Trioza erytreae
(African citrus psyllid)

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Identity

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Preferred Scientific Name

• Trioza erytreae (Del Guercio)

Preferred Common Name

• African citrus psyllid

Other Scientific Names

• Aleurodes erytreae Del Guercio
• Spanioza eritreae Del Guercio
• Spanioza erythreae Del Guercio
• Spanioza erytreae Del Guercio
• Spanioza merwei
• Trioza citri Laing
• Trioza erythreae Del Guercio
• Trioza merwei Pettey

International Common Names

• English: African citrus psylla; African citrus psyllid; citrus psylla (African); two-spotted citrus psyllid
• Spanish: piojillo de los cítricos
• French: chermes des agrumes
• Portuguese: psila africana dos citrinos

Local Common Names

• Germany: ostafrikanischer Zitrusblattfloh

EPPO code

• TRIZER (Trioza erythreae)

Summary of Invasiveness

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The invasive African psyllid, Trioza erytrea, transmits the causal agent of the African form of citrus huanglongbing (greening) disease, Liberibacter africanum, a very destructive disease of citrus plants. It does this under natural conditions in Africa and the Middle East, and has been shown experimentally to transmit the Asian form, Liberibacter asiaticum. The psyllid itself severely distorts leaves, which become stunted and galled. T. erytreae affects species in the family Rutaceae, occurring on wild hosts as well as on Citrus species.

T. erytreae is listed as an A1 quarantine pest by EPPO (OEPP/EPPO, 1988) and is also a quarantine pest for CPPC and OIRSA. The importation of plants for planting and cut branches of citrus from countries where either citrus greening bacterium or either of its vectors occur has been prohibited (OEPP/EPPO, 1990). T. erytreae occurs in Africa and parts of the Middle East but could probably establish and spread in Mediterranean countries without difficulty.

Besides its role in citrus greening, the psyllid has itself significant damage potential.

Taxonomic Tree

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• Domain: Eukaryota
•     Kingdom: Metazoa
•         Phylum: Arthropoda
•             Subphylum: Uniramia
•                 Class: Insecta
•                     Order: Hemiptera
•                         Suborder: Sternorrhyncha
•                             Unknown: Psylloidea
•                                 Family: Triozidae
•                                     Genus: Trioza
•                                         Species: Trioza erytreae

Description

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Orange, cylindrical, with a sharp point anteriorly; laid on leaf margins of young, actively growing foliage.

Nymph

Dorso-ventrally compressed and varying in colour from yellow, olive-green to dark grey; has a marginal fringe of white, waxy filaments; largely sedentary; forms distinct colonies and settles on the underside of young leaves, where, after a few days of feeding, it produces distinctive cup-shaped, open galls.

Adult

Winged, pale and delicate initially, later becoming light brown. Males are smaller than females and have a blunt tip to the abdomen, the latter ending in a sharp point in females. When feeding, adults take up a distinctive stance, with the abdomen raised at an angle of about 35° to the feeding surface.

Distribution

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The distribution of T. erytreae is wider than that of Liberibacter africanum (the African form of citrus huanglongbing (greening) disease), which is the major pathogen it transmits (EPPO/CABI, 1997). It occurs in the Congo Democratic Republic, St. Helena, Sudan, Uganda, Zambia and, recently, Madeira, where the bacterium has not been recorded.

See also CABI/EPPO (1998, No. 151).

Distribution Table

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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

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Like the other vector of citrus greening (Diaphorina citri), T. erytreae is listed as an A1 quarantine pest by EPPO (OEPP/EPPO, 1988) and is also a quarantine pest for CPPC and OIRSA. It is primarily a pest in tropical climates and as such could certainly become established in citrus-growing countries in the Americas and Asia. In Asian countries where the Asian form of citrus huanglongbing (greening) disease is present, its presence could facilitate spread and considerably add to the difficulties of huanglongbing control. It could probably also establish and spread without difficulty in citrus-growing countries with a Mediterranean climate. 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. Besides its role in the spread of citrus huanglongbing disease, the psyllid itself has significant damage potential.

Hosts/Species Affected

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T. erytreae affects species in the family Rutaceae, occurring on wild hosts (e.g. Clausena anisata) as well as on Citrus species.

Host Plants and Other Plants Affected

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Growth Stages

Top of page Vegetative growing stage

Symptoms

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T. erytreae severely distorts leaves, which become stunted and galled, and appear dusted with faecal pellets. Young leaves, especially, may be yellow. The presence of small pit galls on young leaves can indicate T. erytreae (USDA, 2012).

List of Symptoms/Signs

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Species Vectored

Top of page citrus huanglongbing (greening) disease (citrus greening)
Liberibacter africanus (African greening)

Biology and Ecology

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A bibliography of T. erytreae up to 1987 has been compiled by Van den Berg and Fletcher (1988) and a general review has been presented by Van den Berg (1990). T. erytreae has a temperature sensitivity similar to that of Liberibacter africanus (the agent of citrus huanglongbing (greening) in Africa; Schwarz and Green, 1970; Catling, 1973). It is very sensitive to hot, dry weather (the eggs and first-instar nymphs being particularly vulnerable). It is favoured by cooler, moist areas above 500-600 m altitude, where citrus growth flushes tend to be prolonged. Green and Catling (1971) used maximum saturation deficit as an accurate predictor of the geographical distribution of T. erytreae.

Sex ratios fluctuate in the field, but females always predominate. There is a pre-oviposition period of 3-7 days, but this is considerably extended in the absence of young foliage; longevity is also prolonged under such conditions. Mating occurs 2-4 times a day and eggs may be laid immediately. Eggs are supplied with a sharp point that is driven through the leaf epidermis and is thought to be responsible for maintaining a favourable internal water relationship. Females remain fertile for 11-16 days in the absence of males, and maximum egg production occurs towards the middle of their life span, which normally lasts 17-50 days; up to 2000 eggs may be laid per female. There is an incubation period of 6-15 days and nymphal development (five instars) takes 17-43 days, both periods being inversely related to mean temperature and directly related to nutritional value of the leaves. The temperature threshold for nymphal development is around 10-12°C. There is no diapause. Van den Berg et al. (1990) have studied the daily activities and habits of adults, and egg hatching and moulting in T. erytreae, while Van den Berg et al. (1991a) have studied mating, fertility and oviposition.

T. erytreae transmits the causal agent of the African form of citrus huanglongbing (greening) disease, Liberibacter africanus, under natural conditions in Africa and the Middle East (McClean and Oberholzer, 1965). It has been shown experimentally that T. erytreae is also able to transmit the Asian form, Liberibacter asiaticus (Massonie et al., 1976). In Mauritius and Reunion, where both forms occur, T. erytreae probably transmits both.

Natural enemies

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Means of Movement and Dispersal

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T. erytreae is only likely to spread locally by natural dispersal, up to distances of 1.5 km (Van den Berg and Deacon, 1988). 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 derived from these nymphs, are capable of transmitting L. africanum to citrus. International movement on citrus fruits is extremely unlikely.

Impact

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The main economic importance of T. erytreae is as the vector of the very serious citrus huanglongbing (greening) disease caused by Liberibacter species (EPPO/CABI, 1997). Heavy infestations of T. erytreae also cause severe leaf distortion and the development of conspicuous pits on the leaf surface.

Risk and Impact Factors

Top of page Invasiveness

• Invasive in its native range
• Proved invasive outside its native range
• Abundant in its native range
• Highly mobile locally
• Fast growing
• Has high reproductive potential

Impact outcomes

• Host damage
• Increases vulnerability to invasions
• Negatively impacts agriculture
• Negatively impacts livelihoods
• Reduced native biodiversity
• Threat to/ loss of native species
• Damages animal/plant products
• Negatively impacts trade/international relations

Impact mechanisms

• Pest and disease transmission

Likelihood of entry/control

• Highly likely to be transported internationally accidentally
• Highly likely to be transported internationally illegally

Detection and Inspection

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The presence of small pit galls on young leaves may indicate African citrus psyllid (USDA, 2012).

Similarities to Other Species/Conditions

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T. erytreae is similar to Diaphorina citri, the Asian citrus psyllid, which is the vector of citrus huanglongbing (greening) in Asia. The geographical range of the two species did not originally overlap, but they now occur together in Mauritius, Reunion and Saudi Arabia.

Prevention and Control

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Chemical Control

Insecticides such as dimethoate can be used against T. erytreae, for which there is an active monitoring programme in orchards in South Africa.

Biological Control

In Reunion, T. erytreae has been successfully controlled by the introduction of a parasite, Tamarixia dryi, from South Africa (Aubert et al., 1980). Research on the biological control of the vectors has also been carried out in Mauritius. Aubert (1987) and Van den Berg (1990) report the results for Mauritius and also Reunion. In South Africa, numerous predators occur but have not been found to reduce populations to economically acceptable levels (Van den Berg et al., 1987).

Cultural Practices

T. erytreae enters orchards from indigenous hosts in the surrounding vegetation (Van den Berg et al., 1991b), so it is recommended that these hosts are removed.

Phytosanitary Measures

Because of the difficulty of ensuring freedom from eggs or nymphs, importation of plants for planting and cut branches of citrus from countries where Liberibacter africanum and its vector occur should be prohibited (OEPP/EPPO, 1990). It is possible to fumigate citrus budwood material against T. erytreae (FAO, l983).

References

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Aubert B, 1987. Trioza erytreae Del Guercio and Diaphorina citri Kuwayama (Homoptera: Psylloidea), the two vectors of citrus greening disease: biological aspects andpossible control strategies. Fruits, 42(3):149-162, 189-192.

Aubert B; Bové JM; Etienne J, 1980. La lutte contre la maladie du greening des agrumes à l'ile de la Réunion. Résultats et perspectives. Fruits, 35:605-624.

Berg MA van den, 1990. The citrus psylla, Trioza erytrep (Del Guercio) (Hemiptera: Triozidae): a review. Agriculture, Ecosystems & Environment, 30(3-4):171-194

Berg MA van den; Deacon VE, 1988. Dispersal of the citrus psylla, Trioza erytrep (Hemiptera: Triozidae), in the absence of its host plants. Phytophylactica, 20(4):361-368

Berg MA van den; Deacon VE; Fourie CJ; Anderson SH, 1987. Predators of the citrus psylla, Trioza erytrep (Hemiptera: Triozidae), in the Lowveld and Rustenburg areas of Transvaal. Phytophylactica, 19(3):285-289

Berg MA van den; Deacon VE; Steenekamp PJ, 1991. Dispersal within and between citrus orchards and native hosts, and nymphal mortality of citrus psylla, Trioza erytreae (Hemiptera: Triozidae). Agriculture, Ecosystems & Environment, 35(4):297-309

Berg MA van den; Fletcher CD, 1988. A bibliography of the citrus psylla, Trioza erytrep (Del Guercio) (Hemiptera: Triozidae), up to 1987. Phytoparasitica, 16(1):47-61

Bohlen E, 1973. Crop pests in Tanzania and their control. Berlin, Germany: Verlag Paul Parey.

CABI/EPPO, 1998. Distribution maps of quarantine pests for Europe (edited by Smith IM, Charles LMF). Wallingford, UK: CAB International, xviii + 768 pp.

CABI/EPPO, 2006. Trioza erytreae. Distribution Maps of Plant Pests, No. 234. Wallingford, UK: CAB International.

CABI/EPPO, 2016. Trioza erytreae. [Distribution map]. Distribution Maps of Plant Pests, No.December. Wallingford, UK: CABI, Map 234 (2nd revision).

Catling HD, 1973. Notes on the biology of the South African citrus psylla, Trioza erytreae (Del Guercio) (Homoptera: Psyllidae). Journal of the Entomological Society of Southern Africa, 36(2):299-306

EPPO, 1990. Specific quarantine requirements. EPPO Technical Documents, No. 1008. Paris, France: European and Mediterranean Plant Protection Organization.

EPPO, 2011. EPPO Reporting Service. EPPO Reporting Service. Paris, France: EPPO. http://archives.eppo.org/EPPOReporting/Reporting_Archives.htm

EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm

European and Mediterranean Plant Protection Organization, 1988. EPPO data sheets on quarantine organisms Opogona sacchari (Bojer) Lepidoptera: Tineidae. EPPO Bulletin, 18(3):513-516

FAO, 1983. International plant quarantine treatment manual. FAO Plant Production and Protection Paper No. 50. Rome, Italy: FAO.

Green GC; Catling HD, 1971. Weather-induced mortality of the citrus psylla Trioza erytreae, a vector of greening virus, in some citrus-producing areas of South Africa. Agricultural Meteorology, 8:305-317.

Massonie G; Garnier M; Bové JM, 1976. Transmission of Indian citrus decline by Trioza erytrep (Del Guercio), the vector of South African greening. In: Calavan EC, ed. Proceedings of the Seventh Conference of the International Organization of Citrus Virologists. Univ. California. Riverside USA, 18-20

McClean APD; Oberholzer PCJ, 1965. Citrus psylla, a vector of the greening disease of sweet orange. South African Journal of Agricultural Science, 8:297-298.

Schwarz RE; Green GC, 1970. Citrus-greening and the citrus Psyllid Trioza erytreae - a temperature-dependent agent-vector complex. Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz, 77(9):490-493

Smith IM; McNamara DG; Scott PR; Holderness M, 1997. Quarantine pests for Europe. Second Edition. Data sheets on quarantine pests for the European Union and for the European and Mediterranean Plant Protection Organization. Quarantine pests for Europe. Second Edition. Data sheets on quarantine pests for the European Union and for the European and Mediterranean Plant Protection Organization., Ed. 2:vii + 1425 pp.; many ref.

Tumminelli R; Maltese U; Pedrotti C, 2006. New parasites invade citrus fruit. (Nuovi parassiti insidiano gli agrumi.) Informatore Agrario, 62(3):61-63. http://www.informatoreagrario.it

USDA, 2012. .

Van den Berg MA; Deacon VE; Jager K de, 1990. Ecology of the citrus psylla, Trioza erytreae. 1. Daily activities and habits of adults. 2. Egg hatching and moulting. Phytophylactica, 22:323-328, 329-333.

Van den Berg MA; Deacon VE; Thomas CD, 1991a. Ecology of the citrus psylla, Trioza erytreae (Hemiptera: Triozidae). 3. Mating, fertility and oviposition. Phytophylactica, 23(3):195-200

Contributors

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27/03/13 Updated by:

Esther Arengo, National Agricultural Research Laboratories, Uganda 

Distribution Maps

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