Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-26T05:00:59.479Z Has data issue: false hasContentIssue false
  • English
  • Français

Reproduction of Ooencyrtus submetallicus (Hymenoptera: Encyrtidae) in egg densities of Euschistus heros (Hemiptera: Pentatomidae)

Published online by Cambridge University Press:  17 November 2021

Willian Yoshio Sanomia Open the ORCID record for Willian Yoshio Sanomia [Opens in a new window] ,
Fabricio Fagundes Pereira Open the ORCID record for Fabricio Fagundes Pereira [Opens in a new window] ,
Ivana Fernandes da Silva ,
Carlos Reinier Garcia Cardoso  and
Jéssica Terilli Lucchetta
Willian Yoshio Sanomia*
Affiliation:
Faculdade de Ciências Agrárias, Universidade Federal da Grande Dourados, Rodovia Dourados/Itahum, Km 12, 79.804-970, Dourados, Mato Grosso do Sul, Brazil
Fabricio Fagundes Pereira
Affiliation:
Faculdade de Ciências Biológicas e Ambientais, Universidade Federal da Grande Dourados, Rodovia Dourados/Itahum, Km 12, 79.804-970, Dourados, Mato Grosso do Sul, Brazil
Ivana Fernandes da Silva
Affiliation:
Faculdade de Ciências Biológicas e Ambientais, Universidade Federal da Grande Dourados, Rodovia Dourados/Itahum, Km 12, 79.804-970, Dourados, Mato Grosso do Sul, Brazil
Carlos Reinier Garcia Cardoso
Affiliation:
Faculdade de Ciências Biológicas e Ambientais, Universidade Federal da Grande Dourados, Rodovia Dourados/Itahum, Km 12, 79.804-970, Dourados, Mato Grosso do Sul, Brazil
Jéssica Terilli Lucchetta
Affiliation:
Faculdade de Ciências Biológicas e Ambientais, Universidade Federal da Grande Dourados, Rodovia Dourados/Itahum, Km 12, 79.804-970, Dourados, Mato Grosso do Sul, Brazil
*
*Corresponding author. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Knowledge about the ideal host ratio per female parasitoid reared in glass tubes is important for obtaining descendants with better biological quality. The study aimed to evaluate the reproduction of Ooencyrtus submetallicus (Hymenoptera: Encyrtidae) females in egg densities of Euschistus heros (Hemiptera: Pentatomidae) to find the most adequate relationship between parasitoids and hosts aiming at the parasitoid multiplication. The experiment was conducted with E. heros eggs at densities (parasitoid:host) of 1:3, 1:6, 1:9, 1:12, 1:15, or 1:18 with 24 hours of parasitism by O. submetallicus. The parasitoid females and the egg carton were placed in glass tubes and kept in a climate-controlled chamber. The percentage of parasitism was affected by the nonparasitised eggs. The emergence of adult parasitoids, number of parasitised eggs, number of individual parasitoids emerging per egg, the length of the parasitoids’ posterior tibiae, and the parasitoids’ longevity, life cycle, and sex ratio were not affected by the different densities of nonparasitised eggs subjected to treatments. Ooencyrtus submetallicus parasitised and developed in E. heros eggs in all evaluated densities, with 1:6 presenting the best combination of parasitoid and host.

Type
Research Paper
Information
The Canadian Entomologist , Volume 154 , Issue 1 , 2022 , e4
Check for updates
Copyright
© The Author(s), 2021. Published by Cambridge University Press on behalf of the Entomological Society of Canada

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Subject editor: Rayda Krell

References

Bai, B., Luck, R.F., Foster, L., Stephens, B., and Janssen, J.A.M. 1992. The effect of host size on quality attributes of the egg parasitoid, Trichogramma pretiosum . Entomologia Experimentalis et Applicata, 64: 37–48.CrossRefGoogle Scholar
Battisti, A., Ianne, P., Milani, N., and Zanata, M. 1990. Preliminary accounts on the rearing of Ooencyrtus pityocampae (Mercet) (Hym., Encyrtidae). Journal of Applied Entomology, 110: 121–127.CrossRefGoogle Scholar
Bueno, A.F., Sosa-Gómez, D., Corrêa-Ferreira, B., Moscardi, F., and Bueno, R. 2012. Inimigos naturais das pragas da soja. In Soja: manejo integrado de insetos e outros artrópodes-praga. Edited by C.B. Hoffman-Campo, B.S. Corrêa-Ferreira, and F. Moscardi. Embrapa Soja, Brazilian Agricultural Research Corporation, Brasil. Pp. 493–629.Google Scholar
Bueno, R.C.O.F., Parra, J.R.P., Bueno, A.F., and Haddad, M.L. 2009. Desempenho de Tricogramatídeos como potenciais agentes de controle de Pseudoplusia includens (Walker) (Lepidoptera: Noctuidae). Neotropical Entomology, 38: 389–394.CrossRefGoogle Scholar
Cobert, S.A. 1985. Insect chemosensory responses: a chemical legacy hypothesis. Ecological Entomology, 10: 143–153.Google Scholar
Corrêa-Ferreira, B.S. and Moscardi, F. 1995. Seasonal occurrence and host spectrum of egg parasitoids associated with soybean stink bugs. Biological Control, 5: 196–202.CrossRefGoogle Scholar
Cusmano, A., Duvic, B., Jouan, V., Ravallec, M., Legeai, F., Peri, E., et al. 2018. First extensive characterization of the venom gland from an egg parasitoid: structure, transcriptome and functional role. Journal of Insect Physiology, 107: 68–80.CrossRefGoogle Scholar
Depieri, R.A. and Panizzi, A.R. 2011. Duration of feeding and superficial and in depth damage to soybean seed by selected species of stink bugs (Heteroptera: Pentatomidae). Neotropical Entomology, 40: 197–203.CrossRefGoogle Scholar
Eduardo, W.I., Toscano, L.C., Tomquelski, G.V., Maruyama, W.I., and Morando, R. 2018. Action thresholds for the soybean stink bug complex: phytotechnical and physiological parameters and egg parasitism. Revista Colombiana de Entomología, 44: 165–171.CrossRefGoogle Scholar
Espinosa, M.S., Virla, E.G., and Cuozzo, S. 2016. Wolbachia infections responsible for thelytoky in dryinid wasps: the case of Gonatopus bonaerensis Virla (Hymenoptera: Dryinidae). Neotropical Entomology, 46: 409–413.CrossRefGoogle Scholar
Esselbaugh, C.O. 1946. A study of the eggs of the Pentatomidae Hemiptera. Annals of the Entomological Society of America, 39: 667–691.CrossRefGoogle Scholar
Faca, E.C., Pereira, F.F., Fernandes, W.C., da Silva, I.F., Costa, V.A., and Wengrat, A.P.G.S. 2021. Reproduction of Ooencyrtus submetallicus (Hymenoptera: Encyrtidae) and Trissolcus sp. aff. urichi (Hymenoptera: Scelionidae) in eggs of Nezara viridula (Hemiptera: Pentatomidae) of different ages. Journal of Agricultural Science, 13: 96–106.CrossRefGoogle Scholar
Fallahzadeh, M. and Japoshvili, G. 2010. Checklist of Iranian encyrtids (Hymenoptera: Chalcidoidea), with descriptions of new species. Journal of Insect Science, 10: 1–24.CrossRefGoogle Scholar
Faria, A.F., Torres, J.B., and Farias, A.M.I. 2000. Resposta funcional de Trichogramma pretiosum Riley (Hym.: Trichogrammatidae) parasitando ovos de Tuta absoluta (Meyrick) (Lep.: Gelechiidae): efeito da idade do hospedeiro. Anais da Sociedade Entomológica do Brasil, 29: 85–93.CrossRefGoogle Scholar
Ferreira, N.G.P. 2016. Ooencyrtus submetallicus (Hymenoptera: Encyrtidae): um potencial parasitoide de Euschistus heros e Chinavia pengue (Hemiptera: Pentatomidae). Master’s thesis. Universidade Federal da Grande Dourados, Dourados, Mato Grosso do Sul, Brazil.Google Scholar
Flanders, S.E. 1950. Regulation of ovulation and egg disposal in the parasitic Hymenoptera. The Canadian Entomologist, 82: 134–140.CrossRefGoogle Scholar
Godfray, H.C.J. 1987. The evolution of clutch size in parasitic wasps. The American Naturalist, 129: 221–233.CrossRefGoogle Scholar
Godfray, H.C.J. 1994. Parasitoids: behavioral and evolutionary ecology. Princeton University Press, New Jersey, United States of America.CrossRefGoogle Scholar
Godoy, K.B., Galli, J.C., and Ávila, C.J. 2005. Parasitism on eggs of stinkbugs Euschistus heros (Fabricius) and Piezodorus guildinii (Westwood) (Hemiptera: Pentatomidae) in São Gabriel do Oeste (Mato Grosso do Sul State, Brazil). Ciência Rural, 35: 455–458.CrossRefGoogle Scholar
Goulart, R.M., De Bortoli, S.A., Thuler, R.T., Pratissoli, D., Vianna, C.L.T.P., and Volpe, H.X.L. 2008. Avaliação da seletividade de inseticidas a Trichogramma spp. (Hymenoptera: Trichogrammatidae) em diferentes hospedeiros. Arquivos do Instituto Biológico, 75: 69–77.CrossRefGoogle Scholar
Greenberg, S.M., Nordlund, D.A., and Wu, Z. 1998. Influence of rearing host on adult size and oviposition behavior of mass-produced female Trichogramma minutum Riley and Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae). Biological Control, 11: 43–48.CrossRefGoogle Scholar
Heimpel, G.E. and Lundgren, J.G. 2000. Sex ratios of commercially reared biological control agents. Biological Control, 19: 77–93.CrossRefGoogle Scholar
Houseweart, M.W., Jennings, D.T., Welty, C., and Southard, S.G. 1983. Progeny production by Trichogramma minutum (Hymenoptera: Trichogrammatidae) utilizing eggs for Choristoneura fumiferana (Lepidoptera: Tortricidae) and Sitotroga cerealella (Lepidoptera: Gelechiidae). The Canadian Entomologist, 115: 1245–1252.CrossRefGoogle Scholar
Kapranas, A. and Tena, A. 2015. Encyrtid parasitoids of soft scale insects: biology, behavior, and their use in biological control. Annual Review of Entomology, 60: 195–211.CrossRefGoogle ScholarPubMed
Kaser, J.M. and Ode, P.J. 2016. Hidden risks and benefits of natural enemy-mediated indirect effects. Current Opinion in Insect Science, 14: 105–111.CrossRefGoogle ScholarPubMed
Kazmer, D.J. and Luck, R.F. 1991. Female body size, fitness and biological control quality: field experiments with Trichogramma pretiosum . Les Colloques de INRA, 56: 37–40.Google Scholar
Laumann, R.A., Moraes, M.C.B., Pareja, M., Botelho, A.C., Maia, A.N.A., Leonardecz, E., and Borges, M. 2008. Comparative biology and functional response of Trissolcus spp. (Hymenoptera: Scelionidae) and implications for stink bugs (Hemiptera: Pentatomidae) biological control. Biological Control, 44: 32–41.CrossRefGoogle Scholar
Legner, E.F. and Bay, E.C. 1965. Ooencyrtus submetallicus Howard in an extraordinary host-relationship with Hippelates pusio Loew. The Canadian Entomologist, 97: 556–557.CrossRefGoogle Scholar
Mainali, B.P. and Lim, U.T. 2012. Annual pattern of occurrence of Riptortus pedestris (Hemiptera: Alydidae) and its egg parasitoids Ooencyrtus nezarae Ishii and Gryon japonicum (Ashmead) in Andong, Korea. Crop Protection, 36: 37–42.CrossRefGoogle Scholar
Medeiros, M.A., Schimidt, F.V.G., Loiácono, M.S., Carvalho, V.F., and Borges, M. 1997. Parasitismo e predação em ovos de Euschistus heros (Fab.) (Heteroptera: Pentatomidae) no Distrito Federal, Brasil. Anais da Sociedade Entomológica do Brasil, 26: 397–401.CrossRefGoogle Scholar
Monti, M.M., Nugnes, F., Gualtieri, L., Gebiola, M., and Bernardo, U. 2016. No evidence of parthenogenesis-inducing bacteria involved in Thripoctenus javae thelytoky: an unusual finding in Chalcidoidea. Entomologia Experimentalis et Applicata, 160: 292–301.CrossRefGoogle Scholar
Moreira, M.D., dos Maria, S.C.F., Beserra, E.B., Torres, J.B., and Almeida, R.P. 2009. Parasitismo e superparasitismo de Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) em ovos de Sitotroga cerealella (Oliver) (Lepidoptera: Gelechiidae). Neotropical Entomology, 38: 237–242.CrossRefGoogle Scholar
Noyes, J. 2019. Universal Chalcidoidea database [online]. Available at http://www.nhm.ac.uk/chalcidoids [accessed 16 February 2019].Google Scholar
Oliveira, F.A.L.D., Silva, R.O., Oliveira, N.R.X.D., Andrade, G.S., Pereira, F.F., Zanuncio, J.C., et al. 2018. Reproduction of Trichospilus diatraeae (Hymenoptera: Eulophidae) with different densities and parasitism periods in Anticarsia gemmatalis (Lepidoptera: Noctuidae) pupae. Folia Biologica (Kraków), 66: 103–110.CrossRefGoogle Scholar
Olson, D.M. and Andow, D.A. 1998. Larval crowding and adult nutrition effects on longevity and fecundity of female Trichogramma nubilale Ertle & Davis (Hymenoptera: Trichogrammatidae). Environmental Entomology, 27: 508–514.CrossRefGoogle Scholar
Pacheco, D.J.P. and Corrêa-Ferreira, B.S. 1998. Potencial reprodutivo e longevidade do parasitoide Telenomus podisi Ashmead, em ovos de diferentes espécies de percevejos. Anais da Sociedade Entomológica do Brasil, 27: 585–591.CrossRefGoogle Scholar
Pacheco, D.J.P. and Corrêa-Ferreira, B.S. 2000. Parasitismo de Telenomus podisi Ashmead (Hymenoptera: Scelionidae) em populações de percevejos pragas da soja. Anais da Sociedade Entomológica do Brasil, 29: 295–302.CrossRefGoogle Scholar
Panizzi, A.R., Bueno, A.F., and Silva, F.A.C. 2013. Insetos que atacam vagens e grãos. In Soja: manejo integrado de insetos e outros artrópodes-praga. Edited by C.B. Hoffman-Campo, B.S. Corrêa-Ferreira, F. Moscardi. Embrapa Soja, Brazilian Agricultural Research Corporation, Brazil. Pp. 335–420.Google Scholar
Panizzi, A.R. and Lucini, T. 2016. What happened to Nezara viridula (L.) in the Americas? Possible reasons to explain populations decline. Neotropotical Entomology, 45: 619–628.CrossRefGoogle ScholarPubMed
Papaj, D.R. 2000. Ovarian dynamics and host use. Annual Review of Entomology, 45: 423–448.CrossRefGoogle ScholarPubMed
Pereira, F.F., Barros, R., and Pratissoli, D. 2004. Desempenho de Trichogramma pretiosum Riley e T. exiguum Pinto & Platner (Hymenoptera: Trichogrammatidae) submetidos a diferentes densidades de ovos de Plutella xylostella (Lepidoptera: Plutellidae). Ciência Rural, 34: 1669–1674.CrossRefGoogle Scholar
Pereira, F.F., Zanuncio, J.C., Pastori, P.L., Chichera, R.A., Andrade, G.S., and Serrão, J.E. 2010. Reproductive biology of Palmistichus elaeisis (Hymenoptera: Eulophidae) with alternative and natural hosts. Zoologia, 27: 887–891.CrossRefGoogle Scholar
Pereira, K.S., Guedes, N.M., Serrão, J.E., Zanuncio, J.C., and Guedes, R.N.C. 2017. Superparasitism, immune response and optimum progeny yield in the gregarious parasitoid Palmistichus elaeisis . Pest Management Science, 73: 1101–1109.CrossRefGoogle Scholar
Peri, E., Cusumano, A., Agro, A., and Colazza, S. 2011. Behavioral response of the egg parasitoid Ooencyrtus telenomicida to host-related chemical cues in a tritrophic perspective. BioControl, 56: 163–171.CrossRefGoogle Scholar
Polanczyk, R.A., Barbosa, W.F., Celestino, F.N., Pratissoli, D., Holtz, A.M., Milanez, A.M., et al. 2011. Influência da densidade de ovos de Diaphania hyalinata (L.) (Lepidoptera: Crambidae) na capacidade de parasitismo de Trichogramma exiguum Pinto & Platner e Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae). Neotropical Entomology, 40: 238–243.Google Scholar
Queiroz, A.P., Bueno, A.D., Pomari-Fernandes, A., Grande, M.L.M., Bortolotto, O.C., and Silva, D.M. 2017. Quality control of Telenomus remus (Hymenoptera: Platygastridae) reared on the factitious host Corcyra cephalonica (Lepidoptera: Pyralidae) for successive generations. Bulletin of Entomological Research, 107: 791–798.CrossRefGoogle ScholarPubMed
Rosenheim, J.A. 1993. Single-sex broods and the evolution of nonsiblicidal wasps. The American Naturalist, 141: 90–104.CrossRefGoogle Scholar
Shapiro, S.S. and Wilk, M.B. 1965. An analysis of variance test for normality. Biometrika, 52: 591–611.CrossRefGoogle Scholar
Silva, C.C., Laumann, R.A., Blassioli, M.C., Pareja, M., and Borges, M. 2008. Euschistus heros mass rearing technique for the multiplication of Telenomus podisi . Pesquisa agropecuária brasileira, 43: 575–580.CrossRefGoogle Scholar
Silva, F.A.S. and Azevedo, C.A.V. 2016. The Assistat software, version 7.7 and its use in the analysis of experimental data. African Journal of Agricultural Research, 11: 3733–3740.Google Scholar
Silva, F.A., Silva, J.J., Depieri, R.A., and Panizzi, A.R. 2012. Feeding activity, salivary amylase activity, and superficial damage to soybean seed by adult Edessa meditabunda (F.) and Euschistus heros (F.) (Hemiptera: Pentatomidae). Neotropical Entomology, 41: 386–390.CrossRefGoogle Scholar
Silva, G.V., Pasini, A., Bueno, A.F., Bortolotto, O.C., Barbosa, G.C., and Cruz, Y.K.S. 2014. No impact of Bt soybean that express Cry1Ac protein on biological traits of Euschistus heros (Hemiptera, Pentatomidae) and its egg parasitoid Telenomus podisi (Hymenoptera, Platygastridae). Revista Brasileira de Entomologia, 58: 285–290.CrossRefGoogle Scholar
Silva, S.A. 2017. Controle biológico de Erinnyis ello (Linnaeus, 1758) (Lepidoptera: Sphingidae) com parasitoides na cultura da mandioca. Ph.D. thesis. Universidade Federal da Grande Dourados, Dourados, Mato Grosso do Sul, Brazil.Google Scholar
Sorensen, J.G., Addison, M.F., and Terblanche, J.S. 2012. Mass-rearing of insects for pest management: challenges, synergies and advances from evolutionary physiology. Crop Protection, 38: 87–94.CrossRefGoogle Scholar
Stouthamer, R. 1997. Wolbachia-induced parthenogenesis. In Influential passengers: inherited microorganisms and arthropod reproduction. Edited by S.L. O’Neill, A.A. Hoffmann, J.H. Werren. Oxford University Press, Oxford, United Kingdom. Pp. 102–124.Google Scholar
Tuelher, E.S., da Silva, E.H., Rodriques, H.S., Hirose, E., Guedes, R.N.C., and Oliveira, E.E. 2018. Area-wide spatial survey of the likelihood of insecticide control failure in the neotropical brown stink bug Euschistus heros . Journal of Pest Science, 91: 849–859.CrossRefGoogle Scholar
Tunca, H., Colombel, E., Ben Soussan, T., Buradino, M., Galio, F., and Tabone, E. 2015. Optimal biological parameters for rearing Ooencyrtus pityocampae on the new laboratory host, Philosamia ricini . Journal of Applied Entomology, 140: 527–525.CrossRefGoogle Scholar
Tunca, H., Colombel, E., Venard, M., and Tabone, E. 2017. Incidence of superparasitism in the egg parasitoid, Ooencyrtus kuvanae Howard (Hymenoptera: Encyrtidae). Biocontrol Science and Technology, 27: 796–808.CrossRefGoogle Scholar
Waage, J.K. and Ng, D. 1984. The reproductive strategy of a parasitic wasp: optimal progeny and sex allocation in Trichogramma evanescens . Journal of Animal Ecology, 53: 401–415.CrossRefGoogle Scholar
Wilson, F. and Woolcock, L.T. 1960. Temperature determination of sex in a parthenogenetic parasite, Ooencyrtus submetallicus (Howard) (Hymenoptera: Encyrtidae). Australian Journal of Zoology, 8: 153–169.CrossRefGoogle Scholar
Zanuncio, J.C., Oliveira, H.N., Torres, J.B., and Pratissoli, D. 2000. Egg parasitoids of Podisus sculptus distant (Heteroptera: Pentatomidae) in an eucalyptus plantation in the Brazilian Amazonian region. Revista de Biologia Tropical, 48: 989–992.Google Scholar