Deforestation and Bovine Rabies Outbreaks in Costa Rica, 1985-2020.

In Latin America, rabies virus has persisted in a cycle between Desmodus rotundus vampire bats and cattle, potentially enhanced by deforestation. We modeled bovine rabies virus outbreaks in Costa Rica relative to land-use indicators and found spatial-temporal relationships among rabies virus outbreaks with deforestation as a predictor.

Potentially Zoonotic Enteric Infections in Gorillas and Chimpanzees, Cameroon and Tanzania.

Despite zoonotic potential, data are lacking on enteric infection diversity in wild apes. We employed a novel molecular diagnostic platform to detect enteric infections in wild chimpanzees and gorillas. Prevalent Cryptosporidium parvum, adenovirus, and diarrheagenic Escherichia coli across divergent sites and species demonstrates potential widespread circulation among apes in Africa.

Host-pathogen interactions under pressure: A review and meta-analysis of stress-mediated effects on disease dynamics.

Human activities have increased the intensity and frequency of natural stressors and created novel stressors, altering host-pathogen interactions and changing the risk of emerging infectious diseases. Despite the ubiquity of such anthropogenic impacts, predicting the directionality of outcomes has proven challenging. Here, we conduct a review and meta-analysis to determine the primary mechanisms through which stressors affect host-pathogen interactions and to evaluate the impacts stress has on host fitness (survival and fecundity) and pathogen infectivity (prevalence and intensity). We assessed 891 effect sizes from 71 host species (representing seven taxonomic groups) and 78 parasite taxa from 98 studies. We found that infected and uninfected hosts had similar sensitivity to stressors and that responses varied according to stressor type. Specifically, limited resources compromised host fecundity and decreased pathogen intensity, while abiotic environmental stressors (e.g., temperature and salinity) decreased host survivorship and increased pathogen intensity, and pollution increased mortality but decreased pathogen prevalence. We then used our meta-analysis results to develop susceptible-infected theoretical models to illustrate scenarios where infection rates are expected to increase or decrease in response to resource limitations or environmental stress gradients. Our results carry implications for conservation and disease emergence and reveal areas for future work.

Genetic Diversity of Bartonella spp. in Cave-Dwelling Bats and Bat Flies, Costa Rica, 2018.

To determine Bartonella spp. dynamics, we sampled bats and bat flies across 15 roosts in Costa Rica. PCR indicated prevalence of 10.7% in bats and 29.0% in ectoparasite pools. Phylogenetic analysis of 8 sequences from bats and 5 from bat fly pools revealed 11 distinct genetic variants, including 2 potentially new genotypes.

Molecular characterization of Giardia duodenalis and evidence for cross-species transmission in Northern Argentina.

Anthropogenic activities, such as human population expansion and land-use change, create ecological overlap between humans, domesticated animals, and wildlife and can exacerbate the zoonotic transmission of parasites. To improve our understanding of this dynamic, we employed multi-locus genotyping to conduct a cross-sectional study of the potential for zoonotic transmission of the protozoan parasite Giardia duodenalis among humans, household associated livestock and dogs, and black and gold howler monkeys (Alouatta caraya) in the Corrientes Province of Argentina. We found Giardia prevalence to be highest in howler monkeys (90.3% (47/52)), followed by humans (61.1% (22/36)), dogs (44.4% (16/36)), and cattle (41.9% (18/43)). We further established that howler monkeys exclusively harbored strains of assemblage B (100%) while humans were infected with either assemblage A (13.3%) or B (80%) or A and B (6.7%), and cattle and dogs were infected with either assemblage A (cattle, 94.1%; dogs, 80%)), A and C (10%), or their host-adapted assemblage (cattle, 5.9%; dogs, 10%). Our finding of G. duodenalis in both humans and domesticated animals (assemblage A) and humans and wild primates (assemblage B) suggests that cross-species transmission of multiple assemblages of G. duodenalis may occur in rural complexes such as northern Argentina where people, domesticated animals, and wildlife overlap. We further highlight the need to investigate the implications of these results for human health, the economics of livestock production, and wildlife conservation in this and similar systems.

The Gombe Ecosystem Health Project: 16 years of program evolution and lessons learned.

Infectious disease outbreaks pose a significant threat to the conservation of chimpanzees (Pan troglodytes) and all threatened nonhuman primates. Characterizing and mitigating these threats to support the sustainability and welfare of wild populations is of the highest priority. In an attempt to understand and mitigate the risk of disease for the chimpanzees of Gombe National Park, Tanzania, we initiated a long-term health-monitoring program in 2004. While the initial focus was to expand the ongoing behavioral research on chimpanzees to include standardized data on clinical signs of health, it soon became evident that the scope of the project would ideally include diagnostic surveillance of pathogens for all primates (including people) and domestic animals, both within and surrounding the National Park. Integration of these data, along with in-depth post-mortem examinations, have allowed us to establish baseline health indicators to inform outbreak response. Here, we describe the development and expansion of the Gombe Ecosystem Health project, review major findings from the research and summarize the challenges and lessons learned over the past 16 years. We also highlight future directions and present the opportunities and challenges that remain when implementing studies of ecosystem health in a complex, multispecies environment.

The relationship between pinworm (Trypanoxyuris) infection and gut bacteria in wild black howler monkeys (Alouatta pigra).

Gut bacteria may coexist with other groups of organisms, such as nematode parasites, that inhabit the gastrointestinal tract of primates; however, the possible effects of endoparasites on bacterial communities are frequently overlooked. Here we explored whether infection with Trypanoxyuris, an oxyurid gastrointestinal parasite, is associated with changes in the gut bacterial community of wild black howler monkeys (Alouatta pigra), by comparing gut bacterial communities of consistently infected individuals and individuals that never tested positive for Trypanoxyuris throughout different months across the year. We additionally controlled for other sources of variation reported to influence the primate microbiome including individual identity, social group, and seasonality. Trypanoxyuris infection was not related to differences in gut bacterial alpha diversity, but was weakly associated with differences in gut bacterial community structure. In contrast, among the covariates considered, both individual identity and social group were more strongly associated with variation in the howler gut bacterial community. Our results suggest that gastrointestinal parasites may be associated, to some extent, with shifts in the gut bacterial communities hosted by free-ranging primates, although a causal link still needs to be established. Further studies of wild primate hosts infected with parasite species with different pathogenicity are needed to better elucidate health-related consequences from the parasite-microbiome interplay.

Gregariousness is associated with parasite species richness in a community of wild chimpanzees.

Increased risk of pathogen transmission through proximity and contact is a well-documented cost of sociality. Affiliative social contact, however, is an integral part of primate group life and can benefit health. Despite its importance to the evolution and maintenance of sociality, the tradeoff between costs and benefits of social contact for group-living primate species remains poorly understood. To improve our understanding of this interplay, we used social network analysis to investigate whether contact via association in the same space and/or physical contact measured through grooming were associated with helminth parasite species richness in a community of wild chimpanzees (Pan troglodytes schweinfurthii). We identified parasite taxa in 381 fecal samples from 36 individuals from the Kasekela community of chimpanzees in Gombe National Park, Tanzania, from November 1, 2006 - October 31, 2012. Over the study period, eight environmentally transmitted helminth taxa were identified. We quantified three network metrics for association and grooming contact, including degree strength, betweenness, and closeness. Our findings suggest that more gregarious individuals - those who spent more time with more individuals in the same space - had higher parasite richness, while the connections in the grooming network were not related to parasite richness. The expected parasite richness in individuals increased by 1.13 taxa (CI: 1.04, 1.22; p = 0.02) per one standard deviation increase in degree strength of association contact. The results of this study add to the understanding of the role that different types of social contact plays in the parasite richness of group-living social primates.

Integrating Health Systems and Science to Respond to COVID-19 in a Model District of Rural Madagascar.

There are many outstanding questions about how to control the global COVID-19 pandemic. The information void has been especially stark in the World Health Organization Africa Region, which has low per capita reported cases, low testing rates, low access to therapeutic drugs, and has the longest wait for vaccines. As with all disease, the central challenge in responding to COVID-19 is that it requires integrating complex health systems that incorporate prevention, testing, front line health care, and reliable data to inform policies and their implementation within a relevant timeframe. It requires that the population can rely on the health system, and decision-makers can rely on the data. To understand the process and challenges of such an integrated response in an under-resourced rural African setting, we present the COVID-19 strategy in Ifanadiana District, where a partnership between Malagasy Ministry of Public Health (MoPH) and non-governmental organizations integrates prevention, diagnosis, surveillance, and treatment, in the context of a model health system. These efforts touch every level of the health system in the district-community, primary care centers, hospital-including the establishment of the only RT-PCR lab for SARS-CoV-2 testing outside of the capital. Starting in March of 2021, a second wave of COVID-19 occurred in Madagascar, but there remain fewer cases in Ifanadiana than for many other diseases (e.g., malaria). At the Ifanadiana District Hospital, there have been two deaths that are officially attributed to COVID-19. Here, we describe the main components and challenges of this integrated response, the broad epidemiological contours of the epidemic, and how complex data sources can be developed to address many questions of COVID-19 science. Because of data limitations, it still remains unclear how this epidemic will affect rural areas of Madagascar and other developing countries where health system utilization is relatively low and there is limited capacity to diagnose and treat COVID-19 patients. Widespread population based seroprevalence studies are being implemented in Ifanadiana to inform the COVID-19 response strategy as health systems must simultaneously manage perennial and endemic disease threats.

Correction: Altitude and human disturbance are associated with helminth diversity in an endangered primate, Procolobus gordonorum.

[This corrects the article DOI: 10.1371/journal.pone.0225142.].

Antimicrobial Resistance Creates Threat to Chimpanzee Health and Conservation in the Wild.

Infectious disease is recognized as the greatest threat to the endangered chimpanzees made famous by the groundbreaking work of Dr. Jane Goodall at Gombe National Park (GNP), Tanzania. The permeable boundary of this small protected area allows for regular wildlife-human and wildlife-domestic animal overlap, which may facilitate cross-species transmission of pathogens and antimicrobial resistance. Few studies have examined the prevalence of antimicrobial resistance in wild ape populations. We used molecular techniques to investigate the presence of genes conferring resistance to sulfonamides (often used to treat diarrheal illness in human settings in this region) and tetracycline (used in the past-though much less so now) in fecal specimens from humans, domestic animals, chimpanzees, and baboons in and around GNP. We also tested stream water used by these groups. Sulfonamide resistance was common in humans (74%), non-human primates (43%), and domestic animals (17%). Tetracycline resistance was less common in all groups: humans (14%), non-human primates (3%), and domestic animals (6%). Sul resistance genes were detected from 4/22 (18%) of streams sampled. Differences in sul gene frequencies did not vary by location in humans nor in chimpanzees.

Social contact behaviors are associated with infection status for Trichuris sp. in wild vervet monkeys (Chlorocebus pygerythrus).

Social grooming in the animal kingdom is common and serves several functions, from removing ectoparasites to maintaining social bonds between conspecifics. We examined whether time spent grooming with others in a highly social mammal species was associated with infection status for gastrointestinal parasites. Of six parasites detected, one (Trichuris sp.) was associated with social grooming behaviors, but more specifically with direct physical contact with others. Individuals infected with Trichuris sp. spent significantly less time grooming conspecifics than those not infected, and time in direct contact with others was the major predictor of infection status. One model correctly predicted infection status for Trichuris sp. with a reliability of 95.17% overall when the variables used were time spent in direct contact and time spent grooming others. This decrease in time spent grooming and interacting with others is likely a sickness behavior displayed by individuals with less energy or motivation for non-essential behaviors. This study emphasizes the possible links between host behavior and parasitic infections and highlights the need for an understanding of a study population's parasitic infections when attempting to interpret animal behavior.

COVID-Clarity demands unification of health and environmental policy.

Spillover of novel pathogens from wildlife to people, such as the virus responsible for the COVID-19 pandemic, is increasing and this trend is most strongly associated with tropical deforestation driven by agricultural expansion. This same process is eroding natural capital, reducing forest-associated health co-benefits, and accelerating climate change. Protecting and promoting tropical forests is one of the most immediate steps we can take to simultaneously mitigate climate change while reducing the risk of future pandemics; however, success in this undertaking will require greater connectivity of policy initiatives from local to global, as well as unification of health and environmental policy.

Effects of anthropogenic habitat disturbance and Giardia duodenalis infection on a sentinel species' gut bacteria.

Habitat disturbance, a common consequence of anthropogenic land use practices, creates human-animal interfaces where humans, wildlife, and domestic species can interact. These altered habitats can influence host-microbe dynamics, leading to potential downstream effects on host physiology and health. Here, we explored the effect of ecological overlap with humans and domestic species and infection with the protozoan parasite Giardia duodenalis on the bacteria of black and gold howler monkeys (Alouatta caraya), a key sentinel species, in northeastern Argentina. Fecal samples were screened for Giardia duodenalis infection using a nested PCR reaction, and the gut bacterial community was characterized using 16S rRNA gene amplicon sequencing. Habitat type was correlated with variation in A. caraya gut bacterial community composition but did not affect gut bacterial diversity. Giardia presence did not have a universal effect on A. caraya gut bacteria across habitats, perhaps due to the high infection prevalence across all habitats. However, some bacterial taxa were found to vary with Giardia infection. While A. caraya's behavioral plasticity and dietary flexibility allow them to exploit a range of habitat conditions, habitats are generally becoming more anthropogenically disturbed and, thus, less hospitable. Alterations in gut bacterial community dynamics are one possible indicator of negative health outcomes for A. caraya in these environments, since changes in host-microbe relationships due to stressors from habitat disturbance may lead to negative repercussions for host health. These dynamics are likely relevant for understanding organism responses to environmental change in other mammals.

Research and Conservation in the Greater Gombe Ecosystem: Challenges and Opportunities.

The study of chimpanzees in Gombe National Park, Tanzania, started by Jane Goodall in 1960, provided pioneering accounts of chimpanzee behavior and ecology. With funding from multiple sources, including the Jane Goodall Institute (JGI) and grants from private foundations and federal programs, the project has continued for sixty years, providing a wealth of information about our evolutionary cousins. These chimpanzees face two main challenges to their survival: infectious disease - including simian immunodeficiency virus (SIVcpz), which can cause Acquired Immune Deficiency Syndrome (AIDS) in chimpanzees - and the deforestation of land outside the park. A health monitoring program has increased understanding of the pathogens affecting chimpanzees and has promoted measures to characterize and reduce disease risk. Deforestation reduces connections between Gombe and other chimpanzee populations, which can cause loss of genetic diversity. To promote habitat restoration, JGI facilitated participatory village land use planning, in which communities voluntarily allocated land to a network of Village Land Forest Reserves. Expected benefits to people include stabilizing watersheds, improving water supplies, and ensuring a supply of forest resources. Surveys and genetic analyses confirm that chimpanzees persist on village lands and remain connected to the Gombe population. Many challenges remain, but the regeneration of natural forest on previously degraded lands provides hope that conservation solutions can be found that benefit both people and wildlife. Conservation work in the Greater Gombe Ecosystem has helped promote broader efforts to plan and work for conservation elsewhere in Tanzania and across Africa.

Three new Prototapirella species, Opisthotrichum janus, and Troglocorys cava add to Entodiniomorphida (Ciliophora, Trichostomatia) diversity in mountain gorillas in Rwanda.

Recently, a high number of Entodiniomorphida species was discovered in Virunga mountain gorillas (Gorilla beringei beringei) in Rwanda compared to other primates. Thirteen species of five genera (Troglocorys, Gorilloflasca, Prototapirella, Troglodytella, and Opisthotrichum) were identified with 10 species in Gorilloflasca, Prototapirella, and Troglodytella being host-specific, to our current knowledge. The remaining three species have been described for other herbivorous mammals; Prototapirella gorillae for western lowland gorillas; Troglocorys cava for western lowland gorillas, chimpanzees, and guinea baboons; Opisthotrichum janus in the family Ophryoscolecidae is regarded as specific to African antelopes. Here, we show the first indication that wild herbivorous hindgut fermenting mammals might have rumen ophryoscolecids in the intestine sympatric with their native intestinal ciliates. We also describe three new Prototapirella species, P. sabyinyo, P. sulcata, and P. curiosa. The somatic ciliary zones of the three new species are atypical of Prototapirella while their buccal infraciliature is not different from that of other Prototapirella species.

Comprehensive Knowledge of Reservoir Hosts is Key to Mitigating Future Pandemics.

Coronavirus disease 2019 (COVID-19) and other epidemics (such as severe acute respiratory syndrome [SARS], Ebola, and H1N1) are stark reminders that knowledge of animal behavior and ecosystem health are key to controlling the spread of zoonotic diseases early in their onset. However, we have very limited information about the set of behavioral and ecological factors that promote viral spillover and the effects that has on ecosystem health and disease transmission. Thus, expanding our current knowledge of reservoir hosts and pandemics represents an urgent and critical tool in ecological epidemiology. We also propose to create an integrative database that ranks animal species in terms of their likelihood as hosts for specific infectious diseases. We call for a global and cooperative effort of field and laboratory scientists to create, maintain, and update this information in order to reduce the severity of future pandemics.

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.