Tamika J. Lunn

and 4 more

AbstractIdentifying the areas and drivers of high-risk interfaces for human-wildlife interaction is crucial for managing and reversing human zoonotic disease risk. We suggest that continent-wide improvement to African housing is inadvertently creating roosting habitat for synanthropic free-tailed bats (family Molossidae), and opportunity for human exposure to bat-associated pathogens. We mapped building use by free-tailed bats from 1,109 buildings along a residential gradient in rural south-eastern Kenya where viruses of concern have been detected. We show that bats frequently roost in human-occupied buildings; almost one-in-ten buildings showed evidence of bat occupation (9.2%), and one-in-13 were active roosts (7.6%). We identified modern-build style and triangular roofing as building-level predictors of bat occupation, and the proportion of modern buildings as a landscape-level predictor of bat occupancy. Given the international focus on building improvement in Africa, and the increasing access to improved housing already reported in the literature, we suggest that this is a rapidly accelerating exposure interface that needs urgent attention and investment. Ethical pre-emptive exclusion of bats (by sealing bat entrance points) and restoration of natural roosting habitats should be prioritized as One Health land-use planning strategies in rural Africa.  Introduction The emergence and re-emergence of zoonotic disease is driven by ecosystem changes at the landscape level 1. Ecosystem disturbances through anthropogenic land use changes have been key drivers of emerging infectious diseases over the last century 2. Changes to ecosystem features – such as wildlife abundance, community composition, demography, behaviour, movement, contact patterns, and pathogen susceptibility – directly and indirectly alter the risk of pathogen transmission from wildlife to humans, through modifying disease dynamics within wildlife hosts and contact between wildlife and humans1. Because spatial overlap between wildlife reservoirs and humans is a key requirement for cross-species transmission (spillover), studies that investigate how human activities increase exposure to wildlife are critical for mitigating the transmission and emergence of zoonoses 3.Urbanisation commonly results in destruction and fragmentation of wildlife habitat, with ensuing encroachment creating human-wildlife interfaces at the edges of anthropogenic areas. For synanthropic wildlife, urbanisation can additionally create habitat and increase key resources, creating mosaics of human-wildlife interfaces within anthropogenic areas. Human pathogen exposure from synanthropic wildlife has been observed for various zoonoses, including tick-borne bacterial pathogens and viral infections (e.g., McFarlane et al. 2012; Bermúdez et al. 2016; Bermúdez et al. 2017). Identifying the specific drivers of these high-risk interfaces is especially important in global hotspots for emerging infectious diseases 7,8, countries with limited resources for disease surveillance, prevention and control7, and for taxonomic groups identified to harbour zoonotic pathogens 9. However, information on wildlife-human exposure remains limited for many under-resourced disease hotspots, particularly in sub-Saharan Africa and parts of Asia, as well as for many host taxa, including bats. These deficiencies are exacerbated by limited understanding of basic bat ecology in remote parts of Africa and Asia 10.African molossid bats, or free-tailed bats, are some of the most widely distributed and abundant bats on the African continent11. Several Molossid species host zoonoses-associated viral families, including corona-, filo-, paramyxo-, rota-, astro-, flavi-, and lyssaviruses12–17. Two Molossid species (Mops condylurusand Mops pumilus ) are also putative ebolavirus hosts, both showing evidence of infection in the wild, and the ability to replicate ebolaviruses without morbidity following experimental inoculation18–20.Synanthropic free-tailed bat species are increasingly using human-built structures as roosts, instead of natural roosts in tree hollows and rock crevasses 21. Continent-wide changes to African housing have seen human dwellings change from traditional buildings with natural materials (e.g., mud walls and thatch roofs), to modern-style buildings with finished materials and modern design elements, including structural beams and ceilings22. Spaces in ceilings, and between beams and walls, create roosting habitat for free-tailed bats, and appear to sustain larger colonies than natural roosts and traditional buildings (up to thousands in modern housing) 23. Changing patterns of bat-bat and bat-human contact through the use of these anthropogenic structures creates an exposure interface that may increase pathogen transmission, both among bat species and from bats to humans.Given the limited information available on basic bat ecology and wildlife-human exposure in remote parts of Africa, particularly at landscape scales, this study aimed to: 1) map high-risk interfaces of bat-human exposure along a residential gradient in rural south-eastern Kenya, and 2) to identify building- and landscape-level attributes of bat-human exposure risk. This study provides empirical information on the roosting of anthropogenic free-tailed bats in south-eastern Kenya, and describes the conditions in which housing improvement (without proper consideration of local bat ecology) could facilitate the emergence of zoonotic disease in remote parts of Africa. This information is critical to better understand bat-virus exposure interfaces that drive disease risk, and to inform strategies for One Health land-use planning in changing landscapes.

Tamika J. Lunn

and 4 more

Tamika Lunn

and 6 more

1. Fruit bats (Family: Pteropodidae) are animals of great ecological and economic importance, yet their populations are threatened by ongoing habitat loss and human persecution. A lack of ecological knowledge for the vast majority of Pteropodid bat species presents additional challenges for their conservation and management. 2. In Australia, populations of flying-fox species (Genus: Pteropus) are declining and management approaches are highly contentious. Australian flying-fox roosts are exposed to management regimes involving habitat modification, either through human-wildlife conflict management policies, or vegetation restoration programs. Details on the fine-scale roosting ecology of flying-foxes are not sufficiently known to provide evidence-based guidance for these regimes and the impact on flying-foxes of these habitat modifications is poorly understood. 3. We seek to identify and test commonly held understandings about the roosting ecology of Australian flying-foxes to inform practical recommendations and guide and refine management practices at flying-fox roosts. 4. We identify 31 statements relevant to understanding of flying-fox roosting structure, and synthesise these in the context of existing literature. We then contribute contemporary data on the fine-scale roosting structure of flying-fox species in south-eastern Queensland and north-eastern New South Wales, presenting a 13-month dataset from 2,522 spatially referenced roost trees across eight sites. 5. We show evidence of sympatry and indirect competition between species, including spatial segregation of black and grey-headed flying-foxes within roosts and seasonal displacement of both species by little red flying-foxes. We demonstrate roost-specific annual trends in occupancy and abundance and provide updated demographic information including the spatial and temporal distributions of males and females within roosts. 6. Insights from our systematic and quantitative study will be important to guide evidence-based recommendations on restoration and management and will be crucial for the implementation of priority recovery actions for the preservation of these species into the future.

Tamika Lunn

and 6 more

Models of host-pathogen interactions help to explain infection dynamics in wildlife populations and to predict and mitigate the risk of zoonotic spillover. Insights from models inherently depend on the way contacts between hosts are modelled, and crucially, how transmission scales with animal density.Bats are important reservoirs of zoonotic disease and are among the most gregarious of all mammals. Their population structures can be highly heterogenous, underpinned by ecological processes across different scales, complicating assumptions regarding the nature of density-transmission scaling. Although models commonly parameterise transmission using metrics of total abundance, whether this is an ecologically representative approximation of host-pathogen interactions is not routinely evaluated.We collected a 13-month dataset of roosting Pteropus spp. from 2,522 spatially referenced trees across eight roosts to compare density estimates across scales (roost-level, subplot-level, tree-level). We then focus on tree-level measures of abundance and density, the scale most likely to be relevant for virus transmission between tree-roosting Pteropus , and evaluate whether roost features at different scales are predictive of local dynamics.Our density estimates varied greatly by scale. Mean density ofPteropus at the roost level was 13-fold lower than at a subplot-level that accounted for heterogenous distributions of bats (0.38 bats/m2 vs 5.13 bats/m2). Additionally, roost-level measures (roost abundance and roost area) did not represent tree-level abundance or tree-level density, with models explaining minimal variation in tree-level measures.This indicates that basic measures, such as roost-level population counts, may not provide adequate approximations for population dynamics at scales relevant for transmission, and that alternative measures are needed to compare transmission potential between roosts. From the best candidate models, the best predictor of local population structure was tree density within roosts, where roosts with low tree density had a higher abundance but lower density of bats (more spacing between bats) per tree.Together, these data highlight unpredictable and counterintuitive relationships between abundance and density, and between measures at different scales. More nuanced modelling of transmission, spread and spillover from bats likely requires alternative approaches to integrating contact structure in host-pathogen models, rather than simply modifying the transmission function.