The establishment of a collaborative surveillance program with indigenous hunters to characterize primate health in Southern Guyana.

The consumption of primates is integral to the traditional subsistence strategies of many Indigenous communities throughout Amazonia. Understanding the overall health of primates harvested for food in the region is critical to Indigenous food security and thus, these communities are highly invested in long-term primate population health. Here, we describe the establishment of a surveillance comanagement program among the Waiwai, an Indigenous community in the Konashen Amerindian Protected Area (KAPA). To assess primate health in the KAPA, hunters performed field necropsies on primates harvested for food and tissues collected from these individuals were analyzed using histopathology. From 2015 to 2019, hunters conducted 127 necropsies across seven species of primates. Of this sample, 82 primates (between 2015 and 2017) were submitted for histopathological screening. Our histopathology data revealed that KAPA primates had little evidence of underlying disease. Of the tissue abnormalities observed, the majority were either due to diet (e.g., hepatocellular pigment), degenerative changes resulting from aging (e.g., interstitial nephritis, myocyte lipofusion), or nonspecific responses to antigenic stimulation (renal and splenic lymphoid hyperplasia). In our sample, 7.32% of individuals had abnormalities that were consistent with a viral etiology, including myocarditis and hepatitis. Internal parasites were observed in 53.66% of individuals and is consistent with what would be expected from a free-ranging primate population. This study represents the importance of baseline data for long-term monitoring of primate populations hunted for food. More broadly, this research begins to close a critical gap in zoonotic disease risk related to primate harvesting in Amazonia, while also demonstrating the benefits of partnering with Indigenous hunters and leveraging hunting practices in disease surveillance and primate population health assessment.

Sustainability and comanagement of subsistence hunting in an indigenous reserve in Guyana.

Although hunting is a key component of subsistence strategies of many Amazonians, it is also one of the greatest threats to wildlife. Because indigenous reserves comprise over 20% of Amazonia, effective conservation often requires that conservation professionals work closely with indigenous groups to manage resource use. We used hunter-generated harvesting data in spatially explicit biodemographic models to assess the sustainability of subsistence hunting of indigenous Waiwai in Guyana. We collected data through a hunter self-monitoring program, systematic follows of hunters, and semistructured interviews. We used these data to predict future densities of 2 indicator species, spider monkeys (Ateles paniscus) and bearded sakis (Chiropotes sagulatus), under different scenarios of human population expansion and changing hunting technology. We used encounter rates from transect surveys and hunter catch-per-unit effort (CPUE) to validate model predictions. Paca (Cuniculus paca) (198 /year), Currosaw (Crax alector) (168), and spider monkey (117) were the most frequently harvested species. Predicted densities of spider monkeys were statistically indistinguishable from empirically derived transect data (Kolmogorov-Smirnov D = 0.67, p = 0.759) and CPUE (D = 0.32, p = 1.000), demonstrating the robustness of model predictions. Ateles paniscus and C. sagulatus were predicted to be extirpated from <13% of the Waiwai reserve in 20 years, even under the most intensive hunting scenarios. Our results suggest Waiwai hunting is currently sustainable, primarily due to their low population density and use of bow and arrow. Continual monitoring is necessary, however, particularly if human population increases are accompanied by a switch to shotgun-only hunting. We suggest that hunter self-monitoring and biodemographic modeling can be used effectively in a comanagement approach in which indigenous parabiologists continuously provide hunting data that is then used to update model parameters and validate model predictions.

Mixed-species associations in cuxiús (genus Chiropotes).

Polyspecific or mixed-species associations, where two or more species come together to forage and travel as a unit, have been reported in many primate species. These associations appear to offer a number of benefits to the species involved including increased foraging efficiency and decreased risk of predation. While several researchers have suggested that cuxiús (genus Chiropotes) form mixed-species associations, previous studies have not identified the circumstances under which cuxiús form associations or whether they form associations more often than would be expected by chance. Here we present data on the formation of mixed-species associations by four species of cuxiús at eight different sites in Brazil, Suriname, and Guyana. We analyzed data from two of the study sites, (Biological Dynamics of Forest Fragments Project (BDFFP), Brazil and the Upper Essequibo Conservation Concession (UECC), Guyana, to assess whether associations occurred more than would be expected by chance encounters and identify the factors influencing their formation. Cuxiús showed a high degree of inter-site variation in the frequency of time spent in association (ranging from 2 to 26% of observation time) and duration of associations (mean duration from 22 min to 2.5 hr). Sapajus apella was the most common association partner at most sites. At BDFFP, cuxiús formed associations more frequently but not for longer duration than expected by chance. For much of the year at UECC, associations were not more frequent or longer than chance. However, during the dry season, cuxiús formed associations with S. apella significantly more often and for longer duration than predicted by chance. Cuxiús at UECC formed associations significantly more often when in smaller subgroups and when foraging for insects, and alarm called significantly less frequently during associations. We suggest cuxiús form mixed-species associations at some sites as an adaptive strategy to decrease predation risk and/or increase foraging efficiency.

Geographic comparison of plant genera used in frugivory among the pitheciids Cacajao, Callicebus, Chiropotes, and Pithecia.

Pitheciids are known for their frugivorous diets, but there has been no broad-scale comparison of fruit genera used by these primates that range across five geographic regions in South America. We compiled 31 fruit lists from data collected from 18 species (three Cacajao, six Callicebus, five Chiropotes, and four Pithecia) at 26 study sites in six countries. Together, these lists contained 455 plant genera from 96 families. We predicted that 1) closely related Chiropotes and Cacajao would demonstrate the greatest similarity in fruit lists; 2) pitheciids living in closer geographic proximity would have greater similarities in fruit lists; and 3) fruit genus richness would be lower in lists from forest fragments than continuous forests. Fruit genus richness was greatest for the composite Chiropotes list, even though Pithecia had the greatest overall sampling effort. We also found that the Callicebus composite fruit list had lower similarity scores in comparison with the composite food lists of the other three genera (both within and between geographic areas). Chiropotes and Pithecia showed strongest similarities in fruit lists, followed by sister taxa Chiropotes and Cacajao. Overall, pitheciids in closer proximity had more similarities in their fruit list, and this pattern was evident in the fruit lists for both Callicebus and Chiropotes. There was no difference in the number of fruit genera used by pitheciids in habitat fragments and continuous forest. Our findings demonstrate that pitheciids use a variety of fruit genera, but phylogenetic and geographic patterns in fruit use are not consistent across all pitheciid genera. This study represents the most extensive examination of pitheciid fruit consumption to date, but future research is needed to investigate the extent to which the trends in fruit genus richness noted here are attributable to habitat differences among study sites, differences in feeding ecology, or a combination of both.

Spatial foraging in free ranging bearded sakis: traveling salesmen or Lévy Walkers?

According to optimal foraging theory and most current models of primate socioecology, primate foraging involves a series of decisions concerning when is the most optimal time to leave a food patch, how to travel to the next patch in an efficient manner, and how to minimize the time and distance traveled to all patches throughout the course of the day. In this study, I assess how bearded sakis solve these challenges by presenting data on their patch use, distance minimization, and by comparing their movements with non-deterministic foraging patterns. The study group, composed of 38 ± 15 individuals, fed significantly longer in higher quality patches (quality defined by patch size and productivity) and in those that contained ripe fruit pulp. However, group size was not a significant predictor of patch occupancy. Bearded sakis traveled relatively directly between food patches, sometimes over distances > 300 m. In addition, they chose the optimal daily path among all patches visited on 9 of 17 occasions, and on average traveled only 21% more than the least distance route. Bearded saki step lengths were consistent with a Brownian rather than a Lévy Walk pattern while waiting times were consistent with a Lévy pattern. However, the distribution of their turning angles indicated a high degree of directional persistence between patches. These results suggest that bearded sakis exploit food patches that are randomly distributed spatially but heterogenous in patch quality. They appear to encode the locations of high quality food patches and minimize travel between them, despite opportunistically feeding from more abundant and randomly distributed, lower quality patches en route.

Gis analysis of patch use and group cohesiveness of bearded sakis (chiropotes sagulatus) in the upper essequibo conservation concession, Guyana.

This study examines how northern bearded sakis (Chiropotes sagulatus) in Guyana adjust group cohesiveness according to the distribution and quality of food patches. I introduce a GIS based method for quantifying food patch quality and how it relates to bearded saki group spread and group size. While the concept of food patch is central to most models of primate socioecology, defining what constitutes a patch has been notoriously problematic in primate studies. In addition, researchers have struggled to quantify group spread and group cohesiveness. Advances in spatial analysis software in the last decade now allow primate researchers to better quantify these variables. Group spread in bearded sakis was not significantly greater in lower quality patches and sakis were not more spread out during feeding than during other activities. However, the study group was significantly less spread out during social behavior. Bearded saki group size was significantly correlated with both monthly fruit abundance and patch quality. In fact, mean daily patch quality explained ∼40% of the variation in foraging party size. These results suggest that bearded sakis may rely on a highly fluid social structure to mitigate the effects of intragroup feeding competition while living in large groups. Sakis do not adjust group spread on a patch-by-patch basis but rather fission into smaller foraging parties when resources become scarce seasonally and patch quality is low. This study shows that GIS is a powerful tool for modeling the relationship between group cohesiveness and resource quality and distribution.

Feeding Ecology of northern bearded sakis (Chiropotes sagulatus) in Guyana.

Bearded sakis (genus Chiropotes) are among the most highly specialized primate seed predators. However, long-term studies of the genus in continuous forests, with a full community of sympatric primates, are rare. Here I present data on monthly variation in the diet of Chiropotes sagulatus from a long-term study in a continuous forest in Guyana. Bearded sakis had an extremely diverse diet, exploiting more than 175 species of plants. Consistent with their highly specialized dental morphology for seed eating, seeds made up 75% of the annual diet. Sakis exploited a wide variety of mechanically protected fruits and often exploited the same plant species for more than 3 months. They consumed a high percentage of seeds in all months and seed consumption was significantly correlated with fruit abundance. When fruit became scarcer, sakis consumed a higher percentage of non-seed food items, including insects, mature fruit, and flowers. Insects were especially important during the leanest months, making up almost 40% of feeding time. Bearded saki dietary diversity (in terms of plant species) showed little variability across months. These results confirm sakis to be highly specialized seed predators. Sakis preferentially consume seeds when they are available. However, when seeds become scarce, sakis become generalists, supplementing their diet with mature fruit, insects, and flowers. The ability of bearded sakis to consume a diversity of highly abundant plant species, fruit in several stages of maturity, and a variety of different types of resources buffers them from the detrimental effects of resource scarcity.

A mixed-methods approach to understanding domestic dog health and disease transmission risk in an indigenous reserve in Guyana, South America.

Domestic dogs (Canis lupus familiaris) can transmit a variety of pathogens due to their ubiquitousness in urban, rural and natural environments, and their close interactions with wildlife and humans. In this study, we used a mixed-methods approach to assess the role of domestic dogs as potential intermediaries of disease transmission from wildlife to humans among indigenous Waiwai in the Konashen Community Owned Conservation Area, Guyana. To address these objectives we 1) performed physical examinations and collected biological samples to assess Waiwai domestic dog health, and 2) administered questionnaires to characterize the role of dogs in the community and identify potential transmission pathways between wildlife, dogs, and humans. We observed ectoparasites on all dogs (n = 20), including: fleas (100%), ticks (15%), botflies (30%), and jigger flea lesions (Tunga penetrans) (80%). Ten percent of dogs were seropositive for Ehrlichia canis/ewingii, 10% were positive for Dirofilaria immitis, and one dog was seropositive for Leishmania infantum. All dogs (n = 20) were seronegative for: canine distemper virus, Brucella canis, Leptospira serovars, Trypanosoma cruzi, Anaplasma phagocytophilum/platys and Borrelia burgdorferi. Our questionnaire data revealed that the Waiwai remove ectoparasites from their dogs, clean up dog feces, and administer traditional and/or Western medicine to their dogs. White blood cell, strongyle-type ova, and eosinophil counts were lower in dogs that were not frequently used for hunting, dogs that did receive traditional and/or western medicine, and dogs that were frequently kept in elevated dog houses, although differences were not statistically significant. While our results suggest that the Waiwai have developed cultural practices that may promote dog health and/or prevent zoonotic disease transmission, more research is necessary to determine the efficacy of these practices. Our study provides important data on the health of dogs and the potential for disease transmission to humans in a zoonotic hotspot.

Roadside monkeys: anthropogenic effects on moor macaque (Macaca maura) ranging behavior in Bantimurung Bulusaraung National Park, Sulawesi, Indonesia.

A growing body of research focuses on how anthropogenic factors affect the behavior and ecology of primates and their ecosystems. Infrastructural development, such as roads, is an increasingly pervasive anthropogenic impact that destroys primate habitat, affects the distribution and dispersal of primates, and facilitates human-primate interactions. At our field site in Bantimurung-Bulusaraung National Park, Sulawesi, Indonesia, a major road bisects the habitat of the endangered moor macaque (Macaca maura). Beginning in 2015, we observed a behavioral shift by our main study group: they began spending more time along the road foraging in trash pits and waiting for provisions from vehicles. Our objective in this study was to examine how access to anthropogenic foods has affected the group's ranging behavior by comparing ranging data collected before (2010-2011) and after the shift (2016-2017). In contrast to what we expected, home ranges were significantly larger and daily travel distance was significantly longer after the shift compared to before. As predicted, mean distance to the road decreased after the shift. These results likely reflect the irregular and spatially dispersed nature of provisioning at this site. The macaques appear to be attracted to the road because it presents opportunities to obtain palatable and energy-dense foods. Our results indicate that moor macaques are able to flexibly adjust their ranging behavior in response to anthropogenic impacts. However, given the risks of being in proximity to roads and humans, management of this emerging human-macaque interface is needed.

An Ethnographic Approach to Characterizing Potential Pathways of Zoonotic Disease Transmission from Wild Meat in Guyana.

The hunting, butchery, and consumption of wild meat is an important interface for zoonotic disease transmission. Despite this, few researchers have used ethnography to understand the sociocultural factors that may increase zoonotic disease transmission from hunting, particularly in Amazonia. Here, we use ethnographic methods consisting of structured, semi-structured and unstructured interviews, and participant observation to address questions pertaining to wild meat consumption, pathways of zoonotic disease transmission, food security, and the cultural identity of indigenous Waiwai in the Konashen Community Owned Conservation Area, Guyana. Our data revealed that the majority of Waiwai eat wild meat two to three times/week and 60% of respondents reported butchery-related injuries. However, semi-structured and unstructured interviews, and participant observation data indicate that the Waiwai do not perceive most cuts from butchery as injuries, despite being a potential route of pathogen exposure. Additionally, participant observation revealed that hunting is integral to Waiwai identity and the Waiwai exhibit a cultural aversion to domestic meats. These findings provide valuable insights into the interplay of hunting and wild meat consumption and disease in Amazonia and demonstrate how an ethnographic approach provides the contextual data necessary for identifying potential pathways of zoonotic transmission from wild meat.