Dayoub, Ahmad Malek ¹ ; Dib, Hazem ² and Boubou, Angham ³

¹Department of Plant Protection, Faculty of Agriculture, Tishreen University, Latakia, Syria.
²Department of Plant Protection, Faculty of Agriculture, Tishreen University, Latakia, Syria & Univ. Avignon, Aix Marseille Univ., CNRS, IRD, IMBE, Pôle Agrosciences, 301 rue Baruch de Spinoza, BP 21239, 84916 Avignon, France.
³✉ Department of Plant Protection, Faculty of Agriculture, Tishreen University, Latakia, Syria.

2022 - Volume: 62 Issue: 3 pages: 597-607

Original research

Keywords

Abstract

Introduction

The tomato red spider mite, Tetranychus evansi Baker & Pritchard, considered to have originated in South America, has emerged as a destructive invasive pest of solanaceous crops worldwide (Boubou et al. 2011; Navajas et al. 2013).

The Syrian coastal region, which includes Latakia and Tartus governorates, is one of the main solanaceous crop producers in Syria and provides more than 50% of the total national tomato (Solanum lycopersicum L.; Solanaceae) production in both protected and open-field conditions (AASA 2018). Tetranychus evansi was first detected in Latakia governorate in 2011, on tomato and black nightshade (Solanum nigrum L.) (Zriki et al. 2015). According to Migeon et al. (2009), the Mediterranean climate of the Syrian coastal region is highly favorable for development and establishment of T. evansi, and resulting outbreaks could be dramatic.

Due to the threat that this mite represents to agriculture in this region, information about its distribution, host plants and associated natural enemies is crucial for designing successful pest management programs. In a recent study, we reported new records of this mite species and of two associated predaceous insects, namely Feltiella acarisuga (Vallot) (Diptera: Cecidomyiidae) and Stethorus gilvifrons (Mulsant) (Coleoptera: Coccinellidae) on tomato and black nightshade plants in Latakia governorate (Dayoub et al. 2020). In the present study, we complete the previous reports and report additional localities, host plants, and predators identified in association with T. evansi in the Syrian coastal region.

Material and methods

Surveys were conducted in 187 sites distributed across all districts of Latakia and Tartus governorates (Figure 1), from March to November of 2019 and 2020. Because of the economic importance and widespread cultivation of solanaceous crops in this area, sampling efforts were restricted to plants of this family. At each site, samples were taken from crops in open fields and/or greenhouses and from weeds from the surroundings of cultivated plots or spontaneously growing along roads and watercourses. Crops sampled were eggplant (Solanum melongena L.) in 55 open field and 21 greenhouse crops, tomato in 11 open field and 24 greenhouse crops, tobacco (Nicotiana tabacum L.) in 22 open field crops, and potato (Solanum tuberosum L.) in 17 open field crops. Weeds included 70 samples of black nightshade (S. nigrum), 10 samples of red nightshade (Solanum villosum Mill.), and 7 samples of jimson weed (Datura sp.).

A total of 237 plant samples were collected, each consisting of 30 leaves of each solanaceous species. Each sample was placed in a plastic bag and transported to the laboratory, where leaves were examined under a stereomicroscope (Micros, Ladybird MZ1240, Austria). Mites were counted and collected with a fine brush in 70% ethanol, and later mounted in Hoyer's medium for identification. However, when spider mites were too numerous, their numbers were visually estimated. When mixed populations of T. evansi and Tetranychus urticae Koch were present, the respective numbers of nymphs and adults were estimated according to the presence of spots and body coloration. Then, 20 males and 20 females of each of them were collected and mounted to confirm the identification. Predatory insects belonging to the families Cecidomyiidae, Coccinellidae, Staphylinidae and Thripidae, well known as natural enemies of spider mites (Chazeau 1985), were also counted and collected. Cecidomyiid and coccinellid insects were prepared for identification as in Dayoub et al. (2020). For coccinellid insects, male genitalia were extracted and then mounted in a drop of glycerin on a slide to examine important diagnostic features. To identify cecidomyiid predators, some of the ethanol preserved adults were cleared in KOH and subsequently slide-mounted in Hoyer's medium. Adult thrips were macerated in KOH, dehydrated using absolute ethanol, and mounted in Hoyer's medium, following the method of Mirab-Balou and Chen (2010).

Mites were identified at family level using the keys by Krantz and Walter (2009). Identification was carried out to species level whenever possible and to genus level otherwise, using the identification keys provided in the following publications: Tetranychidae (Baker and Pritchard 1960; Jeppson et al. 1975; Seeman and Beard 2011), Tenuipalpidae (Beard et al. 2015; Mesa et al. 2009; Welbourn et al. 2003), Tarsonemidae (Nucifora and Vacante 2004; Zhang 2003), Phytoseiidae (Barbar 2013; Döker et al. 2016, 2020; Ferragut 2018; Kreiter et al. 2016, 2020), Anystidae (Smith Mayer and Ueckermann 1987), Stigmaeidae (Fan et al. 2016; Gonzalez 1963; Koç et al. 2005) and Iolinidae (Panou et al. 2001). Predatory insects were identified using the identification keys provided by: Cecidomyiidae (Gagné 1995, 2018), Coccinellidae (Kapur 1948), and Thripidae (Mirab-Balou et al. 2013; Mound 2011).

Slide-mounted specimens were deposited as voucher specimens at the laboratory of Plant Protection Research, Faculty of Agriculture, Tishreen University, Latakia, Syria****. For the purpose of this paper, only plant samples infested with T. evansi were presented in the results.

Results

Tetranychus evansi was found in 29 sites (15.5% of the sampling sites), from all districts in the governorates of Latakia (19 sites) and Tartus (10 sites), at elevations ranging from 17 to 1110 meters above sea level (Table 1, Figure 1). Sixteen of the sites were cultivations in open fields; in nine of these, T. evansi was collected from crop plants only, in three from adjacent solanaceous weeds only, and in four from both crop plants and weeds. Thirteen of the sites were uncultivated, where black nightshade grew naturally along roads and watercourses (Table 1). Despite comparable sampling efforts, T. evansi was not reported from greenhouse crops nor in tobacco fields.

Out of 237 plant samples, T. evansi was found in 34 samples (14.3%) from five plant species: tomato (3 samples), eggplant (7), potato (4), black nightshade (18) and red nightshade (2). In 64.7% of these samples (22), no other phytophagous mites were observed in association with T. evansi, and 68.2% of the samples with T. evansi as the sole phytophagous mite (15 out of 22) referred to heavily infested black and red nightshade plants (Table 1).

Five phytophagous mite species were identified in association with T. evansi on 12 samples, and T. urticae was the most frequent (83.3%), particularly on cultivated plants (Table 1).

A total of 515 specimens of predators belonging to four species of insects and ten species of mites were found (Table 1). Predatory insects were more frequent (76.5%) and abundant (415 specimens) than predatory mites (respectively 47.1% and 102 specimens).

Feltiella acarisuga was the most frequent and abundant predator; 288 specimens of this acarophagous gall midge were collected in 22 (out of 34) samples of all plant species infested by T. evansi (Table 2). The second most frequent (14 samples) and abundant (131 specimens) predatory insect was S. gilvifrons, collected mainly on S. nigrum and S. melongena.Scolothrips longicornis Priesner (Thysanoptera: Thripidae) was the third most frequent and abundant predator. It was found in seven samples, mostly of S. nigrum. Preliminary observations conducted in the laboratory showed that larvae and adults of S. longicornis preyed on all developmental stages of T. evansi (Figure 2).

This is the first record of S. longicornis in Syria. Diagnostic morphological characters of this species include: (1) the presence of three dark bands or spots on forewings (including clavus); (2) a pronotum lacking a pair of posteromesad discal setae; (3) the absence of any dark/shaded patterns on the thorax and abdomen; (4) the white color of the antennal segment II; and (5) the males are hemimacropterous (Figure 3).

The most common predatory mites collected in this study belonged to Phytoseiidae, and Phytoseiulus persimilis Athias-Henriot was the most frequent and abundant species among them (Tables 1, 2). In addition, among other predatory mites found in this study, Anystis baccarum (L.) is reported for the first time in Syria.

Discussion

Tetranychus evansi was shown to be widely distributed in the Syrian coastal region, though at low frequencies. It was found in a variety of landscapes and elevations, ranging from the coastal plains to high altitudes in the Coastal Mountain Range. Our current data on the occurrence of T. evansi in this region agree with predictions by Migeon et al. (2009) using CLIMEX® model. The Syrian coastal region was categorized as a very suitable habitat for T. evansi, owing to its Mediterranean climate, particularly mild winters, which favor the establishment of this mite (Migeon et al. 2009). According to this model, that would be the case for large areas of northwestern, northeastern, and southwestern Syria. Therefore, additional surveys are needed to investigate the distribution of this mite in these regions, where solanaceous crops are also grown.

In this study, T. evansi was collected from wild and cultivated solanaceous plants. Its frequent occurrence, at high population levels, on black nightshade is of particular interest, as this plant is very common at the Syrian coast, especially in irrigated fields and alongside watercourses, and could serve as a reservoir of T. evansi, threatening nearby solanaceous crops. However, it could also serve as a reservoir of natural enemies of this mite.

On field-cultivated tomato, eggplant, and potato plants, T. evansi was observed at very high population levels at some sites of Latakia and Tartus governorates (i.e., Al-Dakleyiah and Besaysin). The absence of T. evansi in samples from greenhouses is puzzling, but it could be due to the heavy usage of various synthetic acaricides (up to 10 sprays a month) (AMD, personal observations) in these agricultural systems. Previous studies showed the sensitivity of T. evansi to different acaricides (Blair 1989; Migeon 2007; Gotoh et al. 2011; Toroitich et al. 2014). However, the potential selection for resistance when relying heavily on synthetic pesticides for controlling spider mites should not be disregarded (Azandémè-Hounmalon et al. 2015). Therefore, finding alternative, effective, and sustainable methods to manage T. evansi populations, such as the use of biological control agents, is necessary.

The presence of F. acarisuga, S. gilvifrons, and S. longicornis at various developmental stages on cultivated and wild solanaceous plants infested with T. evansi, mostly in the absence of any other prey on the same plant, suggested that they were developing solely on this mite. Their biology and efficacy as control agents of T. evansi should be the subject of future research.

The gall midge F. acarisuga has been mentioned as an important cosmopolitan predator of Tetranychidae (Gagné 1995; Gagné and Jaschhof 2017). It is considered a key natural enemy that reduces the population density of spider mites in diverse cropping systems (Gillespie et al. 1997; Sharaf 1984). Feltiella acarisuga is commercially mass-reared in many countries for use in augmentative biological control programs (Van Lenteren 2012). This predator was also found in association with T. evansi in other invaded regions, viz. Spain (Escudero et al. 2005) and Japan (Abe et al. 2011). In northeastern Brazil, where the mite has been considered to have originated, larvae of Feltiella curtistylus Gagné were found preying on T. evansi on tomato plants (Gagné 1995).

Stethorus gilvifrons is an indigenous species widely distributed in the Middle East and southern Europe (Kovář 2007). Earlier surveys in the Syrian coastal region suggested this species to be an important predator of T. urticae on several solanaceous plants (Mofleh 2010), as well as of Panonychus citri (McGregor) and Eutetranychus orientalis (Klein) in citrus orchards (Qerhili 2015). The tropical congener, Stethorus tridens Gordon, is considered a promising biocontrol agent of T. evansi. This voracious predator can develop and reproduce when feeding on T. evansi under laboratory conditions (Britto et al. 2009; Fiaboe et al. 2007).

In this study, the predatory thrips S. longicornis was recorded for the first time in Syria. Species of the genus Scolothrips Hinds are obligate predators of tetranychid and tenuipalpid mites and have the potential for use in the biological control of these mites. Two Scolothrips species were previously reported from Syria in local publications: S. latipennis Priesner (Obeid 2007) and S. sexmaculatus (Pergande) (Mofleh 2010). However, there are probably misidentifications in earlier studies under the name S. sexmaculatus in areas outside North America (Masumoto 2010; Laurence Mound, personal communication), and no voucher specimens are available to confirm the identity of previous Scolothrips records in Syria.

This is also the first report of S. longicornis preying upon T. evansi. Species of Scolothrips are commercially available and distributed under the name ''six-spotted thrips'' (Mound 2011). Scolothrips longicornis is a native beneficial thrips in the Mediterranean and Middle East areas (Fathipour and Maleknia 2016). The potential of this predatory thrips for the biological control of several spider mites, including T. urticae, has also been reported (García-Marí and González-Zamora 1999; Pakyari et al. 2011; Heidarian et al. 2012).

Regarding phytoseiids, previous evaluations of 12 species, including the two most common in the present study, P. persimilis and Typhlodromus (Anthoseius) recki Wainstein, have reported T. evansi to be an unsuitable prey (de Moraes and McMurtry 1985; Escudero and Ferragut 2005; Tixier et al. 2020). In contrast, Brazilian and Argentine populations of the phytoseiid species Phytoseiulus longipes Evans, which were found in association with T. evansi on solanaceous plants, showed promising results in the biological control of T. evansi under laboratory and greenhouse conditions (Ferrero et al. 2007, 2011; Furtado et al. 2006, 2007). However, because P. longipes is a neotropical species, its introduction into Syria will encounter regulatory and environmental challenges. Therefore, efforts should be concentrated on testing promising natural enemies identified in this study (i.e., F. acarisuga, S. gilvifrons, and S. longicornis) and on the detection of additional biocontrol candidates.

Acknowledgements

The authors thank Dr Laurence A. Mound (CSIRO) for the helpful discussion on the identity of Scolothrips species, and Alain Migeon (UMR CBGP (INRAE – Montpellier – France)) for his valuable comments on an earlier version of this paper. We also express our appreciation to the editor (Prof. Serge Kreiter) and three anonymous reviewers whose constructive comments and valuable suggestions greatly improved this manuscript.

References

1. AASA. 2018. Annual Agricultural Statistical Abstract. Damascus, Syria: Department of Planning and Statistics Division of Agricultural Statistics, Ministry of Agriculture and Agrarian Reform.
2. Abe J., Ganaha-Kikumura T., Yukawa J. 2011. Morphological features, distribution, prey mites, and life history traits of Feltiella acarisuga (Vallot) (Diptera: Cecidomyiidae) in Japan. Appl. Entomol. Zool., 46(2): 271-279. https://doi.org/10.1007/s13355-011-0038-x
3. Azandémè-Hounmalon G.Y., Affognon H.D., Komlan F.A., Tamò M., Fiaboe K.K.M., Kreiter S., Martin T. 2015. Farmers' control practices against the invasive red spider mite, Tetranychus evansi Baker & Pritchard in Benin. Crop Protection, 76: 53-58. https://doi.org/10.1016/j.cropro.2015.06.007
4. Baker E.W., Pritchard A.E. 1960. The tetranychoid mites of Africa. Hilgardia, 29(11). https://doi.org/10.3733/hilg.v29n11p455
5. Barbar Z. 2013. Survey of phytoseiid mite species (Acari: Phytoseiidae) in citrus orchards in Lattakia governorate, Syria. Acarologia. 53 (3): 247-261. https://doi.org/10.1051/acarologia/20132098
6. Beard J.J., Ochoa R., Braswell W.E., Bauchan G.R. 2015. Brevipalpus phoenicis (Geijskes) species complex (Acari: Tenuipalpidae)-a closer look. Zootaxa, 3944, 1-67. https://doi.org/10.11646/zootaxa.3944.1.1
7. Blair B.W. 1989. Laboratory screening of acaricides against Tetranychus evansi Baker & Pritchard. Crop Protection, 8(3): 212-216. https://doi.org/10.1016/0261-2194(89)90029-X
8. Boubou A., Migeon A., Roderick G.K., Navajas M. 2011. Recent emergence and worldwide spread of the red tomato spider mite, Tetranychus evansi: Genetic variation and multiple cryptic invasions. Biol. Invasions, 13(1): 81-92. https://doi.org/10.1007/s10530-010-9791-y
9. Britto E.P.J., Gondim M.G.C., Torres J.B., Fiaboe K.K.M., de Moraes G.J., Knapp M. 2009. Predation and reproductive output of the ladybird beetle Stethorus tridens preying on tomato red spider mite Tetranychus evansi. BioControl, 54(3): 363-368. https://doi.org/10.1007/s10526-008-9178-5
10. Chazeau J. 1985. Predaceous insects. Spider Mites: Their Biology, Natural Enemies and Control, 1: 211-246.
11. Dayoub A.M., Dib H., Boubou A. 2020. First record of two insects preying on the red tomato spider mite Tetranychus evansi (Acari: Tetranychidae) in Latakia governorate, Syria. Acarologia, 60(4): 872-877. https://doi.org/10.24349/acarologia/20204406
12. de Moraes G.J., McMurtry J.A. 1985. Comparison of Tetranychus evansi and T. urticae [Acari: Tetranychidae] as prey for eight species of phytoseiid mites. Entomophaga, 30(4): 393-397. https://doi.org/10.1007/BF02372345
13. Döker I., Kazak C., Karut K. 2016. Contributions to the Phytoseiidae (Acari: Mesostigmata) fauna of Turkey: morphological variations, twelve new records, re-description of some species and a revised key to the Turkish species. Syst. Appl. Acarol., 21(4): 505-527. https://doi.org/10.11158/saa.21.4.10
14. Döker I., Kazak C., Karut K. 2020. The genus Amblyseius Berlese (Acari: Phytoseiidae) in Turkey with discussion on the identity of Amblyseius meridionalis. Syst. Appl. Acarol., 25(8): 1395-1420. https://doi.org/10.11158/saa.25.8.4
15. Escudero L.A., Baldó-Gosálvez M., Ferragut F. 2005. Eficacia de los fitoseidos como depredadores de las arañas rojas de cultivos hortícolas Tetranychus urticae, T. turkestani, T. ludeni y T. evansi (Acari: Tetranychidae). Bol. San. Veg. Plagas, 31: 377-383.
16. Escudero L.A., Ferragut F. 2005. Life-history of predatory mites Neoseiulus californicus and Phytoseiulus persimilis (Acari: Phytoseiidae) on four spider mite species as prey, with special reference to Tetranychus evansi (Acari: Tetranychidae). Biol. Control, 32(3): 378-384. https://doi.org/10.1016/j.biocontrol.2004.12.010
17. Fan Q.-H., Flechtmann C.H.W., Moraes G.J.D. 2016. Annotated catalogue of Stigmaeidae (Acari: Prostigmata), with a pictorial key to genera. Zootaxa, 4176(1): 1-199. https://doi.org/10.11646/zootaxa.4176.1.1
18. Fathipour Y., Maleknia B. 2016. Mite predators. In Ecofriendly pest management for food security (pp. 329-366). Academic Press. https://doi.org/10.1016/B978-0-12-803265-7.00011-7
19. Ferragut F. 2018. New records of phytoseiid mites of the subfamilies Typhlodrominae and Phytoseiinae (Acari: Phytoseiidae) from Spain, with description of a new species and re-description of four species of Typhlodromus Scheuten. Syst. Appl. Acarol., 23(5): 883-910. https://doi.org/10.11158/saa.23.5.8
20. Ferrero M., Calvo F.J., Atuahiva T., Tixier M.S., Kreiter S. 2011. Biological control of Tetranychus evansi Baker & Pritchard and Tetranychus urticae Koch by Phytoseiulus longipes Evans in tomato greenhouses in Spain [Acari: Tetranychidae, Phytoseiidae]. Biol. Control, 58(1): 30-35. https://doi.org/10.1016/j.biocontrol.2011.03.012
21. Ferrero M., Moraes G.J.D., Kreiter S., Tixier M.S., Knapp M. 2007. Life tables of the predatory mite Phytoseiulus longipes feeding on Tetranychus evansi at four temperatures (Acari: Phytoseiidae, Tetranychidae). Exp. Appl. Acarol., 41(1): 45-53. https://doi.org/10.1007/s10493-007-9053-6
22. Fiaboe K.K.M., Gondim M.G.C., Moraes G.J.D., Ogol C.K.P.O., Knapp M. 2007. Bionomics of the acarophagous ladybird beetle Stethorus tridens fed Tetranychus evansi. J. Appl. Entomol., 131(5): 355-361. https://doi.org/10.1111/j.1439-0418.2007.01189.x
23. Furtado I.P., Moraes G.J.D., Kreiter S., Knapp M. 2006. Search for effective natural enemies of Tetranychus evansi in south and southeast Brazil. Exp. Appl. Acarol., 40(3): 157-174. https://doi.org/10.1007/s10493-006-9045-y
24. Furtado I.P., De Moraes G.J., Kreiter S., Tixier M.-S., Knapp M. 2007. Potential of a Brazilian population of the predatory mite Phytoseiulus longipes as a biological control agent of Tetranychus evansi (Acari: Phytoseiidae, Tetranychidae). Biol. Control, 42(2): 139-147. https://doi.org/10.1016/j.biocontrol.2007.04.016
25. Gagné R.J. 1995. Revision of tetranychid (Acarina) mite predators of the genus Feltiella (Diptera: Cecidomyiidae). Ann. Entomol. Soc. Am., 88(1): 16-30. https://doi.org/10.1093/aesa/88.1.16
26. Gagné R.J. 2018. Key to adults of North American genera of the subfamily Cecidomyiinae (Diptera: Cecidomyiidae). Zootaxa, 4392(3): 401-457. https://doi.org/10.11646/zootaxa.4392.3.1
27. Gagné R.J., Jaschhof M. 2017. A Catalog of the Cecidomyiidae (Diptera) of the World. 4th Edition. Digital Version 3. USDA, Washington, USA. https://www.ars.usda.gov/ARSUserFiles/80420580/Gagne_2017_World_Cat_4th_ed.pdf
28. García-Marí F., González-ZamoraJ.E. 1999. Biological control of Tetranychus urticae (Acari: Tetranychidae) with naturally occurring predators in strawberry plantings in Valenica, Spain. Exp. Appl. Acarol., 23(6): 487-495. https://doi.org/10.1023/A:1006191519560
29. Gillespie D.R., Quiring D.J.M., Greenwood M. 1997. Collection and selection of natural enemies of twospotted spider mites for biological control. J. Entomol. Soc. Brit. Col. 94: 7-11.
30. Gonzalez R.H. 1963. Four new mites of the genus Agistemus Summers. Acarologia, 5: 342-350.
31. Gotoh T., Fujiwara S., Kitashima Y. 2011. Susceptibility to acaricides in nine strains of the tomato red spider mite Tetranychus evansi (Acari: Tetranychidae). Intern. J. Acarol., 37(2): 93-102. https://doi.org/10.1080/01647954.2010.497498
32. Heidarian M., Fathipour Y., Kamali K. 2012. Functional response, switching, and prey-stage preference of Scolothrips longicornis (Thysanoptera: Thripidae) on Schizotetranychus smirnovi (Acari: Tetranychidae). J. Asia Pac. Entomol., 15(1): 89-93. https://doi.org/10.1016/j.aspen.2011.09.003
33. Jeppson L.R., Keifer H.H., Baker E.W. 1975. Mites injurious to economic plants. Berkeley: Univ. of California Press. pp. 614. https://doi.org/10.1525/9780520335431
34. Kapur A.P. 1948. On the Old World species of the genus Stethorus Weise (Coleoptera, Coccinellidae). Bull. Entomol. Res., 39(2): 297-320. https://doi.org/10.1017/S0007485300022434
35. Koç K., Çobanoğlu S., Madanlar N. 2005. Agistemus duzgunesae sp. n. (Acari, Stigmaeidae) from Turkey. Biologia (Bratislava), 60(2): 121-124.
36. Kovář I. 2007. Coccinellidae In Löbl I., Smetana A. Catalogue of Palaearctic Coleoptera, 4: 568-631.
37. Krantz G.W., Walter D.E. 2009. A Manual of Acarology. Third Edition. Lubbock: Texas Tech University Press. pp. 807.
38. Kreiter S., dos Santos V.V., Tixier M.-S., Fontaine O. 2016. An unexpected occurrence of Amblyseius swirskii (Athias-Henriot) in La Réunion Island (Acari: Phytoseiidae). Acarologia, 56(2): 175-181. https://doi.org/10.1051/acarologia/20162254
39. Kreiter S., Payet R.-M., Douin M., Fontaine O., Fillâtre J., Le Bellec F. 2020. Phytoseiidae of La Réunion Island (Acari: Mesostigmata): three new species and two males described, new synonymies, and new records. Acarologia, 60(1): 111-195 https://doi.org/10.24349/acarologia/20204361
40. Masumoto M. 2010. Key to genera of the subfamily Thripinae (Thysanoptera: Thripidae) associated with Japanese plant quarantine. Res. Bull. Pl. Prot. Japan, 46: 25-59.
41. Mesa N.C., Ochoa R., Welbourn W.C., Evans G.A., Moraes G.J.D. 2009. A catalog of the Tenuipalpidae (Acari) of the world with a key to genera. Zootaxa, 2098(1): 1-185. https://doi.org/10.11646/zootaxa.2098.1.1
42. Migeon A. 2007. Acarien rouge de la tomate: Nouvelles observations et perspectives. PHM Revue Horticole, 488 (février), 20-24.
43. Migeon A., Ferragut F., Escudero-Colomar L.A., Fiaboe K.K.M., Knapp M., de Moraes G.J., Ueckermann E., Navajas M. 2009. Modelling the potential distribution of the invasive tomato red spider mite, Tetranychus evansi (Acari: Tetranychidae). Exp. Appl. Acarol., 48(3): 199-212. https://doi.org/10.1007/s10493-008-9229-8
44. Mirab-Balou M., Chen X.-X. 2010. A new method for preparing and mounting thrips for microscopic examination. J. Environ. Entomol., 32(1): 115-121.
45. Mirab-Balou M., Minaei K., Chen X.-X. 2013. An illustrated key to the genera of Thripinae (Thysanoptera, Thripidae) from Iran. Zookeys, 317, 27. https://doi.org/10.3897/zookeys.317.5447
46. Mofleh M. 2010. The efficiency of some predators in biological control of Tetranychus urticae (Koch) (Acari: Tetranychidae) in greenhouses [Ph.D.]. Latakia, Syria: Tishreen University. pp. 125. [in Arabic]
47. Mound L.A. 2011. Species recognition in the genus Scolothrips (Thysanoptera, Thripidae), predators of leaf-feeding mites. Zootaxa, 2797(1): 45-53. https://doi.org/10.11646/zootaxa.2797.1.4
48. Navajas M., de Moraes G.J., Auger P., Migeon A. 2013. Review of the invasion of Tetranychus evansi: Biology, colonization pathways, potential expansion and prospects for biological control. Exp. Appl. Acarol., 59(1-2): 43-65. https://doi.org/10.1007/s10493-012-9590-5
49. Nucifora A., Vacante V.2004. Citrus mites in Italy. VII. The family Tarsonemidae. Species collected and notes on ecology. Acarologia, 44(1/2): 49-67.
50. Obeid A.F. 2007. Ecological and biological studies on the twospotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae) and its natural enemies on potato and common bean in Idlib governorate, Syria [M.Sc.]. Aleppo, Syria: Aleppo University. pp. 127. [in Arabic]
51. Pakyari H., Fathipour Y., Enkegaard A. 2011. Effect of temperature on life table parameters of predatory thrips Scolothrips longicornis (Thysanoptera: Thripidae) fed on twospotted spider mites (Acari: Tetranychidae). J. Econ. Entomol., 104(3): 799-805. https://doi.org/10.1603/EC10144
52. Panou H.N., Emmanouel N.G., Kazmierski A. 2001. Neopronematus, a new genus of the subfamily Pronematinae (Acari: Prostigmata: Tydeidae) and a new species from Greece. Acarologia, 41(3): 321-325.
53. Qerhili S. 2015. A survey and an ecological study of the phytophagous mites and their natural enemies in lemon orchards Citrus limon in Latakia governorate [Ph.D.]. Damascus, Syria: Damascus University. pp. 121. [in Arabic]
54. Seeman O.D., Beard J.J. 2011. Identification of exotic pest and Australian native and naturalised species of Tetranychus (Acari: Tetranychidae). Zootaxa, 2961(1): 1-72. https://doi.org/10.11646/zootaxa.2961.1.1
55. Sharaf N.S. 1984. Studies on natural enemies of tetranychid mites infesting eggplant in the Jordan Valley. Ztschr. f. Angew. Ent., 98(1-5): 527-533. https://doi.org/10.1111/j.1439-0418.1984.tb02745.x
56. Smith Mayer M.P., Ueckermann E.A. 1987. A taxonomic study of some Anystidae (Acari: Prostigmata). Entomology Memoir (Pretoria), 68, Article 68.
57. Tixier M.S., Douin M., Rocio O., Gonzalez L., Pount B., Kreiter S. 2020. Distribution and biological features of Typhlodromus (Anthoseius) recki (Acari: Phytoseiidae) on Tetranychus urticae, T. evansi (Acari: Tetranychidae) and Aculops lycopersici (Acari: Eriophyidae). Acarologia, 60(4): 684-697. https://doi.org/10.24349/acarologia/20204396
58. Toroitich F.J., Knapp M., Nderitu J.H., Olubayo F.M., Obonyo M. 2014. Susceptibility of geographically isolated populations of the tomato red spider mite (Tetranychus evansi Baker & Pritchard) to commonly used acaricides on tomato crops in Kenya. J. Entomol. Acarol. Res., 46(1): 18-25. https://doi.org/10.4081/jear.2014.1469
59. Van Lenteren J.C. 2012. The state of commercial augmentative biological control: Plenty of natural enemies, but a frustrating lack of uptake. BioControl, 57(1): 1-20. https://doi.org/10.1007/s10526-011-9395-1
60. Welbourn W.C., Ochoa R., Kane E.C., Erbe E.F. 2003. Morphological observations on Brevipalpus phoenicis (Acari: Tenuipalpidae) including comparisons with B. californicus and B. obovatus. Exp. Appl. Acarol., 30(1): 107-133. https://doi.org/10.1023/B:APPA.0000006545.40017.a0
61. Zhang Z.Q. 2003. Mites of greenhouses: Identification, biology and control. Wallingford, UK: CABI Publishing. pp. 244.
62. Zriki G., Shaabo A., Boubou A. 2015. A preliminary survey of the spider mites (Acari: Tetranychidae) in Latakia governorate of Syria. Acarologia, 55(3): 303-309. https://doi.org/10.1051/acarologia/2015217

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