1. Many host–parasite interaction dynamics show distinct seasonality. Parasite population growth and invasion success are generally explained by host density dependence, while the direct influence of environmental factors on parasite life history traits has been underreported.
2. In waterbodies, resource availability and environmental conditions change with season (temperature, irradiance and rainfall patterns) and with depth (light, temperature and chemical gradients). Hence, hosts and parasites live in a spatially and temporally variable environment. Such environmental variation leads to structured populations, which in turn have implications for host–parasite interaction dynamics. Nevertheless, time-series data on the vertical distribution of aquatic hosts and their parasites are rare.
3. We present a dataset spanning 1.5 years (2008–2010) of weekly sampling in Lake Maarsseveen (the Netherlands) focussing on the dynamics of the diatom Asterionella formosa and its parasite, the chytrid Zygorhizidium planktonicum, at four depths. Environmental variables measured included ice cover, temperature, global irradiance, light extinction, pH, soluble reactive silicate (SRSi), dissolved nitrate and ortho-phosphate.
4. We observed four host blooms, two in early spring and one each in summer and autumn. Each host bloom was followed by a time-lagged parasite epidemic. Blooms and epidemics started in the uppermost water layers and showed a time lag in onset date with increasing depth.
5. Host abundance was related to SRSi, global irradiance, Schmidt stability and parasite abundance in the upper 10 m, whereas at 15 m only a relationship with parasite abundance prevailed. Parasite abundance was related to host abundance, light extinction, temperature, SRSi, stability and global irradiance within the upper 10 m; again, at 15 m, parasite abundance correlated only with host abundance and disease prevalence.
6. Host vertical distribution was less aggregated during isothermal conditions than during thermal stratification, when host abundance was higher in the mixed, photic epilimnion and lower in the dark, colder hypolimnion. Parasite vertical distribution was patchy most of the year. Parasite epidemics seemed to reduce host vertical patchiness as they impacted higher density patches in the photic zone more strongly, a result of both higher host abundance and favourable environmental conditions for the parasite.
7. Seasonal variability and vertical gradients in biotic and abiotic factors expose host and parasite individuals to different environmental conditions even within a single population. Environmental variability affects parasite transmission rates through changes in host abundance and through changes in the strength and outcome of host–parasite interactions.