Systematic & Applied Acarology 22(3): 410–422 (2017) ISSN 1362-1971 (print) http://doi.org/10.11158/saa.22.3.7 ISSN 2056-6069 (online)

Article

Effect of temperature on life table parameters of Phytoseius plumifer () fed on Eotetranychus hirsti (Tetranychidae)

JAHANSHIR SHAKARAMI* & FERESHTEH BAZGIR Department of Plant Protection, Faculty of Agriculture, Lorestan University, Khoramabad, Iran. Corresponding author: Jahanshir Shakarami, Phone: +986633431917, Fax: +986633400289, E-mail: [email protected]

Abstract

Eotetranychus hirsti Pritchard & Baker (Tetranychidae) is one of the important pests of fig trees that is widely distributed in fig orchards of Iran. The predatory Phytoseius plumifer Canestrini & Fanzago is a phytoseiid mite on fig that can feed and reproduce on E. hirsti. The effect of four constant temperatures (20, 25, 30 and 35°C) on demographic parameters of P. plumifer fed on nymphal stages of E. hirsti was determined under laboratory conditions at 50 ± 5% RH and a photoperiod of 16:8 h (L: D). The total developmental time of immature stages of this predator decreased with increasing temperature from 20°C to 35°C, and varied from

17.13±0.23 to 6.55±0.19 days for females. The lower temperature threshold (Tmin) and thermal constant (K) for the total immature stages of this predator was estimated 10.33˚C and 166.67 degree-days by the ordinary linear model, 11.17˚C and 147.87 degree-days by the Ikemoto linear model, respectively. Female longevity was 67.79, 47.00, 35.11, and 27.42 days at 20, 25, 30 and 35°C, respectively. The highest values of total fecundity and daily fecundity were obtained at 25˚C (35.71±1.73 eggs) and 30˚C (1.57±0.02 eggs), respectively. The value of the −1 intrinsic rate of increase (rm) increased as increasing temperature from 20°C (0.064±0.0012 day ) to 30°C (0.180±0.0023 day−1), and then decreased at 35°C (0.153±0.0037 day−1). The highest and lowest values of the mean generation time (T) were 32.75±0.95 and 14.18±0.51 days, which were obtained at 20°C and 35°C, respectively. The results of this study revealed that of P. plumifer is effective predator of the fig spider mite and develops effectively at a broad range of temperatures.

Key words: , biology, temperature, life table, fecundity

Introduction

The fig is a fairly important world crop, with an estimated annual production of 1,077,211 tons of fruit. Iran is the fifth largest producer and exporter of figs, having produced more than 87,000 tons in 2012 (FAO 2013). There are 750 hectares of fig farms in Pol-e-Dokhtar region in south of Lorestan province, Iran (33˚30΄N, 48˚25΄E) with an average yield of 20 t/ha which is usually sent to other provinces and countries. The phytophagous mite Eotetranychus hirsti Pritchard & Baker is one of the spider from Tetranychidae family that is an important pest of fig orchards in Iran and other fig growing areas in the world (Baradaran et al. 2002). This mite for the first time was reported on fig trees from Coimbatore, Hyderabad and Pusa, India (Hirst 1926). Control of the mites in fig orchards in Iran is mainly based on the use of chemical pesticides (Khanjani and Haddad Irani-Nejad 2006). In 1938 Cherian reported fig spider mite caused severe problems and prevented ripping of fruits. This mite is the key pest of fig trees in Iran and reported from different regions (Beyzavi et al. 2013). Continuous application of chemical pesticides has harmful effects on environment and natural enemies; therefore, the use of nonchemical methods such as biological control for management of

410 © Systematic & Applied Acarology Society fig pests is absolutely vital. Phytoseiid mites are important biological control agents of phytophagous mites, thrips and whiteflies. They have been extensively used in biological control programs (Helle and Sabelis 1985; Lindquist et al. 1996; McMurtry and Croft 1997; Sabelis and Van Rijn 1997; Gerson et al. 2003). The predatory mite Phytoseius plumifer (Canestrini and Fanzago) has been reported from different countries in the world, and is also a common predator in fig orchards in Iran (Zaher et al. 1969; Sepasgozarian 1975; Castagnoli and Ligouri 1985; Tixier et al. 1998; Kamali et al. 2001). This predatory mite is closely associated with phytophagous mites, tetranychid and eriophyoid mites, and is one of the most abundant natural enemies and efficient predator of them (Rasmy and Elbanhawy 1974; Castagnoli and Ligouri 1985; Hajizadeh et al. 2002; Kouhjani-Gorji et al. 2008, 2009, 2012; Nadimi et al. 2009; Khodayari et al. 2013). Various studies have been conducted on different aspects of biological characteristics of P. plumifer on Tetranychus urticae Koch and Rhyncaphytoptus ficifoliae Keifer in Iran (Kouhjani-Gorji et al. 2008, 2009, 2012; Nadimi et al. 2009; Hamedi et al. 2010; Louni et al. 2014). Temperature is the main abiotic factor that has substantial effects on life history of pests and their natural enemies (Liu and Tsai 1998; Broufas and Koveos 2001; Gotoh and Nagata 2001; Gotoh et al. 2004; Kouhjani-Gorji et al. 2009; Ullah et al. 2012; Bazgir et al. 2015). In the field of biological control, temperature is useful factor for the selection of natural enemies that are best adapted to the conditions that favor the target pest (Obrycki and Kring 1998). A survey of the literature indicated that no information was available concerning the development and life table parameters of P. plumifer with fed on E. hirsti. Studies on biological characteristics of this predator at different temperatures are few (Nawar et al. 2001; Kouhjani-Gorji et al. 2008, 2009, 2012; Rasmy et al. 2011). Therefore, the aim of the current study was to investigate the effect of different temperatures on life table parameters (e.g. survival, adult longevity, fecundity, and population growth parameters) of P. plumifer fed on E. hirsti under laboratory conditions, and the results of this research can be useful in the field of biological control of fig spider mite.

Materials and methods

Stock cultures of predator and prey In June 2015, P. plumifer specimens were originally collected from fig orchards infested by E. hirsti in Khorramabad, Iran. The predators were conveyed to the laboratory and reared on the fig leaf disks infested by a combination of different developmental stages of E. hirsti in experimental units. The predators were individually transferred to the leaf disks with a suitable paintbrush, and fed daily with immature stages of E. hirsti. Mites were transferred to new and fresh leaf disks every 2 weeks or at shorter intervals. Prior to using the predatory mites in experiments, they had been reared for several generations. The Agricultural faculty of Lorestan University, southwestern Iran, was the place where fig leaves infested with E. hirsti were collected from fig orchards during the summer 2015. Then, the infested leaves were conveyed to laboratory condition. Afterwards, E. hirsti were reared on fig leaves in laboratory condition at 27 ± 1°C, 50 ± 5% RH and 16:8 h (L:D) photoperiod. E. hirsti reared in laboratory were utilized as prey in experiments.

Experimental units and conditions The experiments were carried out in the laboratory at four constant (±1˚) temperatures (20, 25, 30 and 35˚C), 50 ± 5% RH and a photoperiod of 16:8 (L: D) hours. Temperatures used in this study were based on the temperature range of fig production area at Lorestan province. The experiments were run utilizing arenas composed of a piece of fig leaf (40 mm in diameter), which was placed upside

2017 SHAKARAMI & BAZGIR: EFFECT OF TEMPERATURE ON PHYTOSEIUS PLUMIFER 411 down on water-saturated foam mat covered with wet filter paper, inside plastic Petri dishes (60 mm in diameter) with a hole in its centre (10 mm in diameter) covered with fine nylon mesh to allow ventilation. In order to keep the leaves fresh and preventing the mites from escaping, these arenas were placed in the larger Petri dishes (90 mm) filled with water. The predatory mites were transferred to new arenas every 2 or 3 days.

Development, reproduction and survival In each temperature to determine the developmental time, sixty gravid females of P. plumifer were taken randomly from the stock culture and placed in the rearing units with some prey mites. After 12 hours, eggs laid by P. plumifer were transferred to new rearing units (one in each unit). To determine the duration of the immature stages (egg, larva, protonymph and deutonymph) of this predator, development from egg to adult stage were observed at 24 h intervals and monitored during the developmental time. Every day E. hirsti were added to each experimental unit to provide sufficient prey for P. plumifer. When the female was in the last day of the deutonymphal stage, it was transferred into the each experimental unit accompanied with a single young male, and pre- oviposition, oviposition and post-oviposition periods, female and male longevity, fecundity, offspring sex ratio and mortality were determined. If necessary, males that happened to drown in the wet filter paper or died were replaced by new ones, but females died because of improper handling were excluded from data analysis.

Linear model The ordinary linear model and Ikemoto model were used to predict the developmental rate, estimate the lower temperature threshold (Tmin) and thermal constant (K) of P. plumifer. Linear models have been frequently used in similar studies for estimate the lower temperature threshold and thermal constant (Tsoukanas et al. 2006; Haghani et al. 2007; Ganjisaffar et al. 2011). The linear models formulas are as follows:

Dr = a + bT

Ordinary linear (Simpson 1903)

Dt.T = K + Dt

Ikemoto linear (Ikemoto and Takai 2000)

Where Dt is the developmental time (days), Dr is the developmental rate obtained as the reciprocal of the developmental days (1/days) at temperature T, T is the temperature (°C), a is the intercept and b is the slope of the linear function. In the ordinary linear model, the lower temperature threshold

(Tmin) and the thermal constant (K) (cumulative degree-days) for immature stages of P. plumifer were calculated as Tmin = -a/b and K = 1/b, respectively (Campbell et al. 1974).

Population growth parameters The life table was constructed considering the females of the cohort studied. Using age-specific survival rate (lx) and age-specific fecundity (mx) life table, population growth parameters including net reproductive rate (R0), mean generation time (T), doubling time (DT), intrinsic rate of natural λ increase (rm) and finite rate of increase ( ) were calculated using the methods recommended by Birch (1948).

Data analysis Data of developmental time, survivorship, fecundity and adult longevity of P. plumifer were tested for normality by Minitab 14 software (Minitab 2004). All data were normally distributed and

412 SYSTEMATIC & APPLIED ACAROLOGY VOL. 22 analyzed with one-way analysis of variance (ANOVA) (Proc GLM, SAS Institute 2003) followed by Tukey’s range test (α = 0.01). The ANOVA and mean comparison were carried out using the SAS v.9.1 software (Proc GLM, SAS Institute 2003). Tests of significance for population level life table parameters among the different temperatures were conducted using the jackknife procedure (Meyer et al. 1986; Maia et al. 2000). In this procedure, jackknife pseudo-values of each life table parameter were calculated for n females by following equation: A(j) = n × A(all) - (n - 1) × A(i) Where A(j) is the jackknife pseudo-value, n is the number of females, A(all) is the calculated life table parameters for all females and A(i) is the calculated parameters for (n−1) females. Various λ population growth parameters including: rm, R0, T, and DT were inserted in this equation instead of “A”. Subsequently, the mean values of n -1 jackknife pseudo-values for each temperature were analyzed using one-way ANOVA and if significant differences were detected, a Tukey’s range test was run (P< 0.01). The obtained sex ratios of progeny were compared to the expected ratio of 1:1 by a Chi-square test (χ2, P<0.05). The Student t-test was used to determine the significant difference between the duration of immature stages of males and females (P<0.05). The Weibull frequency distribution was used to describe the age-specific survival of P. plumifer. The probability that an individual lives at least to time t was estimated by fitting survivorship schedules (lx) of P. plumifer to the following equation (Pinder et al. 1978): S(t) = exp[-(t/b)c] t > 0 Based on this model, t is age (day), b is the scale parameter that is inversely related to the mortality rate and c is the shape parameters that allow the model to produce survival distribution of different forms, from exponential to an extreme inverted sigmoid shape (Deevey 1947; Pinder et al. 1978).

Results

Developmental time The development times of immature stages for males and females of P. plumifer fed on E. hirsti at four different temperatures are demonstrated in Table 1. Temperature had a significant influence on incubation (F = 103.53; df = 3,122; P<0.0001), larval (F = 36.94; df = 3,122; P<0.0001), protonymphal (F = 177.97; df = 3,122; P<0.0001), deutonymphal (F = 207.53; df = 3,122; P<0.0001), and total immature (F = 564.47; df = 3,122; P<0.0001) periods of females. The deutonymphal stage was the longest for each temperature tested, decreasing from 6.25 ± 0.17 days at 20°C to 2.30 ± 0.12 days at 35°C and the larval stage was the shortest at all temperatures and varied from 1.42 ± 0.10 days at 20˚C to 0.52 ± 0.05 day at 35˚C (Table 1). Duration of the whole immature phase (egg to adult emergence) decreased with increasing temperature from 20˚C (17.13 ± 0.23 days) to 35˚C (6.55 ± 0.19 days) (Table 1). Also, temperature had a significant effect on incubation (F = 77.12; df = 3,79; P < 0.0001), larval (F = 22.58; df = 3,79; P < 0.0001), protonymphal (F = 100.13; df = 3,79; P<0.0001), deutonymphal (F = 218.66; df = 3,79; P<0.0001) and overall immature (F = 461.73; df = 3,79; P<0.0001) periods of the males. Total developmental time in males decreased with increasing temperature from 20°C to 35°C (Table 1). Also, the males developed faster than females at temperature of 20˚C (T = 3.24; P = 0.002), but at 25˚C (T = 1.39; P = 0.171), 30˚C (T = 1.36; P = 0.181) and 35˚C (T = 1.32; P = 0.193) there were no difference between the developmental times of males and females.

2017 SHAKARAMI & BAZGIR: EFFECT OF TEMPERATURE ON PHYTOSEIUS PLUMIFER 413 TABLE 1. Developmental time (day ± SE) of Phytoseius plumifer (female and male) fed on nymphal stages of Eotetranychus hirsti at four constant temperatures, 50 ± 5% RH and 16: 8 h (L:D) photoperiod.

Temperature (°C) Developmental stage 20 25 30 35 Female Egg 4.17 ± 0.13 a 2.38 ± 0.10 b 1.79 ± 0.09 c 1.57 ± 0.11 c

Larva 1.42 ± 0.10 a 1.03 ± 0.05 b 0.83 ± 0.04 b 0.52 ± 0.05 c

Protonymph 5.29 ± 0.13 a 3.21 ± 0.08 b 2.45 ± 0.08 c 2.17 ± 0.11 c

Deutonymph 6.25 ± 0.17 a 3.38 ± 0.10 b 2.68 ± 0.08 c 2.30 ± 0.12 c

Immature stages 17.13 ± 0.23 a 10.00 ± 0.19 b 7.75 ± 0.14 c 6.55 ± 0.19 d

Male Egg 3.83 ± 0.12 a 2.35 ± 0.13 b 1.63 ± 0.11 c 1.45 ± 0.14 c

Larva 1.26 ± 0.09 a 1.00 ± 0.06 ab 0.84 ± 0.05 b 0.48 ± 0.05 c

Protonymph 4.91 ± 0.14 a 3.08 ± 0.15 b 2.32 ± 0.13 c 2.05 ± 0.11 c

Deutonymph 6.09 ± 0.12 a 3.20 ± 0.12 b 2.63 ± 0.11 c 2.19 ± 0.13 c

Immature stages 16.09 ± 0.23 a 9.63 ± 0.19 b 7.42 ± 0.20 c 6.17 ± 0.22 d

Note: Means followed by different letters within the same row for each sex are significantly different (P < 0.01, Tukey’s test).

Linear models

The estimated values of the lower temperature threshold (Tmin) and thermal constant (K) by two linear models for each developmental stage of P. plumifer female and male are presented in Table 2. In both linear models, the lower temperature threshold was minimum for the stage of protonymph. The maximum value of estimated Tmin was for larval stage by the ordinary linear and deutonymphal stage by the Ikemoto model. Tmin for different stages of P. plumifer calculated from 8.83°C to 12.04°C for females and from 8.74°C to 11.93°C for males by the ordinary linear model, and from 10.35°C to 11.94°C for females and from 9.97°C to 12.15°C for males by the Ikemoto model (Table 2). As shown, the maximum value of estimated thermal constant (K) was for protonymphal and deutonymphal stages, and minimum value was for larval stage, in both linear models. The value of the thermal constant for the total immature stages was calculated 166.67 degree-days for females and 142.86 degree-days for males by the ordinary linear model, and 147.87 degree-days for females and 142.30 degree-days for males by the Ikemoto model (Table 2).

Reproduction parameters The reproduction parameters of P. plumifer are presented in Table 3. According to the obtained results, effect of temperature was highly significant on the different reproductive parameters, including pre-oviposition period (F = 70.29; df = 3,109; P<0.0001), oviposition period (F = 29.46; df = 3,109; P<0.0001), post-oviposition period (F = 44.11; df = 3,109; P<0.0001), daily fecundity (F = 130.83; df = 3,109; P<0.0001) and total fecundity (F = 19.51; df = 3,109; P<0.0001) of P. plumifer. Duration of the pre-oviposition period varied from 4.84 ± 0.32 to 1.77 ± 0.15 days. In general, the oviposition period decreased with increasing temperatures, from 20°C to 35°C, and the shortest period was found at 35°C (16.19 ± 1.18 days). Duration of the post-oviposition period significantly decreased with increasing temperature from 20°C to 35°C, the longest period was observed at 20° C

414 SYSTEMATIC & APPLIED ACAROLOGY VOL. 22 at more than 28 days and the shortest was found at 35°C (9.46 ± 0.55 days). The highest value of total fecundity was observed at 25˚C (35.71 ± 1.73 eggs) and the value of this parameter was lower at temperatures out of this range. The maximum number of eggs per female per day (1.57 ± 0.02 eggs) was recorded at 30˚C and the minimum value (0.73 ± 0.02 eggs per female per day) at 20˚C. All the temperatures had a significant effect on the longevity (F = 107.98; df = 3,109; P<0.0001) and life span (F = 163.04; df = 3,109; P<0.0001) of this predator females. As the temperature increased, the longevity period decreased and reached to its lowest value (27.42 ± 1.19 days) at 35°C. The life span decreased from 84.89 ± 2.74 to 34.06 ± 1.14 days as temperature increased from 20°C to 35°C (Table 3).

TABLE 2. The regression equation, lower temperature threshold (Tmin) and thermal constant (K) estimated by two linear regression for various immature stages of Phytoseius plumifer fed on Eotetranychus hirsti.

2 Model Developmental stage Tmin (°C) K (degree-days) Regression equation R Ordinary linear Female

Egg 09.93 ± 1.74 37.04 ± 3.20 Dr = -0.268 + 0.027 T 0.971

Larva 12.04 ± 0.82 12.82 ± 2.88 Dr = -0.939 + 0.078 T 0.922

Protonymph 08.83 ± 0.45 55.56 ± 4.09 Dr = -0.159 + 0.018 T 0.971

Deutonymph 10.00 ± 0.43 55.56 ± 4.01 Dr = -0.180 + 0.018 T 0.965

Immature stages 10.33 ± 0.23 166.67 ± 6.72 Dr = -0.062 + 0.006 T 0.983 Male

Egg 10.79 ± 0.68 34.48 ± 3.11 Dr = -0.313 + 0.029 T 0.974

Larva 11.93 ± 1.08 12.35 ± 3.68 Dr = -0.966 + 0.081 T 0.852

Protonymph 08.74 ± 0.63 52.63 ± 5.00 Dr = -0.166 + 0.019 T 0.977

Deutonymph 10.05 ± 0.54 52.63 ± 4.29 Dr = -0.191 + 0.019 T 0.964

Immature stages 09.43 ± 0.25 142.86 ± 6.35 Dr = -0.066 + 0.007 T 0.990 Ikemoto Female Egg 11.65 ± 1.30 34.03 ± 3.48 DT = 34.03 + 11.65 D 0.976 Larva 10.77 ± 2.87 14.08 ± 2.88 DT = 14.08 + 10.77 D 0.876 Protonymph 10.35 ± 1.46 49.94 ± 5.12 DT = 49.94 + 10.35 D 0.962 Deutonymph 11.94 ± 1.48 48.98 ± 5.88 DT = 48.98 + 11.94 D 0.970 Immature stages 11.17 ± 1.14 147.87 ±12.68 DT = 147.87 + 11.17 D 0.980 Male Egg 11.58 ± 1.07 31.93 ± 2.66 DT = 31.93 + 11.58 D 0.983 Larva 10.84 ± 4.77 13.34 ± 4.48 DT = 13.34 + 10.84 D 0.721 Protonymph 09.97 ± 1.32 48.32 ± 4.33 DT = 48.32 + 09.97 D 0.966 Deutonymph 12.15 ± 1.53 46.49 ± 5.88 DT = 46.49 + 12.15 D 0.969 Immature stages 10.99 ± 0.91 142.30 ± 9.62 DT = 142.30 + 10.99 D 0.986

In all the tested temperatures, the sex ratio of P. plumifer was female biased and varied from 52 to 67% daughters, with the highest value recorded at 30˚C. Significant difference was observed with the expected ratio of 1:1 at 30°C (χ2 = 5.952; df = 1; P = 0.015), but at 20°C (χ2 = 0.080; df = 1; P = 0.777), 25°C (χ2 = 3.438; df = 1; P = 0.064) and 35°C (χ2 = 1.288; df = 1; P = 0.256) there was no significant difference with the expected ratio of 1:1.

2017 SHAKARAMI & BAZGIR: EFFECT OF TEMPERATURE ON PHYTOSEIUS PLUMIFER 415 TABLE 3. Mean (±SE) pre-oviposition, oviposition and post-oviposition periods, adult longevity, life span, fecundity, daily fecundity and sex ratio of Phytoseius plumifer females fed on nymphal stages of Eotetranychus hirsti at four constant temperatures, 50 ± 5% RH and 16: 8 h (L:D) photoperiod.

Temperature (°C) Parameters 20 25 30 35 Pre-oviposition 4.84 ± 0.32 a 3.13 ± 0.12 b 1.95 ± 0.08 c 1.77 ± 0.15 c Oviposition 34.84 ± 2.08 a 26.39 ± 1.21 b 21.46 ± 1.05 bc 16.19 ± 1.18 c Post-oviposition 28.11 ± 2.25 a 17.48 ± 1.18 b 11.70 ± 0.67 c 9.46 ± 0.55 c Female longevity 67.79 ± 2.64 a 47.00 ± 1.42 b 35.11 ± 1.16 c 27.42 ± 1.19 d Female life span 84.89 ± 2.74 a 56.97 ± 1.50 b 42.91 ± 1.15 c 34.06 ± 1.14 d Fecundity 25.42 ± 1.72 b 35.71 ± 1.73 a 33.54 ± 1.57 a 20.19 ± 1.29 b Daily fecundity 0.73 ± 0.02 c 1.36 ± 0.03 b 1.57 ± 0.02 a 1.28 ± 0.04 b Sex ratio (F/F + M) 0.52 0.63 0.67 0.58

Note: Means followed by different letters within the same row for each sex are significantly different (P < 0.01, Tukey’s test).

Age-specific survival and fecundity rate

The age-specific survival rate (lx) and age-specific fecundity rates (mx) of P. plumifer females at different temperatures are given in Figure 1. The specific survival rate (lx) started to decline at earlier ages with increasing temperature from 20 to 35˚C. This rate at the time of adult emergence, recorded 0.77, 0.89, 0.95 and 0.86 at 20, 25, 30 and 35˚C, respectively. The estimated value of the c parameter (>1) by Weibull function showed that the survival curve of P. plumifer was type I at all temperatures tested (Table 4). Also, the values of the respective parameters and coefficients of goodness of fit of this function are presented in Table 4.

TABLE 4. Goodness of fit and respective parameters of the Weibull frequency distribution fitted to age-specific survivorship (lx) of Phytoseius plumifer fed on Eotetranychus hirsti at four constant temperatures. Parameters Temperature (˚C) 20 25 30 35 R2 0.87 0.90 0.98 0.93

2 R adj 0.87 0.90 0.98 0.92 b 80.57 57.47 44.61 32.64 c 1.223.775.342.69

As shown in Figure 1, at 20, 25, 30 and 35˚C, the first oviposition occurred on days 15, 9, 7 and 6, respectively, and daily egg production peaked on the 29th day at 20°C (0.49 eggs), 16th day at 25°C (1.18 eggs), 12th day at 30°C (1.37 eggs) and 12th day at 35°C (1.03 eggs). The lowest and highest values of fecundity rates (mx) occurred at 20 and 30°C, respectively.

Demographic parameters The estimated life table parameters for P. plumifer at four constant temperatures are presented in

Table 5. The results showed that as temperature increased, the intrinsic rate of increase (rm) (F = 326.92; df = 3,109; P<0.0001) and finite rate of increase (λ) (F = 303.66; df = 3,109; P<0.0001) significantly increased and were highest at 30˚C (0.180 and 1.198 day-1, respectively), then decreased at 35°C and reached 0.153 ± 0.0037 day-1 and 1.165 ± 0.0043 day-1, respectively. The net

416 SYSTEMATIC & APPLIED ACAROLOGY VOL. 22 reproductive rate (R0) varied from 8.05 ± 0.54 to 20.68 ± 0.97 females/female, and the highest value was recorded at 30˚C (F = 55.55; df = 3,109; P<0.0001). The average generation time (T) decreased from 32.75 ± 0.95 to 14.18 ± 0.51 days as temperature increased from 20°C to 35°C (F = 189.56; df = 3,109; P<0.0001). The population doubling time (DT) was significantly different at temperatures tested (F = 581.03; df = 3,109; P<0.0001). The value of DT decreased as the temperature increased from 20°C (10.87 ± 0.20 day) to 30°C (3.84 ± 0.05 day), then slightly increased at 35°C (4.53 ± 0.11 day) (Table 5).

TABLE 5. Population growth parameters (±SE) of Phytoseius plumifer females fed on nymphal stages of Eotetranychus hirsti at four constant temperatures, 50 ± 5% RH and 16: 8 h (L:D) photoperiod.

Parameters Temperature (°C) 20 25 30 35 Net reproductive rate (female offspring 8.05 ± 0.54 b 18.45 ± 0.89 a 20.68 ± 0.97 a 8.75 ± 0.56 b per female) Intrinsic rate of increase (day−1) 0.064 ± 0.0012 d 0.138 ± 0.0018 c 0.180 ± 0.0023 a 0.153 ± 0.0037 b Mean generation time (day) 32.75 ± 0.95 a 21.17 ± 0.48 b 16.80 ± 0.33 c 14.18 ± 0.51 d Doubling time (day) 10.87 ± 0.20 a 5.03 ± 0.07 b 3.84 ± 0.05 d 4.53 ± 0.11 c Finite rate of increase (day−1) 1.066 ± 0.0013 d 1.148 ± 0.0021 c 1.198 ± 0.0028 a 1.165 ± 0.0043 b

Note: Means followed by different letters within the same row are significantly different (P < 0.01, Tukey’s test).

FIGURE 1. The age-specific survival rate (lx) and age-specific fecundity rates (mx) of Phytoseius plumifer females fed on nymphal stages of Eotetranychus hirsti at four constant temperatures, 50 ± 5% RH and 16: 8 h (L:D) photoperiod.

Discussion

This study was the first to evaluate the development and biological parameters of P. plumifer on fig spider mite, E. hirsti. Our results showed that this predator developed successfully over the range of

2017 SHAKARAMI & BAZGIR: EFFECT OF TEMPERATURE ON PHYTOSEIUS PLUMIFER 417 20–35˚C. The results of this study provided biological information that represents the first step for the evaluation of P. plumifer as possible control agent of E. hirsti in fig orchards. In a previous work, effect of different temperatures on the demographic parameters of this predator was studied on corn pollen and nymphal stages of T. urticae (Kouhjani-Gorji et al. 2008, 2009, 2012). Temperature had a significant effect on developmental time of various immature stages, as when temperature increased from 20 to 35˚C, total developmental time varied from 17.13 to 6.55 days. Kouhjani-Gorji et al. (2008) reported that P. plumifer fed on T. urticae for complete juvenile development, required 15.9 days at 20˚C and 5.3 days at 35˚C. The diversity in development time of P. plumifer at similar temperatures was attributed to factors such as diet (prey) and host plants. Total developmental time at 25˚C reported for P. plumifer on R. ficifoliae (Louni et al. 2014) and on T. urticae (Rasmy et al. 2011) was 8.73 and 9.80 days, respectively. Lower thermal threshold and thermal constant are important descriptors of the thermal requirements of an insect species and their adaptations to local climatic conditions also are indicators for forecasting its potential distribution and abundance (Campbell et al. 1974; Huang et al. 2008; Jarošík et al. 2011; Bonato et al. 2011). The R2 values estimated by the ordinary linear and Ikemoto models were somewhat the same (0.983 and 0.980, respectively). This showed that both linear models are useful and efficient for describing temperature dependent development, estimating the lower temperature threshold (Tmin), and thermal constant (K) of P. plumifer. This study showed that a threshold temperature of 10.33˚C and 166.67 accumulated day degrees were required for P. plumifer to complete one generation by the ordinary linear model, while by the Ikemoto model were estimated these values 11.17 °C and 147.87 degree-days (DD).

The Tmin is higher than that reported for P. fragariae (8˚C) (De Vasconcelos et al. 2008), Typhlodromus bagdasarjani Wainstein and Arutunjan (9.2˚C) (Ganjisaffar et al. 2011) and

Phytoseiulus macropilis Banks (8.4˚C) (Ali 1998). Conversely, this Tmin for P. plumifer is lower than that reported for P. plumifer (10.7˚C) (Kouhjani-Gorji et al. 2008), Neoseiulus womersleyi Schicha (11.6˚C) (Lee and Ahn 2000) and Neoseiulus fallacis Garman (11.2˚C) (Genini et al. 1991). Our findings disclosed that oviposition period and adult longevity of P. plumifer declined with increasing temperatures. Our results are in agreement with the works of Kouhjani-Gorji et al. (2012), Xia et al. (2012), Ganjisaffar et al. (2011), Broufas and Koveos (2001) and Gotoh et al. (2004), who observed that the oviposition period and adult longevity of P. plumifer, N. barkeri, T. bagdasarjani, Euseius finlandicus Oudemans and Neoseiulus californicus McGregor decreased in response to temperature increase. Adult longevity at 30˚C reported for P. plumifer on T. urticae (Nawar et al. 2001) and on T. urticae and corn pollen (Kouhjani-Gorji et al. 2012) were 41.5 and 43.8 days, respectively that are longer than that reported in our finding (35.11 days). The total fecundity of P. plumifer increased with increasing temperatures from 20°C to 25°C and then decreased from 25˚C to 35°C again, similar to the results of some other studies (e.g. Gotoh et al. 2004; Kasap and Sekeroglu 2004; Kouhjani-Gorji et al. 2012). We found that the survival rate of P. plumifer is affected by temperature, the survival curve was type I throughout the temperature range of 20 to 35˚C, showing that most adults died after their oviposition period (Slobodkin 1962). Similarly, a quadratic response curve (type I) for survival rate of N. barkeri (Jafari et al. 2010) and P. fragariae (De Vasconcelos et al. 2008) were reported for the temperature range of 15 to 37˚C and 15 to 30°C, respectively. According to Sabelis (1985), the sex ratio of phytoseiid mites is broadly female biased and varies within and between species. Our experiments revealed that the sex ratio of the P. plumifer at all temperatures was female biased. Similar results were reported for N. barkeri (Xia et al. 2012) and E. finlandicus (Kasap 2009).

The intrinsic rate of increase (rm) is a key demographic parameter useful that describing the growth potential of a population under prevailing climatic and feeding conditions, as a reflection of the overall effects of temperature and food on the population’s development, reproduction, and

418 SYSTEMATIC & APPLIED ACAROLOGY VOL. 22 survival characteristics (Sabelis 1985; Janssen and Sabelis 1992; Krips et al. 1998). Our findings −1 disclosed that the higher value of rm for P. plumifer feeding on E. hirsti was 0.180 day at 30ºC; therefore, a rapid population growth of this predator at or around this temperature could be expected.

The rm of P. plumifer was greater at higher temperatures because in these temperatures adults of this predator are able to produce larger numbers of offspring, the sex ratio (%females) is greater and the life span time is shorter. Kouhjani-Gorji et al. (2012) reported the higher value of rm for P. plumifer feeding on T. urticae was 0.257 day−1 at 30ºC, that was greater than obtained in our study at similar temperature. The diversity in the two studies may be due to the host spider mite (prey) variation and genetic diversity between strains of P. plumifer. The optimum temperature for rm of the species E. finlandicus (Kasap 2009), Neoseiulus umbraticus (Chant) (Kazak et al. 2002) and N. barkeri (Jafari −1 et al. 2010) were around 30˚C and rm values were 0.220, 0.180 and 0.256 day , respectively. Comparing our results with Kouhjani-Gorji et al. (2012) it can be concluded that E. hirsti as food source increased the developmental time and oviposition period and decreased the fecundity of females, altogether resulting in a considerably decreased the intrinsic rate of increase and finite rate of increase. This study and other studies on the of P. plumifer (e.g. Nawar et al. 2001; Kouhjani-Gorji et al. 2008, 2009, 2012; Rasmy et al. 2011), shows that it appears to be a promising biocontrol agent for many phytophagous species. Although temperature has a great influence on the development and reproduction of P. plumifer fed on E. hirsti, this mite can develop successfully and propagate with a high fecundity rate at a temperature range of 20–35˚C. E. hirsti is the serious pest of fig orchards in Iran that due to the absence of effective biological control agents, the heavy use of chemical pesticides, and pest resistance, may soon cause considerable damage to the fig trees. This study confirmed that P. plumifer has a high inherent potential for the control of the E. hirsti especially at 30˚C, and the presented information will be important in the management of this pest in fig orchards.

Acknowledgments

We are grateful to the Department of Plant Protection, Lorestan University, for financial support of this research.

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Submitted: 22 Jul. 2016; accepted by Qing-Hai Fan: 2 Feb. 2017; published: 13 Mar. 2017

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