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Heterorhabditis amazonensis to Control Euschistus heros (Hemiptera: Pentatomidae) in Laboratory and Field Conditions

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Abstract

This study evaluated the potential of entomopathogenic nematodes (EPNs) to control Euschistus heros (Fabricius) under laboratory and field conditions. Eight isolates of the species Heterorhabditis amazonensis were evaluated on field-collected and laboratory-reared insect populations. The isolates that performed best in the virulence test were evaluated for in vivo production on Galleria mellonella Fabricius larvae. Then, these were evaluated in field conditions on E. heros from the laboratory and field populations. The isolates IBCB-n46, NEPET11, and IBCB-n40 caused the highest mortality in adult E. heros from laboratory rearing (100, 94, and 80%, respectively), and IBCB-n46 and NEPET11 were the best against the field population (71 and 47% mortality, respectively). In the assay to evaluate production, the isolate IBCB-n46 achieved the best result (3.4 × 105 IJs/g per larvae), followed by isolates UEPN05 (1.4 × 105 IJs/g per larvae) finally NEPET11 (7.5 × 104 IJs/g per larvae). In the assay in field conditions, all treatments differed from the control treatment, no significant differences were observed in the evaluated factors (isolates and insect populations), and the highest percentage of mortality was obtained by the UEPN05 isolate when applied to insects from the laboratory (18.57% mortality).

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References

  • Almenara DP, Rossi C, Neves MRC, Winter E (2012) Nematoides entomopatogênicos. In: Tópicos Avançados em Entomologia Molecular. São Paulo: Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular pp 01–40

  • Alves SB, Lopes RB (2008) Controle Microbiano de pragas na América Latina FEALQ Piracicaba, pp 171–202

  • Alves VS, Moino AJ, Santa-Cecilia LVC, Rohde C, Tramontin MAS (2009) Testes em condições para o controle de Dysmicoccus texensis (Tinsley) (Hemiptera, Pseudococcidae) em cafeeiro com nematoides entomopatogênicos do gênero Heterorhabditis (Rhabditida, Heterorhabditidae). Rev Bras Entomol 53:139–143. https://doi.org/10.1590/S0085-56262009000100029

    Article  Google Scholar 

  • Andaló V, Moreira GF, JrA M (2009) Studies of two new populations of Heterorhabditis amazonensis (Rhabditida: Heterorhabditidae). Nematropica 39:199–211

    Google Scholar 

  • Boff M, Wiegers GL, Gerritsen LJM, Smits PH (2000) Development of the entomopathogenic nematode Heterorhabditis megidis strain NLH-E 87.3 in Galleria mellonella. Nematol 2:303–308. https://doi.org/10.1163/156854100509178

    Article  Google Scholar 

  • Bueno AF, Batistela MJ, Bueno RCOF, França-NeTO JB, Nishikawa MAN, Filho AL (2011) Effects of integrated pest management, biological control and prophylactic use of insecticides on the management and sustainability of soybean. Crop Prot 30:937–945. https://doi.org/10.1016/j.cropro.2011.02.021

    Article  Google Scholar 

  • Burjanadze M, Gorgadze O, De Luca F, Troccoli A, Lortkipanidze M, Kharabadze N, Arjevanidze M, Fanelli E, Tarasco E (2020) Potential of native entomopathogenic nematodes for the control of brown marmorated stink bug Halyomorpha halys in Georgia. Bioc Sci Technol 30:1–13. https://doi.org/10.1080/09583157.2020.1776217

    Article  Google Scholar 

  • Caldas C, Cherqui A, Pereira A, Simões N (2002) Purification and characterization of an extracellular protease from Xenorhabdus nematophila involved in insect immunosuppression. Appl Env Microbiol 68:1297–1304. https://doi.org/10.1128/aem.68.3.1297-1304.2002

    Article  CAS  Google Scholar 

  • Corrêa-Ferreira BS, Panizzi AR (1999) Percevejo da soja e seu manejo. Londrina: Embrapa soja, Embrapa Soja. Circular técnica n. 24.

  • Corrêa-Ferreira BS, Sosa-Gómez DR (2017) Percevejos e o sistema de produção soja-milho. Londrina: Embrapa Soja, Circular Técnica 397.

  • Dell’Acqua R, Tomazini MDO, Harakava R, Oliveira CMG, Rosa JMO, Leite LG (2013) Molecular caracterization of entomopathogenic nematodes (Rhabditida: Steinernematidae e Heterorhabditidae) from Mato Grosso do Sul and São Paulo states, Brazil. Nematol Bras 37:66–74

    Google Scholar 

  • Doneze GS (2019) Caracterização molecular de nematoides entomopatogênicos (isolados UEPN 02, 05 e 06) nativos da região norte do Paraná. Universidade Estadual do Norte do Paraná, Trabalho de Conclusão de Curso

    Google Scholar 

  • Dowds BC, Peters A (2002) Virulence mechanisms. In: Gaugler, R. Entomopathogenic Nematology. London: CABI Publishing.

  • Ferreira DF (2019) Sisvar: a computer analysis system to fixed effects split plot type designs. Rev Bras Biom 37:529–535. https://doi.org/10.28951/rbb.v37i4.450

  • Golin V (2014) Incidência natural, biologia, seletividade e efeito de liberações inoculavas de parasitoides de ovos (Hymenoptera: Platygastridae) no controle de Euschistus heros (Fabricius) (Hemiptera: Pentatomidae) no Mato Groso. Universidade Federal do Paraná, Tese

    Google Scholar 

  • Guide BA (2019) Identificação e aspectos biológicos do nematoide entomopatogênico Heterorhabditis amazonensis isolado UEL 08. Universidade Estadual de Londrina, Tese

    Google Scholar 

  • Guide BA, Alves VS, Fernandes TAP, Marcomini MC, Meneghin AM, Neves PMOJ (2019) Pathogenicity and virulence of entomopathogenic nematodes against Dichelops melacanthus Dallas (Hemiptera: Pentatomidae). Sem Ciênc Agrár 40:1417–1426. https://doi.org/10.5433/1679-0359.2019v40n4p1417

    Article  Google Scholar 

  • Hoffmann-Campo CB, Moscardi F, Corrêa-Ferreira BS, Oliveira LJ, Sosa-Gómez DR, Panizzi AR, Corso I, Gazzoni DL, Oliveira EB de (2000) Pragas da soja no Brasil e seu manejo integrado. Londrina: Embrapa-CNPSo. 70 p. (Embrapa Soja. Circular Técnica, 30).

  • Instituto Agronômico Do Paraná – IAPAR (2020) Agrometeorologia: Dados diários de Londrina. Available from: <http://www.iapar.br/modules/conteudo/conteudo.php?conteudo=2603> Accessed: Oct 18, 2020.

  • Kaya HK (1990) Soil ecology. In: Gaugler R, Kaya HK (eds) Entomopathogenic Nematodes in biological control. CRC Press, Boca Raton, FL, pp 93–116

    Google Scholar 

  • Koppenhöfer AM, Kaya HK, Taormino SP (1995) Infectivity of entomopathogenic nematodes (Rhabditida: Steinernematidae) at diferente soil depths and moistures. J Invertebr Pathol 65:193–199. https://doi.org/10.1006/jipa.1995.1028

    Article  Google Scholar 

  • Leite LG, Machado LA, Aguillera MM, Rodrigues RCD, Negrisoli Junior AS (2005) Screening of entomopathogenic nematodes (Nemata: Rhabditida) and the efficiency of Heterorhabditis sp. against the Sugarcane Root Spittlebug Mahanarva fimbriolata (Fabr.) (Hemiptera: Cercopidae). Neotrop Entomol 34:785–790. https://doi.org/10.1590/s1519-566x2005000500010

    Article  Google Scholar 

  • Leite GL, Tavares FM, Botelho OSM, Filho AB, Polanezyk RA, Schmidt FS (2012) Eficiência de nematoides entomopatogênicos e inseticidas químicos contra Sphenophorus levis e Leucothyreus sp. em cana-de-açúcar. Pesq Agropec Trop 42:40–48. https://doi.org/10.1590/S1983-40632012000100006

    Article  Google Scholar 

  • Lewis ED, Campbell J, Griffin C, Kaya H, Peters A (2006) Behavioral ecology of entomopathogenic nematodes. Biol Control 38:66–79. https://doi.org/10.1016/j.biocontrol.2005.11.007

    Article  Google Scholar 

  • Maizels RM, Blaxter ML, Scott AL (2001) Immunological genomics of Brugia malayi filarial genes implicated in immune evasion and protective immunity. Parasite Immunol 23:327–344. https://doi.org/10.1046/j.1365-3024.2001.00397

    Article  CAS  PubMed  Google Scholar 

  • Mikaia N (2018) EPNs Steinernema carpocapsae and Heterorhabditis bacteriophora for control of the Brown Marmorated Stink Bug (BMSB) Halyomorpha halys (Hemiptera, Pentatomidae). Bull Georgian Natl Acad Scienc 12:89–94

    Google Scholar 

  • Molina JPA, López NJC (2001) Producción in vivo de três entomonematodos con dos sistemas de infección en dos hospedantes. Rev Colomb Entomolog 27:73–78

    Google Scholar 

  • Mourão APM, Panizzi AR (2000) Diapausa e diferentes formas sazonais em Euschistus heros (Fabr.) (Hemiptera: Pentatomidae) no Norte do Paraná. An Soc Entomol Bras 29:205–218. https://doi.org/10.1590/S0301-80592000000200002

    Article  Google Scholar 

  • Nanzer SLL, Recchia GH, Chacon-Orozco JG, Silva RSA, Cardoso JFM, Leite LG (2021) Assessment of entomopathogenic nematodes and their symbiotic bacteria to control the stink bugs Euschistus heros and Dichelops melacanthus (Heteroptera: Pentatomidae) in the soybean-corn succession system. Turk J Zoolog 45:356–371. https://doi.org/10.3906/zoo-2104-53

    Article  CAS  Google Scholar 

  • Ozer N, Unlu IO (2003) Evaluation of the reproductive potential and competition between two entomopathogenic nematodes, Steinernema feltiae Filipjev, 1934 (Rhabditida: Steinernematidae) and Heterorhabditis bacteriophora, Poinar 1976 (Rhabditida: Heterorhabditidae). Turk J Biol 27:149–155

    Google Scholar 

  • Panizzi AR, Bueno AF, Silva FAC (2012) Soja: manejo integrado de insetos e outros artrópodes-praga (1° ed.) Embrapa. Londrina.

  • Panizzi AR, Niva CC (1994) Overwintering strategy of the bown stink bug in northern Paraná. Pesqui Agropecu Bras 29:509–511

    Google Scholar 

  • Panizzi AR, Slansky JRF (1985) Review of phytophagous pentatomids (Hemiptera: Pentatomidae) associated with soybean in Americas. Fla Entomol 68:184–214. https://doi.org/10.2307/3494344

    Article  Google Scholar 

  • Pushnya M, Rodionova H, Snesareva E (2020) Development of the elements of the biological system for protecting crops against the southern green stink bug Nezara viridula L. Bio Web Conf 21:00037. https://doi.org/10.1051/bioconf/20202100037

    Article  Google Scholar 

  • Ribeiro PA (2018) Caracterização molecular de isolados de nematoides entomopatogênicos. Universidade Federal de Uberlândia, Trabalho de Conclusão de Curso

    Google Scholar 

  • Selvan S, Campbell JF, Gaugler R (1993) Density-dependent effects on entomopathogenic nematodes (Heterorhabditidae and Steinernematidae) within an insect host. J Invertebr Pathol 62:278–274. https://doi.org/10.1006/jipa.1993.1113

    Article  Google Scholar 

  • Simões N, Rosa JS (1996) Pathogenicity and host specificity of entomopathogenic nematodes. Bioc Sci Technol 6:403–412. https://doi.org/10.1080/09583159631370

    Article  Google Scholar 

  • Shapiro-Ilan DI, Gaugler R, Tedders WL, Brown I, Lewis EE (2002) Optimization of inoculation for in vivo production of entomopathogenic nematodes. J Nematol 34:343–350

    PubMed  PubMed Central  Google Scholar 

  • Shapiro-Ilan DI, Han R, Dolinksi C (2012) Entomopathogenic nematode production and application technology. J Nematol 44:206–217

    PubMed  PubMed Central  Google Scholar 

  • Shin BS, Choi RN, Lee CU (2001) Effects of cadmium on total lipid content and fatty acids of the greater wax moth, Galleria mellonella. Korean J Ecol Environ 24:349–352

    Google Scholar 

  • Sosa-Gómez DR, Corrêa-Ferreira BS, Kraemer B, Pasini A, Husch PE, Vieira CED, Marinez CBR, Lopez ION (2020) Prevalence, dameje, management and inseticide resistence of stink bug populations (Hemiptera: Pentatomidade) in commoditie croups. Agric Forest Entomol 22:99–118. https://doi.org/10.1111/afe.12366

    Article  Google Scholar 

  • Silva-Santa MF, Alves LFA, Ferreira TT, Bonini AK (2021) Selection and characterization of Beauveria bassiana fungus and their potencial to control the brown stink bug. Bioc Sc Technol p.1–13. https://doi.org/10.1080/09583157.2021.1970716

  • Vivan LM, Degrande PE (2011) Pragas da soja. Fundação MT, Bol Pesqui Soja 11:239–297

    Google Scholar 

  • Voss M, Andaló V, Negrisoli ASJ, Barbosa-Negrisoli CR (2009) Manual de técnicas laboratoriais para obtenção, manutenção e caracterização de nematoides entomopatogênicos. Passo Fundo: Embrapa Trigo

  • White GF (1927) A method for obtaining infective nematodes larvae from cultures. Sci 66:302–303

    Article  CAS  Google Scholar 

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Acknowledgements

We would like to thank EMBRAPA for providing the insects and a place to conduct the study.

Funding

This study was financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001, Fundação Araucária and Universidade Estadual do Norte do Paraná – UENP/PROPG/EDITORA UENP..

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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Douglas Martins Cecconello, Samuel Roggia, Gabriela Souza Doneze, Mariana Ferracin de Macedo e Viviane Sandra Alves. The first draft of the manuscript was written by Douglas Martins Cecconello and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Viviane Sandra Alves.

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Cecconello, D.M., Roggia, S., Doneze, G.S. et al. Heterorhabditis amazonensis to Control Euschistus heros (Hemiptera: Pentatomidae) in Laboratory and Field Conditions. Neotrop Entomol 51, 292–298 (2022). https://doi.org/10.1007/s13744-021-00936-5

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