Developmental Changes in Feeding Behavior and Maternal Influences in Wild Javan Gibbons (Hylobates moloch)

Abstract

Immature primates acquire skills through social learning from more experienced individuals. The needing-to-learn hypothesis posits that prolonged juvenility evolved to support such social learning under social and ecological challenges. In particular, feeding complexity—food requiring complex skills—poses challenges. Despite prolonged juvenility, the development of feeding behavior and social learning in gibbons remain poorly understood. We examined the feeding behavior of four offspring (aged 9 to 50 months) and their mothers in three habituated groups of wild Javan gibbons (Hylobates moloch) in Gunung Halimun-Salak National Park, Indonesia (December 2019 to January 2022). We analyzed the effects of immature age and food size on 1) immature’s dietary breadth and diet similarity with mothers, 2) daily proportion of time the immature spent feeding and co-feeding with mothers, and 3) responsibility for maintaining close proximity to mothers during feeding, using the Hinde index. Immature dietary breadth increased with age, whereas diet similarity with mothers decreased with age. Daily feeding time increased with age, but this increase was weaker for medium than for small food. Co-feeding time with mothers decreased with age, with a significantly stronger decline for medium than for small food. Although immatures became less responsible for maintaining proximity to mothers during feeding with age, they stayed closer when feeding on large than on small food. Our results showed developmental changes in feeding behavior and suggested maternal influences on information acquisition in wild Javan gibbons, highlighting how social and ecological factors shape feeding development and potential social learning in immature primates.

Introduction

Primates face social and ecological pressures that are cognitively demanding (Sawaguchi, 1992). Social complexity, such as large group size and complex social structures, is associated with brain size in primates and is suggested to have driven primate cognitive evolution (Byrne & Bates, 2007; Deaner et al., 2003; Dunbar, 1998; Reader & Laland, 2002). Ecological complexity, such as features of the diet, the spatiotemporal distribution of food, and extractive feeding, also has been proposed to drive the evolution of primate intelligence (DeCasien et al., 2017; MacLean et al., 2009; Shultz & Dunbar, 2022; Milton, 1981; Gibson, 1986; Rosati, 2017). These two complexities operate together at different intensities in different species of primates, and both social and ecological challenges have been proposed to have led to prolonged juvenile periods in primates (Walker et al., 2006).

The needing-to-learn hypothesis posits that immature primates need time to acquire adult-level social and feeding skills to overcome social and ecological challenges, which in turn leads to the prolonged juvenile periods (Ross, 1999). Prolonged juvenile periods can compensate for the costs associated with delayed maturation, such as reduced chances of reproduction (Ross & Jones, 1999). Evidence from species with complex feeding skills, such as chimpanzees (Pan troglodytes) (Rapaport & Brown, 2008) and capuchin monkeys (Cebus capucinus) (Eadie, 2015), supports the needing-to-learn hypothesis. Studies of frugivorous primates provide stronger support for the needing-to-learn hypothesis than studies of folivorous primates, likely owing to the relatively greater complexity of frugivore foraging niches (Clutton‐Brock & Harvey, 1980; Schuppli et al., 2016a). For example, despite similar body size in two sympatric species, frugivorous spider monkeys (Ateles geoffroyi) have longer periods of maternal dependence than folivorous howler monkeys (Aloutta palliata), suggesting that cognitive challenges from the fruit-eating environment may have led to prolonged juvenility (Milton, 1981).

Investigating age-related variation in feeding behavior helps us to understand how feeding skills develop in immature primates, including the potential role of social learning as immatures grow up. Despite being primarily dependent on suckling, infant primates start consuming solid food in their early development (Rapaport & Brown, 2008). As the nutritional requirements of infants change, the time spent suckling gradually decreases, while feeding time spent on solid food consumption increases until weaning (Matsumoto, 2017). The dietary breadth of infants also increases until weaning and eventually becomes similar to that of adults (Lonsdorf et al., 2021). There may be important maternal influences on early feeding development as infants spend most of their time with their mothers and are physically dependent on them, which can provide opportunities to learn from mothers. For example, infant Japanese macaques (Macaca fuscata) spend considerable time co-feeding with their mothers, showing synchronous feeding behavior with their mothers (Ueno, 2005). Immature mountain gorillas (Gorilla gorilla beringei) can learn socially from their mothers by close co-feeding or observational learning, eventually showing a very similar diet to their mothers (Rapaport & Brown, 2008). After weaning, maternal influences on the development of feeding behavior may decrease with age of immatures. For example, immature orangutans (Pongo pygmaeus wurmbii) slowly decrease co-feeding time with their mothers and show decreased diet similarity with their mothers, suggesting developmental changes in the feeding behavior (Jaeggi et al., 2010). However, juveniles still stay close to their mothers in feeding contexts, indicating potential maternal influences on diet during juvenility (Schiel & Huber, 2006; O’Mara & Hickey, 2012).

Proximity to a feeding individual reflects social tolerance, which is considered critical in opportunities for social learning (van Schaik, 2002; van Schaik et al., 1999). Immature orangutans actively maintain proximity to their mothers while foraging, suggesting that being close to competent individuals enables immature orangutans to acquire information about food items and food-processing skills (Jaeggi et al., 2008). As close observation of other’s behavior facilitates feeding efficiency through social learning, the frequency of these behaviors may increase with greater foraging difficulty. Foraging difficulty can arise from factors such as food size and complex food processing skills (Jordano, 1995; Martin, 1985; McGraw & Daegling, 2012). For example, golden-backed uakaris (Cacajao ouakary) prefer small over large fruit; the latter took six times longer to process despite being equally abundant (Dias da Silva et al., 2020). Similarly, immature capuchin monkeys consume more easily accessible food items and fewer difficult-to-acquire ones than adults, reflecting developmental limitations in physical ability and feeding competence (Eadie, 2015). Additionally, immature primates selectively observe social partners based on food size (Perry & Jimenez, 2006). Immature orangutans tend to approach skilled adults more closely and observe them more frequently when manipulating difficult food items compared to easy ones (Schuppli et al., 2016a). Infant chimpanzees approach their mothers and observe intently while their mothers crack nuts, suggesting that immatures learn socially from others by approaching and observing behavior (Schuppli & van Schaik, 2019).

In gibbons (family Hylobatidae), immaturity accounts for approximately 28% of the lifespan (Brockelman et al., 1998; Geissmann, 1991), potentially allowing them to acquire complex skills through social learning during development. Immature gibbons consume their first solid food at 4 months of age and wean typically around 22 months of age (Berkson, 1966; Treesucon, 1984; Yi et al., 2020). Immature gibbons need to overcome ecological obstacles, such as the spatial and temporal variability of food resources, food size, and difficult-to-process food items that have thick shells and difficult-to-obtain food items that grow on tree trunks or on the ground (Asensio et al., 2011; Kim et al., 2011; Yi et al., 2020). Moreover, gibbons have socially tolerant intra-group relationships (Burns et al., 2011; Rutberg, 1983), which may allow immature individuals to acquire information through close observation of others, including in feeding contexts. Such socially tolerant relationships may allow immature individuals to acquire information through close observation of others, including in feeding contexts. Immature Javan gibbons (Hylobates moloch) acquire adult-level knowledge of food during their infancy through food solicitation toward their mothers, which leads to tolerated food transfers from mothers to immatures (Yi et al., 2020). However, beyond this food solicitation and tolerated food transfer, how immature gibbons develop and learn feeding skills from other group members remains unstudied.

Our study species, the Javan gibbon, is a pair-living primate in which offspring remain in their natal group with both parents for 8 to 10 years or more (Brockelman et al., 1998; Geissmann, 1991). During this prolonged developmental period, they face ecological challenges, such as the spatial and temporal variability of food resources and the need to process difficult-to-obtain items (Kim et al., 2011; Yi et al., 2020). Javan gibbons live in socially tolerant groups, where adults maintain a low frequency of aggression to juvenile offspring, which may allow immatures to have more opportunities of social learning (Choi et al., 2023). These ecological and social characteristics make the Javan gibbons a valuable species for investigating developmental changes in feeding behavior and the potential social learning in feeding context.

Therefore, to investigate developmental changes in feeding behaviors and social influences, we examined the effect of age of the immature and food size on (1) daily dietary breadth and diet similarity with the mother to assess changes in feeding diversity and overlap, (2) the daily proportion of time the immature spent feeding and co-feeding with the mother to evaluate shifts in feeding independence, and (3) the frequency of approaches and withdrawals between the mother and immature using the Hinde index (Hinde & Atkinson, 1970) to measure patterns of proximity maintenance. We applied a simple measure—food size—as an ecological parameter, which enables us to investigate whether such basic ecological factors influence feeding behavior of immatures and potential social learning during development.

Methods

Study Site and Subjects

The study site was in the Citalahab Sentral area of Gunung Halimun-Salak National Park (GHSNP), West Java, Indonesia (− 6.740350, 106.530280) (Fig. S1 in Supplementary Material). Ewha Womans University established the research site in 2007 and have conducted research on the behavior and ecology of Javan gibbons in collaboration with IPB University and an Indonesian NGO called Yayasan Konservasi Ekosistem Alam Nusantara (KIARA). The study subjects were three habituated groups (A, B, and S) of wild Javan gibbons, each consisting of an adult male–female pair and their offspring (Table 1). Although the paternity was not confirmed, because the pair has not been changed and extra-pair copulation has not been observed during long-term observation over 18 years, we used the term “parents,” “mother,” and “father” to indicate the only adults in each group.

Table 1. Composition of three study groups of Javan gibbons (Hylobates moloch) in Gunung Halimun-Salak National Park, Indonesia from December 2019 to January 2022

Group/adult pair (male & female)	Offspring	Sex	Date of birth	Age range during the study	Age class during the study
A/ Aris & Ayu*	Amore	Male	Dec 2010	9 years – 11 years	Adult
	Awan	Male	Dec 2013	6 years – 8 years	Adolescent
	Ajaib*	Unknown	Oct 2018	1 year 2 months – 3 years 3 months	Infant (disappeared in Feb 2021)
	Arush	Unknown	Nov 2021	0 month – 2 months	Infant
B/ Kumis & Keti*	KimKim	Male	Apr 2011	8 years 8 months – 10 years 9 months	Adult (dispersed in Mar 2020)
	Komeng	Male	May 2014	5 years 7 months – 7 years 8 months	Adolescent
	Kendeng*	Male	Nov 2017	2 years 1 month – 4 years 2 months	Juvenile
S/ Sahri & Surti*	Salwa	Male	Unknown	Unknown	Adult (dispersed in Dec 2020—Mar 2021)
	Sanha	Female	May 2014	5 years 7 months – 7 years 8 months	Adolescent
	Setia*	Male	Jan 2018	1 year 11 months – 4 years	Juvenile
	Soojung*	Male	Feb 2021	0 month – 11 months	Infant

*Each group’s focal individuals, mother and immature

We followed the age class categories described by Brockelman et al. (1998): 0–2 years as infants, 2–5 years as juveniles, 5–8 years as adolescents, and over 8 years as adults. We based the age class on the beginning of the study period (December 2019) (Table 1). Unfortunately, one of the immatures (Ajaib) disappeared in February 2021, so we included data for Ajaib and his mother Ayu until this point. Because of the low visibility of young infants, which might result in low data quality, we excluded a newborn infant (Arush) from the data.

Data Collection

The two first co-authors and four local field assistants collected behavioral data from the three groups from December 2019 to January 2022. We followed mothers and their immatures in each group from sleeping tree to sleeping tree. We used scan and focal sampling (Altmann, 1974). During scan sampling, we recorded data every 10 min by using binoculars, as follows: (1) the proximity between immatures and their parents (measured in meters), (2) the activity of each group member (foraging, moving, resting, grooming, social and solitary play), and (3) the food species consumed when foraging (recorded at the species level). We also used 30-min focal sampling sessions conducted every hour (i.e., 30 min of data recording followed by a 30-min break) to record data from both the mother and the immature. Two observers, the first author and a research assistant, collected focal data concurrently, with one observer focusing on the mother and the other on the immature. During each focal sample, we recorded the feeding behaviors of the mother and the immature, defined as starting when a focal individual brings a food item to the mouth and ending when the food item is fully swallowed. Specifically, we recorded: 1) the food species and parts consumed, 2) the feeding time(s) spent on each food item, 3) the frequency of approaches (within 1 m) and withdrawals between the mother and the immature while feeding, 4) the number of food items consumed by the mother and the immature, and 5) food size classes of each food item.

We used food size as a simple measure of foraging difficulty. We measured diameter of food items and classified them into three size categories: small (food size < immature hand size, < 1 cm; n = 45 food items); medium (food size = immature hand size, 1–3 cm; n = 39); large (food size > immature hand size, > 3 cm; n = 18) (Table S1 and Fig S2 in Supplementary Material). We defined co-feeding time as when mother and immature ate the same food item in the same feeding tree and within 5 m (Jaeggi & Gurven, 2013; Rapaport, 2006; Schiel & Huber, 2006).

We estimated food availability based on monthly phenology data from the study groups'feeding trees with a diameter at breast height (dbh) > 10 cm and woody lianas with dbh > 7 cm in 25 plots (10 m × 50 m) within the home ranges of the study groups. We selected phenology plots randomly at the crossroads of grid trails (200-m × 200-m intervals) and oriented randomly along trail intersections (Kim et al., 2011). We scored food abundance at 4 levels (0: no foods, 1: present but few, 2: moderately present, 3: abundant). We summed the scores and divided the sum by the number of trees—85 in total—to represent monthly food availability. The scores included the presence of food items—such as fruits, flowers, and leaves—known to be part of the Javan gibbons’ diet.

Statistical Analysis

For all analyses, we included observation days with at least 4 h of data, as shorter observation duration may not provide a representative sample of feeding behaviors and social interactions between the mother and the immature. The daily observation duration for included data ranged 4 to 11 h. In total, we included 875 h of observations over 120 days (group A: 205.5 h over 26 days; group B: 383 h over 56 days, group S: 286.5 h over 38 days). Immature age ranged from 9 to 50 months so that we could examine developmental changes before and after weaning. We controlled for food availability in all analyses.

Daily dietary breadth

We defined daily dietary breadth as the number of food items consumed on a given day (Bray et al., 2018). We calculated the daily dietary breadth for both the mother and the immature. We tested whether immature age affected the immature's daily dietary breadth (model 1a). We included the immature's daily dietary breadth as the response variable. We included immature age (months) as an explanatory variable, daily observation time as an offset, food availability as a control factor, group ID as a random factor, and immature age as a random slope within gibbon group ID.

Diet similarity

To examine the diet similarity between mothers and immatures, we calculated the Jaccard similarity index from the daily dietary data. The index was defined as a/(a + b + c), where a = the number of food items consumed by both the mother and immature, b = the number of food items consumed by only the mother, and c = the number of food items consumed by only the immature (Jaccard, 1912). Values of the index ranged from 0 (no similarity) to 1 (totally the same). We tested whether age of the immature affected diet similarity between mothers and immatures (model 1b). We included the Jaccard similarity index as the response variable, immature age (months) as an explanatory variable, monthly food availability as a control factor, group ID as a random factor, immature age as a random slope within the gibbon group ID.

Daily proportion of time spent feeding and co-feeding with mothers

We calculated the daily proportion of the time spent feeding and co-feeding with the mother by food size class based on the immature's daily dietary data. We defined the daily proportion of time spent feeding as [immature’s daily feeding time/daily observation time] and the daily proportion of time spent co-feeding with mother was defined as [immature’s daily co-feeding time with mother/immatures’ daily feeding time]. We also calculated the daily proportion of time spent feeding on each food size class that was spent co-feeding with the mother. This measure reflects the degree to which immatures rely on co-feeding with their mothers when consuming foods of different sizes. In this case, the immature’s daily feeding time includes when immatures feed alone or with other group members, such as their mother, presumed father, and presumed siblings. We tested whether immature age and food size classes affected the daily proportion of time spent feeding (model 2a) and co-feeding with mothers (model 2b). We included the daily proportion of time spent feeding and co-feeding with mothers as response variables. We included the interaction between immature age (months) and food size classes as an explanatory variable, food availability as a control factor, group ID as a random factor, and the immature age as a random slope within the gibbon group ID.

Approaches and leaves between mother and immature (Hinde index)

We calculated the Hinde index for mother-immature dyads when both were feeding to determine whether the mother or the immature was more responsible for maintaining close proximity (< 1 m) (van Adrichem et al., 2006). We considered who approached (< 1 m) and left (> 1 m) the other while either the mother or the immature was feeding, or they were co-feeding. The index is defined as [AP_o/(AP_o + AP_m)] – [LV_o/(LV_o + LV_m)], where AP_o = the proportion of approaches from the immature to its mother, AP_m = the proportion of approaches from the immature to its mother, and from the mother to its immature, LV_o = the proportion of leaves from the immature to its mother LV_m = the proportion of leaves from the immature to its mother and from the mother to its immature (Hinde & Atkinson, 1970). The values of the index ranged from − 1 (mother was entirely responsible for maintaining proximity) to 1 (immature was entirely responsible for maintaining proximity). We tested whether the interaction between the immature age and food size classes affected the Hinde index (model 3). We included the Hinde index as the response variable. We included the interaction between the immature age (months) and food size classes as the explanatory variable, food availability as a control factor, group ID as a random factor, and the immature age as a random slope within the gibbon group ID.

We used generalized linear mixed models (GLMMs) with a Gaussian distribution (model 1a, model 3) and a beta family distribution (model 1b, model 2a, model 2b), using glmmTMB package (Magnusson et al., 2017). For all analyses, we used variance inflation factors (VIFs) using the car package (Fox et al., 2012) to check multicollinearity and found VIFs from all models to be less than 4. We found there was no zero-inflation by using the DHARMa package (Hartig & Hartig, 2017). We included food availability as a control factor and conducted full-null model comparisons using analysis of variance (ANOVA). We used the summary function and confint function with 95% confidence intervals (CIs). We used R for all analyses (version 4.1.3; R Core Development Team, 2020). We set alpha at 0.05 for all statistical tests.

Ethical note

This research was approved by the Indonesian Ministry of Research and Technology (RISTEK) with Letter of Research Permit Number 434/E5/E5.4/SIP/2019 and acquired all the legal requirements of Indonesia including research permit from the study site, Gunung-Halimun Salak National Park in Indonesia (SIMAKSI No. 91/P/TNGHS/2019). We used non-invasive and behavioral observation data only. The authors declare that they have no conflict of interest.

Results

Daily Dietary Breadth and Diet Similarity with Mothers

Daily dietary breadth of immatures significantly increased with their age (full-null model comparison: χ² = 76.02, degrees of freedom (df) = 3, p < 0.001) (Table 2; Fig. 1). Before weaning (22 months), immatures had a mean daily dietary breadth of 8.3 food items (SD = 2.5) per day (Fig. 1). After weaning, immature’s daily dietary breadth exceeded that of their mothers (mean = 10.5, SD = 2.8), with a mean of 13.5 food items (SD = 3.7) per day at the age of 24 months. Diet similarity between mother and immature decreased significantly with immature age (full-null model comparison: χ² = 14.57, df = 1, p < 0.001) (Table 2; Fig. 2).

Table 2. Results of models testing the influence of age on daily dietary breadth, diet similarity with the mother, immature's daily proportion of time spent feeding, co-feeding with mother, approaches and leaves between immature and mother, and food size in immature wild Javan gibbons (Hylobates moloch) in Gunung Halimun-Salak National Park, West Java, Indonesia, from December 2019 to January 2022

	Estimate	SEM	z	Lower CI	Upper CI	pa
Model 1a: Effects of immature age (months) on immature’s daily dietary breadth
(Intercept)	− 2.505	1.678	− 1.493	− 5.793	0.783	0.135
Immature age	0.080	0.018	4.400	0.045	0.116	< 0.001***
Model 1b: Effects of immature age (months) on the diet similarity between mother and immature
(Intercept)	1.330	0.280	4.750	0.781	1.879	< 0.001***
Immature age	− 0.026	0.007	− 3.846	− 0.039	− 0.013	< 0.001***
Model 2a: Effects of immature age (months) and food size classes on immature’s daily proportion of time spent feeding
(Intercept)	− 0.522	0.576	− 0.906	− 1.652	0.608	0.365
Immature age	0.057	0.026	2.168	0.006	0.109	0.030*
Food size classes (small vs. medium)	0.486	0.820	0.593	− 1.121	2.094	0.553
Food size classes (small vs. large)	− 1.592	0.821	− 1.939	− 3.201	0.017	0.052
Immature age x Food size classes (medium)	− 0.139	0.038	− 3.672	− 0.213	− 0.065	< 0.001***
Immature age x Food size classes (large)	− 0.026	0.037	− 0.698	− 0.099	0.047	0.485
Model 2b: Effects of immature age (months) and food size classes on immature’s daily proportion of time spent co-feeding with mother
(Intercept)	1.650	0.791	2.084	0.099	3.201	0.037*
Immature age	− 0.069	0.036	− 1.945	− 0.139	− 0.001	0.050*
Food size classes (small vs. medium)	1.644	0.982	1.674	− 0.281	3.570	0.094
Food size classes (small vs. large)	− 0.366	0.992	− 0.369	− 2.311	1.579	0.713
Immature age x Food size classes (medium)	− 0.099	0.045	− 2.225	− 0.187	− 0.012	0.026*
Immature age x Food size classes (large)	− 0.024	0.045	− 0.529	− 0.111	0.064	0.597
Model 3: Effects of immature age (months) and food size classes on approaches and leaves between mother and immature (Hinde index)
(Intercept)	0.724	0.074	9.777	0.579	0.869	< 0.001***
Immature age	− 0.008	0.001	− 6.943	− 0.011	− 0.006	< 0.001***
Food size classes (small vs. medium)	− 0.051	0.056	− 0.923	− 0.161	− 0.058	0.356
Food size classes (small vs. large)	0.115	0.056	2.062	0.006	0.224	0.039*
Immature age x Food size classes (medium)	0.003	0.002	1.558	− 0.001	0.006	0.119
Immature age x Food size classes (large)	− 0.002	0.002	− 1.468	− 0.006	0.001	0.142

SEM standard error of the mean, CI confidence interval.

^ap-values in bold are significant (* < 0.05; ** < 0.01; *** < 0.001). The reference level of the food size classes is “small”.

[See PDF for image]

Fig. 1

Daily dietary breadth in immatures and their mothers by immature age in wild Javan gibbons (Hylobates moloch) in Gunung Halimun-Salak National Park, Indonesia, from December 2019 to January 2022. Shaded area indicates the 95% confidence interval

[See PDF for image]

Fig. 2

Diet similarity between mother and immature (Jaccard similarity index) by immature age in wild Javan gibbons (Hylobates moloch) in Gunung Halimun-Salak National Park from December 2019 to January 2022. The shaded area indicates 95% confidence interval

Daily proportion of time spent feeding and co-feeding with mothers

Daily feeding time increased significantly with immature age, and this age-related increase was moderated by food size class, specifically for medium food items, where the increase in feeding time was significantly smaller than for small food items (full-null model comparison: χ² = 107.96, df = 5, p < 0.001) (Table II; Fig. 3). There was no significant interaction between age and large food items (Table II). Additionally, there was no significant main effect of food size class, indicating that feeding time differences were not driven by food size alone.

[See PDF for image]

Fig. 3

Daily proportion of time spent feeding by immature age (months) and food size class in wild Javan gibbons (Hylobates moloch) in Gunung Halimun-Salak National Park from December 2019 to January 2022. Shaded area indicates 95% confidence interval

Co-feeding time with mothers significantly decreased with immature age and this age-related decrease was moderated by food size class (full-null model comparison: χ² = 26.576, df = 5, p < 0.001) (Table II). The decline in co-feeding time was significantly stronger for medium food items than for small food items (Table II; Fig. 4). There was no significant interaction effect of age and large food items on co-feeding time with mothers. Likewise, we found no significant main effect of food size class, suggesting that food size did not influence co-feeding time independently.

[See PDF for image]

Fig. 4

Daily proportion of time spent co-feeding with the mother by immature age (months) and food size class in wild Javan gibbons (Hylobates moloch) in Gunung Halimun-Salak National Park from December 2019 to January 2022. Shaded area indicates 95% confidence interval

Approaches and Leaves Between Mother and Immatures (Hinde Index)

Despite the decrease in the Hinde index with immature age, immatures consistently displayed a greater responsibility for maintaining proximity to their mothers than their mothers did, even after weaning (the mean value of the Hinde index remained above 0 across development). There were no significant interactions between immature age and food size classes on the Hinde index, indicating that the effect of age on proximity maintenance did not vary by food size class (full-null model comparison: χ² = 87.47, df = 5, p < 0.001) (Table II; Fig. 5). Immatures became significantly less responsible for maintaining proximity to their mother as they aged (Table II). Immatures were also more responsible for maintaining proximity to their mother when feeding on large food items than small food items, while we found no significant differences between small and medium food items. Immatures frequently approached and stayed close to their mother while foraging for large food items (Fig. 6).

[See PDF for image]

Fig. 5

Approaches and leaves between mother and immature (Hinde index) by immature age and food size class in wild Javan gibbons (Hylobates moloch) in Gunung Halimun-Salak National Park from December 2019 to January 2022. Shaded area indicates 95% confidence interval

Fig. 6 [Images not available. See PDF.]

Infant Javan gibbon (Hylobates moloch) co-feeding on a difficult food item (Tereup, Artocarpus elasticus) with its mother and sibling in Gunung Halimun-Salak National Park.

Copyright ^© Saein Lee

Discussion

Our results show that immature wild Javan gibbons show gradual developmental changes in feeding behavior and suggest that these are influenced by social learning from their mothers. Immature age and food size are associated with changes in feeding behavior in immature wild Javan gibbons. Dietary breadth increased with age, while diet similarity with the mother decreased to less than 50% at around 26 months. After weaning, immatures exhibited a broader diet that included food items not consumed by their mothers, indicating increasing dietary independence. Immature’s total feeding time increased and co-feeding time with mother decreased with age. Feeding time also varied with food size, while time co-feeding with the mother declined as the immatures became older. The responsibility for proximity between immatures and their mothers varied with food size. Immatures were more responsible for maintaining proximity to their mothers during early development and while eating large food items compared to small ones. This behavior is likely, because the immatures'need to acquire information about specific food items through close observation.

Immature gibbons achieved adult-like dietary breadth in early juvenility, as they consumed approximately ten food items per day (1.96 food items per hour), similar to their mothers. Our results are similar to those for orangutans, who showed similar diet repertoires to adults around weaning age and exceeded their mother’s diet repertoire size after weaning (Schuppli et al., 2016b, 2021) and for ring-tailed lemurs (Lemur catta), who also showed increased dietary diversity across development and achieved an adult-like diet in early juvenility (O’Mara & Hickey, 2012). The continuous increase in dietary breadth, leading to a broader diet than of their mothers, suggests that immatures acquire food-recognition skills across development and based on this, continue to explore food items through independent exploration or social influences from non-mother group members. Immature Javan gibbons showed decrease in the time < 1 m to their mothers with but an increase in the time spent close to their presumed fathers and siblings (Lee, unpublished data). As immatures grow older, they may face increasing ecological challenges that require them to acquire foraging skills and dietary knowledge beyond what they can learn from their mothers (Schuppli et al., 2021). Therefore, our results suggest that immature Javan gibbons continue to expand their dietary breadth after achieving adult-like dietary breadth, with expanded learning opportunities throughout their development.

We also found that diet similarity with mothers decreased with immature age, with < 0.75 diet similarity around the age of weaning. In contrast, immature chimpanzees showed a nonlinear increase in diet similarity with immature age, and reached maximum similarity at 6 years of age, which they then maintained (Lonsdorf et al., 2021). Immature wild orangutans also showed an increase in diet similarity with their mother until the age of 5.5 years (Schuppli et al., 2016b). These contrasts indicate that immature Javan gibbons begin to broaden their diet earlier in development compared to great apes, potentially reflecting earlier feeding independence or social learning from group members other than the mother. During early infancy, immature vervet monkeys (Cercopithecus aethiops) exhibit a diet that is highly similar to their mothers’. This diet similarity enables immatures to manage foraging costs related to their physical immaturity and limited knowledge of available food sources (Hauser, 1993). Likewise, immature Javan gibbons may reduce foraging costs by synchronizing diet breadth with their mothers in early development. Our study shows that the feeding behavior of immature wild Javan gibbons is greatly influenced by their mothers during early infancy, but immatures gradually develop their own dietary repertoires as they become independent.

Our results showing an increase in feeding time with immature age are consistent with findings for other primate species. Immature gorillas and orangutans also showed an increase in the daily proportion of time spent feeding with their age before weaning (Nowell & Fletcher, 2007; van Adrichem et al., 2006). Moreover, immature wild Javan gibbons spent less time feeding on large than small food items in early development, which concurs with the findings for immature capuchin monkeys (Eadie, 2015). Although the gibbon diet is generally considered to be composed of relatively easy-to-acquire food compared to chimpanzees, orangutans, and capuchins (Boesch & Boesch, 1990; Fragaszy et al., 2004; van Schaik et al., 2003), our results indicate that the development of immature gibbons is still influenced by potential foraging difficulty, measured as the size of food.

We found that co-feeding time between mothers and immatures decreased with immature age. Our finding is consistent with findings of decreased co-feeding time with parents during juvenility and adolescence in wild Javan gibbons at the same study site (Choi et al., 2023). Aggression from parents to juveniles and adolescents increased in the feeding context while co-feeding decreased, suggesting that immature gibbons may benefit from co-feeding in early infancy and juvenility, but less after juvenility due to the cost of competition. We did not find a significant interaction between immature age and food size concerning co-feeding time with mothers. However, we found that immature wild Javan gibbons heavily relied on co-feeding during early infancy, accounting for more than half of their feeding time across all food size classes. Co-feeding is especially important for infant primates to gain information about specific food items by observing others (Rapaport & Brown, 2008), and it has been observed in many primate species (mantled howler monkeys, Alouatta palliata Whitehead, 1986; brown lemurs, Eulemur fulvus Tarnaud, 2004; chimpanzees, Pan troglodytes Kuroda, 1984; Bornean orangutans, Pongo pygmaeus wurmbii Jaeggi et al., 2008) but not in gibbons. Together, previous findings and our results suggest that wild Javan gibbons acquire feeding information, such as foraging skills related to the size of food items, through co-feeding with their mothers, particularly during infancy and juvenility.

The reduction in co-feeding time with mothers as immatures age, as shown in our results, suggests a shift toward increased feeding independence. This may reflect greater reliance on individual exploration or potential social learning from other group members, such as presumed fathers or siblings. Independent exploration and social learning from nonmaternal individuals have been identified as important strategies for skill acquisition in other primates, particularly in species with slow life histories and extended juvenile periods (Bandini & Harrison, 2020; Boyd & Richerson, 1988; Krakauer, 2005; Whitehead, 1986). While our study in pair-living Javan gibbons focuses on potential learning from mothers, previous work in other pair-living primates, such as owl monkeys (Aotus azarai) and titi monkeys (Callicebus torquatus torquatus), has shown that immatures often interact with and learn from their fathers and siblings rather than from mothers in the feeding context (Starin, 1978; Wolovich et al., 2008). Observational data from our ongoing work with the same study population show that immature Javan gibbons engage in social interactions with other group members such as fathers and siblings during feeding (Lee et al., unpublished data). These additional data will broaden our understanding of the potential role of social learning from different group members—not only mothers—in the development of feeding behavior in immature Javan gibbons.

We found that immatures maintained proximity to their mothers in early development when feeding on large foods compared with small ones. Our results indicate that immature wild Javan gibbons manage their foraging costs by staying close to their mothers even after weaning (Rapaport & Brown, 2008). Our findings are consistent with prior research on wild Javan gibbons at the same study site, which showed that immature gibbons solicited difficult-to-process food more than easy-to-process food regardless of the nutritional value, implying information transfer (Yi et al., 2020). These results also align with the finding that immature orangutans showed a higher frequency of approaching, observing, and begging behaviors toward their mothers as foraging difficulty increased (Jaeggi et al., 2008, 2010). Our results suggest that immature wild Javan gibbons stay close to their mother to obtain social information about food items during development. Because maternal tolerance does not vary in response to ecological challenges in wild Javan gibbons (Yi et al., 2020), immatures may benefit from this tolerance for acquiring information during their prolonged juvenile periods.

Conclusions

Our study shows that immatures showed age-related differences in feeding behavior and that food size class, a potential indicator of foraging difficulty, has a significant influence on the development of feeding behavior in immature, wild, Javan gibbons. Moreover, our study highlights that immature wild Javan gibbons may acquire information from their mothers in feeding contexts. Our findings suggest that immature Javan gibbons approach and stay close to their mothers selectively based on food size class to acquire information about food items through co-feeding and obtain an adult-like dietary breadth around the time of weaning. These results stress the importance of maternal influences on the development of immatures’ feeding behavior in primates. However, future study of immatures and other group members in feeding contexts is required to assess selective social learning in gibbons. Our research contributes to filling gaps in the understanding of feeding development and maternal influences in primates by providing empirical evidence of how both ecological factors (such as foraging difficulty) and social factors (such as potential learning from mothers during co-feeding) shape the development of feeding behaviors in wild Javan gibbons. Unlike previous studies that have largely focused on great apes or species with larger group sizes and more complex social structures, our study highlights the role of maternal influences in the feeding development of pair-living primates, who live in relatively small groups. By examining the interaction between immature age and food size classes, we show how immatures adjust their feeding strategies over time, potentially balancing independent exploration with social influences from both mothers and other group members. These findings enhance our understanding of primate feeding development and provide indirect evidence of potential social learning processes, contributing to broader discussions on the evolutionary significance of social influences in shaping foraging behaviors across primate species.

Acknowledgements

SL was financially supported by the National Geographic Society research grant (EC-KOR- 55029R- 18), POSCO International, and the Biodiversity Foundation in Republic of Korea. This work was supported by the Ewha Womans University Research Grant of 2025. We thank the Indonesian Ministry of Research and Technology (RISTEK), the Indonesian Ministry of Environment and Forestry for granting us a letter of research permit, and the authorities of Gunung Halimun-Salak National Park for granting us the national park entrance permit. We also thank the field team: Muhammad Nur, Isra Kurnia, Nandar Pratama, Alan Kusuma, M. Abdul Azis, Indra Lesmana for their hard work and dedication in the field. We greatly thank the editors and reviewers for reviewing and improving the manuscript.

Author contributions

SL, YY, AH developed the concept of the study. SL and RO collected data. SL analyzed the data and wrote the manuscript. SL, RO, YY, AC, AM, and JCC provided feedback and contributed to completing the final draft. JCC and YY were corresponding authors. All authors contributed to the article and approved the submitted version.

Funding

National Geographic Society, EC-KOR- 55029R- 18, Saein Lee, POSCO International, Ewha Womans University Research Grant of 2025.

Data Availability

The datasets analyzed during the current study are available as supplementary material.

Declarations

Inclusion and Diversity

While citing references scientifically relevant for this work, we also actively worked to promote gender balance in our reference list.

Conflict of interest

We declare no conflict of interest.

Joanna M. Setchell

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