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Abstract
The transmission of parasites and pathogens among vertebrates often depends on host population size, host species diversity, and the extent of crowding among potential hosts, but little is known about how these variables apply to most vector-borne pathogens such as the arboviruses (arthropod-borne viruses). Buggy Creek virus (BCRV; Togaviridae: Alphavirus) is an RNA arbovirus transmitted by the swallow bug (Oeciacus vicarius) to the cliff swallow (Petrochelidon pyrrhonota) and the introduced house sparrow (Passer domesticus) that has recently invaded swallow nesting colonies. The virus has little impact on cliff swallows, but house sparrows are seriously affected by BCRV. For house sparrows occupying swallow nesting colonies in western Nebraska, USA, the prevalence of BCRV in nestling sparrows increased with sparrow colony size at a site but decreased with the number of cliff swallows present. If one nestling in a nest was infected with the virus, there was a greater likelihood that one or more of its nest-mates would also be infected than nestlings chosen at random. The closer a nest was to another nest containing infected nestlings, the greater the likelihood that some of the nestlings in the focal nest would be BCRV-positive. These results illustrate that BCRV represents a cost of coloniality for a vertebrate host (the house sparrow), perhaps the first such demonstration for an arbovirus, and that virus infection is spatially clustered within nests and within colonies. The decreased incidence of BCRV in sparrows as cliff swallows at a site increased reflects the “dilution effect,” in which virus transmission is reduced when a vector switches to feeding on a less competent vertebrate host.
Highlights
Two key variables in understanding the transmission of most parasites and pathogens are host population size and the extent of crowding among potential hosts
Sparrow colony size was inversely correlated with nest spacing and with average distance to the nearest infected nest within a colony: the mean distance between nests in a colony decreased as colony size increased (n = 14 colonies; rs = 20.89, p,0.0001), and the mean distance from a focal nest to the nearest one that contained a Buggy Creek virus (BCRV)-positive nestling decreased as colony size increased
The percentage of BCRV-positive swallow bug pools in a colony containing both cliff swallow and house sparrow nests was directly correlated with the percentage of BCRV-positive house sparrow nests in that colony (Figure 3)
Summary
Two key variables in understanding the transmission of most parasites and pathogens are host population size and the extent of crowding among potential hosts. Many viral pathogens are known to require minimum population sizes of viable (susceptible) hosts in order to persist in a local area [9,10,11,12]. Most of what we understand about the effects of population size and spacing on parasite or pathogen persistence comes from work on directly transmitted ectoparasites or viruses. Little is known about how vertebrate-host group size and spacing affects transmission of vector-borne pathogens [15,16]; in some of these, transmission may even be reduced in areas of high host density [7,17]
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