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

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.

Negative density-dependent parasitism in a group-living carnivore

“…We note two potential sources of negative density dependence untested by our modelling approach: the encounter-dilution effect [77,78] and micronutrient impacts on immunity [79].…”

Assessing the direct and indirect effects of food provisioning and nutrient enrichment on wildlife infectious disease dynamics

“…For example, there is strong theoretical and empirical support for increased measles transmission and persistence in dense human populations [34,35]. However, weak, nonlinear or absent relationships between host population size and transmission rates (or prevalence) are common in wildlife populations because host-parasite contact rates can saturate or even decline at high host densities [19,[36][37][38]. These relationships may arise for several reasons.…”

Large scale patterns of trematode parasite communities infecting Cerastoderma edule along the Atlantic coast from Portugal to Morocco

“…Similarly, Thieltges and Reise (2007) demonstrated higher metacercariae abundance (the trematode parasitic stage occurring in the second intermediate host) positively correlated to an increase in abundance and diversity of the higher trophic level host communities. On the other hand, higher host density can also promote a dilution effect and therefore decrease the parasite burden in a specific host (Buck et al, 2017;Magalhães et al, 2016;Mouritsen et al, 2003). Concerning the abiotic environmental factors, different conditions of temperature (Achiorno and Martolrelli, 2016;de Montaudouin et al, 2016a), salinity and pH (Koprivnikar et al, 2010(Koprivnikar et al, , 2014Mouritsen, 2002;, among others, can also have an influence on trematode dynamics (Wilson et al, 2002).…”