Skip to main content
SpringerLink
Log in

Neighbouring crop diversity mediates the effect of Bt cotton on insect community and leaf damage in fields

  • Original Paper
  • Published:
Transgenic Research Aims and scope Submit manuscript

Abstract

Effects of large-scale cultivation of transgenic crops on agricultural biodiversity remain unclear, particularly in the context of complex ecological interactions between transgenic crops and other organisms. Here we conducted a comprehensive survey to investigate the number of species, population abundance, community evenness and dominance of insects and weeds as well as leaf damage to weeds in Bt and non-Bt cotton fields at 27 sites across northern China. The role of neighbouring crop diversity around cotton fields in controlling insects and weeds in the cotton fields was also assessed. In addition, we conducted a 3-year field experiment to verify the results of the survey. Weed diversity in Bt and non-Bt cotton fields was similar, but the species number and diversity indices of insects are significantly decreased in Bt fields aligning with reduced leaf damage to broadleaf plant species including cotton as well as crops in neighbouring plots. The leaf damage to Bt and non-Bt cotton negatively associates with the diversity of neighbouring crops in cotton fields. Our study demonstrates the neighbouring crop diversity mediates the effects of Bt crops on agricultural diversity in complex interactions among transgenic crops, in-field weed and insect communities, and neighbouring crops.

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

Similar content being viewed by others

References

  • Álvarez-Alfageme F, Bigler F, Romeis J (2010) 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46

    Google Scholar 

  • Andow DA, Zwahlen C (2006) Assessing environmental risks of transgenic plants. Ecol Lett 9:196–214

    Article  CAS  Google Scholar 

  • Arshad M, Suhail A (2010) Studying the sucking insect pests community in transgenic Bt cotton. Int J Agric Biol 12:764–768

    Google Scholar 

  • Balog A, Kiss J, Szekeres D, Szénási Á, Markó V (2010) Rove beetle (Coleoptera: Staphylinidae) communities in transgenic Bt (MON810) and near isogenic maize. Crop Prot 29:567–571

    Article  Google Scholar 

  • Baltazar BM et al (2015) Pollen-mediated gene flow in maize: implications for isolation requirements and coexistence in Mexico, the center of origin of maize. PLoS ONE 10:e0131549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bohan DA et al (2005) Effects on weed and invertebrate abundance and diversity of herbicide management in genetically modified herbicide-tolerant winter-sown oilseed rape. Philos Trans R Soc B Biol Sci 272:463–474

    Article  Google Scholar 

  • Carpenter JE (2011) Impact of GM crops on biodiversity. GM Crops 2:7–23

    Article  PubMed  Google Scholar 

  • Carriere Y, Fabrick JA, Tabashnik BE (2016) Can pyramids and seed mixtures delay resistance to Bt crops? Trends Biotechnol 34:291–302

    Article  CAS  PubMed  Google Scholar 

  • Carrière Y et al (2009) Landscape effects of transgenic cotton on non-target ants and beetles. Basic Appl Ecol 10:597–606

    Article  Google Scholar 

  • Chen M, Ye GY, Liu ZC, Fang Q, Hu C, Peng YF, Shelton AM (2009) Analysis of Cry1Ab toxin bioaccumulation in a food chain of Bt rice, an herbivore and a predator. Ecotoxicology 18:230–238

    Article  CAS  PubMed  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Ellstrand N et al (2013) Introgression of crop alleles into wild or weedy populations. Annu Rev Ecol Evol Syst 44:325–345

    Article  Google Scholar 

  • Heard MS et al (2003) Weeds in fields with contrasting conventional and genetically modified herbicide-tolerant crops. I. Effects on abundance and diversity. Philos Trans R Soc Ser B Biol Sci 358:1819–1832

    Article  CAS  Google Scholar 

  • ISAAA (2016) Global Status of Commercialized Biotech/GM Crops: 2016. ISAAA Brief 52: Ithaca, NY

  • Jin L, Zhang H, Lu Y, Yang Y, Wu K, Tabashnik BE, Wu Y (2015) Large-scale test of the natural refuge strategy for delaying insect resistance to transgenic Bt crops. Nat Biotechnol 33:169–174

    Article  CAS  PubMed  Google Scholar 

  • Kruger GR et al (2009) U.S. grower views on problematic weeds and changes in weed pressure in glyphosate-resistant corn, cotton, and soybean cropping Systems. Weed Technol 23:162–166

    Article  CAS  Google Scholar 

  • Lawo NC, Wackers FL, Romeis J (2010) Characterizing indirect prey-quality mediated effects of a Bt crop on predatory larvae of the green lacewing, Chrysoperla carnea. J Insect Physiol 56:1702–1710

    Article  CAS  PubMed  Google Scholar 

  • Li X, Liu B (2013) A 2-year field study shows little evidence that the long-term planting of transgenic insect-resistant cotton affects the community structure of soil nematodes. PLoS ONE 8:e61670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Wei W, Ma K, Li JS, Liang Y, Darmency H (2013) Consequences of gene flow between oilseed rape (Brassica napus) and its relatives. Plant Sci 211:42–51

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Li J, Neal Stewart C, Luo Z, Xiao N (2015) The effects of the presence of Bt-transgenic oilseed rape in wild mustard populations on the rhizosphere nematode and microbial communities. Sci Total Environ 530–531:263–270

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Liu F, Wang C, Quan Z, Li J (2016) Effects of Bt-transgenic rice cultivation on planktonic communities in paddy fields and adjacent ditches. Sci Total Environ 565:690–697

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Luo Z, Zhao Y, Xiao N (2019) The selective feeding of cotton bollworms (Helicoverpa armigera) on transgenic and non-transgenic cotton leaves from consecutive cultivation fields. Int J Pest Manag. https://doi.org/10.1080/09670874.2019.1603412

    Article  Google Scholar 

  • Lu Y et al (2010) Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science 328:1151–1154

    Article  CAS  PubMed  Google Scholar 

  • Lu Y, Wu K, Jiang Y, Guo Y, Desneux N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487:362–365

    Article  CAS  PubMed  Google Scholar 

  • Marquardt P, Krupke C, Johnson WG (2012) Competition of transgenic volunteer corn with soybean and the effect on western corn rootworm emergence. Weed Sci 60:193–198

    Article  CAS  Google Scholar 

  • Marvier M, McCreedy C, Regetz J, Kareiva P (2007) A meta-analysis of effects of Bt cotton and maize on nontarget invertebrates. Science 316:1475–1477

    Article  CAS  PubMed  Google Scholar 

  • Meissle M, Romeis J (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

    Article  CAS  Google Scholar 

  • Naranjo S (2005) Long-term assessment of the effects of transgenic Bt cotton on the function of the natural enemy community. Environ Entomol 34:1211–1223

    Article  CAS  Google Scholar 

  • Norris RF, Kogan M (2005) Ecology of interactions between weeds and arthropods. Annu Rev Entomol 50:479–503

    Article  CAS  PubMed  Google Scholar 

  • Ouyang F, Men X, Yang B, Su J, Zhang Y, Zhao Z, Ge F (2012) Maize benefits the predatory beetle, Propylea japonica (Thunberg), to provide potential to enhance biological control for aphids in cotton. PLoS ONE 7:e44379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parolin P, Bresch C, Poncet C, Desneux N (2012) Functional characteristics of secondary plants for increased pest management. Int J Pest Manag 58:369–377

    Article  Google Scholar 

  • Qiao F, Huang J, Rozelle S, Wilen J (2010) Natural refuge crops, buildup of resistance, and zero-refuge strategy for Bt cotton in China. Sci China Life Sci 53:1227–1238

    Article  PubMed  Google Scholar 

  • Romeis J, Meissle M, Bigler F (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat Biotechnol 24:63–71

    Article  CAS  PubMed  Google Scholar 

  • Rosi-Marshall EJ et al (2007) Toxins in transgenic crop byproducts may affect headwater stream ecosystems. Proc Natl Acad Sci USA 104:16204–16208

    Article  PubMed  Google Scholar 

  • Sanders CJ, Pell JK, Poppy GM, Raybould A, Garcia-Alonso M, Schuler TH (2007) Host-plant mediated effects of transgenic maize on the insect parasitoid Campoletis sonorensis (Hymenoptera: Ichneumonidae). Biol Control 40:362–369

    Article  Google Scholar 

  • Schuldt A et al (2010) Tree diversity promotes insect herbivory in subtropical forests of south-east China. J Ecol 98:917–926

    Article  PubMed  PubMed Central  Google Scholar 

  • Smagghe G et al (2012) Increased frequency of pink bollworm resistance to Bt toxin Cry1Ac in China. PLoS ONE 7:e29975

    Article  CAS  Google Scholar 

  • Tabashnik BE, Brévault T, Carrière Y (2013) Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol 31:510–521

    Article  CAS  PubMed  Google Scholar 

  • R Development Core team (2008). R: a language and environment for statistical computing

  • Whitehouse ME et al (2014) Target and nontarget effects of novel “triple-stacked” Bt-transgenic cotton 1: canopy arthropod communities. Environ Entomol 43:218–241

    Article  CAS  PubMed  Google Scholar 

  • Wolfenbarger LL, Naranjo SE, Lundgren JG, Bitzer RJ, Watrud LS (2008) Bt crop effects on functional guilds of non-target arthropods: a meta-analysis. PLoS ONE 3:e2118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu K (2007) Monitoring and management strategy for Helicoverpa armigera resistance to Bt cotton in China. J Invertebr Pathol 95:220–223

    Article  PubMed  Google Scholar 

  • Wu K, Guo Y (2005) The evolution of cotton pest management practices in China. Annu Rev Entomol 50:31–52

    Article  CAS  PubMed  Google Scholar 

  • Wu K, Lu Y, Feng H, Jiang Y, Zhao J (2008) Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin-containing cotton. Science 321:1676–1678

    Article  CAS  PubMed  Google Scholar 

  • Yu HL, Li YH, Wu KM (2011) Risk assessment and ecological effects of transgenic Bacillus thuringiensis crops on non-target organisms. J Integr Plant Biol 53:520–538

    Article  PubMed  Google Scholar 

  • Zeilinger AR, Olson DM, Andow DA (2016) Competitive release and outbreaks of non-target pests associated with transgenic Bt cotton. Ecol Appl 26:1047–1054

    Article  PubMed  Google Scholar 

  • Zhang H et al (2011) Early warning of cotton bollworm resistance associated with intensive planting of Bt cotton in China. PLoS ONE 6:e22874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Ma Y, Niu L, Ma W, Mannakkara A, Chen L, Lei C (2013) Bt cotton expressing Cry1Ac/Cry2Ab or Cry1Ac/epsps does not harm the predator Propylaea japonica through its prey Aphis gossypii. Agric Ecosyst Environ 179:163–167

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Mr. Huang H, Ms. Yao Y and Bao MX and local farmers for their assistance in field investigation as well as Dr. Ouyang F in insect identification and Dr. Zhang JL in weed identification. This work was financially supported by the National Environmental Protection Public Welfare Science and Technology Research Program of China (grant 201309038).

Author information

Authors and Affiliations

  1. State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, 8 Dayangfang, Beijing, 100012, China

    Yongbo Liu

  2. CSIRO Agriculture and Food, Black Mountain, Canberra, ACT, 2601, Australia

    Zhongkui Luo

Authors
  1. Yongbo Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhongkui Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Y.L. designed the study. Y.L. and J.L. performed the field investigation. Y.L. and Z.L. performed the analyses and wrote the paper. All authors contributed to interpreting the results and discussions and gave final approval for publication.

Corresponding author

Correspondence to Yongbo Liu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 1272 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Y., Luo, Z. Neighbouring crop diversity mediates the effect of Bt cotton on insect community and leaf damage in fields. Transgenic Res 28, 357–367 (2019). https://doi.org/10.1007/s11248-019-00155-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11248-019-00155-0

Keywords

Search

Navigation