Tanja H. Schuler

Parasitoid behaviour and Bt plants

Transgenic crops that express genes targeted against insect pests may also affect non-target insects. For example, lacewings and monarch butterflies have been reported to be susceptible to toxins from Bacillus thuringiensis (Bt) that are expressed in Bt transgenic plants, although these results were obtained in small-scale laboratory assays in which insects were exposed to high levels of transgenically expressed toxin in no-choice tests. We show here that the behaviour of non-target insects can also play a part in determining how their populations will be affected by Bt plants.

Population-scale laboratory studies of the effect of transgenic plants on nontarget insects

Studies of the effects of insect‐resistant transgenic plants on beneficial insects have, to date, concentrated mainly on either small‐scale ‘worst case scenario’ laboratory experiments or on field trials. We present a laboratory method using large population cages that represent an intermediate experimental scale, allowing the study of ecological and behavioural interactions between transgenic plants, pests and their natural enemies under more controlled conditions than is possible in the field. Previous studies have also concentrated on natural enemies of lepidopteran and coleopteran target pests. However, natural enemies of other pests, which are not controlled by the transgenic plants, are also potentially exposed to the transgene product when feeding on hosts. The reduction in the use of insecticides on transgenic crops could lead to increasing problems with such nontarget pests, normally controlled by sprays, especially if there are any negative effects of the transgenic plant on their natural enemies. This study tested two lines of insect‐resistant transgenic oilseed rape (Brassica napus) for side‐effects on the hymenopteran parasitoid Diaeretiella rapae and its aphid host, Myzus persicae. One transgenic line expressed the δ‐endotoxin Cry1Ac from Bacillus thuringiensis (Bt) and a second expressed the proteinase inhibitor oryzacystatin I (OC‐I) from rice. These transgenic plant lines were developed to provide resistance to lepidopteran and coleopteran pests, respectively. No detrimental effects of the transgenic oilseed rape lines on the ability of the parasitoid to control aphid populations were observed. Adult parasitoid emergence and sex ratio were also not consistently altered on the transgenic oilseed rape lines compared with the wild‐type lines.

Tritrophic choice experiments with bt plants, the diamondback moth (Plutella xylostella) and the parasitoid Cotesia plutellae.

Parasitoids are important natural enemies of many pest species and are used extensively in biological and integrated control programmes. Crop plants transformed to express toxin genes derived from Bacillus thuringiensis (Bt) provide high levels of resistance to certain pest species, which is likely to have consequent effects on parasitoids specialising on such pests. A better understanding of the interaction between transgenic plants, pests and parasitoids is important to limit disruption of biological control and to provide background knowledge essential for implementing measures for the conservation of parasitoid populations. It is also essential for investigations into the potential role of parasitoids in delaying the build-up of Bt-resistant pest populations. The diamondback moth (Plutella xylostella), a major pest of brassica crops, is normally highly susceptible to a range of Bt toxins. However, extensive use of microbial Bt sprays has led to the selection of resistance to Bt toxins in P. xylostella. Cotesia plutellae is an important endoparasitoid of P. xylostella larvae. Although unable to survive in Bt-susceptible P. xylostella larvae on highly resistant Bt oilseed rape plants due to premature host mortality, C. plutellae is able to complete its larval development in Bt-resistant P. xylostella larvae. Experiments of parasitoid flight and foraging behaviour presented in this paper showed that adult C. plutellae females do not distinguish between Bt and wildtype oilseed rape plants, and are more attracted to Bt plants damaged by Bt-resistant hosts than by susceptible hosts. This stronger attraction to Bt plants damaged by resistant hosts was due to more extensive feeding damage. Population scale experiments with mixtures of Bt and wildtype plants demonstrated that the parasitoid is as effective in controlling Bt-resistant P. xylostella larvae on Bt plants as on wildtype plants. In these experiments equal or higher numbers of parasitoid adults emerged per transgenic as per wildtype plant. The implications for integrated pest management and the evolution of resistance to Bt in P. xylostella are discussed.

Movement of transgenic plant-expressed Bt Cry1Ac proteins through high trophic levels

The movement of Bacillus thuringiensis (Berliner) (Bt) Cry1Ac endotoxin through high trophic levels was assessed to help elucidate the effects of Bt toxin on non‐target insects. The diamondback moth (Plutella xylostella L., Lepidoptera: Plutellidae), the parasitic wasp (Cotesia vestalis Haliday, Hymenoptera: Braconidae) and the predatory green lacewing Chrysoperla carnea (Stephen) (Neuroptera: Chrysopidae) were used as a model system in this laboratory study. Bt‐resistant P. xylostella larvae fed Cry1Ac‐expressing transgenic oilseed rape (OSR, Brassica napus L., Cruciferae), before and after parasitization by C. vestalis, consumed Cry1Ac with the ingested plant material but only a proportion of Cry1Ac consumed was recovered from the bodies and faeces of P. xylostella larvae. Cry1Ac was not detected in newly emerged parasitoid larvae. In contrast, Cry1Ac was detected in C. carnea larvae fed on resistant P. xylostella larvae reared on Bt OSR. However, no Cry1Ac could be detected in C. carnea larvae when the lacewings were transferred to P. xylostella larvae reared on conventional OSR and tested 24–48 h. The metabolizing ability of Cry1Ac is discussed for the larvae of P. xylostella and C. carnea.

Laboratory studies of the effects of reduced prey choice caused by Bt plants on a predatory insect

Crops transformed to express Bacillus thuringiensis (Bt) toxins can cause close to 100% mortality of certain target pest species. This study assessed the effect of target pest reduction on the predatory insect Chrysoperla carnea (Stephens) in the presence of alternative prey. Numbers of lacewings recovered from Bt oilseed rape (cultivar Oscar, event O52) did not differ significantly from numbers of lacewings recovered from conventional oilseed rape in cage experiments with the target pest Plutella xylostella (Linnaeus) and the non-target pest Myzus persicae (Sulzer) when aphid densities were high. However, significantly fewer lacewings were recovered from Bt plants as aphid densities were lowered. Lacewing weights were not affected by plant type.