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Title: Competitive release and outbreaks of non-target pests associated with transgenic Bt cotton

Author
item ZEILINGER, ADAM - UNIVERSITY OF MINNESOTA
item OLSON, DAWN
item ANDOW, DAVID - UNIVERSITY OF MINNESOTA

Submitted to: Ecological Applications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/6/2015
Publication Date: 1/5/2016
Citation: Zeilinger, A.R., Olson, D.M., Andow, D.A. 2016. Competitive release and outbreaks of non-target pests associated with transgenic Bt cotton. Ecological Applications. 26(4):1047-1054. https://doi.org/10.1890/15-1314.
DOI: https://doi.org/10.1890/15-1314

Interpretive Summary: The adoption of transgenic Bt cotton has, in some cases, led to environmental and economic benefits through reduced insecticide use. However, the distribution of these benefits, and associated risks, among cotton-growing regions has been uneven due to outbreaks of non-target or secondary pests in some regions, thereby requiring the continued use of insecticides. In the southeastern United States, Bt cotton adoption has resulted in increased abundance of and damage from the stink bug pests, Euschistus servus and Nezara viridula (Heteroptera: Pentatomidae). While the impact of increased stink bug abundance has been well-documented, the causes have remained unclear. We tested the hypothesis that herbivory by Bt-susceptible Helicoverpa zea deters stink bug oviposition and increases leaving rates on damaged non-Bt cotton plants. We found that both E. servus and N. viridula strongly preferred ovipositing on undamaged plants rather than H. zea-damaged plants, but we found differences in leaving rates only for E. servus. Our results indicate that competition between the stink bug species and H. zea occurs at the whole-plant scale, in field plots, and is mediated by induced plant resistance. Competitive release of stink bug populations in Bt cotton contributes to outbreaks, though the relative importance of competitive release remains an open question. Ecological risk assessments of Bt crops would benefit from more mechanistic understandings of non-target pest outbreaks.

Technical Abstract: This study tests a competitive release hypothesis that Helicoverpa zea larval herbivory will 1) deter oviposition and increase leaving rates of the stink bugs, Euchistus servus and Nezara viridula and that 2) that these effects will be stronger for E. servus than for N. viridula. By spatially separating the herbivores, the experiments are designed to specifically test for plant-mediated competition. For the oviposition study, non-Bt glyphosate-tolerant transgenic cotton plants were grown in greenhouses and insects were field collected and reared in the laboratory. Plant treatments were heliothine damaged and undamaged plants. To obtain leaf damage, we placed a 3rd instar larva of on 2 mid-level leaves per plant and confined to the leaf with a 23.76 cm2 cage clip cage for three days. One stink bug gravid female was placed into a screened arena (42cm ' 30cm ' 4cm lwh) with the uppermost main stem leaf of a heliothine damaged and an undamaged plant. Both cotton leaves remained connected to the plants and neither leaf was damaged, thereby testing stink bug responses to systemically induced plant resistance. Mated N. virdiula and E. servus females was individuallly introduced to the cage at the center, after being chilled, along with a moistened cotton wick and two undamaged cotton bolls, one by each leaf. The cage was checked daily for an egg mass. For the leaving rate study, non-Bt glyphosate-tolerant DP147 cotton was planted in two 300 m2 plots at the Bellflower experimental farm, USDA-ARS, Tifton, GA, and randomly assigned to two treatments: (1) undamaged control plants or (2) plants damaged by heliothines. Three days after heliothine damage began, we placed a single adult stink bug female of either species, 5-7 days old since molting, on a 1st position for square of the plant. The trials were started at 21:00. The location of each stink bug was recorded as being on the original square or on a different part of the plant, or off the plant at 10 min, 1 hr, 12 hr, and 24 hr from the start. For both stink bug species, significantly more egg masses were found on the undamaged than the damaged plant. For E. servus, egg masses on undamaged plants contained significantly more eggs than egg masses on damaged plants. Leaving rates were constant for N. viridula and did not differ with plant treatment. Leaving rates for E. servus were not constant and were significantly greater from H. zea-damaged plants than from undamaged plants. Our results indicate that competition between the stink bug species and H. zea occurs at the whole-plant scale and is mediated by induced plant resistance.