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Journal of Pest Science

, Volume 93, Issue 1, pp 91–102 | Cite as

Electropenetrography of spotted wing drosophila (Drosophila suzukii) on pesticide-treated strawberry

  • Raul Narciso C. GuedesEmail author
  • Felix A. Cervantes
  • Elaine A. Backus
  • Spencer S. Walse
Original Paper

Abstract

Many behaviors are associated with host selection by arthropod pests. The treatment of a host, such as with a pesticide, may impact behaviors involved in this selection whose understanding yields opportunities for pest management. AC–DC electropenetrography (EPG) allows real-time monitoring of insect behaviors, but its use has emphasized feeding activities of hemipteroid insects. Recent improvement in electropenetrography (AC–DC) has made it amenable for use with non-hemipteroid species, such as the invasive spotted wing drosophila (Drosophila suzukii). Therefore, AC–DC EPG was used for the first quantitative study of a non-hemipteroid insect to monitor behaviors of spotted wing drosophila on strawberry fruits treated with either the fungicide fenhexamid or the insecticide spinetoram, in addition to a non-treated control. EPG was used to characterize three behavioral phases of the insect: non-probing (i.e., resting, grooming, and walking), feeding, and egg-laying. The first two phases were affected by sublethal pesticide exposure, but egg-laying was not. Both pesticides decreased the number of non-probing events, but increased their overall durations, while the opposite took place with feeding, especially in spinetoram-treated strawberry. Regarding feeding activity, both pesticides compromised insect dabbing and ingestion with particularly strong impairment by spinetoram, which also compromised how long the females survived (i.e., longevity). EPG revealed valuable insights regarding the behavioral assessment of pesticide-treated hosts by an insect pest. Specifically, the feeding of female of spotted wing drosophila was significantly impaired on strawberries treated with spinetoram compromising female longevity. Though deserving further attention, the fungicide fenhexamid exhibited a relatively mild effect on feeding, but did not affect adult longevity.

Keywords

Fruit fly Feeding behavior Electrical penetration graph Spynosins Spinetoram Fenhexamid 

Notes

Acknowledgements

Financial support was provided by the CAPES Foundation (Brazilian Ministry of Education; Finance Code 001) and USDA-ARS, which was greatly appreciated. The research was also supported in part by an appointment to the Agricultural Research Service (ARS) Research Participation Program administered by the Oak Ridge Institute for Science and Education (ORISE) through an interagency agreement between the U.S. Department of Energy (DOE) and the U.S. Department of Agriculture (USDA). ORISE is managed by Oak Ridge Associated Universities (ORAU) under DOE contract number DE-SC0014664. All opinions expressed in this paper are the authors’ and do not necessarily reflect the policies and views of CAPES, USDA, ARS, DOE, or ORAU/ORISE. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. USDA is an equal opportunity provider and employer.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and institutional guidelines for the care and use of animals were considered in the present study.

Informed consent

The authors of this manuscript accept that the paper is submitted for publication in the Journal of Pest Science, and report that this paper has not been published or accepted for publication in another journal, nor is under consider at another journal.

References

  1. Asplen MK, Anfora G, Biondi A et al (2015) Invasion biology of spotted wing Drosophila (Drosohila suzikii): a global perspective and future priorities. J Pest Sci 88:469–494.  https://doi.org/10.1007/s10340-015-0681-z CrossRefGoogle Scholar
  2. Backus EA (2000) Our own jabberwocky: clarifying the terminology of certain piercing-sucking behaviors of homopterans. In: Walker GP, Backus EA (eds) Principles and applications of electronic monitoring and other techniques in the study of homopteran feeding behavior. Entomological Soceity of America, Annapolis, pp 1–13Google Scholar
  3. Backus EA, Bennett WH (1992) New AC electronic insect feeding monitor for fine-structure analysis of waveforms. Ann Entomol Soc Am 85:437–444.  https://doi.org/10.1093/aesa/85.4.437 CrossRefGoogle Scholar
  4. Backus EA, Bennett WH (2009) The AC–DC correlation monitor: new EPG design with flexible input resistors to detect both R and emf components for any piercing-sucking hemipteran. J Insect Physiol 55:869–884.  https://doi.org/10.1016/j.jinsphys.2009.05.007 CrossRefPubMedGoogle Scholar
  5. Backus, EA, Cervantes FA, Godfrey L, Akbarc W, Clark TL, Rojas MG (2018) Certain applied electrical signals during EPG cause negative effects on stylet probing behaviors by adult Lygus lineolaris (Hemiptera: Miridae). J Insect Physiol 105:64–75CrossRefGoogle Scholar
  6. Backus EA, Cline AR, Ellerseick MR, Serrano MS (2007) Lygus hesperus (Hemiptera: Miridae) feeding on cotton: new methods and parameters for analysis of nonsequential electrical penetration graph. Ann Entomol Soc Am 100:296–310CrossRefGoogle Scholar
  7. Backus EA, Vervantes FA, Guedes RNC, Li AY, Wayadande AC (2019) AC–DC electropenetrography for in-depth studies of feeding and oviposition behaviors. Ann Entomol Soc Am.  https://doi.org/10.1093/1esa/saz009 CrossRefGoogle Scholar
  8. 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
  9. Bernays EA (1991) Evolution of insect morphology in relation to plants. Philos Trans R Soc B Biol Sci 333:257–264.  https://doi.org/10.1098/rstb.1991.0075 CrossRefGoogle Scholar
  10. Blande JD, Holopainen JK, Niinemets Ü (2014) Plant volatiles in polluted atmospheres: stress responses and signal degradation. Plant Cell Environ 37:1892–1904.  https://doi.org/10.1111/pce.12352 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Blanke A, Ruhr PT, Mokso R et al (2015) Structural mouthpart interaction evolved already in the earliest lineages of insects. Proc R Soc B 282:20151033.  https://doi.org/10.1098/rspb.2015.1033 CrossRefPubMedGoogle Scholar
  12. Boina DR, Youn Y, Folimonova S, Stelinski LL (2011) Effects of pymetrozine, an antifeedant of Hemiptera, on Asian citrus psyllid, Diaphorina citri, feeding behavior, survival and transmission of Candidatus Liberibacter asiaticus. Pest Manag Sci 67:146–155.  https://doi.org/10.1002/ps.2042 CrossRefPubMedGoogle Scholar
  13. Bruck DJ, Bolda M, Tanigoshi L et al (2011) Laboratory and field comparisons of insecticides to reduce infestation of Drosophila suzukii in berry crops. Pest Manag Sci 67:1375–1385.  https://doi.org/10.1002/ps.2242 CrossRefPubMedGoogle Scholar
  14. Calatayud PA, Seligmann CD, Polanía MA, Bellotti AC (2001) Influence of parasitism by encyrtid parasitoids on the feeding behaviour of the cassava mealybug Phenacoccus herreni. Entomol Exp Appl 98:271–278.  https://doi.org/10.1023/A:1018947527397 CrossRefGoogle Scholar
  15. Casida JE, Durkin KA (2013) Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annu Rev Entomol 58:99–117.  https://doi.org/10.1146/annurev-ento-120811-153645 CrossRefPubMedGoogle Scholar
  16. Cervantes FA, Backus EA (2018) EPG waveform library for Graphocephala atropunctata (Hemiptera: Cicadellidae): Effect of adhesive, input resistor, and voltage levels on waveform appearance and probing behaviors. J Insect Physiol 109:21–40CrossRefGoogle Scholar
  17. Cervantes FA, Backus EA, Godfrey L et al (2017a) Ecology and behavior correlation of electropenetrography waveforms from Lygus lineolaris (Hemiptera: Miridae) feeding on cotton squares with chemical evidence of inducible tannins. J Econ Entomol 110:2068–2075.  https://doi.org/10.1093/jee/tox198 CrossRefPubMedGoogle Scholar
  18. Cervantes FA, Backus EA, Godfrey L et al (2017b) Behavior characterization of an EPG waveform library for adult Lygus lineolaris and Lygus hesperus (Hemiptera: Miridae) feeding on cotton squares. Ann Entomol Soc Am 109:684–697.  https://doi.org/10.1093/aesa/saw039 CrossRefGoogle Scholar
  19. 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
  20. Civolani S, Cassanelli S, Chicca M et al (2014) An EPG study of the probing behavior of adult Bemisia tabaci Biotype Q (Hemiptera: Aleyrodidae) following exposure to cyantraniliprole. J Econ Entomol 107:910–919.  https://doi.org/10.1603/EC13511 CrossRefPubMedGoogle Scholar
  21. Cole RA, Riggall W, Morgan A (1993) Electronically monitored feeding behaviour of the lettuce root aphid (Pemphigus bursarius) on resistant and susceptible lettuce varieties. Entomol Exp Appl 68:179–185CrossRefGoogle Scholar
  22. Coronado-gonzalez PA, Vijaysegaran S, Robinson AS (2008) Functional morphology of the mouthparts of the adult Mediterranean fruit fly, Ceratitis capitata. J Insect Sci 8:1–11CrossRefGoogle Scholar
  23. Daniels M, Bale JS, Newbury HJ et al (2009) A sublethal dose of thiamethoxam causes a reduction in xylem feeding by the bird cherry-oat aphid (Rhopalosiphum padi), which is associated with dehydration and reduced performance. J Insect Conserv 55:758–765.  https://doi.org/10.1016/j.jinsphys.2009.03.002 CrossRefGoogle Scholar
  24. Deprá M, Poppe JL, Schmitz HJ et al (2004) The first records of the invasive pest Drosophila suzukii in the South American continent. J Pest Sci 87:379–383.  https://doi.org/10.1007/s10340-014-0591-5 CrossRefGoogle Scholar
  25. Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on benefitial arthropods. Annu Rev Entomol 52:81–206.  https://doi.org/10.1146/annurev.ento.52.110405.091440 CrossRefGoogle Scholar
  26. Ebert TA, Backus EA, Cid M et al (2015) A new SAS program for behavioral analysis of electrical penetration graph data. Comput Electron Agric 116:80–87.  https://doi.org/10.1016/j.compag.2015.06.011 CrossRefGoogle Scholar
  27. Garzo E, Moreno A, Hernando S et al (2015) Electrical penetration graph technique as a tool to monitor the early stages of aphid resistance to insecticides. Pest Manag Sci 72:707–718.  https://doi.org/10.1002/ps.4041 CrossRefPubMedGoogle Scholar
  28. Gatehouse JA (2002) Plant resistance towards insect herbivores: a dynamic interaction. New Phytol 156:145–169.  https://doi.org/10.1046/j.1469-8137.2002.00519.x CrossRefGoogle Scholar
  29. Guedes RNC, Smagghe G, Stark JD, Desneux N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annu Rev Entomol 61:43–62.  https://doi.org/10.1146/annurev-ento-010715-023646 CrossRefPubMedGoogle Scholar
  30. Guedes RNC, Walse SS, Throne JE (2017) Sublethal exposure, insecticide resistance, and community stress. Curr Opin Insect Sci 21:47–53.  https://doi.org/10.1016/j.cois.2017.04.010 CrossRefPubMedGoogle Scholar
  31. Guedes RNC, Corbett S, Rodriguez M, Walse JJGSS (2018) Pesticide-mediated disruption of spotted wing Drosophila flight response to raspberries. J Appl Entomol 142:457–464.  https://doi.org/10.1111/jen.12500 CrossRefGoogle Scholar
  32. Guedes RNC, Cervantes FA, Backus EA, Walse SS (2019) Substrate-mediated feeding and egg-laying by spotted wing drosophila: waveform recognition and quantification via electropenetrography. J Pest Sci 92:495–507.  https://doi.org/10.1007/s10340-018-1065-y CrossRefGoogle Scholar
  33. 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
  34. Harrewijn P (1997) Pymetrozine, a fast-acting and selective inhibitor of aphid feeding. In-situ studies with electronic monitoring of feeding behaviour. Pestic Sci 49:130–140CrossRefGoogle Scholar
  35. Harrewijn P, Piron PGM, Mollema C (1996) Electrically recorded probing behaviour of thrips species on optimal and suboptimal hosts. Entomol Exp Appl 80:43–45CrossRefGoogle Scholar
  36. Hauser M (2011) A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. Pest Manag Sci 67:1352–1357.  https://doi.org/10.1002/ps.2265 CrossRefPubMedGoogle Scholar
  37. He Y, Zhao J, Zheng Y et al (2013) Assessment of potential sublethal effects of various insecticides on key biological traits of the tobacco whitefly, Bemisia tabaci. Int J Biol Sci 9:246–255.  https://doi.org/10.7150/ijbs.5762 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Holopainen JK, Blande JD (2013) Where do herbivore-induced plant volatiles go? Front Plant Sci 4:1–13.  https://doi.org/10.3389/fpls.2013.00185 CrossRefGoogle Scholar
  39. Itskov PM, Moreira J-M, Vinnik E et al (2014) Automated monitoring and quantitative analysis of feeding behaviour in Drosophila. Nat Commun 5:4560.  https://doi.org/10.1038/ncomms5560 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Jaenike J (1990) Host specialization in phytophagous insects. Annu Rev Ecol Syst 21:243–273CrossRefGoogle Scholar
  41. Jurgens A, Bischoff M (2016) Changing odour landscapes: the effect of anthropogenic volatile pollutants on plant—pollinator olfactory communication. Funct Ecol.  https://doi.org/10.1111/1365-2435.12774 CrossRefGoogle Scholar
  42. Kindt F, Joosten NN, Peters D, Tjallingii WF (2003) Characterisation of the feeding behaviour of western flower thrips in terms of electrical penetration graph (EPG) waveforms. J Insect Physiol 49:183–191.  https://doi.org/10.1016/S0022-1910(02)00255-X CrossRefPubMedGoogle Scholar
  43. Labandeira CC (1997) Insect mouthparts: ascertaining the paleobiology of insect feeding strategies. Annu Rev Entomol 28:153–193Google Scholar
  44. Lee JC, Bruck DJ, Dreves AJ et al (2011) Spotted wing drosophila, Drosophila suzukii, across perspectives. Pest Manag Sci 67:1349–1351.  https://doi.org/10.1002/ps.2271 CrossRefPubMedGoogle Scholar
  45. Lee JC, Dalton DT, Swoboda-Bhattarai KA, Bruck DJ, Burrack HJ, Strik BC, Woltz JM, Walton VM (2016) Characterization and manipulation of fruit susceptibility to Drosophila suzukii. J Pest Sci 89:771–780.  https://doi.org/10.1007/s10340-015-0718-3 CrossRefGoogle Scholar
  46. Leroux P (1996) Recent developments in the mode of action of fungicides. Pestic Sci 47:191–197CrossRefGoogle Scholar
  47. Lihoreau M, Poissonnier L, Isabel G, Dussutour A (2016) Drosophila females trade off good nutrition with high-quality oviposition sites when choosing foods. J Exp Biol 219:2514–2524.  https://doi.org/10.1242/jeb.142257 CrossRefPubMedGoogle Scholar
  48. Lin Q-C, Zhai Y-F, Zhou C-G, Li L-L, Zhuang Q-Y, Zhang X-Y, Zalom FG, Yu Y (2014) Behavioral rhythms of Drosophila suzukii and Drosophila melanogaster. Fla Entomol 97:1424–1433.  https://doi.org/10.1653/024.097.0417 CrossRefGoogle Scholar
  49. Losel PM, Goodman LJ (1993) Effects on the feeding behaviour of Nilaparvata lugens (Stal) of sublethal concentrations of the foliarly applied nitromethylene heterocycle 2-nitromethylene-1,3-thiazinan-3-yl-carbamaldehyde. Physiol Entomol 18:67–74CrossRefGoogle Scholar
  50. Morita M, Ueda T, Yoneda T, Koyanagi T (2007) Flonicamid, a novel insecticide with a rapid inhibitory effect on aphid feeding. Pest Manag Sci 973:969–973.  https://doi.org/10.1002/ps.1423 CrossRefGoogle Scholar
  51. Nisbet AJ, Woodford JAT, Strang RHC, Connolly JD (1993) Systemic antifeedant effects of azadirachtin on the peach-potato aphid Myzus persicae. Entomol Exp Appl 68:87–98CrossRefGoogle Scholar
  52. McLean DL, Kinsey MG (1964) A technique for electronically recording aphid feeding and salivation. Nature 202:1358–1359CrossRefGoogle Scholar
  53. Plantamp C, Estragnat V, Fellous S et al (2017) Where and what to feed? Differential effects on fecundity and longevity in the invasive Drosophila suzukii. Basic Appl Ecol 19:56–66.  https://doi.org/10.1016/j.baae.2016.10.005 CrossRefGoogle Scholar
  54. Rangasamy M, Mcauslane HJ, Backus EA, Cherry RH (2015) Differential probing behavior of Blissus insularis (Hemiptera: Blissidae) on resistant and ausceptible St. Augustinegrasses. J Econ Entomol 108:780–788.  https://doi.org/10.1093/jee/tou061 CrossRefPubMedGoogle Scholar
  55. Rota-Stabelli O, Blaxter M, Anfora G (2013) Drosophila suzukii. Curr Biol 23:R8–R9.  https://doi.org/10.1016/j.cub.2012.11.021 CrossRefPubMedGoogle Scholar
  56. Salgado VL, Sparks TC (2010) The spinosyns: chemistry, biochemistry, mode of action, and resistance. In: Gilbert LI, Latrou K, Gill SS (eds) Comprehensive molecular insect science. Elsevier, Oxford, pp 137–173Google Scholar
  57. Sih A (2013) Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview. Anim Behav 85:1077–1088.  https://doi.org/10.1016/j.anbehav.2013.02.017 CrossRefGoogle Scholar
  58. Simpson SJ, Clissold FJ, Lihoreau M et al (2015) Recent advances in the integrative nutrition of arthropods. Annu Rev Entomol 60:293–311.  https://doi.org/10.1146/annurev-ento-010814-020917 CrossRefPubMedGoogle Scholar
  59. Smirle MJ, Zurowski CL, Ayyanath M et al (2017) Laboratory studies of insecticide efficacy and resistance in Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) populations from British Columbia, Canada. Pest Manag Sci 73:130–137.  https://doi.org/10.1002/ps.4310 CrossRefPubMedGoogle Scholar
  60. Smith TB, Kinnison MT, Strauss SY et al (2014) Prescriptive evolution to conserve and manage biodiversity. Annu Rev Ecol Evol Syst 45:1–22.  https://doi.org/10.1146/annurev-ecolsys-120213-091747 CrossRefGoogle Scholar
  61. Sparks TC, Crouse GD, Durst G (2001) Natural products as insecticides: the biology, biochemistry and quantitative structure-activity relationships of spinosyns and spinosoids. Pest Manag Sci 57:896–905.  https://doi.org/10.1002/ps.358 CrossRefPubMedGoogle Scholar
  62. Stoffolano JG Jr, Haselton AT (2013) The adult dipteran crop: a unique and overlooked organ. Annu Rev Entomol 58:205–228.  https://doi.org/10.1146/annurev-ento-120811-153653 CrossRefPubMedGoogle Scholar
  63. Tait G, Grassi A, Pfab F, Crava CM, Dalton DT, Magarey R et al (2018) Large-scale spatial dynmaics of Drosophila suzukii in Trentino, Italy. J Pest Sci 91:1213–1224.  https://doi.org/10.1007/s10340-018-0985-x CrossRefGoogle Scholar
  64. Tariq K, Noor M, Backus EA et al (2017) The toxicity of flonicamid to cotton leafhopper, Amrasca biguttula (Ishida), is by disruption of ingestion: an electropenetrography study. Pest Manag Sci 73:1661–1669.  https://doi.org/10.1002/ps.4508 CrossRefPubMedGoogle Scholar
  65. 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.  https://doi.org/10.1016/j.cropro.2013.08.003 CrossRefGoogle Scholar
  66. Tjallingii FT (1978) Electronic recording of penetration behaviour by aphids. Ent Exp Appl 24:721–730CrossRefGoogle Scholar
  67. Vijaysegaran S, Walter GH, Drew RAI (1997) Mouthpart structure, feeding mechanisms, and natural food sources of adult Bactrocera (Diptera: Tephritidae). Ann Entomol Soc Am 90:184–201CrossRefGoogle Scholar
  68. Walker GP (2000) A Beginner’s guide to electronic monitoring. In: Walker GP, Backus EA (eds) Principles and applications of electronic monitoring and other techniques in the study of homopteran feeding behavior. Entomological Soceity of America, Annapolis, pp 14–40Google Scholar
  69. Walse SS, Krugner R, Tebbets JS (2012) Postharvest treatment of strawberries with methyl bromide to control spotted wing drosophila, Drosophila suzukii. J Asia Pac Entomol 15:451–456.  https://doi.org/10.1016/j.aspen.2012.05.003 CrossRefGoogle Scholar
  70. Wong JS, Cave AC, Lightle DM, Mahaffee WF, Naranjo SE, Wiman NG et al (2018) Drosophila suzukii flight performance reduced by starvation but not affected by humidity. J Pest Sci 91:1269–1278.  https://doi.org/10.1007/s10340-018-1013-x CrossRefGoogle Scholar
  71. Xue K, Wang X-Y, Huang C-H et al (2009) Stylet penetration behaviors of the cotton aphid Aphis gossypii on transgenic Bt cotton. Insect Sci 16:137–146.  https://doi.org/10.1111/j.1744-7917.2009.00265.x CrossRefGoogle Scholar
  72. Yang C, Hamel C, Vujanovic V, Gan Y (2011) Fungicide : modes of action and possible impact on nontarget microorganisms. ISRN Ecol ID 130289.  https://doi.org/10.5402/2011/130289
  73. Youn Y, Backus EA, Serikawa RH, Lukasz L (2011) Correlation of an electrical penetration graph waveform with walking by Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae). Fla Entomol 94:1084–1087CrossRefGoogle Scholar

Copyright information

© This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply  2019

Authors and Affiliations

  1. 1.USDA-ARS San Joaquin Valley Agricultural Sciences CenterParlierUSA
  2. 2.Departamento de EntomologiaUniversidade Federal de ViçosaViçosaBrazil

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