Human behaviors driving disease emergence.

Interactions between humans, animals, and the environment facilitate zoonotic spillover-the transmission of pathogens from animals to humans. Narratives that cast modern humans as exogenous and disruptive forces that encroach upon "natural" disease systems limit our understanding of human drivers of disease. This review leverages theory from evolutionary anthropology that situates humans as functional components of disease ecologies, to argue that human adaptive strategies to resource acquisition shape predictable patterns of high-risk human-animal interactions, (2) humans construct ecological processes that facilitate spillover, and (3) contemporary patterns of epidemiological risk are emergent properties of interactions between human foraging ecology and niche construction. In turn, disease ecology serves as an important vehicle to link what some cast as opposing bodies of theory in human ecology. Disease control measures should consider human drivers of disease as rational, adaptive, and dynamic and capitalize on our capacity to influence ecological processes to mitigate risk.

Child and adolescent foraging: New directions in evolutionary research.

Young children and adolescents in subsistence societies forage for a wide range of resources. They often target child-specific foods, they can be very successful foragers, and they share their produce widely within and outside of their nuclear family. At the same time, while foraging, they face risky situations and are exposed to diseases that can influence their immune development. However, children's foraging has largely been explained in light of their future (adult) behavior. Here, we reinterpret findings from human behavioral ecology, evolutionary medicine and cultural evolution to center foraging children's contributions to life history evolution, community resilience and immune development. We highlight the need to foreground immediate alongside delayed benefits and costs of foraging, including inclusive fitness benefits, when discussing children's food production from an evolutionary perspective. We conclude by recommending that researchers carefully consider children's social and ecological context, develop cross-cultural perspectives, and incorporate children's foraging into Indigenous sovereignty discourse.

Changes in physiological stress and behaviour in semi-free-ranging red-capped mangabeys (Cercocebus torquatus) following antiparasitic treatment.

Parasites are ubiquitous in wildlife populations, but physiological and behavioural responses of hosts to infection are difficult to measure. We experimentally treated semi-free-ranging red-capped mangabeys (Cercocebus torquatus) in Nigeria with antiparasitic drugs and examined subsequent changes in glucocorticoid production and individual behaviour. Because both parasites and stress impact energy balance and health, we measured (i) behavioural time re-allocation via activity budgets, (ii) social relationships (e.g. social connectivity and dominance hierarchy stability) and (iii) body condition. We collected triplicate faecal samples (n = 441) from 49 individuals prior to and following treatment. Cortisol levels fluctuated in parallel with parasite abundance. Elevations in cortisol, but not parasitism, were related to reduced body condition. Behaviour also shifted according to infection status, with uninfected individuals spending more time foraging and less time resting and vigilant compared with when they were infected. Time spent feeding, travelling or socializing did not differ between pre- and post-treatment time periods. Group cohesion, but not dominance stability, changed following treatment, suggesting parasite-induced social avoidance. Together, these findings show a coordinated response to infection that promotes host tolerance through stress and energy conservation, reduces transmission risk and increases protection when infected hosts are vulnerable.

VESPA: an optimized protocol for accurate metabarcoding-based characterization of vertebrate eukaryotic endosymbiont and parasite assemblages.

Protocols for characterizing taxonomic assemblages by deep sequencing of short DNA barcode regions (metabarcoding) have revolutionized our understanding of microbial communities and are standardized for bacteria, archaea, and fungi. Unfortunately, comparable methods for host-associated eukaryotes have lagged due to technical challenges. Despite 54 published studies, issues remain with primer complementarity, off-target amplification, and lack of external validation. Here, we present VESPA (Vertebrate Eukaryotic endoSymbiont and Parasite Analysis) primers and optimized metabarcoding protocol for host-associated eukaryotic community analysis. Using in silico prediction, panel PCR, engineered mock community standards, and clinical samples, we demonstrate VESPA to be more effective at resolving host-associated eukaryotic assemblages than previously published methods and to minimize off-target amplification. When applied to human and non-human primate samples, VESPA enables reconstruction of host-associated eukaryotic endosymbiont communities more accurately and at finer taxonomic resolution than microscopy. VESPA has the potential to advance basic and translational science on vertebrate eukaryotic endosymbiont communities, similar to achievements made for bacterial, archaeal, and fungal microbiomes.

A systematic mapping review of links between handling wild meat and zoonotic diseases.

1.Hunting, trade, and consumption of wildlife present a serious threat to global public health as it places humans in close contact with zoonotic pathogens.2.We systematically mapped the literature on wild meat handling and zoonotic disease transmission (1996-2022) using the online database Web of Science and Google search engine and identified 6229 articles out of which 253 were finally selected for use in our mapping review; 51 of these provided specific information regarding transmission risks.3.The reviewed studies reported 43 zoonotic pathogens (17 bacteria, 15 viruses, and 11 parasites) that could pose a potential risk to human health.4.Sixteen hygienic and sanitary behaviours were described in the reviewed studies. Disease surveillance was the most frequent. Most of the surveillance studies were carried out in Europe and were less common in the tropics.5.To inform policy and practical actions effectively, it is imperative to broaden our understanding of how various mitigation behaviours can be employed to minimize the risk of transmission.

Typical intracranial myiasis in Nigerian red river hogs (Potamochoerus porcus) caused by an unknown bot fly (Diptera: Oestridae).

We report an unknown taxon of bot fly (Diptera: Oestridae: Oestrinae) in red river hogs (Potamochoerus porcus Linnaeus, 1758) in Cross River State, Nigeria. From direct observation and interviews with local hunters, we document that, remarkably, the parasite typically occurs within the intracranial supra-meningeal space - i.e., between the inner wall of the skull and the brain - but without causing visible inflammation or clinical signs. The parasite is most similar (up to 87.9%) to Rhinoestrus usbekistanicus based on cytochrome oxidase subunit 1 DNA sequencing but is sufficiently divergent phylogenetically to represent a new or previously un-sequenced taxon. Morphologically, the parasite shares some, but not all, features with R. nivarleti. Local cultural belief systems attribute aspects of red river hog behavior (e.g. intelligence, elusiveness) to the parasite, suggesting a prolonged presence in the red river hog population. The parasite's unusual anatomic location may be aberrant, or it may be a protective adaptation to life in red river hogs, which forage vigorously with their snouts.

Zootherapy as a potential pathway for zoonotic spillover: a mixed-methods study of the use of animal products in medicinal and cultural practices in Nigeria.

BACKGROUND: Understanding how and why people interact with animals is important for the prevention and control of zoonoses. To date, studies have primarily focused on the most visible forms of human-animal contact (e.g., hunting and consumption), thereby blinding One Health researchers and practitioners to the broader range of human-animal interactions that can serve as cryptic sources of zoonotic diseases. Zootherapy, the use of animal products for traditional medicine and cultural practices, is widespread and can generate opportunities for human exposure to zoonoses. Existing research examining zootherapies omits details necessary to adequately assess potential zoonotic risks. METHODS: We used a mixed-methods approach, combining quantitative and qualitative data from questionnaires, key informant interviews, and field notes to examine the use of zootherapy in nine villages engaged in wildlife hunting, consumption, and trade in Cross River State, Nigeria. We analyzed medicinal and cultural practices involving animals from a zoonotic disease perspective, by including details of animal use that may generate pathways for zoonotic transmission. We also examined the sociodemographic, cultural, and environmental contexts of zootherapeutic practices that can further shape the nature and frequency of human-animal interactions. RESULTS: Within our study population, people reported using 44 different animal species for zootherapeutic practices, including taxonomic groups considered to be "high risk" for zoonoses and threatened with extinction. Variation in use of animal parts, preparation norms, and administration practices generated a highly diverse set of zootherapeutic practices (n = 292) and potential zoonotic exposure risks. Use of zootherapy was patterned by demographic and environmental contexts, with zootherapy more commonly practiced by hunting households (OR = 2.47, p < 0.01), and prescriptions that were gender and age specific (e.g., maternal and pediatric care) or highly seasonal (e.g., associated with annual festivals and seasonal illnesses). Specific practices were informed by species availability and theories of healing (i.e., "like cures like" and sympathetic healing and magic) that further shaped the nature of human-animal interactions via zootherapy. CONCLUSIONS: Epidemiological investigations of zoonoses and public health interventions that aim to reduce zoonotic exposures should explicitly consider zootherapy as a potential pathway for disease transmission and consider the sociocultural and environmental contexts of their use in health messaging and interventions.

Eating Bushmeat Improves Food Security in a Biodiversity and Infectious Disease "Hotspot".

Hunting and consumption of wild animals, colloquially known as "bushmeat," is associated with health trade-offs. Contact with wildlife increases exposure to wildlife-origin zoonotic diseases yet bushmeat is an important nutritional resource in many rural communities. In this study, we test the hypothesis that bushmeat improves food security in communities that hunt and trade bushmeat regularly. We conducted 478 interviews with men and women in six communities near Cross River National Park in Nigeria. We used interview responses to relate prevalence and diversity of bushmeat consumption to household food security status. Animal-based foods were the most commonly obtained items from the forest, and 48 types of wild vertebrate animals were consumed within the past 30 days. Seventy-five percent of households experienced some degree of food insecurity related to food access. Bushmeat consumption was significantly associated with relatively higher household food security status. Rodents were more important predictors of food security than other animal taxa. Despite increased bushmeat consumption in food-secure households, food-insecure households consumed a higher diversity of bushmeat species. Results show that consumption of bushmeat, especially rodents, is uniquely related to improved food security. Reliance on a wider diversity of species in food-insecure households may in turn affect their nutrition, exposures to reservoirs of zoonotic infections, and impact on wildlife conservation. Our results indicate that food security should be addressed in conservation and public health strategies aimed at reducing human-wildlife contact, and that improved wildlife protection, when combined with alternative animal-based foods, would positively affect food security in the long term.

Captive-born cotton-top tamarins (Saguinus oedipus) respond similarly to vocalizations of predators and sympatric nonpredators.

What types of cues do callitrichid primates use to detect and respond to predators? Do they respond to predator-specific cues or to more general cues? The evidence for these questions remains conflicting. We presented captive-born and reared cotton-top tamarins with no previous exposure to predators (or predator cues) with vocalizations from three potential predators of cotton-top tamarin in the wild (white hawk, jaguar, and tayra) and with vocalizations from sympatric nonpredators (black-faced antthrush and red howler monkey). Vocalizations from predators and from nonpredator mammals elicited equivalent arousal, fear, and vocal responses. Howler monkey roars produced the strongest responses. The results suggest that predator-naïve cotton-top tamarins do not recognize specific predator vocalizations, but may respond to vocal qualities (low-frequency, noisy sounds) that indicate large body size, threat, or aggression. On the other hand, tamarins responded much more strongly to the higher frequency calls from the hawk than the antthrush, suggesting another mechanism must also be involved. The failure of captive-reared tamarins to distinguish between vocalizations of predators and nonpredator mammals has important implications for reintroduction studies.

Demography and health of "village dogs" in rural Western Uganda.

"Village dogs" in developing economies are assumed to be heavily burdened by infectious disease. We followed a cohort of 61 village dogs in rural western Uganda prospectively for fifteen months to measure changes in health and demographic outcomes, and to examine risk factors for morbidity and mortality. The mean (±standard deviation) number of dogs per household was 2.4 (±2.0), of which 56.0% were male and 44.0% female. For females, average age at first estrus was 1.7 (±0.6)years with a mean litter size of 3.8 (±1.5). In the first, second and third parities, average puppy mortality per litter was 3.2 (±2.5), 2.4 (±2.1) and 3.4 (±2.9), respectively. The main causes of morbidity and mortality were infectious disease (46.1%), culling (euthanasia) by owners (30.8%), and attacks by baboons, Papio anubis (23.1%). Cox proportional hazard regression showed that a clinical diagnosis of anemia significantly predicted morbidity (HR=4.3 (95% CI: 1.1-17.8); p<0.05), and younger age significantly predicted mortality (HR=3.6 (95% CI: 1.2-10.6); p<0.05). Our results indicate that infectious disease is indeed important to the health and survival in village dogs in this setting, but that cultural practices related to ownership and interactions with wildlife also contribute substantially to morbidity and mortality.

Combining Footwear with Public Health Iconography to Prevent Soil-Transmitted Helminth Infections.

Shoes are effective for blocking soil-transmitted helminths (STHs) that penetrate the skin. Unfortunately, shoe-wearing is uncommon in many areas where STHs are prevalent, in part because local populations are unaware of the health benefits of wearing shoes. This is especially true in low-literacy populations, where information dissemination through written messages is not possible. We launched a public health intervention that combines a public health image with sandals. The image is a "lenticular image" that combines two alternating pictures to depict the efficacy of shoes for preventing STH infection. This image is adhered to the shoe, such that the message is linked directly to the primary means of prevention. To create a culturally appropriate image, we conducted five focus group discussions, each with a different gender and age combination. Results of focus group discussions reinforced the importance of refining public health messages well in advance of distribution so that cultural acceptability is strong. After the image was finalized, we deployed shoes with the image in communities in western Uganda where hookworm is prevalent. We found that the frequency of shoe-wearing was 25% higher in communities receiving the shoes than in control communities. Microscopic analyses of fecal samples for parasites showed a sustained reduction in infection intensity for parasites transmitted directly through the feet when people received shoes with a public health image. Our results show that combining culturally appropriate images with public health interventions can be effective in low-literacy populations.

Primate reinfection with gastrointestinal parasites: behavioural and physiological predictors of parasite acquisition.

Infectious disease transmission is a cost of sociality in humans and other animals. Nevertheless, the mechanisms linking social behaviour to infection risk are poorly known. We conducted a field experiment to examine how host intrinsic traits, behaviour and physiology affect infection of nonhuman primates with gastrointestinal parasites. We measured rate to reinfection in a social group of red-capped mangabeys, Cercocebus torquatus, following chemotherapeutic treatment for parasite infections. By measuring behaviour, infection and glucocorticoid levels, we compared the relative effects of space sharing, directional contact and physiological stress on risk of acquiring new infections. We found that, within proximity networks, individuals that were central and well connected and that had a tendency to switch groups were at increased risk of infection with helminths. Protozoan infections, however, were acquired more uniformly across the population. In general, position in the social network and, in particular, space sharing appears to be more important than the immunosuppressive effects of physiological stress or host traits in determining risk of infection. Our results suggest that future studies of disease ecology within wildlife populations should focus on measures of network association in addition to individual host traits.

Social Behaviours and Networks of Vervet Monkeys Are Influenced by Gastrointestinal Parasites.

Substantial research has shown that while some parasite infections can be fatal to hosts, most infections are sub-clinical and non-lethal. Such sub-clinical infections can nonetheless have negative consequences for the long-term fitness of the host such as reducing juvenile growth and the host's ability to compete for food and mates. With such effects, infected individuals are expected to exhibit behavioural changes. Here we use a parasite removal experiment to quantify how gastrointestinal parasite infections affect the behaviour of vervet monkeys (Chlorocebus aethiops) at Lake Nabugabo, Uganda. Behavioural profiles and the structure of nearest neighbour relationships varied significantly. As predicted, after deworming the duration of the resting events decreased, which is consistent with the idea that parasite infections are energetically costly. In contrast to what was predicted, we could not reject the null hypothesis and we observed no change in either the frequency or duration of grooming, but we found that the duration of travel events increased. A network analysis revealed that after deworming, individuals tended to have more nearest neighbours and hence probably more frequent interactions, with this effect being particularly marked for juveniles. The heightened response by juveniles may indicate that they are avoiding infected individuals more than other age classes because it is too costly to move energy away from growth. We consider that populations with high parasite burden may have difficulties developing social networks and behaviours that could have cascading effects that impact the population in general.

Drivers of bushmeat hunting and perceptions of zoonoses in Nigerian hunting communities.

Bushmeat hunting threatens biodiversity and increases the risk of zoonotic pathogen transmission. Nevertheless, limited information exists on patterns of contact with wildlife in communities that practice bushmeat hunting, especially with respect to social drivers of hunting behavior. We used interview responses from hunters and non-hunters in rural hunting communities in Nigeria to: 1) quantify contact rates with wildlife, 2) identify specific hunting behaviors that increase frequency of contact, 3) identify socioeconomic factors that predispose individuals to hunt, and 4) measure perceptions of risk. Participants engaged in a variety of behaviors that increased contact with wild animals, including: butchering to sell (37%), being injured (14%), using body parts for traditional medicine (19%), collecting carcasses found in forests and/or farms (18%), and keeping as pets (16%). Hunters came into contact with wildlife significantly more than non-hunters, even through non-hunting exposure pathways. Participants reported hunting rodents (95%), ungulates (93%), carnivores (93%), primates (87%), and bats (42%), among other prey. Reported hunting frequencies within taxonomic groups of prey were different for different hunting behaviors. Young age, lower education level, larger household size, having a father who hunts, and cultural group were all associated with becoming a hunter. Fifty-five percent of respondents were aware that they could contract diseases from wild animals, but only 26% of these individuals reported taking protective measures. Overall, hunters in this setting frequently contact a diversity of prey in risky ways, and the decision to become a hunter stems from family tradition, modified by economic necessity. Conservation and public health interventions in such settings may be most efficient when they capitalize on local knowledge and target root socio-economic and cultural drivers that lead to hunting behavior. Importantly, interventions that target consumption alone will not be sufficient; other drivers and modes of interaction with wildlife must also be considered.

Lung fluke (Paragonimus africanus) infects Nigerian red-capped mangabeys and causes respiratory disease.

Eggs of the lung fluke genus Paragonimus were detected in red-capped mangabeys (Cercocebus torquatus) in Nigeria. We assess the role of these primates as potential sylvatic hosts and the clinical effects of the parasite on monkeys. DNA sequenced from eggs in feces were 100% identical in the ITS2 region to Paragonimus africanus sequences from humans in Cameroon. Paragonimus-positive monkeys coughed more than uninfected monkeys. Experimental de-worming led to reduction in parasite intensity and a corresponding reduction of coughing to baseline levels in infected monkeys. This report provides the first evidence of Paragonimus sp. in C. torquatus, of P. africanus in Nigerian wildlife, and the first molecular evidence of the parasite in African wildlife. Coughing, sometimes interpreted as a communication behavior in primates, can actually indicate infection with lung parasites. Observations of coughing in primates may, in turn, provide a useful mechanism for surveillance of Paragonimus spp, which are re-emerging human pathogens, in wildlife reservoirs.