The influence of photoperiod on development and population growth performance of the Phytoseiulus persimilis fed on Tetranychus urticae

ABSTRACT Environmental factors, such as photoperiod, can play an important role in the development of mites. The influence of photoperiod (L:D = 4:20, 8:16, 12:12, 16:8 and 20:4) on the development and population parameters of the predatory mite, Phytoseiulus persimilis Athias-Henriot fed on two-spotted spider mite, Tetranychus urticae Koch was examined under laboratory conditions. Pre-adult development decreased with increasing photoperiod until 12 h, after which the development period progressively increased. Longevity of both sexes demonstrated significant differences throughout photoperiods, with the longest at 20:4 L:D and the shortest at 8:16 L:D. The highest value of mean total fecundity was 13.62 egg/female at 12:12 L:D photoperiod. The net reproductive rate (R0), the intrinsic rate of increase (r) and the finite rate of increase (λ), showed the highest value at 12:12 L:D. The R0, r and λ for P. persimilis increased with increasing photoperiod from 4:20 to 12:12 L:D, but decreased sharply at the 16:8 and 20:4 L:D treatments. Our findings indicate that photoperiod has a significant role in advancing the rate of development, survival rate, and reproduction for commercial production of P. persimilis, with a 12:12 photoperiod length recognized as the ideal period for commercial production in culture.


Introduction
Phytoseiulus persimilis Athias-Henriot is an important beneficial predatory mite that shows varying degrees of specialization on mites, particularly Tetranychus urticae Koch (McMurtry et al. 2013;Moghadasi et al. 2016).Phytoseiulus persimilis is a native natural enemy used on different crops to control mites with a worldwide distribution (Broufas et al. 2006;McMurtry et al. 2013).However, predatory mites are not as gluttonous as predatory insects; nevertheless, a short life cycle, high survival rate, and easy to mass rear mean they are important species used for biocontrol of T. urticae in IPM programmes (Moghadasi et al. 2016).
Phytoseiulus persimilis demonstrates all the life stages: the egg, larva, two nymph stages, and adult, with longevity varying according to prey species, temperature, and photoperiod.The predation rate of this species is about 700 eggs of two-spotted spider mite in their lifetime (Moghadasi et al. 2016).Some studies on the biology of P. persimilis, including the functional response, predation rate, life table, and influence of temperature on biology and oviposition, have been conducted (e.g., Amano and Chant 1977;Abad-Moyano et al. 2009;Guadalupe Rojas et al. 2013;Moghadasi et al. 2016).However, information on the effect of photoperiod on development and life table parameters is not available.
As P. persimilis is present throughout the year, easy to rear and maintain, and amenable to mass production, the species has been extensively utilized for pest control in outdoor and indoor environments (Zou et al. 2016).The successful use of P. persimilis in controlling two-spotted spider mite has been demonstrated in orchards and greenhouses (Huffaker et al. 1970;Van Lenteren 2003;Zhang 2003).Although some environmental conditions, such as photoperiod, are known to affect the life history traits of beneficial organisms (De Block and Stoks 2003;Omkar and Pathak 2006;Aksit et al. 2007;Pakyari and McNeill 2020), the optimal photoperiod for rearing P. persimilis has not yet been recognized.
Photoperiod is a foreseeable variable during every month of the year and acts as the basic signal for changing seasons, leading to changes in reproduction and growth of mite and insect species (Pakyari and McNeill 2020).Photoperiod is also one of the important regulation factors for diapause (Omkar and Pathak 2006).Many studies have indicated the effect of photoperiod on some aspects of biology, such as oviposition, feeding and population parameters (Whittaker and Kirk 2004;Pakyari and McNeill 2020).
Life tables are essential tools in population ecology as they provide comprehensive information on the development rate, reproduction, and survival of a population.Life table methodology and theory have been explored in most ecology textbooks (Carey 1993).Stage-specific consumption rate and the life table in the prey-predator model is worthy of investigation because as the predator age structure changes, consumption rates change due to nonpredatory stages (such as the egg and pupal stages).It is also valuable in applying predation theory to biocontrol programmes.Hassell (1978) indicated that the critical step in recognizing prey-predator interactions involves considering the age structure of both prey and predator.Nevertheless, most life tables only consider the contribution from the female component of the population (Birch 1948), omitting the contribution of males and their associated prey consumption rate.Historically, the traditional life table also did not consider stage differentiation.However, Chi (1988) proposed a new approach based on the age-stage two-sex life table.This method was used in many studies based on predators and parasitoids (Farhadi et al. 2011;Ding et al. 2020;Ou et al. 2021;Wang et al. 2022).In this study, the age-stage, two-sex life table approach was used to assess the effect of photoperiod on population parameters of P. persimilis fed on T. urticae.This result would guide us in determining the optimal photoperiod for commercial production of P. persimilis.

Rearing of prey and predator
Adults of P. persimilis and T. urticae were gathered from cucumber and bean greenhouses in the Pakdasht county, Tehran province.These were protected on detached bean leaves, which were placed upside down on a layer of dampened sponge in a plastic container (15 × 10 × 5 cm).The sponge borders were surrounded with dampened tissue to supply moisture and prevent P. persimilis from escaping.Ventilation was supplied by a 2 cm diameter hole drilled into the lid of the container and wrapped by fine mesh cloth to prevent the mites from escaping.The containers were held in a growth chamber at controlled conditions of 25 ± 0.5°C, 75 ± 5% RH, and a 16:8 (L:D) h.Every 2 days, P. persimilis individuals were transferred to a new container.The colony of predatory mites on T. urticae were kept for 3 months before being used for bioassays.

Test arena
Seedlings of Phaseolus calcaratus Roxburgh "Goli" were grown to the fourth-fifth leaf stage in 15-cm-diameter pots in the greenhouse.Tetranychus urticae were maintained on detached bean leaves (3 cm in diameter) with thin veins (Phaseolus vulgaris L. cv.Sunray).Test arenas were prepared from detached bean leaves (3 cm in diameter) with thin veins placed upside down on a layer of dampened sponge in plastic containers (1 cm deep × 6 cm in diameter).The sponge borders were surrounded with dampened tissue to supply moisture and prevent mites from escaping.Ventilation was supplied by a 2 cm diameter hole at the centre of the container lid and wrapped by fine cloth mesh to prevent the mites from escaping.

Experimental design
The laboratory experiments were performed at five constant photoperiods (4:20, 8:16, 12:12, 16:8 and 20:4 L:D), 75 ± 5% RH and 25 ± 0.5°C in controlled environment chambers (Binder KBWS 240).To calculate the effect of photoperiod on the development of P. persimilis, 50 eggs (<24 h old) laid by 20 pairs of adults and maintained at mentioned conditions were collected and transferred individually into the test arena.The container was maintained in each incubator under the mentioned conditions.Larvae were kept individually in a test arena, and 30 eggs of T. urticae were supplied daily as prey.The development and survival of P. persimilis were checked every 12 h.After the adult emergence, males and females were maintained as pairs.Each P. persimilis pair was supplied with 75 eggs of T. urticae every day.Oviposition and survival were recorded every 12 h until the death of the last predatory mite.Life-history parameters containing pre-oviposition, oviposition period, adult male and female longevity, total oviposition per female (fecundity), and sex ratio were monitored at each photoperiod.

Data analysis
The gathered data were analysed by the computer programme TWOSEX MSChart (Chi 2020) according to the age-stage, twosex life table theory (Chi and Liu 1985).Using the bootstrap resampling method with 100,000 iterations, the standard errors and variances of the life table parameters and population parameters were estimated.The differences between treatments were evaluated using the paired bootstrap test.Table 1 lists the computed population parameters together with their equations and definitions.
Table 1.Population parameters, their definitions, and equations used in calculations for the predatory mite Phytoseulus persimilis reared on eggs of Tetranychus urticae.

Parameter and equation
Definition Adult pre-ovipositional period: The period between the adult emergence and the first oviposition Total pre-ovipositional period: The period from birth to the first oviposition Age-stage specific survival rate: The probability that a newly laid egg will survive to age x and stage j 18 .n xj is the number of individuals to survive to age x and stage j, and n 01 is the number of newborn offspring used at the beginning of the life table study (Chi 1988).Net reproductive rate (R 0 ): The total number of offspring that an average individual (including females, males, and those that died in the immature stage) can produce during its lifetime (Goodman 1982).
The intrinsic rate of increase (r): The rate of natural increase in a closed population with constant age-specific survival and reproduction schedules and a stable age distribution.The population size will increase at the rate of e r per time unit.It is calculated by using the Euler-Lotka equation with age indexed from zero (Goodman 1982).
The finite rate of increase (λ): A multiplication factor of a population at each time unit.The population size will increase at the rate of λ per time unit (Goodman 1982).

Mean generation time (T):
T The period that a population requires to increase to R 0 -fold of its size as the time approaches infinity and the population settles down to a stable age-stage distribution (Goodman 1982).Age-stage specific life expectancy (e xj ): The lifespan that an individual of age x and stage j, is expected to survive (Chi 1988).
The reproductive value (v xj ): The contribution of an individual of age x and stage j to the future population (Chi 1988).

Result
The developmental time for each stage of P. persimilis at the five photoperiods are shown in Table 2. Photoperiod had a significant influence on the development of each stage, with pre-adult development found to decrease with increasing light period until 12:12 L:D, after which the development period progressively increased.The pre-adult development ranged from 4.98 to 7.85 days at 12:12 and 20:4 L:D photoperiods, respectively.Female and male adult durations demonstrated significant differences throughout photoperiods, the longest at 20:4 L:D (14.55 and 14.17 days for females and males, respectively) and the shortest at 8:16 L:D (8.53 and 9.46 days for females and males, respectively).The overall pre-adult survival rates at 8:16, 12:12, and 16:8 L:D were all ≥66% but significantly lower at 4:20 L:D.Longevity of both sexes showed significant differences throughout photoperiods with the longest at 20:4 L:D (22.36 and 22.08 days for females and males, respectively) and the shortest at 8:16 L:D (14.45 and 15.29 days for females and males, respectively) (Table 3).The adult preoviposition period (APOP) and total preoviposition period (TPOP) reached their highest values at 20:4 L:D.Oviposition period under 12:12 L:D was the longest (9.44 days).The highest value of mean total fecundity was 45.12 egg/female at 12:12 L:D.The sex ratio of offspring increased with increasing light period from 4:20 to 12:12 L:D, but decreased at the 16:8 and 20:4 L:D treatments (Table 3).
The s xj for P. persimilis allowed us to exactly determine the stage overlapping and differentiation of stages due to differences in development rates (Figure 1).The maximum S xj was recorded at 12:12 L:D.The l x , m x , l x m x and f xj for different photoperiods are presented in Figure 2. The maximum oviposition period was recorded at 12:12 L:D.The higher m x was observed at 12:12 L:D treatment (Figure 2).
The e xj of P. persimilis evaluated lifetime staging for age x and stage j was forecasted to live after age x at different treatments.The life expectancy for P. persimilis male and female was decreased with increasing light period up to 12:12 L:D, after which it increased (Figure 3).The v xj is illustrated in Figure 4.At 12:12 photoperiod, the maximum reproductive value was 7.01 at age 10.However, the minimum v xj was 3.89 at the age of 10 at 16:8 L:D.
The life table parameters of P. persimilis at five photoperiod treatments are listed in Table 4.The net reproductive rate (R 0 ), the intrinsic rate of increase (r), and the finite rate of increase (λ) showed the highest value at 12:12 L:D.R 0 , r and λ of P. persimilis increased with increasing light period from 4:20 to 12:12 L:D, but sharply decreased at 16:8 and 20:4 L:D.Mean generation time (T) was the lowest at 8:16 and 12:12 L:D and the highest at 20:4 L:D.

Discussion
Results achieved in this research provide valuable information on the life history traits and population parameters of P. persimilis fed on two-spotted spider mite eggs over various photoperiods.The current research demonstrated that P. persimilis can continue successful reproduction across various photoperiods, but different photoperiods greatly influenced fecundity and survival.
Compared to the age-stage two-sex life table technique, Huang and Chi noted that the female age-specific method produces a non-normal distribution and raises variances.They also pointed out that this technique might overestimate the variability of the population parameters.Errors related to the utilization of female age-specific life table in data analysis have been reviewed by Chi et al. (2020).The age-stage, two-sex life table technique indicated that P. persimilis is susceptible to photoperiod duration.The parameters R 0 , r and λ significantly increased from 4:20 to 12:12 L:D, but T demonstrated a significant increase with increasing photoperiod from 12:12 to 20:4 L:D.
The pre-adult development of P. persimilis decreased with increasing light period.Similarly, the immature development of Neoseiulus barkeri Hughes was decreased as the photoperiod  increased until 12:12 L:D then increased with prolonging photoperiod (Zou et al. 2016).The consequences of this research were similar, demonstrating that P. persimilis could develop faster at 12:12 photoperiod.There are many similarities between twospotted spider mites and phytoseiid diapause.Phytoseiid diapause is explained as fecundity arrest and phytoseiid mite species might be seen through winter (Morewood 1993).Phytoseiulus persimilis did not exhibit diapause in the current study and the culture utilized might be non-diapausing after frequent generations.Similar results were indicated in N. barkeri (Zou et al. 2016).With an important effect on the life table, photoperiod is a critical abiotic factor for many arthropods (Shah et al. 2011).The development time of T. urticae immature stages increase as the light period decreased (Yang et al. 2020), and this study demonstrates that development time is photoperiod-dependent.Such information will be helpful for field release and biocontrol of two-spotted spider mites in both fields and greenhouse conditions.Similar examinations with other phytoseiids revealed that the photoperiod affects the developmental rate in various manners.For example, Zou et al. (2016) indicated that N. barkeri development was modified between short and long days.Smith and Newsom (1970) showed that the development of N. fallacis German varies significantly between long and short-day photoperiods.Nevertheless, the development rate of Amblyseius brazilli El-Banhawy and A. swirskii Athias-Henriot was demonstrated to be slower under shorter periods than longer ones (El-Banhawy 1977;El-Tawab et al. 1982).
The conclusions of this study demonstrate that P. persimilis can continue to reproduce even under short day conditions; therefore, P. persimilis can be a good candidate for controlling two-spotted spider mites at short-day conditions (from autumn to spring, in indoor crops).At all photoperiod treatments, there were more females than males produced, however the percentage of females were significantly lower under short photoperiod lengths (60 and 61% at 4:20 and 8:16 L:D, respectively).Photoperiod was shown to effect oviposition by P. persimilis, with more eggs produced at a photoperiod of 12:12 L:D and lowest under 4:20 L:D).
Controlling the photoperiod can enhance the efficiency of mass rearing beneficial insect agents.The finding of this study highlights the crucial role of photoperiod in optimizing the reproductive performance and development of P. persimilis during mass rearing, with a 12:12 L:D regimen recognized as the optimum light regime for mass rearing in culture.

Figure 2 .
Figure 2. Age-specific survival rate (l x ), age-specific fecundity (m x ), age-specific maternity (l x m x ), and age-stage-specific fecundity (f xj ) of Phytoseiulus persimilis reared on the eggs of Tetranychus urticae at five photoperiods.

Figure 3 .
Figure 3. Age-stage-specific life expectancy (e xj ) of Phytoseiulus persimilis reared on the eggs of Tetranychus urticae at five photoperiods.

Figure 4 .
Figure 4. Age-stage-specific reproductive values (v xj ) for Phytoseiulus persimilis reared on the eggs of Tetranychus urticae at five photoperiods.

Table 2 .
Mean (± SE) development time (days) and survival rate of immature stages of Phytoseiulus persimilis reared on Tetranychus urticae eggs at five photoperiods.
Values followed by different letters within the same row are significantly different (paired bootstrap test, p < 0.05).Figure 1.Age-stage specific survival rate (s xj ) of Phytoseiulus persimilis reared on eggs of Tetranychus urticae at five photoperiods.

Table 4 .
Mean (±SE) of population parameters of Phytoseiulus persimilis reared on eggs of Tetranychus urticae at five photoperiods.