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RETRACTED ARTICLE: Impact of cold storage on the performance of entomophagous insects: an overview

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This article was retracted on 15 May 2021

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Abstract

Mass rearing for commercial production of high quality beneficial insects is considered as an important tool for biological control programmes worldwide, especially those based on augmentative releases. Low temperature storage is a valuable method for increasing the shelf life of entomophagous insects. Insect predators and parasitoids are used extensively in biological control programmes and, because of this, studies on cold storage started over 90 years ago. The ability to store reared biocontrol agents at low temperatures for certain duration provides an opportunity to accumulate or stockpile sufficient number of entomophagous insects for field release at proper weather conditions and make them available during high demand periods to the concerned farmers. Cold stored natural enemies can be synchronously released in the fields during critical stages of pest outbreaks. Cold storage also helps to keep viable stock of natural enemies when not needed and to minimize laboratory operations by prolonging their survival and delaying eclosion. Cold storage tolerance is highly plastic trait influenced by a range of biotic and abiotic factors experienced before, during and after cold exposure. These factors ultimately affect the development, longevity, fecundity, parasitization, sex-ratio and other fitness parameters along with morphology, behaviour and physiology of entomophagous insects. For the successful implementation of a cold storage project, knowledge of these diverse factors that cause storage and post-storage effects is essential. The potential of cold storage protocols in improving mass rearing and commercial production of bioagents is thus reviewed to access the strategies, innovations, techniques, devices and wisdom involved in the process of cold storage of entomophagous insects worldwide.

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References

  • Abdel-Baky, N. F., Ragab, M. E., Gahanim, A. A., El-Nagar, M. E., & El-Mtewally, M. M. (2015). Influence of cold storage on the viability of Vedalia beetle, Rodolia cardinalis (Mulsant) (Coleoptera: Coccinellidae). Plant Protection and Pathology, 6(6), 915–927.

    Article  Google Scholar 

  • Abdel-Gawad, H. A. S., Sayed, A., & Ahmed, S. A. (2010). Impact of cold storage temperature and period on performance of Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae). Australian Journal of Basic and Applied Sciences, 4(8), 2188–2195.

    Google Scholar 

  • Abdel-Salam, A. H., & Abdel-Baky, N. F. (2000). Possible storage of Conccinella undecimpunctata (Coleoptera: Coccinellidae) under low temperature and its effect on some biological characteristics. Journal of Applied Entomology, 124(3–4), 169–176.

    Article  Google Scholar 

  • Abdel-Salam, A. H., Ellington, J. J., El-Adl, M. A., El-Naga, A. M., & Ghanim, A. A. (1997). Effect of cold storage on survival, longevity and fecundity of Harmonia axyridis adults. In: Proceedings of the 1st National Conference, Mansoura University September 1997, Egypt. In 58–72 pp.

    Google Scholar 

  • Abdel-Salam, A. H., El-Serafi, H. A. K., Mohamed, N. A., & Twafik, W. A. (2014). Cold storage of the egg parasitoid, Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) and its effect on some biological characteristics. Journal of Plant Protection and Pathology, 5(2), 215–223.

    Article  Google Scholar 

  • Abdullah, K., Ellington, J. J., & Yasmin, S. (2009). Storage studies of Anaphes iole Girault (Hymenoptera: Mymaridae) at different developmental stages, temperatures and light-dark regimes. Agriculturae Conspectus Scientificus, 74(4), 319–326.

    Google Scholar 

  • Ahmad, M. J., & Ahmad, S. B. (2014). Effect of cold storage on laboratory performance of Trichogramma cacoeciae and T. embryophagum. Journal of Biological Control, 28(3), 137–143.

    Google Scholar 

  • Alam, M. S., Alam, M. Z., Alam, S. N., Miah, M. R. U., & Mian, M. I. H. (2016). Effect of storage duration on the stored pupae of parasitoid Bracon hebetor (say) and its impact on parasitoid quality. Bangladesh Journal of Agricultural Research, 41(2), 297–310.

    Article  Google Scholar 

  • Alim, M. A., & Lim, U. T. (2009). Refrigeration of Riptortus clavatus (Hemiptera: Alydidae) eggs for the parasitization by Gryon japonicum (Hymenoptera: Scelionidae). Biocontrol Science and Technology, 19, 315–325.

    Article  Google Scholar 

  • Alim, M. A., & Lim, U. T. (2010). Biological attributes of Ooencyrtus nezarae Ishii (Hymenoptera: Encyrtidae) reared on refrigerated eggs of Riptortus pedestris (=clavatus) Fabricius (Hemiptera: Alydidae). Asia Pacific Entomologist, 13, 139–143.

    Article  Google Scholar 

  • Almeida, M. A., Geden, C. J., & Prado, A. P. (2002). Influence of feeding treatment, host density, temperature and cold storage on attack rates of Tachinaephagus zealandicus Ashmead (Hymenoptera: Encyrtidae). Environmental Entomology, 31(4), 732–738.

    Article  Google Scholar 

  • Al-Tememi, N. K., & Ashfaq, M. (2005). Effect of low temperature storage on the fecundity and parasitizing efficacy of Bracon hebetor (say). Journal of Agricultural Research, 43(2), 155–160.

    Google Scholar 

  • Amaral, B. B., Souza, B., Bezerra, C. S. A., Viana de Sousa, A. L., & Carvalho, C. F. (2013). Storing eggs of Chrysoperla externa (Hagen, 1861) (Neuroptera: Chrysopidae) for management of large-scale rearing. Acoreana, 9, 103–109.

    Google Scholar 

  • Amice, G., Vernon, P., Outreman, Y., van Alphen, J., & van Baaren, J. (2008). Variability in responses to thermal stress in parasitoids. Ecological Entomology, 33, 701–708.

    Google Scholar 

  • Andersen, J. L., Manenti, T., Sorensen, J. G., MacMillan, H. A., Loeschcke, V., & Overgaard, J. (2015). How to assess Drosophila cold tolerance: Chill coma temperature and lower lethal temperature are the best predictors of cold distribution limits. Functional Ecology, 29, 55–65.

    Article  Google Scholar 

  • Anguilletta, M. J. (2009). Thermal adaptation: A theoretical and empirical synthesis. Oxford: Oxford University Press.

    Book  Google Scholar 

  • Anwar, M., ul-Abdin, Z., Abbas, S. K., Tahir, M., Hussain, F., & Manzoor, A. (2016). Effect of cold storage on the survival, sex ratio and longevity of ectoparasitoid, Bracon hebetor (Say) (Hymenoptera: Braconidae). Pakistan Journal of Zoology, 48(6), 1775–1780.

    Google Scholar 

  • Archer, T. L., Murray, C. L., Eikenbary, R. D., Starks, K. J., & Morrison, R. D. (1973). Cold storage of Lysiphlebus testaceipes mummies. Environmental Entomology, 2(6), 1104–1108.

    Article  Google Scholar 

  • Archer, T. L., Bogart, R. K., & Eikenbary, R. D. (1976). The influence of cold storage on the survival and reproduction by Aphelinus asychis adults. Environmental Entomology, 5(4), 623–625.

    Article  Google Scholar 

  • Awad, M., Kalushkov, P., Nedvedova, T. and Nedved, O. (2013). Fecundity and fertility of ladybird beetle Harmonia axyridis after prolonged cold storage BioControl, 58: 657–666.

    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). Journal of Stored Products and Research, 44, 232–240.

    Article  Google Scholar 

  • Ballal, C., Singh, S., Jalali, S., & Kumar, P. (1989). Cold tolerance of cocoons of Allorhogas pyralophagus (Hymenoptera: Braconidae). BioControl, 34(1), 463–468.

    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). Biological Control, 35, 68–77.

    Article  Google Scholar 

  • Benelli, M., Marchetti, E., & Dindo, M. L. (2017). Effects of storage at suboptimal temperatures on the in vitro-reared parasitoid Exorista larvarum (Diptera: Tachinidae). Journal of Economic Entomology, 110(4), 1476–1482.

    Article  CAS  PubMed  Google Scholar 

  • Bernardo, U., Iodice, L., Sasso, R., & Pedata, P. A. (2008). Effects of cold storage on Thripobius javae (=T. semiluteus) (Hymenoptera: Eulophidae). Biocontrol Science and Technology, 18, 921–933.

    Article  Google Scholar 

  • Bhargavi, M., & Naik, K. V. (2015). Effect of low temperature storage of trichocards parasitized by Trichogramma chilonis (Ishii) and Trichogramma japonicum (Ashmead). Asian Journal of Bio Science, 10(1), 43–47.

    Article  Google Scholar 

  • Binazzi, F., Peverieri, G. S., Benassai, D., & Roversi, P. F. (2015). The effects of short-term cold storage on the survival of the endoparasitoid Ooencyrtus pityocampae Mercet (Hymenoptera: Encyrtidae). Redia, 98, 31–36.

    Google Scholar 

  • Bourdais, D., Vernon, P., Krespi, L., le Lannic, J., & van Baaren, J. (2006). Antennal structure of male and female Aphidius rhopalosiphi De Stefani Perez (Hymenoptera: Braconidae): Description and morphological alterations after cold storage or heat exposure. Microscopic Research Technology, 69, 1005–1013.

    Article  Google Scholar 

  • Bourdais, D., Vernon, P., Krespi, L., & van Baaren, J. (2012). Behavioural consequences of cold exposure on males and females of Aphidius rhopalosiphi De Stephani Perez (Hymenoptera: Braconidae). BioControl, 57, 349–360.

    Article  Google Scholar 

  • Bueno, J. R., & van Cleave, H. W. (1997). The effect of cold storage on the emergence of Aphelinus perpallidus, a parasitoid of Monellia caryella. Southwestern Entomologist, 22(1), 39–51.

    Google Scholar 

  • Bueno, V. H. P., Carvalho, L. M., & van Lenteren, J. C. (2014). Performance of Orius insidiosus after storage, exposure to dispersal material, handling and shipment processes. Bulletin of Insectology, 67(2), 175–183.

    Google Scholar 

  • Cagnotti, C. L., Lois, M., Lopez, S. N., Botto, N. E., & Viscarret, M. A. (2018). Cold storage of Trichogramma nerudai using an acclimation period. BioControl. https://doi.org/10.1007/s10526-018-9885-5.

    Article  Google Scholar 

  • Carriere, Y., & Boivin, G. (2001). Constraints on the evolution of thermal sensitivity of foraging in Trichogramma: Genetic trade-offs and plasticity in maternal selection. The American Naturalist, 157, 570–581.

    Article  CAS  PubMed  Google Scholar 

  • Chang, Y. F., Tauber, M. J., Tauber, C. A., & Nyrop, J. P. (2003). Interpopulation variation in Chrysoperla carnea reproduction: Implications for mass rearing and storage. Entomologia Experimentalis et Applicata, 95, 293–302.

    Article  Google Scholar 

  • Chapman, R. F. (1982). The insects. Structure and function, 3rd Ed (p. 770). Cambridge: Harvard University Press.

    Google Scholar 

  • Chen, W. L., & Leopold, R. A. (2007). Progeny quality of Gonatocerus ashmeadi (Hymenoptera: Mymaridae) reared on stored eggs of Homalodisca coagulate (Hemiptera: Cicadellidae). Economic Entomology, 100, 685–694.

    Article  Google Scholar 

  • Chen, C. P., Delinger, D. L., & Lee, R. E. (1987). Cold-shock injury and cold rapid hardening in the flesh fly, Sarcophaga crassipalpis. Physiological Zoology, 60, 297–304.

    Article  Google Scholar 

  • Chen, W. L., Leopold, R. A., & Boetel, M. A. (2008a). Cold storage of adult Gonatocerus ashmeadi (Hymenoptera: Mymaridae) and effects on maternal and progeny fitness. Journal of Economic Entomology, 101, 1760–1770.

    Article  PubMed  Google Scholar 

  • Chen, W. L., Leopold, R. A., & Harris, M. O. (2008b). Cold storage effects on maternal and progeny quality of Gonatocerus ashmeadi (Hymenoptera: Mymaridae). Biological Control, 46, 122–132.

    Article  Google Scholar 

  • Chen, Q., Peng, Z., Xu, C., Tang, C., Lu, B., Jin, Q., Wen, H., & Wan, F. (2010). Biological assessment of Tetrastichus brontispae, a pupal parasitoid of coconut leaf beetle Brontispa longissima. Biocontrol Science and Technology, 20, 283–295.

    Article  CAS  Google Scholar 

  • Chen, H., Opitb, G. P., Shenga, P., & Zhang, H. (2011). Maternal and progeny quality of Habrobracon hebetor say (Hymenoptera: Braconidae) after cold storage. Biological Control, 58(3), 255–261.

    Article  Google Scholar 

  • Chen, H., Zhang, H., Zhu, K. Y., & Throne, J. (2013). Performance of diapausing parasitoid wasps, Habrobracon hebetor after cold storage. Biological Control, 64(3), 186–194.

    Article  Google Scholar 

  • Chong, J. H., & Oetting, R. D. (2006). Influence of temperature, nourishment and storage period on the longevity and fecundity of the mealybug parasitoid Anagyrus sp. nov. nr. sinope Noyes and Menezes (Hymenoptera: Encyrtidae). Environmental Entomology, 35(5), 1198–1207.

    Article  Google Scholar 

  • Chown, S. L., & Nicolson, S. W. (2004). Insect physiological ecology: Mechanisms and patterns. Oxford: Oxford University Press.

    Book  Google Scholar 

  • Chown, S. L., & Terblanche, J. S. (2006). Physiological diversity in insects: Ecological and evolutionary contexts. Advances in Insect Physiology, 33, 50–152.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cingolani, M. F., Greco, N. M., & Liljesthrom, G. G. (2015). Cold-storage of Piezodorus guildinii (Hemiptera: Pentatomidae) eggs for rearing Telenomus podisi (Hymenoptera: Platygastridae). Journal of Agriculture Science and Technology, 17, 1507–1516.

    Google Scholar 

  • Colinet, H. (2007). An ecological and biochemical approach to cold resistance in an aphid parasitoid Aphidius colemani (Hymenoptera: Aphidiiinae). Ph.D. Thesis, University Catholic of Louvain, Louvain-la-Neuve.

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

    Article  Google Scholar 

  • Colinet, H., & Hance, T. (2009). Male reproductive potential of Aphidius colemani (Hymenoptera: Aphidiinae) exposed to constant or fluctuating thermal regimes. Environmental Entomology, 38, 242–249.

    Article  CAS  PubMed  Google Scholar 

  • Colinet, H., & Hance, T. (2010). Inter-specific variation in the response to low temperature storage in different aphid parasitoids. Annals of Applied Biology, 156, 147–156.

    Article  Google Scholar 

  • Colinet, H., Renault, D., Hance, T., & Vernon, P. (2006). The impact of fluctuating thermal regimes on the survival of a cold-exposed parasitic wasp, Aphidius colemani. Physiological Entomology, 31, 234–240.

    Article  Google Scholar 

  • Colinet, H., Vernon, P., & Hance, T. (2007). Does thermal-related plasticity in size and fat reserves influence supercooling abilities and cold-tolerance in Aphidius colemani (Hymenoptera: Aphidiinae) mummies? Journal of Thermal Biology, 32, 374–382.

    Article  Google Scholar 

  • Correa-Ferreira, B. S., & Moscardi, F. (1993). Storage techniques of stink bug eggs for laboratory production of the parasitoid Trissolcus basalis (Wollaston). Pesquisa Agropecuaria Brasileira, 28, 1247–1253.

    Google Scholar 

  • Costa, V. H. D., Soares, M. A., Junior, S. L., Silveira, R. D., Reis, T. C., & Pires, E. M. (2016). Egg storage of Podisus nigrispinus (Hemiptera: Pentatomidae) predators at low temperatures. Revista Arvore, 40(5), 877–884.

    Article  Google Scholar 

  • Coudron, T. A., Ellersieck, M. R., & Shelby, K. S. (2007). Influence of diet on long-term cold storage of the predator Podisus maculiventris (say) (Heteroptera: Pentatomidae). Biological Control, 42, 186–195.

    Article  Google Scholar 

  • Couillien, D., & Gregoire, J. C. (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 

  • Daane, K. M., Wang, X., Johnson, M. W., & Cooper, M. L. (2013). Low temperature storage effects on two olive fruit fly parasitoids. BioControl, 58, 175–185.

    Article  CAS  Google Scholar 

  • Danks, H. V. (1987). Insect dormancy: An ecological perspective. Ottawa: Biological Survey of Canada.

    Google Scholar 

  • Danks, H. V. (2002). The range of insect dormancy responses. European Journal of Entomology, 99, 127–142.

    Article  Google Scholar 

  • Daval, S. K. (2014). Biology, storage studies and toxicity of insecticides to Crysoperla zastrowi arabica (Henry) under laboratory conditions. MSc. (Agri.) Thesis Dr. Balasaheb Sawant Konkan Krishi Vidyapeeth, Dapoli. 66 pp.

  • David, J. R., Araripe, L. O., Chakir, M., Legout, H., Lemos, B., Petavy, G., Rohmer, C., Joly, D., & Moreteau, B. (2005). Male sterility at extreme temperatures: A significant but neglected phenomenon for understanding Drosophila climatic adaptations. Journal of Evolutionary Biology, 18, 838–846.

    Article  CAS  PubMed  Google Scholar 

  • De Bach, P. (1943). The effect of low storage temperature on reproduction in certain parasitic Hymenoptera. Pan-Pacific Entomologist, 19, 112–119.

    Google Scholar 

  • De Clercq, P., & Degheele, S. (1993). Cold storage of the predatory bugs Podisus maculiventris (say) and Podisus sagitta (Fabricius) (Heteroptera: Pentatomidae). Parasitica, 49(1–2), 27–41.

    Google Scholar 

  • Deng, D. A. (1982). Experiments on feeding with artificial diets and cold storage of Harmonia axyridis Pallas. Insect Knowledge, 19, 11–12.

    Google Scholar 

  • Denlinger, D. L., & Lee, R. E. (1998). Physiology of cold sensitivity. In G. J. Hallman & D. L. Denlinger (Eds.), Temperature sensitivity in insects and application in integrated Pest management (pp. 55–96). Boulder: Westview Press.

    Google Scholar 

  • Dileep, R. C. (2012). Performance of egg parasitoid Trichogramma chilonis (Ishii) under laboratory conditions. M.Sc. Thesis, Dr. Balasaheb Sawant Konkan Krishi Vidyapeeth, College of Agriculture, Dapoli, Ratnagiri (p. 157). India: Maharashtra.

    Google Scholar 

  • Dindo, M. L., & Grenier, S. (2014). Production of dipteran parasitoids. In J. A. Morales-Ramos, M. G. Guadalupe Rojas, & D. I. Shapiro-Ilan (Eds.), Mass production of beneficial organisms: Invertebrates and entomopathogens. Academic press (pp. 101–143). London: United Kingdom.

    Chapter  Google Scholar 

  • Dutton, A., & Bigler, F. (1995). Flight activity assessment of the egg parasitoid Trichogramma brassicae (Hym.: Trichogrammatidae) in laboratory and field conditions. Entomophaga, 40, 223–233.

    Article  Google Scholar 

  • Easwaramoorthy, S., Kurup, N. K., Santhalakshmi, G., & Shanmugasundaram, M. (2000). Effect of low temperature storage on the viability of puparia of Sturmiopsis inferens Townsend (Diptera: Tachinidae) a larval parasitoid of sugarcane moth borers. Journal of Biological Control, 14(1), 63–65.

    Google Scholar 

  • Ferran, A. (1983). On some co-physiological characteristics of predation at Semiadalia undecimnotata Schn. (Coleoptera: Coccinellidae). Ph.D. Thesis (p. 158). France: University of Toulouse.

    Google Scholar 

  • Flanders, S. E. (1938). The effect of cold storage on reproduction of parasitic Hymenoptera. Journal of Economic Entomology, 31, 633–634.

    Google Scholar 

  • Flanders, S. E. (1956). The mechanism of sex-ratio regulation in the parasitic Hymenoptera. Social Insects, 3, 325–334.

    Article  Google Scholar 

  • Foerster, L. A., & Doetzer, A. K. (2006). Cold storage of the egg parasitoids Trissolcus basalis (Wollaston) and Telenomus podisi Ashmead (Hymenoptera: Scelionidae). Biological Control, 36, 232–237.

    Article  Google Scholar 

  • Foerster, L. A., Doetzer, A. K., & de Castro, L. C. F. (2004). Emergence, longevity and fecundity of Trissolcus basalis and Telenomus podisi after cold storage in the pupal stage. Pesquisa Agropecuaria Brasileira, 39(9), 841–845.

    Article  Google Scholar 

  • Forouzan, F., Jalali, M. A., Ziaaddini, M., & Rad, H. H. (2018). Effect of cold storage on biological traits of Psix saccharicola (Hymenoptera: Platygastridae), an egg parasitoid of Acrosternum arabicum (Hemiptera: Pentatomidae). Journal of Economic Entomology. https://doi.org/10.1093/jee/toy087.

    Article  PubMed  Google Scholar 

  • Frere, I., Balthazar, C., Sabri, A., & Hance, T. (2011). Improvement in the cold storage of Aphidius ervi (Hymenoptera: Aphidiinae). European Journal of Environmental Sciences, 1(1), 33–40.

    Article  Google Scholar 

  • Fusco, R. A., Rhoads, L. D., & Blumenthal, M. (1978). Compsilura concinnata: Effect of temperature on laboratory propagation. Environmental Entomology, 7, 5–18.

    Article  Google Scholar 

  • Gagne, I., & Coderre, D. (2001). Cold storage of Coleomegilla maculata larvae. Biocontrol Science and Technology, 11, 361–369.

    Article  Google Scholar 

  • Garcia, V. P., Wajnberg, E., Pizzol, J. M. L., & Oliveira, M. (2002). Diapause in the egg parasitoid Trichogramma cordubensis: Role of temperature. Journal of Insect Physiology, 48, 349–355.

    Article  Google Scholar 

  • Gardner, J., Hoffmann, M. P., Pitcher, S. A., & Nyrop, J. P. (2012). Recurrent warming to improve cold storage of Trichogrammatids (Hymenoptera: Trichogrammatidae). Biocontrol Science and Technology, 22(3), 261–270.

    Article  Google Scholar 

  • Gautam, R. D. (1986). Effect of cold storage on the adult parasitoid Telenomus remus Nixon (Scelionidae: Hymenoptera) and the parasitized eggs of Spodoptera litura (Fabr.) (Noctuidae: Lepidoptera). Journal of Entomological Research, 10, 125–131.

    Google Scholar 

  • Geden, C. J., & Kaufmann, P. E. (2007). Development of Spalangia cameroni and Muscidifurax raptor (Hymenoptera: Pteromalidae) on live house fly (Diptera: Muscidae) pupae and pupae killed by heat shock, irradiation and cold. Environmental Entomology, 36, 34–39.

    Article  CAS  PubMed  Google Scholar 

  • Ghosh, E., & Ballal, C. R. (2018). Short-term storage of the egg parasitoids, Trichogramma and Trichogrammatoidea. Egyptian Journal of Biological Pest Control, 28(34). https://doi.org/10.1186/s41938-018-0039-y.

  • Gibert, P., Moreteau, B., Petavy, G., Karan, D., & David, J. R. (2001). Chill-coma tolerance, a major climatic adaptation among Drosophila species. Evolution, 55, 1063–1068.

    Article  CAS  PubMed  Google Scholar 

  • Gilkeson, L. A. (1990). Cold storage of the predatory midge Aphidoletes aphidimyza (Diptera: Cecidomyiidae). Journal of Economic Entomology, 83(13), 965–970.

    Article  Google Scholar 

  • Greco, C. F., & 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. Journal of Applied Entomology, 122, 311–314.

    Article  Google Scholar 

  • Gross, H. R., & Johnson, R. (1985). Archytas marmoratus (Diptera: Tachinidae): Advances in large-scale rearing and associated biological studies. Journal of Economic Entomology, 78, 1350–1353.

    Article  Google Scholar 

  • Gupta, P. R., & Bhardwaj, P. C. (2002). Storage conditions conducive for holding the egg parasitoid, Trichogrammatoidea bactrae Nagaraja. Journal of Biological Control, 16(1), 19–25.

    CAS  Google Scholar 

  • Hackermann, J., Rott, A. S., Tschudi-Rein, K., & Dorn, S. (2008). Cold stored ectoparasitoid of Cydia fruit moths released under different temperature regimes. BioControl, 53, 857–867.

    Article  Google Scholar 

  • Hamalainen, M. (1977). Storing dormant Coccinella septempunctata and Adalia bipunctata (Col.: Coccinellidae) adults in the laboratory. Annales Agriculturae Fenniae, 16, 184–187.

    Google Scholar 

  • Hamalainen, M., & Markkula, M. (1977). Cool storage of Coccinella septempunctata and Adalia bipunctata (Col.: Coccinellidae) eggs for use in the biological control in greenhouses. Annales Agriculturae Fenniae, 16, 132–136.

    Google Scholar 

  • Hance, T., van Baaren, J., Vernon, P., & Boivin, G. (2007). Impact of extreme temperatures on parasitoids in a climate change perspective. Annual Review of Entomology, 52, 107–126.

    Article  CAS  PubMed  Google Scholar 

  • Hanna, A. D. (1935). Fertility and tolerance of low temperature in Euchalcidia carybori Hanna (Hymenoptera: Chalcidinae). Bulletin of Entomological Research, 26, 315–322.

    Article  Google Scholar 

  • Harvey, J. A., Cloutier, J., Visser, B., Ellers, J., Wackers, F. L., & Gols, R. (2012). The effect of different dietary sugars and honey on longevity and fecundity in two hyperparasitoid wasps. Journal of Insect Physiology, 58, 816–823.

    Article  CAS  PubMed  Google Scholar 

  • Hassan, S. A., Beyer, H., Dannemann, K., Heil, M., Pfister, J., Reichel, W. and Winstel, K. (1990). Mass breeding and application of Trichogramma: Results of inter laboratory tests for the control of the corn sucker (Ostrinia nubilalis). In: Conference on Plant health for sustainable agriculture, 11–12 May, 2015, Ljubljana, Slovenia. pp. 387-394.

  • Hazell, S. P., & Bale, J. S. (2011). Low temperature thresholds: Are chill coma and CT (min) synonymous? Journal of Insect Physiology, 57, 1085–1089.

    Article  CAS  PubMed  Google Scholar 

  • Herard, F., Keller, M. A., Lewis, W. J., & Tumlinson, J. H. (1988). Beneficial arthropod behavior mediated by airborne semiochemicals. III. Influence of age and experience on flight chamber responses of Microplitis demolitor Wilkinson. Journal of Chemical Ecology, 14, 1553–1596.

    Google Scholar 

  • Hodkova, M., & Hodek, I. (2004). Photoperiod, diapause and cold-hardiness. European Journal of Entomology, 101, 445–458.

    Article  Google Scholar 

  • Hoffmann, A. A., Sorensen, J. G., & Loeschcke, V. (2003). Adaptation of Drosophila to temperature extremes: Bringing together quantitative and molecular approaches. Journal of Thermal Biology, 28, 175–216.

    Article  Google Scholar 

  • Hofsvang, T., & Hagvar, E. B. (1977). Cold storage tolerance and supercooling points of mummies of Ephedrus cerasicola Stary and Aphidius colemani Viereck (Hymenoptera: Aphidiidae). Norwegian Journal of Entomology, 24, 1–6.

    Google Scholar 

  • Ismail, M., Vernon, P., Hance, T., & van Baaren, J. (2010). Physiological costs of cold exposure on the parasitoid Aphidius ervi without selection pressure and under constant or fluctuating temperatures. BioControl, 55, 729–740.

    Article  Google Scholar 

  • Ismail, M., Vernon, P., Hance, T., Pierre, J. S., & van Baaren, J. (2012). What are the possible benefits of small size for energy-constrained ectotherms in cold stress conditions? Oikos, 121, 2072–2080.

    Article  Google Scholar 

  • Ismail, M., van Baaren, J., Hance, T., Pierre, J., & Vernon, P. (2013). Stress intensity and fitness in the parasitoid Aphidius ervi (Hymenoptera: Braconidae): Temperature below the development threshold combined with a fluctuating thermal regime is a must. Ecological Entomology, 38, 355–363.

    Article  Google Scholar 

  • Jackson, C. G. (1986). Effects of cold storage of adult Anaphes ovijentatus on survival, longevity and ovipostion. Southwestern Entomologist, 11(3), 149–153.

    Google Scholar 

  • Jalali, S. K., & Singh, S. P. (1992). Differential response of four Trichogramma species to low temperatures for short-term storage. Entomophaga, 37(1), 159–165.

    Article  Google Scholar 

  • Jalali, S. K., Singh, S. P., Ballal, C. R., & Kumar, P. (1990). Response of Cotesia marginiventris (Hymenoptera: Braconidae) to low temperature in relation to its biological potential. Entomon, 15(3), 217–220.

    Google Scholar 

  • Jayanth, K. P., & Nagarkatti, S. (1985). Low temperature storage of adults of Bracon brevicornis Wesmael (Hymenoptera: Braconidae). Entomon, 10, 39–41.

    Google Scholar 

  • Khosa, S. S., & Brar, K. S. (2000). Effect of storage on the emergence and parasitization efficiency of laboratory reared and field collected populations of Trichogramma chilonis Ishii. Journal of Biological Control, 14(2), 71–74.

    Google Scholar 

  • Kidane, D., Yang, N. W., & Wan, F. H. (2015). Effect of cold storage on the biological fitness of Encarsia sophia (Hymenoptera: Aphelinidae), a parasitoid of Bemisia tabaci (Hemiptera: Aleyrodidae). European Journal of Entomology, 112(3), 460–469.

    Article  Google Scholar 

  • 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 

  • Knight, J. D., Bale, J. S., Franks, F., Mathias, S. F., & Baust, J. G. (1986). Insect cold hardiness supercooling points and pre-freeze mortality. Cryo Letters, 7, 192–203.

    Google Scholar 

  • Kostal, V., Vambera, J., & Bastl, J. (2004). On the nature of pre-freeze mortality in insects: Water balance, ion homeostasis and energy charge in the adults of Pyrrhocoris apterus. Journal of Experimental Biology, 207(9), 1509–1521.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, P., Shenhmar, M., & Brar, K. S. (2005). Effect of low temperature storage on the efficiency of three species of trichogrammatids. Journal of Biological Control, 19, 17–21.

    Google Scholar 

  • Lacoume, S., Bressac, C., & Chevrier, C. (2007). Sperm production and mating potential of males after a cold shock on pupae of the parasitoid wasp Dinarmus basalis (Hymenoptera: Pteromalidae). Journal of Insect Physiology, 53, 1008–1015.

    Article  CAS  PubMed  Google Scholar 

  • Ladurantaye, Y., Khelifi, M., Cloutier, C., & Coudron, T. A. (2010). Short-term sorage conditions for transport and farm delivery of the stink bug Perillus bioculatus for the biological control of the Colorado potato beetle. Canadian Biosystems Engineering, 52, 1–7.

    Google Scholar 

  • Larentzaki, E., Powell, G., & Copland, M. J. W. (2007). Effect of cold storage on survival, reproduction and development of adults and eggs of Franklinothrips vespiformis (Crawford). Biological Control, 43(3), 265–270.

    Article  Google Scholar 

  • Larios, G. B., Sivinski, J., Holler, T., & Aluja, M. (2002). The effects of chilling on the fecundity and life span of mass-reared parasitoids (Hymenoptera: Braconidae) of the Mediterra-nean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Biocontrol Science and Technology, 12, 205–215.

    Article  Google Scholar 

  • Lee, R. E., & Denlinger, D. L. (2010). Rapid cold hardening: Ecological significance and under pinning mechanisms. In D. L. Denlinger & R. E. Lee (Eds.), Low temperature biology of insects (pp. 35–58). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Legrand, M. A. (2005). Overwintering strategies of the parasitoid Aphidius rhopalosiphi De Stefani Perez (Hymenoptera: Aphidiiinae). Ph.D. Thesis, Catholic University of Louvain, Louvain-la-neuve.

  • Legrand, M. A., Salin, C., Langer, A., & Hance, T. (2004). Are mummy characteristics reliable indicators of diapause and cold tolerance in the parasitoid wasp Aphidius rhopalosiphi (Braconidae: Aphidiinae). Cryo Letters, 25, 161–166.

    CAS  PubMed  Google Scholar 

  • Leopold, R. A. (1998). Cold storage of insects for integrated pest management. In G. J. Hallman & D. L. Denlinger (Eds.), Temperature sensitivity in insects and application in integrated Pest management (pp. 235–267). Boulder: Westview Press.

    Google Scholar 

  • Leopold, R. A. (2007). Colony maintenance and mass rearing: Using cold storage technology for extending the shelf life of insects. In M. J. B. Vreysen, A. S. Robinson, & J. Hendrichs (Eds.), Area-wide control of insect pests (pp. 149–162). Netherlands: Springer.

    Chapter  Google Scholar 

  • Leppla, N. C., Bloem, K. A. and Luck, R. F. (2002). Quality control for mass-reared arthropods. In: Proceedings of the eighth and ninth workshops IOBC working group on quality control of mass-reared arthropods. University of Florida, USA.

  • Levie, A., Vernon, P., & Hance, T. (2005). Consequences of acclimation on survival and reproductive capacities of cold-stored mummies of Aphidius rhopalosiphi (Hymenoptera: Aphidiinae). Journal of Economic Entomology, 98, 704–708.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y., Zhang, L., Zhang, Q., Chen, H., & Denlinger, D. L. (2014). Host diapauses status and host diets augmented with cryoprotectants enhance cold hardiness in the parasitoid Nasonia vitripennis. Journal of Insect Physiology, 70, 8–14.

    Article  CAS  PubMed  Google Scholar 

  • Lins, J. C., Paesbueno, V. H., Sidney, L. A., Silva, D. B., Sampaio, M. V., Pereira, J. M., Schroden, Q. S., & van Lenteren, J. C. (2013). Cold storage affects mortality, body mass, lifespan, reproduction and flight capacity of Praon volucre (Hymenoptera: Braconidae). European Journal of Entomology, 110(2), 263–270.

    Article  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 (Coleptera: Chrysomelidae). Journal of Insect Science, 14(1), 257–262.

    PubMed  PubMed Central  Google Scholar 

  • Lopez, S. N., & Botto, E. (2005). Effect of cold storage on some biological parameters of Eretmocerus corni and Encarsia formosa (Hymenoptera: Aphelinidae). Biological Control, 33, 123–130.

    Article  Google Scholar 

  • Lopez-Arroyo, J. I., Tauber, C. A., & Tauber, M. J. (2000). Storage of lacewing eggs: Post-storage hatching and quality of subsequent larvae and adults. Biological Control, 18, 165–171.

    Article  Google Scholar 

  • Luczynski, A., Nyrop, J. P., & Shi, A. (2007). Influence of cold storage on pupal development and mortality during storage and on post-storage performance of Encarsia formosa and Eretmocerus eremicus (Hymenoptera: Aphelinidae). Biological Control, 40, 107–117.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • MacMillan, H. A., & Sinclair, B. J. (2011). Mechanisms underlying insect chill-coma. Journal of Insect Physiology, 57, 12–20.

    Article  CAS  PubMed  Google Scholar 

  • Mahi, H., Rasekh, A., & Shisehbor, P. (2017). The impact of cold storage on mating behavior of emerging adults and progeny fitness, in a parasitoid wasp, Lysiphlebus fabarum, under constant and fluctuating temperatures. Applied Entomology and Phytopathology, 85(1), 1–10.

    Google Scholar 

  • Mahmoud, A. M. A., & Lim, U. T. (2007). Evaluation of cold-stored eggs of Dolycoris baccarum (Hemiptera: Pentatomidae) for parasitization by Trissolcus nigripedius (Hymenoptera: Scelionidae). Biological Control, 43, 287–293.

    Article  Google Scholar 

  • Mainali, B. P., & Lim, U. T. (2013). Quality assessment of Riptortus pedestris (Hemiptera: Alydidae) eggs cold-stored at different temperature and relative humidity regime. Biological Control, 64, 132–137.

    Article  Google Scholar 

  • Manjoo, S., & Bajpai, N. K. (2012). Effect of storage at different temperatures on the biological parameters of Cotesia flavipes Cameron. Journal of Biological Control, 26(2), 157–161.

    Google Scholar 

  • Mansour, A. N. (2017). Influence of cold storage on some biological aspects of the gregarious parasitoid, Bracon hebetor (say) (Hymenoptera: Braconidae). Egyptian Journal of Biological Pest Control, 27(2), 205–210.

    Google Scholar 

  • Marwan, I. A., & Tawfiq, M. M. (2006). Response of Aphidius matricariae Haliday (Hymenoptera: Aphidiidae) from mummified Myzus persicae Sulzer (Homoptera: Aphididae) to short term cold storage. International Pest Control, 48, 262–265.

    Google Scholar 

  • McDonald, R. C., & Kok, L. T. (1990). Post refrigeration viability of Pteromalus puparum (Hymenoptera: Pteromalidae) prepupae within host chrysalids. Journal of Entomological Science, 25, 409–413.

    Article  Google Scholar 

  • Michel, C. (2007). General study of the impact of cold on survival and the morphology of the reproductive system of Aphidius ervi (Hymenoptera: Aphidiinae). Thesis dissertation, University Catholic of Louvain, Louvain-la-Neuve.

  • Miller, J. C. (1995). A comparison of techniques for laboratory propagation of a south American ladybeetle, Eriopis connexa (Coleoptera: Coccinellidae). Biological Control, 5, 462–465.

    Article  Google Scholar 

  • Mills, N. J., & Nealis, V. G. (1992). European field collections and Canadian releases of Ceranthia samarensis (Dipt.: Tachinidae), a parasitoid of the gypsy moth. Entomophaga, 37, 181–191.

    Article  Google Scholar 

  • Morales-Ramos, J. A., Guadalupe Rojas, M., & Shapiro-Ilan, D. I. (2014). Mass production of beneficial organisms: Invertebrates and entomopathogens. London: Academic Press.

    Google Scholar 

  • Muhammad, R., Ahmad, Q., Rashidi, S. M. M., & Ahmad, N. (2013). Role of irradiated and chilled host Sitotroga cerealella eggs to enhance the parasitic potential of egg parasitoid Trichogramma chilonis (Ishii). Academic Journal of Entomology, 6(3), 133–138.

    Google Scholar 

  • Nadeem, S. (2010). Improvement in production and storage of Trichogramma chilonis (Ishii), Chrysoperla carnea (Stephens) and their hosts for effective field releases against major insect pests of cotton. M.Sc. Thesis University of Agriculture, Faisalabad. pp. 187.

  • Nadeem, S., Ashfaq, M., Hamed, M., & Ahmed, S. (2010). Optimization of short and long term storage duration for Trichogramma chilonis (Ishii) (Hymenoptera: Trichogrammatidae) at low temperatures. Pakistan Journal of Zoology, 42, 63–67.

    Google Scholar 

  • Nadeem, S., Hamed, M., Nadeem, M. K., & Hasnain, M. (2014). Effect of storage duration and low temperatures on reproductive characteristics of Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). Pakistan Journal of Zoology, 46(1), 31–35.

    Google Scholar 

  • Nahiyoon, S. A., Bukero, A., Lanjar, A. G., Solangi, A. W., Nahiyoon, R. H., & Chandio, W. A. (2016). Effect of five lowest temperatures on the storage of pupal parasitoid, Dirhinus giffardii. Science International (Lahore), 28(5), 4759–4762.

    Google Scholar 

  • Nakama, P. A., & Foerster, L. S. A. (2001). Effect of alternating temperatures on development and emergence of Trissolcus basalis (Wollaston) and Telenomus podisi Ashmead (Hymenoptera: Scelionidae). Neotropical Entomology, 30, 269–275.

    Article  Google Scholar 

  • Navarro, M. A. 1998. Trichogramma spp. production, use and management in Colombia. Impretec, Guadalajara de Buga. 176 p.

  • Okine, J. S., Mitchell, E. R., & Hu, G. Y. (1996). Low temperature effect on viability of Diadegma insulare (Hymenoptera: Ichneumonidae) pupae and effect of this parasitoid on feeding rate of diamondback moth larvae (Lepidoptera: Plutellidae). Florida Entomologist, 79(4), 503–509.

    Article  Google Scholar 

  • Oliveira, L., Melo, R., & Tavares, J. (1998). Response of Glyptapanteles militaris (Walsh) (Hymenoptera: Braconidae), a larval parasitoid of the armyworm, Mythimna unipuncta (Haworth) (Lepidoptera: Noctuidae), to different temperatures. Journal of Hymenopteran Research, 7(2), 268–273.

    Google Scholar 

  • Osman, M. Z., & Selman, B. J. (1993). Storage of Chrysoperla carnea Steph. (Neuroptera: Chrysopidae) eggs and pupae. Journal of Applied Entomology, 115, 420–424.

    Article  Google Scholar 

  • Ozder, N. (2004). Effect of different cold storage periods on parasitization performance of Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae) on eggs of Ephestia kuehniella (Lepidoptera: Pyralidae). Biocontrol Science and Technology, 14(5), 441–447.

    Article  Google Scholar 

  • Ozder, N. (2008). Effect of cold storage of adult Trichogramma brassicae, T. cacoeciae and T. evanescens (Hymenoptera: Trichogrammatidae). Archives of Phytopathology and Plant Protection, 41(4), 296–299.

    Article  Google Scholar 

  • Ozder, N., & Saglam, O. (2004). Effect of short term cold storage on the quality of Trichogramma brassicae, T. cacoeciae and T. evanescens (Hymenoptera: Trichogrammatidae). The Great Lakes Entomologist, 37(3–4), 183–187.

    Google Scholar 

  • Ozgokce, M. S., Atlihan, R., & Karaca, I. (2006). The life table of Cryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae) after different storage periods. Journal of Food Agriculture and Environment, 4(1), 282–287.

    Google Scholar 

  • Pandey, R. R. (2002). Mass production of Anagyrus ananatis Gahan (Hymenoptera: Encyrtidae) for the augmentative biological control of pink pineapple mealybug Dysmicoccus brevipes (Cockerell) (Hemiptera: Pseudococcidae). Ph.D. Thesis submitted to University of Hawaii. 278 pp.

  • Pandey, R. R., & Johnson, M. W. (2005). Effects of cool storage on Anagyrus ananatis Gahan (Hymenoptera: Encyrtidae). Biological Control, 35, 9–16.

    Article  Google Scholar 

  • Perdomo, J. M., Caicedo, D. R. and Rincon, F. C. (2017). Effect of different temperatures and cold storage on pupae of Apanteles gelechiidivoris Marsh (Hymenoptera: Braconidae), parasitoid of Tuta absoluta Meyrick (Lepidoptera: Gelechiidae). In: 19th International Conference on Agricultural, Biotechnology, Biological and Biosystems Engineering, July 17–18, 2017, held at Rome, Italy. International Journal of Agricultural and Biosystems Engineering, 11(7): 24mmat.org/abstracts/59160.

  • Pereira, F. F., Zanuncio, J. C., Serrao, J. E., Pastori, P. L., & Ramalho, F. S. (2009). Reproductive performance of Palmistichus elaeisis Delvare and LaSalle (Hymenoptera: Eulophidae) with previously refrigerated pupae of Bombyx mori L. (Lepidoptera: Bombycidae). Brazilian Journal of Biology, 69, 865–869.

    Article  CAS  Google Scholar 

  • Peres, W. A. A., & Correa-Ferreira, B. S. (2004). Methodology of mass multiplication of Telenomus podisi ash. And Trissolcus basalis (Woll.) (Hymenoptera: Scelionidae) on eggs of Euschistus heros (fab.) (Hemiptera: Pentatomidae). Neotropical Entomology, 33(4), 457–462.

    Article  Google Scholar 

  • Pervez, A., & Omkar, G. A. K. (2006). Ecology and biological control application of multicoloured Asian ladybird, Harmonia axyridis: A review. Biocontrol Science and Technology, 16, 111–128.

    Article  Google Scholar 

  • Peverieri, G. S., Furlan, P., Benassai, D., Strong, W. B., & Roversi, P. F. (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 

  • Pitcher, S. A., Hoffmann, M. P., Gardner, J., Wright, M. G., & Kuhar, T. P. (2002). Cold storage of Trichogramma ostriniae reared on Sitotroga cerealella eggs. BioControl, 47, 525–535.

    Article  Google Scholar 

  • Polgar, L. (1986). Effect of cold storage on the emergence, sex-ratio and fecundity of Aphidius matricariae. In I. Hodek (Ed.), Ecology of Aphidophaga (pp. 255–260). Dordrecht: Netherlands.

    Google Scholar 

  • Prasad, L., & Ansari, I. A. (2000). Effect of cold storage on the survival of Copidosoma varicorne (Nees) (Hymenoptera: Encyrtidae) a parasitoid of Dichomeris eridantis Meyr. (Lepidoptera: Gelechiidae). Indian Forester, 126, 647–652.

    Google Scholar 

  • Press, J. W., & Arbogast, R. T. (1991). Effect of low temperature on survival of immatures of the parasite Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae). Journal of the Kansas Entomological Society, 64(3), 345–348.

    Google Scholar 

  • Queiroz, A. P., Bueno, A. F., Pomari-Fernandes, A., Grande, M. L. M., Bortolotto, O. C., & Silva, D. M. (2016). Low temperature storage of Telenomus remus (Nixon) (Hymenoptera: Platygastridae) and its factitious host Corcyra cephalonica (Stainton) (Lepidoptera: Pyralidae). Neotropical Entomology. https://doi.org/10.1007/s13744-0160442-6.

  • Quezada, J. R., & De Bach, P. (1973). Bioecological and population studies of the cottony-cushion scale, Icerya purchase mask. And its natural enemies, Rodalia cardinalis Mul. And Cryptochaetum iceryae will. In Southern California. Hilgardia, 41, 631–688.

    Article  Google Scholar 

  • Rahimi-Kaldeh, S., Ashouri, A., & Bandani, A. (2017). Long-term storage of sexual and asexual Trichogramma brassicae (Hymenoptera: Trichogrammatidae). Biocontrol Science and Technology, 27(11), 1339–1347.

    Article  Google Scholar 

  • Rathee, M. (2014). Effect of cold storage on some biological characteristics of parasitoid, Aenasius bambawalei Hayat (Hymenoptera: Encyrtidae). M.Sc. Thesis submitted to CCS Haryana Agricultural University (p. 74). India: Hisar.

    Google Scholar 

  • Rathee, M., & Ram, P. (2014). Effect of cold storage of Aenasius bambawalei Hayat (Hymenoptera: Encyrtidae) during pupal stage on its key biological characteristics. Journal of Biological Control, 28(2), 11–17.

    Google Scholar 

  • Rathee, M., & Ram, P. (2016). Mortality of Aenasius bambawalei Hayat following cold storage in mummies of Phenacoccus solenopsis Tinsley. Research in Environment and Life Sciences, 9(10), 1215–1217.

    Google Scholar 

  • Rathee, M., Ram, P., & Mehra, S. (2015). Response of Aenasius bambawalei Hayat (Hymenoptera: Encyrtidae) adults to low temperature storage in relation to key biological parameters. Journal of Biological Control, 29(1), 119–121.

    Article  Google Scholar 

  • Rawat, U. S., Sangal, S. K., & Pawar, A. D. (1992). Development of Chilocorus bijugus Mulsant, a predator of San Jose scale, Quadraspidiotus perniciosus (Comstock) at different levels of temperature and relative humidity. Journal of Insect Science, 5(2), 137–140.

    Google Scholar 

  • Renault, D., Hance, T., Vannier, G., & Vernon, P. (2003). Is body size an influential parameter in determining the duration of survival at low temperatures in Alphitobius diaperinus panzer (Coleoptera: Tenebrionidae)? Journal of Zoology, 259(4), 381–388.

    Article  Google Scholar 

  • Riddick, E. W. (2001). Effect of cold storage on emergence, longevity, fertility, and survival of Cotesia marginiventris (Hymenoptera: Braconidae). Journal of Entomological Science, 36, 366–379.

    Article  Google Scholar 

  • Riddick, E. W., & Wu, Z. (2010). Potential long-term storage of the predatory mite Phytoseiulus persimilis. BioControl, 55, 639–644.

    Article  Google Scholar 

  • Rigaux, M., Vernon, P., & Hance, T. (2000). Relationship between acclimation of Aphidius rhopalosiphi (De Stefani Perez) in autumn and its cold tolerance (Hymenoptera: Braconidae: Aphidiinae). Announcements – Faculty of Agricultural and Applied Biological Sciences, Ghent University, 5, 253–263.

    Google Scholar 

  • Rinehart, J. P., Yocum, G. D., & Denlinger, D. L. (2000). Thermotolerance and rapid cold hardening ameliorate the negative effects of brief exposures to high or low temperatures on fecundity in the flesh fly, Sarcophaga crassipalpis. Physiological Entomology, 25, 330–336.

    Article  Google Scholar 

  • Rossi, M. M. (1993). Bioecological study of parasitoids oophages Trichogramma cacoeciae Marchal and T. evanescens West. (Hym.: Trichogrammatidae) and nymphal parasitoid Dibrachys affinis Masi (Hym.: Pteromalidae) associated with Lobesia botrana Den. and Schiff. (Lepidoptera: Tortricidae). University of Rennes I, U. F. R. Science and Philosophy.

  • Ruan, C., Du, W., Wang, X., Zhang, J., & Zang, L. (2012). Effect of long-term cold storage on the fitness of pre-wintering Harmonia axyridis (Pallas). BioControl, 57, 95–102.

    Article  Google Scholar 

  • Rudolf, E. J., Malausa, C., Millot, P., & Pralavario, R. (1993). Influence of cold temperature on biological characteristics of Orius laevigatus and Orius majusculus (Het.: Anthocoridae). Entomophaga, 38, 317–325.

    Article  Google Scholar 

  • Rundle, B. J., Thomson, L. J., & Hoffmann, A. A. (2004). Effects of cold storage on field and laboratory performance of Trichogramma carverae (Hymenoptera: Trichogrammatidae) and the response of three Trichogramma spp. (T. carverae, T. brassicae and T. funiculatum) to cold. Journal of Economic Entomology, 97, 213–221.

    Article  PubMed  Google Scholar 

  • Sagarra, L. A., Vincent, C., & Stewart, R. K. (2000). Fecundity and survival of Anagyrus kamali Moursi (Hymenoptera: Encyrtidae) under different feeding and storage conditions. European Journal of Entomology, 97, 177–181.

    Article  Google Scholar 

  • Saini, E. (1997). Storage of Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae). Revista de Investigaciones Agropecuarias, 28, 69–72.

    Google Scholar 

  • Sajid, N., Muhammad, A., Muhammad, H., & Sohail, A. (2010). Optimization of short and long term storage duration for Trichogramma chilonis (Ishii) (Hymenoptera: Trichogrammatidae) at low temperatures. Pakistan Journal of Zoology, 42, 63–67.

    Google Scholar 

  • Saleh, A., Allawi, T. F., & Ghabeish, I. (2010). Mass rearing of Neochrysocharis formosa (Westwood) (Eulophidae: Hymenoptera), a parasitoid of leaf miners (Agromyzidae: Diptera). Journal of Pest Science, 83, 59–67.

    Article  Google Scholar 

  • Sandanayaka, W. R. M., Davis, V. A., Chhagan, A., Connolly, P. G., & Charles, J. G. (2015). Influence of cold storage on survival and fitness of Mastrus ridens, an ectoparasitoid of codling moth. New Zealand Plant Protection, 68, 197–203.

    Article  Google Scholar 

  • Schread, J. C., & Garman, P. (1934). Some effects of refrigeration on the biology of Trichogramma in artificial breeding. The Journal of the New York Entomological Society, 42, 268–283.

    Google Scholar 

  • Senal, D., Demirozer, O., & Karaca, I. (2017). Investigation on the storage possibilities of Rhyzobius lophantae Blaisdell (Coleoptera: Coccinellidae) at different temperatures and periods. Phytoparasitica, 45, 175–182.

    Article  Google Scholar 

  • Seyahooei, M. A., Mohammadi-Rad, A., Hesami, S., & Bagheri, A. (2018). Temperature and exposure time in cold storage reshape parasitic performance of Habrobracon hebetor (Hymenoptera: Braconidae). Journal of Economic Entomology. https://doi.org/10.1093/jee/toy004.

    Article  PubMed  Google Scholar 

  • Shands, W. A., & Simpson, G. W. (1972). Insect predators for controlling aphids on potatoes. Spatial distribution of introduced eggs of two species of predators in small fields. Journal of Economic Entomology, 65, 805–809.

    Article  Google Scholar 

  • Shintani, Y., & Ishikawa, Y. (2007). Relationship between rapid cold-hardening and cold acclimation in the eggs of the yellow-spotted longicorn beetle, Psacothea hilaris. Journal of Insect Physiology, 53, 1055–1062.

    Article  CAS  PubMed  Google Scholar 

  • Shreve, S. M., Kelty, J. D., & Lee Jr., R. E. (2004). Preservation of reproductive behaviors during modest cooling: Rapid coldhardening fine-tunes organismal response. Journal of Experimental Biology, 207, 1797–1802.

    Article  PubMed  Google Scholar 

  • Silva, R. J., Cividanes, F. J., Pedroso, E. C., Barbosa, J. C., Matta, D. H., Correia, E. T., & Otuka, A. K. (2013). Effect of low-temperature storage on Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae). Neotropical Entomology, 42, 527–533.

    Article  CAS  PubMed  Google Scholar 

  • Silva, G. V., Bueno, A. F., Favetti, B. M., & Neves, P. M. O. J. (2018). Use of low temperature storage to preserve host and parasitoid to improve the rearing of Telenomus podisi (Hymenoptera: Platygastridae) on Euschistus heros (Hemiptera: Pentatomidae) eggs. Neotropical Entomology https://doi.org/10.1007/s13744-018-0609-4.

  • Sinclair, B. J., Coello Alvarado, L. E., & Ferguson, L. V. (2015). An invitation to measure insect cold tolerance: Methods, approaches, and workflow. Journal of Thermal Biology, 53, 180–197.

    Article  PubMed  Google Scholar 

  • Singh, R., & Srivastava, M. (1988). Effect of cold storage on mummies of Aphis craccivora Koch subjected to different pre-storage temperature on per cent emergence of Trioxys indicus Subba Rao and Sharma. International Journal of Tropical Insect Science, 9(5), 655–657.

    Article  Google Scholar 

  • Singhamuni, S. A. A., Hemachandra, K. S., & Sirisena, U. G. A. I. (2015). Potential for mass rearing of the egg parasitoids, Trichogramma chilonis and Tricogramma achaeae (Hymenoptera: Trichogrammatidae) on Corcyra cephalonica eggs. Tropical Agricultural Research, 27(1), 1–12.

    Article  Google Scholar 

  • Slachta, M., Vambera, J., Zahradnickova, H., & Kostal, V. (2002). Entering diapauses is a prerequisite for successful cold-acclimation in adult Graphosoma lineatum (Heteroptera: Pentatomidae). Journal of Insect Physiology, 48(11), 1031–1039.

    Article  CAS  PubMed  Google Scholar 

  • Storey, K. B., & Storey, J. M. (1988). Freeze tolerance in animals. Physiological Reviews, 68, 27–84.

    Article  CAS  PubMed  Google Scholar 

  • Stray, P. (1971). Storage of Aphidius smithi (Hym., Aphidiidae) for mass-release. Bulletin of the Laboratory of Agricultural Entomology, Filippo Silvestri. Portici., 28, 224–228.

    Google Scholar 

  • Tang, B., Xu, L., & Hou, Y. (2014). Effects of rearing conditions on the parasitism of Tetrastichus brontispae on its pupal host Octodonta nipae. BioControl, 59, 647–657.

    Article  Google Scholar 

  • Tauber, M. J., Tauber, C. A., & Gardescu, S. (1993). Prolonged storage of Chrysoperla carnea (Neuroptera: Chrysopidae). Environmental Entomology, 22, 843–848.

    Article  Google Scholar 

  • Tauber, M. J., Albuquerque, G. S., & Tauber, C. A. (1997a). Storage of non-diapausing Chrysoperla externa adults: Influence on survival and reproduction. Biological Control, 10, 69–72.

    Article  Google Scholar 

  • Tauber, M. J., Tauber, C. A., & Arroyo, J. I. L. (1997b). Life history variation in Chrysoperla carnea implications for rearing and storing a Mexican population. Biological Control, 8, 185–190.

    Article  Google Scholar 

  • Tezze, A. A., & Botto, E. N. (2004). Effect of cold storage on the quality of Trichogramma nerudai (Hymenoptera: Trichogrammatidae). Biological Control, 30, 11–16.

    Article  Google Scholar 

  • Tormos, J., Beitia, F., Alonso, M., Asis, J. D., & Gayubo, S. F. (2010). Assessment of Ceratitis capitata (Diptera, Tephritidae) pupae killed by heat or cold as hosts for rearing Spalangia cameroni (Hymenoptera: Pteromalidae). Annals of Applied Biology, 156(2), 179–185.

    Article  Google Scholar 

  • Tunca, H., Yesil, A. N., & Caliskan, T. F. (2014). Cold storage possibilities of a larval parasitoid, Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae). Turkish Entomology Journal, 38(1), 19–29.

    Article  Google Scholar 

  • Uckan, F., & Ergin, E. (2003). Temperature and food source effects on adult longevity of Apanteles galleriae Wilkinson (Hymenoptera: Braconidae). Environmental Entomology, 32, 441–446.

    Article  Google Scholar 

  • Uckan, F., & Gulel, A. (2001). The effects of cold storage on the adult longevity, fecundity and sex-ratio of Apanteles galleriae Wilkinson (Hymenoptera: Braconidae). Turkish Journal of Zoology, 25, 187–191.

    Google Scholar 

  • van Baaren, J., Outreman, Y., & Boivin, G. (2005). Effect of low temperature exposure on oviposition, behaviour and patch exploitation strategy in parasitic wasps. Animal Behaviour, 70, 153–163.

    Article  Google Scholar 

  • van Lenteren, J. C. (2012). The state of commercial augmentative biological control: Plenty of natural enemies, but a frustrating lack of update. BioControl, 57, 1–20.

    Article  Google Scholar 

  • van Lenteren, J. C., & Tommasini, M. G. (2002). Mass production, storage, shipment and quality control of natural enemies. In R. Albajes, M. L. Gullino, J. C. van Lenteren, & Y. Elad (Eds.), Mass production, storage, shipment and quality control of natural enemies, Integrated Pest and Disease Management in Greenhouse Crops (pp. 276–294). Netherlands: Springer.

    Google Scholar 

  • van Lenteren, J. C., & Tommasini, M. G. (2003). Mass production, storage, shipment and release of natural enemies. In J. C. van Lenteren (Ed.), Quality control and production of biological control agents-theory and testing procedures (pp. 181–189). Oxon: CABI Publishing.

    Chapter  Google Scholar 

  • Venkatesan, T., Singh, S. P., & Jalali, S. K. (2000). Effect of cold storage on cocoons of Goniozus nephantidis Muesebeck (Hymenoptera: Bethylidae) stored for varying periods at different temperature regimes. Journal of Entomological Research, 24, 43–47.

    Google Scholar 

  • Viel, S. R., Carvalho, J. S., Varari, A. M., & Bortoli, S. A. (2008). Pupae storage effect of Cotesia flavipes (Cameron, 1891) (Hymenoptera: Braconidae) in low temperature. Plant Health Bulletin: Pests, 34, 21–26.

    Google Scholar 

  • Vigneswaran, S., Jethva, D. M., Wadaskar, P. S., & Balas, T. K. (2017). Effect of cold temperature durations on the emergence and parasitization efficiency of laboratory reared Trichogramma chilonis (Ishii). International Journal of Current Microbiology and Applied Sciences, 6(5), 1191–1199.

    Article  CAS  Google Scholar 

  • Visser, B., & Ellers, J. (2008). Lack of lipogenesis in parasitoids: A review of physiological mechanisms and evolutionary implications. Journal of Insect Physiology, 54, 1315–1322.

    Article  CAS  PubMed  Google Scholar 

  • Wadaskar, P. S., Jethva, D. M., Vigneswaran, S., & Rode, N. S. (2015). Studies on effect of temperature and relative humidity on biology of rice moth Corcyra cephalonica (Stainton) under laboratory condition. The Ecoscan, 9(1&2), 201–204.

    Google Scholar 

  • Waggoner, M., Bernal, J., & Gonzalez, D. (1997). Effect of short-term cold storage on mummy-stage survival in two parasites of the Russian wheat aphid. Southwestern Entomologist, 22(1), 73–77.

    Google Scholar 

  • Whitaker-Deerberg, R. L., Michels, G. J., Wendel, L. E., & Farooqui, M. (1994). The effect of short-term cold storage on emergence of Aphelinus asychis (Hymenoptera: Aphelinidae) mummies. Southwestern Entomologist, 19(2), 115–118.

    Google Scholar 

  • Yan, Z., Yue, J. J., Bai, C., Peng, Z. Q., & Zhang, C. H. (2017). Effects of cold storage on the biological characteristics of Microplitis prodeniae (Hymenoptera: Braconidae). Bulletin of Entomological Research, 107, 506–512.

    Article  CAS  PubMed  Google Scholar 

  • Yigit, A., Canhilal, R., & Zaman, K. (1994). Cold storage of some natural enemies of citrus mealybug, Planococcus citri (Risso) (Homoptera: Pseudococcidae). Bulletin of III. Turkey Biological Control, 7, 137–146.

    Google Scholar 

  • Yilmaz, S., Karaborklu, S., & Ayvaz, A. (2008). Effect of cold temperature durations on the performance of the adult Trichogramma evanescens (Westwood) (Hymenoptera: Trichogrammatidae). Turkey Entomological Journal, 31(4), 269–278.

    Google Scholar 

  • Yocum, G. D., Zdarek, J., Joplin, K. H., Lee Jr., R. E., Smith, D. C., Manter, K. D., & Denlinger, D. L. (1994). Alteration of the eclosion rhythm and eclosion behaviour in the flesh fly, Sarcophaga crassipalpis, by low and high temperature stress. Journal of Insect Physiology, 40, 13–21.

    Article  Google Scholar 

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Acknowledgements

Thanks are extended to Dr. (Mrs.) Asha Kawatra, Dean, Post Graduate Studies, CCSHAU, Hisar for providing necessary and handful library facilities. We would like to acknowledge the other faculty members of the Department of Entomology for their needful help in compiling this review. No funds have been provided from any source.

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Rathee, M., Ram, P. RETRACTED ARTICLE: Impact of cold storage on the performance of entomophagous insects: an overview. Phytoparasitica 46, 421–449 (2018). https://doi.org/10.1007/s12600-018-0683-5

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