Cited by 231Insect Resistance and GeneticsGenetically Modified Organisms ResearchInsect-Plant Interactions and Control

The DOI matches its Crossref record; 319 of the 352 references it cites were found in a registry or an index; 4 of the 176 sources its claims cite were checked for support.

Genetically engineered crops help support conservation biological control

Open access

Abstract

• Insecticidal Bt crops were grown on more than 100 million hectares in 2017. • Risk assessment considers exposure and toxicity of natural enemies to Bt proteins. • Bt proteins appear not to harm natural enemies. • Reduced insecticide use in Bt crops can enhance the conservation of natural enemies. • Bt technology represents a powerful tool for IPM. Genetically engineered (GE) crops producing insecticidal proteins from Bacillus thuringiensis (Bt) (mainly Cry proteins) have become a major control tactic for a number of key lepidopteran and coleopteran pests, mainly in maize, cotton, and soybean. As with any management tactic, there is concern that using GE crops might cause adverse effects on valued non-target species, including arthropod predators and parasitoids that contribute to biological control. Such potential risks are addressed prior to the commercial release of any new GE plant. Over the past 20+ years, extensive experience and insight have been gained through laboratory and field-based studies of the non-target effects of crops producing Cry proteins. Overall, the vast majority of studies demonstrates that the insecticidal proteins deployed today cause no unintended adverse effects to natural enemies. Furthermore, when Bt crops replace synthetic chemical insecticides for target pest control, this creates an environment supportive of the conservation of natural enemies. As part of an overall integrated pest management (IPM) strategy, Bt crops can contribute to more effective biological control of both target and non-target pests. The growing use of insecticidal seed treatments in major field crops (Bt or not) may dampen the positive gains realized through reductions in foliar and soil insecticides. Nonetheless, Bt technology represents a powerful tool for IPM.

Overview

AI snapshot

Written from the paper’s full text.

TL;DR

This review synthesizes 20+ years of evidence and concludes that Bt crops generally cause no unintended adverse effects on arthropod natural enemies and can support conservation biological control when they replace broad-spectrum insecticides. However, insecticidal seed treatments may dampen these benefits.

Key findings

  • Bt crops expressing Cry/Vip proteins were grown on 101 million hectares worldwide in 2017, with adoption above 80% in some regions; herbicide-tolerant GE crops were grown on 166.4 million hectares. Bt eggplant use in Bangladesh rose from 20 farmers in 2014 to over 27,000 in 2018.
  • Laboratory bitrophic studies covered 20 natural enemy species from 6 orders and 12 families; tritrophic studies with confirmed or expected exposure covered 6 hymenopteran parasitoids from 4 families, 32 predators from 12 families in 5 orders, and one entomopathogenic nematode. Meta-analysis found no negative effects of Bt plants/Cry proteins on natural enemies; parasitoid reproduction was higher on Bt-fed hosts, driven by a single study, and removing that study reduced the effect size to a non-significant 0.0633.
  • As of late 2008, over 63 field studies covering six classes, >21 orders, and >185 species concluded that nontarget effects of Bt crops are minimal or negligible, especially compared with insecticide use. A notable exception is specialist parasitoids in Bt maize, whose abundance may decline when their target hosts are effectively controlled.
  • In Arizona Bt cotton, the IPM strategy cumulatively saved growers over $500 million since 1996 ($274/ha/year) and prevented over 25 million pounds of active ingredient from being used; Bt cotton was described as a keystone technology enabling conservation biological control.

Methods

  • Narrative review with quantitative synthesis of laboratory bitrophic and tritrophic studies and field studies on Bt crops and natural enemies.
  • Meta-analysis of tritrophic studies used Hedge’s d, a random effects model, bias-corrected bootstrapped 95% confidence intervals, and MetaWin v2.1; only one independent metric per life-history trait was retained, and for multigeneration studies the final exposed generation was used.
  • Field evidence was summarized from prior meta-analyses and case studies in Bt cotton and Bt maize systems.

Limitations

  • Stated: agro-ecosystem complexity means indirect effects may only become visible once GE plants are grown in farmer fields; effects of herbicide-tolerant crop systems on arthropods and biological control are difficult to predict; insecticidal seed treatments may counteract gains from reduced foliar and soil insecticides; some claimed unexpected non-target effects were not verified and likely artifacts.
  • Stated/evident: Bt technology is largely limited to maize, cotton, and soybean and to relatively few countries in Europe and Africa, so conclusions depend on the available published studies.
  • Evident: this is a review with an embedded meta-analysis, not new empirical field or laboratory data; the parasitoid reproduction result was driven by a single study and became non-significant when that study was removed.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1016/j.biocontrol.2018.10.001

Cites

319 of 319 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Verification

Claims the paper makes

105 Not checked yet · 50 Own interpretation · 14 No basis given · 8 Own result · 5 Own method · 1 Supported so far · 1 Partly supported · accuracy not yet measured

Verify all 172 references — free account

Show all 115 claims

  • It may state two separate claims as one. 54
  • Probably not a substantial claim. 20
69 of 69
  • The paper relies on this without support.

    The published laboratory and field studies reviewed are representative and unbiased with respect to the non-target effects of Bt crops.

    “Over the past 20+ years, extensive experience and insight have been gained through laboratory and field-based studies of the non-target effects of crops producing Cry proteins.”
    “Overall, the vast majority of studies demonstrates that the insecticidal proteins deployed today cause no unintended adverse effects to natural enemies.”
  • The paper relies on this without support.

    In today's Bt-transgenic plants, expression of insecticidal genes is driven by constitutive promotors (e.g., CaMV 35s) and the proteins are constantly produced in most plant tissues.

    “In today's Bt-transgenic plants, the expression of the insecticidal genes is driven by constitutive promotors (i.e., CaMV 35s) and the proteins are constantly produced in most plant tissues.”
  • The paper relies on this without support.

    The CYP71A1 gene encodes an enzyme that catalyzes the conversion of tryptamine to serotonin.

    “The gene encodes for an enzyme that catalyzes the conversion of tryptamine to serotonin.”
3 of 3

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Items 201–319 of 319

Research works printed but not linked: 6

  1. CERA, 2012. A Review of the Environmental Safety of Vip3Aa. Center for Environmental Risk Assessment, ILSI Research Foundation, Washington DC, USA. Available online: <http://ilsi.org/wp-content/uploads/sites/5/2016/06/vip3Aa_EN.pdf>.
  2. CERA, 2013b. A Review of the Environmental Safety of the Cry1F Protein. Center for Environmental Risk Assessment, ILSI Research Foundation, Washington DC, USA. Available online: <http://ilsi.org/researchfoundation/wp-content/uploads/sites/5/2016/05/Cry1f-monograph.pdf>.
  3. EFSA Panel on Genetically Modified Organisms (GMO), 2009, EFSA J., 1149, 1
  4. Liu, 2014, Natural enemies delay insect resistance to Bt plants, PLoS One, 9
  5. Meissle, 2004, Implications for the parasitoid Campoletis sonorensis (Hymenoptera: Ichneumonidae) when developing in Bt maize-fed Spodoptera littoralis larvae (Lepidoptera: Noctuidae), IOBC/WPRS Bull., 27, 117
  6. Pertry, I., Sanou, E.I.R., Speelman, S., Ingelbrecht, I., 2016. The success story of Bt cotton in Burkina Faso: a role model for sustainable cotton production in other cotton growing countries? In: De Buck, S., Ingelbrecht, I., Heijde, M., Van Montagu, M. (Eds.), Innovative Farming and Forestry Across the Emerging World: The Role of Genetically Modified Crops and Trees. International Industrial Biotechnology Network (IIBN), e-book, pp. 81–93. Available online: <https://biblio.ugent.be/publication/8500337/file/8501700>.

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Metadata

Authors
Romeis, J., Naranjo, S. E., Meissle, M., & Shelton, A. M.
Affiliations
  • Agroscope (CH)
  • Agricultural Research Service (US)
  • Cornell University (US)
Corresponding author
Romeis, Jörg
Venue
Biological Control
Publisher
Elsevier BV
Published
2019-03
Volume
130
Pages
136-154
ISSN
1049-9644 (ISSN-L)
OpenAlex
W2894891153
Cited by
231
References
352
Citations by year
2026: 21 · 2025: 22 · 2024: 22 · 2023: 24 · 2022: 41 · 2021: 33 · 2020: 44 · 2019: 23
FWCI
9.00
Type
journal article
Language
en
Open access
Locations
Biological Control (publishedVersion, cc-by)
Funders
Agroscope
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Insect Resistance and Genetics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Genetically Modified Organisms Research
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
Keywords
Bt crops, Bacillus thuringiensis, Cry proteins, conservation biological control, natural enemies, non-target effects, insecticidal seed treatment, integrated pest management, insecticide reduction, genetically modified crops

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