Effects of elevated CO2 on environmentally-mediated immunity in a specialist herbivore

Background/Question/Methods: The host immune response is a central line of defense against infection and depends upon local abiotic and biotic conditions. Given the rapid rate of environmental change, understanding the importance of environmental context in determining the strength, activity and variability of the immune response has become increasingly important. Insect immunity is determined strongly by diet nutritional and phytochemical quality. Here, we investigate the influence of elevated CO₂ on the immune response of monarch caterpillars, Danaus plexippus, to infection by a sub-lethal, protozoan parasite, Ophryocystis elektroscirrha, and simulated parasitoid attack. Certain species of milkweed host plants with high concentrations of toxic steroids known as cardenolides protect monarchs from infection by the parasite and reduce the fitness costs of infection. Yet we know very little about how plant secondary metabolites and nutrient concentrations combine to influence the monarch’s immune response. To investigate the effects of phytochemistry on monarch immunity and determine how elevated CO₂ will alter this relationship, we fed monarchs two species of milkweed; A. curassavica (medicinal), and A. incarnata (non-medicinal); grown under ambient and elevated concentrations of CO₂. We then measured the monarch immune response, along with foliar chemistry, to understand the mechanisms underlying monarch immunity under future atmospheric conditions.

Results/Conclusions: The immune enzyme activity of early-instar monarchs declined in response to O. elektroscirrha infection by 25% when larvae were reared on milkweed grown under ambient CO₂ conditions but was “rescued” by consuming foliage grown under elevated CO₂ (F_1,134= 5.80, p=0.0174). Additionally, infection and a diet of foliage from elevated CO₂ increased the hemocyte concentrations of early-instar monarchs by 48% (F_1,107= 5.57, p=0.0201). The strength of the monarch immune response (total immune enzyme activity and hemocyte concentrations) increased with decreasing diet nutritional quality induced by elevated CO₂ (F_1,132=6.25, p=0.0136). This increased immune response despite reductions in the nutritional quality of plants could reflect differences in young host resource allocation. Conversely, the immune defense of late-instar monarchs showed no response to elevated CO­₂ but declined by 11% when monarchs were fed “medicinal” milkweed containing more lipophilic and diverse cardenolides (F_1,130=4.92, p=0.0283). These data suggest that monarchs may experience an ecological cost to feeding on toxic plant species in the form of increased vulnerability to parasitism. By improving our understanding of the host immune function as it depends on diet quality and environment, we can begin to make more powerful predictions about alterations in trophic cascades and emerging infectious diseases.