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 To test the prediction, we applied meta-analyses to analyze published and unpublished results of food selection for protein and fiber concentrations from 24 studies (some with multiple species) of folivorous primates.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.

Pathogenic enterobacteria in lemurs associated with anthropogenic disturbance.

As human population density continues to increase exponentially, speeding the reduction and fragmentation of primate habitat, greater human-primate contact is inevitable, making higher rates of pathogen transmission likely. Anthropogenic effects are particularly evident in Madagascar, where a diversity of endemic lemur species are threatened by rapid habitat loss. Despite these risks, knowledge of how anthropogenic activities affect lemur exposure to pathogens is limited. To improve our understanding of this interplay, we non-invasively examined six species of wild lemurs in Ranomafana National Park for enteric bacterial pathogens commonly associated with diarrheal disease in human populations in Madagascar. Patterns of infection with Enterotoxigenic Escherichia coli, Shigella spp., Salmonella enterica, Vibrio cholerae, and Yersinia spp. (enterocolitica and pseudotuberculosis) were compared between lemurs inhabiting intact forest and lemurs inhabiting degraded habitat with frequent exposure to tourism and other human activity. Fecal samples acquired from humans, livestock, and rodents living near the degraded habitat were also screened for these bacteria. Remarkably, only lemurs living in disturbed areas of the park tested positive for these pathogens. Moreover, all of these pathogens were present in the human, livestock, and/or rodent populations. These data suggest that lemurs residing in forests altered or frequented by people, livestock, or peridomestic rodents, are at risk for infection by these diarrhea-causing enterobacteria and other similarly transmitted pathogens.

Morphometrics and pattern of growth in wild sifakas (Propithecus edwardsi) at Ranomafana National Park, Madagascar.

We summarize morphometric data collected over a period of 22 years from a natural population of rainforest sifakas (Propithecus edwardsi) at Ranomafana National Park, Madagascar, and we use those data to document patterns of growth and development. Individually identified, known-age sifakas were successfully captured, measured, and released. We found that body segment lengths increased faster during growth than did body mass, with individuals attaining adult lengths earlier than adult mass. Females can begin reproducing before they are fully grown, but this may not be common. With the exception of hand length, we found no significant sex difference in any adult metric including body mass, chest, and limb circumferences, body segment lengths, and canine tooth height; however, body masses of individual females fluctuated more, independently of pregnancy, than did those of males. We found considerable interannual fluctuation in body mass with single individuals differing more within the same season in different years than from season to season in the same year. Such body mass fluctuation may be a consequence of eastern Madagascar's variable and unpredictable environment in which rainfall during any selected month varies from year to year.

Low Levels of Fruit Nitrogen as Drivers for the Evolution of Madagascar's Primate Communities.

The uneven representation of frugivorous mammals and birds across tropical regions - high in the New World, low in Madagascar and intermediate in Africa and Asia - represents a long-standing enigma in ecology. Several hypotheses have been proposed to explain these differences but the ultimate drivers remain unclear. Here, we tested the hypothesis that fruits in Madagascar contain insufficient nitrogen to meet primate metabolic requirements, thus constraining the evolution of frugivory. We performed a global analysis of nitrogen in fruits consumed by primates, as collated from 79 studies. Our results showed that average frugivory among lemur communities was lower compared to New World and Asian-African primate communities. Fruits in Madagascar contain lower average nitrogen than those in the New World and Old World. Nitrogen content in the overall diets of primate species did not differ significantly between major taxonomic radiations. There is no relationship between fruit protein and the degree of frugivory among primates either globally or within regions, with the exception of Madagascar. This suggests that low protein availability in fruits influences current lemur communities to select for protein from other sources, whereas in the New World and Old World other factors are more significant in shaping primate communities.

Possible fruit protein effects on primate communities in madagascar and the neotropics.

BACKGROUND: 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. METHODOLOGY/PRINCIPAL FINDINGS: 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. CONCLUSIONS/SIGNIFICANCE: 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.

Dental senescence in a long-lived primate links infant survival to rainfall.

Primates tend to be long-lived, and, except for humans, most primate females are able to reproduce into old age. Although aging in most mammals is accompanied by dental senescence due to advanced wear, primates have low-crowned teeth that wear down before old age. Because tooth wear alters crown features gradually, testing whether early dental senescence causes reproductive senescence has been difficult. To identify whether and when low-crowned teeth compromise reproductive success, we used a 20-year field study of Propithecus edwardsi, a rainforest lemur from Madagascar with a maximum lifespan of >27 years. We analyzed tooth wear in three dimensions with dental topographic analysis by using Geographical Information Systems (GIS) technology. We report that tooth wear exposes compensatory shearing blades that maintain dental function for 18 years. Beyond this age, female fertility remains high; however infants survive only if lactation seasons have elevated rainfall. Therefore, low-crowned teeth accommodate wear to a point, after which reproductive success closely tracks environmental fluctuations. These results suggest a tooth wear-determined, but rainfall-mediated, onset of reproductive senescence. Additionally, our study indicates that even subtle changes in climate may affect reproductive success of rainforest species.