Abstract
Substrate suitability is a key determinant of feeding and egg-laying decisions by arthropods and rigorous observation of such activities provides important management insight. Electropenetrography (EPG) was used to analyze feeding and egg-laying by the spotted wing drosophila (Drosophila suzukii (Matsumura)) on artificial diet and strawberry fruits. Three behavioral phases were recognized on both substrates: non-probing, feeding, and egg-laying. The non-probing phase encompassed a family of waveforms consisting of resting (coded as Z), grooming (G), and walking (W). The feeding phase encompassed waveforms representing substrate dabbing (D) and ingestion (I), while the egg-laying phase encompassed abdominal probing (P) and egg-laying (L) per se. The egg-laying phase was similar on diet and strawberry. In contrast, non-probing events were more frequent, but shorter, leading to less overall non-probing on diet compared with strawberry. Dabbing was more frequent and lasted longer overall on diet, but ingestion events lasted longer on strawberry. Therefore, although the flies fed (dabbed and ingested) for longer overall on diet, each ingestion event was longer on strawberries. Our results suggest that strawberry fruits are a more suitable and preferred food source because they led to extended periods of sustained ingestion. These findings demonstrate the first application of EPG for characterizing substrate-specific feeding and egg-laying behaviors of a key phytophagous pest, offering intriguing insight into management as well as host selection behaviors.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
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 (2004) 88:469–494. https://doi.org/10.1007/s10340-015-0681-z
Atallah J, Teixeira L, Salazar R et al (2014) The making of a pest: the evolution of a fruit-penetrating ovipositor in Drosophila suzukii and related species. Proc R Soc B 281:20132840. https://doi.org/10.1098/rspb.2013.2840
Backus EA (1994) History, development, and applications of the AC electronic monitoring system for insect feeding. In: Ellsbury MM, Backus EA, Ullman DL (eds) History, development, and application of AC electronic insect feeding monitors. Thomas Say Publications, Entomological Society of America, Annapolis, pp 1–50
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 Society of America, Annapolis, pp 1–13
Backus EA (2016) Sharpshooter feeding behavior in relation to transmission of Xylella fastidiosa: a model for foregut-borne transmission mechanisms. In: Brown JK (ed) Vector-mediated transmission of plant pathogens. American Phytopathological Society, St. Paul, pp 175–193
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
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
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 data. Ann Entomol Soc Am 100:296–310
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
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
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
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
Cervantes FA, Backus EA, Godfrey L et al (2017) 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
Cervantes FA, Backus EA, Perring TM (2018) EPG waveform library for Graphocephala atropunctata (Hemiptera: Cicadellidae): effect of input resistor and voltage levels on waveform appearance and probing behaviors. J Insect Physiol 109:21–40. https://doi.org/10.1016/j.jinsphys.2018.05.008
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 65:149–160
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 68:179–185
Coronado-Gonzalez PA, Vijaysegaran S, Robinson AS (2008) Functional morphology of the mouthparts of the adult mediterranean fruit fly, Ceratitis capitata. J Insect Sci 8:1–11
Deprá M, Poppe JL, Schmitz HJ et al (2014) The first records of the invasive pest Drosophila suzukii in the South American continent. J Pest Sci (2004) 87:379–383. https://doi.org/10.1007/s10340-014-0591-5
Ebert TA, Backus EA, Cid M, Ferreres A, Rogers ME (2015) A new SAS program for behavioral analysis of electrical penetration graph data. Comp Electron Agric 116:80–87. https://doi.org/10.1016/j.compag.2015.06.011
Fox CW, Czesak ME (2000) The evolutionary ecology of progeny size in arthropods. Annu Rev Entomol 45:341–369. https://doi.org/10.1146/annurev.ecolsys.34.011802.132339
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
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
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
Guedes RNC, Corbett S, Rodriguez M, Goto JJ, Walse SS (2018) Pesticide-mediated disruption of spotted wing Drosophila flight response to raspberries. J Appl Entomol (in press). https://doi.org/10.1111/jen.12500
Hamby KA, Bellamy DE, Chiu JC et al (2016) Biotic and abiotic factors impacting development, behavior, phenology, and reproductive biology of Drosophila suzukii. J Pest Sci (2004) 89:605–619. https://doi.org/10.1007/s10340-016-0756-5
Harrewijn P, Piron PGM, Mollema C (1996a) Electrically recorded probing behaviour of thrips species on optimal and suboptimal hosts. Entomol Exp Appl 80:43–45
Harrewijn P, Tjallingii WF, Mollema C (1996b) Electrical recording of plant penetration by western flower thrips. Entomol Exp Appl 79:345–353
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
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 (2004) 89:643–651. https://doi.org/10.1007/s10340-016-0737-8
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
Jaenike J (1990) Host specialization in phytophagous insects. Annu Rev Ecol Syst 21:243–273
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
Labandeira CC (1997) Insect mouthparts: ascertaining the paleobiology of insect feeding strategies. Annu Rev Entomol 28:153–193
Lasa R, Tadeo E, Dinor LA et al (2017) Fruit firmness, superficial damage, and location modulate infestation by Drosophila suzukii and Zaprionus indianus: the case of guava in Veracruz, Mexico. Entomol Exp Appl 162:4–12. https://doi.org/10.1111/eea.12519
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
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
Lucini T, Panizzi AR (2017) Feeding behavior of the stink bug Dichelops melacanthus (Heteroptera: Pentatomidae) on maize seedlings: an EPG analysis at multiple input impedances and histology correlation. Ann Entomol Soc Am 110:160–171. https://doi.org/10.1093/aesa/saw070
McLean DL, Kinsey MG (1964) A technique for electronically recording aphid feeding and salivation. Nature 202:1358–1359
Nam KJ, Hardie J (2012) Reproduction and probing behaviour of the bird cherry-oat aphid Rhopalosiphum padi on detached leaves and leaves on intact seedlings of the winter host, bird cherry Prunus padus. Physiol Entomol 37:196–200. https://doi.org/10.1111/j.1365-3032.2011.00809.x
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
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. https://doi.org/10.1093/jee/tou061
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
Serrano MS, Backus EA, Cardona C (2000) Comparison of electronic monitoring data and field evaluations to characterize tolerant genotypes of common beans to Empoasca kraemeri Ross & Moore (Homoptera: Cicadellidae). J Econ Entomol 93:1796–1809
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
Stewart TJ, Wang X-G, Molinar A, Daane KM (2014) Factors limiting peach as a potential host for Drosophila suzukii (Diptera: Drosophiilidae). J Econ Entomol 107:1771–1779. https://doi.org/10.1603/EC14197
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
Tjallingii WF (2000) Comparison of AC and DC systems for electronic monitoring of stylet penetration activities by hompterans. In: Walker GP, Backus EA (eds) Principles and applications of electronic monitoring and other techniques in the study of homopteran feeding behavior. Entomological Society of America, Annapolis, pp 41–69
Tosh CR, Powell G, Hardie J (2003) Decision making by generalist and specialist aphids with the same genotype. J Insect Physiol 49:659–669. https://doi.org/10.1016/S0022-1910(03)00066-0
Vijaysegaran S, Walter GH, Drew RAI (1997) Mouthpart structure, feeding mechanisms, and natural food sources of adult Bactrocera (Diptera: Tephritidae). Ann Entomol Soc Am 90:184–201
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 Society of America, Annapolis, pp 14–40
Walker GP, Perring TM (1994) Feeding and oviposition behavior of whiteflies (Homoptera: Aleyrodidae) interpreted from AC electronic feeding monitor waveforms. Ann Entomol Soc Am 87:363–374. https://doi.org/10.1093/aesa/87.3.363
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
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
Youn Y, Backus EA, Serikawa RH, Stelinski LL (2011) Correlation of an electrical penetration graph waveform with walking by Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae). Flor Entomol 94:1084–1087
Acknowledgements
Financial support was provided by the CAPES Foundation (Brazilian Ministry of Education), and USDA-ARS, which was greatly appreciated. The research was 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 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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
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.
Additional information
Communicated by A. Biondi.
Rights and permissions
About this article
Cite this article
Guedes, R.N.C., Cervantes, F.A., Backus, E.A. et al. Substrate-mediated feeding and egg-laying by spotted wing drosophila: waveform recognition and quantification via electropenetrography. J Pest Sci 92, 495–507 (2019). https://doi.org/10.1007/s10340-018-1065-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-018-1065-y