Nutritional geometry of female chimpanzees (Pan troglodytes).

Primate foraging is influenced by the spatial and temporal distribution of foods, which may facilitate or constrain optimal nutrient intakes. Chimpanzees are frugivorous primates that mainly subsist on ripe fruit that is typically low in available protein (AP) and high in easily digestible carbohydrates. Because chimpanzees prefer ripe fruit and often eat it in large quantities compared with other foods, we hypothesized that protein intake would be tightly regulated while non-protein energy (NPE) would vary with fruit intake. To test this hypothesis, we conducted all-day follows on female chimpanzees, recorded all types of food consumed (i.e., drupes, figs, and non-fruit foods), estimated the nutritional contributions of these foods to daily NPE and AP intake and investigated how the ratio of NPE to AP varied due to changes in the types of foods consumed. Although the proportions of drupes, figs, and non-fruit foods varied in their diets, female chimpanzees maintained a relatively stable intake of AP while intake of NPE varied depending on the daily diet, demonstrating that like other frugivorous primates studied to date, chimpanzees prioritize protein. The mean daily ratio of NPE to AP was 7:1, which is similar to that of other frugivorous primates studied. Our results support the hypothesis that frugivorous animals may generally prioritize AP, while maximizing NPE intake within that constraint, and could shed light on aspects of human dietary evolution.

Bearded saki feeding strategies on an island in Lago Guri, Venezuela.

Free-ranging bearded sakis (Chiropotes spp.) live in relatively large social groups (22-65+), inhabit very large home ranges (200-1,000 ha), and travel long distances (1.8 to >7 km) each day. While these characteristics would seem to reduce their ability to occupy habitat fragments, several studies suggest otherwise. The key to their success may lie in their dietary adaptations. Bearded sakis are strongly frugivorous, but are primarily seed eaters, and are able to ingest both young and mature fruit. We examined feeding activities of a group of bearded sakis over a 19-month period on a 180 ha island in Lago Guri, Venezuela. Given their feeding adaptations, we predicted that they would minimize peaks and troughs in plant species used for food, limit seasonal variation in the mechanical properties of foods ingested, and balance ingestion of energy-rich foods (e.g. lipids, nonstructural carbohydrates (TNC), and/or free simple sugars). We found that bearded sakis on Danto Manchado had a diverse (plant-based) diet, but two resources (Pradosia caracasana, Sapotaceae, and Oryctanthus alveolatus, Loranthaceae) provided a stable dietary base and were present in the diet almost every month. Second, we found little variation in the mechanical-resistance properties of fruits opened seasonally. Third, they alternated months ingesting foods with high TNC content and months of high lipid content. This may be an attempt to balance energy intake from available foods. Finally, their social propensity to split up into subgroups may predispose them to reduce group sizes to accommodate smaller available areas. We suggest that bearded sakis use both ecological and behavioral mechanisms to survive in smaller-than-typical areas. Longer-term studies (beyond a few generations) of bearded sakis in habitat fragments would allow us to estimate minimum survival area and identify critical resources or resource combinations.

Vertical stratification of the nutritional value of fruit: macronutrients and condensed tannins.

Competing successfully for the best feeding sites is an important behavioral strategy but little is known about how feeding sites vary nutritionally within a fruit tree. To answer this question we tested how the nutritional value of a fruit is influenced by its ripeness and its height within the tree crown. A complementary objective was to assess the nutritional value of the midripe fruit, a food item rarely mentioned in the literature despite being exploited on a daily basis by many frugivores. We measured how the dry weight of pulp, water content, and concentration of macronutrients and condensed tannins varied within the tree crowns of 15 fruit species. Collections occurred early in the fruiting cycle, so as to assess the amount of food in the tree before its exploitation by primates. We found that (1) the upper crown produced fruit densities 4.2 times higher, and a fruit crop 4.8 times larger, than the lower crown of the same tree; (2) considering only midripe and ripe stages, upper-crown fruits contained 28.6% more dry pulp, 21.1% more water, and 13.5% more sugars per dry matter than lower-crown fruits of the same tree; (3) midripe fruits contained 80% of the concentrations of sugars of ripe fruits, making them a sweeter food item than one would expect from the intermediate color of their epidermis; (4) cellulose, hemicellulose, proteins, and ash proportionally decreased in concentration while dry pulp and sugars increased during ripening; and (5) ripe fruits were usually rare in the tree (<0.5% of all fruit available) compared to midripe fruits (3-8%). Overall, upper-crown feeding sites produced a higher density and quality of food than lower-crown sites of the same tree. Our data therefore provide a clear nutritional explanation for why tree-feeding frugivores compete for the highest feeding sites.

Optimal foraging on the roof of the world: Himalayan langurs and the classical prey model.

Optimal foraging theory has only been sporadically applied to nonhuman primates. The classical prey model, modified for patch choice, predicts a sliding "profitability threshold" for dropping patch types from the diet, preference for profitable foods, dietary niche breadth reduction as encounter rates increase, and that exploitation of a patch type is unrelated to its own abundance. We present results from a 1-year study testing these predictions with Himalayan langurs (Semnopithecus entellus) at Langtang National Park, Nepal. Behavioral data included continuous recording of feeding bouts and between-patch travel times. Encounter rates were estimated for 55 food types, which were analyzed for crude protein, lipid, free simple sugar, and fibers. Patch types were entered into the prey model algorithm for eight seasonal time periods and differing age-sex classes and nutritional currencies. Although the model consistently underestimated diet breadth, the majority of nonpredicted patch types represented rare foods. Profitability was positively related to annual/seasonal dietary contribution by organic matter estimates, whereas time estimates provided weaker relationships. Patch types utilized did not decrease with increasing encounter rates involving profitable foods, although low-ranking foods available year-round were taken predominantly when high-ranking foods were scarce. High-ranking foods were taken in close relation to encounter rates, while low-ranking foods were not. The utilization of an energetic currency generally resulted in closest conformation to model predictions, and it performed best when assumptions were most closely approximated. These results suggest that even simple models from foraging theory can provide a useful framework for the study of primate feeding behavior.

INFLUENCE OF FRUIT AVAILABILITY ON MACRONUTRIENT AND ENERGY INTAKE BY FEMALE CHIMPANZEES.

Daily energy intake of adult female mammals is influenced by environmental conditions and physiological requirements, including reproduction. We examined the effects of fruit availability on macronutrient and metabolisable energy intake by adult female chimpanzees (Pan troglodytes schweinfurthii) of the Kanyawara community in Kibale National Park, Uganda from January 2014 through June 2015. Drupe fruits were abundant for four months, whereas the other fourteen months were dominated by fig fruits. The mean daily intake of food (dry matter) and metabolisable energy, did not differ between drupe-months and fig-months. However, foraging costs were higher during fig-months, as indicated by a 20% increase in feeding time. Furthermore, during drupe-months female chimpanzees ingested more water-soluble carbohydrates and lipids, and less available protein and neutral detergent fibre. Although metabolisable energy intake did not differ consistently between drupe-months and fig-months, they consumed more on days when ripe fruit dominated the diet than when leaves and pithy stems dominated the diet. Our data suggest that differences in diet quality between drupes and figs can have important effects on frugivore foraging, and that they influence net energy gain more by their effects on macronutrient composition or foraging cost than by their direct impact on energy intake.