Play and exercise in the California ground squirrel

Anim . Behav., 1977,25,782-786

SHORT COMMUNICATIONS Gerbil Drinking Patterns Research has been directed to establishing the precise timing of meals and drinks in the laboratory rat (K . Oatley . Nature, Lond., 229, 494-496, 1971), as part of an investigation of behavioural regulation . It was shown that while rats have some tendency to drink before feeding, most drinking occurs just after a meal . This accords with observations made on other species such as the dog (E . A . Robinson & E . F . Adolph . Am. J. Physiol., 139, 39-44, 1943) that feeding has a thirstprovoking effect, though in the case of the rat a close examination of behaviour shows that it is anticipating rather than responding to the dehydrating effect of food in the gut (K . Oatley & F. M . Toates, Psychon . Sci., 16, 225-226, 1969). In the study reported here the timing of meals and drinks was examined in the Mongolian gerbil (Meriones unguiculatus), a species in which the peculiarity of starvation polydipsia has been extensively investigated (J. W. Wright . Anim . Behav., 24, 300-304, 1976), but which has received little attention in terms of normal behavioural regulation. It was felt that a species different in natural habitat and in some aspects of fluid control might yield valuable comparative data . Subjects were six male Mongolian gerbils, of mean weight, 65 g. They were housed in a modified Campden rodent test chamber 25 x 23 x 21 cm, with a food compartment containing a photocell circuit which recorded when a pellet of food was taken and at the same time automatically delivered another pellet . Food was 45-mg precision food pellets supplied by Campden Instruments Ltd . Water was taken from a spout connected to a drinkometer. Food and water were available ad libitum at all times . A 12-h dark-12 h light artificial light cycle was employed . A meal was defined as more than three pellets taken at intervals of 3 min or less,

15 10 . 5

although in practice most meals consisted of many more pellets than this taken one immediately after the other . Figure 1 shows a histogram of when water was taken in relation to meals over a 24-hr period . It can be seen that 68 % of the daily water intake was made in the 5 min immediately before a meal . There was no evidence of post-meal drinking. Each animal behaved in the way shown in this pooled histogram in both the light and dark phases . In fact feeding generally took place immediately at the termination of drinking when the two were associated, though some meals took place with no closely associated drinking and some drinks with no associated feeding. All drinks observed were used in the construction of Fig . 1 . The actual manner of drinking was different from that of the rat, quite apart from its meal association . The daily intake was in the form of 10 to 18 distinct, rapid and unbroken bouts . This is in contrast to the interrupted nature of the rat's drinking . Food intake was in 16 to 22 meals . As a check we ran three rats in our equipment and obtained a result almost identical to Oatley's. Under ad libitum conditions there is no evidence of a feeding-to-drinking excitation in the gerbil, though that is not to say that it would not appear under other experimental conditions . The results suggest that body fluid deficit which arises in the time following drinking exerts an inhibition on feeding and this inhibition is lifted by drinking. Water-deprived gerbils cut down on their food intake ( C . L. Kutscher. Ann. N. Y. Acad. Sci., 157,539-552, 1969) . It is curious how rapid any such disinhibition must operate, implying a mouth or gut factor. Alternatively, the animal is executing a rather clever preprogrammed sequence : '(1) drink, (2) eat' . A simple attention, arousal or exploratory activity model could hardly explain the consistent temporal order of activities . More experimentation and model building in this area is needed, taking comparative aspects into account . Further, we believe that the drinking-feeding pattern may play a role in determining that polydipsia will result during food deprivation in the gerbil, but not in the rat . If under ad libitum conditions food-seeking activity is commonly preceded by drinking, this pattern may well persist when food is withdrawn . An increasing number of food-seeking explorations would be expected to occur under food deprivation . Additional experimentation in this direction is indicated . F . M. ToATES & B . EWART Division of Psychology, Preston Polytechnic, Preston, Lancs . (Received 1 February 1977 ; MS. number: S-7) Play and Exercise in the California Ground Squirrel (Spermophilus beecheyi) Brownlee (1954) suggested that play behaviour functions to exercise muscles that are later used in serious adult behaviour . Fagen (1976) has critically examined this hypothesis, and has evidence that the majority of pony foals' exercise is during play (Fagen unpublished) . Fagen (personal communication ; Young & Fagen, in press) suggested that by plotting the duration of playbouts as a survivorship function (the logarithm of the number of bouts that exceed a given bout length versus

5

Fig . 1 . Histogram showing the time at which drinking took place relative to the meal nearest in time to the drink. Intervals of 5 min were measured both before the start and after the end of a meal . 782



783

SHORT COMMUNICATIONS the bout length) one could test Brownlee's hypothesis . The strength and endurance of muscles are best maintained if muscles are exercised to near fatigue (Astrand & Rodahl 1970) . Let us assume that (1) play has a primary function, and (2) if this function is to keep muscles in shape, it controls the durations of the play bouts . Then, play-bouts should last long enough to exercise the muscles involved to near fatigue. The probability of a bout ending would then be low during the necessary exercise period, and increase rapidly thereafter . A convenient mathematical model that has these characteristics assumes that the probability of a bout ending is a linear function of time, increasing from zero at the start to one at the end of the longest of all bouts . We then obtain the equation (z - 1)! (1/x

x)!

where y is the predicted number of bouts longer than x, x is the length of a bout in seconds, z is the longest duration any bout may last, and b is the total number of bouts (y intercept) . This model is a convex curve on a log survivorship plot . A commonly cited characteristic of play is that it is easily interrupted (Loizos 1966) . If random events independent of play control the lengths of play-bouts by interrupting them, then the probability of a bout ending would be independent of the duration of the bout, and one would predict a straight line (exponential decay) on the log survivorship plot . I measured the durations of 127 bouts of social play between young California ground squirrels under natural conditions . (Solitary play is rare in these squirrels .) Play-bouts were operationally defined as silent interactions that ended with the unhurried separation of the interactants, and contained at least one of the following

motor patterns : lateral curve, push with forepaw, pounce, and wrestle . A bout lasted from the time the squirrels approached within 5 cm until they began independent activities . Figure 1 shows the survivorship plot of the data . The best fitting (least squares) curve under the muscle exercise hypothesis is shown, which takes the form

1 \ x (610)! Y --

43 611

/1{

(610 - x) !

Based on this line, one-quarter of the bouts should fall in each of the intervals 0 to 18, 19 to 28, 29 to 40, and greater than 40 s (Slater 1974) . The number observed in each of these intervals was 99, 16, 8, and 4 respectively . This is significantly different from predicted (x2 = 192 . 3, df = 3, P << 0 .005) . The muscle exercise hypothesis is not supported . Also shown in Fig. 1 is the best fitting linear regression line (r = 0 .98) . The equation for this line is y = 105 .4 (0 .9311)x, where 0.9311 is the probability of the bout continuing for longer than duration x . This line predicts that one-quarter of all bouts should fall in each of the intervals 0 to 4, 5 to 10, 11 to 19, and greater than 19 s, The number of bouts falling in each of these intervals was 30, 42, 31, and 24 respectively. This is not significantly different than predicted (x2 = 5 . 31, df = 3, 0 . 10 < P < 0 . 20), and the hypothesis of control of play durations by random events cannot be rejected . The lack of support for the muscle-exercise hypothesis may be due to invalid assumptions behind the model . Even if some random events control the duration of play bouts (as supported by the second test above), it could be possible that the relatively infrequent long play-bouts are sufficient to keep muscles in shape . If this be the case, we are once again left to speculate on the function of the shorter bouts.

T (seconds) Fig . 1 . A survivorship plot of the number of play-bouts lasting longer than the length of a play-bout (T) shown on the abscissa . The straight line is the best-fitting linear regression line (r = 0 . 98) ; the curved line is the best-fitting curve under the muscle exercise hypothesis



784

ANIMAL BEHAVIOUR, 25, 3

I would like to thank Robert Fagen for commenting on an early draft of the manuscript. This work was supported by N .I.M .H. Grant 1 R03 MH27071-01 . D . L. McDoNALD Department of General Science, Oregon State University, Corvallis, Oregon 97331 . References Astrand, P . O . & Rodahl, K. 1970 . Textbook of Work Physiology. New York : McGraw-Hill Book Co . Brownlee, A . 1954 . Play in domestic cattle : an analysis of its nature. Brit . Vet. J., 110, 48-68 . Fagen, R . M . 1976. Exercise, play, and physical training in animals . In : Perspectives in Ethology, Vol . 2 (Ed. by P. P. G. Bateson & P. H. Klopfer), pp . 189-219. New York : Plenum . Loizos, C. 1966. Play in animals . Symp. Zool. Soc. Lond., 18, 1-9 . Slater, P . J . B. 1974. The temporal pattern of feeding in the zebra finch . Anim . Behav ., 22, 506-515 . Young, D . Y. & Fagen, R . M . (in press) . Temporal patterns of behaviour : durations, latencies, and sequences . In : Handbook of Quantitative Ethology (Ed. by P. Colgan), Chapter 3 . New York : Wiley-Interscience . (Received 6 October 1976 ; revised 10 January 1977 ; MS. number : As-4) Succesful Replication of, and Selective Breeding for, Classical Conditioning in the Blowfly Phormia regina Until now, no reports of conditioning or learning in Diptera have withstood the tests of independent replication and detailed analysis. Whereas the advantages of Drosophila for behaviour-genetic analyses have long been recognized, those of the blowfly, Phormia regina, have not, though it has been subjected to intensive physiological and much behavioural analysis (V . G . Dethier. The Hungry Fly . Cambridge, Mass . : Harvard University Press 1976) . Evidence for conditioning in Diptera, however, remained elusive (F . R. Yeatman & J. Hirsch . Anim . Behav ., 19, 454-462, 1971), until M. C. Nelson's thorough demonstration of classical conditioning in Phormia built on the careful analyses of responses and conditions by Dethier and his colleagues ( M . C. Nelson . J. comp . physiol. Psycho l., 77, 353-368, 1971) . This report describes the first successful independent replication of conditioning in Diptera and a sevengeneration response to bidirectional selection validating genetic correlates of an initial distribution of individual differences (IDs) . An unconditioned proboscis-extension response, elicited by a 0 . 5-M sucrose stimulus applied to the labellar lobes, can be conditioned to a neutral stimulus of either distilled water or 1-M saline applied to the front tarsi, if control is included for sensitization, known as the central excitatory state (CES). The conditioning procedure with CES control consists of trials presenting in succession three stimuli, the first two being neutral (CS 1 and CS2) and the third unconditioned (US), with temporal contiguity but not overlap between CS, and CS2 (each presented for 4 s), but partial overlap between CS2 and US (presented during the last second of CS2), and a 10-min inter-trial interval (ITI) . Two neutral stimuli, rather than one, permit CS 1 to drain off responses resulting from US-produced CES and CS 2 to measure

the strength of the conditioned association . The 10-min ITI permits the CES to wane . Flies, deprived of food and water for 3 days from eclosion, were mounted by their wings on wax-coated applicator sticks . The proportion of flies responding with proboscis extension to CS2 steadily increased over 15 trials . In addition to the foregoing, Nelson performed six control experiments . Her basic results have now been corroborated in an independent replication (L. A . McCauley, M .A . thesis, University of Illinois at Urbana-Champaign, 1973) . Furthermore, both studies agreed in their distributions of IDs when flies were graded as `good', `fair' and `poor' learners according to their number of conditioned responses over the last eight trials . This suggested the possibility of selection and further behaviour-genetic analysis . Bidirectional selective breeding was therefore undertaken to produce lines of bright (B) and dull (D) flies. The criteria for bidirectional selection were `good' and `poor' performance in our replication of Nelson . A sample of 39 flies was trained, graded and segregated into three groups of 14 good, 10 fair and 15 poor learners . The B and D lines were established with the 14 good and 15 poor learners, respectively, along with a control line of untrained flies from another sample . After training, individuals were carefully removed from applicator sticks (to minimize wing injury) and mated . Beginning with generation 3 in both lines, the sexes were segregated within 8 h of eclosion to obtain virgin females for selection . The lines were maintained at 27 C on a 15-h light/9-h dark schedule . In this study, the order of presentation of CS 1 and CS 2 (water and saline) was reversed on alternate generations

GENERATION

Fig. 1 . The mean conditioning scores (average of conditioned responses to CS 2 on trials 8 to 15) and 95 confidence intervals for each generation of selection . (Some confidence intervals have been slightly displaced for clarity.) The selected lines were tested every generation and the control on generations 1, 3, 5 and 7 .