Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
Review
. 2018 Jul 19;13(7):e0200131.
doi: 10.1371/journal.pone.0200131. eCollection 2018.

Effects of transgenic Bacillus thuringiensis cotton on insecticide use, heliothine counts, plant damage, and cotton yield: A meta-analysis, 1996-2015

Daniel Fleming  1 , Fred Musser  1 , Dominic Reisig  2 , Jeremy Greene  3 , Sally Taylor  4 , Megha Parajulee  5 , Gus Lorenz  6 , Angus Catchot  1 , Jeffrey Gore  7 , David Kerns  8 , Scott Stewart  9 , Deborah Boykin  10 , Michael Caprio  1 , Nathan Little  11
Affiliations
Free PMC article
Review

Effects of transgenic Bacillus thuringiensis cotton on insecticide use, heliothine counts, plant damage, and cotton yield: A meta-analysis, 1996-2015

Daniel Fleming et al. PLoS One. .
Free PMC article

Abstract

The primary management tactic for lepidopteran pests of cotton in the United States of America (USA) is the use of transgenic cotton that produces Bacillus thuringiensis Berliner (Bt) toxins. The primary target pests of this technology are Helicoverpa zea (Boddie) and Heliothis virescens (F.) in the eastern and central Cotton Belt of the USA. Concerns over the evolution of resistance in H. zea to Bt toxins and scrutiny of the necessity of Bt crops has escalated. We reviewed published and unpublished data from field trials of Bt cotton in the eastern and central Cotton Belt of the USA through 2015 to evaluate the effectiveness of Bt cotton (Bollgard, Bollgard II, WideStrike, WideStrike 3, and TwinLink). Bt cotton reduced insecticide usage, reduced heliothine pest numbers and damage, and provided a yield benefit, but Bollgard II and WideStrike efficacy declined in the Midsouth over the period evaluated. In the Southeastern region, heliothine damage remained constant through 2015, but yield benefits declined from 2010 until 2015. Resistance of H. zea to several Bt toxins is the most plausible explanation for the observed changes in Bt cotton efficacy. The introduction of new Bt toxins such as found in Widestrike 3 and Twinlink may preserve the benefits of Bt crops. However, while both Widestrike 3 and Twinlink had less damage than Widestrike, damage levels of both were similar to Bollgard II.

PubMed Disclaimer

Conflict of interest statement

While the agriculture industry did not fund the analysis presented in this manuscript, all the authors affiliated with a university routinely conduct research for Monsanto, Bayer CropSciences and Dow Agrosciences as well as other agrichemical companies. Most of the trial data reported in this manuscript was gathered as part of trials that were funded by these biotechnology companies. DF was a post-doc at Mississippi State University when most of the work was done and is currently employed by Provivi, Inc. Beyond providing his salary, Provivi, Inc did not have any role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. These competing interests do not alter the authors’ adherence to PLOS ONE policies on sharing data and materials.

Figures

Fig 1
Fig 1. Map of the eastern and central Cotton Belt of the United States indicating the regions and states of trial locations used for analyses in this paper.
Fig 2
Fig 2. Changes in insecticide applications and yield losses in cotton due to heliothine infestations in the eastern Cotton Belt of the United States, 1986–2015.
Compiled from Williams [1].
Fig 3
Fig 3. The PRISMA flow diagram[43].
Fig 4
Fig 4. Least square mean ± SE of the response ratio of heliothine counts among comparisons of transgenic Bacillus thuringiensis (Bt) and non-Bt cotton in trials from the eastern and central Cotton Belt of the United States.
Response ratio = ln ([Technology 1 meanx + 1] / [Technology 2 meanx + 1]). Comparisons marked by * indicate the technologies differed (t-test, p<0.05).
Fig 5
Fig 5. Least square mean ± SE of the response ratio of damage among comparisons of transgenic Bacillus thuringiensis (Bt) and non-Bt cotton in trials from the eastern and central Cotton Belt of the United States.
Response ratio = ln ([Technology 1 meanx + 1] / [Technology 2 meanx + 1]). Comparisons marked by * indicate the technologies differed (t-test, p<0.05).
Fig 6
Fig 6. Least square mean ± SE of the response ratio of yield among comparisons of transgenic Bacillus thuringiensis (Bt) and non-Bt cotton in trials from the eastern and central Cotton Belt of the United States.
Response ratio = ln ([Technology 1 meanx +1] / [Technology 2 meanx + 1]). Comparisons marked by * indicate the technologies differed (t-test, p<0.05).
Fig 7
Fig 7
Change over time of heliothine counts in Bollgard II (A) and WideStrike (B) cotton by region of the eastern and central Cotton Belt of the United States. Bollgard II Midsouth equation: 0.0429x - 1.5111, Southeast equation: 1.569x - 0.05243x2–12.1179; WideStrike Midsouth equation: 0.0750x - 1.8438, Southeast equation: 0.9008x - 0.03258x2–6.5835. Response ratio (A) = ln ([Bollgard II meanx + 1] / [non-Bt meanx + 1]); Response ratio (B) = ln ([WideStrike meanx + 1] / [non-Bt meanx + 1]).
Fig 8
Fig 8
Change over time of damage in Bollgard II (A) and WideStrike (B) cotton by region of the eastern and central Cotton Belt of the United States. Bollgard II Midsouth equation: 0.0759x - 2.7923; Southeast equation: -1.9273; WideStrike Midsouth equation: 0.0776x – 2.4088; Southeast equation: -1.214. Response ratio (A) = ln ([Bollgard II meanx + 1] / [non-Bt meanx + 1]); Response ratio (B) = (ln([WideStrike meanx + 1] / [non-Bt meanx + 1]).
Fig 9
Fig 9
Least square mean ± SE of the response ratio of region of Bollgard (A) and WideStrike 3 (B) damage data from trials in the eastern and central Cotton Belt of the United States. Regions not sharing the same uppercase letter are different (Least square means α = 0.05). Response ratio (A) = ln ([Bollgard meanx + 1] / [non-Bt meanx + 1]); Response ratio (B) = ln ([WideStrike 3 meanx + 1] / [non-Bt meanx + 1]).
Fig 10
Fig 10
Least square mean ± SE of the response ratio of plant part of Bollgard (A) and Bollgard II (B) damage data from trials in the eastern and central Cotton Belt of the United States. Plant parts not sharing the same uppercase letter are different (Least square means α = 0.05). Response ratio (A) = ln ([Bollgard meanx + 1] / [non-Bt meanx + 1]); Response ratio (B) = ln ([Bollgard II meanx + 1] / [non-Bt meanx + 1]).
Fig 11
Fig 11. Change over time of yield in Bollgard II cotton by region in trials from the eastern and central Cotton Belt of the United States.
Midsouth equation: 0.8941x - 0.02767x2–6.4911; Southeast equation: 0.7171x - 0.02489x2–4.1691. Response ratio = ln ([Bollgard II meanx + 1] / [non-Bt meanx + 1]).
Fig 12
Fig 12. Change over time of yield in WideStrike cotton in trials from the eastern and central Cotton Belt of the United States.
Equation: 0.593x - 0.01954x2–3.8209. Response ratio = ln ([WideStrike meanx + 1 ] / [non-Bt meanx + 1]).
Fig 13
Fig 13. Least square mean ± SE of the response ratio of region of Bollgard cotton yield in trials from the eastern and central Cotton Belt of the United States.
Regions not sharing the same uppercase letter are different (Least square means α = 0.05). Response ratio = ln ([Bollgard meanx + 1] / [non-Bt meanx + 1]).
Fig 14
Fig 14
Change over time of heliothine counts (A) and damage (B) of the comparison of Bollgard 2: WideStrike cotton in trials from the eastern and central Cotton Belt of the United States. Heliothine counts equation: 0.3345x - 0.01305x2–2.2011, Damage equation: -0.0303x - 0.0581. Response ratio (A and B) = ln ([Bollgard II meanx + 1] / [WideStrike meanx + 1]).
Fig 15
Fig 15. Least square mean ± SE of the response ratio of plant part of the comparison of Bollgard II: Bollgard damage in trials from the eastern and central Cotton Belt of the United States.
Plant parts not sharing the same uppercase letter are different (Least square means α = 0.05). Response ratio = ln ([Bollgard II meanx + 1] / [Bollgard meanx + 1]).
Fig 16
Fig 16
Least square mean ± SE of the response ratio of damage by region of (A) Bollgard II: WideStrike, (B) Bollgard II: WideStrike 3, (C) TwinLink: WideStrike, and (D) WideStrike 3: WideStrike comparisons in trials from the eastern and central Cotton Belt of the United States. Regions not sharing the same uppercase letter are different (Least square means α = 0.05). Response ratio (A) = ln ([Bollgard II meanx + 1] / [WideStrike meanx + 1]); Response ratio (B) = ln ([Bollgard II meanx + 1] / [WideStrike 3 meanx + 1]); Response ratio (C) = ln ([TwinLink meanx + 1] / [WideStrike meanx + 1]); Response ratio (D) = ln ([WideStrike 3 meanx + 1] / [WideStrike meanx + 1]).
Fig 17
Fig 17. Least square mean ± SE of the response ratio of damage by region of the Bollgard II: WideStrike comparison in trials from the eastern and central Cotton Belt of the United States.
Regions not sharing the same uppercase letter are different (Least square means α = 0.05). Response ratio = ln ([Bollgard II meanx + 1] / [WideStrike meanx + 1]).
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Williams MR. Cotton insect losses [Internet]. Mississippi State University; 1986–2015. [cited 2016 April 20]. Available from: http://www.entomology.msstate.edu/resources/cottoncrop.asp.
    1. Leigh TF, Roach SH, Watson TF. Biology and ecology of important insect and mite pests of cotton In: King EG, Phillips JR, Coleman RJ, editors. Cotton Insect and Mites: Characterization and Management. Memphis, TN: The Cotton Foundation; 1996. p. 17–85.
    1. Wechsler SJ. Recent trends in GE adoption 2017. Available from: https://www.ers.usda.gov/data-products/adoption-of-genetically-engineere....
    1. Parker Jr. CD. Temporal distribution of heliothines in corn-cotton cropping systems of the Mississippi Delta and relationships to yield and population growth [Dissertation]: Mississippi State University; 2000.
    1. Caprio MA, Luttrell RG, MacIntosh S, Rice ME, Siegfried B, Witkowski JF, et al. An evaluation of insect resistance management in Bt field corn: a science-based framework for risk assessment and risk management. Washington, D.C.: International Life Sciences Institute/Health and Environmental Sciences Institute; 1999.

Publication types

MeSH terms

Grants and funding

This project was partially funded through United States Department of Agriculture Specific Cooperative Agreement USDA-SCA 58-6402-3-038 received by FM. This agreement provided support in the form of salary for one author (DF). NL was the USDA representative overseeing the agreement who participated as a co-author from idea development through paper review. Additional support came from Mississippi State University Hatch Project MIS-311280 for the support of FM.

LinkOut - more resources