Anim. Behav., 19X,23, 527-542

SOME

FACTORS

AFFECTING

MOTHER-INFANT

RHESUS BY L. E. WHITE

M.R.C.

RELATIONS

IN

MONKEYS & R. A. HINDE*

Unit on the Development and Integration

of Behaviour, Madingley,

Cambridge

Abstract. The effects of six independent variables on rhesus mother-infant relations are examined by comparing subgroups of mother-infant pairs differing in only one of the variables. Variables compared and discussed include mother’s parity, previous experience and social status, sex of the infant and the presence of peers. All variables except maternal parity appeared to affect the relationship, but none produced effects that were wholly consistent over all comparisons. Further tentative analyses were made of some age effects and interactions between variables which may have accounted for the inconsistencies.

When rhesus monkey infants are reared by their mothers in small social groups in the laboratory, dramatic variations in the motherinfant relationships are to be seen. For example, in observations during the morning hours on this colony the number of half minutes in which lo-week-old infants were off their mothers has varied from 15 to 78 per cent of those in which observations were made. Such differences in mother-infant interaction might have considerable consequences for later development. The sources of these differences are not easy to track down. Among those that have been suggested are the sex of the infant, maternal parity, maternal social status, and the early experience of the mother (see Discussion). One obvious course is to compare groups of mother-infant pairs differing in only one of these variables, bearing in mind that there may be yet other variables whose importance is not yet recognized: since the importance of each variable may change with age, it would of course be necessary to analyse the data separately for each age range. Only rarely, however, has it been possible to achieve group sizes adequate to permit generalizations from such studies (see Discussion). Furthermore, there is a strong possibility that the several variables may interact : for instance maternal care might differ with some aspect of the mothers’ early experience in subordinate but not in dominant mothers. With species of almost unlimited availability, like rats, the importance of such interactions could be assessed by an analysis of variance (e.g. Denenberg 1970), but it is hardly feasible to

obtain monkey subjects with characteristics to fit all the sub-groups that such an analysis would require. Faute de mieux, it is necessary to use the material that is available. In this paper data rhesus collected on captive group-living monkeys have been used in an attempt to assess the importance of each of a number of variables by comparing mother-infant pairs equated for the others. Since for each variable (e.g. sex of infant) it was possible to make a number of comparisons in which the other variables (e.g. maternal parity) were equated within each comparison, but differed between comparisons, some indications of interaction could be obtained. Where differences in the mother-infant relationship are found, it is important to determine whether they are due more immediately to differences between the mothers or to differences between the infants. Thus if one found that male infants spent less time off their mothers than females, this could be because males sought contact with their mothers more than females, or because mothers rejected females more than they did males. This problem has been approached by looking not merely at the measures of mother-infant interactions themselves, but at the relations between measures. For instance, if male infants were off their mothers more than female infants, and also received more maternal rejections than females, their greater time off could be due mainly to a difference between the ways in which mothers respond to male and female infants. If, however, male infants were rejected less than female infants, the greater time off would be due mainly to an immediate difference between males and females. Of course, any difference in either party is likely to produce complex consequences for the

*Present address of both authors: Medical Research Council Unit on the Development and Integration of Behaviour, Madingley, Cambridge, CB3 8AA. 521

528

ANIMAL

BEHAVIOUR,

relationship, but this type of approach can provide a first stage in their analysis (Hinde 1969). Methods The animals (sources specified below) lived in groups each consisting of a male, two to four females, and their young. Each group occupied an outside pen (5.40 x 240 x 240 m) communicating with an inside room (1.80 x 1 a35 x 2.25 m). Data were collected on check-sheets divided into half-minute periods (see Hinde 1974, Fig. 1). Observations were made between 09.00 and 13.00 hours, and each pair was watched for 6 hr a week, every other week, or every fourth week. Most of the infants were used for experiments in week 30, and in some cases earlier: this analysis includes all data to week 28. All data for each pair for each fortnight (weeks 1 and 2, 3 and 4, etc.) were pooled, but due to the varied observation schedules employed, data were not available for every pair for every fortnight. The number of pairs available for comparison in any fortnight was thus often less than the number given below (see Table I). The dependent variables used were as follows : (i) Time off i.e. the number of half-minutes in which the infant was off its mother, expressed as a percentage of the number watched. (ii) The absolute frequency of rejections (R) i.e. the number of times the mother rejected its infant’s attempts to make ventro-ventral or nipple contact, expressed as the number per 100 half-minutes. (iii) The relative frequency of rejections [R/(&&,, + Mki + R)] i.e. the ratio of the times the infant was rejected (R) to the total number of times it gained ventro-ventral or nipple contact on its own (&UC,) or its mother’s (M/C,) initiative, or attempted unsuccessfully to gain contact (R). (iv) Maternal initiative in ventro-ventral contacts 100 M/& or %MkM i Mk, + Mk, 1 i.e. the number of ventro-ventral contacts initiated by the mother (Mk,) expressed as a percentage of the total number initiated by mother or infant (Mk,). (v) Infant’s role in ventro-ventral contact (%Mk, - Qk,) i.e. the difference between

23,

3

the percentage of contacts initiated by the infant [lo0 Mk,/(Mk, + Mk,)] and the percentage terminated by him [IO0 Bk,/(Bk, + Ilk,)]. This provides an index of the relative role of the infant in determining the amount of ventroventral contact (Hinde & White 1974). Data for this measure were recorded only for the more recently studied infants. (vi) Restrains i.e. the number of half-minutes/ 100 half-minutes in which the mother physically restrained the infant from going more than 60 cm from her. Data on this measure were incomplete for many dyads. (vii) Time at a distance (> 60 cm) i.e. the number of half-minutes in which the infant was recorded more than 60 cm from its mother, expressed as a percentage of the time the infant was off. (viii) Infant’s role in maintaining proximity to its mother when off her (%Ap, - YJ,) i.e. the percentage of approaches (motherinfant distance decreases from > 60 cm to < 60 cm) due to the infant [lo0 &/(Ap, + A&l minus the percentage of leavings (distance mcreases) due to the infant [ 100 L&i + &,)I. In each set of comparisons given in the Results, data on time off are considered first, and then data on measures (ii) to (vi) are used to assess whether any differences in time off were due primarily to differences between mothers or differences between infants (see Introduction). Then data on the time the infant spent at a distance from its mother are considered. Finally the measure of the infants’ role in maintaining proximity is used to assess responsibility for differences in the time spent at a distance from the mother. The data were based on sixty-three motherinfant dyads. They were classified in terms of the following characters: (i) Sex of infant. (ii) Source of mother (i.e. colony-bred or alien: the original sources of most of the alien animals were not known). (iii) Parity of mother (i.e. primiparous or multiparous). (iv) Number of infants previously borne by mother in colony. Introduced animals which had bred previously were divided into those having their first, or their second or later, infant in the colony. (v) Dominance status of mother. Assessments for infants born between March 1969 and November 1970 were based on a detailed study by Richards (1972). In other cases qualitative notes, but no quantitative data, were available. The mothers were classed as dominant (i.e. dominant to all other animals in the pen except

WHITE

& HINDE:

MOTHER-INFANT

RELATIONS

IN MONKEYS

529

Table L Number of Mother-hfant Pairs In Each S&-group* Mother: colony-bred (c)

Mother: alien (A)

Parity of mother Sex of infant

status of mother Dominant

Subordinate

3

Female (9)

2

(S)

Intermediate (I)

I Subordinate (S)

Primip. (P)

Previous infant in colony (X2.)

1

1

3

I

2

6+1

3

2 -I- 1

6

1

2

0+1

4+1

2+2

3+2

7

2

1

Dominant@) 1

Multip. (X)

(D)

Intermediate (I)

Male ($)

Primip. (P)

First infant in colony (Xl)

2

1

*Where two figures are given, the first indicates the number for whom peers were available, and the second the number for whom peers were not available (lo). Where only one figure is given, peers were available. The subgroups are referred to in subsequent tables by the initials given in parentheses.

for the alpha male), subordinate (subordinate to all other adults) or intermediate. (vi) Presence of potential playmates. For present purposes another individual less than 2 years old when the infant was born was classed as a potential playmate. The number of infants available in each of these categories are shown in Table I. For ease of reference, each sub-group in Table I is referred to in subsequent tables by the initials given in Table I: thus CIJP refers to colony-born mothers of intermediate status having a male infant when primiparous. Analysis of Data The relations between the independent variables (categories of mother-infant dyads) and the measures of mother-infant interaction were assessed as follows. Pairs of sub-groups differing only in the factor in question were selected from Table I. For instance, for parity the following pairs of sub-groups were selected: CIJP versus CI$X; CI$!P versus C&)X; CI?P/O versus CI?X/O; CS?P versus CSYX; ADJP versus ADSXr ; AISP versus AIJX r ; ASdP versus ASJX r. No pairs were available for comparison for female infants of alien mothers, since for no maternal status were infants available in both primiparous and multiparous (first infant in colony) categories. It will be seen that this method involved sub-groups containing very few individuals, often as few as one, and that

this was partially compensated by the availability of several pairs of sub-groups for each variable. For each independent variable, three types of comparison were then possible : (i) Within each pair of sub-groups, each fortnight could be treated as providing independent assessments of the behaviour of the subjects in those sub-groups. A matched pairs sign test could then be used to assesswhether the number of fortnights in which the median was higher for one sub-group was greater than could be accounted for by chance. This has two disadvantages. First, since the same individuals are involved, the test permits conclusions only about the particular sets of individuals involved. These are more likely to be representative of the population as a whole, the larger the subgroup. Second, there could be an interaction with age, the independent variable being associated with a difference between the sub-groups over one age span but not over another. (ii) Differences between sub-groups could be assessedseparately for each fortnight by a MannWhitney U-test (one-tailed). In most cases the number of dyads in each sub-group was too small for this to be possible, the more so since data were not available for every dyad for every fortnight. (iii) Since, for each independent variable, a number of pairs of sub-groups are available for comparison, matched pairs tests could be used for the different pairs of sub-groups in each

ANIMAL

530

BEHAVIOUR,

fortnight. Here there is a danger of interaction with factors other than age: for instance, a given independent variable might affect a measure of mother-infant interaction in males but not in females. However, the comparisons are independent, since each pair involves different groups of monkeys. Since the number of pairs available for comparison was sometimes small, indications of consistency between comparisons, even though not reaching statistical significance, have been given in the tables. In what follows, the results of statistical tests must be viewed in the light of the above discussion. Results Effects of Parity Data. Table I shows that comparisons were possible for seven pairs of sub-groups. The number of dyads available was small in all cases, the most substantial ones involving four with two (CI$JP : CIYX) and three with two (ASJP : ASdXi) mother-infant pairs. In no case could significance have been reached in comparisons of individual fortnights. The differences are summarized in Table II. Time off. In four of the seven comparisons, primipares’ infants were off less than otherwise comparable multipares’ in the majority of fortnights, though in no case was the difference

23,

3

significant. In two comparisons the opposite was the case, in one the difference reaching significance. One comparison was equivocal. Within fortnight comparisons indicated that the offspring of primipares tended to be off less in the early weeks and more later, but in no fortnight were all differences between subgroups consistent in direction. Relative roles in determining differences in time off. No data were available for one of the comparisons. In the others, they were in general consistent with the view that the differences in time off were primarily due to differences between mothers. Thus where the primipares’ infants were usually off less than the multipares’, they also were usually rejected less and had a higher proportion of ventro-ventral contacts initiated by their mothers. Where the primipares’ infants were usually off more, the reverse was the case. The sub-group comparisons were most consistent in showing that primipares’ infants were rejected most over approximately the same age range as when they were off most. > 60 cm. Of the four comparisons in which primipares’ infants were off their mothers less, in two they went to a distance from her significantly less often. In the other two the comparison was equivocal. In the sub-group pair that had yielded equivocal comparisons for time off, the primipares’ infants went to a

(A) PrhllipWOlW with (B) Multipanrus Mothers

Table II. Coagarhg

For each pair of sub-groups: No. of fortnights median A > median B No. of fortnightly comparisons CIdP: CIaX

CIQP: CIQX

Time off

4111

7110

l/5

218

R

1/9*

519

114

O/8**

519

519

214

218

619

s/11

315

418

114

217

114

Sub-groups compared

R/(Mkl

f Mk,

% Mkr-

%Bkr

+ R)

CIQP/O: CSQP: CIQX/O CSQX

6110

ADGP: ADdXl 6112

AIc?P: AIdXl

AS$Xr

AWP:

8/9*+ 9/g+*

A>B

B>A

6113

14, 18,22

2, 4, 6

319

14

8/9*

7112

10, 14, 18

l/P*

6112

Restrains

417

317

> @cm

l/lo*+

10/11** 214

215 316

2/12*

519

2/12+*

318

7110

516

t/9*

719

8111

% API-

%LI

*Difference significant at P < 0.05 ondaikd

113

sign test; **P < 0925.

Fortnights in which 414,415, 516, 616, 617 or 7/7 differences were in the same direction

26

WHITE

& HINDE:

MOTHER-INFANT

distance less often. In the two pairs in which the primpares’ infants were off more than comparable multipares’ infants they also went to a distance from their mothers more. Roles in maintenance of proximity. The results of these comparisons are difficult to interpret. In these comparisons the sub-group in which the infants went to a distance from their mothers more, also tended to have higher scores for the infant’s role in maintaining proximity. This suggests that the differences are due to differences between mothers. However, in one other comparison in which primipares’ infants were away from their mothers less, the infant’s role in maintaining proximity was marginally greater than comparable multipares’ infants. Discussion. These data do not reveal any important differences between mother-infant relations between dyads in which the mothers were primiparous and those in which they were multiparous. Such differences as there were between the groups compared seem to have been due primarily to differences between mothers. The absence of any major differences is in harmony with the findings of Seay (1966). His data were based on monkeys living in a Wisconsin playpen apparatus (e.g. Hansen 1966). The mother-infant dyads lived separately, but for two daily, hour-long sessions each infant could interact with another infant in a play area. Access to this play area was through a hole large enough for the infants to go freely to and fro, but too small for the mothers to follow. Seay did find that primiparous mothers ‘retrieval grimaced’ more and showed fewer infant-directed presents, than the multipares. These gestures are not often seen in our colony, and may be a result of the filter restricting the mother’s access to the infant in the Wisconsin apparatus. Seay points out that the ‘grimace’ resembles the ‘fear grin’ (Hinde & Rowe11 1962): the difference may therefore represent greater insecurity on the part of the primipares. Seay also found a higher frequency of negative maternal responses (i.e. rejections, etc.) in the multipares. Although this and other studies cited by Seay failed to reveal any large differences, one must concur with Seay’s view that these studies do not indicate that such differences do not exist. Studies involving larger but still comparable groups would be of great interest. Effect of Source of Mother Data. Table I shows that comparisons

of

RELATIONS

IN MONKEYS

531

colony-bred with otherwise equivalent subgroups of introduced mothers are possible in six cases (colony-bred multipares are here compared with introduced multipares having their second or later infant in the colony). The most substantial comparisons involve four with three (CIQP : AI?,) and two with seven (CIQX : AI?Xz) mother-infant pairs, both of which could yield significant differences in individual fortnights. The differences are summarized in Table III. Time off. In all comparisons infants of colonyborn mothers were off less than those of introduced mothers in most fortnights, three of the differences being significant. Mann-Whitney tests of differences in particular fortnights within pairs of sub-groups were equivocal, but there were two fortnights in which, for the five sub-groups for which data were then available, the differences were all in the same direction. Inspection of the data suggested that the differences were most marked in the 12 to 20 week age range, the infants of colony-bred mothers continuing to spend a considerable time on their mothers when the infants of introduced mothers were becoming more independent. Relative roles in determining differences in time off. Data were available for only five of the six comparisons. In two of these, colony-born mothers rejected their infants less than introduced mothers in most fortnights, and initiated a higher proportion of ventro-ventral contacts. This indicates that the difference in time off was due more to differences between the mothers, the colony-born mothers rejecting less and initiating contact relatively more. In the other three cases the proportion of ventro-ventral contacts initiated by the mothers again tended to be higher in the colony-born sub-groups (significant in one case, marginal in the others), but the differences in rejection scores were complex. In all three of these cases comparisons of the overall frequency of rejections yielded a marginally greater number of comparisons in which colony-bred mothers rejected their infants more than introduced mothers, but in each case the difference was in the opposite direction in the early weeks. Furthermore, in two of these cases the relative frequency of rejections tended to be lower in the colony-bred mothers. A possible explanation is given below. Within-fortnight comparisons (Table III) indicated that in those comparisons in which

CIJX:

%

Lr

317

1/g**

8/9*

5110

317

For * and ** see.Table II. tP < 0.05 Mann-Whitney U-test, one-tailed.

% API -

>6Ocm

Restrains

%Mkr

419

5110

10*+/10

- % Bkl

219

R/(Mk, + MkM + R) O/9*+

% Mb

519

O/8**

R

5/11

&TX2

1/10**

cI$P: AW

Time off

sub-groups compared

6113

10*/13

3110

10**/11

2/11*

1/13**

6114

CI?P: AWP

314

0/5*

3%

CS?X:

O/6** O/6+

4110

516

217

517

217

617

o/7**

ASOX

16

496

A>B 14

B>A

6, 10, 14, 18*, 22*

A>B

18

6, IO*, 14

6, 10

2,8, 10. 14,* t8*,26

B>A

Fortnights in which 414, 415, 5151, 516 or 6/6 differences were in the same direction

Mothers

For all sub-groups fortnights for which difference is signiflcant~

Mothers with (B) Introduced

218

10**/11

6/8

w

3/11

AI?X2

c1px:

No. of fortnights median A > median B No. of fortnightly comparisons

For each pair of sub-groups:

Table III. Comparing (A) Colony-Born

WHITE

& HINDE:

MOTHER-INFANT

colony-bred mothers rejected their infants less, the differences were most marked in weeks 6 to 19,. and overall the differences in maternal initiative in ventro-ventral contact were most marked in weeks 14 to 22. It is over this age range that the frequency of rejections first increases markedly and the proportion of ventroventral contacts initiated by the mother decreases. In other words the colony-bred mothers did not start to reject their infants as soon, and continued to exercise initiative in nipple contacts until later, than did the introduced mothers. Similar tendencies could account for higher absolute rejection scores of some of the colonybred mothers in the later weeks, for an infant whose mother increased her frequency of rejections late could require a higher absolute frequency at a given age than one who had grown more accustomed to rejections. > 60 cm. In two of the comparisons infants of colony-born mothers went to a distance from their mothers less than infants of introduced mothers in a significant majority of fortnights, and in one case the difference was significant in the opposite direction. The other comparisons were equivocal. Roles in maintenance of proximity. Differences in the infants’ role in maintaining proximity tended to be in the same direction as differences in time spent at a distance, suggesting that the latter reflected differences between mothers. Table IV. Comparing (A) Mdtipares

RELATIONS

IN MONKEYS

533

Discussion. The clear tendency for infants of colony-bred mothers to be off less appeared to be due to a later increase in the rejecting behaviour of their mothers, and a later decrease in the mothers’ initiative in ventro-ventral contacts. The differences in time at a distance were equivocal. Most colony-bred mothers were living in a group with their own mothers and/or siblings, and it may be that they had less need to be concerned with their own social relations, and thus more time for their infants, than introduced mothers. Effect of Number of Infants Mother Has Borne in the Colony Data. We are concerned here with the four comparisons between mothers having their first infant in the colony and mothers having their second or later infant in the colony. The most substantial comparisons involved two with six (AIdXt : AIGX2 and AS&Xi : A&3X2) mother-infant pairs, which could yield significant differences in individual fortnights. The differences are summarized in Table IV. Time off. All four comparisons suggested a tendency for first infants born to mothers in the colony to be off less than later ones : in two cases, involving subordinate sub-groups, the differences were significant, but in the other two, involving

Having First Infant in Pen with (B) Multipares Having Later Infant in Pen For each pair of subgroups :

No. of fortnights median A > median B No. of fortnightly comparisons Sub-groups compared Time off R

R/(Mk,

+ MkM + R)

% Mb., %Mk,

- %Bk,

Restrains >6Ocm %API

-

%LI

ADdX1:

AIGX1:

ASdXl

AS?Xi:

ADm2

ATd’x2

ASdX2

ASEX2

6/13

3/10

3/13*

o/7**

9113

l/lo+*

6/11

315

S/13

3/10

3112

l/4

1/13**

9/11*

13/13**

6/6**

S/14

218

l/8*

l/7

2/10

318

12/13*

416

10/14

7110

3112

o/7**

S/12

s/10

1/13**

l/5

For *, ** and t see Tables II and III.

Fortnights in which For all subgroups : sub-group comparisons fortnights for which yielded four differences difference is significantt in the same direction A>B

B>A

A>B

B>A 18

10, 14, 18

22

6, 10, 18.22 2,22

6,10 10, 18,22

534

ANIMAL

BEHAVIOUR,

dominant or intermediate sub-groups, they were only marginal. Relative roles in determining differences in time off. In three of the four cases the multipares having their first infant in the pen tended to reject their infants less often or on a smaller proportion of occasions, to restrain their babies more (two only), to initiate a higher proportion of ventro-ventral contacts (three significant), and to play the major role in ventro-ventral contact (i.e. %Mk, - %Bk, lower; one difference significant). All these correlations suggest that the shorter time that first infants spent off their mothers as compared with later infants was mainly a consequence of differences between the mothers. In the fourth case, one of the two in which the tendency for the first infant to be off less was only marginal, and the only one involving dominant sub-groups, all relationships tended to be in the opposite direction, i.e. the first infant tended to be rejected more, the mother to initiate a smaller proportion of contacts (difference significant), and to play a smaller role in ventro-ventral contacts. Although this comparison involved only 1 : 3 dyads, and most of the differences were marginal, the trends suggest that the difference between mothers who have and have not had an infant in the colony before varies with their dominance status. > 60 cm. In the two comparisons involving subordinate mothers, the first infants were not only off their mothers less in most fortnights, they also went to a distance from them less (one difference significant). In the two comparisons involving dominant or intermediate mothers the first infants tended to go to a distance from their mothers more than later infants. Roles in maintenance of proximity. In the two comparisons in which first infants went to a distance from their mothers less than later infants, the infant’s role in the maintenance of proximity tended to be less (one difference significant), i.e. the difference in time at a distance was primarily due to differences between mothers. In one of the other two cases the data were also compatible with the hypothesis that differences in time at a distance were due more to differences between mothers. Discussion. The overall trend, clear in two of the four comparisons, and detectable in a third, was for infants of multipares having their first infants in the colony to be off and at a distance

23,

3

from their mothers less than later infants. The differences were primarily due to differences between mothers, because for first infants the increase in maternal rejections came later and they were taken on by the mother more than later infants. These conclusions are based on comparisons between intermediate or subordinate sub-groups. In the fourth comparison, which involved dominant sub-groups, there were no clear differences in time off or time at a distance, and the differences in other measures tended to be equivocal or in the opposite direction. The explanation of these differences may lie in the behaviour of other females in the group to the infants. Such females covet young infants, and their attentions are resented by mothers. Subordinate mothers can protect their babies only by restricting their movements (Rowell, Hinde & Spencer-Booth 1964). At first subordinate females may also be unsure of the behaviour of the adult male in the group; by the time they have had two or more infants in the group they may be better able to predict his behaviour. Thus it is suggested that multipares having their first infant in the colony tend, if of intermediate or subordinate status, to be less secure than otherwise comparable mothers having later babies, and need to protect their babies by being restrictive. In dominant mothers this does not arise. Effect of Dominance Data. Table I shows that (a) four comparisons are possible between dominant and subordinate sub-groups, one involving three with six pairs (ADJX2 : ASJX2); (b) five are possible between dominant and intermediate sub-groups, one involving three with six pairs (AD$Xa : AI?JXz); and (c) six are possible between intermediate and subordinate sub-groups, one involving six with six pairs (AIGX2 : AS$Xz). The differences are summarized in Tables V, VI and VII. Time off. In two of the four comparisons between dominant and subordinate sub-groups offspring of dominant mothers were off more than those of subordinate mothers in significantly more fortnights than vice versa: the other two comparisons, one of which involved a substantial number of pairs, were equivocal. The four comparisons were, however, consistent in the 14 to 18-week period. Comparisons between the offspring of dominant and intermediate mothers were equivocal. Two (including

WHITE

& HINDE:

MOTHER-INFANT

RELATIONS

IN MONKEYS

535

Table V. Comparing (A) Dominant w&b (B) Subordinate Mothers For each pair of subgroups: No. of fortnights median A > median B No. of fortnightly comparisons Sub-groups compared

CD$‘X: csox

I$F

Time off

13/13**

11/12*+

R + MkM + RI

9; ML, %Mk,

A%Xl

ASJX2

A>B

6/13

8114

2

1/12**

R/(Mk,

- %5k,

Fortnights in which 3/3 or 414 differences were in the same direction

B>A

A>B

B>A

14,16, 18

8113

6.12

12

20

6/12

11/13**

9114

12,24,28

20

3/13*

1/14**

11/14**

719

11/14*

13/13*+

Restrains

AD$X2:

ADGX1:

For all subgroups: fortnights for which difference is signiticant~

6/13

>6Ocm

13/13**

%AP, - %L*

12/12**

20 4,6,10,

18,22,28

o/12*+

9/11*

9/11*

6114

12,14

11/12*

8113

16, 18,20,22

11/12++

For *, ** and t see Tables II and III. Table VI. Comparing (A) Dominant with (B) Intermediate Mothers For each pair of sub-groups : For all sub-groups : fortnights for which difference is significantt

No. of fortnights median A > median B No. of fortnightly comparisons Sub-groups compared

CD?X: CIPX

Time off

10/11**

yux;l:

AD;22

g&P:

%+:I 1/9**

2

5/10

11/14*

1/12**

A>B

B>A

22

10

Fortnights in which 3/3,4/S or 515 differences were in the same direction A>B

B>A 10

R

3/11

719

2/12**

8, 12

R/(Mk, + Mkb, + R)

3/11

719

6112

8, 12

% Mb,

4/10

lo/lo**

10/12

4

516

9114

l/7

5/10

5/11

8114

7/10

8112

%Mk,

- %%

Restrains

7110

> 6Ocm

9/11+

%AP, - %L,

6/10

O/8**

10 o/14**

4,6,8,26

For *, **, and t see Tables II and III.

the three with six comparison) gave dominant mothers off in significantly more fortnights, the two involving primipares gave them off in significantly fewer, and one was equivocal. Offspring of intermediate mothers tended to be off more in more fortnights than those of sub-

ordinate mothers (three out of six comparisons significant, though the most substantial comparison was equivocal), and there were several weeks in which all groups showed considerable consistency. The finding of clearer differences between intermediates and subordinates than

318

%AP,

619

619

For * , **, t see Tables II and III.

%L,

8/8**

>6Ocm

-

l/7

Restrains

--k,

419

8/9**

%Mk,

%

4/l 1

1/9**

% Mk,

517

9/9*+

1/9**

8/9**

+ R

8/10

+ Mk,

718’

RIMkr

8/9**

5/10

l/8’

R

AIdP: ASJP 10/10**

CI$?X: csg2x

9/11*

8/g**

CI?P: CSOP

8113 2/12**

11/11** 10/11** O/6*

l/7

315

W3

2/12

316

9/14

618

317

317

517

217

AIOX2: ASPX2

4113

9113

10/12**

6113

AI$X2: ASdXz

6

12

12

A>B

20

B>A

For all sub-groups : fortnights for which difference is significant7

witb (B) Subordinate Mothers

3/11

5/11

4/11

9112

AIJX1: A&3X I

No. of fortnights median A > median B No. of fortnightly comparisons

Time off

Sub-groups compared

(A) Intermediate

For each pair of sub-groups :

Table VII. Comparbg

22

lo**, 12

8

6, 8*, 22

lo,26

6,8*,

6, 8*, 12, 22

8,14**,

A>B

14

6

6**

918 lo** f 22**

B>A

Fortnights in which 414, 4/S 516 or 616 differences were in the same direction

WHITE

& HINDE:

MOTHER-INFANT

between dominants and intermediates suggests that the dominant/subordinate difference is a peculiarity of the latter rather than the former. Relative roles in determining differences in time off. Data were available for only three of the dominant versus subordinate comparisons. In all three the infants of the dominant mothers played the greater role in ventro-ventral contacts in the majority of fortnights (difference significant in two), the difference being consistent for all comparisons in six fortnights spread through the period. At 12 weeks all three comparisons indicated more rejections in the dominant mother group. These findings indicate that the differences in time off at that age were due mainly to differences between mothers. However, only one of the comparisons gave similar data throughout the period: here the dominant group showed a lower frequency of restraining and a higher absolute and relative frequency of rejections in most fortnights. In another comparison, although the infants’ relative role in ventro-ventral contact was again usually higher in the dominant group, the frequency of rejections was lower. Such a finding, that one mother both initiated ventroventral contacts and rejected them less than the other, could be described by saying that she exercised less control. In the third dominant versus subordinate mother comparison there was no consistent difference in the time the infant spent off its mother, but the dominant mother tended to initiate a higher proportion of nipple contacts, restrain her baby more often, but play a smaller role in determining ventro-ventral contacts. Adequate data are available for only three of the comparisons between dominant and intermediate mothers. Only one difference was significant, and clear trends again hard to specify. In the intermediate versus subordinate comparisons, clear trends were more apparent. In all six cases the proportion of ventro-ventral contacts initiated by the mother tended to be lower for the intermediate status mothers in the majority of fortnights (difference significant in two cases). In three of the four cases for which data are available the infants’ role in ventroventral contact was higher with the intermediate mothers in the majority of fortnights (significant in one comparison). In most, but not all, cases rejections also tended to be higher (difference significant in two). Within-fortnight comparisons indicate that the intermediate mothers’ tendency to reject

RELATIONS

IN MONKEYS

537

their infants more, and to initiate ventroventral contacts less, than the subordinate mothers was most consistent in weeks 6 to 12. These findings are consistent with the view that the overall tendency for the time the infant spends off its mother to increase with dominance status, seen most clearly in the comparison between intermediate and subordinate mothers, is due primarily to a tendency for subordinate mothers to reject their infants less, and initiate ventro-ventral contact with them more, in the 6 to 12 week period. Time at a distance from mother. Three of the four comparisons between dominant and subordinate sub-groups show that the offspring of dominant mothers tend to go to a distance from their mothers more than the offspring of subordinate mothers in a significant majority of fortnights. All four comparisons showed a consistent difference in this direction in weeks 12 to 14. The comparisons between dominant and intermediate sub-groups were equivocal, one dominant and two intermediate sub-groups being greater in a significant majority of fortnights: there was, however, a fairly consistent tendency for the intermediates to be at a distance more in the early weeks. The intermediate versus subordinate comparison showed intermediate groups to be at a distance more in more fortnights in five comparisons (significant in three), with one showing a difference in the opposite direction. The difference tended to be consistent between comparisons in weeks 6 to 8. Roles in maintenance of proximity. The infants of the higher status group tended to play a greater role in the maintenance of proximity in all dominant versus subordinate (two out of three significant) and dominant versus intermediate comparisons for which data were available. This was also true for three of the four intermediate versus subordinate comparisons in which the infants of the higher status group tended to be at a distance more. In all these cases the data are thus in keeping with the view that the differences in time at a distance are due more to differences between mothers. The other two intermediate versus subordinate comparisons were also in keeping with this view, though the differences in time at a distance were in the opposite direction or equivocal. Diiion. There is a general trend through all these comparisons for the offspring of the higher status mothers to be off their mothers

ANIMAL

538

BEHAVIOUR.

more and be at a distance from their mothers more, than those of lower status mothers, with the main difference being between the intermediate and subordinate mothers. The differences appear to be due primarily to greater maternal initiative in establishing ventro-ventral contact, and less frequent maternal rejections, by the low status mothers, and their greater role in the maintenance of proximity. The differences appear to be most marked in the 6 to 14 week period. The differences in time at a distance from mothers were perhaps more consistent than those in time off the mother. The probable explanations again lie in the extent to which females other than the mother coveted the infants and the mother’s fear of the adult male, and the consequent necessity for subordinate mothers to restrict their infants. This finding runs contrary to that of Nathan, Kaufman & Rosenbhun (1972) with bonnet macaques. In a study of four mother-infant dyads living in two separate groups, these authors found more maternal-infant contact with the more dominant mothers. Two points must be made here. First, it is by no means clear how far this finding can be generalized to other bonnets: these authors do not mention the sexes of the infants, so that this and many other factors in addition to dominance could have been affecting the mother-infant relationship.-Second, there may be a species difference: bonnet

23,

3

mothers allow other females to handle their infants more than do rhesus, so that the effect of dominance on mother-infant relations may differ. Perhaps it should be added that we would expect any relations between dominance and the mother-infant relationship to be somewhat subject to change with circumstances. Great care should be taken in applying the dominance/ subordinacy dimension to monkey groups (Gartlan 1968; Hinde 1974), though Richards (1972) showed it to have considerable validity in the particular circumstances of this colony. In any case, it is subordinacy that is the principle issue here (cf. Rowell 1966), and it is to be expected that a monkey mother might meet the problem of subordinate status in a number of ways: for instance she might be over-restrictive to protect the infant from others or inattentive as she attended to her own social relationships. Effect of Peers Data. Table I shows that five pairs of subgroups are available for comparison. In no pair were the numbers sufficiently substantial for comparisons across fortnights. The differences are summarized in Table VIII. Time off. In two of the pairs of sub-groups there was a significant tendency for infants with peers present to be off more than infants without: these involved mothers of intermediate

Table VIII. Comparlng (A) Infants with Peers Present with (B) Infants Witbout For each pair of &-groups

:

No. of fortnights median A > median B No. of fortnightly comparisons CIQP: Sub-groups compared CIQP/O

CIQX: CIQX/O

AIZX2: AI&XdO

ASSXI: AS&Xl/O

AIQP: AIQP/O

A>B

B>A

Time off

s/s*

5/l 1

5/11

l/llf’

R

215

5/11

5/10

4/11

14,22

RI(Mk, + MkM f RI

o/2+

3/10

4110

2112

10, 12, 14

% MkpA

0/5*

7110

4110

9113

%Mk

- %Bk,

l/4

4/l 1

216

6/11

>6OClll

315

2/10

7/10

3112

313

4110

2/10

o/13**

- %&

For *, and **, see Tables II.

8

20

218

515

Restrains

%4JI

11/14*

Fortnights in which 313, 414, 4/S or S/5 differences were in the same direction

14 10/11*+ 12, 14, 16

WHITE

& HINDE:

MOTHER-INFANT

dominance status. In one pair of subordinate sub-groups there was a significant tendency in the opposite direction. Differences in the other two comparisons were equivocal, and there was little indication of consistency between comparisons at any one age. Relative roles in determining differences in times off. Data were available for only four comparisons. In one case the absolute frequency of rejections was higher in the sub-group with peers present than in the sub-group without in all fortnights up to week 10. In the other cases the absolute frequency of rejections was equivocal, but the relative frequency tended to be lower and (in two out of three cases) the maternal initiative higher in the groups with peers in the majority of fortnights. In the case of the comparison involving subordinate sub-groups, in which the infants with peers were off less, a possible explanation is as follows. Perhaps the infants with peers tried to leave their mothers more, and hence were rejected less. The mothers, being subordinate and thus attempting to retain control of their infants, increased their initiative in ventro-ventral contacts to the extent that the time off was actually less than that of the comparable subgroup (see Discussion). Time at a distance. In one comparison, involving mothers of intermediate status, there was a significant tendency for infants with peers present to be at a distance more than infants without. Of the other three intermediate status comparisons, two were equivocal and one showed a tendency in the opposite direction, as did also the comparison between subordinate status mothers. Roles in the maintenance of proximity. Three of the four infants with peers present playeda smaller relative role in the maintenance of proximity than those without in most fortnights. That this did not result in an increase in time at a distance is presumably due to over-compensation by the mother. Discussion. Most of our infants had peers, so few comparisons were possible and discussion can only be very speculative. However, the data suggest that an infant with peers present tends to leave his mother more than one without, and that the mother’s response varies with her dominance status : a subordinate mother may permit her infant to depart from her less if he has peers than if he has none. If the protection of the infant from the maternal responses

RELATIONS

IN MONKEYS

539

of other females were the sole issue, we should expect the differences to be in the opposite direction: with more infants present, the threat from such females would be diluted. The difference may therefore be due to the behaviour of the mothers of the peers or the peers themselves. Mothers sometimes interfere in play on behalf of their own infants: a subordinate female could protect her infant only by restricting his playing. Indeed, a squeak of pain from the infant of a dominant female can direct her aggression on to the mother of the offending playmate. These results are compatible with those of an earlier study (Hinde & Spencer-Booth 1967), in which mother-infant dyads living in groups were compared with mother-infant dyads segregated in similar pens. Infants of the segregated dyads were off their mothers more than those of the group-living dyads, and went to a distance from them more often. The differences were due primarily to differences between the mothers, and presumably resulted from a need for groupliving mothers to protect their infants from the attentions of other females (see also Hinde 1969). However, the segregated infants, while going to a distance from their mothers in more half-minutes than the group-living infants, spent fewer whole half-minutes away. It was suggested that this was because they had no peers to play with. Effect of Sex Data. Table I shows that comparisons are possible between seven pairs of subgroups. One involves three with four pairs (CIBP : CIQP) and another six with seven pairs (AIJX2 : AIyX2). The comparisons are summarized in Table IX. Time off. Four of the seven comparisons showed a tendency for male infants to be off less than female, the two comparisons based on the most substantial data yielding significant differences. There was also one significant difference, based only on one pair with two, in the opposite direction. The tendency for males to be off less was more pronounced in the early weeks, and seemed to have largely disappeared after about 3 months. Relative roles in determining time off. The data must be considered in the light of the finding that, while male infants tended to be off less than females, this difference was most marked and most consistent in the few weeks after the infants started to leave their mothers at all, and later the reverse tended to be the case. Thus

1/9**

417

6114

619

1/14**

6112

%Mk, - %Bk,

Restrains

>6Ocm

%AP,

For l , ** and t see Tables IL and III.

%L,

10/13*

% Mk,

-

6113

319

4112

RI(Mk, + Mkhi + R)

517

318

117

316

s/13

9/13*

ADdP: AD?P

R

219

CIJX : CIVX

3114’

CIJP: CWP

Time off

sub-groups compared

117

3/6

7111 7113

619

10114

8112

5!12

9112 719

313

415

7113

317

417

3111

4114

319

217

8/l 1

7113

6110

517

10/11*+

10113’

6/10

W

AS$X2: ASQX2

6/13

ASdX1: ASgX1

2/13**

AIdX2: AIYX2

S/IO

AIdP: AI?P

No. of fortnights median A > median B No. of fortnightly comparisons

For each pair of sub-groups:

8, 18

12, 14, 18

A>B

4

10,14

696

B>A

For all sub-groups : fortnights for which difference is significant?

Table IX. Comparing (A) Male with (B) Female Infants

20

6

10

18,22

16

22

22

18

6*+ , 22

8+ 10

18,22*, 24

B>A 12,20

A>B

Fortnights showing 313, 414 4/5,5/5,5/6,$i/6,6/7 or 717 differenTkziox same

WHITE

8c HINDE:

MOTHER-INFANT

differences in rejection rates or maternal initiative in ventro-ventral contacts based on the whole 2%week-period cannot usefully be compared with the data on time off, and it is necesssary to consider the age-ranges separately. In those first few weeks there were no consistent differences in the frequency of rejections, but the mothers of males did tend to be responsible for a smaller proportion of ventroventral contacts and the male infants tended to play a greater relative role in ventro-ventral contact. Thus at this age the data are compatible with the view that males are off less because of a difference between male and female infants, and not because mothers treat male and female infants differently. The overall tendency for male infants to be rejected more than female infants, significant in the most substantial comparison between subgroups, was most marked in the 12 to 18-week period and most consistent across comparisons in the 18 to 24-week period. During this period the time spent off the mothers differed little between male and female infants, though the males were having a smaller proportion of their contacts initiated by the mother and being restrained less than females. Thus at this age it would appear that the mothers behave more negatively to males because males are more clinging, and/or that males seek their mothers more in spite of their mothers’ more negative responses to them. Time at a distance from mothers. There was a tendency for males to go to a distance from their mothers less than females in three comparisons (significant in one), a tendency in the opposite direction in one other, and three comparisons were equivocal. Relative roles in the maintenance of proximity. In one comparison males tended to take a significantly smaller role, but this involved only one with two pairs, and all other comparisons were equivocal. Discussion. The present data indicated that male infants are off their mothers less than female infants, the difference being most marked around the end of thesecond month, and due more to a difference between the infants than in the mothers’ behaviour to them. Later, the difference in time off disappeared and mothers P,gnEd less positively to male than to female There were no consistent sex differences in time at a distance from the mother or in roles in the maintenance of proximity.

RELATIONS

IN MONKEYS

541

These findings provide more detail than an earlier analysis of a part of this sample (Hinde & Spencer-Booth 1967), but the earlier study showed that after 30 weeks male infants tended to be off their mothers more than females. Thus we have a general picture of male infants staying on or near their mothers more than female infants in the first 10 weeks, little difference between them in weeks 10 to 30, and the opposite tendency thereafter. This is in harmony with data on pig-tailed macaque infants (Jensen, Bobbitt & Gordon 1968): mother-male infant dyads are at first more mutually dependent than mother-female infant dyads, but show a rapidly increasing trend to greater independence. The difference seems to be due to differences in maternal responsiveness to male and female infants. After the greater dependence of the male infants in the early weeks, their mothers punished them more and restrained them less than did the mothers of female infants. The age trend towards greater independence in males than in females is no doubt related to the greater incidence of social play in males (Harlow & Harlow 1965), which itself appears to be the consequence of different antenatal hormonal environments (Goy & Phoenix 1971). However, Mitchell (1968), analysing data on rhesus mother-infant dyads kept in a Wisconsin play pen apparatus, obtained rather different results. In the first 90 days, he found that mothers of females restrained their infants more than did mothers of males, had more contacts with them and fewer withdrawals from them. In the second three months, the mothers of males presented to their infants more than mothers of females and groomed female infants more than males. These differences between the two studies probably depend on differences in apparatus and in methods of analysis. With regard to the second, the lumping of data across a go-day period could obscure the age-changes discussed here. The apparatus, which prevented the mother from contacting the infant once it reached the playpen area, probably had a more profound effect. The great frequency with which females were restrained and contacted could for instance have been a consequence of the fact that the males tried to leave the mother’s pen for the playpen less often. Perhaps there was more physical contact with female infants because it was more necessary to restrain them. However, this cannot be the whole story, for female infants also initiated more physical contact with their mothers than did male infants.

542

ANIMAL

BEHAVIOUR,

General Discussion In this analysis the effects of six independent variables on mother-infant relations in rhesus monkeys have been considered. The procedure of attempting to equate sub-groups for all factors except the one under examination led in many cases to minimal group sizes, but this was partially compensated by the number of comparisons that could be made. The analysis shows that the effect of several of the independent variables considered changed with age, in some cases over a few weeks. There were also a number of cases of interaction between variables. Although the hypotheses presented to account for these are speculative, the occurrence of interactions seems indisputable. Perhaps the most noteworthy findings are that all but one of the variables considered appeared to affect the relationship, but none of them produced effects that were wholly consistent over all comparisons. This implies on the one hand that comparisons between groups of monkeys that are not deliberately equated for these factors must be viewed with caution unless the samples are very large; and on the other that important variables other than those considered must also influence the relationship. Indeed, even some of those considered here involved crude dichotomies: dominant versus subordinate, or peers present or absent ; they thus disregarded the diverse possible consequences of dominant or subordinate status, or the differing effects of peers of different sex or degrees of blood relationship, or the mothers’ ages. Indeed when one starts to reflect on the complexity of the social nexus in even a small rhesus group (Hinde 1972; Hanby, in preparation), it is hardly surprising that the different comparisons concerned with a particular variable are rarely consistent. Furthermore, one variable likely to be of crucial importance, the degree of blood relationship with the other social companions in the group, we have not attempted to assess in detail. But it would seem that the method of attempting to make comparisons only between animals equated for as many as possible of the relevant variables under consideration is of value. Acknowledgments This work was supported by the Medical Research Council and The Royal Society. Some of the data were collected by Y. Spencer-Booth, S. Richards, S. Atkinson, L. Davies, C. Perkis, J. P. Hanby, M. Leslie and M. Simpson. We are grateful to members of the Department of Veterinary Clinical Studies, Cambridge and

23,

3

especially to R. Lavell, A. R. Jennings and D. E. Bostock, for advice and help; to F. Jolley and R. Seekings for taking care of the animals, and to J. Hanby and M. Simpson for their comments on the manuscript. REFERENCES Denenberg, V. H. (1970). Experimental programming of life histories and the creation of individual differences. In: Efects of lkrly Ekperiwtce (Ed. by M. R Jones).University of Miami Press. Gartlan, S. (1968). Structure.and function in primate societies.Folia Primatol., 8, 89-120. Goy, R. H. & Phoenix, C. H. (1971). The effects of testosteroneproptonate administeredbefore birth on the development of behavior in genetic female rhesusmonkeys. In: Steroid Hormones and Brain Function (Ed. bv C. H. Sawver & R. A. Gorski). University of California Press. Hanby, J. P. (In preparation). Hansen, E. W. (1966). Development of maternal and mfant behavior in the rhesusmonkey. Behaviour, 30. 107-149. Harlow, H. & Harlow, M. (1965). The affectional systems.In : Behavior ofNon-Human Primates, Vo12 (Ed. bv Schrier& Stollnitz).New York: Academic

Press.-

Hinde, R. A. (1969). Analyzing the roles of the partners in a behavioural interaction-mother-infant relations in rhesusmacaques. Arm. N. Y. Acad. Sci., 159. 651-667. Hinde, R.‘A. (1972). Social behaviour and its development in sub-human primates. Condon Lectures, Eugene,Oregon. Hinde. R. A. (1974). On the de&n of check-sheets.