Preferred name: Diaphorina citri
Authority: Kuwayama
Taxonomic position: Animalia: Arthropoda: Hexapoda: Insecta: Hemiptera: Sternorrhyncha: Psyllidae
Other scientific names: Euphalerus citri (Kuwayama)
Common names in English: Asian citrus psyllid, citrus psylla, citrus psyllid
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Notes on taxonomy and nomenclature EPPO Categorization: A1 list
EU Categorization: A1 Quarantine pest (Annex II A)
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EPPO Code: DIAACI

D. citri is confined to Rutaceae, occurring on wild hosts and on cultivated Citrus, especially grapefruit (Citrus paradisi), lemons (C. limon) and limes (C. aurantiifolia). Murraya paniculata, a rutaceous plant often used for hedges, is a preferred host. Within the EPPO region, host species are generally confined to countries surrounding the Mediterranean Sea.

Host list: Aegle marmelos, Afraegle paniculata, Archidendron lucidum, Atalantia buxifolia, Atalantia, Balsamocitrus dawei, Casimiroa edulis, Citroncirus webberi, Citroncirus, Citrus australasica, Citrus australis, Citrus glauca, Citrus halimii, Citrus hassaku, Citrus hystrix, Citrus inodora, Citrus latipes, Citrus maxima, Citrus medica, Citrus reshni, Citrus reticulata, Citrus sunki, Citrus taiwanica, Citrus trifoliata, Citrus webberi, Citrus x amblycarpa, Citrus x aurantiifolia var. macrophylla, Citrus x aurantiifolia, Citrus x aurantium var. paradisi, Citrus x aurantium var. sinensis, Citrus x aurantium, Citrus x limon var. limettioides, Citrus x limon, Citrus x limonia var. jambhiri, Citrus x limonia var. volkameriana, Citrus x limonia, Citrus x nobilis, Citrus, Clausena anisum-olens, Clausena excavata, Clausena harmandiana, Clausena indica, Clausena lansium, Cordia myxa, Ficus carica, Fortunella japonica, Fortunella sp., Fortunella, Glycosmis pentaphylla, Limonia acidissima, Merrillia caloxylon, Murraya koenigii, Murraya paniculata, Rutaceae, Swinglea glutinosa, Triphasia trifolia, Vepris lanceolata, Zanthoxylum ailanthoides, Zanthoxylum asiaticum, x Citrofortunella microcarpa, x Citrofortunella sp.

The distribution of D. citri is wider than that of the causal agent of citrus huanglongbing (HLB) disease originally associated with this vector, 'Candidatus Liberibacter asiaticus'. D. citri occurs in Afghanistan, some states of Brazil, Macau, Myanmar, and Singapore, where the associated bacterium has not yet been recorded.

EPPO Region: Cyprus, Israel
Africa: Benin, Ethiopia, Ghana, Kenya, Mauritius, Nigeria, Reunion, Tanzania
Asia: Afghanistan, Bangladesh, Bhutan, Cambodia, China (Aomen (Macau), Fujian, Guangdong, Guangxi, Guizhou, Hainan, Henan, Hunan, Jiangxi, Sichuan, Xianggang (Hong Kong), Yunnan, Zhejiang), East Timor, India (Andhra Pradesh, Arunachal Pradesh, Assam, Bihar, Delhi, Gujarat, Haryana, Himachal Pradesh, Jammu & Kashmir, Karnataka, Kerala, Lakshadweep, Madhya Pradesh, Maharashtra, Manipur, Meghalaya, Punjab, Rajasthan, Sikkim, Tamil Nadu, Telangana, Tripura, Uttar Pradesh, West Bengal), Indonesia (Java, Maluku, Nusa Tenggara, Sumatra), Iran, Israel, Japan (Kyushu, Ryukyu Archipelago), Laos, Malaysia (Sabah, Sarawak, West), Maldives, Myanmar, Nepal, Oman, Pakistan, Philippines, Saudi Arabia, Singapore, Sri Lanka, Taiwan, Thailand, United Arab Emirates, Vietnam, Yemen
North America: Mexico, United States of America (Alabama, Arizona, California, Florida, Georgia, Hawaii, Louisiana, Mississippi, South Carolina, Texas)
Central America and Caribbean: Antigua and Barbuda, Bahamas, Barbados, Belize, Cayman Islands, Costa Rica, Cuba, Dominica, Dominican Republic, Guadeloupe, Haiti, Jamaica, Martinique, Montserrat, Nicaragua, Puerto Rico, Saint Lucia, St Vincent and the Grenadines, Virgin Islands (US)
South America: Argentina, Brazil (Amazonas, Bahia, Ceara, Para, Pernambuco, Rio de Janeiro, Santa Catarina, Sao Paulo), Colombia, French Guiana, Paraguay, Uruguay, Venezuela
Oceania: American Samoa, Guam, Northern Mariana Islands, Papua New Guinea

D. citri has a short life cycle and high fecundity. Its optimal developmental temperature ranges from 25-28°C (Liu and Tsai, 2000), and it is, therefore, best adapted to tropical and subtropical conditions, although mean temperatures above 30°C reduce its survival and fertility. Pairing starts soon after emergence, the insects being most active in spring and summer, once mean temperatures are above 12°C (Udell et al., 2017). Eggs are laid inside half-folded leaves in buds, in leaf axils or other suitable places on the young tender parts of the tree (shoots or flushes). Females have a pre-oviposition period of about 10 days at their optimal temperature, and can lay up to 800 eggs during their lifetime (Liu and Tsai, 2000). Eggs hatch within 3-10 days (3 days at 28°C and 10 days at 15°C) and nymphs pass through five instars in 11-40 days. The complete life cycle takes 14-50 days, with up to 9-14 overlapping generations per year at mean temperatures of 20-25°C. However, as the eggs are laid exclusively on young flushes and nymphs can only develop on tender plant tissue, the number of generations per year is limited by the sprouting activity of citrus trees, and population fluctuations are closely correlated with tree phenology during the growing season (Udell et al., 2017). D. citri overwinters as an adult, which can live for up to six months. Adults are highly active and jump at the slightest disturbance. Nymphs will move away when disturbed, but normally lead a sedentary existence, clustered in groups.

D. citri is known to be the most efficient vector of 'Ca. Liberibacter asiaticus', the most aggressive causal agent of huanglongbing disease. Together, these two organisms constitute the most destructive citrus pathosystem worldwide (Gottwald, 2010). D. citri can also transmit ‘Candidatus Liberibacter africanus’ and ‘Candidatus Liberibacter americanus’. In areas in which these three bacteria species coexist, D. citri can transmit them indiscriminately (Ajene et al., 2020; Gottwald, 2010).

Symptoms

High densities of D. citri nymphs feeding on tender shoots can stunt and twist them. Lateral leaf notching is a characteristic form of damage associated with this insect (Aubert, 1987). However, at low insect densities, this symptom may go unnoticed. Both adults and immature insects secrete a semi-solid honeydew. Sooty mold may occur in the presence of high psyllid densities and humid environmental conditions. 

Morphology

Eggs

Yellow, almond-shaped and tapering at the distal end; 0.01-0.15 mm.

Nymph

Light-yellow to dark-brown or green, bearing well-developed wing pods.

Adult

Adults are about 2-4 mm long, with a yellowish-brown body, greenish-brown or pinkish-brown abdomen, and greyish-brown legs. Males are smaller than females. The wings are transparent, mottled with white and brown spots and a broad, beige, band is present at the periphery of the distal part, slightly interrupted near the apex. The terminal segments of the antennae are black. Two darker segments are also found in the middle of the antennae.

The EPPO Diagnostic Protocol on D. citri provides guidance on how to detect and identify the pest (EPPO Standard PM 7/52).

Detection and inspection methods

Several sampling methods have been proposed and tested for the detection and monitoring of D. citri. The sampling methods recommended depend on the goals of the monitoring program. For early detection, suction sampling devices for the capture of adults, and yellow sticky traps are mostly recommended. For regular D. citri management actions, the stem tap sampling of adults provides reliable information rapidly. The visual sampling of nymphs in tender shoots during the major citrus sprouting periods of the tree growing season is recommended for determinations of the number of D. citri generations (Monzo and Stansly, 2020). Detailed protocols for surveillance, sampling and detection are indicated in the EPPO Standard PM 9/27 (2020) and in the EFSA pest survey card (EFSA, 2019).

D. citri has a substantial flight capacity. It can disperse locally over distances of at least 2 km, within 12 days, when food and oviposition resources (tender citrus shoots) are scarce (Lewis-Rosenblum et al., 2015). Eggs and nymphs can be carried over longer distances on citrus material (budwood, grafted trees, rootstock seedlings) from infected areas. Trailers transporting oranges from groves to packing houses have also been recognized as a source of adult vector dispersal (Halbert et al. 2010). Adults and, 5th or 6th-instar nymphs can transmit 'Ca. Liberibacter asiaticus' to citrus plants. However, cleaned fruit, that has been washed and is without leaves at the end of the packing process is not considered to pose a risk. The rutaceous plant Murraya paniculata, frequently used as an ornamental bush or hedge, is one of the preferred hosts of D. citri. This plant can carry D. citri eggs or nymphs, and its introduction into disease- and vector-free regions creates a risk of introduction of huanglongbing or its vector.

Economic impact

The economic impact of D. citri results principally from its role as a vector of huanglongbing, the most damaging citrus disease in the world (Gottwald, 2010). The presence of this pathosystem systematically drastically affects the citrus industry (Hodges and Spreens, 2012), and significantly impairs integrated pest management strategies (Grafton-Cardwell et al., 2013). This pathosystem greatly decreases tree productivity, increases management costs considerably, and may also have deleterious effects on fruit quality (Tansey et al., 2017). Intensive management programs for this pathosystem also have a negative impact on biological control processes for this crop, with important economic consequences (Monzo and Stanlsy, 2020a). In addition, direct feeding by D. citri causes leaf curling and notching. Under heavy infestations, sprouting shoots die, resulting in blossom and fruitlet drop.  

Control

There are no curative treatments for huanglongbing, and there are no tolerant or resistant plants. The management of this pathosystem is therefore entirely dependent on efficient vector control (Grafton-Cardwell et al., 2013). Insecticide-based strategies are the most effective, but must be compatible with biological control (Monzo et al., 2014; Qureshi et al., 2009). Broad-spectrum insecticide use in the winter is recommended, as only adult psyllids are found on citrus plants at this time of the year (Qureshi and Stansly, 2010). More selective active ingredients must be used during the tree growing season, when biological control is more relevant (Monzo et al., 2014; Qureshi and Stansly, 2009). Due to the high frequency of insecticide applications against this vector in huanglongbing management programs, the rotation of modes of action is essential, to reduce the risk of resistance (Tiwari et al., 2011). Economic thresholds have also been proposed, for spraying based on D. citri abundance, as a means of reducing the number of applications (Monzo and Stansly 2017). Biological control alone is not sufficient to prevent the spread of huanglongbing, but it can help to reduce the frequency of applications in commercial groves and is the most efficient management strategy for citrus trees in non-commercial citrus growing areas, such as those in urban gardens (Kistner et al. 2016; Monzo and Stansly, 2020a). The parasitoid Tamarixia radiata has been introduced into several citrus-growing regions worldwide, with various degrees of success (Chen and Stansly, 2014). Conservation biological control of naturally occurring predators can also greatly reduce the size of D. citri populations during the citrus growing season (Qureshi and Stansly, 2009; Monzo et al. 2014).

Phytosanitary risk

D. citri could probably establish itself and spread in Mediterranean countries without difficulty. The presence of D. citri would greatly increase the risk of introduction and spread of huanglongbing. However, in addition to its role in spreading huanglongbing, this psyllid has a significant potential for damage in its own right. Biological control may be possible, but there is no guarantee that it could keep populations at sufficiently low levels to prevent transmission of huanglongbing.

Considering the severity of huanglongbing, EPPO has recommended to prohibit the importation of citrus plants for planting and cut branches or buds of citrus from areas or countries where citrus huanglongbing (or either of its vectors) are present. In the EU territory, it is also forbidden to import fruit from third countries with their peduncles and leaves. In disease free countries as those of the Mediterranean area, awareness, monitoring, surveillance, pest risk assessment, quarantine measures and action plans are advised (Duran-Vila et al., 2014; Siverio et al., 2017). Procedures for official control with the aim of detecting, containing and eradicating huanglongbing and its vectors are provided in the EPPO Standard PM 9/27 (EPPO, 2020). As surveys should be carried out in all the EU member countries, a pest survey card was prepared by the European Food Safety Authority (EFSA, 2019) to assist EU Member States in planning their huanglongbing annual survey activities.

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Chen X & Stansly PA (2014) Biology of Tamarixia radiata (Hymenoptera: Eulophidae), parasitoid of the citrus greening disease vector Diaphorina citri (Hemiptera: Psylloidea): a mini review. Florida Entomologist, 97, 1404-1413.

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Lewis-Rosenblum H, Martini X, Tiwari S & Stelinski LL (2015) Seasonal movement patterns and long-range dispersal of Asian citrus psyllid in Florida citrus. Journal of Economic Entomology 108, 3-10.

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Monzo C & Stansly PA (2017) Economic injury levels for Asian citrus psyllid control in process oranges from mature trees with high incidence of huanglongbing. PLoS One, 12. https://doi.org/10.1371/journal.pone.0175333

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Monzo C & Stansly PA (2020b) Sampling and economic thresholds for Asian citrus psyllid. In Asian Citrus Psyllid. Biology, Ecology and Management of the Huanglongbing Vector. JA Qureshi and PA Stansly editors. CABI, 352 pp.

Qureshi JA & Stansly PA (2009) Exclusion techniques reveal significant biotic mortality suffered by Asian citrus psyllid Diaphorina citri (Hemiptera: Psyllidae) populations in Florida citrus. Biological Control 50, 129-136.

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Tansey JA, Vanaclocha P, Monzo C, Jones M & Stansly PA (2017) Costs and benefits of insecticide and foliar nutrient applications to huanglongbing‐infected citrus trees. Pest Management Science 73, 904-916.

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This datasheet was extensively revised in 2020 by Cesar Monzo from Instituto Valenciano de Investigaciones Agrarias (IVIA), Moncada, Valencia, Spain. His valuable contribution is gratefully acknowledged.

EPPO (2024) Diaphorina citri. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-12-22)

This datasheet was first published in the EPPO Bulletin in 1988 and revised in the two editions of 'Quarantine Pests for Europe' in 1992 and 1997 as well as in 2020. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.

CABI/EPPO (1992/1997) Quarantine Pests for Europe (1^st and 2^nd edition). CABI, Wallingford (GB).

EPPO (1988) Data sheets on quarantine organisms No. 151, Citrus greening bacterium and its vectors Diaphorina citri & Trioza erytreae. Bulletin OEPP/EPPO Bulletin 18, 497-507.