Showing papers by "Martha M. Robbins published in 2021"

A deepening understanding of animal culture suggests lessons for conservation.

Abstract: A key goal of conservation is to protect biodiversity by supporting the long-term persistence of viable, natural populations of wild species. Conservation practice has long been guided by genetic, ecological and demographic indicators of risk. Emerging evidence of animal culture across diverse taxa and its role as a driver of evolutionary diversification, population structure and demographic processes may be essential for augmenting these conventional conservation approaches and decision-making. Animal culture was the focus of a ground-breaking resolution under the Convention on the Conservation of Migratory Species of Wild Animals (CMS), an international treaty operating under the UN Environment Programme. Here, we synthesize existing evidence to demonstrate how social learning and animal culture interact with processes important to conservation management. Specifically, we explore how social learning might influence population viability and be an important resource in response to anthropogenic change, and provide examples of how it can result in phenotypically distinct units with different, socially learnt behavioural strategies. While identifying culture and social learning can be challenging, indirect identification and parsimonious inferences may be informative. Finally, we identify relevant methodologies and provide a framework for viewing behavioural data through a cultural lens which might provide new insights for conservation management.

The long lives of primates and the 'invariant rate of ageing' hypothesis.

Abstract: Is it possible to slow the rate of ageing, or do biological constraints limit its plasticity? We test the 'invariant rate of ageing' hypothesis, which posits that the rate of ageing is relatively fixed within species, with a collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the highly regular relationship between life expectancy and lifespan equality seen in humans. We next demonstrate that variation in the rate of ageing within genera is orders of magnitude smaller than variation in pre-adult and age-independent mortality. Finally, we demonstrate that changes in the rate of ageing, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of ageing hypothesis, implying biological constraints on how much the human rate of ageing can be slowed.

Maximizing the acquisition of unique reads in noninvasive capture sequencing experiments

Abstract: Noninvasive samples as a source of DNA are gaining interest in genomic studies of endangered species. However, their complex nature and low endogenous DNA content hamper the recovery of good quality data. Target capture has become a productive method to enrich the endogenous fraction of noninvasive samples, such as faeces, but its sensitivity has not yet been extensively studied. Coping with faecal samples with an endogenous DNA content below 1% is a common problem when prior selection of samples from a large collection is not possible. However, samples classified as unfavourable for target capture sequencing might be the only representatives of unique specific geographical locations, or to answer the question of interest. To explore how library complexity may be increased without repeating DNA extractions and generating new libraries, in this study we captured the exome of 60 chimpanzees (Pan troglodytes) using faecal samples with very low proportions of endogenous content (<1%). Our results indicate that by performing additional hybridizations of the same libraries, the molecular complexity can be maintained to achieve higher coverage. Also, whenever possible, the starting DNA material for capture should be increased. Finally, we specifically calculated the sequencing effort needed to avoid exhausting the library complexity of enriched faecal samples with low endogenous DNA content. This study provides guidelines, schemes and tools for laboratories facing the challenges of working with noninvasive samples containing extremely low amounts of endogenous DNA.

Dominance style is a key predictor of vocal use and evolution across nonhuman primates

Abstract: Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships.

Primate phageomes are structured by superhost phylogeny and environment.

Abstract: Humans harbor diverse communities of microorganisms, the majority of which are bacteria in the gastrointestinal tract These gut bacterial communities in turn host diverse bacteriophage (hereafter phage) communities that have a major impact on their structure, function, and, ultimately, human health However, the evolutionary and ecological origins of these human-associated phage communities are poorly understood To address this question, we examined fecal phageomes of 23 wild nonhuman primate taxa, including multiple representatives of all the major primate radiations We find relatives of the majority of human-associated phages in wild primates Primate taxa have distinct phageome compositions that exhibit a clear phylosymbiotic signal, and phage-superhost codivergence is often detected for individual phages Within species, neighboring social groups harbor compositionally and evolutionarily distinct phageomes, which are structured by superhost social behavior Captive nonhuman primate phageome composition is intermediate between that of their wild counterparts and humans Phage phylogenies reveal replacement of wild great ape-associated phages with human-associated ones in captivity and, surprisingly, show no signal for the persistence of wild-associated phages in captivity Together, our results suggest that potentially labile primate-phage associations have persisted across millions of years of evolution Across primates, these phylosymbiotic and sometimes codiverging phage communities are shaped by transmission between groupmates through grooming and are dramatically modified when primates are moved into captivity

Recent genetic connectivity and clinal variation in chimpanzees

Abstract: Much like humans, chimpanzees occupy diverse habitats and exhibit extensive behavioural variability. However, chimpanzees are recognized as a discontinuous species, with four subspecies separated by historical geographic barriers. Nevertheless, their range-wide degree of genetic connectivity remains poorly resolved, mainly due to sampling limitations. By analyzing a geographically comprehensive sample set amplified at microsatellite markers that inform recent population history, we found that isolation by distance explains most of the range-wide genetic structure of chimpanzees. Furthermore, we did not identify spatial discontinuities corresponding with the recognized subspecies, suggesting that some of the subspecies-delineating geographic barriers were recently permeable to gene flow. Substantial range-wide genetic connectivity is consistent with the hypothesis that behavioural flexibility is a salient driver of chimpanzee responses to changing environmental conditions. Finally, our observation of strong local differentiation associated with recent anthropogenic pressures portends future loss of critical genetic diversity if habitat fragmentation and population isolation continue unabated.

Discovery of Novel Herpes Simplexviruses in Wild Gorillas, Bonobos, and Chimpanzees Supports Zoonotic Origin of HSV-2.

Abstract: Output Status: Forthcoming/Available Online Additional co-authors: Hjalmar Kuehl, Kevin E Langergraber, Kevin Lee, Nadege F Madinda, Sonja Metzger, Lucy Jayne Ormsby, Martha M Robbins, Volker Sommer, Tara Stoinski, Erin G Wessling, Roman M Wittig, Yisa Ginath Yuh, Fabian H Leendertz, Sebastien Calvignac-Spencer

Structure of Chimpanzee Gut Microbiomes across Tropical Africa

Abstract: Understanding variation in host-associated microbial communities is important given the relevance of microbiomes to host physiology and health. Using 560 fecal samples collected from wild chimpanzees (Pan troglodytes) across their range, we assessed how geography, genetics, climate, vegetation, and diet relate to gut microbial community structure (prokaryotes, eukaryotic parasites) at multiple spatial scales. We observed a high degree of regional specificity in the microbiome composition, which was associated with host genetics, available plant foods, and potentially with cultural differences in tool use, which affect diet. Genetic differences drove community composition at large scales, while vegetation and potentially tool use drove within-region differences, likely due to their influence on diet. Unlike industrialized human populations in the United States, where regional differences in the gut microbiome are undetectable, chimpanzee gut microbiomes are far more variable across space, suggesting that technological developments have decoupled humans from their local environments, obscuring regional differences that could have been important during human evolution. IMPORTANCE Gut microbial communities are drivers of primate physiology and health, but the factors that influence the gut microbiome in wild primate populations remain largely undetermined. We report data from a continent-wide survey of wild chimpanzee gut microbiota and highlight the effects of genetics, vegetation, and potentially even tool use at different spatial scales on the chimpanzee gut microbiome, including bacteria, archaea, and eukaryotic parasites. Microbial community dissimilarity was strongly correlated with chimpanzee population genetic dissimilarity, and vegetation composition and consumption of algae, honey, nuts, and termites were potentially associated with additional divergence in microbial communities between sampling sites. Our results suggest that host genetics, geography, and climate play a far stronger role in structuring the gut microbiome in chimpanzees than in humans.

Chest beats as an honest signal of body size in male mountain gorillas (Gorilla beringei beringei)

Abstract: Acoustic signals that reliably indicate body size, which usually determines competitive ability, are of particular interest for understanding how animals assess rivals and choose mates. Whereas body size tends to be negatively associated with formant dispersion in animal vocalizations, non-vocal signals have received little attention. Among the most emblematic sounds in the animal kingdom is the chest beat of gorillas, a non-vocal signal that is thought to be important in intra and inter-sexual competition, yet it is unclear whether it reliably indicates body size. We examined the relationship among body size (back breadth), peak frequency, and three temporal characteristics of the chest beat: duration, number of beats and beat rate from sound recordings of wild adult male mountain gorillas. Using linear mixed models, we found that larger males had significantly lower peak frequencies than smaller ones, but we found no consistent relationship between body size and the temporal characteristics measured. Taken together with earlier findings of positive correlations among male body size, dominance rank and reproductive success, we conclude that the gorilla chest beat is an honest signal of competitive ability. These results emphasize the potential of non-vocal signals to convey important information in mammal communication.

Variability of weaning age in mountain gorillas (Gorilla beringei beringei).

Abstract: OBJECTIVES Weaning is a key life history milestone for mammals that represents both the end of nutritional investment from the perspective of mothers and the start of complete nutritional independence for the infants. The age at weaning may vary depending on ecological, social, and demographic factors experienced by the mother and infant. Bwindi mountain gorillas live in different environmental conditions and have longer interbirth intervals than their counterparts in the Virunga Volcanoes, yet other life history characteristics of this population remain less well known. We use long-term data from Bwindi Impenetrable National Park, Uganda to examine factors related to weaning age. MATERIALS AND METHODS We analyzed data on infants born in four mountain gorilla groups in Bwindi to quantify their age of weaning (defined as last nipple contact) and to test if the sex of offspring, parity, and dominance rank of mother influences age of weaning. We also compared the age at weaning and time to conception after resumption of mating in Bwindi and Virunga gorillas. RESULTS Bwindi gorillas were weaned at an average age of 57.5 months. No difference was found between age of weaning for primiparous and multiparous mothers, nor did maternal dominance rank influence age of weaning, but sons were weaned at a later age than daughters. The majority of Bwindi mothers were still suckling when they resumed mating and mothers generally conceived before they weaned their previous offspring. The age of weaning was significantly later in Bwindi than in Virunga gorillas. After mothers resumed mating, the time to conceiving the next offspring was not significantly longer for Bwindi females than Virungas females (6 vs. 4 months). DISCUSSION Later weaning age for sons than daughters is similar to findings of other studies of great apes. Bwindi mountain gorillas are weaned at approximately the same age as western gorillas and chimpanzees, which is more than a year later than Virunga mountain gorillas. The results of this study suggest that variation in ecological conditions of populations living in close geographic proximity can result in variation in life history patterns, which has implications for understanding the evolution of the unique life history patterns of humans.

Assessing attitudes towards gorilla conservation via employee interviews

Abstract: To determine the effectiveness of conservation strategies, not only should we monitor biological variables, such as population size and levels of illegal activity, but also we should examine changes in attitudes and behavior of local community members. Here, I use semistructured interviews of employees at two field sites, in Bwindi Impenetrable National Park, Uganda and Loango National Park, Gabon, to understand if their employment influenced their attitude towards gorillas and conservation and led to behavior change. In contrast to western views of gorillas as "gentle giants," staff viewed gorillas as dangerous animals before working for these projects. Overall, employment leads to viewing conservation and gorillas more positively, and in many cases, viewing the gorillas as kin. The most common value attributed to the gorillas was economic, yet intrinsic and non-use existence values were frequently mentioned. Loango staff, but not Bwindi staff, reported behavior change related to hunting and bushmeat consumption, which likely is related to bushmeat consumption being commonplace in Gabon but not in Uganda. The Bwindi staff seemed to have a more positive and broader outlook toward conservation than the Loango staff, possibly because they had more years of formal education, they worked with gorillas longer, there is more history of conservation activities in Bwindi, and/or they have been less directly affected by negative consequences of conservation (e.g., crop raiding). This study shows the importance of explaining that gorillas are not dangerous if not provoked and using their human-like characteristics as a means to change conservation values and interest of local communities, while concurrently recognizing that providing economic benefits and reducing negative effects of wildlife are a reality for conservation buy-in.

Dissecting the two mechanisms of scramble competition among the Virunga mountain gorillas

Abstract: Two mechanisms have been proposed to explain why scramble competition can increase the travel requirements of individuals within larger groups. Firstly, individuals in larger groups may be more likely to encounter food sites where other group members have already eaten, leading to greater asynchronous “individual” travel to find fresh sites. Secondly, when food sites are aggregated into patches, larger groups may need to visit more patches to obtain the same amount of food per capita, leading to greater synchronous “group” travel between patches. If the first mechanism can be mitigated by increasing group spread, then we expect the second mechanism to be more sensitive to group size. Here, we examine the individual travel and group travel of the Virunga mountain gorillas, along with potential implications for the two mechanisms of scramble competition. Asynchronous individual travel accounted for 67% of the total travel time, and the remainder arose from group travel. Group spread increased significantly for larger groups, but not enough to prevent an increase in individual travel. Contrary to expectations, group travel decreased with size among most groups, and we found only limited evidence of patch depletion that would cause the second mechanism of scramble competition. Collectively, our results illustrate how the influence of group size can differ for individual travel versus group travel, just as it differs among species for overall travel. Studies that distinguish between the two mechanisms of scramble competition may enhance our understanding of ecological constraints upon group size, including potential differences between frugivores and folivores. Feeding competition provides insight into how group size can influence the foraging patterns of social animals, but two key mechanisms are not typically compared. Firstly, larger groups may visit more patches to access the same amount of food per capita (group travel). Secondly, their individuals may also need to move past more spots where another member has already eaten (individual travel). Contrary to expectations, we found that group travel decreased with size for most groups of mountain gorillas, which may reflect extra travel by smaller groups to avoid larger groups. Individual travel increased with size in most groups, even though gorillas in larger groups compensated by spreading out over a broader area. The two mechanisms revealed patterns that were not apparent in our previous study of overall travel. Our approach may help to explain potential differences between folivores and frugivores.