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Development of Cleruchoides noackae, an egg-parasitoid of Thaumastocoris peregrinus, in eggs laid on different substrates, with different ages and post-cold storage

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Abstract

Cleruchoides noackae Lin and Huber (Hymenoptera: Mymaridae) is an egg parasitoid of Thaumastocoris peregrinus Carpintero and Dellapé (Hemiptera: Thaumastocoridae). The parasitism and development of C. noackae was studied in T. peregrinus eggs of different ages, laid on eucalyptus leaves or paper towel and stored at 5 °C. The emergence, sex ratio and development of C. noackae and hatched nymphs of T. peregrinus were evaluated. This parasitoid had an emergence rate higher than 60% from zero to one, one to two, and two to three-day old eggs and lower than 10% for those 3–4 and 4–5 days old. The female proportion was 78% and the egg-adult period for C. noackae was 19.5 days. The use of T. peregrinus eggs up to three days old, laid on paper towel and stored at 5 °C for 14 days did not affect the biological parameters of C. nockae and should be used for mass rearing of this parasitoid.

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References

  • Alim MA, Lim UT (2009) Refrigeration of Riptortus clavatus (Hemiptera: Alydidae) eggs for the parasitization by Gryon japonicum (Hymenoptera: Scelionidae). Biocontrol Sci Technol 19:315–325

    Article  Google Scholar 

  • Ayvaz A, Karasa E, Karaborklu S, Tuncbilek A (2008) Effects of cold storage, rearing temperature, parasitoid age and irradiation on the performance of Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae). J Stored Prod Res 44:232–240

    Article  Google Scholar 

  • Barbosa LR, Santos F, Buhrer CB, Nichele LA, Wilcken CF, Soliman EP (2016) Criação massal do percevejo bronzeado, Thaumastocoris peregrinus: Carpinteiro and Dellapé, 2006 (Hemiptera, Thaumastocoridae). Brasília, DF. Available in: http://ainfo.cnptia.embrapa.br/digital/bitstream/item/145907/1/Criacao-massal-do-percevejo-bronzeado.pdf. Accessed 02 Dec 2017

  • Barbosa LR, Rodrigues AP, Soler LS, Fernandes BV, Castro BMCC, Wilcken CF, Zanuncio JC (2017) Establishment in the field of Cleruchoides noackae (Hymenoptera: Mymaridae), an exotic egg parasitoid of Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae). Fla Entomol 100:372–374

    Article  Google Scholar 

  • Bonte M, De Clercq P (2010) Impact of artificial rearing systems on the developmental and reproductive fitness of the predatory bug Orius laevigatus. J Insect Sci 10:1–11

    Article  Google Scholar 

  • Brodeur J, Boivin G (2004) Functional ecology of immature parasitoids. Annu Rev Entomol 49:27–49

    Article  CAS  PubMed  Google Scholar 

  • Castañé AC, Zapata R (2005) Rearing the predatory bug Macrolophus caliginosuson a meat-based diet. Biol Control 34:66–72

    Article  Google Scholar 

  • Chen WL, Leopold RA (2007) Progeny quality of Gonatocerus ashmeadi (Hymenoptera: Mymaridae) reared on stored eggs of Homalodisca coagulata (Hemiptera: Cicadellidae). J Econ Entomol 100:685–694

    Article  PubMed  Google Scholar 

  • Colazza S, Cusumano A, Giudice DL, Peri E (2014) Chemo-orientation responses in hymenopteran parasitoids induced by substrate-borne semiochemicals. BioControl 59:1–17

    Article  CAS  Google Scholar 

  • Constant B, Grenier S, Bonnot G (1996) Artificial substrate for egg laying and embryonic development by the predatory bug Macrolophus caliginosus (Heteroptera: Miridae). Biol Control 7:140–147

    Article  Google Scholar 

  • Corrêa-Ferreira BS, Moscardi F (1993) Storage techniques of stink bug eggs for laboratory production of the parasitoid, Trissolcus basalis (Wollaston). Pesqui Agropecu Bras 28:1247–1253

    Google Scholar 

  • De Puysseleyr V, De Man S, Höfte M, De Clercq P (2013) Plantless rearing of the zoophytophagous bug Nesidiocoris tenuis. BioControl 58:205–213

    Article  Google Scholar 

  • De Puysseleyr V, Höfte M, De Clercq P (2014) Continuous rearing of the predatory anthocorid Orius laevigatus without plant materials. J Appl Entomol 138:45–51

    Article  Google Scholar 

  • Demétrio CGB, Hinde J (1997) Half-normal plots and overdispersion. GLIM Newsletter 27:19–26

    Google Scholar 

  • Demétrio CGB, Hinde J, Moral RA (2014) Models for overdispersed data in entomology. In: Ferreira CP, Godoy WAC (eds) Ecological modelling applied to entomology. Entomology in focus. Springer, Cham, pp 219–259

    Google Scholar 

  • Elliott JM (2003) A comparative study of the functional response of four species of carnivorous stoneflies. Freshwater Biol 48:191–202

    Article  Google Scholar 

  • Fatouros NE, Dicke M, Mumm R, Meiners T, Hilker M (2008) Foraging behavior of egg parasitoids exploiting chemical information. Behav Ecol 19:677–689

    Article  Google Scholar 

  • Foerster LA, Doetzer AK, Castro LCF (2004) Emergence, longevity and fecundity of Trissolcus basalis and Telenomus podisi after cold storage in the pupal stage. Pesqui Agropecu Bras 39:841–845

    Article  Google Scholar 

  • Greco CF, Stilinovic D (1998) Parasitization performance of Trichogramma spp. (Hym., Trichogrammatidae) reared on eggs of Sitotroga cerealella Oliver (Lep., Gelechiidae), stored at freezing and subfreezing conditions. J Appl Entomol 122:311–314

    Article  Google Scholar 

  • Hassell MP (2000) Host-parasitoid population dynamics. J Anim Ecol 69:543–566

    Article  Google Scholar 

  • Hinde J, Demétrio CGB (1998) Overdispersion: model and estimation. Comput Stat Data Anal 27:151–170

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363

    Article  PubMed  Google Scholar 

  • Huber JT (1986) Systematics, biology, and hosts of the Mymaridae and Mymarommatidae (Insecta: Hymenoptera): 1758–1984. In: Thomas DE (ed) Entomography: an annual review for biosystematics. Entomography Publications, Sacramento, pp 185–243

    Google Scholar 

  • Huber JT, Mendel Z, Protasov A, LaSalle J (2006) Two new Australian species of Stethynium (Hymenoptera: Mymaridae), larval parasitoids of Ophelimus maskelli (Ashmead) (Hymenoptera: Eulophidae) on Eucalyptus. J Nat Hist 40:1909–1921

    Article  Google Scholar 

  • Irvin NA, Hoddle MS (2005) Determination of Homalodisca coagulata (Hemiptera: Cicadellidae) egg ages suitable for oviposition by Gonatocerus ashmeadi, Gonatocerus triguttatus, and Gonatocerus fasciatus (Hymenoptera: Mymaridae). Biol Control 32:391–400

    Article  Google Scholar 

  • Jacobs DH, Neser S (2005) Thaumastocoris australicus Kirkaldy (Heteroptera: Thaumastocoridae): a new insect arrival in South Africa, damaging to Eucalyptus trees: research in action. S Afr J Sci 101:233–236

    Google Scholar 

  • Kant R, Minor MA (2017) Parasitoid Diaeretiella rapae (Hymenoptera: Braconidae) adjusts reproductive strategy when competing for hosts. Environ Entomol 46:521–527

    Article  PubMed  Google Scholar 

  • King BH (1987) Offspring sex ratios in parasitoid wasps. Q Rev Biol 62:367–396

    Article  Google Scholar 

  • Ko K, Liu Y, Hou M, Babendreier D, Zhang F, Song K (2014) Evaluation for potential Trichogramma (Hymenoptera: Trichogrammatidae) strains for control of the striped stem borer (Lepidoptera: Crambidae) in the Greater Mekong subregion. J Econ Entomol 107:955–963

    Article  Google Scholar 

  • Kristoffersen AB, Lingjaerde C, Stenseth NC, Shimada M (2001) Non-parametric modeling of non-linear density dependence: a three-species host-parasitoid system. J Anim Ecol 70:808–819

    Article  Google Scholar 

  • Laudonia S, Sasso R (2012) The bronze bug Thaumastocoris peregrinus: a new insect recorded in Italy, damaging to Eucalyptus trees. Bull Insectol 65:89–93

    Google Scholar 

  • Lin NQ, Huber JT, La Salle J (2007) The Australian genera of Mymaridae (Hymenoptera: Chalcidoidea). Zootaxa 1596:1–111

    Google Scholar 

  • Liu SS, Zhang GM, Zhang F (1998) Factors influencing parasitism of Trichogramma dendrolimi on eggs of the Asian corn borer, Ostrinia furnacalis. Biol Control 42:273–287

    Google Scholar 

  • Liu K, Fu B, Lin J, Fu Y, Peng Z, Jin Q (2014) Effect of temperatures and cold storage on performance of Tetrastichus brontispae (Hymenoptera: Eulophidae), a parasitoid of Brontispa longissima (Coleoptera: Chrysomelidae). J Insect Sci 14:1–6

    Google Scholar 

  • Lundgren JG (2011) Reproductive ecology of predaceous Heteroptera. Biol Control 59:37–52

    Article  Google Scholar 

  • Lynch LD, Bowers G, Begon M, Thompson DJ (1998) A dynamics refuge model and population regulation by insect parasitoids. J Anim Ecol 67:270–279

    Article  Google Scholar 

  • Lytle JL, Morse JG, Triapsitsyn S (2012) Biology and host specificity of Gonatocerus deleoni (Hymenoptera: Mymaridae), a potential biocontrol agent of Homalodisca vitripennis (Hemiptera: Cicadellidae) in California, USA. BioControl 57:61–69

    Article  Google Scholar 

  • Mahmoud AMA, Lim UT (2007) Evaluation of cold-stored eggs of Dolycoris baccarum (Hemiptera: Pentatomidae) for parasitization by Trissolcus nigripedius (Hymenoptera: Scelionidae). Biol Control 43:287–293

    Article  Google Scholar 

  • Mainali BP, Lim UT (2013) Quality assessment of Riptortus pedestris (Hemiptera: Alydidae) eggs cold-stored at different temperature and relative humidity regime. Biol Control 64:132–137

    Article  Google Scholar 

  • Millar JG, Paine TD, Hoddle M (2000) Biological control of a newly introduced pest, the eucalyptus tortoise beetle, Trachymela sloanei. University of California, Division of Agriculture and Natural Resources Slosson Report, Davis, pp 1999–2000

    Google Scholar 

  • Mutitu EK, Garnas JR, Hurley BP, Wingfield MJ, Harney M, Bush SJ, Slippers B (2013) Biology and rearing of Cleruchoides noackae (Hymenoptera: Mymaridae), an egg parasitoid for the biological control of Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae). J Econ Entomol 106:1979–1985

    Article  PubMed  Google Scholar 

  • Pak GA, Buis CEM, Heck ICC, Hermans MLG (1986) Behavioural variations among strains of Trichogramma spp.: host-age selection. Entomol Exp Appl 40:247–258

    Article  Google Scholar 

  • Parra JRP (2010) Mass rearing of egg parasitoids for biological control programs. In: Cônsoli FL, Parra JRP, Zucchi RA (eds) Egg parasitoids in agroecosystems with emphasis on Trichogramma. Springer, Heidelberg, pp 267–292

    Google Scholar 

  • Pereira FF, Zanuncio JC, Serrão JE, Zanuncio TV, Pratissoli D, Pastori PL (2010) The density of females of Palmistichus elaeisis Delvare and LaSalle (Hymenoptera: Eulophidae) affects their reproductive performance on pupae of Bombyx mori L. (Lepidoptera: Bombycidae). An Acad Bras Cienc 82:323–331

    Article  PubMed  Google Scholar 

  • Peverieri GS, Furlan P, Benassai D, Caradonna S, Strong WB, Roversi PF (2013) Host egg age of Leptoglossus occidentalis (Heteroptera, Coreidae) and parasitism by Gryon pennsylvanicum (Hymenoptera, Platygastridae). J Econ Entomol 106:633–640

    Article  PubMed  Google Scholar 

  • Peverieri GS, Furlan P, Benassai D, Strong WB, Roversi PF (2015) Long-term storage of eggs of Leptoglossus occidentalis for the mass-rearing of its parasitoid Gryon pennsylvanicum. BioControl 60:293–306

    Article  Google Scholar 

  • Pizzol J, Desneux N, Wajnberg E, Thiéry D (2012) Parasitoid and host ages have independent impact on various biological traits in a Trichogramma species. J Pest Sci 85:489–496

    Article  Google Scholar 

  • Pratissoli D, Zanuncio JC, Vianna UR, Andrade JS, Guimarães EM, Espindula MC (2004) Fertility life table of Trichogramma pretiosum and Trichogramma acacioi on eggs of Anagasta kuehniella at different temperatures. Pesqui Agropecu Bras 39:193–196

    Article  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. https://www.r-project.org/

  • Reis AR, Ferreira L, Tomé M, Araújo C, Branco M (2012) Efficiency of biological control of Gonipterus platensis (Coleoptera: Curculionidae) by Anaphes nitens (Hymenoptera: Mymaridae) in cold areas of the Iberian Peninsula: implications for defoliation and wood production in Eucalyptus globulus. For Ecol Manage 270:216–222

    Article  Google Scholar 

  • Schmidt JM (1994) Host recognition and acceptance by Trichogramma. In: Wajnberg E, Hassan SA (eds) Biological control with egg parasitoids. CAB International, Wallingford, pp 165–200

    Google Scholar 

  • Silva RB, Zanuncio JC, Serrão JE, Lima ER, Figueiredo MLC, Cruz I (2009) Suitability of different artificial diets for development and survival of stages of the predaceous ladybird beetle Eriopis connexa. Phytoparasitica 37:115–123

    Article  Google Scholar 

  • Song LW, Wen XY, Zang LS, Ruan CC, Shi SS, Shao XW, Zhang F (2015) Parasitism and suitability of different egg ages of the Leguminivora glycinivorella (Lepidoptera: Tortricidae) for three indigenous Trichogramma species. J Econ Entomol 108:933–939

    Article  PubMed  Google Scholar 

  • Sousa JM, Spence JR (2001) Host age and parasitism by Tiphodytes gerriphagus (Hymenoptera: Scelionidae), an egg parasitoid of water striders (Heteroptera: Gerridae). Ann Entomol Soc Am 94:681–685

    Article  Google Scholar 

  • Souza AR, Candelaria MC, Barbosa L, Wilcken CF, Campos JM, Serrão JE, Zanuncio JC (2016) Longevity of Cleruchoides noackae (Hymenoptera: Mymaridae), an egg parasitoid of Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae), with various honey concentrations and at several temperatures. Fla Entomol 99:33–37

    Article  Google Scholar 

  • De Carvalho Spínola-Filho PR , Leite GLD, Soares MA, Alvarenga AC, De Paulo PD, Tuffi-Santos LD, Zanuncio JC (2014) Effects of duration of cold storage of host eggs on percent parasitism and adult emergence of each of ten Trichogrammatidae (Hymenoptera) species. Fla Entomol 97(1):14–21

    Article  Google Scholar 

  • St-Onge M, Cormier D, Todorova S, Lucas E (2016) Conservation of Ephestia kueniella eggs as hosts for Trichogramma ostriniae. J Appl Entomol 140:218–222

    Article  Google Scholar 

  • Strand MR (1986) The physiological interactions of parasitoids with their hosts and their influence on reproductive strategies. In: Waage J, Greathead D (eds) Insect Parasitoids. Academic Press, London, pp 97–136

    Google Scholar 

  • Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172

    Article  Google Scholar 

  • Vinson SB (1998) The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol Control 11:79–96

    Article  Google Scholar 

  • Zhang JJ, Ren BZ, Yuan XH, Zang LS, Ruan CC, Sun GZ, Shao XW (2014) Effects of host-egg ages on host selection and suitability of four Chinese Trichogramma species, egg parasitoids of the rice striped stem borer, Chilo suppressalis. BioControl 59:159–166

    Article  CAS  Google Scholar 

  • Zhou Y, Abram PK, Boivin G, Brodeur J (2014) Increasing host age does not have the expected negative effects on the fitness parameters of an egg parasitoid. Entomol Exp Appl 151:106–111

    Article  Google Scholar 

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Acknowledgements

We are grateful to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Project: 142131/2012-1 e 445512/2014-8), Empresa Brasileira de Pesquisa Agropecuária (EMBRAPA), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG) and the Programa Cooperativo sobre Proteção Florestal/PROTEF of Instituto de Pesquisas e Estudos Florestais/IPEF for their financial support. Dr. Phillip John Villani (The University of Melbourne, Australia) revised and corrected the English language used in this manuscript.

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Correspondence to Leonardo Rodrigues Barbosa.

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Barbosa, L.R., Rodrigues, Â.P., de Souza, L.N. et al. Development of Cleruchoides noackae, an egg-parasitoid of Thaumastocoris peregrinus, in eggs laid on different substrates, with different ages and post-cold storage. BioControl 63, 193–202 (2018). https://doi.org/10.1007/s10526-017-9863-3

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