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.

Cattle aggregations at shared resources create potential parasite exposure hotspots for wildlife.

Globally rising livestock populations and declining wildlife numbers are likely to dramatically change disease risk for wildlife and livestock, especially at resources where they congregate. However, limited understanding of interspecific transmission dynamics at these hotspots hinders disease prediction or mitigation. In this study, we combined gastrointestinal nematode density and host foraging activity measurements from our prior work in an East African tropical savannah system with three estimates of parasite sharing capacity to investigate how interspecific exposures alter the relative riskiness of an important resource - water - among cattle and five dominant herbivore species. We found that due to their high parasite output, water dependence and parasite sharing capacity, cattle greatly increased potential parasite exposures at water sources for wild ruminants. When untreated for parasites, cattle accounted for over two-thirds of total potential exposures around water for wild ruminants, driving 2-23-fold increases in relative exposure levels at water sources. Simulated changes in wildlife and cattle ratios showed that water sources become increasingly important hotspots of interspecific transmission for wild ruminants when relative abundance of cattle parasites increases. These results emphasize that livestock have significant potential to alter the level and distribution of parasite exposures across the landscape for wild ruminants.

Large-herbivore nemabiomes: patterns of parasite diversity and sharing.

Amidst global shifts in the distribution and abundance of wildlife and livestock, we have only a rudimentary understanding of ungulate parasite communities and parasite-sharing patterns. We used qPCR and DNA metabarcoding of fecal samples to characterize gastrointestinal nematode (Strongylida) community composition and sharing among 17 sympatric species of wild and domestic large mammalian herbivore in central Kenya. We tested a suite of hypothesis-driven predictions about the role of host traits and phylogenetic relatedness in describing parasite infections. Host species identity explained 27-53% of individual variation in parasite prevalence, richness, community composition and phylogenetic diversity. Host and parasite phylogenies were congruent, host gut morphology predicted parasite community composition and prevalence, and hosts with low evolutionary distinctiveness were centrally positioned in the parasite-sharing network. We found no evidence that host body size, social-group size or feeding height were correlated with parasite composition. Our results highlight the interwoven evolutionary and ecological histories of large herbivores and their gastrointestinal nematodes and suggest that host identity, phylogeny and gut architecture-a phylogenetically conserved trait related to parasite habitat-are the overriding influences on parasite communities. These findings have implications for wildlife management and conservation as wild herbivores are increasingly replaced by livestock.

The effects of herbivore aggregations at water sources on savanna plants differ across soil and climate gradients.

Water sources in arid and semiarid ecosystems support humans, wildlife, and domestic animals, forming nodes of activity that sculpt surrounding plant communities and impact critical grazing and soil systems. However, global aridification and changing surface water supply threaten to disrupt these water resources, with strong implications for conservation and management of these ecosystems. To understand how effects of herbivore aggregation at water impact plant communities across contexts, we measured herbivore activity, plant height, cover (trees, grasses, forbs, and bare ground), diversity, and composition at 17 paired water sources and matrix sites across a range of abiotic factors in a semiarid savanna in Kenya. The effects of proximity to surface water and herbivore aggregation on plant communities varied substantially depending on soil and rainfall. In arid areas with nutrient-poor sandy soils, forb and tree cover were 50% lower at water sources compared to neighboring matrix sites, bare ground was 20% higher, species richness was 15% lower, and a single globally important grazing grass (Cynodon dactylon) dominated 60% of transects. However, in mesic areas with nutrient-rich finely textured soils, species richness was 25% higher, despite a 40% increase in bare ground, concurrent with the decline of a dominant tall grass (Themeda triandra) and increase in C. dactylon and other grass species near water sources. Recent rainfall was important for grasses; cover was higher relative to matrix sites only during wet periods, a potential indication of compensatory grazing. These findings suggest that effects of herbivore aggregation on vegetation diversity and composition will vary in magnitude, and in some cases direction, depending on other factors at the site. Where moisture and nutrient resources are high and promote the dominance of few plant species, herbivore aggregations may maintain diversity by promoting grazing lawns and increasing nondominant species cover. However, in arid conditions and sites with low nutrient availability, diversity can be substantially reduced by these aggregations. Our results highlight the importance of considering abiotic conditions when managing for effects of herbivore aggregations near water. This will be particularly important for future managers in light of growing global aridification and surface water changes.

Interacting effects of wildlife loss and climate on ticks and tick-borne disease.

Both large-wildlife loss and climatic changes can independently influence the prevalence and distribution of zoonotic disease. Given growing evidence that wildlife loss often has stronger community-level effects in low-productivity areas, we hypothesized that these perturbations would have interactive effects on disease risk. We experimentally tested this hypothesis by measuring tick abundance and the prevalence of tick-borne pathogens (Coxiella burnetii and Rickettsia spp.) within long-term, size-selective, large-herbivore exclosures replicated across a precipitation gradient in East Africa. Total wildlife exclusion increased total tick abundance by 130% (mesic sites) to 225% (dry, low-productivity sites), demonstrating a significant interaction of defaunation and aridity on tick abundance. When differing degrees of exclusion were tested for a subset of months, total tick abundance increased from 170% (only mega-herbivores excluded) to 360% (all large wildlife excluded). Wildlife exclusion differentially affected the abundance of the three dominant tick species, and this effect varied strongly over time, likely due to differences among species in their host associations, seasonality, and other ecological characteristics. Pathogen prevalence did not differ across wildlife exclusion treatments, rainfall levels, or tick species, suggesting that exposure risk will respond to defaunation and climate change in proportion to total tick abundance. These findings demonstrate interacting effects of defaunation and aridity that increase disease risk, and they highlight the need to incorporate ecological context when predicting effects of wildlife loss on zoonotic disease dynamics.

Parasite responses to large mammal loss in an African savanna.

Biodiversity loss can alter disease transmission; however, the magnitude and direction of these effects vary widely across ecosystems, scales, and pathogens. Here we experimentally examine the effects of one of the most globally pervasive patterns of biodiversity decline, the selective loss of large wildlife, on infection probability, intensity and population size of a group of common rodent-borne parasites - macroparasitic helminths. Consistent with previous work on vector-borne pathogens, we found that large wildlife removal causes strong and systematic increases of rodent-borne parasites, largely due to increases in rodent density, as rodents are released from competition with larger herbivores. Although we predicted that increased host density would also increase per capita infection among all directly transmitted parasites, this additional amplification occurred for only two of three examined parasites. Furthermore, the actual effects of large mammal loss on per capita infection were mediated by the complex suite of abiotic and biotic factors that regulate parasite transmission. Thus, while these results strongly suggest that large wildlife loss will cause systematic increases in rodent parasite populations, they also underscore the difficulty of making more specific predictions for a given parasite based on simple attributes such as transmission mode or life history strategy. Instead, detailed information on the ecology of each parasite species would be necessary to make more accurate predictions of how biodiversity loss will affect infection.

Shifting mammal communities and declining species richness along an elevational gradient on Mount Kenya.

Conservation areas encompassing elevation gradients are biodiversity hotspots because they contain a wide range of habitat types in a relatively small space. Studies of biodiversity patterns along elevation gradients, mostly on small mammal or bird species, have documented a peak in diversity at mid elevations. Here, we report on a field study of medium and large mammals to examine the impact of elevation, habitat type, and gross primary productivity on community structure. Species richness was observed using a camera trap transect with 219 sites situated across different habitat types from 2329 to 4657 m above the sea level on the western slope of Mt Kenya, the second highest mountain in Africa. We found that the lowest elevation natural habitats had the highest species richness and relative abundance and that both metrics decreased steadily as elevation increased, paralleling changes in gross primary productivity, and supporting the energy richness hypothesis. We found no evidence for the mid-domain effect on species diversity. The lowest elevation degraded Agro-Forestry lands adjacent to the National Park had high activity of domestic animals and reduced diversity and abundance of native species. The biggest difference in community structure was between protected and unprotected areas, followed by more subtle stepwise differences between habitats at different elevations. Large carnivore species remained relatively consistent but dominant herbivore species shifted along the elevation gradient. There was some habitat specialization and turnover in species, such that the elevation gradient predicts a high diversity of species, demonstrating the high conservation return for protecting mountain ecosystems for biodiversity conservation.

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.

Water sources aggregate parasites with increasing effects in more arid conditions.

Shifts in landscape heterogeneity and climate can influence animal movement in ways that profoundly alter disease transmission. Water sources that are foci of animal activity have great potential to promote disease transmission, but it is unknown how this varies across a range of hosts and climatic contexts. For fecal-oral parasites, water resources can aggregate many different hosts in small areas, concentrate infectious material, and function as disease hotspots. This may be exacerbated where water is scarce and for species requiring frequent water access. Working in an East African savanna, we show via experimental and observational methods that water sources increase the density of wild and domestic herbivore feces and thus, the concentration of fecal-oral parasites in the environment, by up to two orders of magnitude. We show that this effect is amplified in drier areas and drier periods, creating dynamic and heterogeneous disease landscapes across space and time. We also show that herbivore grazing behaviors that expose them to fecal-oral parasites often increase at water sources relative to background sites, increasing potential parasite transmission at these hotspots. Critically, this effect varies by herbivore species, with strongest effects for two animals of concern for conservation and development: elephants and cattle.

Migration in the Anthropocene: how collective navigation, environmental system and taxonomy shape the vulnerability of migratory species.

Recent increases in human disturbance pose significant threats to migratory species using collective movement strategies. Key threats to migrants may differ depending on behavioural traits (e.g. collective navigation), taxonomy and the environmental system (i.e. freshwater, marine or terrestrial) associated with migration. We quantitatively assess how collective navigation, taxonomic membership and environmental system impact species' vulnerability by (i) evaluating population change in migratory and non-migratory bird, mammal and fish species using the Living Planet Database (LPD), (ii) analysing the role of collective navigation and environmental system on migrant extinction risk using International Union for Conservation of Nature (IUCN) classifications and (iii) compiling literature on geographical range change of migratory species. Likelihood of population decrease differed by taxonomic group: migratory birds were more likely to experience annual declines than non-migrants, while mammals displayed the opposite pattern. Within migratory species in IUCN, we observed that collective navigation and environmental system were important predictors of extinction risk for fishes and birds, but not for mammals, which had overall higher extinction risk than other taxa. We found high phylogenetic relatedness among collectively navigating species, which could have obscured its importance in determining extinction risk. Overall, outputs from these analyses can help guide strategic interventions to conserve the most vulnerable migrations.This article is part of the theme issue 'Collective movement ecology'.

Conservation of biodiversity as a strategy for improving human health and well-being.

The Earth's ecosystems have been altered by anthropogenic processes, including land use, harvesting populations, species introductions and climate change. These anthropogenic processes greatly alter plant and animal communities, thereby changing transmission of the zoonotic pathogens they carry. Biodiversity conservation may be a potential win-win strategy for maintaining ecosystem health and protecting public health, yet the causal evidence to support this strategy is limited. Evaluating conservation as a viable public health intervention requires answering four questions: (i) Is there a general and causal relationship between biodiversity and pathogen transmission, and if so, which direction is it in? (ii) Does increased pathogen diversity with increased host biodiversity result in an increase in total disease burden? (iii) Do the net benefits of biodiversity conservation to human well-being outweigh the benefits that biodiversity-degrading activities, such as agriculture and resource utilization, provide? (iv) Are biodiversity conservation interventions cost-effective when compared to other options employed in standard public health approaches? Here, we summarize current knowledge on biodiversity-zoonotic disease relationships and outline a research plan to address the gaps in our understanding for each of these four questions. Developing practical and self-sustaining biodiversity conservation interventions will require significant investment in disease ecology research to determine when and where they will be effective.This article is part of the themed issue 'Conservation, biodiversity and infectious disease: scientific evidence and policy implications'.