Counterintuitive scaling between population abundance and local density: Implications for modelling transmission of infectious diseases in bat populations

Abstract

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 heterogeneous, underpinned by ecological processes across different scales, complicating assumptions regarding the nature of contacts and transmission. 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 tree‐roosting Pteropus spp. from 2,522 spatially referenced trees across eight roosts to empirically evaluate the relationship between total roost abundance and tree‐level measures of abundance and density—the scale most likely to be relevant for virus transmission. We also evaluate whether roost features at different scales (roost level, subplot level, tree level) are predictive of these local density dynamics. Roost‐level features were not representative of tree‐level abundance (bats per tree) or tree‐level density (bats per m2 or m3), with roost‐level models explaining minimal variation in tree‐level measures. Total roost abundance itself was either not a significant predictor (tree‐level 3D density) or only weakly predictive (tree‐level abundance). This indicates that basic measures, such as total abundance of bats in a roost, 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 strongest 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 total abundance and local density. 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.

Ecological conditions predict the intensity of Hendra virus excretion over space and time from bat reservoir hosts

“…Spatiotemporal sampling is especially critical in the study of infectious disease (Becker, Crowley, et al, 2019; Plowright et al, 2019), because pathogen shedding and transmission are both inherently spatial and temporal processes (Grenfell et al, 2001; Lunn et al, 2021). Connecting such data with changing ecology of wildlife further requires studies of abiotic and biotic correlates and host behaviour and demography at similar or biologically meaningful spatial and temporal scales (Becker, Washburne, et al, 2019; Lunn et al, 2021; Ostfeld et al, 2006). Here, the ecological conditions that predict HeV shedding from flying foxes were derived from data collected over approximately 25 years and from diverse sources (Eby & Law, 2008; Eby et al, 1999; Lunn et al, 2021) (Eby et al, 2022a).…”

Density dependence and disease dynamics: moving towards a predictive framework

“…Importantly, it is often expected that increasing population size will increase density, but size and density can scale idiosyncratically (e.g. (Lunn et al 2021)), so this is not necessarily true.…”

Spatial scaling of gregarious host populations and nonlinearities in infectious disease transmission

“…We now have the tools to address these complexities and modelling the dynamics of transmission has become a sophisticated exercise of technical capabilities. However, as Lunn, Peel, Eby, et al (2021) stress, it is also critical to identify both the ecological scale that is representative of the transmission process and the host population unit that is biologically meaningful for these processes.…”