Jan F. Gogarten

Assessing the Evidence Supporting Fruit Bats as the Primary Reservoirs for Ebola Viruses.

Since their discovery 40 years ago, Ebola viruses (in the following: EBOV; family Filoviridae, genus Ebolavirus) continue to emerge unpredictably and cause Ebola virus disease (EVD) in humans and susceptible animals in tropical Africa (Leroy et al. 2004; Feldmann and Geisbert 2011). The scale of the current epidemic in West Africa demonstrates the impact that a single spillover event can have (Baize et al. 2014; Gire et al. 2014). Meanwhile, the reservoir(s) and ecology of EBOV remain largely unknown (Groseth et al. 2007; Feldmann and Geisbert 2011), hampering prediction of future outbreaks. To date, the only laboratory-confirmed sources of human EVD outbreaks were infected great apes and duikers (Leroy et al. 2004). However, these species are unlikely reservoirs as high mortality rates rule out an indefinite infection chain (Leroy et al. 2004; Bermejo et al. 2006; Wittmann et al. 2007). Scientists are therefore searching for other hosts where EBOV circulate without major negative effects; fruit bats have received the most research attention and are frequently referred to as the reservoir for African EBOV (Centers for Disease Control and Prevention 2014b; O’Shea et al. 2014; World Health Organization 2014). We review current evidence and highlight that fruit bats may not represent the main, or the sole, reservoir. We discuss evidence implicating insectivorous bats and reiterate that bats themselves might not be the ultimate reservoir for EBOV. Knowing which species are involved will facilitate an understanding of factors allowing spillover to susceptible human and wildlife populations (Viana et al. 2014; Plowright et al. 2015).

Reproductive seasonality is a poor predictor of receptive synchrony and male reproductive skew among nonhuman primates

Among nonhuman primates, male reproductive skew (i.e., the distribution of reproductive success across males) appears to be affected primarily by receptive synchrony and the number of males per group. These factors have been assumed to depend on reproductive seasonality, with strong seasonality increasing receptive synchrony, which in turn reduces the strength of male monopolization associated with more males and lower skew. Here we tested the importance of reproductive seasonality for 26 populations representing 15 species living in multimale groups. We obtained data from the literature on paternity, number of males per group, receptive synchrony, and three measures of seasonality of reproduction. We analyzed these data using bivariate regressions and hierarchical regression by sets and controlled for the effect of evolutionary relationships using phylogenetic generalized least squares. As expected, alpha male paternity decreased as the number of males per group increased as well as with increasing female receptive synchrony. Reproductive seasonality did not explain variation in reproductive skew over and above the variation explained by synchrony and the number of males. Reproductive seasonality alone only explained a small proportion of the variation in skew, and there was no strong association between reproductive seasonality and synchrony. The effects of receptive synchrony and reproductive seasonality as well as their link were reduced if we excluded captive populations. These results indicate that across primates male reproductive skew is related to the number of competitors in a group and that seasonality does not reliably predict synchrony or male reproductive skew.

SEASONAL MORTALITY PATTERNS IN NON-HUMAN PRIMATES: IMPLICATIONS FOR VARIATION IN SELECTION PRESSURES ACROSS ENVIRONMENTS

Examining seasonal mortality patterns can yield insights into the drivers of mortality and thus potential selection pressures acting on individuals in different environments. We compiled adult and juvenile mortality data from nine wild non‐human primate taxa to investigate the role of seasonality in patterns of mortality and address the following questions: Is mortality highly seasonal across species? Does greater environmental seasonality lead to more seasonal mortality patterns? If mortality is seasonal, is it higher during wet seasons or during periods of food scarcity? and Do folivores show less seasonal mortality than frugivores? We found seasonal mortality patterns in five of nine taxa, and mortality was more often tied to wet seasons than food‐scarce periods, a relationship that may be driven by disease. Controlling for phylogeny, we found a positive relationship between the degree of environmental seasonality and mortality, with folivores exhibiting more seasonal mortality than frugivores. These results suggest that mortality patterns are influenced both by diet and degree of environmental seasonality. Applied to a wider array of taxa, analyses of seasonal mortality patterns may aid understanding of life‐history evolution and selection pressures acting across a broad spectrum of environments and spatial and temporal scales.

Competing pressures on populations: long-term dynamics of food availability, food quality, disease, stress and animal abundance

Despite strong links between sociality and fitness that ultimately affect the size of animal populations, the particular social and ecological factors that lead to endangerment are not well understood. Here, we synthesize approximately 25 years of data and present new analyses that highlight dynamics in forest composition, food availability, the nutritional quality of food, disease, physiological stress and population size of endangered folivorous red colobus monkeys (Procolobus rufomitratus). There is a decline in the quality of leaves 15 and 30 years following two previous studies in an undisturbed area of forest. The consumption of a low-quality diet in one month was associated with higher glucocorticoid levels in the subsequent month and stress levels in groups living in degraded forest fragments where diet was poor was more than twice those in forest groups. In contrast, forest composition has changed and when red colobus food availability was weighted by the protein-to-fibre ratio, which we have shown positively predicts folivore biomass, there was an increase in the availability of high-quality trees. Despite these changing social and ecological factors, the abundance of red colobus has remained stable, possibly through a combination of increasing group size and behavioural flexibility.

Increasing Group Size Alters Behavior of a Folivorous Primate

Group size influences many aspects of mammalian social life, including stress levels, disease transmission, reproductive rates, and behavior. However, much of what is known about the effects of group size on behavioral ecology has come from comparisons across multiple groups of different sizes. These findings may be biased because behavioral differences across groups may be more indicative of how environmental variation influences animal behavior, rather than group size itself. To partially circumvent this limitation, we used longitudinal data to examine how changes in group size across time affect the behavior of folivorous red colobus monkeys (Procolobus rufomitratus) of Kibale National Park, Uganda. Controlling for food availability, we demonstrated that increasing group size resulted in altered activity budgets, based on 6 yr of data on a group that increased from 57 to 98 members. Specifically, as group size increased, individuals spent less time feeding and socializing, more time traveling, and increased the diversity of their diet. These changes appear to allow the monkeys to compensate for greater scramble competition apparent at larger group sizes, as increasing group size did not show the predicted relationship with lower female fecundity. Our results support recent findings documenting feeding competition in folivorous primates. Our results also document behavioral flexibility, an important trait that allows many social mammals to maximize the benefits of sociality (e.g., increased vigilance), while minimizing the costs (e.g., increased feeding competition).

The ecology of primate retroviruses – An assessment of 12 years of retroviral studies in the Taï national park area, Côte d'Ivoire

The existence and genetic make-up of most primate retroviruses was revealed by studies of bushmeat and fecal samples from unhabituated primate communities. For these, detailed data on intra- and within-species contact rates are generally missing, which makes identification of factors influencing transmission a challenging task. Here we present an assessment of 12 years of research on primate retroviruses in the Taï National Park area, Côte dIvoire. We discuss insights gained into the prevalence, within- and cross-species transmission of primate retroviruses (including towards local human populations) and the importance of virus-host interactions in determining cross-species transmission risk. Finally we discuss how retroviruses ecology and evolution may change in a shifting environment and identify avenues for future research.

Persistent anthrax as a major driver of wildlife mortality in a tropical rainforest

Anthrax is a globally important animal disease and zoonosis. Despite this, our current knowledge of anthrax ecology is largely limited to arid ecosystems, where outbreaks are most commonly reported. Here we show that the dynamics of an anthrax-causing agent, Bacillus cereus biovar anthracis, in a tropical rainforest have severe consequences for local wildlife communities. Using data and samples collected over three decades, we show that rainforest anthrax is a persistent and widespread cause of death for a broad range of mammalian hosts. We predict that this pathogen will accelerate the decline and possibly result in the extirpation of local chimpanzee (Pan troglodytes verus) populations. We present the epidemiology of a cryptic pathogen and show that its presence has important implications for conservation.

Seasonal mortality patterns in primates: implications for the interpretation of dental microwear.

The microscopic traces of use wear on teeth have been extensively studied to provide information that will assist in elucidating the dietary habits of extinct hominin species. It has been amply documented that dental microwear provides information pertaining to diet for living animals, where there is a strong and consistent association between dental microwear patterns and different types of foods that are chewed. The details of occlusal surface wear patterns are capable of distinguishing among diets when the constituent food items differ in their fracture properties. For example, the microwear traces left on the teeth of mammals that crush hard, brittle foods such as nuts are generally dominated by pits, whereas traces left on the teeth of mammals that shear tough items such as leaves tend to be characterized by scratches. These microwear features result from and thus record actual chewing events. As such, microwear patterns are expected to be variably ephemeral, as individual features are worn away and replaced or overprinted by others as the tooth wears down in subsequent bouts of mastication. Indeed, it has been demonstrated, both in the laboratory and the wild, that short‐term dietary variation can result in the turnover of microwear. Because occlusal microwear potentially reflects an individuals diet for a short time (days, weeks, or months, depending on the nature of the foods being masticated), tooth surfaces sampled at different times will display differences that relate to temporal (for example, seasonal) differences in diet.

Flexible decision-making in grooming partner choice in sooty mangabeys and chimpanzees

Living in permanent social groups forces animals to make decisions about when, how and with whom to interact, requiring decisions to be made that integrate multiple sources of information. Changing social environments can influence this decision-making process by constraining choice or altering the likelihood of a positive outcome. Here, we conceptualized grooming as a choice situation where an individual chooses one of a number of potential partners. Studying two wild populations of sympatric primate species, sooty mangabeys (Cercocebus atys atys) and western chimpanzees (Pan troglodytes verus), we tested what properties of potential partners influenced grooming decisions, including their relative value based on available alternatives and the social relationships of potential partners with bystanders who could observe the outcome of the decision. Across 1529 decision events, multiple partner attributes (e.g. dominance ranks, social relationship quality, reproductive state, partner sex) influenced choice. Individuals preferred to initiate grooming with partners of similar global rank, but this effect was driven by a bias towards partners with a high rank compared to other locally available options. Individuals also avoided grooming partners who had strong social relationships with at least one bystander. Results indicated flexible decision-making in grooming interactions in both species, based on a partners value given the local social environment. Viewing partner choice as a value-based decision-making process allows researchers to compare how different species solve similar social problems.