The Project Gutenberg eBook ofMetabolic Adaptation to Climate and Distribution of the Raccoon Procyon Lotor and Other ProcyonidaeThis ebook is for the use of anyone anywhere in the United States and most other parts of the world 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 atwww.gutenberg.org. If you are not located in the United States, you will have to check the laws of the country where you are located before using this eBook.Title: Metabolic Adaptation to Climate and Distribution of the Raccoon Procyon Lotor and Other ProcyonidaeAuthor: John N. MugaasKathleen P. Mahlke-JohnsonJohn SeidenstickerRelease date: May 5, 2011 [eBook #36036]Language: EnglishCredits: Produced by Colin Bell, Tom Cosmas, Joseph Cooper and theOnline Distributed Proofreading Team at http://www.pgdp.net*** START OF THE PROJECT GUTENBERG EBOOK METABOLIC ADAPTATION TO CLIMATE AND DISTRIBUTION OF THE RACCOON PROCYON LOTOR AND OTHER PROCYONIDAE ***
This ebook is for the use of anyone anywhere in the United States and most other parts of the world 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 atwww.gutenberg.org. If you are not located in the United States, you will have to check the laws of the country where you are located before using this eBook.
Title: Metabolic Adaptation to Climate and Distribution of the Raccoon Procyon Lotor and Other ProcyonidaeAuthor: John N. MugaasKathleen P. Mahlke-JohnsonJohn SeidenstickerRelease date: May 5, 2011 [eBook #36036]Language: EnglishCredits: Produced by Colin Bell, Tom Cosmas, Joseph Cooper and theOnline Distributed Proofreading Team at http://www.pgdp.net
Title: Metabolic Adaptation to Climate and Distribution of the Raccoon Procyon Lotor and Other Procyonidae
Author: John N. MugaasKathleen P. Mahlke-JohnsonJohn Seidensticker
Author: John N. Mugaas
Kathleen P. Mahlke-Johnson
John Seidensticker
Release date: May 5, 2011 [eBook #36036]
Language: English
Credits: Produced by Colin Bell, Tom Cosmas, Joseph Cooper and theOnline Distributed Proofreading Team at http://www.pgdp.net
*** START OF THE PROJECT GUTENBERG EBOOK METABOLIC ADAPTATION TO CLIMATE AND DISTRIBUTION OF THE RACCOON PROCYON LOTOR AND OTHER PROCYONIDAE ***
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY · NUMBER 542
Metabolic Adaptation to Climateand Distribution of the RaccoonProcyon lotorand Other Procyonidae
John N. Mugaas, John Seidensticker,and Kathleen P. Mahlke-Johnson
SMITHSONIAN INSTITUTION PRESSWashington, D.C.1993
ABSTRACT
Mugaas, J. N., J. Seidensticker, and K. Mahlke-Johnson. Metabolic Adaptation to Climate and Distribution of the RaccoonProcyon lotorand Other Procyonidae.Smithsonian Contributions to Zoology, number 542, 34 pages, 8 figures, 12 tables, 1993.—Although the family Procyonidae is largely a Neotropical group, the North American raccoon,Procyon lotor, is more versatile in its use of climate, and it is found in nearly every habitat from Panama to 60°N in Canada. We hypothesized that most contemporary procyonids have remained in tropic and subtropic climates because they have retained the metabolic characteristics of their warm-adapted ancestors, whereasProcyon lotorevolved a different set of adaptations that have enabled it to generalize its use of habitats and climates. To test this hypothesis we comparedProcyon lotorwith several other procyonids (Bassariscus astutus,Nasua nasua,Nasua narica,Procyon cancrivorus, andPotos flavus) with respect to (1) basal metabolic rate (Ḣb), (2) minimum wet thermal conductance (Cmw), (3) diversity of diet (Dd), (4) intrinsic rate of natural increase (rmax), and, where possible, (5) capacity for evaporative cooling (Ec). We measured basal and thermoregulatory metabolism, evaporative water loss, and body temperature of both sexes ofProcyon lotorfrom north central Virginia, in summer and winter. Metabolic data for other procyonids were from literature, as were dietary and reproductive data for all species.
Procyon lotor differed from other procyonids in all five variables. (1)Procyon lotor's mass specific Ḣb(0.46 mL O2·g-1·h-1) was 1.45 to 1.86 times greater than values for other procyonids. (2) Because of its annual molt,Procyon lotor's Cmwwas about 49% higher in summer than winter, 0.0256 and 0.0172 mL O2·g-1·h-1·°C-1, respectively. The ratio of measured to predicted CmwforProcyon lotorin winter (1.15) was similar to values calculated forPotos flavus(1.02) andProcyon cancrivorus(1.25). Values for other procyonids were higher than this, but less than the value forProcyon lotor(1.76) in summer. On a mass specific basis,Bassariscus astutushad the lowest Cmwwith a ratio of 0.85. (3)Procyon lotorutilized three times as many food categories asProcyon cancrivorus,Nasua nasua, andBassariscus astutus; about two times as many asNasua narica; and nine times as many asPotos flavus. (4) Intrinsic rate of natural increase correlated positively with Ḣb.Procyon lotorhad the highest rmax(2.52 of expected) andPotos flavusthe lowest (0.48 of expected). The other procyonids examined also had low Ḣb, but their rmax's were higher than predicted (1.11-1.32 of expected). Early age of first female reproduction, fairly large litter size, long life span, high-quality diet, and, in one case, female social organization all compensated for low Ḣband elevated rmax. (5) Although data on the capacity for evaporative cooling were incomplete, this variable appeared to be best developed inProcyon lotorandBassariscus 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 lotorhad the highest composite score (1.47) andPotos flavusthe 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 thatProcyon lotordiffered 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 Ḣbthat is higher than the procyonid norm appears to be the cornerstone of its success.
Official publication dateis handstamped in a limited number of initial copies and is recorded in the Institution's annual report,Smithsonian Year.Series cover design:The coralMontastrea cavernosa(Linnaeus).
Library of Congress Cataloging-in-Publication DataMugaas, 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] 93-3119permanent paperThe 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
Metabolic Adaptation to Climateand Distribution of the RaccoonProcyon lotorand 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 asBassariscus,Arctonasua,Cyonasua,Paranasua,Nasua, andProcyon(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 toArctonasua(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 ofBassaricyonandPotosare 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).BassariscusandBassaricyonrepresent 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).
OrderCarnivoraBowdich, 1821SuborderCaniformiaKretzoi, 1945FamilyProcyonidaeGray, 1825SubfamilyPotosinaeTrouessart, 1904GenusPotosE. Geoffroy and G. Cuvier, 1795P. flavus(S.A., C.A., M.)GenusBassaricyonAllen, 1876B. 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.)SubfamilyProcyoninaeGray, 1825GenusBassariscusCoues, 1887B. astutus(M., wU.S.)B. sumichrasti(C.A., M.)GenusNasuaStorr, 1780N. narica[B](nS.A., C.A., M., swU.S.)N. nasua[B](S.A., sC.A.)GenusNasuellaHollister, 1915N. olivacea(S.A.)GenusProcyonStorr, 1780P. 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.)
OrderCarnivoraBowdich, 1821SuborderCaniformiaKretzoi, 1945FamilyProcyonidaeGray, 1825SubfamilyPotosinaeTrouessart, 1904GenusPotosE. Geoffroy and G. Cuvier, 1795P. flavus(S.A., C.A., M.)GenusBassaricyonAllen, 1876B. 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.)SubfamilyProcyoninaeGray, 1825GenusBassariscusCoues, 1887B. astutus(M., wU.S.)B. sumichrasti(C.A., M.)GenusNasuaStorr, 1780N. narica[B](nS.A., C.A., M., swU.S.)N. nasua[B](S.A., sC.A.)GenusNasuellaHollister, 1915N. olivacea(S.A.)GenusProcyonStorr, 1780P. 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 ofBassaricyonare 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 ofProcyonare 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 Ḣb. Basal and thermoregulatory metabolism of several procyonids have been measured: kinkajou,Potos flavus(Müller and Kulzer, 1977; McNab, 1978a; Müller and Rost, 1983), coatis,Nasua nasua(Chevillard-Hugot et al., 1980; Mugaas et al., in prep.), andNasua narica(Scholander et al., 1950c; Mugaas et al., in prep.), ringtail,Bassariscus astutus(Chevalier, 1985), and crab-eating raccoon,Procyon cancrivorus(Scholander et al., 1950c). In general, these species have Ḣb's that are 40%-80% of the values predicted for them by the Kleiber (1961:206) equation. Lower than predicted Ḣbis viewed as an energy-saving adaptation for procyonids living in relatively stable tropical climates (Müller and Kulzer, 1977; Chevillard-Hugot et al., 1980; Müller and Rost, 1983). This implies that lower than predicted Ḣbis a general procyonid condition and that it represents a characteristic that evolved in response to the family's long association with tropical and subtropical forest environments.
The Atypical Procyonid
Although most procyonids are found in only tropical to subtropical climates, the North American raccoon,Procyon lotor, (Figure 1) has a much broader distribution that extends from tropical Panama (8°N) to southern Canada. In Alberta, Canada, its range reaches the edge of the Hudsonian Life Zone at 60°N (for distribution maps see Hall and Kelson, 1959:878-897, and Poglayen-Neuwall, 1975). Range extensions and an increase in numbers have been noted in Canada and in parts of the United States since the 19th century (Lotze and Anderson, 1979; Kaufmann, 1982; Nowak and Paradiso, 1983:977-985). Thus,Procyon lotoris 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 thatProcyon lotorhas deviated from the typical procyonid portrait and has become the consummate generalist of the Procyonidae.
North American raccoonFigure 1.—North American raccoon,Procyon lotor.
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 lotorpossesses 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 givenProcyon lotorthe 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 comparingProcyon lotorwith several other procyonids (Bassariscus astutus,Nasua nasua,Nasua narica,Procyon cancrivorus, andPotos flavus) on the basis of their (1) basal metabolic rate (Ḣb), (2) minimum wet thermal conductance (Cmw), (3) diversity of diet (Dd), (4) intrinsic rate of natural increase (rmax), and, when data were available, (5) capacity for evaporative cooling (Ec). 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.