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Abstract:
Insect parasitoids can play ecologically important roles in virtually all terrestrial plant–insect herbivore interactions, yet
whether parasitoids alter the defensive traits that underlie interactions between plants and their herbivores remains a
largely unexplored question. Here, we examined the reciprocal trophic interactions among populations of the wild cabbage
Brassica oleracea that vary greatly in their production of defensive secondary compounds – glucosinolates (GSs), a generalist
herbivore, Trichoplusia ni, and its polyembryonic parasitoid Copidosoma floridanum. In a greenhouse environment, plants
were exposed to either healthy (unparasitized), parasitized, or no herbivores. Feeding damage by herbivores induced
higher levels of the indole GSs, glucobrassicin and neoglucobrassicin, but not any of the other measured GSs. Herbivores
parasitized by C. floridanum induced cabbage plants to produce 1.5 times more indole GSs than levels induced by healthy
T. ni and five times more than uninduced plants. As a gregarious endoparasitoid, C. floridanum causes its host T. ni to feed
more than unparasitized herbivores resulting in increased induction of indole GSs. In turn, herbivore fitness parameters
(including differential effects on male and female contributions to lifetime fecundity in the herbivore) were negatively
correlated with the aliphatic GSs, sinigrin and gluconapin, whereas parasitoid fitness parameters were negatively correlated
with the indole GSs, glucobrassicin and neoglucobrassicin. That herbivores and their parasitoids appear to be affected by
different sets of GSs was unexpected given the intimate developmental associations between host and parasitoid. This study
is the first to demonstrate that parasitoids, through increasing feeding by their herbivorous hosts, can induce higher levels
of non-volatile plant chemical defenses. While parasitoids are widely recognized to be ubiquitous in most terrestrial insect
herbivore communities, their role in influencing plant–insect herbivore relationships is still vastly underappreciated.