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.

Seasonal adaptations in energy budgeting in the primate Lepilemur leucopus.

The spiny forest of South Madagascar is one of the driest and most unpredictable habitats in Africa. The small-bodied, nocturnal primate Lepilemur leucopus lives in this harsh habitat with high diurnal and seasonal changes in ambient temperature. In this study, we investigated seasonal adaptions in energy budgeting of L. leucopus, which allow it to live under these conditions by measuring resting metabolic rate using open-flow respirometry. No signs of heterothermy were detected, and resting metabolic rate was significantly lower in the warmer wet season than in the colder dry season. In fact, L. leucopus possesses one of the lowest mass-specific metabolic rates measured so far for an endotherm, probably the result of adaptations to its habitat and folivorous and potentially toxic diet. Surprisingly, we identified a shift of the thermoneutral zone from between 25 and 30 °C in the wet season to between 29 and 32 °C in the cool dry season. L. leucopus seems to be more affected by the hot daytime temperatures during the dry season and thermoregulation seems to be more costly during this time, which makes this shift of the thermoneutral zone advantageous. Our findings suggest that L. leucopus has a very small scope to unfavorable conditions, making it highly vulnerable, e.g., to changing conditions due to climate change.

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.

The contribution of community wisdom to conservation ecology.

Scientists have traditionally collected data on whether a population is increasing, decreasing, or staying the same, but such studies are often limited by geographic scale and time frame. This means that for many species, understanding of trends comes from only part of their ranges at particular periods. Working with citizen scientists has the potential to overcome these limits. Citizen science has the added benefit of exposing citizens to the scientific process and engaging them in management outcomes. We examined a different way of using citizen scientists (instead of data collection). We asked community members to answer a question directly and thus examined whether community wisdom can inform conservation. We reviewed the results of 3 mail-in surveys that asked community members to say whether they thought koala populations were increasing, decreasing, or staying the same. We then compared the survey results with population trends derived from more traditional research. Population trends identified through community wisdom were similar to the trends identified by traditional research. The community wisdom surveys, however, allowed the question to be addressed at much broader geographical scales and time frames. Studies that apply community wisdom have the benefit of engaging a broad section of the community in conservation research and education and therefore in the political process of conserving species.

Nutritional correlates of koala persistence in a low-density population.

It is widely postulated that nutritional factors drive bottom-up, resource-based patterns in herbivore ecology and distribution. There is, however, much controversy over the roles of different plant constituents and how these influence individual herbivores and herbivore populations. The density of koala (Phascolarctos cinereus) populations varies widely and many attribute population trends to variation in the nutritional quality of the eucalypt leaves of their diet, but there is little evidence to support this hypothesis. We used a nested design that involved sampling of trees at two spatial scales to investigate how leaf chemistry influences free-living koalas from a low-density population in south east New South Wales, Australia. Using koala faecal pellets as a proxy for koala visitation to trees, we found an interaction between toxins and nutrients in leaves at a small spatial scale, whereby koalas preferred trees with leaves of higher concentrations of available nitrogen but lower concentrations of sideroxylonals (secondary metabolites found exclusively in eucalypts) compared to neighbouring trees of the same species. We argue that taxonomic and phenotypic diversity is likely to be important when foraging in habitats of low nutritional quality in providing diet choice to tradeoff nutrients and toxins and minimise movement costs. Our findings suggest that immediate nutritional concerns are an important priority of folivores in low-quality habitats and imply that nutritional limitations play an important role in constraining folivore populations. We show that, with a careful experimental design, it is possible to make inferences about populations of herbivores that exist at extremely low densities and thus achieve a better understanding about how plant composition influences herbivore ecology and persistence.