Asian Form of Huanglongbing: History
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Contributor:
Sui S. Leong
,
Stephen C. T. Leong
,
George A. C. Beattie

The Asian citrus psyllid (ACP), Diaphorina citri Kuwayama, transmits ‘Candidatus Liberibacter asiaticus’ (CLas), a phloem-limited bacterium associated with the severe Asian form of huanglongbing (HLB), and the most destructive disease of citrus. The pathogen and the psyllid, both of South Asian origin, are now widespread in citrus regions of Asia and the Americas. There is no cure for the disease. Application of synthetic pesticides, in some instances more frequently than fortnightly, to minimize incidence of ACP in citrus orchards, has not prevented inevitable impacts of the disease in regions of Asia where CLas is present. Despite the inevitable spread of the disease, significant progress has been made in Sarawak since the mid-1990s towards effectively implementing integrated pest management (IPM) programs for stemming the impact of the disease and detrimental consequences of over-reliance on synthetic pesticides. Growers are encouraged to plant pathogen-free trees, remove diseased trees, monitor incidence of the psyllid, and to use pesticides judiciously to reduce their detrimental impacts on natural enemies. Knowledge has been enhanced through research on seasonal incidence of the psyllid, use of mineral oils, development of protocols and iodine–starch test kits for detecting infected trees, PCR for confirming the presence of CLas in symptomatic leaves, methods for monitoring incidence the psyllid, and training extension staff and growers. However, major impediments to increasing the average longevity of trees beyond <5 years in poorly managed orchards, based on marcotting (air layering), and >12 years in well-managed orchards, based on pathogen-free trees, still need to be addressed. These include grower knowledge, marcotting, aggressive marketing of synthetic pesticides, high prices of mineral oils, spray application procedures, and better reliance on natural enemies of the psyllid.

  • citrus
  • Diaphorina citri
  • ‘Candidatus Liberibacter asiaticus’

1. Introduction

The genus Citrus (Rutaceae: Aurantioideae: Aurantieae) includes species and hybrids of widely cultivated fruits (grapefruit, kumquats, lemons, limes, oranges, and pomelos) in tropical and subtropical regions of the world [1][2][3][4]. The genus is believed to have originated from the region comprising Northeast South Asia, South and Southwest China, Indochina, and Malesia [5]. In Malaysia, citrus is grown in commercial orchards, small holdings, and backyards. It is an important fruit crop in the East Malaysian state of Sarawak in northern Borneo, where it provides a livelihood to many growers who supply mainly to the domestic market. The total area of commercial orchards in the state was approximately 3250 ha in 2005 [6]. An estimated 28.35 metric tonnes of fresh orange fruit/juice were exported to Singapore, Peninsular Malaysia, and Brunei in 2005. The most important production areas in Sarawak are located in the Samarahan Division adjacent to the state capital Kuching (1.5548° N, 110.3594° E), with some major plantings in Sarikei, Sibu, and Bintulu Divisions, some 140, 190, and 350 km, respectively, northeast of Kuching.
The major impediments to production are the severe Asian form of huanglongbing (HLB) putatively associated with a phloem-limited Gram-negative bacterium ‘Candidatus Liberibacter asiaticus’ (CLas) (α-Proteobacteria) and the Asian citrus psyllid (ACP), Diaphorina citri Kuwayama (Hemiptera: Sternorrhyncha: Psyllidae), the most widely distributed vector of the pathogen that has severely affected citrus production in Asia and the Americas [7][8][9][10][11][12]. The psyllid was noted as being present in Malaysia by Clausen [13]. Symptoms resembling HLB were first noticed in Malaysia in the 1970s in lowland peninsular orchards near Kampung Jerangau (4.8370° N, 103.1971° E, 20 m above sea level (ASL); Kuala Dungun, in Terengganu; Ulu Tiram, in Johor (1.5974° N, 103.8150° E, 25 m ASL); and the highland area near Ringlet (4.4146° N, 101.3846° E, 1110 m ASL) in the Cameron Highlands in Pahang [14][15][16][17], but no bacterium-like organisms were observed in sectioned fixed leaves examined under an electron microscope in France [18]. Broadbent [18] observed symptoms typical of the disease in grapefruit (Citrus × aurantium L.), sweet orange (C. × aurantium), and mandarin (C. × aurantium) leaves in the Cameron Highlands. Grapefruit were severely affected while lemons (C. × limon (L.) Osbeck), limes (Mexican, Key, alemow: C. × aurantiifolia (Christm.) Swingle, syn. C. × macrophylla Wester), and Dancy tangerine (C. × aurantium) appeared to have some tolerance. However, no bacterium-like organisms were observed in sections of young leaves [18]. Symptoms were also reported from the Cameron Highlands by Catling [19]. Information provided by Ko [20] and Saamin et al. [21] suggests that the first record of the disease in Peninsular Malaysia was related to the introduction of C. × aurantium seedlings, in this instance Tanaka’s ‘C. suhuiensis’, a mandarin variety from Sihui (23.3534° S, 112.8964° E ), near Guangzhou in Guangdong, mainland China, to Terengganu, from China in the 1950s and 1960s. The presence of the disease was confirmed when the pathogen CLas was detected in sectioned leaves from symptomatic plants in the Cameron Highlands in 1987 [22][23][24]. The disease was first detected in Sarawak in the Samarahan Division in 1988 [25]. Since then, research and extension activities undertaken by the Sarawak Department of Agriculture (SDOA) and universities in the state have focused on minimising the impact of the disease. Intensive pesticide programs lead to insecticide resistance and are harmful to pollinators and beneficial insects. Therefore, it is important to design IPM strategies that minimise the utilisation of pesticides, especially neonicotinoids and other broad-spectrum materials, and maximise the use of natural enemies, especially the primary ectoparasitoid Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) and the primary endoparasitoid Diaphorencyrtus aligarhensis (Shafee, Alam and Argarwal) (Hymenoptera: Encyrtidae), as well as several predators, including the weaver ant, Oecophylla smaragadina Fabricius (Hymenoptera: Formicidae). 

2. Origin and Distribution of Asian HLB

Although the disease was first recognized as transmissible in China [8], the first unambiguous description of symptoms is within text in which Husain and Nath [26] describe damage caused by the psyllid: small and insipid fruit, dieback, and death of trees caused by a ‘toxin’ injected into plant tissues by the psyllid. The pathogen probably originated in association with a non-citrus host in South Asia. It did not originate in mainland China or Taiwan. The disease was not described, as oft cited, by Reinking [27], who observed citrus maladies in Guangdong in mainland China, or in Taiwan by Sawada (1913) [28], as claimed recently by Zhou [29] and Guo et al. [30]. The first authentic record of HLB in mainland China appears to have been made in Guangdong in 1938 [31][32], four years after ACP was recorded in the province [33][34][35]. HLB was first recorded in Taiwan in 1951 [35][36]. It is now widespread in Asia, the Americas, and is present in the Mascarene Islands, New Guinea, and, most recently, Africa [7][37][38][39][40][41][42].

2.1. Host Susceptibility to HLB

All citrus species and hybrids are susceptible to the Asian form of HLB, although some species, e.g., C. cavaleriei H. Lév. ex. Cavalerie (China), C. gracilis Mabb. (Australia), and C. hystrix DC (Indochina and Malesia), have not been evaluated or fully evaluated. The least susceptible species, in approximate order of increasing susceptibility, with their geographic origin in parentheses, include C. glauca (Lindl.) Burkill (Australia); C. halimii B.C. Stone (Malaysia and Thailand); C. australasica F. Muell., C. inodora F. M. Bailey, and C. × virgata Mabb. (Australia); C. (Poncirus) trifoliata L. (China); C. × oliveri Mabb. (C. australasica × C. × microcarpa Bunge) and C. australis (A.Cunn ex Mudie) Planchon (Australia); and C. latipes (Swingle) Tanaka (Northeast South Asia) [43][44]. The susceptibility to CLas of species of Citrus (Oxanthera) from New Caledonia and of C. polyandra Tan. (syn. Clymenia polyandra (Tan.) Swingle) from New Ireland in Papua New Guinea has not been determined.
In Malaysia, Shokrollah et al. [45] assessed the susceptibility of 18 citrus ‘species’ to HLB following graft transmission of CLas from infected mandarin plants. The pathogen was detected by PCR in 15 of the species 6 months after grafting. Susceptibility was categorised into five symptom groups: severe (72–58% severity), comprising ‘limau madu’ and Cleopatra mandarins, and sweet orange; moderate (50–41% severity), comprising kumquat (C. (Fortunella) japonica Thunb. cv. Kasturi Chinai), C. aurantiifolia (cv. ‘machrophylla’), and calamondin (C. × microcarpa Bunge); mild (25–17% severity), comprising citron (C. medica L.), C. aurantiifolia, Citrus sp. (natural genotype), and rough lemon (C. × otaitensis (Risso and Poit.) Risso syn. C. jambhiri Lush.); tolerant (no symptoms but PCR positive), comprising sour orange (C. × aurantium) and C. aurantiifolia (cv. ‘limau nipis’)); and resistant (no symptoms and PCR negative), comprising pomelo (C. maxima (Burm.) Merr., cv. limau Bali), limau purut or leech lime (C. hystrix), and Citrus sp. (cv. ‘Limau Tembikai’).
CLas-infected trees become unproductive (30–100% reduction in yield) and may die in 5–8 years, or less, of infection, depending on the susceptibility to the disease of the host plant species/hybrid [8]. Short lifespans (<3 years) of trees are often related to marcotting (air layering) (Beattie, personal observation). There is currently no cure for HLB, the best control strategy being the prevention of the disease [8]. Movement of infected citrus material by land, sea, and air is the most efficient way of disseminating HLB over large distances. Entry of CLas to parts of Southeast Asia and Malesia, and to the Mascarene Islands, has been linked to human migration and movement of plants from China, after the pathogen was introduced to China [10][39][46][47]. The use of disease-free planting material from reliable sources is the first and most important step towards good disease management. Mother trees from which budwood is obtained must be kept in well-maintained insect-proof screenhouses.
Initial lack of awareness of this disease, slow introduction of diagnostic tests, and rapid propagation of non-certified planting material by citrus growers to expand their orchards have contributed to poor management of HLB in Malaysia. The reluctance of growers to remove infected trees due to limited knowledge about the pathogen, its mode of spread by ACP, and the cost of vector control, have contributed to the problem. Surveys in 2004 by Azizah and Zazali [48] revealed that approximately 70% of the cultivated area (3526 ha) of citrus in Peninsular Malaysia was affected. In Terengganu, the area affected increased from 641 ha in 2001 to 1262 ha in 2004 [48].
HLB in Sarawak destroyed 1143 ha of orchards, comprising ‘limau langkat’ (C. × aurantium, Tanaka’s ‘C. suhuiensis’) or mandarin orange, sour or bitter orange, and leech lime, in the Samarahan Division by 1991. Economic losses in the state were estimated to be 6.5 million Malaysian ringgit (RM) (1.6 million United States dollar (USD) [49][50][51]. Citrus fruits had to be imported from neighbouring countries, such as Indonesia and Thailand, to meet the local demand. After the decline of the citrus industry in the Samarahan Division, the SDOA started producing disease-free planting material in 1996. The disease-free planting material was produced using budwood obtained through shoot tip micro-propagation [52].

3. Origins and Distribution of ACP

ACP originated on the Indian subcontinent. Spread of the psyllid eastward to Southeast and East Asia appears to have been linked to movement of infested host plants from Southern India and Sri Lanka to Java in Western Indonesia, and subsequently to Ambon and Timor in Eastern Indonesia, Luzon in the Philippines, Macao, and Taiwan [46]. Although ACP was first described from specimens collected from citrus in ‘Shinchiku Prefecture’ in northern Taiwan [53], then Japanese occupied ‘Formosa’, it was first recorded in Java in 1900 [46]. The psyllid now occurs in South Asia, East Asia, Malesia, New Guinea in Australasia, Arabia and Israel in West Asia, Caribbean islands; North, Central and South America; some Pacific Ocean islands; and the Maldives and Mascarene islands in the Indian Ocean [46]. It was recorded in Africa in 2015 [54] and was recently recorded in Israel in 2021 [55].

3.1. Host Susceptibility to ACP

Known hosts of ACP were reviewed by Beattie [56]. Among 87 seed-source field-planted seedlings of 76 Citrus species and hybrids, and 11 Citrus relatives colonised by ACP adults over 4 months in summer and early autumn in Florida, the least susceptible Citrus species and hybrids were C. trifoliata, C. inodora, C. glauca, C. halimii, C. australasica, C. × virgata, C. × leiocarpa hort. ex Tan., incertae sedis (Koji mandarin), and sour orange. The most colonised, including Citrus relatives, were C. reticulata, Bergera koenigii L. (curry leaf) (Aurantioideae: Clauseneae), Murraya paniculata (L.) Jack (orange jasmine) (Aurantieae), C. medica, and C. aurantiifolia (lime, Key or Mexican lime, alemow) [57]. Lim et al. (1990-citrus greening) [24] cited C. hystrix, C. maxima, C. reticulata L. (including C. suhuiensis), C. × aurantiifolia, C. × limon, C. × microcarpa Bunge, Rangpur lime (C. × otaitensis), B. koenigii and Clausena excavata Burm.f. (Clauseneae), and M. paniculata as hosts in Malaysia. In Sarawak, Leong et al. [57] reported that ACP can colonise and breed on ‘limau langkat’, orange jasmine, and curry leaf, and that orange jasmine is the preferred host. ACP completes its life cycle (from egg to adult) in the shortest period (18.5 days) on orange jasmine, followed by ‘limau lankat’ (19.0 days) and curry leaf (23.0 days) [57]. The susceptibility of species of Citrus (Oxanthera) from New Caledonia and C. polyandra from Papua New Guinea as hosts of ACP has not been determined.

3.2. Biology of ACP and Influence of Abiotic Factors

ACP has a high capacity to increase in numbers on highly suitable hosts in monocultures [26][58][59], but in the absence of HLB it is a minor pest. It is not able to build up massively on rutaceous host trees or shrubs in forests [59] but is capable of surviving in low-density populations in natural habitats on sparsely spaced host plants with limited immature flush growth suitable for oviposition and development of nymphs [59]. Liu and Tsai [60] studied development, survival, longevity, reproduction, and life table parameters of ACP in growth chambers at temperatures ranging from 10 °C to 33 °C and relative humidities between 75 and 80%. Populations reared at 10 °C and 33 °C failed to develop [60]. However, populations can flourish in Köppen–Geiger BWh desert and BSh hot semi-arid zones of South Asia, where average daily maximum temperatures over several weeks can reach 45–50 °C [46]. The effects of different temperatures on the life history parameters, including development times and longevity for different geographic populations, have been assessed several times [60][61][62][63][64][65]. A meta-analysis of published ACP temperature-dependent development literature by Milosavljevic et al. [65], synthesising datasets of five globally distributed populations (Brazil, California, China, Florida, and Japan) reared under different constant temperatures on six different host plants (i.e., Rangpur lime, Natal and Pêra oranges, kumquat, mandarin, and orange jasmine), together with the results of the study on Volkamer lemon (C. × otaitensis), revealed convergence in estimates of developmental parameters. These results have implications for predicting ACP invasions and establishment risks, and subsequent population dynamics across various climactic gradients and geographic regions. Ahmad [66] estimated that >4.5 million adults and nymphs were present in March (spring) 1959 in a one-acre (0.4 ha) irrigated orchard comprising 110 mature C. × aurantiifolia trees near Multan (30.1981° N, 71.4685° E, 129 m ASL) in the hot-desert Punjab region of Pakistan. Husain and Nath [26] recorded up to 807 eggs per female, but in other studies, fecundity ranged from 180 to near 1900 eggs per female, depending on the ambient conditions of the host plants [60][67][68][69]. Heavy rainfall, particularly monsoon rains, washes eggs and nymphs of plants [46]. Aubert [9][10][11] mentioned that ACP mortality increases with higher rainfall and relative humidity, and that monthly rainfall above 150 mm is associated with low populations due to eggs and young nymphs being washed off plant surfaces.
ACP has been recorded at elevations up to 1250 m above sea level near Kuala Terla (4.5467° N, 101.4162° E) in the Cameron Highlands in Peninsular Malaysia [23][24]. Massive populations were observed on HLB-infected trees in a neglected orchard, but no psyllids were observed on infected trees at 1450 m ASL [23][24]. Om et al. [70] rarely recorded it at elevations above 1200 m in Bhutan and suggested that UV-B, which increases with increasing elevations above sea level, may affect survival of the psyllid. They found no relationship between abundance of the psyllid at elevations ranging from 800 to 1500 m and tree growth, ambient air temperatures, relative humidity, rainfall, or natural enemies [70][71].

4. Natural Enemies of ACP in Asia

Natural enemies of ACP in Asia include the primary parasitoids T. radiata and D. aligarhensis, predators such as ladybirds (Coleoptera: Coccinellidae), lacewings (Neuroptera: Chrysopidae), ants (Hymenoptera: Formicidae), thrips (Thysanoptera: Phlaeothripidae), syrphid flies (Diptera: Syrphidae), bugs (Hemiptera: Geocoridae), mantids (Mantodea: Mantidae), mites (Acari: Phytoseiidae), and spiders (Acari: Clubionidae, Gnaphosidae and Salticidae), and six species of entomopathogenic fungi [46]. The importance of O. smaragadina has been overlooked [72]. It occurs naturally in Borneo and elsewhere in tropical and subtropical citrus regions in Asia, New Guinea, and northern Australia, and has been recognised as an important predator of citrus pests in Asia, particularly China and Vietnam, for some 1700 years [71]. It preys on eggs of ACP, and incidence of psyllid and HLB has been recorded as lower in unsprayed orchards than in orchards sprayed with synthetic pesticides [72][73].

This entry is adapted from the peer-reviewed paper 10.3390/insects13100960

References

  1. Mabberley, D.J. A classification for edible citrus: An update, with a note on Murraya (Rutaceae). Telopea 2022, 25, 271–284.
  2. Mabberley, D.J. Australian Citreae with notes on other Aurantioideae (Rutaceae). Telopea 1998, 7, 333–344.
  3. Mabberley, D.J. Citrus (Rutaceae): A review of recent advances in etymology, systematics and medical applications. Blumea 2004, 49, 481–498.
  4. Mabberley, D.J. Mabberley’s Plant Book: A Portable Dictionary of Plants, Their Classification and Uses, 4th ed.; Cambridge University Press: Cambridge, UK, 2017; p. 128.
  5. Talon, M.; Wu, G.; Albert, G.; Frederick, G.; Rokhsar, D.S. The Origin of Citrus; Talon, M., Caruso, M., Gmitter, F.G., Jr., Eds.; Elsevier: London, UK, 2020; pp. 9–31.
  6. Department of Agriculture Sarawak. Agricultural Statistics of Sarawak; Department of Agriculture Sarawak: Sarawak, Malaysia, 2005; p. 147.
  7. Halbert, S.E.; Manjunath, K.L. Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: A literature review and assessment of risk in Florida. Fla. Entomol. 2004, 87, 330–353.
  8. Bove, J.M. Huanglongbing: A destructive, newly-emerging, century-old disease of citrus. J. Plant Pathol. 2006, 88, 7–37.
  9. Aubert, B. Trioza erytreae del Guercio and Diaphorina citri Kuwayama (Homoptera: Psylloidea), the two vectors of citrus greening disease: Biological aspects and possible control strategies. Fruits 1987, 42, 149–162.
  10. Aubert, B. Towards an integrated management of citrus greening disease. In Proceedings of the 10th Conference International Organization of Citrus Virologists, Riverside, CA, USA, 1–4 June 1988; Timmer, L.W., Garnsey, S.M., Navarro, L., Eds.; International Organization of Citrus Virologists: Riverside, CA, USA, 1988; pp. 226–230.
  11. Aubert, B. Integrated activities for the control of huanglongbing-greening and its vector Diaphorina citri Kuwayama in Asia. In Proceedings of the Fourth International Asia-Pacific Conference on Citrus Rehabilitation, Chiang Mai, Thailand, 12 September 1990; Aubert, B., Tontyaporn, S., Buangsuwon, D., Eds.; NDP-FAO Press: Chiang Mai, Thailand, 1990; pp. 133–144.
  12. Tiwari, S.; Mann, R.S.; Rogers, M.E.; Stelinski, L.L. Insecticide resistance in field populations of Asian citrus psyllid in Florida. Pest Manag. Sci. 2011, 67, 1258–1268.
  13. Clausen, C.P. The Citrus Insects of Tropical Asia; Circular 266; United States Department of Agriculture: Washington, DC, USA, 1933; p. 35.
  14. Tanaka, H.; Ueno, I. Report on the Visit to Malaysia to Survey Agronomic Practices and Diseases of Citrus; MARDI: Selangor, Malaysia, 1978; p. 22.
  15. Lim, W.H.; Shamsudin, O.M.; Ko, W.W. Citrus greening disease and alternate hosts of the vector, Diaphorina citri Kuw., in P. Malaysia. MAPPS Newsl. 1990, 13, 56–58.
  16. Lim, W.H.; Shamsudin, O.M.; Ko, W.W. Citrus greening disease in Malaysia: Status report. In Proceedings of the Fourth International Asia Pacific Conference on Citrus Rehabilitation, Chiang Mai, Thailand, 4–10 February 1990; Aubert, B., Tontyaporn, S., Buangsuwon, D., Eds.; FAO UNDP: Rome, Italy, 1990; pp. 100–105.
  17. Osman, M.S.; Lim, W.H. Studies on vector distribution, etiology and transmission of greening disease of citrus in P. Malaysia. In Proceedings of the Asian Citrus Rehabilitation Conference, Malang, Indonesia, 4–14 July 1989; Setyobudi, L., Bahar, F.A., Winarno, M., Whittle, A.M., Eds.; FAO UNDP INS/84/007. Ministry of Agriculture, Republic of Indonesia Agency for Agricultural Research and Development: Jakarta, Indonesia, 1992; pp. 157–165.
  18. Broadbent, P. Citrus Greening and Virus Disease in China and South East Asia; Asia and Pacific Plant Technical Document FAO DOC. No. 132; Food and Agriculture Organization of the United Nations: Rome, Italy, 1983.
  19. Catling, D. Consultancy on Citrus Greening Disease in South and South East Asia; FAO TCP RAS 4509; Food and Agriculture Organization: Phnom Penh, Cambodia, 1985; p. 41.
  20. Ko, W.W. Citrus diseases in Malaysia. In Proceedings of the Sixth International Asia Pacific Workshop on Integrated Citrus Health Management, Kuala Lumpur, Malaysia, 24–30 June 1991; pp. 147–162.
  21. Saamin, S.; Osman, M.; Ko, W.W.; Osman, M.S. Malaysian citrus Industry development perspectives. In Proceedings of the Sixth International Asia Pacific Workshop on Integrated Citrus Health Management, Kuala Lumpur, Malaysia, 24–30 June 1991.
  22. Garnier, M.; Bové, J.M. Report on Virus and Virus-like Diseases of Citrus in Malaysia with Special Reference to Citrus Greening; FAO-UNDP Report; FAO-UNDP: Rome, Italy, 1990; p. 17.
  23. Aubert, B. Malaysian citriculture report of visits October 19th–22nd 1987 and February 23rd–28th 1989. In Proceedings of the Asian Citrus Rehabilitation Conference, Malang, Indonesia, 4–14 July 1989; Setyobudi, L., Bahar, F.A., Winarno, M., Whittle, A.M., Eds.; FAO UNDP INS/84/007. Ministry of Agriculture, Republic of Indonesia Agency for Agricultural Research and Development: Jakarta, Indonesia, 1992; pp. 16–28.
  24. Lim, W.H.; Ko, W.W.; Shamsudin, M.O. Evidence for the presence of greening disease of citrus in P. Malaysia. In Proceedings of the Third International Conference on Plant Protection in the Tropics, Kuala Lumpur, Malaysia, 12–18 December 1990; Malaysian Plant Protection Society: Kuala Lumpur, Malaysia, 1990; Volume VI, pp. 120–125.
  25. Ng, T.T. Introductory Address. In Proceedings of the In-house Mini-seminar on “Citrus Greening Disease Rehabilitation Programme”, Agriculture Institute Semongok, Siburan, Malaysia, 25–27 June 1996.
  26. Husain, M.A.; Nath, D. The citrus psylla (Diaphorina citri, Kuw.) . Mem. Dep. Agric. India Entomol. Ser. 1927, 10, 5–27.
  27. Reinking, O.A. Diseases of economic plants in southern China. Philipp. Agric. 1919, 8, 109–135.
  28. Sawada, K. Citrus likubing(pre-report). Taiwan Agric. Rep. 1913, 83, 903–914.
  29. Zhou, C. The status of citrus huanglongbing in China. Trop. Plant Pathol. 2020, 45, 279–284.
  30. Guo, Y.-J.; Li, Y.-H.; Su, Z.-Q.; Xu, P.-P.; Qiu, B.-L.; Ji, Q.-H.; Khan, M.M. Temporal rhythm affects the efficiency of Asian citrus psyllid (Diaphorina citri) to acquire huanglongbing pathogen. Agronomy 2021, 11, 1956.
  31. Chen, Q. A report of a study on yellow shoot disease of citrus in Chaoshan. New Agric. Quart. Bull. 1943, 3, 142–177.
  32. Lin, K.H. Observations on yellow shoot of citrus: Aetiological studies of yellow shoot of citrus. Acta Phytopathol. Sin. 1956, 2, 1–42.
  33. Jiang, Z.; Condit, I.J.; He, F.M.; Hoffmann, W.E.; Wang, H.Z. Observations on the culture of oranges near Swatow, China. Lingnan Agric. J. 1935, 1, 175–248.
  34. He, F.M.; Djou, Y.W. Notes on citrus pests. Lingnan Agric. J. 1935, 2, 165–218. (In Chinese)
  35. Hoffmann, W.E. Diaphorina citri Kuw. (Homoptera: Chermidae), a citrus pest in Kwangtung. Lingnan Sci. J. 1936, 15, 127–132.
  36. Su, H.J.; Huang, A.L. The nature of likubin organism, life cycle morphology and possible strains. In Proceedings of the Fourth International Asia Pacific Conference on Citrus Rehabilitation, Chiang Mai, Thailand, 4–10 February 1990; Aubert, B., Tontyaporn, S., Buangsuwon, D., Eds.; FAO UNDP: Rome, Italy, 1990; pp. 106–110.
  37. Hall, D.G.; Richardson, M.L.; Ammar, E.-D.; Halbert, S.E. Asian citrus psyllid, Diaphorina citri, vector of huanglongbing disease. Entomol. Exp. Appl. 2013, 146, 207–223.
  38. Hollis, D. A new citrus-feeding psyllid from the Comoro Islands, with a review of the Diaphorina amoena species group (Homoptera). Sys. Entomol. 1987, 12, 47–61.
  39. Beattie, G.A.C.; Barkley, P. Huanglongbing and Its Vectors: A Pest-Specific Contingency Plan for the Citrus and Nursery and Garden Industries; Horticulture Australia: Sydney, Australia, 2009; Volume 2, p. 272.
  40. Saponari, M.; De Bac, G.; Breithaupt, J.; Loconsole, G.; Yokomi, R.K.; Catalano, L. First report of ‘Candidatus Liberibacter asiaticus’ associated with huanglongbing in sweet orange in Ethiopia. Plant Dis. 2010, 94, 482.
  41. Ajene, I.J.; Khamis, F.; Mohammed, S.; Rasowo, B.; Ombura, F.L.; Pietersen, G.; van Asch, B.; Ekesi, S. First report of field population of Trioza erytreae carrying the huanglongbing-associated pathogen, ‘Candidatus Liberibacter asiaticus’, in Ethiopia. Plant Dis. Notes 2019, 103, 1766.
  42. Ajene, I.J.; Khamis, F.M.; van Asch, B.; Pietersen, P.; Seid, N.; Rwomushana, I.; Ombura, F.L.O.; Momany, G.; Finyange, P.; Rasowo, B.A.; et al. Distribution of Candidatus Liberibacter species in Eastern Africa, and the first report of Candidatus Liberibacter asiaticus in Kenya. Sci. Rep. 2020, 10, 3919.
  43. Folimonova, S.Y.; Robertson, C.J.; Gamsey, S.M.; Dawson, W.O. Examination of the responses of different genotypes of citrus to huanglongbing (citrus greening) under different conditions. Phytopathology 2009, 23, 1346–1354.
  44. Ramadugu, C.; Keremane, M.L.; Halbert, S.E.; Duan, Y.P.; Roose, M.L.; Stover, E. Long-term field evaluation reveals huanglongbing resistance in Citrus relatives. Plant Dis. 2016, 9, 1858–1869.
  45. Shokrollah, H.; Abdullah, T.L.; Sijam, K.; Abdullah, S.N.A.; Abdullah, N.A.P. Differential reaction of citrus species in Malaysia to huanglongbing (HLB) disease using grafting method. Am. J. Agric. Biol. Sci. 2009, 4, 338.
  46. Beattie, G.A.C. Management of the Asian citrus psyllid in Asia. In Asian Citrus Psyllid: Biology, Ecology and Management of the Huanglongbing Vector; Qureshi, J.A., Stansly, P.A., Eds.; CAB International: Wallingford, UK, 2020; pp. 179–209.
  47. Wang, X.; Chen, J.; Lu, N.; Fu, Z.Q. Dual functions of a stable peptide against citrus huanglongbing disease. Trends Plant Sci. 2021, 26, 668–670.
  48. Azizah, M.J.; Zazali, C. Status Kemerebakan dan Impak Penyakit Greening Limau Terhadap Industry Limau di Malaysia; Jabatan Pertanian Malaysia Press: Kuala Lumpur, Malaysia, 2005.
  49. Wee, N.G. Development plan on replanting of citrus in 7MP: Mechanics, physical and financial schedule. In Proceedings of the In-house Mini-seminar on “Citrus Greening Disease Rehabilitation Programme”, Department of Agriculture, Sarawak, Malaysia, 25–27 June 1996.
  50. Eng, L. The threat of citrus greening disease (huanglongbing) to the citrus industry in Sarawak. In Proceedings of the Sarawak Fruit Seminar 2007, Sibu, Sarawak, Malaysia, 8–9 August 2007; p. 9.
  51. Eng, L.; Lau, C.Y.; Poili, E.; Azizah, M.J. Status of huanglongbing in Malaysia and the rehabilitation of infected orchards. In Proceedings of the FFTC-PPRI-NIFTS Joint Workshop on Management of Citrus Greening and Virus Diseases for the Rehabilitation of Citrus Industry in the ASPAC, Hanoi, Vietnam, 8–12 September 2008; Ku, T.Y., Pham, T.H.H., Eds.; Department of Agriculture Vietnam: Hanoi, Vietnam, 2008; pp. 137–146.
  52. Teo, C.H. Micropropagation of disease-free citrus planting materials, their disease indexing and certification. In Citrus Greening Disease Rehabilitation Programme, The Agriculture Institute Semongok; Technology Promotion Publication, Department of Agriculture: Sarawak, Malaysia, 1996.
  53. Kuwayama, S. Die psylliden Japans. I. Trans. Sopporo Nat. Hist. Soc. 1908, 2, 149–189, .
  54. Shimwela, M.M.; Narouei-Khandan, M.A.; Halbert, S.E.; Keremane, M.L.; Minsavage, G.V.; Timilsina, S.; Massawe, D.P.; Jones, J.B.; van Bruggen, A.H.C. 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. 2016, 146, 349–368.
  55. Ministry of Agriculture & Rural Development of Israel. A New Immigrant: The Ministry of Agriculture Is Fighting a New and Destructive Disease that Has Invaded Israel. 2022. Available online: https://www.gov.il/en/Departments/news/diaphorina_citri (accessed on 26 January 2022).
  56. Beattie, G.A.C. Hosts of the Asian citrus psyllid. In Asian Citrus Psyllid: Biology, Ecology and Management of the Huanglongbing Vector; Qureshi, J.A., Stansly, P.A., Eds.; CABI Digital Library: London, UK, 2020; pp. 67–86.
  57. Leong, S.C.T.; Abang, F.; Beattie, A.; Kueh, R.J.H.; Wong, S.K. Influence of host plant species and flush growth stage on the Asian citrus psyllid, Diaphorina citri Kuwayama. Am. J. Agric. Biol. Sci. 2011, 6, 536–543.
  58. Westbrook, C.J.; Hall, D.G.; Stover, E.; Duan, Y.P.; Lee, R.F. Colonization of Citrus and Citrus-related germplasm by Diaphorina citri (Hemiptera: Psyllidae). HortScience 2011, 46, 997–1005.
  59. Aubert, B. Management of the citrus greening disease in Asian orchards. In Proceedings of the Second Asian/Pacific Regional Workshop on Citrus Greening, Lipa, Philippines, 20–26 November 1988; Aubert, B., Ke, C., Gonzales, C., Eds.; FAO-UNDP: Rome, Italy, 1988; pp. 51–52.
  60. Liu, Y.H.; Tsai, J.H. Effects of temperature on biology and life table parameters of the Asian citrus psyllid, Diaphorina citri Kuwayama (Homoptera: Psyllidae). Ann. Appl. Biol. 2000, 137, 201–206.
  61. Nakata, T. Temperature-dependent development of the citrus psyllid, Diaphorina citri (Homoptera: Psylloidea), and the predicted limit of its spread based on overwintering in the nymphal stage in temperate regions of Japan. Appl. Entomol. Zool. 2006, 41, 383–387.
  62. Fung, Y.C.; Chen, C.N. Effects of temperature and host plant on population parameters of the citrus psyllid (Diaphorina citri Kuwayama). Formos. Entomol. 2006, 26, 109–123.
  63. Nava, D.E.; Torres, M.L.G.; Rodrigues, M.D.L.; Bento, J.M.S.; Parra, J.R.P. Biology of Diaphorina citri (Hem., Psyllidae) on different hosts and at different temperatures. J. Appl. Entomol. 2007, 131, 709–715.
  64. Nava, D.E.; Gomez-Torres, M.L.; Rodrigues, M.D.; Bento, J.M.S.; Haddad, M.L.; Parra, J.R.P. The effects of host, geographic origin, and gender on the thermal requirements of Diaphorina citri (Hemiptera: Psyllidae). Environ. Entomol. 2010, 39, 678–684.
  65. Milosavljević, I.; McCalla, K.A.; Morgan, D.J.W.; Hoddle, M.S. The effects of constant and fluctuating temperatures on development of Diaphorina citri (Hemiptera: Liviidae), the Asian citrus psyllid. J. Econ. Entomol. 2020, 113, 633–645.
  66. Ahmad, R. Citrus psylla: Its damage, population and efficacy of some insecticides against it. Pak. J. Sci. 1961, 13, 195–200.
  67. Pande, Y.D. Biology of citrus psylla, Diaphorina citri Kuw. (Hemiptera: Psyllidae). Israel J. Ent. 1971, 6, 307–311.
  68. Huang, B. Citrus psyllid. In Chinese Agricultural Encyclopedia, Insect Volume Insect; Wu, Z.F., Tan, J.J., Li, C.Y., Chen, C.M., Zhang, S.M., Cao, C.Y., Eds.; Agriculture Press: Beijing, China, 1990; pp. 119–120.
  69. Tsai, J.H.; Liu, Y.H. Biology of Diaphorina citri (Homoptera: Psyllidae) on four host plants. J. Econ. Entomol. 2000, 93, 1721–1725.
  70. Om, N.; Beattie, G.A.C.; Donovan, N.J.; Holford, P. Raw Data on the Development of Diaphorina communis on Mandarin and Curry Leaf under Field and Laboratory Conditions in 2014. Figshare. 2021. Dataset. Available online: https://figshare.com/articles/dataset/Raw_data_on_the_development_of_Diaphorina_communis_on_mandarin_and_curry_leaf_under_field_and_laboratory_conditions_in_2014/14603883 (accessed on 14 January 2022).
  71. Om, N. The Roles of Psyllids, Host Plants and Environment in the Aetiology of Huanglongbing in Bhutan. Ph.D. Thesis, Western Sydney University, Penrith, NSW, Australia, 2022.
  72. Beattie, G.A.C.; Holford, P. Can Oecophylla smaragdina be used to suppress incidence of CVPD in citrus orchards in Indonesia? 1st International Conference on Agriculture, Food, and Environment 2021. IOP Conf. Ser. Earth Environ. Sci. 2022, 1018, 012030.
  73. Nguyen, T.T.C. Một số kết quả nghiên cứu về sự liên hệ giữa kiến vàng Oecophylla smaragdina và bệnh greening trên cam quýt . Plant Prot. Bull. Vietnam 1995, 6, 16–19.
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