Arboreal monkeys facilitate foraging of terrestrial frugivores

Terrestrial animals feed on fruit dropped by arboreal frugivores in tropical forests around the world, but it remains unknown whether the resulting spatial associations of these animals are coincidental or intentionally maintained. On Barro Colorado Island, Panama, we used a combination of acoustic playback experiments, remote camera monitoring, and GPS tracking to quantify the frequency of such interactions, determine who initiates and maintains spatial associations, and test whether terrestrial animals adopt a strategy of acoustic eavesdropping to locate fruit patches created by foraging primates. Indeed, 90% of fruits collected in fruit fall traps had tooth marks of arboreal frugivores, and terrestrial frugivores visited fruit trees sooner following visits by GPS-collared monkeys. While our play back experiments were insufficient to support the hypothesis that terrestrial frugivores use auditory cues to locate food dropped by arboreal primates, analyses of movement paths of capuchin monkeys (Cebus capucinus), spider monkeys (Ateles geoffroyi), and coatis (Nasua narica) reveal that observed patterns of interspecific attraction are not merely a byproduct of mutual attraction to shared resources. Coatis were significantly more likely to initiate close encounters with arboreal primates than vice versa and maintained these associations by spending significantly longer periods at fruiting trees when collared primates were present. Our results demonstrate that terrestrial frugivores are attracted to arboreal primates, likely because they increase local resource availability. Primates are often among the first species in a habitat to be extirpated by hunting; our results suggest that their loss may have unanticipated consequences for the frugivore community

Coupling of coastal activity with tidal cycles is stronger in tool-using capuchins (Cebus capucinus imitator)

Terrestrial mammals exploiting coastal resources must cope with the challenge that resource availability and accessibility fluctuate with tidal cycles. Tool use can improve foraging efficiency and provide access to structurally protected resources that are otherwise unavailable (e.g. molluscs and fruits). To understand how variable accessibility of valuable resources shapes behavioural patterns, and whether tool use aids in the efficient exploitation of intertidal resources, we compared the relationship between tidal cycles and activity patterns of tool-using versus non-tool-using groups of white-faced capuchin monkeys on Jicarón Island in Coiba National Park, Panama. Although tool use on Jicarón is localized to a small stretch of coast (approx. 1 km), all coastal groups forage on intertidal resources. Using more than 5 years of camera trap data at varying distances from the coast, we found that capuchins on Jicarón showed increased coastal activity during specific parts of the tidal cycle, and that this relationship differed between tool-using and non-tool-using groups, as well as between seasons. Activity patterns of tool-using capuchins were more strongly and consistently tied to tidal cycles compared with non-tool-users, indicating that tool use might allow for more efficient exploitation of tidal resources. Our findings highlight the potential of tool use to aid niche expansion

Nutritional ecology of wild Bornean orangutans (Pongo pygmaeus wurmbii) in a peat swamp habitat: Effects of age, sex, and season

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

A Quantitative Framework for Identifying Patterns of Route-Use in Animal Movement Data

Animal movement along repeatedly used, “habitual” routes could emerge from a variety of cognitive mechanisms, as well as in response to a diverse set of environmental features. Because of the high conservation value of identifying wildlife movement corridors, there has been extensive work focusing on environmental factors that contribute to the emergence of habitual routes between protected habitats. In parallel, significant work has focused on disentangling the cognitive mechanisms underlying animal route use, as such movement patterns are of fundamental interest to the study of decision making and navigation. We reviewed the types of processes that can generate routine patterns of animal movement, suggested a new methodological workflow for classifying one of these patterns—high fidelity path reuse—in animal tracking data, and compared the prevalence of this pattern across four sympatric species of frugivorous mammals in Panama. We found the highest prevalence of route-use in kinkajous, the only nocturnal species in our study, and propose that further development of this method could help to distinguish the processes underlying the presence of specific routes in animal movement data.publishe

Nutritional Differences between Two Orangutan Habitats: Implications for Population Density

<div><p>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.</p></div

Daily caloric intake (a), total feeding time (b), and fruit feeding time compared (c).

<p>Site differences in (a) Daily caloric intake (t-statistic = 12.26, p < 0.0001), (b) Total feeding time (t-statistic = -6.35, p < 0.0001), and (c) Fruit feeding time (t-statistic = -7.19, p < 0.0001) between the two sites. T = Tuanan, S = Sabangau. Generalized additive mixed models (GAMM) were used. A positive t-statistic indicates Tuanan is higher. See <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0138612#pone.0138612.t003" target="_blank">Table 3</a> for models and full statistical results.</p

Site variation in (a) Daily caloric intake, (b) Daily feeding time (min), and (c) Daily time spent feeding on fruit (min).

<p>All models include the variable age/sex class: FLM = flanged male; NUF = nulliparous independent female; UFM = unflanged adult male; AF = adult female; Age/Sex class comparisons are against AF. FAI = Percentage of fruiting trees.</p

Percentage of fruiting trees over the entire study period in Tuanan (red) and Sabangau (blue).

<p>Percentage of fruiting trees over the entire study period in Tuanan (red) and Sabangau (blue).</p

Variation in macronutrient composition in the orangutan diets in Tuanan (T) and Sabangau (S).

<p>All comparisons are based on organic matter (OM) and Wilcoxon Signed Rank Test were used. A significant negative Z-statistic indicates Tuanan is greater. (a) Lipids (Z = -2.17, p = 0.03); (b) Total non-structural carbohydrates (TNC; Z = -5.43, p < 0.0001); (c) Neutral detergent fiber (NDF; Z = 5.63, p < 0.0001); (d) Crude protein (CP; Z = 0.64, p = 0.52); (e) Metabolizable energy (Kcal/100 g OM) (Z = -5.55, p < 0.0001); (f) Metabolizable energy/item (Kcal)(Z = -2.64, p = 0.008). See <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0138612#pone.0138612.t001" target="_blank">Table 1</a> for complete statistical results.</p