Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-26T12:59:58.991Z Has data issue: false hasContentIssue false

Development and reproduction of Spodoptera eridania (Lepidoptera: Noctuidae) and its egg parasitoid Telenomus remus (Hymenoptera: Platygastridae) on the genetically modified soybean (Bt) MON 87701×MON 89788

Published online by Cambridge University Press:  24 September 2014

O.C. Bortolotto
Affiliation:
Departamento de Zoologia, Universidade Federal do Paraná, Setor de Ciências Biológicas, CEP: 81531-980, Curitiba, PR, Brazil Embrapa Soja, Laboratório de Parasitoides, CEP 86001-970, Londrina, PR, Brazil
G.V. Silva
Affiliation:
Departamento de Zoologia, Universidade Federal do Paraná, Setor de Ciências Biológicas, CEP: 81531-980, Curitiba, PR, Brazil Embrapa Soja, Laboratório de Parasitoides, CEP 86001-970, Londrina, PR, Brazil
A. de Freitas Bueno*
Affiliation:
Embrapa Soja, Laboratório de Parasitoides, CEP 86001-970, Londrina, PR, Brazil
A.F. Pomari
Affiliation:
Embrapa Soja, Laboratório de Parasitoides, CEP 86001-970, Londrina, PR, Brazil Faculdade de Filosofia, Ciências e Letras, Departamento de Biologia, Universidade de São Paulo, CEP: 140414040-901, Ribeirão Preto, SP, Brazil
S. Martinelli
Affiliation:
Monsanto LLC, 800 North Lindbergh Blvd, Saint Louis, MO 63167, USA
G. P. Head
Affiliation:
Monsanto LLC, 800 North Lindbergh Blvd, Saint Louis, MO 63167, USA
R. A. Carvalho
Affiliation:
Monsanto do Brasil Ltda, Av. Nações Unidas, 12.901, São Paulo, SP 04578-910, Brazil
G.C. Barbosa
Affiliation:
Embrapa Soja, Laboratório de Parasitoides, CEP 86001-970, Londrina, PR, Brazil Faculdade Filadélfia, Curso de Agronomia, CEP: 86020-000, Londrina, PR, Brazil
*
*Author for correspondence Phone: +55 (43) 33716208 E-mail: [email protected]

Abstract

Genetically modified crops with insect resistance genes from Bacillus thuringiensis Berliner (Bt-plants) are increasingly being cultivated worldwide. Therefore, it is critical to improve our knowledge of their direct or indirect impact not only on target pests but also on non-target arthropods. Hence, this study evaluates comparative leaf consumption and performance of Spodoptera eridania (Cramer), a species that is tolerant of the Cry1Ac protein, fed with Bt soybean, MON 87701×MON 89788 or its non-Bt isoline. We also assessed the comparative performance of the egg parasitoid Telenomus remus Nixon on eggs of S. eridania produced from individuals that fed on these two soybean isolines as larvae. Results showed that Bt soybean reduced by 2 days larval development and increased by 3 days adult male longevity. Therefore, we conclude that the effect of Bt soybean MON 87701×MON 89788 on S. eridania development and reproduction is small, and favorable to pest development. These differences are less likely to directly result from the toxin presence but indirectly from unintended changes in plant characteristics caused by the insertion of the transgene. Our results should be viewed as an alert that S. eridania populations may increase in Bt soybeans, but on the other hand, no adverse effects of this technology were observed for the egg parasitoid T. remus which can help to prevent S. eridania outbreaks on these crops.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adamczyk, J.J., Greenberg, S., Armstrong, J.S., Mullins, W.J., Braxton, L.B., Lassiter, R.B. & Siebert, M.W. (2008) Evaluations of Bollgard®, Bollgard II®, and Widestrike® technologies against beet and fall armyworm larvae (Lepidoptera: Noctuidae). Florida Entomologist 91, 531536.Google Scholar
Berman, K.H., Harrigan, G.G., Riordan, S.G., Nemet, M.A., Hanson, C., Smith, M. & Sorbet, R. (2010) Compositions of forage and seed from second-generation glyphosate-tolerant soybean MON 89788 and insect-protected soybean MON 87701 from Brazil are equivalent to those of conventional soybean (Glycine max). Journal of Agriculture and Food Chemistry 58, 62706276.CrossRefGoogle ScholarPubMed
Bernardi, O., Malvestiti, G.S., Dourado, P.M., Oliveira, W.S., Martinelli, S., Berger, G.U., Head, G.P. & Omoto, C. (2012) Assessment of the high-dose concept and level of control provided by MON 87701×MON 89788 soybean against Anticarsia gemmatalis and Pseudoplusia includens (Lepidoptera: Noctuidae) in Brazil. Pest Management Science 68, 10831091.Google Scholar
Bernardi, O., Sorgatto, R.J., Barbosa, A.D., Domingues, F.A., Dourado, P.M., Carvalho, R.A., Martinelli, S., Head, G.P. & Omoto, C. (2014) Low susceptibility of Spodoptera cosmioides, Spodoptera eridania and Spodoptera frugiperda (Lepidoptera: Noctuidae) to genetically-modified soybean expressing Cry1Ac protein. Crop protection 58, 3340.Google Scholar
Bueno, R.C.O.F., Carneiro, T.R., Bueno, A.F., Pratissolli, D., Fernandes, O.A. & Vieira, S.S. (2010 a) Parasitism capacity of Telenomus remus Nixon (Hymenoptera: Scelionidae) on Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) eggs. Brazilian Archives of Biology and Technology 53, 133139.CrossRefGoogle Scholar
Bueno, R.C.O.F., Carneiro, T.R., Pratissolli, D., Bueno, A.F. & Fernandes, O.A. (2010 b) Biology and thermal requirements of Telenomus remus reared on fall armyworm Spodoptera frugiperda eggs. Ciência Rural 38, 16.CrossRefGoogle Scholar
Bueno, R.C.O.F., Bueno, A.F., Moscardi, F., Parra, J.R.P. & Hoffmann-Campo, C.B. (2011) Lepidopteran larva consumption of soybean foliage: basis for developing multiple-species economic thresholds for pest management decisions. Pest Management Science 67, 160164.Google ScholarPubMed
Burr, I.W. & Foster, L.A. (1972) A Test for Equality of Variances. Mimeo Series No. 282, 26 p. West Lafayette, University of Purdue.Google Scholar
Carpenter, J.E. & Gianessi, L.P. (2001) Agricultural Biotechnology: Updated Benefit Estimates, pp. 148. National Center for Food and Agricultural Policy, Available at: http://ucbiotech.org/biotech_info/PDFs/Carpenter_2001_Updated_Benefits.pdf.Google Scholar
Cattaneo, M.G., Yafuso, C., Schmidt, C., Huang, C.H. & Rahman, M. (2006) Farm-scale evaluation of the impacts of transgenic cotton on biodiversity, pesticide use, and yield. Proceedings of the National Academy of Sciences of the USA 103, 75717576.Google Scholar
Comissão Técnica Nacional de Biossegurança (2010) Ministério da Ciência & Tecnologia.Google Scholar
Delaney, K.J. (2012) Nerium oleander indirect leaf photosynthesis and light harvesting reductions after clipping injury or Spodoptera eridania herbivory: high sensitivity to injury. Plant Science 185–186, 218226.CrossRefGoogle ScholarPubMed
Dhillon, M.K. & Sharma, H.C. (2013) Comparative studies on the effects of Bt-transgenic and non-transgenic cotton on arthropod diversity, seed cotton yield and bollworms control. Journal of Environmental Biology 34, 6773.Google Scholar
Faria, C.A., Wackers, F.L., Pritchard, J., Barrett, D.A. & Turlings, T.C.J. (2007) High susceptibility of Bt maize to aphids enhances the performance of parasitoids of lepidopteran pests. PLoS ONE 7, 111.Google Scholar
Fehr, W.R. & Caviness, C.E. (1977) Stages of Soybean Development. Ames, University of Science and Technology, Special Report 80, p. 11.Google Scholar
Greenberg, S.M., Li, Y.X. & Liu, T.X. (2010) Effect of age of transgenic cotton on mortality of lepidopteran larvae. Southwestern Entomologist 35, 261268.Google Scholar
Hansen, L.S., Gabor, Lovei, L. G. & Szekacs, A. (2012) Survival and development of a stored-product pest, Sitophilus zeamais (Coleoptera: Curculionidae), and its natural enemy, the parasitoid Lariophagus distinguendus (Hymenoptera: Pteromalidae), on transgenic Bt maize. Pest Management Science 69, 602606.CrossRefGoogle Scholar
Head, G., Carrol, M., Clark, T., Galvan, T., Huckaba, R.M., Price, P., Samuel, L. & Storer, N.P. (2014) Efficacy of SmartStax insect-protected corn hybrids against corn rootworm: The value of pyramiding the Cry3Bb1 and Cry34/35Ab1 proteins. Crop Protection 57, 3847.Google Scholar
Hoffmann-Campo, C.B., Ramos Netro, J.A., Oliveira, M.C.N. & Oliveira, L.J. (2006) Detrimental effect of rutin on Anticarsia gemmatalis . Pesquisa Agropecuária Brasileira 41, 14531459.Google Scholar
Hutchison, W.D., Burkness, E.C., Mitchell, P.D., Moon, R.D., Leslie, T.W., Fleischer, S.J., Abrahamson, M., Hamilton, K.L., Steffey, K.L., Gray, M.E., Hellmich, R.L., Kaster, L.V., Hunt, T., Wright, R.J., Pecinovsky, K., Rabaey, T.L., Flood, B.R. & Saun, E.S. (2010) Area wide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers. Science 330, 222225.Google Scholar
James, C. (2013) Global Status of Commercialized Biotech/GM Crops. Executive Summary, 13 p. Ithaca, ISAAA Briefs.Google Scholar
Kim, Y.S., Roh, J.Y., Kang, J.N., Wang, Y., Shim, H.J., Li, M.S., Choi, J.Y. & Je, Y.H. (2008) Mutagenesis of Bacillus thuringiensis cry1Ac gene and its insecticidal activity against Plutella xylostella and Ostrinia furnacalis . Biological Control 47, 222227.CrossRefGoogle Scholar
Kouser, S. & Qaim, M. (2011) Impact of Bt cotton on pesticide poisoning in smallholder agriculture: a panel data analysis. Ecological Economics 70, 21052113.Google Scholar
Liu, X.X., Sun, C.G. & Zhang, Q.W. (2005 a) Effects of transgenic Cry1A+CpTI cotton and Cry1Ac toxin on the parasitoid, Campoletis chlorideae (Hymenoptera: Ichneumonidae). Insect Science 12, 101107.CrossRefGoogle Scholar
Liu, X.X., Zhang, Q.W., Zhao, J.Z., Cai, Q.N., Xu, H.L. & Li, J.C. (2005 b) Effect of the Cry1Ac toxin of Bacillus thunringiensis on Microplitis mediator, a parasitoid of the cotton bollworm (Helicoverpa armigera). Entomologia Experimentalis et Applicata 114, 205213.Google Scholar
Lu, Y., Wu, K., Jiang, Y., Guo, Y. & Desneux, L. (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487, 362367.Google Scholar
Luttrell, R.G., Wan, L. & Knighten, K. (1999) Variation in susceptibility of noctuid larvae (Lepidoptera) attacking cotton and soybean to purified endotoxin proteins and commercial formulations of Bacillus thuringiensis . Journal of Economic Entomology 92, 2132.Google Scholar
Michereff-Filho, M., Torres, J.B., Andrade, L.N.T. & Nunes, M.U. (2008) Effect of some biorational insecticides on Spodoptera eridania in organic cabbage. Pest Management Science 64, 761767.CrossRefGoogle ScholarPubMed
Miranda, R., Zamudio, F.Z. & Bravo, A. (2001) Processing of Cry1Ab delta-endotoxin from Bacillus thuringiensis by Manduca sexta and Spodoptera frugiperda midgut proteases: role in protoxin activation and toxin inactivation. Insect Biochemistry and Molecular Biology 31, 11551163.Google Scholar
Morales, J., Gallardo, J.S., Vásquez, C. & Rios, Y. (2000) Patrón de emergência, longevidad, parasitismo y proporción sexual de Telenomus remus (Hymenoptera: Scelionidae) com relación al cogollero del maíz. Bioagro 12, 4754.Google Scholar
Motavalli, P.P., Kremer, R.J., Fang, M. & Means, N.E. (2004) Impact of genetically modified crops and their management on soil microbially mediated plant nutrient transformation. Journal of Environmental Quality 33, 816824.Google Scholar
Naranjo, S.E. (2009) Impacts of Bt crops on non-target organisms and insecticide use patterns. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 4, 121.Google Scholar
Pomari, A.F., Bueno, A.F., Bueno, R.C.O.F. & Menezes, A.O.M. (2012) Biological characteristics and thermal requirements of the biological control agent Telenomus remus (Hymenoptera: Platygastridae) reared on eggs of different species of the genus Spodoptera (Lepidoptera: Noctuidae). Annals of Entomological Society of America 105, 7381.CrossRefGoogle Scholar
Pons, X., Lumbierres, B., Lopez, C. & Albajes, R. (2005) Abundance of non-target pests in transgenic Bt-maize: a farm scale study. European Journal of Entomology 102, 7379.Google Scholar
Rahman, K., Abdullah, M.A.F., Ambati, S., Taylor, M.D. & Adang, M.J. (2012) Differential protection of Cry1Fa toxin against Spodoptera frugiperda larval gut proteases by cadherin orthologs correlates with increased synergism. Applied Environmental Microbiology 78, 354362.Google Scholar
Romeis, J., Meissle, M. & Bigler, F. (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nature Biotechnology 24, 6371.Google Scholar
Sanders, C.J., Pell, J.K., Poppy, G.M., Raybould, A., Garcia-Alonso, M. & Schuler, T.H. (2007) Host-plant mediated effects of transgenic maize on the insect parasitoid Campoletis sonorensis (Hymenoptera: Ichneumonidae). Biological Control 40, 362369.Google Scholar
Santos, K.B., Neves, P.M.O.J. & Meneguim, A.M. (2005) Biologia de Spodoptera eridania (Cramer) (Lepidoptera: Noctuidae) em diferentes hospedeiros. Neotropical Entomology 34, 903910.Google Scholar
Santos, K.B. dos, Neves, P.M.O.J., Meneguim, A.M., Santos, R.B., Santos, W.J., Villas Boas, G., Dumas, V., Martins, E., Praça, L.B., Queiroz, P., Colin Berry, C. & Monnerat, R. (2009) Selection and characterization of the Bacillus thuringiensis strains toxic to Spodoptera eridania (Cramer), Spodoptera cosmioides (Walker) and Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae). Biological Control 50, 157163.Google Scholar
SAS (2001) User's Guide: Statistics. 6th edn. Cary, NC, SAS Institute.Google Scholar
Schnepf, E., Crickmor, N., Van Rie, J., Lereclus, D., Baum, J., Feitelson, J., Zeigler, D.R. & Dean, D.H. (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbial Molecular Biology Research 62, 775806.Google Scholar
Shapiro, S.S. & Wilk, M.B. (1965) An analysis of variance test for normality. Biometrika 52, 591611.CrossRefGoogle Scholar
Sisterson, M.S., Biggs, R.W., Manhardt, N.M., Carrière, Y., Dennehy, T.J. & Tabashnik, B.E. (2007) Effects of transgenic Bt cotton on insecticide use and abundance of two generalist predators. Entomologia Experimentalis et Applicata 124, 305311.CrossRefGoogle Scholar
Zurbrugg, C., Honemann, L., Meissle, M., Romeis, J. & Nentwig, W. (2010) Decomposition dynamics and structural plant components of genetically modified Bt maize leaves do not differ from leaves of conventional hybrids. Transgenic Research 19, 257267.CrossRefGoogle Scholar
Van den Berg, J. & Van Wyk, A. (2006) The effect of Bt maize on Sesamia calamistis in South Africa. Entomologia Experimentalis et Applicata 122, 4551.CrossRefGoogle Scholar
Vojtech, E., Meissle, M. & Poppy, G.M. (2005) Effects of Bt maize on the herbivore Spodoptera littoralis (Lepidoptera: Noctuidae) and the parasitoid Cotesia marginiventris (Hymenoptera: Bracondiae). Transgenic Research 14, 133144.Google Scholar
Wolfenbarger, L.L., Naranjo, S.E., Lundgren, J.G., Bitzer, R.J. & Watrud, L.S. (2008) Bt crop effects on functional guilds of non-target arthropods: a meta-analysis. PLoS ONE 3, e-2118.Google Scholar
Yu, H.L., Yun, H.L. & Kong, M.W. (2011) Risk assessment and ecological effects of transgenic Bacillus thuringiensis crops on non-target organisms. Journal of Integrative Plant Biology 53, 520538.Google Scholar
Yu, H., Li, Y., Li, X., Romeis, J. & Wu, K. (2013) Expression of Cry1Ac in transgenic Bt soybean lines and their efficiency in controlling lepidopteran pests. Pest Management Science 69, 13261333.Google Scholar
Zhang, S.Y., Fie, B.Y., Cui, J. & Li, D.M. (2006) Biology of Campoletis chlorideae (Uchida) (Hym.: Ichneumonidae) developing in Bt-treated, Bt-resistant Helicoverpa armigera (Hübner) (Lep.: Noctuidae) larvae. Journal of Applied Entomology 130, 268274.Google Scholar
Zhao, J.H., Ho, P. & Azadi, H. (2011) Benefits of Bt cotton counterbalanced by secondary pests? Perceptions of ecological change in China. Environmental Monitoring and Assessment 173, 985994.CrossRefGoogle ScholarPubMed