Biology and management of Bemisia whitefly vectors of cassava virus pandemics in Africa

Pest Management Science

Volumn 70, Issue 10, 2014, Pages 1446-1453

  Legg, James P ^a   Shirima, Rudolph ^a   Tajebe, Lensa S ^b   Guastella, Devid ^b   Boniface, Simon ^a   Jeremiah, Simon ^c   Nsami, Elibariki ^d   Chikoti, Patrick ^e   Rapisarda, Carmelo ^b  

^a Regional Hub for Eastern Africa   (Tanzania)

^b UNIVERSITY OF CATANIA   (Italy)

^c Ukiriguru Agricultural Research Institute   (Tanzania)

^d National Biological Control Programme SRI Kibaha   (Tanzania)

^e Mt Makulu Research Station   (Zambia)

Author keywords

Cassava; CBSD; CMD; Control; Superabundant

Indexed keywords

BIOLOGICAL CONTROL; DICOTYLEDON; DISEASE TRANSMISSION; DISEASE VECTOR; HOST PLANT; INSECTICIDE; INTEGRATED PEST MANAGEMENT; NATURAL ENEMY; VIRAL DISEASE; WHITEFLY;

AFRICA; UNITED STATES;

ALEYRODIDAE; BEMISIA; BEMISIA TABACI; MANIHOT ESCULENTA;

INSECTICIDE;

AFRICA; ANIMAL; BEGOMOVIRUS; DISEASE CARRIER; GENETICS; HEMIPTERA; MANIHOT; PARASITOLOGY; PEST CONTROL; PHYSIOLOGY; PLANT DISEASE; POTYVIRIDAE; PROCEDURES; VIROLOGY;

AFRICA; ANIMALS; BEGOMOVIRUS; HEMIPTERA; INSECT VECTORS; INSECTICIDES; MANIHOT; PEST CONTROL; PLANT DISEASES; POTYVIRIDAE;

EID: 84925115558     PISSN: 1526498X     EISSN: 15264998     Source Type: Journal    
DOI: 10.1002/ps.3793     Document Type: Article

References (98)

1. Olson KM and Schaal BA, Evidence on the origin of cassava: phylogeography of Manihot esculenta. Proc Natl Acad Sci USA 96:5586-5591 (1999).
2. Jones WO, Manioc in Africa. Stanford University Press, Redwood City, CA, 315 pp. (1959).
3. FAOSTAT, FAO Database. [Online]. Food and Agriculture Organisation of the United Nations, Rome, Italy (2013). Available: http://faostat.fao.org/site/567/default.aspx [29 July 2013].
4. Jarvis A, Ramirez-Villegas J, Campo BVH and Navarro-Racines C, Is cassava the answer to African climate change adaptation? Trop Plant Biol 5(1):9-29 (2012).
5. Warburg O, Die Kulturpflanzen Usambaras. Mitt Deutsch Schutz 7:131 (1894).
6. Storey HH, Virus diseases of East African plants. VI-A progress report on studies of the disease of cassava. East Afr Agric J 2:34-39 (1936).
7. Bock KR and Woods RD, The etiology of African cassava mosaic disease. Plant Dis 67:994-995 (1983).
8. Fauquet CM and Stanley J, Geminivirus classification and nomenclature: progress and problems. Ann Appl Biol 142:165-189 (2003).
9. Hong YG, Robinson DJ and Harrison BD, Nucleotide sequence evidence for the occurrence of three distinct whitefly-transmitted geminiviruses in cassava. J Gen Virol 74:2437-2443 (1993).
10. Legg JP and Fauquet CM, Cassava viruses in Africa. Plant Mol Biol 56:585-599 (2004).
11. Patil BL and Fauquet CM, Cassava mosaic geminiviruses: actual knowledge and perspectives. Mol Plant Pathol 10:685-701 (2009).
12. Zhou X, Liu Y, Calvert L, Muñoz C, Otim-Nape GW, Robinson DJ. et al, Evidence that DNA-A of a geminivirus associated with severe cassava mosaic disease in Uganda has arisen by interspecific recombination. J Gen Virol 78:2101-2111 (1997).
13. Harrison BD, Zhou X, Otim-Nape GW, Liu Y and Robinson DJ, Role of a novel type of double infection in the geminivirus-induced epidemic of severe cassava mosaic in Uganda. Ann Appl Biol 131:37-448 (1997).
14. Gibson RW, Legg JP and Otim-Nape GW, Unusually severe symptoms are a characteristic of the current epidemic of mosaic virus disease of cassava in Uganda. Ann Appl Biol 128:479-490 (1996).
15. Legg JP, Emergence, spread and strategies for controlling the pandemic of cassava mosaic virus disease in east and central Africa. Crop Prot 18(10):627-637 (1999).
16. Legg JP, Epidemiology of a whitefly-transmitted cassava mosaic geminivirus pandemic in Africa, in Bemisia: Bionomics and Management of a Global Pest, ed. by Stansly PA and Naranjo SE. Springer, Dordrecht/Heidelberg/London/New York, pp. 233-257 (2010).
17. Legg JP, Owor B, Sseruwagi P and Ndunguru J, Cassava mosaic virus disease in East and Central Africa: epidemiology and management of a regional pandemic. Adv Virus Res 67:355-418 (2006).
18. Burundi: Famine Declared in Two Provinces. [Online]. Reuters (11 January 2005). Available: http://www.irinnews.org/report/52635/burundi-government-declares-famine-in-two-provinces [accessed 10 May 2014].
19. Thresh JM, Otim-Nape GW and Jennings DL, Exploiting resistance to African cassava mosaic virus. Asp Appl Biol 39:51-60 (1994).
20. Legg J, Whyte J, Kapinga R and Teri J, Special topics on pest and disease management: management of the cassava mosaic disease pandemic in East Africa, in Whiteflies and Whitefly-borne Viruses in the Tropics: Building a Knowledge Base for Global Action, ed. by Anderson P and Morales F. Centro Internacional de Agricultura Tropical, Cali, Colombia, pp. 332-338 (2005).
21. Otim-Nape GW, Bua A, Thresh JM, Baguma Y, Ogwal S, Ssemakula GN. et al, The Current Pandemic of Cassava Mosaic Virus Disease in East Africa and its Control. Natural Resources Institute, Chatham, UK (2000).
22. Alicai T, Omongo CA, Maruthi MN, Hillocks RJ, Baguma Y, Kawuki R. et al, Re-emergence of cassava brown streak disease in Uganda. Plant Dis 91:24-29 (2007).
23. Hillocks RJ and Jennings DL, Cassava brown streak disease: a review of present knowledge and research needs. Int J Pest Manag 49:225-234 (2003).
24. Legg JP and Raya M, Survey of cassava virus diseases in Tanzania. Int J Pest Manag 44:17-23 (1998).
25. Nichols RFJ, The brown streak disease of cassava: distribution, climatic effects and diagnostic symptoms. East Afr Agric J 15:154-160 (1950).
26. Jeremiah SC and Legg JP, Cassava Brown Streak Virus. [Online]. (2008). Available: http://www.youtube.com/watch?v=nCJdws9CnUw [accessed 10 May 2014].
27. Mbanzibwa DR, Tian YP, Tugume AK, Mukasa SB, Tairo F, Kyamanywa S. et al, Genetically distinct strains of cassava brown streak virus in the Lake Victoria basin and the Indian Ocean coastal area of East Africa. Arch Virol 154:353-359 (2009).
28. Winter S, Koerbler M, Stein B, Pietruszka A, Paape M and Butgereitt A, Analysis of cassava brown streak viruses reveals the presence of distinct virus species causing cassava brown streak disease in East Africa. J Gen Virol 91:1365-1372 (2010).
29. Legg JP, Jeremiah SC, Obiero HM, Maruthi MN, Ndyetabula I, Okao-Okuja G. et al, Comparing the regional epidemiology of the cassava mosaic and cassava brown streak pandemics in Africa. Virus Res 159:161-170 (2011).
30. Mbanzibwa DR, Tian YP, Tugume AK, Mukasa SB, Tairo F, Kyamanywa S. et al, Simultaneous virus-specific detection of the two cassava brown streak-associated viruses by RT-PCR reveals wide distribution in East Africa, mixed infections and infections in Manihot glaziovii. J Virol Meth 171:394-400 (2010).
31. Mbanzibwa DR, Tian YP, Tugume AK, Patil BL, Yadav JS, Bagewadi B. et al, Evolution of cassava brown streak disease-associated viruses. J Gen Virol 92:974-987 (2011).
32. Bigirimana S, Barumbanze P, Ndayihanzamaso P, Shirima R and Legg JP, First report of cassava brown streak disease and associated Ugandan cassava brown streak virus in Burundi. New Dis Rep 24:26 (2011).
33. Mulimbi W, Phemba X, Assumani B, Kasereka P, Muyisa S, Ugentho H. et al, First report of Ugandan cassava brown streak virus on cassava in Democratic Republic of Congo. New Dis Rep 26:11 (2012).
34. Kufferath H and Ghesquière J, La mosaïque du manioc. Compte Rendu Soc Biol 109:1146-1148 (1932).
35. Storey HH and Nichols RFW, Studies on the mosaic of cassava. Ann Appl Biol 25:790-806 (1938).
36. Dubern J, Transmission of African cassava mosaic geminivirus by the whitefly (Bemisia tabaci). Trop Sci 34:82-91 (1994).
37. Bock KR, Studies on cassava brown streak virus disease in Kenya. Trop Sci 34:134-145 (1994).
38. Maruthi MN, Hillocks RJ, Mtunda K, Raya MD, Muhanna M, Kiozia H. et al, Transmission of Cassava brown streak virus by Bemisia tabaci (Gennadius). J Phytopathol 153:307-312 (2005).
39. Mound LA and Halsey SH, Whitefly of the World. A Systematic Catalogue of the Aleyrodidae (Homoptera) with Host Plant and Natural Enemy Data. John Wiley & Sons, Chichester, UK (1978).
40. Mound LA, Host-correlated variation in Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae). Proc R Entomol Soc Lond 38:171-180 (1963).
41. Russel LM, Synonyms of Bemisia tabaci (Gennadius) (Homoptera, Aleyrodidae). Bull Brooklyn Entomol Soc 52:22-123 (1957).
42. Brown JK, Phylogenetic biology of the Bemisia tabaci sibling species group, in Bemisia: Bionomics and Management of a Global Pest, ed. by Stansly PA and Naranjo SE. Springer, Dordrecht/Heidelberg/London/New York, pp. 31-67 (2010).
43. Gill RJ and Brown JK, Systematics of Bemisia and Bemisia relatives: can molecular techniques solve the Bemisia tabaci complex conundrum - a taxonomist's viewpoint, in Bemisia: Bionomics and Management of a Global Pest, ed. by Stansly PA and Naranjo SE. Springer, Dordrecht/Heidelberg/London/New York, pp. 5-29 (2010).
44. Dinsdale A, Cook L, Riginos C, Buckley YM and De Barro P, Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase I to identify species level genetic boundaries. Ann Entomol Soc Am 103:196-208 (2010).
45. Boykin LM, Armstrong KF, Kubatko L and De Barro P, Species delimitation and global biosecurity. Evol Bioinform 8:1-37 (2012).
46. Tay WT, Evans GA, Boykin LM and De Barro PJ, Will the real Bemisia tabaci please stand up? PLoS ONE 7:e50550 (2012).
47. Boykin LM, Bemisia tabaci nomenclature: lessons learned. Pest Manag Sci DOI: 10.1002/ps.3709 (2014).
48. Campbell BC, Steffen-Campbell JD and Gill R, Origin and radiation of whiteflies: an initial molecular phylogenetic assessment, in Bemisia 1995: Taxonomy, Biology, Damage, Control and Management, ed. by Gerling D and Mayer RT. Intercept, Andover, UK, pp. 29-51 (1996).
49. Boykin LM, Shatters RG, Jr, Rosell RC, McKenzie CL, Bagnall RA, De Barro P. et al, Global relationships of Bemisia tabaci (Hemiptera: Aleyrodidae) revealed using Bayesian analysis of mitochondrial COI DNA sequences. Mol Phyl Evol 44:1306-1319 (2007).
50. De Barro PJ, The Bemisia species complex: questions to guide future research. J Integr Agric 11(2):187-196 (2012).
51. Abdullahi I, Winter S, Atiri GI and Thottappilly G, Molecular characterization of whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae), populations infesting cassava. Bull Entomol Res 93:97-106 (2003).
52. Berry SD, Fondong V, Rey C, Rogan D, Fauquet CM and Brown JK, Molecular evidence for five distinct Bemisia tabaci (Homoptera: Aleyrodidae) geographic haplotypes associated with cassava in sub-Saharan Africa. Ann Entomol Soc Am 97:852-859 (2004).
53. Esterhuizen LL, Mabasa KG, van Heerden SW, Czosnek H, Brown JK, van Heerden JH. et al, Genetic identification of members of the Bemisia tabaci cryptic species complex from South Africa reveals native and introduced haplotypes. J Appl Entomol 137:122-135 (2013).
54. Gnankiné O, Mouton L, Henri H, Terraz G, Houndété T, Martin T. et al, Distribution of Bemisia tabaci (Homoptera: Aleyrodidae) biotypes and their associated symbiotic bacteria on host plants in West Africa. Insect Conserv Divers 6:411-421 (2012).
55. Legg JP, French R, Rogan D, Okao-Okuja G and Brown JK, A distinct Bemisia tabaci (Gennadius) (Hemiptera: Sternorrhyncha: Aleyrodidae) genotype cluster is associated with the epidemic of severe cassava mosaic virus disease in Uganda. Mol Ecol 11:1219-1229 (2002).
56. Maruthi MN, Colvin C, Thwaites RM, Banks GK, Gibson G and Seal SE, Reproductive incompatibility and cytochrome oxidase I gene sequence variability amongst host-adapted and geographically separate Bemisia tabaci populations (Hemiptera: Aleyrodidae). Syst Entomol 29:560-568 (2004).
57. Burban C, Fishpool LDC, Fauquet C, Fargette D and Thouvenel J-C, Host-associated biotypes within West African populations of the whitefly Bemisia tabaci (Genn.) (Hom., Aleyrodidae). J Appl Entomol 113:416-423 (1992).
58. Legg JP, Host-associated strains within Ugandan populations of the whitefly Bemisia tabaci (Genn.) (Hom., Aleyro didae). J Appl Entomol 120:523-527 (1996).
59. Sseruwagi P, Maruthi MN, Colvin J, Rey MEC, Brown JK and Legg JP, Colonisation of non-cassava plant species by cassava whiteflies (Bemisia tabaci) (Gennadius) (Hemiptera: Aleyrodidae) in Uganda. Entomol Exp Applic 119:145-153 (2006).
60. Sseruwagi P, Legg JP, Maruthi MN, Colvin J, Rey MEC and Brown JK, Genetic diversity of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) populations and presence of the B biotype and a non-B biotype that can induce silverleaf symptoms in squash, in Uganda. Ann Appl Biol 147:253-265 (2005).
61. Legg JP and Ogwal S, Changes in the incidence of African cassava mosaic geminivirus and the abundance of its whitefly vector along south-north transects in Uganda. J Appl Entomol 122:69-178 (1998).
62. Otim-Nape GW, Thresh JM and Fargette D, Bemisia tabaci and cassava mosaic virus disease in Africa, in Bemisia 1995: Taxonomy, Biology, Damage, Control and Management, ed. by Gerling D and Meyer RT. Intercept, Andover, UK, pp. 319-350 (1996).
63. Colvin J, Omongo CA, Govindappa MR, Stevenson PC, Maruthi MN, Gibson G. et al, Host-plant viral infection effects on arthropod-vector population growth, development and behaviour: management and epidemiological implications. Adv Virus Res 67:419-452 (2006).
64. Omongo CA, Kawuki R, Bellotti AC, Alicai T, Baguma Y, Maruthi MN. et al, African cassava whitefly, Bemisia tabaci, resistance in African and South American cassava genotypes. J Integr Agric 11:327-336 (2012).
65. Legg JP, Sseruwagi P, Boniface S, Okao-Okuja G, Shirima R, Bigirimana S. et al, Spatio-temporal patterns of genetic change amongst populations of cassava Bemisia tabaci whiteflies driving virus pandemics in East and Central Africa. Virus Res DOI: 10.1016/j.virusres.2013.11.018 (2013).
66. Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE. et al, Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332(6026):254-256 (2011).
67. Gnankiné O, Mouton L, Henri H, Terraz G, Houndété T, Martin T. et al, Distribution of Bemisia tabaci (Homoptera: Aleyrodidae) biotypes and their associated symbiotic bacteria on host plants in West Africa. Insect Conserv Divers 6:411-421 (2012).
68. Dittrich V, Hassan SO and Ernst GH, Sudanese cotton and the whitefly: a case study of the emergence of a new primary pest. Crop Prot 4:161-176 (1985).
69. Legg JP, Gerling D and Neuenschwander PN, Biological control of whiteflies in sub-Saharan Africa, in Biological Control in IPM Systems in Africa, ed. by Neuenschwander P, Borgemeister C and Langewald J. CABI International, Wallingford, UK, pp. 87-100 (2003).
70. Golding FD, Cassava mosaic in southern Nigeria. Bull Dep Agric Niger 11:1-10 (1936).
71. Squire FA, Annual report of the Federal Department of Agricultural Research, Ibadan 1959-60. Government Printers, Lagos, Nigeria (1961).
72. Fishpool LDC and Burban C, Bemisia tabaci: the whitefly vector of African cassava mosaic geminivirus. Trop Sci 34:55-72 (1994).
73. Robertson IAD, Final report: Cassava/Whitefly Project - part of Crop Virology Project R3177 at the Kenya Agricultural Research Institute. Department for International Development, London, UK (1985).
74. Legg JP, The ecology of Bemisia tabaci (Gennadius) (Homoptera), vector of African cassava mosaic geminivirus in Uganda. Doctoral Thesis, University of Reading, Reading, UK, 183 pp. (1995).
75. Legg JP, Bemisia tabaci: the whitefly vector of cassava mosaic geminiviruses in Africa: an ecological perspective. Afr Crop Sci J 2:437-448 (1994).
76. Legg J and James B, Whiteflies as vectors of plant viruses in cassava and sweetpotato in Africa: conclusions and recommendations, in Whiteflies and Whitefly-borne Viruses in the Tropics: Building a Knowledge Base for Global Action, ed. by Anderson P and Morales F. Centro Internacional de Agricultura Tropical, Cali, Colombia, pp. 98-111 (2005).
77. Otim M, Legg J, Kyamanywa S, Polaszek A and Gerling D, Occurrence and activity of Bemisia tabaci parasitoids on cassava in different agro-ecologies in Uganda. Biocontrol 50:87-95 (2004).
78. Otim M, Legg J, Kyamanywa S, Polazsek A and Gerling D, Population dynamics of Bemisia tabaci (Homoptera: Aleyrodidae) parasitoids on cassava mosaic disease-resistant and susceptible varieties. Biocontrol Sci Technol 16:205-214 (2006).
79. Otim M, Kyalo G, Kyamanywa S, Asiimwe P, Legg JP, Guershon M. et al, Parasitism of Bemisia tabaci (Homoptera: Aleyrodidae) by Eretmocerus mundus (Hymenoptera: Aphelinidae) on cassava. Int J Trop Insect Sci 28:158-167 (2008).
80. Asiimwe P, Ecaat JS, Otim M, Gerling D, Guershon M, Kyamanywa S. et al, Life table analysis of mortality factors affecting populations of Bemisia tabaci on cassava in Uganda. Entomol Exp Applic 122:37-44 (2007).
81. Asiimwe P, Kyamanywa S, Gerling D and Legg JP, Evaluation of Serangium n. sp. (Coleoptera: Coccinellidae) a predator of Bemisia tabaci (Homoptera: Aleyrodidae) on cassava. J Appl Entomol 131:76-80 (2007).
82. Hilje L, Costa HS and Stansly PA, Cultural practices for managing Bemisia tabaci and associated viral diseases. Crop Prot 20:801-812 (2001).
83. Dixon AGO, Bandyopadhyay R, Coyne D, Ferguson M, Ferris RSB, Hanna R. et al, Cassava: from a poor farmer's crop to a pacesetter of African rural development. Chron Hort 43:8-14 (2003).
84. Patil BL, Ogwok E, Wagaba H, Mohammed IU, Yadav JS, Bagewadi B. et al, RNAi mediated resistance to diverse isolates belonging to two virus species involved in Cassava brown streak disease. Mol Plant Pathol 12:31-41 (2010).
85. Ariyo OA, Dixon AGO and Atiri GI, Whitefly Bemisia tabaci (Homoptera: Aleyrodidae) infestation on cassava genotypes grown at different ecozones in Nigeria. J Econ Entomol 98:611-617 (2005).
86. Avicor SW, Eziah VY, Owusu EO and Wajidi MFF, Insecticide susceptibility of Bemisia tabaci to Karate and Cydim Super and its associated carboxylesterase activity. Sains Malays 43:31-36 (2014).
87. Otoidobiga LC, Vincent C and Stewart RK, Susceptibility of field populations of adult Bemisia tabaci Gennadius (Homoptera: Aleyrodidae) and Eretmocerus sp. (Hymenoptera: Aphelinidae) to cotton insecticides in Burkina Faso (West Africa). Pest Manag Sci 59:97-106 (2003).
88. Houndété TA, Kétoh GK, Hema OSA, Brévault T, Glitho IA and Martin T, Insecticide resistance in field populations of Bemisia tabaci (Hemiptera: Aleyrodidae) in West Africa. Pest Manag Sci 66:1181-1185 (2010).
89. Gnankiné O, Ketoh G and Martin T, Dynamics of the invasive Bemisia tabaci (Homoptera: Aleyrodidae) Mediterranean (MED) species in two West African countries. Int J Trop Insect Sci 33:99-106 (2013).
90. Gnankiné O, Mouton L, Savadogo A, Martin T, Sanon A, Dabire RK. et al, Biotype status and resistance to neonicotinoids and carbosulfan in Bemisia tabaci (Hemiptera: Aleyrodidae) in Burkina Faso, West Africa. Int J Pest Manag 59:95-102 (2013).
91. Jeremiah S, The role of whitefly (Bemisia tabaci) in the spread and transmission of cassava brown streak disease in the field. PhD Thesis, University of Dar es Salaam, Dar es Salaam, Tanzania, 229 pp. (2012).
92. Legg JP, Asiimwe P, Sseruwagi P and Brown JK, Changes in the Biology of Bemisia tabaci on Cassava in Africa and their Impact on Virus Disease Pandemics. [Online]. (2006). Available: http://www.insectscience.org/8.04/ref/abstract51.html [accessed 10 May 2014].
93. Stern VM, Smith RF, van den Bosch R and Hagen KS, The integrated control concept. Hilgardia 29:81-101 (1959).
94. Ellsworth PC and Martinez-Carrillo JL, IPM for Bemisia tabaci: a case study from North America. Crop Prot 20:853-869 (2001).
95. Naranjo SE and Ellsworth PC, 50 years of the integrated control concept: moving the model and implementation forward in Arizona. Pest Manag Sci 65:1267-1286 (2009).
96. Stansly PA and Natwick ET, Integrated systems for managing Bemisia tabaci in protected and open field agriculture, in Bemisia: Bionomics and Management of a Global Pest, ed. by Stansly PA and Naranjo SE. Springer, Dordrecht/Heidelberg/London/New York, pp. 467-497 (2010).
97. Naranjo SE and Ellsworth PC, The contribution of conservation biological control to integrated management of Bemisia tabaci in cotton. Biol Control 51:458-470 (2009).
98. Kontsedalov S, Gottlieb Y, Ishaaya I, Nauen R, Horowitz R and Ghanim M, Toxicity of spiromesifen to the developmental stages of Bemisia tabaci biotype B. Pest Manag Sci 65:5-13 (2008).