Changes in the environment within which hosts and parasites interact can impact disease dynamics. Both host tolerance, the ability to mitigate the fitness costs of infection at a given pathogen load, and parasite virulence, the parasite-induced reduction in host fitness, can vary with the quality of host diet. Global change has direct effects on plant physiology which manifest themselves as changes in host-plant nutritional quality and defensive chemistry. The interaction between the monarch butterfly, Danaus plexippus, and its protozoan parasite, Ophryocystis elektroscirrha (OE) depends heavily on host plant chemistry. Monarch larvae that feed on milkweed plants with higher concentrations of cardenolides (toxic secondary metabolites) suffer lower rates of infection, and maintain higher fitness. Critically, elevated atmospheric CO2 (eCO2) causes changes in both cardenolide concentrations and the nutritional quality of milkweed. Together, these data motivate the question of our study: will the tolerance of monarchs and the virulence of OE change as atmospheric CO2 concentrations continue to increase? We grew four species of Asclepias under eCO2 to explore the changes in phytochemistry. 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.
Elevated CO2 reduced the effectiveness of medicinal milkweeds against monarch parasites. Specifically, monarch tolerance to OE declined under eCO2 in those monarchs reared on the highest cardenolide (most medicinal) milkweed, A. curassavica, while tolerance remained unchanged on the lower cardenolide species. Moreover, the virulence of OE increased under eCO2 in monarchs reared on A. curassavica, and remained unchanged on the lower cardenolide milkweeds. Importantly, elevated CO2 caused declines in the cardenolide concentration of A. curassavica, but had no effect on cardenolides in the other three species.
Together, these results suggest that eCO2 causes declines in monarch tolerance to infection and increases in parasite virulence on once-medicinal milkweed species by reducing cardenolide concentrations. We suggest that this increase in parasite impact under eCO2 may also result from declining plant nutritional quality that occurs in conjunction with a loss of plant medicinal quality. While elevated CO2 can lead to a reduction in milkweed cardenolide concentrations, our data suggest that the most toxic forms of cardenolides in A. curassavica remain active under eCO2. Nutrient starvation may increase the per unit toxicity of secondary metabolites, which may compromise host tolerance and increase parasite virulence.