Effect of temperature on life history of the predatory mite Amblyseius (Neoseiulus) californicus (Acari: Phytoseiidae)

Amblyseius (Neoseiulus) californicus is an indigenous mite in Japan that feeds on many spider mite species. We evaluated the development, survivorship and life-history parameters of A. californicus on a diet of eggs of Tetranychus urticae (red form). More than 97.3% of A. californicus eggs hatched and more than 81.6% of newly hatched larvae attained maturity at temperatures between 15 and 35 degrees C. Females oviposited at 37.5 degrees C, but no eggs hatched. At 40 degrees C, no females laid eggs. The lower threshold temperature from egg to oviposition was 10.3 degrees C and the thermal constant was 86.2 degree-days. Based on these data, the maximum number of generations that could complete development in a year under field conditions in Ibaraki, central Japan, would be between 21 and 28. At 25 degrees C, females laid a mean of 41.6 eggs during a mean oviposition period of 19.4 days. The intrinsic rates of natural increase (rm) were 0.173 at 20 degrees C, 0.274 at 25 degrees C and 0.340 at 30 degrees C.     

Molecular and morphological boundaries of the predatory mite Neoseiulus californicus (McGregor) (Acari: Phytoseiidae)

Neoseiulus californicus (McGregor) is a natural enemy of pest mites used worldwide in many crops. Its correct identification is thus essential to ensure biological control success. The present study aimed to characterize molecular and morphological intraspecific variations for assisting in the diagnosis of the species and to build baseline information about expected variations within a commercially important phytoseiid species. Morphological and molecular [12S rRNA, cytochrome b mitochondrial (mt)DNA, and internal transcribed spacer] analyses were carried out on fourteen populations collected worldwide and on one mass‐reared strain. The genetic distances between the specimens of N. californicus and another related species were high and no overlap was observed, sustaining the reliability of such molecular methods for assisting a specific diagnosis. Furthermore, the genetic distances between populations of N. californicus were very low and overlap between intra‐ and interpopulations distances was observed, except for two populations collected in France (Marsillargues and Midi‐Pyrénées). The high mitochondrial differentiation between these two latter populations and the others questions their specific status: do they belong to the species N. californicus or to another cryptic species? However, using nuclear DNA marker analyses, no distinct differences were observed. Furthermore, even if significant morphological differences were observed between the populations, these differences were very small and the standard errors within each population were very low. We thus concluded that all the populations studied belong to the species N. californicus, despite unexpected high mitochondrial variations. The present study thus displays the importance of an integrative taxonomic approach for avoiding misidentifications. A discussion on morphological and mtDNA variations in relation to diagnostic reliability is developped. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 393–406.     

The effects of prestarvation diet on starvation tolerance of the predatory mite Neoseiulus californicus (Acari: Phytoseiidae)

Understanding the factors affecting stress tolerance in phytoseiid mites is critical for their integration into biological control programs. In the present study, the effects of diet (varying in prey species, physiological status and phenotype) are examined on the future starvation tolerance of the predatory mite Neoseiulus californicus McGregor (Acari: Phytoseiidae). The predators are fed from egg to adulthood on diapausing or nondiapausing Tetranychus urticae, Tetranychus kanzawai (wild and albino strains) or the nondiapausing species Panonychus citri (wild and albino strains). Thereafter, 3‐day‐old mated adult females are held without food at 25 ± 1 °C and a relative humidity of 98 ± 2%. The survival of these starved females is observed daily until all females have died. The survival curves and mean survival times of N. californicus are found to vary among prey types and are significantly longer when the predator is fed with diapausing prey. This enhanced survival is consistent with high concentrations of glycogen and triacylglyceride in the body of the predator at the onset of starvation. The predators fed nondiapausing prey have shorter survival times, and the glycogen and triacylglyceride contents in their bodies are low or undetectable. The protein contents of the predator's body are similar after consuming different prey types, except for a high concentration when fed the albino strain of P. citri. Protein content is unlikely to play a direct role in starvation tolerance, although it may affect the response to varying glycogen and triacylglyceride levels. These findings indicate that nutritional value of prey has a strong impact on the starvation tolerance of N. californicus.     

Using high relative humidity and low air temperature as a long-term storage strategy for the predatory mite Neoseiulus californicus (Gamasida: Phytoseiidae)

The survival time of an indigenous Japanese strain of Neoseiulus californicus (McGregor) was investigated at high and low relative humidities (RHs) of approximately 100% and 80%, respectively, at an air temperature of 5 °C. Five life stages, larva, protonymph, deutonymph and unmated and mated adult female, were tested in 1.5-mL polypropylene vials, in which the RH was adjusted by either adding or omitting a water-saturated filter paper. The survival curves and median survival time (LT₅₀) were significantly different between high and low RHs, and the mean survival time (MST) was 1.6–2.3 times longer at high RH than that at low RH, except in larvae, in which tolerances to high RH and/or low air temperature were not well developed. At high RH, the MST of the mated adult females was 63.1 d and was 1.4 times longer than that of unmated adult females. These results indicate that the suitable water content in the body was probably maintained by increasing the RH at the low air temperature, which is considered to be a primary factor affecting the survival time of N. californicus. Moreover, the nutrient content in the body, such as eggs and male sperm in the mated adult females, could have positive effects on prolonging their survival time. These findings will help to construct an efficient long-term storage method for N. californicus.     

Effect of hexythiazox and spiromesifen resistance on the life cycle of the predatory mite Neoseiulus californicus (Acari: Phytoseiidae)

Neoseiulus californicus (McGregor) (Acari: Phytoseiidae) is one of the most important and effective predators of Tetranychus spp. (Acari: Tetranychidae). This study analyzed the effects of hexythiazox and spiromesifen resistance on biological characteristics of N. californicus. Pre-oviposition, oviposition, post-oviposition times, adult lifespan, total number of eggs laid per female, net reproductive rate (R₀), intrinsic rate of increase (r_m), doubling time (DT), mean generation time (T) and finite rate of increase (λ) were compared among three populations: 63.9-fold hexythiazox resistant (HEX14), 53.6-fold spiromesifen resistant (SPR13) and a susceptible base population. Pre-oviposition and oviposition times, mean number of eggs/female, adult lifespan, R₀ and r_m values were all significantly higher for the two resistant populations than for the susceptible population. Life tables of HEX14, SPR13 and the susceptible population showed that R₀ was 35.0, 26.5 and 19.4 (females/female generation), r_m was 0.35, 0.32 and 0.30 (females/female/day), DT was 1.92, 2.07 and 2.27 days, T was 9.8, 9.8 and 9.7 days, and λ was 1.43, 1.39 and 1.35 (individuals/female/day), respectively.     

Factors affecting ambulatory dispersal in the predaceous mite Neoseiulus californicus (Acari: Phytoseiidae)

Experiments conducted in the laboratory showed that different biotic and abiotic factors affected the ambulatory dispersal behaviour of Neoseiulus californicus. The experimental set-up comprised dwarf alfalfa (Medicago polymorpha) infested or unifested by Tetranychus urticae. Temperatures were measured with thermocouples. Trials were performed at three temperatures, three prey densities, three light intensities, two relative humidities (RHs) and two vegetative states of alfalfa plants, turgid and withered. Deutonymphs were the most dispersive followed by young ovipositional females. High temperatures (35°C), high light intensities (40 000 lux) and drought-stressed alfalfa increased the dispersal of N. californicus. The availability of food in the environment and high moisture (80% RH) slowed down dispersion. The main factors which seem to elicit dispersal behaviour are the deprivation of food and high temperatures which result in an increase in the walking speed of the mite. In addition, other factors tested either increase or reduce the ambulatory dispersal of N. californicus. According to our results, individuals could move from ground cover into apple trees before spring. © Rapid Science Ltd. 1998     

Mating duration and egg production of the predaceous mite Neoseiulus californicus (Acari: Phytoseiidae) vary with temperature

Effects of constant temperature on mating duration and total fecundity of Neoseiulus californicus females mated once were investigated at 18 °C, 25 °C, 30 °C, and 35 °C with a photoperiod of 16L:8D. Adult mites grown and maintained at 25 °C mated for 315.3 min on average and produced 46.1 eggs per female. These values varied significantly by temperature: 553.6 and 13.9 (18 °C), 261.2 and 26.6 (30 °C), and 253.6 and 23.9 (35 °C), respectively. Duration of copulation was negatively correlated with temperature. However, total egg production peaked at 25 °C and decreased at lower and higher temperatures. Reduced sperm transfer and/or survival rate of sperm in the female body may account for decreased egg production when temperatures are not optimal.     

Effects of temperature on the establishment potential of the predatory mite Amblyseius californicus McGregor (Acari: Phytoseiidae) in the UK

Amblyseius californicus was introduced into the UK in the early 1990s as a biocontrol agent against glasshouse red spider mite Tetranychus urticae. This study investigated the effects of temperature on the establishment potential of A. californicus in the UK in the light of recent reports of their successful overwintering outside of glasshouse environments. The developmental thresholds were 9.9 and 8.6 °C respectively using simple and weighted linear regression. Using the day-degree requirement per generation calculated by weighted regression (143 day-degrees) in combination with climate data, it was estimated that up to seven generations would be possible annually outdoors in the UK. Non-diapausing adult females froze at −22 °C, with 100% mortality after reaching their freezing temperature. Up to 90% of mites died before freezing after short exposures to low temperatures. Significant acclimation responses occurred; 90% of acclimated individuals survived 26 days exposure at 0 °C and 11 days at −5 °C (acclimated mites were reared at 19 °C, 6L:18D followed by 1 week at 10 °C, 12L:12D). Non-diapausing adult females survived over 3 months outdoors in winter under sheltered conditions and oviposition was observed. The experimental protocol used in this study is discussed as a pre-release screen for the establishment potential of other Amblyseius species, and similar non-native biocontrol agents.     

Mating, cross-mating and related behaviours of Neoseiulus californicus and Neoseiulus fallacis (Acari: Phytoseiidae)

The pairings of Neoseiulus californicus (McGregor) and Neoseiulus fallacis (Garman) from western North America were monitored for tending by adult males, males in the mating position and oviposition and the activity of female deutonymphs and adults. The N. fallacis × N. californicus (♂ × ♀) tests had fewer males tending the deutonymphs but more in the mating position with new females than the reciprocal test. Afterwards, most of the females appeared gravid and approximately 20% produced an egg. Some eggs did not hatch but others became adult males, which mated with their mothers, but no eggs were produced. F1 males tended and mated with new N. fallacis females which had normal offspring. When held with new N. californicus females, F1 males tended the deutonymphs but were not seen mating and no eggs were laid. The pairings of N. californicus× N. fallacis had more males tending, less in the mating position and the females appeared non-gravid and produced no eggs. When same-species males were added to females held with F1 males for 15–20 days, normal levels and sexes of the progeny were produced. The female and male adults of N. fallacis were more active (ambulatory) than those of N. californicus. In within-species tests, the males had a high activity except while tending and mating, the female deutonymphs were inactive and the just mated females were more active than the ovipositing females. The timing of the tending and mating differed in the cross-pairings. Overall, these and other life-history data show that these two mites are distinct species, but that their males are promiscuous in tending and mating. This revised version was published online in November 2006 with corrections to the Cover Date.     

Risk assessment of Cry toxins of Bacillus thuringiensis on the predatory mites Euseius concordis and Neoseiulus californicus (Acari: Phytoseiidae)

Genetically modified plants carrying Cry toxins of Bacillus thuringiensis (Bt) are widely used for pest control. Possible adverse effects as a result of the use of this control technique to non-target organisms is still a concern; however, few studies have addressed the effects of Bt crops on phytoseiid predatory mites. Phytoseiids are important for the natural control of phytophagous mites, but they can also feed on pollen, plant exudates, etc. Thus, phytoseiids may ingest Bt toxins through several pathways. In this paper, we evaluate the direct effect of Bt-toxins by feeding the predators on Bt cell suspensions, on solution of a Bt toxin and the tri-trophic effect by Bt expressed in transgenic plants. We present a method of conducting toxicological tests with Phytoseiidae which can be useful in studies of risk analysis of toxins to be expressed by genetically engineered plants. This method was used to evaluate the potential effect of ingestion of suspensions of Bt (1.25 × 10⁸ spores/ml) and of purified protein Cry1Ia12 (0.006 mg/ml and 0.018 mg/ml) on Euseius concordis, a predatory mite that develops and reproduces best on pollen. The effects of genetically modified Bollgard^® cotton, which carries the Cry1Ac protein, on Neoseiulus californicus, a selective predator that feeds more on spider mites than on pollen or insects, was determined by feeding them with Tetranychus urticae reared in Bollgard^® cotton and on the non-transgenic isoline. When E. concordis was fed with suspension of Bt isolate derived from product Dipel^® PM, no significant effects were detected. Similarly, Cry1Ia12 Bt toxin, at a concentration of 0.006 mg/ml, did not affect E. concordis. At a concentration of 0.018 mg/ml, however, the intake of this protein reduced the reproduction of E. concordis. There were no effects of Bollgard^® cotton on the biological traits and on the predatory capacity of N. californicus. Results indicate that the Cry toxins of B. thuringiensis studied, at the concentrations used in the field or expressed in transgenic plants, should not affect the predatory mites E. concordis and N. californicus.     

Effects of thermal stress on lipid peroxidation and antioxidant enzyme activities of the predatory mite,Neoseiulus cucumeris (Acari: Phytoseiidae)

Changes in temperature are known to cause a variety of physiological stress responses in insects and mites. Thermal stress responses are usually associated with the increased generation of reactive oxygen species (ROS), resulting in oxidative damage. In this study, we examined the time-related effect (durations for 1, 2, 3, and 5 h) of thermal stress conditions—i.e., relatively low (0, 5, 10, and 15 °C) or high (35, 38, 41, and 44 °C) temperatures—on the activities of antioxidant enzymes including catalase (CAT), superoxide dismutase (SOD), peroxidase (POX), glutathione S-transferases (GSTs), and total antioxidant capacity (T-AOC) of the predatory mite Neoseiulus cucumeris. Also the lipid peroxidation (LPO) levels of the predatory mite were measured under thermal stress conditions. The results confirmed that thermal stress results in a condition of so-called oxidative stress and the four antioxidant enzymes play an important role in combating the accumulation of ROS in N. cucumeris. CAT and POX activity changed significantly when the mites were exposed to cold and heat shock, respectively. The elevated levels of SOD and GSTs activity, expressed in a time-dependent manner, may have an important role in the process of antioxidant response to thermal stress. However, the levels of LPO in N. cucumeris were high, serving as an important signal that these antioxidant enzyme-based defense mechanisms were not always adequate to counteract the surplus ROS. Thus, we hypothesize that thermal stress, especially extreme temperatures, may contribute much to the generation of ROS in N. cucumeris, and eventually to its death.     

Acaricidal and biological activities of Titanium dioxide and Zinc oxide nanoparticles on the two-spotted spider mite,Tetranychus urticae Koch (Acari: Tetranychidae) and their side effects on the predatory mite,Neoseiulus californicus (Acari: Phytoseiidae)

The excessive application of pesticides raises environmental pollution levels, necessitating the need to identify alternative substances that do not cause ecological damage. In this context, the toxicity and residual efficacy of titanium dioxide (TiO₂) and zinc oxide (ZnO) nanoparticles (NPs) compared to abamectin against adult females of T. urticae was evaluated under laboratory and greenhouse conditions. In addition, the effects of tested NPs on the biological parameters of T. urticae as well as their side effects on the predatory mite, Neoseiulus californicus were examined. In laboratory bioassays, LC₅₀ values of TiO₂ and ZnO NPs were 5.82 and 7.09 mg L^–1, respectively, compared to 4.90 mg L^–1 in abamectin 72 hr post-treatment. TiO₂ and ZnO NPs had a prolongation effect on both the developmental and reproductive durations with mean life spans of 33.18 ± 0.72 days and 30.53 ± 0.82 days in the case of TiO₂ and ZnO NPs, respectively, compared to 24.65 ± 0.53 days in the normal case. Treated T. urticae females produced lesser fecundities (10–22 eggs less than the normal mean) and decreased hatchability rates. The highest mortality percentages in T. urticae populations were 92.4 % and 90.0 % after 24 h of spraying with TiO₂ and ZnO NPs, respectively, compared to 98.4 % in abamectin. In contrast, tested NPs demonstrated less toxicity in N. californicus populations with no phytotoxicity on treated leaves. This study is the first in Egypt to investigate the NPs control of T. urticae mites infesting cucumber plants and the effects on their biology and natural enemies.     

Predatory behaviors of Neoseiulus californicus and Galendromus helveolus (Acari: Phytoseiidae) attacking Oligonychus perseae (Acari: Tetranychidae)

Predatory behaviors of Neoseiulus californicus (McGregor) and Galendromus helveolus (Chant) attacking Oligonychus perseae Tuttle, Baker and Abbatiello on avocado leaves were videotaped and analyzed. Behaviors were recorded for “fresh” predators that were used ≤ 48 hr post receipt from a commercial insectary and “cold stored” predators that were maintained at 12°C for ≈ 14 days. Fresh and cold stored G. helveolus were observed to attack O. perseae only after invading webbed nests. Conversely, fresh and cold stored N. californicus employed three different modes of predatory attack: (1) intercepting and attacking migrant O. perseae outside of web nests; (2) attacking prey through nest webbing; or (3) invading and attacking O. perseae inside nests. Predatory efficacy of both N. californicus and G. helveolus was reduced following cold storage, as both species engaged in certain predatory behaviors less frequently in comparison to predators that were not stored at low temperatures. Our observed results for N. californicus and G. helveolus attacking O. perseae are interpreted in relation to the chaetotaxy hypothesis, which proposes that phytoseiid invasion efficiency and propensity of webbed nests is facilitated by dorsal setal lengths. This revised version was published online in July 2006 with corrections to the Cover Date.     

Functional response of Neoseiulus californicus (Acari: Phytoseiidae) to Tetranychus urticae (Acari: Tetranychidae) on strawberry leaves

Neoseiulus californicus (McGregor) is a predatory mite employed for biological control of the agricultural pest Tetranychus urticae (Koch). We explored whether environmental differences, in this case the trichome densities of abaxial leaf surfaces of strawberry cultivars (‘Maehyang’ and ‘Sulhyang’ varieties) affect the functional response of adult female N. californicus preying on immature stages (egg, larva and nymph) of T. urticae. We also evaluated the functional response of N. californicus to eggs of T. urticae at different temperatures (15, 20, 25, 30 and 35°C). We conducted a logistic regression of the proportion of prey consumed as a function of initial prey density to identify functional response types, and used nonlinear least‐squares regression and the random predator equation to estimate attack rates and handling times. The functional response of adult female N. californicus to T. urticae was not influenced by non‐glandular trichomes on abaxial leaves but was affected by temperature. Overall, adult female N. californicus exhibited a type 2 functional response to T. urticae. The handling time of N. californicus was highest (1.9970 h) against T. urticae nymphs. The attack rate did not change much at 15–30°C, but was significantly higher at 35°C. The handling time decreased significantly with increasing temperature at 15–35°C. At 35°C, the attack rate was highest (0.2087) and the handling time was lowest (0.9511 h).     

Humidity‐controlled cold storage of Neoseiulus californicus (Acari: Phytoseiidae): effects on male survival and reproductive ability

Humidification can suppress water loss from an organism and has great potential for improving the cold storage of short‐lived arthropods, such as predatory mites. The effectiveness of humidity‐controlled cold storage was recently verified for Neoseiulus californicus (McGregor) females but was not examined for males. Combining both males and females in one storage protocol might increase the predator population because it would enhance the opportunity for multiple mating, which is necessary for females to maximize their egg production. Newly emerged adult males were stored at an air temperature of 5°C and relative humidity (RH) of 100% or 80%. The median survival time (LT₅₀) was 32 days at 100% RH and 14 days at 80% RH; the survival curves differed significantly. Males stored at 100% RH for 0, 10, 20 and 30 days were introduced to virgin females for mating at 25°C to evaluate their reproductive ability. The pre‐oviposition period was significantly prolonged in the females mated with males stored for ≥20 days. No negative effects of storage were observed on the oviposition period, total number of eggs or net reproduction rate (R₀) in the females mated with males stored for ≤20 days or on the mean generation time (T) for those stored for 30 days. A slight decrease in the intrinsic rate of increase (r_m) was observed in the females mated with males stored for ≥20 days. Our storage method can preserve N. californicus males for 20 days with only a minor reduction in their survival and reproductive ability.     

温度对加州新小绥螨以截形叶螨为猎物的发育及繁殖的影响

在15～35℃、RH80%～85%条件下,研究了加州新小绥螨Neoseiulus (Amblyseius) californicus (Mcgregor)以截形叶螨Tetranychus truncatus Ehara为猎物时,不同螨态的发育和实验种群生命表。结果表明,加州新小绥螨在此温度范围内能完成世代发育,世代发育历期随着温度升高而逐渐缩短。该螨能适应35℃的高温条件,雌性的发育历期最短仅为6.14d。平均产卵期和平均寿命均随着温度的上升逐渐缩短。20℃～25℃时,该螨的平均产卵量最大,达53.73粒/雌。净增殖率在20℃时最高(48.2525),且雌雄性比最大。15℃时内禀增长率和周限增长率均最低,分别为0.0638和1.0659,种群倍增时间最长(10.8669d),35℃时内禀增长率和周限增长率均最高,分别为0.1954和1.2158,种群倍增时间最短(3.5477d)。     

Effect of long-term feeding history on functional and numerical response of Neoseiulus californicus (Acari: Phytoseiidae)

The functional and numerical responses of the predatory mite Neoseiulus californicus to eggs and protonymphs of Tetranychus urticae were studied on excised strawberry leaflet discs under laboratory conditions (25 ± 1°C, 75–85% RH and 16L : 8D). Four strains of the phytoseiid were compared: three originated from a long-term mass-rearing with different food (T. urticae, Dermatophagoides farinae and Quercus spp. pollen) and under controlled conditions, while the fourth was directly collected from a natural environment and therefore considered a wild strain. The different nutritional histories affected the responses of N. californicus on tetranychids. On the whole, the wild strain gave better performance. When egg prey was administered this strain and the one mass-reared on two-spotted spider mites showed similar functional as well as numerical responses; on the contrary, when protonymphs were furnished, the wild strain did not differ from that mass-reared on pollen. The strain previously fed on house dust mites gave the worst performance and also showed the lowest percentages of females in the progeny. The functional responses obtained were predominantly type II curves. In all cases considered, no stored energy was allocated for reproduction and, with the exception of the wild strain on eggs, the prey was exploited less efficiently as the consumption increased. In spite of the differences evidenced in this experiment all strains were characterized by high predation and oviposition rates. Thus the results obtained suggest no drawbacks in the use of mass-reared N. californicus as biocontrol agents. © Rapid Science Ltd. 1998     

Use of polypropylene bags for mass rearing Neoseiulus baraki (Acari: Phytoseiidae), a predatory mite of Aceria guerreronis Keifer (Acari: Eriophyidae)

An efficient, low cost and practicable mass rearing method for the predatory mite, Neoseiulus baraki Athias-Henriot (Acari: Phytoseiidae) was developed using a bag made of two-ply polypropylene (gauge 150, 24 cm × 36 cm) sheets. Introducing 20 N. baraki females into the bag produced a mean number 5218 ± 212.10 offspring in 6 weeks with a 260-fold increase of the initial population.     

Effect of tomato leaf hairiness on functional and numerical response of Neoseiulus californicus (Acari: Phytoseiidae)

The objective of this study was to determine whether differences in hairiness of tomato plants affect the functional and numerical response of the predator Neoseiulus californicus McGregor attacking the two-spotted spider mite, Tetranychus urticae Koch. Two tomato hybrids with different density of glandular hairs were used. The functional response was measured by offering eggs and adults of T urticae at densities ranging from 4 to 64 items per tomato leaflet (surface ca. 6.3 cm2); eggs were offered to predator protonymphs and deutonymphs, adult spider mites to adult predators. The number of spider mites eaten as a function of initial density was fitted to the disc equation. Predator densities were regressed against initial prey densities to analyze the numerical response. The number of eggs and adults of T. urticae eaten by N. californicus was extremely low in both hybrids. The nymphal stage of N. californicus and prey density had a significant effect on the number of T urticae eggs eaten by the predator, while hybrid had no effect. The functional response fitted reasonably well to the Holling model. The handling time (Th) and the attack rate (a) were very similar among the two hybrids. The numerical response indicated that the absolute density of predators increased with changes in spider mite densities but the relative predator/prey density decreased in both hybrids. Tomato hairiness prevented N. californicus from exhibiting a strong numerical response and the predator functional response was much lower than observed in other host plants and other phytoseiids. This result shows the need to consider plant attributes as an essential and interactive component of biological control practices.