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

PLoS One. 2013 May 13;8(5):e63554. doi: 10.1371/journal.pone.0063554. Print 2013.


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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacillus thuringiensis Toxins
  • Bacterial Proteins / biosynthesis
  • Bacterial Proteins / metabolism
  • Bacterial Proteins / pharmacology*
  • China
  • Endotoxins / biosynthesis
  • Endotoxins / metabolism
  • Endotoxins / pharmacology*
  • Feeding Behavior / drug effects*
  • Female
  • Flight, Animal / drug effects*
  • Gossypium / genetics
  • Gossypium / immunology
  • Gossypium / parasitology
  • Hemolysin Proteins / biosynthesis
  • Hemolysin Proteins / metabolism
  • Hemolysin Proteins / pharmacology*
  • Larva / drug effects
  • Larva / physiology
  • Oviposition / drug effects*
  • Oviposition / physiology
  • Pest Control, Biological
  • Plant Leaves / genetics
  • Plant Leaves / immunology
  • Plant Leaves / parasitology
  • Plants, Genetically Modified
  • Pupa / drug effects
  • Pupa / physiology
  • Spodoptera / drug effects*
  • Spodoptera / physiology
  • Transgenes


  • Bacillus thuringiensis Toxins
  • Bacterial Proteins
  • Endotoxins
  • Hemolysin Proteins
  • insecticidal crystal protein, Bacillus Thuringiensis

Grant support

This work was funded by projects under the National Department of Transgenic Crops Cultivation Research Foundation (No. 2009ZX08011-018B), the National Department of Public Benefit Research Foundation (201203020, 200903051), and the National Natural Science Foundation of China (No. 31000850, 31071677, 30871641). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.