Effects of heat stresses on fitness of three commercial predatory mites

Effects of heat stresses on fitness of three commercial predatory mites | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Effects of heat stresses on fitness of three commercial predatory mites Xuemin Hao, Endong Wang, Hong Yan, Peipei Zhao, Fujing Sheng, and 4 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-3886808/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract 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 Neoseiulus californicus short-term high temperatures developmental stage Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Figure 6 Figure 7 Introduction 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. Materials and methods 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 mm 3 ) with a 10 mm diameter hole in the middle, bean leaf disc and two pieces of rectangular glass (30×20×1 mm 3 ) 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. Results 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 ( χ 2 (5) = 28.810, p < 0.001), compared with the decreased survival rate of N. californicus from 39°C ( χ 2 (5) = 11.690, p = 0.039). A series of high temperature stresses did not significantly affect the survival rate of N. barkeri ( χ 2 (5) = 9.886, p = 0.079). High temperatures at adult stage also damaged mite survival rates. A. orientalis completely died at 40°C ( χ 2 (4) = 288.900, p < 0.001), while N. barkeri and N. californicus reduced life time by 50% ( N. californiulus : χ 2 (4) = 121.800, p < 0.001; N. barkeri : χ 2 (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 ( χ 2 (4) = 101.406, p < 0.001) and N. barkeri was shortened from 23.96 d to 10.42 d ( χ 2 (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℃ ( χ 2 (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 ( χ 2 (4) = 96.857, p < 0.001), and that of N. barkeri from 13.30 d to 4.32 d ( χ 2 (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℃ ( χ 2 (4) = 155.174, p < 0.001). The total fecundity of N. californicus was reduced about 60% from 27.74 to 10.76 ( χ 2 (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 ( χ 2 (4) = 127.798, p < 0.001), 2.93 to 1.47 eggs in N. californicus ( χ 2 (4) = 86.044, p < 0.001), and 1.78 to 0.56 eggs in N. barkeri ( χ 2 (4) = 135.474, p < 0.001). Discussion 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. Declarations 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). 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Acta Ecol Sin 28:4830–4840 Additional Declarations No competing interests reported. Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-3886808","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":268580993,"identity":"75fa5f43-bf1c-4dc0-9535-736ef8bf99da","order_by":0,"name":"Xuemin Hao","email":"","orcid":"","institution":"Yangtze University","correspondingAuthor":false,"prefix":"","firstName":"Xuemin","middleName":"","lastName":"Hao","suffix":""},{"id":268580994,"identity":"97f7d648-bc06-4313-ba37-3512548f595d","order_by":1,"name":"Endong Wang","email":"","orcid":"","institution":"Chinese Academy of Agricultural Sciences","correspondingAuthor":false,"prefix":"","firstName":"Endong","middleName":"","lastName":"Wang","suffix":""},{"id":268580995,"identity":"ccc3e7ed-5d66-45c5-b9dc-15e0fb4e883f","order_by":2,"name":"Hong Yan","email":"","orcid":"","institution":"Chinese Academy of Agricultural Sciences","correspondingAuthor":false,"prefix":"","firstName":"Hong","middleName":"","lastName":"Yan","suffix":""},{"id":268580996,"identity":"1f11a635-b184-4ae8-9da6-a43c11951db7","order_by":3,"name":"Peipei Zhao","email":"","orcid":"","institution":"Chinese Academy of Agricultural Sciences","correspondingAuthor":false,"prefix":"","firstName":"Peipei","middleName":"","lastName":"Zhao","suffix":""},{"id":268580997,"identity":"5afab417-b8d8-43e8-9c70-ce7312c14b9e","order_by":4,"name":"Fujing Sheng","email":"","orcid":"","institution":"Shandongzhongke Beneficial Insect Resources Utilization Technology Innovation Center","correspondingAuthor":false,"prefix":"","firstName":"Fujing","middleName":"","lastName":"Sheng","suffix":""},{"id":268580998,"identity":"9bb75d3a-43bd-4e50-8bd6-5111789f6d9f","order_by":5,"name":"Qin Ren","email":"","orcid":"","institution":"Jining Normal University","correspondingAuthor":false,"prefix":"","firstName":"Qin","middleName":"","lastName":"Ren","suffix":""},{"id":268580999,"identity":"36a3afce-5bd9-44cc-b231-0cb1d7a9dde3","order_by":6,"name":"Meike Liu","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAAw0lEQVRIiWNgGAWjYBACPmYGBsaGCgkefvbGxgcfiNHCBtZyxkZOsudws+EMorQAMWNjW5qxwY30NmkOorSw85hunMF2OHHDzYcN0gwMdnK6DQQdxmN2cwPP4cSZtxMbjAsYko3NDhCj5YHE4cQ+oJbkGQwHErcRp8XgcGLDzYMNh3mI1rIhIc1Y4AZjYzORWtjKbs44AArkxGbGGQZE+IWf//C2m73/QFF5/PmPDxV2cgS1oAED0pSPglEwCkbBKMABAHYbRRVlie1rAAAAAElFTkSuQmCC","orcid":"","institution":"Yangtze University","correspondingAuthor":true,"prefix":"","firstName":"Meike","middleName":"","lastName":"Liu","suffix":""},{"id":268581000,"identity":"c948f308-2641-4f9e-9352-8d598cf7390b","order_by":7,"name":"Bo Zhang","email":"","orcid":"","institution":"Chinese Academy of Agricultural Sciences","correspondingAuthor":false,"prefix":"","firstName":"Bo","middleName":"","lastName":"Zhang","suffix":""},{"id":268581001,"identity":"36879e5f-4c12-4ecc-ab27-26a699622f23","order_by":8,"name":"Xuenong Xu","email":"","orcid":"","institution":"Chinese Academy of Agricultural Sciences","correspondingAuthor":false,"prefix":"","firstName":"Xuenong","middleName":"","lastName":"Xu","suffix":""}],"badges":[],"createdAt":"2024-01-22 03:29:44","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-3886808/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-3886808/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":50107562,"identity":"ff2abcdc-a3ca-4caf-8b35-6b5a671dc55e","added_by":"auto","created_at":"2024-01-24 16:17:29","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":65154,"visible":true,"origin":"","legend":"\u003cp\u003eSurvival rates of eggs and female adults of \u003cem\u003eAmblyseius orientalis\u003c/em\u003e, \u003cem\u003eNeoseiulus californicus\u003c/em\u003e, \u003cem\u003eNeoseiulus barkeri\u003c/em\u003e under high temperature stress.\u003c/p\u003e","description":"","filename":"Fig.1.png","url":"https://assets-eu.researchsquare.com/files/rs-3886808/v1/d0148dfde99b6d04b3379ccf.png"},{"id":50106981,"identity":"75a3abf0-8645-46bc-b63e-ad7ee9c3186f","added_by":"auto","created_at":"2024-01-24 16:09:29","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":44546,"visible":true,"origin":"","legend":"\u003cp\u003eDevelopmental duration of predatory mites after their eggs treated with 39°C high temperature stress. *, \u003cem\u003ep\u003c/em\u003e \u0026lt; 0.05, **, \u003cem\u003ep\u003c/em\u003e \u0026lt; 0.01, ***, \u003cem\u003ep\u003c/em\u003e \u0026lt; 0.001.\u003c/p\u003e","description":"","filename":"Fig.2.png","url":"https://assets-eu.researchsquare.com/files/rs-3886808/v1/ee63ad24ecdb1bb17ff55fda.png"},{"id":50106980,"identity":"2013c741-278d-425c-92d7-09bc8df3b347","added_by":"auto","created_at":"2024-01-24 16:09:29","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":62657,"visible":true,"origin":"","legend":"\u003cp\u003ePre-oviposition, oviposition and post-oviposition of predatory mites after their eggs treated with high temperature at 39°C. *, \u003cem\u003ep\u003c/em\u003e \u0026lt; 0.05, **, \u003cem\u003ep\u003c/em\u003e \u0026lt; 0.01, ***, \u003cem\u003ep\u003c/em\u003e \u0026lt; 0.001. Pre-O, pre-oviposition period; Ovi, oviposition period;Post-O, post-oviposition period.\u003c/p\u003e","description":"","filename":"Fig.3.png","url":"https://assets-eu.researchsquare.com/files/rs-3886808/v1/a205e7f0435de3011c0625cb.png"},{"id":50106978,"identity":"7f372e3a-9e63-4a46-a30f-5e7248eb7ad6","added_by":"auto","created_at":"2024-01-24 16:09:29","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":88697,"visible":true,"origin":"","legend":"\u003cp\u003eThe developmental duration and longevity after the eggs treated by 39°C. *, \u003cem\u003ep\u003c/em\u003e \u0026lt; 0.05, **, \u003cem\u003ep\u003c/em\u003e \u0026lt; 0.01, ***, \u003cem\u003ep\u003c/em\u003e \u0026lt; 0.001.\u003c/p\u003e","description":"","filename":"Fig.4.png","url":"https://assets-eu.researchsquare.com/files/rs-3886808/v1/3d10bed56f0e12db072116ec.png"},{"id":50107563,"identity":"ef945dbf-98a7-4005-b329-17e004975b33","added_by":"auto","created_at":"2024-01-24 16:17:29","extension":"png","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":44082,"visible":true,"origin":"","legend":"\u003cp\u003eFecundity of predatory mites after adults treated by 39 °C. *, \u003cem\u003ep\u003c/em\u003e \u0026lt; 0.05, **, \u003cem\u003ep\u003c/em\u003e \u0026lt; 0.01, ***, \u003cem\u003ep\u003c/em\u003e \u0026lt; 0.001.\u003c/p\u003e","description":"","filename":"Fig.5.png","url":"https://assets-eu.researchsquare.com/files/rs-3886808/v1/d269260c39cdbe7b236d0b6c.png"},{"id":50106982,"identity":"aaf70908-56d2-4299-98ac-bad8d88c2ca3","added_by":"auto","created_at":"2024-01-24 16:09:29","extension":"png","order_by":6,"title":"Figure 6","display":"","copyAsset":false,"role":"figure","size":126216,"visible":true,"origin":"","legend":"\u003cp\u003eComparison of pre-oviposition period, oviposition period, post-oviposition period and longevity of female adults of three predatory mites after high temperature exposure during adult stage. Different lower-case letters indicated significant differences in each group (\u003cem\u003ep\u003c/em\u003e \u0026lt; 0.05).\u003c/p\u003e","description":"","filename":"Fig.6.png","url":"https://assets-eu.researchsquare.com/files/rs-3886808/v1/71997bd60649dd395112c15c.png"},{"id":50106984,"identity":"1a4a0c16-e401-4dcf-acc4-307971c9d37b","added_by":"auto","created_at":"2024-01-24 16:09:29","extension":"png","order_by":7,"title":"Figure 7","display":"","copyAsset":false,"role":"figure","size":58061,"visible":true,"origin":"","legend":"\u003cp\u003eLifetime fecundity and daily reproduction of female adults of three predatory mites after adult heat stress. Different lower-case letters indicated significant differences in each group (\u003cem\u003ep\u003c/em\u003e \u0026lt; 0.05).\u003c/p\u003e","description":"","filename":"Fig.7.png","url":"https://assets-eu.researchsquare.com/files/rs-3886808/v1/2e951c4e95a1c7dc2d2ba5dc.png"},{"id":57726093,"identity":"ad8b8803-8678-455c-95b1-5a9bf4107892","added_by":"auto","created_at":"2024-06-04 20:46:38","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":921200,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3886808/v1/f312a516-4cd0-47c5-a6cd-4e1d8737d1bb.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Effects of heat stresses on fitness of three commercial predatory mites","fulltext":[{"header":"Introduction","content":"\u003cp\u003eGreenhouses 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. \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2002\u003c/span\u003e; Gerson and Weintraub \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Van Lenteren \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; McMurtry et al. \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). 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. \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). For example, \u003cem\u003eAmblyseius orientalis\u003c/em\u003e is effective in controlling \u003cem\u003ePanonychus citri\u003c/em\u003e, \u003cem\u003ePanonychus ulmi\u003c/em\u003e, \u003cem\u003eTetranychus urticae\u003c/em\u003e and \u003cem\u003eTetranychus viennensis\u003c/em\u003e on vegetables and fruits (Sheng et al. \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Zheng et al. \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2008\u003c/span\u003e). \u003cem\u003eNeoseiulus californicus\u003c/em\u003e and \u003cem\u003eNeoseiulus barkeri\u003c/em\u003e are widely accepted by their moderate prices and excellent control efficients.\u003c/p\u003e \u003cp\u003eExtreme 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. \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2012\u003c/span\u003e). For example, the hatching rate of \u003cem\u003eNeoseiulus bicaudus\u003c/em\u003e decreased significantly after their eggs were treated with high temperatures (Li et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2009\u003c/span\u003e). \u003cem\u003eEuseius nicholsi\u003c/em\u003e could not reproduce normally at 43\u0026deg;C (Yuan et al. \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). \u003cem\u003eN. californicus\u003c/em\u003e mortality increased after high temperature exposed to egg stage (Lopez-Martinez et al. \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2008\u003c/span\u003e; Vollmer et al. \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2004\u003c/span\u003e). 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.\u003c/p\u003e \u003cp\u003eVariation of heat resistance present in different development stages of insects (Kingsolver et al. \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Zhang et al. \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). Phytoseiid species generally have five stages, including egg, larva, protonymph, deutonymph and adult (Wu 1997). They develop and survive optimally at 25\u0026ndash;30\u0026deg;C (Kolokytha et al. \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). 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, \u003cem\u003eA. orientalis\u003c/em\u003e, \u003cem\u003eN. californicus\u003c/em\u003e and \u003cem\u003eN. barkeri\u003c/em\u003e to explore their fitness after heat exposure at two life stages.\u003c/p\u003e \u003cp\u003eBy 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.\u003c/p\u003e"},{"header":"Materials and methods","content":"\u003cp\u003e \u003cb\u003eMite rearing\u003c/b\u003e \u003c/p\u003e \u003cp\u003e \u003cem\u003eA. orientalis\u003c/em\u003e, \u003cem\u003eN. californicus\u003c/em\u003e and \u003cem\u003eN. barkeri\u003c/em\u003e 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. \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e2022\u003c/span\u003e; Wei et al. \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2023\u003c/span\u003e; Yan et al. \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). All three predatory mites fed on the \u003cem\u003eTetranychus urticae\u003c/em\u003e, which was reared on bean leaves. All mites were maintained in the incubators (RXZ, Ningbo, China) at 25\u0026thinsp;\u0026plusmn;\u0026thinsp;1\u0026deg;C, 70\u0026thinsp;\u0026plusmn;\u0026thinsp;5% RH and L14:D10 photoperiod.\u003c/p\u003e \u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eEffects of heat stresses on phytoseiid eggs\u003c/h2\u003e \u003cp\u003eAdequate numbers of adult females of \u003cem\u003eA. orientalis\u003c/em\u003e, \u003cem\u003eN. californicus\u003c/em\u003e and \u003cem\u003eN. barkeri\u003c/em\u003e were placed in small arenas with only prey \u003cem\u003eT. urticae\u003c/em\u003e for 24 h to lay eggs (Yan et al. \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Briefly, the arena was a tiny device with four tightly clipped layers: a transparent acrylic board (30\u0026times;20\u0026times;3 mm\u003csup\u003e3\u003c/sup\u003e) with a 10 mm diameter hole in the middle, bean leaf disc and two pieces of rectangular glass (30\u0026times;20\u0026times;1 mm\u003csup\u003e3\u003c/sup\u003e) each at top and bottom. The eggs were then randomly moved to clean plastic petri dishes (diameter\u0026thinsp;=\u0026thinsp;10 cm). Water bath was set for five treatments of 35, 36, 37, 38, and 39\u0026deg;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\u0026deg;C. Survival and developmental stages (egg, larva, protonymph and deutonymph) were recorded every 12 h until adulthood. Approximate 100 \u003cem\u003eA. orientalis\u003c/em\u003e, 60 \u003cem\u003eN. californicus\u003c/em\u003e and 50 \u003cem\u003eN. barkeri\u003c/em\u003e were recorded respectively. These predatory mites treated by 39\u0026deg;C were then mated. We observed their reproduction periods (pre-oviposition, oviposition and post-oviposition stages), fecundity and longevity for 100 \u003cem\u003eA. orientalis\u003c/em\u003e, 60 \u003cem\u003eN. californicus\u003c/em\u003e and 50 \u003cem\u003eN. barkeri\u003c/em\u003e, respectively.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eEffects of heat stresses on predatory mite female adult\u003c/h2\u003e \u003cp\u003eThe deutonymphs of \u003cem\u003eA. orientalis\u003c/em\u003e, \u003cem\u003eN. californicus\u003c/em\u003e and \u003cem\u003eN. barkeri\u003c/em\u003e were randomly selected and placed in new plastic boxes (d\u0026thinsp;=\u0026thinsp;16 cm, h\u0026thinsp;=\u0026thinsp;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\u0026deg;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\u0026deg;C. We daily recorded the indices of egg production and survival rate for 100 \u003cem\u003eA. orientalis\u003c/em\u003e, 50 \u003cem\u003eN. californicus\u003c/em\u003e and 50 \u003cem\u003eN. barkeri\u003c/em\u003e, respectively.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003eData analysis\u003c/h2\u003e \u003cp\u003eAll 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\u0026deg;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.\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cdiv id=\"Sec7\" class=\"Section2\"\u003e \u003ch2\u003eEffect of high temperature on survival of three predatory mites\u003c/h2\u003e \u003cp\u003eBoth \u003cem\u003eN. barkeri\u003c/em\u003e and \u003cem\u003eN. californicus\u003c/em\u003e were more tolerant to heat stress than \u003cem\u003eA. orientalis\u003c/em\u003e (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). Shocked by high temperatures at egg stage, the survival rate of \u003cem\u003eA. orientalis\u003c/em\u003e decreased from 37\u0026deg;C (\u003cem\u003eχ\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e\u003csub\u003e(5)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;28.810, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001), compared with the decreased survival rate of \u003cem\u003eN. californicus\u003c/em\u003e from 39\u0026deg;C (\u003cem\u003eχ\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e\u003csub\u003e(5)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;11.690, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.039). A series of high temperature stresses did not significantly affect the survival rate of \u003cem\u003eN. barkeri\u003c/em\u003e (\u003cem\u003eχ\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e\u003csub\u003e(5)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;9.886, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.079). High temperatures at adult stage also damaged mite survival rates. \u003cem\u003eA. orientalis\u003c/em\u003e completely died at 40\u0026deg;C (\u003cem\u003eχ\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e\u003csub\u003e(4)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;288.900, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001), while \u003cem\u003eN. barkeri\u003c/em\u003e and \u003cem\u003eN. californicus\u003c/em\u003e reduced life time by 50% (\u003cem\u003eN. californiulus\u003c/em\u003e: \u003cem\u003eχ\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e\u003csub\u003e(4)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;121.800, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001; \u003cem\u003eN. barkeri\u003c/em\u003e: \u003cem\u003eχ\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e\u003csub\u003e(4)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;110.800, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003eEffects of high temperature at egg stage on mite development and reproduction\u003c/h2\u003e \u003cp\u003eThe developmental time of three predatory mites were all significantly shortened after high temperature treated at egg stage (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). The egg period of \u003cem\u003eN. californiulus\u003c/em\u003e was shortened from 1.78 d to 0.96 d. (Z = -8.632, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001) and the protonymph stage from 1.40 d to 0.87 d (Z = -7.991, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001). As a heat tolerant species, \u003cem\u003eN. barkeri\u003c/em\u003e deutonymph was also affected by high temperature for reducing developmental time from 2.53 d to 1.68 d (Z = -6.238, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eHeat stress on egg stage can shorten the oviposition time of three predatory mites (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e). The pre-oviposition period was significantly shorter in the \u003cem\u003eN. californius\u003c/em\u003e and \u003cem\u003eN. barkeri\u003c/em\u003e, while no significant change in \u003cem\u003eA. orientalis\u003c/em\u003e (\u003cem\u003eN. californius\u003c/em\u003e: Z = -5.253, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001; \u003cem\u003eN. barkeri\u003c/em\u003e: Z = -3.970, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001). The oviposition period of \u003cem\u003eN. californicus\u003c/em\u003e was shortened from 19.46 d to 11.50 d (Z = -6.151, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001), whereas \u003cem\u003eN. barkeri\u003c/em\u003e was less affected by temperature (\u003cem\u003et\u003c/em\u003e\u003csub\u003e(43)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;2.381, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.022). The post-oviposition time of \u003cem\u003eN. californicus\u003c/em\u003e and \u003cem\u003eN. barkeri\u003c/em\u003e was also strikingly reduced after high treatment (\u003cem\u003eN. californicus\u003c/em\u003e: \u003cem\u003et\u003c/em\u003e\u003csub\u003e(107)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;5.291, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001; \u003cem\u003eN. barkeri\u003c/em\u003e: \u003cem\u003et\u003c/em\u003e\u003csub\u003e(43)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;5.518, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eThe negative effect of heat stress on egg stage can be passed over to reproductive stage by reducing the fecundity of three predatory mites (Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003e). The total fecundity of \u003cem\u003eA. orientalis\u003c/em\u003e and \u003cem\u003eN. californicus\u003c/em\u003e decreased by 50% (\u003cem\u003eA. orientali\u003c/em\u003e: \u003cem\u003et\u003c/em\u003e\u003csub\u003e(64)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;8.036, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001; \u003cem\u003eN. californicus\u003c/em\u003e: \u003cem\u003et\u003c/em\u003e\u003csub\u003e(107)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;12.712, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001). The daily fecundity of \u003cem\u003eA. orientalis\u003c/em\u003e and \u003cem\u003eN. barkeri\u003c/em\u003e was accordingly affected by heat stress (\u003cem\u003eA. orientalis\u003c/em\u003e: \u003cem\u003et\u003c/em\u003e\u003csub\u003e(64)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;8.241, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001; \u003cem\u003eN. barkeri\u003c/em\u003e: \u003cem\u003et\u003c/em\u003e\u003csub\u003e(43)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;4.164, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec9\" class=\"Section2\"\u003e \u003ch2\u003eEffects of adult heat stress on mite reproduction and longevity\u003c/h2\u003e \u003cp\u003eHeat stress at adult stage reduced the longevity of three predatory mites (Fig.\u0026nbsp;\u003cspan refid=\"Fig6\" class=\"InternalRef\"\u003e6\u003c/span\u003e). \u003cem\u003eA. orientalis\u003c/em\u003e 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 \u003cem\u003eN. californicus\u003c/em\u003e was shortened from 30.80 d to 12.54 d (\u003cem\u003eχ\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e\u003csub\u003e(4)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;101.406, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001) and \u003cem\u003eN. barkeri\u003c/em\u003e was shortened from 23.96 d to 10.42 d (\u003cem\u003eχ\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e\u003csub\u003e(4)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;89.183, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001). The oviposition period was mostly affected by temperature in \u003cem\u003eA. orientalis\u003c/em\u003e, since the duration was decreased from 18.26 d to 3.82 d at 39℃ (\u003cem\u003eχ\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e\u003csub\u003e(4)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;127.398, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001). The oviposition period of \u003cem\u003eN. californicus\u003c/em\u003e was shortened from 19.46 d to 6.14 d at 40\u0026deg;C (\u003cem\u003eχ\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e\u003csub\u003e(4)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;96.857, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001), and that of \u003cem\u003eN. barkeri\u003c/em\u003e from 13.30 d to 4.32 d (\u003cem\u003eχ\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e\u003csub\u003e(4)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;109.549, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eAdult heat stress also decreased lifetime fecundity and daily reproduction in three predatory mites (Fig.\u0026nbsp;\u003cspan refid=\"Fig7\" class=\"InternalRef\"\u003e7\u003c/span\u003e). The total fecundity of \u003cem\u003eA. orientalis\u003c/em\u003e was most affected by high temperature, while that of \u003cem\u003eN. barkeri\u003c/em\u003e was the least. No reproduction was available in \u003cem\u003eA. orientalis\u003c/em\u003e, since all mites died at 40℃ (\u003cem\u003eχ\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e\u003csub\u003e(4)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;155.174, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001). The total fecundity of \u003cem\u003eN. californicus\u003c/em\u003e was reduced about 60% from 27.74 to 10.76 (\u003cem\u003eχ\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e\u003csub\u003e(4)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;137.721, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001) and \u003cem\u003eN. barkeri\u003c/em\u003e was reduced by about 70% from 10.22 to 2.98 eggs in the treatments of 37\u0026deg;C to 40\u0026deg;C. Correspondingly, mite daily fecundity after treated by 39\u0026deg;C decreased from 1.47 to 0.78 eggs in \u003cem\u003eA. orientalis\u003c/em\u003e (\u003cem\u003eχ\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e\u003csub\u003e(4)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;127.798, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001), 2.93 to 1.47 eggs in \u003cem\u003eN. californicus\u003c/em\u003e (\u003cem\u003eχ\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e\u003csub\u003e(4)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;86.044, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001), and 1.78 to 0.56 eggs in \u003cem\u003eN. barkeri\u003c/em\u003e (\u003cem\u003eχ\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e\u003csub\u003e(4)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;135.474, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003eTemperature affects invertebrate developmental rate, behavioral response, survival and reproduction (Hoffmann \u003cem\u003eet al.\u003c/em\u003e 2011; Colinet et al. \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2015\u003c/span\u003e), and predatory mites are no exception. The optimal temperature for \u003cem\u003eN. barkeri\u003c/em\u003e development is about 24\u0026deg;C and in the range of 16 to 32\u0026deg;C can develop and reproduce (Xia et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2012\u003c/span\u003e). More than 97% of \u003cem\u003eN. californicus\u003c/em\u003e eggs are able to hatch from 15 to 35\u0026deg;C (Gotoh et al. \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2004\u003c/span\u003e). Short-term high temperature stress has been reported to reduce survivals of \u003cem\u003eN. californicus\u003c/em\u003e (Yuan et al. \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2015\u003c/span\u003e), \u003cem\u003ePanonychus citri\u003c/em\u003e (Yang et al. \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2014\u003c/span\u003e), and \u003cem\u003eMononychellus tanajoa\u003c/em\u003e (Lu et al. \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). Survival of \u003cem\u003eN. barkeri\u003c/em\u003e eggs decreased dramatically after short-term heat exposure at 38\u0026deg;C, 40\u0026deg;C and 42\u0026deg;C (Li et al. \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). When \u003cem\u003eP. persimilis\u003c/em\u003e was treated at 40\u0026deg;C for 2 h, 75% eggs survived; when treated at 40\u0026deg;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\u0026deg;C, and the \u003cem\u003eN. barkeri\u003c/em\u003e eggs were more heat resistant than the other two species. The tolerance of these three predatory mite adults also showed that \u003cem\u003eN. barkeri\u003c/em\u003e was more resistant to heat stress. Although \u003cem\u003eN. barkeri\u003c/em\u003e showed some advantages compared to other species, short-term high temperatures still reduced the survival rates, adversely affecting their population growth.\u003c/p\u003e \u003cp\u003eHigh temperatures can not only cause the death of predatory mites, but also reduce their fecundity (Vollmer et al. \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Silbermann and Tatar \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2000\u003c/span\u003e). When short-term exposed at 38℃ and 40℃ at egg stage, the fitness of \u003cem\u003eN. barkeri\u003c/em\u003e was significantly decreased (Jafari et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Jafari et al. \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Xia et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2012\u003c/span\u003e), and daily fecundity of female adults treated at 40℃ significantly decreased than that at 38℃ (Li et al. \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). 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. \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Speakman and Garratt 2013). The fact of the least variable of daily fecundity and most reduction of life span in \u003cem\u003eN. californicus\u003c/em\u003e 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. \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Forster et al. \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). 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.\u003c/p\u003e \u003cp\u003eConsistent with our research, damage caused by heat stress was often at the cost of longevity and reproduction (Yang et al. \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Yuan et al. \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). It has been reported that the lifetime fecundity of \u003cem\u003eN. californicus\u003c/em\u003e at 30\u0026deg;C is significantly lower than that at 20\u0026deg;C and 25\u0026deg;C, and the daily reproduction at 20\u0026deg;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. \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2004\u003c/span\u003e). The adult females of \u003cem\u003eMononychellus tanajoa\u003c/em\u003e did not lay eggs after being treated with 42\u0026deg;C for 4 h (Lu et al. \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). After 2 h of 40\u0026deg;C treatment, the fecundity of \u003cem\u003eN. barkeri\u003c/em\u003e decreased by more than 50%, indicating that the short-term high temperature can limit its population expansion (Li et al. \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). 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 \u003cem\u003eA. orientalis\u003c/em\u003e treated with same duration of 39℃ at egg stage and adult stage were 17.84 and 4.22 eggs, and that of \u003cem\u003eN. barkeri\u003c/em\u003e 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. \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). 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.\u003c/p\u003e \u003cp\u003eHigh 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. \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). In this experiment, we compared the heat tolerance of three common commercial predatory mites. The results showed that \u003cem\u003eA. orientalis\u003c/em\u003e was more sensitive to high temperature and it may not be suitable for high temperature environments. \u003cem\u003eN. barkeri\u003c/em\u003e 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. \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Silbermann and Tatar \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2000\u003c/span\u003e; Zhang et al. \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). 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.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e \u003ch2\u003eConflict of interest\u003c/h2\u003e \u003cp\u003eThe authors have declared that no competing interest exits.\u003c/p\u003e \u003c/p\u003e\u003ch2\u003eAuthor Contribution\u003c/h2\u003e\u003cp\u003eXuemin 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. 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Acta Ecol Sin 28:4830\u0026ndash;4840\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"Biological control, Amblyseius orientalis, Neoseiulus californicus, Neoseiulus californicus, short-term high temperatures, developmental stage","lastPublishedDoi":"10.21203/rs.3.rs-3886808/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3886808/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eTo explore the performances of predatory mites under high temperature, we selected three predatory mites \u003cem\u003eAmblyseius orientalis\u003c/em\u003e, \u003cem\u003eNeoseiulus californicus\u003c/em\u003e and \u003cem\u003eNeoseiulus barkeri\u003c/em\u003e 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 \u003cem\u003eN. barkeri\u003c/em\u003e were most tolerant to heat stress than \u003cem\u003eN. californicus\u003c/em\u003e and \u003cem\u003eA. orientalis\u003c/em\u003e. After heat treatment of 39\u0026deg;C on egg, three predatory mites all presented shorter developmental period and longevity as well as lower fecundity. The oviposition period of \u003cem\u003eN. californicus\u003c/em\u003e was shortened by nearly 50% and the total egg production of \u003cem\u003eA. orientalis\u003c/em\u003e decreased by about 40%. However, the \u003cem\u003eN. barkeri\u003c/em\u003e 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 \u003cem\u003eA. orientalis\u003c/em\u003e was reduced from 18.26 days to 3.82 days at 39℃, and 100% mortality occurred at 40\u0026deg;C. The longevity of \u003cem\u003eN. californicus\u003c/em\u003e and \u003cem\u003eN. barkeri\u003c/em\u003e suffered at 40℃ was shortened by about 50%. Our study confirmed that \u003cem\u003eN. barkeri\u003c/em\u003e is tolerant to high temperatures at some extent, while \u003cem\u003eA. orientalis\u003c/em\u003e 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.\u003c/p\u003e","manuscriptTitle":"Effects of heat stresses on fitness of three commercial predatory mites","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-01-24 16:09:24","doi":"10.21203/rs.3.rs-3886808/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"a8ddd578-a801-439a-86fe-0719f9f46e33","owner":[],"postedDate":"January 24th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2024-06-04T20:38:31+00:00","versionOfRecord":[],"versionCreatedAt":"2024-01-24 16:09:24","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-3886808","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3886808","identity":"rs-3886808","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}