ORIGINAL ARTICLE

Gijsbertus G. J. van Adrichem Æ Sri Suci Utami

Serge A. Wich Æ Jan A. R. A. M. van Hooff

Elisabeth H. M. Sterck

The development of wild immature Sumatran orangutans(Pongo abelii ) at Ketambe

Received: 2 August 2004 / Accepted: 19 March 2006 / Published online: 3 May 2006� Japan Monkey Centre and Springer-Verlag 2006

Abstract Orangutans have the longest immature periodand inter-birth interval of all ape species. This may beexplained by a slow life history, the need to developskills or by their relatively solitary lifestyle, which pre-vents a mother from associating with two offspring. Thisstudy of wild immature orangutans at the KetambeResearch Station, Indonesia, describes, with partlycross-sectional, partly longitudinal data, their develop-ment to independence. The study subjects ranged from 1to 11 years of age. Data on their activity budget, diet,mother–offspring proximity and maintenance of prox-imity, association with conspecifics and play behaviorwere collected. The results indicate that immatureorangutans can provide for their own food and trans-port, and therefore were independent of direct maternalcare, at an age of possibly 3 but more clearly 6 years.This is similar to chimpanzees, and refutes the slow lifehistory hypothesis. Immature orangutans remain withintheir mother’s vicinity until the age of 8 years, indicatinga dependence on indirect maternal care, and this coin-cides with the period during which the mother does notproduce another offspring. A female orangutan seemsunable to associate with an older immature while caringfor a new infant. This is consistent with the solitary-lifestyle hypothesis and corroborates the results ob-tained with the Sumatran orangutan population at SuaqBalimbing. However, why an immature depends indi-

rectly on its mother for such a long period remains un-clear. It is possible that it needs to develop ecological orsocial skills or needs the protection of its mother.Unfortunately, no data were available to distinguishbetween these possibilities.

Keywords Orangutan Æ Development Æ Independence ÆImmatures Æ Time budget

Introduction

Primates have a relatively prolonged immature phaseand a slow growth rate compared to other mammalswhen scaled on the basis of body size (Harvey et al.1987; Janson and van Schaik 1993; Ross 1998; Ross andJones 1999). This is especially true for the great apespecies. A long immature phase has been linked to a longinter-birth interval. Great apes, however, vary in thelength of their inter-birth interval (Wich et al. 2004).Orangutan inter-birth intervals are considerably longerthan any of the other great apes (Wich et al. 2004), withthe inter-birth interval of chimpanzees measuring be-tween 5.1 and 6.2 years, gorillas between 3.9 and4.6 years, and bonobos between 4.5 and 8 years, whilethe inter-birth interval of orangutans is 7.0–9.3 years(Galdikas and Wood 1990; Knott 2001; Wich et al.2004). Since weaning of a previous offspring usuallycoincides with the birth of a next offspring (general:Nicolson 1987; chimpanzees: Pusey 1983; gorillas: Watts1991), a long inter-birth interval seems to suggest anextremely long period of dependence in orangutans.

Several sets of hypotheses have been proposed toexplain the slow life history of orangutans compared tothe other great apes. The first set of hypotheses focuseson the slow orangutan life history as an effect of generallife history theory (Charnov 1991, 1993; Stearns 2000).Accordingly, the development of orangutans may beslow in order to reduce the chance of immature mor-tality due to malnutrition (Janson and van Schaik 1993).

G. G. J. van Adrichem Æ S. S. Utami Æ S. A. WichJ. A. R. A. M. van Hooff Æ E. H. M. Sterck (&)Behavioural Biology, Utrecht University,P.O. Box 80086, 3508 TB Utrecht, The NetherlandsE-mail: e.h.m.sterck@bio.uu.nl

S. S. UtamiFacultas Biologi, Universitas Nasional,Jl. Sawo Manila-Pasar Minggu,Jakarta, Indonesia

E. H. M. SterckAnimal Science Department,Biomedical Primate Research Center,P.O. Box 3306, 2280 GH Rijswijk, The Netherlands

Primates (2006) 47: 300–309DOI 10.1007/s10329-006-0193-9

Orangutan development may be slower than that ofchimpanzees due to their more energetically costlyarboreal habits (Knott 1998, 2001; van Schaik andDeaner 2003; Wich et al. 2004). Moreover, it has beensuggested that frugivorous animals have slower life his-tories than folivorous ones (Leigh 1994; but see Rossand Jones 1999). This might also explain why orangu-tans have a slower development than the terrestrial andfolivorous gorillas (Wich et al. 2004). Second, develop-ment-of-skills hypotheses suggest that a long juvenileperiod may be necessary to acquire social (Joffe 1997)and/or foraging skills (e.g., Poirier and Smith 1974; Rossand Jones 1999). Immatures may need to learn socialskills (Joffe 1997) or about food sources (Galdikas1995), the location of food patches and efficient travel(Horr 1977) to achieve ecological independence. Therelatively long development of orangutans to ecologicalindependence has been attributed to the relative unpre-dictability of food availability in the forests whereorangutans occur (Wheatley 1982; Galdikas 1995; Knott1998). This may be reinforced by the phenomenon ofmast years, during which many tree species produceabundant food, and a number of species, includingspecies important for orangutans, typically fruit only inthese years (Knott 1998; Wich and van Schaik 2000).Since mast years occur at irregular and long intervals,immature orangutans may require an extended period tolearn about these important food sources.

While the previous hypotheses predict a relativelylong immature period for orangutan immatures relativeto chimpanzees, this was not found to be the case in arecent paper for the immatures of the Sumatran orang-utan population at Suaq Balimbing (van Noordwijk andvan Schaik 2005). Data on this population suggest thatimmatures gain locomotor and nutritional independencefrom their mother at an age comparable to that ofchimpanzees, although longer than the immature phaseof gorillas (van Noordwijk and van Schaik 2005).Moreover, ecological independence is gained at a similarage in orangutans and chimpanzees. These results seemto refute the hypotheses of slow development and a longperiod required for learning skills. However, they cannotexplain the long orangutan inter-birth interval relative tochimpanzees. Adult female orangutans and chimpanzeesmay, however, differ in the costs of association. It hasbeen suggested that the general food availability inSoutheast Asia is lower than in Africa (Terborgh andvan Schaik 1987). As a result, orangutan mothers maynot be able to associate permanently with both a newinfant and an older offspring (Borneo: Galdikas andTeleki 1981). However, the older immature may need toassociate with its mother for the acquisition of particularskills (see above) or for protection from predators orcompetitors. This gave rise to a third hypothesis, thesolitary-lifestyle hypothesis (van Noordwijk and vanSchaik 2005). This hypothesis argues that orangutanmothers associate with the latest offspring until it isecologically independent, but since she cannot perma-nently associate with an older immature while caring for

an infant, the mother has an extended inter-birth inter-val. This hypothesis combines an extended ecologicaldependence of the immature on its mother, to learn skillsfrom their mother (i.e., the second hypothesis) or toobtain her protection, with ecological limitations ongroup formation.

The solitary-lifestyle hypothesis (van Noordwijk andvan Schaik 2005) has recently been proposed to explainthe behavior of the immature orangutans of Suaq Ba-limbing, Sumatra. This hypothesis is specific toorangutans and depends on one population of orangu-tans. Such hypotheses always run the risk of formingpost hoc explanations for the results found. Therefore,tests with independent data are required. Here we testthe validity of the solitary-lifestyle hypothesis of vanNoordwijk and van Schaik with data on the orangutansof the Ketambe Research Station, Sumatra.

We provide partly longitudinal, partly cross-sectionaldata on the behavioral development of four immaturesof the Ketambe Research Station, Sumatra. The averageinter-birth interval at Ketambe is 9.3 years (Wich et al.2004) and thus almost a year longer than in Suaq Ba-limbing (Wich et al. 2004; van Noordwijk and vanSchaik 2005). We indicate when immatures in the Ket-ambe population reach locomotor, nutritional and eco-logical independence of their mother and discuss thesetimes in relation to the above-mentioned hypotheses.

Methods

Study area and subjects

This study was conducted at the Ketambe ResearchStation (3�41¢N, 97�39¢E), Gunung Leuser NationalPark, Leuser Ecosystem, Northern Sumatra, Indonesia.The area consists mainly of undisturbed primary low-land rain forest as described by Rijksen (1978) and vanSchaik and Mirmanto (1985).

The orangutan population at Ketambe ResearchStation is well known and has been studied since 1971(Rijksen 1978; Schurmann 1982; Schurmann and vanHooff 1986; Sugardjito 1986; Mitrasetia 1995; Utami2000; Wich et al. 2004). All individuals that visit the arearegularly are recognized. The four study animals forwhom data of several years were available (Setia, Yossa,Herman, Chris) were born in the wild. Other immatureswere also observed, but no systematic data were avail-able. Setia and Yossa are the sons of wild Sina and Yet,respectively. Chris is the daughter of wild Ans (whosemother was rehabilitant Binjai) and Herman is the sonof rehabilitant Getty. Sina gave birth to her subsequentoffspring in March 2001, Yet in April 2001 and Ans inFebruary 1996. Getty died in 1997 when Herman was9 years old. In this study, these four animals were fol-lowed in four different years (1993, 1994, 1995 and 1999;Table 1). The combined data from the four animalsencompasses the ages 1–11 years, although no data wereobtained for immatures of 4, 9 and 10 years old. The low

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number of individuals did not allow for conclusions onsex differences in development.

Data collection

The data were collected from April 1993 until October1995 by S.S. Utami and field assistants and from Feb-ruary 1999 until August 1999 by G.G.J. van Adrichemwith the help of S.S. Utami and field assistants. Datawere collected in a standardized manner.

The behavior of a study animal was recorded usingthe instantaneous focal-animal sampling technique(Martin and Bateson 1993), recording behavior everyminute. Days were excluded from analysis for certaintypes of behavior if a bout longer than 30 min wasmissing, or if more than 90 observation minutes in totalwere missing between 0600 and 1900 hours for this typeof behavior. Minutes were missing when the animal wasfound later on a day or when it moved into dense foli-age. For example, on some days it was possible to recordenough minutes on the category ‘‘distance to mother’’,while not enough minutes on the category ‘‘activitybudget’’ were recorded. Consequently the number ofdays used varies for the different analyses.

In the activity budget the following behavioral cate-gories were distinguished: feeding, solitary play, socialplay, moving, clinging and resting. Feeding started whenthe focal animal picked a food item and ended when thefocal animal did not take a food item for more than aminute and had stopped chewing. Solitary play is mov-ing and object manipulation without a clear goal. Socialplay is the play performed together with a conspecificimmature or subadult individual. Moving is the changeof location of the total body that is not in a feeding orplaying context. Resting occurs when the focal animal isnot feeding, playing or moving (thus clinging is includedin resting). Clinging, hanging on the mother, is alsoanalyzed separately from resting. The diet was subdi-vided into six classes: figs, fruit, leaves, insects, mother’s

milk and other. The absence or presence (within 30 m)of the two nearest neighbors was recorded. The distanceto the two nearest neighbors within 30 m was measuredwith three classes: 0–2 m (within reach); 2–10 m (withinthe same canopy); and 10–30 m (30 m is the maximumvisibility for the observer).

The activity budget data of the immatures werecompared with the data of six adult females. Adult fe-males have a roughly similar body size to older imma-tures (Rijksen 1978) and are therefore considered as areasonable reference point for immature requirements.Immatures were considered to reach nutritional andlocomotor independence when this behavior becamecomparable to that of adult females. These data werecollected by Margriet Berents and the field assistantsfrom February to September 1998 using the samemethods. Data were collected for an average of 11(range 5–16) follow days per female.

An approach–leave (A–L) index was calculated forinitiative to maintain or break contact between motherand offspring. A bout of ‘approach’ or ‘leave’ startedwhen one animal passed one of the distance classes: 1, 2,3, 4, 5, 10, 15, 20 or 30 m. The ‘approach’ and ‘leave’were considered to have ended when one of the animalsinitiated, respectively, a ‘leave’ or an ‘approach’. Theapproach index was calculated by taking the proportionof approaches made by the offspring (Apo) of the totalnumber of approaches made by offspring and mother(Apm) minus the proportion of leaves made by the off-spring (Lvo) of the total number of leaves made by off-spring and mother [Apo/(Apo + Apm)] � [Lvo/(Lvo + Lvm)] (Hinde and Atkinson 1970). The magni-tude of the result falls within the range �1 to +1. Re-sults of �1 and +1 mean the initiative to maintainproximity is, respectively, taken completely by the mo-ther or the offspring. A result of 0 indicates that both themother and the offspring initiate the same proportion of‘approaches’ as they do ‘leaves’. For this analysis onlyobservation days were included in which both the totalnumber of ‘approaches’ and the total number of ‘leaves’

Table 1 Name, sex, age, number and period of observation days per focal animal used in the analyses of behavior. A–L index Approach–leave index

Individual Sex Birthdate

Age(years)

Activitybudget

Diet Solitarydays

A–Lindex

Distanceto mother

Observationperiod

Setia Male Jan 1993 2 1 1 1 – 1 Jan 19956 4 4 7 7 7 May–Jun and Aug 1999

Yossa Male Aug 1992 1 5 5 5 5 5 Nov 1993 and Feb 19943 2 2 3 1 3 Aug–Sep 19956 9 9 9 9 9 Mar–Jul 19997 4 4 4 3 4 Aug 1999

Herman Male Feb 1988 5 18 12 18 15 18 May and Nov 1993–Jan 19946 15 15 16 14 16 Nov–Dec 1994 and Jan 19957 1 1 1 1 1 Oct 199511 9 9 8 – – Jun–Aug 1999

Chris Female Sep 1987 5 8 – 8 5 8 Apr–May 19936 5 5 5 4 5 Nov 1993–Jan 19947 1 1 1 2 2 Aug 19958 4 4 5 4 5 Sep 199511 7 7 9 3 9 Feb–Apr and Jun–Aug 1999

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were at least 7. This to decrease the standard deviationamong the different days.

Two measures for the association of the immatureanimal with conspecifics were calculated (Wich et. al.1999). First, the proportion of social days was calculatedas the number of days with at least one conspecific otherthan the mother within 30 m for any amount of timedivided by the total number of observation days at thatage. Second, the time spent social was the proportion oftime spent on a day with at least one conspecific otherthan the mother within 30 m divided by the totalobservation time that day. Immatures were consideredto reach ecological independence when they no longerassociated on a daily basis with their mother.

Statistics

For analyses of the data, daily values were calculated(except for the association with conspecifics calculatedas the proportion of social days because each day al-ready has a value, 0 or 1) and from these values averageswere calculated per individual per month. From themonthly averages, averages were calculated for eachyear of age. With the limited data set no exhaustivestatistical analyses were possible. This results in partlydescriptive results. Statistical tests were conducted whenpossible. Since the data showed a normal distribution,parametric statistical tests were employed. The testswere two-tailed with a =0.05. All statistics were calcu-lated using SPSS (SPSS, Chicago, IL).

Results

Gradual changes with age of developing orangutans areshown for activity budget, distances to the mother andthe initiative to maintain this, the percentage of timeneighbors are present and the amount of solitary andsocial play. ANCOVA tests, with the individual as factorand age as covariant, showed no interaction effect be-tween individual identity and age for all types ofbehavior (Table 2). The effects of individual identity andage on behavior are reported.

Activity budget

The effects of immature age on the activity budgets weredetermined (Fig. 1). The proportion of time spent rest-ing decreased and the time spent feeding increased sig-nificantly with age, whereas age had no significant effecton moving (Table 2). Significant individual differencesoccurred for time spent moving, and a trend appearedfor time spent resting, indicating that different individ-uals had different developmental trajectories. Since thereis no interaction with age, this effect is not considered inthe remainder of the paper. Visual inspection of the data(Fig. 1a,b) suggests that the level of feeding and restingleveled at an age of 6 years. The immature time budgetdata are compared with the data of adult females. Theaverage value and the range of feeding, resting andmoving are shown (Fig. 1a,b,d). Feeding reached theadult female range at 3 years and all data were withinthis range starting from 6 years of age. One individual(aged 7 years) was feeding more often and several indi-viduals (aged 7–11 years) were resting less than the adultfemale range.

Clinging to the mother is observed until the age of6 years (Fig. 1c). An ANCOVA-test excluding imma-tures of 8 years and older showed that the proportion oftime spent clinging decreased significantly with age(Table 2). Visual inspection reveals a large drop in theproportion of time spent clinging to the mother between2 and 3 years of age (Fig. 1c). This corresponds to anincrease in the proportion of time spent moving(Fig. 1d), possibly indicating that after 2 years of ageimmature orangutans usually travel independently.Immature moving showed a much wider variation thanfemale moving from the age of 3 to 7 years. It seemed toconverge within the female range possibly at the age of8, but more likely at 11 years of age.

The diet of immature orangutans from the age of 1 to11 years did not show any apparent changes with age(Fig. 2). The amount of time spent suckling was very lowthroughout the study period and no substantial decreasewas visible. Suckling behavior was no longer present inthe activity budget at 8 years of age. It was expected thata large proportion of the feeding time of young immatureindividuals would consist of suckling. However, alsothese young immature animals were observed to spendonly a small proportion of the time suckling (Fig. 2).

Distance between mother and offspring

The distance between mother and offspring increasedgradually with increasing age of the offspring (Fig. 3).Accordingly, the amount of time immatures were adistance of 0–2 m of their mother significantly decreasedwith age and the amount of time spent > 30 m signifi-cantly increased with age (ANCOVA, Table 2). Visualinspection of the data indicates a large increase in dis-tance at the age of 3 years, the distance changed frommostly within 2 m to larger distances. Similarly, at

Table 2 Results of ANCOVA-tests for immature activity budget,distance to mother and the A–L index. Significance of effect of thefactor individual identity and the covariate age and their interac-tion

Behaviour n Interaction Individual Age

F P F P F P

Moving 15 0.963 0.462 3.829 0.046 0.346 0.570Resting 15 0.513 0.686 3.474 0.059 15.381 0.003Feeding 15 0.351 0.790 0.877 0.486 12.828 0.005Play 15 1.141 0.396 0.375 0.773 1.430 0.259Clinging 12 1.800 0.287 1.050 0.428 18.943 0.003Distance 0–2 m 14 0.375 0.775 1.617 0.253 24.348 0.010Distance >30 m 14 3.018 0.116 0.845 0.503 11.484 0.008A–L index 13 3.525 0.097 0.058 0.980 2.215 0.175

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7 years of age an increase in the time spent at more than30 m distance from their mother is apparent.

Approach and leave between mother and offspring

The A–L index showed that the offspring was usuallyresponsible for maintaining proximity with its mother

(Fig. 4) and this did not change significantly withimmature age (Table 2). Visual inspection indicates nosudden changes. Remarkably, the only data point wherethe mother was responsible for maintaining proximitywas found for the oldest individual.

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Fig. 1 The relationshipbetween age and the proportionof time spent per day while afeeding, b resting (includingclinging), c clinging and dmoving. In a, b, and d data ofsix adult females arerepresented for comparison.Solid horizontal line Averagetime budget of these six adultfemales, dotted lines minimumand maximum values

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Fig. 2 The relationship between age and the proportion of timespent per day feeding on each food category

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Fig. 3 The relationship between age and distance to the mother,measured as the proportion of time spent per day in each distancecategory

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Association with conspecifics

The time spent in association with the mother or otherconspecifics was determined. Until 8 years of age im-matures associated with their mother every day(Fig. 5a). At an age of 11 years, however, they weretraveling solitarily for periods of a few days at a time.

The time per day spent in association gives a slightlydifferent picture. After 6 years of age the immatureanimals started to range more than 30 m away fromtheir mother (Fig. 5b). Although at 7 and 8 years of ageimmature animals were not close to their mother, theywere rarely solitary because they often joined otherconspecifics (Fig. 5b). However, by 11 years of age theimmature was solitary for a substantial proportion offocal time (65%, Fig. 5b).

Play

The total time spent playing did not differ significantlywith age (Table 2). Play was divided into solitary playand social play, but due to their infrequent occurrence itwas not possible to test the results statistically. At 1 and2 years of age solitary play occurred in approximately20% of observations, but was exhibited at a low level at3 years of age and older (Fig. 6).

The relationship between social play and the presenceof potential play partners was investigated. The focalanimals were rarely observed to play with their mother,and hardly ever with other adults (females and flangedmales). Therefore, only juveniles, adolescents and un-flanged males were considered potential play partnerswhen present within 30 m. A significant relationshipexisted between the occurrence of social play and theproportion of time play partners were within 30 m(ANCOVA: F =72.152; P =0.001; n =15), but thiswas difficult to interpret since the interaction betweenindividual identity and possible play partners was also

significant (ANCOVA: F =13.083, P =0.003, n =15).Social play was almost absent until the age of 6 yearsand peaked at 8 years of age.

Discussion

Orangutan females have longer inter-birth intervals thanother great apes, and the Ketambe orangutan popula-tion has the longest of them all (Wich et al. 2004). Threeexplanations have been suggested to account for thislong inter-birth interval: an effect of a general slow lifehistory pace; a need for immatures to develop skills; theobligate relatively solitary lifestyle that prevents a mo-ther from associating with two offspring. Data of an-other Sumatran orangutan population at SuaqBalimbing suggest that the long inter-birth interval inorangutans is attributable to the ecological costs of themother associating with more than one offspring (vanNoordwijk and van Schaik 2005). We investigatedwhether the hypothesis suggested for Suaq Balimbinghas general applicability and can also account for the

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Fig. 4 The relationship between age and the mother–immatureapproach–leave (A–L) index. (See Methods section for the formulafor calculation of this relationship)

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Fig. 5 The proportion of days (a) and the proportion of minutes(b) spent within 30 m of the mother or another conspecific inrelation to immature age. When data of more than one individualof the same age were pooled, the s.e. is given

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characteristics of the immature period in the distant (in astraight line 70 km, but separated by a high mountainrange), although also Sumatran, orangutan populationat Ketambe.

The Ketambe immatures reached nutritional inde-pendence possibly at an age of 3 years and most likely atan age of 6 years. Unfortunately, no, or only limited,data were available for animals from 3 to 4 years of ageand a more accurate estimate of the age of independentfeeding was therefore not possible. Their feeding timewas similar to that of adult females, although this mayoverestimate their food intake since immatures are lessefficient at harvesting food than adults (Massen 2004,S.A. Wich, personal observation). This potential lowerfood intake may be compensated by lower foodrequirements, because immatures have a smaller bodysize than adult females (Bogin 1999). Accordingly, the 3-year-old immature was not seen to suckle during the day(Fig. 2), potentially indicating that 3-year-old orangu-tans can largely or completely obtain their own food.Some caution is necessary though, since this was basedon very few data. In addition, also for orangutans of 1and 2 years of age only a small amount of time sucklingis observed, but this may be an underestimate since it isdifficult to observe this behavior when the animals are indense foliage, clinging to their mother or in a day ornight nest. Moreover, older immatures were also ob-served to suckle. Altogether, the amount of time theanimals are suckling might be a poor indicator for theamount and quality of milk the animals receive. Sincethe amount of suckling in infants may be underestimatedand the amount and quality of the milk cannot beestablished, suckling time appears to be a poor indicatorof independence.

Another indication of independence was given by theimmature moving pattern. Possibly at 3 but, due to thelimited number of data at this age, more clearly at6 years of age the Ketambe immatures reached loco-motor independence. They clung to their mother only aminor proportion of their time and were moving atsimilar or even higher rates than adult females. They

were also often found beyond their mother’s reach, al-though they were never far from their mother until theage of 6 years. The relatively high proportion of movingfound for some individuals may indicate that immaturesbetween 3 and 7 years of age were less efficient in trav-eling than adult females. However, these immaturesmaintained contact with their mother, indicating thatthey could keep up with her, or at least that their motherbehaved so the immatures could maintain proximity.Although we cannot determine whether the mothersadjusted their behavior to their offspring’s locomotorabilities, these immatures were largely responsible fortheir own transport.

Overall, possibly 3-year-old, but more clearly 6-year-old orangutans seemed able to provide their own foodand transport. This age of independence of directmaternal care is similar to that found for the Suaq Ba-limbing orangutans (van Noordwijk and van Schaik2005) and other data on orangutan development (pre-vious Ketambe data—locomotor independence at5 years: Rijksen 1978; Borneo—locomotor indepen-dence at 4 years: Galdikas 1985, or 5 years, Bard 1995;independent feeding at 4–5 years: Bard 1992). Further-more it shows similarity with the age of nutritional andlocomotor independence in chimpanzees (Clark 1977;Pusey 1983; van de Rijt-Plooij and Plooij 1987; Hiraiwa-Hasegawa 1990a, b, c), and a similar or older age ofindependence than in gorillas (Schaller 1972; Fossey1983; Watts and Pusey 1993). Thus, in line with thefindings of other populations of orangutans and chim-panzees, also at Ketambe direct maternal care is notrequired for immatures of possibly 3-year-old, but moreclearly immatures of 6 years and older. Accordingly, alow growth rate or long nursing period do not seem toresult in a relatively long dependency of immatureorangutans, yet this population has a very long inter-birth interval. This indicates that the slow-life-historyhypotheses cannot explain this combination of features.

Although we have no data on social skills, social playwas almost absent during the first years of life, com-mencing only at an age of 7–8 years. Since social playmay be essential to develop social skills (Sugardjito et al.1987; Fagen 1993), this seems to suggest that thedeveloping skills hypothesis may account for the longfemale investment in her latest offspring.

Even though possibly 3-year-old, but more clearly 6-year-old immatures at Ketambe have reached nutri-tional and locomotor independence, they are in dailycontact with their mother until 8 years of age. They startto leave their mother during part of the day at 7 years ofage, but only the oldest, 11-year-old immature wastraveling independently and alone, similar to adult fe-male orangutans (Wich et al. 1999). This indicates thatthese immatures are ecologically dependent until an ageof 8–10 years. These results are similar to those of otherstudies on orangutans (van Noordwijk and van Schaik2005) and chimpanzees (Pusey 1983).

The cause of the long period of association with themother cannot be determined with our data. Anecdotal

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Fig. 6 The relationship between age and the proportion of time perday spent playing solitarily or with another conspecific, and theproportion of time potential play-partners (other than the mother)were present

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evidence, however, suggests that immatures are ecolog-ically dependent on their mother. An orangutan mothermay provide her latest offspring with protection againstpredators or competitors. At Ketambe, both tigers(Pantera tigris) and clouded leopards (Neofelis nebulosa)can prey on orangutans (Rijksen 1978). Predation maybe an especially serious risk for immature orangutansweighing less than 10 kg, as indicated by repeated kill-ings of immature rehabilitants at Ketambe by a cloudedleopard (Rijksen 1978). In contrast to this high risk forimmatures without a mother, the predation rate on wildimmatures appears low, as evidenced by the loworangutan mortality and the low incidence of predationon wild orangutans (Wich et al. 2004). In addition, it hasbeen suggested that a mother provides protectionagainst competitors. Yet while aggression from otherprimate species, such as pig-tailed macaques (Macacanemestrina) and siamang (Symphalangus syndactylus),may sometimes cause an adolescent orangutan to bedisplaced in a food patch (S.A. Wich, personal obser-vation), this is of such low frequency that it cannot ex-plain the exceptionally long mother–offspringassociation. Furthermore, aggression from adults toimmature orangutans is uncommon and therefore alsoan unlikely explanation for the long mother–offspringassociation. Thus, the mother may provide protectionfor the immature against predation, but probably notagainst competitors. However, predation is a potentialcause of mortality also in chimpanzees (Boesch 1991;Boesch and Boesch 2000; Nishida et al. 2003). There-fore, the risk of predation does not explain why the in-ter-birth interval is longer in orangutans than inchimpanzees.

Immatures may also associate with their mother toobtain special skills. Recent data from an orangutanpopulation in Borneo suggest that immatures are al-ready competent at acquiring and processing many fooditems at an estimated age of 4 years, well before leavingtheir mother (Massen 2004). Yet their skills will accountonly for the food species they have already encountered.Due to the mast phenomenon of the Southeast Asianforests (Wich and van Schaik 2000), many trees fruitonly once every several years (Fredriksson et al. 2006;Wich et al. 2006) and it may take years before orangutanimmatures have encountered all relevant tree specieswith their locations and way of processing. However,more data are required to address whether the excep-tionally long association with the mother is necessary tolearn about rare but essential food.

The inter-birth interval of the Ketambe orangutansindicates that a female starts a new reproductive cycleonly when her previous offspring has reached a relativelyold age. This is in keeping with the solitary life-stylehypothesis, which assumes that females are unable tostart a new reproductive cycle when accompanied on adaily basis by her last offspring (van Noordwijk and vanSchaik 2005). This interpretation is also consistent withthe data on the time spent with conspecifics (Fig. 5b),

which suggest that females with offspring do not havemany associates.

In conclusion, our data corroborate the solitary life-style hypothesis proposed to explain the slow repro-ductive rate of the Suaq Balimbing orangutans. AtKetambe, immature orangutans of possibly 3 years, butmore clearly 6 years and older do not require directmaternal care to obtain sufficient food or transport.However, they obviously depend on their mother’spresence until an age of 8–10 years. Since adult femalesaccompanied by offspring seem to refrain from associ-ating with additional conspecifics, this suggests that afemale cannot combine the care of an infant with thecare of a relatively independent but associated offspring.Therefore, the solitary lifestyle hypothesis is not a posthoc hypothesis explaining the results of one populationonly, but seems a general explanation for the long inter-birth interval in orangutans. However, whether imma-tures associate with their mother until 8–10 years of ageto obtain foraging or social skills or to receive protectionremains an open question.

Acknowledgements We wish to thank the Indonesian Institute ofSciences (LIPI) in Jakarta, the Indonesian Nature ConservationService (PHPA) in Jakarta, Medan and Kutacane, UniversitasNasional (UNAS) in Jakarta and the Leuser Development Pro-gramme in Medan for granting permission and giving support toconduct scientific research in the Ketambe Research Station situ-ated in the Leuser Ecosystem. We thank the Netherlands Foun-dation for the Advancement of Tropical Research (WOTRO) andthe Netherlands Organization for Scientific Research (NWO) forlong-term financial support for the research at Ketambe. We thankthe European Commission and the Indonesian Government forfunding the Leuser Development Programme. We gratefullyacknowledge Matplin, Sulaeman, Abu Lubis, and SusannahThorpe for their help in the field with the data collection. Fur-thermore, we would like to thank Kim Bard, Estelle Nijssen, AnneRusson, Susannah Thorpe and two anonymous referees for com-ments which improved the manuscript and Han de Vries for hishelp with the statistical analyses.

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