Effects of entomopathogenic nematodes on evolution of pink bollworm resistance to Bacillus thuringiensis toxin Cry1Ac.

The evolution of resistance by pests can reduce the efficacy of transgenic crops that produce insecticidal toxins from Bacillus thuringiensis (Bt). However, fitness costs may act to delay pest resistance to Bt toxins. Meta-analysis of results from four previous studies revealed that the entomopathogenic nematode Steinernema riobrave (Rhabditida: Steinernematidae) imposed a 20% fitness cost for larvae of pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), that were homozygous for resistance to Bt toxin Cry1Ac, but no significant fitness cost was detected for heterozygotes. We conducted greenhouse and laboratory selection experiments to determine whether S. riobrave would delay the evolution of pink bollworm resistance to Cry1Ac. We mimicked the high dose/refuge scenario in the greenhouse with Bt cotton (Gossypium hirsutum L.) plants and refuges of non-Bt cotton plants, and in the laboratory with diet containing Cry1Ac and refuges of untreated diet. In both experiments, half of the replicates were exposed to S. riobrave and half were not. In the greenhouse, S. riobrave did not delay resistance. In the laboratory, S. riobrave delayed resistance after two generations but not after four generations. Simulation modeling showed that an initial resistance allele frequency > 0.015 and population bottlenecks can diminish or eliminate the resistance-delaying effects of fitness costs. We hypothesize that these factors may have reduced the resistance-delaying effects of S. riobrave in the selection experiments. The experimental and modeling results suggest that entomopathogenic nematodes could slow the evolution of pest resistance to Bt crops, but only under some conditions.

Effects of four nematode species on fitness costs of pink bollworm resistance to Bacillus thuringiensis toxin Cry1Ac.

Evolution of resistance by pests can reduce the efficacy oftransgenic crops that produce insecticidal toxins from the bacterium Bacillus thuringiensis Berliner (Bt). In conjunction with refuges of non-Bt host plants, fitness costs can delay the evolution of resistance. Furthermore, fitness costs often vary with ecological conditions, suggesting that agricultural landscapes can be manipulated to magnify fitness costs and thereby prolong the efficacy of Bt crops. In the current study, we tested the effects of four species of entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) on the magnitude and dominance of fitness costs of resistance to Bt toxin CrylAc in pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae). For more than a decade, field populations of pink bollworm in the United States have remained susceptible to Bt cotton Gossypium hirsutum L. producing CrylAc; however, we used laboratory strains that had a mixture of susceptible and resistant individuals. In laboratory experiments, dominant fitness costs were imposed by the nematode Steinernema riobrave Cabanillas, Poinar, and Raulston but no fitness costs were imposed by Steinernema carpocapsae Weiser, Steinernema sp. (ML18 strain), or Heterorhabditis sonorensis Stock, Rivera-Orduño, and Flores-Lara. In computer simulations, evolution of resistance to Cry1Ac by pink bollworm was substantially delayed by treating some non-Bt cotton refuge fields with nematodes that imposed a dominant fitness cost, similar to the cost observed in laboratory experiments with S. riobrave. Based on the results here and in related studies, we conclude that entomopathogenic nematodes could bolster insect resistance management, but the success of this approach will depend on selecting the appropriate species of nematode and environment, as fitness costs were magnified by only two of five species evaluated and also depended on environmental factors.

Effects of pink bollworm resistance to Bacillus thuringiensis on phenoloxidase activity and susceptibility to entomopathogenic nematodes.

Widespread planting of crops genetically engineered to produce insecticidal toxins from the bacterium Bacillus thuringiensis (Bt) imposes selection on many key agricultural pests to evolve resistance to Bt. Fitness costs can slow the evolution of Bt resistance. We examined effects of entomopathogenic nematodes on fitness costs of Bt resistance in the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), a major pest of cotton, Gossypium hirsutum L., in the southwestern United States that is currently controlled by transgenic cotton that produces Bt toxin Cry1Ac. We tested whether the entomopathogenic nematodes Steinernema riobrave Cabanillas, Poinar, and Raulston (Rhabditida: Steinernematidae) and Heterorhabditis bacteriophora Poinar (Rhabditida: Heterorhabditidae) affected fitness costs of resistance to Cry1Ac in two laboratory-selected hybrid strains of pink bollworm reared on non-Bt cotton bolls. The nematode S. riobrave imposed a recessive fitness cost for one strain, and H. bacteriophora imposed a fitness cost affecting heterozygous resistant individuals for the other strain. Activity of phenoloxidase, an important component of insects' immune response, did not differ between Bt-resistant and Bt-susceptible families. This suggests phenoloxidase does not affect susceptibility to entomopathogenic nematodes in Bt-resistant pink bollworm. Additionally, phenoloxidase activity does not contribute to Bt resistance, as has been found in some species. We conclude that other mechanisms cause higher nematode-imposed mortality for pink bollworm with Bt resistance genes. Incorporation of nematode-imposed fitness costs into a spatially explicit simulation model suggests that entomopathogenic nematodes in non-Bt refuges could delay resistance by pink bollworm to Bt cotton.

Screening hybrid poplar clones for susceptibility to Cryptorhynchus lapathi (Coleoptera: Curculionidae).

The poplar-and-willow borer, Cryptorhynchus lapathi (L.) (Coleoptera: Curculionidae), is a wood-boring pest of economic importance in irrigated hybrid poplar (Populus spp.) farms in eastern Washington and Oregon. There is no practical insecticide control tactic against either the larval or adult stage of C. lapathi. To assess variability in C. lapathi toward clone preference, we initiated a no-choice study on 180 caged trees that consisted of five clones in a randomized complete block design. C. lapathi was significantly more successful at establishing a population in two clones with Populus trichocarpa X P. deltoides (TxD) parentage (female x male) than in either of two clones with P. deltoides x P. nigra (DxN) parentage (female x male), or a single clone with P. deltoides x P. maximowiczii (DxM) parentage (female X male). There were no significant differences in the rate of weevil development among infested clones, with the exception of DxM trees. Larvae in DxM clones developed on average to the fourth size grouping and those in the two TxD clones developed on average to the fifth size grouping, and this difference was significant. These results corroborate our general damage surveys conducted in the field. Our findings provide growers with the option to choose less susceptible varieties when replanting.

An endemic population of western poplar clearwing moths (Lepidoptera: Sesiidae) invades a monoculture of hybrid poplar.

Western poplar clearwing, Paranthrene robiniae (Hy. Edwards) (Lepidoptera: Sesiidae), is endemic in Pacific Northwest riparian habitats at low population densities. These moths have colonized commercial hybrid poplar (Populus spp.) plantings. Moth populations increased rapidly and became a major pest. Trap catches of male moths in mid-season surveys increased 190-fold from 95 in 2001 to >18,500 in 2002 across 6597 ha of poplars monitored. The outbreak of western poplar clearwings was widespread in 2002. Pheromone-baited traps placed one trap per 81.75 ha over 13,274 ha of commercial poplars captured >108,000 male moths in 2002. Damage to commercial poplars included girdling of saplings and burrows in limbs and trunks of trees. Repeated applications of chlorpyrifos failed to reduce the abundance of moths in 2002. Two management strategies over two separate plantations of approximately 6500 ha each were contrasted. Future control strategies recommend a halt to the use of contact insecticides that target adult moths. Short-term (3-5 yr) control should involve a pheromone-based mating disruption strategy followed eventually by selection of a clone that is less susceptible to P. robiniae attack.