Faculté des sciences

Transgene products in honeydew : estimating risks for non-target insects

Hogervorst, Petronella Alida Maria ; Rahier, Martine (Dir.)

Thèse de doctorat : Université de Neuchâtel, 2006 ; 1888.

Insect-resistant genetically modified (GM) crops could harm organisms other than the pests targeted by the toxin. These so-called non-target organisms include parasitoids and predators that are important for natural pest regulation, which could be exposed to the expressed insecticidal proteins through feeding on transgenic plant tissue or through feeding on target or non-target herbivores... Plus

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    Summary
    Insect-resistant genetically modified (GM) crops could harm organisms other than the pests targeted by the toxin. These so-called non-target organisms include parasitoids and predators that are important for natural pest regulation, which could be exposed to the expressed insecticidal proteins through feeding on transgenic plant tissue or through feeding on target or non-target herbivores containing the transgene product. In this thesis, honeydew excreted by phloem-feeding insects is addressed as an additional route of exposure to insecticidal proteins. Since honeydew is commonly used by insects as a sugar source, a broad range of non-target organisms could potentially be exposed to transgene products. The importance of this exposure route was studied for GM wheat expressing snowdrop lectin (Galanthus nivalis agglutinin, GNA) to control phloem-feeding insects, such as aphids. Since risk is defined by both hazard and exposure, these aspects were studied for GNA-containing honeydew. Three predator species (Adalia bipunctata, Coccinella septempunctata and Chrysoperla carnea) were tested for their sensitivity towards GNA. Longevity of the species studied was directly affected by GNA dissolved in a sucrose solution. This was confirmed by the fact that digestive enzymes in the guts of the predator larvae were unable to break down GNA. Whilst A. bipunctata and C. septempunctata excreted most of the GNA, C. carnea accumulated the toxin in the gut since they are not able to excrete faeces. Moreover, GNA was found to bind to glycoproteins in the gut, being a prerequisite for its toxicity, and transferred into the insects’ haemolymph. As a first step in studying honeydew as an exposure route, the nutritional suitability of honeydew from three aphid species feeding on potato or wheat plants was investigated for the aphid parasitoid Aphidius ervi. The different honeydews were all relatively suitable food sources for adult parasitoids, but not always as suitable as a sucrose solution. The sugar composition of the honeydews differed significantly among the three aphid species on both potato and wheat. Multivariate analysis showed that small differences in parasitoid longevity could to some extent be explained by honeydew sugar composition, indicating that sugar composition is an important factor in determining the nutritional quality of honeydew. When sensitivity towards GNA was tested for adult A. ervi, a direct dose-dependent effect on longevity was found. To study GNA-exposure through honeydew, the aphid Rhopalosiphum padi was fed on a GNA-containing artificial diet. Honeydew collected from these aphids contained 10-40% of the GNA concentration that was present in the aphid diet. When feeding on this honeydew, A. ervi suffered a reduction in longevity that was more pronounced than was to be expected based on the detected GNA concentration in the honeydew. Analysis of carbohydrate and amino acid composition revealed that a change in honeydew composition caused by a GNA-effect on the aphids could be a possible explanation for the additional reduction in parasitoid longevity. Honeydew from aphids feeding on GNA-expressing wheat did not affect the longevity of A. ervi compared to honeydew from non-transformed wheat plants, which was probably due to low GNA expression levels in the plants. In order to establish the importance of honeydew feeding for adult aphidophagous insects, aphid parasitoids, hoverflies and green lacewings were collected in wheat fields. Analyses of the insects’ sugar profiles revealed that the majority of the insects had recently consumed sugars. Especially the two green lacewing species (Chrysoperla lucasina and C. carnea) were found to be at a high nutritional state. Recent honeydew feeding was detected in 35% of the hoverflies (Episyrphus balteatus) and 63% of the parasitoids (Aphidius spp.) that had been classified as having consumed sugars. These results demonstrate that aphid honeydew is an important food source for aphid parasitoids, and to a lesser extent for hoverflies, in wheat fields. To assess if honeydew consumption could be important for omnivorous predators, it was studied whether C. carnea larvae use honeydew as a food source in the presence of aphids, their preferred prey. Both in a choice and a no-choice situation, it was found that honeydew was utilized by the larvae, but to a lesser extent than aphids. Furthermore, previous feeding on aphids or honeydew reduced the subsequent consumption of honeydew. Having shown that GNA in honeydew poses a hazard for a range of non-target insects and that predators and parasitoids will be exposed to GNA in honeydew, this thesis demonstrates that transgene products in honeydew pose a risk for honeydew-feeding non-target insects. This route of exposure should thus be considered in future risk assessment of transgenic plants expressing phloem-transported insecticidal compounds.