Abstract
Identifying 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.