عنوان مقاله [English]
Background and Objectives
Bracon hebetor Say is a well-known cosmopolitan ectoparasitoid that attacks the larvae of various lepidopteran pests, especially cotton boll worm, Helicoverpa armigera. Cold storage is a general technique for long-term preservation of this parasitoid in insectaries. Most parasitoids require sugar supplemental sources as a source of energy in adult stage. Because of the need to enhance cold storage efficacy in commercial insectaries, this study was carried out to assess effects of feeding frequencies and mating status on biological and reproductive characteristics of maternal wasps and their progeny (F1) stored in refrigerator (5±1˚C) for two durations of 7 and 14 days.
Materials and Methods
B. hebetor reared on the 4-5 instars larvae of Anagasta kuehniella in a climate-controlled room, at 26 ± 2˚C, 50±5% RH, and a 16:8 (L:D)h. photoperiod. The effect of feeding frequency was studied in three levels of "without feeding" (starved wasps), "one-time feeding" before cold storage, and "two-time feedings" (before and during cold storage). Mating status was investigated in two "mated" and "unmated" levels. After each treatment, adult parasitoids were stored inside a refrigerator (5±1˚C) for two periods of 7 and 14 days, and mortality, longevity and fecundity of maternal parasitoids were subsequently assessed. Immature’s developmental time and mortality, percentage of adult emergence and sex ratio were also investigated for progenies in next generation. The experiment was carried out using a factorial experimental design and obtained data were analyzed using SAS software, and LSD mean comparison test.
Results showed that sugar feeding and mating of parasitoid before beginning of cold storage decreased mortality during storage and increased fecundity compared to starved and unmated wasps. The highest mortality of females (33.2%) was observed in starved and unmated wasps that were stored in refrigerator for 14 days. In contrast, the lowest mortality of females (7.71%) belonged to mated parasitoids that fed twice (before and during cold storage) on honey solution and stored for 7 days. Feeding on honey solution by maternal adult parasitoids reduced immature’s mortality and their developmental time in progenies of next generation. Means of immature’s mortality and developmental time in fed wasps (22.82 percent and 11.17 days, respectively) were significantly lower than starved ones (30.64 percent and 11.77 days, respectively).
According to our results, feeding on honey solution increased cold-tolerance of both male and female B. hebetor adults. So that, honey-fed adult parasitoids had lower mortality and higher fecundity than starved ones. Similar to feeding, our results showed that mated parasitoids had higher survival and fecundity than unmated ones. Also, feeding and mating of cold-stored maternal parasitoids had a positive effect on the survival and development of progenies in next generation. In conclusion, spraying honey solution on the rearing cages of B. hebetor and providing sufficient time for mating before storing in refrigerator, are recommended to improved cold-storage efficacy of this parasitoid in insectaries.
Al-Tememi, N.K., and 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.
Ashraf, S., Zain ul Abedin, Abbas S.K., Ahmad Khan, R.S., Tahir, M., Rasool, S., Anwar, M., and Hussain, F. 2017. Effect of different diet concentrations on longevity and fecundity of parasitic wasp Bracon hebetor (Say) (Hymenoptera:Braconidae).Pakistan Journal of Zoology, 49(3): 761-767.
Askari Seyahooei, M., Bagheri, A., Bavaghar, M., Doust, A., and Parichehreh, Sh. 2018. Mating and carbohydrate feeding impacts on life-history traits of Habrobracon hebetor (Hymenoptera: Braconidae). Journal of Economic Entomology, doi: 10.1093/jee/toy253.
Barke, J., Leach, I.M., and Beukeboom, L.W. 2005. Fitness of arrhenotokous and thelytokous Venturia canescens.Proceedings of the Netherlands Entomological Society Meeting,16: 27-35.
Bayram, A., Ozcan, H., and 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.
Carrillo, M.A., Heimpel, G.E., Moon, R.D., Cannon, C.A., and Hutchison, W.D. 2005. Cold hardiness of Habrobracon hebetor (Say) (Hymenoptera: Braconidae), a parasitoid of pyralid moths. Journal of Insect Physiology, 51: 759-768.
Chen, H., Opit, G.P., Sheng, P., and Zhang, H. 2011. Maternal and progeny quality of Habrobracon hebetor Say (Hymenoptera: Braconidae) after cold storage. Biological Control, 58: 255-261.
Chen, H., Zhang, H., Zhu, K.Y., and Throne, J. 2013. Performance of diapausing parasitoid wasps, Habrobracon hebetor, after cold storage. Biological Control, 64: 186-194.
Colinet, H., and Boivin, G. 2011. Insect parasitoids cold storage: a comprehensive review of factors of variability and consequences. Biological Control, 58: 83-95.
Colinet, H., and Hance, T. 2010. Interspecific variation in the response to low temperature storage in different aphid parasitoids. Annals of Applied Biology, 156: 147-156.
Coudron, T.A., Ellersieck, M.R., and 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.
Coudron, T.A., Popham, H.J.R., and Ellersieck, M.R. 2009. Influence of diet on cold storage of the predator Perillus bioculatus (F.). BioControl, 45(6): 773-783.
Ghazy, N.A., Ohyama, K., Amano, H., and Suzuki, H. 2014. Cold storage of the predatory mite, Neoseiulus californicus is improved by pre-storage feeding on the diapausing spider mite Tetranychus urticae. BioControl, 59(2): 185-194.
Gündüz, E.A., Gulel, A., Işitan, O.V., Boz, A., and Cesur, O. 2010. Effects of sugar feeding on lipid, glycogen, and total sugar levels of a female parasitoid, Bracon hebetor (Say) (Hymenoptera: Braconidae).Turkish Journal of Agriculture and Forestry, 34: 343-347.
Gündüz, E.A., Gulel, A., Işitan, O.V., Gülel, A., Boz, A., and Polat, P. 2011. Lipid, total sugar and glycogen composition in the parasitoid, Bracon hebetor Say, 1836 (Hymenoptera: Braconidae) during starvation. Turkish BulletinofEntomology, 1(4): 221-227.
Hamzehpour Chenari, E. 2013. Effect of cold storage on development and reproduction of Bracon hebetor Say (Hymenoptera: Braconidae) under laboratory conditions. M.Sc. Thesis. Gorgan University of Agricultural Sciences and Natural Resources (In Farsi with English abstract).
Hanna, A.D. 1935. Fertility and tolerance of low temperature in Euchalcidia carybori Hanna (Hymenoptera: Chalcidinae). Bulletin of Entomological Research, 26: 315-322.
Howard, R.W., and Baker, J.E. 2003. Cuticular hydrocarbons and wax esters of the ectoparasitoid Habrobracon hebetor: Ontogenetic, reproductive, and nutritional effects. Archives of Insect Biochemistry and Physiology, 53:1-18.
Huang, X.F. 1986. Use of Habrobracon hebetor Say in granary pest control. Chinese Journal of Biological Control, 2: 78-80.
Johnson, J.A., Valero, K.A., Hannel, M.M., and Gill, R.F., 2000. Seasonal occurrence of postharvested dried fruit insects and their parasitoids in a culled fig house. Journal of Economic Entomology, 93: 1380-1390.
Leopold, R.A., 2007. Colony maintenance and mass-rearing: using cold storage technology for extending shelf-life of insects. In: Vreysen, M.J.B., Robinson, A.S., and Hendrichs, J. (Eds.). Area-Wide Control of Insect Pests. Springer, Netherlands. pp. 149-162.
Leopold, R.A. and Chen, W. 2007. Cold storage of the adult stage of Gonatocerus ashmeadi Girault: The impact on maternal and progeny quality. In: Esser, T., Blincoe, P., West, D., Mochel, M., and Veling, S. (Eds.), Proceedings of the 2007 Pierce’s Disease Research Symposium, San Diego, CA. pp. 42-46.
Mahi, H., Rasekh, A., Shishebor, P. 2014a. Chill storage of bisexual population of Lysiphlebus fabarum (Braconidae: Aphidiinae). Plant Protection, 37(2): 65-78 (In Farsi with English abstract).
Mahi, H., Rasekh, A., Michaud, J.P., Shishebor, P. 2014b. Biology of Lysiphlebus fabarum following cold storage of larvae and pupae. Entomologia Experimentalis et Applicata, 153(1): 10-19.
Mousapour, Z., Askarianzadeh, A., and Abbasipour, H. 2015. Cold storage of adult parasitoid wasp, Habrobracon hebetor (Say) (Hymenoptera: Braconidae) and the flour moth larvae, Anagasta kuehniella (Zeller) at 12°C. Plant Pests Research, 5(3): 17-29 (In Farsi with English abstract).
Mousapour, Z., Askarianzadeh, A., and Abbasipour,H. 2014. Effect of cold storage of pupae parasitoid wasp, Habrobracon hebetor (Say) (Hymenoptera: Braconidae), on its efficiency. Archives of Phytopathology and Plant Protection, 47(8): 966-972.
Najafi Navaei, I., Taghizadeh, M., Javanmoghaddam, H., Oskoo, T. and Attaran, M.R. 2002. Efficiency of parasitoid wasps, Trichogramma pintoii and Habrobracon hebetor against Ostrinia nubilalis and Helicoverpa sp. on maize in Moghan. Proceedings of the 15th Iranian Plant Protection Congress. Razi University of Kermanshah, Iran. P. 327.
Okine, J.S., Mitchell, E.R., and 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.
Olson, D. M., Fadamiro, H., Lundgren, J.G., and Heimpel, G.E. 2000. Effects of sugar feeding on carbohydrate and lipid metabolism in a parasitoid wasp. Physiological Entomology, 25: 17-26.
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.
Rivers, D.B., Jr Lee, R.E., and Denlinger, D.L. 2000. Cold hardiness of the fly pupal parasitoid Nasonia vitripennis is enhanced by its host Sarcophaga crassipalpis. Journal of Insect Physiology, 46: 99-106.
Rössler, Y., and DeBach, P., 1972. The biosystematic relations between a thelytokous and an arrhenotokous form of Aphytis mytilaspidis (Le Baron) [Hymenoptera: Aphelinidae] I. The reproductive relations. BioControl, 17: 391-423.
SAS Institute Inc. 2002. SAS System for Windows Version 9.0, Cary, NC, USA.
Scharf, I., Daniel, A., Macmillan, H.A., and Katz, N. 2017. The effect of fasting and body reserves on cold tolerance in 2 pit-building insect predators. Current Zoology, 63(3): 287-294.
Tunca, H., Yeşil, A.N., and Çalişkan, T.F. 2014. Cold storage possibilities of a larval parasitoid, Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae). Turkish Journal of Entomology, 38 (1): 19-29.
Uçkan, F. and Ergin, E. 2003. Temperature and food source effects on adult longevity of Apanteles galleriae Wilkinson (Hymenoptera: Braconidae). Environmental Entomology, 32: 441-446.
Wang, Z., and Smith, S.M. 1996. Phenotypic differences between thelytokous and arrhenotokous Trichogramma minutum from Zeiraphera canadensis. Entomologia Experimentalis et Applicata, 78(3): 315-323.
Yazdanian, M., Khabbaz Saber, H. and Afshari, A. 2014. Effect of sugar concentration and feeding frequency on adult’s longevity and progeny production of the parasitoid wasp, Habrobracon hebetor (Hymenoptera: Braconidae). Plant Pests Research, 3(4): 1-16 (In Farsi with English abstract).
Yazdanian, M., Haddad Irani Nejad, K. and Mashhadi Jafarloo, M. 2005. Determining the number of larval instars of the Mediterranean flour moth, Anagasta kuehniella (Lepidoptera, Phycitidae) in laboratory conditions. Agricultural Science, 15: 45-54 (In Farsi with English abstract).