Development and Reproduction of Neoseiulus californicus (Acari: Phytoseiidae) and Tetranychus urticae (Acari: Tetranychidae) Under Simulated Natural Temperature

Development and Reproduction of Neoseiulus californicus (Acari: Phytoseiidae) and Tetranychus... Abstract Although laboratory observations provide basic knowledge of the development and reproduction of predacious and phytophagous mites, little is known of their behavior under natural conditions. Using a closed system designed to simulate natural climate patterns, we investigated the development and reproduction of the predatory mite Neoseiulus californicus (McGregor) (Acari: Phytoseiidae) and the pest mite Tetranychus urticae Koch (Acari: Tetranychidae) at air temperatures typical of June to October at three latitudes (Aomori, Tottori, and Naha) in Japan. The peaks of development in both species showed similar trends at each location. The shortest developmental times for both species were observed during August in Aomori, from July to September in Tottori and during August and September in Naha. Development of T. urticae was not completed during October in Aomori due to the decreased air temperature. High reproduction (number of eggs produced during 5 d from the first oviposition) of N. californicus was attained at the conditions that shortened the developmental times (i.e., high-temperature months). T. urticae showed a reproduction trend similar to that of N. californicus except for the low number of eggs produced during August in Naha due to the high mortality of adult females and during October in Tottori due to diapause incidence. This information is in agreement with field observations and together might be useful for planning biological control programs for phytophagous mites and for successful establishment of predacious mites in new habitats. environment, development, diapause, mite, mortality Abundant data on favorable environments for the population growth of both predacious and phytophagous mites have been collected from laboratory observations (e.g., Gerson et al. 2003, Zhang 2003, Hoy 2011). However, the mites’ biology as affected by the natural environment is not fully understood (Montserrat et al. 2013a). Environmental conditions in the field fluctuate diurnally and seasonally among climatic and geographic regions, and could have substantial effects on economically important mites that laboratory studies cannot reveal (Jones et al. 2005, Montserrat et al. 2013a, Paaijmans et al. 2013, Vangansbeke et al. 2015a). The predatory phytoseiid mite Neoseiulus californicus (McGregor) (Acari: Phytoseiidae) is a well-known, effective biocontrol agent against spider mites, other pest mites, and small pest insects (Castagnoli and Simoni 2003). It is classified as a type II generalist: in addition to mites and insects, it also feeds on honeydew and pollen grains (McMurtry and Croft 1997, Khanamani et al. 2017a,b,c). The species is distributed worldwide, being highly adaptable to various environmental conditions (Hart et al. 2002, Greco et al. 2005). In Japan, N. californicus is distributed extensively: it is observed abundantly throughout the year in the central and southwestern regions but with low frequency in the northern and far southern regions (Amano 2001, Amano et al. 2004, Ohno et al. 2012). The two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), is a cosmopolitan polyphagous pest of a wide range of economically important plants (Jeppson et al. 1975, Zhang 2003, Tuan et al. 2016). In Japan, it is distributed extensively and is considered the pest that causes the most damage to crops (Takafuji and Kamibayashi 1984, Takafuji et al. 2000, Ohno et al. 2009). Several populations of T. urticae particularly those from central and northern Japan survive winter by entering into diapause—a state of developmental and metabolic arrest in response to short day-length and low air temperature (Gotoh and Shinkaji 1981, Takafuji and Kamibayashi 1984, Takafuji et al. 1991). Air temperature is a factor widely recognized as a critical influence on species distribution and abundance (Bale and Walters 2001, Hance et al. 2007, Culos and Tyson 2014, Ghazy et al. 2016). Air temperature variation can affect success in the biological control of T. urticae (Vangansbeke et al. 2015b, El-Taj et al. 2016). In addition, pest control failure in the use of phytoseiid mites is often due to the difficulty of predicting air temperatures that influence predator–prey population dynamics (Jones et al. 2005, Montserrat et al. 2013b). The long north–south extent of Japan creates wide variation in climate among regions. We investigated the development and fecundity of N. californicus and T. urticae under natural patterns of air temperatures simulated in a closed system (Suzuki unpublished; Nishide et al. 2017a,b). We selected three cities along the latitudinal gradient in Japan: Aomori (northern), Tottori (central), and Naha (southern). We simulated the air temperature patterns typical of these locations from early summer to mid-autumn (June to October), when N. californicus and T. urticae are most active in Japan (Takafuji and Kamibayashi 1984, Kishimoto 2002, Shibao et al. 2004, Funayama 2010, Sudo et al. 2010). This allowed us to compare the patterns of development and fecundity of each mite species under seasonally and geographically different climates and so to estimate pest occurrence and thus the best timing for the release of the predator. The results should help to explain why N. californicus is more abundant in central Japan than in the north and south, and to provide useful knowledge for the conservation of natural enemies. Materials and Methods Mites The population of N. californicus was collected from a chrysanthemum field in Ohta, Katsuragi, Nara prefecture and a population of T. urticae was collected from a rose garden in Kyoto city, Kyoto prefecture, Japan. The Japanese populations of N. californicus, in general, do not enter diapause but T. urticae population used in the current study do (Gotoh and Shinkaji 1981, Gotoh et al. 2005). T. urticae was used intentionally to examine the timing for diapause incidence at the defined localities. The N. californicus population was maintained on leaflets of kidney bean (Phaseolus vulgaris L.) infested with T. urticae reared on kidney bean plants. Both species were kept in the laboratory at 25°C under a relative humidity of 60–70% and a 16:8 (L:D) h photoperiod. Simulating Natural Climate Patterns From a climate database (Meteorological Data System, Kagoshima, Japan), we obtained hourly average air temperatures and light intensities measured in Aomori (40°49.3′N, 140°46.1′E, 3 m in altitude), Tottori (35°29.2′N, 134°14.3′E, 7 m), and Naha (26°12.4′N, 127°41.1′E, 28 m) from June to October over 20 yr (1981 to 2000). We used a computer-controlled closed system to simulate natural climate conditions (Suzuki unpublished; Nishide et al. 2017a,b). The light intensity of 0 to 1.4 kW m−2 obtained from the climate database was converted to a duty ratio of 0 to 100% for controlling the output of LEDs (Suzuki et al. 2011, 2014), at which 100% was 17 W m−2. The system software created a schedule of 1-min intervals with corresponding set values of air temperature (TSV) and light intensity (ISV). Because the environmental data were hourly, the software interpolated the 1-min values of TSV and ISV. The software continuously measured the process values of air temperature (TPV) and light intensity (IPV). It adjusted TSV by switching on or off an air heater (TSR210-A; Tescom, Tokyo, Japan) or a refrigerator (JF-NU40B; Haier Japan Sales, Osaka, Japan) every 10 s. It adjusted ISV and day length according to the LED schedule (Fig. 2). Relative humidity was not simulated but recorded throughout the experiments. Experimental Procedures Groups of gravid females of each mite species were introduced onto kidney bean leaflets and allowed to lay eggs for 24 h at the defined air temperature for each location and month. Newly laid eggs (~40 eggs per species per treatment) were transferred individually to fresh leaf disks (10 mm diameter). Immature N. californicus were provided with sufficient T. urticae (all life stages) as prey. The developmental time of both species until adult emergence was recorded. Newly emerged adult females were transferred onto kidney bean leaf disks (25 mm diameter, a maximum of 5 females per leaf disk) for observation of their reproduction. Adult N. californicus females were provided with sufficient T. urticae (all life stages) as prey. Equal numbers of adult males were introduced into each female group to fertilize the females. The number of eggs laid in the first 5 d from the first oviposition was recorded. The males were removed at the end of the observation. Statistical Analysis To evaluate the success of the climate simulations, we examined the relationships of TSV with TPV and of ISV with IPV by linear regression. The day length was the daily duration (h) when IPV > 0 W m−2. Two-way analysis of variance (ANOVA) was used to examine the effects of location and month and their interactions on the developmental times and reproduction (the developmental times were square-root-transformed to meet the assumptions of normality). Differences in the developmental times among months within the same location were analyzed by one-way ANOVA on ranks followed by Dunn’s method for multiple comparison when indicated. Eggs produced per female over 5 d from the first oviposition were analyzed by one-way ANOVA followed by Scheffé’s test. Regression analysis was performed in Python’s statsmodels package (Python Software Foundation, https://www.python.org). ANOVAs were performed in R v. 3.4.0 software (R Core Team 2016). Results Accuracy of Air Temperature and Photoperiod Simulation Figure 1 shows the hourly average of simulated natural air temperature of Aomori, Tottori, and Naha from June to October. More than 98% of the variance in TSV and 94–99% in ISV could be explained by the changes in TPV and IPV, respectively (Table 1; Supp. Figs. S1–S3). The average of simulated daily photoperiod is shown in Fig. 2. Although not simulated during the experiments, measured relative humidity ranged from 70 to 95%, 80 to 95%, and 70 to 90% in Aomori, Tottori, and Naha, respectively, while the natural range is 70–80 for the three locations from June to October. The high humidity was corresponding to the high-temperature months (data not shown). Fig. 1. View largeDownload slide Hourly average of simulated natural air temperature of Aomori, Tottori, and Naha from June to October. Fig. 1. View largeDownload slide Hourly average of simulated natural air temperature of Aomori, Tottori, and Naha from June to October. Table 1. Coefficients of determination (R2) of the linear relationships between the set and measured values of air temperature and relative light intensity in the simulation system Location Month R2 Air temperature Relative light intensity Aomori June 0.999 0.986 July 0.996 0.948 August 0.999 0.982 September 0.996 0.983 October 0.999 0.975 Tottori June 1.000 0.991 July 0.999 0.983 August 0.999 0.982 September 0.997 0.974 October 0.999 0.979 Naha June 0.996 0.989 July 0.997 0.992 August 0.996 0.993 September 0.993 0.986 October 0.988 0.937 Location Month R2 Air temperature Relative light intensity Aomori June 0.999 0.986 July 0.996 0.948 August 0.999 0.982 September 0.996 0.983 October 0.999 0.975 Tottori June 1.000 0.991 July 0.999 0.983 August 0.999 0.982 September 0.997 0.974 October 0.999 0.979 Naha June 0.996 0.989 July 0.997 0.992 August 0.996 0.993 September 0.993 0.986 October 0.988 0.937 View Large Table 1. Coefficients of determination (R2) of the linear relationships between the set and measured values of air temperature and relative light intensity in the simulation system Location Month R2 Air temperature Relative light intensity Aomori June 0.999 0.986 July 0.996 0.948 August 0.999 0.982 September 0.996 0.983 October 0.999 0.975 Tottori June 1.000 0.991 July 0.999 0.983 August 0.999 0.982 September 0.997 0.974 October 0.999 0.979 Naha June 0.996 0.989 July 0.997 0.992 August 0.996 0.993 September 0.993 0.986 October 0.988 0.937 Location Month R2 Air temperature Relative light intensity Aomori June 0.999 0.986 July 0.996 0.948 August 0.999 0.982 September 0.996 0.983 October 0.999 0.975 Tottori June 1.000 0.991 July 0.999 0.983 August 0.999 0.982 September 0.997 0.974 October 0.999 0.979 Naha June 0.996 0.989 July 0.997 0.992 August 0.996 0.993 September 0.993 0.986 October 0.988 0.937 View Large Fig. 2. View largeDownload slide Simulated natural photoperiod (mean) in Aomori, Tottori, and Naha by month. Fig. 2. View largeDownload slide Simulated natural photoperiod (mean) in Aomori, Tottori, and Naha by month. Development and Fecundity of N. californicus Location, month, and their interaction had significant effects on the developmental time and fecundity of N. californicus (P < 0.0001; Table 2). Air temperature had a significant effect on developmental time by month (Aomori, H = 109.394; Tottori, H = 120.213; Naha, H = 89.129; all df = 4, P < 0.001; Fig. 3A). In Aomori, the developmental time was shortest (~5 d) in August temperatures and longest (~14 d) in June temperatures. In Tottori, it was shorter (4.0–4.6 d) in July to September temperatures and longest (~10 d) in October temperatures. In Naha, it was significantly shorter (~4 d) in July and August temperatures than in June, September, and October temperatures (~5 d). Table 2. Two-way ANOVA of the developmental time and fecundity of Neoseiulus californicus as affected by location and month Source df Sum of squares Mean square F P Development  Location 2 56.93 28.463 2209.0 <0.0001  Month 4 50.06 12.516 971.3 <0.0001  Interaction 8 25.48 3.186 247.2 <0.0001  Residuals 369 4.75 0.013 – – Fecundity  Location 2 872.8 436.4 142.073 <0.0001  Month 4 497.5 124.4 40.490 <0.0001  Interaction 8 204.2 25.5 8.308 <0.0001  Residuals 45 138.2 3.1 – – Source df Sum of squares Mean square F P Development  Location 2 56.93 28.463 2209.0 <0.0001  Month 4 50.06 12.516 971.3 <0.0001  Interaction 8 25.48 3.186 247.2 <0.0001  Residuals 369 4.75 0.013 – – Fecundity  Location 2 872.8 436.4 142.073 <0.0001  Month 4 497.5 124.4 40.490 <0.0001  Interaction 8 204.2 25.5 8.308 <0.0001  Residuals 45 138.2 3.1 – – View Large Table 2. Two-way ANOVA of the developmental time and fecundity of Neoseiulus californicus as affected by location and month Source df Sum of squares Mean square F P Development  Location 2 56.93 28.463 2209.0 <0.0001  Month 4 50.06 12.516 971.3 <0.0001  Interaction 8 25.48 3.186 247.2 <0.0001  Residuals 369 4.75 0.013 – – Fecundity  Location 2 872.8 436.4 142.073 <0.0001  Month 4 497.5 124.4 40.490 <0.0001  Interaction 8 204.2 25.5 8.308 <0.0001  Residuals 45 138.2 3.1 – – Source df Sum of squares Mean square F P Development  Location 2 56.93 28.463 2209.0 <0.0001  Month 4 50.06 12.516 971.3 <0.0001  Interaction 8 25.48 3.186 247.2 <0.0001  Residuals 369 4.75 0.013 – – Fecundity  Location 2 872.8 436.4 142.073 <0.0001  Month 4 497.5 124.4 40.490 <0.0001  Interaction 8 204.2 25.5 8.308 <0.0001  Residuals 45 138.2 3.1 – – View Large Fig. 3. View largeDownload slide (A) Developmental time and (B) fecundity of Neoseiulus californicus under simulated natural air temperatures in three locations (mean ± SEM). Numerical values on bars indicate the number of individuals tested. Bars with the same letter are not significantly different (P > 0.05). Fig. 3. View largeDownload slide (A) Developmental time and (B) fecundity of Neoseiulus californicus under simulated natural air temperatures in three locations (mean ± SEM). Numerical values on bars indicate the number of individuals tested. Bars with the same letter are not significantly different (P > 0.05). Air temperature significantly affected egg production by month in Aomori (F4,15 = 24.659, P < 0.001) and Tottori (F4,15 = 25.913, P < 0.001) but not in Naha (F4,15 = 2.865, P = 0.060; Fig. 3B). Egg production peaked in August (13.0 eggs per female per 5 d) in Aomori temperatures, in September (16.5 eggs) in Tottori temperatures, and in August (18.0 eggs) in Naha temperatures. Mortality of N. californicus About 5% of immature N. californicus exposed to Aomori temperatures in June and October died, but none exposed to Tottori and Naha temperatures died. Maximum mortality rates in adults were 6% in Aomori temperatures in September, 5% in Tottori temperatures in June, and 10% in Naha temperatures in June. Development and Fecundity of T. urticae Location, month, and their interaction had significant effects on the developmental time and fecundity of T. urticae (Table 3). Air temperature had a significant effect on developmental time in different months (Aomori, H = 85.075, df = 3; Tottori, H = 104.404, df = 4; Naha, H = 85.450, df = 4; all P < 0.001; Fig. 4A). In Aomori, the developmental time was the shortest (10 d) in August and longest (26 d) in June. Those reared in October temperatures in Aomori did not reach the adult stage, even at the end of November (two-thirds of mites reached deutonymphal stage). In Tottori, it was shortest (~8 d) at July to September temperatures, but was 15 d in June and 23 d in October. In Naha, it ranged from 7 d in July to 10 d in June. Table 3. Two-way ANOVA of the developmental time and fecundity of Tetranychus urticae as affected by location and month Source df SS MS F P Development  Location 2 47.02 23.512 2691.8 <0.0001  Month 4 81.13 20.281 2322.0 <0.0001  Interaction 7 41.17 5.882 673.4 <0.0001  Residuals 295 2.58 0.009 – – Fecundity  Location 2 7,253 3,626 74.82 <0.0001  Month 4 4,591 1,148 23.68 <0.0001  Interaction 7 9,833 1,405 28.98 <0.0001  Residuals 40 1,939 48 – – Source df SS MS F P Development  Location 2 47.02 23.512 2691.8 <0.0001  Month 4 81.13 20.281 2322.0 <0.0001  Interaction 7 41.17 5.882 673.4 <0.0001  Residuals 295 2.58 0.009 – – Fecundity  Location 2 7,253 3,626 74.82 <0.0001  Month 4 4,591 1,148 23.68 <0.0001  Interaction 7 9,833 1,405 28.98 <0.0001  Residuals 40 1,939 48 – – View Large Table 3. Two-way ANOVA of the developmental time and fecundity of Tetranychus urticae as affected by location and month Source df SS MS F P Development  Location 2 47.02 23.512 2691.8 <0.0001  Month 4 81.13 20.281 2322.0 <0.0001  Interaction 7 41.17 5.882 673.4 <0.0001  Residuals 295 2.58 0.009 – – Fecundity  Location 2 7,253 3,626 74.82 <0.0001  Month 4 4,591 1,148 23.68 <0.0001  Interaction 7 9,833 1,405 28.98 <0.0001  Residuals 40 1,939 48 – – Source df SS MS F P Development  Location 2 47.02 23.512 2691.8 <0.0001  Month 4 81.13 20.281 2322.0 <0.0001  Interaction 7 41.17 5.882 673.4 <0.0001  Residuals 295 2.58 0.009 – – Fecundity  Location 2 7,253 3,626 74.82 <0.0001  Month 4 4,591 1,148 23.68 <0.0001  Interaction 7 9,833 1,405 28.98 <0.0001  Residuals 40 1,939 48 – – View Large Fig. 4. View largeDownload slide (A) Developmental time and (B) fecundity of Tetranychus urticae under simulated natural air temperatures in three locations (mean ± SEM). Numerical values on bars indicate the number of individuals tested. Bars with the same letter are not significantly different (P > 0.05). Fig. 4. View largeDownload slide (A) Developmental time and (B) fecundity of Tetranychus urticae under simulated natural air temperatures in three locations (mean ± SEM). Numerical values on bars indicate the number of individuals tested. Bars with the same letter are not significantly different (P > 0.05). Air temperature significantly affected egg production by month in Aomori (F3,11 = 35.461), Tottori (F4,15 = 36.070), and Naha (F4,14 = 19.974) (all P < 0.001; Fig. 4B). Egg production peaked in July and September in Aomori temperatures (~40 eggs per female per 5 d), in August in Tottori temperatures (54 eggs; significantly different only from October), and in September in Naha temperatures (84 eggs), and was smallest in August in Naha temperatures (32 eggs). Mortality of T. urticae Mortality of larvae and nymphs reached 31% in June temperatures and 15% in July temperatures in Aomori, 15% in August temperatures in Tottori, and 16% in July temperatures and 15% in August temperatures in Naha. The adult mortality was 0% in Aomori temperatures, 5–11% in June to August temperatures in Tottori, and 65 to 83% in July and August temperatures in Naha. Diapause of T. urticae Adult females entered diapause (65%, n = 17) in October temperatures in Tottori. No diapause was observed under other air temperature conditions. Discussion Development and Reproduction Our results indicate variations in the development and fecundity of N. californicus and T. urticae in response to simulated natural temperature regimes typical of June to October at three different latitudes in Japan. The developmental time of N. californicus was shortest and fecundity was greatest when reared under the air temperatures of Naha (south). The results of T. urticae were the same, except that high temperatures in August in Naha hindered reproduction. The months at which the shorter developmental times recorded were fairly consistent between species reared in each location: August temperatures in Aomori, July to September temperatures in Tottori, and July to August temperatures in Naha. This result is consistent with the finding that the occurrences of N. californicus and T. urticae are synchronized in pear orchards in Ibaraki Prefecture (36°20′30.48″N, 140°26′48.48″E) and in Satsuma mandarin trees in Shizuoka Prefecture (34°58′37.56″N, 138°22′59.16″E) (Kishimoto 2002, Katayama et al. 2006). Although Holtzer et al. (1988) reported that environmental factors, particularly air temperature, affect the biology of predatory and phytophagous mites similarly, our results indicate that this is true only of their development, because high temperatures inhibited the reproduction of T. urticae, but not that of N. californicus (Figs. 2B and 3B). In addition to the interspecific variation in the response of the two species to air temperature, variation in response to other environmental factors such as relative humidity which was high during the high-temperature months might have contributed to T. urticae reproduction decline (Boudreaux 1958, Ghazy and Suzuki 2014). Both species were able to complete development in all locations from June to October except for T. urticae reared in October temperatures in Aomori. The developmental success of N. californicus in October temperatures in Aomori might be explained by their short developmental time, which allowed them to develop while air temperatures still averaged 16°C, which is well above the thermal developmental threshold of approximately 10°C (Hart et al. 2002, Gotoh et al. 2004). Although the developmental threshold of T. urticae is similar to that of N. californicus, its developmental time is usually longer (8 to 14 d) than that of the latter (~5 d) when reared at 25°C (Bonato 1999, Bounfour and Tanigoshi 2001, Canlas et al. 2006, Kavousi et al. 2009). Adult N. californicus females reproduced under all conditions, but fecundity was low in June and October temperatures in Aomori and in October temperatures in Tottori, which seemed to be due to decreasing air temperatures (~17°C). N. californicus is able to develop and reproduce at a temperature as low as 15°C (Gotoh et al. 2004, Kim et al. 2009, El-Taj and Jung 2012). Because T. urticae did not complete development in October temperatures in Aomori, they did not reproduce. Fecundity was maximum when they were reared in September temperatures in Naha, and was minimum when reared in October temperatures in Tottori where many females entered diapause. The development and reproduction as affected by lower temperature months reported here are to some extent comparable to those reported for T. urticae at a constant air temperature of 15°C where the developmental time was 25 d and the female reproduced 1.7 eggs per day (Bounfour and Tanigoshi 2001). Diapause Japanese populations of N. californicus do not enter diapause (Gotoh et al. 2005). When 65% of adult T. urticae females entered diapause under October conditions in Tottori (~17°C, day length 11.6:12.4 h), the fecundity of N. californicus was only reduced. In T. urticae, the critical day length for inducing diapause was 12.5 h d−1 for a population from Akita (Suzuki and Takeda 2009) and 13 h d−1 for one from Sapporo (Gotoh 1986a). Although day lengths in Aomori (11.4:12.6 h) and Naha (12.5:11.5 h) in October (Fig. 1) were shorter than or comparable to these critical day lengths, diapause was not observed, this could be due to the lower temperature in Aomori (~14°C), which prevented completion of development, and the higher temperature in Naha (~25°C), which prevented induction of diapause. The timing of the appearance of diapausing females of T. urticae was comparable to that observed in the field (Okuhara and Hamamura 1979). Populations of T. urticae collected from different regions in Japan showed different capacities for diapause (Takafuji and Kamibayashi 1984, Takafuji and Morishita 2001). For example, populations from Okinawa had little or no capacity and overwintered without diapause (Takafuji and Gotoh 1999), whereas populations collected from central Japan showed a mix of diapausing and non-diapausing behaviors (Gotoh and Shinkaji 1981, Takafuji and Kamibayashi 1984, Takafuji et al. 1991). Although T. urticae populations in northern Japan generally enter diapause, mites reared in October temperatures in Aomori did not, even by November, because they did not complete development, and remained alive by the end of November temperatures in Aomori. Gotoh (1986a) similarly reported some non-diapausing individuals in the field in Sapporo (43°3′43.56″N, 141°21′15.84″E) from September to November. The timing at which eggs are exposed to diapause-inducing conditions may affect the incidence of diapause at the adult stage (Gotoh and Shinkaji 1981): if eggs are exposed to mid to late September temperatures, which we did not test, some females may enter diapause. Mites that were still alive at the end of November in our study would probably not be able to overwinter without diapause, because only diapausing females were observed in overwintering sites (Gotoh 1986b). Mortality Mortality of N. californicus during the developmental period was zero except in June and October temperatures in Aomori, when it was very low (~5%), apparently on account of the low temperatures (~17°C). Mortality of T. urticae juveniles was induced by lower temperatures in Aomori and by higher temperatures in Naha. Mortality of adult N. californicus was rare and was, in general, less than 10%. Adult females of T. urticae experienced high mortality in July (65%) and August (83%) temperatures in Naha, when conditions are hot and dry (Takafuji and Kamibayashi 1984, Montserrat et al. 2013a,b). Conclusion Our results indicate that N. californicus is highly adaptable to temperatures in Naha from June to October, in Tottori from July to September, and in Aomori during August, and T. urticae is highly adaptable to temperatures in Naha in September, in Tottori and Aomori from July to September. Although not investigated in the current study, other environmental factors such as relative humidity which is critical to mite development and reproduction may have contributed to the observed interspecific variations. This information, together with the previous results of field observations could be useful for predicting the population dynamics of these species at different latitudes and for determining the most efficient timing for the release of predatory mites for controlling spider mites. Supplementary Data Supplementary Data are available at Environmental Entomology online. Acknowledgments This study was supported by a Japan Society for the Promotion of Science (JSPS) KAKENHI grant (JP 25450069) and a JSPS Fellowship (JP 25-03084). We thank Masao Ohyama for his technical assistance in developing the simulation system used in this study. References Cited Amano , H . 2001 . Species structure and abundance of invertebrate natural enemies in sustainable agroecosystems , pp 167 – 182 . In M. Shiomi , H. Koizumi (eds.), Structure and function in agroecosystem design and management , CRC Press , New York, NY . Amano , H. , Y. Ishii , and Y. Kobori . 2004 . Pesticide susceptibility of two dominant phytoseiid mites, Neoseiulus californicus and N. womersleyi, in conventional Japanese fruit orchards (Gamasina: Phytoseiidae) . J. Acarol. Soc. Jap . 13 : 65 – 70 . Google Scholar CrossRef Search ADS Bale , J. S. , and K. F. A. Walters . 2001 . Overwintering biology as a guide to the establishment potential of non-native arthropods in the UK , pp. 343 – 354 . In D. 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Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Environmental Entomology Oxford University Press

Development and Reproduction of Neoseiulus californicus (Acari: Phytoseiidae) and Tetranychus urticae (Acari: Tetranychidae) Under Simulated Natural Temperature

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10.1093/ee/nvy067
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Abstract

Abstract Although laboratory observations provide basic knowledge of the development and reproduction of predacious and phytophagous mites, little is known of their behavior under natural conditions. Using a closed system designed to simulate natural climate patterns, we investigated the development and reproduction of the predatory mite Neoseiulus californicus (McGregor) (Acari: Phytoseiidae) and the pest mite Tetranychus urticae Koch (Acari: Tetranychidae) at air temperatures typical of June to October at three latitudes (Aomori, Tottori, and Naha) in Japan. The peaks of development in both species showed similar trends at each location. The shortest developmental times for both species were observed during August in Aomori, from July to September in Tottori and during August and September in Naha. Development of T. urticae was not completed during October in Aomori due to the decreased air temperature. High reproduction (number of eggs produced during 5 d from the first oviposition) of N. californicus was attained at the conditions that shortened the developmental times (i.e., high-temperature months). T. urticae showed a reproduction trend similar to that of N. californicus except for the low number of eggs produced during August in Naha due to the high mortality of adult females and during October in Tottori due to diapause incidence. This information is in agreement with field observations and together might be useful for planning biological control programs for phytophagous mites and for successful establishment of predacious mites in new habitats. environment, development, diapause, mite, mortality Abundant data on favorable environments for the population growth of both predacious and phytophagous mites have been collected from laboratory observations (e.g., Gerson et al. 2003, Zhang 2003, Hoy 2011). However, the mites’ biology as affected by the natural environment is not fully understood (Montserrat et al. 2013a). Environmental conditions in the field fluctuate diurnally and seasonally among climatic and geographic regions, and could have substantial effects on economically important mites that laboratory studies cannot reveal (Jones et al. 2005, Montserrat et al. 2013a, Paaijmans et al. 2013, Vangansbeke et al. 2015a). The predatory phytoseiid mite Neoseiulus californicus (McGregor) (Acari: Phytoseiidae) is a well-known, effective biocontrol agent against spider mites, other pest mites, and small pest insects (Castagnoli and Simoni 2003). It is classified as a type II generalist: in addition to mites and insects, it also feeds on honeydew and pollen grains (McMurtry and Croft 1997, Khanamani et al. 2017a,b,c). The species is distributed worldwide, being highly adaptable to various environmental conditions (Hart et al. 2002, Greco et al. 2005). In Japan, N. californicus is distributed extensively: it is observed abundantly throughout the year in the central and southwestern regions but with low frequency in the northern and far southern regions (Amano 2001, Amano et al. 2004, Ohno et al. 2012). The two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), is a cosmopolitan polyphagous pest of a wide range of economically important plants (Jeppson et al. 1975, Zhang 2003, Tuan et al. 2016). In Japan, it is distributed extensively and is considered the pest that causes the most damage to crops (Takafuji and Kamibayashi 1984, Takafuji et al. 2000, Ohno et al. 2009). Several populations of T. urticae particularly those from central and northern Japan survive winter by entering into diapause—a state of developmental and metabolic arrest in response to short day-length and low air temperature (Gotoh and Shinkaji 1981, Takafuji and Kamibayashi 1984, Takafuji et al. 1991). Air temperature is a factor widely recognized as a critical influence on species distribution and abundance (Bale and Walters 2001, Hance et al. 2007, Culos and Tyson 2014, Ghazy et al. 2016). Air temperature variation can affect success in the biological control of T. urticae (Vangansbeke et al. 2015b, El-Taj et al. 2016). In addition, pest control failure in the use of phytoseiid mites is often due to the difficulty of predicting air temperatures that influence predator–prey population dynamics (Jones et al. 2005, Montserrat et al. 2013b). The long north–south extent of Japan creates wide variation in climate among regions. We investigated the development and fecundity of N. californicus and T. urticae under natural patterns of air temperatures simulated in a closed system (Suzuki unpublished; Nishide et al. 2017a,b). We selected three cities along the latitudinal gradient in Japan: Aomori (northern), Tottori (central), and Naha (southern). We simulated the air temperature patterns typical of these locations from early summer to mid-autumn (June to October), when N. californicus and T. urticae are most active in Japan (Takafuji and Kamibayashi 1984, Kishimoto 2002, Shibao et al. 2004, Funayama 2010, Sudo et al. 2010). This allowed us to compare the patterns of development and fecundity of each mite species under seasonally and geographically different climates and so to estimate pest occurrence and thus the best timing for the release of the predator. The results should help to explain why N. californicus is more abundant in central Japan than in the north and south, and to provide useful knowledge for the conservation of natural enemies. Materials and Methods Mites The population of N. californicus was collected from a chrysanthemum field in Ohta, Katsuragi, Nara prefecture and a population of T. urticae was collected from a rose garden in Kyoto city, Kyoto prefecture, Japan. The Japanese populations of N. californicus, in general, do not enter diapause but T. urticae population used in the current study do (Gotoh and Shinkaji 1981, Gotoh et al. 2005). T. urticae was used intentionally to examine the timing for diapause incidence at the defined localities. The N. californicus population was maintained on leaflets of kidney bean (Phaseolus vulgaris L.) infested with T. urticae reared on kidney bean plants. Both species were kept in the laboratory at 25°C under a relative humidity of 60–70% and a 16:8 (L:D) h photoperiod. Simulating Natural Climate Patterns From a climate database (Meteorological Data System, Kagoshima, Japan), we obtained hourly average air temperatures and light intensities measured in Aomori (40°49.3′N, 140°46.1′E, 3 m in altitude), Tottori (35°29.2′N, 134°14.3′E, 7 m), and Naha (26°12.4′N, 127°41.1′E, 28 m) from June to October over 20 yr (1981 to 2000). We used a computer-controlled closed system to simulate natural climate conditions (Suzuki unpublished; Nishide et al. 2017a,b). The light intensity of 0 to 1.4 kW m−2 obtained from the climate database was converted to a duty ratio of 0 to 100% for controlling the output of LEDs (Suzuki et al. 2011, 2014), at which 100% was 17 W m−2. The system software created a schedule of 1-min intervals with corresponding set values of air temperature (TSV) and light intensity (ISV). Because the environmental data were hourly, the software interpolated the 1-min values of TSV and ISV. The software continuously measured the process values of air temperature (TPV) and light intensity (IPV). It adjusted TSV by switching on or off an air heater (TSR210-A; Tescom, Tokyo, Japan) or a refrigerator (JF-NU40B; Haier Japan Sales, Osaka, Japan) every 10 s. It adjusted ISV and day length according to the LED schedule (Fig. 2). Relative humidity was not simulated but recorded throughout the experiments. Experimental Procedures Groups of gravid females of each mite species were introduced onto kidney bean leaflets and allowed to lay eggs for 24 h at the defined air temperature for each location and month. Newly laid eggs (~40 eggs per species per treatment) were transferred individually to fresh leaf disks (10 mm diameter). Immature N. californicus were provided with sufficient T. urticae (all life stages) as prey. The developmental time of both species until adult emergence was recorded. Newly emerged adult females were transferred onto kidney bean leaf disks (25 mm diameter, a maximum of 5 females per leaf disk) for observation of their reproduction. Adult N. californicus females were provided with sufficient T. urticae (all life stages) as prey. Equal numbers of adult males were introduced into each female group to fertilize the females. The number of eggs laid in the first 5 d from the first oviposition was recorded. The males were removed at the end of the observation. Statistical Analysis To evaluate the success of the climate simulations, we examined the relationships of TSV with TPV and of ISV with IPV by linear regression. The day length was the daily duration (h) when IPV > 0 W m−2. Two-way analysis of variance (ANOVA) was used to examine the effects of location and month and their interactions on the developmental times and reproduction (the developmental times were square-root-transformed to meet the assumptions of normality). Differences in the developmental times among months within the same location were analyzed by one-way ANOVA on ranks followed by Dunn’s method for multiple comparison when indicated. Eggs produced per female over 5 d from the first oviposition were analyzed by one-way ANOVA followed by Scheffé’s test. Regression analysis was performed in Python’s statsmodels package (Python Software Foundation, https://www.python.org). ANOVAs were performed in R v. 3.4.0 software (R Core Team 2016). Results Accuracy of Air Temperature and Photoperiod Simulation Figure 1 shows the hourly average of simulated natural air temperature of Aomori, Tottori, and Naha from June to October. More than 98% of the variance in TSV and 94–99% in ISV could be explained by the changes in TPV and IPV, respectively (Table 1; Supp. Figs. S1–S3). The average of simulated daily photoperiod is shown in Fig. 2. Although not simulated during the experiments, measured relative humidity ranged from 70 to 95%, 80 to 95%, and 70 to 90% in Aomori, Tottori, and Naha, respectively, while the natural range is 70–80 for the three locations from June to October. The high humidity was corresponding to the high-temperature months (data not shown). Fig. 1. View largeDownload slide Hourly average of simulated natural air temperature of Aomori, Tottori, and Naha from June to October. Fig. 1. View largeDownload slide Hourly average of simulated natural air temperature of Aomori, Tottori, and Naha from June to October. Table 1. Coefficients of determination (R2) of the linear relationships between the set and measured values of air temperature and relative light intensity in the simulation system Location Month R2 Air temperature Relative light intensity Aomori June 0.999 0.986 July 0.996 0.948 August 0.999 0.982 September 0.996 0.983 October 0.999 0.975 Tottori June 1.000 0.991 July 0.999 0.983 August 0.999 0.982 September 0.997 0.974 October 0.999 0.979 Naha June 0.996 0.989 July 0.997 0.992 August 0.996 0.993 September 0.993 0.986 October 0.988 0.937 Location Month R2 Air temperature Relative light intensity Aomori June 0.999 0.986 July 0.996 0.948 August 0.999 0.982 September 0.996 0.983 October 0.999 0.975 Tottori June 1.000 0.991 July 0.999 0.983 August 0.999 0.982 September 0.997 0.974 October 0.999 0.979 Naha June 0.996 0.989 July 0.997 0.992 August 0.996 0.993 September 0.993 0.986 October 0.988 0.937 View Large Table 1. Coefficients of determination (R2) of the linear relationships between the set and measured values of air temperature and relative light intensity in the simulation system Location Month R2 Air temperature Relative light intensity Aomori June 0.999 0.986 July 0.996 0.948 August 0.999 0.982 September 0.996 0.983 October 0.999 0.975 Tottori June 1.000 0.991 July 0.999 0.983 August 0.999 0.982 September 0.997 0.974 October 0.999 0.979 Naha June 0.996 0.989 July 0.997 0.992 August 0.996 0.993 September 0.993 0.986 October 0.988 0.937 Location Month R2 Air temperature Relative light intensity Aomori June 0.999 0.986 July 0.996 0.948 August 0.999 0.982 September 0.996 0.983 October 0.999 0.975 Tottori June 1.000 0.991 July 0.999 0.983 August 0.999 0.982 September 0.997 0.974 October 0.999 0.979 Naha June 0.996 0.989 July 0.997 0.992 August 0.996 0.993 September 0.993 0.986 October 0.988 0.937 View Large Fig. 2. View largeDownload slide Simulated natural photoperiod (mean) in Aomori, Tottori, and Naha by month. Fig. 2. View largeDownload slide Simulated natural photoperiod (mean) in Aomori, Tottori, and Naha by month. Development and Fecundity of N. californicus Location, month, and their interaction had significant effects on the developmental time and fecundity of N. californicus (P < 0.0001; Table 2). Air temperature had a significant effect on developmental time by month (Aomori, H = 109.394; Tottori, H = 120.213; Naha, H = 89.129; all df = 4, P < 0.001; Fig. 3A). In Aomori, the developmental time was shortest (~5 d) in August temperatures and longest (~14 d) in June temperatures. In Tottori, it was shorter (4.0–4.6 d) in July to September temperatures and longest (~10 d) in October temperatures. In Naha, it was significantly shorter (~4 d) in July and August temperatures than in June, September, and October temperatures (~5 d). Table 2. Two-way ANOVA of the developmental time and fecundity of Neoseiulus californicus as affected by location and month Source df Sum of squares Mean square F P Development  Location 2 56.93 28.463 2209.0 <0.0001  Month 4 50.06 12.516 971.3 <0.0001  Interaction 8 25.48 3.186 247.2 <0.0001  Residuals 369 4.75 0.013 – – Fecundity  Location 2 872.8 436.4 142.073 <0.0001  Month 4 497.5 124.4 40.490 <0.0001  Interaction 8 204.2 25.5 8.308 <0.0001  Residuals 45 138.2 3.1 – – Source df Sum of squares Mean square F P Development  Location 2 56.93 28.463 2209.0 <0.0001  Month 4 50.06 12.516 971.3 <0.0001  Interaction 8 25.48 3.186 247.2 <0.0001  Residuals 369 4.75 0.013 – – Fecundity  Location 2 872.8 436.4 142.073 <0.0001  Month 4 497.5 124.4 40.490 <0.0001  Interaction 8 204.2 25.5 8.308 <0.0001  Residuals 45 138.2 3.1 – – View Large Table 2. Two-way ANOVA of the developmental time and fecundity of Neoseiulus californicus as affected by location and month Source df Sum of squares Mean square F P Development  Location 2 56.93 28.463 2209.0 <0.0001  Month 4 50.06 12.516 971.3 <0.0001  Interaction 8 25.48 3.186 247.2 <0.0001  Residuals 369 4.75 0.013 – – Fecundity  Location 2 872.8 436.4 142.073 <0.0001  Month 4 497.5 124.4 40.490 <0.0001  Interaction 8 204.2 25.5 8.308 <0.0001  Residuals 45 138.2 3.1 – – Source df Sum of squares Mean square F P Development  Location 2 56.93 28.463 2209.0 <0.0001  Month 4 50.06 12.516 971.3 <0.0001  Interaction 8 25.48 3.186 247.2 <0.0001  Residuals 369 4.75 0.013 – – Fecundity  Location 2 872.8 436.4 142.073 <0.0001  Month 4 497.5 124.4 40.490 <0.0001  Interaction 8 204.2 25.5 8.308 <0.0001  Residuals 45 138.2 3.1 – – View Large Fig. 3. View largeDownload slide (A) Developmental time and (B) fecundity of Neoseiulus californicus under simulated natural air temperatures in three locations (mean ± SEM). Numerical values on bars indicate the number of individuals tested. Bars with the same letter are not significantly different (P > 0.05). Fig. 3. View largeDownload slide (A) Developmental time and (B) fecundity of Neoseiulus californicus under simulated natural air temperatures in three locations (mean ± SEM). Numerical values on bars indicate the number of individuals tested. Bars with the same letter are not significantly different (P > 0.05). Air temperature significantly affected egg production by month in Aomori (F4,15 = 24.659, P < 0.001) and Tottori (F4,15 = 25.913, P < 0.001) but not in Naha (F4,15 = 2.865, P = 0.060; Fig. 3B). Egg production peaked in August (13.0 eggs per female per 5 d) in Aomori temperatures, in September (16.5 eggs) in Tottori temperatures, and in August (18.0 eggs) in Naha temperatures. Mortality of N. californicus About 5% of immature N. californicus exposed to Aomori temperatures in June and October died, but none exposed to Tottori and Naha temperatures died. Maximum mortality rates in adults were 6% in Aomori temperatures in September, 5% in Tottori temperatures in June, and 10% in Naha temperatures in June. Development and Fecundity of T. urticae Location, month, and their interaction had significant effects on the developmental time and fecundity of T. urticae (Table 3). Air temperature had a significant effect on developmental time in different months (Aomori, H = 85.075, df = 3; Tottori, H = 104.404, df = 4; Naha, H = 85.450, df = 4; all P < 0.001; Fig. 4A). In Aomori, the developmental time was the shortest (10 d) in August and longest (26 d) in June. Those reared in October temperatures in Aomori did not reach the adult stage, even at the end of November (two-thirds of mites reached deutonymphal stage). In Tottori, it was shortest (~8 d) at July to September temperatures, but was 15 d in June and 23 d in October. In Naha, it ranged from 7 d in July to 10 d in June. Table 3. Two-way ANOVA of the developmental time and fecundity of Tetranychus urticae as affected by location and month Source df SS MS F P Development  Location 2 47.02 23.512 2691.8 <0.0001  Month 4 81.13 20.281 2322.0 <0.0001  Interaction 7 41.17 5.882 673.4 <0.0001  Residuals 295 2.58 0.009 – – Fecundity  Location 2 7,253 3,626 74.82 <0.0001  Month 4 4,591 1,148 23.68 <0.0001  Interaction 7 9,833 1,405 28.98 <0.0001  Residuals 40 1,939 48 – – Source df SS MS F P Development  Location 2 47.02 23.512 2691.8 <0.0001  Month 4 81.13 20.281 2322.0 <0.0001  Interaction 7 41.17 5.882 673.4 <0.0001  Residuals 295 2.58 0.009 – – Fecundity  Location 2 7,253 3,626 74.82 <0.0001  Month 4 4,591 1,148 23.68 <0.0001  Interaction 7 9,833 1,405 28.98 <0.0001  Residuals 40 1,939 48 – – View Large Table 3. Two-way ANOVA of the developmental time and fecundity of Tetranychus urticae as affected by location and month Source df SS MS F P Development  Location 2 47.02 23.512 2691.8 <0.0001  Month 4 81.13 20.281 2322.0 <0.0001  Interaction 7 41.17 5.882 673.4 <0.0001  Residuals 295 2.58 0.009 – – Fecundity  Location 2 7,253 3,626 74.82 <0.0001  Month 4 4,591 1,148 23.68 <0.0001  Interaction 7 9,833 1,405 28.98 <0.0001  Residuals 40 1,939 48 – – Source df SS MS F P Development  Location 2 47.02 23.512 2691.8 <0.0001  Month 4 81.13 20.281 2322.0 <0.0001  Interaction 7 41.17 5.882 673.4 <0.0001  Residuals 295 2.58 0.009 – – Fecundity  Location 2 7,253 3,626 74.82 <0.0001  Month 4 4,591 1,148 23.68 <0.0001  Interaction 7 9,833 1,405 28.98 <0.0001  Residuals 40 1,939 48 – – View Large Fig. 4. View largeDownload slide (A) Developmental time and (B) fecundity of Tetranychus urticae under simulated natural air temperatures in three locations (mean ± SEM). Numerical values on bars indicate the number of individuals tested. Bars with the same letter are not significantly different (P > 0.05). Fig. 4. View largeDownload slide (A) Developmental time and (B) fecundity of Tetranychus urticae under simulated natural air temperatures in three locations (mean ± SEM). Numerical values on bars indicate the number of individuals tested. Bars with the same letter are not significantly different (P > 0.05). Air temperature significantly affected egg production by month in Aomori (F3,11 = 35.461), Tottori (F4,15 = 36.070), and Naha (F4,14 = 19.974) (all P < 0.001; Fig. 4B). Egg production peaked in July and September in Aomori temperatures (~40 eggs per female per 5 d), in August in Tottori temperatures (54 eggs; significantly different only from October), and in September in Naha temperatures (84 eggs), and was smallest in August in Naha temperatures (32 eggs). Mortality of T. urticae Mortality of larvae and nymphs reached 31% in June temperatures and 15% in July temperatures in Aomori, 15% in August temperatures in Tottori, and 16% in July temperatures and 15% in August temperatures in Naha. The adult mortality was 0% in Aomori temperatures, 5–11% in June to August temperatures in Tottori, and 65 to 83% in July and August temperatures in Naha. Diapause of T. urticae Adult females entered diapause (65%, n = 17) in October temperatures in Tottori. No diapause was observed under other air temperature conditions. Discussion Development and Reproduction Our results indicate variations in the development and fecundity of N. californicus and T. urticae in response to simulated natural temperature regimes typical of June to October at three different latitudes in Japan. The developmental time of N. californicus was shortest and fecundity was greatest when reared under the air temperatures of Naha (south). The results of T. urticae were the same, except that high temperatures in August in Naha hindered reproduction. The months at which the shorter developmental times recorded were fairly consistent between species reared in each location: August temperatures in Aomori, July to September temperatures in Tottori, and July to August temperatures in Naha. This result is consistent with the finding that the occurrences of N. californicus and T. urticae are synchronized in pear orchards in Ibaraki Prefecture (36°20′30.48″N, 140°26′48.48″E) and in Satsuma mandarin trees in Shizuoka Prefecture (34°58′37.56″N, 138°22′59.16″E) (Kishimoto 2002, Katayama et al. 2006). Although Holtzer et al. (1988) reported that environmental factors, particularly air temperature, affect the biology of predatory and phytophagous mites similarly, our results indicate that this is true only of their development, because high temperatures inhibited the reproduction of T. urticae, but not that of N. californicus (Figs. 2B and 3B). In addition to the interspecific variation in the response of the two species to air temperature, variation in response to other environmental factors such as relative humidity which was high during the high-temperature months might have contributed to T. urticae reproduction decline (Boudreaux 1958, Ghazy and Suzuki 2014). Both species were able to complete development in all locations from June to October except for T. urticae reared in October temperatures in Aomori. The developmental success of N. californicus in October temperatures in Aomori might be explained by their short developmental time, which allowed them to develop while air temperatures still averaged 16°C, which is well above the thermal developmental threshold of approximately 10°C (Hart et al. 2002, Gotoh et al. 2004). Although the developmental threshold of T. urticae is similar to that of N. californicus, its developmental time is usually longer (8 to 14 d) than that of the latter (~5 d) when reared at 25°C (Bonato 1999, Bounfour and Tanigoshi 2001, Canlas et al. 2006, Kavousi et al. 2009). Adult N. californicus females reproduced under all conditions, but fecundity was low in June and October temperatures in Aomori and in October temperatures in Tottori, which seemed to be due to decreasing air temperatures (~17°C). N. californicus is able to develop and reproduce at a temperature as low as 15°C (Gotoh et al. 2004, Kim et al. 2009, El-Taj and Jung 2012). Because T. urticae did not complete development in October temperatures in Aomori, they did not reproduce. Fecundity was maximum when they were reared in September temperatures in Naha, and was minimum when reared in October temperatures in Tottori where many females entered diapause. The development and reproduction as affected by lower temperature months reported here are to some extent comparable to those reported for T. urticae at a constant air temperature of 15°C where the developmental time was 25 d and the female reproduced 1.7 eggs per day (Bounfour and Tanigoshi 2001). Diapause Japanese populations of N. californicus do not enter diapause (Gotoh et al. 2005). When 65% of adult T. urticae females entered diapause under October conditions in Tottori (~17°C, day length 11.6:12.4 h), the fecundity of N. californicus was only reduced. In T. urticae, the critical day length for inducing diapause was 12.5 h d−1 for a population from Akita (Suzuki and Takeda 2009) and 13 h d−1 for one from Sapporo (Gotoh 1986a). Although day lengths in Aomori (11.4:12.6 h) and Naha (12.5:11.5 h) in October (Fig. 1) were shorter than or comparable to these critical day lengths, diapause was not observed, this could be due to the lower temperature in Aomori (~14°C), which prevented completion of development, and the higher temperature in Naha (~25°C), which prevented induction of diapause. The timing of the appearance of diapausing females of T. urticae was comparable to that observed in the field (Okuhara and Hamamura 1979). Populations of T. urticae collected from different regions in Japan showed different capacities for diapause (Takafuji and Kamibayashi 1984, Takafuji and Morishita 2001). For example, populations from Okinawa had little or no capacity and overwintered without diapause (Takafuji and Gotoh 1999), whereas populations collected from central Japan showed a mix of diapausing and non-diapausing behaviors (Gotoh and Shinkaji 1981, Takafuji and Kamibayashi 1984, Takafuji et al. 1991). Although T. urticae populations in northern Japan generally enter diapause, mites reared in October temperatures in Aomori did not, even by November, because they did not complete development, and remained alive by the end of November temperatures in Aomori. Gotoh (1986a) similarly reported some non-diapausing individuals in the field in Sapporo (43°3′43.56″N, 141°21′15.84″E) from September to November. The timing at which eggs are exposed to diapause-inducing conditions may affect the incidence of diapause at the adult stage (Gotoh and Shinkaji 1981): if eggs are exposed to mid to late September temperatures, which we did not test, some females may enter diapause. Mites that were still alive at the end of November in our study would probably not be able to overwinter without diapause, because only diapausing females were observed in overwintering sites (Gotoh 1986b). Mortality Mortality of N. californicus during the developmental period was zero except in June and October temperatures in Aomori, when it was very low (~5%), apparently on account of the low temperatures (~17°C). Mortality of T. urticae juveniles was induced by lower temperatures in Aomori and by higher temperatures in Naha. Mortality of adult N. californicus was rare and was, in general, less than 10%. Adult females of T. urticae experienced high mortality in July (65%) and August (83%) temperatures in Naha, when conditions are hot and dry (Takafuji and Kamibayashi 1984, Montserrat et al. 2013a,b). Conclusion Our results indicate that N. californicus is highly adaptable to temperatures in Naha from June to October, in Tottori from July to September, and in Aomori during August, and T. urticae is highly adaptable to temperatures in Naha in September, in Tottori and Aomori from July to September. Although not investigated in the current study, other environmental factors such as relative humidity which is critical to mite development and reproduction may have contributed to the observed interspecific variations. This information, together with the previous results of field observations could be useful for predicting the population dynamics of these species at different latitudes and for determining the most efficient timing for the release of predatory mites for controlling spider mites. Supplementary Data Supplementary Data are available at Environmental Entomology online. 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Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

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Environmental EntomologyOxford University Press

Published: May 14, 2018

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