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Diversity and abundance of flower-visiting insects in Bt and non-Bt cotton fields of Maputaland (KwaZulu Natal Province, South Africa)

Published online by Cambridge University Press:  01 December 2008

J.-L. Hofs*
Affiliation:
CIRAD, UR Systems of Annual Crops, F-34398Montpellier, France
A.S. Schoeman
Affiliation:
Department of Zoology and Entomology, Faculty of Natural and Agricultural Sciences, University of Pretoria, Pretoria0002, South Africa
J. Pierre
Affiliation:
INRA, UMR 1099 Biologie des Organismes et des Populations Appliquée à la Protection des Plantes, F-35650, Le Rheu, France
*
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Abstract

We studied the abundance and diversity of flower-visiting insects on Bt and non-Bt cotton plants in the Makhathini Flats region of South Africa during the 2003/2004 and 2004/2005 crop seasons to detect any impact of the Bt toxin (Cry1Ac). Bt cotton cultivars produced more flowers than non-Bt cultivars regardless of the cropping conditions (farmers' fields or research station), probably due to the fact that Bt cotton is not susceptible to flower bud pests. The results obtained in both crop seasons highlighted the prevalence of honeybees (Apis mellifera L.), various Nitidulidae and a unique Meloidae species (Mylabris oculata Thunberg) as flower visiting insects in this area. No impact of the Bt phenotype on insect abundance and diversity could be drawn on the basis of our comparative results on Bt and non-Bt cotton plants, and no direct effect of these transgenic plants was actually noted. The potential role of some of the inventoried insects, especially M. oculata, in the dispersal of transgenic pollen is discussed.

Type
Research Paper
Copyright
Copyright © ICIPE 2009

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References

Ambrose, D. P. and Claver, M. A. (1999) Suppression of cotton leafworm (Spodoptera litura), flower beetle (Mylabris pustulata) and red cotton bug (Dysdercus cingulatus) by Rhynocoris marginatus (Fabr.) (Het. Reduviidae) in cotton field cages. Journal of Applied Entomology 123, 225229.CrossRefGoogle Scholar
Armstrong, J. S., Leser, J. and Kraemer, G. (2000) An inventory of the key predators of cotton pests on Bt and non-Bt cotton in West Texas, pp. 10301033. In Proceedings of the 2000 Beltwide Cotton Conference, January 4–8, San Antonio, Texas (edited by Dugger, C. P. and Richter, D. A.). Memphis, Tennessee, USA.Google Scholar
Arpaïa, S., Fiore, M. C., Clemente, A. and Scardi, M. (2001) Insect biodiversity in Bt-expressing canola and its isogenic untransformed control in experimental fields, Abstract, Volume of 11th International Symposium on Insect–Plant Relationships, Helsingør, Denmark. p. 51.Google Scholar
Badendreier, D., Reichhart, B., Romeis, J. and Bigler, F. (2008) Impact of insecticidal proteins expressed in transgenic plants on bumblebee microcolonies. Entomologia Experimentalis et Applicata 126, 148157.CrossRefGoogle Scholar
Bhatti, M. A., Duan, J., Head, G., Jiang, J., McKee, M. J., Nickson, T. E., Pilcher, C. L. and Pilcher, C. D. (2005) Field evaluation of the impact of corn rootworm (Coleoptera: Chrysomelidae)-protected Bt corn on ground-dwelling invertebrates. Environmental Entomology 34, 13251335.CrossRefGoogle Scholar
Blanche, R. and Cunningham, S. A. (2005) Rain forest provides pollinating beetles for Atemoya crops. Journal of Economic Entomology 98, 11931201.CrossRefGoogle ScholarPubMed
Burraston, K. N., Gardner, J. S. and Booth, G. M. (2005) SEM evaluation of the plant-pollinator interactions between nitidulid beetles and a native tropical Malvaceae species Gossypium tomentosum on Kauai. Microscopy and Microanalysis 11 (suppl. 2), 11501151.CrossRefGoogle Scholar
Candolfi, M. P., Brown, K., Grimm, C., Reber, B. and Schmidli, H. (2004) A faunistic approach to assess potential side effects of genetically modified Bt-corn on non-target arthropods under field conditions. Biocontrol Science and Technology 14, 129170.CrossRefGoogle Scholar
Cattaneo, M. G., Yafuso, C., Schmidt, C., Huang, C. Y., Rahman, M., Olson, C., Ellers-Kirk, C., Orr, B. J., Marsh, S. E., Antilla, L., Dutilleul, P. and Carrière, Y. (2006) Farm-scale evaluation of the impact of transgenic cotton on biodiversity, pesticide use, and yield. Proceedings of the National Academy of Sciences 103, 75717576.CrossRefGoogle ScholarPubMed
Couilloux, R. (1965) Observations sur la faune du cotonnier dans le basin du Logone Tchad (exception faite des chenilles de la capsule). Coton et Fibres Tropicales 20, 517530.Google Scholar
Daly, T. and Buntin, G. D. (2005) Effect of Bacillus thuringiensis transgenic corn for lepidopteran control on non-target arthropods. Environmental Entomology 34, 12921301.CrossRefGoogle Scholar
Delvare, G. and Aberlenc, H. P. (1989) Les insectes d'Afrique et d'Amérique tropicale. Clé pour la reconnaissance de familles. CIRAD, Montpellier. 302 pp.Google Scholar
Duan, J. J., Marvier, M., Huesing, J., Dively, G. and Huang, Z. Y. (2008) A meta-analysis of effects of Bt crops on honey bees (Hymenoptera: Apidae). PLoS ONE, e1415doi: 10.1371/journal.pone.0001415.CrossRefGoogle ScholarPubMed
El-Sarrag, M. S. A., Ahmed, H. M. and Siddig, M. A. (1993) Insect pollinators of certain crops in the Sudan and the effect of pollination on seed yield and quality. Journal of King Saud University, Agricultural Sciences 5, 253262.Google Scholar
French, B. W., Chandler, L. D., Ellsbury, M. M., Fuller, B. M. and West, M. (2004) Ground beetle (Coleoptera: Carabidae) assemblage in a transgenic corn-soybean cropping system. Environmental Entomology 33, 554563.CrossRefGoogle Scholar
Haughton, A. J., Champion, G. T., Hawes, C., Heard, M. S., Brooks, D. R., Bohan, D. A., Clark, S. J., Dewar, A. M., Firbank, L. G., Osborne, J. L., Perry, J. N., Rothery, P., Roy, D. B., Scott, R. J., Woiwod, I. P., Birchall, C., Skellern, M. P., Walker, J. H., Baker, P., Bell, D., Browne, E. L., Dewar, A. J. G., Garner, B. H., Haylock, L. A., Horne, S. L., Mason, N. S., Sands, R. J. N. and Walker, M. J. (2003) Invertebrate responses to the management of genetically modified herbicide-tolerant and conventional spring crops. II. Within field epigeal and aerial arthropods. Philosophical Transactions of the Royal Society of London B358, 18631877.Google Scholar
Hawes, C., Haughton, A. J., Osborne, J. L., Roy, D. B., Perry, J. N., Rothery, P., Bohan, D. A., Brooks, D. R., Champion, G. T., Dewar, A. M., Heard, M. S., Woiwod, I. P., Daniels, R. E., Young, M. W., Parish, A. M., Scott, R. J., Firbank, L. G. and Squire, G. R. (2003) Responses of plants and invertebrate trophic groups to contrasting herbicide regimes in the farm scale evaluations of genetically modified herbicide-tolerant crops. Philosophical Transactions of the Royal Society of London B 358, 18991913.Google ScholarPubMed
Head, G., Moar, W., Eubanks, M., Freeman, B., Ruberson, J., Hagerty, A. and Turnipseed, S. (2005) A multi-year, large-scale comparison of arthropod populations on commercially managed Bt and non-Bt cotton fields. Environmental Entomology 34, 12571266.Google Scholar
Hofs, J.-L., Hau, B. and Marais, D. (2006) Boll distribution patterns in Bt and non-Bt cultivars. I. Study on commercial irrigated farming systems in South Africa. Field Crops Research 98, 203209.CrossRefGoogle Scholar
Hofs, J.-L., Schoeman, A. S., Mellet, M. and Vaissayre, M. (2005) Impact des cotonniers génétiquement modifiés sur la biodiversité de la faune entomologique: le cas du coton Bt en Afrique du Sud. International Journal of Tropical Insect Science 25, 6372.CrossRefGoogle Scholar
James, C. (2007) Executive summary of global status of commercialized biotech/GM crops: 2006, ISAAA Briefs 37. ISAAA, Ithaca, New York.Google Scholar
Jasinski, J., Eisley, B., Young, C., Wilson, H. and Kovach, J. (2001) Beneficial arthropod survey in transgenic and non-transgenic fields in Ohio. Special Circular-Ohio Agricultural Research and Development Center 179, 99102.Google Scholar
Kevan, P. G. and Becker, H. G. (1983) Insects as flower visitors and pollinators. Annual Review of Entomology 28, 407453.CrossRefGoogle Scholar
Klinkhammer, P. G. L. and de Jong, T. L. (1990) Effects of plant density and sex differential reward visitation in the protandrous Echium vulgare (Boraginacae). Oikos 57, 399405.CrossRefGoogle Scholar
Li, X. J. (1981) Preliminary observations on pollination by Haptonchus luteolus. Insect Knowledge 18, 202203.Google Scholar
Llewellyn, D., Tyson, C., Constable, G., Duggan, B., Beale, S. and Steel, P. (2007) Containment of regulated genetically modified cotton in the field. Agriculture Ecosystems and Environment 121, 419429.CrossRefGoogle Scholar
Lozzia, G. C. (1999) Biodiversity and structure of ground beetle assemblages (Coleoptera: Carabidae) in Bt corn and its effects on nontarget insects. Bollettino di Zoologia Agraria e di Bachicoltura 31, 3758.Google Scholar
Marvier, M., McCreedy, C., Regetz, J. and Kareiva, P. (2007) A meta-analysis of effects of Bt cotton and maize on non-target invertebrates. Science 316, 14751477.CrossRefGoogle Scholar
Mellet, M. A., Schoeman, A. S., Broodryk, S. W. and Hofs, J.-L. (2004) Bollworm (Helicoverpa armigera (Hubner) Lepidoptera: Noctuidae) occurrences in Bt- and non-Bt-cotton fields, Marble Hall, Mpumalanga, South Africa. African Entomology 12, 107115.Google Scholar
Moffett, J. O., Stith, L. S., Burkhardt, C. C. and Shipman, C. W. (1975) Influence of cotton genotypes on floral visits of honeybees. Crop Science 15, 782784.CrossRefGoogle Scholar
Naranjo, S. E., Ruberson, J. R., Sharma, H. C., Wilson, L. and Wu, K. (2008) The present and the future role of insect-resistant Bt cotton in IPM, pp. 159194. In Integration of Insect-Resistant GM Crops Within IPM Programs (edited by Romeis, J., Shelton, A. M. and Kennedy, G. G.). Springer, Dordrecht.Google Scholar
Pierre, J., Marsault, D., Genecque, E., Renard, M., Champolivier, J. and Pham-Delegue, M. H. (2003) Effects of herbicide-tolerant transgenic oilseed rape genotypes on honey bees and other pollinating insects under field conditions. Entomologia Experimentalis et Applicata 108, 159168.CrossRefGoogle Scholar
Pope, O. A., Simpson, D. M. and Duncan, E. N. (1944) Effects of corn barriers on natural crossing in cotton. Journal of Agricultural Research 68, 347361.Google Scholar
Rodger, J. G., Balkwill, K. and Gemmill, B. (2004) African pollination studies: where are the gaps? International Journal of Tropical Insect Science 24, 528.CrossRefGoogle Scholar
Romeis, J., Meissle, M. and Bigler, F. (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nature Biotechnology 24, 6371.CrossRefGoogle ScholarPubMed
Romeis, J., Shelton, A. M. and Kennedy, G. G. (Eds) (2008) Integration of Insect-Resistant GM Crops Within IPM Programs. Springer, Dordrecht. 429 pp.Google Scholar
Roy, D. B., Bohan, D. A., Haughton, A. J., Hill, M. O., Osborne, J. L., Clark, S. J., Perry, J. N. and Schmidt, J. (1983) Flowering plant density and pollinator visitation in Senecio (Compositae). Oecologia 60, 97102.Google Scholar
Roy, D. B., Bohan, D. A., Haughton, A. J., Hill, M. O., Osborne, J. L., Clark, S. J., Perry, J. N., Rothery, P., Scott, R. J., Brooks, D. R., Champion, G. T., Hawes, C., Heard, M. S. and Firbank, L. G. (2003) Invertebrates and vegetation of field margins adjacent to crop subject to contrasting herbicide regimes in the Farm Scale Evaluations of the genetically modified herbicide-tolerant crops. Philosophical Transactions of the Royal Society London B 358, 18791898.Google ScholarPubMed
Schmidt, J. (1983) Flowering plant density and pollinator visitation in Senecio (Compositae). Oecologia 60, 97102.CrossRefGoogle Scholar
Scholtz, C. H. and Holm, E. (1989) Insects of Southern Africa. University of Pretoria, Pretoria. 502 pp.Google Scholar
Schuler, T. H., Denholm, I., Jouanin, L., Clark, S. J. and Poppy, G. M. (2001) Population scale laboratory studies of the effect of transgenic plants on non target insects. Molecular Ecology 10, 18451853.CrossRefGoogle Scholar
Simpson, D. M. and Duncan, E. N. (1956) Cotton pollen dispersal by insects. Agronomy Journal 48, 305308.CrossRefGoogle Scholar
Tomimatsu, H. and Ohara, M. (2003) Floral visitors of Trillium camschatcense (Trilliacea) in fragmented forests. Plant Species Biology 18, 123127.CrossRefGoogle Scholar
Toschki, A., Hothorn, L. A. and Rob-Nickoll, M. (2007) Effects of cultivation of genetically modified Bt maize on epigeic arthropods (Aranae Carabidae). Environmental Entomology 36, 967981.CrossRefGoogle Scholar
Umbeck, P. F., Barton, K. A., Nordheim, E. V., McCarty, J. C., Parott, W. L. and Jenkins, J. N. (1991) Degree of pollen dispersal by insects from a field test of genetically engineered cotton. Journal of Economic Entomology 84, 19431950.CrossRefGoogle Scholar
Van Deynze, A. E., Sundstrom, F. J. and Bradford, K. J. (2005) Pollen mediated gene flow in California depends on pollinator activity. Crop Science 45, 15651570.CrossRefGoogle Scholar
Waller, G. D., Vaissière, B. E., Moffet, J. O. and Martin, J. H. (1985) Comparison of carpenter bees (Xylocopa varipuncta Patton) (Hymenoptera: Antophoridae) and honey bees (Apis mellifera L.) (Hymenoptera: Apidae) as pollinators of male-sterile cotton in cages. Journal of Economic Entomology 78, 143150.CrossRefGoogle Scholar
Whitehouse, M. E., Wilson, L. J. and Fitt, G. P. (2005) A comparison of arthropod communities in transgenic Bt and conventional cotton in Australia. Environmental Entomology 34, 12241241.CrossRefGoogle Scholar
Wold, S. J., Burkness, E. C., Hutchinson, W. D. and Venette, R. C. (2001) In field monitoring of beneficial insect populations in transgenic corn expressing a Bacillus thuringiensis toxin. Journal of Entomological Science 36, 177187.CrossRefGoogle Scholar
Wolfenbarger, L., Naranjo, S. E., Lundgren, J. G., Bitzer, R. J. and Watrud, L. S. (2008) Bt crop effects on functional guilds of non-target arthropods: a meta-analysis. PLoS One, e2118doi 10.1371/journal.pone.0002118.CrossRefGoogle ScholarPubMed
Zhang, G.-F., Wan, F.-H., Lövei, G. L., Liu, W.-X. and Guo, Y.-Y. (2006 a) Transmission of Bt toxin to the predator Propylaea japonica (Coleoptera: Coccinellidae) through its aphid prey feeding on transgenic Bt cotton. Environmental Entomology 35, 143150.CrossRefGoogle Scholar
Zhang, S.-Y., Li, D.-M., Cui, J. and Xie, B.-Y. (2006 b) Effects of Bt-toxin Cry1Ac on Propylaea japonica Thunberg (Col., Coccinellidae) by feeding on Bt-treated Bt-resistant Helicoverpa armigera (Hübner) (Lep., Noctuidae) larvae. Journal of Applied Entomology 130, 206212.CrossRefGoogle Scholar