Life history of Neoseiulus agrestis (Karg) (Acari: Phytoseiidae) fed on the storage mite, Thyreophagus sp. (Acari: Acaridae) at different temperatures

The development and life history parameters of Neoseiulus agrestis feeding on the storage mite, Thyreophagus sp., were studied at three different temperatures of 20, 25, and 30 °C. The results show that juvenile development and oviposition period as well as reproductive potential of this predatory mite are significantly affected by the temperature. The development times of immature and the life expectancy of adults ranged from 11.36 to 6.06 days and 58.71 to 38.65 days, respectively, depending on the temperature. The average total number of eggs laid per female at 20 °C (27.21), 25 °C (46.38), and 30 °C (61.12) differed significantly from each other. The highest net reproductive rate (R0) was 51.95 (offspring/individual) at 30 °C, although there was no significant difference from that obtained at 25 °C (37.10). Furthermore, the highest intrinsic rate of increase (rm) is 0.286 day-1 at 30 °C. Moreover, the highest finite rate of increase (λ = 1.331 day-1) and the shortest mean generation time (T = 13.786 days) and doubling time (DT = 2.418 days) were also determined at 30 °C. Our results indicate that N. agrestis successfully completed immature development and can survive and reproduce at all temperatures tested. However, a number of biological traits of this predator are affected by the temperature on this food source. Finally, a temperature of 30 °C seems to be more suitable for mass rearing of this predator on Thyreophagus sp. Further studies should be carried out to determine the biological characteristics and life cycle parameters of N. agrestis on various important pests such as spider mites, whiteflies and thrips.


Introduction
Predatory mites belonging to the family Phytoseiidae (Acari: Mesostigmata) are one of the most widely utilized groups for the biological control of certain phytophagous mites and insect species (McMurtry et al. 2013). Although more than 2500 phytoseiid species are currently known, only a few have been studied with regard to their potential as biological control agents (Tsolakis et al. 2013; Knapp et al. 2018). On the other hand, knowledge of the life history and demographic parameters of phytoseiid mites is one of the most important steps for the evaluation of their potential on their prey (Tsolakis et al. 2016; Ben Chaaban et al. 2018. Previous studies have shown that the life history and demographic parameters of phytoseiid mites are differentially affected by several important factors such as temperature, relative humidity, host plant, prey species, age, and pesticide application (Sugawara et al. 2017; Tsolakis et al. 2019. Neoseiulus agrestis (Karg) was first described based on the material collected from soil in Germany (Karg 1960). It has been reported from a series of western Palearctic countries, but also in central Asia (Kazakhstan) and the USA (Demite et al. 2023). This species is a generalist predator that belongs to the Type III-e feeding habits from soil/litter habitats but may periodically move up onto low-growing plants (McMurtry et al. 2013). Although there has been limited knowledge on the biological control potential of N. agrestis, two Neoseiulus species, N. barkeri (Hughes) and N. cucumeris (Oudemans) both showing the same lifestyle, have been extensively utilized for the biological control of mites and especially thrips (Zhang 2003; Knapp et al. 2018). In addition, both N. barkeri and N. cucumeris are produced using several species of acarid mites as prey, and they are available commercially worldwide . Since N. agrestis is a parthenogenetic species and its male is not known so far, it's mass rearing may be easier and require less effort compared to sexual species (Khaustov et al. 2022; Moradi et al. 2023. Storage mites [Carpoglyphus lactis (L.) and Thyreophagus entomophagus (Laboulbène & Robin)] have been used as factitious prey for commercial production of different species of phytoseiid mites particularly Amblyseius swirskii Athias-Henriot since 2005 (Bolckmans and van Houten 2006; Fidgett and Stinson 2008; Massaro et al. 2016; McGregor et al. 2020; Pirayeshfar et al. 2021. The genus Thyreophagus is distributed worldwide, containing species occurring in stored food, house dust, bark, subcortical habitats, scale insect associations, and nests of wasps and bees . According to Fidgett and Stinson (2008), suitability of different storage mites was evaluated for A. swirskii. Successful development and reproduction of this predatory mite were reported on Thyreophagus entomophagus (Laboulbène & Robin) which can easily serve as a food source for the mass rearing of predatory mites. In this study, as a first step in determining the optimal temperature for mass rearing, the life history and demographic parameters of N. agrestis, fed on the storage mite Thyreophagus sp., were studied at three temperatures under laboratory conditions.

Mite colonies
Initial colonies of Thyreophagus sp. were obtained from the Institute of Environmental and Agricultural Biology (X-BIO), Tyumen State University, Tyumen, Russia. The mites were mass-reared in transparent plastic containers (12 X 8 X 4 cm) with a mesh ventilated cover (100 micrometers pore size). The containers were kept in desiccators with a saturated NaCl solution providing 90% relative humidity and incubated at 25 ± 1°C. The temperature and humidity conditions were monitored by using a data logger during the experiments. The rearing diet contained a yeast powder biomass (Pripravich, RU) (Fidgett and Stinson 2008). The predatory mite, N. agrestis was collected from steppe soil (top surface 2 cm) in Altai Republic, Russia (Khaustov et al. 2022). The stock culture of the predator was maintained in the plastic containers described above using Thyreophagus sp. as food source. The prey and the predator rearing units were kept separately in incubators (SANYO Electric Biomedical co., Japan) at 25 ºC and 90 ± 5% RH and 12:12 L:D. The predatory mites were reared for one to three generations, before being used in experiments.

Pre-adult duration and survival
The pre-adult duration (developmental time from egg to adult) and survival of the predators were individually observed by using transparent plastic containers (3 cm in diameter and 1.8 cm deep). The lid of the experimental test units was drilled (2 cm in diameter) and covered with a fine mesh (30 micrometers in size) to allow ventilation. More than 50 females of the predator obtained from the stock culture were transferred to experimental arenas using a brush (number 000) under a stereo microscope (Zeiss, Stemi-305, Germany). Subsequently, egg laying was observed in the arenas at two-hour intervals. Then one egg was transferred to each experimental unit using a brush. Sufficient amounts of Thyreophagus sp. (> 20 individuals) mixed with yeast powder were provided as a food source for the predators at daily intervals. In total, 20 replicates were used for each temperature. The duration of the immature stages including egg, larva, protonymph, and deutonymph were separately determined at three temperatures (20, 25 and 30 ºC, and a constant humidity 90 ± 5% RH and photoperiod 16:8 L:D), based on the observations conducted at 12-hour intervals.

Adult longevity and fecundity
The individuals which successfully reached adulthood were individually monitored at daily intervals to obtain the preoviposition, oviposition, and postoviposition periods as well as the number of eggs produced in the same experimental units and conditions described earlier.
The observations were finalized when the last individual of the original female had died. Therefore, longevity of females was also recorded.

Life history and population parameters
Even though N. agrestis is a parthenogenetic species and no males were observed in the population, its life history and population parameters were estimated by using age-stage, two-sex life table analysis program (Chi and Liu 1985). Because, the immatures were also considered for the life table analysis. The age-stage-specific survival rate (s xj ) (where x and j are age and stage, respectively); the age-stage specific fecundity (f xj ); the age-specific survival rate (l x ); the age-specific fecundity (m x ), adult preoviposition period (APOP), total preoviposition period (TPOP), and the life table parameters including the net reproductive rate (R 0 ) , intrinsic rate of increase (rm), finite rate of increase (λ), gross reproductive rate (GRR), DT doubling time and mean generation time (T) were calculated in the TWOSEX-MSChart computer program (Chi, 2020). The standard errors were estimated by using the bootstrap method, and the differences were determined with the paired bootstrap test (Efron and Tibshirani 1993). Although the temperature had a significant effect on its immature development, N. agrestis successfully reached adulthood at the three temperatures (Table 1). The duration of each developmental stage was significantly different from each other based on the temperature, except for larva at all temperatures and for deutonymph at 25 ºC and 30 ºC. No significant differences, however, were detected among the immature survival rates obtained at different temperatures tested (Table 1). Similar to the immature development, total pre-oviposition (TPOP), adult pre-oviposition (APOP), and longevity of N. agrestis were significantly affected by the temperature (Table 2). In contrast, no significant difference was detected among oviposition periods (OP) obtained at different temperatures. The shortest TPOP (7.59 days), APOP (1.53 days), OP (20.82 days) and total female longevity (38.65 days) were obtained at 30 ºC and these values were significantly different than those obtained at 20 ºC and 25 ºC, except OP. However, the OP obtained at 30 ºC (20.82 days) is still numerically lower than those obtained at the other two temperatures (21.69 days at 25 ºC and 22.21 days at 20 ºC). The highest total mean number of offspring produced per female was obtained at 30 ºC (61.12) followed by 25 ºC (46.38) and 20 ºC (27.21). In addition, these values are significantly different from each other. The highest intrinsic rate of increase (r = 0.286 day -1 ), finite rate of increase (λ = 1.331 day -1 ), reproductive rate (R 0 = 51.950 offspring/individual), and gross reproductive rate (GRR = 65.620 offspring/individual) were detected at 30 ºC and these values were significantly different from those obtained at the other two temperatures, except R 0 which was statistically similar to that obtained at 25 ºC (37.100 offspring/individual) (Table 3). In addition, the shortest mean generation time (T = 13.786 days), and doubling time (DT = 2.418 days) were also detected at 30°C, and these values were significantly higher than those obtained at the other two temperatures.

Life history and population parameters
The age-stage survival rate curves (Sxj) show the probabilities of survival rate of newly emerged N. agrestis individuals to age x and stage j ( Figure 1A). The variations in pre-adult Figure 1 A -Age-stage specific survival rate (Sxj) of Neoseiulus agrestis fed on Thyreophagus sp. at three different temperatures under laboratory conditions; B -Age-specific survival rate (l x ), age-specific fecundity (m x ), and age-specific maternity (l x m x ) of Neoseiulus agrestis fed on Thyreophagus sp. at three different temperatures under laboratory conditions. development rates resulted in overlaps of different developmental stages at three temperatures. The highest survival rates of females were 0.70, 0.80 and 0.85 at 20°C, 25°C, and 30°C, respectively. The age-specific survival rate (l x ) showed a similar pattern of gradual decline during the development at three different temperatures, but l x declined faster at 30°C compared to the other two temperatures ( Figure 1B). The first oviposition occurred at 20, 25 and 30°C , on the days 13 th , 8 th , and 6 th , respectively. The oviposition stopped at 20, 25 and 30°C, on the days 52 nd , 46 th , and 44 th , respectively. The highest fecundity (m x ) at 20, 25 and 30°C were recorded on the days 20 th (0.68 eggs/female), 13 rd (1.22 eggs/female) and 14 th (1.97 eggs/female), respectively. The age-stage-specific life expectancy (e xj ) of a newly emerged individual were 42.85, 37.20 and 33.55 days at 20, 25 and 30°C, respectively (Figure 2A). In general, the (e xj ) value obtained at 30°C was lower compared to the those obtained at other two temperatures, which demonstrated that life expectancies might be shorter at high temperatures. The highest age-stage-specific reproductive values (v xj ) of N. agrestis at 20°C, 25°C, and 30°C were detected on 15 th (8.70), 12 nd (10.51) and 10 th (12.21) days, respectively ( Figure 2B).

Discussion
Similar to many other insects and mites, the longevity and fecundity of adult females of N. agrestis are significantly affected by temperature. Previous studies reported that temperature is one of the most important abiotic factors that affect the life history and demographic parameters of phytoseiids (Tsoukanas et al. 2006; Vangansbeke et al. 2013; Yazdanpanah et al. 2022.
In this regard, knowledge about a suitable temperature is important and considered the first step for their mass rearing and usage in biological control. This study presents the first and preliminary data regarding the life history and demographic parameters of N. agrestis fed on Thyreophagus sp. Our results confirm that N. agrestis has thelytokous parthenogenesis since no males were produced by the females during the life history study (Kolodochka 1975). Parthenogenesis is common among not only phytoseiids but also other groups of mites (Oliver 1983). However, most phytoseiid species are believed to be arrhenotokous (males arise from unfertilized eggs) and pseudo-arrhenotokous where males arise from fertilized eggs but become haploids after inactivation or elimination of the paternal chromosome (Sabelis 1985; Hoy 1985. In contrast, thelytokous parthenogenesis is reported for a series of species including Amblyseius guatemalensis (Chant), A. herbicolus (Chant), A. parasundi (Blommers), N. agrestis, N. salish (Chant and Hansell), Typhlodromus transvaalensis (Nesbitt), Transeius herbarius (Wainstein) (Amitai et al. 1969; Kolodochka 1974, 1975; Hoy 1985; Akimov and Kolodochka 1991; Zhang and Zhang 2021. According to the results, offspring of N. agrestis could develop into adults when Thyreophagus sp. was provided as prey at all temperatures tested. Nevertheless, certain life history and demographic parameters were affected by the temperature. The immature developmental periods of N. agrestis obtained at 25ºC are more or less in line with those reported for another theylotkous phytoseiid mite, A. herbicolus fed on Carpoglyphus lactis (L.) at the same temperature (Zhang and Zhang 2021), except for the duration of larva and protonymph which are shorter in the current study. In addition, our results are also similar to those reported by Huang et al. (2013) for N. barkeri fed on Tyrophagus putrescentiae (Schrank) at 25 ºC. In contrast, Moradi (2023) reported generally lower immature developmental times, for N. neoagrestis fed on T. putrescentiae, a similar species to N. agrestis in terms of feeding habits and morphology. In addition, the immature developmental periods of N. agrestis found in this study were also longer than those reported for N. cucumeris females fed on C. lactis (Ji et al. 2015). Furthermore, much shorter immature developmental times were also reported for Neoseiulus longispinosus (Evans) (Rahman et al. 2013). These results clearly show that immature developmental periods of phytoseiid mites vary depending on predator species and their prey. Similar to the immature developmental times pre-oviposition, oviposition and total fecundity of N. agrestis adult females are also influenced by the temperature. Our results are also generally in line with those reported for Neoseiulus neoagrestis Khaustov & Döker by Moradi et al. (2023) and also for Neoseiulus californicus (McGregor) fed on Tetranychus urticae Koch by Gotoh et al. (2004). In contrast, the values for oviposition (21.69 days), longevity (45.31 days) and total fecundity (46.38 eggs/female) of N. agrestis found in this study at 25 ºC are much higher than those reported by Zhang et al. (2003) and Zhang (2021) for A. herbicolus fed on C. lactis at the same temperature. The authors reported oviposition (13.40 days), longevity (19.08 days) and total fecundity (21.6 eggs/female) for A. herbicolus. In addition, values found in the present study are also higher than those reported by Rahman et al. (2013) for N. longispinosus fed on Oligonychus coffeae (Nietner), except OP which is lower in N. agrestis. On the contrary, much higher values of oviposition are reported for N. cucumeris fed on C. lactis at the same temperature (Ji et al. 2015).
The intrinsic rate of increase (r m ), finite rate of increase (λ), reproductive rate (R 0 ) and gross reproductive rate (GRR) in the present study were higher than those in N. neoagrestis reported by Moradi et al. (2023) at all temperatures tested. In contrast, generation time (T), except at 30 ºC and doubling time (DT) observed in the current study are lower than those reported by Moradi et al. (2023). Although slightly higher intrinsic rate of increase (r m ) and finite rate of increase (λ) values are reported for N. californicus fed on T. urticae (red form), the net reproductive rate found in this study are higher than those reported for N. californicus (Gotoh et al. 2004).
In conclusion, this study reports for the first time the life history of N. agrestis, a promising biological control agent. Our results show that temperature is one of the key factor that affect the life history parameters of N. agrestis. In addition, as better life table parameters and shorter immature developmental times are obtained at 30°C, we suggest this temperature for the mass rearing of this predator on the prey Thyreophagus sp. Further studies should be conducted to determine life table parameters and biological control potential of N. agrestis against several pest species such as spider mites, thrips and whiteflies under laboratory and greenhouse conditions.