Abstract
Biocontrol solutions (macroorganisms, microorganisms, natural substances, semiochemicals) are presented as potential alternatives to conventional plant protection products (PPPs) because they are supposed to have lower impacts on ecosystems and human health. However, to ensure the sustainability of biocontrol solutions, it is necessary to document the unintended effects of their use. Thus, the objectives of this work were to review (1) the available biocontrol solutions and their regulation, (2) the contamination of the environment (soil, water, air) by biocontrol solutions, (3) the fate of biocontrol solutions in the environment, (4) their ecotoxicological impacts on biodiversity, and (5) the impacts of biocontrol solutions compared to those of conventional PPPs. Very few studies concern the presence of biocontrol solutions in the environment, their fate, and their impacts on biodiversity. The most important number of results were found for the organisms that have been used the longest, and most often from the angle of their interactions with other biocontrol agents. However, the use of living organisms (microorganisms and macroorganisms) in biocontrol brings a specific dimension compared to conventional PPPs because they can survive, multiply, move, and colonize other environments. The questioning of regulation stems from this specific dimension of the use of living organisms. Concerning natural substances, the few existing results indicate that while most of them have low ecotoxicity, others have a toxicity equivalent to or greater than that of the conventional PPPs. There are almost no result regarding semiochemicals. Knowledge of the unintended effects of biocontrol solutions has proved to be very incomplete. Research remains necessary to ensure their sustainability.
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References
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EFSA (European Food Safety Authority), Anastassiadou M, Arena M, Auteri D, Brancato A, Bura L, Cabrera LC, Chaideftou E, Chiusolo A, Crivellente F, De Lentdecker C, Egsmose M, Fait G, Greco L, Ippolito A, Istace F, Jarrah S, Kardassi D, Leuschner R, Lostia A, Lythgo C, Magrans O, Mangas I, Miron I, Molnar T, Padovani L, Morte JMP, Pedersen R, Reich H, Santos M, Sharp R, Sturma J, Szentes C, Terron A, Tiramani M, Vagenende B, Villamar-Bouza L (2020a) Peer review of the pesticide risk assessment of the active substance abamectin. EFSA J 18:28. https://doi.org/10.2903/j.efsa.2020.6227
EFSA (European Food Safety Authority), Anastassiadou M, Maria A, Auteri D, Brancato A, Bura L, Carrasco Cabrera L, Chaideftou E, Chiusolo A, Marques DC, Crivellente F, De Lentdecker C, Egsmose M, Fait G, Greco L, Ippolito A, Istace F, Jarrah S, Kardassi D, Leuschner R, Lostia A, Lythgo C, Magrans O, Mangas I, Miron I, Molnar T, Padovani L, Parra Morte JM, Pedersen R, Reich H, Santos M, Serafimova R, Sharp R, Stanek A, Sturma J, Szentes C, Terron A, Tiramani M, Vagenende B, Villamar-Bouza L (2020b) Conclusion on the peer review of the pesticide risk assessment of the active substance kieselgur (diatomaceous earth). EFSA J 18:6054. https://doi.org/10.2903/j.efsa.2020.6054
EFSA (European Food Safety Authority), Anastassiadou M, Arena M, Auteri D, Brancato A, Bura L, Carrasco Cabrera L, Chaideftou E, Chiusolo A, Marques DC, Crivellente F, De Lentdecker C, Egsmose M, Fait G, Greco L, Ippolito A, Istace F, Jarrah S, Kardassi D, Leuschner R, Lostia A, Lythgo C, Magrans O, Mangas I, Miron I, Molnar T, Padovani L, Parra Morte JM, Pedersen R, Reich H, Santos M, Serafimova R, Sharp R, Stanek A, Sturma J, Szentes C, Terron A, Tiramani M, Vagenende B, Villamar-Bouza L (2020c) Conclusion on pesticides peer review of the pesticide risk assessment of the active substance garlic extract. EFSA J 18:6116. https://doi.org/10.2903/j.efsa.2020.6116
EFSA (European Food Safety Authority), Anastassiadou M, Arena M, Auteri D, Brancato A, Bura L, Carrasco Cabrera L, Chaideftou E, Chiusolo A, Court Marques D, Crivellente F, De Lentdecker C, Egsmose M, Fait G, Greco L, Ippolito A, Istace F, Jarrah S, Kardassi D, Leuschner R, Lostia A, Lythgo C, Magrans O, Mangas I, Miron I, Molnar T, Padovani L, Parra Morte JM, Pedersen R, Reich H, Santos M, Serafimova R, Sharp R, Stanek A, Sturma J, Szentes C, Terron A, Tiramani M, Vagenende B, Villamar-Bouza L (2020d) Conclusion on the peer review of the pesticide risk assessment of the active substance blood meal. EFSA J 18:6006. https://doi.org/10.2903/j.efsa.2020.6006
EFSA (European Food Safety Authority), Anastassiadou M, Arena M, Auteri D, Brancato A, Bura L, Cabrera LC, Chaideftou E, Chiusolo A, Crivellente F, De Lentdecker C, Egsmose M, Fait G, Greco L, Ippolito A, Istace F, Jarrah S, Kardassi D, Leuschner R, Lostia A, Lythgo C, Magrans O, Mangas I, Miron I, Molnar T, Padovani L, Morte JMP, Pedersen R, Reich H, Santos M, Sharp R, Szentes C, Terron A, Tiramani M, Vagenende B, Villamar-Bouza L, EFSA (2021a) Peer review of the pesticide risk assessment of the active substance Bacillus amyloliquefaciens strain QST 713 (formerly Bacillus subtilis strain QST 713). EFSA J 19:6381. https://doi.org/10.2903/j.efsa.2021.6381
EFSA (European Food Safety Authority), Alvarez F, Arena M, Auteri D, Borroto J, Brancato A, Carrasco Cabrera L, Castoldi AF, Chiusolo A, Colagiorgi A, Colas M, Crivellente F, De Lentdecker C, Egsmose M, Fait G, Gouliarmou V, Ferilli F, Greco L, Ippolito A, Istace F, Jarrah S, Kardassi D, Kienzler A, Leuschner R, Lava R, Linguadoca A, Lythgo C, Magrans O, Mangas I, Miron I, Molnar T, Padovani L, Parra Morte JM, Pedersen R, Reich H, Santos M, Sharp R, Szentes C, Terron A, Tiramani M, Vagenende B, Villamar-Bouza L (2021b) Conclusion on the peer review of the pesticide risk assessment of the active substance pelargonic acid (nonanoic acid). EFSA J 19:6813. https://doi.org/10.2903/j.efsa.2021.6813
EFSA (European Food Safety Authority), Alvarez F, Anastassiadou M, Arena M, Auteri D, Brancato A, Bura L, Cabrera LC, Castoldi AF, Chaideftou E, Chiusolo A, Colagiorgi A, Colas M, Crivellente F, De Lentdecker C, Egsmose M, Fait G, Greco L, Ippolito A, Istace F, Jarrah S, Kardassi D, Kienzler A, Leuschner R, Lava R, Alberto L, Lostia A, Lythgo C, Magrans O, Mangas I, Miron I, Molnar T, Padovani L, Morte JMP, Pedersen R, Reich H, Santos M, Sharp R, Szentes C, Terron A, Tiramani M, Vagenende B, Villamar-Bouza L (2021c) Peer review of the pesticide risk assessment of the active substance potassium hydrogen carbonate. EFSA J 19:6593. https://doi.org/10.2903/j.efsa.2021.6593
EFSA (European Food Safety Authority), Alvarez F, Arena M, Auteri D, Binaglia M, Castoldi AF, Chiusolo A, Colagiorgi A, Colas M, Crivellente F, De Lentdecker C, Egsmose M, Fait G, Ferilli F, Gouliarmou V, Nogareda LH, Ippolito A, Istace F, Jarrah S, Kardassi D, Kienzler A, Lanzoni A, Lava R, Linguadoca A, Lythgo C, Magrans O, Mangas I, Miron I, Molnar T, Padovani L, Parra Morte JM, Serafimova R, Sharp R, Szentes C, Terron A, Theobald A, Tiramani M, Villamar-Bouza L (2022a) Conclusion on the peer review of the pesticide risk assessment of the active substance rape seed oil. EFSA J 20:7305. https://doi.org/10.2903/j.efsa.2022.7305
EFSA (European Food Safety Authority), Alvarez F, Arena M, Auteri D, Borroto J, Brancato A, Carrasco Cabrera L, Castoldi AF, Chiusolo A, Colagiorgi A, Colas M, Crivellente F, De Lentdecker C, Egsmose M, Fait G, Gouliarmou V, Ferilli F, Greco L, Ippolito A, Istace F, Jarrah S, Kardassi D, Kienzler A, Lava R, Leuschner R, Linguadoca A, Lythgo C, Magrans O, Mangas I, Miron I, Molnar T, Padovani L, Parra Morte JM, Pedersen R, Reich H, Santos M, Serafimova R, Sharp R, Szentes C, Terron A, Tiramani M, Vagenende B, Villamar-Bouza L (2022b) Conclusion on the peer review of the pesticide risk assessment of the active substance sheep fat. EFSA J 20:7073. https://doi.org/10.2903/j.efsa.2022.7073
EFSA (European Food Safety Authority), Alvarez F, Arena M, Auteri D, Borroto J, Brancato A, Cabrera LC, Castoldi AF, Chiusolo A, Colagiorgi A, Colas M, Crivellente F, De Lentdecker C, Egsmose M, Fait G, Gouliarmou V, Ferilli F, Greco L, Ippolito A, Istace F, Jarrah S, Kardassi D, Kienzler A, Lava R, Leuschner R, Linguadoca A, Lythgo C, Magrans O, Mangas I, Miron I, Molnar T, Padovani L, Parra Morte JM, Pedersen R, Reich H, Santos M, Serafimova R, Sharp R, Szentes C, Terron A, Tiramani M, Vagenende B, Villamar-Bouza L (2022c) Conclusion on the peer review of the pesticide risk assessment of the active substance fish oil. EFSA J 20:7079. https://doi.org/10.2903/j.efsa.2022.7079
EFSA (European Food Safety Authority), Alvarez F, Arena M, Auteri D, Binaglia M, Castoldi AF, Chiusolo A, Colagiorgi A, Colas M, Crivellente F, De Lentdecker C, Egsmose M, Fait G, Ferilli F, Gouliarmou V, Nogareda LH, Ippolito A, Istace F, Jarrah S, Kardassi D, Kienzler A, Lanzoni A, Lava R, Leuschner R, Linguadoca A, Lythgo C, Magrans O, Mangas I, Miron I, Molnar T, Padovani L, Parra Morte JM, Rizzuto S, Serafimova R, Sharp R, Szentes C, Terron A, Theobald A, Tiramani M, Villamar-Bouza L (2022d) Conclusion on the peer review of the pesticide risk assessment of the active substance quartz sand. EFSA J 20:7552. https://doi.org/10.2903/j.efsa.2022.7552
EFSA (European Food Safety Authority), Alvarez F, Arena M, Auteri D, Castoldi AF, Chiusolo A, Colagiorgi A, Colas M, Crivellente F, De Lentdecker C, Egsmose M, Fait G, Gouliarmou V, Ferilli F, Ippolito A, Istace F, Jarrah S, Kardassi D, Kienzler A, Lava R, Linguadoca A, Lythgo C, Magrans O, Mangas I, Miron I, Molnar T, Padovani L, Parra Morte JM, Serafimova R, Sharp R, Szentes C, Terron A, Theobald A, Tiramani M, Villamar-Bouza L (2022e) Conclusion on the peer review of the pesticide risk assessment of the active substance heptamaloxyloglucan. EFSA J 20:7210. https://doi.org/10.2903/j.efsa.2022.7210
EFSA (2008) Conclusion regarding the peer review of the pesticide risk assessment of the active substance sulfur. EFSA J 221:1–70. https://doi.org/10.2903/j.efsa.2009.221r
EFSA (2009) Conclusion regarding the peer review of the pesticide risk assessment of the active substance paraffin oils (CAS 64742–46-7, 72623–86-0, 97862–82-3). EFSA J 7:1–59. https://doi.org/10.2903/j.efsa.2009.216r
EFSA (2010a) Conclusion on the peer review of the pesticide risk assessment of the active substance indolylbutyric acid. EFSA J 8:1720. https://doi.org/10.2903/j.efsa.2010.1720
EFSA (2010b) Conclusion on the peer review of the pesticide risk assessment of the active substance 6-benzyladenine. EFSA J 8:1716. https://doi.org/10.2903/j.efsa.2010.1716
EFSA (2011) Conclusion on the peer review of the pesticide risk assessment of the active substance pepper dust extraction residue (listed in Annex I to Directive 91/414/EEC as pepper). EFSA J 9:2285. https://doi.org/10.2903/j.efsa.2011.2285
EFSA (2012a) Conclusion on the peer review of the pesticide risk assessment of the active substance [Trichoderma atroviride strain I-1237]. EFSA J 10:2706. https://doi.org/10.2903/j.efsa.2012.2706
EFSA (2012b) Conclusion on the peer review of the pesticide risk assessment of the active substance Candida oleophila strain O. EFSA J 10:2944. https://doi.org/10.2903/j.efsa.2012.2944
EFSA (2012c) Conclusion on the peer review of the pesticide risk assessment of the active substance iron sulfate. EFSA J 10:2521. https://doi.org/10.2903/j.efsa.2012.2521
EFSA (2012d) Conclusion on the peer review of the pesticide risk assessment of the active substance potassium phosphonates. EFSA J 10:2963. https://doi.org/10.2903/j.efsa.2012.2963
EFSA (2012e) Conclusion on the peer review of the pesticide risk assessment of the active substance eugenol. EFSA J 10:2914. https://doi.org/10.2903/j.efsa.2012.2914
EFSA (2012f) Conclusion on the peer review of the pesticide risk assessment of the active substance geraniol. EFSA J 10:2915. https://doi.org/10.2903/j.efsa.2012.2915
EFSA (2012g) Conclusion on the peer review of the pesticide risk assessment of the active substance thymol. EFSA J 10:2916. https://doi.org/10.2903/j.efsa.2012.2916
EFSA (2012h) Conclusion on the peer review of the pesticide risk assessment of the active substance plant oils/clove oil. EFSA J 10:2506. https://doi.org/10.2903/j.efsa.2012.2506
EFSA (2012i) Conclusion on the peer review of the pesticide risk assessment of the active substance gibberellic acid (GA3). EFSA J 10:2507. https://doi.org/10.2903/j.efsa.2012.2507
EFSA (2012j) Conclusion on the peer review of the pesticide risk assessment of the active substance gibberellins (GA4, GA7) (approved as giberelline). EFSA J 10:2502. https://doi.org/10.2903/j.efsa.2012.2502
EFSA (2013a) Conclusion on the peer review of the pesticide risk assessment of the active substance Aureobasidium pullulans (strains DSM 14940 and DSM 14941). EFSA J 11:3183. https://doi.org/10.2903/j.efsa.2013.3183
EFSA (2013b) Conclusion on the peer review of the pesticide risk assessment of the active substance Bacillus pumilus QST 2808. EFSA J 11:3346. https://doi.org/10.2903/j.efsa.2013.3346
EFSA (2013c) Conclusion on the peer review of the pesticide risk assessment of the active substance disodium phosphonate. EFSA J 11:3213. https://doi.org/10.2903/j.efsa.2013.3213
EFSA (2013d) Conclusion on the peer review of the pesticide risk assessment of the active substance pyrethrins. EFSA J 11:3032. https://doi.org/10.2903/j.efsa.2013.3032
EFSA (2013f) Conclusion on the peer review of the pesticide risk assessment of the active substance maltodextrin. EFSA J 11:3007. https://doi.org/10.2903/j.efsa.2013.3007
EFSA (2013g) Conclusion on the peer review of the pesticide risk assessment of the active substance orange oil. EFSA J 11:3090. https://doi.org/10.2903/j.efsa.2013.3090
EFSA (2013h) Conclusion on the peer review of the pesticide risk assessment of the active substance acetic acid. EFSA J 11:3060. https://doi.org/10.2903/j.efsa.2013.3060
EFSA (2013i) Conclusion on the peer review of the pesticide risk assessment of the active substance fatty acids C7 to C18 (approved under Regulation (EC) No 1107/2009 as fatty acids C7 to C20). EFSA J 11:3023. https://doi.org/10.2903/j.efsa.2013.3023
EFSA (2014a) Conclusion on the peer review of the pesticide risk assessment of the active substance cerevisane (cell walls of Saccharomyces cerevisiae strain LAS117). EFSA J 12:3583. https://doi.org/10.2903/j.efsa.2014.3583
EFSA (2014b) Conclusion on the peer review of the pesticide risk assessment of the active substance COS-OGA. EFSA J 12:3868. https://doi.org/10.2903/j.efsa.2014.3868
EFSA (2014c) Conclusion on the peer review of the pesticide risk assessment of the active substance terpenoid blend QRD-460. EFSA J 12:3816. https://doi.org/10.2903/j.efsa.2014.3816
EFSA (2015) Conclusion on the peer review of the pesticide risk assessment of the active substance ferric phosphate. EFSA J 13:3973. https://doi.org/10.2903/j.efsa.2015.3973
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Acknowledgements
This review was done under the framework of the French collective scientific assessment (CSA) about the “Impacts of plant protection products on biodiversity and ecosystem services” coordinated by INRAE and Ifremer for the French Ministries of Ecological Transition and Territorial Cohesion, of Higher Education and Research, and of Agriculture and Food Sovereignty. This action was also led by the Ministries for Agriculture and Food Sovereignty, for an Ecological Transition and Territorial Cohesion, for Health and Prevention, and of Higher Education and Research, with the financial support of the French Office for Biodiversity, as part of “the national call for projects on the Ecophyto II+ plan, part 1, years 2020–2021,” with the fees for diffuse pollution coming from the Ecophyto II+ plan. The authors would like to acknowledge Dr. Thierry Caquet, the INRAE scientific Director of Environment, and the general directorate of the Ifremer, and Dr. Guy Richard, head of the INRAE Directorate for Collective Scientific Assessment, Foresight and Advanced Studies (DEPE). They also would like to thank Dr. Nicolas Ris (INRAE) for his expertise on macroorganisms; Sophie Leenhardt (INRAE), project manager of the CSA; Dr. Stéphane Pesce (INRAE) and Dr. Wilfried Sanchez (Ifremer), scientific leaders of the CSA together with Dr. Laure Mamy (INRAE); and Lucile Wargniez for the illustrations.
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This work was funded by the French Office for Biodiversity (OFB) through the national Ecophyto plan.
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Marcel Amichot, Cédric Bertrand, Bruno Chauvel, Marie-France Corio-Costet, Fabrice Martin-Laurent, and Laure Mamy contributed equally to the study conception and design, to the data collection, and to the writing of the first draft of the manuscript and of the subsequent revisions. Sophie Le Perchec helped to produce and to mobilize the bibliographic corpus. All authors read and approved the final manuscript.
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Amichot, M., Bertrand, C., Chauvel, B. et al. Natural products for biocontrol: review of their fate in the environment and impacts on biodiversity. Environ Sci Pollut Res (2024). https://doi.org/10.1007/s11356-024-33256-3
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DOI: https://doi.org/10.1007/s11356-024-33256-3