Host density increases parasite recruitment but decreases host risk in a snail-trematode system

TitleHost density increases parasite recruitment but decreases host risk in a snail-trematode system
Publication TypeJournal Article
Year of Publication2017
AuthorsBuck J.C, Hechinger R.F, Wood A.C, Stewart T.E, Kuris A.M, Lafferty K.D
JournalEcology
Volume98
Pagination2029-2038
Date Published2017/08
Type of ArticleArticle
ISBN Number0012-9658
Accession NumberWOS:000406759200005
KeywordsCarpinteria Salt Marsh; Cerithidea; Cerithideopsis californica; consequences; dilution; diversity; encounter-dilution; flatworm; group-size; horn snail; infection; inverse density dependence; metaanalysis; parasite; Platyhelminthes; population-dynamics; Protection; safety in numbers; selfish herd; trophic interactions
Abstract

Most species aggregate in local patches. High host density in patches increases contact rate between hosts and parasites, increasing parasite transmission success. At the same time, for environmentally transmitted parasites, high host density can decrease infection risk to individual hosts, because infective stages are divided among all hosts in a patch, leading to safety in numbers. We tested these predictions using the California horn snail, Cerithideopsis californica (=Cerithidea californica), which is the first intermediate host for at least 19 digenean trematode species in California estuaries. Snails become infected by ingesting trematode eggs or through penetration by free-swimming miracidia that hatch from trematode eggs deposited with final-host (bird or mammal) feces. This complex life cycle decouples infective-stage production from transmission, raising the possibility of an inverse relationship between host density and infection risk at local scales. In a field survey, higher snail density was associated with increased trematode (infected snail) density, but decreased trematode prevalence, consistent with either safety in numbers, parasitic castration, or both. To determine the extent to which safety in numbers drove the negative snail-density-trematode-prevalence association, we manipulated uninfected snail density in 83 cages at eight sites within Carpinteria Salt Marsh (California, USA). At each site, we quantified snail density and used data on final-host (bird and raccoon) distributions to control for between-site variation in infective-stage supply. After three months, overall trematode infections per cage increased with snail biomass density. For egg-transmitted trematodes, per-snail infection risk decreased with snail biomass density in the cage and surrounding area, whereas per-snail infection risk did not decrease for miracidium-transmitted trematodes. Furthermore, both trematode recruitment and infection risk increased with infective-stage input, but this was significant only for miracidium-transmitted species. A model parameterized with our experimental results and snail densities from 524 field transects estimated that safety in numbers, when combined with patchy host density, halved per capita infection risk in this snail population. We conclude that, depending on transmission mode, host density can enhance parasite recruitment and reduce per capita infection risk.

DOI10.1002/ecy.1905
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