Monarch butterflies as hosts of parasitoid wasps: Defense chemistry, host choice behaviors, and parasitism in the field
Despite the ecological and economic importance of plant-herbivore-parasitoid interactions, defining and predicting parasitoids’ host range remains a challenge. The tradeoffs hypothesis invokes the evolutionary difficulty of simultaneously adapting to uniquely defended resources to explain the high host specificity characteristic of most phytophagous and parasitoid insects. However, when empirically tested, many specialists perform well on atypical hosts, suggesting that narrow diet breadth does not necessarily tradeoff with physiological performance across hosts. Monarch larvae sequester cardenolides from milkweeds, which could, in turn, influence parasitoid performance. These toxins are effective against most would-be vertebrate predators, but their roles in interactions with invertebrate enemies remains poorly understood. We measured the performance of two parasitoids, Pteromalus cassotis and Pteromalus puparum by exposing pupae (monarch: high- and low-cardenolide diets, Pieris rapae: cardenolide-free) to single parasitoids and documenting resultant brood characteristics. P. cassotis is known to parasitize monarchs in nature while P. puparum has never been recorded from monarch hosts. We also studied host choice behaviors of P. cassotis when simultaneously presented two hosts of differing species. Finally, we used field experiments and field observations at several locations in the Eastern U.S to begin to describe the spatial and temporal patterns of this host-parasitoid relationship.
Non-toxic P. rapae were suitable hosts for both parasitoid species, while monarch hosts were suitable only for P. cassotis. The survival of P. cassotis individuals to adulthood was equivalent in both species, though brood size did not correspond linearly with host size across species. Within monarchs, the survival to adulthood and lifespan of P. cassotis individuals did not vary with host toxicity. Additionally, host toxicity had no effect on the survival of hosts, suggesting that this species interaction is unaffected by ecologically relevant concentrations of sequestered cardenolides. In two-host choice trials, P. cassotis females more frequently chose the D. plexippus host than P. rapae host (19/29 vs. 2/29). Together, these experimental data support the hypothesis that P. cassotis is a specialist on monarchs (and perhaps related species) due to behavioral preferences rather than physiological tradeoffs across hosts. Finally, field observations and experiments show that the prevalence of monarch parasitism by P. cassotis varies widely by location, season, and year. To date, parasitism of monarchs by P. cassotis has been documented in MN, WI, TX, GA, and OK. An apparent local extinction of P. cassotis has occurred in MN following very low monarch densities in 2012.