Early Deaelopment and Parenting, Vol. 3 (I), 19-28 (7994)

Eoolutionary Ro ots of IntuitiueP arenting: Maternal Competencein Chimpanzees

Kim A. BardYerkes Regional Pimate Research Center, Emory Uniaersity,Atlanta, GA 30322, USA

Intuitive parenting behaviours have been shown to be universalin humans and appear to be based on psychobiologicalpreadaptedness. This study is an exploration of the evolutionaryroots of intuitive parenting through naturalistic observationof mother chimpanzees' interaction with their very young infants.Maternal competence is demonstrated initially through thebehaviours of carrying the newborn infant and allowing the infantto nurse. Very early mother-infant interactions include play,'exercise', cradling and grooming. Chimpanzee mothers also assesstheir offspring's behavioural state and muscle tone through visualinspections and movement of legs, arms, fingers and toes.Chimpanzee mothers and infants, as early as 2 weeks ol age, spendsome time in mutual gaze. Neonatal chimpanzees are capable ofsustained face-to-face interactions, as these were observed innursery-re.rred chimpanzee interactions with human adults;however, it appears that chimpanzee mothers encourage mutualgaze with their infants for only brief durations. Chimpanzees withgood maternal competence exhibit sensitive responsivity to infants'communicatory signals. Thus the results of this study support theclaim that there are evolutionary and comparative foundations ofintuitive parenting evident in the maternal behaviour and maternalcompetence of chimpanzees.

Key words: Infant chimpanzees, primate parenting, mutual gaze.

During parent-infant interactions in humans thereare episodes in which parents stimulate theinfant's integrative development (i.e. learning andcognitive capacities). These episodes, labelleddidactic interventions, are times when the adult is'contingent, easily predictable, and manipulatableby the infant' (e.9. Papoudek and PapouSek, 1987).

Address for correspondence: Kim A. Bard, PhD, ResearchScientist, Division of Reproductive Biology, Yerkes RegionalPrimate Research Center, Emory University, Atlanta,GA 30322, USA

ccc 1057-3s93 I 9 4 I 07ffit9 -10A 1994 by ]ohn Wiley & Sons, Ltd.

The behaviours are labelled 'intuitive' becausethey occur without conscious rational thought butthey are not refledve. According to the Papoudeks,intuitive behaviours occur more quickly thanthose based on rational thought and less quicklythan those based on reflective acts. Intuitivebehaviours appear to be universal across cultures,gender, age and parental status, althoughexperience with infants is probably a necessary

Precursor.Intuitive parenting behaviours (documented to

date only in the human species) consist of behavioursthat (1) provide adequate conditions for adult-infant

Receioeil 14 Aoil L992Accepted 12 ApnI N93

20 K. A. Bttrd

engagement, (2) provide adequate stimulation,and finally (3) provide supporr to the infant'sintegrative process (Papou5ek and Papou5ek, 7987).Th,e conditions for engagement include having theinfants in a quiet behaviourai state, in face-to-faceposition. Adequaie stimulation consists, in part, inhaving the adult engage in exaggerated facial andvocai expressiveness appropriate to the in_fant's age(e.g. 'motherese' or baby talk). The support ofintegrative capacities can be observed when theadult engages in contingent action, repetitive gamesand encourages imitation games. Non-human andespeciallv non-vocal behavioural examples includeassessing muscle tone, assessing behavioural state,acting contingently or turn-taking with rhythmictickles or pokes, and emphasizing or 'marking'

in fants ' appropr iate fac ia l expressions ( . gAdamson and Bakeman, 1984). Intuit ive parentinebehaviours appear to be based on 'psychobiologica'i

preadaptedness' (Papou5ek and Papou5ek, 1987,p.675). Thus it is reasonable to assume that thereis_ an evolutionary root to intuitive parenting.The specific aim of this project was to investigate theevolutionary root of intuitive behaviours throughnaturalistic observations and microanalytic analvsisof chimpanzee mothers and infants, close phyieticrelatives of humans. This perspective wil l alsoprovide a heuristic framework to better understandthe components of leamed materna-l behaviour in thechimpanzee. Knowledge of behaviours indicative ofmatemal competence is important for fwo additionalreasons: to devise intervention procedures to helpchimpanzees 'at risk' for developing maternilinadequacies and to assess the maternal competenceof each new mother so as not to put her ofisprrngat risk for iniurv.

METHOD

htujects

All aduit female chimpanzees at the yerkes lvlainCenj91 .,vho gave birth to a live infant from Januarv1,7987 through January 7,7992 and who displayedthe minimum maternal behaviour of picking up andcarrying their newborn rvere subjects of this study(see Table 1). During this period, 10 mothersexhibited 'good' maternal competence, defined asdisplaying maternal behaviour sufficient to care fortheir offspring for at least 3 months. Four additionalmothers exhibited'marginallv adequate' maternalcompetence; they init ially picked up and carriedtheir infants but their infants were removed andplaced in the nursery due primarily to unresponsivecare and additionallv due to i l lness (N:1), over-grooming (N: i), exiessive holding of infant awavf rom the mo the r ' s bodv (N : I ) and i n j u r v (N :1 j .The third category of mothers (N=12) exhibited'poor' maternal competence, defined as either notpicking up the infant or not cradling the infant.These infants were placed in the nursery.

Procedure

Normal behaviour patterns were exhibited throughspontaneous natural interactions. No restrictionswere placed on the location of the chimpanzeesduring videotaping. Mother-infant pairs werevideotaped for t hour between 9.30 am and11.30 am. Videotapes were collected daily from theday after birth through 30 days of age and thentwice a week from 4 weeks through 12 weeks of age.

These videotaped observations were used to codebehavioural state of neonatal chimpanzees (Bard,

Table 1' . ogmgqlnnlc information for chimpanzee females who gave birth from Januarv 1,,7987 to January l, 1992and are included in this study

Mother/infant Previousliveoffspring

Mother's earlyrearing

Maternalcompetence

Interactional caregivingVideotape coded

Joice/OlinLeslie/DaraVivienne/WiImaBarbi/ElviraLil'One/PollyannaCynthia/AliciaCissie/TravisMartha/KengeeEricka/RowenaGaye/Magnum

2110

00212

Nursery? Probable wildNurseryMotherProbable wildMotherNurseryNursery? Probable wildProbable wild

GoodGoodGoodGoodGoodGoodGoodMarginalMarginalMarginal

ContextContextContextContextContextContextContextContextContextContext

Eye gazeEye gazeEye gazeEye gaze

Eye gaze

Eye gazeEye gazeEye gaze

[ntuitiae Parenting in Chimpanzees 27

Table 2. Interactional caregiving context: behavioural codes and definitions

Croom-For infants less than 3 months al l grooming bouts are mothers groorning infants (see van Lawick-Goodall ,1968 and Goodall , 1986 for detai is).

Cradk-Mother supports the bodv of the infant against her bodv, primarilv with an arm or leg oressed againstthe infant's back, or the mother provides support while her infantls sitting or standing nearbv but not veitrallvclinging to the mother. Maternal support includes active cradling and more passive maintenance of ventral-ventralcontact, such as that found r.,r'hen mother lies down on her back and infant lies on her stomach rvithout additionalcradl ing.

Reposition-Mother moves the infant's body to a different location, usually on her bodv but can move infant offher bodv.

Res,train-Mother prevents infant from moving, usually preventing the infant from moving off her bodv.Hold-Mother grasps the arm, leg or body of her infant-Saieguardlprotecf -Mother Proiects her infant from harm, such as preventing the infant from falling or from the touch

of others.Soo/fte-Mother acts in any wav to calm ihe infant, for example bv rocking.Caress-I{other touches the infant gently with her hand or l ips (e.g. kiss).Play-.Social plav between moiher and infant rvhich includes pokes, patting, plavful gnawing and tickling, usuallr.

rhythmic in nature and accompanied by smiles ( i .e. play f ices; elboi l , t9e+y.Exercise-Mother acts in a wav that encourages motor development: moving the infant in a way that engages the

infa,ni in physical activities such as standing, walking or supporting their own weight with theii arms (see Yerkes,1943, for ciescriptions).

Assessment- Motlier checks either the infant's muscle tone, by pulling or stretching infant's arms or legs, or theinfant 's behavioural state, such as sleeping, nursing or distreis.

Ex:'nnine-Mo_ther inspects_the infani's physical appearance with careful looking rvhile moving ihe infant around.Mav precede grooming but is a distinct activitv.

Noi i'l.sible-The activity of either the mother or infant is not visible or the tvpe of activitv js unclear.

in press) and early expressions of iaterality incradling the infant and infant reaching (Hopkinset al. , 1993) . For this studv, one videotaped sessionwas seiected from each of the followine threeperiods based on the age of the infant: 2--l 'weeks,6-8 weeks and 10-12 weeks. Selection criteriaincluded good visibility and prototypic interactions.We tried to select those sessions that best tvpifiedthe interaciional styie of each mother-infant pairduring each age period.

Co ding of Interactional Caregiaing:Context and Eye Gaze

Two independent coding systems were applied tothese videotaped observations. The first codingsystem was interactional caregiving context, whichconsisted of characterizing the type of interactionthat occurred (such as grooming or playing) basedon Papou5ek and Papoudek's (1987) specificationof intuitive parental care (see Table 2, see alsoPapoudek et al. (1991)). Categories were mutuallyexclusive and exhaustive and coding was continuousfrom the beginning to the end of each hour-longvideotaped observation. The second coding systemwas eye gaze. The categories again were mutuallyexclusive and exhaustive (Table 3). The mother'seye gaze was classified as looking at the baby(specifically looking at either the infant's face or

the infant's body) or not looking at the baby. Inaddition, for this initial analysis, mutual eye gazewas determined. For the period of time when themother was looking at ihe infant's face, a yes-nodecision was made u,ith regard to whether theinfant looked at the mother's face or not. In bothcoding systems, uncertainties due to inability toclassify or to lack of visibility were ciassified witha distinct category.

RESULTS

Int er o b s eru er Agr e ement

Int eractional Caregiaing Cont extsThree independent observers coded context from

videotapes: two primary observers each coded50o/o of the corpus (total of 28 sessions) and thethird observer coded 38o/o. Cohen's kappa is a

Table 3. Eye gaze: behavioural codes and definitions

Infant face-Mother looks directly into the infant's face.Infant body-Mother is clearly looking at the infant

including the arms, legs, body and head, but does notlook at the face of the infant.

None-Mother is clearly not looking at the infant.Uncertain-Either the mother is not visible or the direction

of the mother's eye gaze is not certain.

22 K. A. Bard

conservative and preferred statistic to evaluateinterobserver agreement since it removes fromobserved agreement that amount of agreementdue to chance alone (Bakeman and Gottman,1986). Agreement (assessed on 11olo of the corpus)between the primary codes was good: per centaSreement was 83.4 and Cohen's kappa was 0.6with high chance agreement of 59o/o. Agreement(assessed on approximately 18o/o of the corpus)between the secondary coder and each of theprimary coders was also good: per cent agreementwas 81 and 85, respectively, each with Cohen'skappa of 0.56 with high chance agreement of56.50lo and 68.7Vo, respectively. An additional coderwas unreliable. Due to the dropping of this coder'sdata, not all of the videotapes have been coded.Thus, results are available for seven 'good' mothers,out of 1C possible, and three out of four 'marginal'

mothers.

Eye gazeFour independent observers coded eye gaze from

videotapes. A subset of the videotaped sessionswas chosen in advance, five 'good' mothers andthree 'marginal' mothers; one was coded at fwo ageperiods and one additional at each of the twoage periods. Two primary observers (CH and LC)coded approximately 50o/o of the corpus (total of 19sessions) and two secondary observers (B] and KB)coded 37o/o and 2L0/o of the corpus, respectively.Agreement between the primary observers (assessedon 1,60/o of the corpus) was excellent: per centagreement was 88.5 and Cohen's kappa was 0.69.Agreement between each of the secondary codersand each of the primary coders (assessed on 11oloof the corpus) was also excellent: Bj with CH percent agreement was 88.1. and Cohen's kappa was0.57;KB with CH per cent agreement was 92.8 andCohen's kappa0.78; BJ with LC per cent agreementwas 89.1and Cohen's kappa 0.56; and KB with LCper cent agreement was 0.96 and Cohen's kappa0.74. Agreement between the two secondaryobservers (B| with KB) was also excellent: per centagreement was 89.5 and Cohen's kappa was 0.70.

Interactional Carcgiaing Contexts

Videotaped observations lasted for approximatelyL hour for each mother and each age period. Duringmost of this hour it was possible to determinewhether or not interactional caregiving contextsoccurred. Visibility was approximately fro/o at2-4 weeks and 5-8 weeks and approximately 80o/oat 10-72 weeks. The amount of active time was

calculated; active time was defined as time whenthe chimpanzees were visible and an interactionalcaregiving context was observed. Interactive care-giving contexts occurred during all the visible timefor chimpanzees with good matemal competence butthis was not the case for subjects with marginalmaternal competence. In addition, there were nodata reported for the 10-12 weeks interval formothers with marginal maternal competencebecause most of the in-fants had been removedfrom their inadequate care and placed in thenursery.

The single most frequently occurring caregivingcontext found in chimpanzees was cradling (Figure1). Mothers of infants of all three age groups spentan equal proportion of time just cradling theirtheir inJants. Mothers spent approximately 70o/o olvisible time cradling their infants without engagingin any other caregiving. Other activities were

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cooo&

2 - 4 6 - 8 1 0 - 1 2

In fon t oge (weeks )

Figure 1. Per cent of visible time spent by chimpanzeemothers cradling their infants less than 3 months ofage without engaging in any additional interactionalcaregiving activity.

2 - 4 6 - 8 1 0 - 1 2

In fon t oge (weeks )

Figure 2. Total time spent by chimpanzee mothers inhteractional @r€ving activity additional to cradling theirinfants at three different ages.

a

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G o o d m o m s O ( n = 7 )

Morginol moms O (n=J)

Good moms O (n-7)

Morginol moms O (n=J)

Intuitiae Parenting in Chimpanzees /-J

Good moms O (n=7)

Morginol moms O (n=J)

2 - 4 6 - 8 1 0 - 1 2

ln fon t oge (weeks )

Figure 3. Per cent of active time spent by chimpanzeemothers in grooming their infants at three differenta8es.

Good mom3 O (n=7)

Morginol moms O (n-3)

2 - 4 6 - E 1 0 - 1 2

In fon t cAe (weeks )

Figure 5. Per cent of active time spent by chimpanzeemothers in holding their infants at three different ages.

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Figure 4. Per cent of active time spent by chimpanzeemothers in playing with their infants at three differentages.

conducted in addition to cradling. The amount oftime mothers spent engaged in these additionalactivities varied from 3 minutes to 30 minutesout of an hour (Figure 2). Particularly frequentactivities were: (1) grooming, approximately 30o/oof active time at all three ages (Figure 3); (2) play,on the average 15o/o of active time at all ages; infantssmiled as mothers tickled them and contingentturn-taking was often observed during play bouts(Figure 4); and (3) holding, an activity that occupiedan average ol 70o/o of time (Figure 5).

Mothers repositioned their infants by movingthem around on their body (Figure 6). Typically,mothers repositioned their infants if they fussedor in order to move them into cradling position.Repositioning bouts were typically short, occupieda relatively small percentage of time (approximately5o/o of active time) and occurred an average of8-11 times during an hour.

. In font oge (weeks)

Figure 6. Number of times in an hour that chimpanzeemothers repositioned their infants at three differenta8es.

Some types of caregiving contexts appeared tochange in frequency of occurrence or duration oftime based on infant age. These results must beconsidered tentative as the sample size is very small.The amount of time mothers spent examining orinspecting the infants' general appearance washighest when their infants were 2-4 weeks of age(almost 15o/o of active time) and decreased toapproximately 3o/o of active time by the time theirinfants were 6-8 weeks of age (Figure 7). Theamount of time mothers spent assessing either theirinfant's behavioural state or changes in the infant'smusde tone was higher at both at 2-4week and 5-&week periods compared with the 10-L2-week period(Figure 8). Soothing, caressing and safeguardinginteractions occurred on the average 4olo of the timewith all the infants (Figure 9). The increase at 6-8weeks of age was due primarily to one mother'slarge percentage of safeguarding. Most mothersspent time encouraging their infant's motordevelopment with exercise (Figure 10). Exercise

G o o d m o m s O ( n = 7 )

M o r g i n o l m o m s O ( n = J )

G o o d m o m s a ( n = 7 )

M o r g i n o l m o m s O ( n = f , )

24 K. A. Bard

Good moms O (n=7)

M o r g i n o l m o m s O ( n = J )

2 - 4 6 - 8 l 0 - 1 2

ln fon t oge ( r veeks )

Figure 7. Per cent of active time spent by chimpanzeemothers in inspecting their inJants at three different ages.

G o o d m o m s a ( n = 7 )

Vorginol f roms O (n=J)

2 - 4 6 - 8 1 0 - 1 2

ln fon t oge (weeks )

Figure 10. Per cent of active time spent by chimpanzeemothers in exercising their infants at three different ages.

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Eo

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in fon t oge (weeks )

Figure 8. Per cent of active time spent by chimpanzeemothers in assessing their infants at three different ages.

Good moms O (n:7)

M o r g i n o l m o m s O ( n = J )

t?6 . _ 8 1 0 - 1 2

In font o9e (weeks)

Figure 9. Per cent of active time spent by chimpanzeemothers in soothing, caressing and safeguarding theirinfants at three different ages.

occurred more often when infants were 6-8 weeksof age compared with the other age periods. Manychimpanzees were quite active by 10-12 weeks ofage. Their increased activity corresponded to theincreased amount of time spent in restraining infantmovements (Figure 11).

20

1 5

5

0

G o o d m o m s O ( n = 7 )

M o r g i n o l m o m s O ( n = J )

In font oge (weeks)

Figure 11. Per cent of active time spent by chimpanzeemothers in restraining their infants at three different ages.

Only a few interactional caregiving contextsappeared to distinguish good maternal behaviourfrom marginal maternal behaviour. These results,however. must be considered tentative as therewere only three marginal mothers and individualdifferences among both good and marginalchimpanzee mothers can be quite dramatic (e.9.Yerkes and Tomlin, 1935; Yerkes and Elder, 1937).

The most dramatic diJferences between chim-panzees with good maternal competence comparedto those with marginal competence is that onlymarginally competent mothers (two of the three)placed infants on the floor out of contact (Figure 12).Sometimes these mothers Lransported their infantsby dragging or pushing them instead of cradlingthem as would competent mothers. When marginalmothers did engage in caregiving with their infants,they appeared to mismatch their behaviour with iheappropr iate caregiv ing for the age oftheir infant. For example, marginal mothers triedto encourage walking when their offspring wereonly 2-4 weeks old. More importantly, 'marginal'

mothers appeared, at best, to be particularly

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Intttitice Parenting in Chimpanzees 25

601

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G o o d m o m s a ( n = 7 )

M o r g i n o l m o m s O ( n = J )

2 - 4 6 - I

I n fon t oge (weeks )

Figure 12. Per ceni of active time spent by chimpanzeemothers placing their infants on the ground.

unresponsive to their infant's signals, especiallvdistress vocalizations, and, at their worst, appearedto actually encourage contingent behavroursinvolving distress.

in addition, 'marginal' compared with 'good'

mothers appeared to differ in timing in behaviourdevelopmentall;,, for example grooming (Figure 3),holding (Figure 5) and more time trying to oiavwith visibly unhappy 2-4-week-olds (Figure .1).lVlarginailv competent cirimpanzees compared rviththose u.ith good competence spent iess time soothing,caressing or protecting their 2-4-week-olds (Figure9), inspecting their 2-4-week-olds (Figure 7) orassessing either behavioural state or motoric tone(Figure 8).

Mutual Eye Gaze

Chimpanzee mothers spent 20olo of visible time, asubstantial portiorr of time each hour, looking attheir infants. It appeared that mothers spent moretime looking at younger infants (Figure 13). Morespecifically, chimpanzee mothers spent 12 minutesin an hour, on the average, looking at their infantsand half of that time, 6 minutes, was spent lookingat the babies' face (Figure 1.4). Future analysiswill specify in detail which of the interactionalcaregiving contexts are most often associated withmothers' looking at their infant and which areassociated with looking at infants' face. It was clearthat chimpanzee mothers look at their infants' facein the interactive caregiving contexts of assessing,playing, examining and grooming.

Not only do chimpanzee mothers gaze at the facesof their infants but infants gaze at the faces oftheir mothers. Moreover, numerous occurrences ofmutual gaze were found. Ten times in an hour, onthe average, mothers were found to engage in a

G o o d m o m s O ( n = 5 )

M o r g i n o l f l o m s O ( n = 2 )

2 - 4

l n f o n t

Figure 13. Per ceni ofmothers spent looking ata8es .

active time that ch.impanzeer l r rthclr rnlants r) l three culterent

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2 - 4 6 - 8 1 0 - 1 2

ln fo r : t cge (weeks )

Figure 14. Per cent of looking time that chimpanzeemothers spent looking at the faces of their infants at threedi i ferent ages.

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in fon t oge (weeks )

Figure 15. Number of times that chimpanzee mothersand their infants at three different ages engaged in mutuaieye gaze during an hour-long observation.

mutual gaze with their 2-t1-week-old and 5-8-week-old infants. The average number of mutual gazesdecreased to eight times in an hour when infantswere 10-12 weeks old (Figure 15).

J 5

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2 5

2 0

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10 K. A. Bard

There were some differences in eye gaze betweenchimpanzee mothers with good competence andthose with marginal competence. Marginallycompetent chimpanzees looked more at their2--{-week-old infants and less at their 6-8-week-olds.One marginal mother looked at her 2-4-week-oldinJant's face quite alot (23o/o of visible time) whereasthe other did not look very often or very long at her2-4-week-old infant's face (0.8olo of visible time).Boih marginal mothers spent very little time lookingat the face of their 6-8-week-old inJants (averageless than lo/o of visible time). The number ofmutual gazes between marginal mothers and their2-4-week-old infants were within the range of thatof good mothers but the number of mutual gazesbetween marginal mothers with 6-8-week-oldinfants were decreased substantially less comparedr,r'ith the number found between good mothers andtheir 6-8-week-old infants. It appears that eye gazeis another sensitive indicator of the quality ofmother-infant interactons.

DISCUSSION

lnfuitive parenting in chimpanzees includes providingsupportive care (i.e. cradling, grooming), enjoyinginteractions (i.e. playing), being responsive (i.e.soothing, assessing, inspecting) and nurturingdevelopment (i.e. exercising: Rogers and Davenport,1970; Yerkes, 7943). Chimpanzee mothers withgood maternal competence engage their infants ininteractions from early in life. There are manyinstances of encouragement or exercising of skillsin infants during the first 3 months of life. Motordevelopment is stimulated through maternalmanoeuvres such as standing the infants whileholding their hands. Mothers repeatedly andalternatively stimulate their infant to hold theirweight with legs and then with arms. Encouragingof early crawling is accomplished in a similar way.Because mother-infant contact is rarely broken inthese early months, these stimulating exercises aretypically performed on mother's body. 'Sooner orlater every mother encourages and variously aidsher baby to learn to creep, stand erect, climb, andfinally to walk and run' (Yerkes and Tomlin, 1935,p. 333).

Early mother-infant communication in chim-panzees is often accomplished with touch (Plooij,7979) and accompanied by vision and audition.Mothers monitor their infant's behavioural state bystretching and moving infants' toes, fingers, armsand legs and sometimes just by looking at them.

During play, infant smiles are sometimes 'marked'

as critical feahres by the mother with an emphasizedtouch (e.g. Adamson and Bakeman, 1984). Whenthe infant smiles, in response to a tickle in the neckor groin, the mother may place her index finger onthe infant's lower gums and exaggerate the smileby pushing gently on the gums.

Although marginal mothers exhibit intuitiveparenting behaviours, there appears to be somemismatching of emotional signals between infantsand marginal mothers. The overall impression givenby chimpanzees with marginal maternal competenceis that they are out of tune with their infants. Infantcues of discomJort tend to be disregarded bymarginal mothers. Caregiving is applied accordingto mother's personai agenda rather than that ofthe infant's. The mismatching may include aninsensitivity to infant crying, treating newborns asif they were much older infants, and either a lackof enjoyment or a lack of gentle caregiving.

Mothers appear to be sensitive to infants' eyegaze and will shift their own gaze away very shortlvafter mutual eye gaze is attained. That instances ofmutual eye gaze are deemed important by bothparfners is illusfrated by one example. One marginalmother often dangled her infant off her body byholding his arms in her feet while she lay on herback on the floor. At2-4 weeks of age he found thisdistressing and often showed unhappiness with apout face and occasional soft whimper. From thebeginning of the observation he had been rootingin search of the nipple, and, 30-40 minutes later,being held away from mother's body was particularivdistressing. He exhibited a small pout face and helooked directly at his mother. She was lookingaround and not at him. As he held his expression,and his eye gaze, she moved her eyes in hisdirection. As the gaze became mutual, he exhibitedan exaggerated pouting expression and emitted alittle whimper and she immediately gathered himto her breast and finally he was able to nurse. Evenat this young age, the infant chimpanzee seems tobe sensitive to the power of the period of mutualeye gaze for communication.

Chimpanzee mothers spend considerable amountsof their time gazing at their young infants andgazing at their infants' face. Chimpanzee infants

Baze at their mothers' faces. There are numerousinstances of mutual gaze every hour within thein-fant's first months of life. We are uncertain aboutthe role played by maternal eye gaze and mutualeye Baze in chimpanzees. Mutual eye gaze inhuman mother-infant pairs is the foundationfor an intricate system of communication (Tronick

Intuit iae P arenting in Chimpanzees 27

et al. , 1979) and intelpersonal interaction (Trevarthen,1979) . In monkeys, mutual eye gaze is exceedinglyrare, and prolonged gazeby an individual monkeyconstitutes a threat. In chimpanzees, mothers arevery attentive to infants, even to the extent ofmonitoring behavioural states as subtle as sleep,startles and cessation of nursing. Very young infantchimpanzees appear to have a greater visual acuityat 30 cm than 15 cm but development of acuity iscomparable to human in{ants (Bard ef aI., 1994).Previous reports of mother-infant chimpanzees orgreat apes indicate very limited episodes of mutualgaze (e.g. Plooij, 1979; Rijt-Plooij and Plooll, 1987;Papouiek et al., 1991). It appears that chimpanzeemothers, however, regulate the duration of mutualgazesby looking away within seconds of achievingmutual eye contact. Short mutual Bazes aredetermined by mothers and not by infants' ability.Neonatal chimpanzees reared in a nursery withhuman adults (due to inadequate maternal care)engage in extended eye-to-eye contact (Bard et al.,1992). Earlv social environments seem to influencethe expression of behaviour as early as 30 days oflife (Bard, in press a; Bard et al., 7992, 7993).Thus, it may be that eye gaze is one of the earlybehaviours that is culturally regulated.

Maternal competence can be simply defined asrearing an infant and incompetence defined asan infant requiring nursery-rearing. Bard (inpress b) argued that the necessary condition forthe emergence of adult competence appears tobe interaction with conspecifics of both sameand diJferent age classes. It appears that earlyexperience facilitates the development of cognitive,social and reproductive competence (e.g. Bard andCardner, 1993; Bard and McDonald, 1994). Theseconditions, however, are not sufficient for theemergence of maternai competence. Although earlymother-rearing provides many benefits, it is not asufficient condition for the expression of maternalcompetence. The most important early experienceappears to be giving care to a younger individual,i.e. direct'hands-on' exposure rather than receivingcompetent maternal care (Bard, in press b). Theoptimal period during which these skills are learnedis during the juvenile period or early adolescence(Bard, in press b).

The uniqueness of human characteristics amongprimates is often a tenuously held position (e.9.Bard et al., 7992; van Lawick-Goodall, 1968).Currently, one area of controversy is teaching,i.e. whether ape parents deliberately instructtheir offspring (Bard and Vauclair, 1984; Bard,1.993; Boesch , 1991). Intuitive parenting behaviours

represent the foundation upon which teaching isbuilt (Papou5ek and Papoudek, 1987). With theuse of encouragement behaviours (Whiten, 1992)or exercise (as used in the present article), apemothers create a supportive environment in whichinfants practise developing skills. Typically, apemothers set up environmental parameters in whichdeveloping skills .a. be practised rather than actuailydemonstrating new skills, as human motherstypically do (Bard, 1993). Recent observations inferal chimpanzees, however, suggest that deliberatedemonstrations do occur in the development oftool-using behaviour (Boesch, 1991) and in thedevelopment of understanding the meaning ofa new communicatory signal (Rijt-Plooij andPlooij, 1987). Perhaps teaching, like tool use andmanufacture and communication, is a behaviourthat is particularly difficult to observe, especiailvunder field conditions. The examples pro.rided byfield researchers clearly indicate that the ability todemonstrate actions to enhance another's under-standing is within the ability of adult chimpanzees.

CONCLUSIONS

1. Behavioura-l repertoires are similar for chimpanzeeswith good maternal competence and those withmarginal maternal competence with two majorexceptions: (a) marginal mothers lack appropriateresponsivity to infani crying and (b) poor mothersmay act in ways that cause infants to cry, includingplacing of very young infants out of physicalcontact.2. Mutual eye gaze occurs in mother-infantchimparzee interactions. Mothers appear to regulatethe duration of mutual grzeby looking away shortlvafter mutual eye contact is achieved.3. Intuitive parenting in chimpanzees is expressedin interaction even with very young infants.Intuitive behaviours reflect sensitive responsivityduring which the mother engages in contingentbehaviour and encourages development of infantcapacities. These behaviours parallel those observedin intuitive parenting in humans.

ACKNOWLEDGEMENTS

Funding was provided by NIH Base Grant RR-00155to the Yerkes Regional Primate Research Centerof Emory University, NIH Grant RR-03591 toR. B. Swenson of the Yerkes Center, NICHDIntramural Research Program funds through the

28 K. A. Bard

Laboratorv of Comparative Ethoiogy, a Max-Planck Society siipend in cooperation with theDevelopmental Psychobiology project to ProfessorH. Papoudek at the Max-Planck Institute forPsychiatry, NICHD-NRSA Research FellowshipHD-07105 to K. A. Bard and NIH Grant RR-06158to K. A. Bard. The Yerkes Center is fuliy accreditedby the American Association for Accreditation ofLaboratory Animal Care. I am extremeiv gratefulto the foilorving people for their assistance: theveterinary staff of the Yerkes Center (jack Orkin,Elizabeth Strobert, Karen Ihde and Brent Swenson);the research assistants who collected the videotapedobservations (Meredith iv{oynahan, Laura Plice,Hon'arcl Coffman, Carolvn Fort, Kathy Cardnerand Josh Schneider); the research assistants whofacilitated data analysis (Jennifer Fineran, SheryllVii l iams, Elizabeth 8e11, Lorissa Creen, LindsayCook and Bernice Pelea); and especially the researchassistants 'who appiied the coding systems to thevideotaped observations (Dana Padgett, MathildeScherer, Benjamin Jones, Lindsev Cohen andClaudia F{erdieckerhoffl. The manuscript was muchimproved due to input frtrm Kathleen A. Platzrnan.Speciai appreciation for their continuing support r,rfthis project is extended to Carolvn Fort, StephenSuomi and Nlechthild and Hanui Papou5ek,

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