Skip to main content
SpringerLink
Log in

Bt Soybean Cry1Ac Does Not Affect Development, Reproduction, or Feeding Behavior of Red-Banded Stink Bug Piezodorus guildinii (Hemiptera: Pentatomidae)

  • Pest Management
  • Published:
Neotropical Entomology Aims and scope Submit manuscript

Abstract

Bt soybean cultivation is increasing worldwide. The Cry1Ac protein expressed in Bt soybean efficiently controls several lepidopteran pests. The stink bug, Piezodorus guildinii (Westwood), a major pest for soybean in the Americas, is not controlled by Bt crops, although possible sub-lethal effects may occur. Even if there were no negative effects for sting bug, ingesting toxins could affect its bio-controllers. We tested through ELISA detection if P. guildinii ingests Cry1Ac from Bt soybean and possible effects on its development, reproduction, survival, and feeding behavior. Biological traits were evaluated under controlled conditions of nymphs and adults feeding on pods of near-isogenic cultivars DM5958iPRO (Bt) and DM59i (non-Bt). Feeding behavior was recorded using an AC-DC electropenetrography (EPG) device. Results indicated that P. guildinii ingested the Cry1Ac protein; however, nymphal period and accumulated survival percentage did not differ between cultivars. Feeding on Bt soybean pods did not affect fecundity (i.e., number of egg masses and eggs/female) nor egg viability. Different feeding behaviors were only detected on the pathway phase (stylet penetration into plant tissue), which was more pronounced in the Bt cultivar. However, the total duration of the feeding activities on seeds was numerically higher (ca. 2X) on Bt plants compared to non-Bt. This is the first study to demonstrate that P. guildinii does ingest the Cry1Ac protein and excrete it without being absorbed, probably explaining the lack of direct adverse effects on its biological parameters. EPG could indicate that Bt soybean plants might be less palatable than non-Bt to red-banded stink bug.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

The data that support the findings of this study are available on demand.

References

  • Amutkan D, Suldudere Z, Candan S (2015) Ultrastructure of digestive canal of Graphosoma lineatum (Linnaeus, 1758) (Heteroptera: Pentatomidae). J Entomol Res Soc 17:75–96

    Google Scholar 

  • Backus EA, Bennett WH (2009) The AC-DC Correlation Monitor: new EPG design with flexible input resistors to detect both R and emf components for any piercing-sucking hemipteran. J Insect Physiol 55:869–884

    Article  CAS  PubMed  Google Scholar 

  • Baur ME, Sosa-Gomez DR, Ottea J, Leonard BR, Corso IC, Da Silva JJ, Temple J, Boethel DJ (2010) Susceptibility to insecticides used for control of Piezodorus guildinii (Heteroptera: Pentatomidae) in the United States and Brazil. J Econ Entomol 103:869–876

    Article  CAS  PubMed  Google Scholar 

  • Bayer (2022) Crop Science R&D Pipeline Update Webinar February 2022. https://www.bayer.com/en/investors/crop-science-rd-pipeline-update-webinar-2022-02. Accessed 9 Aug 2022

  • Bell HA, Down RE, Fitches EC, Edwards JP, Gatehouse AMR (2003) Impact of genetically modified potato expressing plant-derived insect resistance genes on the predatory bug Podisus maculiventris (Heteroptera: Pentatomidae). Biocontrol Sci Technol 13:729–741

    Article  Google Scholar 

  • Bell HA, Down RE, Edwards JP, Gatehouse JA, Gatehouse AMR (2005) Digestive proteolytic activity in the gut and salivary glands of the predatory bug Podisus maculiventris (Heteroptera: Pentatomidae); effect of proteinase inhibitors. Eur J Entomol 102:139–145

    Article  CAS  Google Scholar 

  • Bortolotto OC, Pomari-Fernandes A, Bueno RDF, Bueno ADF, da Kruz YKS, Queiroz AP, Sanzovo A, Ferreira RB (2015) The use of soybean integrated pest management in Brazil: a review. Agron Sci Biotechnol 1:25–32

    Article  Google Scholar 

  • Brandt SL, Coudron TA, Habibi J, Brown GR, Ilagan OM, Wagner RM, Wright MK, Backus EA, Huesing JE (2004) Interaction of two Bacillus thuringiensis δ-endotoxins with the digestive system of Lygus hesperus. Curr Microbiol 48:1–9

    Article  CAS  PubMed  Google Scholar 

  • Bueno AD, Panizzi AR, Hunt TE, Dourado PM, Pitta RM, Gonçalves J (2021) Challenges for adoption of integrated pest management (IPM): the soybean example. Neotrop Entomol 50:5–20

    Article  CAS  PubMed  Google Scholar 

  • Cervantes FA, Backus AE, Godfrey L, Rojas MG, Akbar W, Clark TL (2019) Quantitative differences in feeding behavior of Lygus lineolaris (Hemiptera: Miridae) on transgenic and nontransgenic cotton. J Econ Entomol 112:1920–1925

    Article  CAS  PubMed  Google Scholar 

  • Corrêa-Ferreira BS, de Azevedo J (2002) Soybean seed damage by different species of stink bugs. Agric for Entomol 4:145–150

    Article  Google Scholar 

  • da Cunha FM, Caetano FH, Wanderley-Teixeira V, Torres JB, Teixeira AAC, Alves LC (2012) Ultra-structure and histochemistry of digestive cells of Podisus nigrispinus (Hemiptera: Pentatomidae) fed with prey reared on Bt-cotton. Micron 43:245–250

    Article  PubMed  Google Scholar 

  • EnviroLogix (2013) QuickStik kit for quickscan cry1a(c) soy bulk soybean. Portland, USA, 11p.https://www.envirologix.com/wp-content/uploads/2018/04/AS075-STC-WS3-Cry1-1F-CP4-V3-021914.pdf. Accessed 20 Nov 2022

  • Fehr WR, Caviness CE (1977) Stages of soybean development. Iowa State University Special Report 87:929–931

  • Food and Agriculture Organization of the United Nations - FAOSTAT (2019) Production crops 2019.https://www.fao.org/faostat/en/#data/QCL. Accessed 20 Nov 2022

  • Jesus FGD, Junior ALB, Alves GC, Zanuncio JC (2014) Behavior, development, and predation of Podisus nigrispinus (Hemiptera: Pentatomidae) on Spodoptera frugiperda (Lepidoptera: Noctuidae) fed transgenic and conventional cotton cultivars. Ann Entomol Soc 107(3):601–606

    Article  Google Scholar 

  • Justiniano W, Fernandes MG, Viana CLTP (2014) Diversity, composition and population dynamics of arthropods in the genetically modified soybeans Roundup Ready® RR1 (GT 40-3-2) and Intacta RR2 PRO® (MON87701 x MON89788). J Agric Sci 6:33

    Google Scholar 

  • Lucini T, Panizzi AR, Backus EA (2016) Characterization of an EPG waveform library for redbanded stink bug, Piezodorus guildinii (Hemiptera: Pentatomidae), on soybean plants. Ann Entomol Soc Am 109:198–210

    Article  Google Scholar 

  • Olson DM, Ruberson JR, Zeilinger AR, Andow DA (2011) Colonization preference of Euschistus servus and Nezara viridula in transgenic cotton varieties, peanut, and soybean. Entomol Exp Appl 139:161–169

    Article  Google Scholar 

  • Panizzi AR, McPherson JE, James DG, Javahery M, McPherson RM (2000) Stink bugs (Pentatomidade). In: Schaefer CW, Panizzi AR (eds) Heteroptera of Economic Importance, 1st edn. CRC Press, Florida, pp 421–474

    Google Scholar 

  • Panizzi AR, Lucini T, Aldrich JR (2022) Dynamics in pest status of phytophagous stink bugs in the Neotropics. Neotrop Entomol 51:18–31

    Article  CAS  PubMed  Google Scholar 

  • Pons X, Lumbierres B, López C, Albajes R (2005) Abundance of nontarget pests in transgenic Bt-maize: a farm scale study. Eur J Entomol 102:73–79

    Article  CAS  Google Scholar 

  • Raps A, Kehr J, Gugerli P, Moar WJ, Bigler F, Hilbeck A (2001) Immunological analysis of phloem sap of Bacillus thuringiensis corn and of the nontarget herbivore Rhopalosiphum padi (Homoptera: Aphididae) for the presence of Cry1Ab. Mol Ecol 10:525–533

    Article  CAS  PubMed  Google Scholar 

  • Romeis J, Dutton A, Bigler F (2004) Bacillus thuringiensis toxin (Cry1Ab) has no direct effect on larvae of the green lacewing Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). J Insect Physiol 50:175–183

    Article  CAS  PubMed  Google Scholar 

  • Schünemann R, Roggia S, Muraro DS, Knaak N, Fiuza LM (2018) Insecticidal potential of Bacillus thuringiensis for the biological control of neotropical brown stink bug. Entomol Exp Appl 166:131–138

    Article  Google Scholar 

  • Silva GV, Pasini A, Bueno ADF, Bortolotto OC, Barbosa GC, Cruz YKS (2014) No impact of Bt soybean that express Cry1Ac protein on biological traits of Euschistus heros (Hemiptera, Pentatomidae) and its egg parasitoid Telenomus podisi (Hymenoptera, Platygastridae). Rev Bras Entomol 58:285–290

    Article  Google Scholar 

  • Sun J, Mooney H, Wu W, Tang H, Tong Y, Xu Z, Huang B, Cheng Y, Yang X, Wei D, Zhang F (2018) Importing food damages domestic environment: Evidence from global soybean trade. Proc Natl Acad Sci USA 115:5415–5419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Temple JH (2011) Redbanded stink bug, Piezodorus guildinii (Westwood): pest status, control strategies, and management in Louisiana soybean. Doctoral Dissertation, Baton Rouge, Louisiana State University, USA

  • Torres JB, Ruberson JR (2008) Interactions of Bacillus thuringiensis Cry1Ac toxin in genetically engineered cotton with predatory heteropterans. Transgenic Res 17:345–354

    Article  CAS  PubMed  Google Scholar 

  • Torres JB, Ruberson JR, Adang MJ (2006) Expression of Bacillus thuringiensis Cry1Ac protein in cotton plants, acquisition by pests and predators: a tritrophic analysis. Agric Entomol 8:191–202

    Article  Google Scholar 

  • Torres JB, Barros EM, Coelho RR, Pimentel RM (2010) Zoophytophagous pentatomids feeding on plants and implications for biological control. Arthropod Plant Interact 4:219–227

    Article  Google Scholar 

  • Wilson EB (1927) Probable inference, the law of succession, and statistical inference. J Am Stat Assoc 22:209–212

    Article  Google Scholar 

  • Yu H, Romeis J, Li Y, Li X, Wu K (2014) Acquisition of Cry1Ac protein by non-target arthropods in Bt soybean fields. PLoS ONE 9:1–8

    Google Scholar 

  • Zerbino MS, Panizzi AR (2019) The underestimated role of pest pentatomid parasitoids in Southern South America. Arthropod-Plant Interact 13:703–718

    Article  Google Scholar 

  • Zerbino MS, Altier N, Panizzi AR (2016) Performance of nymph and adult of Piezodorus guildinii (Westwood) (Hemiptera: Pentatomidae) feeding on cultivated legumes. Neotrop Entomol 45:114–122

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank “Dr. Mario A. Cassinoni” Experimental Station the Embrapa Unit at Passo Fundo, RS, for support.

Funding

This research was part of a scholarship from Agencia Nacional de Investigación e Innovación ANII-Uruguay (POS_NAC_2011_1_3559) and Comisión Académica de Posgrado CAP- Universidad de la República, Uruguay to SA.

Author information

Authors and Affiliations

  1. Est. Exp. “Dr. Mario A. Cassinoni”, Department of Plant Protection, Polo Agroalimentario y Agroindustrial Paysandú, Centro Universitario Regional Litoral Norte, Universidad de La República, Paysandú, Uruguay

    Silvana Abbate

  2. Deparment of Crop and Forest Sciences, Agrotecnio-Cerca Center, University of Lleida, Lleida, Spain

    Xavier Pons

  3. Plataforma de Bioinsumos, Instituto Nacional de Investigación Agropecuaria (INIA) Las Brujas, Canelones, Uruguay

    Nora Altier

  4. Laboratório de Entomología, Empresa Brasileira de Pesquisa Agropecuária (Embrapa) Trigo, Passo Fundo, RS, Brazil

    Tiago Lucini & Antônio Ricardo Panizzi

  5. Est. Exp. “Dr. Mario A. Cassinoni”, Department of Plant Protection, Facultad de Agronomía, Universidad de La República, Paysandú, Uruguay

    Sebastián Bonansea, Agustina Armand Pilón, Horacio Silva, Giuliana De Souza & Luciano Irigoyen

  6. Est. Exp. “Dr. Mario A. Cassinoni”, Department of Biometry and Statistics, Facultad de Agronomía, Universidad de La República, Paysandú, Uruguay

    Oscar Bentancur

Authors
  1. Silvana Abbate
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xavier Pons
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nora Altier
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tiago Lucini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sebastián Bonansea
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Oscar Bentancur
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Agustina Armand Pilón
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Horacio Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Giuliana De Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Luciano Irigoyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Antônio Ricardo Panizzi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SA, XP, NA, ARP, and TL conceived and designed the research. SA, ARP, TL, SB, AAP, HS, GDS, and LI co-worked on published data. OB, HS, and SA analyzed the data. SA wrote the paper with the contributions of ARP, XP, NA, TL, and HS. All authors read and approved the manuscript.

Corresponding author

Correspondence to Silvana Abbate.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Edited by Marcos R de Faria

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abbate, S., Pons, X., Altier, N. et al. Bt Soybean Cry1Ac Does Not Affect Development, Reproduction, or Feeding Behavior of Red-Banded Stink Bug Piezodorus guildinii (Hemiptera: Pentatomidae). Neotrop Entomol 53, 415–423 (2024). https://doi.org/10.1007/s13744-024-01128-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13744-024-01128-7

Keywords

Search

Navigation