The spitting image of plant defenses: effects of plant secondary chemistry on the efficiency of caterpillar regurgitant as an anti-predator defense

Authors: DESURMONT, GAYLORD - European Biological Control Laboratory (EBCL); KHOLER, ANGELA - Neuchatel University - Switzerland; MAAG, DANIEL - Neuchatel University - Switzerland; LAPLANCHE, DIANE - Neuchatel University - Switzerland; XU, HAO - Neuchatel University - Switzerland; BAUMANN, JULIEN - Neuchatel University - Switzerland; DEMAIRE, CAMILLE - Neuchatel University - Switzerland; DEVENOGES, DELPHINE - Neuchatel University - Switzerland; GLAVAN, MARA - Neuchatel University - Switzerland; MANN, LESLIE - Neuchatel University - Switzerland; TURLINGS, TED - Neuchatel University - Switzerland

Submitted to: Journal of Chemical Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/16/2017
Publication Date: 7/5/2017
Citation: Desurmont, G., Kholer, A., Maag, D., Laplanche, D., Xu, H., Baumann, J., Demaire, C., Devenoges, D., Glavan, M., Mann, L., Turlings, T.C. 2017. The spitting image of plant defenses: effects of plant secondary chemistry on the efficiency of caterpillar regurgitant as an anti-predator defense. Journal of Chemical Ecology. DOI 10.1002/ece3.3174.

Interpretive Summary: The use of insect natural enemies to control plant pests is an important component of sustainable production of crops. Understanding the interactions between plants, insects that feed on the plants, and natural enemies (predators and parasites) that control the insect pests is important for managing effective biological control strategies. It is known that caterpillars of many different species defend themselves by spitting on their predators and parasitic wasps. Many caterpillars are also known to use the toxins from the plants they consume as a defense. However it is not known if plant toxins directly impact the efficacy of the spit. Here we studied the cabbageworm Pieris brassicae and the efficacy of its spit against its natural enemy, the parasitic wasp Cotesia glomerata. We tested caterpillars feeding on 10 different plant species and varieties which contained different amounts of toxins. Our results showed that the the amount and type of toxins contained in the plant did not affect efficacy of the spit, but that there were some differences among the plant species. The spit from caterpillars feeding on radish was more effective than from caterpillars feeding on cabbage or other crucifers. The active ingredient of caterpillar spit is still unknown. This study helps us better understand the interactions between insect pests and their natural enemies in nature, for example suggesting that this parasitoid may be less effective on radish than on other crops in the mustard family.

Technical Abstract: In the arms race between plants, herbivores, and their natural enemies, specialized herbivores may use plant defenses for their own benefit. In such cases, variation in secondary chemistry among host plants may affect the benefits that herbivores derive from these defenses. Caterpillars of Pieris brassicae, a specialized herbivore of glucosinolate-containing plants, are known to actively spit on attacking natural enemies, including their main parasitoid, the braconid wasp Cotesia glomerata. Here we tested the hypothesis that variation in the secondary metabolites of their host plants affects the efficiency of caterpillar regurgitant as an anti-predator defense. We studied natural regurgitation events of caterpillars on parasitoids using a total of 10 host plants with different glucosinolate profiles. We then studied manual applications of water or regurgitant on parasitoids during parasitization events. Results revealed that parasitoids spent more time grooming after exposure to spit when foraging on radish and nasturtium than on Brassica spp., and when the regurgitant came in contact with the wings rather than any other body part. All parameters of parasitoid behavior (initial attack duration, attack interruption, grooming time, and likelihood of a second attack) were more strongly affected when regurgitant was applied rather than water. The proportion of parasitoids re-attacking a caterpillar within 15 minutes was the lowest when regurgitant originated from radish-fed caterpillars. However, we found no correlation between glucosinolate content and regurgitant effects, and parasitoid behavior was equally affected when regurgitant originated from a glucosinolate-deficient Arabidopsis thaliana mutant line. In conclusion, host plant species affects to a certain extent the efficiency of spit from P. brassicae caterpillars as a defense against parasitoids, but this is not due to glucosinolate content. The ecological relevance of this anti-predator defense remains to be explored in the field.