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Assessment of prey-mediated effects of the coleopteran-specific toxin Cry3Bb1 on the generalist predator Atheta coriaria (Coleoptera: Staphylinidae)

Published online by Cambridge University Press:  24 November 2011

M. García ,
F. Ortego ,
P. Castañera  and
G.P. Farinós
M. García
Affiliation:
Centro de Investigaciones Biológicas, CSIC, Ramiro de Maeztu, 9, 28040 Madrid, Spain
F. Ortego
Affiliation:
Centro de Investigaciones Biológicas, CSIC, Ramiro de Maeztu, 9, 28040 Madrid, Spain
P. Castañera
Affiliation:
Centro de Investigaciones Biológicas, CSIC, Ramiro de Maeztu, 9, 28040 Madrid, Spain
G.P. Farinós*
Affiliation:
Centro de Investigaciones Biológicas, CSIC, Ramiro de Maeztu, 9, 28040 Madrid, Spain
*
*Author for correspondence Fax: +34 915360432 E-mail: [email protected]
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Abstract

A laboratory study was carried out to assess the potential prey-mediated effects of Cry3Bb1-expressing Bt maize on the fitness and predatory ability of Atheta coriaria Kraatz (Coleoptera: Staphylinidae), using Tetranychus urticae Koch (Acari: Tetranychidae) as prey. The concentration of Cry3Bb1 toxin through the trophic chain significantly decreased from Bt maize (21.7 μg g−1 FW) to mites (5.6 μg g−1 FW) and then to A. coriaria adults (1.4 μg g−1 FW), but not from mites to A. coriaria L1–L3 larvae (4.1–4.6 μg g−1 FW). Interestingly, the toxin levels detected in A. coriaria larvae represent more than 20% of the concentration found in Bt maize, and the toxin was detected up to 48 h after exposure. To our knowledge, this is the highest level of exposure ever reported in a predatory beetle to the Cry3Bb1 protein. When A. coriaria larvae were reared on Bt-fed mites, Bt-free mites or rearing food, no significant differences among treatments were observed in development, morphological measurements of sclerotized structures and body weight. Moreover, no negative effects on reproductive parameters were reported in adults feeding on Bt-fed prey after 30 days of treatment, and survival was not affected after 60 days of exposure. Similarly, predatory ability and prey consumption of A. coriaria larvae and adults were not affected by exposure to the toxin. All together, these results indicate a lack of adverse effects on A. coriaria, a species commonly used as a biological control agent. The use of A. coriaria as a surrogate species for risk assessment of GM crops that express insecticidal proteins is discussed.

Keywords

Bt maizerisk assessmentnon-target insectstaphylinidstritrophic interactions
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 102 , Issue 3 , June 2012 , pp. 293 - 302
Copyright
Copyright © Cambridge University Press 2011

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References

Ahmad, A., Wilde, G.E., Whitworth, R.J. & Zolnerowich, G. (2006) Effect of corn hybrids expressing the coleopteran-specific Cry3Bb1 protein for corn rootworm control on aboveground insect predators. Journal of Economic Entomology 99, 1085–1095.Google Scholar
Álvarez-Alfageme, F., Ferry, N., Castañera, P., Ortego, F. & Gatehouse, A.M.R. (2008) Prey mediated effects of Bt maize on fitness and digestive physiology of the red spider mite predator Stethorus punctillum Weise (Coleoptera: Coccinellidae). Transgenic Research 17, 943–954.CrossRefGoogle Scholar
Álvarez-Alfageme, F., Bigler, F. & Romeis, J. (2011) Laboratory toxicity studies demonstrate no adverse effects of Cry1Ab and Cry3Bb1 to larvae of Adalia bipunctata (Coleoptera: Coccinellidae): the importance of study design. Transgenic Research 20, 467–479.Google Scholar
Andow, D.A., Lövei, G.L. & Arpaia, S. (2006) Ecological risk assessment for Bt crops. Nature Biotechnology 24, 749–751.Google Scholar
Arpaia, S., De Marzo, L., Di Leo, G.M., Santoro, M.E., Mennella, G. & van Loon, J.J.A. (2000) Feeding behaviour and reproductive biology of Colorado potato beetle adults fed transgenic potatoes expressing the Bacillus thuringiensis Cry3B endotoxin. Entomologia Experimentalis et Applicata 95, 31–37.Google Scholar
Balog, A., Kiss, J., Szekeres, D., Szenasi, A. & Marko, V. (2010) Rove beetle (Coleoptera: Staphylinidae) communities in transgenic Bt (MON810) and near isogenic maize. Crop Protection 29, 567–571.Google Scholar
Bhatti, M.A., Duan, J., Head, G., Jiang, C.J., McKee, M.J., Nickson, T.E., Pilcher, C.L. & Pilcher, C.D. (2005) Field evaluation of the impact of corn rootworm (Coleoptera: Chrysomelidae)-protected Bt corn on ground-dwelling invertebrates. Environmental Entomology 34, 1325–1335.CrossRefGoogle Scholar
Bohac, J. (1999) Staphylinid beetles as bioindicators. Agriculture, Ecosystems & Environment 74, 357–372.Google Scholar
Bravo, A., Gill, S.S. & Soberon, M. (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49, 423–435.Google Scholar
Brunke, A.J., Bahlai, C.A., Sears, M.K. & Hallett, R.H. (2009) Generalist predators (Coleoptera: Carabidae, Staphylinidae) associated with millipede populations in sweet potato and carrot fields and implications for millipede management. Environmental Entomology 38, 1106–1116.Google Scholar
Carney, V.A., Diamond, J.C., Murphy, G.D. & Marshall, D. (2002) The potential of Atheta coriaria Kraatz (Coleoptera: Staphylinidae), as a biological control agent for use in greenhouse crops. IOBC/WPRS Bulletin 25, 37–40.Google Scholar
Caro, T.M. & O'Doherty, G. (1999) On the use of surrogate species in conservation biology. Conservation Biology 13, 805–814.Google Scholar
Chege, P.G, Clark, T.L. & Hibbard, B.E. (2005) Alternate host phenology affects survivorship, growth, and development of Western Corn Rootworm (Coleoptera: Chrysomelidae) larvae. Environmental Entomology 34, 1441–1447.CrossRefGoogle Scholar
Daly, H.V. (1985) Insect morphometrics. Annual Review of Entomology 30, 415–438.Google Scholar
de la Poza, M., Pons, X., Farinós, G.P., López, C., Ortego, F., Eizaguirre, M., Castañera, P. & Albajes, R. (2005) Impact of farm-scale Bt maize on abundance of predatory arthropods in Spain. Crop Protection 24, 677–684.Google Scholar
Delbac, L., Lecharpentier, P. & Thiery, D. (2010) Larval instars determination for the European Grapevine Moth (Lepidoptera: Tortricidae) based on the frequency distribution of head-capsule widths. Crop Protection 29, 623–630.CrossRefGoogle Scholar
Duan, J.J., Head, G., McKee, M.J., Nickson, T.E., Martin, J.W. & Sayegh, F.S. (2002) Evaluation of dietary effects of transgenic corn pollen expressing Cry3Bb1 protein on a non-target ladybird beetle, Coleomegilla maculata. Entomologia Experimentalis et Applicata 104, 271–280.Google Scholar
Duan, J.J., Paradise, M.S., Lundgren, J.G., Bookout, J.T., Jiang, C.J. & Wiedenmann, R.N. (2006) Assessing nontarget impacts of Bt corn resistant to corn rootworms: Tier-1 testing with larvae of Poecilus chalcites (Coleoptera: Carabidae). Environmental Entomology 35, 135–142.Google Scholar
Dyar, H.G. (1890). The number of molts of Lepidopterous larvae. Psyche (Camb.) 5, 420–422.Google Scholar
Farinós, G.P., de la Poza, M., Hernandez-Crespo, P., Ortego, F. & Castañera, P. (2008) Diversity and seasonal phenology of aboveground arthropods in conventional and transgenic maize crops in Central Spain. Biological Control 44, 362–371.Google Scholar
Ferry, N., Mulligan, E., Majerus, M. & Gatehouse, A. (2007) Bitrophic and tritrophic effects of Bt Cry3A transgenic potato on beneficial, non-target, beetles. Transgenic Research 16, 795–812.Google Scholar
García, M., Ortego, F., Castañera, P. & Farinós, G.P. (2010) Effects of exposure to the toxin Cry1Ab through Bt maize fed-prey on the performance and digestive physiology of the predatory rove beetle Atheta coriaria. Biological Control 55, 225–233.CrossRefGoogle Scholar
Helyer, N., Brown, K. & Cattlin, N.D. (2003) A Colour Handbook of Biological Control in Plant Protection. London, UK, Manson Publishing Press.Google Scholar
ICH (2005) Harmonised tripartite guideline: validation of analytical procedures: Text and methodology Q2 (R1). in International conference on harmonisation of technical requirements for registration of pharmaceuticals for human use. http://www.ich.org/LOB/media/MEDIA417.pdf (accessed 25 July 2011).Google Scholar
Icoz, I. & Stotzky, G. (2008) Cry3Bb1 protein from Bacillus thuringiensis in root exudates and biomass of transgenic corn does not persist in soil. Transgenic Research 17, 609–620.Google Scholar
James, C. (2010) Global Status of Commercialized Biotech/GM Crops: 2010. Ithaca, NY, USA, International Service for the Acquisition of Agri-Biotech Applications Brief No. 42.Google Scholar
Jandricic, S., Scott-Dupree, C.D., Broadbent, A.B., Harris, C.R. & Murphy, G. (2006) Compatibility of Atheta coriaria with other biological control agents and reduced-risk insecticides used in greenhouse floriculture integrated pest management programs for fungus gnats. Canadian Entomologist 138, 712–722.Google Scholar
Klimaszewski, J., Assing, V., Majka, C.G., Pelletier, G., Webster, R.P. & Langor, D. (2007) Records of adventive aleocharine beetles (Coleoptera: Staphylinidae: Aleocharinae) found in Canada. Canadian Entomologist 139, 54–79.Google Scholar
Li, Y. & Romeis, J. (2010) Bt maize expressing Cry3Bb1 does not harm the spider mite, Tetranychus urticae, or its ladybird beetle predator, Stethorus punctillum. Biological Control 53, 337–344.Google Scholar
Lövei, G.L. & Arpaia, S. (2005) The impact of transgenic plants on natural enemies: a critical review of laboratory studies. Entomologia Experimentalis et Applicata 114, 1–14.Google Scholar
Lundgren, J.G. & Wiedenmann, R.N. (2002) Coleopteran-specific Cry3Bb toxin from transgenic corn pollen does not affect the fitness of a nontarget species, Coleomegilla maculata DeGeer (Coleoptera: Coccinellidae). Environmental Entomology 31, 1213–1218.Google Scholar
Meinke, L.J., Sappington, T.W., Onstad, D.W., Guillemaud, T., Miller, N.J., Komáromi, J., Levay, N., Furlan, L., Kiss, J. & Toth, F. (2009) Western corn rootworm (Diabrotica virgifera virgifera LeConte) population dynamics. Agricultural and Forest Entomology 11, 29–46.Google Scholar
Meissle, M. & Romeis, J. (2009) The web-building spider Theridion impressum (Araneae: Theridiidae) is not adversely affected by Bt maize resistant to corn rootworms. Plant Biotechnology Journal 7, 645–656.Google Scholar
Miethling-Graff, R., Dockhorn, S. & Tebbe, C.C. (2010) Release of the recombinant Cry3Bb1 protein of Bt maize MON88017 into field soil and detection of effects on the diversity of rhizosphere bacteria. European Journal of Soil Biology 46, 41–48.Google Scholar
Miller, K.V. & Williams, R.N. (1983) Biology and host preference of Atheta coriaria (Coleoptera: Staphylinidae), an egg predator of Nitidulidae and Muscidae. Annals of the Entomological Society of America 76, 158–161.Google Scholar
Miller, N., Estoup, A., Toepfer, S., Bourguet, D., Lapchin, L., Derridj, S., Kim, K.S., Reynaud, P., Furlan, L. & Guillemaud, T. (2005) Multiple transatlantic introductions of the western corn rootworm. Science 310, 992–992.Google Scholar
Porcar, M., García-Robles, I., Domínguez-Escribá, L. & Latorre, A. (2010) Effects of Bacillus thuringiensis Cry1Ab and Cry3Aa endotoxins on predatory Coleoptera tested through artificial diet-incorporation bioassays. Bulletin of Entomological Research 100, 297–302.Google Scholar
Rauschen, S., Schaarschmidt, F. & Gathmann, A. (2010) Occurrence and field densities of Coleoptera in the maize herb layer: implications for Environmental Risk Assessment of genetically modified Bt-maize. Transgenic Research 19, 727–744.Google Scholar
Rohlf, F.J. (2008) TpsDig 2.12. Ecology and Evolution. Stony Brook. NY, USA, State University of New York.Google Scholar
Stacey, D., Graser, G., Mead-Briggs, M. & Raybould, A. (2006) Testing the impact on non-target organisms of insecticidal proteins expressed in transgenic crops. IOBC/WPRS Bulletin 29, 171–179.Google Scholar
Todd, J.H., Ramankutty, P., Barraclough, E.I. & Malone, L.A. (2008) A screening method for prioritizing non-target invertebrates for improved biosafety testing of transgenic crops. Environmental Biosafety Research 7, 35–56.Google Scholar
Vaughn, T., Cavato, T., Brar, G., Coombe, T., DeGooyer, T., Ford, S., Groth, M., Howe, A., Johnson, S., Kolacz, K., Pilcher, C., Purcell, J., Romano, C., English, L. & Pershing, J. (2005) A method of controlling corn rootworm feeding using a Bacillus thuringiensis protein expressed in transgenic maize. Crop Science 45, 931–938.CrossRefGoogle Scholar
Wheeler, D. (1996) The role of nourishment in oogenesis. Annual Review of Entomology 41, 407–431.CrossRefGoogle ScholarPubMed