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

Bulletin of Entomological Research

Volumn 102, Issue 3, 2012, Pages 293-302

  Garcia M ^a   Ortego, F ^a   Castanera P ^a   Farinos G P ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

Bt maize; non target insect; risk assessment; staphylinids; tritrophic interactions

Indexed keywords

CRY3BBL ENDOTOXIN, BACILLUS THURINGIENSIS; ENDOTOXIN;

ADULT; BEETLE; BIOCONTROL AGENT; BIOPESTICIDE; FEEDING; FITNESS; GENE EXPRESSION; GENERALIST; GENETICALLY MODIFIED ORGANISM; LABORATORY METHOD; LARVA; MITE; MORPHOLOGY; NONTARGET ORGANISM; PREDATOR-PREY INTERACTION; PROTEIN; RISK ASSESSMENT; TOXIN; TRITROPHIC INTERACTION; TROPHIC STRUCTURE;

ANIMAL; ARTICLE; BEETLE; DRUG EFFECT; FEMALE; FOOD CHAIN; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; MAIZE; MALE; PARASITOLOGY; PREDATION; REPRODUCTION; TETRANYCHIDAE; TRANSGENIC PLANT;

ANIMALS; BEETLES; ENDOTOXINS; FEMALE; FOOD CHAIN; LARVA; MALE; PLANTS, GENETICALLY MODIFIED; PREDATORY BEHAVIOR; REPRODUCTION; TETRANYCHIDAE; ZEA MAYS;

ACARI; ATHETA CORIARIA; COLEOPTERA; HEXAPODA; STAPHYLINIDAE; TETRANYCHIDAE; TETRANYCHUS URTICAE; ZEA MAYS;

EID: 84861016437     PISSN: 00074853     EISSN: 14752670     Source Type: Journal    
DOI: 10.1017/S0007485311000666     Document Type: Article

References (43)

1. Ahmad, A., Wilde, G.E., Whitworth, R.J. & Zolnerowich, G. (2006) Effect of corn hybrids expressing the coleopteranspecific Cry3Bb1 protein for corn rootworm control on aboveground insect predators. Journal of Economic Entomology 99, 1085-1095. (Pubitemid 44645591)
2. 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.
3. 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.
4. Andow, D.A., Lövei, G.L. & Arpaia, S. (2006) Ecological risk assessment for Bt crops. Nature Biotechnology 24, 749-751.
5. 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. (Pubitemid 30247426)
6. 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.
7. 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. (Pubitemid 41434328)
8. Bohac, J. (1999) Staphylinid beetles as bioindicators. Agriculture, Ecosystems & Environment 74, 357-372. (Pubitemid 29384426)
9. 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. (Pubitemid 46350780)
10. 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.
11. 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.
12. Caro, T.M. & O'Doherty, G. (1999) On the use of surrogate species in conservation biology. Conservation Biology 13, 805-814. (Pubitemid 29368642)
13. 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. (Pubitemid 43015916)
14. Daly, H.V. (1985) Insect morphometrics. Annual Review of Entomology 30, 415-438.
15. 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. (Pubitemid 40689466)
16. 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.
17. 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. (Pubitemid 36093412)
18. 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. (Pubitemid 44607823)
19. Dyar, H.G. (1890). The number of molts of Lepidopterous larvae. Psyche (Camb.) 5, 420-422.
20. 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.
21. 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. (Pubitemid 350060759)
22. 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.
23. Helyer, N., Brown, K. & Cattlin, N.D. (2003) A Colour Handbook of Biological Control in Plant Protection. London, UK, Manson Publishing Press.
24. 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).
25. 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. (Pubitemid 351938247)
26. 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.
27. 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. (Pubitemid 44892555)
28. 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. (Pubitemid 47289456)
29. 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.
30. 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. (Pubitemid 40191485)
31. 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. (Pubitemid 36101246)
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. Rohlf, F.J. (2008) TpsDig 2.12. Ecology and Evolution. Stony Brook. NY, USA, State University of New York.
40. 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.
41. 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. (Pubitemid 351498679)
42. 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. (Pubitemid 40670276)
43. Wheeler, D. (1996) The role of nourishment in oogenesis. Annual Review of Entomology 41, 407-431.