Behavioral and chemical mechanisms of plant-mediated deterrence and attraction among frugivorous insects

Authors: ZEILINGER, ADAM - University Of Minnesota; Olson, Dawn; MACLEAN, DANIEL - Agrofresh, Inc; MORI, N - Kyoto University; NAKATA, R - Kyoto University; ANDOW, DAVID - University Of Minnesota

Submitted to: Ecological Entomology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/18/2015
Publication Date: 7/1/2015
Citation: Zeilinger, A., Olson, D.M., Maclean, D., Mori, N., Nakata, R., Andow, D.A. 2015. Behavioral and chemical mechanisms of plant-mediated deterrence and attraction among frugivorous insects. Ecological Entomology. 40: 532-542. https://doi.org/10.1111/een.12221.
DOI: https://doi.org/10.1111/een.12221

Interpretive Summary: Herbivory often induces systemic plant resistance traits that affect subsequent herbivores in species-specific ways, with much of this focusing on herbivory on vegetative plant tissues. We sought to investigate interactions between herbivores mediated through fruit feeding, through detailed studies of feeding preference by subsequent fruit feeders. We investigated interactions between two herbivorous stink bug species Nezara viridula and Euschistus servus [Heteroptera: Pentatomidae] and two heliothine species Helicoverpa zea and Heliothis virescens [Lepidoptera: Noctuidae] on cotton plants, Gossypium hirsutum. First, we used measures of stink bug movement to investigate if selection behavior, acceptance behavior, or both, determine feeding preference of stink bugs for heliothine-damaged and undamaged plants. Second, we measured stink bug consumption to test if stink bug preference was related to the edibility of the host plant choices. Finally, we measured systemic induction by heliothines of phenolic-based secondary compounds in developing cotton bolls. We found species-specific changes in feeding preference by the stink bug species: competitive interactions occurred between E. servus and H. zea whereas facilitative interactions occurred between E. servus and H. virescens. Heliothine herbivory did not affect N. viridula feeding behavior. We also found a systemically induced reduction in chlorogenic acid in bolls from plants damaged by H. virescens, but no effect from H. zea herbivory. Feeding avoidance of H. zea-damaged plants and preference for H. virescens plants was determined by selection behaviors and acceptance behaviors depending on species. Response to H. zea herbivory may have involved tissue-bound induced resistance, but phenolic compounds were likely not responsible for the responses.

Technical Abstract: A number of studies have now reported increased levels of non Bt-targeted secondary pests in Bt crops. Although pesticide reduction plays a role, interactions between the secondary pests and the targeted primary pest may also be important. Feeding preference—attractiveness (selection behavior, acceptance behavior) and edibility, was determined for the stink bug species, Nezara viridula and Euchistus servus by caging them on undamaged bolls of cotton plants previously damaged by Heliocoverpa zea or Hethothis virescens and undamaged plants in paired choice tests. The location of the stink bug was observed for 10 continuous minutes immediately after the stink bug was placed in the cage, then 30 min, 1 hr, 12 hr, 18 hr, 24 hr, and 36 hr after the stink bug was placed in the cage. Stink bug preference was determined by parameterizing attraction and leaving rates in a biostatistical model. In addition to measuring stink bug behavioral responses to heliothine herbivory, the quantity of phenolic secondary compounds were measured in cotton bolls from heliothine-damaged and undamaged plants. Higher numbers of E. servus nymphs occurred on the undamaged plants than on H. zea-damaged plants indicationg competition. In contrast, higher numbers of E. servus occurred on H. virescens-damaged plants than undamaged plants indicating facilitation. There were no differences in the number of N. viridula nymphs between paired choices, whichever heliothine species damaged the plant. Boll damage by both heliothine species reduced overall concentrations of the phenolic compounds chlorogenic acid and anthocyanin. However, the pattern of stink bug attraction and leaving rates indicated that something other than changes in these phenolic concentrations were responsible for their behavior. Our analysis of stink bug preference between heliothine-damaged and undamaged cotton plants yielded information on the mechanisms underlying that preference. Such a mechanistic understanding of preference clearly provides valuable information for fu