Effects of heat stresses on fitness of three commercial predatory mites

doi:10.21203/rs.3.rs-3886808/v1

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Effects of heat stresses on fitness of three commercial predatory mites

https://doi.org/10.21203/rs.3.rs-3886808/v1

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To explore the performances of predatory mites under high temperature, we selected three predatory mites Amblyseius orientalis, Neoseiulus californicus and Neoseiulus barkeri to investigate the survival rate, development duration and fecundity after their eggs and female adults were treated with high temperatures. The results showed that both eggs and adults of N. barkeri were most tolerant to heat stress than N. californicus and A. orientalis. After heat treatment of 39°C on egg, three predatory mites all presented shorter developmental period and longevity as well as lower fecundity. The oviposition period of N. californicus was shortened by nearly 50% and the total egg production of A. orientalis decreased by about 40%. However, the N. barkeri was the least affected by high temperature with its fecundity reduced by only 30%. The short-term high temperature treatment at adult stage also had negative effect on the oviposition period and longevity. The oviposition period of A. orientalis was reduced from 18.26 days to 3.82 days at 39℃, and 100% mortality occurred at 40°C. The longevity of N. californicus and N. barkeri suffered at 40℃ was shortened by about 50%. Our study confirmed that N. barkeri is tolerant to high temperatures at some extent, while A. orientalis is more heat sensitive in either two life stage. In sum, the understanding of the heat resistance of commercial predatory mites can improve the better application of biocontrol agents when selecting mite species for pest mite control in the field.

Biological control

Amblyseius orientalis

Neoseiulus californicus

short-term high temperatures

developmental stage

Greenhouses play important roles in promoting modern agriculture for fruit and vegetable productions in cold area and seasons. To control spider mites in greenhouse, predatory mites have been widely produced and applied in greenhouses for decades worldwide (Nomikou et al. 2002; Gerson and Weintraub 2007; Van Lenteren 2012; McMurtry et al. 2013). As a group of powerful biocontrol agents, at least six native predatory mites are commercially used for greenhouse pest control in China (Chen et al. 2023). For example, Amblyseius orientalis is effective in controlling Panonychus citri, Panonychus ulmi, Tetranychus urticae and Tetranychus viennensis on vegetables and fruits (Sheng et al. 2014; Zheng et al. 2008). Neoseiulus californicus and Neoseiulus barkeri are widely accepted by their moderate prices and excellent control efficients.

Extreme high temperatures often occur during daytime by solar radiation in greenhouses. Unfortunately, predatory mites are found to be suppressed by heat stress (Jafari et al. 2012). For example, the hatching rate of Neoseiulus bicaudus decreased significantly after their eggs were treated with high temperatures (Li et al. 2009). Euseius nicholsi could not reproduce normally at 43°C (Yuan et al. 2015). N. californicus mortality increased after high temperature exposed to egg stage (Lopez-Martinez et al. 2008; Vollmer et al. 2004). All these results demonstrated that temperature has significant effect on the survival and development of predatory mites, however, few studies comparatively studied the heat adaptation among different predatory mites.

Variation of heat resistance present in different development stages of insects (Kingsolver et al. 2011; Zhang et al. 2015). Phytoseiid species generally have five stages, including egg, larva, protonymph, deutonymph and adult (Wu 1997). They develop and survive optimally at 25–30°C (Kolokytha et al. 2011). To our knowledge, limited research has reported whether heat tolerance correlates to developmental stages in phytoseiid mites. To compare heat tolerances of different predatory mites at specific stage and understand which species are more heat resistant under high temperature, we selected three commercial predatory mites, A. orientalis, N. californicus and N. barkeri to explore their fitness after heat exposure at two life stages.

By investigating the development and reproduction of three predatory mites after their eggs or one-day-old adults exposed to different heat stresses, our study aims to clarify the heat tolerance of different predatory mites that are frequently used in biological control. We expect to determinate heat resistant levels of these predatory mites which can establish populations after unexpected heat shock in the greenhouses. In short, our research helps to select the optimal mite predators under high temperature conditions for effective biological control.

Mite rearing

A. orientalis, N. californicus and N. barkeri were maintained in the Predatory Mite Research Group in the Institute of Plant Protection from Chinese Academy of Agricultural Sciences for many years (Lu et al. 2022; Wei et al. 2023; Yan et al. 2023). All three predatory mites fed on the Tetranychus urticae, which was reared on bean leaves. All mites were maintained in the incubators (RXZ, Ningbo, China) at 25 ± 1°C, 70 ± 5% RH and L14:D10 photoperiod.

Effects of heat stresses on phytoseiid eggs

Adequate numbers of adult females of A. orientalis, N. californicus and N. barkeri were placed in small arenas with only prey T. urticae for 24 h to lay eggs (Yan et al. 2021). Briefly, the arena was a tiny device with four tightly clipped layers: a transparent acrylic board (30×20×3 mm³) with a 10 mm diameter hole in the middle, bean leaf disc and two pieces of rectangular glass (30×20×1 mm³) each at top and bottom. The eggs were then randomly moved to clean plastic petri dishes (diameter = 10 cm). Water bath was set for five treatments of 35, 36, 37, 38, and 39°C. The control group was treated at 25℃ without water bath. The petri dishes were wrapped in a sealing plastic bag and soaked in the water bath for 4 h. Twenty eggs were treated at each temperature with each of five replicates. After heat shock, these eggs were moved by a fine brush into the small arenas and placed in the incubator at control temperature of 25°C. Survival and developmental stages (egg, larva, protonymph and deutonymph) were recorded every 12 h until adulthood. Approximate 100 A. orientalis, 60 N. californicus and 50 N. barkeri were recorded respectively. These predatory mites treated by 39°C were then mated. We observed their reproduction periods (pre-oviposition, oviposition and post-oviposition stages), fecundity and longevity for 100 A. orientalis, 60 N. californicus and 50 N. barkeri, respectively.

Effects of heat stresses on predatory mite female adult

The deutonymphs of A. orientalis, N. californicus and N. barkeri were randomly selected and placed in new plastic boxes (d = 16 cm, h = 9 cm). After mating for 24 h, the one-day-old female adults were placed in dry ziplock bags and submerged in water bath, which was set to 36, 37, 38 and 39°C for 4 h. The control group was treated at 25℃ without water bath. A group of 20 adults was applied for each treatment, which contained five replicates. The mites were then moved individually to small arena and reared in the incubator under 25°C. We daily recorded the indices of egg production and survival rate for 100 A. orientalis, 50 N. californicus and 50 N. barkeri, respectively.

Data analysis

All data were analyzed with IBM SPSS Statistics 27.0. The Kruskal-Wallis tests were used to determine the survival rate of three predatory mites under different temperatures. Independent T-test and Mann-Whitney test were used to compare the developmental duration, fecundity and longevity of predatory mites under control and 39°C. One-way ANOVA and Kruskal-Wallis test were used to examine the differences of oviposition period and fecundity of three predatory mites under different treatments. All graphs were performed using Graphpad version 9.5.0.

Effect of high temperature on survival of three predatory mites

Both N. barkeri and N. californicus were more tolerant to heat stress than A. orientalis (Fig. 1). Shocked by high temperatures at egg stage, the survival rate of A. orientalis decreased from 37°C (χ²₍₅₎ = 28.810, p < 0.001), compared with the decreased survival rate of N. californicus from 39°C (χ²₍₅₎ = 11.690, p = 0.039). A series of high temperature stresses did not significantly affect the survival rate of N. barkeri (χ²₍₅₎ = 9.886, p = 0.079). High temperatures at adult stage also damaged mite survival rates. A. orientalis completely died at 40°C (χ²₍₄₎ = 288.900, p < 0.001), while N. barkeri and N. californicus reduced life time by 50% (N. californiulus: χ²₍₄₎ = 121.800, p < 0.001; N. barkeri: χ²₍₄₎ = 110.800, p < 0.001).

Effects of high temperature at egg stage on mite development and reproduction

The developmental time of three predatory mites were all significantly shortened after high temperature treated at egg stage (Fig. 2). The egg period of N. californiulus was shortened from 1.78 d to 0.96 d. (Z = -8.632, p < 0.001) and the protonymph stage from 1.40 d to 0.87 d (Z = -7.991, p < 0.001). As a heat tolerant species, N. barkeri deutonymph was also affected by high temperature for reducing developmental time from 2.53 d to 1.68 d (Z = -6.238, p < 0.001).

Heat stress on egg stage can shorten the oviposition time of three predatory mites (Fig. 3). The pre-oviposition period was significantly shorter in the N. californius and N. barkeri, while no significant change in A. orientalis (N. californius: Z = -5.253, p < 0.001; N. barkeri: Z = -3.970, p < 0.001). The oviposition period of N. californicus was shortened from 19.46 d to 11.50 d (Z = -6.151, p < 0.001), whereas N. barkeri was less affected by temperature (t₍₄₃₎ = 2.381, p = 0.022). The post-oviposition time of N. californicus and N. barkeri was also strikingly reduced after high treatment (N. californicus: t₍₁₀₇₎ = 5.291, p < 0.001; N. barkeri: t₍₄₃₎ = 5.518, p < 0.001).

The negative effect of heat stress on egg stage can be passed over to reproductive stage by reducing the fecundity of three predatory mites (Fig. 5). The total fecundity of A. orientalis and N. californicus decreased by 50% (A. orientali: t₍₆₄₎ = 8.036, p < 0.001; N. californicus: t₍₁₀₇₎ = 12.712, p < 0.001). The daily fecundity of A. orientalis and N. barkeri was accordingly affected by heat stress (A. orientalis: t₍₆₄₎ = 8.241, p < 0.001; N. barkeri: t₍₄₃₎ = 4.164, p < 0.001).

Effects of adult heat stress on mite reproduction and longevity

Heat stress at adult stage reduced the longevity of three predatory mites (Fig. 6). A. orientalis was most sensitive to high temperature, as its life span decreased by 50% after treated by 37℃, and all died at 40℃. In the same treatment, the longevity of N. californicus was shortened from 30.80 d to 12.54 d (χ²₍₄₎ = 101.406, p < 0.001) and N. barkeri was shortened from 23.96 d to 10.42 d (χ²₍₄₎ = 89.183, p < 0.001). The oviposition period was mostly affected by temperature in A. orientalis, since the duration was decreased from 18.26 d to 3.82 d at 39℃ (χ²₍₄₎ = 127.398, p < 0.001). The oviposition period of N. californicus was shortened from 19.46 d to 6.14 d at 40°C (χ²₍₄₎ = 96.857, p < 0.001), and that of N. barkeri from 13.30 d to 4.32 d (χ²₍₄₎ = 109.549, p < 0.001).

Adult heat stress also decreased lifetime fecundity and daily reproduction in three predatory mites (Fig. 7). The total fecundity of A. orientalis was most affected by high temperature, while that of N. barkeri was the least. No reproduction was available in A. orientalis, since all mites died at 40℃ (χ²₍₄₎ = 155.174, p < 0.001). The total fecundity of N. californicus was reduced about 60% from 27.74 to 10.76 (χ²₍₄₎ = 137.721, p < 0.001) and N. barkeri was reduced by about 70% from 10.22 to 2.98 eggs in the treatments of 37°C to 40°C. Correspondingly, mite daily fecundity after treated by 39°C decreased from 1.47 to 0.78 eggs in A. orientalis (χ²₍₄₎ = 127.798, p < 0.001), 2.93 to 1.47 eggs in N. californicus (χ²₍₄₎ = 86.044, p < 0.001), and 1.78 to 0.56 eggs in N. barkeri (χ²₍₄₎ = 135.474, p < 0.001).

Temperature affects invertebrate developmental rate, behavioral response, survival and reproduction (Hoffmann et al. 2011; Colinet et al. 2015), and predatory mites are no exception. The optimal temperature for N. barkeri development is about 24°C and in the range of 16 to 32°C can develop and reproduce (Xia et al. 2012). More than 97% of N. californicus eggs are able to hatch from 15 to 35°C (Gotoh et al. 2004). Short-term high temperature stress has been reported to reduce survivals of N. californicus (Yuan et al. 2015), Panonychus citri (Yang et al. 2014), and Mononychellus tanajoa (Lu et al. 2014). Survival of N. barkeri eggs decreased dramatically after short-term heat exposure at 38°C, 40°C and 42°C (Li et al. 2021). When P. persimilis was treated at 40°C for 2 h, 75% eggs survived; when treated at 40°C for 4 h, only 11.7% eggs hatched (Guo and Dong 1987). Our experiment showed that the eggs of all three predatory mites were wrinkled at 39°C, and the N. barkeri eggs were more heat resistant than the other two species. The tolerance of these three predatory mite adults also showed that N. barkeri was more resistant to heat stress. Although N. barkeri showed some advantages compared to other species, short-term high temperatures still reduced the survival rates, adversely affecting their population growth.

High temperatures can not only cause the death of predatory mites, but also reduce their fecundity (Vollmer et al. 2004; Silbermann and Tatar 2000). When short-term exposed at 38℃ and 40℃ at egg stage, the fitness of N. barkeri was significantly decreased (Jafari et al. 2010; Jafari et al. 2012; Xia et al. 2012), and daily fecundity of female adults treated at 40℃ significantly decreased than that at 38℃ (Li et al. 2021). In our study, three predatory mites were able to develop and lay eggs normally after being exposed to high temperature for 4 h in the egg stage, but the durations of development, oviposition and longevity were significantly shortened. It suggests that predatory mites may take a tradeoff between longevity and reproduction in the adverse environment (Travers et al. 2015; Speakman and Garratt 2013). The fact of the least variable of daily fecundity and most reduction of life span in N. californicus might result from energy prioritization for reproduction. High temperature can accelerate the development of insects and eventually lead to the reduction of adult size (Czarnoleski et al. 2013; Forster et al. 2011). However, we did not observe the reduction of body size of adult mites during experiments, when they were provided sufficient prey after heat exposure and the heat exposure is short.

Consistent with our research, damage caused by heat stress was often at the cost of longevity and reproduction (Yang et al. 2014; Yuan et al. 2015). It has been reported that the lifetime fecundity of N. californicus at 30°C is significantly lower than that at 20°C and 25°C, and the daily reproduction at 20°C is the lowest. With the increase of temperature, the pre-oviposition period, oviposition period and total longevity of adults become shorter (Gotoh et al. 2004). The adult females of Mononychellus tanajoa did not lay eggs after being treated with 42°C for 4 h (Lu et al. 2014). After 2 h of 40°C treatment, the fecundity of N. barkeri decreased by more than 50%, indicating that the short-term high temperature can limit its population expansion (Li et al. 2021). In our experiment, the damage caused by short-term high temperature in adult stage was greater than that in egg stage. The total fecundity of A. orientalis treated with same duration of 39℃ at egg stage and adult stage were 17.84 and 4.22 eggs, and that of N. barkeri was 12.04 and 5.34 eggs, respectively. Compared with development and survival, reproduction is most sensitive to temperature. The longer the adult female exposed to high temperature, the more likely their fecundity could be affected (Ma et al. 2015). The damage caused by high temperature at egg stage may be restored in the subsequent development process, and the damage to reproduction is indirect. Whereas the harm caused by high temperature at adult stage is more direct, leading to the reduction of fecundity.

High temperature is vital to restrict the stable population growth. The acceleration of growth rate and the decrease of reproduction may be related to the long-term high temperature adaptation for better survival (Li et al. 2021). In this experiment, we compared the heat tolerance of three common commercial predatory mites. The results showed that A. orientalis was more sensitive to high temperature and it may not be suitable for high temperature environments. N. barkeri was the most heat-resistant species, but the fecundity and longevity still reduced. Although physiological processes or behavioral responses can help organisms resist adverse environments, predatory mites still could be at the expense of fecundity or survival. Therefore, heat stress eventually reduces individual growth and inhibits population establishment in the greenhouses for biocontrol application (Roux et al. 2010; Silbermann and Tatar 2000; Zhang et al. 2013). Based on understanding of different predatory mite in response to heat stress, we can select heat tolerant species and increase the releasing times to promote the control efficiency against pest mites.

Conflict of interest

The authors have declared that no competing interest exits.

Author Contribution

Xuemin Hao: Formal analysis, Visualization, Writing- Original draft preparation, reviewing and editing. Endong Wang: Supervision and Editing. Hong Yan: Writing- Original draft reviewing and editing. Peipei Zhao: Preparation, Investigation. Fujing Sheng: Preparation, Investigation. Xuenong Xu: Validation, Supervision and Editing. Bo Zhang: Conception, Funding, Supervision and Writing. Meike Liu: Supervision and Editing. Qin Ren: Supervision and Editing.

Acknowledgements

This work was supported by the National Key R&D Program of China (2023YFD1400600).

Chen XX, Du YJ, Huang JH (2023) Advances in research and application of biological control of crop pests and diseases in China. Plant Prot 49:340–370. https://doi.org/10.16688/j.zwbh.2023433
Colinet H, Sinclair BJ, Vernon P, Renault D (2015) Insects in fluctuating thermal environments. Annu Rev Entomol 7:123–140. https://doi.org/10.1146/annurev-ento-010814-021017
Czarnoleski M, Cooper BS, Kierat J, Angilletta MJ Jr (2013) Flies developed small bodies and small cells in warm and in thermally fluctuating environments. J Exp Biol 216:2896–2901. https://doi.org/10.1242/jeb.083535
Forster J, Hirst AG, Atkinson D (2011) How do organisms change size with changing temperature? The importance of reproductive method and ontogenetic timing. Funct Ecol 25:1024–1031. https://doi.org/10.1111/j.1365-2435
Gerson U, Weintraub PG (2007) Mites for the control of pests in protected cultivation. Pest Manag Sci 63:658–676. https://doi.org/10.1002/ps.1380
Gotoh T, Yamaguchi K, Mori K (2004) Effect of temperature on life history of the predatory mite Amblyseius (Neoseiulus) californicus (Acari: Phytoseiidae). Exp Appl Acarol 32:15–30. https://doi.org/10.1023/b:appa.0000018192.91930.49
Guo Yujie D Huifang (1987) Effects of temperature and humidity on the development and survival of the small Chilean phytoseiid mite. Chin J Biol Control 3:19–22
Heidarian M, Fathipor Y, Sedaratian-Jahromi A (2020) Biological traits of acarophagous thrips, Scolothrips longicornis (Thysanoptera: Thripidae) on Schizotetranychus smirnovi (Acari: Tetranychidae): Application of female age-specific and age-stage, two-sex life tables. Syst Appl Acarol 25:512–524. https://doi.org/10.11158/saa.25.3.11
Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adaptation. Nature 24:479–485. https://doi.org/10.1038/nature09670
Jafari S, Fathipour Y, Faraji F (2012) Temperature-dependent development of Neoseiulus barkeri (Acari: Phytoseiidae) on Tetranychus urticae (Acari: Tetranychidae) at seven constant temperatures. Insect Sci 19:220–228. https://doi.org/10.1111/j.1744-7917.2011.01444.x
Jafari S, Fathipour Y, Faraji F, Bagheri M (2010) Demographic response to constant temperatures in Neoseiulus barkeri (Phytoseiidae) fed on Tetranychus urticae (Tetranychidae). Syst Appl Acarol 15:83–99
Jafari S, Fathipour Y, Faraji F (2012) The influence of temperature on the functional response and prey consumption of Neoseiulus barkeri (Acari: Phytoseiidae) on Tetranychus urticae (Acari: Tetranychidae). J Entomol Soc Iran 31:39–52
Kingsolver JG, Woods HA, Buckley LB, Potter KA, MacLean HJ, Higgins JK (2011) Complex life cycles and the responses of insects to climate change. Integr Comp Biol 51:719–732. https://doi.org/10.1093/icb/icr015
Kolokytha PD, Fantinou AA, Papadoulis GT (2011) Temperature and diet effects on immature development of predatory mite Typhlodromus athenas Swirski and Ragusa (Acari: Phyotseiidae). Environ Entomol 40:1577–1584. https://doi.org/10.1603/EN11098
Li HY, Liu YH, Liu HQ, Yao YS, Lei HD (2009) Effects of high temperature on Amblyseius nicholsi. Chin Biocontrol 25:1–5. https://doi.org/10.16409/j.cnki.2095-039x.2009.s1.00
Li WZ, Li HL, Z G et al (2021) Effects of short-term heat stress on the development and reproduction of predatory mite Neoseiulus barkeri (Acari, Phytoseiidae). Syst Appl Acarol 26:713–723. https://doi.org/10.11158/saa.26.4.5
Lopez-Martinez G, Elnitsky MA, Benoit JB, Lee RE Jr, Denlinger DL (2008) High resistance to oxidative damage in the Antarctic midge Belgica antarctica, and developmentally linked expression of genes encoding superoxide dismutase, catalase and heat shock proteins. Insect Biochem Mol Biol 38:796–804. https://doi.org/10.1016/j.ibmb.2008.05.006
Lu F, Chen Q, Chen Z, Lu H, Xu X, Jing F (2014) Effects of heat stress on development, reproduction and activities of protective enzymes in Mononychellus mcgregori. Exp Appl Acarol 63:267–284. https://doi.org/10.1007/s10493-014-9784-0
Lu Q, Lv J, Wang E, Xu X (2022) Impact of starvation on paternal reproductive investment in Neoseiulus californicus. Exp Appl Acarol 87:1–18. https://doi.org/10.1007/s10493-022-00717-8
Ma G, Rudolf VH, Ma CS (2015) Extreme temperature events alter demographic rates, relative fitness, and community structure. Glob Chang Biol 21:1794–1808. https://doi.org/10.1111/gcb.12654
McMurtry JA, De Moraes GJ, Sourassou NF (2013) Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Syst Appl Acarol 18:297–320. https://doi.org/10.11158/saa.18.4.1
Nomikou M, Janssen A, Schraag R, Sabelis MW (2002) Phytoseiid predators as potential biological control agents for Bemisia tabaci. Exp Appl Acarol 27:57–68. https://doi.org/10.1023/A:1017976725685
Roux O, Le Lann C, van Alphen JJ, van Baaren J (2010) How does heat shock affect the life history traits of adults and progeny of the aphid parasitoid Aphidius avenae (Hymenoptera: Aphidiidae)? Bull Entomol Res 100:543–549. https://doi.org/10.1017/S0007485309990575
Sheng FJ, Wang ED, Xu XN, Wang BM (2014) Life table of experimental population of Amblyseius orientalis feeding on Carpoglyphus lactis. Chin J Biol Control 30:194–198. https://doi.org/10.16409/j.cnki.2095-039x.2014.02.004
Silbermann R, Tatar M (2000) Reproductive costs of heat shock protein in transgenic Drosophila melanogaster. Evolution 54:2038–2045. https://doi.org/10.1111/j.0014-3820.2000
Speakman JR, Garratt M (2014) Oxidative stress as a cost of reproduction: beyond the simplistic trade-off model. BioEssays 36:93–106. https://doi.org/10.1002/bies.201300108
Travers LM, Garcia-Gonzalez F, Simmons LW (2015) Live fast die young life history in females: evolutionary trade-off between early life mating and lifespan in female Drosophila melanogaster. Sci Rep 20:15469. https://doi.org/10.1038/srep15469
Van Lenteren JC (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. Biocontrol 57:1–20. https://doi.org/10.1007/s10526-011-9395-1
Vollmer JH, Sarup P, Kaersgaard CW, Dahlgaard J, Loeschcke V (2004) Heat and cold-induced male sterility in Drosophila buzzatii: genetic variation among populations for the duration of sterility. Heredity (Edinb) 92:257–262. https://doi.org/10.1038/sj.hdy.6800405
Wei J, Liu Y, Sheng F, Wang E, Zhang B, Xu X (2023) Predatory mite Amblyseius orientalis prefers egg stage and low density of Carpoglyphus lactis prey. Exp Appl Acarol 90:267–276. https://doi.org/10.1007/s10493-023-00805-3
WN (1997) Chinese Economic Insects. Book 53, Ticks and Mites of the subclass Phytophthora. Science Press
Xia B, Zou Z, Li P, Lin P (2012) Effect of temperature on development and reproduction of Neoseiulus barkeri (Acari: Phytoseiidae) fed on Aleuroglyphus ovatus. Exp Appl Acarol 56:33–41. https://doi.org/10.1007/s10493-011-9481-1
Yan H, Wang E, Wei GS, Zhang B, Xu X (2023) Both host and diet shape bacterial communities of predatory mites. Insect Sci. https://doi.org/10.1111/1744-7917.13253
Yan JY, Zhang B, Li G, Xu XN (2021) Bacterial communities in predatory mites are associated with species and diet types. Biocontrol 66:803–811. https://doi.org/10.1007/s10526-021-10112-8
Yang LH, Huang H, Wang JJ (2014) Effect of exposure to heat stress on survival and fecundity of Panonychus citri. Scientia Agricultura Sinica 47:693–701
Yuan XP, Wang XD, Wang JW, Zhao YY (2015) Effects of brief exposure to high temperature on Neoseiulus californicus. Chin J Appl Ecol 26:853–858. https://doi.org/10.13287/j.1001-9332.20150122.002
Zhang W, Rudolf VH, Ma CS (2015) Stage-specific heat effects: timing and duration of heat waves alter demographic rates of a global insect pest. Oecologia 179:947–957. https://doi.org/10.1007/s00442-015-3409-0
Zhang W, Zhao F, Hoffmann AA, Ma CS (2013) A single hot event that does not affect survival but decreases reproduction in the diamondback moth, Plutella xylostella. PLoS ONE 8:e75923. https://doi.org/10.1007/s10493-014-9784-0
Zheng FQ, Zhang XH, Mo TL, Zheng JQ, Wu JB (2008) Ecological niches and guilds of main insect pests and their natural enemies on apple trees. Acta Ecol Sin 28:4830–4840

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Effects of heat stresses on fitness of three commercial predatory mites

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Abstract

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Introduction

Materials and methods

Effects of heat stresses on phytoseiid eggs

Effects of heat stresses on predatory mite female adult

Data analysis

Results

Effect of high temperature on survival of three predatory mites

Effects of high temperature at egg stage on mite development and reproduction

Effects of adult heat stress on mite reproduction and longevity

Discussion

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Conflict of interest

Author Contribution

Acknowledgements

References

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