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Assessment of a commercial spider venom peptide against spotted-wing Drosophila and interaction with adjuvants

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Abstract

Chemical control of insect pests in food crops is dominated by broad-spectrum insecticides from a few classes, and there is an urgent need for alternative modes of action. We examined the efficacy of a spider venom peptide, GS-omega/kappa-Hxtx-Hv1a (hereafter, Hv1a) for control of spotted-wing Drosophila and evaluated the importance of phagostimulants and adjuvants for its efficacy. Topical and residual activity of Hv1a was low, with only 17.5% of exposed adult D. suzukii dying after 72 h. In contrast, 100% adult mortality was observed after 24 h when three adjuvants were added to Hv1a. Survival of eggs of D. suzukii oviposited into blueberries was also reduced by exposure to Hv1a combined with the same adjuvants, indicating that Hv1a activity against D. suzukii in the laboratory, but requires penetration of the insect cuticle for efficacy. In a field trial in blueberries, Hv1a gave comparable control to phosmet, and significantly reduced infestation in fruit. This biopesticide adds a new mode of action to the options available for integrated pest management of this and other insect’s pests.

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References

  • Asplen MK et al (2015) Invasion biology of spotted wing Drosophila (Drosophila suzukii): a global perspective and future priorities. J Pest Sci 88:469–494

    Article  Google Scholar 

  • Audsley N, Matthews J, Nachman R, Weaver RJ (2007) Metabolism of cydiastatin 4 and analogues by enzymes associated with the midgut and haemolymph of Manduca sexta larvae. Gen Comp Endocrinol 153:80–87

    Article  PubMed  CAS  Google Scholar 

  • Becher PG, Jensen RE, Natsopoulou ME et al (2018) Infection of Drosophila suzukii with the obligate insect-pathogenic fungus Entomophthora muscae. J Pest Sci 91:781–787

    Article  Google Scholar 

  • Biondi A, Zappalà L, Stark JD, Desneux N (2013) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS ONE 8:e76548

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bonning BC, Chougule NP (2014) Delivery of intrahemocoelic peptides for insect pest management. Trends Biotechnol 32:91–98

    Article  PubMed  CAS  Google Scholar 

  • Cao C-W, Liu G-F, Wang Z-Y, Yan S-C, Ma L, Yang C-P (2010) Response of the gypsy moth, Lymantria dispar to transgenic poplar, Populus simonii × P. nigra, expressing fusion protein gene of the spider insecticidal peptide and Bt-toxin C-peptide. J Insect Sci 10:200

    PubMed  PubMed Central  Google Scholar 

  • Casartelli M, Corti P, Leonardi MG, Fiandra L, Burlini N, Pennacchio F, Giordana B (2005) Absorption of albumin by the midgut of a lepidopteran larva. J Insect Physiol 51:933–940

    Article  PubMed  CAS  Google Scholar 

  • Chen J, Fine JD, Mullin CA (2018) Are organosilicon surfactants safe for bees or humans? Sci Total Environ 612:415–421

    Article  PubMed  CAS  Google Scholar 

  • Cini A, Anfora G, Escudero-Colomar LA, Grassi A, Santosuosso U, Seljak G, Papini A (2014) Tracking the invasion of the alien fruit pest Drosophila suzukii in Europe. J Pest Sci 87:559–566

    Article  Google Scholar 

  • Costa LG (2006) Current issues in organophosphate toxicology. Clin Chim Acta 366:1–13

    Article  PubMed  CAS  Google Scholar 

  • 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(2):640–653

    Article  PubMed  Google Scholar 

  • Daane KM, Wang XG, Biondi A et al (2016) First exploration of parasitoids of Drosophila suzukii in South Korea as potential classical biological agents. J Pest Sci 89:823–835

    Article  Google Scholar 

  • Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106

    Article  PubMed  CAS  Google Scholar 

  • Eberl DF, Ren D, Feng G, Lorenz LJ, Van Vactor D, Hall LM (1998) Genetic and developmental characterization of Dmca1D, a calcium channel α 1 subunit gene in Drosophila melanogaster. Genetics 148:1159–1169

    PubMed  PubMed Central  CAS  Google Scholar 

  • Environmental Protection Agency (2014) GS-omega/kappa-Hxtx-Hv1a; Exemption From the Requirement of a Tolerance. https://www.federalregister.gov/documents/2014/02/26/2014-04092/gs-omegakappa-hxtx-hv1a-exemption-from-the-requirement-of-a-tolerance. Accessed 16 Oct 2017

  • Fanning PD, Grieshop MJ, Isaac R (2017) Efficacy of biopesticides on spotted wing drosophila, Drosophila suzukii Matsumura in fall red raspberries. J App Entomol 142(1–2):26–32

    Google Scholar 

  • Farnsworth D, Hamby K, Bolda M, Goodhue R, Williams J, Zalom F (2017) Economic analysis of revenue losses and control costs associated with the spotted wing drosophila (Drosophila suzukii (Matsumura)) in the California raspberry industry. Pest Manag Sci 73(6):1083–1090

    Article  PubMed  CAS  Google Scholar 

  • Fitches EC, Pyati P, King GF, Gatehouse JA (2012) Fusion to snowdrop lectin magnifies the oral activity of insecticidal ω-hexatoxin-Hv1a peptide by enabling its delivery to the central nervous system. PLoS ONE 7:e39389

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fletcher JI et al (1997) The structure of a novel insecticidal neurotoxin, ω-atracotoxin-HV1, from the venom of an Australian funnel web spider. Nat Struct Mol Biol 4:559–566

    Article  CAS  Google Scholar 

  • Garriga A, Morton A, Garcia-del-Pino F (2018) Is Drosophila suzukii as susceptible to entomopathogenic nematodes as Drosophila melanogaster? J Pest Sci 91:789–798

    Article  Google Scholar 

  • Goodhue RE, Bolda M, Farnsworth D, Williams JC, Zalom FG (2011) Spotted wing drosophila infestation of California strawberries and raspberries: economic analysis of potential revenue losses and control costs. Pest Manag Sci 67:1396–1402

    Article  PubMed  CAS  Google Scholar 

  • Graf JF (1993) The role of insect growth regulators in arthropod control. Parasitol Today 12:471–474

    Article  Google Scholar 

  • Guedes RNC, Smagghe G, Stark JD, Desneux N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Ann Rev Entomol 61:43–62

    Article  CAS  Google Scholar 

  • Haye T, Girod P, Cuthbertson AGS et al (2016) Current SWD IPM tactics and their practical implementation in fruit crops across different regions around the world. J Pest Sci 89:643–651

    Article  Google Scholar 

  • Healy K (2005) Book review: an R and S-PLUS companion to applied regression. Soc Methods Res 34:137–140

    Article  Google Scholar 

  • Herzig V, Bende NS, Alam MS, Tedford HW, Kennedy RM, King GF (2014) Methods for deployment of spider venom peptides as bioinsecticides. Adv Insect Physiol 47:389–411

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Bio J 50:346–363

    Article  Google Scholar 

  • Jiang H, Zhu Y, Chen Z (1995) Insect resistance of transformed tobacco plants with gene of the spider insecticidal peptide. Acta Bot Sin 38:95–99

    Google Scholar 

  • Khan SA, Zafar Y, Briddon RW, Malik KA, Mukhtar Z (2006) Spider venom toxin protects plants from insect attack. Transgenic Res 15:349–357

    Article  PubMed  CAS  Google Scholar 

  • King GF (2007) Modulation of insect Ca V channels by peptidic spider toxins. Toxicon 49:513–530

    Article  PubMed  CAS  Google Scholar 

  • King GF (2011) Venoms as a platform for human drugs: translating toxins into therapeutics. Exp Opin Biol Ther 11:1469–1484

    Article  CAS  Google Scholar 

  • King GF, Hardy MC (2013) Spider-venom peptides: structure, pharmacology, and potential for control of insect pests. Ann Rev Entomol 58:475–496

    Article  CAS  Google Scholar 

  • Lai T, Su J (2011) Assessment of resistance risk in Spodoptera exigua (Hübner)(Lepidoptera: Noctuidae) to chlorantraniliprole. Pest Manag Sci 67:1468–1472

    Article  PubMed  CAS  Google Scholar 

  • Leach H, Van Timmeren S, Isaacs R (2016) Exclusion netting delays and reduces Drosophila suzukii (Diptera: Drosophilidae) infestation in Raspberries. J Econ Entomol 109:2151–2158

    Article  Google Scholar 

  • Leach H, Moses J, Hanson E et al (2018) Rapid harvest schedules and fruit removal as non-chemical approaches for managing spotted wing Drosophila. J Pest Sci 91:219–226

    Article  Google Scholar 

  • Lewis C (1980) The penetration of cuticle by insecticides. In: Miller TA (ed) Cuticle techniques in arthropods. Springer, New York, pp 367–400

    Chapter  Google Scholar 

  • Lounibos LP (2002) Invasions by insect vectors of human disease. Ann Review Entomol 47:233–266

    Article  CAS  Google Scholar 

  • Mazzetto F, Marchetti E, Amiresmaeili N et al (2016) Drosophila parasitoids in northern Italy and their potential to attack the exotic pest Drosophila suzukii. J Pest Sci 89:837–850

    Article  Google Scholar 

  • McCutchen B, Hoover K, Preisler H, Betana M, Herrmann R, Robertson J, Hammock B (1997) Interactions of recombinant and wild-type baculoviruses with classical insecticides and pyrethroid-resistant tobacco budworm (Lepidoptera: Noctuidae). J Econ Entomol 90:1170–1180

    Article  PubMed  CAS  Google Scholar 

  • Mota-Sanchez, Wise (2017) Arthropod Pesticide Resistance Database. Assessed 15 Oct 2017

  • Nakasu EY, Williamson SM, Edwards MG, Fitches EC, Gatehouse JA, Wright GA, Gatehouse AM (2014) Novel biopesticide based on a spider venom peptide shows no adverse effects on honeybees. Proc R Soc Lond B Biol Sci 281:20140619

    Article  CAS  Google Scholar 

  • Nicholson GM, Willow M, Howden MEH, Narahashi T (1994) Modification of sodium channel gating and kinetics by versutoxin from the Australian funnel-web spider Hadronyche versuta. Pflügers Arch 428:400–409

    Article  PubMed  CAS  Google Scholar 

  • Nikolouli K, Colinet H, Renault D et al (2018) Sterile insect technique and Wolbachia symbiosis as potential tools for the control of the invasive species Drosophila suzukii. J Pest Sci 91:489–503

    Article  Google Scholar 

  • Oerke E-C (2006) Crop losses to pests. J Agric Sci 144:31–43

    Article  Google Scholar 

  • Pardo-Lopez L, Soberon M, Bravo A (2012) Bacillus thuringiensis insecticidal three-domain Cry toxins: mode of action, insect resistance and consequences for crop protection. FEMS Microbiol Rev 37:3–22

    Article  PubMed  CAS  Google Scholar 

  • Pimentel D (2009) Pesticides and pest control. In: Peshin R, Dhawan AK (eds) Integrated pest management: innovation-development process. Springer, Dordrecht, pp 83–87

    Chapter  Google Scholar 

  • R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

  • Rossi Stacconi MV, Buffington M, Daane KM et al (2015) Host stage preference, efficacy and fecundity of parasitoids attacking Drosophila suzukii in newly invaded areas. Biol Control 84:28–35

    Article  Google Scholar 

  • Rossi Stacconi MV, Amiresmaeili N, Biondi A et al (2018) Host location and dispersal ability of the cosmopolitan parasitoid Trichopria drosophilae released to control the invasive spotted wing Drosophila. Biol Control 117:188–196

    Article  Google Scholar 

  • Smith TM, Stratton GW (1986) Effects of synthetic pyrethroid insecticides on nontarget organisms. In: Gunther FA (ed) Residue reviews. Springer, New York, pp 93–120

    Chapter  Google Scholar 

  • Smith JJ, Herzig V, King GF, Alewood PF (2013) The insecticidal potential of venom peptides. Cell Mol Life Sci 70:3665–3693

    Article  PubMed  CAS  Google Scholar 

  • Tedford HW, Sollod BL, Maggio F, King GF (2004) Australian funnel-web spiders: master insecticide chemists. Toxicon 43:601–618

    Article  PubMed  CAS  Google Scholar 

  • Van Timmeren S, Isaacs R (2013) Control of spotted wing drosophila, Drosophila suzukii, by specific insecticides and by conventional and organic crop protection programs. Crop Prot. 54:126–133

    Article  CAS  Google Scholar 

  • Van Timmeren S, Mota-Sanchez D, Wise JC, Isaacs R (2017a) Baseline susceptibility of spotted wing Drosophila (Drosophila suzukii) to four key insecticide classes. Pest Manag Sci 74(1):78–87

    Article  PubMed  CAS  Google Scholar 

  • Van Timmeren S, Diepenbrock LM, Bertone MA, Burrack HJ, Isaacs R (2017b) A filter method for improved monitoring of Drosophila suzukii (Diptera: Drosophilidae) larvae in fruit. J Integr Pest Manag 8:23

    Google Scholar 

  • Walsh DB et al (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

    Article  Google Scholar 

  • Wang C, St Leger RJ (2007) A scorpion neurotoxin increases the potency of a fungal insecticide. Nat Biotechnol 25:1455

    Article  PubMed  CAS  Google Scholar 

  • Wang XG, Kaçar G, Biondi A, Daane KM (2016) Life-history and host preference of Trichopria drosophilae, a pupal parasitoid of spotted wing drosophila. Biocontrol 61:387–397

    Article  CAS  Google Scholar 

  • Windley MJ, Herzig V, Dziemborowicz SA, Hardy MC, King GF, Nicholson GM (2012) Spider-venom peptides as bioinsecticides. Toxins 4:191–227

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wise J, Whalon M (2009) A systems approach to IPM integration, ecological assessment and resistance management in tree fruit orchards. In: Ishaaya I, Rami Horowitz A (eds) Biorational control of arthropod pests: application and resistance management. Springer, Dordrecht, pp 325–345

    Chapter  Google Scholar 

  • Wise JC, Vanderpoppen R, Vandervoort C, O’Donnell C, Isaacs R (2015) Curative activity contributes to control of spotted-wing Drosophila (Diptera: Drosophilidae) and blueberry maggot (Diptera: Tephritidae) in highbush blueberry. Can Entomol 147:109–117

    Article  Google Scholar 

  • Wise JC, VanWoerkom A, Isaacs R (2017) Control of spotted wing Drosophila in blueberries, 2016. ATM 42:tsx064-tsx064 https://doi.org/10.1093/amt/tsx064

  • Yee WL (2014) Comparison of the brown sugar, hot water, and salt methods for detecting Western cherry fruit fly (Diptera: Tephritidae) larvae in sweet cherry. Fla Entomol 97:422–430

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Zhang X, Candas M, Griko N, Rose-Young L, Bulla L (2005) Cytotoxicity of Bacillus thuringiensis Cry1Ab toxin depends on specific binding of the toxin to the cadherin receptor BT-R1 expressed in insect cells. Cell Death Differ 12:1407

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors acknowledge the excellent assistance of Elizabeth Espeland with bioassays and maintaining cultures of Drosophila suzukii. The authors would like to thank the anonymous reviewers for their valuable comments and suggestions to improve the quality of the paper.

Funding

This study was funded in part by the USDA National Institute for Food and Agriculture through the Specialty Crop Research Initiative (award 2015-51181-24252) and the Organic Research and Extension Initiative (award 2015-51300-24154). This research was supported in part by chemical companies providing pesticides and/or research funding.

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Correspondence to Philip D. Fanning.

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All applicable international, national and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors. Informed consent was obtained from all individual participants included in the study.

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Communicated by A. Biondi.

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Fanning, P.D., VanWoerkom, A., Wise, J.C. et al. Assessment of a commercial spider venom peptide against spotted-wing Drosophila and interaction with adjuvants. J Pest Sci 91, 1279–1290 (2018). https://doi.org/10.1007/s10340-018-1016-7

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