Publication #EENY-033
Asian Citrus Psyllid, Diaphorina citri Kuwayama (Insecta: Hemiptera: Psyllidae)1
Introduction
The Asiatic or oriental citrus psyllid, Diaphorina citri, Kuwayama, is widely distributed in southern Asia. It is an important pest of citrus in several countries, particularly India, where there has been a serious decline of citrus in recent years. This psyllid did not occur in North America or Hawaii but was reported in Brazil, by Costa Lima (1942; Rio de Janeiro) and Catling (1970). However, in June 1998, the insect was detected in Florida, distributed along Highway 1 on the east coast of Florida, from Broward to St. Lucie counties and was apparently limited to dooryard host plantings at the time of its discovery. By September 2000, this pest had spread to 31 counties in Florida (Halbert 2001). D. citri, and one of its parasites, is also present in the Rio Grande Valley of Texas. Both species appear to have been accidentally introduced in the spring of 2001 on potted Murraya originating in Florida (Michaud). D. citri often has been referred to as "citrus psylla", but this is the same common name often applied to Trioza erytreae (Del Guercio), the psyllid pest of citrus in Africa. T. erytreae, to avoid confusion, should be referred to as the African citrus psyllid or the two-spotted citrus psyllid (the latter name in reference to a pair of spots on the base of the abdomen in late stage nymphs). These two psyllids are the only known vectors of the etiologic agent of citrus greening disease and are the only economic species on citrus in the world. Three other species of Diaphorina have been reported on citrus (two in Swaziland, one in India), but these are non-vector species of relatively little importance. Description and Identification
Adults
3 to 4 mm long; body brown mottled; head light brown (black in Trioza erytreae); forewing broadest apical half, mottled, and with brown band extending around periphery of outer half of wing, the band slightly interrupted near apex (broadest at middle, unspotted, and transparent in T. erytreae); antennae with black tip and two small light brown spots on middle segments (nearly all black in T. erytreae); living insect covered with whitish, waxy secretion, making it appear dusty. Figure 1. Adult Asiatic or oriental citrus psyllid, Diaphorina citri, Kuwayama.
Nymphs
0.25 mm long in 1st instar, 1.5 to 1.7 mm in last (5th) instar; color generally yellowish orange; no abdominal spots (advanced nymphs of T. erytreae with two basal dark abdominal spots); wing pads massive (small pads in T. erytreae); large filaments confined to apical plate of abdomen (T. erytreae with fringe of fine white filaments around whole body, including head). Figure 2. Nymph of the Asiatic or oriental citrus psyllid, Diaphorina citri, Kuwayama.
Figure 3. The white waxy excretions of the nymphs are an indicator of the Asiatic or oriental citrus psyllid, Diaphorina citri, Kuwayama.
Eggs
Approximately 0.3 mm long, elongate, almond-shaped, thicker at base, and tapering toward distal end; fresh eggs pale, but then turning yellow and finally orange at time of hatching; eggs placed on plant tissue with long axis vertical to surface (long axis horizontal to surface in T. erytreae). Figure 4. Eggs of the Asiatic or oriental citrus psyllid, Diaphorina citri, Kuwayama.
Figure 5. Adult female and nymphal instars of Asiatic citrus psyllid.
Life History
Eggs are laid on tips of growing shoots on and between unfurling leaves. Females may lay more than 800 eggs during their lives. Nymphs pass through five instars. Total life cycle requires from 15 to 47 days, depending upon the season. Adults may live for several months. There is no diapause but populations are low in winter (the dry season). There are 9 to 10 generations a year; 16 have been observed in field cages. Numerous papers have appeared containing life history information, among them the following: Atwal et al. (1970), Capoor et al. (1974), Catling (1970), Husain & Nath (1927), Mangat (1961), Mathur (1975), Pande (1971), USDA, ARS (1959), and Wooler et al. (1974). Damage
Injury caused by psyllids results from the withdrawal of large quantities of sap from the foliage, and transmission of the organisms that cause greening disease. The once flourishing citrus industry in India is slowly being wiped out by dieback. The once flourishing citrus industry in India is slowly being wiped out by dieback. This dieback has multiple causes but primarily it is due to greening disease. What is now generally accepted as greening disease has been called citrus chlorosis in Java, leaf-mottling and leaf-mottle yellows in the Philippines, likubin (rapid decline) in Taiwan, and huang long bing (yellow dragon disease) in China. Figure 6. Feeding damage caused by the Asiatic or oriental citrus psyllid, Diaphorina citri, Kuwayama, to citrus foliage.
Host Plants
Mainly Citrus spp., at least two species of Murraya, and at least three other genera all in Rutaceae. Distribution
D. citri ranges primarily in tropical and subtropical Asia and has been reported from the following geographical areas: China, India, Myanmar, Taiwan, Philippine Islands, Malaysia, Indonesia, Sri Lanka, Pakistan, Thailand, Nepal, Cecum, Hong Kong, Ryukyu Islands, Afghanistan, Saudi Arabia, Reunion, Mauritius, and Brazil. The discovery of D. citri in Saudi Arabia (Wooler et al., 1974) is the first record from the Near East. T. erytreae also occurs in Saudi Arabia, preferring the eastern and highland areas where the extremes of climate are present, whereas D. citri is widespread in the western, more equitable coastal areas. Survey and Detection
Nymphs, which are always found on new growth, move in a slow, steady manner when disturbed. The adults leap when disturbed and may fly a short distance. They are usually found in large numbers on the lower sides of the leaves with heads almost touching the surface and the body raised almost to a 30 degree angle. The period of greatest activity of the psyllid corresponds with the periods of new growth of citrus. There are no galls or pits formed on the leaves as caused by many other kinds of psyllids; the nymphs are completely exposed (the nymphs of T. erytreae are partially enclosed in a pit). Citrus trees in advanced stages of decline are somewhat similar to those affected by tristeza. Field recognition of greening in Asia from symptoms alone is often difficult. Very similar leaf symptoms may be caused by a wide variety of factors varying from nutritional disorders to the presence of other diseases such as root rots and gummosis, tristeza, and exocortis. Capoor et al. (1974) described greening symptoms of citrus as trees showing stunted growth, sparsely foliated branches, unseasonal bloom, leaf and fruit drop, and twig dieback. Young leaves are chlorotic, with green banding along the major veins. Mature leaves have yellowish-green patches between veins, and midribs are yellow. In severe cases, leaves become chlorotic and have scattered spots of green. Fruits on greened trees are small, generally lopsided, underdeveloped, unevenly colored, hard, and poor in juice. The columella was found to be almost always curved in sweet orange fruits and apparently the most reliable diagnostic symptom of greening. Most seeds in diseased fruits are small and dark colored. Schwarz et al. (1974) listed 4 reasons why the symptoms of greening in Southeast Asia were often different from those in South Africa. These reasons included the more tropical climate of Asia keeping mature fruit green, citrus variety differences, differences in the heat tolerance of the vectors leading to different disease distribution in the grove, and differences in the virulence of the strains of the pathogen. Disease Transmission
Capoor et al. (1974) reported a high percentage of transmission by tissue grafts. They found that 4th and 5th instar nymphs and adults could effect transmission. D. citri requires an incubation period of about 21 days in which to transmit the pathogen, which it retains for life following a short access feeding (15 to 30 minutes) on a diseased plant. It is unnecessary for adult psyllids arising from infectious nymphs to have access feeding on diseased shoots in order to become vectors. Adult psyllids were able to transmit greening in a minimum infection feeding of 15 minutes but the percentage of transmission was low. One hundred percent infection was obtained when the psyllids fed for one hour or more. Capoor et al. (1974) strongly indicated that the pathogen multiplied in the body of the psyllid and that there was an absence of transovarial transmission. They summarized differences between D. citri and Trioza erytreae in various aspects of greening transmission. Moll and van Vuuren (1977, p. 38) concluded that the greening causal agent most closely resembles a gram-negative bacterium under the electron microscope. They designated the pathogen as a bacterium-like organism. Figure 7. Symptoms of greening disease, Liberobacter spp, on citrus.
Management
Many workers in India have reported that D. citri can be controlled effectively with a wide range of modern insecticides. Bindra et al. (1974) reported that for overall effectiveness against nymphs and adults at different intervals after spraying several chemicals were effective. Injection of trees with tetracycline antibiotics to control greening disease has been effective where the vector can be kept under control. In countries where greening has spread over long distances, it has occurred because of the movement of infected and infested nursery stock; only clean and healthy plants should be transported. In areas of low incidence of greening, the relatively few infected trees should be removed to prevent them from being reservoirs of the pathogen. Tests in India by Raychaudhuri et al. (1974) showed that the greening organisms of infected budwood could be deactivated by either hot (moist) air, hot water, or 21 days in the heat therapy chamber. Natural enemies of D. citri include syrphids, chrysopids, at least 12 species of coccinellids, and several species of parasitic wasps, the most important of which is Tamarixia radiata (Waterston). T. radiata was introduced in Florida (intentionally) and the Rio Grande Valley of Texas (accidentally) (Michaud). Figure 8. Nymphs of the Asiatic or oriental citrus psyllid, Diaphorina citri, Kuwayama, killed by the ectoparasitoid wasp Tamarixia radiata.
Selected References
Anonymous. 2005. Citrus Greening. FDACS-Division of Plant Industry. http://www. doacs.state.fl.us/pi/chrp/greening/citrusgreening.html (7 April 2006). Anonymous. 2006. Huanglongbing / Citrus Greening (Liberibacter asiaticus). Southern Pant Diagnostic Network. http://spdn.ifas.ufl.edu/Citrus% 20_Greening.htm (7 April 2006). Atwal AS, Chaudhary JP, Ramzan M. 1970. Studies on the development and field population of citrus psylla, Diaphorina citri Kuwayama (Psyllidae: Homoptera). Journal of Research Punjab Agricultural University 7: 333-338. Bindra OS, Sohi BS, Batra RC. 1974. Note on the comparative efficacy of some contact and systemic insecticides for the control of citrus psylla in Punjab. Indian Journal of Agricultural Science 43: 1087-1088. Capoor SP, Rao DG, Viswanath SM. 1974. Greening disease of citrus in the Deccan Trap Country and its relationship with the vector, Diaphorina citri Kuwayama. p. 43-49. In Weathers LG, Cohen M (ed.) Proceedings of the 6th Conference of the International Citrus Virology, University of California, Division of Agricultural Sciences. Catling HD. 1970. Distribution of the psyllid vectors of citrus greening disease, with notes on the biology and bionomics of Diaphorina citri. FAO Plant Protection Bulletin 18: 8-15. Costa Lima AM. da. 1942. Homopteros. Insetos do Brazil 3: 1-327. Esc. Na. Agron. Min. Agr. Culbert D. (2006). Citrus Greening – Another Threat to Agriculture. http://okeechobee.ifas.ufl. edu/News%20columns/Citrus%20Greening% 20Disease.htm (7 April 2006). Halbert SE. (March 2006). Asian citrus psyllid - A serious exotic pest of Florida citrus. http://www. doacs.state.fl.us/pi/enpp/ento/dcitri.htm (7 April 2006). Halbert SE, Sun X, Dixon W. (January 2001). Asian citrus psyllid update. http://doacs.state.fl.us/ pi/enpp/ento/asian-citrus-psyllid.htm (14 October 2002). Halbert SE, Núñezb CA. 2004. Distribution of the Asian citrus psyllid, Diaphorina citri Kumayama (Rhynchota: Psyllidae), in the Caribbean Bason. Florida Entomologist 87: 401–402. Hoy MA, Nguyen R. (June 1998). Citrus psylla: here in Florida - an action plan. Pest Alert. http://pestalert.ifas.ufl.edu/hoy-0615.htm (June 1998). Hoy MA, Nguyen R. (April 2000). Classical biological control of Asian citrus psylla - update on Tamarixia radiata releases and first releases of Diaphorencyrtus aligarhensis. Florida IPM. http://ipm.ifas.ufl.edu/ipm2/agricultural/fruit/citrus/Asp_hoy2.htm (30 December 2003). Hoy MA, Nguyen R, Jeyaprakash A. (1999). Classical biological control of Asian citrus psyllid in Florida. Florida IPM. http://ipm.ifas.ufl.edu/ipm2/ agricultural/fruit/ citrus/citrus_psyllid.htm (30 December 2003). Husain MA, Nath D. 1927. The citrus psylla (Diaphorina citri, Kuw.) (Psyllidae: Homoptera) Memoirs of the Department of Agriculture India 10: 1-27. Knapp JL, Halbert SE, Lee R, Hoy MA, Clark R, Kesinger M. (Unknown). The Asian Citrus Psyllid and Citrus Greening Disease. Florida IPM. http://ipm.ifas.ufl.edu/agricultural/fruit/citrus/ASP-hoy.htm. (23 December 2006). Mangat BS. 1961. Citrus psylla (Diaphorina citri Kuway) and how to control it. Citrus Industry 42: 20. Mathur RN. 1975. Psyllidae of the Indian subcontinent. Indian Council of Agricultural Research, New Delhi. 429 p. Michaud JP. Personal communication. (19 October 2002). Miyakawa T, Tanaka H, Matsui C. 1974. Studies on citrus greening disease in southern Japan. p. 40-42 In Weathers LG, Cohen M (ed.) Proceedings of the 6th Conference of the International Citrus Virology, University of California, Division of Agricultural Sciences. Moll JN, van Vuuren SP. 1977. Greening disease in Africa. 1977 International Citrus Congress, Orlando, Florida, Program and Abstracts. 95 p. Pande YD. 1971. Biology of citrus psylla, Diaphorina citri Kuw. (Hemiptera: Psyllidae). Israel Journal of Entomology 6: 307-310. Raychaudhuri SP, Nariani, Ghosh SK, Viswanath SM, Kumar D. 1974. Recent studies on citrus greening in India. p. 53-57 In Weathers LG, Cohen M (Ed.) Proceedings of the 6th Conference of the International Citrus Virology, University of California, Division of Agricultural Sciences. Rogers ME, Stansly PA. 200). Biology and management of the Asian citrus psyllid, Diaphorina citri Kuwayama, in Florida Citrus. EDIS. ENY-739. http://edis.ifas.ufl.edu/IN668 (23 May 2007). Schwarz RE, Knorr LC, Prommintara M. 1974. Citrus greening disease in Thailand FAO Technical Document No. 93: 1-14. United States Department Agriculture, Agricultural Research Service. 1959. Insects not known to occur in the United States. Citrus psylla (Diaphorina citri Kuwayama). No. 88 of Series. Cooperative Economic Insect Report 9: 593-594. Wooler A, Padgham D, Arafat A. 1974. Outbreaks and new records. Saudi Arabia. Diaphorina citri on citrus. FAO Plant Protection Bulletin 22: 93-94. Footnotes
1. This document is EENY-033 (IN160), one of a series of Featured Creatures from the Entomology and Nematology Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida. Published: June, 1998. Revised: May 2007. This document is also available on Featured Creatures Website at http://creatures.ifas.ufl.edu. Please visit the EDIS Website at http://edis.ifas.ufl.edu.
2. F. W. Mead, Entomology and Nematology Department, Division of Plant Industry, Gainesville, FL 32611.The Institute of Food and Agricultural Sciences (IFAS) is an Equal
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