Redundancy between belowground direct and indirect defenses in common milkweed A. syriaca

Background/Question/Methods Upon herbivore attack, plants rely on a matrix-like type of responses, generally involving direct and indirect defenses. Direct defenses can act by physical or chemical means, via toxic or antinutritive effects; indirect defenses typically act by providing rewards or cues for predators or parasitoids to locate their host herbivores (e.g., volatile organic compounds or extrafloral nectar). Belowground, the release of terpenoid volatiles in the soil has been shown to attract entomopathogenic nematodes foraging for herbivorous insect larvae. In the milkweeds (Asclepias spp.), plants are predominantly defended in the shoots by the production of cardenolides and latex, whereas belowground mainly by cardenolides.  Despite the fact that larvae of the specialist beetle Tetraopes tetraophthalmus are major herbivores of Asclepias syriaca, little was previously known about root defenses in the common milkweed.  In common garden experiments, we tested whether insect damaged A. syriaca roots attract more nematodes than undamaged plants. We then analyzed volatile organic compounds from roots of damaged and undamaged plants. Finally, by screening and selecting milkweed genotypes for high and low root cardenolides, we examined the relationship between allocation to cardenolides and indirect defense in the roots.
Results/Conclusions

Results show that entomopathogenic nematodes (Heterorhabditis bacteriophora) are extremely efficient in killing beetle larvae, and that attacked plants are more attractive than healthy plants.  We also found higher level of volatiles emitting from damaged roots. Field results show that T. tetraophthalmus larvae survive better on low cardenolide genotypes of A. syriaca compared to high cardenolide genotypes, but the presence of nematodes in the soil reduces larval survival to similar levels in both high and low cardenolides genotypes. Thus, we conclude that direct and indirect defenses act redundantly in A. syriaca roots to reduce the impact of a specialist herbivore in the field.