How does parasite environmental transmission stage concentration change before, during, and after disease outbreaks?

Outbreaks of environmentally transmitted parasites require that
susceptible hosts encounter transmission stages in the environment and
become infected, but we also know that transmission stages can be in the
environment without triggering disease outbreaks. One challenge for
understanding the relationship between environmental transmission stages
and disease outbreaks is that the distribution and abundance of
transmission stages outside of their hosts have been difficult to
quantify. Thus, we have limited data about how changes in transmission
stage abundance influence disease dynamics; moreover, we do not know
whether the relationship between transmission stages and outbreaks differs
among parasite species. We used digital PCR to quantify environmental
transmission stages of five parasites in six lakes in southeastern
Michigan every two weeks from June to November 2021. At the same time, we
quantified infection prevalence in hosts and host density. Our study
focused on eight zooplankton host species (Daphnia spp. and Ceriodaphnia
dubia) and five of their parasites from diverse taxonomic groups
(bacteria, yeast, microsporidia, and oomycete) with different infection
mechanisms. We found that parasite transmission stage concentration
increased prior to disease outbreaks for all parasites. However, parasites
differed significantly in the relative timing of peaks in transmission
stage concentration and infection outbreaks. The ‘continuous shedder’
parasites had transmission stage peaks at the same time as or slightly
after the outbreak peaks. In contrast, parasites relying on host death for
transmission (‘obligate killers’) had transmission stage peaks before
outbreak peaks. For most parasites, lakes with outbreaks had higher spore
concentrations than those without outbreaks, especially once an outbreak
began; the exception was for a parasite, Pasteuria ramosa, with very
strong genotypic specificity of infection. Overall, our results show that
disease outbreaks are tightly linked to transmission stage concentration;
outbreaks were preceded by increases in transmission stage concentration
in the environment and then were fueled by the production of more
transmission stages during the outbreak itself, with concentrations
decreasing to pre-outbreak levels as outbreaks waned. Thus, tracking
transmission stages in the environment improves our understanding of the
drivers of disease outbreaks and reveals how parasite traits may affect
these dynamics.