Quality Control of the Parasitoid Wasp Trichogramma euproctidis (Hymenoptera: Trichogrammatidae) over 50 Continuous Generations of Rearing on Ephestia kuehniella

Articles in Press

Document Type : Original Article

Authors
Seyedeh Afsaneh Hoseini
Parviz Shishehbor
Seyed Ali Hemmati
Arash Rasekh
Department of Plant Protection, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Islamic Republic of Iran.
Abstract
Trichogramma euproctidis (Girault) (Hymenoptera: Trichogrammatidae), an economically important biocontrol agent of lepidopterous pests, was continuously reared on Ephestia kuehniella Zeller for 50 generations. The effects of continuous rearing on this host were evaluated by comparing biological parameters among different generations (G1–G50). The number of E. kuehniella eggs parasitized by T. euproctidis was significantly affected by generation. Female preadult developmental time was significantly different among consecutive generations, ranging from 9.66 (at G1) to 12.18 d (at G10). Significant differences were detected in female longevity of T. euproctidis among subsequent generations and the highest longevities were found in G5 and G30. However, no significant difference was found in adult emergence rate (survival rate) and sex ratio (female%) among different generations. The highest intrinsic rate of increase (r = 0.373 day⁻¹), finite rate of increase (λ = 1.452 day⁻¹), and net reproductive rate (R₀ = 91.57 females/female) were recorded in G30, whereas lower values were observed after prolonged rearing. Our results indicate that T. euproctidis colonies maintained acceptable biological quality under laboratory rearing conditions for up to 30 generations, whereas a decline in some performance parameters was observed after prolonged rearing.
Keywords
Biological pest control
Egg parasitoids
Generational fitness
Mass-rearing performance
Trichogramma euproctidis.
Subjects
1.   Atashi, N., Shishehbor, P., Seraj, A. A., Rasekh, A., Hemmati, S. A. and Riddick, E. W. 2021. Effect of Helicoverpa armigera egg age on development, reproduction and life table parameters of Trichogramma euproctidis. Insects 12: 569. https://doi.org/10.3390/insects12070569
2.   Badran, F., Y. Fathipour, A. Bagheri, M. Attaran, G. V. P. Reddy. 2022. Effects of prolonged mass rearing on life history traits of Habrobracon hebetor (Hymenoptera: Braconidae). Int J Pest Manag, 68(3). 246–255.
3.   Bellutti, N. 2011. Effects of mass rearing on life-history traits of an invasive fruit moth species. BOKU Vienna, Grapholita molesta (Busck) Institute of Forest Entomology, Forestathology and Forest Protection, p. 35.
4.   Birch, L. C. 1948. The intrinsic rate of natural increase of an insect population. J. Anim. Ecol., 17(1): 15-26. https://doi.org/10.2307/1605
5.   Brindley, T. A. 1930. The growth and development of Ephestia kuehniella Zeller (Lepidoptera) and Tribolium confusum Duval (Coleoptera) under controlled conditions of temperature and relative humidity. Ann. Entomol. Soc. Am., 24(1): 1-17. https://doi.org/10.1093/aesa/23.4.741
6.   Carey, J. R. 1993. Applied Demography for Biologists, with Special Emphasis on Insects; Oxford University Press: Oxford, UK. 1993
7.   Chailleux, A., Desneux, N., Seguret, J., Khanh, H. D. T., Maignet, P. and Tabone, E. 2012. Assessing European egg parasitoids as a mean of controlling the invasive South American tomato pinworm Tuta absoluta. PLoS ONE 7: e48068.
8.   Consoli, F. L., Parra, J. R. P. and Zucchi, R. A. 2010. Egg parasitoids in agroecosystems with emphasis on Trichogramma. Springer, New York, USA.
9.   Dodiya, R.D., Barad, A.H., Pathan, N.P. and Raghunandan, B.L. 2023. Trichogramma: A promising biocontrol agent. Int J Econ Plants 10: 192–199.
10.  Ferracini, C., Boivin, G. and Alma, A. 2006. Costs and benefits of host feeding in the parasitoid Trichogramma turkestanica. Entomol. Exp. Appl., 121: 229-234. https://doi.org/10.1111/j.1570-8703.2006.00479.x
11.  Ghaemmaghami, E., Fathipour, Y., Bagheri, A., Talebi, A. A. and Reddy, G. V. P. 2021a. Quality control of the parasitoid wasp Trichogramma brassicae (Hymenoptera: Trichogrammatidae) over 45 generations of rearing on Sitotroga cerealella. Insect Sci., 28: 180- 190.
12.  Ghaemmaghami, E., Fathipour, Y., Bagheri, A., Talebi, A. A. and Reddy, G. V. P. 2021b. Continuous rearing on Ephestia kuehniella reshaped quality of the parasitoid wasp Trichogramma brassicae (Hymenoptera: Trichogrammatidae). J. Asia-Pacific Entomol., 24: 166- 174.
13.  Gorji, Z., Shishehbor, P., Kocheili, F., Riahi, E. 2024. Quality control of the predatory mite Euseius scutalis (Acari: Phytoseiidae) against Tetranychus turkestani (Acari: Tetranychidae) over 30 generations of rearing on cattail pollen. Acarologia 64(3): 1-14. https://doi.org/10.24349/gz0z-vqgh
14.  Gowda, B.G., Pandi, G. G.P., Ullah, F., Patil, N.B., Sahu, M., Adak, T., Pokhare, S., Yadav, M.K., Mahendiran, A., Mittapelly, P., Desneux, N., Rath, P.C. 2021. Performance of Trichogramma japonicum under field conditions as a function of the factitious host species used for mass rearing. PLoS One 19: 16(8):e0256246. doi: 10.1371/journal.pone.0256246.
15.  Gurr, G. and Nicol, H. I. 2001. Effect of food on longevity of adults of Trichogramma carverae Oatman and Pinto and Trichogramma brassicae Bezdenko (Hymenoptera: Trichogrammatidae). Aust. J. Entomol., 39: 185–187.
16.  Hansen, L. S. and Jensen, K. M. V. 2002. Effect of Temperature on Parasitism and Host- Feeding of Trichogramma turkestanica (Hymenopetra: Trichogrammatidae) on Ephestia kuehniella (Lepidopeta: Pyralidae). J. Eco. Entomol., 95(1): 50-56. https://doi.org/10.1603/0022-0493-95.1.50
17.  Hegazi, E., Alder, C., Khafagi, W. and Agamy, E. 2019. Host preference and parasitic capacity of new candidates of Trichogramma species (Hym.: Trichogrammatidae) against some stored products moths. J. Stored Product Res., 80: 71-78. https://doi.org/10.1016/j.jspr.2018.11.006
18.  Khanamani, M., Fathipour, Y., Talebi, A. A. and Mehrabadi, M. 2017. Quantitative analysis of long-term mass rearing of Neoseiulus californicus (Acari: Phytoseiidae) on almond pollen. J. Econ. Entomol., 110: 1442–1450.
19.  Laurentis, V.L., Ramalho, D.G., Santos, N.A. et al. 2019. Performance of Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) on eggs of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Sci Rep  9: 1156. https://doi.org/10.1038/s41598-018-37797-9
20.  Lessard, E. and Boivin, G. 2013. Effect of age and huger on host-feeding behavior by female Trichogramma euproctidis (Hymenoptera: Trichogrammatidae). Can. Entomol., 145: 53-60. https://doi.org/10.4039/tce.2012.86
21.  Li, L. L. 1994. Worldwide use of Trichogramma for biological control in dif­ferent crops. In: Wajnberg E, Hassan S A (eds) Biological control with egg parasitoids. CAB International, Wallingford, UK, pp 37–54.
22.  Lü, X., Han, S. and Li, L. 2015. Biochemical analyses of Trichogramma dendrolimi (Hymenoptera: Trichogrammatidae) in vitro and in vivo rearing for 10 generations. Fla. Entomol., 98: 911–915.
23.  Lü, X., Han, S., Li, Z. and Li, L. 2017. Biological characters of Trichogramma dendrolimi (Hymenoptera: Trichogrammatidae) reared in vitro versus in vivo for thirty generations. Scientific Rep., 7: 17928.
24.  Maia, A. H. N., Alfredo, J. B. and Campanhola, C. 2000. Statistical influence on associated fertility life table parameters using Jackknife technique: computational aspects. J. Econ. Entomol., 93: 511-518. https://doi.org/10.1603/0022-0493-93.2.511
25.  Miyatake, T. 1998. Genetic changes of life history and behavioral traits during mass-rearing in the melon Fly, Bactrocera cucurbitae (Diptera: Tephritidae). Res. Popul. Ecol., 40: 301–310.
26.  Modares Awal, M. 2012. List of agricultural pests and their natural enemies in Iran. Third edition, Ferdowsi University Press, 285p.
27.  Moghaddassi Y, Ashouri A, Bandani AR, Leppla NC, Shirk PD. 2019. Effect of Ephestia kuehniella (Lepidoptera: Pyralidae) larval diet on egg quality and parasitism by Trichogramma brassicae (Hymenoptera: Trichogrammatidae). J Insect Sci 19(4):10. doi: 10.1093/jisesa/iez076.
28.  Naranjo-Guevara, N., dos Santos, L. A. O.,  Barbosa, N. C.C.P., Castro, A. C.M.C.C., and  Fernandes, O.A. 2020. Long-Term Mass Rearing Impacts Performance of the Egg Parasitoid Telenomus remus (Hymenoptera: Platygastridae). J Entomol Sci 55(1): 69-86. https://doi.org/10.18474/0749-8004-55.1.69
29.  Ningthoujam, K., Moirangthem, Z., Pathak, M. et al. 2025. Host suitability and parasitism of Trichogramma pretiosum on Galleria melonella and Corcyra cephalonica for the management of fall armyworm. Sci Rep 15: 34154. https://doi.org/10.1038/s41598-025-14656-y
30.  Nordlund, D. A., Wu, Z. X. and Greenberg, S. M. 1997. In vitro rearing of Trichogramma minutum Riley (Hymenoptera: Trichogrammatidae) for ten generations, with quality assessment comparisons of in vitro and in vivo reared adults. Biol. Control 9: 201–207.
31.  Pakyari, Hajar, and Rostislav Zemek. 2025. The effect of light cycles on the predation characteristics of Phytoseiulus persimilis (Acari: Phytoseiidae) feeding on Tetranychus urticae (Acari: Tetranychidae). Plants 14 (5): 687. https://doi.org/10.3390/plants14050687
32.  Parra, J. R. P. 2010. Mass rearing of egg parasitoids for biological control programs. In: Cônsoli FL, Parra JRP,  Zucchis RA (eds) Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma. Springer, Netherlands, Dordrecht, pp 267–292.
33.  Pintureau, B. 2008. Les especes europeennes de Trichogrammes, ILV ed, In Libro Veritas, Cergy-Pontoise, France.
34.  Platner, J.D., Velten, R.K., Planoutene, M. and Pinto, J.D. 1999. Slide mounting techniques for Trichogramma (Trichogrammatidae) and other minute parasitic Hymenoptera. Entomol News 110: 56–64.
35.  Pratissoli, D., Oliveira, H., Roberto Goncalves, J. and Zanuncio, J. 2004. Changes in biological characteristics of Trichogramma pretiosum (Hym.: Trichogrammatidae) reared on eggs of Anagasta kuehniella (Lep.: Pyralidae) for 23 generations. Bio. Sci. Tech., 14: 313–319.
36.  Sadat, F., Nazari, A., Jafari, S. et al. How long-term mass rearing affects the quality of the Trichogramma embryophagum (Hartig) (Hymenoptera: Trichogrammatidae) reared on Sitotroga cerealella (Olivier) eggs. Egypt J Biol Pest Control 31, 119 (2021). https://doi.org/10.1186/s41938-021-00456-9
37.  Sørensen, J. G., Addison, M. F. and Terblanche, J. S. 2012. Mass-rearing of insects for pest management: Challenges, synergies and advances from evolutionary physiology. J. Crop. Prot., 38: 87–94.
38.  SPSS. 2018. SPSS for windows. Version 22.0; SPSS Institute Inc. Chicago, Il. USA.
39.  St-Onge, M., Cormier, D., Todorova, S., & Lucas, É. 2014. Comparison of Ephestia kuehniella Eggs Sterilization Methods for Trichogramma ostriniae Rearing. Biol Control, 70: 73–77. https://doi.org/10.1016/j.biocontrol.2013.12.006 
40.  Sumer, F., Tuncbilek, A. S., Oztemiz, S., Pintureau, B., Rugman-Jones, P. and Stouthamer, R. 2009. A molecular key to the common species of Trichogramma of the Mediterranean region. Biocon, 54: 617-624. https://doi.org/10.1007/s10526-009-9219-8
41.  Tabebordbar, F., Shishehbor, P. and Ebrahimi, E. 2020. Suitability of different egg ages of Ephestia kuehniella (Lep.: Pyralidae) for the development, reproduction and life table parameters of Trichogramma euproctidis (Hym.: Trichogrammatidae). J. Crop Prot., 9: 89–99.
42.  Tabebordbar, F., Shishehbor, P., Ebrahimi, E., Polaszek, A. and Ugine, T. A. 2022. Effect of different constant temperatures on life history and life table parameters of Trichogramma euproctidis (Hymenoptera: Trichogrammatidae). J. Econ. Entomol., 15: 474- 481. https://doi.org/10.1093/jee/toac007
43.  Tabebordbar, F., Formisano, G., Shishehbor, P., Ebrahimi, E., Giorgini, M., Sørensen, J.G. 2023. Variation among populations of Trichogramma euproctidis (Hymenoptera: Trichogrammatidae) revealed by life table parameters: perspectives for biological control. J Econ Entomol 116(4):1119-1127. doi: 10.1093/jee/toad075.
44.  Tuncbilek, A. S., Cinar, N. and Canpolat, U. 2012. Effect of artificial diets and floral nectar on longevity and progeny production of Trichogramma euproctidis Girault (Hymenoptera: Trichogrammatidae). Turkish J. Entomol., 36: 183-191.
45.  van Lenteren, J., Hale, A., Klapwijk, J. N., van Schelt, J. and Steinberg, S. 2002. Guidelines for quality control of commercially produced natural enemies. In: van Lenteren, J. (Ed) Quality control and production of biological control agents: theory and testing procedures. CAB International, Wallingford, UK, pp 265-303.
46.  van Lenteren, J. C. 2003. Quality control and production of biological control agents: Theory and testing procedures. CABI.
47.  Zhang, Y.-H.; Xue, J.-Z.; Tariq, T.; Li, T.-H.; Qian, H.-Y.; Cui, W.-H.; Tian, H.; Monticelli, L.S.; Desneux, N.; Zang, L.-S. 2024. Parasitism and suitability of Trichogramma chilonis on large eggs of two factitious hosts: Samia cynthia ricini and Antheraea pernyi. Insects 15: 2. https://doi.org/10.3390/insects15010002
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Available Online from 05 September 2026