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Cold storage and gamma irradiation of Sitotroga cerealella Olivier eggs (Lepidoptera: Gelechiidae) in relation to the success of parasitism by Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae)


The performance of parasitism by the egg parasitoid, Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae) on eggs of Angoumois grain moth, Sitotroga cerealella Olivier (Lepidoptera: Gelechiidae) was investigated under cold storage and gamma irradiation treatments of the host eggs. Cold storage treatment could improve the parasitoid mass rearing techniques and reduced the costs of biological control programs, while gamma irradiation might be used as a supplementary support at the times of high demand. The suitability of the S. cerealella eggs, stored at – 20 °C for 0.5, 1, or 2 h. as a host for T. evanescens was evaluated. The sensitivity of S. cerealella eggs to gamma irradiation treatments and the acceptability of irradiated eggs for parasitism by T. evanescens females for the parental P and F1 generations were examined. The results revealed that parasitism was drastically reduced more than adult’s emergence and sex-ratio (% of females) after cold storage periods of S. cerealella eggs. Moreover, the parasitism percentages were relatively reduced to (97.1, 96.1, 93.03, and 92.7 %) after irradiating the S. cerealella eggs at 40, 60, 80, and 100 Gy, respectively than the control (97.3% emergence). The percentages of emergence and females’ percent were slightly decreased by gamma irradiation doses, while, equal preferred by the F1 generation of parasitoid that produced from irradiated S. cerealella eggs.


Trichogramma spp. is among the most important natural enemies used widely around the world to control the lepidopteran insect pests. They have a wide host range and can be easily be mass produced (Li, 1994). Augmentative release of the egg parasitoid to manage the stored product pests is a promising technique as a bio-control agent (Grieshop et al. 2006). The utilization of T. evanescens against lepidopteran stored–product pests has gradually increased in many regions for the control of the Mediterranean flour moth Ephestia kuehniella Zeller, the warehouse moth Ephestia elutella (Hübner) and the Indian meal moth Plodia interpunctella (Hübner) (Prozell and Schoeller, 1998). The costs of mass rearing of Trichogramma spp. on natural hosts are relatively high, so, the eggs of the grain moth, Sitotroga cerealella Olivier (Lepidoptera: Gelechiidae) are often used as an alternative host (Vieira and Tavares, 1995). Storing large numbers of Trichogramma and host eggs is desirable as the field requirements can vary, in order to face a fluctuating demand. The low temperature has been applied to kill the host eggs before being exposed to the egg parasitoid, (Bradley et al. 2004). In addition, the ultra violet light (UV) irradiation treatment has been suggested to kill eggs of insect hosts of Trichogramma spp. (Voegele et al. 1974 and Goldstein et al. 1983). However, the UV radiation is a weak penetrating power, and it makes the UV treatment less applicable than ionizing radiation, while, Gamma radiation has very high penetration ability and could be used successfully to kill the host eggs (Brower 1982; Ayvas and Tuncbileck 2006 and Ayvaz et al. 2008). The irradiated and un-irradiated eggs with gamma radiation were equal acceptable for parasitism by Trichogramma spp. (Saour 2004 and Ayvaz et al. 2008). The radio sensitivity of the eggs has to be investigated, in order to determine the appropriated irradiation dose. In lepidopteran insects, combined treatments; release of partial sterile insects and Trichogramma may proof practical and would be a potential control strategy.

The objectives of this study were to determine the effects of cold storage periods and gamma radiation rates of S. cerealella eggs on the performance of T. evanescens, in order to assess the potential of using both treatments for increasing the efficacy of using Trichogramma parasitoids.

Materials and methods

S. cerealella rearing

A colony of S. cerealella was originally obtained from the Center of Bio-organic Agricultural Services (CBAS), Aswan Governorate, Egypt. S. cerealella was reared and maintained at 26 ± 1 °C and 85 ± 5% R.H. Mass rearing technique was carried out as described by Abdel-Hameid (2018).

Rearing of T. evanescens

T. evanescens, used in this study, was originally obtained from CBAS. The parasitoid was reared on the eggs of S. cerealella glued on small carton cards, each carrying about 500 eggs. Rearing was carried out by exposing the egg-cards of Sitotroga to the parasitoid in cages covered with cotton-cloth.

Effect of cold storage

One-day-old S. cerealella eggs, mounted on cards, were separately placed in glass vials (1.6 cm diameter × 10 cm height) to be killed by cold storage at (− 20 °C) for 0.5, 1, and 2 h. Storage was carried out in a deep freezer. The frozen eggs were introduced into glass vials to the parasitoid adults (3 egg cards, carrying S. cerealella eggs + 1 card of the parasitized eggs). The emerged adults were placed, individually, in glass vials. Percentages of emerged adults, the % parasitism and sex-ratio (% of females), were recorded. For each storage period, 50 replicates and a control were used.

Effect of irradiation

For studying the acceptance of irradiated S. cerealella eggs for parasitism by T. evanescens females, 24-h-old eggs were used. Egg cards carrying S. cerealella eggs were exposed to gamma radiation dosages in a gamma cell supplied with a Co-60 source rounded the cylindrical irradiation chamber (Issledovatel Gamma Irradiator, Techsnabexport Co. Ltd. USR) located at Cyclotron Project-Nuclear Research Center, Atomic Energy Authority, Cairo, Egypt, with a dose rate of 0.55 Gy/s. Five replicates of 500 eggs, each was irradiated at different doses (0, 40, 60.80, and 100 Gy). The treated eggs were transferred to normal rearing conditions and introduced into the glass vials to be exposed to the parasitoid (3 egg cards” carrying S. cerealella eggs + 1 card of the parasitized eggs).

Parasitism percent per card was scored 5 days after incubation. The number of emerging parasitoid adults was recorded, and the percentages of parasitism and females were calculated. A new S. cerealella eggs card was introduced to the newly emerged wasps (F1 generation) that emerged from irradiation treatments. Percentages of parasitism, adult emergence, and females’ percentage were determined in each treatment.

Statistical analysis

The statistical analysis of data was conducted using ANOVA technique using SPSS Ver. 19.0. The significance between means was determined by the multiple-range test (Duncan at P < 0.05). Data were designed according to Steel et al. (1997).

Results and discussions

S. cerealella eggs (whether treated by irradiation or cold storage) showed acceptable rates for parasitism by T. evanescens females (Tables 1, 2 and 3).

Table 1 Effects of different cold storage periods of Sitotroga cerealella eggs at − 20 °C on Trichogramma evanescens parasitism, emergence rate, and sex ratio
Table 2 Effects of gamma irradiation of S. cerealella eggs (different rates) on T. evanescens parasitism, emergence rate and sex ratio (parental, P generation)
Table 3 Effects of gamma irradiation of S. cerealella eggs (different rates) on T. evanescens parasitism, emergence rate and sex-ratio (F1 generation)

Effect of cold exposure periods

When the S. cerealella eggs were stored at – 20 °C, the parasitism percentages significantly reduced to (21.50, 18.54, and 10.55%) at the storage periods, 30, 60, and 120 min, respectively than the control (97.10 %) (Table 1). As shown in the same table, the high numbers of the parasitoid adult emergences were recorded at the storage treatment of 30 min than those recorded in 60- and 120-min cold storage. While, there was insignificant difference in the percentage of females within the 3 storage treatments (30, 60, and 120 min). Statistical analysis of data showed highly significant differences in percentages of parasitism and emergence, among the different cold storage treatments. The results indicated that the 3 storage periods applied (30, 60, and 120 min) to S. cerealella eggs sharply declined the acceptability of T. evanescens parasitism, while the longer periods 60 and120 drastically reduced the adult emergence percentages of parasitoid. However, the female percentages were relatively similar in the 3 storage period treatments. These results agree with Karabörklü and Ayvaz (2007) who found that the parasitization and emergence of T. evanescens adults reduced depending on the storage periods of E. kuehniella and S. cerealella eggs. Moreover, they found that the storage temperature and periods decreased the adult longevity of the parasitoid in case of S. cerealella more than in E. kuehniella eggs. Also, it was reported that the cold treatment of host eggs reduced the Trichogramma performance (parasitism rate, emergence, and sex ratio) (Bradley et al. 2004). The present results contradict with those of Karabörklü and Ayvaz (2007) who found that the percentage of sex ratio of T. evanescens that emerged after cold storage of the host eggs was relatively similar to the control treatment. The parasitoid T. evanescens had a high tolerance to temperatures and was used to control Plodia interpunctella and Cadra cautella (Walker) in storage to protect the stored products (Scholler and Hassan 2001).

Irradiation of S. cerealella eggs

Irradiation of 1–24 h. old eggs with 40, 60, 80, and 100 Gy doses, slightly affected the performance parameters of T. evanescens. The parasitism percentages were relatively reduced (97.1, 96.1, 93.03, and 92.7%) in 40, 60, 80, and 100 Gy, respectively than the control treatment (97.3%) (Table 2). The reduction of parasitism was significant in (60, 80, and 100 Gy) than the 40 Gy and control treatments. The same trend was recorded in the percentages of emerged adults, where they were recorded, at the 4 rate treatments being, significantly reduced to (93.23 and 91.5% at 80 and 100 Gy), respectively than (96.96, 95.16, and 97.5%) in 40, 60 Gy and control, respectively. As shown in the same table, although, the females’ percentage resulted from the eggs exposed to 100 Gy dose reached (90.0%), it was significantly reduced than the recorded (97.66, 95.3%) at the control and 40 Gy, respectively and insignificantly decreased than that recorded (93 and 91%) at 60 and 80 Gy. In similar studies, Brower (1982) reported that equal parasitization was recorded by T. pretiosum on the eggs from un-irradiated and irradiated Indian meal moth P. interpunctella adults with 150 Gy. This finding may be due to a high radio-tolerance of P. interpunctella than to the other insect species (Brower, 1975). Similarly, Saour (2004) found that irradiated potato tuber moth, Phthorimaea operculella (Zeller), with 150 Gy and non-irradiated parental crosses influenced by the Trichogramma parasitoid at the same rate. The present results contradict with those of Cossentine et al. (1996) on codling moth Cydia pomonella and Carpenter et al. (2004) on false codling moth Cryptophlebia leucotreta, who found significant declines in the performance of T. platneri and T. cryptophlebiae, respectively, when the host adults were irradiated by gamma radiation. Also, Mikhaiel et al. (2019) found that both sub-sterilizing doses (125 and 175 Gy) and egg ages had a negative impact on the parasitism with T. evanescens on E. calidella eggs.

The data in Table 3 presented that the performance parameters of F1 generation of T. evanescens adults that emerged from irradiated S. cerealella eggs were relatively similar with un-irradiated ones. The results showed that the percentages of parasitism and emergence rates were insignificantly different than those recorded in the control treatments. While, the female percentages of T. evanescens F1 previously emerged from irradiated host with 60, 80, and 100 Gy were significantly decreased to 85.30, 84.6, and 81.67%, respectively than (94.00 and 92.33%) of 40 Gy and control treatments, respectively. These findings on the effect of fertile and sterile host eggs on T. evanescens may help for lepidopterous pests’ management in both field and storage conditions. The obtained results are in line with Voegele et al. (1974) who found that irradiated eggs of E. kuehniella with the UV irradiation were equally preferred by T. evanescens with non-irradiated ones. In contrast, Mikhaiel et al. (2019) reported that there were preferences in parasitism when the eggs from irradiated E. calidella were used as host to T. evanescens and un-irradiated ones.


Cold storage periods of S. cerealella eggs as host significantly, reduced the parasitism, emergence rates, and female percentage of T. evanescens. Furthermore, some biological parameters were slightly reduced by irradiated S. cerealella eggs with gamma irradiation doses. These findings in particular could be utilized to improve the quality of mass-reared T. evenescens.


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The authors wish to express his deep and sincere thanks to Dr. Fawzy Faiek Shalaby, Emeritus Professor of Economic Entomology, Plant Protection Department, Faculty of Agriculture, Benha Univeristy, for suggesting the problem, keen and close supervision, scientific guidance, valuable and fruitful advices and constructive criticism throughout the whole period of this study, and also for revising the manuscript.

Availability of data and material

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.


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NFA put the idea of research and prepare a plan for the search and responsible for S. cerealella rearing. EIRM performed the samples preparation of the S. cereallela and T. evanescens, and was a major contributor in writing the manuscript, collecting references and responsible for publishing and participating in the steps of carrying out the research. MAL studying the effect of cold storage and making statistical analysis. SWAA studying the effect of irradiation by (Issledovatel Gamma Irradiator, Techsnabexport Co. Ltd. USR) located at Cyclotron Project-Nuclear Research Center, Atomic Energy Authority, Cairo, Egypt. All of the authors of this manuscript contributed equally to the design and/or execution of the experiments described in the manuscript. All authors read and approved the final manuscript.

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Correspondence to I. R. M. Elzoghby.

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Abdel-Hameid, N.F., Elzoghby, I.R.M., Mehany, A.L. et al. Cold storage and gamma irradiation of Sitotroga cerealella Olivier eggs (Lepidoptera: Gelechiidae) in relation to the success of parasitism by Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae). Egypt J Biol Pest Control 29, 86 (2019).

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  • Irradiation
  • Cold storage
  • Eggs
  • Sitotroga cerealella
  • Trichogramma evanescens