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Low Temperature Storage of Telenomus remus (Nixon) (Hymenoptera: Platygastridae) and its Factitious Host Corcyra cephalonica (Stainton) (Lepidoptera: Pyralidae)

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Abstract

We conducted three bioassays to evaluate the effect of low-temperature storage of eggs (host) and pupae and adults (parasitoid) on the biology and parasitism capacity of the egg parasitoid Telenomus remus (Nixon) (Hymenoptera: Platygastridae). Viable stored Corcyra cephalonica (Stainton) (Lepidoptera: Pyralidae) eggs were parasitized to the same degree or even higher than fresh eggs when stored until 14 days at 5°C or until 21 days at 10°C. In contrast, the percentage of parasitized sterilized eggs was equal to the control only when stored for 7 and 14 days. Survival of T. remus pupae declined with storage time at both studied temperatures (5 and 10°C). However, after 7 days of storage, survival of pupae was still 86.3 and 64.9% at 10 and 5°C, respectively. The number of adult male survivors remained similar until the fourth storage day at both 5 and 10°C. In contrast, female survival did not differ until day 8 at 10°C or day 6 at 5°C. Parasitism capacity of stored adults was not altered by storage compared with the control. Therefore, we conclude that the maximal storage time at 10°C is 21 days for viable C. cephalonica eggs and 7 days for T. remus pupae, while parasitoid adults should not be stored for more than 4 days at either 5 or 10°C.

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References

  • Ayvaz A, Karasu E, Karabörklü S, Tunçbilek 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 

  • Bayram A, Ozcan H, Kornosor S (2005) Effect of cold storage on the performance of Telenomus busseolae Gahan (Hymenoptera: Scelionidae), an egg parasitoid of Sesamia nonagrioides (Lefebvre) (Lepidoptera: Noctuidae). Biol Control 35:68–77

    Article  Google Scholar 

  • Bernardi EB, Haddad ML, Parra JRP (2000) Comparison of artificial diets for rearing Corcyra cephalonica (Stainton, 1865) (Lepidoptera: Pyralidae) for Trichogramma mass production. Rev Bras Biol 60:45–52

    Article  CAS  PubMed  Google Scholar 

  • Bernardo U, Iodice L, Sasso R, Pedata PA (2008) Effects of cold storage on Thripobius javae (= T. semiluteus) (Hymenoptera: Eulophidae). Biocontrol Sci Techn 18:921–933

    Article  Google Scholar 

  • Bueno RCODF, Carneiro TR, Pratissoli D, Bueno ADF, Fernandes OA (2008) Biology and thermal requirements of Telenomus remus reared on fall armyworm Spodoptera frugiperda eggs. Ciênc Rural 38:1–6

    Article  Google Scholar 

  • Burr IW, Foster LA (1972) A test for equality of variances. Mimeo series n° 282. Purdue University, West Lafayette, 26p

    Google Scholar 

  • Carvalho JS, Vacari AM, De Bortoli SA, Viel SR (2008) Efeito do armazenamento de pupas de Cotesia flavipes (Cameron, 1891) (Hymenoptera: Braconidae) em baixa temperatura. Bol Sanid Veg 34:21–26

    Google Scholar 

  • Cave RD (2000) Biology, ecology and use in pest management of Telenomus remus. BioControl 21:21–26

    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 

  • Colinet H, Boivin G (2011) Insect parasitoids cold storage: a comprehensive review of factors of variability and consequences. Biol Control 58:83–95

    Article  Google Scholar 

  • Cônsoli FL, Kitajima EW, Parra JRP (1999) Ultrastructure of the natural and factitious host eggs of Trichogramma galloi Zucchi and Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae). Int J Insect Morphol Embryol 28:211–231

    Article  Google Scholar 

  • Couillien D, Grégoire JC (1994) Take-off capacity as a criterion for quality control in mass-produced predators, Rhizophagus grandis (Coleoptera: Rhizophagidae) for the biocontrol of bark beetles, Dendroctonus micans (Coleoptera: Scolytidae). Entomophaga 39:385–395

    Article  Google Scholar 

  • Cruz I, Figueiredo MLC, Oliveira CE, Vasconcelos CA (1999) Damage of Spodoptera frugiperda (Smith) in different maize genotypes cultivated in soil under three levels of aluminium saturation. Int J Pest Manag 45:293–296

    Article  Google Scholar 

  • Corrêa-Ferreira BS, Moscardi F (1993) Técnicas de armazenamento de ovos do percevejo-verde visando à multiplicação do parasitóide Trissolcus basalis (Wollaston). Pesq Agropec Bras 28:1247–1253

    Google Scholar 

  • Foerster LA, Doetzer AK (2006) Cold storage of the egg parasitoids Trissolcus basalis (Wollaston) and Telenomus podisi Ashmead (Hymenoptera: Scelionidae). Biol Control 36:232–237

    Article  Google Scholar 

  • Gardner J, Hoffmann MP, Pitcher SA, Nyrop JP (2012) Recurrent warming to improve cold storage of Trichogrammatids (Hymenoptera: Trichogrammatidae). Biocontrol Sci Techn 22:261–270

    Article  Google Scholar 

  • Gautam RD (1986) Effect of cold storage on the adult parasitoid Telenomus remus Nixon (Scelionidae: Hymenoptera) and the parasitised eggs of Spodoptera litura (Fabr.) (Noctuidae: Lepidoptera). J Entomol Res 10:125–131

    Google Scholar 

  • Gharbi N (2014) Influences of cold storage period and rearing temperature on the biological traits of Trichogramma oleae (Hymenoptera: Trichogrammatidae). Tunis J Plant Prot 9:143–153

    Google Scholar 

  • Hassan SA, Beyer H, Dannemann K, Heil M, Pfister J, Reichel W, Winstel, K (1990) Massenzucht and Anwendung von Trichogramma: 11. Ergebnisse von Ringversuchen zur Bekämpfung des Maiszünslers (Ostrinia nubilalis). Gesunde Pflanzen, 387–394

  • Kivan M, Kilic N (2005) Effects of storage at low-temperature of various heteropteran host eggs on the egg parasitoid, Trissolcus semistriatus. BioControl 50:589–600

    Article  Google Scholar 

  • Leopold RA (1998) Cold storage of insects for integrated pest management. In: Hallman GJ, Denlinger DL (eds) Temperature sensitivity in insects and application in integrated pest management. Westview Press, Boulder, pp 235–267

    Google Scholar 

  • López SN, Botto E (2005) Effect of cold storage on some biological parameters of Eretmocerus corni and Encarsia formosa (Hymenoptera: Aphelinidae). Biol Control 33:123–130

    Article  Google Scholar 

  • Lysyk TJ (2004) Effects of cold storage on development and survival of three species of parasitoids (Hymenoptera: Pteromalidae) of house fly, Musca domestica L. Environ Entomol 33:823–831

    Article  Google Scholar 

  • Macedo LPM, Maracajá PB, Bezerra CES (2006) Técnicas de armazenamento de ovos de insetos para programas de controle biológico. Rev Verde 1:1–19

    Google Scholar 

  • Nakama PA, Foerster LA (2001) Efeito da alternância de temperaturas no desenvolvimento e emergência de Trissolcus basalis (Wollaston) e Telenomus podisi Ashmead (Hymenoptera: Scelionidae). Neotrop Entomol 30:269–275

    Article  Google Scholar 

  • Navarro MA (1998) Trichogramma spp. producción, uso y manejo en Colombia. Impretec, Guadalajara de Buga, 176p

    Google Scholar 

  • Pereira FF, Zanuncio JC, Serrão JE, Pastori PL, Ramalho FS (2009) Reproductive performance of Palmistichus elaeisis Delvare and LaSalle (Hymenoptera: Eulophidae) with previously refrigerated pupae of Bombyx mori L. (Lepidoptera: Bombycidae). Braz J Biol 69:865–869

  • Pogue GM (2002) A world revision of the genus Spodoptera Guenée (Lepidoptera: Noctuidae). Mem Am Entomol Soc 43:1–202

    Google Scholar 

  • Pomari AF, Bueno AF, Bueno RCOF, Menezes ADO (2012) Biological characteristics and thermal requirements of the biological control agent Telenomus remus (Hymenoptera: Platygastridae) reared on eggs of different species of the genus Spodoptera (Lepidoptera: Noctuidae). Ann Entomol Soc Am 105:73–81

    Article  Google Scholar 

  • Pomari AF, Bueno AF, Bueno RCOF, Menezes Junior AO, Fonseca ACPF (2013) Releasing number of Telenomus remus (Nixon) (Hymenoptera: Platygastridae) against Spodoptera frugiperda Smith (Lepidoptera: Noctuidae) in corn, cotton and soybean. Cien Rural 43:377–382

    Article  Google Scholar 

  • Pomari-Fernandes A, De Queiroz AP, de Freitas BA, Sanzovo AW, De Bortoli SA (2015) The importance of relative humidity for Telenomus remus (Hymenoptera: Platygastridae) parasitism and development on Corcyra cephalonica (Lepidoptera: Pyralidae) and Spodoptera frugiperda (Lepidoptera: Noctuidae) eggs. Ann Entomol Soc Am 108:11–17

    Article  Google Scholar 

  • Pratissoli D, Vianna UR, Oliveira HN, Pereira FF (2003) Efeito do armazenamento de ovos de Anagasta kuehniella (Lepidoptera: Pyralidae) nas características biológicas de três espécies de Trichogramma (Hymenoptera: Trichogrammatidae). Rev Ceres 50: 95–103

  • Sá VGM, Fonseca BVC, Boregas KGB, Waquil JM (2009) Sobrevivência e desenvolvimento larval de Spodoptera frugiperda (J E Smith) (Lepidoptera: Noctuidae) em hospedeiros alternativos. Neotrop Entomol 38:108–115

    Article  Google Scholar 

  • Santos GP, Cosenza GW, Albino JC (1980) Biologia de Spodoptera latifascia (Walk., 1856) (Lepidoptera: Noctuidae) sobre folhas de eucalipto. Rev Bras Entomol 24:153–155

    Google Scholar 

  • SAS Institute (2009) SAS/STAT: user’s guide. Version 9.2. SAS Institute, Cary

    Google Scholar 

  • Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611

    Article  Google Scholar 

  • Storey KB, Storey JM (1988) Freeze tolerance in animals. Physiol Rev 68:27–84

    CAS  PubMed  Google Scholar 

  • Tezze AA, Botto EN (2004) Effect of cold storage on the quality of Trichogramma nerudai (Hymenoptera: Trichogrammatidae). Biol Control 30:11–16

    Article  Google Scholar 

  • van Lenteren JC (2003) Quality control and production of biological control agents: theory and testing procedures. CABI, Wallingford, 327p

    Book  Google Scholar 

  • van Steenburg WE (1934) Trichogramma minutum Rilley as a parasite of the oriental fruit moth (Laspeyresia molesta Busck.) in Ontario. Can J Res 10:287–314

    Article  Google Scholar 

  • Voegelé J, Brun P, Daumal J (1974) Les Trichogrammes 1 – Modalités de la prise de possession et de l´élimination de l´hôte chez le parasite embryonnaire Trichogramma brasiliensis (Hymenoptera: Chalcidoidea). Ann Soc Entomol France 10: 757–761.

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Acknowledgments

The authors would like to thank Embrapa Soja, the “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)”, and the “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq), grant number 303779/2015-2, for funds that supported this research. Thanks are also extended to Dagmar Frisch for the English revision of this manuscript. This paper was approved for publication by the Editorial Board of Embrapa Soja.

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Authors and Affiliations

  1. Instituto Agronômico do Paraná (IAPAR), Londrina, Paraná, Brasil

    A P Queiroz & D M Silva

  2. Empresa Brasileira de Pesquisa Agropecuária — Embrapa Soja, Londrina, Paraná, Brasil, 86001-970

    A F Bueno

  3. Univ Federal da Fronteira Sul, Laranjeiras do Sul, Paraná, Brasil

    A POMARI-FERNANDES

  4. Univ Estadual de Londrina, Londrina, Paraná, Brasil

    M L M Grande & O C Bortolotto

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  1. A P Queiroz
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  2. A F Bueno
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  3. A POMARI-FERNANDES
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  4. M L M Grande
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  5. O C Bortolotto
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  6. D M Silva
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Correspondence to A F Bueno.

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Edited by Tiago C da Costa Lima — Embrapa

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Queiroz, A.P., Bueno, A.F., POMARI-FERNANDES, A. et al. Low Temperature Storage of Telenomus remus (Nixon) (Hymenoptera: Platygastridae) and its Factitious Host Corcyra cephalonica (Stainton) (Lepidoptera: Pyralidae). Neotrop Entomol 46, 182–192 (2017). https://doi.org/10.1007/s13744-016-0442-6

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