Advertisement

Natural compounds for controlling Drosophila suzukii. A review

  • Doriane Dam
  • Daniel Molitor
  • Marco BeyerEmail author
Review Article
Part of the following topical collections:
  1. Pest control

Abstract

The drosophilid fly Drosophila suzukii is an invasive pest that has recently started threatening fruit production in Europe. In contrast to many other fruit flies, D. suzukii is able to lay eggs in ripening and mature fruits where larvae develop, rendering fruits unmarketable. This preference for ripening fruit requires pest control shortly before harvest, implying a high risk of residues on the fruit if synthetic insecticides are used. As the current management practices largely rely on chemical control, the need for alternative solutions has emerged. Here, we review the studies published up to now on the efficacy of natural compounds against D. suzukii. Several natural compounds were identified that act as repellents, contact or ingestion toxicants, fumigants, ovicides or oviposition deterrents. The most promising compounds of each group were (i) essential oils (EOs) such as the EO of thyme or its major ingredient thymol which repelled flies from fresh fruits for at least 24 h; (ii) Leptospermum ericoides and L. scoparium EOs, which expressed contact toxicity at a LD50 < 1.2 μg/fly; (iii) the combination of erythritol and sucrose, which was a potent ingestion toxicant against adults and (iv) a chitinase from Euphorbia characias against larvae (both of the latter two resulted in 100% mortality); (v) the EO ingredients perilla aldehyde, geranial and neral showed the highest insecticidal activities as fumigants (LC50 < 1.52 mg/l air for males and 2.6 mg/l air for females) and (vi) powdered sulphur was reported to be the most efficient oviposition deterrent, reducing the number of eggs deposited into the fruits by 76%. To enable a wider use of the natural compounds in sustainable agriculture, more information on (i) potential effects on non-target organisms, (ii) field performance and (iii) life cycle analyses results is currently needed.

Keywords

Climate change Crop protection Insecticides Reducing pesticides Spotted wing drosophila 

Abbreviations

AChE

Acetylcholinesterase

AST

Average survival time

BA

Butyl anthranilate

CT

Concentration tested

DEET

N,N-diethyl-meta-toluamide

DMB

Methyl 2,4-dimethoxy-6-methylbenzoate

EA

Ethyl anthranilate

EO

Essential oil

ESE

Ethanolic seed extract

GST

Glutathione-S-transferase

MDA

Methyl N,N-dimethylanthranilate

Notes

Acknowledgements

We thank the Institut Viti-Vinicole (IVV) of Luxembourg for financially supporting the project BioViM, the European Union for supporting the project Clim4Vitis (grant agreement No 810176), Mareike Schulz (IVV) for helpful discussions and Lindsey Auguin for language editing.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Asplen MK, Anfora G, Biondi A, Choi D-S, Chu D, Daane KM, Gibert P, Gutierrez AP, Hoelmer KA, Hutchison WD, Isaacs R, Jiang Z-L, Kárpáti Z, Kimura MT, Pascual M, Philips CR, Plantamp C, Ponti L, Vétek G, Vogt H, Walton VM, Yu Y, Zappalà L, Desneux N (2015) Invasion biology of spotted wing Drosophila (Drosophila suzukii): a global perspective and future priorities. J Pest Sci 88:469–494.  https://doi.org/10.1007/s10340-015-0681-z CrossRefGoogle Scholar
  2. Bellamy DE, Sisterson MS, Walse SS (2013) Quantifying host potentials: indexing postharvest fresh fruits for spotted wing Drosophila, Drosophila suzukii. PLoS One 8:e61227.  https://doi.org/10.1371/journal.pone.0061227 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bernardi D, Ribeiro L, Andreazza F, Neitzke C, Oliveira EE, Botton M, Nava DE, Vendramim JD (2017) Potential use of Annona by products to control Drosophila suzukii and toxicity to its parasitoid Trichopria anastrephae. Ind Crop Prod 110:30–35.  https://doi.org/10.1016/j.indcrop.2017.09.004 CrossRefGoogle Scholar
  4. Biganski S, Jehle JA, Kleespies RG (2018) Bacillus thuringiensis serovar. israelensis has no effect on Drosophila suzukii Matsumura. J Appl Entomol 142:33–36.  https://doi.org/10.1111/jen.12415 CrossRefGoogle Scholar
  5. Choi M-Y, Tang SB, Ahn S-J, Amarasekare KG, Shearer P, Lee JC (2017) Effect of non-nutritive sugars to decrease the survivorship of spotted wing drosophila, Drosophila suzukii. J Insect Physiol 99:86–94.  https://doi.org/10.1016/j.jinsphys.2017.04.001 CrossRefPubMedGoogle Scholar
  6. Choi M-Y, Lucas H, Sagili R, Cha DH, Lee JC (2019) Effect of eythritol on Drosophila suzukii (Diptera: Drosophilidae) in the presence of naturally-occurring sugar sources, and on the survival of Apis mellifera (Hymenoptera: Apidae). J Econ Entomol 112:981–985.  https://doi.org/10.1093/jee/toy362 CrossRefPubMedGoogle Scholar
  7. Cini A, Ioriatti C, Anfora G (2012) A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management. Bull Insectol 65:149–160Google Scholar
  8. Cowles RS, Rodriguez-Saona C, Holdcraft R, Loeb GM, Elsensohn JE, Hesler SP (2015) Sucrose improves insecticide activity against Drosophila suzukii (Diptera: Drosophilidae). J Econ Entomol 108:640–653.  https://doi.org/10.1093/jee/tou100 CrossRefPubMedGoogle Scholar
  9. Dayan FE, Duke SO, Sauldubois A, Singh N, McCurdy C, Cantrell C (2007) p-Hydroxyphenylpyruvate dioxygenase is a herbicidal target site for β-triketones from Leptospermum scoparium. Phytochemistry 68:2004–2014.  https://doi.org/10.1016/j.phytochem.2007.01.026 CrossRefPubMedGoogle Scholar
  10. Dorsaz M, Fischer S, Baroffio C-A (2017a) Lutter contre Drosophila suzukii (Matsumura) sans insecticides: est-ce une utopie? Presented at the Association Française de Protection des Plantes - 6ème conférence sur les moyens alternatifs de protection pour une production intégrée, LilleGoogle Scholar
  11. Dorsaz M, Kuonen F, Baroffio C-A (2017b)Current spotted wing drosophila IPM tactics and their practical implementation in berry crops in Switzerland. Acta Hortic 827–832.  https://doi.org/10.17660/ActaHortic.2017.1156.122
  12. Enan E (2001) Insecticidal activity of essential oils: octopaminergic sites of action. Comp Biochem Physiol Part C Toxicol Pharmacol 130:325–337.  https://doi.org/10.1016/S1532-0456(01)00255-1 CrossRefGoogle Scholar
  13. Erland LAE, Rheault MR, Mahmoud SS (2015) Insecticidal and oviposition deterrent effects of essential oils and their constituents against the invasive pest Drosophila suzukii (Matsumura) (Diptera: Drosophilidae). Crop Prot 78:20–26.  https://doi.org/10.1016/j.cropro.2015.08.013 CrossRefGoogle Scholar
  14. Feng Y, Zhang A (2017) A floral fragrance, methyl benzoate, is Zn efficient green pesticide. Sci Rep 7.  https://doi.org/10.1038/srep42168
  15. Hamby KA, Bellamy DE, Chiu JC, Lee JC, Walton VM, Wiman NG, York RM, Biondi A (2016) Biotic and abiotic factors impacting development, behavior, phenology, and reproductive biology of Drosophila suzukii. J Pest Sci 89:605–619.  https://doi.org/10.1007/s10340-016-0756-5 CrossRefGoogle Scholar
  16. Haye T, Girod P, Cuthbertson AGS, Wang XG, Daane KM, Hoelmer KA, Baroffio C, Zhang JP, Desneux N (2016) Current SWD IPM tactics and their practical implementation in fruit crops across different regions around the world. J Pest Sci 89:643–651.  https://doi.org/10.1007/s10340-016-0737-8 CrossRefGoogle Scholar
  17. Jang M, Kim J, Yoon KA, Lee SH, Park CG (2017) Biological activity of Myrtaceae plant essential oils and their major components against Drosophila suzukii (Diptera: Drosophilidae). Pest Manag Sci 73:404–409.  https://doi.org/10.1002/ps.4430 CrossRefPubMedGoogle Scholar
  18. Kim J, Jang M, Lee K-T, Yoon KA, Park CG (2016a) Insecticidal and enzyme inhibitory activities of sparassol and its analogues against Drosophila suzukii. J Agric Food Chem 64:5479–5483.  https://doi.org/10.1021/acs.jafc.6b01528 CrossRefPubMedGoogle Scholar
  19. Kim J, Jang M, Shin E, Kim J, Lee SH, Park CG (2016b) Fumigant and contact toxicity of 22 wooden essential oils and their major components against Drosophila suzukii (Diptera: Drosophilidae). Pestic Biochem Physiol 133:35–43.  https://doi.org/10.1016/j.pestbp.2016.03.007 CrossRefPubMedGoogle Scholar
  20. Krause Pham C, Ray A (2015) Conservation of olfactory avoidance in Drosophila species and identification of repellents for Drosophila suzukii. Sci Rep 5.  https://doi.org/10.1038/srep11527
  21. La Guerche S, Chamont S, Blancard D, Dubourdieu D, Darriet P (2005) Origin of (−)-geosmin on grapes: on the complementary action of two fungi, Botrytis Cinerea and Penicillium Expansum. Antonie Van Leeuwenhoek 88:131–139.  https://doi.org/10.1007/s10482-005-3872-4 CrossRefPubMedGoogle Scholar
  22. Langille AB, Arteca EM, Newman JA (2017) The impacts of climate change on the abundance and distribution of the spotted wing Drosophila (Drosophila suzukii) in the United States and Canada. PeerJ 5:e3192.  https://doi.org/10.7717/peerj.3192 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Lowe EM, Balis FM (2012) Chapter 18: dose-effect and concentration-effect analysis. In: Principles of Clinical Pharmacology. pp. 289–300CrossRefGoogle Scholar
  24. Martos S, Spanò D, Agustí N, Poschenrieder C, Pintus F, Moles L, Medda R (2017) A chitinase from Euphorbia characias latex is a novel and powerful plant-based pesticide against Drosophila suzukii. Ann Appl Biol 171:252–263.  https://doi.org/10.1111/aab.12369 CrossRefGoogle Scholar
  25. Miller, P., Peters, B., 2017. Flavesone: a novel insecticide for the control of urban pests. Presented at the ninth international conference on urban pests, Birmingham, pp. 245–251Google Scholar
  26. Park CG, Jang M, Yoon KA, Kim J (2016) Insecticidal and acetylcholinesterase inhibitory activities of Lamiaceae plant essential oils and their major components against Drosophila suzukii (Diptera: Drosophilidae). Ind Crop Prod 89:507–513.  https://doi.org/10.1016/j.indcrop.2016.06.008 CrossRefGoogle Scholar
  27. Park C, Jang M, Shin E, Kim J (2017) Myrtaceae plant essential oils and their β-triketone components as insecticides against Drosophila suzukii. Molecules 22:1050.  https://doi.org/10.3390/molecules22071050 CrossRefPubMedCentralGoogle Scholar
  28. Pautasso M (2013) Ten simple rules for writing a literature review. PLoS Comput Biol 9:e1003149.  https://doi.org/10.1371/journal.pcbi.1003149 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Pérez-Guerrero S, Molina JM (2016) Short communication: laboratory approach to the use of sulphur and kaolin as preventive control against Drosophila suzukii. Span. J Agric Res 14:e10SC01.  https://doi.org/10.5424/sjar/2016142-8592 CrossRefGoogle Scholar
  30. Porteus A (2008) Dictionary of environmental science and technology. Dictionnary Environ Sci TechnolGoogle Scholar
  31. Renkema JM, Wright D, Buitenhuis R, Hallett RH (2016) Plant essential oils and potassium metabisulfite as repellents for Drosophila suzukii (Diptera: Drosophilidae). Sci Rep 6.  https://doi.org/10.1038/srep21432
  32. Renkema J, Buitenhuis R, Hallett R (2017) Reduced Drosophila suzukii infestation in berries using deterrent compounds and laminate polymer flakes. Insects 8:117–133.  https://doi.org/10.3390/insects8040117 CrossRefPubMedCentralGoogle Scholar
  33. Sampson BJ, Marshall DA, Smith BJ, Stringer SJ, Werle CT, Magee DJ, Adamczyk JJ (2017a) Erythritol and lufenuron detrimentally alter age structure of wild Drosophila suzukii (Diptera: Drosophilidae) populations in blueberry and blackberry. J Econ Entomol 110:530–534.  https://doi.org/10.1093/jee/tow307 CrossRefPubMedGoogle Scholar
  34. Sampson BJ, Werle CT, Stringer SJ, Adamczyk JJ (2017b) Ingestible insecticides for spotted wing Drosophila control: a polyol, erythritol, and an insect growth regulator, Lufenuron. J Appl Entomol 141:8–18.  https://doi.org/10.1111/jen.12350 CrossRefGoogle Scholar
  35. Sampson BJ, Easson MW, Stringer SJ, Werle CT, Magee D, Adamczyk JJ (2019) Laboratory and field assessments of erythritol derivatives on the survival, reproductive rate, and control of Drosophila suzukii (Diptera: Drosophilidae). J Econ Entomol 112:173–180.  https://doi.org/10.1093/jee/toy274 CrossRefPubMedGoogle Scholar
  36. Scanga SE, Hasanspahič B, Zvorničanin E, Samardžić Koženjić J, Rahme AK, Shinn-Thomas JH (2018) Erythritol, at insecticidal doses, has harmful effects on two common agricultural crop plants. PLoS One 13:e0192749.  https://doi.org/10.1371/journal.pone.0192749 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Schultz M, Molitor DD (2016) Die Kirschessigfliege - eine neue Herausforderung für den Luxemburger Weinbau. Lëtzebuerger Beien-Ztg 127:354–359Google Scholar
  38. Shawer R, Tonina L, Tirello P, Duso C, Mori N (2018) Laboratory and field trials to identify effective chemical control strategies for integrated management of Drosophila suzukii in European cherry orchards. Crop Prot 103:73–80.  https://doi.org/10.1016/j.cropro.2017.09.010 CrossRefGoogle Scholar
  39. Strack T, Cahenzli F, Daniel C (2017) Kaolin, lime and rock to control Drosophila suzukii. Presented at the Ökologschen Landbau weiterdenken: Verantwortung übernhemen, Vertrauen stärkenGoogle Scholar
  40. Swoboda-Bhattarai KA, Burrack HJ (2014) Influence of edible fruit coatings on Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) oviposition and development. Int J Pest Manag 60:279–286.  https://doi.org/10.1080/09670874.2014.971453 CrossRefGoogle Scholar
  41. Tang SB, Lee JC, Jung JK, Choi M-Y (2017) Effect of erythritol formulation on the mortality, fecundity and physiological excretion in Drosophila suzukii. J Insect Physiol 101:178–184.  https://doi.org/10.1016/j.jinsphys.2017.07.015 CrossRefPubMedGoogle Scholar
  42. Wallingford A, Connelly HL, Dore Brind’Amour G, Boucher MT, Mafra-Neto A, Loeb GM (2016a) Field evaluation of an oviposition deterrent for management of spotted-wing Drosophila, Drosophila suzukii, and potential nontarget effects. J Econ Entomol 109:1779–1784.  https://doi.org/10.1093/jee/tow116 CrossRefPubMedGoogle Scholar
  43. Wallingford A, Hesler SP, Cha DH, Loeb GM (2016b) Behavioral response of spotted-wing drosophila, Drosophila suzukii Matsumura, to aversive odors and a potential oviposition deterrent in the field: Drosophila suzukii deterrents. Pest Manag Sci 72:701–706.  https://doi.org/10.1002/ps.4040 CrossRefPubMedGoogle Scholar
  44. Wallingford A, Cha DH, Linn CE, Wolfin MS, Loeb GM (2017) Robust manipulations of pest insect behavior using repellents and practical application for integrated pest management. Environ Entomol 46:1041–1050.  https://doi.org/10.1093/ee/nvx125 CrossRefPubMedGoogle Scholar
  45. Wallingford A, Cha DH, Loeb GM (2018) Evaluating a push-pull strategy for management of Drosophila suzukii Matsumura in red raspberry: push-pull for D. suzukii management. Pest Manag Sci 74:120–125.  https://doi.org/10.1002/ps.4666 CrossRefPubMedGoogle Scholar
  46. Walsh DB, Bolda MP, Goodhue RE, Dreves AJ, Lee J, Bruck DJ, Walton VM, O’Neal SD, Zalom FG (2011) Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. J Integr Pest Manag 2:G1–G7.  https://doi.org/10.1603/IPM10010 CrossRefGoogle Scholar
  47. Yousef M, Aranda-Valera E, Quesada-Moraga E (2018) Lure-and-infect and lure-and-kill devices based on Metarhizium brunneum for spotted wing Drosophila control. J Pest Sci 91:227–235.  https://doi.org/10.1007/s10340-017-0874-8 CrossRefGoogle Scholar

Copyright information

© INRA and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Environmental Research and Innovation DepartmentLuxembourg Institute of Science and TechnologyBelvauxLuxembourg

Personalised recommendations