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The primate adolescent period is characterized by a series of changes in physiology, behavior, and social relationships. Orangutans have the slowest life history and the longest period of dependency of all primates. As members of a semisolitary species with high levels of sexual coercion, adolescent female orangutans face a unique combination of challenges when achieving independence from their mother. This study examined the mating behavior of adolescent female orangutans and compared it with that of adult females to assess whether mating behavior reflects distinct strategies at these different points in the life cycle. Data were collected in Gunung Palung National Park on the island of Borneo over 20 years. Mating events from adolescent (n = 19) and adult females (n = 26) were scored and compared. Adolescent female mating events had significantly higher mating scores (indicating more proceptivity) than those of adult females (β = 1.948,p = .001). Adolescent females also engaged in elaborate sociosexual interactions with different flanged males, behaviors that were never observed during mating events of adult females. These interactions involved characteristic behavior on the part of both the adolescent females and the flanged males. Given these findings and the documentation of similar accounts of adolescent female–flanged male mating from the island of Sumatra, we propose that adolescent female orangutans display distinctive behavioral repertoires throughout the genusPongowhich serves to overcome male ambivalence toward nulliparous females, establish familiarity, and evaluate coercive tendencies in flanged males. We suggest that these behavioral patterns are an integral part of female social development in a female philopatric, but highly dispersed species where consistent social support is absent after ranging independence is achieved.

 

Seed dispersal is important for forest growth, maintenance, and regeneration. Orangutans are large-bodied frugivores with ecological roles as seed predators and seed dispersers. However, little is known about orangutans’ ecological roles and how they relate to orangutans’ patterns of frugivory. We investigated Bornean orangutans’ (Pongo pygmaeus wurmbii) ecological roles at the Cabang Panti Research Station in Gunung Palung National Park, Indonesian Borneo. We collected orangutan feces (n=401) and analyzed them for intact seeds (August 2018 to March 2020). We observed orangutan fruit handling behavior for 306 feeding bouts for 53 fruit genera to measure how often orangutans swallow, spit, or predate seeds. We used Ivlev’s Electivity Index to analyze fruit preference using long-term feeding data and phenology data (2014-2019). Lastly, we combined fruit preference with fruit handling behavior using the seed dispersal effectiveness framework to identify which fruit taxa were most effectively dispersed. Orangutans dispersed seeds in 71.8% of fecal samples with a mean of 27.9 ±4.5 (SD=0.95) seeds (>2mm) per fecal sample. Orangutans predated seeds more often than spitting or swallowing seeds (predating= 42.1% of fruit feeding time; spitting= 21.8%; swallowing= 12.5%; mixed behaviors= 10.6%, not observed=12.0%). Additionally, the top five preferred fruit genera, (Dialium, Sindora, Scaphium, Magnifera, and Spatholobus) were highly predated (0 to 5% of seeds dispersed). We identified Alangium and Tetramerista as the most effectively dispersed genera, orangutans frequently dispersed and preferred these fruits. We found orangutans are frequent seed predators, but this overlaps with their seed dispersal role, and we describe orangutans’ seed dispersal contribution. Funders: NSF (9414388, BCS-1638823, BCS-0936199); National Geographic; USFish/Wildlife (F18AP00898, F15AP00812, F13AP00920, 96200-0-G249, 96200-9-G110); Leakey; Disney Conservation Fund; Wenner-Gren; Nacey-Maggioncalda; Conservation-Food-Health; Orangutan Conservancy; Woodland Park Zoo; Boston University GRAF 

Due to extreme incongruence in parental investment, the potential for sexual conflict in orangutan reproductive strategies is high. Female orangutans prefer flanged males, but with intense male-male competition and sexual coercion, it is unclear how females are able to exert choice. We hypothesized that female orangutans use initiation and maintenance of associations with preferred males as a mechanism of female choice. We used encounter rates and behavioral measures of proximity maintenance to distinguish between the role of female choice and male coercion in male-female associations in Gunung Palung National Park, West Kalimantan, Indonesia. From May 2018-April 2019, we collected data on initiation, termination, and proximity maintenance during associations between males and cycling females (females without dependent offspring or with offspring over 6 years old). Encounters between cycling females and flanged males were more likely to be female-initiated (83.3%), while encounters with unflanged males were more likely to be male-initiated (80%) (N=16, p=0.035, Fisher’s exact test). Additionally, the Brown Index indicates significantly more female proximity maintenance when cycling females associated with flanged males than unflanged males (N=33, W = 198.5, p= 0.012). However, using long-term data on male-female associations, we found that dyads of flanged males and females were less likely to encounter other males compared to dyads of unflanged males and females (N=542, χ2= 3.3051, df=1, p=0.035). This indicates that flanged males may also use associations to mate guard females. These data indicate that there are behavioral manifestations of both female choice and male coercion in orangutan associations. Funders: NSF (DGE-1247312, BCS-1638823, BCS-0936199), Boston University, Leakey Foundation, Disney Conservation Fund, and US Fish and Wildlife Service (F18AP00898) 

When female chimpanzees, orangutans, and callitrichids share challenging‐to‐process resources with their offspring, they improve offspring access to foods and calories which would otherwise be unavailable. Adult chimpanzees share foods rarely, but when they do, sharing valuable resources solidifies inter‐individual bonds (e.g., when building coalitions or eliciting copulations). While maternal‐offspring food sharing has been studied in wild orangutans, the context in which adult orangutans share food and feed in proximity is poorly known. We use 27 years of research on orangutans in West Kalimantan, Indonesia, to examine this behavior. Food sharing and tolerance were observed during 2,131 follows between 1994‐2019. Mother‐infant food sharing occurred in 78%, of these follows, female‐female sharing in 22%, male‐female sharing in 32%, and male‐male in just 1%. Adult females shared foods at different rates with adult males than with offspring (Chi‐square = 49.27,p< .01,N= 589 events). Eighty‐one percent of mother‐offspring food sharing/tolerance was fruit, compared to only 71% of male‐female food sharing/tolerance. Durio, Lithocarpus, and Willughbeia (hard‐to‐process fruits) were most frequently shared by mothers. Twenty‐three percent of male‐female food sharing/tolerance occurred while eating termites; only 3% of mother‐infant sharing did. Only two of 350 mouth‐to‐mouth or hand‐to‐mouth transfers involved adult males and females. Mothers increase their offspring’s access to challenging resources, while food sharing/tolerance among adult males and females is not limited to valuable resources, but may indicate strong social tolerance or affiliation in generally solitary adults 

Habituation, or the process of an animal becoming comfortable with human observers, is an essential part of wild primate observational studies. Despite the importance of this process, questions remain as to what counts as habituated for a particular species, how individuals and species react to humans, and how age-sex classes differ in these responses. To address these questions, we analyzed data from over 25 years of research on wild Bornean orangutans from Gunung Palung National Park, Indonesia, drawing from 8,383 follows and 82,413 hours of observation. We categorized the degree of agitation with humans by totaling the number of alarm vocalizations, giving each follow a score of 1-10. We then looked at behavioral measures using a GLMM to control for individual and food availability. This revealed that individuals with the highest vocalization scores spent a greater percentage of the day traveling (b=40.5, p < 0.0001), stayed higher in the canopy (b=16, p < 0.0001) and spent less time eating (b=205, p < 0.0001) than did animals that did not vocalize. Our analysis also revealed a less common, but frequently observed, opposing response to humans, which was to hide, often inside of a day nest, and emit no vocalizations. Individual orangutans were observed to switch between these two ’strategies’ to evade human observers. We discuss the implications of this behavior as well as present evidence that the reaction of other orangutans mediates the response of focal individuals to humans, suggesting the importance of social learning in this behavior. 

Orangutan habitats are characterized by fluctuations in the availability of ripe fruits. During non-fruiting periods orangutans typically incorporate more lower-quality foods such as pith and bark in their diet. Condensed tannins (CT) are secondary plant compounds that bind to proteins, thus impeding the digestibility of proteins, and tending to make foods bitter or unpalatable. We analyzed condensed tannin content in 129 plant samples collected from Gunung Palung National Park in Borneo, Indonesia between 1994 and 2001. We predicted that CT concentrations would be highest in bark, and that there would be a correlation between protein and condensed tannin content. We used ANOVA with Bonferonni’s method for post-hoc comparisons to test for differences in tannin content between plant parts, and Pearson’s correlation to test for relationships between tannin concentrations and other nutrients. There were significant differences in condensed tannin content (F(4)=2.70, p=0.03) but no differences after adjusting the alpha-level for post-hoc comparisons. Whole fruit (including the skin) tended to have the highest CT concentration. However, we found no correlation between CT and concentration of nutrients including crude protein (R=0.12, p=0.19, N=127), free simple sugars (R=-0.09, p=0.40, N=100), or fiber (R=-0.38, p=0.67, N=128). This underscores that plants rich in desirable nutrients may also be rich in antifeedants, posing challenges for orangutan consumption and digestion even as they provide a source of high-quality energy. Additionally, for some food categories where high tannin content is predicted, such as bark, orangutans may be choosing to eat species that are lower in these compounds. 

The socioecological model predicts that food availability and risk of parasite transmission influence sociality in primates. As a semi-solitary ape inhabiting the masting forests of Southeast Asia, orangutans provide a unique opportunity to compare social and non-social periods and highly variable foraging conditions within one population. This study compared two data collection periods when fruit availability differed markedly to determine whether sociality and parasite prevalence decrease as expected during periods of fruit scarcity. Fecal samples were analyzed using direct smear and fecal concentration techniques on-site at Cabang Panti Research Station from 2013-2014 and 2018-2019. From the high fruit period to the low fruit period, sociality decreased from 54% of focal follows containing a social event to 29%, while overall parasite prevalence remained the same at 100%. Interesting differences arose for certain parasite species, however. Enterobius sp. prevalence decreased during the low fruit period for both sexes but even more so for males (50% to 29% for females; 56% to 0 for males). Prevalence of Trichuris sp. increased for females during the low fruit period (5% to 43%) while prevalence among males remained the same. These results lend support to the prediction that social contact influences transmission risk for some parasite species, while other parasites may be more responsive to factors such as changes in reproductive state. These findings suggest that differences in the behavioral strategies of the sexes and the differential energetic demands of life history stages have an influence on parasitic infection patterns. 

The juvenile risk aversion hypothesis suggests an extended life history is an adaptation to unpredictable environments, such as those that characterize Bornean orangutans. We examined how changes in infant and juvenile activity budgets changed over time and with varying periods of food availability. We hypothesized that during periods of low food availability juvenile orangutans would trade-off developmentally important behavior, such as play, in order to conserve energetic resources. We tested this hypothesis using 924 follows of infant (0-4 years) and juvenile (5-8 years) orangutans, collected over a 25 year period, encompassing period fo high and low food availability at Gunung Palung National Park, Indonesia. Using a GLMM to control for individual and examining both age and food availability we found that overall, infant and juveniles played less during period of low food availability compared to medium and high food availability (b= -14.3, p < 0.0001) and that play behavior varied significantly by age (b=-5.9,m p < 0.0001). Infants in the 1-2 age category showed the highest percentage of play, comprising 42% of their overall activity budget, with play dropping to 14% by age 4. We also found signficant interaction effects between age and food availability on play behavior (b=2.1, p < 0.0001). We discuss the ways that infants and juvenile trade off energetically expensive behavior through different development periods as well as the role that maternal behavior may play in buffering infants and juveniles of coping with periods of low food availability. 

Biomarkers including reproductive hormones and indicators of energy balance can be used to analyze health status and physiology in wild animals. Non-invasive collection of urine or feces enables biomarker monitoring, important for critically endangered species like orangutans. Hormonal measurements must control for urine concentration, typically done using creatinine or specific gravity. Specific gravity measurement compares the density of urine with the density of water. Creatinine is a breakdown product of muscle metabolism that is excreted from the body at a relatively stable rate, and it is an indicator of relative muscle mass in many species. Here, we measure specific gravity in urine samples from captive female orangutans using a digital hand-held urine specific gravity refractometer. We compare specific gravity to previously measured creatinine values and assess the influence of time of collection and refractometer temperature on specific gravity. We found a significant positive correlation between specific gravity and creatinine concentrations (N=1021, Pearson’s R=0.578, p<0.001). While we found no significant correlation between the time that samples were collected and specific gravity readings (N= 314, Pearson’s R=0.079, p=0.17), readings from morning samples were slightly but significantly lower (N=255, mean=1.008) than afternoon samples (N=60, mean=1.009) (independent samples t-test, t312=-1.969, p=0.05). We found a significant negative correlation between specific gravity and refractometer temperature (Pearson’s R=-0.23, p<0.001), highlighting the need to control for urine temperature when using thawed samples. 

Due to extreme incongruence in parental investment, the potential for sexual conflict in orangutan reproductive strategies is high. Female orangutans prefer flanged males, but with intense male-male competition and sexual coercion, it is unclear how females are able to exert choice. We hypothesized that female orangutans use initiation and maintenance of associations with preferred males as a mechanism of female choice. We used encounter rates and behavioral measures of proximity maintenance to distinguish between the role of female choice and male coercion in male-female associations in Gunung Palung National Park, West Kalimantan, Indonesia. From May 2018-April 2019, we collected data on initiation, termination, and proximity maintenance during associations between males and cycling females (females without dependent offspring or with offspring over 6 years old). Encounters between cycling females and flanged males were more likely to be female-initiated (83.3%), while encounters with unflanged males were more likely to be male-initiated (80%) (N=16, p=0.035, Fisher’s exact test). Additionally, the Brown Index indicates significantly more female proximity maintenance when cycling females associated with flanged males than unflanged males (N=33, W = 198.5, p= 0.012). However, using long-term data on male-female associations, we found that dyads of flanged males and females were less likely to encounter other males compared to dyads of unflanged males and females (N=542, χ2= 3.3051, df=1, p=0.035). This indicates that flanged males may also use associations to mate guard females. These data indicate that there are behavioral manifestations of both female choice and male coercion in orangutan associations. Funders: NSF (DGE-1247312, BCS-1638823, BCS-0936199), Boston University, Leakey Foundation, Disney Conservation Fund, and US Fish and Wildlife Service (F18AP00898)