Background

Biological control is one of the most effective and successful control methods in greenhouses and fields in Integrated Pest Management (IPM) programs since the 1900s (Van Lenteren and Godfray 2005). The application methods of biological control are classical, augmentative and conservation. In the augmentative biological control, the natural enemies have to be commercially mass reared in bio-factories prior its release in the agroecosystem (De Puysseleyr 2014). This method is generally used in greenhouses, fruit orchards, vineyards, cotton, maize, and soybean and can be environmentally friendly control instead of chemical control (Uygun et al. 2016). More than 170 predators and parasitoids are commercially used globally, and 100 are applied with augmentative biological control. Especially professional production, new mass-rearing techniques, quality control protocols, shipment, and developed release methods help to spread the augmentative biological control and reach farmers adequately (Cock et al. 2010).

The Orius genus is considered as important generalist predators of many small soft-body arthropod pests which widely uses in augmentative biocontrol programs in various agroecosystems, especially greenhouses (Gerling et al. 2001). In addition, it can feed not only on thrips but also whiteflies, mites, aphids, and lepidopteran eggs (van Lenteren and Bueno 2003). Many studies indicated that the predatory bugs can be integrated with other biocontrol agents including some parasitoid wasps (Pirzadfar et al. 2020). Moreover, this predator is the zoo-phytophagous, which can feed on pollen and sap for survival (Armer et al. 1998). The minute pirate bug, Orius laevigatus Fieber (Hemiptera: Anthocoridae) is one of the most effective biological control agents commercially used in augmentative biological control programs in Europe.

Orius laevigatus is a successful predator that can feed on a wide range of prey. Alternative prey can be supplementary during the mass rearing of natural enemies, and nutritional contents of the preference of different prey by beneficial organisms are one of the critical factors (Evans et al. 1999). Some researchers have studied different prey preferences and life table parameters of Orius species (Arnó et al. 2008; Zuma et al. 2022). Generally, prey preferences and life table parameters of Orius species were done on different aphids, thrips, whitefly, or interactions of these prey species. In addition, Ballal et al. (2012) studied the predatory potential of two anthocorid species on two different mealybug species, Paracoccus marginatus Williams and Granara de Willink and Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae). In addition, different prey preferences (Aphids, mealybugs, and E. kuehniella) on Orius albidipennis were studied by Amer et al. (2021). Limited studies have been done on mealybugs and other potential prey preferences of O. laevigatus.

This study focused on the two-sex life table parameters of O. laevigatus on different prey of P. solenopsis, P. citri and Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). The alternative prey potential of mealybugs was observed in the laboratory conditions during this study. Number of daily and total laid eggs, APOP (Adult Pre-ovipositional period), TPOP (Total pre-ovipositional period), Ovipositional, and post-ovipositional periods, fecundity, and longevity of O. laevigatus, in addition, life table parameters were calculated on two-sex life table analysis (Chi et al. 2020). The primary aim of this study was to estimate the potential use of mealybugs in the mass-rearing of O. laevigatus. Moreover, fundamental studies on the potential use of O. laevigatus against two different mealybug species were determined at this study.

Methods

Planococcus citri and Phenacoccus solenopsis cultures

Mealybug cultures were lasted in climate rooms separately at 25 °C, 65 ± 10% R.H and 16: 8 (L: D) in the Biological Control Research Institute. Potato sprouts were used for the stock culture of the two mealybug species.

Orius laevigatus culture

The predatory bug culture was obtained from Biological Control Research Institute, E. kuehniella eggs and sugary water soaked in cotton were used as a food source in the mass rearing of this predator and Kalanchoe blossfeldiana Poelln. (Rosales: Crassulaceae) leaves were used as an ovipositional substrate in controlled climate rooms with above mentioned conditions. In addition, O. laevigatus was reared on P. citri and P. solenopsis for using in life table experiments.

Design of the experiment

Experiments were carried out with P. citri, P. solenopsis¸ and eggs of E. kuehniella separately. The newly hatched nymphs, which were reared on each prey separately, were placed into 9 mm Petri dishes and egg-hatching duration and immature stages of O. laevigatus (N1, N2, N3, N4, and N5) were recorded for each prey individually. After that, O. laevigatus individuals, one day age female and male, which completed their immature stages, were placed into plastic containers together. Each container included one female and one male of O. laevigatus. Moreover, mixed nymphs and adults of P. citri and P. solenopsis were given as prey daily for each experiment separately, and K. blossfeldiana leaves as ovipositional substrate were used for oviposition. In addition, the same experimental design was carried out for E. kuehniella eggs.

Experiments were done with 40 replications in controlled climate cabinets with above mentioned conditions for each prey separately. Counting was recorded daily for life table parameters of O. laevigatus on the three prey.

Life table analysis

The life table parameters of O. laevigatus, reared on P. solenopsis, P. citri, and E. kuehniella, were analysed by the computer program TWOSEX-MS Chart (Chi and Liu 1985; Chi 1988, 2018). The age-stage-specific fecundity (fxj), age-stage-specific survival rate (Sxj), age-specific fecundity (mx) and age-specific survival rate (lx), were calculated from the daily records of the survival and fecundity of all individuals. net reproduction rate (R0), finite rate of increase (λ), the intrinsic rate of increase (r), mean generation time (T), gross reproductive rate (GRR), and the number of female adults (Nf) were calculated in this study (Table 1). 100,000 bootstrap method was used for the calculation of means and standard errors. In addition, statistical differences between prey were determined with the “Paired bootstrap method” (p < 0.05) (Chi et al. 2022). All formulas used for analysis are given below in table (1):

Table 1 Parameters and equations in the life table analysis (Chi et al. 2022; Wei et al. 2020)
Full size table

Results

In this study, life table parameters of O. laevigatus were determined using three different prey species. The pre-adult period of O. laevigatus was 25.13 ± 0.26, 26.67 ± 0.33, and 13.17 ± 0.20 days when reared on P. solenopsis, P. citri, and E. kuehniella, respectively [df = 2,117; p = 0.0003]. The pre-adult duration was longer for O. laevigatus reared on mealybug species than for E. kuehniella. The egg-hatching period was shorter for O. laevigatus reared on E. kuehniella, and the duration of nymphal stages was longer for O. laevigatus reared on P. citri, and P. solenopsis. Additionally, this study revealed a shorter pre-adult period and longer adult longevity for O. laevigatus when reared on E. kuehniella. (Table 2, Figs. 1, 2, and 3). The immature and mature stages of Orius laevigatus showed statistically significant differences between three different prey in this study (p < 0.05) (Table 2).

Table 2 The immature and mature stages of Orius laeivgatus on different prey
Full size table
Fig. 1
figure 1

(a Age-stage specific survival rate (sxj), b Age-specific survival rate (lx), age-specific fecundity (mx), and age-specific maternity (lxmx) of O. laevigatus reared on E. kuehniella

Full size image
Fig. 2
figure 2

(a Age-stage specific survival rate (sxj), b Age-specific survival rate (lx), age-specific fecundity (mx), and age-specific maternity (lxmx) of Orius laevigatus reared on P. solenopsis

Full size image
Fig. 3
figure 3

(a Age-stage specific survival rate (sxj), b Age-specific survival rate (lx), age-specific fecundity (mx), and age-specific maternity (lxmx) of Orius laevigatus reared on P. citri

Full size image

This study showed that the APOP (Adult pre-ovipositional period) and TPOP (Total pre-ovipositional period) of O. laevigatus were longer when fed on P. citri and P. solenopsis than on E. kuehniella. Furthermore, the ovipositional period was twice as long as when E. kuehniella was used as a prey compared to P. solenopsis and P. citri. The worst performance in terms of oviposition was observed when P. citri was used as prey. The total fecundity of O. laevigatus was 129.73 ± 5.98, 42.6 ± 2.47, and 28.00 ± 1.69 [df = 2,117; p = 0.0001], and daily fecundity was 4.41 ± 0.08, 3.47 ± 0.08, and 7.4 ± 0.10 [df = 2,117; p = 0.0001] on E. kuehniella, P. solenopsis, and P. citri, respectively. Additionally, the adult longevity was 20.9 ± 0.47, 15.17 ± 0.31, and 14.03 ± 0.39 [df = 2,117; p = 0.0091] on E. kuehniella, P. solenopsis, and P. citri, respectively (Table 3). Based on these results, E. kuehniella was the most suitable prey for mass-rearing of O. laevigatus. Mealybug species were found to be ineffective for mass-rearing, but O. laevigatus may still be used as an alternative option in augmentative biological control against P. solenopsis. APOP, TPOP Oviposition, Postoviposition period, Total and daily fecundity of O. laevigatus showed statistically significant differences between three different prey in this study (p < 0.05) (Table 3).

Table 3 APOP ((Adult preoviposition period), TPOP (Total preoviposition period), Oviposition, Postoviposition period, Total and daily fecundity of Orius laevigatus on different prey
Full size table

Life table parameters of O. laevigatus were determined on the two different mealybug species and E. kuehniella. The net Reproduction rate (R0) was 57.23 ± 11.35, 17.27 ± 3.57, and 11.05 ± 2.30 [df = 2,117; p = 0.0005] on E. kuehniella, P. solenopsis, and P. citri, respectively. In addition, the intrinsic rate of increase (r) and finite rate of increase values (λ) was better on P. solenopsis (0.084 ± 0.006, 1.088 ± 0.007) than P. citri. Moreover, the mean generation time was 23.41 ± 0.30, 33.56 ± 0.30, and 34.42 ± 0.59 [df = 2,117; p = 0.0001] on E. kuehniella, P. solenopsis, and P. citri, respectively (Table 4). According to the results of this study, E. kuehniella showed the best performance in terms of life table parameters, and P. solenopsis may be used as a prey for mass-rearing of O. laevigatus, or this predator may be applied as an alternative biological control agent in greenhouses in the augmentative biological control against P. solenopsis. The age-specific survival rates (lx), age-specific fecundities of the total population (mx), and age-specific maternity (lxmx) of O. laevigatus reared on E. kuehniella, P. solenopsis, and P.citri, respectively were shown in Figs. (1, 2 and 3).The life table parameters of O. laevigatus showed statistically significant differences between three different prey in this study (p < 0.05) (Table 4).

Table 4 Life table parameters of Orius laevigatus on different prey
Full size table

Discussion

Prey choice is one of the most critical factors in the mass-rearing of predators. studies were conducted to determine the most suitable prey for the mass-rearing of O. laevigatus. Arnó et al. (2008) studied two different Orius species on Bemisia tabaci Genn. (Hemiptera: Aleyrodidae) and Franklinella Occidentalis Pergande. (Thysanoptera: Thripidae) for prey preference. The study showed that O. laevigatus and O. majusculus could feed on whitefly nymphs and eggs but prefered thrips when presented with whiteflies and thrips. Zuma et al. (2022) researched the effect of E. kuehniella eggs as an alternative prey and alyssum as a companion plant against Macrosiphum euphorbiae Thomas (Hemiptera: Aphididae) (aphid). According to the results of the study, E. kuehniella eggs and alyssum, a companion plant, can positively affect the O. laevigatus population. They suppressed the aphid population easily with this alternative option. In addition, different larval diets for E. kuehniella and their effects on O. laevigatus performance were studied, the CY diet (95% cornmeal + 5% yeast) for E. kuehniella, and the best results were obtained when O. laevigatus was fed with these eggs, regarding fecundity, longevity, and nymphal development (Pehlivan 2021). Prey preference of Orius niger Wolff (Hemiptera: Anthocoridae) was studied on Thrips tabaci Lindeman (Thysanoptera: Thripidae), Aphis gossypii Glover (Hemiptera: Aphididae) and Tetranychus urticae Koch (Acari: Tetranychidae) under laboratory conditions. The numbers of prey consumed recorded were: 0.54, 0.35 and 0.089 for T. tabaci, A. gossypii and T. urticae. (Salehi et al. 2011). Moreover, the predator–prey interactions for O. laevigatus and O. majusculus on three thrips species were studied, and the results showed that the reproductive parameters of two Orius species were positive. However, leaf-inhabitant thrips was more suitable than F. occidentalis (Rahman et al. 2022). Effects of three different temperatures (15, 25, and 35 °C) on life table parameters of O laevigatus and O. albidipennis on F. occidentalis were studied. Although the best performance for fecundity was obtained at 25 ℃ for both predators, predation activity was better at 35 ℃, and O. laevigatus consumed more individuals than O. albidipennis (Cocuzza et al. 1997). In addition, life table parameters of O. laevigatus on B. tabaci were observed and finite rate of increase (λ): 1.12 females/female/day, net reproduction rate (Ro): 20 females/female/generation, rm: 0.12, mean generation time (T): 25.7 days, gross reproductive rate (GRR): 46 insects/female/generation was found in this study (Hamdan 2012). Many studies conducted on different prey preferences and life table parameters of Orius species, and E. kuehniella, showed one of the best performances in terms of the mass-rearing of this predator. The results showed similar results for E. kuehniella with our study.

Furthermore, there are limited studies about using mealybug species as prey for anthocorid predators. Fabres and Ferrero (1980) detected the predation activity for Cardiastethus exiguus Poppius (Hemiptera: Anthocoridae) on the Cassava Mealybug (Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae)). Tohamy et al. (2008) determined O. albidipennis as a predator of Saccharicoccus sacchari Cockerell (Hemiptera: Pseudococcidae) (The pink sugarcane mealybug). Elbahrawy et al. (2020) conducted a study about the monitoring and management of P. solenopsis on green bean plants, and they found many predators and parasitoids during their surveys. O. laevigatus was recorded as a predator of P. solenopsis with other coccinellids and chrysopids predators. In addition, Orius species was recorded as a predator of mealybugs in studies (El Aalaoui and Sbaghi 2021). The predatory potential of Anthocoris muraleedharani Yamada and Blaptostethus pallescens Poppius (Hemiptera: Anthocoridae) on P. marginatus and P. solenopsis was studied under laboratory conditions. A. muraleedharani can feed with P. solenopsis but cannot feed with P. marginatus. B. pallescens fed with both P. solenopsis and P. marginatus. The longevity of B pallescens was reduced when fed with P. marginatus. Regarding higher adult longevity, shorter nymphal duration, and predatory potential, A. muraleedharani was better than B. pallescens (Ballal et al. 2012). The effects of different prey on O. albidipennis were studied, and E. kuehniella, A. craccivora, and P. citri were used as alternative prey and the results showed that the highest total fecundity was 112.7, 96.4, 55.42, and daily fecundity was 8.18, 5.24, and 3.06 on E. kuehniella, A. craccivora, and P. citri, respectively (Amer et al. 2021).

In general, aphids, mites, and whiteflies were used as an alternative prey for Orius species above studies (Venzon et al. 2002; Van Lenteren and Bueno 2003). In addition other anthocorid predators were studied by some researchers (Ballal et al. 2012). Mealybugs were not common prey for this predator. However, the results of this study showed that P. solenopsis may be better than P. citri in terms of life table parameters. In addition, the results of the life table parameters of O. laevigatus on P. citri were similar and matched up with Amer et al. (2021). The findings regarding the life table parameters of O. laevigatus feeding on E. kuehniella were consistent with previous studies conducted by Zuma et al. (2022). Moreover, it was determined that E. kuehniella emerged as the most suitable prey choice for mass-rearing purposes. Moreover, P. solenopsis was invasive and established in Türkiye since 2012 (Kaydan et al. 2013) therefore O. laevigatus may be an alternative predator for this mealybug species and it may be combined with other natural enemies after conducting further studies about the interactions between O. laevigatus and P. solenopsis.

Conclusion

This study determined the life table parameters of O. laevigatus on P. citri and P. solenopsis for the mass-rearing of the predator. Generally, E. kuehniella eggs were used for the mass-rearing of O. laevigatus. The most suitable prey was eggs of E. kuehniella. Although mealybug species had a lower potential when used as prey for O. laevigatus, P. solenopsis had better results than P. citri. Therefore, O. laevigatus may be used against P. solenopsis by combining with other predators and parasitoids in augmentative biological control programs. Further studies should be done to determine the predatory potential of O. laevigatus against P. solenopsis in laboratory and field conditions for the contribution to biological control in integrated pest management.