Development of Integrated Pest Management (IPM) Strategies for Whitefly (Bemisia tabaci)-Transmissible Geminiviruses

Chapter

Abstract

Worldwide outbreaks of Bemisia tabaci whiteflies, especially biotype B, have facilitated the emergence of whitefly-transmitted geminiviruses (WTG). These viruses cause economically important diseases of vegetable and fiber crops, especially in tropical and subtropical regions of the world. Because small populations of whiteflies can efficiently spread WTGs, management of these diseases is more challenging than for whiteflies alone. In this chapter, we discuss (1) why WTGs have emerged worldwide, (2) key aspects of the biology of WTGs and B. tabaci, and (3) how these aspects shape the development of an integrated pest management (IPM) approach for these diseases. The generalized IPM package involves strategies for (1) before the growing season, such as the use of virus- and whitefly-free transplants and propagative stock, and resistant varieties; (2) during the growing season, such as whitefly population suppression, roguing virus-infected plants, floating row covers and reflective mulches; and (3) after the growing season, such as region-wide sanitation, weed management and implementation of a host-free period. Different combinations of strategies will be used depending on the crop, cropping system, and properties of the virus and the whitefly vector. This is illustrated with two case ­studies: IPM for WTGs in an annual (tomato) and a perennial (cassava) crop.

References

  1. Ahmed NE, Kanan HO, Sugimoto Y, Ma YQ, Inanago S (2001) Effect of imidacloprid on incidence of Tomato yellow leaf curl virus. Plant Dis 85:84–87CrossRefGoogle Scholar
  2. Akad F, Webb S, Nyoike TW, Liburd OE, Turechek W, Adkins S, Polston JE (2008) Detection of Cucurbit leaf crumple virus in Florida. Plant Dis 92:648CrossRefGoogle Scholar
  3. Antignus Y (2000) Manipulation of wavelength dependent behavior of insects:an IPM tool to impede epidemics and restrict spread of insect-borne viruses. Virus Res 71:213–220PubMedCrossRefGoogle Scholar
  4. Antignus Y, Lachman O, Pearlsman M, Omer S, Unis H, Messila Y, Ucko O, Koren A (2003) Squash leaf curl geminivirus a new illegal immigrant from the Western Hemisphere, a threat to cucurbit crops in Israel. Phytoparasitica 31:415Google Scholar
  5. Ausher R (1997) Implementation of integrated pest management in Israel. Phytoparasitica 25:119–141CrossRefGoogle Scholar
  6. Berlinger MJ, Dahan R, Mordechi S (1986) The prevention of Tomato yellow leaf curl virus by controlling its vector, Bemisia tabaci. Hassadeh 66:686–689Google Scholar
  7. Berlinger MJ, Taylor RAJ, Lebiush-Mordechi J, Shalhevet S, Spharim I (2002) Efficiency of insect exclusion screens for preventing whitefly transmission of tomato yellow leaf curl virus of tomatoes in Israel. Bull Entomol Res 92:367–373PubMedCrossRefGoogle Scholar
  8. Briddon RW (2003) Cotton leaf curl disease, a multicomponent begomovirus complex. Mol Plant Pathol 4:427–434PubMedCrossRefGoogle Scholar
  9. Brown JK, Frohlich DR, Rosell RC (1995) The sweetpotato or silverleaf whiteflies: biotypes of Bemisia tabaci or a species complex? Annu Rev Entomol 40:511–534CrossRefGoogle Scholar
  10. Byrne DN, Bellows TS Jr, Parrella MP (1990) Whiteflies in agricultural systems. In: Gerling D (ed.) Whiteflies: their bionomics, pest status and management. Intercept, Great BritainGoogle Scholar
  11. Castle S, Palumbo J, Prabhaker N (2009) Newer insecticides for plant virus disease management. Virus Res 141:131–139PubMedCrossRefGoogle Scholar
  12. Chen LF, Gilbertson RL (2009) Curtovirus-cucurbit interaction: acquisition host plays a role in leafhopper transmission in a host-dependent manner. Phytopathology 99:101–108PubMedCrossRefGoogle Scholar
  13. Chowda Reddy RV, Colvin J, Muniyappa V, Seal S (2005) Diversity and distribution of ­begomoviruses infecting tomato in India. Arch Virol 150:845–867CrossRefGoogle Scholar
  14. Chu CC, Natwick ET, Perkins HH, Brushwood DE, Henneberry TJ, Castle SJ, Cohen AA, Boykin MA (1998) Upland cotton susceptibility to Bemisia argentifolii (Homoptera: Aleyrodidae) infestations. J Cotton Sci 2:1–9Google Scholar
  15. Chu CC, Barnes E, Natwick ET, Chen TY, Ritter D, Henneberry TJ (2007) Trap catches of ­sweetpotato whitefly (Homoptera: Aleyrodidae) in the Imperial Valley, California, from 1996 to 2002. Insect Sci 14:165–170CrossRefGoogle Scholar
  16. Cohen S, Berlinger M (1986) Transmission and cultural control of whitefly-borne viruses. Agric Ecosyst Environ 17:89–97CrossRefGoogle Scholar
  17. Cohen S, Kern J, Harpaz I, Ben-Joseph R (1988) Epidemiological studies of the tomato yellow leaf curl virus (TYLCV) in the Jordan Valley, Israel. Phytoparasitica 16:259–270CrossRefGoogle Scholar
  18. Colvin J, Omongo C, Maruthi M, Otim-Nape G, Thresh J (2004) Dual begomovirus infections and high Bemisia tabaci populations: two factors driving the spread of a cassava mosaic disease pandemic. Plant Pathol 53:577–584CrossRefGoogle Scholar
  19. Csizinszky AA, Schuster DJ, Kring JB (1995) Color mulches influence yield and insect pest ­populations in tomatoes. J Am Soc Hortic Sci 120:778–784Google Scholar
  20. Czosnek H, Laterrot H (1997) A worldwide survey of tomato yellow leaf curl viruses. Arch Virol 142:1391–1406PubMedCrossRefGoogle Scholar
  21. Czosnek H, Ghanim M, Morin S, Rubenstein G, Fridman V, Zeidan M (2001) Whiteflies: vectors and victims (?) of geminiviruses. Adv Virus Res 57:291–322PubMedCrossRefGoogle Scholar
  22. De Barro PJ (1995) Bemisia tabaci biotype B: a review of its biology density and control. CSIOR Division of Entomology, Technical paper no. 33, 59 ppGoogle Scholar
  23. Dik AJ, Albajes R (1999) Principles of epidemiology, population biology, damage relationships, and integrated control of diseases and pests. In: Albajes R, Lodovica-Gullino M, van Lenteren JC, Elad Y (eds.) Integrated pest and disease management in greenhouse crops. Springer, HeidelbergGoogle Scholar
  24. Dixon AGO, Ogbe FO, Okechukwu RU (2010) Cassava mosaic disease in Sub-Saharan Africa: a feasible solution for an unsolved problem. Outlook Agric 39:89–94CrossRefGoogle Scholar
  25. Ellsworth PC, Martinez-Carrillo JL (2001) IPM for Bemisia tabaci: a case study from North America. Crop Prot 20:853–869CrossRefGoogle Scholar
  26. Ellsworth PC, Diehl JW, Dennehy TJ, Naranjo SE (1994) Sampling sweet potato whiteflies in ­cotton. University of Arizona, IPM Series No. 2Google Scholar
  27. Fargette D, Colon LT, Bouveau R, Fauquet C (1996) Components of resistance of cassava to African cassava mosaic virus. Eur J Plant Pathol 102:645–654CrossRefGoogle Scholar
  28. Fargette D, Konate G, Fauquet C, Muller E, Peterschmitt M, Thresh JM (2006) Molecular ecology and emergence of tropical plant viruses. Ann Rev Phytopathol 44:235–260CrossRefGoogle Scholar
  29. Fauquet CM, Briddon RW, Brown JK, Moriones E, Stanley J, Zerbini M, Zhou X (2008) Geminivirus strain demarcation and nomenclature. Arch Virol 153:783–821PubMedCrossRefGoogle Scholar
  30. Froissart R, Doumayrou J, Vuillaume F, Alizon S, Michalakis Y (2010) The virulence-­transmission trade-off in vector-borne plant viruses: a review of (non-) existing studies. Philos Trans R Soc B 365:1907–1918CrossRefGoogle Scholar
  31. Ghanim M, Morin S, Czosnek H (2001) Rate of Tomato yellow leaf curl virus translocation in the circulative transmission pathway of its vector, the whitefly Bemisia tabaci. Phytopathology 91:188–196PubMedCrossRefGoogle Scholar
  32. Gilbertson RL, Rojas MR, Kon T, Jaquez J (2007) Introduction of Tomato yellow leaf curl virus into the Dominican Republic: the development of a successful integrated pest management strategy. In: Czosnek H (ed.) Tomato yellow leaf curl virus disease. Springer, Heidelberg, pp 279–303CrossRefGoogle Scholar
  33. Gillespe DR, Quiring D (1987) Yellow sticky traps for detecting and monitoring greenhouse whitefly (Homoptera: Aleyrodidae) adults on greenhouse tomato crops. J Econ Entomol 80:675–679Google Scholar
  34. Gould JR, Naranjo SE (1999) Distribution and sampling of Bemisia argentifolii (Homoptera: Aleyrodidae) and Eretmocerus eremicus (Hymenoptera: Aphelinidae) on cantaloupe vines. J Econ Entomol 92:402–408Google Scholar
  35. Gusmao MR, Picanco MC, Guedes RNC, Galvan TL, Pereira EJG (2006) Economic injury level and sequential sampling plan for Bemisia tabaci in outdoor tomato. J Appl Entomol 130:160–166CrossRefGoogle Scholar
  36. Guthrie J (1990) Controlling African cassava mosaic disease. CTA, WageningenGoogle Scholar
  37. Hanson P, Green SK, Kuo G (2006) Ty-2, a gene on chromosome 11 conditioning geminivirus resistance in tomato. Rep Tomato Genet Co-op 56:17–18Google Scholar
  38. Hilje L, Stansly PA (2008) Living mulch ground covers for management of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) and Tomato yellow mottle virus (ToYMoV) in Costa Rica. Crop Prot 27:10–16CrossRefGoogle Scholar
  39. Hilje L, Costa HC, Stansly PA (2001) Cultural practices for managing Bemisia tabaci and associated viral diseases. Crop Prot 20:801–812CrossRefGoogle Scholar
  40. Holt J, Colvin J, Muniyappa V (1999) Identifying control strategies for tomato leaf curl virus ­disease using an epidemiological model. J Appl Ecol 36:625–633CrossRefGoogle Scholar
  41. Ishaaya I, Mendelson Z, Melamed-Madjar V (1988) Effect of buprofezin on embryo genesis and progeny formation of sweet potato whitefly (Homoptera: Aleyrodidae). J Econ Entomol 81:781–784Google Scholar
  42. Ji Y, Scott JW (2005) Identification of RAPD markers linked to Lycopersicon chilense derived resistance genes on chromosome 6 of tomato. Acta Hortic 695:407–411Google Scholar
  43. Ji Y, Schuster DJ, Scott DJ (2007) Ty-3, a begomovirus resistance locus near the tomato yellow leaf curl virus resistance locus Ty-1 on chromosome 6 of tomato. Mol Breed 20:271–284CrossRefGoogle Scholar
  44. Jiu M, Zhou X-P, Tong L, Xu J, Yang X et al (2007) Vector-virus mutualism accelerates population increase of an invasive whitefly. PLoS ONE 2(1):e182. doi:10.1371/journal.pone.0000182PubMedCrossRefGoogle Scholar
  45. Jones DR (2003) Plant viruses transmitted by whiteflies. Eur J Plant Pathol 109:195–219CrossRefGoogle Scholar
  46. Jones RAC (2004) Using epidemiological information to develop effective integrated virus disease management strategies. Virus Res 100:5–30PubMedCrossRefGoogle Scholar
  47. Kerns DL, Palumbo JC (1995) Using admire on desert vegetable crops. Univ Arizona Coop Ext Pub. #195017Google Scholar
  48. Lapidot M, Friedmann M (2002) Breeding for resistance to whitefly-transmittted geminiviruses. Ann Appl Biol 140:109–127CrossRefGoogle Scholar
  49. Legg JP, Fauquet CM (2004) Cassava mosaic geminiviruses in Africa. Plant Mol Biol 56:585–599PubMedCrossRefGoogle Scholar
  50. Mason G, Rancati M, Bosco D (2000) The effect of thiamethoxam, a second generation neonicotinoid insecticide, in preventing transmission of tomato yellow leaf curl geminivirus (TYLCV) by the whitefly Bemisia tabaci (Gennadius). Crop Prot 19:473–479CrossRefGoogle Scholar
  51. Mejia L, Teni RE, Vidavski F, Czosnek H, Lapidot M, Nakhla MK, Maxwell DP (2005) Evaluation of tomato germplasm and selection of breeding lines for resistance to begomoviruses in Guatemala. Acta Hortic 695:251–255Google Scholar
  52. Morales FJ (2001) Conventional breeding for resistance to Bemisia tabaci-transmitted geminiviruses. Crop Prot 20:825–834CrossRefGoogle Scholar
  53. Naranjo SE, Flint HM (1995) Spatial distribution of adult Bemisia tabaci (Homoptera: Aleyrodidae) in cotton, and development and validation of fixed-precision sampling plans for estimating population density. Environ Entomol 24:261–270Google Scholar
  54. Naranjo SE, Ellsworth PC, Chu CC, Henneberry TJ, Riley DG, Watson TF, Nichols RL (1998) Action thresholds for the management of Bemisia tabaci (Homoptera: Aleyrodidae) in cotton. J Econ Entomol 91:1415–1426Google Scholar
  55. Natwick ET, Durazo A III (1985) Polyester covers protect vegetables from whiteflies and virus disease. Calif Agric 39:21–22Google Scholar
  56. Natwick ET, Laemmlen FF (1993) Protection from phytophagous insects and virus vectors in honeydew melons using rowcovers. Fla Entomol 76:120–126CrossRefGoogle Scholar
  57. Nauen R, Bretschneider T, Elbert A, Fisher R, Tiemann R (2003) Spirodiclofen and spiromesifen. Pestic Outlook 14:243–245CrossRefGoogle Scholar
  58. Nichols RL, Chu CC, Ellsworth PC, Henneberry TJ, Naranjo SJ, Riley DG, Toscano NC, Watson TF (1994) Determining an action threshold to prevent whitefly outbreaks. Phytoparasitica 22:349Google Scholar
  59. Nyoike TW, Liburd OE, Webb SE (2008) Suppression of whiteflies, Bemisia tabaci (Hemiptera: Aleyrodidae) and incidence of Cucurbit leaf crumple virus, a whitefly-transmitted virus of ­zucchini squash new to Florida, with mulches and imidacloprid. Fla Entomol 91:460–465CrossRefGoogle Scholar
  60. Oliveira MRV, Henneberry TJ, Anderson P (2001) History, current status, and collaborative research projects for Bemisia tabaci. Crop Prot 20:709–723CrossRefGoogle Scholar
  61. Orozco-Santos M, Perez-Zamora O, Lopez-Arriaga M (1995) Floating row cover and transparent mulch to reduce insect population, virus diseases and increase yield in cantaloupe. Fla Entomol 78:493–501CrossRefGoogle Scholar
  62. Palumbo JC, Tonhasca Jr A, Byrne DN (1994) Sampling plans and action thresholds for whiteflies on spring melons. University of Arizona IPM Series Number 1Google Scholar
  63. Perring TM (2001) The Bemisia tabaci species complex. Crop Prot 20:725–737CrossRefGoogle Scholar
  64. Polston JE, Anderson PK (1997) The emergence of whitefly-transmitted geminiviruses in tomato in the Western Hemisphere. Plant Dis 81:1358–1369CrossRefGoogle Scholar
  65. Polston JE, Sherwood T (2003) Pymetrozine interferes with transmission of Tomato yellow leaf curl virus by the whitefly Bemisia tabaci. Phytoparasitica 31:490–498CrossRefGoogle Scholar
  66. Ribeiro SG, Ambrozevicius AC, Avilla AC, Bezerra IC, Calegario RF, Fernandes JJ, Lima MF, de Mello RN, Rocha RF, Zerbini FM (2003) Distribution and genetic diversity of tomato-infecting begomoviruses in Brazil. Arch Virol 148:281–295PubMedCrossRefGoogle Scholar
  67. Rojas MR, Gilbertson RL, Russell DR, Maxwell DP (1993) Use of degenerate primers in the polymerase chain reaction to detect whitefly-transmitted geminiviruses. Plant Dis 77:340–347CrossRefGoogle Scholar
  68. Rojas MR, Hagen C, Lucas WJ, Gilbertson RL (2005) Exploiting chinks in the plant’s armor: evolution and emergence of geminiviruses. Ann Rev Phytopathol 43:361–394CrossRefGoogle Scholar
  69. Rojas MR, Kon T, Natwick ET, Polston JE, Akad F, Gilbertson RL (2007) First report of Tomato yellow leaf curl virus associated with tomato yellow leaf curl disease in California. Plant Dis 91:1056CrossRefGoogle Scholar
  70. Rosell RC, Torres-Jerez I, Brown JK (1999) Tracing the geminivirus-whitefly transmission pathway by polymerase chain reaction in whitefly extracts, saliva, hemolymph, and honeydew. Phytopathology 89:239–246PubMedCrossRefGoogle Scholar
  71. Rubenstein G, Morin S, Czosnek H (1999) Transmission of Tomato yellow leaf curl geminivirus to imidacloprid treated tomato plants by the whitefly Bemisia tabaci (Homoptera: Aleyrodidae). J Econ Entomol 92:658–662Google Scholar
  72. Salati R, Nahkla MK, Rojas MR, Guzman P, Jaquez J, Maxwell DP, Gilbertson RL (2002) Tomato yellow leaf curl virus in the Dominican Republic: characterization of an infectious clone, virus monitoring in whiteflies, and identification of reservoir hosts. Phytopathology 92:487–496PubMedCrossRefGoogle Scholar
  73. Schuster DJ, Stansly PA, Polston JE, Gilreath PR, McAvoy E (2007) Management of whiteflies, whitefly-vectored plant virus, and insecticide resistance for vegetable production in Southern Florida. ENY-735 (IN695), IFAS Extension, University of Florida, GainesvilleGoogle Scholar
  74. Seal SE, van den Bosch F, Jeger MJ (2006) Factors influencing begomovirus evolution and their increasing global significance: implications for sustainable control. Crit Rev Plant Sci 25:23–46CrossRefGoogle Scholar
  75. Seo JS, Gepts P, Gilbertson RL (2004) Genetics of resistance to the geminivirus, Bean dwarf mosaic virus, and the role of the hypersensistive response. Theor Appl Genet 108:786–793PubMedCrossRefGoogle Scholar
  76. Stansly PA, Natwick ET (2010) Integrated systems for managing Bemisia tabaci in protected and open field agriculture. In: Stansly PA, Naranjo SE (eds.) Bemisia: bionomics and management of a global pest. Springer, HeidelbergCrossRefGoogle Scholar
  77. Stern VM, Smith RF, van den Bosch R, Hagen KS (1959) The integrated control concept. Hilgardia 29:81–101Google Scholar
  78. Suwwan MA, Akkawi M, Al-Musa AM, Mansour A (1988) Tomato performance and incidence of tomato yellow leaf curl (TYLC) virus as affected by type of mulch. Sci Hortic 37:39–45CrossRefGoogle Scholar
  79. Tarr SAJ (1951) Leaf curl disease of cotton. The Commonwealth Mycological Institute, KewGoogle Scholar
  80. Thresh JM, Cooter RJ (2005) Strategies for controlling cassava mosaic virus disease in Africa. Plant Pathol 54:587–614CrossRefGoogle Scholar
  81. Ucko OS, Cohen S, Ben-Joseph R (1998) Prevention of virus epidemics by a crop-free period in the Arava region of Israel. Phytoparasitica 26:313–321CrossRefGoogle Scholar
  82. Varma A, Malathi VG (2003) Emerging geminivirus problem: a serious threat to crop production. Ann Appl Biol 142:145–162CrossRefGoogle Scholar
  83. Webb SE, Linda SB (1992) Evaluation of spun-bounded polyethylene row covers as a method of excluding insects and viruses affecting fall-grown squash in Florida. J Econ Entomol 85:2344–2352Google Scholar
  84. Wyatt SD, Brown JK (1996) Detection of subgroup III geminivirus isolates in leaf extracts by degenerate primers and polymerase chain reaction. Phytopathology 86:1288–1293CrossRefGoogle Scholar
  85. Zhou Y-C, Noussourou M, Kon T, Rojas MR, Jiang H, Chen L-F, Gamby K, Foster R, Gilbertson RL (2008) Evidence for local evolution of tomato-infecting begomovirus species in West Africa: characterization of tomato leaf curl Mali virus and tomato yellow leaf crumple virus from Mali. Arch Virol 153:693–706PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Robert L. Gilbertson
    • 1
  • Maria Rojas
    • 1
  • Eric Natwick
    • 2
  1. 1.Department of Plant PathologyUniversity of California-DavisDavisUSA
  2. 2.UC Desert Research and Extension CenterUniversity of California Cooperative ExtensionHoltvilleUSA

Personalised recommendations