Assessing the role of non-cotton refuges in delaying Helicoverpa armigera resistance to Bt cotton in West Africa

Abstract

Non-cotton host plants without Bacillus thuringiensis (Bt) toxins can provide refuges that delay resistance to Bt cotton in polyphagous insect pests. It has proven difficult, however, to determine the effective contribution of such refuges and their role in delaying resistance evolution. Here, we used biogeochemical markers to quantify movement of Helicoverpa armigera moths from non-cotton hosts to cotton fields in three agricultural landscapes of the West African cotton belt (Cameroon) where Bt cotton was absent. We show that the contribution of non-cotton hosts as a source of moths was spatially and temporally variable, but at least equivalent to a 7.5% sprayed refuge of non-Bt cotton. Simulation models incorporating H. armigera biological parameters, however, indicate that planting non-Bt cotton refuges may be needed to significantly delay resistance to cotton producing the toxins Cry1Ac and Cry2Ab. Specifically, when the concentration of one toxin (here Cry1Ac) declined seasonally, resistance to Bt cotton often occurred rapidly in simulations where refuges of non-Bt cotton were rare and resistance to Cry2Ab was non-recessive, because resistance was essentially driven by one toxin (here Cry2Ab). The use of biogeochemical markers to quantify insect movement can provide a valuable tool to evaluate the role of non-cotton refuges in delaying the evolution of H. armigera resistance to Bt cotton.

Keywords: Bacillus thuringiensis; Bt cotton; biogeochemical markers; genetically engineered crops; insect resistance management; polyphagous pest; refuge strategy.

Figure 1

Sampling locations of Helicoverpa armigera moths in Cameroon (GU, Guider; DJ, Djalingo; TC, Tcholliré). Transgenic cotton producing Bt toxins was recently introduced to West Africa, but only in Burkina Faso. Other Bt crops such as Bt corn have not yet been released in West Africa.

Figure 2

(A–C) Moths trapped in cotton fields (%) that originated from non-cotton host plants. Remaining moths (100 –% indicated by bar) originated from cotton. Moths were trapped at three locations (Guider, Djalingo, and Tcholliré) in Cameroon in 2006. (D) Typical sequence of Helicoverpa armigera host plants in the West Africa cotton belt throughout the cropping season. Curves represent temporal occurrence and relative area of host plants.

Figure 3

Effect of the abundance of sprayed refuges of non-Bt cotton (%) on the evolution of Helicoverpa armigera resistance to Cry1Ac/Cry2Ab cotton at three locations in Cameroon: Guider (•), Djalingo (□), and Tcholliré (Δ). Simulations considered data on movement between non-cotton refuges and cotton fields measured at each site (Fig. 2A–C). For Cry2Ab, the initial resistance allele frequency was 0.0033 (A) or 0.033 (B), and resistance was partially recessive (D_LC = 0.1, dashed line) or semi-dominant (D_LC = 0.5, solid line). For Cry1Ac, the initial resistance allele frequency was 0.0003, and resistance was partially recessive (D_LC = 0.26) (Table 2). The criterion for resistance evolution was >20% survival on Bt cotton.

Figure 4

Effect of the abundance of sprayed refuges of non-Bt cotton (%) on the evolution of Helicoverpa armigera resistance to Cry1Ac/Cry2Ab cotton at Djalingo (Cameroon). Simulations considered data on movement between non-cotton refuges and cotton fields and patterns of long-range migration (Fig. 2). For Cry2Ab, the initial resistance allele frequency was 0.0033, and resistance was semi-dominant (D_LC = 0.5). For Cry1Ac, initial resistance allele frequency was 0.0003, and resistance was partially recessive (D_LC = 0.26) (Table 2). MR1 is the proportion of moths from southern regions colonizing the cotton belt in June–July; MR2 the proportion of moths from the cotton belt contributing to the pool of migrants moving south in October–November. The criterion for resistance evolution was >20% survival on Bt cotton. Results of simulations for MR1/MR2 values of 0/0 were almost identical to results obtained for 0.9/0.9, 0.1/0.9 and 0.1/0.1.