Does superparasitism affect fitness of Ooencyrtus telenomicida, an egg parasitoid of Eurygaster integriceps?

Research Article

Does superparasitism affect fitness of Ooencyrtus telenomicida, an egg parasitoid of Eurygaster integriceps?

Ashkan Rafat¹, Seyed Ali Safavi^1* and Shahzad Iranipour²

1. Department of Plant Protection, Faculty of Agriculture, Urmia University, Urmia, Iran.

2. Department of Plant Protection, Faculty of Agriculture, University of Tabriz, Tabriz, 51666-14888, ‎Iran.‎

Abstract: Ooencyrtus telenomicida Vassiliev (Hym.: Encyrtidae) is an important and broadly distributed egg parasitoid of sunn pest Eurygaster integriceps Puton (Hem.: Scutelleridae) in Iran. Few studies have been carried out on this species. In this research, the life history of O. telenomicida, was studied on E. integriceps eggs under laboratory conditions. All parameters were compared between two levels of parasitism, i.e., superparasitized (SP = two progenies per host egg) and non-superparasitized (NSP = one progeny per host egg). The developmental time of the whole immature stages within the host eggs was 13-17 days. The longevity of adult males and females also ranged between 25-35 and 23-41 days, respectively. The number of eggs was recorded to be 43-191 per female. Moreover, the mean number of daily per capita eggs was 5.3-19.12 per female. The pre-adult survival rate of the two cohorts was 100%, i.e., all wasps from the two cohorts hatched successfully from the host eggs. Superparasitism was observed in all female wasps. Observed sex ratio of the emerged broods was 0.437-0.898 females/total offspring. The intrinsic rate of increase (r) of NSP and SP wasps was estimated 0.224 ± 0.004 and 0.234 ± 0.004 per day, respectively. Net reproductive rate was 76.13 ± 7.55 and 81.6 ± 9.66 females/female/generation for the same cohorts, respectively. The mean generation time was also estimated to be 19.36 ± 0.41 and 18.84 ± 0.40 days for the same treatments, respectively. No significant difference was observed in life table parameters of the two parasitoid cohorts. Therefore, our results showed that superparasitism had no negative effects on the reproductive fitness of O. telenomicida.

Keywords: Intrinsic rate of increase, Life history, Sunn pest, Fecundity

Introduction[1][2]

Sunn pest, Eurygaster integriceps Puton, is the most important insect pest of wheat in Central and West Asia (Radjabi, 1994; Javahery, 1995; Parker et al., 2011). The current strategies for sunn pest management rely mainly on chemical and cultural control (Miller and Morse, 1996; Islamoglu and Karacaoglu, 2018). Chemical measures are costly and may induce resistance in populations with a long history of exposure to pesticides. Therefore, they may be considered as temporary solutions (Alexandrescu et al., 1990; Golmohammadi and Dastranj, 2020; Javadipouya et al., 2023). Current studies are focused on resistant wheat varieties, insect pathogens, predators, and parasitoids (Moore, 1998; Najafi-Mirak, 2012; Davari and Parker, 2018; Iranipour, 2021). Different natural enemies attack the sunn pest, which plays an important role in its control; in some years, they even prevent the need for spraying in certain countries (Kartavtsev, 1974; Udovitsa, 1998). Trissolcus grandis (Thomson), T. vassillievi (Mayr), and Ooencyrtus telenomicida (Vassiliev) are the most common egg parasitoids of E. integriceps (Radjabi and Amirnazari, 1989; Iranipour et al., 1998; Nouri and Asgari, 2000; Iranipour, 2021). Seasonal activities of these parasitic wasps begin before their host, E. integriceps (Safavi, 1973; Radjabi, 2000; Iranipour, 1996, 2021). Egg parasitoids kill their hosts before any feeding damage to the crop. This makes them very attractive in practical biological control programs against insect pests. Therefore, utilization of these beneficial insects can decrease control costs and prevent environmental damage. Ecological studies on natural enemies are required before implementing inundative release or conservation programs (van Lenteren
et al., 2003).

Ooencyrtus telenomicida (Hymenoptera: Encyrtidae) is a generalist, cosmopolitan, gregarious, idiobiont endoparasitoid of cereal bugs present across Europe, Asia, and Sub-Saharan Africa (Zhang et al., 2005; Japoshvili and Noyes, 2006; Triapitsyn et al., 2020). Several herbivorous insects from Heteroptera (families Coreidae, Pentatomidae, Scutelliridae) and Lepidoptera (families Lymantriidae, Notodontidae, and Thaumetopoeidae) have been recorded as hosts for this species. This encyrtid wasp, as well as related species O. fecundus Feniere & Voegele, are also reported as facultative secondary parasitoids of parasitic wasps from the family Scelionidae (Japoshvili and Noyes, 2006), particularly T. basalis (Catalan and Verdu, 2005) and T. grandis (Nassiri et al., 2020; Hatami-Sadr et al., 2024). Intra-guild interaction between Trissolcus spp. (or other scelionid species) and Ooencyrtus spp. has been reported in several crop-pest systems around the world (Corrêa-Ferreira, 1986; Shepard et al., 1994; Ehler, 2002; Mohammadpour et al., 2014; Peri et al., 2014; Cusumano et al., 2012, 2022; Faca et al., 2021; Fusu and Andreadis, 2023).

Superparasitism is a common phenomenon in nature, defined as repeated attacks by conspecific female parasitoids on a single host (conspecific superparasitism) or by an individual female alone (self-superparasitism) (van Alphen and Visser, 1990; Ahmadpour et al., 2013; Iranipour et al., 2020). When a female parasitoid encounters a parasitized host, it may respond in different ways: (1) rejects the host and searches for subsequent hosts; (2) feeds on the host’s haemolymph to produce additional eggs and/or enhance her energy reservoirs; (3) superparasitizes i. e. oviposit an additional egg in the host, or (4) kills one or more eggs or larvae initially laid in the host (infanticide) and replace them with one or more of her own (Strand and Godfray, 1989; Mayhew, 1997; Netting and Hunter, 2000; Goubault et al., 2004; Tunca et al., 2016; Chen et al., 2020). The effects of superparasitism differ between koinobiont and idiobiont parasitoids. In koinobionts, the host continues to feed, grow, and undergo metamorphosis while the parasitoid progeny develops. On the other hand, idiobionts develop in non-developing or paralyzed hosts. In endoparasitoids, superparasitism may be a mechanism of overcoming encapsulation (van Alphen and Visser, 1990; Blumberg and Luck, 1990; Luna et al., 2016). Consequently, such parasitoids should tend to oviposit in a recently parasitized host because their larvae have a higher chance of surviving (van Lenteren, 1981; Mackauer, 1990). Some endoparasitoids leave an external cue to avoid superparasitism (Netting and Hunter, 2000), for example, a spin-like egg stalk protruding from the host’s cuticle, in some Encyrtidae (Maple, 1954). Superparasitism might be an adaptive strategy at least in some situations (van Alphen and Jervis, 1996; Rosenheim and Hongkham, 1996; White and Andow, 2008). The trade-off between the benefits and costs of laying an additional egg in a parasitized host will determine the relative advantage of this behavior. Recent studies have shown that an additional clutch may be beneficial under certain conditions (van der Hoeven and Hemerik, 1990; Visser et al., 1990; Gandon et al., 2006).

Over the past few decades, life tables have been the main tool for ecological studies of populations and species from different origins, under various climate conditions and nutritional states (Lewis, 1942; Leslie, 1945; Birch, 1948; Carey, 1993; Ebert, 1999; Chi et al., 2022). Life history parameters also provide useful criteria for evaluating the relative performance of a predator/parasitoid against a prey/host. Development, reproduction, and survival are life history components that are influenced by both the physiological state of an organism and environmental conditions (Harbison et al., 2001; Uçkan and Ergin, 2003). The intrinsic rate of increase combines those components into a single parameter, making it the most comprehensive life table parameter for comparing species, populations, and their physical conditions (Southwood and Henderson, 2009). Life table studies were initiated approximately 25 years ago in Iran and have since been increasingly developed to study both pest and natural enemy populations (Asgari and Kharrazi Pakdel, 1998; Amir-Maafi, 2000; Asgari, 2001; Iranipour et al., 2003). Such demographic data can be very useful for preliminary screening of the most effective biocontrol agents, performing mass rearing programs, and timing inundative releases.

Numerous life history studies have been conducted on egg parasitoids of the sunn pest and other stink bugs, both from Scelionidae (mainly Trissolcus spp.; Asgari, 2004, Kivan and Kiliç, 2006b; Abdel-Salam et al., 2007; Laumann et al., 2008; Nozad-Bonab et al., 2014; Bazavar et al., 2015; BenaMolaei et al., 2015a, b; Abdi et al., 2017; Teimouri et al., 2019) and Encyrtidae (Ooencyrtus spp.; Bazavar, 2013; Ahmadpour et al., 2013; Ganjisaffar and Perring, 2020; Giovannini et al., 2020). To our knowledge, the life history of O. telenomicida has never been studied on E. integriceps. In this paper, we studied the life history of O. telenomicida on E. integriceps eggs using a traditional female cohort age-specific life table for two levels of parasitism: O. telenomicida developed as singletons (non-superparasitized, NSP) and twins (superparasitized, SP) in E. integriceps eggs.

Materials and Methods

Insect cultures

A stock culture of E. integriceps was established in the laboratory using materials collected in the spring of 2012 from wheat fields in West Azerbaijan, Iran (geo: lat = 45.071810, geo: lon = 37.791190). The adults were reared in plastic containers (24 × 17 × 10 cm) with fine mesh covered to provide ventilation and prevent insects from escaping. Containers were placed in a growth chamber (28 ± 1 °C, 60 ± 5% RH, and 16:8 h L: D), and a diet of soaked wheat grains (Triticum aestivum) and water was daily supplied. A few pieces of folded paper were placed in each container as egg-laying substrates. Parts of papers with egg masses were cut, labeled by date, and kept in the fridge at 8 °C.

The colony of O. telenomicida was established by female wasps that emerged from E. integriceps egg masses, which were placed on delta-shaped traps mounted around wheat fields. They were reared in glass tubes (10 × 1.5 cm diameter) in an incubator with previously mentioned conditions, feeding on a 20% honey solution.

Life table studies

All experiments were conducted under the same laboratory conditions. To obtain a female cohort, one host egg mass (14 eggs per mass, 1-3-day old) per female was exposed to 20 females O. telenomicida for 24 h. Then, the wasps were removed, and the parasitized egg masses were held in the same incubator until emergence. Emerged wasps were divided into two groups: 1) super-parasitized cohort in which two wasps developed per a single host egg, and 2) cohort with a single wasp developed per host. Each group was replicated with 15 randomly selected females, which were kept separately in glass tubes in the incubator. Each female was engaged with a male of the same age and same group of parasitism level on the first day of her life. The wasps were fed with a 20% honey solution renewed weekly.

To estimate life table parameters, each female wasp was daily supplied with two clutches of host eggs (each consisting of 14 eggs) up to death. These eggs were removed the next day, labeled by recording date and replication number, and kept in similar glass tubes until emergence. Longevity of males and females, per capita number of parasitized eggs, age-specific number of offspring emerged per parasitized eggs, and sex ratio of them were evaluated separately for each group. In addition, the influence of female age on reproductive parameters (proportion of parasitized eggs and sex ratio of offspring) was assessed. Female age (x: estimated by including development time of larvae + 0.5), daily fecundity (m_x: number of female progeny/female in each day) and female survivorship (l_x: proportion of females surviving in each day) were computed.

Data analysis

Stable population growth parameters including net productive rate (R₀), gross reproductive rate (GRR), intrinsic rate of increase (r), mean generation time (T), doubling time (DT), finite rate of increase (λ), instantaneous birth rate (b) and instantaneous death rate (d) were calculated for two cohorts of O. telenomicida using female cohort age-specific life table (Carey, 1993; Iranipour et al., 2025a). The intrinsic rate of increase (r) was calculated by using a Macro in Excel (Iranipour, 2018). A comparison between male and female longevity, as well as a comparison between the fecundity of the two cohorts, was carried out using a paired t-test. The intrinsic rate of increase, net reproductive rate, mean generation time, doubling time, and finite rate of increase have been compared using 95% confidence intervals of the differences between randomly paired bootstrap replicates of the two cohorts.

Results

Overall, 29,512 host eggs were offered to females of the two cohorts, from which 1,873 eggs successfully parasitized, and 3,180 wasps emerged, resulting in 74.12% and 25.88% of the progeny being female and male, respectively. The development time of the immature stages of wasps did not differ significantly (t = 1.20, df = 1, 28, P = 0.12) between the two treatments, as it took 14.28 ± 0.06 and 14.19 ± 0.05 days for wasps to emerge from non-superparasitized (NSP) and superparasitized (SP) cohorts, respectively. Female adults of O. telenomicida lived for 33.67 ± 1.15 and 36.6 ± 0.93 d in NSP and SP cohorts, respectively, which was significantly different (t = 1.98, df = 1,28, P = 0.03), and longer than those of the males that took 28.6 ± 0.79 and 29.47 ± 0.74 d, for the same cohorts (t = 0.80, df = 28, P = 0.21). The mean oviposition period of both cohorts was the same (t = 1.31, df = 1, 28, P = 0.10), at 16.67 ± 1.52 and 17.27 ± 1.10 days, respectively. The longest oviposition period was 26 d.

Life time fecundity was 104.2 ± 10.34 and 107.8 ± 10.16 eggs per female in NSP and SP cohorts, respectively (t = 0.25, df = 1,28, P = 0.40). Superparasitism was recorded in all female wasps with an average of 1.73 ± 0.06 and 1.69 ± 0.06 broods per host egg for the same cohorts. The maximum number of wasps that emerged from a host egg was four, which were from one or both sexes. The mean superparasitism rate of O. telenomicida was the same between the SP and NSP cohorts (t = 0.41, df = 1, 28, P = 0.34).

No stable population growth parameter was significantly affected by superparasitism (Table 1). This means that both wasp groups had similar performance on the host eggs. Intrinsic rate of increase (r) of the two cohorts was 0.224 ± 0.004 and 0.234 ± 0.004 d^-1 in NSP and SP cohorts, respectively. No difference was observed between GRR and R₀ values in any cohort. All mortality occurred during the senescence period after oviposition, resulting in convex survivorship curves. On the other hand, age-specific fecundity exhibited a somewhat triangular shape in both cohorts, reaching its peak between the 19th and 20th day of the experiment (Figs. 1A and 1B). The sex ratio of offspring was 0.73 and 0.75 in NSP and SP cohorts, respectively. Life expectancy (e_x) of adult females at commencement of emergence was estimated to be 23.44 and 21.6 d for SP and NSP cohorts, respectively. Mean number of daily eggs showed no significant difference between NSP and SP cohorts (t = 1.05, df = 1,28, P = 0.43). The values were 6.58 ± 0.58 and 6.42 ± 0.55 in the cohorts mentioned above, respectively.

In the NSP cohort, the mean daily number of male offspring was more than in the SP cohort (Fig. 2A), while the number of female offspring was lower (Fig. 2B). However, no significant difference was observed between the sex ratios (t = 0.08, df = 1,28, P = 0.47).

Table 1 Stable population growth parameters of two cohorts of O. telenomicida singleton (NSP) and twin (SP).

Figure 1 Age-specific survival rate (l_x), and age-specific fecundity (m_x) of O. telenomicida, developed on E. integriceps eggs at 25°C. A) singleton wasps; B) twin wasps.

Figure 2 Age-specific progenies of O. telenomicida on E. integriceps egg at 25 °C. A) singleton wasps; B) twin wasps.

Females laid no eggs on the first day of their emergence. Oviposition continued for 7 days until death. The majority of eggs did not fertilize at senescence, leading to an increasing proportion of male progeny. The maximum and minimum number of host eggs parasitized by a female parasitoid was 103 and 26 eggs, respectively, and the maximum and minimum number of progenies per host egg was 2.13 and 1.16 per female, which were both recorded in NSP eggs. The maximum attack rate was 21/d.

No significant difference was observed between the NSP and SP cohorts regarding the daily number of eggs (11.07 ± 0.71 and 9.83 ± 0.65, respectively; t = 1.10; df = 1, 28; P = 0.36). Results showed that the daily fecundity was negatively related to total fecundity. Reproduction interval of O. telenomicida had no significant difference between the two test groups of wasps (t = 1.06, df = 1,28, P = 0.41). The durations were 5.12 ± 0.49 and 3.98 ± 0.39 days in the SP and NSP cohorts, respectively.

Discussion

Theoretically, O. telenomicida should be able to control E. integriceps adequately, given its more rapid population growth rate compared to the target host, E. integriceps (Iranipour et al., 2010). However, this may not be the case in natural settings, where insects are not confined and access to hosts is difficult (Iranipour et al., 2011; Koutsogeorgiou et al., 2024). Nonetheless, the high contribution of Ooencyrtus spp. to the parasitoid complex in egg traps is promising (Nozad-Bonab and Iranipour, 2010; Shafaei et al., 2011). Nozad-Bonab and Iranipour (2010) recorded the highest percentages of parasitism by T. grandis, O. fecundus, and O. telenomicida in wheat fields of Bonab County (respectively 33.33%, 30.61%, and 25.03% of the species), which represents a high potential for O. telenomicida. Of course, success of the O. telenomicida in sunn pest control, depends on many other factors such as its competition potential in presence of the other egg parasitoids (Nassiri et al., 2020; Hatami-Sadr et al., 2024; Jalal-Kor et al., 2024), ability to detect and find the hosts as well as their habitats (van Driesche and Bellows, 1996), density dependence (Hassell, 1978; Iranipour et al., 2011), presence of the alternative hosts particularly preferable ones (Iranipour and Vaez, 2021), relative profitability of the hosts and suitable synchrony between the parasitoid and the host (Jervis and Kidd, 1996; Iranipour, 2021). Fortunately, O. telenomicida has proven to be a superior competitor to other parasitoids, such as Telenomus costalimai. This is apparently due to a physical attack of competing larvae within the host egg (Conde and Rabinovich, 1979). Moreover, O. telenomicida can parasitize all stages of Trissolcus spp. (i.e., pupae, larvae, and eggs), and eliminate them inside the host egg (Safavi, 1973). T. grandis is the most tolerant species against weather changes (Iranipour et al., 2024); however, O. telenomicida has been adapted to harsh winters and dry summers or springs (Zatyaina and Klechkovskii, 1974). Despite the relatively good capacity of O. telenomicida for pest control and its ability to overcome other competitors via hyperparasitism, it actually plays a minor role in sunn pest control (Iranipour et al., 2011; Iranipour and Kharrazi Pakdel, 2012). A possible reason is the lack of proper synchronization with the host (Iranipour and Vaez, 2021).

In this study, it was found that superparasitism has no adverse effect on the efficacy and vitality of O. telenomicida, as both singleton and twins presented the same performance. This finding aligns with the results of Ahmadpour et al. (2013) and Iranipour et al. (2020) on O. fecundus. However, they observed some negative impacts at higher superparasitism levels (i.e., triplets and quadruplets). This may suggest that superparasitism has only minor negative impacts on these species and cannot be considered a significant factor in preventing biological control. The O. telenomicida can distinguish between parasitized and healthy eggs. Nevertheless, some females choose parasitized eggs for further oviposition, even when there are still a few healthy eggs (Ahmadpour et al., 2013). The reason may be that the wasp does not lose a considerable advantage by superparasitism. Recognition of parasitized eggs has already been reported for O. nezarae, which is realized by leaving an egg stalk on the surface of the host eggs. Wasps can distinguish these physical cues for eight days (Takasu and Hirose, 1988). Safavi (1973) suggested that females of O. telenomicida prefer non-parasitized eggs over parasitized ones. Ahmadpour et al. (2013) also showed that superparasitism occurs at a lower rate than expected from a random search, which may imply partial avoidance. It seems that Ooencyrtus species avoid laying their eggs only partially in hosts that are already clutched.

A comparison between the population growth parameters of O. telenomicida in this study and those of other egg parasitoids on the target pest E. integriceps may reveal their relative potential in controlling the sunn pest. The developmental time, longevity, generation time, net replacement rate (R₀), and intrinsic rate of increase (r) are often considered significant criteria for ranking a species' competitive potential. Still, in such a comparison, one must take sufficient care to ensure that the comparison was conducted under similar physical conditions, because variables such as host quality and temperature may have a profound effect on the parameter values. Overall, r is the most comprehensive parameter that summarizes all information in a single parameter. In terms of r, T. grandis (Amir-Maafi, 2000; Nozad-Bonab et al., 2014; Teimouri et al., 2019) and T. vassilievi (Iranipour et al., 2025b) are potentially more efficient control agents than O. telenomicida. The highest value for r was 0.368 and 0.367 d^-1, as recorded by Nozad-Bonab et al. (2014) and Teimouri et al. (2019) for T. grandis at 29 °C and 26 °C, respectively. On the other hand, O. fecundus, with a population growth rate of 0.252 (Ahmadpour et al., 2013), and T. djadetshkoe Rjachovskii, with a growth rate of 0.212 d^-1 (Abdi et al., 2017), are close to O. telenomicida. The difference in life history parameters refers primarily to the inherent differences among the species; however, the other factors such as physical conditions in which the wasps are reared (see Abdi et al. 2017 for a comprehensive discussion on intra-specific variation at different studies), size and quality of the host eggs (Asgari, 2004; Nozad-Bonab and Iranipour, 2013; BenaMolaei et al., 2015 a, b) and the number of generations may also be effective.

Both total fecundity and net replacement rate have been found to vary strongly in different studies. The highest total fecundity among the egg parasitoids of the sunn pest was 355.5 eggs, and the corresponding R₀ was 198 daughters per generation, as recorded for O. fecundus (Ahmadpour et al., 2013). Total fecundity was recorded as 200, 140-187, and 128 for T. grandis by Amir-Maafi et al. (2001), Teimouri et al. (2019), and Bazavar et al. (2015), 217-280 for T. vassilievi (Iranipour et al., 2025b), and 69.4 for T. djadetshkoe (Abdi et al., 2017). The corresponding R₀ values for those species were 158, 105-141, 85, 168-216, and 40, respectively. In addition, R₀ value for T. semistriatus was 130 (Asgari, 2004). Except for T. djadetshkoe (Abdi et al., 2017), the other species were more fecund than O. telenomicida in this study.

Among other parameters, the population growth rate is deeply sensitive to developmental time. A rapid development leads to a higher population growth rate. Additionally, generation time corresponds to developmental time. Hence, a comparison among developmental and/or generation times can provide valuable insight into the performance of a species. Furthermore, a parasitoid that develops faster may possess all resources before the delayed ones. However, the developmental rate of an insect is primarily influenced by temperature, as a slight rise in temperature can shorten developmental time by a few days. Therefore, any comparison must be done at the same temperature. Among the egg parasitoids of the sunn pest, T. grandis has a shorter developmental time compared to O. telenomicida. For example, in different studies, Amir-Maafi et al. (2001) recorded 10.9 days at 25 °C, Nozad-Bonab and Iranipour (2013) 11.7 days at 26 °C, and Teimouri et al. (2019) 10.8-11.1 days at 26 °C. In addition, the developmental time of Trissolcus rufiventris (Mayr) and T. simoni (Mayr) was 10.2 and 12.2 days for males and 10.5 and 12.4 days for females at 26°C, respectively (Kivan and Kiliç, 2006a), which are both shorter than those of O. telenomicida. The developmental time of relative species of O. fecundus at 26 °C (Ahmadpour et al., 2013), and T. vassilievi females at 25°C (Iranipour et al., 2015, BenaMolaei et al., 2015b) has been similar to O. telenomicida, however, in contrast to O. telenomicida, T. vassilievi is a protandrous species, hence, the developmental time of males lasted one day shorter. The mean developmental time of O. pityocampae was 21.4 days from egg to adulthood (Tiberi et al., 1991) which is the longest among the Ooencyrtus species. The generation time of T. grandis was shorter than that of O. telenomicida in all studies (Amir-Maafi, 2000; Nozad-Bonab et al., 2014; Teimouri et al., 2019), except for Bazavar et al. (2015), which reported a similar value. That of the T. vassilievi (Iranipour et al., 2025b) and T. djadetshkoe (Abdi et al., 2017) was close but slightly shorter, T. semistriatus close (Asgari, 2004), and O. fecundus (Ahmadpor et al., 2013) and T. vassilievi close but slightly longer than O. telenomicida in similar conditions. The differences arose from the developmental time and/or oviposition period of the species.

Lifetime is considered an effective factor in biological control. Often, it is believed that a parasitoid's longer longevity controls a pest population more effectively. Of course, it will be critical if the vulnerable stage of a host overlaps sufficiently with the duration of parasitism. The average lifespan of the female O. telenomicida was over a month, which is longer than 25.6 days recorded for female O. pityocampae (Safavi, 1973). The adult lifespan of T. grandis has been recorded as 38.5 d by Amir-Maafi (2000) and 38.6-41.1 d by Teimouri et al. (2019), which is slightly longer than that of O. telenomicida. It is 55.6 d for T. djadetshkoe (Abdi et al., 2017), and 26-32 d for females and 18-21 d for males of T. vassilievi (Iranipour et al., 2025b), although there are records up to 66 d for females, and 58 d for males of the latter species (BenaMolaei et al., 2015a; b). The high variability of longevity in different studies may reflect the effects of environmental conditions, such as host quality, temperature, and others. Therefore, it appears that longevity is not a suitable scale for comparing species, populations, and experimental treatments.

The observed sex ratio in the progeny of the two cohorts in this experiment was strongly female-biased (75%), whereas Safavi (1973) and Ahmadpour et al. (2013) recorded 50 and 55% female progeny for O. telenomicida and O. fecundus, respectively. Safavi (1973) and Tiberi et al. (1991) reported a temperature-dependent telytoky in O. pityocampae, such that females reproduced parthenogenetically (without the contribution of males) at temperatures below 25 °C, and males appeared only above 28-30 °C. Hatami-Sadr et al. (2024) and Jalal-Kor et al. (2024) observed the same phenomenon in O. fecundus, while a decreasing trend in the percentage of female progeny by age was observed in O. telenomicida, so that an initial 65-70% female progeny finally balanced to achieve an identical sex ratio.

In conclusion, O. telenomicida appears to be a promising egg parasitoid of the sunn pest, with the potential to prevent outbreaks of the sunn pest in augmentative release programs when released at suitable timing. Furthermore, superparasitism has no considerable adverse effect on it. However, in comparison to other egg parasitoids, it may be ranked as an inferior species due to a longer developmental and generation time, and lower parasitism and reproductive capacity compared to the majority of the egg parasitoids of the target pest. However, it is still capable of controlling sunn pest, because it has a higher population growth rate than its host.

Conflict of Interest

The authors state that there is no conflict of interest.

Acknowledgements

This research was supported financially by Urmia University as the MSc thesis of the first author, which is acknowledged hereby.

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