EFFECTS OF CHANGING HABITATS ON BAT-VIRUS DYNAMICS

This blog post is provided by Tamika Lunn, Alison Peel, Hamish McCallum, Peggy Eby, Maureen Kessler, Raina Plowright and Olivier Restif, and tells the #StoryBehindThePaper for their article “Spatial dynamics of pathogen transmission in communally roosting species: impacts of changing habitats on bat-virus dynamics”, which was recently published in the Journal of Animal Ecology.

A flying-fox hangs from a eucalypt branch, nodding in and out of sleep as her neighbour fans its wings in a steady, soft beat. It’s a fine winter day, but she can feel the heat of the sun overhead, and its radiation rising from the asphalt of the road beneath. She jolts awake to squabble with her neighbour – it has gotten too close to her roosting space. Unsettled now, she flips herself upside-down so that just her thumbs are gripping onto the branch and her legs dangle over the foliage below. She relieves herself, hearing screams of protest from the flying-foxes below as her stream of urine falls narrowly past. She shakes herself and returns to her hanging position. Looking across the greenspace she sees more bat-filled eucalypt trees, but the trees are few in comparison to the expanses of forest where they used to live. It was not so long ago they would all roam across the country, following bursts of flowering so sweet and plentiful that she could fly sustained for days. She does not have the energy, or incentive, for those long-distance flights anymore. Instead, she and her neighbours return day-after-day to the same crowded roost in metropolitan Queensland, lethargic from the sickly but predictable fruits available here. She starts to doze again. As she drifts back to sleep, she dreams she is soaring above an endless sea of shimmering forest, the taste of pollen hanging sweet in the air.

Flying-foxes (Pteropus spp.) (Photo credit: Peter Hudson/Pennsylvania State University)
Flying-foxes and urbanisation

Flying-foxes evolved to be nomadic in Australia. They would feed on nectar from flowering native forests and hop between roosts like travellers backpacking across Europe. Wide-spread land clearing in eastern Australia – involving the clearance or degradation of >40% of all forest and >80% of Eucalyptus-dominated forests since European colonisation – has restricted food availability for flying-foxes. They are increasingly choosing to subsist on food in human-dominated environments, which are suboptimal but available year-around. Some of these urban bats forgo migration, and split their population into many small, but cramped, roosts close to their introduced food sources to reduce the energetic cost of feeding. The shift of bats into urban and peri-urban areas can have a cascade of negative events, including reduced health of bats, nuisance to human communities, and Hendra virus spillover to horses and successively humans.

Flying-fox roosting in urban space (Photo credit: Elizabeth Shanahan/Montana State University)
Human pressures and zoonotic spillover

Zoonotic diseases are caused by pathogens that originate in animals. When a pathogen is transmitted from an animal reservoir host to another host this is called zoonotic ‘spillover’.

Australian flying-foxes are reservoir hosts of a zoonotic pathogen called Hendra virus. This causes lethal disease in horses and humans, with a fatality rate approaching 90% and 60%, respectively. Flying-foxes release (‘shed’) the pathogen in their urine. Transmission between bats happens through contact with infectious urine, and occurs within roosts through a combination of close contacts with neighbouring bats, contact with urine through the vertical tree column (i.e., being urinated on by bats roosting above), or exposure to small clouds of aerosolised urine. Prevalence of infection in bats is highest in winter.

How does this relate to the urbanisation of flying-foxes in Australia? Human driven land-use change is a major driver of zoonotic pathogen spillover from wildlife. This can operate in four key ways to drive disease emergence and rate of spillover: it can (1) impact the abundance and distribution of wildlife; (2) shape patterns of exposure and susceptibility in wildlife; (3) drive pathogen shedding from wildlife; and (4) create novel contact opportunities between different species. The exact drivers of Hendra virus spread and spillover remain unresolved, but recent spillover cases align with ecological shifts in flying-fox populations. It is likely that urbanisation in this system has impacted all four processes in interacting ways.

Disturbed flying-foxes taking flight (Photo credit: Adrienne Dale/Texas Tech University)
Paper in focus

We wanted to know how change in population structure could influence spread of infection and risk of spillover. This encompasses points (1) and (2) from above: impacts from changed distributions of wildlife and impacts from altered patterns of exposure.

We built spatial models of flying-fox movements within roosts, mimicking the structure of real roosts in Australia. We then simulated the transmission of Hendra virus among bats and measured how fast virtual epidemics spread across different roost types. We showed that roosts with fewer trees and more bats per tree experienced larger and faster epidemics. These sparse roost types are frequently seen in urban environments, as greenspaces have fewer trees available for flying-foxes to roost in, and as a result, hold more bats per tree. This may flag increased spillover risk from these multiplying roost types and will be important for forecasting disease risk across Australia.

Most importantly, this gives compelling evidence that spatial structure and flying-fox aggregation may be a missing piece to understanding patterns in shedding intensity and spillover risk from flying-fox roosts across eastern Australia.

How to prevent zoonotic spillover

Results like these can be used to generate fear of our native wildlife and create pressure to cull or disperse human-associated bats. Such interventions are reactive, short-lived, and can introduce further complications – for example, culling and dispersal of bats can actually increase the risk of disease spillover by causing additional stress to bats and changing movement and contact patterns, making it easier for viruses to multiply and spread.

Preserving ecosystems and restoring natural habitats (termed ‘ecological interventions’) are the preferred alternatives. This ensures animals do not need to forage near where humans live, so stopping spillover before it happens. The BatOneHealth global research team have initiated a landscape restoration project in Australia, to target spillover at its source by reviving ecosystem processes that are natural barriers to spillover. Find out more on our website https://batonehealth.org/

Read the paper

Read the full paper here: Lunn, T.J, Peel, A.J., McCallum, H., Eby, P., Kessler, M., Plowright, R.K. and Restif, O (2021). Spatial dynamics of pathogen transmission in communally roosting species: impacts of changing habitats on bat-virus dynamics. J Anim Ecol. Available at: https://doi.org/10.1111/1365-2656.13566

Flying-fox (Pteropus poliocephalus) hanging while sleeping (Photo credit: Tamika Lunn/Griffith University)
About the authors

Tamika Lunn was a PhD student and Endeavour Fellow during the preparation of this manuscript. She was one of four Australians to receive an Endeavour Postgraduate Scholarship in the final cohort of the Endeavour Leadership Program, which allowed her to travel to Cambridge for nine months under the supervision of Olivier Restif (Senior Lecturer in epidemiology at the University of Cambridge) to learn the mathematical modelling and scientific programming for this research. She has since completed her PhD at Griffith University in 2021 and is currently a postdoc at the University of Arkansas studying the ecology of bats and Bombali ebolavirus in East Africa, alongside Kristian Forbes and Olivier Restif. Maureen Kessler was also a PhD student during the data collection stage of this manuscript and will soon be submitting her own thesis at Montana State University. Alison Peel is a DECRA Research Fellow at Griffith University and was co-primary supervisor of Tamika Lunn during her PhD. Hamish McCallum, the second co-primary supervisor, is a Professor and Director of the Centre for Planetary Health and Food Security at Griffith University. Peggy Eby (adjunct bat ecologist with Griffith University and University of New South Wales) is our go-to bat expert, having over 25 years of involvement with flying-fox conservation and management-based research. Raina Plowright is an Associate Professor at Montana State University. This research was conducted in collaboration with the BatOneHealth global research team.

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