An Experimental Study on

Developmental Changes of
Maternal Discrimination of
Infants in Crab-Eating Monkeys
(MacacafascicularZs)
KOICHI NEGAYAMA
Department of Psychology
Faculty of Human Sciences
Osaka University
Suita, Osaka 565, Japan

SHIGEO HONJO
Tsukuba Primate Center for Medicul Science
Yatabe, Tsukuha
lburagi 305, Japan
Individually reared mother-infant dyads of crab-eating monkeys (Maraca fascirulans) were observed
cross-sectionally in their mother-infant relationship. In infants aged from 0 to 5.0 months, rather drastic changes
were found both at 0.5-1 .O and 2.0-3.0 months of age. For an cxplanation of these changes, developmental
processes of discrimination between mother and infant were analyzed cross-sectionally by exchanging mother-infant
combinations. The results indicated that the first 0 5 months postpartum was characterized as a behaviorally
nondiscriminating stage where nipple discrimination by infants was the only exception. The latter half of the
first month was the beginning of a nonaggressive discrimination stage by mothers, indicated by lipsmacklng
and sniffing and in infants by clinging. When infants reached the age of 2.0-3.0 months, the mothers’
nonaggressive discrimination with lipsmacking decreased, and her aggressive discrimination of alien infants
increased. In addition to maternal visual discrimination of infants’ physical appearances, differences in infants’
odor and/or their method of nipple contact were suggested to affect the mothers’ differential behaviors.

Introduction
Mother-infant dyads of monkeys start with a strong intimacy, and agonistic interactions between the two are gradually incorporated. Under certain laboratory conditions, the mother’s aggressive behaviors toward her infant are caused mainly by her

Reprint requests and correspondence should be sent to Dr. Koichi Negayama. Faculty of Letters, Mukogawa
Women’s University. Nishinomiya. Hyogo 663. Japan.
Received for publication 27 Noveniber 1984
Revised for publication 3 I May I9XS
Developmental Ps,vrhohiolo,sp. I9( I ):4Y -56( 1986)
C 1986 by John Wiley & Sons. Inc.

CCC 00 12- 16301861010049-OXSW.00

50

NEGAYAMA AND HONJO

irritation induced by the infant’s behavior directed to the mother, and are interpreted
to promote the infant’s independence from the mother (Negayama, 1981). Hence, this
maternal aggression seems to be a reflection of an attenuation of their mutual dependency.
Such a change in the mother’s behavior supposedly requires as a precursor an establishment of her discrimination of the infant. This discrimination has been studied in
some primate species (Gulago crassicaudarus and G. senegalensis: Klopfer, 1970; Saimiri sciureus: Kaplan, Winship-Ball, & Sim, 1978; Rosenblum, 1968; Macaca nemestrina: Jensen, 1965). The purpose of these studies was mainly to determine when maternal
discrimination is acquired and by what factors the discrimination is mediated. These
studies were done for a short postnatal period and in situations where mutual body contact
was impossible or highly limited, dealing with only few behavioral criteria.
However, the mother-infant dyad usually exhibits various fundamental behaviors
that require direct contact between them. Furthermore, acquisition of maternal discrimination of her infant may be a gradual process that was not identified by previous studies
carried out for short developmental periods. Thus, in the present study, using crab-eating
monkeys (Macacafuscicularis) of different age groups, various maternal discriminating
behaviors between their own and alien infants will be examined in an environment where
the mother can obtain interactions without obstacles between her and the infant. The
present study consists of two parts: Study I is a general developmental survey of a
mother-infant dyad in Macaca fascicularis under a normative rearing condition; Study
11 is an experiment of mutual discrimination of mother-infant dyads over five months
postpartum.

Study I
Methods
Subjects
Subjects were 95 mother-infant pairs of Macaca fascicularis kept at Tsukuba Primate
Center for Medical Science (TPC) (Table 1). The mothers had conceived and given birth
to the infants at the breeding colony of TPC. Age of the infants ranged from 1 to 139
days. Forty-six of these infants were males and the remaining 49 were females. All the
mothers were wild-originated animals who, on the basis of the shape and size of their

TABLE 1 . Subjects Observed in Study I
Infants’s Age
(months)
0-0.5
0.5-1 .0
1.0-2.0
2.0-3.0
3.0-4.0
4.0-5.0

Total

Number of Mother-Infant Pairs
Male Infants

Female Infants

6
14
5
11

9
9

6

3

8
11
6

46

49

I

DISCRIMINATION OF INFANT IN MACACA FASCZCULARZS

51

nipples, were judged to have had infants before being brought to TPC, although their
entire reproductive histories were unknown. Each pair was kept in an individual cage
measuring 43 cm wide, 60 cm deep, and 60 cm high. The spatial arrangement of the
cages was such that a pair could see, hear, and smell, but not touch other pairs. The
other conditions of feeding and breeding Macaca fascicularis at TPC were described
elsewhere (Honjo, 1985).
Procedure
Each pair in the cage was observed twice, for 5 min each time, by the observer
standing in view at a distance of approximately two meters. Mother-infant bodily contact
and every discernible interaction between the two were recorded at an interval of 15 sec
(see Table 2), and frequencies were counted based on the number of the time units in
which a certain behavior occurred. Developmental change is thus shown cross-sectionally. Only the data having significance levels below 10% were indicated in the following
discussions.
Results
In order to know normative developmental trends of a mother-infant dyad, their
bodily contact, mother’s embracing and aggression to the infant as well as infant’s
clinging to the mother are illustrated in Figure 1. Occurrences of all of these behaviors
changed significantly over five months postpartum (contact: F = 9.02, df = 5/89,
p<.OOl; embrace: F = 3.15, df = 5/89, p<.025; aggression: F = 2.80, df = 5189,
p<.025; clinging: F = 7.55, df = 5/89, p<.OOl). In brief, the mother-infant tie was
attenuated as the infant became older. However, the curves did not show steady trends
but some drastic changes. One of the changes occurred between 0.5 and 1.0 month of
age, when infantile clinging to the mother decreased significantly ( r = 1.86, df = 33,
p< .05) whereas embracing decreased and aggression increased almost significantly in
the mother ( t = 1.53 for the former and 1.67 for the latter, df = 33, p c . 1 0 for both
factors). The other critical point occurred between 2.0 and 3.0 months of age, when
infants’ clinging and mutual bodily contact decreased (clinging: r = 2.01, df = 31,
p<.05; contact: t = 2.75 df = 31, p<.OO5), and mothers’ aggression increased ( t =
1.99 df = 31, p c . 0 5 ) .
TABLE 2. Behavior Categories
Behaviors
~~

Definitions

~~

Mothers’ behaviors
1. Embracing
2. Lipsmacking

3. Sniffing
4. Aggression
Infants’ behaviors
5 . Clinging

6 . On nipple
7. Withdrawal
8. Grinning

Holding an infant tightly in the ventral area with arm(s) closely surrounding it
Puckering the mouth and making a rhythmic movement with the lips while
looking at an infant
Getting the nose close to an infant and examining its odor
Biting, grabbing, hitting, threatening, or missing strike violently directed toward
an infant
Making tight bodily contact with the mother or an alien female by arm(s) and
hand(s)
Holding the nipple of the mother or of an alien female in the mouth
Leaving the mother or an alien female
Baring the teeth with fear

NEGAYAMA AND HONJO

52

I

IWTHER'S EBBRACE

Iao

5

t
Y

u
w

a
Y

n

0

ll.5 1.0

2.0

3.0

4.3

0.5 1.0

5.0

2.3

5.0

INFANT'S
AGE IN

I N F A N T ' S AGE Ill MONTHS

IitFANT'S CLINGING

100

4.0

5.0

MONTIIS

IIITUALB n n i ~CONTACT
~

r

Y

53

a
Y

0
11.5 1.0

1.0

3.0

11.n

ItIFAI4T'S AGE I N MONTHS

5.0

0.5 1.0

2.0

3.0

INFANT'S
AGE IN

Fig. 1. Developmental changes of behavior in mother-infant dyads, *,
<.05, and <.005, respectively.

4.0

5.0

MONTHS

**, and *** indicate p<.10,

Study I1
Methods
Subjects
The second study used 60 mother-infant pairs of Macaca fascicularis. The age of
the infants ranged from 0 to 155 days at the time of the experiment, but the data during
the sixth month of infants' age are not included below because of insufficiency of the
cases in the period. Distribution of the infants' ages is shown in Table 3. Thirty of the
infants were males and the remaining 30 were female. The living conditions were the
same as those in Study I.

Procedure
In each session two mother-infant pairs were tested. The infants' age and sex were
matched in two pairs of each testing. Thirty tests were conducted with 60 pairs in total,
and the age difference between the two infants in each test was 4.9 days on the average
(range = 0-17 days). Each of the two mother-infant pairs were respectively put into

DISCRIMINATION OF INFANT IN MACACA FASCICULARIS

53

TABLE 3 . Subjects Used in Study II
Infant’s Age
(months)

Number of Mother-Infant Pairs
Male Infants

Female Infants

0-0.5
0.5-1 .O
1 .o-2.0
2.O-3 .O
3.04.0
4.0-5.0
5.0-6 .@
Total

”Data in this age range were not sufficient and not shown in
the following illustrations. Number in parentheses indicate number
of pairs also participating in Study I .

testing cage measuring 43 cm wide, 60 cm deep, and 60 cm high for adaptation at
approximately three hr before the experiment. Each test consisted of three 5-min sessions:
Preexchange, Exchange, and Reunion. In the Preexchange session, each mother-infant
pair was observed in the testing cage with no human disturbance. After the session, the
two mother-infant pairs were taken from the cages and separated from each other by
animal technicians. The infants were immediately returned to the respective cages and
the mothers were put into the cages of the alien infants (Exchange session). Thereafter
the mother and alien infant pairs were again separated and exchanged in the same way
as before to re-establish biological mother-infant pairs (Reunion session). Orders of infant
presentation were not counterbalanced as a preliminary study had indicated this was not
necessary. All the mothers had been accustomed to the human handling for periodic
medical checks. In order to avoid an effect of test repetition on the performance, each
pair was examined only once in the present study.
Mothers’ and infants’ behaviors and their bodily contact were recorded with an
interval of 15 sec (see Table 2). Percentages were calculated on the total number of
intervals at which the behavior was observed. Only the results of Exchange and Reunion
sessions were shown for comparison for the sake of simplicity. Again, only p < . 10 are
considered here.

Results
Figure 2 shows the differences in frequencies of the mothers’ behaviors directed to
their own and alien infants and their developmental changes. It is notable that the first
0.5 month was a period when the mothers did not behave discriminatingly toward the
infants at all. Significant discrimination appeared during the latter half of the first month,
in lipsmacking ( t = 1.87, df = 10, p<.05) and sniffing ( t = 2.96, df = 10, p<.O1)
directed to the infants, and the significance of lipsmacking disappeared in infants aged
2-4 months. The earliest discrimination appeared in the mother of a 14-day-old infant.
The number of mothers showing lipsmacking to the alien infant in comparison with that
of mothers showing no lipsmacking changed significantly during the 6-month period (x2
= 16.02, df = 6, p<.025), but did not significantly change with respect to sniffing (x2
= 9.42, df = 6, pc.20). Thus, olfactory cues seem to remain efficient in maternal
discrimination during this period. Sniffing was directed mainly toward naso-oral as well
as anogenital areas of the infant.

NEGAYAMA AND HONJO
l5

0.5 1.0

2.0

3.0

4.0

ISNIFFING

0.5 1.0

5.9

2.0

3.0

INFANT'S
AGE IN

I N F A N T ' S AGE I N MONTliS

4.0

5.0

MONTHS

EtlBRACE

15

AGGRESS I OR

2.9

3.5 1.9

3.0

4.0

I i l F A N T ' S AGE I N MONTHS

Fig. 2.

5.n

0.5 1.n

2.0

3.0

4.0

5.0

I n F A N T ' s AGE I N MONTllS

Mother's behaviors directed to alien infant in Exchange session (square) and to her own infant
*, **, and *** indicatep<.lO, <.05, and <.01, respectively.

in Reunion session (circle).

Less embracing and more aggression were directed to the alien infants after two
months of age, although the discrepancy was almost, but not quite, significant for aggression in the fourth month ( t = 1.54, df = 5, p<.lO).
On the other hand, the infants did not show clear discrimination except for on-nipple
behavior, although significance reached the 10% level for clinging in the latter half of
the first month, and for withdrawal and grinning in the second month (Fig. 3.) Occurrences of on-nipple behavior were sometimes invisible for the observer, because, for
instance, the mother turned her back to him. Therefore, the values shown in the figure
were the ratios of observed number of 15-sec units for this behavior to the number of
15-sec units in which it was to be observed. The figure shows that on-nipple behavior
was directed discriminatingly to the mother and an alien female as early as in the first
half of the first month. The earliest discrimination other than this behavior was first seen
in a 12-day-old female infant grinning spontaneously only to the alien mother.

Discussion
The present cross-sectional comparison of normative mother-infant dyads (Study I)
and maternal discrimination experiment in the dyads (Study 11) using infants of different
age groups revealed some important aspects of the mother-infant relationship in Macaca
,f~iscicularis.
The normative study using infants aged from 0 to 5.0 months postpartum showed
considerably drastic changes occurring both at 0.5-1.0 and 2.0-3.0 months of age. The

DISCRIMINATION OF INFANT IN MACACA FASCZCULARZS

55

CLINGING
I00

ON NIPPLE

0.5 1.0

I
0

11 1.v:.
2.0

LO

!1.3

I N F A N T ' S AGE I N I I O N I H S

5.1

4.0

5.0

IN MONTHS

GRINNING

I

0.5 1.9

3.0

INFANT'S
AGE

I N F A N T ' S AGE I N MOIITIIS

0.

2.0

I

0.5 1.0

2.0

.

3.0

L

11.0

,

5.0

I N F A N T I S AGE I N MONTHS

Fig. 3. Infant's behaviors directed to alien female in Exchange session (square) and to its own mother
in Reunion session (circle). *, **, *** indicate p < . l O , <.05, and <.01, respectively.

data of discrimination experiment indicated that the mother and the infant did not behaviorally discriminate their partners during the first 0.5 month after birth except for
nipple contact by the infant. Jensen (1965) illustrated that Macaca nemestrina mothers
visually discriminated their infants placed adjacent to their cages by 17 days postpartum
with pacing more in the presence of their own infants. The present study indicated that
the mothers and infants actually began to discriminate each other with lipsmacking,
sniffing, and clinging, although the last one was not strongly significant. Thus, the initial
change in normative mother-infant dyads in Study I seems to be actualized by the
beginning of mutual discrimination of the partner's face or other characters in the latter
half of the first month. Until then neither the mothers nor the infants were willing to be
mutually apart in normative dyads. Since the contact-seeking is nondiscriminant in this
stage, this must be the easiest period for adoption.
After the second change in mutual behaviors of the normative mother-infant dyads,
when the mother became more aggressive toward the infant and the infant clung less to
the mother, she discriminated the alien infant with less embracing, whereas the discrepancies between her lipsmacking toward the alien infant and that toward her own infant
became nonsignificant because the former decreased. Furthermore, maternal aggression
occurred almost significantly more to the alien infant than to her own. This stage can be
thus characterized as the stage of decreased intimacy and of increased aggressivity in the
mother toward the alien infant. This may be ascribed to her considerable development
of the discri'mination by the infants' physical appearances and/or to an increase of her
aggressivity to infants at this stage due to loss of their certain babyish characters. The
intermediate period of 0.5-2.0 months when the mother discriminated the alien infant
nonaggressively can be regarded as the transitional stage. Hence, it is concluded that the

56

NEGAYAMA AND HONJO

establishment of maternal behavioral discrimination of infants is a gradual process containing some quantitative as well as qualitative changes in it.
Gender of the infant did not appear to have any influence on the mothers’ performance in this situation.
The infants did not show prominent discrimination except for on-nipple contact. This
is probably due to an experimental setting of the present study: the procedure of sudden
separation of mother and infant and immediate exchange of each partner. This must have
frightened the infants and increased their dependency to the alien partners as well as to
their respective mothers. In spite of this, each infant mouthed its mother’s and the alien
female’s nipples differently even in the earlier half of the first month. This may indicate
the infants’ early ability of discrimination possibly on the nipples’ odor, color, and/or
shape. It is plausible to think that such a differentiation in nipple contact between the
two sets of infants caused different stimulation in the mothers resulting in different
treatments of the infants.
The,present results showed the frequent occurrences of sniffing in the mother predominantly for the infant’s naso-oral as well as anogenital areas. Kaplan, Cubicciotti, &
Redican (1977) also showed olfactory discrimination of mothers by their infants in Saimiri
sciureus. In macaques, blind infants were reportedly not sensitive to their mothers’ odor
(Berkson & Becker, 1975), but at least for the present mothers the importance of olfactory
cues in discriminating the infants was strongly suggested.
In the present situation, both mothers and infants were permitted to interact directly
and freely. Such a situation enabled them to behave in various ways, but at the same
time made it difficult to determine the precise beginning of each mother’s and infant’s
discrimination and to assess the role of the sensory cues related to the discrimination.
Therefore, further experiments under more controlled conditions are needed in both
mothers and infants.

Notes
The authors are grateful for the assistance of Mr. Michihiro Suzuki and Mr. Koji Hanari in conducting
the research. We also thank to Dr. Fumiaki Cho for his arrangement and helpful criticism of the research. Part
of this work was supported by a Grant in Aid for Scientific Research, Ministry of Education, Science and
Culture, No. 5810063, 1983, to Koichi Negayama, and No. 59115005, 1984, to Dr. Masao Kawai.

References
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Primatol., 14175-89.
Jensen, G . D. (1965). Mother-infant relationship in the monkey Macaca nemestrina: Development of specificity
of maternal response to own infant. J . Comp. Physiol. Psychol., 59:305-308.
Kaplan, J. N., Cubicciotti, D., 111, and Redican, W. K. (1977). Olfactory discrimination of squirrel monkey
mothers by their infants. Dev. Psychobiol., 10:447-453.
Kaplan, J. N., Winship-Ball, A , , and Sim, L. (1978). Maternal discrimination of infant vocalizations in squirrel
monkeys. Primates, 19:187-193.
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Negayama, K. (1981). Maternal aggression to its offspring in Japanese monkeys. J . Hum. Evol., 10523-527.
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In L. A . Rosenblum, and R. W. Cooper (eds.), The Squirrel Monkey. New York: Academic Press, Pp.
207-233.

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