Comparative Physiology of Thermoregulation: Special Aspects of Thermoregulation

Comparative Physiology of Thermoregulation, Volume III: Special Aspects of Thermoregulation attempts to do three things: It completes the taxonomic organization of the first two volumes, with a chapter on the ""primitive"" mammals. It deals with special aspects of thermoregulation. Aquatic mammals must be considered in this category because they are the only ""warm-blooded"" animals that live in a medium which has an enormous cooling power compared with that of air. Torpidity is a dramatic thermoregulatory phenomenon displayed by only certain groups of mammals, while the newborn mammal faces special problems in thermoregulation that distinguish it from the adult. Finally, the last chapter complements the arrangement of the first two volumes by its treatment of the evolution of thermoregulation from the standpoint of physiological systems rather than classes of animals. It was initially hoped that this three-volume treatise would provide a useful reference work for the comparative physiologist. The reception accorded to the first two volumes suggests that this hope has been largely realized. However, it appears that the books have their greatest appeal to those engaged in the study of physiological ecology, and this lends to the work a currency which was not entirely anticipated at the time of its conception.

• Language: English
• Publisher: Academic Press
• Release date: Oct 22, 2013
• ISBN: 9781483257433

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Special Aspects of Thermoregulation

Comparative Physiology of Thermoregulation

Volume III

G. CAUSEY WHITTOW

DEPARTMENT OF PHYSIOLOGY, SCHOOL OF MEDICINE, UNIVERSITY OF HAWAII, HONOLULU, HAWAII

Table of Contents

Cover image

Title page

CONTRIBUTORS

Copyright

LIST OF CONTRIBUTORS

PREFACE

CONTENTS OF OTHER VOLUMES

Chapter 1: PRIMITIVE MAMMALS

Publisher Summary

I Introduction

II Phylogeny of Primitive Mammals

III Body Temperature Under Nonstress Conditions

IV Basal or Standard Metabolic Rate

A MONOTREMES AND MARSUPIALS

B PRIMITIVE EUTHERIANS

C RELATIONSHIP BETWEEN METABOLISM AND BODY TEMPERATURE

V Responses of Primitive Mammals to Cold

VI Thermoregulatory Responses to Heat

VII Conclusions

Chapter 2: AQUATIC MAMMALS

Publisher Summary

I Aquatic and Diving Mammals

II Body Temperature

III Metabolic Heat Production

IV Insulation

V Development of Thermoregulation in Infant Aquatic Mammals

VI Aquatic Man

VII Conclusions

Acknowledgments

Chapter 3: TORPIDITY IN MAMMALS

Publisher Summary

I Introduction

II Evolution

III Energy Conservation

IV Patterns of Torpor

V Cellular and Organ Adaptations for Low Body Temperatures

VI Regulation of the Cardiovascular System

VII Nervous System

VIII Endocrine Glands

IX Biochemical Adaptations

X Acclimation

XI Endogenous and Exogenous Rhythms

XII Sleep and Hibernation

XIII Physiological Changes accompanying Hibernation

Chapter 4: THERMOREGULATION IN YOUNG MAMMALS

Publisher Summary

I Introduction

II Body Size and Thermoregulation

III Behavioral Thermoregulation

IV Physical Thermoregulation

V Heat Production

VI The Poikilothermic Response of Newborn Mammals

VII Special Problems Immediately following Birth

VIII Conclusions

Chapter 5: EVOLUTION OF THERMOREGULATION

Publisher Summary

I Introduction

II Body Size, Shape, and Composition

III Body Temperature

IV Heat Production

V Heat Loss

VI Behavior

VII Thermoregulatory Control Mechanisms

VIII Ontogeny of Thermoregulation

IX Conclusions

AUTHOR INDEX

SUBJECT INDEX

CONTRIBUTORS

TERENCE J. DAWSON, DAVID HULL, J.W. HUDSON, LAURENCE IRVING and G. CAUSEY WHITTOW

Copyright

COPYRIGHT © 1973, BY ACADEMIC PRESS, INC.

ALL RIGHTS RESERVED.

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PRINTED IN THE UNITED STATES OF AMERICA

LIST OF CONTRIBUTORS

Numbers in parentheses indicate the pages on which the authors’ contributions begin.

TERENCE J. DAWSON(1),     School of Zoology, University of New South Wales, Kensington, Australia

J.W. HUDSON(97),     Section of Ecology and Systematics, Langmuir Laboratory, Division of Biological Sciences, Cornell University, Ithaca, New York

DAVID HULL(167),     Institute of Child Health, University of London, London, England

LAURENCE IRVING(47),     Institute of Arctic Biology, University of Alaska, Fairbanks, Alaska

G. CAUSEY WHITTOW(201),     Department of Physiology, School of Medicine, University of Hawaii, Honolulu, Hawaii

PREFACE

This third and final volume of Comparative Physiology of Thermoregulation attempts to do three things: It completes the taxonomic organization of the first two volumes, with a chapter on the primitive mammals. It deals with special aspects of thermoregulation. Aquatic mammals must be considered in this category because they are the only warm-blooded animals that live in a medium which has an enormous cooling power compared with that of air. Torpidity is a dramatic thermoregulatory phenomenon displayed by only certain groups of mammals, while the newborn mammal faces special problems in thermoregulation that distinguish it from the adult. Finally, the last chapter complements the arrangement of the first two volumes by its treatment of the evolution of thermoregulation from the standpoint of physiological systems rather than classes of animals.

It was initially hoped that this three-volume treatise would provide a useful reference work for the comparative physiologist. The reception accorded to the first two volumes suggests that this hope has been largely realized. However, it appears that the books have their greatest appeal to those engaged in the study of physiological ecology, and this lends to the work a currency which was not entirely anticipated at the time of its conception. In retrospect, its most appreciated feature would seem to be the comprehensive nature of the accounts of temperature regulation in different groups of animals, something that is rarely achieved by the published proceedings of symposia.

It is a pleasure to record my gratitude to Mrs. Jane Inouye and Miss Myrna Mew of the Department of Physiology, School of Medicine, University of Hawaii and to the stafT of Academic Press for their great help and patience in the preparation of all the volumes.

G. CAUSEY WHITTOW

CONTENTS OF OTHER VOLUMES

VOLUME I

Aquatic Invertebrates

F. JOHN VERNBERG AND WINONA B. VERNBERG

Terrestrial Invertebrates

J. L. CLOUDSLEY-THOMPSON

Fish

F. E. J. FRY AND P. W. HOCHACHKA

Amphibia

BAYARD H. BRATTSTROM

Reptiles

JAMES R. TEMPLETON

Birds

WILLIAM R. DAWSON AND JACK W. HUDSON

AUTHOR INDEX-SUBJECT INDEX

VOLUME II

Rodents

J. S. HART

Carnivores

THOMAS ADAMS

Ungulates

G. CAUSEY WHITTOW

Primates

R. D. MYERS

Man

JAMES D. HARDY, J. A. J. STOLWIJK, AND A. PHARO GAGGE

AUTHOR INDEX-SUBJECT INDEX

Chapter 1

PRIMITIVE MAMMALS

Terence J. Dawson

Publisher Summary

Primitiveness in homeothermy has been attributed variously to animals with relatively low body temperatures, to those with unstable body temperatures, to those with low levels of metabolism, and to those with deficient mechanisms for heat loss. In this chapter, these various aspects of thermoregulation are discussed as they apply to the more morphologically primitive groups of mammals. In this chapter eutherian, rather than placental, is used as the general descriptive term for the nonmarsupial therian mammals; some marsupials have evolved a chorioallantoic placenta. Primitive mammals have been reported as having unusually variable body temperatures, in some cases being referred to as approximately poikilothermic; consequently, there are difficulties associated with determining the normal or desired range of temperatures. Most often, these difficulties are related to the conditions under which measurements are made. In general, such problems apply to all measurements of body or core temperature but become especially important when temperatures are sought for comparisons involving primitive groups. Valid comparisons appear possible when measurements have been made on animals resting in a thermoneutral environment.

I. Introduction

II. Phylogeny of Primitive Mammals

III. Body Temperature under Nonstress Conditions

A. Methodological Considerations

B. Monotremes

C. Marsupials

D. Primitive Eutherians

E. Nychthemeral Rhythms

IV. Basal or Standard Metabolic Rate

A. Monotremes and Marsupials

B. Primitive Eutherians

C. Relationship between Metabolism and Body Temperature

V. Responses of Primitive Mammals to Cold

A. Monotremes

B. Marsupials

C. Primitive Eutherians

D. Hibernation

VI. Thermoregulatory Responses to Heat

A. Introduction

B. Thermoregulatory Responses of Primitive Groups

VII. Conclusions

References

I Introduction

The relationship between the phylogeny of mammals and their homeothermic abilities has been an area of considerable speculation. This interest dates from the latter part of the last century when various workers (de Miklouko-Maclay, 1883, 1884; Semon, 1894; Sutherland, 1897) reported that the body temperatures of monotremes, animals considered to be placed lowest in the scale of mammals (Sutherland, 1897), and marsupials were below and more variable than those found for other mammals. When the metabolic studies of Martin (1902 indicated that not only did these animals have lower body temperatures but also much lower rates of heat production than eutherians,*the idea that anatomically primitive mammals were primitive or inferior homeotherms became widely accepted. Subsequent studies on less advanced eutherians such as the edentates apparently confirmed that they also were endowed with only inferior temperature regulating abilities (Wislocki and Enders, 1935; Britton and Atkinson, 1938; Britton and Atkinson, 1938Irving et al., 1942 and the idea became established that a low and variable body temperature was generally indicative of a primitive level of homeothermism. Eisentraut (1960) classed mammals as higher or lower warmblooded animals depending on whether their activity body temperature was above or below 36°C, phylogenetically old mammals being placed in the lower group.

Initial doubts were cast on the simplicity of this idea when several workers suggested that some marsupials had temperature regulating capabilities equal to those of eutherians (Bartholomew, 1956; Robinson and Morrison, 1957). The issue was still clouded, however, because licking, a supposedly primitive mechanism, was reported to be the principal form of heat dissipation at high temperatures. Recent studies (Dawson, 1969; Dawson et al., 1969; Dawson and Bennett, 1971) have clarified the position of marsupials and shown that some species are excellent homeotherms which utilize similar mechanisms to maintain their body temperatures to those of advanced eutherians. Marsupials, however, do have lower body temperatures and a lower level of standard metabolism than the eutherians (Dawson and Hulbert, 1969, 1970; MacMillen and Nelson, 1969). The problem then is: What is primitive with respect to thermoregulation? There are two aspects to this question; first, the consideration of the level of body temperature under nonstressful conditions; and second, the problem of the stability of body temperature, together with the status of the different mechanisms which are involved in the maintenance of this stability over a wide range of environmental conditions.

Primitiveness in homeothermy has been attributed variously to animals with relatively low body temperatures, to those with unstable body temperatures, to those with low levels of metabolism, and to those with deficient mechanisms for heat loss. In this review these various aspects of thermoregulation are discussed as they apply to the more morphologically primitive groups of mammals. This has been done in order to see if there are patterns of similarity among these animals which enable them to be described, as a group, as primitive homeotherms.

II Phylogeny of Primitive Mammals

Before going on to discuss thermoregulation and primitive mammals, it is necessary to make some general comments about these mammals and their relationships to each other. Table I contains many of the mammals which are regarded by most modern workers as possessing some basic primitive features (Anderson and Jones, 1967; Walker, 1968). Many of them are also highly specialized and discussion is possible about the applicability of the term primitive. This review, however, is not the place for an argument on semantics, and consequently these groups will be referred to as primitive mammals, but with the full understanding that many qualifications of this designation may apply.

TABLE 1

MAMMALS USUALLY CONSIDERED PRIMITIVE

Recent information indicates that the earliest mammals, in the Mesozoic, were much more closely related to one another than was previously thought (Hopson, 1969; Hopson and Grompton, 1969; Parrington, 1971). Contrary to theories of the polyphyletic origin of these mammals from different groups of therapsid reptiles (Kermack, 1967), the evidence now indicates that mammals were derived from a cynodont ancestor, probably within the family Galesauridae in the late Triassic over 200 million years ago. Of this early development and radiation of nontherian mammals there are survivors. These are the three genera of egg-laying monotremes from Australia, the echidnas or spiny anteaters (Tachyglossus and Zaglossus) and the platypus (Ornithorhynchus). The monotremes, in spite of their obvious specialization, have retained many of the features presumed to characterize the earliest mammals, and are therefore uniquely qualified among living tetrapod vertebrates to yield information about the physiology and anatomy of early mammals. There apparently was, however, a very early separation (about 200 million years ago) of the stock leading to the monotremes from that which gave rise to the living marsupials and eutherians, the therians (Hopson, 1969).

The last great radiation has been the radiation of the advanced or therian mammals, which include the marsupials or Metatheria and the placentals or Eutheria. Lillegraven (1969 in his review of the marsupiaeutherian dichotomy in mammalian evolution suggests that the marsupials and eutherians have been distinct for a long time, perhaps since the earliest Cretaceous about 130 million years ago. Another interesting point to come out of Lillegraven’s review was his conclusion that the common ancestor of both groups was probably much more metatherian, i.e., marsupiallike, than eutherian. So while not on the direct line of descent, the more primitive marsupials, such as the smaller opossums and dasyurids, in their mode of life and many structural features, may give a picture of the Mesozoic forms from which the Tertiary mammals have come.

The relationships of the various primitive eutherians are still, to a large extent, unsettled (Szalay, 1968; McKenna, 1969). There appear to be two basic groups among the insectivores but their origins are clouded. The groups comprise on one hand the Erinaceidae, Talpidae, Tenrecidae, Solenodontidae, and Soricidae, and on the other the Macroscelididae and Tupaiidae. The Dermoptera are suggested to have affinities with the latter group of insectivores, while the Tubulidentata and Hyracoidea may be related to the condylarths, which were primitive ungulates. Very little is known about the affinities of the Edentata and Pholidota and their origins are uncertain.

Other groups which may be considered primitive are the bats, order Chiroptera, prosimian primates, and some members of other orders, such as the family Aplodontidae among the rodents. In general these groups will not be discussed since their degree of primitiveness is questionable. Bats have features which are presumed primitive (Jepsen, 1970) and there are indications that some aspects of their thermoregulation may also represent a less advanced position; they usually have lower metabolic rates than other eutherian mammals (Henshaw, 1970; Poczopko, 1971). However, because of the great diversity of thermoregulating patterns in this most specialized group it is difficult to effectively include them in a generalized discussion of primitive mammals. Several excellent reviews of the thermoregulatory capabilities of bats also have been recently published (McNab, 1969; Henshaw, 1970; Lyman, 1970) and consequently those with special interests in this group should consult these reviews.

III Body Temperature Under Nonstress Conditions

The obvious place to start a discussion of primitive mammals and temperature regulation is with body temperature itself, since this is the controlled variable, the end result of the overall process. Primitive mammals have been reported as having unusually variable body temperatures, in some cases being referred to as approximately Poikilothermic (Britton and Atkinson, 1938); consequently there are difficulties associated with determining the normal or desired range of temperatures. These difficulties, most often, are related to the conditions under which measurements are made. In general, such problems apply to all measurements of body or core temperature (Tb) but become especially important when temperatures are sought for comparisons involving primitive groups. Valid comparisons appear possible when measurements have been made on animals resting in a thermoneutral environment. While these conditions may seem easily obtained this unfortunately is not so for measurements on many wild animals.

A METHODOLOGICAL CONSIDERATIONS

Deep rectal or colonic temperature (Tre) is most routinely used to indicate core temperature. While this may not give an accurate assessment of the thermal status of an animal under some conditions, no other easily measured single temperature is better. One of the main problems with this type of measurement is with the depth of insertion of the thermometer, thermocouple, etc. Schmidt-Nielsen et al. (1966) found that in the echidna (Tachyglossus aculeatus) the depth of insertion was very critical, particularly under cold conditions. In this regard the insertion depth of thermometers should be noted when considering some of the early studies which indicated very variable body temperatures in primitive species, e.g., Kredel (1928).

A knowledge of the thermoneutral conditions pertaining to a particular species is important when dealing with primitive animals. While many of the larger advanced mammals have a wide thermoneutral range and also maintain a relatively stable body temperature over a much wider range, the more primitive groups, with perhaps a lower metabolic rate, may have very restricted zones of thermoneutrality (see later discussion); this particularly applies to many of the smaller forms. Lower critical temperatures (Tet) as high as 32°–33°C are possible and measurements made at ambient temperatures (Ta) in the vicinity of 20°C are consequently well outside thermally stress-free conditions. At the other end of the scale, care should be taken to ensure that ambient conditions for measurements are not too hot. While Ta of 30°C may be within the zone of thermoneutrality in many species it may be near the normal body temperature for some of the monotremes. Since these animals are deficient in their ability to prevent overheating, at this Ta their body temperatures rise markedly.

Perhaps the major difficulty which results in considerable problems of interpretation of body temperature measurements is the level of activity of the animals. Periods of intense activity may result in the production of heat at a rate much faster than it can be lost, resulting in a storage of heat and a consequent elevation of body temperature. There are two aspects to the problem: (1) How fast can the body temperature rise during struggling, and (2) how long does it take to return to a steady state after the activity has ceased? The rate of rise is usually more of a problem with smaller animals. Because the metabolism of mammals is related to W⁰.⁷⁵ (Kleiber, 1932, 1961; Dawson and Hulbert, 1969, 1970) the standard or minimal metabolism per unit weight is much greater in small animals than large animals; a 14-gm marsupial mouse has a standard heat production of 6.4 cal/gm hour while that of a 32.5-kg kangaroo is 0.83 cal/gm hour (Dawson and Hulbert, 1970). Maximal metabolism is likewise related to a similar function of weight (Janský, 1965; Pasquis et al., 1970). Consequently a burst of activity in a small mammal will produce a relatively larger increase in heat production per unit weight (i.e., volume), and a greater and more rapid rise in temperature, than would occur in a large mammal. On the other hand, once the body temperature has been elevated much above normal, the rate of decline (rate of heat loss per unit volume) is often slower in large animals since many avenues of heat loss are related to surface area, and larger animals have a lower surface area relative to their volume than have smaller animals.

From the above considerations several of the difficulties which are associated with body temperature measurements, especially single readings, become apparent. Any excitement during the handling of small mammals results in a marked and rapid rise in temperature. Generally speaking, most values reported for normal resting body temperature of small animals should be treated with suspicion unless some form of continuous measurement has been made and activity levels noted. While it may be easier to obtain a reasonable resting body temperature from larger animals, once they are disturbed the Tre may remain elevated for several hours, perhaps upsetting subsequent readings. The only sure way to overcome most of the problems associated with the assessment of body temperature in wild animals is to utilize methods of continuous measurement.

B MONOTREMES

All reports of the body temperatures of monotremes have indicated that this extremely primitive group normally has stress-free temperatures well below the range usually accepted for higher mammals (Table II). The earliest reports of very low temperatures in both the echidna (Echidna hystrix = Tachyglossus aculeatus) and the platypus (Ornithorhynchus paradoxus = O. anatinus) were made by de Miklouko-Maclay (1883, 1884). These findings and additional measurements stimulated suggestions that these species, especially the platypus, were almost Poikilothermic (Sutherland, 1897). Subsequent work by Martin (1902) showed this not to be the case, and while the body temperature of the platypus was low, about 32.7° at 20°C, it was not particularly variable except at higher temperatures. Martin (1902) also confirmed the findings of de Miklouko-Maclay (1883) and Sutherland (1897) that the nonstressed echidna or spiny anteater (T. aculeatus) had a body temperature of approximately 30°C. Many subsequent workers have confirmed these results (Wardlow, 1915; Robinson, 1954; Schmidt-Nielsen et al., 1966; Parer and Metcalfe, 1967a, b; Augee and Ealey, 1968; Augee et al., 1970).

TABLE II

BODY TEMPERATURES OF SOME PRIMITIVE MAMMALSa

aWhere possible body temperatures were obtained from resting animals in their thermoneutral zone.

bSingle values are means and values in parentheses show ranges.

cc Key to references.

a. Parer and Metcalfe (1967a)

b. Robinson and Morrison(1957)

c. Martin(1902)

d. Schmidt-Nielsenetal.(1966)

e. van Rynberk(1913)

f. Morrison(1946)

g. Morrison and Petajan(1962)

h. Britton and Kline (1939)

i. Dawson and Hulbert(1970)

j. Morrison(1965)

k. MacMillen and Nelson(1969)

l. Dawson(1969)

m. Hildwein(1970)

n. Eisentraut(1956)

o. Morrison(1957)

p. Morrison et al.(1959)

q. Galder (1969)

r. Wislocki and Enders(1935)

s. Enders and Davis(1936)

t. Johansen(1961)

u. Bartholomew and Rainy(1971)

v. Taylor and Sale(1969)

C MARSUPIALS

As was the case in monotremes, marsupials were initially reported to have relatively low body temperatures, which were presumed to indicate a stage of development of homeothermy equivalent to their supposed stage of morphological development (Sutherland, 1897; Martin, 1902). The values shown in Table II represent, where possible, recent measurements made under more ideal conditions, i.e., with a knowledge of the thermoneutral zone and with continuous measurement. These measurements for the most part are similar to those reported previously, especially for the larger species. The values given in Table II for the smaller species are lower than those reported by Morrison (1965) and MacMillen and Nelson (1969) for the same or very closely related species. The reason for this difference may lie in the fact that the measurements by Morrison and those by MacMillen and Nelson were made while the animals were being handled.

From Table II it is apparent that the American and Australian marsupials have body temperatures of a similar order, mostly in the range 34°–36°C. It would be of considerable interest to have information about the body temperature of species in the superfamily Gaenolestoidea since this group of opossum–rats from South America is considered as possibly the most conservative of the extant marsupials (Ride, 1962; Hayman et al., 1971).

D PRIMITIVE EUTHERIANS

1 Insectivores

Sutherland in 1897 commented that from the few recorded temperatures of insectivores he judged that they came next (with rodents) above marsupials in increasing homeothermic ability. Current evidence is not as conclusive, since insectivores have been described recently as having very high body temperatures, e.g., the shrew Sorex cinereus (Morrison et al., 1959), and also very low body temperatures, e.g., the tenrec Tenrec ecaudatus (Eisentraut, 1955). A survey of available information (Table II) indicates, however, that most insectivores have relatively low body temperatures, the members of the family Soricidae (shrews) being the exception. Whether the high temperatures recorded for the shrews represent what may be called basal temperatures, or simply reflect the difficulties of measurement associated with these active tiny mammals, is not known. Morrison et al. (1959), in an effort to explain some low body temperatures which were obtained, commented that it may be that these values represent merely the highly unusual condition of complete inactivity.

2 Edentates

The sloths, anteaters, and armadillos of the order Edentata have long been recognized as having low body temperatures (Ozorio de Almeida and Branca de Fialko, 1924a,b; Kredel, 1928; Wislocki, 1933; Wislocki and Enders, 1935; Enders and Davis, 1936; Britton and Atkinson, 1938). The few more recent studies carried out on these animals confirm the relatively low temperatures (Scholander and Krog, 1957; Johansen, 1961). Johansen found that the Tre of the armadillo Dasypus novemcinctus mexicanus was stable at about 34°C when the Ta was 30°C, the temperature at which oxygen consumption was minimal.

3 Other Primitive Groups

Of the body temperature characteristics of other orders of primitive mammals little is known with the exception of the Hyracoidea. Studies by Taylor and Sale (1969) and Bartholomew and Rainy (1971) have indicated that while some members of this group, notably Heterohyrax brucei, have a relatively low body temperature, others have temperatures in the vicinity of 38°C (Taylor and Sale, 1969). The scaly anteater or pangolin Manis tricuspis of the order Pholidota, has been found to have a body temperature in the range 32.2°–35.2°C (Eisentraut, 1956).

Nychthemeral Rhythms

Nychthemeral body temperature rhythms have been reported for several of the primitive mammals. However, because of the conditions of measurement it cannot be determined whether the daily or nychthemeral rhythm is associated with a response to changing ambient temperature, to activity, or to an inherent cycle. Recent studies, using telemetry, on the echidna (Augee et al., 1970), the large kangaroos (Brown and Dawson, 1972), and the rock hyrax (Bartholomew and Rainy, 1971) have not indicated that these primitive species have nychthemeral rhythms markedly different from those found by Bligh and Harthoorn (1965) in advanced eutherian species.

IV Basal or Standard Metabolic Rate

From the preceding discussion it appears that the overall pattern in primitive mammals is one which indicates a lower set of the body thermostat than is the case in the advanced eutherians. Why then the lower regulated body temperature? Since all these animals are supposedly endothermic and rely on a controlled rate of heat production to maintain the body temperature, it is therefore necessary to look at metabolism.

The only valid initial basis for comparison of metabolism is basal or standard metabolic rate (BMR or SMR). This is the minimal level of metabolism and it is attained in thermoneutral surroundings, in a postabsorptive state, and during minimal physical activity. Under these conditions the level of heat production is in excess of the requirement for the maintenance of body temperature, except at the lower critical temperature. In reality the BMR reflects simply the fundamental level of metabolic organization and activity of the animal. Other levels of metabolism, such as maximal metabolism, are generally related to this base value (Jansky´, 1965; Pasquis et al., 1970). This is not entirely true for nonfasting metabolic rate since the specific dynamic effect of feed is related to the type as well as the amount of feed ingested (Kleiber, 1961).

A MONOTREMES AND MARSUPIALS

Information concerning the metabolic levels of primitive mammals tends to be sparse, and only recently have reliable data for monotremes and marsupials become available. The early metabolic studies of Martin (1902) indicated that both the monotremes and marsupials had levels of metabolism which were far below those of eutherian mammals, and these results have been used subsequently in the construction of phylogenies of the development of homeothermy (Johansen, 1962). While recent investigations have shown that both these groups do have a low SMR, the values are not as low as those obtained by Martin (Table III). Unfortunately, recent information is not available for the platypus (O. anatinus).

TABLE III

STANDARD METABOLISM OF VARIOUS PRIMITIVE MAMMALS

aPredicted level is from the equation of Kleiber (1961). SMR = 69 kcal/kg⁰.⁷⁵ day.

bBecause of scarcity of data on monotremes all available is included; that of Martin (1902) may be suspect.

cData on a very small animal is omitted in a recalculation of the data of Enger (1957).

dMuch data on shrews is omitted since thermoneutral conditions may not have been obtained.

There is now good agreement that the marsupials have basal metabolic rates which are approximately 70% of the rates predicted for eutherians by the equation of Kleiber (1961), not 30% as reported by Martin (1902). Dawson and Hulbert (1969, 1970) have shown this to be true for a wide range of Australian marsupials and have suggested the equation

Standrad metabolic rate = 48.6 kcal/kg³/⁴ day

to represent the relationship between standard metabolism and body weight for marsupials. This relationship is very similar to the one reported for twelve species from the family Dasyuridae by MacMillen and Nelson (1969). Other workers, Bartholomew and Hudson (1962) and Arnold and Shield (1970), have obtained similar data from single species.

small amount of information available about the metabolic rates of the American didelphids suggests that they may be similar to the Australian superfamilies. An unpublished observation of T. J. Dawson, E. C. Crawford, and K. Schmidt-Nielsen cited by Dawson and Hulbert (1970) indicates that this may be so for the North American opossum (Didelphis marsupialis virginiana). From his study of the metabolism of some tropical mammals Enger (1957) concluded that the central American form of Didelphis marsupialis had a resting metabolism in accordance with the expected eutherian level. However, analysis of his data (extracted with difficulty from his Fig. 1F) suggests that this may not be correct. Enger examined three individuals, one of which was less than half the weight of the other two, and was thus probably immature. If this small specimen is omitted, then the average SMR of the two larger individuals is approximately 82% of Kleiber’s predicted value. Another possible, but inconclusive, indication of a low SMR in American didelphids comes from the study by Morrison and McNab (1962) of the small Brazilian murine opossum (Marmosa microtarsus). These workers found two apparent levels of SMR, one very similar to the normal eutherian level which they regarded as the true basal level, and one lower, about 58% of the eutherian level. The lower values were obtained as frequently as the higher values and although Morrison and McNab suggested that these values represent some type of depressed metabolic level, it is possible that they are characteristic of the true metabolic level of these small marsupials.

FIG. 1 Comparison of the Metabolism of Small Shrews and Mice. Animals Were Resting but not Fasted and Ta was 28°–30°C; Predicted Values Derived from Kleiber (1961). Redrawn from Hawkins et al. (1960).

B PRIMITIVE EUTHERIANS

Among the eutherian groups that are considered to be primitive, there appears to be a tendency toward low basal metabolic rates (Table III). The low BMR of certain species in the order Edentata has been suspected for some time (Ozorio de Almeida and Branca de Fialko, 1924a, b). In well-controlled studies, Irving et al. (1942) found that the three-toed sloth Bradypus griseus and the two-toed sloth Choloepus hoffmanni had metabolic rates which were well below the predicted eutherian level. Armadillos were also studied by these workers (Scholander et al., 1943) and Enger (1957), and the reported minimal metabolic rates were, in most cases, similar to that found for Dasypus novemcinctus mexicanus by Johansen (1961), which was 57% of the predicted value. Enger (1957) has shown that the low level of metabolism also extends to anteaters of the family Myrmecophagidae.

There has been some controversy concerning the metabolic status of the various groups in the order Insectivora. Recent work carried out under well-controlled conditions has demonstrated that the tenrecoids