The economics of temperature regulation in neutropical bats

Comp. Biochem. Physiol.,

1969, Vol. 31, pp. 227 to 268. Pergamon Press. Printed in Great Britain

T H E ECONOMICS OF TEMPERATURE R E G U L A T I O N IN NEOTROPICAL BATS BRIAN K. McNAB Department of Zoology, University of Florida, Gainesville, Florida, 32601 (Received

12 February 1969)

A b s t r a c t - - 1 . The level and effectiveness of thermoregulation in bats is deter-

mined by the interaction of weight, basal rate of metabolism and thermal conductance. 2. Conductances in tropical bats are greater than expected from weight. 3. Basal rates of metabolism are higher than expected by weight in nectar-, fruit- and meat-eating bats, lower than expected in insectivorous species and intermediate in vampires, this correlation depending upon the seasonal stability of food resources in the environment. 4. Therefore, nectar-, fruit- and meat-eating bats are effective thermoregulators, vampires are marginal regulators and insectivorous species readily enter torpor. 5. Torpor evolved in the tropics in response to the high cost of thermoregulation at a small weight. INTRODUCTION MUCH of biological inquiry is devoted to the study of the means by which organisms are able to maintain internal homeostasis. The capacity for homeostasis varies greatly from one species to another, often in relation to the demands placed by the environment. Still the question remains whether some of the variation in homeostasis is related to the evolution of homeostatic mechanisms. Opinion is divided between those who advocate the importance of historical influences (e.g. Eisentraut, 1960; Cade, 1964) and those who suggest the primacy of ecological control (e.g. Hanu§, 1959; McNab, 1966). Consider thermal homeostasis: to determine the extent to which ecological or historical factors are responsible for the variation in thermoregulation requires that (1)the system determining regulation be understood and (2)the variation in the system's parameters be correlated either with ecology or taxonomy independent of ecology. Obviously, the animals used in the partitioning of responsibility must show varying degrees of homeostasis. Such is the case with bats, where the small, temperate, insectivorous species readily enter torpor (Hock, 1951) and the large, tropical, frugivorous flying foxes regulate their temperatures precisely (Morrison, 1959; Brosset, 1961; Kulzer, 1963, 1965; Bartholomew e t al., 1964). Yet, it is not clear whether this differential response to ambient temperature is associated with size, climate, food habits or taxonomic 227

228

BRIANK. MCNAB

group. Thus, do all large bats regulate body temperature? Or all tropical species ? Or all frugivorous species ? Or only members of the family Pteropidae ? Bats are as unique in the variety of their food habits as they are in their spectrum of temperature regulation. Neotropical bats, for example, feed upon fruit, nectar, vertebrates (including fish) and blood, as well as insects. The few studies available on New World fruit and nectar bats, which are unrelated to those of the Old World, suggest that they, too, regulate their temperatures precisely (Carpenter & Graham, 1967; Morrison & McNab, 1967), but insectivorous members of the fruit-eating family show much less precision of regulation (Reeder & Cowles, 1951 ; Leitner & Ray, 1964). Little is known of the energetics of bats having other food habits: carnivorous bats apparently are precise thermoregulators (Kulzer, 1965; Leitner & Nelson, 1967); there are conflicting data on the thermoregulation of vampires (Wimsatt, 1962; Lyman & Wimsatt, 1966). Food habits seemingly influence temperature regulation, but the basis for this influence is not understood. The cost and level of temperature regulation are determined by the interaction of the basal rate of metabolism, Mb, thermal conductance, C, and body weight, W (McNab, 1966, 1970a). Any factor that influences these parameters could influence thermoregulation. Specifically, certain homoiotherms may have to be energetically parsimonious, thus limiting their capacity for temperature regulation, because of an undependable food supply, since an organism must maintain a balance between its energy input and expenditure. One may ask, then, if food habits have an appreciable influence on Mb, C or W, and therefore upon thermal homeostasis. There are patterns of temperature regulation, however, that are not easily explained by ecological relations. Recent work on insectivorous bats by Brosset (1961) in India and Kulzer (1965) in Africa has shown that tropical members of families that occur in the temperate zone become torpid with a cold exposure, but bats belonging to strictly tropical families maintain intermediate to high body temperatures. It appears as if some bats have carried a propensity for torpor from the temperate regions into the tropics. A definitive analysis of this pattern cannot be made until there is a better understanding of the factors responsible for temperature regulation and torpor. Therefore, it is the object of this paper (1)to clarify the parameters of energetics responsible for temperature regulation and torpor, (2) to evaluate the influence of climate and food habits on these parameters and (3)to determine the pattern of the evolution of thermoregulation and torpor in the order Chiroptera. COLLECTIONS AND METHODS Collections The original data in this paper, consisting of 2500 determinations of body temperature and over 1000 experiments in which the rates of oxygen consumption were measured, were obtained during 1 month in Mexico and 15 months in Brazil. Most coUections in

ECONOMICS OF TEMPERATURE REGULATION I N NEOTROPICAL BATS

229

Mexico were made at two caves: Cueva del Salitre, Lake Tequesquitengo, Morelos, and Gruta de Cacahuamilpa, Guerrero. The studies of temperature regulation in Mexican bats were made in the Instituto de Biologia, Universidad Nacional Aut6noma de M6xico, Mexico City. Brazilian headquarters for the studies on temperature regulation and metabolism were in the Departamento de Fisiologia Germ e Animal, Universidade de Sao Paulo, Sao Paulo. Bats were collected at nearby localities in the state of Sao Paulo: (1) Cotia; (2) valley of the Rio Paraiba at Guararema and Biritiba Mirim; and (3) in the littoral near Bertioga, near $5o Sebasti~o at the Instituto de Biologia Marinha, and near Registro at the Gruta do Diabo. Collecting was also done at Fazenda Bodoquena, Guaicurus, about 100 km southeast of C o r u m b £ State of Mato Grosso. Some trips were made in which physiological measurements, as well as collecting, were accomplished: (1) $5o Jos6 do Rio Preto, $5o Paulo, situated about 400 km north-west of the capital, at the Departamento de Zoologia, Faculdade de Filosofia, Ciencias e Letras; (2) State of Minas Gerais, the collecting occurring near Lagoa Santa and Cordisburgo and the measurements in the laboratory of Dr. J. Pellegrino, Universidade Federal de Minas Gerais in Belo Horizonte; and (3) State of Amazons on the Rio Negro near the junction with the Rio Branco, as a member of the R/V Alpha Helix Amazon Expedition (from the University of California, San Diego).

Methods T h e oxygen consumption and body temperature of bats were measured in response to ambient temperature. Oxygen consumption was monitored by an open system that depends upon a Beckman F-3 Paramagnetic Oxygen-Analyser (McNab, 1966), Body temperature was measured before and after each exposure with a YSI telethermometer. Exposures were for approximately 2 hr or until an individual became quiescent. T h e following measurements of the microclimate were made in day and night roosts: (1) air and surface temperatures (using a YSI telethermometer), (2) radiant temperature (Stoll-Hardy radiometer, Williamson Development Corporation), and (3) relative humidity (Honeywell RH Readout Instrument). Most species of frugivorous, carnivorous and sanguinivorous bats remained healthy in captivity for extended periods of time, although they were generally used within 2 weeks of capture. However, after several attempts to maintain insectivorous species in a healthy condition in the laboratory (especially Noctilio labialis), it became clear that they could not be induced to maintain their original weight, either voluntarily or with hand feeding. Therefore, I decided that all studies on these bats would be done only on individuals that had been in the laboratory less than 24 hr. This requirement restricted the number of insectivorous species to those that could be caught in proximity to a laboratory where the experimental procedures were established. No attempt was made to feed insectivorous bats after this decision was made, and no data are presented here taken on animals prior to this decision.

RESULTS The data on localities of collection, numbers caught, food habits in captivity a n d t h e m i c r o c l i m a t e o f r o o s t s are c o m p i l e d in T a b l e 1 for e a c h s p e c i e s o f b a t t h a t was p h y s i o l o g i c a l l y e x a m i n e d in t h i s s t u d y . T h e r e l a t i o n s h i p s b e t w e e n body temperature and ambient temperature and between the rate of oxygen c o n s u m p t i o n a n d a m b i e n t t e m p e r a t u r e c o n s t i t u t e F i g s . 1-22. Numerical estimates of the parameters of temperature regulation and energetics are s u m m a r i z e d in T a b l e 2 for e a c h s p e c i e s w h e r e a c o m p l e t e (or n e a r l y c o m p l e t e ) set o f d a t a is a v a i l a b l e f r o m t h i s s t u d y or f r o m t h e l i t e r a t u r e .

230

BRIAN K. McNhn TABLE 1--FIELD DATA ON BATS CAUGHT IN MEXICO AND BRAZIL Roost

Species

Saccopteryx leptura Pteropteryx macrotis Noctilio labialis

Localities * collected

Number caught

Food in captivity

Site

13

1

n.f.

Tree trunks

4

7

n.f.

Open caves

3,11

Many

N. leporinus

3,11

Many

Pteronotus rubiginosa P. personatus

2

6

1,2

10

P. davyi Mormoops megalophylla Macrotus waterhousii PhyUostomus discolor P. elongatum P. hastatus Tonatia bidens

Caves

1 Many

n.f. n.f.

Cave Cave

1

Many

n.f.

Caves

11 13 3,4,5,11,13

4,13

Many 1 Many

4

3,13

3

Chrotopterus auritus

4,6,7,8,11

10

GIossophaga soricina

3,4,9,11,13

Carollia perspicillata

n.f.

2 2

T. sylvicola

Anoura caudifer

Crack in bridge Fish, Under shrimp, bridges (at bats night) n.f. Cave n.f.

5,9,10,11 3,4,5,9,11,13

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R.H.++

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--

--

(%)

27-28

81

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(1)

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77-81

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(4)

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20-22

78

(1)

(1)

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14-22

77-93

(4)

(3)

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70-94

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(1)

19-27

70-98

(5)

(4)

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19-26

92-98

(4)

(3)

?

culverts, buildings

231

ECONOMICS OF TEMPERATURE REGULATION IN NEOTROPICAL BATS

TABLE 1

(cont.) Roost

Species

Rhinophylla pumilio Sturnira lilium Uroderma bilobatum Vampyrops lineatus Vampyr essa nymphae Artibeus jamaicemis A. Hturatus A . cinereus A. concolor Ametrida minor

Desmodus rotundus Diaemus youngi DiphyUa ecaudata

Natalus stramineus Histiotus velatus Molossus molossus

Localities* collected

Number caught

Food in captivity

Site

Temperature ++ (°C)

R.H. ++ (%) __

13

9

Fruit

?

R

3,9,11,12

Many

Fruit

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--

13

6

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?

--

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3

11

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--

--

13

5

--

3,13

4

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9,11,12,13

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13 13 13

5 9 1

3,4,5,6,8,9, 11,13 13

Many

4,5,8,9

13

1

Many

11

4

n.f.

11,13

10

n.f.

2

Fruit

T r e e foliage, cave ? ? ?

Fruit Fruit Killed before feed M a m m a l Caves blood Chicken Hollow tree blood (area 7) Chicken Caves and guineapig blood n.f. Cave

Buildings in cemetery ?

-19 (1) ~ -__

98 (1) --m

13-25 (11) 20-22 (1) 19-25 (5)

78-98 (11) --

27-28 (1) 25 (1) --

81 (1) --

80-98 (5)

* Localities: (Mexico) 1, Tequesquitengo ; 2, Cacahuamilpa. (Brazil) 3, Fazenda Bodoq u e n a ; 4, Lagoa Santa; 5, Cordisburgo; 6, Cotia; 7, Guarar6ma; 8, Biritiba M i r i m ; 9, $5o SebastiSo; 10, Registro; 11, $5o Jos6 do Rio Preto; 12, Campus Universidade de S~o Paulo; 13, Rio Negro. t n.f. = insectivorous, n o t fed in captivity. ++Range of values ; the figures in parentheses are the n u m b e r of roosts where measurem e n t s were made.

232

BmAN K. McNAB

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FIC. 1, Relation of body temperature and oxygen consumption to ambient temperature in forty Noctilio labialis.

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FIG. 2. Relation of body temperature and oxygen consumption to ambient temperature in seventeen NoctiIio leporinus. Crosses ( × ) indicate lethal experiments.

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OF TEMPERATURE

REGULATION

IN NEOTROPICAL

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FIG. 3. Relation of body temperature to ambient temperature in six _Pteronotus rubiginosa, eight Pteronotus personatus and fifteen Mormoops megalophylla. Vertical lines represent the mean + 2 S.E. Numbers indicate sample size. 40

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ENVIRONMENTAL TEMPERATURE (.°C~

FIG. 4-. Relation of body temperature to ambient temperature in one Saccopteryx leptura, two Pteropteryx macrotus, fourteen Macrotus waterhousii and twenty-nlne Natalus strarnineus. Vertical lines represent the mean _+2 S.E. Numbers indicate sample size.

234

BRIAN K. McNAB

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FxG. 6. Relation of body temperature mad oxygen consumption to ambient temperature in twelve Phyllostomus discolor and one P. elongatum.

235

ECONOMICS OF TEMPERATURE REGULATIONIN NEOTROPICAL BATS 48

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FIG. 7. Relation of body temperature and oxygen consumption to a m b i e n t temperature in fourteen Phyllostomus hastatus. Crosses ( + ) indicate lethal experiments.

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FIG. 12. Relation of body temperature and oxygen consumption to ambient temperature in seven t~inophylla pumilio. The cross ( + ) indicates a lethal experiment.

BalAN K. McNAB

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FIG. 14. Relation of body temperature and oxygen consumption to ambient t e m p e r a t u r e in t w o gampyrops lineatus and two Uroderma bilobatum.

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E C O N O M I C S OF TEMPERATURE R E G U L A T I O N I N N E O T R O P I C A L BATS

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FIo. 18. Relation of b o d y temperature and oxygen consumption to ambient temperature in one Artibeus cinereus, three Vampyressa nymphae and one Ametrida minor. I n the text these data are referred to as "small stenodermids".

241

E C O N O M I C S OF TEMPERATURE R E G U L A T I O N I N N E O T R O P I C A L BATS

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FIG. 19. Relation of body temperature and oxygen consumption to ambient temperature in forty Desmodus rotundus (twenty-seven from Mexico and thirteen from Brazil). The measurements from Mexico on body temperature only are represented by a mean _+2 S.E. and sample size.

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ECONOMICS OF TEMPERATURE REGULATION I N NEOTROPICAL BATS

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The analysis of these data shall be left to the ensuing sections of this paper; in this section the data available from this study are compared with those available in the literature on the same species. Of the 34 species examined in this paper, only 8 have had their energetics even partially examined before. According to Stones & Wiebers (1965), Gudger (1945) observed that the fish-eating bat Noctilio leporinus had high body temperatures when active and low temperatures when inactive. In fact Gudger simply said that " . . . bats in our temperate l a t i t u d e . . . " have these characteristics, implying that Noctilio is similar. Gudger's original observations were confined to the behavior of these bats in the Caribbean. Morrison & McNab (1967) reported incomplete data on several species. Unfortunately they pooled the data for two species of Artibeus and two species of Phyllostomus. There is good agreement between the level and preciseness of temperature regulation reported by them and those reported here. The only exception is that they describe P. discolor as having poor temperature regulation. It is now apparent that this bat requires a small, but regular, intake of meat; their results may be have been due to a nutritional deficiency. The clear influence of the nutritional state upon temperature regulation is further seen in Molossus. In this study Molossus that were freshly caught in the field showed intermediate thermoregulation, while the poor regulation described by Morrison & McNab (1967) came from force-fed individuals. The force-fed bats gradually lost weight with time; their poor thermoregulation undoubtedly reflected a poor nutritional condition. A similar explanation seems responsible for the difference found by Herreid (1963a, b) between field and laboratory (36 hr or more after capture) values on Tadarida brasiliensis. These data emphasize the importance of using freshly caught specimens of bats that do not readily feed in the laboratory. It is difficult to account for the discrepancy between my data on Desmodus and those of Lyman & Wimsatt (1966). Although the measurements of food intake by Wimsatt (1962) suggested thermoregulation in this vampire, the later study by Lyman & Wimsatt (1966) indicated very poor regulation, similar to that which I found in starved vampires, which suggests again that the nutritional state may have been influential. Their animals were taken from a laboratory colony, while all of mine were field caught. THE ENERGETICS OF THERMOREGULATION

An analysis of the energetics of thermoregulation (McNab, 1970a), based in part on the data presented in this paper, suggests that the level of regulated body temperature (Tb) is determined by the interaction of the (1) basal rate of metabolism, (2)thermal conductance and (3)body weight. It was suggested earlier (McNab, 1966) that Mb and C are determined, in turn, by the habits of the animal in question and the physical characteristics of its environment. In this section various aspects of the thermoregulation of bats will be examined relative to variations in the parameters Mb, C and W.

246

BRIAN K. MCNAB

The determination of M b and C The mean basal rates of metabolism are plotted as a function of body weight for each of the species in this study and for data taken from the literature (Fig. 23). Kleiber's (1960) standard equation relating the basal rate with weight 5,

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Kleiber (1960). is also plotted in this figure. The basal rate of metabolism correlates with food habits: all frugivorous, nectarivorous and carnivorous bats have basal rates equal to, or greater than, the values expected from weight alone, except at very high weights. Insectivorous species have basal rates significantly below this curve. Vampires are intermediate with two of three species having low rates. An interpretation of the influence of food habits will be deferred until later in this article. Conductances are compared in Fig. 24 with weight function described for mammals by Herreid & Kessel (1967). Nearly all bats have higher conductances than expected by weight irrespective of food habits. These data are in accord with those of Scholander et al. (1950) in suggesting that tropical mammals have a poorer insulation than temperate species of the same weight. The mild environmental temperatures and, thus, the reduced rates of heat loss in tropical bats reduce the necessity for a heavy insulation.

Setting the level of body temperature The level at which a homoiotherm regulates its temperature depends upon the ratio of the basal rate of metabolism to conductance, Mb/C, and the extent to which the values for these parameters expected from weight are realized

247

E C O N O M I C S OF T E M P E R A T U R E R E G U L A T I O N I N N E O T R O P I C A L BATS

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(McNab, 1970a). The ratio (Mb/C), expected by weight is equal to (3"4 W-°'2s/1.02 W -°'51) = 3.33 W °'~e. The ratio (Mb/C), is expressed relative to the values expected from weight. As a result the level of body temperature is given by Tb (Mb/C),(Mb/C), + 27.0 = 3.a3(MdC),W°'2e+27.0 (McNab, 1970a). Accordingly, body temperature is plotted as a function of 3.33W °'26 in Fig. 25. The level of Tb is proportional to W °'~6 up to a given weight, which might be =

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248

BRIANK. McNaB

called the "critical" weight, beyond which temperature is constant. The critical weight for bats having ratio (Mb/C)~ equal to 1.0 is about 100 g. If a bat has a ratio (Mb/C)r equal to less than 1.0, the critical weight increases: for a ratio equal to 0.65, the critical weight is about 200 g for bats. But if the ratio is increased to 1.2, the critical weight is reduced to about 40 g. Therefore, small species can in fact have high temperatures, if their energy expenditure is sufficiently high to compensate for their low weight. The high Tb of the small (3"3 g) shrew, Sorex cinereus, is due to a ratio (Mb/C)~ equal to about 2.9 (Fig. 25 ; Morrison et al., 1959). Small bats, then, tend to have lower temperatures than large species, as is clearly seen within the genus Artibeus: the large (70 g) A. literatus has a mean temperature equal to 37.3°C; A. jamaicensis, 45 and 36.2; A. concolor, 20 and 35.3; and .4. cinereus, 10 and 34.7. Similar trends are seen within the genera Noctilio and Phyllostomus, and among insectivorous bats. This weight dependency holds because the ratio (Mb[C)~ remains rather constant within each sequence. But when (Mb/C)~ compensates for weight, body temperature is independent of weight: e.g. see the carnivorous sequence Macroderma, 148 g, and (M~/C)~ = 0.85; Chrotopterus, 96 and 0.97; and Tonatia, 27 and 1.29.

The regulation of body temperature There are at least two aspects of thermoregulation that are of concern: (1) its precision, which may be conveniently measured by the coefficient of variation of Tb (c.v. = 100s/£) over a range in Ta where Tb is independent of Ta and (2) the change in body temperature per unit change in ambient temperature (ATb/ATa). The coefficient of variation is typically about 2 or 3, but increases as both ratios (Mb/C)e and (Mb/C)r decrease (Fig. 26), although Phyllostomus hastatus does not fit the general pattern. A small c.v. can be maintained at a small weight, if the ratio (Mb/C)~ is appreciably above 1.0. McNab (1966) has shown that

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249

ECONOMICS OF TEMPERATURE REGULATION I N NEOTROPICAL BATS

ATdAT~ roughly depends upon the ratio (Mb/C),; inspection of the data on tropical bats (Fig. 27) indicates that ATdATa was usually less than 0.03 over the Ta range from 30 to 10°C, but was greater if (1) the ratio (MblC)r was low or (2) the bat was small. 0,0 ÷

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a. Facultative torpor Given the above analysis for thermoregulation it remains to be seen if all examples of poor regulation can be explained by the interaction of the ratio

250

BRIAN K. McNAB

(Mb/C)r with weight. Specifically, some small, insectivorous bats, such as Saccopteryx, Peropteryx, Pteronotus and Natalus, have poor thermoregulation, even though limited in their distribution to the tropics. Unfortunately, few data on the energetics of these bats are available, but enough is known of other species to estimate the energetics of, say, Natalus. Natalus is very small (weight = 4.2 g; N = 13). It shows little evidence of temperature regulation, ATO/ATa being about 1.0 and the mean AT being 3.1°C (Fig. 4). If the ratio (M~/C)r in Natalus is typical for tropical, insectivorous bats (about 0.6), ATO/AT~is expected to be about 0.67 (Fig. 27), or two-thirds of the observed value. It is difficult to know whether this discrepancy represents an inadequacy in the analysis or whether, once the body temperature has fallen to a low level in such a small animal, To will continue to fall to ambient levels. Nevertheless, the poor thermoregulation in Natalus and the other small, insectivorous bats is mainly due to their small weights and, presumably, low rates of heat production. A similar temperature lability is characteristic of temperate bats. Many data are available on the rates of heat production in temperate bats, but few on conductances, since these bats when quiescent rarely maintain an appreciable A T. The data for Myotis austroriparius (McNab, unpublished observations) and M. myotis (Hanu~, 1959; Mejsnar & J~nsk~?, 1967) suggest that temperate insectivorous bats, like their tropical counterparts, have low ratios (Mb/C)r as a result of low basal rates of metabolism (Table 3). The combination of a low basal rate and a small weight (7 g) in M. austroriparius accounts for only 60 per cent of the fall in TOthat occurs with a decrease in ambient temperature (Table 3). This inability to predict ATO/AT~ is accentuated in larger bats, such as M. myotis. Considering that some temperate bats, e.g. Nyctalus noctula and Lasiurus borealis, weight up to 30 or 40 g, it is clear that the interaction of the ratio (Mb/C)r and W is not able to account for their poor thermoregulation. In seeking an explanation for the occurrence of torpor in temperate bats, there is value in examining the energetics of the pigmy mouse (Baiornys taylori) and the pocket mouse (Perognathuscalifornicus). Both of these mice show a torpor that at times has the daily periodicity typical of temperate bats (Hudson, 1965; Tucker, 1965). At low ambient temperatures the temperatures of these mice fall into two distinct groups: (1) in which a large AT is maintained and (2) in which Tb is nearly equal to Ta. A similar behavior can be seen in the small, frugivorous bat RhinophylIa pumilio (Fig. 12). The small weight (7 g) and low ratio (Mb/C)~ of Baiomys can account for the fall in TO with a decrease in T~ only when an appreciable AT is maintained, but one cannot predict that this mouse will often show no regulation at cool temperatures. This analysis also holds for Perognathus and Rhinophylla. It appears, therefore, that there are two types of torpor, one that is forced upon an animal and another that occurs when thermoregulation is not "attempted", even though the capacity for regulation exists. The first type of torpor may be called "obligatory", and the second "facultative".

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Obligatory torpor occurs in homoiotherms that either are very small or have a limitation to their energy expenditure imposed by food habits, heat exchange, water loss, etc. Actually, both of these factors are identical, since it has already been shown that a large ratio (Mb/C)~ can compensate for a small weight. If that compensation has not occurred, it is presumably because of some ecologically imposed restrictions on energy expenditure. An extreme example of obligatory torpor in mammals is found in the naked mole-rat, Heterocephalus glaber, which has a ratio equal to 0.2 (McNab, 1966) corrected to mean values; most poikilotherms would also fall into this category. The torpor of temperate mammals capable of entering into hibernation and estivation is facultative, as is shown by their capacity for spontaneous arousal, their thermoregulation during hibernation at cold temperatures and their precise maintenance of high body temperatures during periods other than those of hibernation. Facultative torpor may be compared to "turning down the thermostat", and represents a "strategy" to overcome daily or seasonally unfavorable conditions in the environment. The regulated torpor of temperate insectivorous bats is associated with a seasonally restricted food supply and the subsequent necessity to depend upon fat stores for their energy expenditure, which is possible only because of the low body temperatures typical of torpor. The torpor found in small bats has both obligatory and facultative elements. The obligatory aspects are a result of a low ratio (Mb/C)r for the weight and is demonstrated by a low regulated T~ and a high ATb/ATa. The facultative features are shown by the occasional (or repeated) fall of body temperature to ambient levels (e.g. in Rhinophylla and Artibeus cinereus) and by the ability of all small bats, including Natalus, Peropteryx and Rhinophylla, to spontaneously arouse from torpor. Their small weights, however, prohibit the regulation of a high Tb at cool temperatures for long periods. Small bats, irrespective of food habits, are similar in energetics to humming-birds in that they both have periodic feeding habits and, consequently, show torpor. They contrast with shrews of equal weight, which have essentially a continuous feeding schedule; shrews are not known to go into torpor.

b. Peripheral cooling Body temperature was measured after each experiment with a thermistor inserted into the colon. Normally this temperature remains stable for a few seconds to a minute after removal of the animal from the experimental chamber; thereafter Tb gradually rises, reflecting an increase in activity and, if the exposure had been to a low Ta, a reduction in the rate of heat loss. However, on occasion there is a sharp fall in colonic temperature after removal from a cold exposure. Most species of bats in this study showed at times a drop of a few tenths of a °C, but several, e.g. those belonging to the genera Phyllostomus, Sturnira and Artibeus, showed decreases in temperature as great as 2 or 3°C. Apparently the drop in temperature is due to the return to the core of blood that was cooled in the peripheral tissues. In one case a Phyllostomus discolor was

ECONOMICS OF TEMPERATURE REGULATION IN NEOTROPICAL BATS

253

retrieved from an ambient temperature of 24"5°C; the body temperature originally stabilized at 33.8°C, then rapidly fell 1.8°C to stabilize again at 32.0°C. After removing my finger from the base of one wing, the Tb fell to 31.3°C, suggesting that I had restricted the venous return of cool blood to the core. Two parameters of peripheral cooling, the volume of tissue included in the shell and the temperature to which it falls, are of interest because of the large, poorly insulated surface of bats. These parameters are difficult to measure directly. But some insight is given into the factors involved in peripheral cooling by the following model. Assume that the body is divided into two fractions, core and shell, each having a uniform temperature. Then

Tc-A =

where ~ is the mean body temperature, T~ is the core (colonic) temperature, T~ is the shell temperature, V~ is the volume (mass) of the core, V~is the volume (mass) of the shell and Vt is the total volume (mass) of the animal. It follows that VJV, = ATd(T~ - T~). Only ATb and Te are directly known. If the fraction V~/V~is known, T~ can be calculated. An independent estimate of the ratio ~/Vt was based on the assumption that the shell maximally includes the wings, legs, tail, ears, nose leaf and associated membranes. These structures constituted 26 per cent of the total weight in each of two P. discolor and 25 per cent in one P. hastatus. T~, then, can be estimated for given values of Tc and ATb (Table 4). ~ must be equal to or greater than T~, if there is no appreciable evaporative water loss: even in the cases where AT = T ~ - T a is small and AT~ is large, the calculated values for are within 0.4°C of the ambient temperature. But there are many more small than large declines in body temperature, indicating that the entire shell only occasionally falls to ambient levels. Normally, either a large shell is within a few degrees of the core temperature or a small shell, possibly equal to the membranes alone, is near T~. Even for a large ATb the shell could be as small as 5 per cent of the total body mass (Table 4). Presumably the temperature distribution in bats during a cold exposure will vary between the conditions of V~/V,= 0.0, T~ = T~> T, and VJV~= 0.26, T~ > ~ = T~,. The rationale behind peripheral cooling in bats is not clear. Irving (1956) and Irving & Hart (1957) have shown in swine and seals that the cooling of peripheral tissues during a cold exposure reduces thermal conductance. If peripheral cooling conserves heat in tropical bats, conductance should decrease as ATb increases. But C is independent of ATb (Fig. 28). C is correlated with Tc: five of the eight species show a regression coefficient for C on core temperature that is significantly greater than 0"0. Two species of Artibeus had low t-values simply because they show such precise thermoregulation that their range in T~ is small. (Ninety-three per cent of the variation in the t-values is accounted for by the range in Te; r = 0"93, excluding Noctilio labialis.) Noctilio labialis is the only species examined that did not show a dependency of C on T~. Therefore,

254

BRZAN K. MCNAB

TABLE 4

SHELL

VOLUMES AND TEMPERATURES FOR EXTREME VALUES OF PERIPHERAL COOLING IN SOME TROPICAL BATS

Species

NoctiIio labialis PhylIostomus discolor P. discolor P. hastatus Sturnira lilium Artibeus yamaicensis d. lituratus

Ta

Tc

ATb

G/Vt*

Ts t

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29"4 33"8 34.5 35"3 37"9 36.7 39"8

1.0 2.5 2.6 2"0 3'0 0.8 1.2

0"29 0"27 0"13 0"08 0' 13 0"05 0"05

25"6 24"2 24.5 27"6 26"4 33'6 35"2

Symbols: Ta, ambient temperature; To, core temperature; ATb, fall in core temperature after a cold exposure; Vs/Vt, fraction of the total volume constituting the shell; T,, shell temperature. * Assuming T s = T a. Assuming Vs/V~= 0"26.

0

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c. The " relaxation" of temperature regulation Certain species of tropical bats (Phyllostomus discolor, Tonatia bidens and occasionally Chrotopterus auritus and Noctilio leporinus) show a reduction in

ECONOMICS OF TEMPERATURE REGULATION Il~/ NEOTROPICAL BATS

255

core temperatures at mild environmental temperatures, but have higher tempcraturcs at low ambient temperatures. Kulzer (1955) has demonstrated a similar response in the palaeotropical species of the genera Rhinopoma, Taphozous, Asellia and Tadarida; it can also be seen in Leptonycteris (Carpenter & Graham, 1967). Since these bats can maintain a high temperature at ambient temperatures below those at which an intermediate level of regulation occurs, one cannot ascribe this intermediacy to a poor capacity for thermal homeostasis. Some type of "relaxation" of strict thermoregulation apparently is responsible for this behavior, since the precision, as well as the level, of regulation falls. According to Newton's law of cooling a low body temperature may be due to either a low M or a high C. The level of Tb described here is due to a rate of metabolism reduced by about 30 per cent at 20°C; conductances in the temperature range of the reduction are either equal to or less than those found at lower ambient temperatures. In those bats that permit a reduced Tb, the frequency of intermediate temperatures is maximal at ambient temperatures of 20-25°C; the frequency decreases at both higher and lower temperatures (see, especially, P. discolor and T. bidens). Temperatures of 20-25°C are characteristic of the roosts of the bats exhibiting this behavior (Table 1). The "relaxation" of thermoregulation, then, has the effect of reducing the energy expenditure of bats at temperatures that are commonly encountered, but which offer no risk of exposure to lower environmental temperatures because of the thermal stability of the roosts. Although this behavior does not appear to depend upon food habits, it may be correlated with roosting sites, since there is no evidence of its occurrence in foliage-inhabiting bats, such as in members of the Stenoderminae (Artibeus, Vampyrops), in which the roost microclimates are much less stable.

d. Clustering Clustering is well known in both temperate and tropical bats. Twente (1955) and Hall (1962) have argued that it reduces the influence of variations in the external environment due to a collective reduction in the surface-volume ratio. For animals in torpor a cluster tends to preserve a low Tb in spite of short-term variations in ambient temperature. For animals that thermoregulate there is a reduction in the cost of thermoregulation with clustering (Pearson, 1960; Herreid, 1963b). Some preliminary observations were made on P. discolor, a bat fanatically dedicated to compact clusters. The experimental protocol was as follows: a bat was placed in a tall jar and its rate of oxygen consumption was measured at 20°C. After 2 hr it was removed and its Tb measured. Then the bat was returned to the chamber and a second individual added. Their collective oxygen consumption was measured. After 2 hr the second bat, which had remained on top of the first bat, was removed and its temperature measured. The temperature of the first bat was then measured. The bats were replaced in order into the

256

BRI~ K. McNAB

chamber and a third bat was added. This sequence continued once for three bats and again for four. Although one might expect that the bat on the bottom would have the highest Tb because of a reduced temperature differential, Tb was always the highest in the top bat and progressively fell to that in the bottom bat, even though the vertical temperature differential in the chamber was less than 0.5°C (Fig. 29A). Furthermore, the mean temperature of the bats usually fell as the number of bats making up a "cluster" increased (Fig. 29B). As a result, then,

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2,0 ~,=

0-,@ I - - 3

30

i

•,

Ov ~

i

SEQUENCE OF REMOVAL

NUMBERS OF BATS IN CLUSTER

oc

FIG. 29. Influence of clustering on temperature regulation in Phyllostornus discolor. A. Relation of body temperature to the sequence of removal of bats from the experimental chamber. B. Relation of body temperature and the mean rate of metabolism to the size of cluster. Ambient temperature is 20°C. of a reduction in both the ratio surface/volume and the mean body temperature, the minimal rate of metabolism progressively fell with an increase in group size (Fig. 29B). Clearly, the thermolability found in isolated P. discolor at 20°C is accentuated by the presence of additional individuals. It would be of interest to know to what extent a similar influence may occur in T. bidens. THE INFLUENCE OF FOOD HABITS ON ENERGETICS It has been shown that food habits (or its correlate, the basal rate of metabolism) and body weight are the most important factors determining the thermoregulation of bats. This section explores the causes for the correlation of energetics with food habits, which we shall see is closely related to the factors responsible for the geographic distribution of food habits. First, it is important to note that food habits and body weight are interdependent.

ECONOMICS OF TEMPERATUREREGULATIONIN NEOTROPICALBATS

257

The distributions by weight of species having a common food habit have several distinctive features (Fig. 30): (1) they are approximately log-normal, being highly skewed towards small weights; (2) the modular weight class for a WISCONSIN INSECTS - - • - -

/~\

(s.o.o)

.......

4O

. .......

~'~:~._=.,

TAMAULIPAS," MEXICO (24,11,0)

X

4O

,.~zo (D VERACRUZ, MEXICO

a'~4o

.o'il

"

.J

°

•

WEIGHT CLASSES (O)

FIG. 30. Distribution of bats within a food habit by weight in various geographic areas. Numbers indicate species having insectivorous, frugivorous and carnivorous habits, respectively; nectarivorous and sanguinivorous species where excluded. Data assembled from Cockrum (1960), Goodwin & Greenhall (1961), Jackson (1961), Husson (1962), Alvarez (1963) and Hall & Dalquest (1963).

food type remains constant irrespective of the environment, as long as the sample size is large; (3) the modular and smallest weight classes are the least in insectivorous bats, intermediate in frugivorous species and largest in carnivorous bats (with the curious exception of some of the Old World fruit bats); (4) the smallest weight class for each food is more prominent in the tropical lowlands than in subtropical or temperate regions; and (5) insects are the only common food resource in temperate regions. Food habits influence the weight of bats through the frequency distribution of food particles by size: insects are generally small and the vertebrates that constitute a carnivorous diet are relatively large, most fruits being intermediate in size. Much of the great range in weight found within a food habit apparently results from the competitive partitioning of a food resource by food particle size (McNab, 1970b). The large size of flying foxes is potentially accounted for by two facts: (1) the fruits that they use are appreciably larger than those used by small fruit bats (Baker & Baker, 1936; Pijl, 1957), and (2) some of the fruits in the

258

BRIAN K. MCNAB

Old World tropics, such as mango, banana and breadfruit, attain larger sizes than those native to the New World tropics. Since the weight of bats is a variable dependent primarily upon food particle size, most of the variation in temperature regulation found in bats is determined by the correlation of the basal rates of metabolism with food habits (Fig. 23). Why do frugivorous, nectarivorous and carnivorous species have high basal rates, while insectivorous and sanguinivorous species have low rates ? The nutritional quality of the food does not seem to be responsible, since carnivorous and insectivorous species use foods of a similar quality, even though they have markedly different energetics. Furthermore, fruit bats have high rates of energy expenditure, although using foods of high water and low caloric contents. Surely the energetics of vampires cannot be explained by inadequacies in nutritional quality. The factors responsible for the level of metabolism must be sought elsewhere and in doing so each of the major food habits will be examined in turn. The occurrence of fruit and nectar bats in a locality depends upon the presence of a tropical forest rich in trees that flower and bear succulent fruits (e.g. in Tamaulipas, Mexico; Koopman & Martin, 1959). A lowland tropical forest flowers and fruits throughout the year with seasonal maxima synchronized with a wet-dry cycle of rainfall (Richards, 1957; Snow & Snow, 1964; Janzen, 1967). But the dependence upon fruit and nectar as food requires a continual supply (Baker & Baker, 1936). Baker (1936), Snow (1965) and Janzen (1967) have argued that the evolution of year-round reproduction in tropical forests depends upon the presence of obligate fruit and nectar feeders, such as certain birds and bats. Thus, a reciprocal dependency has been established between flowering trees and the bats that feed upon them (Pijl, 1961). Temperate forests are almost devoid of flowering trees and of succulent fruits. Consequently, fruit and nectar bats are excluded from temperate forests (except for a few transient species, such as Leptonycteris nivalis, which follows the Saguaro cactus and Agave into Arizona, only to migrate to Mexico at the end of the flowering period for these plants; Beatty, 1955; Cockrum & Hayward, 1962). It has been suggested that the relative scarcity of nectarivorous bats in Africa may be due to a scarcity of flowers during parts of the year (Pijl, 1957). Most fruit-eating birds, such as parrots, plantain-eaters, toucans, hornbills, and cotingas, are also exclusively tropical. Temperate forest birds that are vegetarian usually feed on dry seeds, and those that feed upon fruits do so in an opportunistic manner, depending heavily upon insects during the breeding season. The natural foods of most carnivorous bats are nearly unknown. Wood-Jones (Troughton, 1947) has proposed that the carnivorous Macroderma gigas feeds mainly on insectivorous bats in Australia. It may be, then, that a carnivorous food habit is the first to disappear along a transect from tropical to temperate conditions (Fig. 30), because bats are neither an abundant nor a seasonally stable food resource in temperate regions. Carnivorous bats are also excluded from tropical islands when the diversity (as related to abundance ?) of bats is low, irrespective of island size (McNab, 1970b).

ECONOMICS OF TEMPERATURE REGULATION I N NEOTROPICAL BATS

259

There is reason to believe that fish-eating bats are physiologically and ecologically distinct from bats that feed upon other vertebrates. First, the two species that have been studied, Noctilio leporinus and Pizonyx vivesi (Carpenter, 1968), have basal rates of metabolism that are low relative to those of other carnivorous species, being approximately equal to the rates expected from weight (Fig. 23). Secondly, the diet of these bats consists to a great extent of foods other than fish, such as insects in Noctilio (Goodwin & Greenhall, 1961 ; Villa-R., 1966) or insects and crustaceans in Pizonyx (Reeder & Norris, 1954; Bloedel, 1955). These data lead to the impression that fish-eating bats are basically insectivorous bats that have had a modest increase in their basal rates to accompany the particle change in their food habits. It is interesting that the closest relative of N. leporinusis completely insectivorous, and that many classify P. vivesi within the insectivorous genus Myotis, one member of which has been shown to take fish in captivity (Brosset & Deboutteville, 1966). Noctilio and Pizonyx may be restricted to tropical and subtropical regions because of the few surface-dwelling fishes occurring in temperate waters. Vampires are limited to the tropics and the adjacent subtropics; this pattern cannot be due to the absence of adequate food supplies in temperate regions, considering the herds of cattle present in contemporary Texas. Some evidence (McNab, 1970c) suggests that vampires may be excluded from temperate regions by a sensitivity to low ambient temperatures induced by their low rates of metabolism. The only explanation for these low rates that I can envisage is that they are an adaptation to balance an energy budget that has a restricted income. This suggestion may appear ludicrous considering the large numbers of cattle, horses, donkeys, chickens and turkeys, not to mention people, that are presently available as food in Latin America. But one should realize that almost all of these domesticated animals were imported into the New World: in Precolumbian times there were relatively few, large, herding mammals, so that there may have been some difficulty for vampires to locate an adequate food supply. If this argument is correct, it should be even more difficult for the vampires specializing on avian blood to find food: both Diaemus and Diphylla have much lower body temperatures than Desmodus, the common, opportunistic species that attacks any available homoiotherm. The distribution of Desmodus also suggests that it faces a limited food supply. There are no vampires living in the West Indies, even though many tropical bats have spread to Jamaica, Cuba, Hispaniola, Puerto Rico, and the Bahamas. The absence of vampires seems correlated with the fact that the largest native mammals living on these islands are rodents of the family Capromyidae. Desmodus, however, was found on Cuba during the Pleistocene (Koopman, 1958), a time at which ground sloths were on Cuba. If the ground sloths supplied most of the food for the vampires, the extinction of the sloths may have eliminated vampires from the Antilles. Temperate insectivorous bats readily enter into a torpor having both obligatory and facultative elements. The resulting reduction in energy expenditure

260

BRIANK. McNAB

of these species is important in temperate climates due to the seasonal undependability of flying insects as a food supply. Yet, insects per se are not responsible for the restriction in energy intake, since some birds that feed heavily, if not exclusively, on insects are able to overwinter in cold climates. These birds eat insect adults, eggs and larvae that have taken refuge from a cold winter behind bark and in crevices. It is the flying nature of the insect food of bats that makes their food supply temporally unstable. Tropical insectivorous bats also have low rates of metabolism. Equally, tropical populations of insects have appreciable seasonal variations in abundance associated with the seasonal fluctuations in the amount of rainfall common to most lowland rain forests (Skutch, 1950; Janzen & Schoener, 1968). If the normal feeding pattern of a bat is interrupted, although only for a night or two, it must depend upon its stored reserves of energy, the size of which is usually proportional to the lean weight (except in special cases, such as in hibernators and migrators). A small weight combines a small energy reserve with a high rate of metabolism. Of two potential solutions for this dilemma, only one, a reduced rate of metabolism with the subsequent relaxation of a rigid homoiothermy, has been used in the tropics; the second, an increased store of energy, does not seem to be utilized, unless that is the explanation for the large fat deposits found in Rhinopoma, Taphozous and Hipposideros (Brosset, 1962a, b; Rosevear, 1965). From the above discussion it appears that the basal rates of metabolism are regulated at levels appropriate to the seasonal stability of the food supplies: if the food supplies are either periodically (flying insects) or chronically (blood) restricted, the bats utilizing these foods have low basal rates of metabolism and, consequently, marginal to poor temperature regulation. But if the food supplies are available at adequate levels throughout the year (like flowers, fruits and vertebrates), bats opt for precise endothermy, which requires high basal rates of metabolism. If this analysis is correct, food habits in a similar manner and pattern should affect energetically expensive functions other than homoiothermy, such as reproduction. For example, one would expect that reproduction would not occur during the periods of inadequate food supplies. Thus, insectivorous bats should have appreciably shorter breeding seasons than fruit, nectar or carnivorous bats. Vampires probably should be similar to fruit bats, since their energy restriction is non-periodic. Data on the reproduction of bats from Trinidad (Goodwin & Greenhall, 1961) and Venezuela (Pirlot, 1967) indicate that fruit-, nectar- and blood-eating bats have breeding seasons approximately twice as long as those for insectivorous species (Table 5). Furthermore, the lengths of the breeding seasons of birds from Trinidad (Snow & Snow, 1964) and Central America (Skutch, 1950) are nearly identical to those of bats of the same food habit (Table 5). It is of interest that the birds that feed on flying insects are also those that have given up a rigid homoiothermy (e.g. Bartholomew et al., 1957; Lasiewski & Thompson, 1966). (The temperature lability of humming-birds, however, is probably related to their small weight and the periodicity of their feeding schedules.)

ECONOMICS OF TEMPERATURE REGULATION I N NEOTROPICAL BATS TABLE

5--REPRODUCTION

IN

TROPICAL BATS AND

BIRDS

IN

RELATION TO FOOD HABITS

Length of reproductive season* Food habits and species

Localities

Mean

Trinidad**

Venezuela §

A. Batst Flying insects Saceopteryx bilineata Pteronotids Molossids

4/12 -5-6/12

1/2 2/6 --

Fruit Carollia perspicillata Nturnira lilium Uroderma bilobatum Vampyrops lineatus Artibeus jamaicensis A. lituratus

9/12 ---1O~12 11/12

8/10 9/10 9/11 8/9 ) 11 / 12

Nectar Glossophaga sorieina

8/12

11/11

12/12

6/10

Trinidad JI

Central America¶

6/12 4/12 6/12

--5/12

Blood Desmodus r otundus

B. Birds~ Flying insects Swifts Swallows Capromulgids

ca 5/12

9-10/12

10/12 ca 9/12

5/12

Fruit Oilbird Manacin

9/12 10/12

9-10/12 --

Nectar Humming-birds Bananaquit

10/12 9/12

12/12 10/12

10/12

* Months showing reproduction/months investigated. t Reproduction indicated in bats by either spermatogenesis or pregnancy; in birds indicated by nest and eggs. ++Goodwin & Greenhall (1961). § Pirlot (1967). II Snow & Snow (1964). ¶ Skutch (1950).

261

262

BRIAN K. MCNAB

It is clear that the type of thermoregulation in bats is determined by their ability to maintain the requisite rate of energy expenditure. For example, if a bat "decides" to be insectivorous, it will have a low basal rate of metabolism and, usually, a small weight; as a result, this bat will be a poor thermoregulator. To this extent, then, it can be said that the characteristics of thermal homeostasis in bats are fixed by the economies of a balanced energy budget. THE EVOLUTION OF HIBERNATION AND FACULTATIVE TORPOR Torpor and hibernation are characteristic of nearly all temperate bats, which has led many biologists to conclude that these states are typical of all bats (Hock, 1951; Twente & Twente, 1964). Some authors (Burbank & Young, 1934; Hock, 1951; Eisentraut, 1960; Kayser, 1961) have even argued that torpor is a "primitive" characteristic of bats. But, as has been shown in this paper, torpor is not typical of tropical bats. Furthermore, it is not clear what is meant by "primitive", if torpor and hibernation are in fact adaptations that permit a balanced energy budget during periods of a restricted income (Hanu~, 1959; Kulzer, 1965; Twente & Twente, 1964). Bats probably originated in the tropics from arboreal insectivores (Allen, 1939; Griffin, 1958), and from there spread into the adjacent subtropics and, finally, into the temperate regions. Twente & Twente (1964) have suggested that torpor originated in the tropics as an adaptation to the cool microclimates of roosting sites, especially caves. From the data presented in this paper, torpor more likely evolved in the tropics because of the ecologically imposed inability of certain species to expend energy at the rates required for precise temperature regulation. The facultative torpor and hibernation of temperate bats probably were derived from the torpor of tropical species. It is of interest then, to ask whether the invasion of a temperate climate depends upon the development of facultative torpor and hibernation. The taxonomic distribution of thermoregulation and torpor in bats is best seen by comparing body temperatures, since no data on rates of metabolism are available for most of the species studied in the Old World. The mean body temperature at an ambient temperature of 25°C is recorded for each species by family in Fig. 31. The families are grouped together by the scheme of Miller (1907), which is primarily based on the structure of the humeral-scapular joint, the Megachiroptera (group I) being the most similar in this joint to non-flying mammals and the Vespertilionoidea (group IV) being the most specialized for flight. Irrespective of familial affiliations the mean temperatures of all fruit-, nectarand meat-eating bats are between 34 and 39°C (the only exception being PhyUostomus discolor, whose peculiar case has been examined before); those of vampires fall between 31 and 35°C. Insectivorous bats have the greatest range in mean temperature (26-35°C), because of the facultative torpor typical of the Rhinolophidae, Vespertilionidae, and probably Mystacinidae (Dwyer, 1962);

263

E C O N O M I C S OF TEMPERATURE R E G U L A T I O N I N INEOTROPICAL BATS

these are the very families that reach their maximal diversity in the temperate zones and include all bats that are known to hibernate. At least two other families, Phyllostomidae and Molossidae, have marginally entered warm temperate areas, e.g. the deserts of south-western United States. The nectarivorous phyllostomids Leptonycteris and Choeronycteris do not enter torpor, but evade periods of inadequate food supplies by migrating to Mexico (Beatty, 1955). The insectivorous phyllostomid Mormoops also migrates to Mexico, although they occasionally winter in Texas (Raun & Baker, 1958); Mormoops probably does not go into a seasonal torpor, since it selects a warm

ix

L

uJ I--3o

( -

0 m

~."

'

o??

? °ol W

I<;

',,2

2" ~* .# ,,,.\.¢\,,...° ~.-°..o.,"# .,,/o.o~o,,.-'~e ,0o"¢ W

FIG. 31. Distribution of body temperature in bats by family when the ambient temperature is 25°C. Data from Table 2 and Kulzer (1965). Question marks suggest temperatures that may be found in families that have had no species studied. microclimate even in winter (Eads et al., 1957). Macrotus, another insectivorous phyllostomid, is a permanent resident over most of its range. It regulates Tb rather well for an insectivorous bat (Leitner & Ray, 1964; Fig. 4), but sometimes goes into torpor (Reeder & Cowles, 1951), especially for short periods in winter when there are noticeable fat deposits (Bradshaw, 1961). No members of Molossidae are known to enter hibernation: they either show daily torpor during adverse periods (Herreid, 1963c; Leitner, 1966) or migrate to the tropics for winter (Villa-R. & Cockrum, 1962). Finally, one may return to the confusing situation that exists in the genera Rhinopoma, Taphazous and Hipposideros. Northern populations of these bats in India store large amounts of fat in the fall and use them during the winter; populations in southern India do not store fat (Brosset 1962a, b). This is exactly what one would expect near the climatic boundary between temperate and tropical conditions (McNab, manuscript in preparation). Curiously, Brosset states that these bats are never found in deep torpor, but have " . . . cycles of extended

264

BRIAN K. MCNAB

rest, during which they live on their biological reserves and do not hunt". A clarification of the ecology and physiology of these bats obviously is needed, especially with regard to the fat deposits. Without doubt, then, the temperature regulation, energetics and behavior of temperate bats in concert are closely attuned to the availability of food in the environment. There is enough flexibility in this system so that no one solution, such as seasonal torpor, is required of all temperate bats. Alternative solutions include (1) the seasonal migration to hospitable climates and (2) short periods of light torpor in areas only occasionally subject to periods of cold weather. Cade's suggestion (1964) for rodents that torpor is mainly a reflection of a "primitive organization" is obviously not appropriate for bats. There is one correlation, however, that is hard to interpret from the viewpoint that energetics is closely attuned to conditions in the environment: tropical members of Rhinolophidae and Vespertilionidae, like their temperate relatives, show little temperature regulation (Kulzer, 1965; personal observations), unlike members of strictly tropical, insectivorous families. Similarly, the fish-eating bat, Pizonyx vivesi, a vespertilionid, does not appear to regulate its Tb when at rest (Carpenter, 1968), unlike Noctilio leporinus (Fig. 2). One explanation for "temperate energetics" in the tropics might be that there has not been adequate time for an appropriate adjustment to occur to the conditions in a tropical environment. The taxonomy and evolution of nycterbiid parasites of bats support the idea that vespertilionids invaded the New World tropics from the north temperate region (Guimar~es & D'Andretta, 1956). Most neotropical vespertilionids, however, are distinguished from temperate species only at the specific or subspecific levels. There are only two genera in this family that are unique to South America, one of which is Histiotus. It is of special significance, then, that quiescent H. velatus can maintain a greater AT (up to 19°C, Fig. 22) than reported for any other species of this family. It behaves like a member of a strictly tropical, insectivorous family, such as Rhinopomidae or Molossidae. Equally, the palaeotropical Miniopterus schreibersi seems to show more temperature independence of T~ than is typical of the cosmopolitan members of Vespertilioninae (Morrison, 1959; Shimoizumi, 1959; Dwyer, 1964). Furthermore, correlated with the conversion of an insectivorous diet in Myotis to the crustacean and fish diet of Pizonyx is an increase in the basal rate of metabolism to a relative level equal to that of N. leporinus (Carpenter, 1968). These data suggest that an appropriate modification in energetics (and thermoregulation) occurs in tropical bats of a temperate origin when there has been sufficient time (and opportunity) to do so, especially as demonstrated by a distinctive change in morphology. We know very little of the evolution of thermoregulation, or of any homeostatic function for that matter. But it is increasingly clear that the efficacy of homeostatic functions is mainly determined by the delicate interactions existing between an organism and its environment, only a small influence at best showing the impress of historical events. It may come to pass that the pathway of

ECONOMICS OF TEMPERATURE REGULATION IN NEOTROPICAL BATS

e v o l u t i o n o f h o m e o s t a s i s is m a i n l y r e c o r d e d in t h e e c o l o g i c a l l y d e t e r m i n e d efficacy is a c c o m p l i s h e d .

means

by which

265 the

Acknowledgements--I should like to thank the very many people in Mexico and Brazil, known and unknown, who gave me indispensable aid. In Mexico Professor Bernardo Villa-R. kindly provided laboratory space and Sr. W. Lopez-Forment aided me in the collecting of specimens. In Brazil special respects must be paid to Professor Paulo Sawaya, who as Director of the Departamento de Fisiologia Geral e Animal and the Instituto de Biologia Marinha, Universidade de S~o Paulo, made laboratory space available and was responsible for contacts that opened many Brazilian doors; Dr. L. Vizotto, Departamento de Zoologia, S~o Jos6 do Rio Preto provided laboratory space, and time and again assisted me in the field; Mr. A. Cohen, cultural attach6 at the American Council in Sao Paulo, who knew how to ship equipment across international boundaries; and Sr. and Sra. Jo~o Balas of S~o Paulo, who not only supplied transportation during my stay, but also made the domestic side of 15 months very pleasant. M y stay in Brazil accumulated many other debts, notably to Drs. M. Nilsson and W. Sugay of the Instituto Biologico (S~o Paulo), Sr. V. Taddei of Silo Jos6 do Rio Preto, Sr. and Sra. Mauricio Verdier of Fazenda Bodoquena, Dr. J. Pelligrino and St. Cello Valle of the Universidade de Minas Gerais, Dr. Colin Little of the University of Bristol (England), and the members of the Departamento de Fisiologia Geral e Animal, especially Drs. E. Mendes and J. Petersen. I should also like to thank Dr. K n u t Schmidt-Nielsen, Duke University, and Captain J. Faughn, University of California, San Diego, for their aid during my stay aboard the Alpha Helix. I want to record the constant encouragement and aid in the field given to me by my wife, Greta. Dr. R. Carpenter, San Diego State College, kindly sent me some of his data before its publication, Drs. F. Nordlie and Archie Carr, University of Florida, made helpful suggestions to improve this manuscript, and Mr. P. Laessle patiently drew the figures. This study was supported by a research grant from the National Science Foundation (GB-3477), a travel grant from the Penrose F u n d (4225) of the American Philosophical Society, and an invitation from the University of California, San Diego, to join the Alpha Helix in Amazonia. REFERENCES ALLEN G. M. (1939) Bats. Harvard University Press, Cambridge. ALVAREZ T. (1963) T h e recent mammals of Tamaulipas, Mexico. Univ. Kansas Publ. Mus. nat. Hist. 14, 363-473. BAKER H. G. (1963) Evolutionary mechanisms in pollination biology. Science 139, 877-883. BAKER J. R. & BAKER Z. (1936) T h e seasons in a tropical rain-forest (New Hebrides)--3. Fruit-bats (Pteropidae). ft. Linn. Soc. (Zool.) 40, 123-141. BARTHOLOMEW G. A., HOWELL T . R. • CADET. J. (1957) T o r p i d i t y in t h e w h i t e - t h r o a t e d

swift, anna hummingbird, and poor-will. Condor 59, 145-155. BARTHOLOMEW G . A., LEITNER P. ~¢. NELSON J. E. (1964) Body t e m p e r a t u r e , oxygen c o n s u m p t i o n , and heart rate in three species of Australian flying foxes. Physiol. Zool. 37,

179-198. BEATTY L. D. (1955) Autecology of the longnose bat, Leptonycteris nivalis (Saussure). M.S. Thesis, University of Arizona, unpublished. BLOEDEL P. (1955) Hunting methods of fish-eating bats, particularly Noctilio leporinus. ft. Mammal. 36, 390-399. BRADSHAW G. VAN R. (1961) A life history study of the California leaf-nosed bat, Macrotus californicus. Ph.D. Thesis, University of Arizona, unpublished. BEOSSET A. (1961) L'hibemation chez les chiropt~res tropicaux. Mammalia 25, 413-452. BROSSET A. (1962a) T h e bats of central and western India. Part 1. )t. Bombay Nat. Hist. Soc. 59, 1-57.

266

B m m K. M c N ~

BROSSET A. (1962b) T h e bats of central and western India. Part 2. ~. Bombay Nat. Hist. Soc. 59, 583-524. BROSSET A. & DEBOUTTEVILLE C. D. (1966) Le r6gime alimentaire du Vespertilion de Daubenton Myotis daubentoni. Mammalia 30, 247-251. BURBANK R. C. & YOUNG J. Z. (1934) Temperature changes and winter sleep of bats. .~. Physiol. 82, 459-467. CADE W. J. (1964) The evolution of torpidity in rodents. Ann. Acad. Sei. fennicae 71, 79112. CARPENTER R. (1968) Salt and water metabolism in the marine fish-eating bat, Pizonyx vivesi. Comp. Biochem. Physiol. 24, 951-964. CARPENTER R. &. GRAHAMJ. B. (1957) Physiological responses to temperature in the longnosed bat, Leptonycteris sanborni. Comp. Biochem. Physiol. 22, 709-722. COCKRUM E. L. (1960) The Recent Mammals of Arizona: their Taxonomy and Distribution. University of Arizona Press, Tucson. COCKRUM E. L. & HAYWARDB. (1962) Hummingbird bats. Nat. Hist. 71, 38-43. D w ~ R P. D. (1962) Studies on the two New Zealand bats. Zool. Public. Victoria Univ. Wellington No. 28, 1-28. D W ~ R P. D. (1964) Seasonal changes in activity and weight of Miniopterus sehreibersi blepotis (Chiroptera) in north-eastern New South Wales. Aust. ~. Zool. 12, 52-69. EADS R. B., WISEMAN J. S. & MENZIES G. C. (1957) Observations concerning the Mexican free-tail bat, Tadarida mexicana, in Texas. Tex. J. Sci. 9, 227-242. EISENTRAUT M. (1960) Heat regulation in primitive mammals and in tropical species. Bull. Mus. comp. Zool. 124, 31-43. GOODWIN G. G. • GREENHALLA. M. (1961) A review of the bats of Trinidad and Tobago. Bull. Am. Mus. nat. Hist. 122, 187-302. GI~II~FIND. R. (1958) Listening in the Dark. Yale University Press, New Haven. GUDGER E. W. (1945) Fisherman bats of the Caribbean region. J . Mammal. 26, 1-15. GUIMAR:~ES L. R. & D'ANDRETTA M. A. V. (1956) Sinopse dos Nyceribiidae (Diptera) do Novo Mundo. Arq. Zool. Est. S~o Paulo 9, 1-184. HALL E. R. & DALQUESTW. W. (1963) T h e mammals of Veracruz. Univ. Kansas Publ. Mus. nat. Hist. 14, 167-352. HALL ]. S. (1962) A life history and taxonomic study of the Indiana bat, Myotis sodalis. Reading Publ. Mus. and Art Gallery, Sci. Publ. 12, 1-68. HANU~ K. (1959) Body temperatures and metabolism in bats at different environmental temperatures. Physiol. Bohemoslov. 8, 250-259. HERREID C. F., I I (1963a) Metabolism of the Mexican free-tailed bat. J . Cell. comp. Physiol. 61, 201-207. HERREID C. F., II (1963b) Temperature regulation and metabolism of Mexican free-tailed bats. Science 142, 1573-1574. HERREID C. F., II (1963c) Survival of a migratory bat at different temperatures, jT. Mammal. 44, 431-433. HEm~EID C. F., I I & I~SSEL B. (1967) Thermal conductance in birds and mammals. Comp. Biochem. Physiol. 21, 405-414. HOCK R. J. (1951) The metabolic rates and body temperatures of bats. Biol. Bull. 101, 289-299. HUDSON J. W. (1965) Temperature regulation and torpidity in the pigmy mouse, Baiomys taylori. Physiol. Zool. 38, 243-254. HussoN A. M. (1962) The bats of Suriname. Zool. Verb. No. 58, 1-282. IRVING L. (1956) Physiological insulation of swine as bare-skinned mammals. ~7. appl. Physiol. 9, 414-420. IaVING L. & HART ]. S. (1957) T h e metabolism and insulation of seals as bare-skinned mammals in cold water. Can.~7. Zool. 35, 497-511. JACKSON H. H. T. (1961) Mammals of Wisconsin. University of Wisconsin Press, Madison.

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267

JANZEND. H. (1967) Synchronization of sexual reproduction of trees within the dry season in Central America. Evolution 21, 620--637. JANZEN D. H. & SCHOENERT. W. (1968) Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season. Ecology 49, 96-110. KAYSERC. (1961) The Physiology of Natural Hibernation. Pergamon Press, New York. KLEIRERM. (1960) The Fire of Life. John Wiley, New York. KOOPMANK. F. (1958) A fossil vampire bat from Cuba. Breviora 90, 1--4. KOOPMANK. F. & MARTINP. S. (1959) Subfossil mammals from the G6mez Farlas region and the tropical gradient of eastern Mexico. J. Mammal. 40, 1-12. KULZER E. (1963) Temperaturregulation bei Flughunden der Gattung Rousettus Gray. Z. vergl. Physiol. 46, 595--618. KULZER E. (1965) Temperaturregulation bei Fledermiiusen (Chiroptera) aus verschiedenen Klimazonen. Z. vergl. Physiol. 50, 1-34. LASIEWSKIR. C. & TI~OMPSONH. J. (1966) Field observation of torpidity in the violet-green swallow. Condor 68, 102-103. LEITNER P. (1966) Body temperature, oxygen consumption, heart rate and shivering in the California mastiff bat, Eumops perotis. Comp. Biochem. Physiol. 19, 431 443. LEITNER P. & NELSONJ. E. (1967) Body temperature, oxygen consumption and heart rate in the Australian false vampire bat, Macroderma gigas. Comp. Biochem. Physiol. 21, 65-74. LEITNER P. & RAY S. P. (1964) Body temperature regulation of the California leaf-nosed bat, Macrotus californicus. Am. Zool. 4, 295. LICVlTP. & LEITNERP. (1967) Physiological responses to high environmental temperatures in three species of microehiropteran bats. Comp. Biochem. Physiol. 22, 371-387. LYMAN C. P. & WIMSATTW. A. (1966) Temperature regulation in the vampire bat, Desmodus rotundus. Physiol. Zool. 39, 101-109. McNAB B. K. (1966) The metabolism of fossorial rodents: a study of convergence. Ecology 47, 712-733. M c N ~ B. K. (1970a) Body weight, Bergmarm's rule and the energetics of temperature regulation. (In press.) MCNAB B. K. (1970b) The structure of tropical bat faunas. (In press.) McNAB B. K. (1970c) The energeties of vampires. (In preparation.) MEISNAR J. & JANSK'2 L. (1967) Seasonal changes of temperature regulation in the bat Myotis myotis Borkh. Physiol. Bohemoslov. 16, 147-152. MILLER G. S., JR. (1907) The families and genera of bats. Bull U.S. Nat. Mus. No. 57, 1-282. MORRISON P. R. (1959) Body temperatures in some Australian mammals--I. Chiroptera. Biol. Bull. 116, 484--497. MORI~ISONP. R. & McNAB B. K. (1967) Temperature regulation in some Brazilian phyllostomid bats. Comp. Biochem. Physiol. 21, 207-221. MORRISON P. R., RYSER F. A. & DAWE A. R. (1959) Studies on the physiology of the masked shrew, Sorex cinereus. Physiol. Zool. 32, 256-271. PEARSONO. P. (1960) The oxygen consumption and bioenergetics of harvest mice. Physiol. Zool. 33, 152-160. PIJL L. VANDER (1957) The dispersal of plants by bats. Acta bot. neerl. 6, 291-315. PIJL L. VAN DER (1961) Ecological aspects of flower evolution--II. Zoophilous flower classes. Evolution 15, 44-59. PIRLOT P. (1967) P~riodicit6 de la reproduction chez les chiropt6res n~o-tropicaux. Mammalia 31,361-366. RAUN G. G. & BAKERJ. K. (1958) Some observations on Texas cave bats. Southwestern Nat. 3, 102-106.

268

Bm~

K. MCNAB

REEDER W. G. & COWLES R. B. (1951) Aspects of thermoregulation in bats. J. Mammal. 32, 389--403. I~EDER W. G. & NORalS K. S. (1954) Distribution, type locality, and habits of the fisheating bat, Pizonyx vivesi. J. Mammal. 35, 81-87. RICHAaDS P. W. (1957) The Tropical Rain Forest. University Press, Cambridge. ROSEVEAR D. R. (1965) The Bats of West Africa. Natural History Museum, London. SCHMIoT-NIELSEN K., DAWSON T. J. & CaAWFORDE. C., Ja. (1966) Temperature regulation in the Echidna (Tachyglossus aculeatus). J. cell. Physiol. 67, 63-72. SCHOLANDER P. F., WALTEaS V., HOCK R. & IaVlN~ L. (1950) Body insulation of some arctic and tropical mammals and birds. Biol. Bull. mar. biol. Lab., Woods Hole 99, 225-236. SmMOIZUMI J. (1959) Studies of the hibernation of bats (1). Sci. Reports T.K.D. Sect. B 9, 1-36. SKUTCH A. F. (1950) T h e nesting seasons of Central American birds in relation to climate and food supply. Ibis 92, 185-222. SNOW D. W. (1965) A possible selective factor in the evolution of fruiting seasons in tropical forest. Oikos 15, 274-281. SNOW D. W. & SNOW B. K. (1964) Breeding seasons and annual cycles of Trinidad landbirds. Zoologica 49, 1-39. STONES R. C. & WIEBERS J. E. (1965) A review of temperature regulation in bats (Chiroptera). Am. Midl. Nat. 74, 155-167. TaOUGHTON E. (1947) Furred Animals of Australia. Charles Scribner's Sons, New York. Tucm~a V. (1965) Oxygen consumption, thermal conductance, and torpor in the California pocket mouse, Perognathus californicus, ft. cell. comp. Physiol. 65, 393-404. TWENTE J. W. (1955) Some aspects of habitat selection and other behavior of caverndwelling bats. Ecology 36, 706-732. TWENTE J. W. & TWENTE J. A. (1964) An hypothesis concerning the evolution of heterothermy in bats. Ann. Acad. Sci. fennicae 71, 435-442. VILLA-R. B. (1966) Los murcidlagos de Mdxico. Instit. Biol., Univ. Nat. Aut. M~x., Mexico City. VILLA-R. B. & COCKRtrM E. L. (1962) Migration in the guano bat Tadarida brasiliensis mexicana (Saussure). 37. Mammal. 43, 43-64. WIMSATT W. A. (1962) Responses of captive common vampires to cold and warm environments, ft. Mammal. 43, 185-191.

Key Word Index--Bats; temperature regulation; thermal conductance; basal rate of metabolism; body temperature; oxygen consumption; torpor; facultative torpor; obligatory torpor; evolution of torpor; energetics ; energetics of temperature regulation; effect of food habits on temperature regulation; peripheral cooling; shell temperature; core temperature; hibernation; clustering; vampires; tropical bats; temperate bats.