Great ape health watch: Enhancing surveillance for emerging infectious diseases in great apes.

Infectious diseases have the potential to extirpate populations of great apes. As the interface between humans and great apes expands, zoonoses pose an increasingly severe threat to already endangered great ape populations. Despite recognition of the threat posed by human pathogens to great apes, health monitoring is only conducted for a small fraction of the world's wild great apes (and mostly those that are habituated) meaning that outbreaks of disease often go unrecognized and therefore unmitigated. This lack of surveillance (even in sites where capacity to conduct surveillance is present) is the most significant limiting factor in our ability to quickly detect and respond to emerging infectious diseases in great apes when they first appear. Accordingly, we must create a surveillance system that links disease outbreaks in humans and great apes in time and space, and enables veterinarians, clinicians, conservation managers, national decision makers, and the global health community to respond quickly to these events. Here, we review existing great ape health surveillance programs in African range habitats to identify successes, gaps, and challenges. We use these findings to argue that standardization of surveillance across sites and geographic scales, that monitors primate health in real-time and generates early warnings of disease outbreaks, is an efficient, low-cost step to conserve great ape populations. Such a surveillance program, which we call "Great Ape Health Watch" would lead to long-term improvements in outbreak preparedness, prevention, detection, and response, while generating valuable data for epidemiological research and sustainable conservation planning. Standardized monitoring of great apes would also make it easier to integrate with human surveillance activities. This approach would empower local stakeholders to link wildlife and human health, allowing for near real-time, bidirectional surveillance at the great ape-human interface.

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.

Entamoeba histolytica infection in humans, chimpanzees and baboons in the Greater Gombe Ecosystem, Tanzania.

Entamoeba histolytica is an enteric parasite that infects approximately 50 million people worldwide. Although E. histolytica is a zoonotic parasite that has the potential to infect nonhuman primates, such transmission is poorly understood. Consequently, this study examined whether E. histolytica is present among humans, chimpanzees and baboons living in the Greater Gombe Ecosystem (GGE), Tanzania. The primary aims were to determine patterns of E. histolytica infection in a system with human-nonhuman primate overlap and to test associations between infection status and potential risk factors of disease. Entamoeba spp. occurred in 60.3% of human, 65.6% of chimpanzee and 88.6% of baboon samples. Entamoeba histolytica occurred in 12.1% of human, 34.1% of chimpanzee and 10.9% of baboon samples. Human E. histolytica infection was associated with gastrointestinal symptoms. This was the first study to confirm the presence of E. histolytica in the GGE. The high sample prevalence of E. histolytica in three sympatric primates suggests that zoonotic transmission is possible and stresses the need for further phylogenetic studies. Interventions targeting better sanitation and hygiene practices for humans living in the GGE can help prevent E. histolytica infection in humans, while also protecting the endangered chimpanzees and other primates in this region.

Health of wild fish exposed to contaminants of emerging concern in freshwater ecosystems utilized by a Minnesota Tribal community.

Fish serve as indicators of exposure to contaminants of emerging concern (CECs)-chemicals such as pharmaceuticals, hormones, and personal care products-which are often designed to impact vertebrates. To investigate fish health and CECs in situ, we evaluated the health of wild fish exposed to CECs in waterbodies across northeastern Minnesota with varying anthropogenic pressures and CEC exposures: waterbodies with no human development along their shorelines, those with development, and those directly receiving treated wastewater effluent. Then, we compared three approaches to evaluate the health of fish exposed to CECs in their natural environment: a refined fish health assessment index, a histopathological index, and high-throughput (ToxCast) in vitro assays. Lastly, we mapped adverse outcome pathways (AOPs) associated with identified ToxCast assays to determine potential impacts across levels of biological organization within the aquatic system. These approaches were applied to subsistence fish collected from the Grand Portage Indian Reservation and 1854 Ceded Territory in 2017 and 2019. Overall, 24 CECs were detected in fish tissues, with all but one of the sites having at least one detection. The combined implementation of these tools revealed that subsistence fish exposed to CECs had histological and macroscopic tissue and organ abnormalities, although a direct causal link could not be established. The health of fish in undeveloped sites was as poor, or sometimes poorer, than fish in developed and wastewater effluent-impacted sites based on gross and histologic tissue lesions. Adverse outcome pathways revealed potential hazardous pathways of individual CECs to fish. A better understanding of how the health of wild fish harvested for consumption is affected by CECs may help prioritize risk management research efforts and can ultimately be used to guide fishery management and public health decisions. Integr Environ Assess Manag 2024;20:846-863. © 2023 The Authors. Integrated Environmental Assessment and Management published by Wiley Periodicals LLC on behalf of Society of Environmental Toxicology & Chemistry (SETAC).

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.

A chemical prioritization process: Applications to contaminants of emerging concern in freshwater ecosystems (Phase I).

Contaminants of emerging concern (CECs), such as pharmaceuticals, personal care products, and hormones, are frequently found in aquatic ecosystems around the world. Information on sublethal effects from exposure to commonly detected concentrations of CECs is lacking and the limited availability of toxicity data makes it difficult to interpret the biological significance of occurrence data. However, the ability to evaluate the effects of CECs on aquatic ecosystems is growing in importance, as detection frequency increases. The goal of this study was to prioritize the chemical hazards of 117 CECs detected in subsistence species and freshwater ecosystems on the Grand Portage Indian Reservation and adjacent 1854 Ceded Territory in Minnesota, USA. To prioritize CECs for management actions, we adapted Minnesota Pollution Control Agency's Aquatic Toxicity Profiles framework, a tool for the rapid assessment of contaminants to cause adverse effects on aquatic life by incorporating chemical-specific information. This study aimed to 1) perform a rapid-screening assessment and prioritization of detected CECs based on their potential environmental hazard; 2) identify waterbodies in the study region that contain high priority CECs; and 3) inform future monitoring, assessment, and potential remediation in the study region. In water samples alone, 50 CECs were deemed high priority. Twenty-one CECs were high priority among sediment samples and seven CECs were high priority in fish samples. Azithromycin, DEET, diphenhydramine, fluoxetine, miconazole, and verapamil were high priority in all three media. Due to the presence of high priority CECs throughout the study region, we recommend future monitoring of particular CECs based on the prioritization method used here. We present an application of a chemical hazard prioritization process and identify areas where the framework may be adapted to meet the objectives of other management-related assessments.

Anthropogenic factors associated with contaminants of emerging concern detected in inland Minnesota lakes (Phase II).

Contaminants of emerging concern (CECs) include a variety of pharmaceuticals, personal care products, and hormones commonly detected in surface waters. Human activities, such as wastewater treatment and discharge, contribute to the distribution of CECs in water, but other sources and pathways are less frequently examined. This study aimed to identify anthropogenic activities and environmental characteristics associated with the presence of CECs, previously determined to be of high priority for further research and mitigation, in rural inland lakes in northeastern Minnesota, United States. The setting for this study consisted of 21 lakes located within both the Grand Portage Indian Reservation and the 1854 Ceded Territory, where subsistence hunting and fishing are important to the cultural heritage of the indigenous community. We used data pertaining to numbers of buildings, healthcare facilities, wastewater treatment plants, impervious surfaces, and wetlands within defined areas surrounding the lakes as potential predictors of the detection of high priority CECs in water, sediment, and fish. Separate models were run for each contaminant detected in each sample media. We used least absolute shrinkage and selection operator (LASSO) models to account for both predictor selection and parameter estimation for CEC detection. Across contaminants and sample media, the percentage of impervious surface was consistently positively associated with CEC detection. Number of buildings in the surrounding area was often negatively associated with CEC detection, though nonsignificant. Surrounding population, presence of wastewater treatment facilities, and percentage of wetlands in surrounding areas were positively, but inconsistently, associated with CECs, while catchment area and healthcare centers were generally not associated. The results of this study highlight human activities and environmental characteristics associated with CEC presence in a rural area, informing future work regarding specific sources and transport pathways. We also demonstrate the utility of LASSO modeling in the identification of these important relationships.

Occurrence of contaminants of emerging concern in aquatic ecosystems utilized by Minnesota tribal communities.

Pharmaceuticals, personal care products, hormones, and other chemicals lacking water quality standards are frequently found in surface water. While evidence is growing that these contaminants of emerging concern (CECs) - those previously unknown, unrecognized, or unregulated - can affect the behavior and reproduction of fish and wildlife, little is known about the distribution of these chemicals in rural, tribal areas. Therefore, we surveyed the presence of CECs in water, sediment, and subsistence fish species across various waterbodies, categorized as undeveloped (i.e., no human development along shorelines), developed (i.e., human development along shorelines), and wastewater effluent-impacted (i.e., contain effluence from wastewater treatment plants), within the Grand Portage Indian Reservation and 1854 Ceded Territory in northeastern Minnesota, U.S.A. Overall, in 28 sites across three years (2016-2018), 117 of the 158 compounds tested were detected in at least one form of medium (i.e., water, sediment, or fish). CECs were detected most frequently at wastewater effluent-impacted sites, with up to 83 chemicals detected in one such lake, while as many as 17 were detected in an undeveloped lake. Although there was no statistically significant difference between the number of CECs present in developed versus undeveloped lakes, a range of 3-17 CECs were detected across these locations. Twenty-two CECs were detected in developed and undeveloped sites that were not detected in wastewater effluent-impacted sites. The detection of CECs in remote, undeveloped locations, where subsistence fish are harvested, raises scientific questions about the safety and security of subsistence foods for indigenous communities. Further investigation is warranted so that science-based solutions to reduce chemical risks to aquatic life and people can be developed locally and be informative for indigenous communities elsewhere.