How rhesus monkey infants budget their time between mothers and peers

Anita. Behav., 1981, 29, 598-609

HOW RHESUS MONKEY INFANTS BUDGET THEIR TIME BETWEEN MOTHERS AND PEERS

By GERRIT DE JONGE, H E R M A N DIENSKE, ELLY-ANN VAN L U X E M B U R G & LOUIS RIBBENS

Primate Center TNO, 151 Lange Kleiweg, Rijswijk, The Netherlands

Abstract. Social play between two rhesus monkey (Macaca mulatta) infants takes place mainly when they are both not in body contact with their mothers. This suggests that social play and mother-infant body contact are potential competitors in the infants' time budgets. We investigated whether the presence of a playmate changed the duration of mother-infant body contact during the first 6 months of life. A decrease in contact would favour play opportunity. Mother-infant pairs were observed alternately alone and together with another pair. Resting, which always occurs during on-mother, was not reduced in the presence of a peer. Body contact during activity phases was reduced in most playing pairs, but only to a large extent in pairs which showed relatively high levels of contact in the situation without a peer. Play opportunity was further increased by synchronization of the rest-activity cycles of the two infants; this occurred without a reduction in mother-infant interactions. No influences by mothers on play opportunity were demonstrated, except that strong maternal interference with resting reduced activity synchronization.

It is well known that early mother-infant interactions in rhesus monkeys (Macaea mulatta) consist mainly of body contact (see e.g. Hansen 1966; Hinde & Simpson 1975). A few weeks after birth, the young also begin to play with other infants (Meier & Devanney 1974; Tartabini & Dienske 1979). Both body contact and social play are probably of great importance for adequate social development (Mitchell 1970; Anderson & Mason 1974; Poirier et al. 1978). It is our experience that most play takes place when infants are off their mothers. This implies that if an infant reduces interactions with its mother, this increases play opportunity. This paper deals with the question of how rhesus infants divide their time between these two im- portant sets of social interactions. This topic is a part of a larger study aiming at the detection of possible relationships between the quality of mother-infant interactions and social play.

Methods Animals

Sixteen adult females and their young were studied. Two females were born in captivity; the others were caught in the wild. All except two were multiparous. We deliberately attempted to select mothers such that the sample showed a wide variety in mothering styles; some of them showed behavioural abnormalities such as loco- motion stereotypies and self-aggression. This variation among mothers was chosen in order to detect the rearing effects of different styles of mothering.

Pregnant females were placed in tactile isolation in single cages until delivery. As soon thereafter as two gave birth, their young were exchanged. This exchange was carried out because otherwise, conclusions on rearing effects would be confounded by the genetic similarity between mother and infant. Of course, cross- fostering would not have been necessary if the question posed in this paper had been the only one investigated.

Exchange took place during mild anaesthesia of the mothers. The foster infants, which were conscious, immediately clung to the strange, narcotized females. After full recovery, all mothers immediately accepted their foster infants without visual or olfactory inspection. Fourteen infants were less than one week old when the exchange took place; the remaining two were aged nine and 13 days.

After exchanges, tetrads of two mother- infant pairs were formed, such that an infant and its natural mother were not in the same tetrad. The two young in each tetrad were of the same sex. Six infants were females. Tetrads were designated with the letters A to H and pairs as AI, A2, B1, B2, etc.

Housing Two experimental cages of 320 x 80 x 160

cm were placed in one windowless room. Arti- ficial light was supplied from 0800 to 2000 hours. The temperature was 24 C. Food was given at 0830 and 1530 hours. Each cage could be divided into compartments, as shown schematically in

598

DE JONGE ET AL. : TIME BUDGETING BY RHESUS INFANTS 599

Fig. 1. Three arrangement were made: (1) S-I, single-pair situation: pairs of a tetrad were separated by an opaque screen that prevented visual and tactile interactions; (2) S-II, double-pair situation: the tetrad remained together in a space of the same size as each pair could use in S-I (i.e. 160 x 80 x 160 cm); and (3) S-OO, situation with two openings: the mothers were enclosed in the end sections by means of two opaque screens with holes just wide enough to permit the infants to pass, but too narrow for the mothers (hole diameter 10 cm). The two holes were situated near opposite corners of the middle section, which hampered looking from one end section into the other. The idea of the small holes was borrowed from the Primate Laboratory at Wisconsin (nuclear family apparatus; see Harlow (1971) and Suomi (1974)).

S-I was continuously maintained until the infants were aged 20 to 30 days in order to be certain of full acceptance within foster mother- infant pairs (however, no signs of unusual re- jection were noted). The weekly schedule sub- sequently became 3 days S-I (including the weekend), 2 days S-OO, and 2 days S-II. However, at the time that tetrads A and B were observed, S-OO had not yet been devised; S-I was maintained for 4 days and S-II for 3 days per week. Changes of situation were ac- complished by insertion or removal of screens at least 44 h before an observation session.

Recording Data were collected weekly during the first 4

weeks after birth, after which a tetrad was ob-

s_,[ S-If [

S-O0 Fig. 1. Diagram of the three experimental situations in which rhesus monkey tetrads were observed. The situations were established by providing appropriate parti- tions. After the infants had reached the ages of 20 to 30 days, tetrads were exposed to all three situations every week. The relative cage height was twice as tall as shown.

served every third week. However, situation changes were made each week. Data for the different situations were always collected during the same week. Recording sessions lasted for 10 000 s (2 h 47 min).

Each of two observers recorded the behaviour of the one mother-infant pair. The observers were seated at 1.5 m from the animals and were in full view of them. As long as the observers remained quietly seated and did not stare at their eyes, the monkeys rarely reacted directly to them.

The behaviour was recorded by using two keyboards, each with 32 keys. Each key corre- sponded with an act; when an act started, the corresponding key was depressed and held down until the act was terminated. Depressing and re- leasing a key each resulted in the recording of an 'event' consisting of the numerical code of the key and the time (in 0.1 s). Onsets were punched as key codes 0 to 63, terminations as 64 to 127. All keys could be operated independently (i.e. acts could be recorded simultaneously or partly overlapping in time).

Ethogram In this paper, the following recorded acts are

used: mother-infant body contact (as defined by Dienske & Metz 1977 and including on-nipple); off-mother; infant immobile (and then mostly sleeping on the mother); vocalization by infant; and the infant-infant play elements approach, flee, seizing, wrestling and quiet side-by-side body contact between infants. It was also recorded whether the mother or the infant initiated onsets and terminations of body contact.

Results A. Some Basic Data

1. Using play opportunity for playing. Two infants rarely interact if they are both on- mother. When one infant is off and its peer on- mother, their social play is restricted to approach, seizing and side-by-side contact. These relatively calm acts are mostly performed, however, when both infants are off-mother. The agile interactions, chasing (recorded as approach by one infant and flee by its peer) and wrestling, take place only if both infants are off their mothers. That play is shown primarily when both infants are off-mother implies that play opportunity is increased if the infants are off-mother simultaneously for longer. A possible increase in this will be studied by comparing 'simultaneously off ' in S-I with that in S-I[ and S-OO.

600 A N I M A L B E H A V I O U R , 29 , 2

In principle, infants might play for a larger propor t ion o f the time if they were only briefly off-mother simultaneously. This would reduce the usefulness o f our index o f play opportunity. Fortunately, infants did not behave in that way. Irrespective o f the duration of simultaneously off, infants on average played 30 % of that time with each other (Fig. 2 shows a linear relationship with a correlation coefficient o f + 0.83). Apparently, activities other than playing (e.g. walking and exploring) were not systematically reduced in favour o f play. This implies that infants are likely to play more if they increase the time in which they are simultaneously off.

20

&

-~ 10-

o age ~ 50 days

�9 age > 50 days

�9 o � 9 �9 o o o �9 �9

o � 9 �9 �9 � 9 o ~ o o o

o o

�9 . o

3'0 6'0

sTmuhaneously off-mother in S-l[ (per cent of time)

Fig. 2. Relationship between the time two infants are simultaneously off and social play in S-II. Each point represents an observation period. Pooled data from eight tetrads.

2. C h a n g e s w i t h a g e in a m o u n t o f ac t iv i ty , on- m o t h e r and play. For a proper quantification o f mother- infant body contact , it is necessary to distinguish between activity and rest (Dienske & Metz 1977; Simpson 1979; Dienske et al. 1980). Resting characteristically comprises im- mobility and sleeping. As we are here interested in play, which occurs mainly during off-mother, a resting phase was also considered to be the whole o f a continuous on-mother bout which included sleeping (see Fig. 3). During these on- mother bouts, an infant is relatively quiet and seldom plays. F rom this definition o f resting, it follows that an active phase lasts f rom the onset of the first off-mother bout following sleep until the end o f the last instance o f off-mother before the next sleeping phase.

The changes with age in the amount o f activity, on-mother during activity phases, and play, are shown in Fig. 4. Activity and on-mother are based on the data f rom S-I; the courses for the other two situations are essentially the same. Play is based on data f rom S-II (in S-OO, the course o f play lags one month behind because at least one infant has to leave its mother 's protection for play to be recorded).

Five developmental stages can be discerned, as follows. (I) A brief ' baby ' stage, lasting about one week, during which the infant is continuously on its mother. I t is no t 'active', according to our definition, a l though it does no t sleep all o f the time. That this phase is not so clear in Fig. 4 is due to individual variation in the dura- t ion of the 'baby ' stage. (2) A stage in which

restTng .

. . . . . . . . . i . . . . . . . . . . . . . . . i . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . i . . . . . . . . . . . . i . . . . . . i 1 i I : I n L . 2 : : i i', i n i t I I l l ,n i l ii I l l l l U l l l l l l l l l r , I ',um',tnnnluumn 3 : ! "" " l ' l g i l l I I m m l l l N i l ; I i I I I I 4

�9 . i i i ........ " ................... .................. " .......................... ~ .................. ................. 15 0 1

r e s t i n g

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . , . . . . . . ~ : . , , i ........... ', ........ , , i : : , . . . . . . . . . . ; ~ 2 mmmm i: i :: mn:.m ! , , :, t ::i: i3 nnamHm e m n u m l n ml i It1 i i I f : D I n i l l n l l l l l m l U l m 1 4

i i ! : ~ 5 7

2 observation time (hours)

Fig. 3. Resting (1 and 5), off-mother (2 and 4) and social play by infants (3) in two mother-infant pairs during 2 h of continuous observation. Data of 1 and 2 refer to one pair, those of 4 and 5 to the other; social play is that of one or both infants. Thick bars during resting denote closure of the infant's eyes. Vertically-interrupted bars correspond to more than one bout per 3 s. Ages: 108 and 112 days.

DE JONGE ET AL.: TIME BUDGETING BY RHESUS INFANTS 601

" I00 . ".z

a c q v e m~ m ~'~w -15 a

k . : , r . . . . . . . . . . . '".. 50 ,~o.,~, o . o . . . . . ~ : : . . . . . . . . . . o . . . . . . . , -~0 ~

o ~o .o ",,' t % _ o I ' "~-o, o ".

. . . . A- \ . l o f social p lay o - 5

' " on -mv the r "

3'0 6'0 9~ 1~0 150 I ~0 0

~ge (days)

Fig. 4. Development of activity (time interval between two resting phases with sleeping), on-mother (mother- infant body contact), and social play between infants, during the first half-year of age. Activity and on-mother are from S -- I, play from S -- IL Mean values of 16 pairs.

activity quickly increases and on-mother de- creases; this lasts, roughly, f rom days 7 to 40, (3) A stage with a marked increase in play, which comprises the second month. It is wor th noting that activity and off-mother, which are required for mos t playing, had already reached a fairly stable level at the start o f this stage. (4) A stage from months 3 to 5, during which behaviour levels are relatively constant. (5) A decrease in play in the sixth month, which may be associated with weaning.

The following analyses will be based on the fairly homogeneous stages (3), (4) and (5).

B. Differences in Body Contact Between the Experimental Situations

1. Rest-activity cycle. This cycle is analysed for the rather constant stage after day 30. All

infants were active during similar percentages of time in the various experimental situations (Table I ; U-test comparing between each pair o f situations: no significant difference between S-I and S-II, or S-I and S-OO). A trend across infants is also lacking; this was tested by combining the P-values per pair with Fisher 's method (see Cox & Hinkley 1974, page 80). This does not lead to significant differences S-I versus S-II :

i = N

z2(df = 2N = 32) = - - 2 ~ In P, = 25, P = 0.81 i = 1

and S-I versus S-OO: ;~2 (df= 24) = 15; P = 0.92. In addition, the durations o f completely observed activity or resting phases of an infant were also similar in different situations (U-test; NS). The same applies to cycle durations (active + next rest).

In summary, the presence o f a playmate does not influence the durations o f activity and rest by infants older than 30 days. Resting is a continuous bout o f mother- infant body contact ; since resting remains unchanged, it can be concluded that, at the level o f the rest-activity cycle, play does not take place at the expense o f mother- infant interaction.

2. Off-mother. The time spent off the mother is analysed for ages over 50 days. Off-mother by definition is restricted to periods o f activity and is therefore expressed as a percentage o f the activity time.

Table I. Percentage of Time Active in the Three Situations Given in Fig. 1. Means of at Least Six Observation Periods per Infant at Ages of Over 30 Days

Infant S-I S-II S-OO Sex of infant

A1 72 73 - - male 2 76 73 - - male

B1 67 67 - - male 2 70 69 - - male

C1 63 66 55 male 2 80 77 74 male

D1 64 67 68 female 2 78 70 75 female

E1 71 76 73 female 2 68 70 65 female

F1 62 71 56 male 2 69 66 70 male

G1 62 52 61 male 2 63 57 57 male

H1 60 64 65 female 2 73 75 79 female

Mean 68.6 68.3 66.7 SD 6.1 6.6 7.9

602 A N I M A L B E H A V I O U R , 29, 2

Most infants spent more time off-mother in S-II than in S-I (Fig. 5). The greatest increase was shown by those infants which remained for relatively short times off-mother in S-I: the regression line (calculated on the assumption that both variables are subject to errors with equal variances; see Sprent 1969) clearly passes the ordinate above the origin. This effect is not due to sampling errors, as the standard errors of the mean are small in relation to the scattering of the points. A similar but less pronounced effect was found for S-OO.

Apparently, most infants reduce body contact with mothers in favour of play. The infants with much body contact in S-I did so to a greater extent; these infants gained more play opportunity by decreasing body contact than did those who already spent much time off-mother in S-I.

One would expect that only for part of the time during which one infant is off-mother, will its playmate also be off-mother and thus available for agile play. So the gain in play opportunity will be relatively small unless they are able to synchronize body contact. This possibility will now be explored.

C. Synchronization of Body Contact 1. A measure for synchronization. Let Trr de-

note the proportion of the time that both infants rest simultaneously, Taa the proportion that both are active, Tra the proportion where infant 1 rests while infant 2 is active, and Tar the

'~176 I -- 90 B1 ~ "

80. D21 t2I

? 70 t 2

~ 1 + 2 ~ F~'E~ 50- Y = 0.7x .,'-~'H-1

o /

30 ./.f .. o 20 ~..,.,. / . , . t S

10 J ' • = x

~o I0 20 30 40 60 70 80 90 100

off (per cent of active) in S-I

Fig. 5. Relationship between the time off-mother in S-I and S-II (means and standard errors). Pair codes are given per point.

reverse case. The following proportions of time can then be defined:

A1 = Taa + Tar (infant 1 active); R1 = Trr + Tra (infant 1 rests); A2 = Taa + Tra (infant 2 active); and Re = Trr + Tar (infant 2 rests).

The product A1A2 gives the expected proportion of time that the two infants are simultaneously active under the null hypothesis of independent cycles; R1R2 gives the same for resting.

The coefficient r that specifies the synchrony of the cycles of the two infants can be computed as follows:

r = (Taa -- A1A2)/~/A1A2R1R~ = (Trr -- R1R2)/%/A1A2R1R2 ---= (TaaTrr - - TarTra)/"v/AIA2R1R2.

This specifies the difference from independent cycles scaled between + 1 (fully synchronized) and -- 1 (fully asynchronous) by the denomi- nator. The coefficient is zero if there is no synchronization. The value of + 1 can be realized only if the two infants not only rest completely simultaneously but also rest during exactly equal percentages of time (see Table II). This Table also gives the behaviour of the coefficient in other cases.

We will call r the synchronization coefficient (this can be interpreted as the cross-correlation at time lag zero of the activities of the two infants scored using a one-zero system).

2. Rest-activity cycle. Figure 6 shows the synchronization coefficients in the three experimental situations as a function of age. In S-I, the coefficient remains close to chance level (zero) during the first three months of age, after which a minor degree of synchronization seems to be apparent. Possibly, the older infants have learned to react to the time of the day or to stimuli such as sounds made by their invisible young partners.

In contrast, the synchronization of the rest- activity cycle in S-II is well-pronounced from the second month onwards. As S-I and S- I I observation sessions were only four days apart in each tetrad, one can confidently conclude that synchronization is a direct reaction to the presence of another pair. As the long body contact during resting (which precludes play) in S-II occurs more often simultaneously than in S-I, this synchronization favours play opportunity.

That synchronization is indeed connected with play is also indicated by the fact that there is no synchronization in the developmental stages be-


Table H. Some Values for the Synchronization Coefficient Obtained with Artificial Data

(Given as ~o of Observation Time)

Simultaneously Synchronization Infant 1 active Infant 2 active active coefficient

50 50 50 + 1.0 50 50 40 q- 0.6 50 50 30 q- 0.2 50 50 25 0.0 50 50 20 -- 0.2 50 50 10 -- 0.6 50 50 0 -- 1.0

50 50 50 + 1.0 50 40 40 + 0.8 50 30 30 -t- 0.7 50 20 20 -/- 0.5 50 10 10 q- 0.3 50 I 1 q- 0.1

10 10 10 q- 1.0 20 20 10 q- 0.4 30 30 10 q- 0.0 40 40 10 -- 0.3 50 50 10 -- 0.6 55 55 10 -- 0.8

fore play starts--i .e, before day 35; compare Fig. 6 (synchronization in S-II) with Fig. 4 (social play in S-II). Synchronization is already at a high level at day 50, when play is still increasing steeply.

There is also a conspicuous degree of synchronization in S-OO. I t develops more slowly than in S-II; this is probably due in part to the fact that infants rarely left their mother 's cages before day 60. This time of being out o f the mother 's reach gradually increased to a maxi- mum, which was reached at day 100. Synchroni- zation, however, develops earlier, as was found in S-II. In S-OO, synchronization continuously

v S- t [

._,- . - - / ' s oo ....

"~ . . . . / I " s-1

i o "m /

; J0 ~V----;7 . . . . S~; ...... % T .. . . 780 age (do/s)

Fig. 6. Development of the degree of synchronization of the active-rest cycle of the two pairs in a tetrad. Means of eight or six tetrads for 2-week periods.

improves. This may be due to each infant gradually learning to collect and use in- formation about the cycle of its peer. To establish whether its peer is resting when it is out o f sight, and infant must pass through the middle section and enter the section o f the other mother.

Activity synchronization is achieved without a change in the mean durations and s tandard errors o f the activity phases (see section B1 above). Phase durations vary enormously (see Dienske et al. 1980). Apparently, synchroniza- t ion is achieved by a rearrangement o f short and long phases.

3. Who is responsible for the synchronization of resting ? Prior to sleeping, the infant becomes more mother-oriented and less active; we called this period o f time the drowsy subphase (Dienske et al. 1980). I t usually takes some time before a mother reacts to the drowsiness o f her infant. During late drowsiness and early sleep, mothers often show a peak in grooming their infants. This may be followed by drowsy mothers nodd ing off. Al though such a mother becomes alert again before her infant does, she usually postpones walking until the infant starts moving its limbs after waking up. These qualita- tive observations indicate that, as a rule, the infants are responsible for the starting and ter- mination o f resting, and thus for rest synchronization.

604 A N I M A L B E H A V I O U R , 2 9 , 2

Probably more convincing evidence for the primary role of the infant in synchronization is the fact that a marked degree of synchronization is achieved in S-OO. In this situation, a mother is able to see the other infant only if she peeps through her hole during the short periods of time when the other infant is visible through the other opening. Consequently, she would be able to play only a minor role in synchronization. Infants, however, can move freely and this enables them to mimic each others' cycles successfully. We consistently noted that an infant soon returned to its mother through the two holes after discovering that its peer was resting.

Some mothers prevented or terminated resting by their infants relatively frequently. In principle, mothers could thereby increase synchronization. In reality, however, these maternal interferences decrease it: synchronization is negatively correlated with the percentage of maternal interferences with resting (Fig. 7). This holds true for the pooled data as well as for the set of observation periods of all separate tetrads.

Each infant in a tetrad was the first to start or terminate resting in an equal proportion of cases (binomial test, no significant differences)

+ I .00-

+0.75- o

.~_ + 0 . 5 0 .

u = +0.25- o

~ 0 -

Q i

- 0 , 2 5 .

D I r = -0 .57"

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E C c F C E

R

2~ 5~ 75 maternal interference with nappTng by infant

(per cent of onsets + termTnafion~ of nappTng)

Fig. 7. Correlation between maternal interference with napping (resting during daytime; Dienske et al. 1980) by the infant and the degree of activity synchronization in S-II. Interferences are (1) maternal preventions and terminations of on-nipple prior to resting, if they lead to numerous vocalizations, and (2) pushing the infant off- mother before the infant had awakened, if leading to many vocalizations. These interferences are summed for both mothers of a tetrad and expressed as a percentage of onsets plus terminations of napping by the two infants, per observation period. Letters correspond to tetrads. The plot shows that maternal interferences decrease synchronization.

This indicates that they both contribute to synchronization.

In conclusion, all evidence shows that the synchronization is due to the two monkey infants, who follow each other's rest-activity cycles. No positive maternal influence could be demonstrated.

4. Off-mother. The synchronization of off- mother was studied only for the third to the sixth month of age. The alternations between on- and off-mother are not homogeneously spread over the activity phase (Dienske at al. 1980). Off- mother bouts in the beginning of many activity phases are much longer than those just prior to sleep. For this reason, we split many activity phases into fully-awake and drowsy subphases. Just as the activity phases of two infants are synchronized, their subphases also tend to occur simultaneously. When we computed the synchronization coefficients over the entire activity phases, their values were larger than those for the separate subphases, because the infants' subphases with long (or short) off bouts tend to occur at the same time (see Fig. 3). These larger coefficients, however, were merely a by-product of the previously described synchronization of the entire cycle. To test for synchronization at the level of the on-off alternations during activity, we computed coefficients for 1000-s intervals that were clearly homogeneous with re- spect to on and off bout lengths (see Dienske et al. 1980, for the methods used to judge time homogeneity).

The results are given in Table III. In S-I, nearly all coefficients are slightly larger than zero. This is possibly due to occasional loud frightening sounds in the building, which immediately led to simultaneous mother-infant body contact in a tetrad. In S-II, coefficients are mostly larger than in S-I; this general difference is significant, using Fisher's method for combining P-values; P values under 0.05 are found for half of the tetrads. A similar positive positive synchronization is found for S-OO.

As in the case of the rest-activity cycle, one may ask who is responsible for off synchronization. Since older infants make and break most off-mother bouts, they contribute more to synchronization than do their mothers. Exactly how much the off-mother synchronization is due to mothers or infants has not yet been assessed. It may be estimated by using the parameters of a continuous time Markov chain (viz. transition tendencies) that suitably characterize the contributions of mother and infant to the transitions


Table HI. Synchronization of Off-Mother: Means of Synchronization Coefficients of at least 16 Intervals of 1000 s per Tetrad

Synchronization coefficient

Tetrad S-I S-II S-O0

P (U test, one tailed)

S-I S-I versus versus S-II S-OO

A -- 0.01 0.18 - - B 0.07 0.t2 - - C 0.05 0.01 0.06 D 0.07 0.17 0.14 E 0.10 0.08 0.08 F 0.02 0.22 0.18 G 0.09 0.08 0.08 H 0.10 0.21 0.16

Mean 0.06 0.13 0.12 SD 0.04 0.07 0.05

Combined P-values

0.00 0.21 0.88 0.36 0.02 0.05 0.64 0.72 0.00 0.00 0.67 0.79 0.00 0.20

z ~ = 44.7, z ~ = 27.7, P < 0.001 P < 0.01

between on-mother , on-nipple and off-mother (see Dienske & Metz 1977 and Dienske et al. 1980). It is no t yet known, however, whether the sequences remain Markovian in the case o f synchronizat ion o f off-mother.

D . The N e t I n c r e a s e in S i m u l t a n e o u s O f f - m o t h e r The observed change in simultaneous off f rom

S-I to S-II and S-OO is given in Table IV. An increase was found in nearly all cases, tetrad C in S-II being the exception.

Table IV also gives approximations o f the separate contributions o f each of the four potential ways by which simultaneous off may be increased. Such an increase would follow f rom: (1) an increase in activity time by one or both infants in a tetrad; (2) an increase in activity synchronizat ion; (3) an increase in the durat ion o f off-mother by one or both pairs or a tetrad; or (4) an increase in off-mother synchronization. To estimate the effect of only one of these sources o f increase, the real simultaneous off (Too) in a social situation (S-II or S-OO) is compared with an imaginary simultaneous off (T*oo) which would result if that measure remained at the same level as in S-I. I f Too -- T * o o > 0, then the observed change in the measure has induced a gain in simultaneous off-mother and thus in play opportunity. For this comparison, we use simultaneous off as a propor t ion o f the observation time (not o f the active time), because we presume that the absolute amount o f social play is the impor tant factor for social development.

The calculation o f the imaginary simultaneous off, T*oo, can be illustrated by showing how we estimate the effect o f activity synchronizat ion in one tetrad (that labelled A in Table I). For this purpose, we use the activity synchronizat ion (ra) of S-I and the active time (as a p ropor t ion o f the observation time, A1 and A2) o f S-II. The simultaneous active time, if ra remains at the same level as in S-I, can be computed by a t ransformation of the formula used for calcu- lating ra in section C I : T*a~ z A1A2 + r~

a/A1A2(1 - - A1) (1 - - A2). For the approxima- tion, we use the means per pair or te trad that correspond to those in Table I (A1 = 0.734; A2 = 0.727; S-II) and Fig. 6 (ra = 0.210; S-I). This results in T*aa-----0.575. This imaginary value is smaller than Taa (Taa = 0.671); this stands to reason, as activity synchronization in S-I (ra = + 0.210) is smaller than that in S-II (ra = + 0.700). This difference leads to a gain in simultaneous off expressed as a proport ion o f the observation time. The imaginary propor t ion o f simultaneous off, T*oo = Too T*a.a/Taa = 0.415 • 0.575/0.671 = 0.356. The gain is Too - - T*oo = 0.415 -- 0.356 ----- +0.059. This proport ion, expressed as a percentage, is given in Table IV.

The most accurate approach is to apply these calculations to each week o f observation and to give the average gain for all weeks. We chose a less cumbersome way, by working with averages o f the observation periods per pair o f a tetrad. To ensure a comparable approximat ion for

606 A N I M A L B E H A V I O U R , 2 9 , 2

}4

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r . ~

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0

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~ . 0 �9 r..r

o ~ c o ~

~6

-t- + + + + +-I- + q + + + [ + + +

§ + 1 + I § + I 1 § I

+ + I + + + + + + + + + + + + +

§ I + + + + + + + + + -I-

I 1 + 1 § 2 4 7 § I + l l l k I

+ § i + § 2 4 7 2 4 7 + + § 2 4 7 k § +

�9 9


both the imaginary and observed values, we computed Taa and Too (which were, of course, measured directly) in a way analogous to that for T*aa. The bias introduced by this easier approach is probably slight.

The estimations of the gains or losses due to the three other measures listed above and for S-OO proceeded analogously.

An alternative procedure is to use the S-II value of the parameter type considered and the S-I values of all of the other parameters. We were unable to develop a rationale for justifying a preference. Calculations using the alternative method resulted in values that differed only slightly from those given in Table IV.

As was to be expected from the results in Table I, the effect of a change in activity duration is negligible. This is due not only to the minute changes per pair but also because, in four tetrads, the increase in one pair is cancelled eut by a decrease in the other.

The separate effect of activity synchronization on simultaneous off, however, is nearly always positive; it amounts to a mean of 3 % for S -- II and 2 % for S -- OO. The additional increase in simultaneous off due to the concomitant synchronization of the fully awake subphases is not included in these figures.

The separate contribution of the increase in off-mother is on average the largest of the four potential mechanisms. In most tetrads, both pairs showed increased off-mother in the social situations (see section B2); consequently, most pairs gained play opportunity. In S-II, much of this effect is due to tetrads D and F, with little off-mother in S-I; tetrad G, however, failed to show an equally great improvement, the failure being due to the mother-infant pair G1 (see Fig. 5). In S-OO, tetrads D and H showed good improvement, but F and G increased off only a little.

The effect of the synchronization of off-mother is of minor importance.

It can be concluded that most pairs sacrificed a certain amount of mother-infant body contact in favour of play opportunity. This effect was greatest as a rule in pairs in which there was much contact when the infant was alone with the mother. In all but one case, the increase in simultaneous off-mother was accompanied by a synchronization of activity. These separate increases are independent of each other, but two or more enhance each other in total. The mutual enhancement of the four effects can be computed as [ ( G 1 G 2 G 3 G 4 ) - - 1] x I00, where G = 1 +

g/100 and g is the gain due to one of the four measures as given in Table iV. The mutual enhancement proved to be very small: the mean total for S-II becomes + 10.3 instead of + 10.0, and that for S-OO becomes + 7.7 instead of + 7.6. These corrected total averages are still smaller than the observed ones. This is probably due to the fact that active synchronization leads to synchronization of the fully awake subphases (with long off-bouts); therefore the total estimated gain is often less than the observed gain. This implies that the separate contribution of activity synchronization is probably larger than is given in Table IV.

Discussion The complexity of monkey life requires that an infant learns many skills. It also has to rest after exercising those skills. An infant must divide its time between various functional activities. This study has been concerned with daytime resting, which takes place on the mother, being on the mother during activity periods, and social play between infants. These classes of behaviour largely exclude each other in time and hence are potential competitors in the developing infant's time budget.

When a playmate was accessible, resting lasted as long as in the situation without a peer. This is easily understandable, as playing is more energetic than, for example, exploration of the environment, and so would be expected to pro- duce at least as great a requirement for resting. An increase of resting could be expected, but was not found.

A reduction in mother-infant body contact when active in favour of play was found in nearly all cases. This reduction was small in pairs with relatively little body contact. Great reductions were only found in those infants which had much contact with their mothers if separated from the other pair. These infants may have compensated for the lack of a peer by interacting very much more with their mothers during on-mother. In those pairs, reduction of contact may not be harmful to a good mother-infant relationship. However, the precise function of body contact during activity is not known, nor can one estimate how much of it is optimal. In nature, fre- quent body contact may favour proximity when the mother moves during foraging, but this possible function cannot be studied in small cages.

Play opportunity was also increased by the synchronization of activity phases and by pro-

608 A N I M A L B E H A V I O U R , 29 ; 2

longation of off-mother. Synchronization is a particularly effective way of increasing play without reducing mother-infant body contact. Syn- chronization of the rest-activity cycle is easy, as the peer's resting is clearly observable and long- lasting. That the synchronization of activity is connected with play is suggested by the fact that synchronization did not occur before play was deveIoped to a moderate degree. In S-OO, play as well as activity synchronization de- veloped about one month later than in S-II.

We regarded the connection between activity synchronization and play primarily as a functional one: when infants synchronize activity, they are able to play more. The causal mechanism of activity synchronization is a different topic. We examined many diagrams of the type given in Fig. 3. Most of them show a similar pattern to that in this Figure after the observation time of 1 h 35 min. At this point the infant represented in the top lines (1 and 2) started a drowsy subphase with little off-mother, connected with a marked decrease of play. The other infant (lines 4 and 5) did not become drowsy (it was off a great deal), but still began resting shortly after its peer had done so. As this was the usual pattern, we believe that infants react to the degree of activity of the peer when synchronizing: they rest earlier or later than expected on the basis of their own drowsiness. An alternative cause of synchronization could be that infants become tired of playing at about the same time. The example in Fig. 3, along with many similar cases, suggests that this is not likely.

Circadian and ultradian activity synchronization have also been reported in four 4-year- old rhesus monkeys that interacted visually and acoustically but were unable to touch each other (Yellin & Hauty 1971). The influence of social factors on biological rhythms is described for several species by Regal & Connolly (1980).

Synchronization of off-mother was less than that of activity. This can be understood from the much shorter duration of off-mother. More- over, off-mother occurs very unpredictably, because of the Markovian nature of the timing of the on-off alternations (Dienske & Metz 1977; Dienske et al. 1980).

On average, only 30 ~ of the time that the infants were simultaneously off was used for play. This suggests that other functional activities such as exploration are not reduced very much when opportunities for play are available.

Chance et al. (1977) found synchronization of 'nursing' in two mother-infant pairs of Macaca fascicularis that were housed together. They be- lieved that a distinction between 'nutritive and non-nutritive nu r s ing . . , is theoretically hazar- dous and operationally ambiguous'. However, we believe precisely the contrary, as Hinde & Spencer-Booth (1967), Dienske & Metz (1977) and Simpson (1979) observed that nursing (taking milk) is entirely restricted to the long resting phases and is absent in the short on- nipple bouts during activity. However, it is worth noting that Chance et al. (1977) reported that synchronization of very long nipple bouts was better than that of short ones. This confirms our findings, which were obtained after an a priori distinction between different levels of analysis.

Hinde & Spencer-Booth (1967) reported differences between rhesus mother-infant interactions in singly caged and group-housed pairs. As in our case, there was no difference in the sleeping time of older infants. In contrast to our findings, single infants spent more time off-mother than did those in groups. Hinde & Spencer-Booth attributed the shorter off times in groups to interference by group members, leading to maternal restriction. This plausible explanation seems not to be applicable to our situations with only two adults. Our mothers remained very peaceful in comparison with those in larger groups. In fact, in most tetrads, we did not observe the usual aggressive signs of dominance. Only two mothers could be regarded as restrictive. This explains why nearly all of our infants were allowed to increase off-mother in the situations with another mother-infant pair.

Most mothers rarely interrupted the (only mildly aggressive) play of their infants. We were also unable to find indications that mothers promoted play opportunity. Play opportunities were mainly increased by the two infants adopt- ing each other's state of activity and by pro- longation of off-mother. However, mothers that often prevented or terminated resting exerted an adverse influence on the synchronization of the rest-activity cycle. None of the measures studied was systematically influenced by the sex of the infants (see Figs 5 and 7, and Tables I, III and IV).

We can conclude that part of the opportunity for play on the days when the social situations were monitored arose as a result of a decrease in mother-infant body contact. Play opportunity was further increased by a synchronization of the activity phases of the two infants, independently


of changes in mo the r - in fan t body contact. Tha t infants possess this very effective mechanism for increasing play oppor tuni ty is in agreement with the opinion (e.g. Poirier et al. 1978) that social play is an indispensible exercise for later social skills.

Acknowledgments We are grateful to J. A. J. Metz for methodo- logical advice, C. Goosen and Dr A. C. Ford for comments on the manuscript , Ms D. van der Velden for typing the text and M. J. van der Vaart for the prepara t ion of the Figures. The investigations were supported in par t by the F o u n d a t i o n for Fundamen ta l Biological Re- search (BION), which is subsidized by the Netherlands Organizat ion for the Advancement of Pure Research (ZWO).

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Dienske, H., Metz, J. A. J., Luxemburg, E. -A. van & Jonge, G. de. 1980. Mother-infant body contact in macaques. II. Further steps towards a repre- sentation as a continuous time Markov chain. Biol. Behav., 5, 61-94.

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Hinde, R. A. & Simpson, M. J. A. 1975. Qualities of mother-infant relationships in monkeys. In: Parent-infant Interaction. CIBA Foundation 33 (Ed. by R. Porter & M. O'Connor), pp. 39-67. Amsterdam: Elsevier.

Hinde, R. A. & Spencer-Booth, Y. 1967. The effect of social companions on mother-infant relations in rhesus monkeys. In: Primate Ethology (Ed. by D. Morris), pp. 267-286. London: Weidenfeld & Nicholson.

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in nuclear family environment versus monkeys reared with mothers and peers. Primates, 15, 311- 320.

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(Received 2 April 1980; revised 26 July 1980; MS. number: 1999)

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How rhesus monkey infants budget their time between mothers and peers