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Characterization of electropenetrography waveforms for the invasive heteropteran pest, Halyomorpha halys, on Vicia faba leaves

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Abstract

The brown marmorated stink bug (BMSB), Halyomorpha halys Stål, has dispersed throughout the northern hemisphere, causing disturbances in agroecosystems and urban areas. Studies are, therefore, needed on the biology, physiology, and ecology of BMSB. This project characterized and partially correlated (via histology of plant tissues) the DC electropenetrography (EPG) waveforms related to non-probing (NP and Z) and both salivary sheath and cell rupture feeding. BMSB feeding behaviors were analyzed in comparison with the five other EPG waveform characterization papers published to date for heteropteran insects. Waveforms consisted of epidermal scanning (Hh1), pathway of stylets through leaf tissue (Hh2), X waves (Hh3), and sustained vascular ingestion (Hh4). In addition, a cell-rupturing phase in mesophyll (Hh2) and putative ingestion of resulting macerate (Hh5) were characterized. The most striking results were (1) the similarities of waveforms with other heteropterans, (2) performance of both sheath and cell rupture feeding strategies from all three plant cell types (xylem, likely phloem, and parenchyma macerate) on the same plant part, and (3) two different-appearing, dual-meaning X waves according to ingestion from xylem (Hh3a) or likely from phloem (Hh3b). This study provides a crucial framework for future, quantitative research on feeding behavior of this important invasive pest, to aid in the development of novel pest management tools.

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References

  • Backus EA (1988) Sensory systems and behaviours which mediate hemipteran plant-feeding: a taxonomic overview. J Insect Physiol 34:151–165. https://doi.org/10.1016/0022-1910(88)90045-5

    Article  Google Scholar 

  • 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 pathogen. American Phytopathological Society, St. Paul, MN, 496 pp

    Google Scholar 

  • Backus EA, Serrano MS, Ranger CM (2005) Mechanisms of hopperburn: an overview of insect taxonomy, behavior, and physiology. Annu Rev Entomol 50:125–151. https://doi.org/10.1146/annurev.ento.49.061802.123310

    Article  CAS  PubMed  Google Scholar 

  • Backus EA, Holmes WJ, Schreiber F et al (2009) Sharpshooter X wave: correlation of an electrical penetration graph waveform with xylem penetration supports a hypothesized mechanism for Xylella fastidiosa inoculation. Ann Entomol Soc Am 102:847–867

    Article  Google Scholar 

  • Backus EA, Rangasamy M, Stamm M et al (2013) Waveform library for chinch bugs (Hemiptera: Heteroptera: Blissidae): characterization of electrical penetration graph waveforms at multiple input impedances. Ann Entomol Soc Am 106:524–539

    Article  Google Scholar 

  • Backus EA, Cervantes FA, Godfrey L et al (2018) Certain applied electrical signals during EPG cause negative effects on stylet probing behaviors by adult Lygus lineolaris (Hemiptera: Miridae). J Insect Physiol 105:64–75. https://doi.org/10.1016/j.jinsphys.2017.12.006

    Article  CAS  PubMed  Google Scholar 

  • Backus EA, Cervantes FA, Guedes RNC et al (2019) AC–DC electropenetrography for in-depth studies of feeding and oviposition behaviors. Ann Entomol Soc Am 112:236–248. https://doi.org/10.1093/aesa/saz009

    Article  Google Scholar 

  • Carpane P, Wayadande A, Backus EA et al (2011) Characterization and correlation of new electrical penetration graph waveforms for the corn leafhopper (Hemiptera: Cicadellidae). Ann Entomol Soc Am 104:515–525. https://doi.org/10.1603/an10052

    Article  Google Scholar 

  • Cervantes FA, Backus EA, Godfrey L et al (2016) 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

    Article  Google Scholar 

  • Chuche J, Backus EA, Thiéry D, Sauvion N (2017) First finding of a dual-meaning X wave for phloem and xylem fluid ingestion: characterization of Scaphoideus titanus (Hemiptera: Cicadellidae) EPG waveforms. J Insect Physiol 102:50–61. https://doi.org/10.1016/j.jinsphys.2017.01.013

    Article  CAS  PubMed  Google Scholar 

  • Dugravot S, Backus EA, Reardon BJ, Miller TA (2008) Correlations of cibarial muscle activities of Homalodisca spp. Sharpshooters (Hemiptera: Cicadellidae) with EPG ingestion waveform and excretion. J Insect Physiol 54:1467–1478. https://doi.org/10.1016/j.jinsphys.2008.05.008

    Article  CAS  PubMed  Google Scholar 

  • Lee D-H, Short BD, Joseph SV et al (2013) Review of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea. Environ Entomol 42:627–641

    Article  Google Scholar 

  • Lucini T, Panizzi AR (2016) Waveform characterization of the soybean stem feeder Edessa meditabunda: overcoming the challenge of wiring pentatomids for EPG. Entomol Exp Appl 158:118–132. https://doi.org/10.1111/eea.12389

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lucini T, Panizzi AR (2018) Electropenetrography (EPG): a breakthrough tool unveiling stink bug (Pentatomidae) feeding on plants. Neotrop Entomol 47:6–18. https://doi.org/10.1007/s13744-017-0574-3

    Article  CAS  PubMed  Google Scholar 

  • Lucini T, Panizzi AR, Backus EA (2016) Characterization of an EPG waveform library for redbanded stink bug, Piezodorus guildinii (Hemiptera: Pentatomidae), on soybean plants. Ann Entomol Soc Am 109:198–210. https://doi.org/10.1093/aesa/sav156

    Article  Google Scholar 

  • Maistrello L, Dioli P, Bariselli M et al (2016) Citizen science and early detection of invasive species: phenology of first occurrences of Halyomorpha halys in Southern Europe. Biol Invasions 18:3109–3116. https://doi.org/10.1007/s10530-016-1217-z

    Article  Google Scholar 

  • Musolin DL, Konjević A, Karpun NN et al (2018) Invasive brown marmorated stink bug Halyomorpha halys (Stål) (Heteroptera: Pentatomidae) in Russia, Abkhazia, and Serbia: history of invasion, range expansion, early stages of establishment, and first records of damage to local crops. Arthropod Plant Interact 12:517–529. https://doi.org/10.1007/s11829-017-9583-8

    Article  Google Scholar 

  • Rice KB, Bergh CJ, Bergmann EJ et al (2014) Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). J Integr Pest Manag 5:1–13. https://doi.org/10.1603/IPM14002

    Article  Google Scholar 

  • Tjallingii WF (1978) Electronic recording of penetration behaviour by aphids. Entomol Exp Appl 24:521–530

    Google Scholar 

  • Tjallingii WF, Prado E (2001) Analysis of circulative transmission by electrical penetration graphs. Virus Insect Plant Interact. https://doi.org/10.1016/b978-012327681-0/50007-8

    Article  Google Scholar 

  • Wayadande AC, Nault LR (1993) Leafhopper probing behavior associated with maize chlorotic dwarf virus transmission to maize. Phytochemistry 83:522–526

    Google Scholar 

  • Wermelinger B, Wyniger D, Forster B (2008) First records of an invasive bug in Europe: Halyomorpha halys Stål (Heteroptera: Pentatomidae), a new pest on woody ornamentals and fruit trees? Mitteilungen der Schweizerischen Entomol Gesellschaft 81:1–8

    Google Scholar 

  • Wiman NG, Walton VM, Shearer PW, Rondon SI (2014) Electronically monitored labial dabbing and stylet ‘probing’ behaviors of brown marmorated stink bug, Halyomorpha halys, in simulated environments. PLoS ONE 9:e113514. https://doi.org/10.1371/journal.pone.0113514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Youn Y, Backus EA, Serikawa RH, Stelinski LL (2012) Correlation of an Electrical Penetration Graph Waveform with Walking by Asian Citrus Psyllid, Diaphorina citri (Hemiptera: Psyllidae). Florida Entomol 94:1084–1087. https://doi.org/10.1653/024.094.0456

    Article  Google Scholar 

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Authors and Affiliations

  1. Functional and Evolutionary Entomology, Gembloux Agro-Bio Tech, University of Liege, Passage des Deportes 2, 5030, Gembloux, Belgium

    Laurent Serteyn, Lola Ponnet & Frederic Francis

  2. USDA, Agricultural Research Service, San Joaquin Valley Agricultural Sciences Center, 9611 South Riverbend Avenue, Parlier, CA, 93648-9757, USA

    Elaine A. Backus

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  1. Laurent Serteyn
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  2. Lola Ponnet
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  3. Elaine A. Backus
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  4. Frederic Francis
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Contributions

LS, LP, and FF conceived and designed research. LS and LP conducted experiments. LS, LP, and EAB analyzed data. LS and EAB wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Laurent Serteyn.

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Handling Editor: Chen-Zhu Wang.

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Elaine A. Backus: 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.

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Serteyn, L., Ponnet, L., Backus, E.A. et al. Characterization of electropenetrography waveforms for the invasive heteropteran pest, Halyomorpha halys, on Vicia faba leaves. Arthropod-Plant Interactions 14, 113–126 (2020). https://doi.org/10.1007/s11829-019-09722-y

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