Time-delayed effects of climate variation on host-parasite dynamics

Parasites are ubiquitous, but widely neglected, components of food webs. Because of their trophic position, parasites may have major direct and indirect effects on community structure. Because the magnitude of these effects is likely to depend on parasite density, this study was undertaken to explore temporal patterns in the density of parasites and the processes responsible for those patterns. Parasitism by Howardula nematodes was monitored in four species of mycophagous Drosophila (D. falleni, D. neotestacea, D. putrida, and D. recens) that were sampled monthly from 1984 through 1998 near Rochester, New York, USA. Adult flies were collected by sweep netting over naturally occurring mushrooms or commercial Agaricus bisportis mushrooms that had been set out as baits. These adults were then dissected to determine whether they were parasitized by Howardula nematodes. The prevalence of parasitism varied substantially among species, being greatest in D. neotestacea (23.0% infected) and least in D. recens (4.8%). Parasitism was greatest in the spring and fall, and least in midsummer. Prevalence of parasitism covaried significantly through time among the three principal host species, D. falleni, D. neotestacea, and D. putrida, in part because the different species often breed in the same individual mushrooms, the site where nematode transmission from adult flies to larvae occurs. The mean prevalence of parasitism across these three species at the end of the season (September) was significantly correlated with the total precipitation from May through August. The mean prevalence of parasitism in the spring collections was significantly correlated with the mean prevalence the previous fall, because flies overwinter as adults. Consequently, the mean prevalence of parasitism in spring was highly correlated with May through August precipitation the previous year. It is hypothesized that rainfall, which stimulates the production of mushrooms (the flies' breeding sites), interacts with density-dependent nematode transmission to influence the prevalence of parasitism in these populations.