Explaining the primate extinction crisis: predictors of extinction risk and active threats.

Explaining why some species are disproportionately impacted by the extinction crisis is of critical importance for conservation biology as a science and for proactively protecting species that are likely to become threatened in the future. Using the most current data on threat status, population trends, and threat types for 446 primate species, we advance previous research on the determinants of extinction risk by including a wider array of phenotypic traits as predictors, filling gaps in these trait data using multiple imputation, and investigating the mechanisms that connect organismal traits to extinction risk. Our Bayesian phylogenetically controlled analyses reveal that insular species exhibit higher threat status, while those that are more omnivorous and live in larger groups have lower threat status. The same traits are not linked to risk when repeating our analyses with older IUCN data, which may suggest that the traits influencing species risk are changing as anthropogenic effects continue to transform natural landscapes. We also show that non-insular, larger-bodied, and arboreal species are more susceptible to key threats responsible for primate population declines. Collectively, these results provide new insights to the determinants of primate extinction and identify the mechanisms (i.e. threats) that link traits to extinction risk.

Sociodemographic Variables Can Guide Prioritized Testing Strategies for Epidemic Control in Resource-Limited Contexts.

BACKGROUND: Targeted surveillance allows public health authorities to implement testing and isolation strategies when diagnostic resources are limited, and can be implemented via the consideration of social network topologies. However, it remains unclear how to implement such surveillance and control when network data are unavailable. METHODS: We evaluated the ability of sociodemographic proxies of degree centrality to guide prioritized testing of infected individuals compared to known degree centrality. Proxies were estimated via readily available sociodemographic variables (age, gender, marital status, educational attainment, household size). We simulated severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) epidemics via a susceptible-exposed-infected-recovered individual-based model on 2 contact networks from rural Madagascar to test applicability of these findings to low-resource contexts. RESULTS: Targeted testing using sociodemographic proxies performed similarly to targeted testing using known degree centralities. At low testing capacity, using proxies reduced infection burden by 22%-33% while using 20% fewer tests, compared to random testing. By comparison, using known degree centrality reduced the infection burden by 31%-44% while using 26%-29% fewer tests. CONCLUSIONS: We demonstrate that incorporating social network information into epidemic control strategies is an effective countermeasure to low testing capacity and can be implemented via sociodemographic proxies when social network data are unavailable.

Predicting primate-parasite associations using exponential random graph models.

Ecological associations between hosts and parasites are influenced by host exposure and susceptibility to parasites, and by parasite traits, such as transmission mode. Advances in network analysis allow us to answer questions about the causes and consequences of traits in ecological networks in ways that could not be addressed in the past. We used a network-based framework (exponential random graph models or ERGMs) to investigate the biogeographic, phylogenetic and ecological characteristics of hosts and parasites that affect the probability of interactions among nonhuman primates and their parasites. Parasites included arthropods, bacteria, fungi, protozoa, viruses and helminths. We investigated existing hypotheses, along with new predictors and an expanded host-parasite database that included 213 primate nodes, 763 parasite nodes and 2319 edges among them. Analyses also investigated phylogenetic relatedness, sampling effort and spatial overlap among hosts. In addition to supporting some previous findings, our ERGM approach demonstrated that more threatened hosts had fewer parasites, and notably, that this effect was independent of hosts also having a smaller geographic range. Despite having fewer parasites, threatened host species shared more parasites with other hosts, consistent with loss of specialist parasites and threat arising from generalist parasites that can be maintained in other, non-threatened hosts. Viruses, protozoa and helminths had broader host ranges than bacteria, or fungi, and parasites that infect non-primates had a higher probability of infecting more primate species. The value of the ERGM approach for investigating the processes structing host-parasite networks provided a more complete view on the biogeographic, phylogenetic and ecological traits that influence parasite species richness and parasite sharing among hosts. The results supported some previous analyses and revealed new associations that warrant future research, thus revealing how hosts and parasites interact to form ecological networks.

Effect of habitat degradation on hantavirus infection among introduced and endemic small mammals of Madagascar.

Hantaviruses are globally distributed zoonotic pathogens capable of causing fatal disease in humans. Rodents and other small mammals are the typical reservoirs of hantaviruses, though the particular host varies regionally. Addressing the risk of hantavirus spillover from animal reservoirs to humans requires identifying the local mammal reservoirs and the predictors of infection in those animals, such as their population density and habitat characteristics. We screened native and non-native small mammals and bats in northeastern Madagascar for hantavirus infection to investigate the influence of habitat, including effects of human land use on viral prevalence. We trapped 227 bats and 1663 small mammals over 5 successive years in and around Marojejy National Park across a range of habitat types including villages, agricultural fields, regrowth areas, and secondary and semi-intact forests. Animals sampled included endemic tenrecs (Tenrecidae), rodents (Nesomyidae) and bats (6 families), along with non-native rodents (Muridae) and shrews (Soricidae). A hantavirus closely related to the previously described Anjozorobe virus infected 9.5% of Rattus rattus sampled. We did not detect hantaviruses in any other species. Habitat degradation had a complex impact on hantavirus prevalence in our study system: more intensive land use increase the abundance of R. rattus. The average body size of individuals varied between agricultural and nonagricultural land-use types, which in turn affected infection prevalence. Smaller R.rattus had lower probability of infection and were captured more commonly in villages and forests. Thus, infection prevalence was highest in agricultural areas. These findings provide new insights to the gradients of hantavirus exposure risk for humans in areas undergoing rapid land use transformations associated with agricultural practices.

Using phylogeographic link-prediction in primates to prioritize human parasite screening.

Objectives: The ongoing risk of emerging infectious disease has renewed calls for understanding the origins of zoonoses and identifying future zoonotic disease threats. Given their close phylogenetic relatedness and geographic overlap with humans, non-human primates (NHPs) have been the source of many infectious diseases throughout human evolution. NHPs harbor diverse parasites, with some infecting only a single host species while others infect species from multiple families. Materials and Methods: We applied a novel link-prediction method to predict undocumented instances of parasite sharing between humans and NHPs. Our model makes predictions based on phylogenetic distances and geographic overlap among NHPs and humans in six countries with high NHP diversity: Columbia, Brazil, Democratic Republic of Congo, Madagascar, China and Indonesia. Results: Of the 899 human parasites documented in the Global Infectious Diseases and Epidemiology Network (GIDEON) database for these countries, 12% were shared with at least one other NHP species. The link prediction model identified an additional 54 parasites that are likely to infect humans but were not reported in GIDEON. These parasites were mostly host generalists, yet their phylogenetic host breadth varied substantially. Discussion: As human activities and populations encroach on NHP habitats, opportunities for parasite sharing between human and non-human primates will continue to increase. Our study identifies specific infectious organisms to monitor in countries with high NHP diversity, while the comparative analysis of host generalism, parasite taxonomy, and transmission mode provides insights to types of parasites that represent high zoonotic risk.

Technological infrastructure, sleep, and rest-activity patterns in a Kaqchikel Maya community.

Sleep duration, quality, and rest-activity pattern-a measure for inferring circadian rhythm-are influenced by multiple factors including access to electricity. Recent findings suggest that the safety and comfort afforded by technology may improve sleep but negatively impact rest-activity stability. According to the circadian entrainment hypothesis, increased access to electric lighting should lead to weaker and less uniform circadian rhythms, measured by stability of rest-activity patterns. Here, we investigate sleep in a Maya community in Guatemala who are in a transitional stage of industrialization. We predicted that (i) sleep will be shorter and less efficient in this population than in industrial settings, and that (ii) rest-activity patterns will be weaker and less stable than in contexts with greater exposure to the natural environment and stronger and more stable than in settings more buffered by technologic infrastructure. Our results were mixed. Compared to more industrialized settings, in our study population sleep was 4.87% less efficient (78.39% vs 83.26%). We found no significant difference in sleep duration. Rest-activity patterns were more uniform and less variable than in industrial settings (interdaily stability = 0.58 vs 0.43; intradaily variability = 0.53 vs 0.60). Our results suggest that industrialization does not inherently reduce characteristics of sleep quality; instead, the safety and comfort afforded by technological development may improve sleep, and an intermediate degree of environmental exposure and technological buffering may support circadian rhythm strength and stability.

Primate malarias as a model for cross-species parasite transmission.

Parasites regularly switch into new host species, representing a disease burden and conservation risk to the hosts. The distribution of these parasites also gives insight into characteristics of ecological networks and genetic mechanisms of host-parasite interactions. Some parasites are shared across many species, whereas others tend to be restricted to hosts from a single species. Understanding the mechanisms producing this distribution of host specificity can enable more effective interventions and potentially identify genetic targets for vaccines or therapies. As ecological connections between human and local animal populations increase, the risk to human and wildlife health from novel parasites also increases. Which of these parasites will fizzle out and which have the potential to become widespread in humans? We consider the case of primate malarias, caused by Plasmodium parasites, to investigate the interacting ecological and evolutionary mechanisms that put human and nonhuman primates at risk for infection. Plasmodium host switching from nonhuman primates to humans led to ancient introductions of the most common malaria-causing agents in humans today, and new parasite switching is a growing threat, especially in Asia and South America. Based on a wild host-Plasmodium occurrence database, we highlight geographic areas of concern and potential areas to target further sampling. We also discuss methodological developments that will facilitate clinical and field-based interventions to improve human and wildlife health based on this eco-evolutionary perspective.

Comparing transmission potential networks based on social network surveys, close contacts and environmental overlap in rural Madagascar.

Social and spatial network analysis is an important approach for investigating infectious disease transmission, especially for pathogens transmitted directly between individuals or via environmental reservoirs. Given the diversity of ways to construct networks, however, it remains unclear how well networks constructed from different data types effectively capture transmission potential. We used empirical networks from a population in rural Madagascar to compare social network survey and spatial data-based networks of the same individuals. Close contact and environmental pathogen transmission pathways were modelled with the spatial data. We found that naming social partners during the surveys predicted higher close-contact rates and the proportion of environmental overlap on the spatial data-based networks. The spatial networks captured many strong and weak connections that were missed using social network surveys alone. Across networks, we found weak correlations among centrality measures (a proxy for superspreading potential). We conclude that social network surveys provide important scaffolding for understanding disease transmission pathways but miss contact-specific heterogeneities revealed by spatial data. Our analyses also highlight that the superspreading potential of individuals may vary across transmission modes. We provide detailed methods to construct networks for close-contact transmission pathogens when not all individuals simultaneously wear GPS trackers.

Enriched sleep environments lengthen lemur sleep duration.

Characteristics of the sleep-site are thought to influence the quality and duration of primate sleep, yet only a handful of studies have investigated these links experimentally. Using actigraphy and infrared videography, we quantified sleep in four lemur species (Eulemur coronatus, Lemur catta, Propithecus coquereli, and Varecia rubra) under two different experimental conditions at the Duke Lemur Center (DLC) in Durham, NC, USA. Individuals from each species underwent three weeks of simultaneous testing to investigate the hypothesis that comfort level of the sleep-site influences sleep. We obtained baseline data on normal sleep, and then, in a pair-wise study design, we compared the daily sleep times, inter-daily activity stability, and intra-daily activity variability of individuals in simultaneous experiments of sleep-site enrichment and sleep-site impoverishment. Over 164 24-hour periods from 8 individuals (2 of each species), we found evidence that enriched sleep-sites increased daily sleep times of lemurs, with an average increase of thirty-two minutes. The effect of sleep-site impoverishment was small and not statistically significant. Though our experimental manipulations altered inter-daily stability and intra-daily variability in activity patterns relative to baseline, the changes did not differ significantly between enriched and impoverished conditions. We conclude that properties of a sleep-site enhancing softness or insulation, more than the factors of surface area or stability, influence lemur sleep, with implications regarding the importance of nest building in primate evolution and the welfare and management of captive lemurs.

Predictions of primate-parasite coextinction.

Future biodiversity loss threatens the integrity of complex ecological associations, including among hosts and parasites. Almost half of primate species are threatened with extinction, and the loss of threatened hosts could negatively impact parasite associations and ecosystem functions. If endangered hosts are highly connected in host-parasite networks, then future host extinctions will also drive parasite extinctions, destabilizing ecological networks. If threatened hosts are not highly connected, however, then network structure should not be greatly affected by the loss of threatened hosts. Networks with high connectance, modularity, nestedness and robustness are more resilient to perturbations such as the loss of interactions than sparse, nonmodular and non-nested networks. We analysed the interaction network involving 213 primates and 763 parasites and removed threatened primates (114 species) to simulate the effects of extinction. Our analyses revealed that connections to 23% of primate parasites (176 species) may be lost if threatened primates go extinct. In addition, measures of network structure were affected, but in varying ways because threatened hosts have fewer parasite interactions than non-threatened hosts. These results reveal that host extinctions will perturb the host-parasite network and potentially lead to secondary extinctions of parasites. The ecological consequences of these extinctions remain unclear. This article is part of the theme issue 'Infectious disease macroecology: parasite diversity and dynamics across the globe'.

Effects of host extinction and vector preferences on vector-borne disease risk in phylogenetically structured host-hector communities.

Anthropogenic disturbance impacts the phylogenetic composition and diversity of ecological communities. While changes in diversity are known to dramatically change species interactions and alter disease dynamics, the effects of phylogenetic changes in host and vector communities on disease have been relatively poorly studied. Using a theoretical model, we investigated how phylogeny and extinction influence network structural characteristics relevant to disease transmission in disturbed environments. We modelled a multi-host, multi-vector community as a bipartite ecological network, where nodes represent host and vector species and edges represent connections among them through vector feeding, and we simulated vector preferences and threat status on host and parasite phylogenies. We then simulated loss of hosts, including phylogenetically clustered losses, to investigate how extinction influences network structure. We compared effects of phylogeny and extinction to those of host specificity, which we predicted to strongly increase network modularity and reduce disease prevalence. The simulations revealed that extinction often increased modularity, with higher modularity as species loss increased, although not as much as increasing host specificity did. These results suggest that extinction itself, all else being equal, may reduce disease prevalence in disturbed communities. However, in real communities, systematic patterns in species loss (e.g. favoring high competence species) or changes in abundance may counteract these effects. Unexpectedly, we found that effects of phylogenetic signal in host and vector traits were relatively weak, and only important when phylogenetic signal of host and vector traits were similar, or when these traits both varied.

Food insecurity related to agricultural practices and household characteristics in rural communities of northeast Madagascar.

Ending hunger and alleviating poverty are key goals for a sustainable future. Food security is a constant challenge for agrarian communities in low-income countries, especially in Madagascar. We investigated agricultural practices, household characteristics, and food security in northeast Madagascar. We tested whether agricultural practices, demographics, and socioeconomics in rural populations were related to food security. Over 70% of respondents reported times during the last three years during which food for the household was insufficient, and the most frequently reported cause was small land size (57%). The probability of food insecurity decreased with increasing vanilla yield, rice yield, and land size. There was an interaction effect between land size and household size; larger families with smaller land holdings had higher food insecurity, while larger families with larger land had lower food insecurity. Other socioeconomic and agricultural variables were not significantly related to food insecurity, including material wealth, education, crop diversity, and livestock ownership. Our results highlight the high levels of food insecurity in these communities and point to interventions that would alleviate food stress. In particular, because current crop and livestock diversity were low, agricultural diversification could improve outputs and mitigate food insecurity. Development of sustainable agricultural intensification, including improving rice and vanilla cultivation to raise yields on small land areas, would likely have positive impacts on food security and alleviating poverty. Increasing market access and off-farm income, as well as improving policies related to land tenure could also play valuable roles in mitigating challenges in food security. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s12571-021-01179-3.

Gibbon sleep quantified: the influence of lunar phase and meteorological variables on activity in Hylobates moloch and Hylobates pileatus.

Sleep in the primate order remains understudied, with quantitative estimates of sleep duration available for less than 10% of primate species. Even fewer species have had their sleep synchronously quantified with meteorological data, which have been shown to influence sleep-wake regulatory behaviors. We report the first sleep duration estimates in two captive gibbon species, the Javan gibbon (Hylobates moloch) and the pileated gibbon (Hylobates pileatus) (N = 52 nights). We also investigated how wind speed, humidity, temperature, lunar phase, and illumination from moonlight influence sleep-wake regulation, including sleep duration, sleep fragmentation, and sleep efficiency. Gibbons exhibited strict diurnal behavior with little nighttime activity and mean total average sleep duration of 11 h and 53 min for Hylobates moloch and 12 h and 29 min for Hylobates pileatus. Gibbons had notably high sleep efficiency (i.e., time score asleep divided by the time they spent in their sleeping site, mean of 98.3%). We found illumination from moonlight in relation to lunar phase and amount of wind speed to be the strongest predictors of sleep duration and high-quality sleep, with increased moonlight and increased wind causing more fragmentation and less sleep efficiency. We conclude that arousal threshold is sensitive to nighttime illumination and wind speed. Sensitivity to wind speed may reflect adaptations to counter the risk of falling during arboreal sleep.

Mitigating Future Respiratory Virus Pandemics: New Threats and Approaches to Consider.

Despite many recent efforts to predict and control emerging infectious disease threats to humans, we failed to anticipate the zoonotic viruses which led to pandemics in 2009 and 2020. The morbidity, mortality, and economic costs of these pandemics have been staggering. We desperately need a more targeted, cost-efficient, and sustainable strategy to detect and mitigate future zoonotic respiratory virus threats. Evidence suggests that the transition from an animal virus to a human pathogen is incremental and requires a considerable number of spillover events and considerable time before a pandemic variant emerges. This evolutionary view argues for the refocusing of public health resources on novel respiratory virus surveillance at human-animal interfaces in geographical hotspots for emerging infectious diseases. Where human-animal interface surveillance is not possible, a secondary high-yield, cost-efficient strategy is to conduct novel respiratory virus surveillance among pneumonia patients in these same hotspots. When novel pathogens are discovered, they must be quickly assessed for their human risk and, if indicated, mitigation strategies initiated. In this review, we discuss the most common respiratory virus threats, current efforts at early emerging pathogen detection, and propose and defend new molecular pathogen discovery strategies with the goal of preempting future pandemics.

Epidemiological transitions in human evolution and the richness of viruses, helminths, and protozoa.

BACKGROUND AND OBJECTIVES: In absolute terms, humans are extremely highly parasitized compared to other primates. This may reflect that humans are outliers in traits correlated with parasite richness: population density, geographic range area, and study effort. The high degree of parasitism could also reflect amplified disease risk associated with agriculture and urbanization. Alternatively, controlling for other variables, cultural and psychological adaptations could have reduced parasitism in humans over evolutionary time. METHODOLOGY: We predicted the number of parasites that would infect a nonhuman primate with human phenotypic characteristics and phylogenetic position, and then compared observed parasitism of humans in eight geopolitical countries to the predicted distributions. The analyses incorporated study effort, phylogeny, and drivers of parasitism in 33 primate species. RESULTS: Analyses of individual countries were not supportive of either hypothesis. When analyzed collectively, however, human populations showed consistently lower than expected richness of protozoa and helminths, but higher richness of viruses. Thus, human evolutionary innovations and new parasite exposures may have impacted groups of parasites in different ways, with support for both hypotheses in the overall analysis. CONCLUSIONS AND IMPLICATIONS: The high level of parasitism observed in humans only applies to viruses, and was not extreme in any of our tests of individual countries. In contrast, we find consistent reductions in protozoa and helminths across countries, suggesting reduced parasitism by these groups during human evolution. We propose that hygienic and technological advances might have extinguished fecal-orally or indirectly transmitted parasites like helminths, whereas higher human densities and host-shifting potential of viruses have supported increased virus richness. LAY SUMMARY: Vastly more parasite species infect humans than any other primate host. Controlling for factors that influence parasite richness, such as the intensity of study effort and body mass, we find that humans may have more viruses, but fewer helminths and protozoa, than expected based on evolutionary analyses of parasitism in other primates.

One health disparities and COVID-19.

The global impact of the COVID-19 pandemic has disproportionately affected some communities and populations more than others. We propose that an interdisciplinary framework of 'One Health Disparities' advances understanding of the social and systemic issues that drive COVID-19 in vulnerable populations. One Health Disparities integrates the social environment with One Health perspectives on the interconnectedness of human, animal, and environmental health. To apply this framework, we consider One Health Disparities that emerge in three key components of disease transmission: exposure, susceptibility, and disease expression. Exposure disparities arise through variation in contact with COVID-19's causative agent, SARS-CoV-2. Disparities in susceptibility and disease expression also exist; these are driven by biological and social factors, such as diabetes and obesity, and through variation in access to healthcare. We close by considering how One Health Disparities informs understanding of spillback into new animal reservoirs, and what this might mean for further human health disparities. LAY SUMMARY: One Health focuses on interconnections between human, animal, and environmental health. We propose that social environments are also important to One Health and help illuminate disparities in the coronavirus pandemic, including its origins, transmission and susceptibility among humans, and spillback to other species. We call this framework One Health Disparities.

Effects of land use, habitat characteristics, and small mammal community composition on Leptospira prevalence in northeast Madagascar.

Human activities can increase or decrease risks of acquiring a zoonotic disease, notably by affecting the composition and abundance of hosts. This study investigated the links between land use and infectious disease risk in northeast Madagascar, where human subsistence activities and population growth are encroaching on native habitats and the associated biota. We collected new data on pathogenic Leptospira, which are bacteria maintained in small mammal reservoirs. Transmission can occur through close contact, but most frequently through indirect contact with water contaminated by the urine of infected hosts. The probability of infection and prevalence was compared across a gradient of natural moist evergreen forest, nearby forest fragments, flooded rice and other types of agricultural fields, and in homes in a rural village. Using these data, we tested specific hypotheses for how land use alters ecological communities and influences disease transmission. The relative abundance and proportion of exotic species was highest in the anthropogenic habitats, while the relative abundance of native species was highest in the forested habitats. Prevalence of Leptospira was significantly higher in introduced compared to endemic species. Lastly, the probability of infection with Leptospira was highest in introduced small mammal species, and lower in forest fragments compared to other habitat types. Our results highlight how human land use affects the small mammal community composition and in turn disease dynamics. Introduced species likely transmit Leptospira to native species where they co-occur, and may displace the Leptospira species naturally occurring in Madagascar. The frequent spatial overlap of people and introduced species likely also has consequences for public health.

Effect of urban habitat use on parasitism in mammals: a meta-analysis.

Rates of urbanization are increasing globally, with consequences for the dynamics of parasites and their wildlife hosts. A small subset of mammal species have the dietary and behavioural flexibility to survive in urban settings. The changes that characterize urban ecology-including landscape transformation, modified diets and shifts in community composition-can either increase or decrease susceptibility and exposure to parasites. We used a meta-analytic approach to systematically assess differences in endoparasitism between mammals in urban and non-urban habitats. Parasite prevalence estimates in matched urban and non-urban mammal populations from 33 species were compiled from 46 published studies, and an overall effect of urban habitation on parasitism was derived after controlling for study and parasite genus. Parasite life cycle type and host order were investigated as moderators of the effect sizes. We found that parasites with complex life cycles were less prevalent in urban carnivore and primate populations than in non-urban populations. However, we found no difference in urban and non-urban prevalence for parasites in rodent and marsupial hosts, or differences in prevalence for parasites with simple life cycles in any host taxa. Our findings therefore suggest the disruption of some parasite transmission cycles in the urban ecological community.

Metabarcoding of eukaryotic parasite communities describes diverse parasite assemblages spanning the primate phylogeny.

Despite their ubiquity, in most cases little is known about the impact of eukaryotic parasites on their mammalian hosts. Comparative approaches provide a powerful method to investigate the impact of parasites on host ecology and evolution, though two issues are critical for such efforts: controlling for variation in methods of identifying parasites and incorporating heterogeneity in sampling effort across host species. To address these issues, there is a need for standardized methods to catalogue eukaryotic parasite diversity across broad phylogenetic host ranges. We demonstrate the feasibility of a metabarcoding approach for describing parasite communities by analysing faecal samples from 11 nonhuman primate species representing divergent lineages of the primate phylogeny and the full range of sampling effort (i.e. from no parasites reported in the literature to the best-studied primates). We detected a number of parasite families and regardless of prior sampling effort, metabarcoding of only ten faecal samples identified parasite families previously undescribed in each host (x̅ = 8.5 new families per species). We found more overlap between parasite families detected with metabarcoding and published literature when more research effort-measured as the number of publications-had been conducted on the host species' parasites. More closely related primates and those from the same continent had more similar parasite communities, highlighting the biological relevance of sampling even a small number of hosts. Collectively, results demonstrate that metabarcoding methods are sensitive and powerful enough to standardize studies of eukaryotic parasite communities across host species, providing essential new tools for macroecological studies of parasitism.