Modulation of drinking by ambient temperature changes

Anim. Behav .,

1970, 18, 753-757

MODULATION OF DRINKING BY AMBIENT TEMPERATURE CHANGES BY

PHILIP BUDGELL

Institute of Experimental Psychology, Oxford

In many species there is a positive correlation between water intake and ambient temperature . Three hypotheses have been proposed to explain this relationship : (a) drinking may be stimulated by local dryness of the oral pharyngeal membranes caused by water evaporation at high environmental temperatures (Gregerson & Cannon 1932) ; (b) drinking may be stimulated by systemic dehydration consequent upon thermoregulatory water loss (Hainsworth, Striker & Epstein 1968) ; and (c) drinking may be altered by deviations from the normal brain temperature (Andersson 1963) . A fourth possibility is that drinking may occur in response to peripheral temperature changes . The evidence suggests that species differ in the manner in which temperature-induced drinking is achieved . Thus in dogs and goats drinking may occur in the absence of dehydration (Andersson 1963 ; Gregerson & Cannon 1932), but in rats it is claimed that dehydration is the most important factor (Hainsworth et al . 1968) . The experiments reported in this paper were designed to investigate the possibility that ambient temperature has a direct effect on drinking, and that water is thus made available for thermoregulatory purposes . Experiment 1 This experiment was conducted in order to investigate the effect of ambient temperature on water intake following deprivation . Methods The subjects were six adult Barbary doves (Streptopelia risoria) which were bred in the Institute colony . They were housed individually on an artificial light-dark cycle (8 hr light to 16 hr dark), at an ambient temperature of 20°C, for 1 week prior to the start of the experiment . Throughout the testing programme, the subjects were allowed 7 days ad libitum access to food and water at 20°C, then deprived of water for 48 hr at the same temperature . The subjects were then transferred individually to another cabinet for 30 min at a specified temperature, and then allowed to drink water, which was at 20 °C, from their normal drinking cup . During the drinking period, subjects were watched through an observation window . Each was seen 753

to take one large draught, and 5 min were then allowed before the water was removed . No animal was observed to take a second draught . After drinking, the birds were started on another testing cycle . The cup was weighed before and after drinking . The tests were run at 20°, 10°, 30°, 0° and 40°C, in that order . Results The results are summarized in Fig . I and show a significant increase in amount drunk as a function of increasing ambient temperature (Kruskal-Wallis P<0 .05) . This finding suggests that drinking can be changed as a direct consequence of ambient temperature changes. 20

15

I

/1 10 m

0 3 5

0 10

20

30

40

Room temperature ( °C)

Fig . 1 . Recovery from 48 hr water deprivation (5-min drinking test) as a function of ambient temperature . Vertical lines indicate range . Kruskal-Wallis, H=11 . 14, P<0-05 .

Experiment 2 The finding, that the amount of water drunk after deprivation varies with the temperature at which drinking occurs, implies that at some temperatures, more water is drunk than is required for restoration of water balance . This possibility is investigated in this experiment .





754

ANIMAL BEHAVIOUR, 18,

4

Methods The six subjects used in the previous experiment were trained to obtain 0 . 1 ml water rewards by pecking in a Skinner box. After 3 weeks training, they were housed individually at 20°C, on an 8 hr light to 16 hr dark cycle . The subjects were tested each day in the Skinner box, and were run to a satiation criterion of 5 min without responding. No water was available in the home cages, so that the daily ration was all obtained in the Skinner box . Each animal was given five successive trials at each of the five test-temperatures, prior to the start of testing proper. The animals were tested at 20°, 10°, 30°, 0° and 40°C, in that order, but on alternate days . On intervening days the tests were run at 20°C, so that each test day was followed by a day at 20 °C. Each subject was weighed daily, before and after testing . As in the previous experiments, each animal was allowed a 30 min acclimatization period before water was made available . Water rewards of 0 . 1 ml, at 20°C, were delivered for each peck, and a record was kept of the number of rewards obtained during each test.

to be equal to the weight of water ingested, showing that water loss during the test period was negligible . Figure 3 shows the quantity of water ingested on between-test days, as a function of the ambient temperature on the previous test day. These results indicate that the temperature at which a test is conducted influences the amount drunk on the next occasion . The most simple

Results As in the previous experiment, water intake in the test situation was found to be an increasing function of ambient temperature (Fig. 2) . In every case the gain in body weight was found

Fig . 3 . Operant water intake at 20°C as a function of temperature on previous day's test . Vertical lines indicate range . Kruskal-Wallis, H=13 . 1, P<0 . 005.

15

10

0 0

10 20 30 Room temperature (°C )

40

Fig. 2 . Water intake during daily operant drinking tests as a function of ambient temperature . Vertical lines indicate range . Kruskal-Wallis, H=23 . 2, P<0 .001 .

e

5

0 3

0 0

10

20

30

i 40

Temperature on previous day

interpretation of these results is that the subjects `under-drink' when tested in the cold, and `overdrink' when tested in the heat . When tested at 20°C on the following day, the imbalance is made up . Experiment 3 It has been reported (McFarland & Wright 1969) that water debt is not affected by ambient temperature during deprivation . This experiment was conducted as a more direct test of this possibility. Methods The subjects were three adult Barbary doves (Streptopelia risoria), which were bred in the Institute colony . They were housed in a temperature-controlled cabinet, on an artificial light-dark cycle (8 hr light to 16 hr dark), at an ambient temperature of 20°C, for 1 week prior to the start of the experiment. Throughout the testing programme the subjects were first allowed 48 hr ad libitum access to food and water at a specified temperature . They were then deprived of water for 48 hr at the same temperature, after which they were transferred



BUDGELL : MODULATION OF DRINKING BY AMBIENT TEMPERATURE

individually to another cabinet for 30 min at 20°C, and then allowed to drink water which was at 20°C from their normal drinking cup . During the drinking period, subjects were watched through an observation window. Each was seen to take one large draught, and 5 min were then allowed before the water was removed . No animal was observed to take a second draught . After drinking, the birds were started on another testing cycle at a different temperature . Each subject was weighed before and after deprivation, and the cup was weighed before and after drinking. Testing cycles were run at 20°, 0°, 30° and 10°C, in that order. Results The results are summarized in Table I . From this it can be seen that there is no difference in the body weight change induced by deprivation at different temperatures . Nor is there any Table I. Water Ingested at 20°C, after 48 hr Deprivation at Various Environmental Temperatures Deprivation Mean change Mean water temperature (°C) in body weight (g) intake (g) 0

20 . 0

14 . 5

10

19 . 7

14 . 4

20

19 . 7

14 . 2

30

19 . 0

14 . 5

difference in the amounts of water drunk after these deprivation periods . These results confirm those from previous work (McFarland & Wright 1969) and reinforce the conclusion that water debt is not affected by the ambient temperature at which deprivation is conducted, at least up to 33°C . Experiment 4 The previous experiments suggest that ambient temperature has a direct influence on both consummatory and appetitive aspects of drinking behaviour. This experiment was designed as a further investigation of the effect on appetitive behaviour. Methods Three Barbary doves were trained to obtain water rewards which were 0 . 1 ml, and at 20°C, by pecking at an illuminated key in a Skinner box installed within a temperature-controlled cabinet. Rewards were delivered on a VI 2-min schedule, and the animals were trained for 10

755

weeks, until they responded at a constant rate for a 3-hr period, following 48 hr water deprivation . After training, the animals were tested every second day, and were water deprived during the intervening periods. Tests were conducted alternately, at a constant temperature of 15°C, and at a temperature varying sinusoidally between 5° and 25°C . Frequencies of 0 . 40, 0 . 50, 0 . 66, 1 .00, 1 . 33, 2 . 00 and 4 .00 cycles per hour were used. The sinusoidal temperature function was generated by a specially designed control system, which maintained an accuracy of ±0-25 - C. The pecks delivered, and rewards obtained, by the subjects were recorded on an event recorder throughout the whole of each 3-hr test period, but the records for the first and last 30-min period were discarded, to avoid possible effects of initial transients, and satiation, respectively . Each subject was tested once at each frequency . Results The results indicated that the mean response rate was the same at all frequencies, and that, due to the nature of the reward schedule, the distribution of rewards obtained was not affected by fluctuations in response rate . The results obtained from two sample test sessions, at different frequencies, are illustrated in Fig . 4, from which it can be seen that both phase-angle and amplitude of response are affected by frequency . Preliminary examination of the results indicated that the frequency response was similar to that of a first-order system . On this basis, the appropriate transfer function is given by the following equation : HU-) =

jwT -}- 1

where k is the gain, and T the time-constant, of the system jw is the complex angular frequency (Milsum 1966) . The phase-angle between input (temperature) and output (response rate) is given by the equation (Milsum 1966) : e = - arctan wT ~- L H(jw). (2) The results provide a series of values of o for corresponding values of w . For example, at a frequency of 1 . 0 cycle per hour the observed phase-lag is 31 .2° : o = - arctan w t = - arctan 21rT = - 31 . 2 (3) From this equation, T = 0 .6056/2,rT hr = 5 . 78 min . On average, the value of T was found to be



7 56

ANIMAL BEHAVIOUR, 18, 4

The expected values of the amplitude ratio, AR, as a function of frequency can now be

calculated. AR = H(jw) = U e v

t0

0 0. E I0

00 d

Fig. 4. Sample results at temperature frequencies of 0 . 5 cycles per hr (top), and 4 cycles per hr (bottom) . Response rate in pecks per 5 min is indicated by crosses, ambient temperature by the continuous curve .

equal to 5 . 57 min, and this value forms the basis of the phase plot illustrated in Fig . 5a, in which the empirical data are matched to a calculated phase curve . 0 \T

(a) 0 0

c

PIN

-30

I

T

-60

if

1\

-90 I I

0 .1

T

1 .0

T

10 r

0

Q -05 0

of r

I I I I I I 00(0 OK) 0 0 C'InW 0M~0 0 000 -- N at 10

1

10

r

r

Fig. 5. Bode plot of mean response rate as a function of temperature frequency . (a) Observed phase lag matched to that of a first-order system (continuous curve) . (b) Observed compared with expected (continuous curve) amplitude ratio . Vertical lines indicate range.

k (1 + (wT2)#

(4)

log10AR=loglok - i (loglo(l+(wT) 2)) . (5) A unity AR can be defined as being achieved when two conditions are satisfied : (1) the average response rate is the same at the lowest observed frequency as at infinite frequency, and (2) the same empirical response amplitude is found at two different low frequencies . The ratio between these and the temperature amplitude is then arbitrarily defined as unity . In practice, both these conditions were satisfied, and this procedure was used in the construction of the predicted curve in Fig . 5b, viz : log 10AR = - j •(log 1 o(l + (_ T)2)) . (6) Comparison with the observed AR, calculated on the same basis, shows good correspondence with the expected values (Fig . 5b) . In other words the observed phase-lag as a function of frequency suggests that the system is a first-order one . Comparison of the observed amplitude ratio, with that calculated on the basis of this prediction, should provide an independent test of this hypothesis . The results of this comparison (Fig . 5b) appear to confirm the hypothesis . The results of this experiment support the view that ambient temperature has a direct effect on operant drinking behaviour . The elicited response rates were sufficiently high to ensure that the subjects obtained every reward possible on the VI schedule . Thus the variations in response rate made no difference to the water ingested, and the experiment can be said to demonstrate the effect of ambient temperature on appetitive drinking behaviour, independently of possible feedback from the consummatory behaviour . Discussion The experiments reported in this paper indicate that both normal and operant drinking are influenced by the ambient temperature at which the drinking-test is conducted . Such drinking can be regarded as a modulation of the normal (20°C) drinking response, so that animals `under-drink' at low temperatures, and 'overdrink' at high temperatures . In other words, drinking behaviour can be changed as a direct consequence of ambient temperature changes, and both consummatory and appetitive aspects of the behaviour are involved in this response .

BUDGELL : MODULATION OF DRINKING BY AMBIENT TEMPERATURE

It has been suggested (McFarland 1970) that drinking in response to ambient temperature changes can be seen as a feed-forward phenomenon, by means of which the animal is able to drink in anticipation of thermoregulatory water loss . The present findings support this view . The results of experiment 4 indicate that appetitive drinking can occur as a rapid response to changing ambient temperature. The frequency response is characteristic of a firstorder system having a time-constant of 5 . 57 min . This can be compared with a time-constant of about 2 min for the hypothalamic temperature response to a step change in ambient temperature, in the 48 hr water deprived Barbary dove (McFarland & Budgell 1970) . It is thus probable that the drinking response is mediated by hypothalamic temperature changes, but the problem requires further investigation . The results of experiment 3 are in agreement with the previous findings (McFarland & Wright 1969), in suggesting that the magnitude of water debt is not affected by the ambient temperature at which deprivation is conducted . In view of the findings (Cade 1964), that the main loss of water in granivorous birds is by pulmocutoneous evaporation, and the fact (Dawson 1958) that the main environmental factor controlling that rate of loss is ambient temperature, the results of experiment 3 may seem surprising . However, it has been suggested that as body temperature is reduced during deprivation it is possible that thermoregulatory water loss is obviated by reduced food intake . Summary Barbary doves deprived of water at different ambient temperatures, but tested at the same temperature, have the same body weight change, and drink the same amounts during the test . However, doves deprived at the same temperature, and tested at different temperatures,

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drink different amounts . The conclusion that ambient temperature has a direct effect on drinking is supported by the finding that the response rate in an operant situation can follow harmonic changes in ambient temperature, thus permitting a frequency analysis of the temperature-drinking system . Acknowledgments This research was supported by a grant from the Science Research Council . The author wishes to express his appreciation to D. J. McFarland and J. Fenton for assistance during the conduct of the experiments . REFERENCES Andersson, B. (1963) . Aspects of the interrelations between central body temperature and food and water intake. In : Brain and Behaviour (Ed. by M . Brazier), Vol . II . Washington : American Institute of Biological Sciences . Cade, T. J . (1964) . Water and salt balance in granivorous birds. In : Thirst (Ed. by M . Wayner) . Oxford : Pergamon Press. Dawson, W . R. (1958) . Relation of oxygen consumption and evaporative water loss to temperature in the Cardinal . Physiol. Zool., 31, 37-48 . Gregerson, M . I. & Cannon, W. B . (1932) . Studies on the regulation of water intake. I . The effect of extirpation of the salivary glands on the water intake of dogs while panting. Am. J. Physiol., 102, 336-343. Hainsworth, F. R., Stricker, E . M . & Epstein, A . N. (1968) . Water metabolism of rats in the heat : dehydration and drinking . Am. J. Physiol., 214, 983-989 . McFarland, D . J. (1970) . Recent developments in the study of feeding and drinking in animals . J. Psychosom . Res., 14, 229-237 McFarland, D . J. & Budgell, P. (1970) . The thermoregulatory role of feather movements in the Barbary dove (Streptopelia risoria) . Physiol.Behav., Behav ., 5, 676-684. McFarland, D . & Wright, P . (1969). Water conservation by inhibition of food intake . Physiol. Behav., 4, 95-99. Milsum, J. H. (1966). Biological Control Systems Analysis . New York : McGraw-Hill . (Received 23 April 1970 ; revised 8 June 1970 ; MS . number: 969)