The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs.

Chimpanzees (Pan troglodytes) harbor rich assemblages of malaria parasites, including three species closely related to P. falciparum (sub-genus Laverania), the most malignant human malaria parasite. Here, we characterize the ecology and epidemiology of malaria infection in wild chimpanzee reservoirs. We used molecular assays to screen chimpanzee fecal samples, collected longitudinally and cross-sectionally from wild populations, for malaria parasite mitochondrial DNA. We found that chimpanzee malaria parasitism has an early age of onset and varies seasonally in prevalence. A subset of samples revealed Hepatocystis mitochondrial DNA, with phylogenetic analyses suggesting that Hepatocystis appears to cross species barriers more easily than Laverania. Longitudinal and cross-sectional sampling independently support the hypothesis that mean ambient temperature drives spatiotemporal variation in chimpanzee Laverania infection. Infection probability peaked at ~24.5 °C, consistent with the empirical transmission optimum of P. falciparum in humans. Forest cover was also positively correlated with spatial variation in Laverania prevalence, consistent with the observation that forest-dwelling Anophelines are the primary vectors. Extrapolating these relationships across equatorial Africa, we map spatiotemporal variation in the suitability of chimpanzee habitat for Laverania transmission, offering a hypothetical baseline indicator of human exposure risk.

Increased signal complexity is associated with increased mating success.

The evolution of complex signals has often been explored by testing multiple functional hypotheses regarding how independent signal components provide selective benefits to offset the costs of their production. In the present study, we take a different approach by exploring the function of complexity per se. We test the hypothesis that increased vibratory signal complexity-based on both proportional and temporal patterning-provides selective benefits to courting male Schizocosa stridulans wolf spiders. In support of this hypothesis, all of our quantified metrics of vibratory signal complexity predicted the mating success of male S. stridulans. The rate of visual signalling, which is mechanistically tied to vibratory signal production, was also associated with mating success. We additionally found evidence that males can dynamically adjust the complexity of their vibratory signalling. Together, our results suggest that complexity per se may be a target of female choice.

Range-wide indicators of African great ape density distribution.

Species distributions are influenced by processes occurring at multiple spatial scales. It is therefore insufficient to model species distribution at a single geographic scale, as this does not provide the necessary understanding of determining factors. Instead, multiple approaches are needed, each differing in spatial extent, grain, and research objective. Here, we present the first attempt to model continent-wide great ape density distribution. We used site-level estimates of African great ape abundance to (1) identify socioeconomic and environmental factors that drive densities at the continental scale, and (2) predict range-wide great ape density. We collated great ape abundance estimates from 156 sites and defined 134 pseudo-absence sites to represent additional absence locations. The latter were based on locations of unsuitable environmental conditions for great apes, and on existing literature. We compiled seven socioeconomic and environmental covariate layers and fitted a generalized linear model to investigate their influence on great ape abundance. We used an Akaike-weighted average of full and subset models to predict the range-wide density distribution of African great apes for the year 2015. Great ape densities were lowest where there were high Human Footprint and Gross Domestic Product values; the highest predicted densities were in Central Africa, and the lowest in West Africa. Only 10.7% of the total predicted population was found in the International Union for Conservation of Nature Category I and II protected areas. For 16 out of 20 countries, our estimated abundances were largely in line with those from previous studies. For four countries, Central African Republic, Democratic Republic of the Congo, Liberia, and South Sudan, the estimated populations were excessively high. We propose further improvements to the model to overcome survey and predictor data limitations, which would enable a temporally dynamic approach for monitoring great apes across their range based on key indicators.

Structure of Chimpanzee Gut Microbiomes across Tropical Africa.

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.

Recent genetic connectivity and clinal variation in chimpanzees.

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.

Community-based conservation and chimpanzee research in Gishwati forest, Rwanda.

As great ape populations around the world continue to decline, largely due to anthropogenic activities, conservation programs aimed at supporting these efforts have had mixed success. Here, we evaluate our community-based conservation program in Gishwati forest, Rwanda, aimed at helping to restore biodiversity and ecosystem services using chimpanzees as a flagship species. We examine the effectiveness of this program on reducing one of the ongoing threats to Gishwati's population of chimpanzees, illegal cattle grazing as well as the program's influence on the size of the chimpanzee population. We monitored illegal cattle grazing during several study periods between 2009 and 2019 in Gishwati forest following the implementation of our conservation program in 2008 that included law enforcement, community engagement, and research components. We found that when our conservation program was active, illegal cattle grazing was reduced to low levels. We also observed an increase in the chimpanzee population size during the 11 years since we started our conservation program. We examine how this reduction in cattle grazing and increase in chimpanzee population size may have been influenced by our community-centered approach and discuss the future of our conservation work in Gishwati.

Chimpanzee seed dispersal in a montane forest fragment in Rwanda.

Primate seed dispersal plays an important role in forest regeneration. It may be particularly important to anthropogenically disturbed habitats such as forest fragments. However, few studies have examined primate seed dispersal in these types of environments. Chimpanzees (Pan troglodytes) are frugivorous and large-bodied, and are therefore able to disperse both large and small seeds, making them an important seed dispersal species. We examined chimpanzee seed dispersal in Gishwati forest, a 14 km2 montane rainforest fragment in Rwanda. We systematically collected ≤24-hr-old fecal samples and counted the number of seeds of each fruit species. We also recorded observations of seeds found in wadges. We found that chimpanzees dispersed at least 18 fruit species in 14 families in their feces. Ninety-five percent of feces had seeds, the most common of which were Ficus spp., Myrianthus holstii, and Maesa lanceolata. We estimated that the Gishwati chimpanzee community with a density of 1.7 individuals per km2 dispersed an average of 592 (>2 mm) seeds km-2 day-1 . We also found that chimpanzees dispersed the seeds of at least two fruit species, Ficus spp. and Chrysophyllum gorungosanum, in their wadges. In addition, 17% of the tree species recorded in our vegetation plots were chimpanzee-dispersed. This study emphasizes the importance of chimpanzees as large seed dispersers in regenerating forest fragments. RESEARCH HIGHLIGHTS: Chimpanzees in Gishwati disperse a significant number of large seeds. Large-bodied seed dispersers, like chimpanzees, are particularly important in regenerating forest fragments.

Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir.

Chimpanzees in west central Africa (Pan troglodytes troglodytes) are endemically infected with simian immunodeficiency viruses (SIVcpzPtt) that have crossed the species barrier to humans and gorillas on at least five occasions, generating pandemic and nonpandemic forms of human immunodeficiency virus type 1 (HIV-1) as well as gorilla SIV (SIVgor). Chimpanzees in east Africa (Pan troglodytes schweinfurthii) are also infected with SIVcpz; however, their viruses (SIVcpzPts) have never been found in humans. To examine whether this is due to a paucity of natural infections, we used noninvasive methods to screen wild-living eastern chimpanzees in the Democratic Republic of the Congo (DRC), Uganda, and Rwanda. We also screened bonobos (Pan paniscus) in the DRC, a species not previously tested for SIV in the wild. Fecal samples (n = 3,108) were collected at 50 field sites, tested for species and subspecies origin, and screened for SIVcpz antibodies and nucleic acids. Of 2,565 samples from eastern chimpanzees, 323 were antibody positive and 92 contained viral RNA. The antibody-positive samples represented 76 individuals from 19 field sites, all sampled north of the Congo River in an area spanning 250,000 km(2). In this region, SIVcpzPts was common and widespread, with seven field sites exhibiting infection rates of 30% or greater. The overall prevalence of SIVcpzPts infection was 13.4% (95% confidence interval, 10.7% to 16.5%). In contrast, none of the 543 bonobo samples from six sites was antibody positive. All newly identified SIVcpzPts strains clustered in strict accordance to their subspecies origin; however, they exhibited considerable genetic diversity, especially in protein domains known to be under strong host selection pressure. Thus, the absence of SIVcpzPts zoonoses cannot be explained by an insufficient primate reservoir. Instead, greater adaptive hurdles may have prevented the successful colonization of humans by P. t. schweinfurthii viruses.

Females are choosier in the dark: environment-dependent reliance on courtship components and its impact on fitness.

A broad understanding of multimodal courtship function necessitates knowledge of the potential information content of signal components, the efficacy of signal components in eliciting the appropriate receiver response, and the fitness consequences of mating decisions based upon various signal components. We present data addressing each of these requirements for the multimodal-signaling wolf spider, Schizocosa floridana Bryant. Using diet manipulations, we first demonstrate that both visual and seismic courtship signals are condition-dependent. Next, using high- and low-quantity diet individuals in mate choice trials across manipulated signaling environments, we demonstrate that the seismic signal is crucial for mating success and further show that female choosiness is environment-dependent. Females mated more with high diet males only in the absence of visual signals, showing no discrimination in the presence of visual signals. Finally, by quantifying the number of offspring produced by our mated females, we reveal that a female's mating environment, in conjunction with her potential resource availability, influences her fitness-in environments in which females exerted choice, heavier females produced more offspring. Together, this comprehensive set of experiments demonstrates that female choosiness varies across environments, leading to direct fitness consequences.

Ground squirrels use an infrared signal to deter rattlesnake predation.

The evolution of communicative signals involves a major hurdle; signals need to effectively stimulate the sensory systems of their targets. Therefore, sensory specializations of target animals are important sources of selection on signal structure. Here we report the discovery of an animal signal that uses a previously unknown communicative modality, infrared radiation or "radiant heat," which capitalizes on the infrared sensory capabilities of the signal's target. California ground squirrels (Spermophilus beecheyi) add an infrared component to their snake-directed tail-flagging signals when confronting infrared-sensitive rattlesnakes (Crotalus oreganus), but tail flag without augmenting infrared emission when confronting infrared-insensitive gopher snakes (Pituophis melanoleucus). Experimental playbacks with a biorobotic squirrel model reveal this signal's communicative function. When the infrared component was added to the tail flagging display of the robotic models, rattlesnakes exhibited a greater shift from predatory to defensive behavior than during control trials in which tail flagging included no infrared component. These findings provide exceptionally strong support for the hypothesis that the sensory systems of signal targets should, in general, channel the evolution of signal structure. Furthermore, the discovery of previously undescribed signaling modalities such as infrared radiation should encourage us to overcome our own human-centered sensory biases and more fully examine the form and diversity of signals in the repertoires of many animal species.

Overview: Animal acoustic communication and the role of the physical environment.

Scientists from many distinct disciplines often use concepts such as habitat, environment, and niche to describe among other things the physical characteristics of the communicative worlds of animals. Often these descriptions center on the physical characteristics most salient to humans' perceptual systems. In this article, the authors advocate an approach to the description and analysis of the physical characteristics of animal communicative worlds based on J. von Uexküll's (1934/1957) concept of the Umwelt. Such an approach emphasizes the physical characteristics of the world as perceived by the organism in question, and its use has often led to novel and unexpected insights into animal communicative systems.

The rattling sound of rattlesnakes (Crotalus viridis) as a communicative resource for ground squirrels (Spermophilus beecheyi) and burrowing owls (Athene cunicularia).

Animal communication involves very dynamic processes that can generate new uses and functions for established communicative activities. In this article, the authors describe how an aposematic signal, the rattling sound of rattlesnakes (Crotalus viridis), has been exploited by 2 ecological associates of rattlesnakes: (a) California ground squirrels (Spermophilus beecheyi) use incidental acoustic cues in rattling sounds to assess the danger posed by the rattling snake, and (b) burrowing owls (Athene cunicularia) defend themselves against mammalian predators by mimicking the sound of rattling. The remarkable similarity between the burrowing owl's defensive hiss and the rattlesnake's rattling reflects both exaptation and adaptation. Such exploitation of the rattling sound has favored alternations in both the structure and the deployment of rattling by rattlesnakes.