Plant secondary metabolites and primate food choices: A meta-analysis and future directions.

The role of plant secondary metabolites (PSMs) in shaping the feeding decisions, habitat suitability, and reproductive success of herbivorous mammals has been a major theme in ecology for decades. Although primatologists were among the first to test these ideas, studies of PSMs in the feeding ecology of non-human primates have lagged in recent years, leading to a recent call for primatologists to reconnect with phytochemists to advance our understanding of the primate nutrition. To further this case, we present a formal meta-analysis of diet choice in response to PSMs based on field studies on wild primates. Our analysis of 155 measurements of primate feeding response to PSMs is drawn from 53 studies across 43 primate species which focussed primarily on the effect of three classes of PSMs tannins, phenolics, and alkaloids. We found a small but significant effect of PSMs on the diet choice of wild primates, which was largely driven by the finding that colobine primates showed a moderate aversion to condensed tannins. Conversely, there was no evidence that PSMs had a significant deterrent effect on food choices of non-colobine primates when all were combined into a single group. Furthermore, within the colobine primates, no other PSMs influenced feeding choices and we found no evidence that foregut anatomy significantly affected food choice with respect to PSMs. We suggest that methodological improvements related to experimental approaches and the adoption of new techniques including metabolomics are needed to advance our understanding of primate diet choice.

Sex and seasonal differences in diet and nutrient intake in Verreaux's sifakas (Propithecus verreauxi).

Fluctuations in food availability are a major challenge faced by primates living in seasonal climates. Variation in food availability can be especially challenging for females, because of the high energetic costs of reproduction. Therefore, females must adapt the particular demands of the different reproductive stages to the seasonal availability of resources. Madagascar has a highly seasonal climate, where food availability can be extremely variable. We investigated the seasonal changes in diet composition, nutrient and energy intake of female and male sifakas (Propithecus verreauxi) in a dry deciduous forest in western Madagascar. We examined how females adjust their diet to different reproductive stages. Seasonality affected the diet of both sexes; particularly in the dry season (Apr-Oct) with low availability of food items, especially fruits, males and females had a reduced nutrient and energy intake compared to the wet season (Nov-Mar) with higher food and fruit availability. The comparison of the diet between sexes in different reproductive stages showed that during the late stage of lactation (Nov-Jan) females had higher food intake, and as a result they had a higher intake of macronutrients (crude protein, fat and non-structured carbohydrates (TNC)) and energy than males. These differences were not present during the pregnancy of females, with both sexes having similar intake of macronutrients and energy during that stage. The increase in the intake of macronutrients observed for females during late lactation could be related to the higher energetic demands of this stage of reproduction. Thus, the observed pattern in the diet indicates that sifaka females are following a capital breeding strategy, whereby females potentially store enough nutrients to cope with the reproduction costs in periods of low food availability.

The importance of protein in leaf selection of folivorous primates.

Protein limitation has been considered a key factor in hypotheses on the evolution of life history and animal communities, suggesting that animals should prioritize protein in their food choice. This contrasts with the limited support that food selection studies have provided for such a priority in nonhuman primates, particularly for folivores. Here, we suggest that this discrepancy can be resolved if folivores only need to select for high protein leaves when average protein concentration in the habitat is low. To test the prediction, we applied meta-analyses to analyze published and unpublished results of food selection for protein and fiber concentrations from 24 studies (some with multiple species) of folivorous primates. To counter potential methodological flaws, we differentiated between methods analyzing total nitrogen and soluble protein concentrations. We used a meta-analysis to test for the effect of protein on food selection by primates and found a significant effect of soluble protein concentrations, but a non-significant effect for total nitrogen. Furthermore, selection for soluble protein was reinforced in forests where protein was less available. Selection for low fiber content was significant but unrelated to the fiber concentrations in representative leaf samples of a given forest. There was no relationship (either negative or positive) between the concentration of protein and fiber in the food or in representative samples of leaves. Overall our study suggests that protein selection is influenced by the protein availability in the environment, explaining the sometimes contradictory results in previous studies on protein selection. Am. J. Primatol. 79:e22550, 2017. © 2016 Wiley Periodicals, Inc.

Marine turtles used to assist Austronesian sailors reaching new islands.

Austronesians colonized the islands of Rapa Nui, Hawaii, the Marquesas and Madagascar. All of these islands have been found to harbor Austronesian artifacts and also, all of them are known nesting sites for marine turtles. Turtles are well known for their transoceanic migrations, sometimes totalling thousands of miles, between feeding and nesting grounds. All marine turtles require land for nesting. Ancient Austronesians are known to have had outstanding navigation skills, which they used to adjust course directions. But these skills will have been insufficient to locate tiny, remote islands in the vast Indo-Pacific oceans. We postulate that the Austronesians must have had an understanding of the marine turtles' migration patterns and used this knowledge to locate remote and unknown islands. The depth and speed at which marine turtles migrate makes following them by outrigger canoes feasible. Humans have long capitalized on knowledge of animal behavior.

Food for folivores: nutritional explanations linking diets to population density.

Ecologists want to explain why populations of animals are not evenly distributed across landscapes and often turn to nutritional explanations. In seeking to link population attributes with food quality, they often contrast nutritionally positive traits, such as the concentration of nitrogen, against negative ones, such as fibre concentration, by using a ratio of these traits. This specific ratio has attracted attention because it sometimes correlates with the biomass of colobine primates across sites in Asia and Africa. Although empirically successful, we have identified problems with the ratio that may explain why it fails under some conditions to predict colobine biomass. First, available nitrogen, rather than total nitrogen, is nutritionally important, while the presence of tannins is the major factor reducing the availability of nitrogen in browse plant species. Second, tannin complexes inflate measures of fibre. Finally, simple ratios may be unsound statistically because they implicitly assume isometric relationships between variables. We used data on the chemical composition of plants from three continents to examine the relationships between the concentrations of nitrogen, available nitrogen, fibre and tannins in foliage and to evaluate the nitrogen to fibre ratio. Our results suggest that the ratio of the concentration of nitrogen to fibre in leaves does sometimes closely correlate with the concentration of available nitrogen. However, the ratio may give misleading results when leaves contain high concentrations of tannins. The concentration of available nitrogen, which incorporates measures of total nitrogen, dry matter digestibility and tannins, should give a better indication of the nutritional value of leaves for herbivorous mammals that can readily be extrapolated to habitats.

Better few than hungry: flexible feeding ecology of collared lemurs Eulemur collaris in littoral forest fragments.

BACKGROUND: Frugivorous primates are known to encounter many problems to cope with habitat degradation, due to the fluctuating spatial and temporal distribution of their food resources. Since lemur communities evolved strategies to deal with periods of food scarcity, these primates are expected to be naturally adapted to fluctuating ecological conditions and to tolerate a certain degree of habitat changes. However, behavioral and ecological strategies adopted by frugivorous lemurs to survive in secondary habitats have been little investigated. Here, we compared the behavioral ecology of collared lemurs (Eulemur collaris) in a degraded fragment of littoral forest of south-east Madagascar, Mandena, with that of their conspecifics in a more intact habitat, Sainte Luce. METHODOLOGY/PRINCIPAL FINDINGS: Lemur groups in Mandena and in Sainte Luce were censused in 2004/2007 and in 2000, respectively. Data were collected via instantaneous sampling on five lemur groups totaling 1,698 observation hours. The Shannon index was used to determine dietary diversity and nutritional analyses were conducted to assess food quality. All feeding trees were identified and measured, and ranging areas determined via the minimum convex polygon. In the degraded area lemurs were able to modify several aspects of their feeding strategies by decreasing group size and by increasing feeding time, ranging areas, and number of feeding trees. The above strategies were apparently able to counteract a clear reduction in both food quality and size of feeding trees. CONCLUSIONS/SIGNIFICANCE: Our findings indicate that collared lemurs in littoral forest fragments modified their behavior to cope with the pressures of fluctuating resource availability. The observed flexibility is likely to be an adaptation to Malagasy rainforests, which are known to undergo periods of fruit scarcity and low productivity. These results should be carefully considered when relocating lemurs or when selecting suitable areas for their conservation.

Plant foods consumed by Pan: exploring the variation of nutritional ecology across Africa.

It has been shown that differences in resource density and nutrient supply affect variation in ranging patterns, habitat use, and sociality. Among nonhuman primates, chimpanzees (Pan troglodytes) and bonobos (P. paniscus) have often been used as models for the link between social system and habitat ecology. Field reports suggest that resource density is higher in habitats occupied by bonobos (compared to chimpanzee habitats), and in the West (compared to the East) of the range of chimpanzees. In this study we compared diet quality at the level of species and populations using information from nutritional analyses of fruit and leaves consumed by chimpanzees (three) and bonobos (one population). Quality of plant foods was assessed on the basis of a) the concentration of macronutrients, fiber, and anti-feedants, and b) associations of different nutrient components. Overall plant samples collected at each site differed in terms of macronutrient content. However, nutritious quality and gross energy content of food samples were similar suggesting that dietary quality reflects selectivity rather than habitat ecology. The quality of plant foods consumed by bonobos was within the range of chimpanzees and the quality of plant foods consumed by western chimpanzees was not higher than that of eastern chimpanzees. While the results showed significant variation across forests inhabited by Pan, they did not match with geographical patterns between and within Pan species as proposed in previous studies. This suggests that the nutritional quality of the habitat is not always a reliable predictor of the quality of the diet.