Does the growing of Bt maize change abundance or ecological function of non-target animals compared to the growing of non-GM maize? A systematic review

Authors: MEISSLE, MICHAEL - Agroscope; Naranjo, Steven; ROMEIS, JOERG - Agroscope

Submitted to: Environmental Evidence
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/20/2022
Publication Date: 6/6/2022
Citation: Meissle, M., Naranjo, S.E., Romeis, J. 2022. Does the growing of Bt maize change abundance or ecological function of non-target animals compared to the growing of non-GM maize? A systematic review. Environmental Evidence. 11. Article 21. https://doi.org/10.1186/s13750-022-00272-0.
DOI: https://doi.org/10.1186/s13750-022-00272-0

Interpretive Summary: Transgenic crops producing the insecticidal protein from a common soil bacteria Bacillus thuringiensis (Bt) have revolutionized crop protection in agriculture. Maize is cultivated worldwide and Bt maize for protection against caterpillar and root-feeding beetle pests is grown in 14 countries. Before a transgenic crop can be commercially cultivated it must undergo a rigorous environmental risk assessment. As a result, hundreds of studies have been conducted in the private and public sector to assess potential non-target impacts on organisms that live in maize fields and surrounding areas. This study presents a systematic review of this literature to answer the question: “Does the growing of Bt maize change abundance or ecological function of non-target animals compared with the growing of non-GM maize?”. An extensive and rigorous literature search was conducted to identify relevant studies to answer this question. We developed a custom-made database that contained quantitative data on invertebrate abundance, activity density (from various traps), or predation/parasitism rates. Additional data not fitting the database criteria were captured for a narrative summary. A critical appraisal process was applied to each record in the database to estimate the risk of bias and the suitability to answer the review question. We then used the quantitative data to perform meta-analyses on different taxonomic levels and ecological functional groups. Meta-analysis is a robust and powerful method to quantify and summarize the results of multiple studies all addressing the same question. The final database contained 120 studies involving 233 field experiments with a total of >7200 records. Untreated Bt maize was either compared to untreated non-Bt maize, or to insecticide-treated non-Bt maize. We also examined the influence of private involvement and peer review on reported effects. Meta-analyses on different taxonomic levels revealed few effects when both Bt maize and non-Bt maize were not treated with insecticides. Bt maize field harboured fewer parasitoids of the European corn borer, the main target pest of Lepidoptera-active Bt maize, compared to non-Bt maize. We also found fewer sap beetles in Bt maize fields. In some analyses, we found a weak adverse effect of Bt maize for rove beetles and hoverflies but a positive effect for ladybeetles. These effects were not consistent in different sensitivity analyses, indicated that one or a few studies could have biased the outcome. Arthropod predators as a group were more abundant in Bt maize when compared to non-Bt maize that used insecticides to control the pest targeted by the Bt trait. The results of the narrative summary confirmed the outcome of meta-analyses and there was no evidence for publication bias or an influence of industry-sponsored studies. Our results largely confirmed other published meta-analysis and narrative summaries, but with a much more comprehensive database. Compared to the effects of broad-spectrum insecticide treatments, the effect of Bt maize on the community of non-target animals is generally negligible. This information will be of value to scientists, pest manager, governmental regulatory bodies and the public at large concerned about the effects on biotechnology on the environment.

Technical Abstract: Background: Hundreds of studies on environmental effects of genetically modified (GM) crops have been published over the past 25 years. Although meta-analyses on non-target effects of GM crops producing insecticidal protein from Bacillus thuringiensis (Bt) have been published, many field studies from Europe and other parts of the world have been published in the last decade, and those data are often not covered by previous meta-analyses. Therefore, we conducted a systematic review to answer the question: “Does the growing of Bt maize change abundance or ecological function of non-target animals compared to the growing of non-GM maize?” Methods: Literature was searched systematically in multiple bibliographic databases, specialized homepages, and reference sections of review articles. Defined inclusion criteria were applied to screen titles, abstracts, and full texts of the retrieved references. A custom-made database was developed with quantitative data on invertebrate abundance, activity density, or predation/parasitism rates. Data not fitting the database were captured in tables for the narrative summary. Critical appraisal was applied to each record in the database to estimate the risk of bias and the suitability to answer the review question. Meta-analyses on different taxonomic levels and functional groups were conducted. Untreated Bt maize was either compared to untreated non-Bt maize, or to insecticide-treated non-Bt maize. The influence of private involvement and peer review on reported effects was investigated. Review findings: The database on non-target effects of Bt maize field trials contains more than 7200 records from 120 publications. Meta-analyses on different taxonomic levels revealed only few effect sizes significantly different to zero when both Bt maize and non-Bt maize were not treated with insecticides. Bt maize harboured fewer parasitoids (Braconidae, Tachinidae) of the European corn borer, the main target pest of Lepidoptera-active Bt maize compared to non-Bt maize. Similarly, sap beetles (Nitidulidae), that are associated with Lepidoptera damage, were recorded less in Bt maize. In some analyses, a weak adverse effect of Bt maize was observed for rove beetles (Staphylinidae) and hoverflies (Syrphidae) and a positive effect for ladybeetles (Coccinellidae). However, those effects were not consistent for the different analyses we conducted and vanished with the removal of individual significant studies. More effects on different taxonomic groups, in particular predators, were evident when untreated Bt maize was compared to pyrethroid-treated non-Bt maize. The results of the narrative summary confirmed the outcome of meta-analyses. There was no evidence for publication bias. Conclusions: Although the extensive dataset available today allowed more detailed meta-analyses than previously, the current work largely confirmed published results. Compared to the effects of broad-spectrum pyrethroid insecticide treatments, the effect of Bt maize on the community of non-target animals is generally negligible.