Koichi Negayama

Department of Psychology, Faculty of Human Sciences, Osaka University, Suita, Osaka 565, Japan

Received 6 February 1981 and accepted 22 July 1981

Keywords : Maternal aggression, offspring's independence, Japanese monkeys.

Maternal Aggression to its Offspring in Japanese Monkeys Aggressive behaviors by mothers toward their offspring and the inter- actions related to them were observed for one year in six separately caged mother-offspring pairs of Japanese monkeys (A/lacaca fuscata). Maternal aggression showed changes both in quality and quantity in the course of the offspring's development, and it was caused mainly by behavior that tile offspring directed toward tile mother. It was inter- preted that their actions increased irritability in the mother, and this interpretation is supported by the fact that the offspring reacted to the mother's aggression by stopping these behaviors and/or retreating from her. Maternal aggression functioned to promote the offspring's inde- pendence from its mother.

1, In troduc t ion

In many species of non-human primates, the mother plays very important roles in the behavioral development of its offspring. It is needless to say that its positive aspects of satisfying physical and psychological needs of the offspring are very important, and mater- nal positive r61e has been emphasized in many studies. But its negative or agonistic aspects cannot be underestimated. Mother-offspring dyad should rather be analysed in the both aspects equally in order to get general view of the relationship.

There are some studies which referred to the negative aspects in maternal behaviors. Hansen (1966), for example, studied on "punishment" in rhesus monkeys, Jensen et al. on "leaving" (e.g. 1967) and oll "hitting behavior" (1969) in pigtail monkeys. In the present study, aggressive behavior was dealt with because it is widely observed in the primate social interactions and has more generality and objectivity. Findings on maternal aggressive behavior toward its offspring may enable us to point out some characteristics of the mother-offspring dyad and to locate the place in the overall social relationships.

This study was designed to clarify the nature and the function of aggressive behaviors by mothers toward their offspring in caged Japanese monkeys (Maeacafuscata).

2. M e t h o d 2.1 Subjects The subjects were six separately caged Japanese monkey mother-offspring pairs. The mothers were captured at 4-10 years of age in the free-ranging group at Katsuyama, in Okayama prefecture, and sent to the laboratory. At 5-19 years of age, they gave birth to the infants who were used for the present study. Two of the six mothers were primiparous, and three of the six infants were male.

2.2 Procedure The pregnant adult females were housed individually in the home cages measured 0-5 m wide, 0-7 m deep, and 1.8 m high, and observation for this study started just after delivery. Each mother-offspring pair was observed for 15 rain weekly for one year, and the total observation time was about 15 hours for each pair. The occurrences of behaviors were recorded by 5 s intervals.

Journal of Human Evolution (1981) 10, 523-527

0047-2484]81/070523+05 $02.00/0 �9 1981 Academic Press Inc. (London) Limited

5 2 4 K. NEGAYAMA

3 . R e s u l t s

I n the earliest stage o f the mother-offspr ing dyad, the mother was highly positive to its off- spring. The mother ' s grooming toward its offspring, one of her major positive behaviors, occurred frequently and the aggressive behavior was rarely seen (Figure 1). Cont ra ry to the rapid decrease of the mother ' s g rooming in the first few months , materna l aggression increased until the offspring became four months old, and thereafter decreased very slowly.

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Figure 1. Maternal grooming ( - - - ) and aggressive behavior (----).

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I 2 3 4 5 6 7 8 9 tO II 12

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Offspring's age in months

The aggressive behaviors include biting, at tack (hitting, grabbing) , lunge, missing strike (rapid hand movemen t to the offspring without touching it; de Waa l et al., 1976), and open-mouthed threat. Biting and threat were the most frequent aggressive behaviors. Whereas threat increased steadily and remained at a high level, bi t ing increased until the offspring became four months old and thereafter decreased. The predominance o f biting over threat was reversed between the fourth and the fifth months ofoffspr ing 's age (Table 1). This mayre f l ec t the inerease of mother-offspr ing discreteness (this will be ment ioned later) and/or the change of offspring's reactiveness to the mother ' s behavior. Mother ' s bit ing had an increasing trend to evoke offspring's scream, which m a y be explained by the increase of severity in the biting as well as by the change of the offspring's reactiveness.

T a b l e 1 P e r c e n t a g e o f o c c u r r e n c e s o f m a t e r n a l a g g r e s s i v e b e h a v i o r s

Month of offspring's age ( .k "~

Behaviors 1st 2nd 3rd 4th 5th 6th 7th 8th 9th 10 th llth 12th

Biting 0.1 1.6 1-9 2.0 1.3 1.0 0.8 1.1 0.6 0.6 0.9 0.9 Attack - - 0.2 0.3 0.6 0.5 0-5 0.8 0.6 0.6 0.6 0.6 0.5 Lunge . . . . 0.0 - - - - 0'0 0.0 - - 0"0 0"0 Missingstrike - - 0"0 - - 0.1 0.1 0"1 0.i 0"1 0.3 0'I 0-3 0"1 Threat - - 0.5 1-2 1.7 1.5 1.9 2.0 2.0 2.0 1.7 2.1 1-8

(--) indicates no data for that month.

MATERNAL AGGRESSION IN JAPANESE MONKEYS 525

I n o rde r to examine the d e t e r m i n a n t s o f m a t e r n a l aggression, offspring's behaviors w h i c h were observed jus t p r io r to i t were analysed b i m o n t h l y (Tab l e 2). T a b l e 2 shows that, in general , m a t e r n a l aggression p r e d o m i n a n t l y followed the contac t - type behav io r b y the offspring such as m a n u a l con tac t w i th a n d r id ing on the m o t h e r in the ear l ie r s tage a n d the non-con tac t - type behaviors such as a p p r o a c h i n g the mo the r in the la ter stage.

Table 2 Percentage of occurrences of aggression-ellcltlng behaviors in offspring

Offspring's age in months A

W - - �9

Behaviors 0-2 2--4 4-6 6-8 8-10 10-12

In contact with mother Clinging to mother and/or on mother's nipple 10'8 8.0 6-2 6.4 2'6 1.1 Manual contacts with mother 22"6 12-3 12"0 I3-7 8"2 8"0 Riding on mother 16.1 23-4 20.1 12.6 10.7 8.3 Jumping at mother 3.2 5.1 0"7 0.8 0.4 Oral contacts with mother 3'2 2"0 3"3 4.5 6.4 2"7 Jumping down to mother - - 0"6 1"6 2"8 5"6 2"7 Jumping up from mother - - 0.3 0"3 1.4 1.7 0"8 Soliciting mother for interaction - - 2.0 1"0 5-9 5"6 1-1 Others 1"1 2.0 1.3 1.1 1"7 1"9 Unknown 8.6 12.3 14.9 12.0 6.4 14.0

Out of contact with mother Approaching mother 12.9 19.7 20.5 14.8 24.9 34-5 Visually orienting mother 1.1 4'0 3.9 6.7 9.0 7.6 Romping about mother - - 1"4 2-9 5.0 3"0 1" I Vocalization - - 1.1 3.6 2.5 3.0 3'0 Others 2.2 0.3 0.7 0.3 - - 0.4 Unknown 18.3 5.4 7.1 9-2 10.7 12.9

(--) indicates no data for that month.

I n the above-men t ioned tendencies , there were some exceptions such as ora l contacts w i th the m o t h e r o ther than "on the n i p p l e " (bit ing, gnawing, l icking), j u m p i n g down to the mothe r , a n d solici t ing the m o t h e r for in te rac t ion by pa t t ing . These were most ly p layfu l behaviors t oward the mother .

Rece iv ing aggression, the offspring r eac ted ma in ly by cessation of these aggression- e l ic i t ing behaviors and w i t h d r a w a l f rom the mother . W h i l e the former was cons tan t ly a t a h igh level, the la t te r increased unt i l four months of the offspring's age (Figure 2).

F igu re 3 shows the change o f discreteness be tween the mo the r and the offspring. T h e discreteness increased in the first five months . T h e recur rence of closeness after this pe r iod m i g h t resul t f rom low t e m p e r a t u r e in winter . T h e offspring's locomot ion increased a n d c l inging to the mo the r decreased unt i l i t became five months old, and these results suggest t ha t the independence of the offspring from the mothe r was la rge ly a t t a ined at five mon ths

old.

4. D i s c u s s i o n

T h e results ind ica te tha t m a t e r n a l aggression to its offspring changed cor respondent ly to the occurrences of m a t e r n a l posi t ive behaviors and offspring's behaviors in the course of the offspring's deve lopment . M a t e r n a l aggression is r ega rded as caused main ly b y the off'spring's behaviors toward its mother , and the details of the behaviors suggest tha t most

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I 0 0

8 0

6 0

a. 4 0

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Figure 2. React ions of offspring to ma te rna l aggression: cessation of aggression-eliciting behavior ( - - - - ) ; wi thdrawal from mother ( - - - ) ; no apparen t change ( . . . . ).

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Offspring's age in months

I 0 0

9 0 -

8 0 -

7 0 -

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Figure 3, Mother-offspr ing discreteness: less than 0"5 m ( - - - - ) ; more than 10 m ( - - - ) .

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I . - - - ' i . . . . . . t I , I I , ,, I I I I I I 2 3 4 5 6 7 8 9 t0 I I 12

Offspring's age in months

of the maternal aggressive behaviors were the result of the mother's irritability which was aroused by these behaviors as Hinde & Spencer-Booth (1967) pointed out.

The maternal aggressive behaviors and the offspring's reactive withdrawal from the mother increased up to four months of offspring's age, and the offspring's independence from its mother which was measured by its locomotion, clinging to her, and mother- offspring discreteness was largely attained at five months of offspring's age. This one- month lag suggests that the increase in maternal aggression might have promoted off- spring's independence from its mother.

In a natural or a semi-natural environments, the mother does not direct so much ag- gression toward its offspring (Murray & Murdoch, 1977; Nash, 1978). A preliminarystudy of mother-offspring dyad in a group of nine Japanese monkeys by the author showed a parallel tendency (not published). These facts indicate that the findings in the present

M A T E R N A L AGGRESSION IN J A P A N E S E MONKEYS 527

s tudy cannot be unduely generalized. The amoun t of space was pointed out to have an influence on the occurrence of "pun i shmen t" (Castell & Wilson, 1971), and the existence of the other animals must have some effect. However, it does not mean tha t the findings of the present study are of limited value. Rather , it should be interpreted that some latent and intrinsic aspects of mother-offspr ing relationship in Japanese monkeys were revealed in the restricted situation of the present study.

As compared with the aggression in other contexts, materna l aggression toward its offswing in this situation had the following characteristics: (1) I n general, the dura t ion was m u c h shorter. (2) Predominance of bit ing was seen in the earlier stage. However , (3) severity was much less in the maternal biting, which never resulted in wounds. (4) Mate rna l aggression showed a gradual change in quali ty in the course o f time. (5) Vocal aggression never occurred.

These characteristics indicate that materna l aggression toward its offspring is somewhat a unique one in overall p r imate aggressive interactions. I t m a y be the reflection o f the speciality of the mother-offspr ing dyad. H o w special the dyad is and what a re the in terna l and external determinants must be clarified further in future studies.

5. S u m m a r y

Materna l aggression to its offspring in six separately caged mother-offspr ing pairs of Japanese monkeys were studied for one year. The results indicate that maternal aggression increased in the first four pos tpar tum months and then decreased very slowly. Whereas threat increased steadily as the offspring developed, bit ing increased until four months of offspring's age and decreased thereafter. Materna l aggression was elicited mainly by the behaviors tha t the offspring directed toward the mother, and materna l aggression was regarded as the result of the mother ' s irritability by those behaviors. The offspring reacted to the mother ' s aggression by stopping those behaviors and/or retreat ing from her. The funct ion o f materna l aggression as promot ing the offspring's independence from its mother and the characteristics of the aggression were discussed.

References Castetl, R. & Wilson, C. (197t). Influence of spatial environment on development of n~other-infant

interaction in pigtail monkeys. Behaviour39, 202-211. de Waal, F. B. M., van Hooff, J. A. R. A. M. & Netto, W. J. (1976). An ethological analysis of types of

agonistic interaction in a captive group of Java-monkeys (Macacafascicularis). Primates 179 257-290. Hansen, E. W. (1966). The development of maternal and infant behavior in the rhesus monkey. Behaviour

27, 107-149. Hinde, R. A. & Spencer-Booth, Y. (1967). The behaviour of socially living rhesus monkeys in their first

two and a half years. Animal Behaviour 15, 169-196. Jensen, G. D., Bobbit, R. A. & Gordon, B. N. (1967). The development of mutual independence in mother-

infant pigtailed monkeys, Macaca nemestrlna. In (S. A. Altmann, Ed.) Social Communication Among Primates, pp. 43-53. Chicago: Chicago Press.

Jensen, G. D., Bobbit, R. A. & Gordon, B. N. (1969). Patterns and sequences of hitting behavior in mother and infant monkeys (Macaca nemestrina). Journal of Psychiatrlc Research 7, 55-61.

Murray, R. D. & Murdoch, K. M. (1977). Mother-infant dyad behavior in the Oregon troop of Japanese macaques. Primates 18, 815-824.

Nash, L. T. (1978). The development of the mother-infant relationship in wild baboons (Papio anubls). Animal Behaviour 26, 746-759.