1932

Abstract

Western flower thrips, , first arose as an important invasive pest of many crops during the 1970s–1980s. The tremendous growth in international agricultural trade that developed then fostered the invasiveness of western flower thrips. We examine current knowledge regarding the biology of western flower thrips, with an emphasis on characteristics that contribute to its invasiveness and pest status. Efforts to control this pest and the tospoviruses that it vectors with intensive insecticide applications have been unsuccessful and have created significant problems because of the development of resistance to numerous insecticides and associated outbreaks of secondary pests. We synthesize information on effective integrated management approaches for western flower thrips that have developed through research on its biology, behavior, and ecology. We further highlight emerging topics regarding the species status of western flower thrips, as well as its genetics, biology, and ecology that facilitate its use as a model study organism and will guide development of appropriate management practices.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-011019-024947
2020-01-07
2024-06-17
Loading full text...

Full text loading...

/deliver/fulltext/ento/65/1/annurev-ento-011019-024947.html?itemId=/content/journals/10.1146/annurev-ento-011019-024947&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Abd-El-Haliem AM, Hoogstrate SW, Schuurink RC 2018. A robust functional genomics approach to identify effector genes required for thrips (Frankliniella occidentalis) reproductive performance on tomato leaf discs. Front. Plant Sci. 9:1852
    [Google Scholar]
  2. 2. 
    Abe H, Shimoda T, Ohnishi J, Kugimiya S, Narusaka M et al. 2009. Jasmonate-dependent plant defense restricts thrips performance and preference. BMC Plant Biol 9:97
    [Google Scholar]
  3. 3. 
    Abe H, Tomitaka Y, Shimoda T, Seo S, Sakurai T et al. 2012. Antagonistic plant defense system regulated by phytohormones assists interactions among vector insect, thrips and a Tospovirus. Plant Cell Physiol 53:204–12
    [Google Scholar]
  4. 4. 
    Abudurexiti A, Adkins S, Alioto D, Alkhovsky SV, Avšič-Županc T et al. 2019. Taxonomy of the order Bunyavirales: update 2019. Arch. Virol. 164:1949–65
    [Google Scholar]
  5. 5. 
    Allen KC, Luttrell RG, Sappington TW, Hesler LS, Papiernik SK 2018. Frequency and abundance of selected early-season insect pests of cotton. J. Integr. Pest Manag. 9:20
    [Google Scholar]
  6. 6. 
    Badillo-Vargas IE, Rotenberg D, Schneweis BA, Whitfield AE 2015. RNA interference tools for the western flower thrips, Frankliniella occidentalis. J. Insect Physiol. 76:36–46
    [Google Scholar]
  7. 7. 
    Bailey SF. 1938. Thrips of economic importance in California Circ. 346, Agric. Exp. Stn., Coll. Agric., Univ. Calif. Berkeley:78 pp.
    [Google Scholar]
  8. 8. 
    Bielza P, Quinto V, Grávalos C, Abellán J, Fernández E 2008. Lack of fitness costs of insecticide resistance in the western flower thrips (Thysanoptera: Thripidae). J. Econ. Entomol. 101:499–503
    [Google Scholar]
  9. 9. 
    Brodbeck BV, Stavisky J, Funderburk JE, Andersen PC, Olson SM 2001. Flower nitrogen status and populations of Frankliniella occidentalis feeding on Lycopersicon esculentum. Entomol. Exp. Appl 99:165–72
    [Google Scholar]
  10. 10. 
    Brødsgaard HF. 1994. Effect of photoperiod on the bionomics of Frankliniella occidentalis (Pergande) (Thysanoptera, Thripidae). J. Appl. Entomol. 117:498–507
    [Google Scholar]
  11. 11. 
    Brødsgaard HF. 1994. Insecticide resistance in European and African strains of western flower thrips (Thysanoptera: Thripidae) tested in a new residue-on-glass test. J. Econ. Entomol. 87:1141–46
    [Google Scholar]
  12. 12. 
    Broughton S, Harrison J. 2012. Evaluation of monitoring methods for thrips and the effect of trap colour and semiochemicals on sticky trap capture of thrips (Thysanoptera) and beneficial insects (Syrphidae, Hemerobiidae) in deciduous fruit trees in Western Australia. Crop Prot. 42:156–63
    [Google Scholar]
  13. 13. 
    Brunner PC, Frey JE. 2010. Habitat-specific population structure in native western flower thrips Frankliniella occidentalis (Insecta, Thysanoptera). J. Evol. Biol. 23:797–804
    [Google Scholar]
  14. 14. 
    Bryan DE, Smith RF. 1965. The Frankliniella occidentalis (Pergande) Complex in California (Thysanoptera: Thripidae) Univ. Calif. Publ. Entomol 10 Berkeley, CA: Univ. Calif. Press
    [Google Scholar]
  15. 15. 
    Buitenhuis R, Shipp JL. 2008. Influence of plant species and plant growth stage on Frankliniella occidentalis pupation behaviour in greenhouse ornamentals. J. Appl. Entomol. 132:86–88
    [Google Scholar]
  16. 16. 
    CAB Int 2018. Frankliniella occidentalis (western flower thrips). Datasheet, Invasive Species Compend., CAB Int. Oxon, UK: https://www.cabi.org/isc/datasheet/24426
  17. 17. 
    Cao L-J, Wang Z-H, Gong Y-J, Zhu L, Hoffmann AA, Wei S-J 2017. Low genetic diversity but strong population structure reflects multiple introductions of western flower thrips (Thysanoptera: Thripidae) into China followed by human-mediated spread. Evol. Appl. 10:391–401
    [Google Scholar]
  18. 18. 
    Cao Y, Zhi J, Cong C, Margolies DC 2014. Olfactory cues used in host selection by Frankliniella occidentalis (Thysanoptera: Thripidae) in relation to host suitability. J. Insect Behav. 27:41–56
    [Google Scholar]
  19. 19. 
    Cao Y, Zhi J, Li C, Zhang R, Wang C et al. 2018. Behavioral responses of Frankliniella occidentalis to floral volatiles combined with different background visual cues. Arthropod Plant Interact 12:31–39
    [Google Scholar]
  20. 20. 
    Chen G, Escobar-Bravo R, Kim HK, Leiss KA, Klinkhamer PGL 2018. Induced resistance against western flower thrips by the Pseudomonas syringae-derived defense elicitors in tomato. Front. Plant Sci. 9:1417
    [Google Scholar]
  21. 21. 
    Childers CC. 1997. Feeding and oviposition injuries to plants. Thrips as Crop Pests T Lewis 505–37 New York: CAB Int.
    [Google Scholar]
  22. 22. 
    Cloyd RA, Raudenbush AL. 2014. Efficacy of binary pesticide mixtures against western flower thrips. HortTechnology 24:449–56
    [Google Scholar]
  23. 23. 
    Cook D, Herbert A, Akin DS, Reed J 2011. Biology, crop injury, and management of thrips (Thysanoptera: Thripidae) infesting cotton seedlings in the United States. J. Integr. Pest Manag. 2:B1–9
    [Google Scholar]
  24. 24. 
    Crawford DL. 1915. Potato curly leaf (caused by Euthrips occidentalis). Calif. State Comm. Hortic. Mon. Bull. 4:389–91
    [Google Scholar]
  25. 25. 
    Davidson MM, Butler RC, Teulon DAJ 2006. Starvation period and age affect the response of female Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) to odor and visual cues. J. Insect Physiol. 52:729–36
    [Google Scholar]
  26. 26. 
    Davidson MM, Nielsen MC, Butler RC, Castane C, Alomar O et al. 2015. Can semiochemicals attract both western flower thrips and their anthocorid predators?. Entomol. Exp. Appl. 155:54–63
    [Google Scholar]
  27. 27. 
    Davidson MM, Perry NB, Larsen L, Green VC, Butler RC, Teulon DAJ 2008. 4-Pyridyl carbonyl compounds as thrips lures: effectiveness for western flower thrips in Y-tube bioassays. J. Agr. Food Chem. 56:6554–61
    [Google Scholar]
  28. 28. 
    de Jager CM, Butot RPT, Klinkhamer PGL, De Jong TJ, Wolff K, Van Der Meijden E 1995. Genetic variation in chrysanthemum for resistance in Frankliniella occidentalis. Entomol. Exp. Appl 77:277–87
    [Google Scholar]
  29. 29. 
    Delphia CM, Mescher MC, De Moraes CM 2007. Induction of plant volatiles by herbivores with different feeding habits and the effects of induced defenses on host-plant selection by thrips. J. Chem. Ecol. 33:997–1012
    [Google Scholar]
  30. 30. 
    Demirozer O, Tyler-Julian K, Funderburk J, Leppla N, Reitz S 2012. Frankliniella occidentalis (Pergande) integrated pest management programs for fruiting vegetables in Florida. Pest Manag. Sci. 68:1537–45
    [Google Scholar]
  31. 31. 
    Duan H-S, Yu Y, Zhang A-S, Guo D, Tao Y-L, Chu D 2013. Sudden widespread distribution of Frankliniella occidentalis (Thysanoptera: Thripidae) in Shandong Province, China. Florida Entomol 96:933–40
    [Google Scholar]
  32. 32. 
    Escobar-Bravo R, Chen G, Kim HK, Grosser K, van Dam NM et al. 2019. Ultraviolet radiation exposure time and intensity modulate tomato resistance to herbivory through activation of jasmonic acid signaling. J. Exp. Bot. 70:315–27
    [Google Scholar]
  33. 33. 
    Escobar-Bravo R, Klinkhamer PGL, Leiss KA 2017. Induction of jasmonic acid-associated defenses by thrips alters host suitability for conspecifics and correlates with increased trichome densities in tomato. Plant Cell Physiol 58:622–34
    [Google Scholar]
  34. 34. 
    Escobar-Bravo R, Ruijgrok J, Kim HK, Grosser K, Van Dam NM et al. 2018. Light intensity-mediated induction of trichome-associated allelochemicals increases resistance against thrips in tomato. Plant Cell Physiol 59:2462–75
    [Google Scholar]
  35. 35. 
    Eur. Comm 2013. Commission Implementing Regulation (EU) No 485/2013 of 24 May 2013 amending Implementing Regulation (EU) No 540/2011, as regards the conditions of approval of the active substances clothianidin, thiamethoxam and imidacloprid, and prohibiting the use and sale of seeds treated with plant protection products containing those active substances. Off. J. Eur. Union 139:12–26
    [Google Scholar]
  36. 36. 
    Facey PD, Méric G, Hitchings MD, Pachebat JA, Hegarty MJ et al. 2015. Draft genomes, phylogenetic reconstruction, and comparative genomics of two novel cohabiting bacterial symbionts isolated from Frankliniella occidentalis. Genome Biol. Evol 7:2188–202
    [Google Scholar]
  37. 37. 
    Farrar JJ, Davis RM. 1991. Relationships among ear morphology, western flower thrips, and Fusarium ear rot of corn. Phytopathology 81:661–66
    [Google Scholar]
  38. 38. 
    Frantz G, Mellinger HC. 2009. Shifts in western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae), population abundance and crop damage. Florida Entomol 92:29–34
    [Google Scholar]
  39. 39. 
    Funderburk J. 2009. Management of the western flower thrips (Thysanoptera: Thripidae) in fruiting vegetables. Florida Entomol 92:1–6
    [Google Scholar]
  40. 40. 
    Funderburk J, Frantz G, Mellinger C, Tyler-Julian K, Srivastava M 2016. Biotic resistance limits the invasiveness of the western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae), in Florida. Insect Sci 23:175–82
    [Google Scholar]
  41. 41. 
    Funderburk JE, Latsha KS. 2005. The entomophilic Thripinema. Nematodes as Biological Control Agents P Grewal, R Ehlers, D Shapiro-Ilan 401–10 Wallingford, UK: CAB Int.
    [Google Scholar]
  42. 42. 
    Gao Y, Lei Z, Reitz SR 2012. Western flower thrips resistance to insecticides: detection, mechanisms and management strategies. Pest Manag. Sci. 68:1111–21
    [Google Scholar]
  43. 43. 
    Goldbach R, Peters D. 1994. Possible causes of the emergence of tospovirus diseases. Sem. Virol. 5:113–20
    [Google Scholar]
  44. 44. 
    Graham SH, Stewart SD. 2018. Field study investigating Cry51Aa2.834_16 in cotton for control of thrips (Thysanoptera: Thripidae) and tarnished plant bugs (Hemiptera: Miridae). J. Econ. Entomol. 111:2717–26
    [Google Scholar]
  45. 45. 
    Guerra-Sobrevilla L. 1989. Effectiveness of aldicarb in the control of the western flower thrips, Frankliniella occidentalis (Pergande), in table grapes in northwestern Mexico. Crop Prot. 8:277–79
    [Google Scholar]
  46. 46. 
    He S, Lin Y, Qian L, Li Z, Xi C et al. 2017. The influence of elevated CO2 concentration on the fitness traits of Frankliniella occidentalis and Frankliniella intonsa (Thysanoptera: Thripidae). Environ. Entomol. 46:722–28
    [Google Scholar]
  47. 47. 
    Hewitt LC, Shipp L, Buitenhuis R, Scott-Dupree C 2015. Seasonal climatic variations influence the efficacy of predatory mites used for control of western flower thrips in greenhouse ornamental crops. Exp. Appl. Acarol. 65:435–50
    [Google Scholar]
  48. 48. 
    Higgins CJ, Myer JH. 1992. Sex ratio patterns and population dynamics of western flower thrips (Thysanoptera: Thripidae). Environ. Entomol. 21:322–30
    [Google Scholar]
  49. 49. 
    Holmes ND, Bennison JA, Maulden KA, Kirk WDJ 2012. The pupation behaviour of the Western flower thrips, Frankliniella occidentalis (Pergande). Acta Phytopathol. Hung. 47:87–96
    [Google Scholar]
  50. 50. 
    Hondelmann P, Nyasani JO, Subramanian S, Meyhoefer R 2017. Genetic structure and diversity of western flower thrips, Frankliniella occidentalis in a French bean agroecosystem of Kenya. Int. J. Trop. Insect Sci. 37:71–78
    [Google Scholar]
  51. 51. 
    Houle JL, Kennedy GG. 2017. Tomato spotted wilt virus can infect resistant tomato when western flower thrips inoculate blossoms. Plant Dis. 101:1666–70
    [Google Scholar]
  52. 52. 
    Hunter WB, Ullman DE. 1992. Anatomy and ultrastructure of the piercing-sucking mouthparts and paraglossal sensilla of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Int. J. Insect Morphol. Embryol. 21:17–35
    [Google Scholar]
  53. 53. 
    Igarashi K, Nomura M, Narita S 2013. Application of a powdered artificial diet to promote the establishment of the predatory bug Geocoris varius (Hemiptera: Geocoridae) on strawberry plants. Appl. Entomol. Zool. 48:165–69
    [Google Scholar]
  54. 54. 
    Kathage J, Castañera P, Alonso-Prados JL, Gómez-Barbero M, Rodríguez-Cerezo E 2018. The impact of restrictions on neonicotinoid and fipronil insecticides on pest management in maize, oilseed rape and sunflower in eight European Union regions. Pest Manag. Sci. 74:88–99
    [Google Scholar]
  55. 55. 
    Kigathi R, Poehling HM. 2012. UV-absorbing films and nets affect the dispersal of western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae). J. Appl. Entomol. 136:761–71
    [Google Scholar]
  56. 56. 
    Kindt F, Joosten NN, Peters D, Tjallingii WF 2003. Characterisation of the feeding behaviour of western flower thrips in terms of electrical penetration graph (EPG) waveforms. J. Insect Physiol. 49:183–91
    [Google Scholar]
  57. 57. 
    Kirk WDJ. 2017. The aggregation pheromones of thrips (Thysanoptera) and their potential for pest management. Int. J. Trop. Insect Sci. 37:41–49
    [Google Scholar]
  58. 58. 
    Kirk WDJ, Hamilton JGC. 2004. Evidence for a male-produced sex pheromone in the western flower thrips Frankliniella occidentalis. J. Chem. Ecol 30:167–74
    [Google Scholar]
  59. 59. 
    Koschier EH. 2008. Essential oil compounds for thrips control—a review. Nat. Prod. Commun. 3:1171–82
    [Google Scholar]
  60. 60. 
    Krumov V, Karadjova O. 2012. Influence of climate change on the potential for establishment of Frankliniella occidentalis (Thysanoptera: Thripidae) in Bulgaria. Acta Phytopathol. Hung. 47:113–16
    [Google Scholar]
  61. 61. 
    Kumm S, Moritz G. 2010. Life-cycle variation, including female production by virgin females in Frankliniella occidentalis (Thysanoptera: Thripidae). J. Appl. Entomol. 134:491–97
    [Google Scholar]
  62. 62. 
    Leiss KA, Choi YH, Abdel-Farid IB, Verpoorte R, Klinkhamer PGL 2009. NMR metabolomics of thrips (Frankliniella occidentalis) resistance in Senecio hybrids. J. Chem. Ecol. 35:219–29
    [Google Scholar]
  63. 63. 
    Leiss KA, Cristofori G, van Steenis R, Verpoorte R, Klinkhamer PGL 2013. An eco-metabolomic study of host plant resistance to Western flower thrips in cultivated, biofortified and wild carrots. Phytochemistry 93:63–70
    [Google Scholar]
  64. 64. 
    Lewis T, ed. 1997. Thrips as Crop Pests New York: CAB Int740 pp.
    [Google Scholar]
  65. 65. 
    Macharia I, Backhouse D, Skilton R, Ateka E, Wu S-B et al. 2015. Diversity of thrips species and vectors of Tomato spotted wilt virus in tomato production systems in Kenya. J. Econ. Entomol. 108:20–28
    [Google Scholar]
  66. 66. 
    Macharia I, Backhouse D, Wu SB, Ateka EM 2016. Weed species in tomato production and their role as alternate hosts of Tomato spotted wilt virus and its vector Frankliniella occidentalis. Ann. Appl. Biol 169:224–35
    [Google Scholar]
  67. 67. 
    Maharijaya A, Vosman B, Verstappen F, Steenhuis-Broers G, Mumm R et al. 2012. Resistance factors in pepper inhibit larval development of thrips (Frankliniella occidentalis). Entomol. Exp. Appl. 145:62–71
    [Google Scholar]
  68. 68. 
    Mainali BP, Lim UT. 2011. Behavioral response of western flower thrips to visual and olfactory cues. J. Insect Behav. 24:436–46
    [Google Scholar]
  69. 69. 
    Maris PC, Joosten NN, Goldbach RW, Peters D 2004. Tomato spotted wilt virus infection improves host suitability for its vector Frankliniella occidentalis. Phytopathology 94:706–11
    [Google Scholar]
  70. 70. 
    Martin NA, Workman PJ. 1994. Confirmation of a pesticide-resistant strain of western flower thrips in New Zealand. Proceedings of the 47th New Zealand Plant Protection Conference, Waitangi, New Zealand, 1994144–48 Hastings, N. Z.: N. Z. Plant Prot. Soc.
    [Google Scholar]
  71. 71. 
    Martini X, Funderburk J, Ben-Yakir D 2019. Repellence of pests. Optical Manipulation of Pests and Beneficial Arthropods D Ben-Yakir. In press Boca Raton, FL: CRC
    [Google Scholar]
  72. 72. 
    Martini X, Guvvala H, Nansen C 2015. The search behavior of omnivorous thrips larvae is influenced by spider mite cues. J. Insect Behav. 28:593–603
    [Google Scholar]
  73. 73. 
    Mautino GC, Sacco D, Ciuffo M, Turina M, Tavella L 2012. Preliminary evidence of recovery from Tomato spotted wilt virus infection in Frankliniella occidentalis individuals. Ann. Appl. Biol. 161:266–76
    [Google Scholar]
  74. 74. 
    McDonald JR, Bale JS, Walters KFA 1997. Effects of sub-lethal cold stress on the western flower thrips, Frankliniella occidentalis. Ann. Appl. Biol. 131:189–95
    [Google Scholar]
  75. 75. 
    Mirnezhad M, Romero-Gonzalez RR, Leiss KA, Choi YH, Verpoorte R, Klinkhamer PGL 2010. Metabolomic analysis of host plant resistance to thrips in wild and cultivated tomatoes. Phytochem. Anal. 21:110–17
    [Google Scholar]
  76. 76. 
    Mirnezhad M, Schidlo N, Klinkhamer PGL, Leiss KA 2012. Variation in genetics and performance of Dutch western flower thrips populations. J. Econ. Entomol. 105:1816–24
    [Google Scholar]
  77. 77. 
    Mollema C, Cole RA. 1996. Low aromatic amino acid concentrations in leaf proteins determine resistance to Frankliniella occidentalis in four vegetable crops. Entomol. Exp. Appl. 78:325–33
    [Google Scholar]
  78. 78. 
    Momol MT, Olson SM, Funderburk JE, Stavisky J, Marois JJ 2004. Integrated management of tomato spotted wilt on field-grown tomatoes. Plant Dis 88:882–90
    [Google Scholar]
  79. 79. 
    Montero-Astua M, Ullman DE, Whitfield AE 2016. Salivary gland morphology, tissue tropism and the progression of tospovirus infection in Frankliniella occidentalis. Virology 493:39–51
    [Google Scholar]
  80. 80. 
    Moritz G, Kumm S, Mound L 2004. Tospovirus transmission depends on thrips ontogeny. Virus Res 100:143–49
    [Google Scholar]
  81. 81. 
    Morse JG, Hoddle MS. 2006. Invasion biology of thrips. Annu. Rev. Entomol. 51:67–89
    [Google Scholar]
  82. 82. 
    Mouden S, Sarmiento KF, Klinkhamer PGL, Leiss KA 2017. Integrated pest management in western flower thrips: past, present and future. Pest Manag. Sci. 73:813–22
    [Google Scholar]
  83. 83. 
    Mound LA. 1983. Natural and disrupted patterns of geographical distribution in Thysanoptera (Insecta). J. Biogeogr. 10:119–33
    [Google Scholar]
  84. 84. 
    Mound LA. 2013. Homologies and host-plant specificity: Recurrent problems in the study of thrips. Florida Entomol 96:318–23
    [Google Scholar]
  85. 85. 
    Mound LA, Walker AK. 1982. Terebrantia (Insecta: Thysanoptera). Fauna N. Z. 1:1–113
    [Google Scholar]
  86. 86. 
    Mujuka EA, Affognon H, Muriithi BW, Subramanian S, Irungu P, Mburu J 2017. Returns to research and outreach for integrated pest management of western flower thrips infesting French bean and tomato in Kenya. Int. J. Trop. Insect Sci. 37:114–24
    [Google Scholar]
  87. 87. 
    Nachappa P, Margolies DC, Nechols JR, Whitfield AE, Rotenberg D 2013. Tomato spotted wilt virus benefits a non-vector arthropod, Tetranychus urticae, by modulating different plant responses in tomato. PLOS ONE 8:e75909
    [Google Scholar]
  88. 88. 
    Nagata T, Inoue-Nagata AK, Van Lent J, Goldbach R, Peters D 2002. Factors determining vector competence and specificity for transmission of Tomato spotted wilt virus. J. Gen. Virol 83:663–71
    [Google Scholar]
  89. 89. 
    Nyasani JO, Meyhöfer R, Subramanian S, Poehling HM 2013. Feeding and oviposition preference of Frankliniella occidentalis for crops and weeds in Kenyan French bean fields. J. Appl. Entomol. 137:204–13
    [Google Scholar]
  90. 90. 
    Nyasani JO, Subramanian S, Orindi B, Poehling H-M, Meyhoefer R 2017. Short range dispersal of western flower thrips in field-grown French beans in Kenya. Int. J. Trop. Insect Sci. 37:79–88
    [Google Scholar]
  91. 91. 
    Ogada PA, Debener T, Poehling H-M 2016. Inheritance genetics of the trait vector competence in Frankliniella occidentalis (Western flower thrips) in the transmission of Tomato spotted wilt virus. Ecol. Evol 6:7911–20
    [Google Scholar]
  92. 92. 
    Ogada PA, Kiirika LM, Lorenz C, Senkler J, Braun H-P, Poehling H-M 2017. Differential proteomics analysis of Frankliniella occidentalis immune response after infection with Tomato spotted wilt virus (Tospovirus). Dev. Comp. Immunol. 67:1–7
    [Google Scholar]
  93. 93. 
    Ogada PA, Maiss E, Poehling HM 2013. Influence of Tomato spotted wilt virus on performance and behaviour of western flower thrips (Frankliniella occidentalis). J. Appl. Entomol. 137:488–98
    [Google Scholar]
  94. 94. 
    Ogada PA, Moualeu DP, Poehling H-M 2016. Predictive models for Tomato spotted wilt virus spread dynamics, considering Frankliniella occidentalis specific life processes as influenced by the virus. PLOS ONE 11:e0154533
    [Google Scholar]
  95. 95. 
    Ogada PA, Poehling H-M. 2015. Sex-specific influences of Frankliniella occidentalis (western flower thrips) in the transmission of Tomato spotted wilt virus (Tospovirus). J. Plant Dis. Protect. 122:264–74
    [Google Scholar]
  96. 96. 
    Olaniran OA, Sudhakar AVS, Drijfhout FP, Dublon IAN, Hall DR et al. 2013. A male-predominant cuticular hydrocarbon, 7-methyltricosane, is used as a contact pheromone in the western flower thrips Frankliniella occidentalis. J. Chem. Ecol 39:559–68
    [Google Scholar]
  97. 97. 
    Pappas ML, Tavlaki G, Triantafyllou A, Broufas G 2018. Omnivore-herbivore interactions: thrips and whiteflies compete via the shared host plant. Sci. Rep. 8:3996
    [Google Scholar]
  98. 98. 
    Pappu HR, Jones RAC, Jain RK 2009. Global status of tospovirus epidemics in diverse cropping systems: Successes achieved and challenges ahead. Virus Res 141:219–36
    [Google Scholar]
  99. 99. 
    Pearsall IA. 2002. Daily flight activity of the western flower thrips (Thysan., Thripidae) in nectarine orchards in British Columbia, Canada. J. Appl. Entomol. 126:293–302
    [Google Scholar]
  100. 100. 
    Rahman T, Broughton S, Spafford H 2011. Effect of spinosad and predatory mites on control of Frankliniella occidentalis in three strawberry cultivars. Entomol. Exp. Appl. 138:154–61
    [Google Scholar]
  101. 101. 
    Rahman T, Spafford H, Broughton S 2010. Variation in preference and performance of Frankliniella occidentalis (Thysanoptera: Thripidae) on three strawberry cultivars. J. Econ. Entomol. 103:1744–53
    [Google Scholar]
  102. 102. 
    Reitz SR. 2009. Biology and ecology of the western flower thrips (Thysanoptera: Thripidae): the making of a pest. Florida Entomol 92:7–13
    [Google Scholar]
  103. 103. 
    Reitz SR, Yearby EL, Funderburk JE, Stavisky J, Momol MT, Olson SM 2003. Integrated management tactics for Frankliniella thrips (Thysanoptera: Thripidae) in field-grown pepper. J. Econ. Entomol. 96:1201–14
    [Google Scholar]
  104. 104. 
    Rhainds M, Shipp L. 2004. Dispersal of adult western flower thrips (Thysanoptera: Thripidae) in greenhouse crops. Can. Entomol. 136:241–54
    [Google Scholar]
  105. 105. 
    Riley DG, Angelella GM, McPherson RM 2011. Pine pollen dehiscence relative to thrips population dynamics. Entomol. Exp. Appl. 138:223–33
    [Google Scholar]
  106. 106. 
    Ripa R, Funderburk J, Rodriguez F, Espinoza F, Mound L 2009. Population abundance of Frankliniella occidentalis (Thysanoptera: Thripidae) and natural enemies on plant hosts in central Chile. Environ. Entomol. 38:333–44
    [Google Scholar]
  107. 107. 
    Rotenberg D, Jacobson AL, Schneweis DJ, Whiffleld AE 2015. Thrips transmission of tospoviruses. Curr. Opin. Virol. 15:80–89
    [Google Scholar]
  108. 108. 
    Rotenberg D, Krishna Kumar NK, Ullman DE, Montero-Astua M, Willis DK et al. 2009. Variation in Tomato spotted wilt virus titer in Frankliniella occidentalis and its association with frequency of transmission. Phytopathology 99:404–10
    [Google Scholar]
  109. 109. 
    Rotenberg D, Whitfield AE. 2018. Molecular interactions between tospoviruses and thrips vectors. Curr. Opin. Virol. 33:191–97
    [Google Scholar]
  110. 110. 
    Roth F, Galli Z, Toth M, Fail J, Jenser G 2016. The hypothesized visual system of Thrips tabaci Lindeman and Frankliniella occidentalis (Pergande) based on different coloured traps’ catches. North-West. J. Zool. 12:40–49
    [Google Scholar]
  111. 111. 
    Rugman-Jones PF, Hoddle MS, Stouthamer R 2010. Nuclear-mitochondrial barcoding exposes the global pest western flower thrips (Thysanoptera: Thripidae) as two sympatric cryptic species in its native California. J. Econ. Entomol. 103:877–86
    [Google Scholar]
  112. 112. 
    Salvalaggio AE, Lopez Lambertini PM, Cendoya G, Huarte MA 2017. Temporal and spatial dynamics of Tomato spotted wilt virus and its vector in a potato crop in Argentina. Ann. Appl. Biol. 171:5–14
    [Google Scholar]
  113. 113. 
    Sampson C, Kirk WDJ. 2012. Flower stage and position affect population estimates of the western flower thrips, Frankliniella occidentalis (Pergande), in strawberry. Acta Phytopathol. Hung 47:133–39
    [Google Scholar]
  114. 114. 
    Sampson C, Kirk WDJ. 2013. Can mass trapping reduce thrips damage and is it economically viable? Management of the western flower thrips in strawberry. PLOS ONE 8:e80787
    [Google Scholar]
  115. 115. 
    Sampson C, Kirk WDJ. 2016. Predatory mites double the economic injury level of Frankliniella occidentalis in strawberry. Biocontrol 61:661–69
    [Google Scholar]
  116. 116. 
    Schneweis DJ, Whitfield AE, Rotenberg D 2017. Thrips developmental stage-specific transcriptome response to tomato spotted wilt virus during the virus infection cycle in Frankliniella occidentalis, the primary vector. Virology 500:226–37
    [Google Scholar]
  117. 117. 
    Scholthof K-BG, Adkins S, Czosnek H, Palukaitis P, Jacquot E et al. 2011. Top 10 plant viruses in molecular plant pathology. Mol. Plant Pathol. 12:938–54
    [Google Scholar]
  118. 118. 
    Schor N, Berman S, Dombrovsky A, Elad Y, Ignat T, Bechar A 2017. Development of a robotic detection system for greenhouse pepper plant diseases. Precision Agric 18:394–409
    [Google Scholar]
  119. 119. 
    Selman IW, Brierley MR, Pegg GF, Hill TA 1961. Changes in the free amino acids and amides in tomato plants inoculated with tomato spotted wilt virus. Ann. Appl. Biol. 49:601–15
    [Google Scholar]
  120. 120. 
    Shakya S, Coll M, Weintraub PG 2010. Incorporation of intraguild predation into a pest management decision-making tool: the case of thrips and two pollen-feeding predators in strawberry. J. Econ. Entomol. 103:1086–93
    [Google Scholar]
  121. 121. 
    Shalileh S, Ogada PA, Moualeu DP, Poehling H-M 2016. Manipulation of Frankliniella occidentalis (Thysanoptera: Thripidae) by Tomato spotted wilt virus (Tospovirus) via the host plant nutrients to enhance its transmission and spread. Environ. Entomol. 45:1235–42
    [Google Scholar]
  122. 122. 
    Shipp JL, Zariffa N. 1991. Spatial patterns and sampling methods for western flower thrips (Thysanoptera: Thripidae) on greenhouse sweet pepper. Can. Entomol. 123:989–1000
    [Google Scholar]
  123. 123. 
    Soria C, Mollema C. 1995. Life-history parameters of western flower thrips on susceptible and resistant cucumber genotypes. Entomol. Exp. Appl. 74:177–84
    [Google Scholar]
  124. 124. 
    Stafford CA, Walker GP, Ullman DE 2011. Infection with a plant virus modifies vector feeding behavior. PNAS 108:9350–55
    [Google Scholar]
  125. 125. 
    Stafford-Banks CA, Rotenberg D, Johnson BR, Whitfield AE, Ullman DE 2014. Analysis of the salivary gland transcriptome of Frankliniella occidentalis. PLOS ONE 9:e94447
    [Google Scholar]
  126. 126. 
    Stafford-Banks CA, Yang LH, McMunn MS, Ullman DE 2014. Virus infection alters the predatory behavior of an omnivorous vector. Oikos 123:1384–90
    [Google Scholar]
  127. 127. 
    Steenbergen M, Abd-el-Haliem A, Bleeker P, Dicke M, Escobar-Bravo R et al. 2018. Thrips advisor: exploiting thrips-induced defences to combat pests on crops. J. Exp. Bot. 69:1837–48
    [Google Scholar]
  128. 128. 
    Steiner MY, Spohr LJ, Goodwin S 2011. Relative humidity controls pupation success and dropping behaviour of western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Aust. J. Entomol. 50:179–86
    [Google Scholar]
  129. 129. 
    Sutherland AM, Parrella MP. 2011. Accuracy, precision, and economic efficiency for three methods of thrips (Thysanoptera: Thripidae) population density assessment. J. Econ. Entomol. 104:1323–28
    [Google Scholar]
  130. 130. 
    Teerling CR, Pierce HD, Borden JH, Gillespie DR 1993. Identification and bioactivity of alarm pheromone in the western flower thrips, Frankliniella occidentalis. J. Chem. Ecol. 19:681–97
    [Google Scholar]
  131. 131. 
    Tentchev D, Verdin E, Marchal C, Jacquet M, Aguilar JM, Moury B 2011. Evolution and structure of Tomato spotted wilt virus populations: evidence of extensive reassortment and insights into emergence processes. J. Gen. Virol. 92:961–73
    [Google Scholar]
  132. 132. 
    Terry LI. 1997. Host selection, communication and reproductive behavior. Thrips as Crop Pests T Lewis 65–118 New York: CAB Int.
    [Google Scholar]
  133. 133. 
    Terry LI, Dyreson E. 1996. Behavior of Frankliniella occidentalis (Thysanoptera: Thripidae) within aggregations, and morphometric correlates of fighting. Ann. Entomol. Soc. Am. 89:589–602
    [Google Scholar]
  134. 134. 
    Terry LI, Kelly CK. 1993. Patterns of change in secondary and tertiary sex ratios of the Terebrantian thrips, Frankliniella occidentalis. Entomol. Exp. Appl. 66:213–25
    [Google Scholar]
  135. 135. 
    Teulon DAJ, Davidson MM, Perry NB, Nielsen MC, Castane C et al. 2017. Methyl isonicotinate—a non-pheromone thrips semiochemical—and its potential for pest management. Int. J. Trop. Insect Sci. 37:50–56
    [Google Scholar]
  136. 136. 
    Teulon DAJ, Hollister B, Butler RC, Cameron EA 1999. Colour and odour responses of flying western flower thrips: Wind tunnel and greenhouse experiments. Entomol. Exp. Appl. 93:9–19
    [Google Scholar]
  137. 137. 
    Tomitaka Y, Abe H, Sakurai T, Tsuda S 2015. Preference of the vector thrips Frankliniella occidentalis for plants infected with thrips-non-transmissible Tomato spotted wilt virus. J. Appl. Entomol 139:250–59
    [Google Scholar]
  138. 138. 
    Trichilo PJ, Leigh TF. 1986. Predation on spider mite eggs by the western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae), an opportunist in a cotton agroecosystem. Environ. Entomol. 15:821–25
    [Google Scholar]
  139. 139. 
    Tsumuki H, Ishida H, Yoshida H, Sonoda S, Izumi Y, Murai T 2007. Cold hardiness of adult western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Appl. Entomol. Zool. 42:223–29
    [Google Scholar]
  140. 140. 
    Tyler-Julian K, Funderburk J, Srivastava M, Olson S, Adkins S 2018. Evaluation of a push-pull system for the management of Frankliniella species (Thysanoptera: Thripidae) in tomato. Insects 9:187
    [Google Scholar]
  141. 141. 
    van Maanen R, Broufas G, Oveja MF, Sabelis MW, Janssen A 2012. Intraguild predation among plant pests: western flower thrips larvae feed on whitefly crawlers. Biocontrol 57:533–39
    [Google Scholar]
  142. 142. 
    Vangansbeke D, Duc Tung N, Audenaert J, Verhoeven R, Gobin B et al. 2016. Supplemental food for Amblyseius swirskii in the control of thrips: feeding friend or foe?. Pest Manag. Sci. 72:466–73
    [Google Scholar]
  143. 143. 
    Wang JC, Zhang B, Li HG, Wang JP, Zheng CY 2014. Effects of exposure to high temperature on Frankliniella occidentalis (Thysanoptera: Thripidae), under arrhenotoky and sexual reproduction conditions. Florida Entomol 97:504–10
    [Google Scholar]
  144. 144. 
    Welter SC, Rosenheim JA, Johnson MW, Mau RFL, Gusukuma-Minuto LR 1990. Effects of Thrips palmi and western flower thrips (Thysanoptera: Thripidae) on the yield, growth, and carbon allocation pattern in cucumbers. J. Econ. Entomol. 83:2092–101
    [Google Scholar]
  145. 145. 
    Whitfield AE, Kumar NKK, Rotenberg D, Ullman DE, Wyman EA et al. 2008. A soluble form of the Tomato spotted wilt virus (TSWV) glycoprotein GN (GN-S) inhibits transmission of TSWV by Frankliniella occidentalis. Phytopathology 98:45–50
    [Google Scholar]
  146. 146. 
    Whitten MMA, Facey PD, Del Sol R, Fernandez-Martinez LT, Evans MC et al. 2016. Symbiont-mediated RNA interference in insects. Proc. R. Soc. Lond. B 283:20160042
    [Google Scholar]
  147. 147. 
    Wijkamp I, Goldbach R, Peters D 1996. Propagation of tomato spotted wilt virus in Frankliniella occidentalis does neither result in pathological effects nor in transovarial passage of the virus. Entomol. Exp. Appl. 81:285–92
    [Google Scholar]
  148. 148. 
    Wu S, Tang L, Zhang X, Xing Z, Lei Z, Gao Y 2018. A decade of a thrips invasion in China: lessons learned. Ecotoxicology 27:1032–38
    [Google Scholar]
  149. 149. 
    Xia C, Chon T-S, Ren Z, Lee J-M 2015. Automatic identification and counting of small size pests in greenhouse conditions with low computational cost. Ecol. Inform. 29:139–46
    [Google Scholar]
  150. 150. 
    Yan D-K, Hu M, Tang Y-X, Fan J-Q 2015. Proteomic analysis reveals resistance mechanism against chlorpyrifos in Frankliniella occidentalis (Thysanoptera: Thripidae). J. Econ. Entomol. 108:2000–8
    [Google Scholar]
  151. 151. 
    Zhang Z-K, Lei Z-R. 2015. Identification, expression profiling and fluorescence-based binding assays of a chemosensory protein gene from the western flower thrips, Frankliniella occidentalis. PLOS ONE 10:e0117726
    [Google Scholar]
  152. 152. 
    Zhao X, Reitz SR, Yuan H, Lei Z, Paini DR, Gao Y 2017. Pesticide-mediated interspecific competition between local and invasive thrips pests. Sci. Rep. 7:40512
    [Google Scholar]
  153. 153. 
    Zheng X, Zhang J, Chen Y, Dong J, Zhang Z 2014. Effects of Tomato zonate spot virus infection on the development and reproduction of its vector Frankliniella occidentalis (Thysanoptera: Thripidae). Florida Entomol 97:549–54
    [Google Scholar]
/content/journals/10.1146/annurev-ento-011019-024947
Loading
/content/journals/10.1146/annurev-ento-011019-024947
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error