Diaphorina citri (Asian citrus psyllid)

Pictures

Picture	Title	Caption	Copyright
Title Adult, museum set specimen Caption Diaphorina citri (Asiatic citrus psyllid); adult, museum set specimen. East Timor KAB DILI, ex. sweeping Fortunella japonica. 30 January, 2000. Adults 3-4 mm long, body brown mottled, head light brown. Forewing broadest apical half, mottled with brown band extending around periphery of outer half of wing, the band slightly interrupted near apex. Antennae with black tip and two small light brown spots on middle segments. Living insect covered with whitish, waxy, secretion, making it appear dusty. Copyright ©K. Walker-2005/PaDIL- CC BY 3.0 AU	Adult, museum set specimen	Diaphorina citri (Asiatic citrus psyllid); adult, museum set specimen. East Timor KAB DILI, ex. sweeping Fortunella japonica. 30 January, 2000. Adults 3-4 mm long, body brown mottled, head light brown. Forewing broadest apical half, mottled with brown band extending around periphery of outer half of wing, the band slightly interrupted near apex. Antennae with black tip and two small light brown spots on middle segments. Living insect covered with whitish, waxy, secretion, making it appear dusty.	©K. Walker-2005/PaDIL- CC BY 3.0 AU
Title Eggs Caption Diaphorina citri (Asiatic citrus psyllid); eggs, are orange-coloured and almond-shaped; 0.01-0.15 mm. Copyright ©Ching-Chin Chien	Eggs	Diaphorina citri (Asiatic citrus psyllid); eggs, are orange-coloured and almond-shaped; 0.01-0.15 mm.	©Ching-Chin Chien
Title Nymphs Caption Diaphorina citri (Asiatic citrus psyllid); 5th instar nymphs. Nymphs are light-yellow to dark-brown, bearing well-developed wing pads. Copyright ©Ching-Chin Chien	Nymphs	Diaphorina citri (Asiatic citrus psyllid); 5th instar nymphs. Nymphs are light-yellow to dark-brown, bearing well-developed wing pads.	©Ching-Chin Chien
Title Natural enemy Caption Diaphorencyrtus diaphorinae (Hymenoptera: Encyrtidae); parasitizing Diaphorina citri (Asiatic citrus psyllid). Copyright ©Ching-Chin Chien	Natural enemy	Diaphorencyrtus diaphorinae (Hymenoptera: Encyrtidae); parasitizing Diaphorina citri (Asiatic citrus psyllid).	©Ching-Chin Chien

Identity

Preferred Scientific Name

• Diaphorina citri Kuwayama

Preferred Common Name

• Asian citrus psyllid

Other Scientific Names

• Euphalerus citri

International Common Names

• English: citrus psylla (Asian)
• Spanish: psila de los cítricos
• French: psylle de l'oranger
• Chinese: ganju musi
• Portuguese: psilideo da l'aranjeira

Local Common Names

• Germany: Suedostasiatischer Citrus-Blattfloh

EPPO code

• DIAACI (Diaphorina citri)

Taxonomic Tree

• Domain: Eukaryota
•     Kingdom: Metazoa
•         Phylum: Arthropoda
•             Subphylum: Uniramia
•                 Class: Insecta
•                     Order: Hemiptera
•                         Suborder: Sternorrhyncha
•                             Unknown: Psylloidea
•                                 Family: Psyllidae
•                                     Genus: Diaphorina
•                                         Species: Diaphorina citri

Description

Eggs

The egg of D. citri is anchored on a slender, stock-like process arising from the plant tissue. It is elongate with a broad basal end and tapering towards its distal and curved end. The average size of the egg measures 0.31 mm long and 0.14 mm wide. Freshly deposited eggs are light yellow, and turn bright orange with two distinct red eye spots at maturity.

Nymph

The average size of first-instar nymphs is 0.30 mm long and 0.17 mm wide. The nymphs have a light pink body and a pair of red compound eyes. Second-instar nymphs are on average 0.45 mm long and 0.25 mm wide. The rudimentary wing pads are visible on the dorsum of the thorax. The average size of third-instar nymphs is 0.74 mm long and 0.43 mm wide. The wing pads are well developed and the segmentation of antenna is evident. The fourth-instar nymphs average 1.01 mm long and 0.70 mm wide. The wing pads are well developed; the mesothoracic wing pads extend towards the one-third of compound eyes and the metathoracic wing pads extend to the third abdominal segment. The fifth-instar nymphs average 1.60 mm long and 1.02 mm wide. The mesothoracic wing pads extend towards the front of the compound eyes; the metathoracic wing pads extend to the fourth abdominal segment. In some mature nymphs, the abdomen turns bluish-green instead of pale orange (Tsai and Liu, 2000).

Adult

The adult is 2.5 mm long, body yellowish-brown, legs greyish-brown. Wings are transparent with white spots or light-brown with a broad, beige, longitudinal band in the centre. Mathur (1975) gives a key to the Indian species of Diaphorina, and a detailed description of the adult. The average size of adult females is 3.3 mm long and 1 mm wide; the mean size of of adult males is 2.7 mm long and 0.8 mm wide (Tsai and Liu, 2000).

Distribution

The distribution of D. citri is wider than that of the citrus huanglongbing (greening) bacterium Liberibacter asiaticus, the major pathogen which it transmits (EPPO/CABI, 1996a): D. citri occurs in Afghanistan, Macau and Singapore where the bacterium has not been recorded.

See also CABI/EPPO (1998, No. 64).

Distribution Table

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Risk of Introduction

Like the other vector of citrus greening (Trioza erytreae; EPPO/CABI, 1996b), D. citri is listed as an A1 quarantine pest by EPPO (OEPP/EPPO, 1988) and is also a quarantine pest for CPPC and OIRSA. Besides its role in citrus huanglongbing (greening), this psyllid has significant damage potential in itself. Though biological control may be possible, there is no guarantee that it could keep populations to a sufficiently low level to prevent transmission of huanglongbing.

Hosts/Species Affected

D. citri is confined to the Rutaceae, occurring on wild hosts as well as on Citrus, especially lemons (C. limon), rough lemon (C. jambhuri), sour orange (C. aurantium), grapefruit (C. paradisi) and limes (C. aurantiifolia). Murraya paniculata, a rutaceous plant often used for hedges, is a preferred host; M. koenigii is a host in India and Sri Lanka.

Sétamou et al. (2016) observed that some native North American rutaceous plants can serve as host plants for D. citri, thus affecting the population dynamics of the pest and the epidemiology of Huanglongbing,

Host Plants and Other Plants Affected

Growth Stages

Symptoms

D. citri stunts and twists young shoots, so that the growing tips present a rosetted appearance. Leaves are badly curled, and may be covered with honeydew and sooty mould; leaves drop prematurely.

List of Symptoms/Signs

Species Vectored

Biology and Ecology

D. citri has a short life cycle and high fecundity (Catling, 1970). It is more prevalent in hot coastal areas. Pairing starts soon after emergence, the insects being most active during March-April in India (Pande, 1971) and May-June in the Philippines (Catling, 1970) and June-July in Brazil (Yamamoto et al., 2001). The host plants (C. jambhiri, C. aurantium, C. paradisi and M. paniculata) on which they were reared had no significant effect on the immature survival and developmental periods or on adult longevity. However, the mean number of eggs laid per female on grapefruit (858 eggs) was significantly more than on other hosts (Tsai and Liu, 2000). Gravid females of D. citri oviposit within 2-cm lengths of the terminal tissue in leaf folds, on petioles, axillary buds, upper and lower surfaces of young leaves and tender stems. The average incubation period of eggs on these four host plants at 25°C is essentially the same, ranging from 4.1 to 4.3 days. All nymphs reared on the four host plants undergo four moults. First- and second-instar nymphs mostly aggregate and feed inside the folded leaves, on the terminal stem and between the axillary bud and the stem of tender shoots. Young nymphs are quite docile and move only when disturbed or over-crowded. The nymphs continuously secrete copious amounts of honeydew from the anus and a thread-like waxy substance from the circumanal glands resulting in the growth of black sooty mould on the lower leaves. The average combined developmental periods for the five nymphal stages are 12.8, 12.6, 13.5 and 13.1 days on orange jessamine, grapefruit, rough lemon and sour orange, respectively.

Adults of D. citri are often found resting on the terminal portion of plant, especially on the lower side of the leaves with their heads either pointing upward or downward to the leaf surface at an angle of 30°. When disturbed they readily take flight for a short distance. The females only oviposit on the tender shoots. In the absence of suitable host tissue, oviposition ceases temporarily. The longest female longevity of D. citri reared on grapefruit, orange jessamine, sour orange and rough lemon at 25°C is 54, 54, 60 and 66 days, respectively (Tsai and Liu, 2000).

In an insectary, at 10, 15, 20, 25, 28 and 33°C, the psyllid populations reared at 10 and 33°C failed to develop. Between 15 and 30°C, the mean developmental period from egg to adult varied from 49.3 days at 15°C to 14.1 days at 28°C. The low-temperature developmental thresholds for the first to fifth instars were estimated at 11.7, 10.7, 10.1, 10.5 and 10.9°C, respectively. The survival of the third to fifth nymphal instars at 15-28°C was essentially the same. The mean longevity of females increased with decreasing temperature within the range 15-30°C. The maximal longevity of individual females was recorded as 117, 60, 56, 52 and 51 days at 15, 20, 25, 28 and 30°C, respectively. The average number of eggs produced per female significantly increased with increasing temperature and reached a maximum of 748.3 eggs at 28°C. The optimum range of temperatures for population growth of D. citri is 25-28°C (Liu and Tsai, 2000). During dry periods, adults are numerous, but nymphs are usually absent. The complete life cycle thus takes 14-48 days, with up to 10 overlapping generations per year. The adults overwinter and can live for up to 6 months. Population fluctuations are closely correlated with the flushing rhythm of citrus trees, as eggs are laid exclusively on young flush points. In southern Florida, USA, D. citri populations occur throughout the seasons on orange jassamine but there are population peaks in October-November, December, May and August, which are positively related to the weekly minimum temperature and rainfall (Tsai et al., 2002).

Yang (1989) carried out an investigation on the effects of light, temperature and humidity on development, production and survival of D. citri. Xu et al. (1994) reported on the longevity of nymphs and adults in Fujian province, China, and recorded that nymphs were killed by temperatures of -1°C and adults by -10°C.

D. citri transmits the Asian form of citrus huanglongbing (greening) disease, Liberibacter asiaticus, under natural conditions in Asia (including Saudi Arabia) (Capoor et al., 1967). It has been shown experimentally that D. citri is also able to transmit the African form, Liberibacter africanus (Lallemand et al., 1986). In Mauritius and Réunion, where both forms occur, D. citri probably transmits both. However, L. asiaticus is not transmitted transovarially by D. citri (Chen, 1998).

D. citri is normally spread only locally by natural dispersal. Citrus material (budwood, grafted trees, rootstock seedlings) from infected areas can carry eggs and/or nymphs over longer distances. Such fifth- or sixth-instar nymphs, as well as the adults born from these nymphs, are capable of transmitting the huanglongbing agent to citrus. This is probably the way in which Liberibacter asiaticum was introduced into Saudi Arabia. The rutaceous plant Murraya paniculata, frequently used as an ornamental bush or hedge, is one of the best hosts of D. citri. Although this plant is not a host for L. asiaticus (Hung et al., 2000), it can carry eggs or nymphs of the vector and its introduction to disease- and vector-free regions could therefore be dangerous. Entry on citrus fruits is extremely unlikely.

Natural enemies

Notes on Natural Enemies

In its native range in southern Asia, D. citri is suppressed by a complex of parasitoids including Tamarixia radiata and Diaphorencyrtus species. T. radiata was introduced into Réunion Island in 1978 and later into Mauritius. On both islands it gave satisfactory control of the pest and suppressed transmission of huanglongbing (greening) disease. Predatory Coccinellidae and Anthocoridae are also recorded from Asia, but most of them have little impact, although Chilocorus nigritus is beneficial in supplementing the action of parasitoids. Aubert (1987) reviewed the natural enemies and concluded that T. radiata is able to control D. citri and prevent transmission of huanglongbing disease when it is free of hyperparasites as in Réunion, but when hyperparasitism is high, as in Taiwan, insecticide applications are necessary to achieve control.

Impact

The main economic importance of D. citri is as the vector of the very serious citrus huanglongbing (greening) disease caused by the bacterium Liberibacter asiaticus (EPPO/CABI, 1996a). In addition, D. citri typically causes defoliation and dieback. Serious damage to growing points can occur, which can lead to dwarfing as well as lack of juice and taste in fruit. Heavy D. citri populations can cause blossom and fruitlet drop. The honeydew excreted by D. citri promotes the growth of sooty mould which not only affects the photosynthetic activity of the tree but also attracts ants which fend off natural enemies of D. citri, resulting in additional pest damage.

Prevention and Control

Chemical Control

Dimethoate, pyridaben, chlorpyrifos, imidacloprid and profenofos are used against D. citri in orchards with low infection rates. Dahiya et al. (1994) report on trials on 12 insecticides (organophosphorus compounds and pyrethroids) against D. citri. Chemical control is used for control of the psyllid in citrus orchards in Réunion and mainland China (Aubert and Quilici, 1984; Qian, 1989; Ke, 1991; Xu et al., 1991). Neem oil and petroleum spray oil are also used against D. citri in India and China (Chakravarthi et al., 1998a; Rae et al., 1997).

Biological Control

Tamarixia radiata was imported into Réunion Island from India in 1978 for control of D. citri. It became established and achieved substantial control in the absence of hyperparasitoids. A second imported parasitoid, Diaphorencyrtus aligarhensis, failed to become established (Aubert et al., 1980). T. radiata was imported into Taiwan from Réunion in 1983, released and established. However, it was not so successful - although it is able considerably to reduce psyllid numbers, it did not interrupt transmission of greening disease. It was found that hyperparasitoids, disturbance and inability to attack psyllids settling in buds reduced its impact in citrus orchards. It was concluded that T. radiata did have a beneficial value in preventing migration of psyllids from hedges of jasmine orange (Murraya paniculata) into citrus orchards, but that in these orchards, where insecticides are applied to control other pests, chemical control is the only effective remedy (Chien and Chu, 1997). Other members of Syrphidae and Coccinellidae have been reported to feed on D. citri. In Saudi Arabia, T. radiata is present but does not keep D. citri populations down to a low level.

Phytosanitary Control

EPPO recommends (OEPP/EPPO, 1990) that importation of plants for planting and cut branches of citrus from countries where Liberibacter asiaticus or L. africanus (the agents of citrus huanglongbing (greening) disease), or either of its vectors occur, should be prohibited. It is possible to fumigate citrus budwood material against D. citri (FAO, l983).

Resistant Cultivars

There is limited information available on host-plant resistance to D. citri; 13 citrus cultivars are reported to be highly resistant (Chakravarthi et al., 1998b).

References

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