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Behavioral effects of insect-resistant genetically modified crops on phytophagous and beneficial arthropods: a review

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Abstract

Behavior is a main component of the survival and performance of arthropods. We have witnessed widespread adoption of insect-resistant genetically modified (IRGM) crops nowadays; however, no literature has reviewed the behavioral effects of IRGM crops on phytophagous and beneficial arthropods. In this review, we assessed the current information related to the effects of IRGM crops on arthropod behavior, mainly including locomotion (mobility, escape behavior and dispersal behavior), foraging (orientation, host plant selection/preference and feeding), mating, oviposition and other behaviors (associative learning). Almost all the studies have been conducted on Bt crops. The behavioral effects have been found in 54.2 %, 22 % and 33 % of the case studies on phytophagous arthropods, arthropod natural enemies and pollinators, respectively. Few behavioral studies have been documented on arthropod pollinators. The majority of cases reporting behavioral effects have derived from target phytophagous arthropods. Among them, locomotion and feeding behavior were the most frequently affected. For arthropod natural enemies, the cases using target prey/host in tri-trophic studies only accounted for a small proportion of behavioral effects observed on foraging behavior (host/prey selection). Overall, the effects through tri-trophic pathways on behaviors of natural enemies are limited. To conclude, while attention needs to be paid to several behavioral effects that may undermine the efficacy of IRGM crops in sustainable pest management, the behavioral effects generally do not disrupt the role of IRGM crops in achieving the goal of integrated pest management and crop production.

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Acknowledgments

We thank the anonymous referees for their valuable comments on the earlier versions of the manuscript.

Funding

This study partially supported by the FP7-PEOPLE-2012-IRSES fund (project ASCII, grant number: 318246), the FP7-PEOPLE-2013-IRSES fund (project APHIWEB, grant no. 611810) and a ‘becas-mixtas’ scholarship (no. 367437) from the Mexican Council for Science and Technology (CONACyT).

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Authors and Affiliations

  1. INRA (French National Institute for Agricultural Research), Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06903, Sophia Antipolis, France

    Peng Han & Nicolas Desneux

  2. Departamento de Producción Agrícola, CUCBA, Universidad de Guadalajara, Km. 15.5 Carr. Guadalajara-Nogales, Predio las Agujas, Zapopan, Jalisco, Mexico

    María Concepción Velasco-Hernández & Ricardo Ramirez-Romero

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  1. Peng Han
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Glossary

Associative learning behavior

The behavior involves the establishment, through experience, of an association between two stimuli or between a stimulus and a response.

Sublethal behavioral effects

The behavioral alteration in an arthropod individual that survives an exposure to plant materials containing genetically modified insect-resistant proteins or other toxic compounds.

Calling behavior

Acoustic signals displayed by males for the purpose of attracting mates and repelling rivals.

Dispersal behavior

The capacity of an arthropod in moving/flight and the potential for its spatial distribution.

Foraging behavior

The behavior of an arthropod searching for food, host or prey.

Refuge-in-the-bag

A tactic that planting of mixed Bt and non-Bt crops for preventing or delaying resistance evolution in target arthropod species.

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Han, P., Velasco-Hernández, M.C., Ramirez-Romero, R. et al. Behavioral effects of insect-resistant genetically modified crops on phytophagous and beneficial arthropods: a review. J Pest Sci 89, 859–883 (2016). https://doi.org/10.1007/s10340-016-0791-2

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