Differential sources of host species heterogeneity influence the transmission and control of multihost parasites

Abstract

Controlling parasites that infect multiple host species often requires targeting single species that dominate transmission. Yet, it is rarely recognised that such 'key hosts' can arise through disparate mechanisms, potentially requiring different approaches for control. We identify three distinct, but not mutually exclusive, processes that underlie host species heterogeneity: infection prevalence, population abundance and infectiousness. We construct a theoretical framework to isolate the role of each process from ecological data and to explore the outcome of different control approaches. Applying this framework to data on 11 gastrointestinal parasites in small mammal communities across the eastern United States reveals variation not only in the magnitude of transmission asymmetries among host species but also in the processes driving heterogeneity. These differences influence the efficiency by which different control strategies reduce transmission. Identifying and tailoring interventions to a specific type of key host may therefore enable more effective management of multihost parasites.

Keywords: Coccidia; community epidemiology; helminth; management; parasitism; species heterogeneity; super-shedder; susceptibility.

Figure 1

Efficacy of control by (a) untargeted, with respect to infection status, and (b) targeted (of infecteds) removal of C_i individuals of key host species i. The efficacy of control is quantified by the proportional reduction in overall contribution to the parasite's transmission pool, ξ^U and ξ^T for untargeted and targeted control respectively (eqns e and 3). In each scenario, the host species is assumed to be responsible for 80% of the total contribution to the parasite's infectious pool, and is either a pure super-abundant host (,; black line), a pure super-infected host (,; red line) or a pure super-shedding host (,; green line). The dashed line represents the maximum reduction in transmission possible by treating only the key host (i.e. the proportion of transmission that is due to the other non-host species). For visualisation, the red lines (super-infecteds) are offset to avoid overlap with super-shedder (panel a) and super-abundant (panel b) key hosts.

Figure 2

Map of field sites in the eastern United States. The number of grids trapped is indicated in parentheses. Pie charts display the host species composition of each site, with pie diameters proportional to the total number of animals captured (range: 35–130).

Figure 3

Contributions of three sources of host heterogeneity for 11 multihost parasites. Symbol sizes are proportional to the total contribution of infective stages produced by each host species. Squares indicate the key host species (π_i > 0.5) for each parasite. Pairwise plots of each source of host heterogeneity are shown in Figs S3–S5.

Figure 4

Efficacy of three control strategies for empirical multihost parasites. Each panel shows the expected reduction in the infectious pool size by random removal of individuals regardless of host species (green) and by targeted (blue) and untargeted (red) removal of the most influential host species (shown in the title of each panel). The dashed line shows the maximum reduction that can be achieved by removing all individuals of the key host species (i.e. the proportion of transmission due to non-key host species). The slopes of targeted, untargeted and random lines are given by the following equations: , and respectively. The J’ values are Pielou's evenness index and quantify the degree of variability across the host community in contributions to parasite transmission; values of J’ lie between 0 (complete dominance by a single species) and 1 (equal contributions of all infected host species).