analysis System, 1982; Ott, 1984:138-175). +Unless indicated otherwise, data are expressed as mean +- standard +deviation (s.d.). + + + +ESTIMATING INTRINSIC RATE OF NATURAL INCREASE + + +We employed the method first described by Cole (1954) to calculate +r_{max}: + + 1 = e^{-r_{max}} + b.e^{-r_{max}(a)} - b.e^{r_{max}(n+1)} Eq. 2 + +where a is potential age of females first producing young, b is +potential annual birth rate of female young, and n is potential age of +females producing their final young. After life-history data were +substituted into Eq. 2, r_{max} was determined by trial and error +substitution (Hennemann, 1983). + +Because r_{max} represents the genetically fixed, physiologically +determined maximum possible rate of increase, data on earliest +possible age of female reproduction, highest possible birth rate of +female young, and longest possible female reproductive life span were +used for a, b, and n, respectively. Calculated values, therefore, +represent physiologically possible, not ecologically possible, +intrinsic rates of increase (Hennemann, 1983, 1984; Hayssen, 1984; +McNab, 1984b). Values of n were derived from longevity records for +captive animals, and as these were all large values of similar +duration (14-16 years), they had very little effect on r_{max}. All +species considered have one litter per year, and because their sex +ratios at birth are about 50:50, variation in b was due to differences +in litter size. Therefore, age of first reproduction and litter size +had the greatest effect on r_{max}. Intrinsic rate of increase scales +to body mass (Fenchel, 1974), and we removed this effect by comparing +each calculated r_{max} with the value expected (r_{maxe}) on the +basis of body mass (Hennemann, 1983). + + + +COMPARISON OF ADAPTIVE UNITS + + +Dimensionless numbers for each of the four variables used in +calculating composite scores were derived as follows. Ratios of +measured to predicted values were used for basal metabolism (H_{br}) +and minimum wet thermal conductance (C_{mwr}). Thermoregulatory +ability at low temperatures is closely related to the ratio +H_{br}/C_{mwr} (McNab, 1966). This ratio was used, therefore, to gauge +each species' cold tolerance. For D_{d} we used the ratio of food +categories actually used by a species to the total number of food +categories taken by all species tested (D_{dr}). The ratio of +calculated to expected intrinsic rates of natural increase was used to +derive r_{maxr}. Composite scores were calculated as + + Composite score = [(H_{br}/C_{mwr}) + D_{dr} + r_{maxr}]/3 Eq. 3 + +The correlation between number of climates these species occupy and +their composite scores was tested by linear regression. + + + + +$Results$ + + + +BODY MASS + + +According to monthly live-trapping records, the body mass of +free-ranging female raccoons increased from 3.6 +-0.6 kg during summer +to 5.6 +-0.8 kg in early winter, and the mass of free-ranging males +increased from 4.0 +-0.5 to 6.7 +-0.9 kg during the same interval. These +seasonal changes in body mass were due to fluctuations in the amount +of body fat and represent a mechanism for storing energy during fall +for use in winter. In summer, captive and trapped male and captive +female raccoons had the same body mass (4.73 +-0.61, 4.41 +-0.70, and +4.67 +-0.88 kg, respectively, Table 2). Mass of captive females did +not change between seasons, whereas captive males were heavier in +winter than summer (p<0.005; Table 2). This seasonal change in mass of +our captive males was of a much smaller magnitude (0.6 kg) than that +observed for wild males (2.7 kg). During winter, captive males (5.34 ++-1.39 kg) were heavier than captive females (4.49 +-0.98 kg; p<0.005; +Table 2). Thus, our captive animals maintained a body mass throughout +the year that was intermediate to the range of values found for wild +raccoons in the same area. + + + TABLE 2.--Body mass in kg and basal metabolism + (mL O_{2}.kg^{-0.75}.h^{-1}) of _Procyon lotor_ + in summer and winter (s.d. = standard deviation + and n = number of observations). + + ----------------+----------------------------------------------------- + Season and sex | Body mass, +-s.d., (n) Basal metabolism, +-s.d., (n) + ----------------+----------------------------------------------------- + Summer | + Trapped male | 4.41 +-0.70 (52) 780 +-112 (20) + Captive male | 4.73 +-0.61 (22) 680 +-102 (8) + Captive female| 4.67 +-0.88 (41) 618 +- 92 (13) + Winter | + Captive male | 5.34 +-1.39 (31) 704 +- 81 (19) + Captive female| 4.49 +-0.98 (42) 667 +-139 (25) + ----------------+----------------------------------------------------- + + + +BASAL METABOLIC RATE + + +Within thermoneutrality, [.H]_{b} (mL O_{2}.g^{-1}.h^{-1}) was +0.54 +-0.09 for trapped males in summer, 0.46 +-0.07 for captive males +in summer, 0.42 +-0.07 for captive females in summer, 0.47 +-0.06 for +captive males in winter, and 0.46 +-0.10 for captive females in winter +(Figures 2, 3). Ratios of these measured values to those predicted by +the Kleiber (1932, 1961:206) equation are 1.28, 1.12, 1.02, 1.17, and +1.09, respectively. To minimize the effect of body size (Mellen, 1963) +and to facilitate comparisons between sexes and seasons and between +captive and trapped animals, basal metabolism also was calculated as a +function of metabolic body size (mL O_{2}.kg^{-0.75}.h^{-1}; Table 2). +Based on this analysis, trapped summer males had a higher basal +metabolism than captive males (p<0.025) or females (p<0.005) in either +season (Table 2). There was no difference in basal metabolism between +captive males and females in either summer or winter, and there was no +seasonal difference in their basal metabolic rates (Table 2). + + + +MINIMUM THERMAL CONDUCTANCE + + +Minimum wet and dry thermal conductances were calculated using Eqs. 4 +and 5 + + C_{mw} = [.H]_{r} / (T_{b} - T_{a}) Eq. 4 + + C_{md} = ([.H]_{r} - [.E]_{eq}) / (T_{b} - T_{a}) Eq. 5 + +where C_{mw} is wet and C_{md} is dry conductance +(mL O_{2}.g^{-1}.h^{-1}. deg.C^{-1}); [.H]_{r} is the lowest resting +metabolic rate measured at each temperature (mL O_{2}.g^{-1}.h^{-1}); +[.E]_{eq} is oxygen equivalent for heat lost by evaporation +[[.E]_{eq} = mL O_{2}.g^{-1}.h^{-1} = [.E].[lambda]/[gamma], where +[.E] is evaporative water loss (mg.g^{-1}.h^{-1}), [lambda] is heat of +vaporization for water (2.43 J/mg), and [gamma] is heat equivalent for +oxygen (20.097 J/mL)]; T_{b} is body temperature ( deg.C); and T_{a} is +chamber air temperature ( deg.C). Only data from animals equipped with +temperature-sensitive radio transmitters were used for these +calculations. + + + TABLE 3.--Minimum wet and dry thermal conductances + (mL O_{2}.g^{-1}.h^{-1}. deg.C^{-1}) of _Procyon lotor_ in summer + and winter. Means of values were calculated from equations 3 + and 4 (s.d. = standard deviation and n = number of observations). + + ----------------------+---------------------------------------- + | Thermal conductance + Season and sex |---------------------------------------- + | Wet +-s.d. (n) Dry +-s.d. (n) + ----------------------+---------------------------------------- + Summer | + Captive, both sexes | 0.0256 +-0.0028 (18) 0.0246 +-0.0019 (12) + Winter | + Captive, female | 0.0172 +-0.0023 (10) 0.0161 +-0.0027 (6) + ----------------------+---------------------------------------- + + + [Illustration: FIGURE 2.--Relationship between oxygen consumption + and chamber air temperature for raccoons in summer: captive + females, open circles; captive males, closed circles; trapped + males, open squares. Sloping lines represent regressions of oxygen + consumption on chamber air temperature, and horizontal lines, basal + metabolism.] + + [Illustration: FIGURE 3.--Relationship between oxygen consumption + and chamber air temperature for raccoons in winter: captive + females, open circles; captive males, closed circles. Solid sloping + line represents regression of oxygen consumption on chamber air + temperature for males and females, and the horizontal line, basal + metabolism for males and females.] + +C_{mw} was calculated for each season from metabolic measurements made +at all air temperatures below T_{lc} (Table 3). Because evaporative +water loss was not measured at temperatures below freezing, C_{md} +was calculated only from metabolic determinations made at air +temperatures between T_{lc} and 0 deg.C. There was no difference +between males and females in summer for either C_{mw} or C_{md} +(mL O_{2}.g^{-1}.h^{-1}. deg.C^{-1}). Data for each sex were combined +to give a summer average of 0.0256 +-0.0028 for C_{mw}, and 0.0246 ++-0.0019 for C_{md} (Table 3). These summer conductances were 49% higher +(p<0.005) than those calculated for winter females (0.0172 +-0.0023, and +0.0161 +-0.0027 for C_{mw} and C_{md}, respectively; Table 3). C_{mw} and +C_{md} were not different from each other in either summer or winter, +which indicated that in both seasons evaporative water loss contributed +very little to heat dissipation at temperatures below T_{n}. Comparisons +of thermal conductances calculated on the basis of metabolic body size +(Mellen, 1963) gave the same results. + + + +EVAPORATIVE WATER LOSS + + +Evaporative water loss increased as chamber temperature increased in +both summer and winter (Figures 4, 5). In summer, the pattern of +increase was different for females and males. Polynomial regressions +for trapped and captive males produced equations that describe a +concave relationship between T_{a} and evaporative water loss, whereas +the equation for females describes a sigmoid curve (Table 4; Figure 4). +For females, water loss increased rapidly at temperatures above 25 deg.C +(Figure 4). The intercepts and coefficients of the X, X squared, and X cubed terms +of the polynomial regression equations (Table 4) were compared +(_t_-tests) to determine if they differed from each other. The +coefficients in the equation for trapped males differed from those for +captive females in the X squared (p<0.05) and X cubed (p<0.025) terms. The +intercept and coefficients of the equation for captive males, however, +were not different from those for either captive females or trapped +males. Although this lack of difference is understandable in the case +of trapped males, where the shape of the two curves is similar +(concave), it is not so clear for the sigmoid curve of captive females +(Figure 4). Perhaps the lack of difference in this case is simply due +to the small number of observations available for captive males (n = 10; +Table 4). Nonetheless, in summer at 35 deg.C, both captive and trapped +males relied less on evaporative cooling than did captive females +(Figure 4). + +In winter, males and females had similar rates of evaporative water +loss across the full range of temperatures tested (Figure 5). +Therefore, data for both sexes were combined. The intercept and +coefficients of this equation (Table 4) did not differ from those for +summer females, but they did differ from those in the regression for +trapped males in the X squared (p<0.05) and X cubed (p<0.025) terms. As was +the case for females in summer, rates of water loss for winter animals +increased most rapidly at temperatures above 25 deg.C (Figure 5). + + [Illustration: FIGURE 4.--Relationship between evaporative water + loss and chamber air temperature for raccoons in summer: captive + females, open circles; captive males, closed circles; trapped + males, open squares. Lines represent polynomial regressions of + evaporative water loss on chamber air temperature.] + + [Illustration: FIGURE 5.--Relationship between evaporative water + loss and chamber air temperature for raccoons in winter: captive + females, open circles; captive males, closed circles. Lines + represent polynomial regressions of evaporative water loss on + chamber air temperature.] + + + TABLE 4.--Polynomial regression equations describing evaporative + water loss (mg.g^{-1}.h^{-1}) of _Procyon lotor_ in summer and + winter (X = chamber temperature ( deg.C), Y = evaporative water loss, + n = number of observations, R squared = coefficient of determination, and + SEE = standard error of estimate). + + --------------+-------------------------------------------------------- + Season and sex| Equation (n) R squared + --------------+-------------------------------------------------------- + Summer | + Trapped male |Y = 0.1899 + 0.0114.X + 0.0011.X squared - 0.00002.X cubed (32) 0.86 + SEE | 0.0885 0.0223 0.0015 0.00003 + Captive male |Y = 0.2174 + 0.0192.X + 0.0009.X squared - 0.00003.X cubed (10) 0.73 + SEE | 0.3983 0.0834 0.0048 0.00008 + Captive | + female |Y = 0.0127 + 0.0943.X - 0.0060.X squared + 0.00013.X cubed (31) 0.64 + SEE | 0.2218 0.0547 0.0036 0.00006 + Winter | + Captive, | + both sexes |Y = 0.1550 + 0.0426.X - 0.0025.X squared + 0.00006.X cubed (57) 0.80 + SEE | 0.0734 0.0192 0.0013 0.00002 + --------------+-------------------------------------------------------- + + + +THERMOREGULATION AT LOW TEMPERATURES + + +_Body Temperature_ + +Body temperatures in Figure 6 are those recorded during metabolic +measurements from animals equipped with surgically implanted, +temperature-sensitive radio transmitters. Each point was recorded +during the lowest level of oxygen consumption at each T_{a}. In both +summer and winter, T_{b}'s were lowest during metabolic measurements +at T_{a}'s around T_{lc}. At T_{a}'s below T_{lc}, T_{b}'s increased +(Figure 6), which is an unusual response. Under similar conditions, +other procyonids either maintain a nearly constant T_{b} or allow it +to fall slightly (Mueller and Kulzer, 1977; Chevillard-Hugot et al., +1980; Mueller and Rost, 1983; Chevalier, 1985). For our raccoons, +confinement in the metabolism chamber at low temperatures must have +stimulated a greater than necessary increase in metabolic rate such +that heat production exceeded heat loss, which caused T_{b} to become +elevated. + + [Illustration: FIGURE 6.--Relationship between body temperature and + chamber air temperature in summer (panel A), and winter (panel B): + captive females, open circles and solid lines; captive males, solid + circles and dashed lines. Solid vertical lines represent lower + critical temperatures.] + + + TABLE 5.--Regression equations describing oxygen consumption + (mL O_{2}.g^{-1}.h^{-1}) of _Procyon lotor_ at temperatures below + their lower critical temperature (I = x-intercept ( deg.C), n = number + of observations, R squared = coefficient of determination, SEE = standard + error of estimate for the y-intercept (a) and slope (b), X = chamber + temperature ( deg.C), and Y = oxygen consumption). + + ----------------+------------------------------------------------------ + Season | SEE + and sex | ----------- + | Equation (n) R squared a b I + ----------------+------------------------------------------------------ + Summer | + Trapped male | Y = 1.09 - 0.0281.X (30) 0.64 0.0353 0.0040 38.8 + Captive male | Y = 0.97 - 0.0258.X (12) 0.91 0.0235 0.0025 37.6 + Captive female| Y = 1.04 - 0.0251.X (29) 0.78 0.0288 0.0026 41.1 + Winter | + Captive, | + both sexes | Y = 0.68 - 0.0193.X (36) 0.68 0.0157 0.0023 35.2 + ----------------+------------------------------------------------------ + + +_Summer_ + +During summer, T_{lc} for male raccoons was 20 deg.C, whereas for females +it was 25 deg.C (Figure 2). Regression equations calculated to describe +oxygen consumption at T_{a}'s below T_{lc} are presented in Table 5. +For three groups of summer animals, slopes of regressions are +identical. This indicates that minimum conductances of these three +groups were equivalent. Intercepts of these equations are different, +which suggests a difference in metabolic cost of thermoregulation +between these groups (Figure 2); captive males had a lower intercept +than either trapped males (p<0.005) or captive females (p<0.05), but +there was no difference in intercepts of captive females and trapped +males. These regression equations, therefore, also were derived using +values of oxygen consumption expressed in terms of metabolic body mass +(Mellen, 1963). Relationships between intercepts of these equations +are different than those for regressions in Table 5. Intercept for +females was intermediate to, and not different from, those of the two +groups of males. However, captive males still had a lower intercept +than trapped males (p<0.025). Thus, in summer, thermoregulatory +metabolism was less expensive for captive than for trapped males, and +in spite of a 5 deg.C difference in their T_{lc}'s (Figure 2), captive +males and females had similar thermoregulatory costs. + +Regression lines for three groups of animals in summer extrapolate to +zero metabolism at values equivalent to, or greater than, normal +T_{b}; 38.8 deg.C for trapped males, 37.6 deg.C for captive males, and 41.1 deg.C +for captive females (Table 5). Thus, all three groups had minimized +thermal conductance at T_{a}'s below T_{lc} (Scholander et al., 1950b; +McNab, 1980b). Minimum wet thermal conductance calculated for raccoons +in summer with Eq. 4 (Table 3) is numerically similar to these "slope" +values (Table 5), and it was, therefore, considered to be the best +estimate of C_{mw} for _Procyon lotor_ during that season +(0.0256 mL O_{2}.g^{-1}.h^{-1}. deg.C^{-1}). + + +_Winter_ + +During winter T_{lc} for both sexes decreased to 11 deg.C (Figure 3). +Regression equations of thermoregulatory metabolism for males and +females in winter are not different from each other in either slope or +intercept. These data, therefore, were combined into a single equation +(Table 5). Slope and intercept of this equation are both lower +(p<0.005 and p<0.05, respectively) than those for summer animals +(Table 5). Identical results were obtained from comparisons using +regressions derived from oxygen consumption expressed in terms of +metabolic body mass (Mellen, 1963). Thermoregulatory costs at any +temperature below 20 deg.C were lower for winter than summer animals +(Figures 2, 3). + + + TABLE 6.--Regression equations describing oxygen consumption + (mL O_{2}.g^{-1}.h^{-1}) of _Procyon lotor_ at temperatures below + their lower critical temperature in winter (A = females with radio + transmitters, B = females without radio transmitters, C = males, + I = x-intercept ( deg.C), n = number of observations, R squared = coefficient + of determination, X = chamber temperature ( deg.C), and Y = oxygen + consumption). + + -----+-------------------------------------- + Group| Equation (n) R squared I + -----+-------------------------------------- + A | Y = 0.63 - 0.0158.X (10) 0.66 40.1 + B | Y = 0.72 - 0.0226.X (11) 0.71 32.1 + C | Y = 0.69 - 0.0200.X (15) 0.79 34.7 + -----+-------------------------------------- + + + [Illustration: FIGURE 7.--Relationship between body temperature and + time of day at various months of the year: captive females, open + circles; captive males, closed circles. Vertical cross-hatched + areas represent civil twilight.] + +The regression line for _Procyon lotor_ in winter (Table 5) +extrapolates to zero metabolism at 35.2 deg.C, which is below normal T_{b} +(Figures 6, 7). This suggests that not all raccoons measured in winter +minimized thermoregulatory metabolism or conductances at T_{a}'s below +T_{lc} (Scholander et al., 1950b; McNab, 1980b). To assess this +possibility, data for these animals were divided into three groups: +(A) females with radio transmitters, (B) females without radio +transmitters, and (C) males (Table 6). Regression equations of +metabolism below T_{lc} were derived for each group, and based on +extrapolated T_{b}'s at zero metabolism, only the two females with +implanted radio transmitters (group A) minimized thermoregulatory +metabolism and conductance. Had animals in groups B and C also +minimized their thermal conductances, while retaining their measured +metabolic rates, their rates of heat production would have been +disproportionately higher than their rates of heat loss. Equation 4 +predicts that under these conditions their body temperatures would +have been elevated to 42.0 deg.C and 40.4 deg.C, respectively. Thus, in order +to avoid such a large increase in body temperature, animals in groups +B and C increased their thermal conductances in preference to lowering +their metabolic rates. The regression equation of thermoregulatory +metabolism for all winter animals (Table 5), therefore, overestimates +minimum metabolic cost of temperature regulation below T_{lc}, and its +slope underestimates C_{mw}. Consequently, the best estimate of C_{mw} +for _Procyon lotor_ in winter is the value calculated for group A +animals with Eq. 4 (0.0172 mL O_{2}.g^{-1}.h^{-1}. deg.C^{-1}; Table 3), +and the minimum cost of thermoregulatory metabolism at any T_{a} below +T_{lc} is best estimated by substituting this value into Eq. 4 and +solving for [.H]_{r}. + + + +THERMOREGULATION AT HIGH TEMPERATURES + + +_Body Temperature_ + +In both summer and winter, T_{b}'s increased during metabolic +measurements at T_{a}'s above T_{lc} (Figure 6). This response also +was seen during metabolic measurements conducted on other procyonids +(Mueller and Kulzer, 1977; Chevillard-Hugot et al., 1980; Mueller and +Rost, 1983; Chevalier, 1985). + + +_Summer_ + +During summer our data suggested that the upper critical temperature +(T_{uc}) was higher than 35 deg.C. The lowest rates of oxygen consumption +at T_{a} = 35 deg.C occurred after 1.5 to 2.5 hours of exposure to that +temperature. Prolonged exposure to this temperature in summer did not +make animals restless, and their rate of oxygen consumption was very +stable throughout each measurement. Body temperature responses at +T_{a} = 35 deg.C were recorded from two males and two females that had +implanted radio transmitters. With the exception of one male, T_{b}'s +were maintained near 38 deg.C (Figure 6). The one exception (a male) +maintained its T_{b} at 39.3 deg.C. At T_{a} = 35 deg.C, summer males had +rates of evaporative water loss that were lower than those of summer +females (Figure 4). At this temperature, males dissipated 35% +-6% and +females 56% +-18% of their metabolic heat via evaporative water loss. +Thus, at T_{a} = 35 deg.C, males must have utilized modes of heat transfer +other than evaporative cooling (convective and conductive heat +transfer) to a greater extent than females. + + +_Winter_ + +Body temperature, evaporative water loss, and metabolic data indicated +that, in winter, T_{uc} was very close to 35 deg.C. In winter, the lowest +level of oxygen consumption was recorded during the first hour after +the chamber had reached T_{a} = 35 deg.C. Unlike summer, animals became +restless after the first hour at 35 deg.C, at which point their oxygen +consumption increased and showed a high degree of variability. Body +temperature responses at 35 deg.C were recorded from both females that had +implanted radio transmitters. In one case, T_{b} rose from 37.9 deg.C at +the end of the first hour to 40.5 deg.C by the end of the second hour, and +as it did not show signs of leveling off, we terminated the +experiment. We exposed that same animal to T_{a} = 35 deg.C one other time +during winter. In that instance, its T_{b} rose to 40.0 deg.C during the +first 30 minutes and was maintained at that level for three hours with +no apparent distress. The other female elevated its T_{b} from 37.3 deg.C +to 39.0 deg.C during the second hour at T_{a} = 35 deg.C and maintained its +T_{b} at that level for two hours. Thus, during winter, prolonged +exposure to T_{a} = 35 deg.C stimulated more of an increase in T_{b} than +it did in summer. During winter, both males and females increased +evaporative water loss at T_{a} = 35 deg.C (Figure 5) but only to the +extent that they dissipated 35% +-10% of their metabolic heat +production. Thus, even in winter, convective and conductive heat +transfers were still the most important modes of heat loss at this +temperature. + + + +DAILY CYCLE OF BODY TEMPERATURE + + +The daily cycle of raccoon T_{b}'s during summer and winter are +presented in Figure 7. In general, T_{b}'s showed a marked circadian +cycle in phase with photoperiod. T_{b}'s rose above 38 deg.C for several +hours each night but remained below 38 deg.C during daytime. During +summer, with the exception of one female whose record was not typical +(Figure 7), T_{b}'s rose above 38 deg.C shortly after sunset, whereas in +winter T_{b}'s did not rise above 38 deg.C until several hours after +sunset. Once T_{b} was elevated it usually remained so until just +before or after sunrise (Figure 7). During summer, T_{b} was above +38 deg.C for 85% or more of the time between sunset and sunrise (87% for +the female with the typical body temperature pattern, and 85% and 98% +for males), whereas in winter it was elevated for only 47%-78% of the +time between sunset and sunrise (47% and 61% for females, and 67% and +78% for males). During night, T_{b} would oscillate between 38 deg.C and +about 39 deg.C, such that two peak values occurred. These peak values +presumably corresponded to two periods of heightened nighttime +activity. During summer, one of these peaks occurred before and the +other after 24:00 hours, whereas in winter both peaks occurred after +24:00 hours. With the exception of one female in winter (Figure 7), +the lowest T_{b} of the day for both sexes was near 37 deg.C, and this +typically occurred during daytime (Figure 7). + + + + +$Discussion$ + + + +BASAL METABOLIC RATE + + +_Background_ + +Basal metabolism represents the minimum energy required by a mammal to +maintain endothermy and basic homeostasis (Lusk, 1917:141; Kleiber, +1932, 1961:251; Benedict, 1938:191-215; Brody, 1945:59; Robbins, +1983:105-111). Mammals with lower than predicted [.H]_{b} maintain +endothermy and enjoy its attendant advantages at a discount, whereas +others, with rates that are higher than predicted, pay a premium +(Calder, 1987). Such variation in [.H]_{b} appears to be tied to +ecological circumstances rather than taxonomic affinities (Vogel, +1980; McNab, 1986a, 1988a, 1989), and depending on environmental +conditions, each rate provides an individual with various advantages +and limitations. During the course of evolution, therefore, each +species' [.H]_{b} evolves to provide it with the best match between +its energy requirements for continuous endothermy, its food supply, +and the thermal characteristics of its environment. + + +_Captive versus Wild Raccoons_ + +Male raccoons trapped in summer had higher [.H]_{b}'s than our captive +animals in any season (Table 2). The higher rate of metabolism of +these trapped males could have been due to the stress of captivity or +to the fact that "wild" animals actually may have higher metabolic +rates than those that have adjusted to captivity. If the latter is +true, then our data for captive animals underestimated the actual +energy cost of maintenance metabolism for _Procyon lotor_ in the wild. +At present, we have no way of determining which of these alternatives +is true. + + +_Seasonal Metabolism of Raccoons_ + +In some temperate-zone mammals, [.H]_{b} is elevated in winter, which +presumably increases their "cold-hardiness." Conversely, lower summer +metabolism is considered to be a mechanism that reduces the potential +for heat stress. Such seasonal variation in [.H]_{b} has been found in +several species: collard peccary, _Tayassu tajacu_ (Zervanos, 1975); +antelope jackrabbit, _Lepus alleni_ (Hinds, 1977); desert cottontail, +_Sylvilagus audubonii_ (Hinds, 1973); and, perhaps, cold-acclimatized +rat, _Rattus norvegicus_ (Hart and Heroux, 1963). Unlike these +species, our captive raccoons showed no seasonal variation in [.H]_{b} +(Table 2). Instead, raccoons achieved "cold-hardiness" in winter and +reduced their potential for heat stress in summer with a large +seasonal change in thermal conductance (Table 3). + + + TABLE 7.--Metabolic characteristics of several procyonid species. + + ---------------------+------------------------------------------------ + |Body Basal[a] Minimum[b] + Species |mass metabolism conductance T_{b}[c] + |(g) ------------ ------------- ------------- + | Meas H_{br} Meas C_{mwr} [alpha] [rho] + ---------------------+------------------------------------------------ + _Bassariscus astutus_| 865 0.43 0.68 0.0288[e] 0.85 37.6 23 + _Procyon cancrivorus_|1160 0.40 0.69 0.0368[e] 1.25 + _Potos flavus_ |2030 0.36 0.51 + _Potos flavus_ |2400 0.32 0.65 38.1 36.0 + _Potos flavus_ |2600 0.34 0.71 0.0200[f] 1.02 + _Nasua nasua_ |3850 0.26 0.60 0.0200[f] 1.24 38.3 36.4 + _Nasua nasua_ |4847 0.33 0.79 0.0238[e] 1.65 39.1 37.9 + _Nasua narica_ |5554 0.25 0.62 0.0208[e] 1.55 38.9 37.4 + _Nasua narica_ |4150 0.42 1.20 0.0341[e] 2.20 + | 0.0224[g] 1.45 + _Procyon lotor_ | + Summer | + Trapped male |4400 0.54 1.28 + Captive male |4790 0.46 1.07 0.0256[f] 1.77 38.4 37.5 + Captive female |4670 0.42 1.02 0.0256[f] 1.79 38.2 37.6 + Winter | + Captive male |5340 0.47 1.17 38.6 37.6 + Captive female |4490 0.46 1.10 0.0172[f] 1.15 38.3 37.3 + ---------------------+------------------------------------------------ + + ---------------------+----------------------------------------------- + | + Species | T_{n}[d] + |--------------- + | T_{lc} T_{uc} References + ---------------------+----------------------------------------------- + _Bassariscus astutus_| 35.5 Chevalier (1985) + _Procyon cancrivorus_| 26 Scholander et al. (1950b, c) + _Potos flavus_ | McNab (1978a) + _Potos flavus_ | 23 30 Mueller and Kulzer (1977) + _Potos flavus_ | 23 33 Mueller and Rost (1983) + _Nasua nasua_ | 25 33 Chevillard-Hugot et al. (1980) + _Nasua nasua_ | 30 35 Mugaas et al. (in prep.) + _Nasua narica_ | 25 35 + _Nasua narica_ | Scholander et al. (1950b, c) + | + _Procyon lotor_ | This study + Summer | + Trapped male | 20 + Captive male | 20 + Captive female | 25 + Winter | + Captive male | 11 + Captive female | 11 + ---------------------+----------------------------------------------- + + [a] Meas is measured basal metabolism (mL O_{2}.g^{-1}.h^{-1}). H_{br} + is the ratio of measured to predicted basal metabolism where the + predicted value is calculated from [.H]_{b} = 3.42.m^{-.25} + (Kleiber, 1932, 1961:206) and m is body mass in grams. + + [b] Meas is measured minimum thermal conductance + (mL O_{2}.g^{-1}.h^{-1}. deg.C^{-1}). C_{mwr} is the ratio of measured + to predicted minimum thermal conductance where the predicted value + is calculated from C_{m} = 1.0.m^{-0.5} (McNab and Morrison, 1963; + Herreid and Kessel, 1967), and m is body mass in grams. + + [c] T_{b} is body temperature during the active ([alpha]) and rest + ([rho]) phases of the daily cycle ( deg.C). + + [d] T_{n} is the thermoneutral zone as defined by the lower (T_{lc}) + and upper (T_{uc}) critical temperatures ( deg.C). + + [e] Conductance calculated as the slope of the line describing oxygen + consumption at temperatures below the lower critical temperature. + + [f] Conductance calculated from C_{mw} = [.H]_{r}/(T_{b} - T_{a}), + where [.H]_{r} is resting metabolic rate at temperatures below + T_{lc}, and other symbols are as described elsewhere. + + [g] Inactive-phase thermal conductance: estimated from Scholander et + al. (1950b), assuming that active-phase thermal conductance is 52% + higher than values determined during the inactive phase (Aschoff, + 1981). + + +_Comparison of Procyon lotor with Other Procyonids_ + +_Procyon lotor_ has a much higher mass-specific [.H]_{b} than other +procyonids (Table 7). To quantify the magnitude of this difference, +we compared the measured value for _Procyon lotor_ with one calculated +for it from a mass-specific least-squares regression equation (Eq. 6; +R squared = 0.78) derived from data for those procyonids with lower than +predicted [.H]_{b}: _Potos flavus_, _Procyon cancrivorus_, +_Nasua nasua_, _Nasua narica_, and _Bassariscus astutus_ (Table 7). + + [.H]_{b} = 2.39.m^{-0.25} Eq. 6 + +[.H]_{b} in Eq. 6 is basal metabolism (mL O_{2}.g^{-1}.h^{-1}) and m +is body mass (g). Measured values of [.H]_{b} for _Procyon lotor_ were +1.45 to 1.86 times greater than those predicted for it by Eq. 6 +(Table 8). + + + TABLE 8.--Basal metabolism (mL O_{2}.g^{-1}.h^{-1}) of _Procyon + lotor_ as predicted by Eq. 6 ([.H]_{b} = 2.39.m^{-0.25}). Body + masses, used to calculate predicted values, and measured values + were taken from Table 7. + + ----------------+-------------------------------- + Season and sex | Predicted Measured/Predicted + ----------------+-------------------------------- + Summer | + Trapped male | 0.29 1.86 + Captive male | 0.29 1.59 + Captive female| 0.29 1.45 + Winter | + Captive male | 0.28 1.68 + Captive female| 0.29 1.59 + ----------------+-------------------------------- + + +_Influence of Diet on Basal Metabolism_ + +BACKGROUND.--With respect to [.H]_{b}, McNab (1986a:1) maintains that +"the influence of climate is confounded with the influence of food +habits," and that departures from the Kleiber (1961) "norm" are best +correlated with diet. Although this does appear to be the case for +diet specialists, the analysis is not so clear-cut for omnivorous +species (McNab, 1986a). His analysis also indicates that an animal's +"behavior" (i.e., whether it is terrestrial, arboreal, subterranean, +aquatic, etc.), secondarily modifies the influence of food habits on +[.H]_{b}. For example, terrestrial frugivores have [.H]_{b}'s that are +very near predicted values, whereas arboreal frugivores have rates +that are much lower than predicted (McNab, 1986a). + + + TABLE 9.--Food habits of some Procyonids. References for foods were + as follows: _Potos flavus_, _Procyon cancrivorus_, and _Nasua nasua_ + taken from Bisbal (1986); _Nasua narica_ taken from Kaufmann + (1962:182-198); _Bassariscus astutus_ taken from Martin et al. + (1951), Taylor (1954), Wood (1954), Toweill and Teer (1977), and + Trapp (1978); _Procyon lotor_ taken from Hamilton (1936), Stuewer + (1943:218-220), Stains (1956:39-51), and Greenwood (1981). Symbols + represent either qualitative (#) or quantitative (+,|) assessments + of feeding habits: # indicates that the animal was observed eating + the food; + and | represent volume and frequency, respectively, of + food utilization. No attempt was made to account for seasonal + variation in the use of these foods. + + + <20% by volume when found. | 1%-19% frequency of occurrence. + ++ >20% by volume when found. || 20%-50% frequency of occurrence. + ||| >50% frequency of occurrence. + + -----------+-------------------------------------------------------------- + |_Potos_ _Procyon_ _Nasua_ _Nasua_ _Bassariscus_ _Procyon_ + Food |_flavus_ _cancrivorus_ _nasua_ _narica_ _astutus_ _lotor_ + -----------+-------------------------------------------------------------- + Mammalia | + | # ++ ||| ++ || + Aves | ++ | + || + Birds' eggs| ||| + Reptilia | + | + ||| # + | + | + Amphibia | + | # + | + Pices | ++ || ++ || + Insecta |++ | + ||| ++ ||| # + || ++ || + Arachnida | ++ ||| # + | + | + Chilopoda | ++ ||| + Diplopoda | # + | + Crustacea | ++ ||| # ++ ||| + Mollusca | + || # + || + Annelida | # + | + Nuts | ++ || + Grains | ++ || + Buds | + | + Fruit |++ ||| ++ # || ++ ||| + Leaves | + | + Grass | + | + -----------+-------------------------------------------------------------- + + +FOOD HABITS OF PROCYONIDS.--Food habits of six procyonids for which +metabolic data are available are presented in Table 9. All six species +clearly have mixed diets. Compared to other species, _Procyon lotor_ +is highly catholic in its diet, taking food from almost twice as +many categories as _Nasua narica_, three times as many as _Procyon +cancrivorus_, _Nasua nasua_, and _Bassariscus astutus_, and nine times +as many as _Potos flavus_. + +For those species for which food habit data are quantified, we used +Eisenberg's (1981:247-251) substrate/feeding matrix method, where +"substrate" is analogous to McNab's (1986a) "behavior," to construct +the following feeding categories that are based on the major food +groups utilized by each species (Table 9). + + 1. _Potos flavus:_ (1) arboreal/frugivore, insectivore. + + 2. _Procyon cancrivorus:_ (1) semiaquatic/crustacivore, + molluscivore, insectivore, piscivore, carnivore. + + 3. _Nasua nasua:_ (1) terrestrial/insectivore, arachnidivore, + carnivore, frugivore. + + 4. _Bassariscus astutus:_ (1) terrestrial/carnivore, insectivore, + frugivore. + + 5. _Procyon lotor:_ (1) terrestrial/carnivore, granivore, + frugivore, insectivore; and (2) semiaquatic/crustacivore, + molluscivore, insectivore, piscivore, carnivore. + +FOOD HABITS AND BASAL METABOLISM.--The most important foods in the +diet of _Procyon lotor_ are vertebrates, nuts, seeds, and fruits +(Table 9). These are the same foods that are eaten by those dietary +specialists that have [.H]_{b}'s equivalent to, or higher than, values +predicted for them by the Kleiber equation (McNab, 1986a). The most +important foods in the diets of _Potos flavus_, _Procyon cancrivorus_, +and _Nasua nasua_ are invertebrates and fruit (Table 9), and these +foods are eaten by dietary specialists that have lower than predicted +[.H]_{b}'s (McNab, 1986a). Major foods in the diet of _Bassariscus +astutus_ are terrestrial vertebrates, insects, and fruit (Table 9). +Dietary specialists that eat terrestrial vertebrates have higher than +predicted [.H]_{b}'s, whereas those that feed on insects have [.H]_{b}'s +that are lower than predicted (McNab, 1986a). Year-round utilization of +vertebrates by _Bassariscus astutus_ suggests that it also should have +a metabolic rate that is equivalent to or higher than predicted, rather +than lower (McNab, 1986a). However, perhaps year-round inclusion of +insects in its diet (Martin et al., 1951; Taylor, 1954; Wood, 1954; +Toweill and Teer, 1977; Trapp, 1978), plus water- and energy-conserving +advantages of a low metabolic rate, each exert a stronger selective +influence on [.H]_{b} than do vertebrates in its diet. + +SUMMARY.--The basal metabolic rate of these procyonids does appear to +be influenced by diet. But, it is apparent from this family's +evolutionary history and tropical origins that climate also has had a +profound influence on its member's metabolism. The history of the +family and the data presented here (Table 7) suggest that lower than +predicted [.H]_{b} is a feature that evolved very early as the primary +metabolic adjustment to a tropical climate. From this perspective, it +could be argued that climate would have been the major selective force +determining [.H]_{b}, whereas food habits would have had a secondary +influence. + + +_Basal Metabolism and Intrinsic Rate of Natural Increase_ + +BACKGROUND.--McNab (1980a) suggested that if food is not restricted +during an animal's reproductive period, the factor that will limit +growth and reproduction will be the rate at which energy can be used +in growth and development. Under these conditions, an increase in +[.H]_{b} would actually increase r_{max} because it would provide a +higher rate of biosynthesis, a faster growth rate, and a shorter +generation time. Hennemann (1983) tested McNab's (1980a) premise and +found a significant correlation between r_{max} and metabolic rate, +independent of body size, for 44 mammal species. A low correlation +coefficient for this relationship, however, indicated to him +(Hennemann, 1983) that factors such as (1) food supply, (2) thermal +characteristics of the environment, and (3) brain size also contribute +toward shaping a species' reproductive potential, particularly when +these factors strongly influence rates of biosynthesis or growth or +for some reason alter generation time. Results of our estimates of +r_{max} for procyonids are presented in Table 10. + +_Procyon lotor._--This species had the highest [.H]_{b} and D_{d}, and +also had the highest r_{max} (1.34; Table 10). Such a high r_{max} may +infer that this trait evolved under conditions where food and +temperature were not limiting to reproduction. Under these conditions +selection could have favored those reproductive characteristics +sensitive to a higher [.H]_{b} (biosynthesis, growth, and generation +time; McNab, 1980a). _Procyon lotor_'s high reproductive potential is +due to its early age of first female reproduction and its large litter +size, characteristics that may reflect metabolically driven increases +in both biosynthesis and growth. + +_Bassariscus astutus._--This species has a low [.H]_{b} but an r_{max} +that was 124% of expected (Table 10). This suggests that r_{max} +evolved under conditions where food and temperature were not +limiting to reproduction. Reduced litter size should restrict this +species' reproductive potential and may be a reflection of its low +[.H]_{b}. The factor that is responsible for increasing its +reproductive potential, however, is its early age of first female +reproduction. _Bassariscus astutus_ is the smallest of these +procyonids, and even though it has a low [.H]_{b}, its small mass +may contribute to its ability to reach adult size and sexual maturity +in its first year. The high quality of its diet (a high proportion of +small vertebrates; Table 9) also may be a factor that is permissive to +early female reproduction. Thus, small body size and diet may be +factors that have allowed this species to evolve a higher than expected +reproductive potential in spite of its low [.H]_{b}. + +_Nasua narica._--This species is one of the largest procyonids +(Table 7), and it possesses characteristics that should limit its +reproductive potential: lower than predicted [.H]_{b} (Table 7), a +relatively low-quality diet (Kaufmann, 1962:182-198; Table 9), and +delayed time of first reproduction (Table 10). In spite of this, +_Nasua narica_ has a higher than expected r_{max} (111% of predicted; +Table 10). The life history feature that enhances _Nasua narica_'s +reproductive potential, and increases r_{max} beyond expected, is its +large litter size. In this species females live in bands. Each year +just before their young are born these bands break up, and each female +seeks out a den for herself and her litter. Once the young are able to +leave the den (approximately five weeks), bands reform. In this +situation, females not only care for their own young but also for those +of other females in the band (Kaufmann, 1962:157-159, 1982, 1987; +Russell, 1983). This social structure may contribute to this species' +ability to produce large litters and in this way increase its +reproductive potential. + + + TABLE 10.--Intrinsic rate of natural increase (r_{max}) of several + procyonids. (a = potential age of females producing first young; + b = potential annual birth rate of female young (= average litter + size/2; average litter size was calculated from the published range + of litter sizes for each species); n = potential age of females + producing their final young; r_{maxe} = intrinsic rate of natural + increase expected from body mass (Hennemann, 1983); r_{maxr} = ratio + of calculated to expected intrinsic rate of natural increase + (r_{max}/r_{maxe}).) + + ---------------------+------------------------------------------------ + | + Species |Body mass a b n r r [a] r [b] + | (g) max maxe maxr + ---------------------+------------------------------------------------ + _Procyon lotor_ | 4940 0.83 2.25 16 1.34 0.53 2.52 + | + | + | + _Bassariscus astutus_| 900 0.83 1.50 14 1.02 0.82 1.24 + | + | + | + _Nasua narica_ | 3900 2.50 2.25 14 0.62 0.56 1.11 + | + _Nasua nasua_ | 3850 + _Procyon cancrivorus_| 1160 0.83 1.50 15 1.02[c] 0.77 1.32 + | 1.75 0.65[c] 0.84 + _Potos flavus_ | 2490 1.75 0.50 12 0.30 0.63 0.48 + | + _Bassaricyon gabbii_ | 1600 1.75 0.50 15 0.32 0.71 0.45 + | + ---------------------+------------------------------------------------ + + ---------------------+------------------------------------------------ + | + Species | References + ---------------------+------------------------------------------------ + _Procyon lotor_ | Dunn and Chapman (1983); Eisenberg (1981:489); + | Kaufmann (1987); Lotze and Anderson (1979); + | Nowak and Paradiso (1983:981); Sanderson + | (1987); Stains (1956:28-31); This study + _Bassariscus astutus_| Kaufmann (1982, 1987); Nowak and Paradiso + | (1983:979, 980); Poglayen-Neuwall and + | Poglayen-Neuwall (1980); Poglayen-Neuwall + | and Toweill (1988); Russell (1983) + _Nasua narica_ | Kaufmann (1982, 1987); Nowak and Paradiso + | (1983:983); Sanderson (1983) + _Nasua nasua_ | Chevillard-Hugot et al. (1980) + _Procyon cancrivorus_| Crandall (1964:312); Poglayen-Neuwall (1987) + | + _Potos flavus_ | Ford and Hoffmann (1988); Nowak and Paradiso + | (1983:984) + _Bassaricyon gabbii_ | Eisenberg (1981:489); Nowak and Paradiso + | (1983:985) + ---------------------+------------------------------------------------ + + [a] r_{maxe} = 4.9.m^{0.2622}, where m is body mass in grams. + + [b] Regression of r_{max} on body mass (m). Assume r_{max} = 1.02 for + _Procyon cancrivorus_: r_{max} = 0.00005.m + 0.623; R = 0.19; + R squared = 0.03; Regression of r_{maxr} (Table 10) on H_{br} (Table 7); + assume _Nasua nasua_ has the same r_{maxr} as _Nasua narica_: + r_{maxr} = 3.35.H_{br} - 1.11; R = 0.93; R squared = 0.86. + + [c] Estimate based on females reproducing in their first (a = 0.83) or + second (a = 1.75) year. + + +_Nasua nasua._--Unfortunately, there is not enough reproductive data +to allow calculation of r_{max} for _Nasua nasua_ (Table 10), therefore, +it is not possible to compare the reproductive potential of this South +American coati with its North American relative, _Nasua narica_. Given +its low [.H]_{b} and relatively low-quality diet of fruit and +terrestrial invertebrates (Table 9), however, r_{max} of _Nasua nasua_ +may be very similar to that of _Nasua narica_. + +_Procyon cancrivorus._--The age of first female reproduction for +_Procyon cancrivorus_ has not been reported. However, if one assumes +females can reproduce in their first year, r_{max} for _Procyon +cancrivorus_ would be 1.02 (132% of expected; Table 10). If, on the +other hand, first female reproduction is delayed until the second year, +r_{max} would be 0.65 (84% of predicted; Table 10). _Procyon +cancrivorus_ has a low [.H]_{b}, reduced litter size, and small body +mass. Its low [.H]_{b} may limit litter size, but as with _Bassariscus +astutus_, the quality of its diet (a high percentage of small +vertebrates; Table 9) and its small body size may make it possible for +females to reproduce in their first year and thus increase the species' +reproductive potential. This reasoning would argue that _Procyon +cancrivorus_ probably enjoys higher, rather than lower, than expected +r_{max}. + +_Potos flavus._--In addition to a low [.H]_{b}, this species possesses +other characteristics that limit its reproductive potential: +low-quality diet, delayed reproduction, and birth of a single young +each year. Because there does not appear to be any other feature of +its life history that can counteract the influence of these factors, +r_{max} in _Potos flavus_ has evolved to be only 48% of expected +(0.30; Table 10). Its close relative, the olingo, _Bassaricyon gabbii_, +appears to share the same condition (Table 10). + +SUMMARY.--This brief survey illustrates that, with the exception of +_Potos flavus_, procyonids tend to have values of r_{max} that are +higher than those predicted for them on the basis of mass (Table 10). +Regression analysis indicates that, within the family, body mass +accounts for only a small amount (3%) of the variation in r_{max}, +whereas the positive slope of the correlation between r_{maxr} and +H_{br} (R = 0.93) suggests that low metabolism has a limiting effect +on r_{max} (see Table 10, footnote f). The implication here is that +low [.H]_{b} would be associated with a lower rate of biosynthesis, +a slower growth rate, and a longer generation time. Procyonids with +low [.H]_{b} but higher than expected r_{max} must possess other +traits that serve to offset the effects of low metabolism. Our survey +indicates that the following features compensate for low [.H]_{b} and +help increase r_{max}: (1) a high-quality diet may make biosynthesis +and growth more efficient, thus optimizing the time element associated +with each of these processes; (2) larger litter sizes and cooperation +in care of the young may increase survivorship in spite of a slower +growth rate; and (3) an early age of first reproduction, a long +reproductive life span, and moderate-size litters (two to four young) +may in the long run add as many individuals to the population as a +shortened generation time. Our survey also suggests that, at the other +extreme, factors such as a low-quality diet, reduced litter size, +absence of cooperative care of the young, delayed age of first +reproduction, and shortened reproductive life span all serve to +decrease r_{max}. Thus, it is obvious that diet, litter size, social +structure, reproductive strategy, and reproductive life span can operate +synergistically with [.H]_{b} to magnify its influence on r_{max} (as +with _Procyon lotor_ and _Potos flavus_), or they can function in +opposition to [.H]_{b} to change the direction of its influence on +r_{max} (as with _Bassariscus astutus_, _Procyon cancrivorus_, _Nasua +narica_, and perhaps _Nasua nasua_). + + +_Basal Metabolism and Climatic Distribution_ + +_Procyon lotor._--The evolution of a higher [.H]_{b} (Tables 7, 8) may +have been the physiological cornerstone that enabled _Procyon lotor_ +to break out of the mold being exploited by other procyonids and to +generalize its use of habitats and climates. Once this basic +physiological change was in place, selection for appropriate +alterations in thermal conductance, capacity for evaporative cooling, +diversity of diet, and energy storage would have provided this species +with the suite of adaptations needed to extend its distribution into +other habitats and climates. Support for this concept follows from the +fact that high levels of [.H]_{b} are associated with (1) cold-hardiness +in mammals that live in cold-temperate and arctic climates (Scholander +et al., 1950c; Irving et al., 1955; Irving, 1972:115, 116; Shield, 1972; +Vogel, 1980; Golightly and Ohmart, 1983); (2) the ability to utilize a +wide variety of food resources and to occupy a large number of different +environments and habitats (McNab, 1980a); and (3) a high intrinsic rate +of natural increase (McNab, 1980a; Hennemann, 1983; Lillegraven et al., +1987; Nicoll and Thompson, 1987; Thompson, 1987). + +OTHER PROCYONIDS.--Other procyonids (_Potos flavus_, _Procyon +cancrivorus_, _Nasua narica_, and _Nasua nasua_) have lower than +predicted [.H]_{b}'s (Table 7), a characteristic that is considered to +be an energy-saving adaptation for those that live in relatively stable +tropical and subtropical habitats (Mueller and Kulzer, 1977; +Chevillard-Hugot et al., 1980; Mueller and Rost, 1983). However, +_Bassariscus astutus_ is found in tropical, subtropical, and temperate +climates. This species is found from tropical Mexico to temperate +regions of the western United States (Kaufmann, 1982, 1987; Nowak and +Paradiso, 1983:979). In the northern part of its distribution, +_Bassariscus astutus_ lives in habitats that are unstable (arid +regions), that are low in productivity, and that characteristically +have marked seasonal changes in temperature. Its lower than predicted +[.H]_{b} could be an important water-conserving adaptation at times when +temperatures are high (McNab and Morrison, 1963; McNab, 1966; MacMillen +and Lee, 1970; Noll-Banholzer, 1979) and an important energy-conserving +mechanism when cold weather may limit food availability and hunting time +(Scholander et al., 1950c; Wang et al., 1973). As will be seen later, +_Bassariscus astutus_ is unique among procyonids with lower than +predicted [.H]_{b}'s in that it also has a lower than predicted +C_{mw} (Table 7). This allows it to use less energy than expected for +thermoregulation at low temperatures. Another species with a similar set +of adaptations (lower than predicted [.H]_{b} and C_{mw}) is the arctic +hare, _Lepus arcticus_ (Wang et al., 1973), which lives in one of +the coldest and least-productive regions on earth. Wang et al. (1973) +suggest that this combination of adaptations allows _Lepus arcticus_ +to better match its energy requirements to the low productivity of its +environment. A similar relationship may hold for _Bassariscus astutus_, +particularly in colder arid portions of its distribution, and may be the +reason that it, but not other procyonids with low [.H]_{b}'s, has been +able to inhabit temperate climates. + + + +MINIMUM THERMAL CONDUCTANCE + + +_Background_ + +Thermal conductance is a measure of the ease with which heat is +passively transferred to or from a body through its tissues and pelt. +Within T_{n}, a mammal is able to vary its thermal conductance over a +wide range of values by changing heat transfer characteristics of both +of these layers. Minimum thermal conductance occurs when total heat +transfer through these layers is reduced to its lowest possible rate. +This minimum value, which is the reciprocal of maximum resistance, +occurs, theoretically, but not always practically (see McNab, 1988b), +at the animal's T_{lc} and is best estimated under standard conditions +in a metabolism chamber (McNab, 1980b; Aschoff, 1981). Minimum thermal +conductance scales to body mass (McNab and Morrison, 1963; Herreid and +Kessel, 1967; McNab, 1970, 1979b; Bradley and Deavers, 1980; Aschoff, +1981). Therefore, to make comparisons between species of various sizes, +we scaled out body mass by expressing C_{mw} as the ratio of measured +to predicted values (C_{mwr}; Table 7). These ratios were used to make +comparisons of heat-transfer characteristics between species that +occupy different habitats or climates. + + +_Effect of Molt on Thermal Conductance_ + +In summer, T_{lc}'s of male and female _Procyon lotor_ (Figure 2) were +very similar to those of other procyonids (22 deg.C-26 deg.C; Table 7). In +winter, T_{lc} of both sexes shifted downward to 11 deg.C (Figure 3). This +seasonal shift in T_{lc} occurred as the result of a seasonal change +in minimum thermal conductance (Table 3). For many northern mammals, a +seasonal change in thermal conductance is partly mediated via cyclic +changes in the insulative quality of their pelt (Scholander et al., +1950a; Irving et al., 1955; Hart, 1956, 1957; Irving, 1972:165). + +_Procyon lotor_ begins to shed its heavy winter coat about the time +its young are born. Molt progresses through summer and by late August +the new coat is complete (Stuewer, 1942). During its summer molt, +_Procyon lotor_'s C_{mw} increased by about 49% over the value for +female raccoons in winter (Table 3). In summer, therefore, it had the +highest mass specific C_{mw} of those procyonids considered +(C_{mwr} = 1.77 and 1.79; Table 7). An increase in thermal conductance +facilitates passive heat loss for temperate and arctic species, and +this serves as an important thermoregulatory adaptation during warm +summer months (Scholander et al., 1950c; Irving et al., 1955; +Hart, 1956, 1957; Irving, 1972:165). This adaptation is particularly +important to those temperate- and arctic-zone species (including +raccoons) whose [.H]_{b}'s do not decrease during summer (Irving et al., +1955). From August on, the fur of _Procyon lotor_ becomes increasingly +longer and heavier, with peak, or prime, condition occurring in late +fall and early winter (Stuewer, 1942). Minimum conductance of our +captive raccoons was lowest in winter (C_{mwr} = 1.15) when their pelts +were in prime condition (Tables 3, 7). Because "primeness" of raccoon +pelts varies geographically, thicker pelts being associated with colder +climates (Goldman, 1950:21; Whitney and Underwood, 1952:24-41), the +degree of seasonal change in C_{mw} must also vary geographically. + +The only other procyonid for which a seasonal molt has been described +is _Bassariscus astutus_. Molt in this species extends from late summer +to late fall (Toweill and Toweill, 1978). How molt effects thermal +conductance in _Bassariscus astutus_ is not known because metabolic +data for this species (Table 7) apparently were collected only when +their pelts were in prime condition (Chevalier, 1985). + +Goldman (1950:20) reports that _Procyon cancrivorus_ does not have a +seasonal molt. Like other tropical procyonids, _Procyon cancrivorus_ +lives in an environment that has the following characteristics: high +even temperatures throughout the year (1 deg.C-13 deg.C difference in monthly +mean temperature), a greater range in temperature between day and +night than in mean monthly temperature throughout the year, uniform +lengths of day and night, seasonal variation in rainfall, and lowest +temperatures during the rainy season(s) (Kendeigh, 1961:340). In such +a stable environment there would be no advantage to a sharply defined +seasonal molt cycle that could place an animal in thermoregulatory +jeopardy by increasing its thermal conductance. This would be +particularly true for animals like tropical procyonids that have lower +than predicted [.H]_{b}'s but that maintain typical eutherian body +temperatures (Table 7). Consequently, molt in all tropical procyonids +may either be prolonged or continuous. This is a feature of their +biology that needs to be examined in more detail. + + +_Comparison of Thermal Conductances_ + +_Procyon lotor_ VERSUS TROPICAL PROCYONIDS.--C_{mwr} for _Procyon +lotor_ in winter was 1.15, which is similar to the values for _Potos +flavus_ and _Procyon cancrivorus_, 1.02 and 1.25, respectively +(Table 7). These two tropical species, therefore, have C_{mw}'s that +are similar on a mass specific basis to the value for _Procyon lotor_ +in winter. However, at their T_{lc}'s, the thermal gradient sustained +by these tropical animals is only about 11 deg.C, whereas for _Procyon +lotor_ in winter it was 26.5 deg.C. Examination of Eq. 4 with respect to +these thermal gradients suggests that tropical procyonids achieve such +low C_{mw}'s by virtue of their lower than predicted [.H]_{b}'s rather +than by having pelts that are exceptionally good insulators. In fact, +the insulation afforded by the pelts of these tropical procyonids is +about the same as that of the 50 g arctic lemming, _Dicrostonyx +groenlandicus rubricatus_, whose coat has an insulative value that is +about half that of the hare, _Lepus americanus_, red fox, _Vulpes fulva +alascensis_, and pine martin, _Martes americana_, animals comparable in +size to these procyonids (Scholander et al., 1950a). Therefore, pelts +of these tropical procyonids do not have the same insulative value as +the prime winter coat of _Procyon lotor_. + +_Nasua narica_ and _Nasua nasua_ have tropical and subtropical +distributions and they are the only procyonids that are diurnal +(Kaufmann, 1962:103-105, 1982, 1987). Because they are active during +the day they experience a more extreme thermal environment (higher +T_{a}'s and solar radiation) than their nocturnal cousins. Values of +C_{mwr} for _Nasua narica_ (1.45 and 1.55) and _Nasua nasua_ (1.24 and +1.65) are higher than those for _Procyon cancrivorus_ or _Potos flavus_ +(Table 7). Thus, these coatis have higher mass specific C_{mw}'s than +their nocturnal tropical cousins. A high C_{mw} reduces the cost of +thermoregulation in hot environments because it increases an animal's +ability to lose excess heat passively. The higher C_{mw}'s of these +coatis serve as an adaptation that contributes to the success of their +diurnal life style as well as their ability to expand their habitat use +to areas with less thermal stability, such as oak and pine woodlands +and deserts. + +_Bassariscus astutus._--This species has the lowest mass specific +C_{mw} of these procyonids (C_{mwr} = 0.85; Table 7), which indicates +that its pelt has a greater insulative value than the coats of _Potos +flavus_, _Procyon cancrivorus_, _Nasua nasua_, or _Nasua narica_. This, +coupled with a lower than predicted [.H]_{b}, allows _Bassariscus +astutus_ to maintain T_{b} with less energy expenditure than is +possible for any other procyonid of comparable size; and this +combination of adaptations provides _Bassariscus astutus_ with a +distinct energy advantage in environments that have low productivity +(Wang et al., 1973). The evolution of a pelt that provides better +insulation must be considered an important contributing factor for +the spread of this species into desert regions of the western United +States. + + + +THERMOREGULATION AND USE OF STORED FAT AT LOW TEMPERATURES + + +_Background_ + +THERMOREGULATION.--At temperatures below a mammal's T_{n}, heat loss +exceeds [.H]_{b}. To maintain T_{b} under these conditions, metabolic +rate must be increased (Eq. 4). _Procyon lotor_ in summer during its +annual molt (Table 5; Figure 2), _Bassariscus astutus_ (Chevalier, +1985), _Nasua nasua_ (Chevillard-Hugot et al., 1980; Mugaas et al., +in prep.), _Nasua narica_ (Scholander et al., 1950b; Mugaas et al., +in prep.), and _Potos flavus_ (Mueller and Kulzer, 1977; Mueller and Rost, +1983) all are able to elevate their metabolic rates by 130% above basal +when they are exposed to T_{a} = 0 deg.C. _Procyon cancrivorus_ responds to +0 deg.C with an increase in metabolic rate of 257% above basal (Scholander +et al., 1950b). All animals listed have about the same T_{lc} and T_{b}, +so the temperature differential producing this response is about the +same for each species. Metabolic ability to defend body temperature +against low ambient temperatures, therefore, is well developed in these +procyonids. Such large increases in metabolic rate are energetically +expensive, and if these animals were routinely exposed to T_{a} = 0 deg.C, +it would be difficult for them to acquire enough food each day to +maintain endothermy. Raccoons in winter pelage, however, need only +elevate their metabolic rate by 47% above basal to maintain endothermy +at T_{a} = 0 deg.C (Table 5; Figure 3). Each year at the completion of its +molt, the raccoon's highly insulative pelt is renewed. This lowers +their T_{lc} by 9 deg.C to 15 deg.C below that measured for them in summer +(Figure 3) and decreases their cost of thermoregulation at low +temperatures. The increased insulative capacity of their pelt is one +of the primary adaptations that has allowed _Procyon lotor_ to extend +its distribution into cold climates. + +STORED FAT.--Cyclic fattening is an integral and important part of a +raccoon's annual cycle (Mugaas and Seidensticker, ms); however, it has +not been reported for other procyonids. During winter in parts of the +United States and Canada, raccoons are confined to their dens for +variable periods of time (days to months) depending on the severity of +the weather (Stuewer, 1943:223-225; Whitney and Underwood, 1952:108-116; +Sharp and Sharp, 1956; Mech et al., 1968; Schneider et al., 1971). +During this confinement, they do not hibernate but rather enter a state +of "dormancy" and become inactive. While dormant they remain endothermic +(T_{b} > 35 deg.C; Thorkelson, 1972:87-90) and derive most of their energy +requirement from fat reserves accumulated during fall. The rate at which +fat stores are consumed during winter dormancy depends on the +thermoregulatory requirement imposed on them by local weather +conditions, the insulative quality of their pelt, and any advantage +they may gain by seeking shelter in a den. + + +_Thermal Model of the Raccoon and Its Den_ + +Heat transfer between an animal and its environment is a function of +the interaction of its body temperature and thermal conductance with +various environmental variables (air temperature, wind speed, vapor +pressure, and thermal radiation). When a raccoon is outside its den, +its thermal conductance (C_{mw}) is the only barrier to heat transfer +with the external environment. However, when it enters a tree den, a +raccoon imposes two other thermal barriers between itself and the +external environment: (1) conductance of the air space between its fur +and the den's walls (C_{a}) and (2) conductance of the den's walls +(C_{d}; Thorkelson, 1972:59-63; Thorkelson and Maxwell, 1974). +Thorkelson and Maxwell (1974) modeled heat transfer of a simulated +raccoon (a water-filled aluminum cylinder equipped with a heater and +covered with a raccoon pelt) in a closed tree den. In their system, +65% of resistance to heat flux was attributable to the pelt, whereas +the remainder (35%) was due to C_{a} and C_{d}. Because resistance is +the inverse of conductance, and resistances for the raccoon and its +den are arranged in series, we can estimate total conductance (C_{t}) +of this system with Eq. 7. + + 1/C_{t} = 1/C_{mw} + 1/C_{a} + 1/C_{d} Eq. 7 + +Minimum thermal conductance C_{mw} for raccoons in winter was +0.0172 mL O_{2}.g^{-1}.h^{-1}. deg.C^{-1} (Table 3). Based on Thorkelson +and Maxwell's (1974) model we let 1/C_{mw} = 0.65(1/C_{t}) = +1/0.0172 mL O_{2}.g^{-1}.h^{-1}. deg.C^{-1}, and 1/C_{a} + 1/C_{d} = +0.35(1/C_{t}). Substituting these values into Eq. 7 and solving +for C_{t} yields 0.0112 mL O_{2}.g^{-1}.h^{-1}. deg.C^{-1}, a value +that is 35% lower than that of the animal alone. Substituting +this value and the value for basal metabolism of winter raccoons +(0.47 mL O_{2}.g^{-1}.h^{-1}; Table 7) into Eq. 4 and solving for +(T_{b} - T_{a}) yields a new temperature differential of 42 deg.C. +Therefore, by using tree dens, raccoons in north central Virginia, +with T_{b} = 37 deg.C (Figure 7), could effectively reduce their T_{lc} +from 11 deg.C to -5 deg.C and markedly reduce their metabolic cost of +thermoregulation. + + +_Metabolic Advantage of the Den_ + +Given prevailing winter temperatures in north central Virginia (see +"Materials and Methods"), adult raccoons in that area should be able +to sustain endothermy most of the time they are in their dens by simply +maintaining [.H]_{b}. Depending on the mass of their stored fat, they +could remain in their dens for several weeks without eating (Mugaas and +Seidensticker, ms). The thermal advantage of a den could be further +enhanced during colder temperatures if two or more raccoons occupied it +at the same time and huddled together, and/or if these animals could +reduce C_{mw} even more by lowering T_{b} and cooling their extremities. +Although we do not have any data to verify the second mechanism, there +are many accounts in natural history literature that document raccoons +occupying dens together (Lotze and Anderson, 1979). This habit could be +particularly important for the young of the year and may be one reason +why they often continue to den with their mothers during winter (Lotze +and Anderson, 1979; Seidensticker et al., 1988). Raccoons that live in +colder climates, such as Minnesota, undoubtedly obtain the same +advantage from a den as Virginia animals, but because of their greater +body mass, longer fur, and potentially lower C_{mw}, T_{lc} of a +Minnesota raccoon in a den could be even lower than what we calculated +for Virginia raccoons. Therefore, when they are in their dens, raccoons +living in very cold climates also may be able to maintain homeothermy +with a basal level of metabolism. + + + +THERMOREGULATION AT HIGH TEMPERATURES + + +_Background_ + +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. + + [Illustration: FIGURE 8.--Relationship between number of climates + in which a species is found and its composite score. Symbols for + _Nasua nasua_ overlap at coordinates (0.64, 2). Solid line + represents linear regression of climates (Y) on composite scores + (X): Y = 2.68.X + 0.24; R = 0.94.] + +_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 + + +Our analysis has illustrated that within Procyonidae there are two +distinct modes of metabolic adaptation to climate. One is typified by +those species with low [.H]_{b}'s (_Bassariscus astutus_, _Nasua +nasua_, _Nasua narica_, _Procyon cancrivorus_, and _Potos flavus_), +and the other by _Procyon lotor_ with its higher [.H]_{b}. Those with +low [.H]_{b}'s have more restricted geographic distributions, and, +with the exception of _Bassariscus astutus_, they are all confined to +tropical and subtropical areas. The fossil history of this family +indicates that it had its origins in tropical forests of North and +Central America. This indicates that those procyonids whose +distributions are still primarily restricted to tropical forests share +many of the metabolic adaptations characteristic of their ancestors. +We speculate, therefore, that ancestral procyonids had a lower than +predicted [.H]_{b}, a pelt with modest to poor insulative quality, +good thermogenic ability but poor heat tolerance, modest to poor +capacity for evaporative cooling, no well-defined molt cycle, no +cyclic period of fattening, nocturnal habits, and a modestly diverse +diet of high-enough quality to provide for an average reproductive +potential. Although this pedigree contributed to the success of this +family in tropical and subtropical forests, it limited the ability of +its members to expand their distributions into cooler, less stable +climates. Viewed in this perspective, _Procyon lotor_'s high basal +metabolic rate, extraordinarily diverse diet, well-defined cyclic +changes in fat content and thermal conductance, high level of heat +tolerance, high capacity for evaporative cooling, and high +reproductive potential all stand out in sharp contrast to the +condition described for other procyonids. This suggests that the North +American raccoon represents culmination of a divergent evolutionary +event that has given this species the ability to break out of the old +procyonid mold and carry the family into new habitats and climates. + + + + +APPENDIX: LIST OF SYMBOLS + + + a potential age of females first producing young + + b potential annual birth rate of female young + + C_{a} conductance of air + + C_{d} conductance of den walls + + C_{m} minimum thermal conductance + + C_{md} minimum dry thermal conductance + + C_{mw} minimum wet thermal conductance + + C_{mwr} ratio of measured to predicted minimum wet thermal + conductance + + C_{t} total conductance + + D_{d} diversity of diet + + D_{dr} ratio of food categories actually used by a species to + the total number of food categories taken by all species + tested + + [.E] evaporative water loss + + E_{c} ratio of evaporative heat lost to metabolic heat produced + + [.E]_{eq} oxygen equivalent for heat lost by evaporation + + [.H]_{b} basal metabolic rate + + [.H]_{r} lowest resting metabolic rate at each temperature + + H_{br} ratio of measured to predicted basal metabolic rate + + m mass of animal + + m_{w} mass of water + + n potential age of females producing their final young + + r_{max} intrinsic rate of natural increase + + r_{maxe} expected intrinsic rate of natural increase + + r_{maxr} ratio of calculated to expected intrinsic rate of natural + increase + + RQ respiratory quotient + + T_{a} chamber air temperature + + T_{b} body temperature + + T_{lc} lower critical temperature + + T_{n} thermoneutral zone + + T_{uc} upper critical temperature + + t time + + [.V]_{a} rate of air flow through U-tubes + + [.V]_{e} rate of air flow into metabolism chamber + + [alpha] active phase of the daily cycle + + [gamma] heat equivalent of oxygen + + [lambda] heat of vaporization of water + + [rho] rest phase of the daily cycle + + + + +LITERATURE CITED + + + Aschoff, Juergen + + 1981. 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