Introduction

Predatory mites have been used commercially for biocontrol of agricultural pests such as spider mites, whitefly, and thrips (Zhang, 2003; Xu et al., 2013a). Recent studies about predator mites have examined (i) the selection of efficient predatory mite species, (ii) interactions among predatory mites, plants and pests, (iii) the effects of chemical pesticides on predatory mites, and (iv) large scale production and field release of predatory mites (Smith & Papacek, 1991; Samsøe-Petersen & Hassan, 1991; Samsøe-Petersen, 1983; Ali et al., 1999; Sznajder et al., 2010; Nomikou et al., 2005; Messelink et al., 2010). Within these studies, Amblyseius swirskii (Athias-Henriot), A. largoensis (Muma) and Iphiseiodes zuluagai (Denmark & Muma) were identified as potential predators of Polyphagotarsonemus latus (van Maanen et al., 2010; Rodriguez et al., 2010; Sarmento et al., 2011). Bdella ueckermanni (Hernandes, Daud and Feres) was reported to be an efficient predator for Controlling Aceria guerreronis Keifer (coconut mite) (Hernandes et al., 2008; Souza et al., 2012; Domingos et al., 2010; Melo et al., 2011; Lima et al., 2012). Phytoseiulus persimilis (Athias-Henriot) was used to protect greenhouse tomatoes (Nihoul, 1993). A. swirskii was identified as a biological control agent with potential to play an important role in pest management in many greenhouse crops (Janssen & Sabelis, 2015; Midthassel et al., 2013).

Several species of genus Neoseiulus, including N. barkeri (Hughes), N. cucumeris (Oudemans), and N. californicus (McGregor), have been proven to be useful predatory mites in agriculture (Fan & Petitt, 1994; Obrist et al., 2006; Xia et al., 2012; Yao et al., 2014; Castagnoli & Simoni, 1999).

In China, N. bicaudus is a newly discovered native species (Wang et al., 2015a). It was first named A. bicaudus (Wainstein, 1962). In a paper published later that year, Deleon (1962) named it Cydnodromus comitatus. Schuster and Pritchard (1963) used the name Amblyseius scyphus in reference to N. bicaudus. A decade later, Tuttle (1973) named it N. comitatus (Deleon). Finally, the mite was named N. bicaudus by Wainstein (1977). N. bicaudus mainly exists in Iran, Russia, Greece, Cyprus, and the United States (Wainstein, 1962; DeLeon, 1962; Karban et al., 1995; Livshitz & Kuznetsov, 1972; Wainstein, 1975; Faraji et al., 2007; Palyvos & Emmanouel, 2009; Asali et al., 2011).

Both the development and the predatory action of mites are affected by environmental factors (Palyvos & Emmanouel, 2011; Weintraub et al., 2007; Felton & Dahlman, 1984), including temperature, humidity, rainfall, light intensity, prey, artificial feeding, and fungicides (Domingos et al., 2010; Schütte & Dicke, 2008; Shinmen et al., 2010; Toyoshima et al., 2009; Kawashima & Jung, 2011; Delisle et al., 2014).

The mites are poikilotherms; temperature is the main abiotic factor influencing their biology, ecology, and population dynamics (Liu, 1986; Palyvos et al., 2009; Ghazy et al., 2012; Palyvos & Emmanouel, 2009; Mesa et al., 1990; Hart et al., 2002). Each mite species has its optimal temperature for development and reproduction (Palyvos & Emmanouel, 2009). Such information is useful for assessing the potential of predator mites to suppress a pest population (Midthassel, 2013). For example, after observing that Proprioseiopsis asetus (Acari: Phytoseiidae) can develop and reproduce at temperatures above 25 °C, Huang et al. (2014) concluded that P. ase tus had significant potential for control of asparagus thrips, Thrips tabaci, in southern China. In contrast, Stavrnides and Mills (2011) concluded that the effectiveness of the predatory mite Galendromus occidentalis (Nesbitt) (Acari: Phytoseiidae) against a common vineyard pest, Tetranychus pacificus McGregor, was limited because high temperature slowed the development of G. occidentalis but increased the development of T. pacificus. The predatory ability of P. persimilis feeding on T. turkestani increased as temperature increased to 27 °C and then declined (Wang et al., 2013a). The searching activity of N. californicus on T. turkestani increased first and then declined as temperature increased. The searching and hunting activities both reached maxima at 28 °C (Wang et al., 2014a).

The mite T. turkestani is a serious pest to many crops including cotton, corn, sorghum, medlar, beans, rape, peanut, hops, alfalfa, and vegetables (Wang et al., 1998; Pang et al., 2003; Wang et al., 2013b; Guo et al., 2013; Li et al., 2014). The mite is mainly distributed in Russia, Kazakhstan, America, the Middle East, and Xinjiang, China. T. turkestani is the most important pest mite in Xinjiang, China (Yang et al., 2013).

The taxonomic characteristics of N. bicaudus are well known; however, little is understood about its ecological and biological characteristics. We hypothesized that if the optimal temperature of the N. bicaudus fed on T. turkestani approach to the range of the optimal temperature of the T. turkestani, N. bicaudus could be an effective predator species for controlling T. turkestani.

We constructed life tables to investigate the developmental stages and life parameters of N. bicaudus feeding on T. turkestani at six temperatures between 18 °C to 35 °C. The objectives of this study were to develop (i) better understanding about the population growth of N. bicaudus, (ii) better methods to establish the population of N. bicaudus in the laboratory, and then (iii) better massrearing technology for industrialization (IV). Eventually, we will release N. bicaudus in the field to control the spider mites.

Materials and methods

Results

Immature development

The development time of immature N. bicaudus decreased significantly as temperature increased from 18 °C to 32 °C (Table 1). The egg to adult phase was 10.02 d at 18 °C and 4.27 d at 32 °C. There was no significant difference in development time between the 32 °C and 35 °C treatments. The duration of the egg stage decreased from 3.16 d at 18 °C to 1.17 d at 32 °C. There was no significant difference between the 32 °C and 35 °C treatments. The larval stage, which was the shortest among the immature stages, decreased from 1.14 d at 18 °C to 0.54 d at 32 °C. There was no significant difference among the 26 °C, 29 °C, and 32 °C treatments. The protonymph stage decreased from 3.05 d at 18 °C to 1.18 d at 32 °C. The difference between the 32 °C and 35 °C treatments was not significant. The duration of the deutonymph stage decreased from 2.67 d at 18 °C to 1.27 d at 35 °C. There was no significant difference between the 32 °C and 35 °C treatments.

The data in Table 1 were used to calculate linear regression equations relating the duration of the egg (R=0.981), larval (R=0.962), protonymph (R=0.968), deutonymph stages (R=0.966) and total immature period (R=0.917) to temperature (Table 2).

TABLE 1.

Development time (days) of immature N. bicaudus feeding on T. turkestani at different temperatures.

TABLE 2.

Regression equations and correlation coefficients showing the relationship between temperature (x, °C) and the duration of each developmental stage (y, days) of immature N. bicaudus feeding on T. turkestani.

Adult development and reproduction

The longevity of adult N. bicaudus was greatest at 22 °C (50.81 d) and least at 35 °C (15.29 d). The pre-oviposition period was longest (4.55 d) at 18 °C. There was in no significant difference in the duration of the pre-oviposition period among the other temperature treatments. The duration of the oviposition period was longest (38.65) at 18 °C. The ovipositiion period generally decreased as temperature increased, with the greatest difference between the 22 °C and 26 °C treatments. The postoviposition period was longest at 22 °C (13.57 d) followed by 26 °C (11.93 d) and 18 °C (7.61 d). There was in no significant difference in the duration of the post-oviposition period among the other temperature treatments.

TABLE 3.

Development time (days) of adult N. bicaudus feeding on T. turkestani at different temperatures.

Fecundity and sex ratio

Total fecundity increased, leveled out, and then decreased as temperature increased (Table 4). Total fecundity was lowest at 18 °C (32.94 eggs/female) and highest at 29 °C (43.82 eggs/ female). There was no significant difference in total fecundity among the 22 °C, 26 °C, 29 °C, and 32 °C treatments. Daily fecundity and daily female fecundity both increased between 18 °C and 22 °C and then leveled out. Daily fecundity was highest at 26 °C (2.55 eggs/day/female). There were no significant difference among the 26 °C, 29 °C, 32 °C, and 35 °C treatments. Daily female fecundity was lowest at 18 °C (0.62 female eggs/day/female) and highest at 26 °C (1.69 female eggs/day/ female). There was no significant difference in daily fecundity among the 26 °C, 29 °C, 32 °C, and 35 °C treatments.

TABLE 4.

Fecundity of N. bicaudus feeding on T. turkestani.

Life table parameters

The net reproductive rate (R₀) ranged from a maximum of 34.60 at 26 °C to a minimum of 16.87 at 35 °C (Table 5). As temperature increased, the mean generation time (T) decreased from 20.75 to 6.95, the doubling time (Dt) decreased from 4.57 to 1.70, the intrinsic rate of natural increase (r_m) rose from 0.15 to 0.40, and the finite rate of increase (λ) rose from 1.16 to 1.50. Age-specific survival rate (l_x) and age-specific fecundity (m_x) of adult females of N. bicaudus

TABLE 5.

Life table parameters of N. bicaudus feeding on T. turkestani.

The population survival rate of N. bicaudus gradually declined as the temperature rose from 18 °C to 35 °C (Fig. 1). The survival rate decreased significantly in the later developmental stages, especially at temperatures between 29 °C and 35 °C. The oviposition period of N. bicaudus was significantly shorter in the 29 °C to 35 °C range than in the 18 °C to 26 °C range. The total fecundity of N. bicaudus increased and then decreased as temperature increased. The total fecundity was greatest at 26 °C. In the 18 °C treatment, the female mites began dying on 44 d. All of the female mites died by 63 d (Fig. 1). In the 35 °C treatment, the female mites began dying on 5 d and all of them died by 23 d. The survival rate declined quickly as temperature increased (Fig. 1). At 18 °C, the daily female fecundity reached a maximum (0.88 female eggs/day/female) on 19 d. At 35 °C, the daily female fecundity reached a maximum (2.24 female eggs/day/female) on 5 d. When temperatures were low, the daily fecundity of N. bicaudus was low but the oviposition period was long. The opposite trend was observed when temperatures were high. The pre-oviposition period and longevity both became gradually shorter as temperature increased. The pre-oviposition period was shortest at 32 °C. The post-oviposition period was significantly shorter at high temperature than at low temperature. The shortest post-oviposition period was at 35 °C.

Discussion

The use of predatory mites to control crop pests such as whitefly, thrips, and aphids in the field is an important part of biological control. Predatory mites have been produced commercially for use as biological control agents against pest insects (Xu et al., 2013a). Life tables of both predator and prey allow the control effects of predatory mite species on harmful mites to be objectively evaluated, thus providing a theoretical foundation for efficient biological control (Prischmann et al., 2005).

At least three predatory mite species (P. persimlis, N. cucumeris and N. californicus) have been introduced in Xinjiang Uygur Autonomous Region for use in pest control. Laboratory populations of all three predatory mites species feeding on T. turkestani have been established. N. cucumeris has been used to control pest mites on pear trees (Zhang et al., 2006a). However, summer-time temperatures are high in Xinjiang and humidity is low. These conditions make it difficult for nonnative mite species to survive (Escudero & Ferragut, 2005; Weintraub & Palevsky, 2008). Native species of predator mite have many advantages for pest control.

Temperature had significant influence on the development and reproduction of N. bicaudus fed on T. turkestani. N. bicaudus developed successfully between 18 °C to 35 °C. The effects of temperature varied significantly depending on the life stage. However, the optimum temperature was about 26 °C. This finding suggests that N. bicaudus, like many predatory mites, has a potential to develop over a wide range of temperatures (Broufas & Koveos, 2001; Hamamura et al., 1976).

FIGURE 1.

Effect of temperature on the survival and daily fecundity of N. bicaudus females feeding on T. turkestani. Abbreviations: lx, age-specific survival rate; m_x, age-specific fecundity.

The immature stages of predatory mites can be affected by temperature. Kolodochka (1985) reported that N. barkeri fed on Tetranychus sp. required 9.2 d to complete juvenile development at 26 °C and 90–95% relative humidity. This was much longer than the juvenile development time of 5.65 d N. bicaudus for our observation in this study. The duration of the egg, larva, protonymph, total immature, and pre-oviposition stages all decreased as temperatures increased from 18 °C to 32 °C and then increased slightly as temperatures increased from 32 °C to 35 °C the same as Gotoh et al (2004). This is consistent with previous observations that insect development rates increase as temperature rise and then slow down when temperatures become too high (Sohrabi & Shishehbor, 2008; Liu, 1986; Yue et al., 2009).

The longevity of N. bicaudus decreased as temperature increased within the temperature range in this study. Total fecundity was higher at 22 °C, 26 °C, and 29 °C than at either 18 °C or 35 °C. Gotoh et al. (2004) reported that at the optimum temperature (25 °C), the maximum fecundity of N. bicaudus was slightly greater than that reported for N. californicus. Both daily fecundity and daily female fecundity were significantly higher at 26 °C, 29 °C, 32 °C, and 35 °C than at either 18 °C or 22 °C (P<0.05).

Daily fecundity and daily female fecundity both reached peaks at 26 °C. The net reproductive rate (R₀) of N. bicaudus increased to a maximum of 34.609 at 26 °C and then decreased. This indicated that the optimal temperature range of N. bicaudus was about 26 °C. A temperature of 26 °C could be used for the development and rearing of N. bicaudus colonies in the laboratory. Net reproductive rate (R₀) of N. bicaudus at 26 °C was slightly lower than N. californicus at the optimum temperature (El Taj & Jung, 2012).

The r_m value is an imperative factor for relating the growth potential of a population under certain climatic, food provisions and as it reflects their general effects on development, reproduction, and survival (Southwood & Henderson 2000). The intrinsic rate of increase recorded in the current experiment for N. bicaudus at 26 °C and 35 °C (0.24 and 0.40, respectively), were considerably higher than the values obtained by Fouly (1997) and Emmert et al. (2008) for Proprioseiopsis asetus at 26 °C and 35 °C (0.18–0.28 and 0.17–0.32, respectively).

The mean generation time and the doubling population time of N. bicaudus fed on T. turkestani were both relatively short at 26 °C compared to values reported for several other predatory mite species (Wang et al., 2014b; Zhang et al., 2012a,b). This suggested that N. bicaudus could be effectively used to control pest mites.

During summers in Xinjiang, the mean daily temperature is about 25 °C and the relative humidity is about 60% (Zhang & Zhang, 2006). Our results show that these conditions are conducive for the development and reproduction of N. bicaudus. The optimal temperature of T. turkestani range from 25–30 °C (Zhang et al., 2006b). The average preying number of N. bicaudus fed on T. turkestani were about 64.4 eggs, 39.4 larvas, 45.0 nymphs, 5.6 adults per day (Wang et al., 2015b).which will in turn be favorable for the management of T. turkestani. These results indicate that N. bicaudus could be a helpful biological control agent for T. turkestani on crops under most of the prevailing weather conditions in Xinjiang.

Other environmental factors such as light and humidity can affect the growth and development of predator mites. The type of prey can also have great effect on the development and reproduction of N. bicaudus (Ferrero et al., 2014; Rasmy et al., 2011). The highest temperatures in Xinjiang range from >35 °C in summer and the lowest temperatures < -23 °C in winter. The development of N. bicaudus may be hindered by these temperature extremes. The effects of brief exposure to very hot or very cold conditions is not known. Additional studies should be done about the effects of these factors in order to make full use of N. bicaudus for biological control in the field.