Advertisement

Apidologie

, Volume 43, Issue 4, pp 384–391 | Cite as

The effects of Bt Cry1Ah toxin on worker honeybees (Apis mellifera ligustica and Apis cerana cerana)

  • Ping-Li Dai
  • Wei Zhou
  • Jie Zhang
  • Wei-Yu Jiang
  • Qiang Wang
  • Hong-Juan Cui
  • Ji-Hu Sun
  • Yan-Yan Wu
  • Ting Zhou
Original article

Abstract

We conducted feeding trials in a laboratory setting to test for possible adverse effects of Cry1Ah toxin mixed thoroughly into sugar syrup (60% w/v sucrose solution) at three concentrations (10 μg/mL, 10 ng/mL, and 1 ng/mL) on the survival, pollen consumption, and hypopharyngeal gland mass of Apis mellifera ligustica and Apis cerana cerana. No significant differences in the survival of A. mellifera or A. cerana were found among groups fed on sugar syrup with or without Cry1Ah toxin. No significant differences were found in the longevity of A. mellifera fed sugar syrup with Cry1Ah toxin compared with the control. No differences were detected in the pollen consumption of A. mellifera ligustica and A. cerana cerana. No significant differences were found in the hypopharyngeal gland weight of 12-day-old honeybees A. mellifera ligustica and A. cerana cerana fed on sugar syrup with Cry1Ah toxin compared with the control. The implications of these results are discussed in terms of the risks of transgenic corn crops for honeybees.

Keywords

Apis mellifera ligustica Apis cerana cerana Bacillus thuringiensis Cry1Ah toxin risk assessment 

Notes

Acknowledgments

We thank two anonymous reviewers for comments that improved the manuscript. This research was supported by the Major State Basic Research Development Program of China (no. 2007CB109203), the Fund for Modern Agro-industry Technology Research System (nycytx-43-kxj6), and the Basic Scientific Program of the Chinese Academy of Agricultural Science (no. 0032010046).

References

  1. Arpaia, S. (1996) Ecological impact of Bt-transgenic plants: 1. assessing possible effects of CryIIIB toxin on honey bee (Apis mellifera L.) colonies. J. Genet. Breed. 50, 315–319Google Scholar
  2. Babendreier, D., Joller, D., Romeis, J., Bigler, F., Widmer, F. (2007) Bacterial community structures in honeybee intestines and their response to two insecticidal proteins, FEMS. Microbiol. Ecol. 59, 600–610CrossRefGoogle Scholar
  3. Babendreier, D., Kalberer, N.M., Romeis, J., Fluri, P., Mulligan, E., Bigler, F. (2005) Influence of Bt-transgenic pollen, Bt-toxin and protease inhibitor (SBTI) ingestion on development of the hypopharyngeal glands in honeybees. Apidologie 36, 585–594CrossRefGoogle Scholar
  4. Babendreier, D., Kalberer, N., Romeis, J., Fluri, P., Bigler, F. (2004) Pollen consumption in honey bee larvae: a step forward in the risk assessment of transgenic plants. Apidologie 35, 293–300CrossRefGoogle Scholar
  5. Desneux, N., Bernal, J.S. (2010) Genetically modified crops deserve greater ecotoxicological scrutiny. Ecotoxicology 19, 1642–1644PubMedCrossRefGoogle Scholar
  6. Desneux, N., Decourtye, A., Delpuech, J.M. (2007) The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52, 81–106PubMedCrossRefGoogle Scholar
  7. Duan, J.J., Marvier, M., Huesing, J., Dively, G., Huang, Z.Y. (2008) A meta-analysis of effects of Bt crops on honey bees (Hymenoptera: Apidae). PlosOne 1, 1415Google Scholar
  8. Fluri, P., Lüscher, M., Wille, H., Gerig, L. (1982) Changes in weight of the pharyngeal gland and haemolymph titres of juvenile hormone, protein and vitellogenin in worker honey bees. J. Insect Physiol. 28, 61–68CrossRefGoogle Scholar
  9. Han, P., Niu, C.Y., Lei, C.L., Cui, J.J., Desneux, N. (2010a) Quantification of toxins in a Cry1Ac + CpTI cotton cultivar and its potential effects on the honey bee Apis mellifera. L. Ecotoxicology 19, 1452–1459CrossRefGoogle Scholar
  10. Han, P., Niu, C.Y., Lei, C.L., Cui, J.J., Desneux, N. (2010b) Use of an innovative T-tube maze assay and the Proboscis Extension Response assay to assess sublethal effects of GM products and pesticides on learning capacity of the honey bee Apis mellifera. L. Ecotoxicology 19, 1612–1619CrossRefGoogle Scholar
  11. Hanley, A.V., Huang, Z.Y., Pett, W.L. (2003) Effects of dietary transgenic Bt corn pollen on larvae of Apis mellifera and Galleria mellonella. J. Apic. Res. 42, 77–81Google Scholar
  12. Haydak, M.H. (1970) Honey bee nutrition. Annu. Rev. Entomol. 15, 143–156CrossRefGoogle Scholar
  13. Huang, Z.Y., Hanley, A.V., Pett, W.L., Langenberger, M., Duan, J.J. (2004) Field and semifield evaluation of impacts of transgenic canola pollen on survival and development of worker honey bees. J. Econ. Entomol. 97, 1517–1523PubMedCrossRefGoogle Scholar
  14. James C. (2009) Global status of commercialized biotech/gm crops: 2009, ISAAA Brief.Google Scholar
  15. Jiang, W.Y., Dai, P.L., Zhang, Y.J., Zhou, T., Lin, Y., Shu, C.L., Zhang, J. (2010) Effect of transgenic cotton with Cry1Ac gene on intestinal bacterial community of Apis mellifera ligustica. China J. Appl. Environ. Biol. 16, 211–215CrossRefGoogle Scholar
  16. Liu, B., Shu, C., Xue, K., Zhou, K.X., Li, X.G., Liu, D.D., Zheng, Y.P., Xu, C.R. (2009) The oral toxicity of the transgenic Bt + CpTI cotton pollen to honey bees (Apis mellifera). Ecotoxicol. Environ. Safe 72, 1163–1169CrossRefGoogle Scholar
  17. Malone, L.A., Burgess, E.P.J., Gatehouse, H.S., Voisey, C.R., Tregidga, E.L., Philip, B.A. (2001) Effects of ingestion of a Bacillus thuringiensis toxin and a trypsin inhibitor on honey bee flight activity and longevity. Apidologie 32, 57–68CrossRefGoogle Scholar
  18. Lovei, G.L., Andow, D.A., Arpaia, S. (2009) Transgenic insecticidal crops and natural enemies: a detailed review of laboratory studies. Environ. Entomol. 38, 293–306PubMedCrossRefGoogle Scholar
  19. Malone, L.A., Burgess, E.P.J., Stefanovic, D. (1999) Effects of a Bacillus thuringiensis toxin, two Bacillus thuringiensis biopesticide formulations, and a soybean trypsin inhibitor on honey bee (Apis mellifera L.) survival and food consumption. Apidologie 30, 465–473CrossRefGoogle Scholar
  20. Malone, L.A., Pham-Delègue, M.H. (2001) Effects of transgene products on honey bees (Apis mellifera) and bumble bees (Bombus sp.). Apidologie 32, 287–304CrossRefGoogle Scholar
  21. Malone, L.A., Todd, J.H., Burgess, E.P.J., Christeller, J.T. (2004) Development of hypopharyngeal glands in adult honey bees fed with a Bt toxin, a biotin-binding protein and a protease inhibitor. Apidologie 35, 655–664CrossRefGoogle Scholar
  22. O’callaghan, M., Glare, T.R., Burgess, E.P.J., Malone, L.A. (2005) Effects of plants genetically modified for insect resistance on nontarget organisms. Annu. Rev. Entomol. 50, 271–292PubMedCrossRefGoogle Scholar
  23. Ramirez-Romero, R., Chaufaux, J., Pham-Delègue, M.H. (2005) Effects of Cry1Ab protoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honeybee Apis mellifera, a comparative approach. Apidologie 36, 601–611CrossRefGoogle Scholar
  24. Ramirez-Romero, R., Desneux, N., Decourtye, A., Chaffiol, A., Pham-Delegue, M.H. (2008) Does Cry1Ab protein affect learning performances of the honey bee Apis mellifera L. (Hymenoptera, Apidae)? Ecotoxicol. Environ. Saf. 70, 327–333PubMedCrossRefGoogle Scholar
  25. Romeis, J., Bartsch, D., Bigler, F., Candolfi, M.P., Gielkens, M.M.C., Hartley, S.E., Hellmich, R.L., Huesing, J.E., Jepson, P.C., Layton, R., Quemada, H., Raybould, A., Rose, R.I., Schiemann, J., Sears, M.K., Shelton, A.M., Sweet, J., Vaituzis, Z., Wolt, J.D. (2008) Assessment of risk of insect-resistant transgenic crops to non-target arthropods. Nat. Biotechnol. 26, 203–208PubMedCrossRefGoogle Scholar
  26. Romeis, J., Hellmich, R.L., Candolfi, M.P., Carstens, K., Schrijver, A.D., Gatehouse, A.M.R., Herman, R.A., Huesing, J.E., McLean, M.A., Raybould, A., Shelton, A.M., Waggoner, A. (2011) Recommendations for the design of laboratory studies on non-target arthropods for risk assessment of genetically engineered plants. Transgenic Res. 20, 1–22PubMedCrossRefGoogle Scholar
  27. Rose, R., Dively, G.P., Pettis, J. (2007) Effects of Bt corn pollen on honey bees: emphasis on protocol development. Apidologie 38, 368–377CrossRefGoogle Scholar
  28. SAS Institute (2000) SAS/STAT User’s Guide, Release 8.01 edition Cary, NC, USA.Google Scholar
  29. Sims, S.R. (1995) Bacillus thuringiensis var. kurstaki (Cry IA (c)) protein expressed in transgenic cotton: effects on beneficial and other nontarget insects. Southwest Entomol 20, 493–500Google Scholar
  30. Then, C. (2010) Risk assessment of toxins derived from Bacillus thuringiensis synergism, efficacy, and selectivity. Environ. Sci. Pollut. Res. 17, 791–797CrossRefGoogle Scholar
  31. Wang, Y., Lang, Z., Zhang, J., He, K., Song, F., Huang, D. (2008) Ubi 1 intron-mediated enhancement of the expression of Bt cry1ah gene in transgenic maize (Zea mays L.). Chin. Sci. Bull. 53, 3185–3190CrossRefGoogle Scholar
  32. Xue, J., Liang, G., Crickmore, N., Li, H., He, K., Song, F., Feng, X., Huang, D., Zhang, J. (2008a) Cloning and characterization of a novel Cry1A toxin from Bacillus thuringiensis with high toxicity to the Asian corn borer and other lepidopteran insects, FEMS. Microbiol. Lett. 280, 95–101CrossRefGoogle Scholar
  33. Xue, K., Deng, S., Wang, R.J., Yan, F.M., Xu, C.R. (2008b) Leaf surface factors of transgenic Bt cotton associated with the feeding behaviors of cotton aphids: A case study on non-target effects. Sci. China Ser. C-Life. Sci. 51, 145–156CrossRefGoogle Scholar
  34. Yang, G.H. (2005) Harm of introducing the western honeybee Apis mellifera L. to the Chinese honeybee Apis cerana F. and its ecological impact. Acta Entomol. Sin 48, 401–406Google Scholar

Copyright information

© INRA, DIB and Springer-Verlag, France 2011

Authors and Affiliations

  • Ping-Li Dai
    • 1
    • 2
  • Wei Zhou
    • 1
  • Jie Zhang
    • 3
  • Wei-Yu Jiang
    • 3
  • Qiang Wang
    • 1
    • 2
  • Hong-Juan Cui
    • 3
  • Ji-Hu Sun
    • 4
  • Yan-Yan Wu
    • 1
    • 2
  • Ting Zhou
    • 1
    • 2
  1. 1.Institute of Apicultural Research, Chinese Academy of Agricultural ScienceBeijingChina
  2. 2.Key Laboratory of Pollinating Insect Biology, Ministry of AgricultureBeijingChina
  3. 3.State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesBeijingChina
  4. 4.Department of PhysiologySecond Military Medical UniversityShanghaiChina

Personalised recommendations