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            Bornean orangutans (Pongo pygmaeus wurmbii), with their long lifespans and inter-birth intervals, and late age at first birth, have the most extended life history of all primates. According to the Ecological Risk Aversion Hypothesis, slow growth is a strategy to avoid starvation in unpredictable environments. When fruits are unavailable, bark and leaves, high in indigestible fiber, dominate orangutan diets. Orangutan hindgut fermentation is critical in the extraction of nutrients from fibrous fallback foods. However, body size and gut passage times are predicted to influence digestive efficiency. We investigated age-sex class differences in fiber digestibility in response to fluctuations in fiber intake. Researchers at Gunung Palung National Park, Indonesia, collected fecal samples during focal follows from 2016-2019 which were analyzed at Boston University’s Primate Ecology Lab. Samples (N=143) were weighed and dried overnight before grinding in a Wiley Mill. Seeds separated from the fecal matter were counted, measured, photographed and identified using our reference database. Dry matter and percent organic matter were determined through drying, ashing, and hot weighing. We used an ANKOM 200 Fiber Analyzer to determine NDF and compared the percent fiber excreted by mother/offspring pairs with feeding data. While adult female and juvenile diets showed similar percentages of fiber intake, juveniles excreted 50% more fiber than their mothers. Our results highlight the influence of body size, with smaller individuals demonstrating a lower capacity for fiber digestion. Juvenile digestive efficiency likely constrains growth, development, and survivorship during periods of low food availability when orangutan diets are high in fiber.more » « less
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            Orangutan diets vary dramatically with food availability. Orangutans preferentially eat fruit when available, but due to dramatic and unpredictable fluctuations in fruit availability, orangutans often consume unripe fruit, bark, seeds, and leaves. Their robust craniodental structure suggests that they are well adapted to consume mechanically challenging foods. Since differences in jaw anatomy and body size pose physiological differences in terms of gape, exerted force, and resistance to wear and breakdown, growth and allometry likely affect an orangutan’s ability to process a mechanically challenging diet. Thus, we predict that orangutans of different ages and sexes process foods differently. Given juveniles' smaller and less powerful craniodental structure, and the time required to develop ecological competence, we hypothesized that juveniles may have more difficulty in processing foods than adults. We recorded the frequency that foods were introduced to the mouth, and chewed with different teeth (incisors, canines, and molars) in 561 feeding videos collected in Gunung Palung National Park in West Kalimantan, Borneo on wild orangutans (Pongo pygmaeus wurmbii). Videos were stratified by age and sex class and foods were categorized by type. Infants and juveniles use their canines significantly more frequently than adult females (p< 0.05) and flanged males (p< 0.05). Molar use also differed by age and sex class (F(3)=2.551, p=0.05), with juveniles chewing with their molars significantly more frequently than adult females (p=0.05). Differences in adult and juvenile oral processing profiles suggest juveniles may process some foods less efficiently than adults.more » « less
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            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 adultsmore » « less
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            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.more » « less
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            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.more » « less
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            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.more » « less
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            Biomarkers including reproductive hormones and indicators of energy balance can be used to analyze health status in wild animals. Non-invasive measures, analyzed through urine or feces, enable biomarker monitoring without interfering with organisms, important for critically endangered species like orangutans. A measure of urine concentration such as creatinine concentrations or specific gravity is necessary when analyzing urine samples. Here, we measure specific gravity in urine samples from three captive female orangutans using a digital hand-held urine specific gravity refractometer. We compare specific gravity to previously measured creatinine values for two orangutans, and assess the influence of time of collection and refractometer temperature on specific gravity for all three. 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 samples collected in the morning were slightly but significantly lower (N=255, mean=1.008) than samples collected in the afternoon (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 the refractometer temperature (Pearson’s R=-0.23, p<0.001). In future studies, specific gravity can be used to determine urine concentration rather than creatinine, which is more costly and requires more time for lab work. Our future research will examine the correlation between specific gravity and creatinine concentrations as orangutans age, and the effects of aging on muscle wasting and reproductive status.more » « less
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            Wild orangutans cope with dramatic, unpredictable fluctuations in food availability throughout development which have significant implications for energy balance for growth, development, and maintenance of body function. Foods that are especially important when preferred fruits are not available (e.g., bark/pith, termites, seeds) can require force, manual manipulation, and/or skill to access. Orangutans’ extended life history may mitigate ecological risk associated with the challenging environment of juvenile growth and development. Given the complexity of important foods, orangutans’ semi-solitary lifestyle, and the relatively brief period between weaning and independence, offspring transition to ecological independence during their extended nursing period. Here, we examine mother-offspring food transfer in the context of nutritional quality and complexity, with handling time as a proxy. Data were collected between July 2009-July 2019 in Gunung Palung National Park, Indonesia. We predict complex food items are transferred most frequently. In 245 observations of food sharing, fruit was most frequently transferred, followed by invertebrates and bark/pith. Handling time and transfer frequency were negatively correlated (Rho=-0.75, p<0.001): slower-eaten fruits were shared more frequently than rapidly-eaten fruits. Fruit size and sharing frequency were also negatively correlated (Rho=-0.73, p<0.001). There was no correlation between sharing frequency and free simple sugar concentration (Rho = 0.36, p=0.13), though sharing frequency and total nonstructural carbohydrate concentration were correlated (Rho=0.46, p=0.04). Food sharing was most common when mothers ate large, slowly-eaten fruits rich in nonstructural carbohydrates. Food sharing allows mothers to transfer more complex foods to their offspring, and may facilitate knowledge transfer as offspring become ecologically competent.more » « less
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            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.more » « less
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            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 11tannin 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. Funders: Boston University Undergraduate Research Opportunities Program, NSF (BCS-1638823, BCS-0936199); National Geographic; USFish/Wildlife (F18AP00898, F15AP00812, F13AP00920, 96200-0-G249, 96200-9-G110, 9414388); Leakey; Disney Wildlife Conservation; Wenner-Gren; Nacey-Maggioncalda; Orangutan Conservancy; Conservation, Food, and Health Foundation.more » « less
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