Camp. Biochcm. Physiol., 1971, Vol. 4OA, pp. 809 to 813. Pergamon Press. Printed in Great Britain

FLUCTUATIONS IN THE PREOPTIC-ANTERIOR HYPOTHALAMIC TEMPERATURE IN THE BAT,

EPTESICUS FUSCUS*

MATTHEW JAY KLUGERT’ and JAMES EDWARD HEATH2

l Department of Zoology, University of Illinois, Urbana, Illinois 61801 and p Department of Physiology and Biophysics, University of Illinois, Urbana, Illinois 61801

(Received 20 March 1971)

Abstract -1. Bats that are internally heat-loaded vasodilate peripherally. 2. When the preoptic-anterior hypothalamus (PO/AH) of Eptesicus fuscus is

heated, only a slight rise in wing temperature occurs along with a small increase in body temperature.

3. Conversely, cooling the PO/AH leads to a slight fall in wing temperature. 4. Furthermore, lesions in the PO/AH fail to abolish thermoregulatory

responses. 5. It is suggested, and determined experimentally, that the PO/AH of E.

fuscus, an open-mouthed flyer, fluctuates in temperature during simulated flight. 6. This fluctuation in the PO/AH is, perhaps, the primary reason for the

decline in importance of the PO/AH as the primary thermal sensor and integrator in E. fuscus.

7. Other open-mouthed flyers are also thermolabile. 8. It is possible that the loss of the PO/AH as a thermally stable area preadapts

these organisms for heterothermy.

INTRODUCTION

THE PREOPTIC-ANTERIOR hypothalamus (PO/AH) of the bat Eptesicus fuscus is less thermally sensitive than the PO/AH in other vertebrates studied. Rectal heating, leading to an elevated body temperature, causes peripheral vasodilation in E. fusm (Kluger & Heath, 1970). This response to internal heat loading is qualitatively measured by observing changes in wing temperature. At an ambient temperature of 30 + 2”C, rectal heating led to an average increase in wing temperature of 4.0X (Kluger & Heath, 1971b). This response is initiated by the stimulation of internal thermal receptors, probably central nervous, and undoubtedly serves as an im- portant thermoregulatory mechanism in bats (Kluger, 1969; Kluger & Heath, 1970). Heating the PO/AH of a normothermic (not heat stressed) bat at 30 it 2°C ambient temperature led to an average increase in body temperature of 0.6”C and in wing temperature of only O%‘C (Kluger & Heath, 1971b). Conversely, cooling the PO/AH of a normothermic bat led to an average decrease in body temperature of -0.4”C and in wing temperature of -O+VC (Kluger & Heath, 1971b).

Furthermore, electrolytically produced lesions in the PO/AH led to little deficit in thermoregulation (Kluger & Heath, 1971a). For example, vasodilation

* This work was supported, in part, by N.S.F. GB 6303 and GB 13797. t Present address: John B. Pierce Foundation Laboratory, 290 Congress Avenue, New

Haven, Connecticut 06519.

810 MATTHEW JAY KLUCER AND JAMES EDWARD HEATH

still occurred when the bats were rectally heated, although the threshold for initiation of this response was raised slightly. That is, vasodilation in the PO/AH- lesioned group occurred at a body temperature of Oa9”C higher than in the controls. Also, the PO/AH-lesioned bats still entered and aroused from hibernation, although

arousal occurred more slowly than in the controls. And, at high ambient tempera- tures, the PO/AH-lesioned bats salivated, urinated and licked themselves at appropriate ambient temperatures, and consumed oxygen at about the same rate as did the controls. It has been suggested that temperature sensitivity and inte-

gration in E. fuscus is probably located at other central nervous sites (Kluger & Heath, 1971a).

This paper is an attempt to determine why the PO/AH of E. fuscus is not the primary thermal sensor and integrator as in other mammals. During flight, most echolocating bat species navigate with their mouths open in order to emit the ultrasonic pulses. Also, the insect-hawking method of food procurement in many bat species (including E. fxwus) necessitates open-mouthed flying. Open-mouthed flying should cause a stream of air to pass over the moist tissues of the oral cavity.

At a normal flight speed of 13-39 km/hr (Patterson & Hardin, 1969) considerable convective and evaporative cooling of the oral and surrounding tissues undoubtedly occurs. If as the result of open-mouthed flying, the temperature of the PO/AH becomes more variable than deep body temperature, then its value as a thermal

receptor and integrator becomes greatly diminished.

MATERIALS AND METHODS

Four big brown bats, E. fuscus, were used in this experiment. Procurement and care of these animals is described elsewhere (Kluger & Heath, 1970).

Deep body (rectal), PO/AH and ambient temperature were monitored using 40-gauge copper-constantan thermocouples attached to a Honeywell recording potentiometer, and calibrated to within 0.1 “C. PO/AH temperature was measured by chronically implanting a hollow metal tube (0.8 mm dia.) 2 mm below the cranial surface, directly over the PO/AH. This tube was attached to the roof of the skull with dental cement. A thermocouple was then lowered 4.5 mm below the surface of the cranium and tightly sealed in place with a polyethylene cap. Histological examinations were performed on three of the bats, con- firming the location of the thermocouple tip near the ventral surface of the forebrain, close to, or in, the PO/AH.

Each bat was placed in a restraining cage (Kluger & Heath, 1970), and PO/AH, rectal and ambient temperature were continuously monitored. The restraining cage with the bat in it was then placed in a wind tunnel facing an airstream of 18.3 km/hr laminar wind flow, when activated. This wind speed simulates a slow flight in this species (see Patterson & Hardin, 1969). The maximum difference between the rectal and PO/AH temperature was then recorded for each bat when (a) the wind tunnel was off, (b) the wind tunnel was turned on, but the bat’s mouth not held open and (c) the wind tunnel was turned on, and the bat’s mouth was held open with a slender stick placed in the angles of the jaw.

RESULTS

In the still air, the maximum difference between rectal and PO/AH temperature varied from O-7 to 1*6”C, with a mean of 1*2”C. When the wind tunnel was turned on, and the mouth of the bat not held open, this maximum difference varied from

FORERRAIN TEMPERATURE IN A BAT

Wind on.

I mouth not held We”

811

31

30

v 0

f 29

2 ? P __

261 I I 1 I I I ‘5 10 15 20 25 30

Time, min

Pro. 1. Graph illustrating the difference between rectal and preoptic-anterior hypothalamic (PO/AH) temperature in the bat E, fuscus (no. 1). When the wind from the wind tunnel was turned on, and the mouth not held open, the maximum difference between rectal and PO/AH temperature was 1.2%. However, when the wind was turned on, and the mouth of the bat held open (simulating flight), the

maximum difference increased to 2-4°C.

wind G” mouth opal

Fm 2, Ranges of maximum difference in body minus preoptic-anterior hypo- thalamic (PO/AH) temperature in B. fusnrs. In still air, the maximum difference between PO/AI-f and rectal temperature in four bats varied between O-7-14”C, with a 1.2% mean. When the wind was turned on, this difference w&s 0*6-1*9X!, with a 14°C mean. However, when the wind tunnel was turned on, and the mouth of the bat was held open, this maximum difference between rectal and PO/AH

temperature varied from l-9 to 2~7°C~ with a 2*3”G mean.

812 NLTTHEWJAY KLUCER AND JAMES EDWARD HEATH

0.6 to 1*9”C with a mean of l*l”C, not statistically different (P>O*OS, Student’s t test) from the previous value. However, when the wind tunnel was turned on, and the mouth of the bat held open, the maximum difference between rectal and PO/AH temperature varied from 1.9 to 2*7”C with a 2*3”C mean, significantly different (I’< O*OS) f rom the two previous mean vaiues (Figs. 1 and 2).

DISCUSSION

During flight, large quantities of internal heat must be dissipated by bats. Peripheral vasodilation in response to internal heat loading (rectal heating) provides one important outlet for excess heat (Kluger & Heath, 1970). Evaporative and convective heat loss from the oral cavity provides another source of heat dissipation. Both of these avenues of heat loss have arisen as the result of preadaptation ; the former for flight, and the latter for echolocation and insect “hawking”. As the bat flies, the PO/AH is cooled. This fluctuation in the PO/AH is, perhaps, the primary reason for the decline in importance of the PO/AH as the thermal sensor and integrator in E. fusczls.

Heterothermy in bats and other small vertebrates is generally believed to have evolved as an adaptive mechanism to conserve energy (Pearson, 1948). Hetero- thermy in bats is confined primarily to those species feeding on flying insects (McNab, 1969), although torpor in some neotropical fruit and nectar eating bats has more recently been reported (Studier & Wilson, 1970). McNab (1969) suggests that the seasonal undependability of flying insects as a food source has led to widespread heterothermy in insectivorous bats, and notes that in birds, those “that feed on flying insects are also those that have given up rigid homiothermy” (Bartholomew et al., 1957; Lasiewski & Thompson, 1966). Undoubtedly, energetic requirements did provide an important selective pressure towards heterothermy in small homiotherms. However, possibly contributing to the selective advantage of energy conservation in insectivorous bats was the loss of the generally thermally stable PO/AH for use as the primary thermal sensor and integrator. Comple- mentary evidence comes from studies on heterothermy in birds, since of all the insectivorous birds, it is only the open-mouthed flyers, or their descendants, which tend to be thermolabile. For example, the swifts, Apus apus and Aeronautes salratis (Koskimies, 1948; Bartholomew et al., 1957), poorwill, Pha~eae~opt~~~s nuttallii and nighthawk, C~~~e~~es ~c~t~penn~s (Jaegar, 1948; Marshall, 1955) and swallow, Tachycineta thalassina (Lasiewski & Thompson, 1966) are all known to enter torpor. Also hummingbirds, thought to have evolved from insectivorous swift-like ancestors (Wagner, 1946), hibernate (Pearson, 1950). This evidence suggests that a study of central control of thermoregulation in these heterotherms and other open-moused flyers should reveal a dearth of thermal receptors and integrators in the PO/AH similar to that found in E. fuscw, resulting in a pre- adaptation for heterothermy.

REFERENCES BARTHOLOMEW G. A., HOWELL 'I'. R.& CADE T. J.(1957)Torpidityin the white-throated

swift, anna hummingbird and poor-will. Condor 59, 145-155.

FOREBRAIN TBMPEBATIJBB IN A BAT 813

JABGAB E. C. (1948) Does the poorwill hibernate ? Condor 50,45-46. KLUGER M. J. (1969) Fluctuations in the wing temperature of the bat in response to internal

heat loading. Am. Zool. 9, 591. KLUGER M. J. & HEATH J. E. (1970) Vasomotion in the bat wing: a thermoregulatory res-

ponse to internal heating. Camp. Biochem. Physiol. 32, 219-226. KLUGER M. J. & HEATH J. E. (1971a) The effect of preoptic-anterior hypothalamic lesions

on thermoregulation in the bat. Am. J. Physiol. 221, 144-149 KLUGER M. J. & HEATH J. E. (1971b) Thermoregulatory responses to preoptic-anterior

hypothalamic heating and cooling in the bat. (Submitted to Z. vergl. Physiol.) KOSKIMIE~ J. (1948) On temperature regulation and metabolism in the swift, Micropus a.

apus, during fasting. Expwientia 4, 274276. LA~IEWSKI R. C. & THOMPSON H. J. (1966) Field observation of torpidity in the violet-green

swallow. Condor 68, 102-103. MCNAB B. K. (1969) The economics of temperature regulation in neotropical bats. Camp.

Biochem. Physiol. 31, 227-268. MARSHALL J. T., JR. (1955) Hibernation in captive goatsuckers. Condor 57, 129-134. PAT~BR~ON A. P. & HARDIN J. W. (1969) Flight speeds of five species of vespertilionid bats.

J. Mamm. 50, 152-153. PEAB~ON 0. P. (1948) Metabolism of small mammals with remarks on the lower limit of

mammalian size. Science, N. Y. 108, 44. PBABsON 0. P. (1950) The metabolism of hummingbirds. Condor 52, 145-152. STUDIER E. H. & WILSON D. E. (1970) Thermoregulation in some neotropical bats. Corn@.

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Key Word bdex-Preoptic-anterior hypothalamus; thermoregulation; heterothermy; Eptesicus fuscus.

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