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Thermoregulatory responses of the pigeon (Columba livia) to selective changes in the inspired air temperature. C. Bech*, W. Rautenberg, and B. May- ...
J Comp Physiol B (I988) 157:747-752

Journal of

Comparative

Systemic, Biochemical, and Environ-

Physiology B Physiology mental

9 Springer-Verlag 1988

Thermoregulatory responses of the pigeon (Columba livia) to selective changes in the inspired air temperature C. Bech*, W. Rautenberg, and B. May-Rautenberg Ruhr-Universit~it Bochum, Falkult/it ffir Biologie, A.G. Temperaturregulation, D-4630 Bochum, Federal Republic of Germany Accepted August 7, 1987

Summary. 1. Metabolic rate (MR) and body and skin temperatures were measured in pigeons at ambient temperatures of 5 ~ and 25 ~ The pigeons were equipped with a mask covering the head, allowing us to change selectively the temperature of the inspired air. 2. Increasing Tinsp at T, of 5 ~ significantly decreased the metabolic rate. At a T~ of 25 ~ lowering T~nspcaused a significant increase in MR, whereas only a slight and insignificant decrease in MR followed a rise in the Tinsp. 3. Beak temperature changed in parallel to the changes in the temperature of the inspired air. 4. It is concluded that there must be peripheral thermoreceptors in the head region, detecting the ambient (inspired) air temperature, and which are important for the initiation of thermoregulatory effector mechanisms. 5. The thermosensitivity of the whole head of pigeons (based on changes in brain temperature) is -1.73 to -3.11 W kg 4 ~ ]. A calculation based on changes in beak skin temperature only gives a thermal sensitivity of the beak of-0.26 to -0.30 W kg oC

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Introduction

Accurate regulation of the internal body temperature in homeothermic animals depends on thermal inputs from thermoreceptors located both within and outside the CNS. In birds, thermoreceptors have been demonstrated in the hypothalamus, Abbreviations: MR metabolic rate; Td ambient temperature;

Tinsp temperature of inspired air; Tvc temperature of the vertebral canal; H P heat production *To whom offprint requests should be sent at the following address: Department of Zoology, University of Trondheim, N-7055 Dragvoll, Norway

the spinal cord, the body core and the skin (Rautenberg etal. 1972; Necker 1977; SimonOppermann etal. 1978; Helfmann etal. 1981; Inomoto and Simon 1981; Mercer and Simon 1984). Birds differ in some respects from mammals regarding the relative importance of the different thermoreceptors in eliciting proper thermoregulatory responses. Whereas the rostral brain stem seems to be a very important thermoreceptive area in mammals (Hammel 1968; Simon 1981; Mercer and Simon 1984), thermal stimulation of the corresponding areas in birds yields only weak, or nonspecific, responses (Mills and Heath 1972; Rautenberg et el. 1972; Simon et el. 1976; Simon-Oppermann et el. 1978; Martin et el. 1981). The spinal cord, on the other hand, has assumed the primary role in the thermoregulatory system of birds, and thermal stimulation there elicits proper thermoregulatory responses (Rautenberg 1969; Rautenberg et el. 1972; Inomoto and Simon 1981; Bech et el. 1982). The influence of thermal input signals from the peripheral areas of the body has been less well studied in birds. Although thermoreceptors in the head have been described, a specific thermoregulatory significance of these receptors has seldom been postulated. In most previous bird studies involving thermal stimulation of the brain, this has been done by invasive techniques, using water-perfused steel tubes inserted into the brain. Although the same technique has been used in mammalian studies, the possibility that the tubes themselves may influence the responses obtained cannot be entirely ruled out. Helfmann etal. (1981) were able to selectively cool the entire head region of geese by using extravascular heat-exchangers. They demonstrated that at least some thermodetection occurred in that part of the body, although no exact location of the receptors involved could be given. Thus, much uncertainity still surrounds the potential importance

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of the thermoreceptors located in the head region of birds. In the present paper we report a study designed to investigate the possibility that genuine thermosensitivity exists in the head of the pigeon, using a non-invasive technique. We studied the effect on certain thermoregulatory variables induced by experimentally heating or cooling the inspired air, thereby selectively altering the temperature of the head.

C. Bech et al.: Yhermosensitivity in pigeons

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Animal preparation. Twelve pigeons (Co[umba livia), with a mean body weight of 428 g (range 330 to 483 g), were used in the experiments, after being acclimatised to an ambient temperature of ca. 25 ~ for at least two weeks. A short segment (2.5-3.5 cm) of nylon tubing (Portex 00) was implanted extradurally, under halothane anesthesia, to serve as a guide for the copper-constantan thermocouple (Finewire, California, type 0.005) used to measure the temperature of the vertebral canal (Tvc). In 3 of the pigeons, a 7.5 cm thermode was in addition implanted extradurally as described by Rautenberg et al. (1972). The thermodes were constructed from Portex 00 tubes bent into a hair-pin shape. Perfusion of these tubes with water from a thermostatically-controlled water-bath enabled us to keep the vertebral temperature at a constant, selected level. A small nylon tube (Portex 00), closed at one end, was also inserted into the brain of each of these same pigeons. During the experiments, a thermocouple was inserted into this tube to measure the brain temperature (Tbrain). Subsequent necropsy revealed that the tube end had been situated within 1.5 m m of the hypothalamUS.

Before each experiment a thermocouple was inserted into the colon to measure the colonic temperature (Tcolon), and thermocouples taped to the skin of the breast, back, beak and foot were used for measuring the respective skin temperatures. A head mask was constructed by attaching a hemispherical, clear plastic helmet (diameter 40 mm) to a plastic disc (diameter 45 mm) providing a tight seal to the upper part of the neck by means of a rubber collar. In this way a small airtight chamber was made that covered only the bird's head. Inlet and outlet tubes enabled us to pump air through this head chamber to measure the oxygen consumption. Each bird was placed in a 7 1 brass chamber in which the ambient temperature could be thermostatically regulated by the temperature of the water perfusing the chamber walls. Dry air was pumped into the mask covering the bird's head (air inflow at the front end). By means of rotary valves, the air either entered the mask directly (thus having the same temperature as that in the body chamber) or it first passed through tubes immersed in a box containing dry ice, thereby being precooled, or it first passed through tubes immersed in a 60 ~ water-bath, thereby being prewarmed. Thermocouples were placed in the head mask beside the inlet tube and in the body chamber to measure the temperature of the inspired air (Tinsp) and ambient temperature (Ta), respectively. Measurements. All the temperatures measured were recorded on a Phillips multipoint recorder (Type PM 8235), which also recorded the rate of air flow through the mask. The flow was maintained at rates between 3 and 41 m i w 1. An aliquot of the air flow was diverted to pass through a Servomex oxygen analyser (Type OA 540), the output of which was also recorded

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4 Fig. 1. Effects on the heat production of pigeons of changes in the temperature of the inspired air. Open bars represent controt values recorded before the stimulation periods while the hatched bars represent the mean values (4- 1 SD) recorded during the last 12 min of the stimulation periods, n number of experiments

on the multipoint recorder. Oxygen consumption was calculated from the recorded flow and the oxygen concentration in the effluent air, using appropriate formulas (Withers 1977). Heat production (HP) was calculated from the measured oxygen consumption using 1 ml 02 (STPD) g I h ~equal to 5.582 W kg I, which is assuming a respiratory exchange ratio of 0.8. Experimentalprotocol. Three different types of experiments were made: 1.5 ~ C warming. The birds were initially held at rest at an ambient temperature of 5 ~C, which was also the temperature maintained in the head mask (Tin@, for at least an hour before the experiments began. The temperature of the air flowing through the mask was then raised to a mean value of 24.5 ~ (SD = 6 . 9 ~ n = I1) for 30 rain. 2.25 ~ C cooling. A one hour rest period with the Ta and the Tinsp both kept at 25 ~C. Tinsp was then lowered to a mean value of 8.7 ~ (SD = 5.6 ~ n = 21) for 30 rain. 3.25 ~ C warming. A one hour rest period with the Ta and the Tinsp both kept at 25 ~C. Tinsp was then raised to a mean value of 41.4 ~ (SD = 3.1 ~ n = 13) for 30 rain. The experiments in which the three pigeons that had been fitted with spinal thermodes were involved, were first run according to one of the three aforementioned schemes. In a further experiment, carried out immediately afterwards, the spinal tubes were perfused with warm water whereby the temperature of the vertebral canal was kept stable during the 30 rain stimulation period. Evaluation and statistics. The mean value for the last 12 rain before the stimulation period and for the last 12 rain of the half hour stimulation period were used in the evaluation of the changes in the measured parameters by the Wilcoxon MatchedPairs Signed-rank test (Siegel 1956), with a significance-level of 0.05. The reason, that only the last part of the stimulation period is used in the evaluations, is that we often observed 'artificial' sharp increases in metabolic rate, probably caused by exitement, at the beginning of the 30 min stimulation period. In experiments, where this was not the case, metabolic rate increased immediately after change of inspired air temperature, reaching a steady level within 2 4 rain.

C. Bech et al.: Thermosensitivity in pigeons

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Results

Figure 1 summarizes the effects on heat production of the experimental alterations in the temperature of the inspired air. At T.d = 5 ~ C, a rise of Tins led to a significant decrease in heat production ~rom 11.63W k g 1 to 9 . 9 5 W kgl. At a T a of 25 oc, lowering of the ~insp led to a significant increase in H P from 6.20 W kg 1 to 8.03 W kg I, whereas a rise

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C. Bech et al.: Thermosensitivity in pigeons 41 o

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Inspired air t-emperat-ure (%)

Fig. 4. Brain temperature plotted in relation to the temperature of the inspired air at two different ambient temperatures (5 ~C and 25 ~

To investigate whether the observed changes in spinal cord temperature could, in turn, have induced the change in heat production, we made some further experiments, in which we kept the spinal cord temperature constant. Fig. 3 shows the results of these experiments. It can be seen that keeping the spinal cord temperature constant had only a limited effect on HP. The induced changes in HP, however, were somewhat reduced in all three series of experiments, although they were insignificant in all cases. Brain temperature turned out to depend on the temperature of the inspired air as well as on Z~. Fig. 4 shows the relationship between Tinsp and Tbrai n at the two different ambient temperatures (5 and 25 o C) used in the experiments. Discussion

The changes in heat production prompt the following question: which thermoreceptors are involved in eliciting the observed changes in heat production? The temperature changes inducing the alteration in thermal input could either have been perceived immediately by peripheral sensors in the pigeon's head, as a direct consequence of the alteration in the temperature of the inspired air, or by the secondary changes in temperature which occur internally in the pigeon's body. Temperature changes in both the spinal cord and deep body were general, although the Tcolon only changed to a small extent and was significant different in only one of the series of experiments. Thus, changes in deep body temperature are not very likely involved in mediating the subsequent changes in HP. The spinal thermosensitvity of pigeons is approximately-1.0 W k g ' ~ -1 (Graf 1980; Mercer and Simon 1984). The increase in the spinal tern-

perature (0.34 ~C) that occurred after the ~insp was raised at a T~ of 25 o C, should thus have induced a decrease in heat production of 0.34 W kg 1, a value which corresponds remarkably well to the recorded decrease of 0.31 W k g I (Fig. 1). However, too much emphasis should not be laid on this apparent similarity, since the observed mean change in HP was not statistically significant. Lowering the rinsp at a T a of 25 ~C was followed by a significant decrease in the Tw of 0.2 ~C, which should have led to an increase in HP of 0.2 W k g 1. However, we found in fact that a much greater increase in HP occurred, of 1.83 W kg 1 (Fig. 1). This suggests that thermoreceptive areas in addition to those in the spinal cord are involved in mediating the response. Also, an experimental rise in the Tinsp at a T.~ of 5 ~C, produced no change in the temperature of the spinal cord (Fig. 2), and yet we observed a significant decrease in HP, of 1.68 W kg 1. Thermoreceptors other than those in the spinal cord must therefore have been involved in mediating the changes in HP observed during these experiments. The thermoreceptors involved in the changes in heat production recorded in the final two series of experiments, must be situated in the head region, i.e. that part situated within the head mask and that was selectively stimulated. Since the thermosensitivity of the hypothalamus has been found to be negligible in all species of birds so far studied (Simon et al. 1986), the changes in brain temperature (Fig. 4) probably had no influence. It is thus tempting to assume that the observed changes in heat production were simply a result of the changes in the input from peripheral thermoreceptors. This assumption is also supported by our observation that the metabolic responses occurred within 2 - 4 min after the change of rinsp , i.e. probably before central body thermoreceptors could have been stimulated. Assuming that the beak temperature is responsible for monitoring the peripheral thermal input, the thermal sensitivity can be calculated from the mean changes in HP (Fig. 1) and in beak temperature (Fig. 2). The observed changes in HP and Tbeak following a rise i n Tinspat a Ta of 5 ~ and a lowering at a T a of 25 o C, correspond to thermal sensitivities of-0.26 and -0.30 W k g ~ ~C 1, respectively. These values are somewhat lower than the two other published values for thermal sensitivity of the skin of birds, being-0.6 W kg ' ~ 1in ducks (Inomoto and Simon 1981) and 1.7 W kg 1 o@1 in pigeons (Rautenberg 1971). Helfmann et al. (1981) calculated the thermal sensitivity of the head of the domestic goose (Anser

C. Bech et al.: Thermosensitivity in pigeons

anser) using changes in brain temperature as an indication of changes in head temperature. They arrived at values between -0.75 and -1.65 W kg 1 ~C i. Using a similar approach in the present study, i.e. changes in brain temperature (Fig. 4) as an indication of temperature changes of the entire head, the calculated mean thermal sensitivities were -1.73 and-3.11 W kg 1~ 1 for the series of experiments in which Tinsp w a s lowered at a T~ of 25 ~C, and raised at a Ta of 5 ~C, respectively. Necker (1972) has described thermoreceptors sensitive to cold in the beak of the pigeon. Although his experimental design rendered a clear distinction of the stimulated areas impossible, the thermoreceptors appeared to be confined to the margins and the inside of the beak. Necker (1972), himself, stated explicitly that "no response could be elicited by cooling or warming the outer side of the beak...". He concluded that the thermoreceptors might possibly be involved in the perception of the temperature of food and water. However, as Necker (1972) also pointed out, the static response curve suggests that the thermoreceptors could also be potentially useful in mediating the input to the thermoregulatory system. By studying the responses of the trigeminal ganglion to thermal stimulation, Necker (1972) showed that the thermosensitive neurons were located on the beak. The observation of Makjavic and Eiken (1985) is therefore interesting, viz. that "the (human) trigeminal pathway provides a powerful contribution to general shivering" and that selective stimulation of the facial area produced a marked increase in EMGactivity in man. Necker and Rautenberg (1975) concluded that the cold receptors present on the tongue (Kitchell et al. 1959) and on the beak (Necker 1972, 1973) of the pigeon were of little importance in autonomic thermoregulation. This conclusion was based on the results of experiments in which peripheral inputs from thermoreceptors originating between vertebrae C 4 and T h 4 had been cut off by spinal deafferentation. In the absence of the peripheral thermal inputs from these areas, pigeons did not respond, by shivering, to either low T a or to deep hypothermia, indicating that the thermoreception (both peripheral and central) originating in parts of the head above the deafferented region played little part in the shivering response (Necker and Rautenberg 1975). However, the increase in T,o produced by the increase in the metabolic rate in response to cooling of the spinal cord apparently had an upper limit. Body temperature increased only to a value ca. 2.0 ~ above normal, and no further increase occurred even with strong spinal cooling. This in-

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dicates the existence of some warmsensitive thermoreceptors situated cranial to the deafferented region, which are able to negate the increased input from the spinal cord thermoreceptors (Necker and Rautenberg 1975). Another indication that peripheral thermoreceptors exist in the head region of the pigeon has been presented by Schmidt (1982), who selectively stimulated the facial skin by pumping air through small tubes pointed towards the nose and the eyes. Cold stimulation of these areas resulted in an increase in the intensity of shivering, as well as an appropriate behavioural thermoregulatory response. This latter response was represented by an increase in the reinforcement-rate resulting in an increase in ambient temperature. Thus, even though there are conflicting opinions on the significance of the peripheral inputs from thermoreceptors in the head region, the results of some studies, including those of the present one, seem to support the view that such input could be important in mediating the thermoregulatory responses of the pigeon. This view may also probably hold true for other species of birds. It is therefore of interest that both Gregory (1973) and Leitner and Roumy (1974) found thermoreceptors to be present on the outside of the bills of ducks. The receptors were most abundant on the bill tip and around the nostrils (Leitner and Roumy 1974). Detection of changes in the temperature of the inspired air may therefore be an important component of avian thermoregulation. Acknowledgements. The study was supported by the Deutsche Forschungsgemeinschaft (SFB 114). We thank Philip Tallentire for improving the language.

References Bech C, Rautenberg W, May B, Johansen K (1982) Regional blood flow changes in response to thermal stimulation of the brain and spinal cord in the Pekin duck. J Comp Physiol 147:71-77 GrafR (1980) Diurnal changes of thermoregulatory functions in pigeons:II. Spinal thermosensitivity. Pfltigers Arch 386: 181-185 Gregory JE (1973) An electrophysiological investigation of the receptor apparatus of the duck's bill. J Physioi 229:151164 Hammel T (1968) Regulation of internal body temperature. Annu Rev Physiol 30:641-710 Helfmann W, Jannes P, Jessen C (1981) Total body thermosensitivity and its spinal and supraspinal fractions in the conscious goose. Pfliigers Arch 391:60 67 Inomoto T, Simon E (1981) Extracerebral deep-body cold sensitivity in the Pekin duck. Am J Physiol 241:R136R145 Kitchell RL, Strom L, Zotterman Y (1959) Electrophysiological

752 studies of thermal and taste reception in chickens and pigeons. Acta Physiol Scand 46 : 133-151 Leitner L-M, Roumy M (1974) Thermosensitive units in the tongue and in the skin of the duck's bill. Pfl/igers Arch 346:151 155 Martin R, Simon E, Simon-Oppermann Ch (1981) Brain stem sites mediating specific and non-specific temperature effects on thermoregulation in the Pekin duck. J Physiol 314: 161173 Mekjavic IB, Eiken O (1985) Inhibition of shivering in man by thermal stimulation of the facial area. Acta Physiol Scand 125:633-637 Mercer JB, Simon E (1984) A comparison between total body thermosensitivity and local thermosensitivity in mammals and birds. Pfliigers Arch 400:228-234 Mills StH, Heath JE (1972) Responses to thermal stimulation of the preoptic area in the house sparrow Passer domesticus. Am J Physiot 222:914-919 Necker R (1972) Response of trigeminal ganglion neurons to thermal stimulation of the beak in pigeons. J Comp Physiol 78 : 307-314 Necker R (1973) Temperature sensitivity of thermoreceptors and mechanoreceptors on the beak of pigeons. J Comp Physiol 87:379-391 Necker R (1977) Thermal sensitivity of different skin areas in pigeons. J Comp Physiol 116:239-246 Necker R, Rautenberg W (1975) Effect of spinal deafferentation on temperature regulation and spinal thermosensitivity in pigeons. Pfliigers Arch 360:287-299 Rautenberg W (1969) Die Bedeutung der zentralnerv6sen Ther-

C. Bech et al.: Thermosensitivity in pigeons mosensitivitfit fiir die Temperaturregulation der Taube. Z Vergl Physiol 62:235-266 Rautenberg W (1971) The influence of skin temperature on the thermoregulatory system of pigeons. J Physiol (Paris) 63:396-398 Rautenberg W, Necker R, May B (1972) Thermoregulatory responses of the pigeon to changes of the brain and the spinal cord temperatures. Pfliigers Arch 338:3142 Schmidt I (1982) Thermal stimulation of exposed skin areas influences behavioral thermoregulation in pigeons. J Comp Physiol 146:201 206 Siegel S (1956) NonI~arametric statistics for the behavioral sciences. McGraw-Hill, New York Simon E (1981) Effects of CNS temperature on generation and transmission of temperature signals in homeotherms. A common concept for mammalian and avian thermoregulation. Pflfigers Arch 392:79-88 Simon E, Pierau F-K, Taylor DCM (1986) Central and peripheral thermal control of effectors in homeothermic temperature regulation. Physiol Rev 66:235-300 Simon E, Simon-Oppermann C, Hammel HT, Kaul R, Maggert J (1976) Effects of altering rostral brain stem temperature on the temperature regulation in the Adelie penguin, Pygoscelis adeliae. Pfl/igers Arch 362:7-13 Simon-Oppermann C, Simon E, Jessen C, Hammel HT (1978) Hypothalamic thermosensitivity in conscious Pekin ducks. Am J Physiol 235:R130-R140 Withers PC (1977) Measurements of VO2, VCO2, and evaporative water loss with a flow-through mask. J Appl Physiol: Respir Environ Exercise Physiol 42:120-123