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Role of EPG in Developing and Assessing Control Methods for Heteropteran Crop Pests

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Electronic Monitoring of Feeding Behavior of Phytophagous True Bugs (Heteroptera)

Part of the book series: Entomology in Focus ((ENFO,volume 6))

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Abstract

The multiple interactions of the electrical penetration graph (EPG) technique with various strategies that can be used to manage pests of crop plants are presented and discussed in this chapter. We here include insecticides, still the main tool in use to control true bug pests worldwide by either contact action or systemic circulation in plants; plants that show resistance in the broad sense, either by traditional plant breeding or by advanced genetically modified (GM) techniques; natural enemies, including parasitoids, pathogens, and zoophytophagous predatory Heteroptera; and gene silencing by interference RNA. These strategies, with the potential to control heteropterans and other crop pests, will benefit from the information that the EPG technique can provide, enhancing their efficiency as pest control measures.

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References

  • Abbate S, Lucini T, Bonansea S, Bentancur O, Altier N, Pons X, Panizzi AR (2019) Bt soybean does not affect feeding behavior of red-banded stink bug Piezodorus guildinii (Hemiptera: Pentatomidae). XIX international plant protection congress, Hyderabad, India, Abstract

    Google Scholar 

  • Agostinetto A, Panizzi AR, Lucini T (2018) Monthly parasitism rate by tachinid flies and egg allocation on the body of Dichelops furcatus. Fla Entomol 101:91–96

    Article  Google Scholar 

  • Aldrich JM, Khrimian A, Zhang A, Shearer PW (2006) Bug pheromones (Hemiptera, Heteroptera) and tachinid fly host-finding. Denisia 50:1015–1031

    Google Scholar 

  • Almeida ACS, Jesus FG, Barrigossi JAF (2020) Unveiling the feeding behavior of Tibraca limbativentris (Hemiptera: Pentatomidae) on rice using an electropenetrography waveform library. J Insect Sci 20:14;1–8

    Google Scholar 

  • Alvarez AE, Tjallingii WF, Garzo E, Vleeshouwers V, Dicke M, Vosman B (2006) Location of resistance factors in the leaves of potato and wild tuber-bearing Solanum species to the aphid Myzus persicae. Entomol Exp Appl 121:145–157

    Article  Google Scholar 

  • Backus EA, Rangasamy M, Stamm M, McAuslane HJ, Cherry R (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

    Google Scholar 

  • Baldin, ELL, Vendramim JD, Lourenção AL (2019) Plant resistance to insects. Fundamentals and applications. University of São Paulo Press, FEALQ, Piracicaba, São Paulo (in Portuguese)

    Google Scholar 

  • Barrera-López AA, Guzmán-Franco AW, Santillán-Galicia M, Tamayo-Mejía F, Bujanos-Muñiz R, García-Ávila CJ, López-Buenfil JÁ (2020) Differential susceptibility of Bagrada hilaris (Hemiptera: Pentatomidae) to different species of fungal pathogens. J Econ Entomol 113:50–54

    PubMed  Google Scholar 

  • Basnet S, Kamble ST (2018a) RNA interference of the muscle actin gene in bed bugs: exploring injection versus topical application for dsRNA delivery. J Insect Sci 18:5;1–5

    Google Scholar 

  • Basnet S, Kamble ST (2018b) Knockdown of the chromatin remodeling gene brahma by RNA interference reduces reproductive fitness and lifespan in common bed bug (Hemiptera: Cimicidae). J Med Entomol 55:534–539

    Article  CAS  PubMed  Google Scholar 

  • Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P, Ilagan O, Johnson S, Plaetinck G, Munyikwa T, Pleau M, Vaughn T, Roberts J (2007) Control of coleopteran insect pests through RNA interference. Nat Biotechnol 25:1322–1326

    Article  CAS  PubMed  Google Scholar 

  • Baverstock J, Roy HE, Pell JK (2010) Entomopathogenic fungi and insect behaviour: from unsuspecting hosts to targeted vectors. BioControl 55:89–102

    Article  Google Scholar 

  • Bloomquist JR (1996) Ion channels as targets for insecticides. Annu Rev Entomol 41:163–190

    Article  CAS  PubMed  Google Scholar 

  • Britt K, Grant GJ, Wiggins GJ, Stewart SD (2016) Prevalence and localized infection on the entomopathogenic fungus Beauveria bassiana on kudzu bug (Hemiptera: Plataspidae) in eastern Tennessee. J Entomol Sci 51:321–324

    Google Scholar 

  • Cagliari D, Dias NP, Santos EA, Rickes LN, Kremer FS, Farias JR, Lenz G, Galdeano DM, Garcia FRM, Smagghe G, Zotti MJ (2020) First transcriptome of the Neotropical pest Euschistus heros (Hemiptera: Pentatomidae) with dissection of its siRNA machinery. Sci Rep 10:4856;1–16

    Google Scholar 

  • Campos M, Knutson A, Heitholt J, Campos C (2010) Resistance to seed feeding by southern green stink bug, Nezara viridula (Linnaeus), in soybean, Glycine max (L.) Merrill. Southwest Entomol 35:233–239

    Article  Google Scholar 

  • Casida JE (2018) Neonicotinoids and other insect nicotinic receptor competitive modulators: progress and prospects. Annu Rev Entomol 63:125–144

    Article  CAS  PubMed  Google Scholar 

  • Casida JE, Durkin KA (2013) Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annu Rev Entomol 58:99–117

    Article  CAS  PubMed  Google Scholar 

  • Casida JE, Quistad GB (1998) Golden age of insecticide research: past, present or future? Annu Rev Entomol 43:1–16

    Article  CAS  PubMed  Google Scholar 

  • Castellanos NL, Smagghe G, Sharma R, Oliveira EE, Christiaens O (2019) Liposome encapsulation and EDTA formulation of dsRNA targeting essential genes increase oral RNAi-caused mortality in the Neotropical stink bug Euschistus heros. Pest Manag Sci 75:537–548

    Article  CAS  PubMed  Google Scholar 

  • Cervantes FA, Backus EA, Godfrey L, Akbar W, Clark TL (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

    Article  Google Scholar 

  • Cervantes FA, Backus EA, Godfrey L, Wallis C, Akbar W, Clark TL, Rojas MG (2017) 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

    Article  CAS  PubMed  Google Scholar 

  • Cervantes FA, Backus EA, Godfrey L, Rojas MG, Akbar W, Clark TL (2019) Quantitative differences in feeding behavior of Lygus lineolaris (Hemiptera: Miridae) on transgenic and nontransgenic cotton. J Econ Entomol 112:1920–1925

    Article  CAS  PubMed  Google Scholar 

  • Chakrabarty S, Jin M, Wu C, Chakraborty P, Xiao Y (2020) Bacillus thuringiensis vegetative insecticidal protein family Vip3A and mode of action against pest Lepidoptera. Pest Manag Sci 76:1612–1617

    Article  CAS  PubMed  Google Scholar 

  • Chen WB, Lu GQ, Cheng HM, Liu CX, Xiao YT, Xu C, Shen ZC, Wu KM (2017) Transgenic cotton coexpressing Vip3A and Cry1Ac has a broad insecticidal spectrum against lepidopteran pests. J Invertebr Pathol 149:59–65

    Article  CAS  PubMed  Google Scholar 

  • Chinchilla-Ramírez M, Garzo E, Fereres A, Gavara-Vidal J, ten Broeke CJM, van Loon JJA, Urbaneja A, Pérez-Hedo M (2021) Plant feeding by Nesidiocoris tenuis: quantifying its behavioral and mechanical componentes. Biol Control 152:104402;1–10

    Google Scholar 

  • Christiaens O, Steve Whyard S, Ana M, Vélez AM, Smagghe G (2020) Double-stranded RNA technology to control insect pests: current status and challenges. Frontiers Plant Sci 11:451;1–10

    Google Scholar 

  • Clark WJ, Harris FA, Maxwell FG, Hartwig EE (1972) Resistance of certain soybean cultivars to bean leaf beetle, striped blister beetle, and bollworm. J Econ Entomol 65:1669–1672

    Article  Google Scholar 

  • Cline AR, Backus EA (2002) Correlations among AC electronic monitoring waveforms, body postures, and stylet penetration behaviors of Lygus hesperus (Hemiptera: Miridae). Environ Entomol 31:538–549

    Article  Google Scholar 

  • Cooper AM, Silver K, Zhang J, Park Y, Zhu KY (2019) Molecular mechanisms influencing efficiency of RNA interference in insects. Pest Manag Sci 75:18–28

    Article  CAS  PubMed  Google Scholar 

  • Corrêa-Ferreira BS, Thomazini MJ, Zamataro CE (1991) Effect of Eutrichopodopsis nitens Blanchard on adult longevity and reproduction of Nezara viridula (L.). Pesq Agropec Bras 26:837–842 (in Portuguese)

    Google Scholar 

  • Corrêa-Ferreira BS, Nunes MC, Uguccioni LD (1998) Occurrence of Hexacladia smithii Ashmead parasitoid of Euschistus heros (F.) adults in Brazil. An Soc Entomol Brasil 27:495–498 (in Portuguese)

    Google Scholar 

  • Corso IC, Gazzoni DL (1998) Sodium chloride: an insecticide enhancer for controlling pentatomids on soybeans. Pesq Agropec Brasil 33:1563–1571

    Google Scholar 

  • Davis-Vogel C, Van Allen B, Van Hemert JL, Sethi A, Nelson ME, Sashital DG (2018) Identification and comparison of key RNA interference machinery from western corn rootworm, fall armyworm, and southern green stink bug. PLoS One 13:e0203160;1–26

    Google Scholar 

  • Dhaliwal GS, Singh R (2004) Host plant resistance to insects: concepts and applications. Panima Publication, New Delhi

    Google Scholar 

  • Dias NP, Cagliari D, Santos EA, Smagghe G, Jurat-Fuentes JL (2020) Insecticidal gene silencing by RNAi in the Neotropical region. Neotrop Entomol 49:1–11

    Article  CAS  PubMed  Google Scholar 

  • Diaz-Montano J, Reese JC, Louis J, Campbell LR, Schapaugh WT (2007) Feeding behavior by the soybean aphid (Hemiptera: Aphididae) on resistant and susceptible soybean genotypes. J Econ Entomol 100:984–989

    Article  PubMed  Google Scholar 

  • Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37

    Article  CAS  PubMed  Google Scholar 

  • Duyn JWV, Turnipseed SG, Maxwell JD (1971) Resistance in soybean to the Mexican bean beetle. I. Source of resistance. Crop Sci 11:572–573

    Article  Google Scholar 

  • Eger JE (1981) Oviposition site preference and related aspects of the parasitism of Brochymena spp. by Trichopoda plumipes in College Station, Texas. Environ Entomol 10:468–471

    Article  Google Scholar 

  • Eghrari K, Brito AH, Baldassi A, Balbuena TS, Fernandes OA, Môro GV (2019) Homozygosis of Bt locus increases Bt protein expression and the control of Spodoptera frugiperda (Lepidoptera: Noctuidae) in maize hybrids. Crop Prot 124:104871

    Article  CAS  Google Scholar 

  • Gerolt P (1969) Mode of entry of contact insecticides. J Insect Physiol 15:563–580

    Article  CAS  PubMed  Google Scholar 

  • Ghaffar MBBA, Pritchard J, Ford-Lloyd B (2011) Brown planthopper (N. lugens Stal) feeding behaviour on rice germplasm as an indicator of resistance. PLoS One 6:e22137;1–113

    Google Scholar 

  • Ghosh SKB, Hunter WB, Park AL, Gundersen-Rindal DE (2017) Double strand RNA delivery system for plant-sap-feeding insects. PLoS One 12:e0171861;1–19

    Google Scholar 

  • Gouli V, Gouli S, Skinner M, Hamilton G, Su Kim J, Parker BL (2012) Virulence of select entomopathogenic fungi to the brown marmorated stink bug, Halyomorpha halys (Stål) (Heteroptera: Pentatomidae). Pest Manag Sci 68:155–157

    Article  CAS  PubMed  Google Scholar 

  • Gurusamy D, Howell JL, Chereddy SCRR, Koo J, Palli SR (2020) Transport of orally delivered dsRNA in southern green stink bug, Nezara viridula. Arch Insect Biochem Physiol 104;e21692;1–18

    Google Scholar 

  • Hirose E, Panizzi AR, Cattelan AJ (2006) Potential use of antibiotic to improve performance of laboratory-reared Nezara viridula (L.) (Heteroptera: Pentatomidae). Neotrop Entomol 35:279–281

    Article  PubMed  Google Scholar 

  • Hori K (2000) Possible causes of disease symptons resulting from the feeding of phytophagous Heteroptera. In: Schaefer CW, Panizzi AR (eds) Heteroptera of economic importance. CRC Press, Boca Raton, pp 11–35

    Google Scholar 

  • Howell JL, Mogilicherla K, Gurusamy D, Palli SR (2020) Development of RNAi methods to control the harlequin bug, Murgantia histrionica. Arch Insect Biochem Physiol 104:e21690;1–14

    Google Scholar 

  • Huvenne H, Smagghe G (2010) Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. J Insect Physiol 56:227–235

    Article  CAS  PubMed  Google Scholar 

  • Jacobson AL, Kennedy GG (2014) Electrical penetration graph studies to investigate the effects of cyantraniliprole on feeding behavior of Myzus persicae (Hemiptera: Aphididae) on Capsicum annuum. Pest Manag Sci 70:836–840

    Article  CAS  PubMed  Google Scholar 

  • Joga MR, Zotti MJ, Smagghe G, Christiaens O (2016) RNAi efficiency, systemic properties, and novel delivery methods for pest insect control: what we know so far. Frontiers Physiol 7:553;1–14

    Google Scholar 

  • Jones WA, Sullivan JM (1979) Soybean resistance to the southern green stink bug, Nezara viridula. J Econ Entomol 72:628–632

    Article  Google Scholar 

  • Kamminga KL, Davis JA, Stock SP, Ritcher AR (2012) First report of a mermithid nematode infecting Piezodorus guildinii and Acrosternum hilare (Hemiptera: Pentatomidae) in the United States. Fla Entomol 95:214–217

    Article  Google Scholar 

  • Karabörklü S, Azizoglu U, Azizoglu ZB (2018) Recombinant entomopathogenic agents: a review of biotechnological approaches to pest insect control. World J Microb Biotechnol 34:14;1–12

    Google Scholar 

  • Kariñho-Betancourt E, Núñez-Farfán J (2015) Evolution of resistance and tolerance to herbivores: testing the trade-off hypothesis. PeerJ 3:e789;1–15

    Google Scholar 

  • Koch KG, Donze-Reiner T, Baird LM, Louis J, Amundsen K, Sarath G, Bradshaw JD, Heng-Moss T (2018) Evaluation of greenbug and yellow sugarcane aphid feeding behavior on resistant and susceptible switchgrass cultivars. Bioenergy Res 11:480–490

    Article  CAS  Google Scholar 

  • Latham JR, Love M, Hilbeck A (2017) The distinct properties of natural and GM cry insecticidal proteins. Biotechnol Genet Eng 33:62–96

    Article  CAS  Google Scholar 

  • Li W, Wyckhuys KAG, Wu K (2016) Does feeding behavior of a zoophytophagous mirid differ between host plant and insect prey items? Arthropod Plant Interact 10:79–86

    Article  Google Scholar 

  • Liu J, Poinar GO Jr, Berry RE (2000) Control of insect pests with entomopathogenic nematodes: the impact of molecular biology and phylogenetic reconstruction. Annu Rev Entomol 45:287–306

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Skinner M, Parker BL, Brownbridge M (2002) Pathogenicity of Beauveria bassiana, Metarhizium anisopliae (Deuteromycotina: Hyphomycetes), and other entomopathogenic fungi against Lygus lineolaris (Hemiptera: Miridae). J Econ Entomol 95:675–681

    Google Scholar 

  • Liu XD, Zhai BP, Zhang XX, Zong MJ (2005) Impact of transgenic cotton plants on a non-target pest, Aphis gossypii Glover. Ecol Entomol 30:307–315

    Google Scholar 

  • Lourenção AL, Miranda MAC, Nagai V (1987) Soybean resistance to insects: VII. Evaluation of stink bug damage to cultivars and lines. Bragantia 46:45–57 (in Portuguese)

    Google Scholar 

  • Lu Z, Dong S, Li C, Li L, Yu Y, Men X, Yin S (2020) Sublethal and transgenerational effects of dinotefuran on biological parameters and behavioural traits of the mirid bug Apolygus lucorum. Sci Rep 10:226;1–8

    Google Scholar 

  • Lucini T, Panizzi AR (2016) Waveform characterization of the soybean stem feeder Edessa meditabunda (F.) (Hemiptera: Heteroptera: Pentatomidae): overcoming the challenge of wiring pentatomids for EPG. Entomol Exp Appl 158:118–132

    Article  CAS  Google Scholar 

  • Lucini T, Panizzi AR (2017a) Feeding behavior of the stink bug Dichelops melacanthus Dallas on corn seedlings: an EPG analysis at multiple input impedances and histology correlation. Ann Entomol Soc Am 110:160–171

    Google Scholar 

  • Lucini T, Panizzi AR (2017b) Probing behavior of Dichelops furcatus (F.) (Heteroptera: Pentatomidae) on wheat plants characterized by electropenetrography (EPG) and histological studies. J Insect Sci 17:65;1–15

    Google Scholar 

  • Lucini T, Panizzi AR (2018) Electropenetrography monitoring of the neotropical brown-stink bug (Hemiptera: Pentatomidae) on soybean pods: an electrical penetration graph-histology analysis. J Insect Sci 18:5;1–14

    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

    Article  Google Scholar 

  • Lucini T, Panizzi AR, Dios RVP (2020) Tachinid fly parasitism and phenology of the Neotropical red-shouldered stink bug, Thyanta perditor (F.) (Heteroptera: Pentatomidae), on the wild host plant, Bidens pilosa L. (Asteraceae). Neotrop Entomol 49:98–107

    Article  CAS  PubMed  Google Scholar 

  • Luedders VD, Dickerson WA (1977) Resistance of selected soybean genotypes and segregating populations to cabbage looper feeding. Crop Sci 17:395–397

    Article  Google Scholar 

  • Marques LH, Santos AC, Castro BA, Moscardini VF, Rossetto J, Silva OAN, Zobiole LHS, Valverde-Garcia P, Babcock JM, Storer NP, Rule DM, Fernandes AO (2017) Field evaluation of soybean transgenic event DAS-81419-2 expressing Cry1F and Cry1Ac proteins for the control of secondary lepidopteran pests in Brazil. Crop Prot 96:109–115

    Article  CAS  Google Scholar 

  • Martin PA, Hirose E, Aldrich JR (2007) Toxicity of Chromobacterium subtsugae to southern green stink bug (Heteroptera: Pentatomidae) and corn rootworm (Coleoptera: Chrysomelidae). J Econ Entomol 100:680–684

    Article  PubMed  Google Scholar 

  • Maxwell FG, Jennings PR (1980) Breeding plants resistant to insects. Wiley, New York

    Google Scholar 

  • McPherson JE, McPherson RM (2000) Stink bugs of economic importance in America north of Mexico. CRC Press, Boca Raton

    Book  Google Scholar 

  • McPherson RM, Buss GR, Roberts PM (2007) Assessing stink bug resistance in soybean breeding lines containing genes from germplasm IAC-100. J Econ Entomol 100:1456–1463

    Article  PubMed  Google Scholar 

  • Miao J, Han BY, Zhang QH (2014) Probing behavior of Empoasca vitis (Homoptera: Cicadellidae) on resistant and susceptible cultivars of tea plants. J Insect Sci 14:223;1–6

    Google Scholar 

  • Mitchell PL, Cooke SB, Smaniotto LF (2018) Probing behavior of Nezara viridula on soybean: characterization and comparison of electrical penetration graph (EPG) waveforms on vegetative and reproductive plant structures. J Agric Urban Entomol 34:19–43

    Article  Google Scholar 

  • Mogilicherla K, Howell JL, Palli SR (2018) Improving RNAi in the brown marmorated stink bug: identification of target genes and reference genes for RT-qPCR. Sci Rep 8:3720;1–9

    Google Scholar 

  • Moscardi F (1999) Assessment of the application of baculoviruses for control of Lepidoptera. Annu Rev Entomol 44:257–289

    Article  CAS  PubMed  Google Scholar 

  • Mustafa T, Alvarez JM, Munyaneza JE (2015) Effect of cyantraniliprole on probing behavior of the potato psyllid (Hemiptera: Triozidae) as measured by the electrical penetration graph technique. J Econ Entomol 108:2529–2535

    Article  CAS  PubMed  Google Scholar 

  • Niva CC, Panizzi AR (1996) Effects of sodium chloride on the behavior of Nezara viridula L. (Heteroptera: Pentatomidae) on soybean pod. An Soc Entomol Brasil 25:252–257 (in Portuguese)

    Google Scholar 

  • Núñez-Farfan J, Fornoni J, Valverde PL (2007) The evolution of resistance and tolerance to herbivores. Annu Rev Ecol Evol Syst 38:541–566

    Article  Google Scholar 

  • O’Brien RD (1966) Mode of action of insecticides. Annu Rev Entomol 11:369–402

    Article  PubMed  Google Scholar 

  • Orians CM, Ward D (2010) Evolution of plant defenses in nonindigenous environments. Annu Rev Entomol 55:439–459

    Article  CAS  PubMed  Google Scholar 

  • Painter RH (1951) Insect resistance in crop plants. McMillan, New York

    Book  Google Scholar 

  • Panda N (1979) Principles of host-plant resistance to insect pests. Hindustan Publication, New Delhi

    Google Scholar 

  • Panizzi AR, da Silva JJ (2010) New records of pentatomids as hosts of Hexacladia smithii Ashmead (Hymenoptera: Encyrtidae) in Southern Brazil. Neotrop Entomol 39:678–679

    Article  PubMed  Google Scholar 

  • Panizzi AR, Slansky F Jr (1985) Review of phytophagous pentatomids associated with soybean in the Americas. Fla Entomol 68:184–214

    Article  Google Scholar 

  • Panizzi AR, McPherson JE, James DG, Javahery M, McPherson RM (2000) Economic importance of stink bugs (Pentatomidae). In: Schaefer CW, Panizzi AR (eds) Heteroptera of economic importance. CRC Press, Boca Raton, pp 421–474

    Google Scholar 

  • Parys KA, Portilla M (2020) Effectiveness of Beauveria bassiana against Piezodorus guildinii (Hemiptera: Pentatomidae), a key pest of soybeans in the neotropics. Biocontrol Sci Tech 30:451–461

    Article  Google Scholar 

  • Pinheiro DH, Moreira RO, Leite NA, Redoan AN, Xavier AS, Barros BA, Carneiro NP (2020) Suitable reference genes for RT-qPCR analysis in Dichelops melacanthus (Hemiptera: Pentatomidae). Mol Biol Rep 47:4989–5000

    Article  CAS  PubMed  Google Scholar 

  • Prado SS, Zucchi TD (2012) Host-symbiont interactions for potentially managing heteropteran pests. Psyche 2012:269473;1–9

    Google Scholar 

  • Price DR, Gatehouse JA (2008) RNAi-mediated crop protection against insects. Trends Biotechnol 26:393–400

    Article  CAS  PubMed  Google Scholar 

  • Qaim M, Zilberman D (2003) Yield effects of genetically modified crops in developing countries. Science 299:900–902

    Article  CAS  PubMed  Google Scholar 

  • Rangasamy M, McAuslane HJ, Backus EA, Cherry AH (2015) Differential probing behavior of Blissus insularis (Hemiptera: Blissidae) on resistant and susceptible St. Augustinegrasses. J Econ Entomol 108:780–788

    Google Scholar 

  • Resquín-Romero G, Cabral-Antúnez C, Sarubbi-Orue H, Garrido-Jurado I, Valverde-García P, Schade M, Butt TM (2020) Virulence of Metarhizium brunneum (Ascomycota: Hypocreales) strains against stinkbugs Euschistus heros and Dichelops furcatus (Hemiptera: Pentatomidae). J Econ Entomol 113:2540–2545

    Google Scholar 

  • Ribeiro A, Castiglioni E (2009) Fluctuaciones de poblacionales de Piezodorus guildinii (Westwood) (Hemiptera: Pentatomidae) en soja y alfafa em Paysandú, Uruguay. Agrociencia Uruguaya 23:32–36

    Google Scholar 

  • Riga M, Denecke S, Livadaras I, Geibel S, Nauen R, Vontas J (2020) Development of efficient RNAi in Nezara viridula for use in insecticide target discovery. Arch Insect Biochem Physiol 103:e21650;1–9

    Google Scholar 

  • Rivera KL, Mitchell PL (2020) Feeding behavior of Nezara viridula first instars: EPG analysis and effect of food availability on subsequent development. J Agric Urban Entomol 36:47–63

    Google Scholar 

  • Roan CC, Hopkins TL (1961) Mode of action of insecticides. Annu Rev Entomol 6:333–346

    Article  CAS  PubMed  Google Scholar 

  • Rossetto CJ, Gallo PB, Razera LF, Bortoletto N, Igue T, Medina PF, Tisseli Filho O, Aquilera V, Veiga RFA, Pinheiro JB (1995) Mechanisms of resistance to stink bug complex in the soybean cultivar IAC-100. An Soc Entomol Brasil 24:517–522

    Google Scholar 

  • Sadasivam S, Thayumanavan B (2003) Molecular host plant resistance to pests. Marcel Dekker, New York

    Book  Google Scholar 

  • Sánchez JA, Lacasa A (2008) Impact of the zoophytophagous plant bug Nesidiocoris tenuis (Heteroptera: Miridae) on tomato yield. J Econ Entomol 101:1864–1870

    Article  PubMed  Google Scholar 

  • Schaefer CW, Panizzi AR (2000) Heteroptera of economic importance. CRC Press, Boca Raton

    Book  Google Scholar 

  • Seiter NJ, Grabke A, Greene JK, Kerrigan JL, Reay-Jones FPF (2014) Beauveria bassiana is a pathogen of Megacopta cribraria (Hemiptera: Plataspidae) in South Carolina. J Entomol Sci 49:326–330

    Google Scholar 

  • Serikawa RH, Backus EA, Rogers ME (2012) Effects of soil-applied imidacloprid on Asian citrus psyllid (Hemiptera: Psyllidae) feeding behavior. J Econ Entomol 105:1492–1502

    Article  CAS  PubMed  Google Scholar 

  • Serteyn L, Ponnet L, Backus EA, Francis F (2020a) Characterization of electropenetrography waveforms for the invasive heteropteran pest, Halyomorpha halys, on Vicia faba leaves. Arthropod Plant Interact 14:113–126

    Article  Google Scholar 

  • Serteyn L, Ponnet L, Saive M, Fauconnier M-L, Francis F (2020b) Changes of feeding behavior and salivary proteome of brown marmorated stink bug when exposed to insect-induced plant defenses. Arthropod Plant Interact 14:101–112

    Article  Google Scholar 

  • Sharma R, Christiaens O, Taning CNT, Smagghe G (2021) RNAi-mediated mortality in Southern green stinkbug Nezara viridula by oral delivery of dsRNA. Pest Manage Sci 77:77–84

    Google Scholar 

  • Silva JPGF, Baldin ELL, Souza ES, Canassa VF, Lourenção AL (2013) Characterization of antibiosis to the redbanded stink bug Piezodorus guildinii (Hemiptera: Pentatomidae) in soybean entries. J Pest Sci 86:649–657

    Article  Google Scholar 

  • Silva JPGF, Baldin ELL, Canassa VF, Souza ES, Lourenção AL (2014) Assessing antixenosis of soybean entries against Piezodorus guildinii (Hemiptera: Pentatomidae). Arthrop Plant Interact 8:349–359

    Google Scholar 

  • Smaniotto LF, Panizzi AR (2015) Interactions of selected species of stink bugs (Hemiptera: Heteroptera: Pentatomidae) from leguminous crops with plants in the neotropics. Fla Entomol 98:7–17

    Article  Google Scholar 

  • Smith CM (1989) Plant resistance to insects. A fundamental approach. Wiley, New York

    Google Scholar 

  • Smith CM, Clement SL (2012) Molecular bases of plant resistance to arthropods. Annu Rev Entomol 57:309–328

    Article  CAS  PubMed  Google Scholar 

  • Smith CM, Khan ZR, Pathak MD (1994) Techniques for evaluating insect resistance in crop plants. CRC Press, Boca Raton

    Google Scholar 

  • Snelling RO (1941) Resistance of plants to insect attack. Bot Rev 7:543–586

    Article  Google Scholar 

  • Spiller NJ, Koenders L, Tjallingii WF (1990) Xylem ingestion by aphids – a strategy for maintaining water balance. Entomol Exp Appl 55:101–104

    Google Scholar 

  • Stout MJ (2013) Reevaluating the conceptual framework for applied research on host-plant resistance. Insect Sci 20:263–272

    Article  PubMed  Google Scholar 

  • Stubbins FL, Agudelo P, Reay-Jones FPF, Greene JK (2015) First report of a mermithid nematode infecting the invasive Megacopta cribraria (Hemiptera: Plataspidae) in the United States. J Invertebr Pathol 127:35–37

    Google Scholar 

  • Stubbins FL, Agudelo P, Reay-Jones FPF, Greene JK (2016) Agamermis (Nematoda: Mermithidae) infection in South Carolina agricultural pests. J Nematol 48:290–296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stubbins FL, Mitchell PL, Turnbull MW, Reay-Jones FPF, Greene JK (2017) Mouthpart morphology and feeding behavior of the invasive kudzu bug, Megacopta cribraria (Hemiptera: Plataspidae). Invertebr Biol 136:309–320

    Article  Google Scholar 

  • Sun YP (1968) Dynamics of insect toxicology-a mathematical and graphical evaluation of the relationship between insect toxicity and rates of penetration and detoxication of insecticides. J Econ Entomol 61:949–955

    Article  CAS  PubMed  Google Scholar 

  • Sun M, Voorrips RE, Steenhuis-Broers G, van’t Westende W, Vosman B (2018a) Reduced phloem uptake of Myzus persicae on an aphid resistant pepper accession. BMC Plant Biol 18:138;1–14

    Google Scholar 

  • Sun Z, Yan F, Wang MQ (2018b) Transgenic expression of Bt in rice does not affect feeding behavior and population density of the brown planthopper, Nilaparvata lugens Stål (Hemiptera: Delphacidae). Entomol Gen 37:35–45

    Article  Google Scholar 

  • Taiz L, Zeiger E (2004) Plant physiology, 3rd edn. Sinauer Associates Inc., Sunderland

    Google Scholar 

  • Tanada Y (1959) Microbiol control of insects. Annu Rev Entomol 4:277–302

    Article  CAS  Google Scholar 

  • Tariq K, Noor M, Backus EA, Hussain A, Ali A, Peng W, Zhang H (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

    Article  CAS  PubMed  Google Scholar 

  • Todd JC, Rouf Mian MA, Backus EA, Finer JJ, Redinbaugh MG (2016) Feeding behavior of soybean aphid (Hemiptera: Aphididae) biotype 2 on resistant and susceptible soybean. J Econ Entomol 109:426–433

    Article  CAS  PubMed  Google Scholar 

  • Tozlu E, Saruhan I, Tozlu G, Kotan R, Dadaşoğlu F, Tekiner N (2019) Potentials of some entomopathogens against the brown marmorated stink bug, Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae). Egypt J Biol Pest Control 29:76;1–8

    Google Scholar 

  • Tuelher ES, Backus EA, Cervantes F, Oliveira EE (2020) Quantifying Lygus lineolaris stylet probing behavior and associated damage to cotton leaf terminals. J Pest Sci 93:663–677

    Article  Google Scholar 

  • Walker WB, Allen ML (2010) Expression and RNA interference of salivary polygalacturonase genes in the tarnished plant bug, Lygus lineolaris. J Insect Sci 10:173;1–13

    Google Scholar 

  • Walker WB, Allen ML (2011) RNA interference-mediated knockdown of IAP in Lygus lineolaris induces mortality in adult and pre-adult life stages. Entomol Exp Appl 138:83–92

    Article  CAS  Google Scholar 

  • Wang YN, Kel KO, Li YH, Han LZ, Liu YM, Hua HX, Peng YF (2016) Comparison of three transgenic Bt rice lines for insecticidal protein expression and resistance against a target pest, Chilo suppressalis (Lepidoptera: Crambidae). Insect Sci 23:78–87

    Article  CAS  PubMed  Google Scholar 

  • Waqas MS, Qian L, Shoaib AAZ, Cheng X, Zhang Q, Elabasy ASS, Shi Z (2019) Lethal and sublethal effects of neonicotinoid insecticides on the adults of Phenacoccus solenopsis (Hemiptera: Pseudococcidae) on tomato plants. J Econ Entomol 112:1314–1321

    Article  CAS  PubMed  Google Scholar 

  • Williamson C, von Wechmar MB (1995) The effect of two viruses on the metamorphosis, fecundity, and longevity of the green stinkbug, Nezara viridula. J Invert Pathol 65:174–178

    Article  Google Scholar 

  • Wilson RC, Doudna JA (2013) Molecular mechanisms of RNA interference. Annu Rev Biophys 42:217–239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue K, Wang XY, Huang CH, Wang RJ, Liu B, Yan FM, Xu CR (2009) Stylet penetration behaviors of the cotton aphid Aphis gossypii on transgenic Bt cotton. Insect Sci 16:137–146

    Article  Google Scholar 

  • Yencho GC, Cohen MB, Byrne PF (2000) Applications of tagging and mapping insect resistance loci in plants. Annu Rev Entomol 45:393–422

    Article  CAS  PubMed  Google Scholar 

  • Yin HD, Wang XY, Xue K, Huang CH, Wang RJ, Yan FM, Xu CR (2010) Impacts of transgenic Bt cotton on the stylet penetration behaviors of Bemisia tabaci biotype B: evidence from laboratory experiments. Insect Sci 17:344–352

    Google Scholar 

  • Zavala JA, Mazza CA, Dillon FM, Chludil HD, Ballaré CL (2015) Soybean resistance to stink bugs (Nezara viridula and Piezodorus guildinii) increases with exposure to solar UV-B radiation and correlates with isoflavonoid content in pods under field conditions. Plant Cell Environ 38:920–928

    Article  CAS  PubMed  Google Scholar 

  • Zhu KY, Palli SR (2020) Mechanisms, applications, and challenges of insect RNA interference. Annu Rev Entomol 65:293–311

    Article  CAS  PubMed  Google Scholar 

  • Zlotkin E (1999) The insect voltage-gated sodium channel as target of insecticides. Annu Rev Entomol 44:429–455

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Embrapa Trigo, Passo Fundo, Rio Grande do Sul, Brazil

    Antônio Ricardo Panizzi & Tiago Lucini

  2. Department of Biology, Winthrop University, Rock Hill, SC, USA

    Paula Levin Mitchell

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  1. Antônio Ricardo Panizzi
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  2. Tiago Lucini
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Panizzi, A.R., Lucini, T., Mitchell, P.L. (2021). Role of EPG in Developing and Assessing Control Methods for Heteropteran Crop Pests. In: Electronic Monitoring of Feeding Behavior of Phytophagous True Bugs (Heteroptera). Entomology in Focus, vol 6. Springer, Cham. https://doi.org/10.1007/978-3-030-64674-5_7

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