Changing resource landscapes and spillover of henipaviruses

Abstract

Old World fruit bats (Chiroptera: Pteropodidae) provide critical pollination and seed dispersal services to forest ecosystems across Africa, Asia, and Australia. In each of these regions, pteropodids have been identified as natural reservoir hosts for henipaviruses. The genus Henipavirus includes Hendra virus and Nipah virus, which regularly spill over from bats to domestic animals and humans in Australia and Asia, and a suite of largely uncharacterized African henipaviruses. Rapid change in fruit bat habitat and associated shifts in their ecology and behavior are well documented, with evidence suggesting that altered diet, roosting habitat, and movement behaviors are increasing spillover risk of bat-borne viruses. We review the ways that changing resource landscapes affect the processes that culminate in cross-species transmission of henipaviruses, from reservoir host density and distribution to within-host immunity and recipient host exposure. We evaluate existing evidence and highlight gaps in knowledge that are limiting our understanding of the ecological drivers of henipavirus spillover. When considering spillover in the context of land-use change, we emphasize that it is especially important to disentangle the effects of habitat loss and resource provisioning on these processes, and to jointly consider changes in resource abundance, quality, and composition.

Keywords: habitat loss; henipavirus; land-use change; resource provisioning; spillover.

Figure 1.

Distribution of henipaviruses and their reservoir hosts. Data on the distribution of pteropodid bats (Chiroptera: Pteropodidae) and flying foxes (Pteropodidae: Pteropus) was generated from the IUCN Red List of Threatened Species. Data on evidence of HNVs in fruit bats and other animals (green) are compiled from the studies that isolated live virus or detected viral RNA from HNVs or HNV-like virus in bats or their excrement, or detected circulating antibodies against HNVs in bats. Data on HNV spillover to domestic animals (blue and purple outlines) or humans (red, orange, yellow) were compiled from government outbreak reports, primary literature, and unpublished data. Study locations reporting evidence of HNVs in animals or humans were mapped to the government unit (state, province, etc.) encompassing those locations. In Australia, this range is further restricted within states by the distribution of flying foxes. With the exception of the Philippines, all areas reporting evidence of HNV spillover or infection in humans also report evidence of HNVs in pteropodid bats. Where known, exact spillover locations are reported (black pins). This map highlights how little data is available on the true distribution of HNVs and their zoonotic potential (for map data see Refs. ,,,,,,,,–188)

Figure 2.

Potential causal pathway between land-use change and spillover. Land-use change includes the cumulative effects of habitat loss and resource provisioning. Reduction in the numbers and size of habitat patches (i.e., habitat loss) and planting of introduced species for landscaping and agriculture (i.e., resource provisioning) change the distribution, abundance, quality, and diversity of available resources, and may create a landscape with restricted and inferior available resources. If altered resource landscapes change key population and individual level factors, a cascade of negative consequences change the density and distribution of bats, prevalence and intensity of infection, shedding from infected bats, and environmental survival of the virus in ways that increase risk of spillover host exposure.