Increased long-flight activity triggered in beet armyworm by larval feeding on diet containing Cry1Ac protoxin

Abstract

Evaluating ecological safety and conducting pest risk analysis for transgenic crops are vitally important before their commercial planting. The beet armyworm, Spodoptera exigua, a long-distance migratory insect pest, is not a direct target of transgenic Cry1Ac-expressing cotton in China, but nevertheless it has recently become an important pest. Migrants leaving their natal field arrive in other appropriate habitat far away in a short time, often followed by larval outbreaks. S. exigua has low susceptibility to Cry1Ac. However, our results from laboratory experiments identified (i) sublethal effects of Cry1Ac protoxin on larval development rate, larval and pupal weight, and adult lifetime fecundity, and (ii) increased long-flight behavior triggered by Cry1Ac which may contribute to larval outbreaks elsewhere. No significant differences in larval mortality, pupation rate, adult emergence rate, longevity, pre-oviposition period, or oviposition period were observed between controls and larvae fed on artificial diet incorporating a low concentration of Cry1Ac protoxin. The negative sublethal effects on some developmental and reproductive traits and lack of effect on others suggest they do not contribute to the observed severity of S. exigua outbreaks after feeding on Cry1Ac cotton. Interestingly, the percentage of long fliers increased significantly when larvae were reared on diet containing either of two low-dose treatments of Cry1Ac, suggesting a possible increased propensity to disperse long distances triggered by Cry1Ac. We hypothesize that negative effects on development and reproduction caused by Cry1Ac in the diet are offset by increased flight propensity triggered by the poor food conditions, thereby improving the chances of escaping adverse local conditions before oviposition. Increased long-flight propensity in turn may amplify the area damaged by outbreak populations. This phenomenon might be common in other migratory insect pests receiving sublethal doses of Bt toxins and warrants further study.

Figure 1. Growth and development of S. exigua fed on artificial diet containing different concentrations of Cry1Ac.

Non-toxic (ck) artificial diet served as a control. A. Larval mortality, pupation rate, adult emergence rate; B. Developmental time; C. Larval and pupal weight. Data are presented as mean ± SEM. Lines sharing the same letter are not significantly different at 5% level by Tukey’s HSD test.

Figure 2. Frequency (%) distribution of pupal weights of S. exigua derived from larvae feeding on different concentrations of Cry1Ac.

Non-toxic (ck) artificial diet served as a control. Sample sizes were 60 for each treatment and the non-toxic control.

Figure 3. Flight performance of newly emerged S. exigua adults derived from larvae feeding on Cry1Ac during a 12-h tethered-flight test.

A. Total flight distance; B. Total flight duration; C. Average flight velocity. Sample sizes for non-toxic (ck) and different concentrations of Cry1Ac treatment were 53, 54, 59, 65, 60 and 62, from left to right, respectively. Data are presented as means ± SE. Bars sharing the same letter are not significantly different at 5% level by Tukey’s HSD test.

Figure 4. Frequency (%) distribution of the furthest flight distance (A) and longest flight duration (B) of S. exiguas during a 12-h flight mill test.

Sample sizes for flight treatments of newly emerged adults derived from larvae feeding on non-toxic (ck) and two low-dose of 3.125 µg g⁻¹ and 25 µg g⁻¹ Cry1Ac incorporated artificial diet were 53, 54 and 59, respectively. Asterisks indicate percentage are significantly different (Chi-Square test, *P<0.05), ns means no significant difference.