Parasite persistence in the environment drives infection dynamics for a butterfly host
Environmentally transmitted parasites are common and include many pathogens of human and wildlife health concern. Successful environmental transmission requires a free-living stage that can persist under variable climatic conditions for long enough to infect a host. Understanding how environmental exposure affects parasite longevity and building free-living parasite stages into mechanistic models of disease spread are key to predicting pathogen invasion, persistence, and control. Here, we explored consequences of environmental transmission on infection outcomes for a protozoan parasite (Ophryocystis elektroscirrha, or OE) that infects monarch butterflies. We first constructed a transmission model for monarch-OE dynamics within a milkweed patch, to examine how parasite persistence in the environment influences prevalence and host population size throughout the breeding season. We also assessed how the rate at which parasites are shed rate into the environment (from infected adults to milkweed leaves) affects disease dynamics. To inform the model, we designed an experiment to measure parasite longevity in field conditions under two environmental treatments (full sun versus partial shade) – providing the first estimates of OE spore persistence in natural rather than laboratory conditions.
Our model indicated that there is a threshold for environmental persistence above which the pathogen can invade, infection prevalence can increase, and host population size can decrease monotonically. Using parameter values consistent with wild monarchs in eastern North America, we show that OE parasites must persist for at least 20 days in order for end-of-season infection prevalence to match observed field prevalence of 6-20%. Consistent with this finding, our experiment showed that most parasite doses remained infectious even after 16 days in the natural environment. While infectivity of experimental parasite doses did not change over time, the severity of infection (measured as parasite load per infected monarch) caused by the environmentally exposed parasites decreased over 2 weeks; the decrease was particularly striking among parasites exposed to sun, rather than shade, conditions. Our model also highlighted that infection prevalence is limited by parasite shedding rate, a process that depends on infected monarchs in the summer-breeding range locating milkweed plants on which to lay eggs (and transfer parasite spores). As milkweed habitats shrink and the monarch population continues to decline in North America, our model may be useful in predicting future dynamics for monarchs and their debilitating protozoan parasite.