ENVIRONMENTAL AND ECOLOGICAL DRIVERS FOR SPILLOVER

Hendra virus spillovers can occur as single events, or in clusters in time and space (Eby et al. 2023). This was most striking in 2011, when there was an unprecedented super­cluster of 23 equine cases in a single 4-month period, primarily in south-east Qld and northern NSW (Eby et al.

2015). Since that time, 84% (16/19) of spillover events have been in subtropical regions, with three of the past five spillovers being in the Hunter-Newcastle region of NSW - each the most southerly recorded spillover event at the time (Williamson et al. 2020; Eby et al. 2022; Taylor et al. 2022; Biosecurity Queensland, 2023). The detection of HeV-g2 in Vic. and SA suggests that anywhere within the distribution of flying-foxes should be considered a risk for HeV spillover (Wang et al. 2021; Annand et al. 2022; Peel et al. 2022).

Numerous studies have explored the potential role of environmental and ecological drivers of HeV infection dynamics in flying-foxes and its transmission to horses. The most recent of these was a seminal study based on 25 yrs of data that tested hypotheses on the mechanisms linking climate, habitat degradation, flying-fox ecology, and Hendra virus spillover (Eby et al. 2023). The study identified that climate-driven food shortages and loss of critical winter-flowering flying-fox diet species are increasingly driving flying-foxes to move to and persist in agricultural and urban areas during winter.

This work builds off a range of earlier foundational studies on the drivers of HeV dynamics and spillover, which are summarised below under the broad categories of drivers of HeV excretion, drivers of virus survival in the environment, and drivers of flying-fox landscape uti­lisation and contact with horses.

Drivers of HeV excretion: The notable interannual, seasonal, and latitudinal variation in HeV prevalence has prompted research into nutritional and physiologi­cal drivers of excretion. While the direct associations between urinary cortisol concentration and HeV excre­tion are inconclusive, two studies detected statistical associations between cortisol concentration, season, and region (Edson et al. 2015a; McMichael et al. 2017). This led to hypotheses of an association between low winter temperatures and increased HeV infection, mediated by the physiological cost of thermoregulation. Individual- and population-level associations have been detected between HeV excretion and body condition, winter nutritional stress or climate-driven food shortages (Plowright et al. 2008; Edson et al. 2019; Becker et al. 2023). Yet others found no association between HeV RNA detection and haematological and biochemical biomarkers for nutritional stress, reproductive stress or extreme metabolic demand (McMichael et al.

Drivers of virus survival in the environment: Predic­tive models based on laboratory virus survival data (Fogarty et al. 2008), indicate that HeV survival in the environment is brief, but highly dependent on microcli­mates, which exhibit significant variability across loca­tion, season and time of excretion (Scanlan et al. 2014; Martin et al. 2015). The relationship between these microclimates and spillover events in these studies is inconclusive, and likely to be additionally influenced by in-paddock vegetation features such as grass length and canopy cover.

Drivers of flying-fox landscape utilisation and contact with horses: Across the distribution of known HeV spillo­ver events, multiple studies have identified that spillover risk increases with proximity to flying-foxes (McFarlane et al. 2011; Smith et al. 2014; Giles et al. 2018; Martin et al. 2018). More specifically, Smith et al. (2014) showed that this positive correlation was strongest when considering the density of occurrence records for black flying-fox and the paraphyletic spectacled flying-fox rather than the grey-headed flying-fox or the little red flying-fox. How­ever, these associations were independent of horse density (McFarlane et al. 2011; Smith et al. 2014). Clearly, the overlapping distribution of both flying-foxes and horses is a necessary condition for spillover, however there are likely additional unidentified risk factors at the property level, such as property attributes, husbandry and man­agement practices, and the occurrence of flying-fox diet species that impact the likelihood of flying-fox-horse interaction.

GPS tracking studies have allowed fine-scale assess­ment of landscape utilisation by black flying-foxes and horses (Field et al. 2016; Kessler et al. 2018) to gain new insight into equine exposure risk. In two winter-spring periods associated with high clusters of HeV spillovers (2011 and 2017), black flying-fox foraging was repeti­tious, over short distances, with individuals foraging in fragmented arboreal and agricultural landscape on non-native plant species, resulting in increased poten­tial contact with horses (Field et al. 2016; Kessler et al. 2018). By contrast, in a winter characterised by abun­dant native flowering and just one HeV spillover (2018) foraging distances were > 5-fold longer, dominated by native winter-flowering eucalypts in intact native for­ests (Kessler et al. 2018). A preliminary equine data logger study identified significant variation between diurnal and nocturnal grazing behaviour that, com­bined with the observed flying-fox foraging behaviour, could contribute to HeV exposure risk (Field et al.

2016).

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