Abstract
The Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Liviidae) is a damaging pest of citrus globally and has recently been detected in Tanzania. Although direct damage by the pest is seldom of economic importance, the insect is more notorious for its ability to vector the fastidious phloem-limited bacterium Candidatus Liberibacter asiaticus (CLas), the putative causal bacterium of Huanglongbing or Asian citrus greening disease. For many years, Trioza erytreae (Del Guercio) (Hemiptera: Triozidae) was known to be the main vector of the African citrus greening disease caused by Candidatus Liberibacter africanus (CLaf), but the recent arrival of D. citri on the continent adds to the dynamics of infection and spread of both diseases on mainland Africa. Following the recent report of the presence of D. citri in Tanzania, an additional delimiting survey was carried out in the region, focusing on Kenya, mainland Tanzania and Zanzibar to detect the presence and ascertain the extent of spread of D. citri. We employed molecular tools based on the use of DNA barcoding to confirm the identity of D. citri. In addition to D. citri, the occurrence of T. erytreae in the same sampling locations is also reported. Adults and nymphs of either D. citri or T. erytreae were collected from citrus at many of the surveyed sites ranging from 19 to 668 m above sea level (masl) in Tanzania, 20–1666 masl in Kenya, and 42–48 masl in Zanzibar. Diaphorina citri was sympatric with T. erytreae at the mid to higher elevations of 1375–1666 masl and no T. erytreae or its open-gall symptoms were detected below 523 masl. Sequences obtained were queried via BLAST and all linked to D. citri of different accession numbers already available on GenBank. This is the first report of the presence of D. citri in Kenya and Zanzibar. The potential implication of the detection and spread of the two pathogens, CLaf and CLas to the citrus industry in East Africa and movement of suitable host plants is discussed.

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References
Alvarez S, Rohrig E, Solís D, Thomas MH (2016) Citrus greening disease (Huanglongbing) in Florida: economic impact, management and the potential for biological control. Agric Res 5:109–118. doi:10.1007/s40003-016-0204-z
Aubert B (1987) Trioza erytreae Del Guercio and Diaphorina citri Kuwayama (Homoptera: Psylloidea), the two vectors of citrus greening disease: biological aspects and possible control strategies. Fruits 42:149–162
Beige C, Kanyagia S, Muriuki S, Otieno S, Seif A, Whittle A (1984) Horticultural crops protection handbook. Ministry of Agriculture and Livestock Development, National Horticultural Research Station, Thika
Bové JM (2006) Huanglongbing: a destructive, newly emerging, century-old disease of citrus. J Plant Pathol 88:7–37
Bové JM (2014) Heat tolerant Asian HLB meets heat-sensitive African HLB in the Arabian Peninsula! Why? J Citrus Pathol 1:1–78
da Graça JV (1991) Citrus greening disease. Annu Rev Phytopathol 29:109–136. doi:10.1146/annurev.py.29.090191.000545
da Graça JV, Kunta M, Sétamou M, Rascoe J, Li W, Nakhla MK, Salas B, Bartels DW (2015) Huanglongbing in Texas: report on the first detections in commercial citrus. J Cit Pathol. iocv_journalcitruspathology_27939
Flores D, Hall DG, Jenkins DA, Sétamou M (2009) Abundance of Asian citrus psyllid on yellow sticky traps in Florida, Puerto Rico, and Texas citrus groves. Southwest Entomol 34(1):1–11. doi:10.3958/059.034.0101
French JV, Khalke CJ, da Graça JV (2001) First record of the Asian citrus psylla, Diaphorina citri Kuwayama (Homoptera: Psyllidae) in Texas. Subtrop Plant Sci 53:14–15
Garnier M, Bové JM (1996) Distribution of the Huanglongbing (greening) Liberobacter species in fifteen African and Asian countries. In: Proceedings of 13th conference IOCV, IOCV, Riverside 1996, pp 388–391
Gottwald TR (2010) Current epidemiological understanding of citrus Huanglongbing. Annu Rev Phytopathol 48:119–139. doi:10.1146/annurev-phyto-073009-114418
Grafton-Cardwell EE, Stelinski LL, Stansly PA (2013) Biology and management of Asian citrus psyllid, vector of the Huanglongbing pathogens. Annu Rev Entomol 58:413–432. doi:10.1146/annurev-ento-120811-153542
Halbert SE, Manjunath KL (2004) Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature review and assessment of risk in Florida. Fla Entomol 87:330–353. doi:10.1653/0015-4040(2004)087[0330:ACPSPA]2.0.CO;2
Hall DG, Hentz MG (2010) Sticky trap and stem-tap sampling protocols for the Asian citrus psyllid (Hemiptera: Psyllidae). J Econ Entomol 103:541–549. doi:10.1603/EC09360
Hall DG, Richardson ML, Ammar ED, Halbert SE (2013) Asian citrus psyllid, Diaphorina citri, vector of citrus Huanglongbing disease. Entomol Exp Appl 146:207–223. doi:10.1111/eea.12025
Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM (2004) Identification of birds through DNA barcodes. PLoS Biol 2(10):e312
Kalyebi A, Aisu G, Ramathani J, Ogwang J, McOwen N, Russell P (2015) Detection and identification of etiological agents (Liberibacter spp.) associated with citrus greening disease in Uganda. Uganda J Agric Sci 16:43–54. doi:10.4314/ujas.v16i1.4
Kobori Y, Nakata T, Ohto Y, Takasu F (2011) Dispersal of adult Asian citrus psyllid, Diaphorina citri Kuwayama (Homoptera: Psyllidae), the vector of citrus greening disease, in artificial release experiments. Appl Entomol Zool 46:27–30. doi:10.1007/s13355-010-0004-z
Lallemand J, Fos A, Bové JM (1986) Transmission de la bacteria associé à la forme africaine de la maladie du “greening” par le psylle asiatique Diaphorina citri Kuwayama. Fruits 41:341–343
Lewis-Rosenblum H, Martini X, Tiwari S, Stelinski LL (2015) Seasonal movement patterns and long-range dispersal of Asian citrus psyllid in Florida citrus. J Econ Entomol 108:3–10. doi:10.1093/jee/tou008
Magomere TO, Obukosia SD, Mutitu E, Ngichabe C, Olubayo F, Shibairo S (2009) PCR detection and distribution of Huanglongbing disease and psyllid vectors on citrus varieties with changes in elevation in Kenya. J Biol Sci 9:697–709. doi:10.3923/jbs.2009.697.709
Narouei-Khandan HA, Halbert SE, Worner SP, van Bruggen AHC (2016) Global climate suitability of citrus Huanglongbing and its vector, the Asian citrus psyllid, using two correlative species distribution modeling approaches, with emphasis on the USA. Eur J Plant Pathol 144:655–670. doi:10.1007/s10658-015-0804-7
OEPP/EPPO (2005a) EPPO Standards PM 7/52(1). Diagnostic protocol for Diaphorina citri. Bulletin OEPP/EPPO Bulletin 35:331–333. doi:10.1111/j.1365-2338.2005.00839.x
OEPP/EPPO (2005b) EPPO Standards PM 7/57(1). Diagnostic protocol for Trioza erytreae. Bull OEPP/EPPO Bull 35:357–360. doi:10.1111/j.1365-2338.2005.00832.x
Purcell AH (1982) Insect vector relationships with prokaryotic plant pathogens. Annu Rev Phytopathol 20:397–417. doi:10.1146/annurev.py.20.090182.002145
Roberts R, Cook G, Grout TG, Khamis F, Rwomushana I, Nderitu PW, Seguni ZS, Materu CL, Steyn C, Pietersen G, Ekesi S, le Roux HF (2017) Resolution of the identity of ‘Candidatus Liberibacter’ species from Huanglongbing-affected citrus in East Africa. Plant Dis. doi:10.1094/PDIS-11-16-1655-RE
Saponari M, De Bac G, Breithaupt J, Loconsole G, Yokomi RK, Catalano L (2010) First report of Candidatus Liberibacter asiaticus associated with Huanglongbing in sweet Orange in Ethiopia. Plant Dis 94:482. doi:10.1094/pdis-94-4-0482a
Sétamou M, Flores D, French JV, Hall DG (2008) Dispersion patterns and sampling plans for Diaphorina citri (Hemiptera: Psyllidae) in citrus. J Econ Entomol 101:1478–1487. doi: 10.1603/0022-0493(2008)101[1478:DPASPF]2.0.CO;2
Sétamou M, da Graça JV, Sandoval JL (2016) Suitability of native North American Rutaceae to serve as hosts for the Asian citrus psyllid (Hemiptera: Liviidae). J Appl Entomol 140:645–654. doi:10.1111/jen.12300
Shimwela MM, Narouei-Khandan HA, Halbert SE, Keremane ML, Minsavage GV, Timilsina S, Massawe DP, Jones JB, van Bruggen AHC (2016) First occurrence of Diaphorina citri in East Africa, characterization of the Ca. Liberibacter species causing Huanglongbing (HLB) in Tanzania, and potential further spread of D. citri and HLB in Africa and Europe. Eur J Plant Pathol 146:346–368. doi:10.1007/s10658-016-0921-y
Acknowledgements
We gratefully acknowledge the financial support for this research by the following organizations and agencies: Deutsche Gesellschaft für Internationale Zusammernarbeit (GIZ) through the project “Strengthening Citrus Production Systems through the Introduction of Integrated Pest Management (IPM) Measures for Pests and Diseases in Kenya and Tanzania (SCIPM)”, Grant Number 14.1432.5-001.00; UK Aid from the UK Government; Swedish International Development Cooperation Agency (Sida); the Swiss Agency for Development and Cooperation (SDC); and the Kenyan Government. The views expressed herein do not necessarily reflect the official opinion of the donors.
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Rwomushana, I., Khamis, F.M., Grout, T.G. et al. Detection of Diaphorina citri Kuwayama (Hemiptera: Liviidae) in Kenya and potential implication for the spread of Huanglongbing disease in East Africa. Biol Invasions 19, 2777–2787 (2017). https://doi.org/10.1007/s10530-017-1502-5
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DOI: https://doi.org/10.1007/s10530-017-1502-5


