Bottom-up regulatory factors have been proposed to exert a strong influence on mammalian population density. Studies relating habitat quality to population density have typically made comparisons ...among distant species or communities without considering variation in food quality among localities. We compared dietary nutritional quality of two Bornean orangutan populations with differing population densities in peatland habitats, Tuanan and Sabangau, separated by 63 km. We hypothesized that because Tuanan is alluvial, the plant species included in the orangutan diet would be of higher nutritional quality compared to Sabangau, resulting in higher daily caloric intake in Tuanan. We also predicted that forest productivity would be greater in Tuanan compared to Sabangau. In support of these hypotheses, the overall quality of the diet and the quality of matched dietary items were higher in Tuanan, resulting in higher daily caloric intake compared to Sabangau. These differences in dietary nutritional quality may provide insights into why orangutan population density is almost two times greater in Tuanan compared to Sabangau, in agreement with a potentially important influence of diet quality on primate population density.
Orangutans show a pronounced sexual dimorphism, with flanged males (i.e., males with fully grown secondary sexual characteristics) reaching twice the size of adult females. Furthermore, adult ...orangutans show sex-specific dispersal and activity patterns. This study investigates sex differences in adult foraging behavior and sheds light on how these differences develop in immatures. We analyzed 11 years of feeding data on ten adult female, seven flanged male, and 14 immature Bornean orangutans (
Pongo pygmaeus wurmbii
) at Tuanan in Central Kalimantan, Indonesia. We found that the diets of the adult females were significantly broader and required more processing steps before ingestion than the diets of flanged males. We also found evidence for a similar difference in overall diet repertoire sizes. For the immatures, we found that whereas females reached 100% of their mothers’ diet spectrum size by the age of weaning, males reached only around 80%. From the age of 4 years on (i.e., years before being weaned) females had significantly broader daily diets than males. We found no difference in daily or overall diet processing intensity of immature males and females but found preliminary evidence that immature males included fewer items of their mother’s diet in their own diets that were processing-intensive. Overall, our results suggest that by eating a broader variety and more complex to process food items, female orangutans go to greater lengths to achieve a balanced diet than males do. These behavioral differences are not just apparent in adult foraging behavior but also reflected in immature development from an early age on.
Significance Statement
In many species, males and females have different nutritional needs and are thus expected to show sex-specific foraging behavior. Sex differences in several aspects of foraging behavior have been found in various species, but it remains largely unclear when and how those develop during ontogeny, which is especially relevant for long-lived altricial species that learn foraging skills over many years. In our study, we analyzed a cross-sectional and longitudinal data set containing more than 750,000 feeding events of adult and immature Bornean orangutans (
Pongo pygmaeus wurmbii
). We found that adult females had significantly broader and more complex diets than males. We also found that these differences started to develop during infancy, suggesting that immature orangutans prepare for their sex-specific foraging niches long before those become physiologically relevant while they are still in constant association with their mothers and before being frequently exposed to other role models.
Various studies have shown that the population densities of a number of forest vertebrates, such as orangutans, are higher on Sumatra than Borneo, and that several species exhibit smaller body sizes ...on Borneo than Sumatra and mainland Southeast Asia. It has been suggested that differences in forest fruit productivity between the islands can explain these patterns. Here we present a large-scale comparison of forest fruit production between the islands to test this hypothesis.
Data on fruit production were collated from Sumatran and Bornean sites. At six sites we assessed fruit production in three forest types: riverine, peat swamp and dryland forests. We compared fruit production using time-series models during different periods of overall fruit production and in different tree size classes. We examined overall island differences and differences specifically for fruiting period and tree size class. The results of these analyses indicate that overall the Sumatran forests are more productive than those on Borneo. This difference remains when each of the three forest types (dryland, riverine, and peat) are examined separately. The difference also holds over most tree sizes and fruiting periods.
Our results provide strong support for the hypothesis that forest fruit productivity is higher on Sumatra than Borneo. This difference is most likely the result of the overall younger and more volcanic soils on Sumatra than Borneo. These results contribute to our understanding of the determinants of faunal density and the evolution of body size on both islands.
Pronounced temporal and spatial variation in the availability of food resources can produce energetic deficits in organisms. Fruit-dependent Bornean orangutans face extreme variation in fruit ...availability and experience negative energy and protein balance during episodes of fruit scarcity. We evaluate the possibility that orangutans of different sexes and ages catabolize muscle tissue when the availability of fruit is low. We assess variation in muscle mass by examining the relationship between urinary creatinine and specific gravity and use the residuals as a non-invasive measure of estimated lean body mass (ELBM). Despite orangutans having a suite of adaptations to buffer them from fruit scarcity and associated caloric deficits, ELBM was lower during low fruit periods in all age-sex classes. As predicted, adult male orangutans had higher ELBM than adult females and immatures. Contrary to expectation, flanged and unflanged males did not differ significantly in ELBM. These findings highlight the precarity of orangutan health in the face of rapid environmental change and add to a growing body of evidence that orangutans are characterized by unique metabolic traits shaped by their unpredictable forest environment.
The ecological factors contributing to the evolution of tropical vertebrate communities are still poorly understood. Primate communities of the tropical Americas have fewer folivorous but more ...frugivorous genera than tropical regions of the Old World and especially many more frugivorous genera than Madagascar. Reasons for this phenomenon are largely unexplored. We developed the hypothesis that Neotropical fruits have higher protein concentrations than fruits from Madagascar and that the higher representation of frugivorous genera in the Neotropics is linked to high protein concentrations in fruits. Low fruit protein concentrations in Madagascar would restrict the evolution of frugivores in Malagasy communities.
We reviewed the literature for nitrogen concentrations in fruits from the Neotropics and from Madagascar, and analyzed fruits from an additional six sites in the Neotropics and six sites in Madagascar. Fruits from the Neotropical sites contain significantly more nitrogen than fruits from the Madagascar sites. Nitrogen concentrations in New World fruits are above the concentrations to satisfy nitrogen requirements of primates, while they are at the lower end or below the concentrations to cover primate protein needs in Madagascar.
Fruits at most sites in the Neotropics contain enough protein to satisfy the protein needs of primates. Thus, selection pressure to develop new adaptations for foods that are difficult to digest (such as leaves) may have been lower in the Neotropics than in Madagascar. The low nitrogen concentrations in fruits from Madagascar may contribute to the almost complete absence of frugivorous primate species on this island.
The effect of aggressive competition over food resources on energy intake rate is analyzed for individuals of three groups of 25-35 white-faced capuchin monkeys, Cebus capucinus, living in and near ...Lomas Barbudal Biological Reserve, Costa Rica. An individual's energy intake rate on a given food species was affected by its rank and the number of agonistic interactions within the feeding tree. Dominant group members had higher energy intake rates relative to subordinate group members whether or not there was agonism within the feeding tree. Low- and mid-ranked individuals had lower energy intake rates in trees with higher amounts of aggression, while energy intake rate of high-ranked individuals was not affected by the amount of aggression in the feeding tree. Energy intake was not influenced by the sex of the individual when rank was held constant statistically. Energy intake was positively correlated with total crown energy (measured in kilojoules) within the feeding tree for two of three study groups. This difference may be explained by the quality of each group's territory. Finally, high-ranked individuals are responsible for the majority of agonism within feeding trees and target middle- and low-ranked individuals equally. These findings fit the predictions of current socioecological models for within-group contest competition over food resources. The results of this study suggest that within-group competition affects energy intake rate in white-faced capuchin monkeys.
Objectives
Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts ...surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late‐stage fermented foods, the ability of primates to detect them, and potential nutritional benefits.
Materials and methods
We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed‐effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates.
Results
Late‐stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%–3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late‐stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures.
Discussion
We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods.
Wild primates consuming fermented fruits.
In many slowly developing mammal species, males reach sexual maturity well before they develop secondary sexual characteristics. Sexually mature male orangutans have exceptionally long periods of ...developmental arrest. The two male morphs have been associated with behavioral alternative reproductive tactics, but this interpretation is based on cross‐sectional analyses predominantly of Northwest Sumatran populations. Here we present the first longitudinal analyses of behavioral changes of 10 adult males that have been observed in both unflanged and flanged morph. We also analyzed long‐term behavioral data on an additional 143 individually identified males from two study sites, Suaq (Sumatra, Pongo abelii) and Tuanan (Borneo, Pongo pygmaeus wurmbii), to assess male mating tactics cross‐sectionally in relation to population, male morph (unflanged and flanged), and other socio‐ecological factors. Both our longitudinal and cross‐sectional results confirm and refine previous cross‐sectional accounts of the differences in mating tactics between the unflanged and the flanged male morphs. In the unflanged morph, males exhibit higher sociability, particularly with females, and higher rates of both copulation and sexual coercion than in the flanged morph. Based on our results and those of previous studies showing that females prefer flanged males, and that flanged males have higher reproductive success, we conclude that unflanged males face a trade‐off between avoiding male‐male contest competition and gaining mating access to females, and thus follow a “best‐of‐a‐bad‐job” mating strategy.
Illustration of behavioral changes by individual male Bornean and Sumatran orang‐utans from the unflanged to the flanged morph (right). Pictures taken by A. Marzec, Suwi, C. Schuppli, G. Duvot (top left to bottom right)
HIGHLIGHTS
Longitudinal data confirm alternative reproductive tactics (ARTs) in orangutans
Within‐male behavioral changes after transition reflect differences between morphs
ARTs were consistent between a Sumatran and a Bornean population
Sexual coercion is neither an individual male trait nor an unflanged male default
The spatial and temporal variation in food abundance has strong effects on wildlife feeding and nutrition. This variation is exemplified by the peatland forests of Central Kalimantan, which are ...characterized by unpredictable fruiting fluctuations, relatively low levels of fruit availability, and low fruit periods (<3% of trees fruiting) that can last nearly a year. Challenged by these environments, large, arboreal frugivores like orangutans must periodically rely on non‐preferred, lower‐quality foods to meet their nutritional needs. We examined variation in nutrient intake among age‐sex classes and seasons over a 7‐year period at the Tuanan Orangutan Research Station in Central Kalimantan. We conducted 2,316 full‐day focal follows on 62 habituated orangutans (Pongo pygmaeus wurmbii). We found differences in total energy and macronutrient intake across age‐sex classes, controlling for metabolic body mass. Intake of both total energy and macronutrients varied with fruit availability, and preference of dietary items increased with their nutritional quality. Foraging‐related variables, such as day journey length, travel time, and feeding time, also varied among age‐sex classes and with fruit availability. Our results add to the growing body of literature suggesting that great variation in foraging strategies exists among species, populations, and age‐sex classes and in response to periods of resource scarcity.
Research Highlights
The spatial and temporal variation in food abundance has strong effects on wildlife feeding and nutrition. Here we present the first long term study of the effects of variation in fruit availability and age/sex class on nutritional ecology of wild Bornean orangutans. We examined variation in nutrient intake of wild orangutans in living in a peat swamp habitat over a 7‐year period at the Tuanan Orangutan Research Station in Central Kalimantan. We conducted 2,316 full‐day focal follows on 62 habituated orangutans (Pongo pygmaeus wurmbii). We found differences in total energy and macronutrient intake across age‐sex classes, controlling for metabolic body mass. Intake of both total energy and macronutrients varied with fruit availability, and preference of dietary items increased with their nutritional quality. Foraging‐related variables, such as day journey length, travel time, and feeding time, also varied among age‐sex classes and with fruit availability. Our results add to the growing body of literature suggesting that great variation in foraging strategies exists among species, populations, and age‐sex classes and in response to periods of resource scarcity.
The reduction of occlusal dimensions in early Homo is often proposed to be a functional adaptation to diet. With their smaller occlusal surfaces, species of early Homo are suggested to have reduced ...food-processing abilities, particularly for foods with high material properties (e.g., increased toughness). Here, we employ chewing efficiency as a measure of masticatory performance to test the relationships between masticatory function and food properties. We predicted that humans are more efficient when processing foods of lower toughness and Young's modulus values, and that subjects with larger occlusal surfaces will be less efficient when processing foods with higher toughness and Young's modulus, as the greater area spreads out the overall bite force applied to food particles. Chewing efficiency was measured in 26 adults using high-speed motion capture and surface electromyography. The dentition of each subject was cast and the occlusal surface was quantified using dental topographic analysis. Toughness and displacement-limited index were negatively correlated with chewing efficiency, but Young's modulus was not. Increased occlusal two-dimensional area and surface area were positively correlated with chewing efficiency for all foods. Thus, larger occlusal surface areas were more efficient when processing foods of greater toughness. These results suggest that the reduction in occlusal area in early Homo was associated with a reduction in chewing efficiency, particularly for foods with greater toughness. Further, the larger occlusal surfaces of earlier hominins such as Australopithecus would have likely increased chewing efficiency and increased the probability of fracture when processing tough foods.
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