Anim. Behav., 1992, 44, 111-115

Environmental influences on play behaviour in immature gelada baboons

L O U I S E B A R R E T T , R O B I N I. M. D U N B A R & P A T S Y D U N B A R Department of Anthropology, University College London, Gower Street, London WCIE 6BT, U.K.

(Received 14 March 1992; initial acceptance 24 April 1991; final acceptance 10 January 1992; MS. number." 3739)

Abstract. Data from gelada baboons, Theropithecus gelada, were used to test the hypothesis of Martin (Anim. Behav., 1982, 30, 294-295) and Lee (Behaviour, 1984, 91, 245-261; Primate Ontogeny, Cognition and Social Behaviour, 1986, Ed. by J. Else & P. C. Lee, Cambridge University Press, pp. 227-237) that the incidence of play behaviour among immature animals can be used as an indicator of environmental conditions. The results provide substantial support for the hypothesis: both the quantity of play (percentage of time spent playing, number of play bouts per hour) and play quality (high-energy versus low-energy actions) were significantly correlated with rainfall, and hence with habitat quality.

In a study of free-ranging vervet monkeys, Cerco- pithecus aethiops, at Amboseli, Kenya, Lee (1984, 1986) demonstrated that the level of play among juveniles was directly related to rainfall and hence to the quality and abundance of food resources. Immature vervets played less during the dry season when dietary quality was low, food resources more widely dispersed and a larger proportion of the time budget allocated to feeding. A similar reduction in the frequency of play in response to a decline in resource availability has been noted in a number of other species (e.g. rhesus macaques, Macaca mulatta: Loy 1970; squirrel monkeys, Saimiri scuireus: Baldwin & Baldwin 1976; baboons, Papio anubis: Oliver & Lee 1978; bighorn sheep, Ovis canadensis: Berger 1980; white-tailed deer, Odocoileus virginianus: Muller-Schwarze et al. 1982; see also Fagen 1981), and has led to the suggestion that play can be used as a sensitive indi- cator of both prevailing environmental conditions and the level of energetic stress imposed on immature animals (Martin 1982; Lee 1986).

In this paper, we use data from free-ranging gelada, Theropithecus gelada, to show that both the quality and quantity of play are extremely sensitive to resource availability.

M E T H O D S

The data used in the following analyses were col- lected by P.D. and R.D., during two 9-month field studies, in 1971-1972 and 1974-1975, of the gelada population inhabiting the Sankaber region of the

Simen Mountains National Park, Ethiopia (see Dunbar & Dunbar 1975).

During the 1971-1972 study, focal animal samples (Altmann 1974) of up to 30 min were recorded from individual subjects of different age- sex classes between September and December 1971 inclusive. In all, 44 samples (totalling 564min) are available for 2-year-old males, 46 samples (670.5rain) for 2-year-old females, 83 samples (1495 min) for 3-year-old males and 133 samples (2139-5 min) for 3-year-old females. A minimum sample of 60 rain per month was imposed for each age-sex class for present purposes. These samples provide data on both the frequency of play bouts (defined as continuous exchanges of play behaviour with at least one play action being exchanged in each consecutive 30-s time interval) and on the behaviour patterns used in play. Play actions were classified as 'low-key' (play bite, mouth, mouth- wrestle, slap at, jump at, jaw-fence, pull tail and object play) or 'high-key' (play box, chase, wrestle, rough-and-tumble), the distinction between these two categories being based on the level of whole- body activity (and hence energy expenditure) involved. For a more detailed description ofgelada play behaviour see Dunbar (1973) and Dunbar & Dunbar (1975). An average of 20-4 play acts were recorded for each class of animal in each month (with months having fewer than five acts being omitted from the analysis).

A second set of data covering a longer period of the year is available from a study of mother-infant behaviour carried out between November 1974 and

0003-3472/92/070111+05 $03.00/0 �9 1992 The Association for the Study of Animal Behaviour 111

112 Animal Behaviour, 44, 1

July 1975. With two exceptions, all the infants included in the sample were born between mid- November and mid-December and thus faced the dry season (December-April inclusive) at approxi- mately the same age. Longitudinal samples were taken on the behaviour of each mother-infant dyad beginning on, or shortly after, the day of birth. In each case, an attempt was made to collect 240 min of data during the infant's first week, second week, second fortnight and at monthly intervals there- after. Sampling sessions consisted of 30-min focal animal samples (Altmann 1974) during which the social interactions of mother and infant were recorded continuously, and scan samples of the activities of mother and infant were taken at 30-s intervals (for further details see Dunbar & Dunbar 1988).

Because infants receive most of their nutrition from their mothers via lactation and are therefore buffered against the effects of variation in the food supply, it would not be appropriate to test the hypothesis by analysing seasonal variation in the total amount of time devoted to play by infants. However, it is possible to test the hypothesis by using the infants as a basis for sampling one form of play by juveniles (namely, play with infants). We thus treated each infant as a source of attraction to the juveniles in its group and asked how often juveniles played with infants given that these were available.

Table 1. Rainfall and biomass data for the Sankaber and Gich regions of the Simen Mountains National Park (1974-1975)

Green biomass* Mean (g dry wt/m 2)

rainfall (ram) Month Sankaber Sankaber Gich

January 6.0 - - 117.2 February 14.0 - - 116.7 March 0.0 18.0 - - April 0.0 - - - - May 319.0 - - - - June 184.0 - - July 391.0 - - 143.0 August 364-0 139.6 178.0 September 138.0 209.0 October 72.0 - - 206-2 November 11.0 173.6 150.6 December 2.0 - - 118.8

*From Iwamoto (1979, Tables 12.6 and 12.10).

For each infant, the amount of time spent play- ing with juveniles per month was determined by calculating the proportion of scan samples on which the infant was recorded as in play with a yearling or a 2- or 3-year-old juvenile. Data on the frequency of play with juveniles (number of play bouts per h) were extracted from the focal sample records by summing the number of play bouts recorded during each time block and then dividing by the number of observation hours.

Data on grass biomass production are available for three of the sampled months for Sankaber (based on data given by Iwamoto 1979). A more extensive sample is available for the nearby Gich sector of the Park (approximately 8 km north-east of Sankaber) which had a similar climatic pattern (Hurni 1982). These data between them provide some evidence to support the claim that grass production correlates with rainfall.

R E S U L T S

September is the last month of the wet season, and both rainfall and grass growth decline progressively through to December (Table I). For all four age- sex classes of juveniles, rates of play correlate positively with rainfall (as a measure of the richness of the habitat; Kendall's T> 0.67; Fig. 1), a result that is significantly unlikely to occur by chance (Fisher's test for exact P-values, ~2= 18.406, df= 2 • P<0.02). Thus, play rates declined as environmental conditions deteriorated.

Figure 2 shows the median percentage of time that the 10 infants spent playing with juveniles. These samples cover the start of the dry season in November, and continue through the dry season into the early months of the wet season in May July. The frequency of play correlates significantly with the rainfall for that month (T=0-59, N=9, P<0.002). Partialling out the effect of infant age confirms that rainfall is the key factor here (Kendall's Txy.z=0.51, N=9 , P<0.05).

This is further substantiated by a comparison of play frequencies between the one infant born late in the study (infant O, born 26 March 1975, approxi- mately 4 months after the median birth date) and all the other infants born between mid-November 1974 and mid-January 1975. The third and fourth months of life provide the most dramatic contrast in terms of the prevailing environmental con- ditions: for the sample of 'early' infants, months three and four coincided with the worst months

Barrett et al.." Gelada play behaviour 113

io

%

4

i

Sept Ocf Nov Dec Month

Figure 1. Monthly variation in the play frequencies of juveniles (1971-1972). O: 2-year-old males; O: 3-year-old males; []: 2-year-old females; � 9 3-year-old females.

f

>, o.

u~

8 500

6

4

2

Nov Dec Jan Feb Mar Apt May Jun Ju[ Month

400

3oo

200 a

100

Figure 2. Monthly variation in rainfall (0 ) and percentage of the time budget devoted to play with juveniles by infant gelada (D), 1974-1975.

of the dry season (February, March and April), whereas in the case of infant O, this stage of development occurred at the beginning of the wet season (June/July), when ecological conditions were approaching the optimum. If habitat quality is the critical factor, then juveniles should have played with infant O at a much higher rate than they did with the other infants at this age. Table II confirms this: in both months 3 and 4, the frequency with which infant O played with juveniles is at least 3 standard deviations above the mean value calcu- lated for the sample of early-born infants. These differences are highly significant (month 3: z = 3.00, P=0.0013, one-tailed; month 4: z=6.08,

P < 0-00003, one-tailed), confirming that ecological constraints acting on juveniles determine the level of social interaction between infant and juvenile gelada.

Finally, to examine whether the quality of play is affected by environmental conditions, the pro- portion of high-key activities was determined for each of the four age-sex classes of juveniles from the 1971 1972 data set. Play was too rare in both November and December to calculate values for any class except 3-year-old males during November. The percentage of high-key play actions shown by each of the age-sex classes clearly declined as habitat conditions deteriorated (Fig. 3).

114 Animal Behaviour, 44, 1

Table II. Frequency of play bouts for early-born offspring compared to the late-born infafit O

Number of play bouts/h

Infant Month 3 Month 4

A 2.4 2-2 B 2.6 2-5 C 1.6 1.7 D 1.5 0"0 E 2.3 1-3 F 2-2 1 "6 G 0.7 0'6 H 1.6 0-2 T 2.2 1.3 O 3.7 6.5

Mean play rate 1.90 1.27 (excluding O) SD 0"60 0"86

I00

8O

v

~' 6o

40

I 2O

o

L i

0 Sepf Ocf Nov Dec

Month

Figure 3. Monthly variation in the percentage of high-key play actions shown by juveniles (1971-1972). �9 2-year- old males; � 9 3-year-old males; []: 2-year-old females; � 9 3-year-old females.

D I S C U S S I O N

We have shown that there is a strong positive corre- lation between habitat quality and both the fre- quency and quality of play by juveniles. Our results thus support the hypothesis that the incidence of play can be used as an index of prevailing environ- mental conditions. Indeed, the gelada data indicate that play is sensitive even to very small changes in habitat quality. This is suggested by the obser- vation that even the very slight increase in rainfall during January-February, which produces a brief flush of new grass growth, results in a rise in the level of play (Fig. 2).

Nutritional analyses of the grasses that make up the bulk of the gelada diet (see Dunbar 1977; Iwamoto 1979) show that both digestible crude protein and metabolizable energy are lower during the dry season than during the wet season (Iwamoto 1979; R. W. Wrangham, personal communication). As a result, the gelada are forced to increase the amount of time spent feeding during this period in order to compensate for a reduced rate of energy intake (Dunbar 1977; see also Dunbar & Dunbar 1988). This decline in forage quality also prompts a shift in the emphasis of the diet from grass blades to the grasses' subterranean root systems. Although these items are abundant, they must be dug up before they can be consumed and therefore require a much longer processing time per unit calorific value than do blades. At least part of the observed increase in dry season feeding time can probably be attributed to this extra handling time. In addition, the lower minimum temperatures typical of the dry season mean that animals have to spend more time feeding, owing to increased thermoregulatory costs (see Iwamoto & Dunbar 1983).

These observations suggest that juvenile gelada are probably forced to operate under essentially the same dry season constraints as the Amboseli ver- vets (see Lee 1984). First, since a larger proportion of each day must be devoted to feeding, juvenile gelada will have less time available for playful inter- actions. Second, and perhaps more importantly, immature gelada will also be constrained energeti- cally: the overall reduction in the amount of energy available from the diet (see Iwamoto 1979) means that the increased energetic costs associated with play cannot be tolerated under impoverished environmental conditions. It seems that, initially, the more vigorous high-key play activities are dropped from the behavioural repertoire (see Fig. 3), but later even the energetically less expensive forms of play are given up.

Our results also demonstrate that seasonal vari- ation in juvenile play behaviour has a major impact on the early social experience of gelada infants; at 3-4 months of age, infant O was frequently engaged in play with juveniles of all age-sex classes, whereas the early-born offspring were far more restricted in their choice of play partners during this stage of development, and had little option but to play alone or with other infants (see also Altmann & Altmann 1979). Since the nature and intensity of play varies considerably between age-sex classes (Dunbar & Dunbar 1975), it seems likely that these

Barrett et al.: Gelada play behaviour 115

differences in early social experience will affect the ability of infants to acquire information about the social environment into which they are becoming integrated (Gomendio 1988), and possibly influence the style of behaviour adopted as an adult (see e.g. Young & Hawkins 1979).

A C K N O W L E D G M E N T S

This paper was prompted by a request for data from Robert Fagen, and we are therefore grateful to him for drawing our attention to this issue. The fieldwork was made possible by grants from the S E R C and the Wenner-Gren Foundat ion for Anthropological Research. Logistic support and permission to work in the Simen Mountains Nat ional Park was generously provided by the Ethiopian Government Wildlife Conservation Organisation, while R.D. and P.D. were sponsored as Visiting Scholars by the Institute of Ethiopian Studies of the University of Addis Ababa. L.B. is currently supported by an N E R C postgraduate studentship. We thank Phyllis Lee, E. Somerville, Nilofer Ghaffar and Craig Roberts for their comments on an earlier draft of this manuscript.

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