Long-lived butterfly parasites can’t take the heat

Debilitating parasite spores that infect monarch butterflies can persist for years at cool temperatures, but are knocked out by heat, according to a new study from researchers at the University of Georgia’s Center for the Ecology of Infectious Diseases.

Parasites can be transmitted between hosts through several ways, but environmental transmission is an important route for many insect parasites in particular. These parasites produce transmission stages that remain dormant in the environment, waiting for a susceptible host. During this time, these transmission stages must resist stressors like heat, ultraviolet radiation, and humidity, which could weaken their ability to infect a new host.

OE (short for Ophryocystis elektroscirrha) is one such environmentally transmitted parasite that infects monarch butterflies throughout their geographic range. Infected monarchs have reduced survival, shorter lives, lower reproductive success, and poorer flight ability compared to uninfected individuals. For transmission to occur from one monarch to another, larvae must consume infectious spores that were scattered onto eggs or milkweed leaves by infected butterflies.

Previous work by CEID member Sonia Altizer, the senior author of the study, has shown that the length of time that OE spores can persist in the environment plays an important role in determining infection levels in monarch populations. However, more research was needed to explore the upper limits of the parasite’s tolerance to heat and time. Said Altizer, “A growing number of studies are testing parasite responses to climate warming — from bacteria infecting corals to worms infecting Arctic wildlife — and showing that some parasites gain an advantage under warming temperatures, while others get clobbered by the heat. These detailed studies are essential for predicting future health impacts of climate change for natural ecosystems.”

Altizer and Jaap de Roode, a postdoctoral researcher at the time of the study, and now a faculty member at Emory University, designed a large-scale experiment to test the environmental persistence of OE spores. They exposed spores to one of four temperatures that ranged from the coolness of a typical refrigerator all the way to the heat of a summer day. The experimental temperatures corresponded to those experienced by monarch butterflies across their range. Spores were exposed for either a short (2 weeks), moderate (35 weeks), or long (93 weeks) time period.

The researchers then fed the parasite spores to monarch caterpillars, recorded whether the caterpillars were ultimately infected as adults, and measured their spore loads (to determine infection intensity).

CEID members Cecilia Sánchez and Isabella Ragonese led the data analysis and writing of the project. The team found that all of the parasites remained highly infective after two weeks, infecting around 95% of monarchs exposed, irrespective of temperature.

However, warmer temperatures dramatically reduced parasite infectivity and spore load at the longer time durations. Spores held over the moderate and long time periods exhibited steep decreases in their ability to infect caterpillars as temperature increased. At the two highest temperature treatments, spores held the longest duration were unable to infect any monarchs. Older spores also caused less intense infections, as measured by spore load.

Parasite genotypes collected from different source populations varied in their ability to tolerate warm temperatures. For example, spores from monarch populations in western North America and Florida seemed better able to tolerate higher temperatures. However, the researchers found that whether spores were sourced from migratory versus non-migratory monarch populations had no consistent effect on infection ability and spore load.

“It wasn’t surprising that the parasites best tolerated the cooler temperatures, because these roughly match the conditions at monarchs’ high-altitude overwintering sites,” said Sánchez, who is now a research scientist at EcoHealth Alliance. “However, we were a little shocked by how badly the spores survived under warmer temperatures, especially given that monarchs inhabit some very hot places like Florida and central California.”

The study’s results indicate that warming temperatures associated with climate change could reduce levels of monarch parasitism, if parasites die before they encounter a new host. However, because temperature change will likely affect other aspects of the butterfly-parasite interaction, such as monarch behavior and parasite development within monarchs, more research is needed to determine the future disease pressures monarch butterflies will face.

Sánchez et al. (2021). Thermal tolerance and environmental persistence of a protozoan parasite in monarch butterflies. Journal of Invertebrate Pathology. https://doi.org/10.1016/j.jip.2021.107544