Development of an early-tier laboratory bioassay for assessing the impact of orally-active insecticidal compounds on larvae of coccinella septempunctata (Coleoptera: Coccinellidae)

Environmental Entomology

Volumn 41, Issue 6, 2012, Pages 1687-1693

  Álvarez Alfageme, Fernando ^a   Pálinkás, Zoltan ^b   Bigler, Franz ^a   Romeis, Jörg ^a  

^a AGROSCOPE RECKENHOLZ TÄNIKON RESEARCH STATION ART   (Switzerland)

^b SZENT ISTVÁN UNIVERSITY   (Hungary)

Author keywords

environmental risk assessment; genetically engineered plants; ladybird beetles; nontarget arthropods

Indexed keywords

ARSENIC ACID DERIVATIVE; DRUG DERIVATIVE; INSECTICIDE; LEUCINE; N [N (3 CARBOXYOXIRANE 2 CARBONYL)LEUCYL]AGMATINE; POTASSIUM DERIVATIVE;

BEETLE; BIOASSAY; ENVIRONMENTAL RISK; GENETIC ENGINEERING; INHIBITOR; INSECTICIDE; LABORATORY METHOD; LARVA; MOTH; NONTARGET ORGANISM; RISK ASSESSMENT; TOXICITY;

ANIMAL; APHID; ARTICLE; BEETLE; BIOASSAY; CHEMISTRY; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; LARVA; METHODOLOGY; MOTH; OOCYTE; RISK ASSESSMENT; TRANSGENIC PLANT; VALIDATION STUDY;

ANIMALS; APHIDS; ARSENATES; BEETLES; BIOLOGICAL ASSAY; INSECTICIDES; LARVA; LEUCINE; MOTHS; OVUM; PLANTS, GENETICALLY MODIFIED; POTASSIUM COMPOUNDS; RISK ASSESSMENT;

ANAGASTA KUEHNIELLA; ARTHROPODA; COCCINELLA SEPTEMPUNCTATA; COCCINELLIDAE; COLEOPTERA; LEPIDOPTERA; PYRALIDAE;

EID: 84871545506     PISSN: 0046225X     EISSN: None     Source Type: Journal    
DOI: 10.1603/EN12032     Document Type: Article

References (41)

1. Ahmad, A., G. E. Wilde, R. J. Whitworth, and G. Zolnerowich. 2006. Effect of corn hybrids expressing the Coleopteran-specific Cry3Bb1 protein for corn rootworm control on aboveground insect predators. J. Econ. Entomol. 99: 1085-1095.
2. Álvarez-Alfageme, F., N. Ferry, P. Castanera, F. Ortego, and A.M.R. Gatehouse. 2008. Prey mediated effects of Bt maize on fitness and digestive physiology of the red spider mite predator Stethorus punctillum Weise (Coleoptera: Coccinellidae). Transgenic Res. 17: 943-954.
3. Álvarez-Alfageme, F., F. Bigler, and J. Romeis. 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 Res. 20: 467-479.
4. Auer, C., and R. Frederick. 2009. Crop improvement using small RNAs: applications and predictive ecological risk assessments. Trends Biotechnol. 27: 644-650.
5. Birch, A.N.E., I. E. Geoghegan, M.E.N. Majerus, J. W. Mc-Nicol, C. A. Hackett, A.M.R. Gatehouse, and J. A. Gatehouse. 1999. Tritrophic interactions involving pest aphids, predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance. Mol. Breed. 5: 77-83.
6. Blackman, R. L. 1967. The effects of different aphid foods on Adalia bipunctata L. and Coccinella 7-punctata. Ann. Appl. Biol. 59: 207-219.
7. [CABI] Centre for Agricultural Bioscience International. 2007. CPC Report Coccinella septempunctata. Crop Protection Compendium, Wallingford, United Kingdom.
8. Duan, J. J., G. Head, M. J. McKee, T. E. Nickson, J. W. Martin, and F. S. Sayegh. 2002. Evaluation of dietary effects of transgenic corn pollen expressing Cry3Bb1 protein on a non-target ladybird beetle, Coleomegilla maculata. Entomol. Exp. Appl. 104: 271-280.
9. Duan, J. J., M. S. Paradise, J. G. Lundgren, and R. N. Wiedenmann. 2005. Genetically modified crops and ground beetles as non-target organisms: developing dietary toxicity assays for larvae of Poecilus chalcites (Coleoptera: Carabidae). Am. Entomol. 51: 227-230.
10. Duan, J. J., D. Teixeira, J. E. Huesing, and C. Jiang. 2008. Assessing the risk to nontarget organisms from Bt corn resistant to corn rootworms (Coleoptera: Chrysomelidae): tier-I testing with Orius insidiosus (Heteroptera: Anthocoridae). Environ. Entomol. 37: 838-844.
11. Fabrick, J., C. Behnke, T. Cazpla, K. Bala, A. G. Rao, K. J. Kramer, and G. R. Reeck. 2002. Effects of a potato cysteine proteinase inhibitor on midgut proteolytic enzyme activityand growth of the southern corn rootworm, Diabrotica undecimpunctatahowardi(Coleoptera: Chrysomelidae).Insect Biochem. Mol. Biol. 32: 405-415.
12. Garcia-Alonso, M., E. Jacobs, A. Raybould, T. E. Nickson, P. Sowig, H. Willekens, P. Van der Kouwe, R. Layton, F. Amijee, A. M. Fuentes, et al. 2006. A tiered system for assessing the risk of genetically modified plants to nontarget organisms. Environ. Biosafety Res. 5: 57-65.
13. Gatehouse, J. A. 2008. Biotechnological prospects for engineering insect-resistant plants. Plant Physiol. 146: 881-887.
14. Harwood, J. D., W. G. Wallin, and J. J. Obrycki. 2005. Uptake of Bt endotoxins by nontarget herbivores and higher order arthropod predators: molecular evidence from a transgenic corn agroecosystem. Mol. Ecol. 14: 2815-2823.
15. Harwood, J. D., R. A. Samson, and J. J. Obrycki. 2007. Temporal detection of Cry1Ab-endotoxins in coccinellid predators from fields of Bacillus thuringiensis corn. Bull. Entomol. Res. 97: 643-648.
16. Hodek, I., and A. Honek. 1996. Ecology of Coccinellidae. Kluwer Academic Publishers, Dordrecht, the Netherlands.
17. Holm, S. 1979. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6: 65-70.
18. Kalushkov, P., and I. Hodek. 2004. The effects of thirteen species of aphids on some life history parameters of the ladybird Coccinella septempunctata. BioControl 49: 21-32.
19. Lawo, N. C., and J. Romeis. 2008. Assessing the utilization of a carbohydrate food source and the impact of insecticidal proteins on larvae of the green lacewing, Chrysoperla carnea. Biol. Control 44: 389-398.
20. Leplé, J. C., M. Bonadé-Bottino, S. Augustin, G. Pilate, V. Dumanois Lê Tan, A. Delplanque, D. Cornu, and L. Jouanin. 1995. Toxicity to Chrysomela tremulae (Coleoptera: Chrysomelidae) of transgenic poplars expressing a cysteine proteinase inhibitor. Mol. Breed. 1: 319-328.
21. Li, Y., and J. Romeis. 2010. Bt maize expressing Cry3Bb1 does not harm the spider mite, Tetranychus urticae, or its ladybird beetle predator, Stethorus punctillum. Biol. Control 53: 337-344.
22. Li, Y., J. Romeis, P. Wang, Y. Peng, and A. M. Shelton. 2011a. Acomprehensive assessment of the effects of Bt cotton on Coleomegilla maculata demonstrates no detrimental effects by Cry1Ac and Cry2Ab. PLoS ONE 6: e22185.
23. Li, Y., J. Ostrem, J. Romeis, M. Chen, X. Liu, R. L. Hellmich, A. M. Shelton, and Y. Peng. 2011b. Development of a tier-1 test assay for assessing the toxicity of insecticidal substances against Coleomegilla maculata. Environ. Entomol. 40: 496-502.
24. Lundgren, J. G., and R. N. Wiedenmann. 2002. Coleopteran-specific Cry3Bb toxin from transgenic corn pollen does not affect the fitness of a nontarget species, Coleomegilla maculata DeGeer (Coleoptera: Coccinellidae). Environ. Entomol. 31: 1213-1218.
25. Lundgren, J. G., and R. N. Wiedenmann. 2005. Tritrophic interactions among Bt (CryMb1) corn, aphid prey, and the predator Coleomegilla maculata (Coleoptera: Coccinellidae). Environ. Entomol. 34: 1621-1625.
26. Malone, L. A., A.M.R. Gatehouse, and B.I.P. Barratt. 2008. Beyond Bt: alternative strategies for insect-resistant genetically modified crops, pp. 357-417. In J. Romeis, A. M. Shelton, and G. G. Kennedy (eds.), Integration of insect resistant genetically modified crops within IPM programs. Springer Science Business Media B.V.
27. Meissle, M., and J. Romeis. 2009. The web-building spider Theridion impressum (Araneae: Theridiidae) is not adversely affected by Bt maize resistant to corn rootworms. Plant Biotechnol. J. 7: 645-656.
28. Moser, S. E., J. D. Harwood, and J. J. Obrycki. 2008. Larval feeding on Bt hybrid and non-Bt corn seedlings by Harmonia axyridis (Coleoptera: Coccinellidae) and Coleomegilla maculata (Coleoptera: Coccinellidae). Environ. Entomol. 37: 525-533.
29. Obrist, L. B., A. Dutton, R. Albajes, and F. Bigler. 2006. Exposure of arthropod predators to Cry1Ab toxin in Bt maize fields. Ecol. Entomol. 31: 143-154.
30. Perry, J. N., C.J.F. ter Braak, P. M. Dixon, J. J. Duan, R. S. Hails, A. Huesken, M. Lavielle, M. Marvier, M. Scardi, K. Schmidt, et al. 2009. Statistical aspects of environmental risk assessment of GM plants for effects on non-target organisms. Environ. Biosafety Res. 8: 65-78.
31. Pilcher, C. D., J. J. Obrycki, M. E. Rice, and L. C. Lewis. 1997. Preimaginal development, survival, and field abundance of insect predators on transgenic Bacillus thuringiensis corn. Environ. Entomol. 26: 446-454.
32. Raybould, A., G. Caron-Lormier, and D. Bohan. 2011. Derivation and interpretation of hazard quotients to assess ecological risks from the cultivation of insect-resistant transgenic crops. J. Agric. Food Chem. 59: 5877-5885.
33. Riddick, E. W., and P. Barbosa. 1998. Impact of Cry3Aintoxicated Leptinotarsa decemlineata (Coleoptera. Chrysomelidae) and pollen on consumption, development, and fecundity of Coleomegilla maculata (Coleoptera: Coccinellidae). Ann. Entomol. Soc.Am.91: 303-307.
34. Romeis, J., D. Bartsch, F. Bigler, M. P. Candolfi, M.M.C. Gielkens, S. E. Hartley, R. L. Hellmich, J. E. Huesing, P. C. Jepson, R. Layton, et al. 2008. Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nat. Biotechnol. 26: 203-208.
35. Romeis, J., R. L. Hellmich, M. P. Candolfi, K. Carstens, A. De Schrijver, A.M.R. Gatehouse, R. A. Herman, J. E. Huesing, M. A. McLean, A. Raybould, et al. 2011. Recommendations for the design of laboratory studies on nontarget arthropods for risk assessment of genetically engineered plants. Transgenic Res. 20: 1-22.
36. Romeis, J., A. Raybould, F. Bigler, M. P. Candolfi, R. L. Hellmich, J. E. Huesing, and A. M. Shelton. 2012. Deriving criteria to select arthropod species for laboratory tests to assess the ecological risks from cultivating arthropod-resistant transgenic crops. Chemosphere, doi: http://dx.doi.org/10. 1016/j.chemosphere.2012.09.035.
37. Rose, R. I. (ed). 2007. White paper on tier-based testing for the effects of proteinaceous insecticidal plant-incorporated protectants on non-target invertebrates for regulatory risk assessment. US Environmental Protection Agency, Washington, DC. (http://www.epa.gov/pesticides/biopesticides/pips/non- target-arthropods.pdf).
38. Sanvido, O., J. Romeis, A. Gathmann, M. Gielkens, A. Raybould, and F. Bigler. 2012. Evaluating environmental risks of genetically modified crops-ecological harm criteria for regulatory decision-making. Environ. Sci. Policy 15: 82-91.
39. Schmuck, R., M. P. Candolfi, R. Kleiner, M. Mead-Briggs, M. Moll, F. Kemmeter, D. Jans, A. Waltersdorfer, and H. Wilhelmy. 2000. A laboratory test system for assessing effects of plant protection products on the plant dwelling insect Coccinella septempunctata L. (Coleoptera: Coccinellidae), pp. 45-56. In M. P. Candolfi, S. Blü mel, R. Forster, F. M. Bakker, C. Grimm, S. A. Hassan, U. Heimbach, M. A. Mead-Briggs, B. Reber, R. Schmuck, et al. (eds.), Guidelines to evaluate side-effects of plant protection products to non-target arthropods. IOBC/WPRS, Gent, Belgium.
40. Stacey, D., G. Graser, M. Mead-Briggs, and A. Raybould. 2006. Testing the impact on non-target organisms of insecticidal proteins expressed in transgenic crops. IOBC/WPRS Bull. 29: 165-172.
41. Tian, J., H. L. Collins, J. Romeis, S. E. Naranjo, R. L. Hellmich, and A. M. Shelton. 2012. Using field-evolved resistance to Cry1F maize in a lepidopteran pest to demonstrate no adverse effects of Cry1F on one of its major predators. Transgenic Res., doi: http://dx.doi.org/10.1007/s11248-012-9604-4.