Joerg U. Ganzhorn

Sensory Basis of Food Detection in Wild Microcebus murinus

Very little is known about how nocturnal primates find their food. Here we studied the sensory basis of food perception in wild-caught gray mouse lemurs (Microcebus murinus) in Madagascar. Mouse lemurs feed primarily on fruit and arthropods. We established a set of behavioral experiments to assess food detection in wild-born, field-experienced mouse lemurs in short-term captivity. Specifically, we investigated whether they use visual, auditory, and motion cues to find and to localize prey arthropods and further whether olfactory cues are sufficient for finding fruit. Visual cues from motionless arthropod dummies were not sufficient to allow reliable detection of prey in choice experiments, nor did they trigger prey capture behavior when presented on the feeding platform. In contrast, visual motion cues from moving prey dummies attracted their attention. Behavioral observations and experiments with live and recorded insect rustling sounds indicated that the lemurs make use of prey-generated acoustic cues for foraging. Both visual motion cues and acoustic prey stimuli on their own were sufficient to trigger approach and capture behavior in the mouse lemurs. For the detection of fruit, choice experiments showed that olfactory information was sufficient for mouse lemurs to find a piece of banana. Our study provides the first experimental data on the sensory ecology of food detection in mouse lemurs. Further research is necessary to address the role of sensory ecology for food selection and possibly for niche differentiation between sympatric Microcebus species.

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.

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.

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.

Possible asynchronous parturition in a multifetal strepsirrhine: Hapalemur meridionalis

Although infrequent among primates, twinning is common among strepsirrhines, a group of primates that includes the lemurs of Madagascar. As with any multifetal pregnancy, complications during gestation or even parturition can arise due to various factors (e.g., amniotic infection, stress). On rare occasions during labour of twins, parturition may be delayed between the two neonates, a phenomenon known as ‘delayed interval delivery’ that has been well-documented among the human medical journals. Based on circumstantial evidence, we report an opportunistic account of a habituated, adult female southern bamboo lemur (Hapalemur meridionalis) from Mandena, southeast Madagascar, first giving birth to an infant in mid-October 2013 (found deceased), and then birthing a live infant sometime between 5-21 days later. Similar to cases reported in human medical literature, the second infant survived and appeared to stay healthy until the conclusion of the study. Our account of asynchronous parturition of twins in a non-human primate is, to our knowledge, the first reported case in the literature.