The effects of elevated atmospheric CO2 concentration on a parasite of monarch butterflies

Background/Question/Methods: Changing environmental conditions strongly alter host-parasite interactions by influencing both parasite replication and host resistance. The effects of global change should be particularly apparent in herbivore host-parasite interactions, as food-plant quality is plastic with respect to environmental conditions and herbivore performance is tightly linked to food resources. Previous work has demonstrated that host plant chemistry influences the performance of a protozoan parasite in its interaction with monarch butterflies. Monarch larvae that feed on milkweed plants with higher concentrations of cardenolides (toxic secondary metabolites) suffer lower rates of infection, maintain higher fitness, and produce fewer new parasites. Critically, elevated concentrations of atmospheric CO₂ (eCO₂) cause changes in both cardenolide concentrations and cardenolide identities in two species of milkweed. Together, these data motivate the general question of our study: will the virulence (decline in monarch lifespan) and transmission potential (butterfly spore load) of the monarch parasite change as atmospheric CO₂ concentrations continue to increase? I grew four species of Asclepias under eCO₂ to explore the generality of changes in the cardenolide compounds produced. Tissue from these plants was then fed to infected and uninfected monarchs to examine the effects of eCO₂-induced changes in phytochemistry on monarch lifespan and infected butterfly spore load. 

Results/Conclusions: Elevated CO₂ caused general declines in the cardenolide concentrations of milkweed, but also induced a shift in the composition of the cardenolides to more toxic forms. Overall, the number of spores produced by infected adult butterflies was lower when they fed on milkweed grown under eCO₂. Our data suggest that the production of more lipophilic cardenolides under eCO₂ reduced the spore load of butterflies and therefore the transmission potential of the parasite. Despite these declines in spore load, there were no positive effects of eCO₂ on the lifespan of infected monarchs. Together, these results suggest that eCO₂ can decouple the typical relationship between parasite spore load and adult monarch longevity. We predict that this decoupling may result from declining plant nutritional quality that occurs in conjunction with increasing plant medicinal quality induced by eCO₂. Therefore, an exploration of the mechanism by which both primary and secondary metabolites interact in this host-parasite system is necessary to better predict future interaction outcomes under global change scenarios.