Effects of arbuscular mycorrhizal fungi on plant-mediated interaction between the monarch butterfly and its protozoan parasite

Background/Question/Methods

Herbivore-parasite interactions have traditionally been studied as 2-way interactions; however, accumulating evidence has shown that they are also mediated by host plants of the herbivores. Specifically, plant nutritional and secondary chemical profiles can alter growth rate, biomass, immune defense and sequestration of the toxic chemicals in the herbivores, all of which can affect their interactions with parasites.

At the same time, variation in plant nutritional and secondary chemical traits are mediated by belowground associates of the plants, among which arbuscular mycorrhizal fungi (AMF) have been shown to be important determinants. However, it remains unexplored whether AMF can affect aboveground interactions between herbivores and their parasites.

We examined the effects of AMF on the interaction between the monarch butterfly (Danaus plexippus) and its protozoan parasite Ophryocystis elektroscirrha. Monarch caterpillars use milkweeds as their larval host plant, which contain cardenolides that can inhibit O. elektroscirrha. In the presence and absence of AMF, we measured adult lifespan and parasite spore load of butterflies reared across three milkweed host species, Asclepias verticillata, A. syriaca and A. latifolia. We also measured key plant traits to examine if effects of AMF can be explained by changes in plant quality.

Results/Conclusions

AMF significantly affected the interaction between the monarch butterfly and its parasite. There were significantly three-way interactions among parasitic infection, AMF inoculation and plant species on butterfly lifespan, suggesting that the effects of AMF on caterpillar-parasite interactions varied among plant species. Specifically, when feeding on A. verticilata and A. latifolia in the presence of AMF, infected monarchs lived longer than those fed on plants without AMF. In contrast, when reared on A. syriaca, infected butterflies lived shorter with AMF inoculation. AMF also had significant effects on spore loads of the parasites. Across all three plant species, AMF inoculation reduced spore load on infected monarchs.  

The analysis of foliar cardenolides, however, did not exhibit clear relationships between AMF inoculation and foliar cardenolide concentration or composition in any of the plant species. Although AMF reduced cardenolide nonpolarity across the species, there was no relationship between cardenolide nonpolarity and monarch lifespan or spore load, suggesting that the indirect effects of AMF on the monarch -parasite relationship were through plant traits other than secondary chemistry.