EPPO Datasheet: Trioza erytreae
Authority: (Del Guercio)
Taxonomic position: Animalia: Arthropoda: Hexapoda: Insecta: Hemiptera: Sternorrhyncha: Triozidae
Other scientific names: Spanioza erythreae Del Guercio, Spanioza merwei (Pettey), Trioza merwei Pettey
Common names in English: African citrus psyllid, citrus psylla, citrus psyllid, two-spotted citrus psyllid
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EPPO Categorization: A2 list
EU Categorization: A2 Quarantine pest (Annex II B)
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EPPO Code: TRIZER
T. erytreae is confined to Rutaceae, occurring on wild and ornamental hosts (Clausena anisata, Vepris lanceolata) and on Citrus, especially lemons (C. limon) and limes (C. aurantiifolia). Within the EPPO region, the host species are generally confined to countries surrounding the Mediterranean Sea.Host list: Calodendrum capense, Casimiroa edulis, Choisya ternata, Citroncirus, Citrus aurantiifolia, Citrus australasica, Citrus deliciosa, Citrus jambhiri, Citrus limon, Citrus maxima, Citrus medica, Citrus paradisi, Citrus reticulata, Citrus sinensis, Citrus tangerina, Citrus unshiu, Citrus x nobilis, Citrus, Clausena anisata, Fortunella, Murraya koenigii, Murraya paniculata, Poncirus trifoliata, Rutaceae, Toddalia asiatica, Vepris lanceolata, Vepris nobilis, Vepris, Zanthoxylum sp., x Citrofortunella microcarpa
GEOGRAPHICAL DISTRIBUTION 2020-08-28
Until the 1990s, T. erytreae was present in Sub-Saharan Africa, Saudi Arabi and the Yemen and on the islands of St. Helena, Mauritius, Reunion and Madagascar. In 1994 and 2002, this psyllid invaded Madeira and the Canary Islands, respectively, in Macaronesia (West Palaearctic). In 2014, T. erytreae reached mainland Europe, where it spread from Galicia (northwestern Spain) to Lisbon in Portugal.
A recent study has suggested that the T. erytreae individuals found in Europe (Madeira, Canary Islands and Galicia) have a similar haplotype and most likely originated from South Africa, although the possibility of a Kenyan origin cannot be excluded (Ajene et al., 2020).
The distribution of T. erytreae is wider than that of the causal agent of citrus huanglongbing (HLB) disease originally associated with this vector, ‘Candidatus Liberibacter africanus’, because the vector occurs in Congo, Sudan and Zambia in Africa, and Portugal and Spain in Europe, where ‘Ca. Liberibacter africanus’ has not yet been recorded.EPPO Region: Portugal (mainland, Madeira), Spain (mainland, Islas Canárias)
Africa: Angola, Cameroon, Comoros, Congo, Democratic republic of the, Eritrea, Ethiopia, Gabon, Kenya, Madagascar, Malawi, Mauritius, Reunion, Rwanda, Saint Helena, Sao Tome & Principe, South Africa, Sudan, Swaziland, Tanzania, Uganda, Zambia, Zimbabwe
Asia: Saudi Arabia, Yemen
Cocuzza et al. (2017) compiled a bibliography for T. erytreae up to 2017, and general reviews have been published by van den Berg & Fletcher (1988) and van den Berg (1990). T. erytreae has a temperature sensitivity similar to that of the ‘Ca. Liberibacter africanus’ (Schwarz & Green, 1970; Catling, 1973). It is very sensitive to extreme heat (temperatures above 32°) and dry weather, with the eggs and first-instar nymphs being particularly vulnerable. Based on this climatic profile and the mortality of the psyllid, Green & Catling (1971) used the maximum saturation deficit as an accurate predictor of the geographical distribution of T. erytreae. It is favoured in cool and moist areas, in which citrus growth flushes tend to be prolonged.
The sex ratio fluctuates 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 two to four times per day, and eggs may be laid immediately. The eggs are equipped 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 lifespan, which is normally 17-50 days. Each female may lay up to 2000 eggs. There is an incubation period of 5-17 days and nymph development (five instars) takes 17-47 days, the lengths of both these periods being inversely related to mean temperature and directly related to the nutritional value of the leaves. The temperature threshold for nymph development appears to be around 10-12°C. There is no diapause. Van den Berg et al. (1990) studied the daily activities and habits of adults, and egg hatching and moulting, in T. erytreae, whereas van den Berg et al. (1991a) studied mating, fertility and oviposition.
T. erytreae transmits ‘Candidatus Liberibacter africanus’ under natural conditions in Africa, parts of Arabia, and some Indian Ocean islands (McClean & Oberholzer, 1965; Gottwall, 2010). T. erytreae has also been shown to transmit ‘Candidatus Liberibacter asiaticus’ and ‘Candidatus Liberibacter americanus’ (Ajene et al., 2020; Gottwall, 2010).
DETECTION AND IDENTIFICATION 2020-08-28
T. erytreae severely distorts leaves, which become stunted and galled, and appear to be dusted with solid white honeydew excreted by the psyllid. High psyllid densities and humid environmental conditions may be associated with the development of sooty mold on the honeydew.
Yellow-orange, cylindrical, with a sharp point at the anterior; laid at the margins of young, actively growing leaves.
Dorso-ventrally compressed and varying in colour from yellow to olive-green or 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.
Adults are about 3-4 mm long. Winged, with a yellowish-green body, initially delicate, later becoming light-brown. Males are smaller than females and have a blunt tip to the abdomen, whereas the abdomen of the female ends in a sharp point. Adults adopt a distinctive stance while feeding, with the abdomen raised at an angle of about 35° to the feeding surface.
Details of the sizes of the nymphs and adults of T. erytreae have been provided by Cocuzza et al. (2016) and Aidoo et al. (2019). The EPPO Diagnostic Protocol for T. erytreae provides guidance on how to detect and identify the pest (EPPO Standard PM 7/57).
Detection and inspection methods
The distinctive cup-shaped, open galls produced by T. erytreae nymphs can be used to detect its presence in recently invaded areas. These galls are produced by nymphs after a few days of feeding on young and tender leaves, and the galls remain in the leaves when the adults emerge and the leaves mature. These galls can, therefore, be used to detect the presence of the psyllid in the current and previous flushes. For the detection of nymphs and adults, monitoring should be carried out during flushing periods. In the Mediterranean Basin, there are three flushing periods for most citrus species: spring, mid-summer and late autumn. The spring flush is the most important in terms of size. However, lemon species flush throughout the year. For confirmation of the detection of T. erytreae and identification of the adults, yellow sticky traps or suction sampling devices can be used to capture the adults. 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).
PATHWAYS FOR MOVEMENT 2020-08-28
T. erytreae is can spread locally by natural means of dispersal, over distances of up to 1.5 km (van den Berg & Deacon, 1988). Eggs and nymphs may be carried over longer distances on citrus material (budwood, grafted trees, rootstock seedlings). Both adults and nymphs can acquire the causal agent of huanglongbing, but only adults can transmit it (McClean 1974; Moll and van Vuuren 1977). The illegal introduction of plant material can lead to the introduction of the disease or the vector. Adults can survive for up to 12 days on recently harvested lemon fruits at 13.5 ± 2ºC, 85.4 ± 10% RH, under an L14 hours:D10 hours photoperiod (Urbaneja-Bernat et al., 2020). Introduction on citrus fruits that have passed through packing house processes involving brushing, washing and the removal of stems and leaves is unlikely.
PEST SIGNIFICANCE 2020-08-28
T. erytreae results principally from its role as a vector of huanglongbing, the most damaging citrus disease in the world (Gottwald, 2010). Heavy infestations with T. erytreae also cause severe leaf distortion, the development of conspicuous pits on the leaf surface and the development of sooty mold on the excreted honeydew.
Several active ingredients of different groups can be used against T. erytreae. In South Africa, control is based on the use of organophosphates and neonicotinoids that are banned in Europe. A list of active ingredients, with their efficacy and mode of action against D. citri, the other vector of huanglongbing, has been published by Qureshi et al. (2014). T. erytreae can enter orchards from other host plants in the surrounding vegetation (van den Berg et al., 1991b), the removal of which is, therefore, recommended.
Experience in areas to which T. erytreae already has spread or into which it has recently been introduced suggests that the eradication of this species is almost impossible (Cocuzza et al., 2017).
On Reunion Island and the Canary Islands, T. erytreae has been successfully controlled by the introduction of the parasitoid Tamarixia dryi from South Africa (Aubert et al., 1980; Hernández-Suárez et al. 2020). This species of parasitoid is highly specific and does not, therefore, represent an environmental risk for native psyllid species (Urbaneja-Bernat et al., 2019). In South Africa, three primary parasitoids and numerous predators occur, but have not been found to reduce populations to economically acceptable levels, probably due to the presence of a hyperparasitoid complex (van den Berg et al., 1987; Pérez-Rodríguez et al., 2019). In Cameroon, the psyllid is also attacked by a complex of parasitoids (Tamesse 2009).
Trioza erytreae is now established in mainland Europe (Galicia in Spain and the Portuguese coast from the northern part of the country to Lisbon), but it has not yet reached the main citrus-producing areas. A study based on water vapor deficit pressure has suggested that the psyllid will be able to spread along the entire Portuguese coast to the Algarve (southern Portugal), the main citrus-producing area in Portugal (Paiva et al., 2020). It would probably be able to establish itself and spread in Mediterranean countries without difficulty, because citrus crops are mostly produced in areas close to the coast with a high relative humidity, but further studies are required to confirm this. In addition to its role as a vector of huanglongbing, this psyllid has a significant potential for damage in its own right. Biological control may be possible, at least on islands, but there is no guarantee that it could keep populations at sufficiently low levels to prevent transmission of huanglongbing.
PHYTOSANITARY MEASURES 2020-08-28
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.
Aidoo OF, Tanga CM, Paris TM, Allan SA, Mohamed SA, Khamis FM, Sétamou M, Borgemeister C, Ekesi S (2019) Size and shape analysis of Trioza erytreae Del Guercio (Hemiptera: Triozidae), vector of citrus huanglongbing disease. Pest Management Science 75, 760-771.
Ajene IJ, Khami FM, van Asch B, Pietersen G, Seid N, Rwomushana I, Ombura FLO, Momanyi G, Finyange P, Rasowo BA, Tanga CM, Mohammed S, Ekesi S (2020) Distribution of Candidatus Liberibacter species in Eastern Africa, and the first report of Candidatus Liberibacter asiaticus in Kenya. Scientific Reports 10, 3919 https://doi.org/10.1038/s41598-020-60712-0
Ajene I, Pietersen G, van Asch B (2020) Mitochondrial genetic variation reveals phylogeographic structure and cryptic diversity in Trioza erytreae. Scientific Reports 10,8893. https://doi.org/10.1038/s41598-020-65880-7.
Aubert B, Bové JM, Etienne J (1980) La lutte contre la maladie du greening des agrumes à l'île de la Réunion. Résultats et perspectives. Fruits 35, 605-624.
Catling HD (1973) Notes on the biology of the South African citrus psylla Trioza erytreae. Journal of the Entomological Society of South Africa 36, 299-306.
Cocuzza GEM, Urbaneja A, Hernández-Suárez E, Siverio F, Di Silvestro S, Tena A, Carmelo R (2017) A review on Trioza erytreae (African citrus psyllid), now in mainland Europe, and its potential risk as vector of “huanglongbing” (HLB) in citrus. Journal of Pest Science 90, 1-17.
EFSA (2019) Parnell S, Camilleri M, Diakaki M, Schrader G & Vos S. Pest survey card on Huanglongbing and its vectors. EFSA Supporting publication 2019, EN-1574. https://doi.org/doi:10.2903/sp.efsa.2019.EN-1574
EPPO (2020) PM 9/27 (1) ‘Candidatus Liberibacter’ species that are casual agents of Huanglongbing disease of citrus and their vectors: procedures for official control. EPPO Bulletin, 50, 122-141.
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.
Gottwald TR (2010). Current epidemiological understanding of citrus huanglongbing. Annual Review of Phytopathology, 48, 119-139.
Hernández-Suárez E, Pérez-Rodríguez J, Suárez-Méndez L, Urbaneja-Bernat P, Rizza R, Siverio F, Piedra-Buena A, Urbaneja A, Tena, A (2020) Control de Trioza erytreae en las Islas Canarias por el parasitoide Tamarixia dryi. Phytoma España 319, 28-32.
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.
Paiva PEB, Cota T, Neto L, Soares C, Tomás JC, Duarte A (2020) Water vapor pressure deficit in Portugal and implications for the development of the invasive African citrus psyllid Trioza erytreae. Insects 11, 229.
Pérez-Rodríguez J, Krüger K, Pérez-Hedo M, Ruíz-Rivero O, Urbaneja A, Tena A (2019) Classical biological control of the African citrus psyllid Trioza erytreae, a major threat to the European citrus industry. Scientific Reports 9, 9440.
Qureshi JA, Kostyk BC, Stansly PA (2014) Insecticidal suppression of Asian citrus psyllid Diaphorina citri (Hemiptera: Liviidae) vector of huanglongbing pathogens. PLoS One, 9(12).
Schwarz RE, Green GC (1970) Citrus greening and the citrus psyllid Trioza erytreae, a temperature-dependent agent-vector complex. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz 79, 490-493.
Tamesse JL (2009) Key for identification of the Hymenopteran parasitoids of the African citrus psylla Trioza erytreae Del Guercio (Hemiptera: Triozidae) in Cameroon. African Journal of Agricultural Research 4, 85–91.
Urbaneja-Bernat P, Hernández-Suárez E, Urbaneja A, Tena A (2020) Preventive measures to limit the spread of Trioza erytreae (Del Guercio) (Hemiptera: Psyllidae) in mainland Europe. Journal of Applied Entomology. https://doi.org/10.1111/jen.12771
Urbaneja-Bernat P, Pérez-Rodríguez J, Krüger K, Catalán J, Rizza R, Hernández-Suárez E, Urbaneja A, Tena A (2019) Host range testing of Tamarixia dryi (Hymenoptera: Eulophidae) sourced from South Africa for classical biological control of Trioza erytreae (Hemiptera: Psyllidae) in Europe. Biological control 135, 110-116.
Van den Berg MA (1990) The citrus psylla, Trioza erytreae: a review. Agriculture, Ecosystems and Environment 30, 171-194.
Van den Berg MA, Deacon VE (1988) Dispersal of the citrus psylla, Trioza erytreae, in the absence of its host plants. Phytophylactica 20, 361-368.
Van den Berg MA, Fletcher CD (1988) A bibliography of the citrus psylla, Trioza erytreae, up to 1987. Phytoparasitica 16, 47-61.
Van den Berg MA, Deacon VE, Fourie CJ, Anderson SH (1987) Predators of the citrus psylla, Trioza erytreae, in the Lowveld and Rustenburg areas of Transvaal. Phytophylactica 19, 285-289.
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. 3. Mating, fertility and oviposition. Phytophylactica 23, 195-200.
Van den Berg MA, Deacon VE, Steenekamp PJ (1991b) Dispersal within and between citrus orchards and native hosts, and nymphal mortality of citrus psylla, Trioza erytreae. Agriculture, Ecosystems and Environment 35, 297-309.
This datasheet was extensively revised in 2020 by Alejandro Tena from Instituto Valenciano de Investigaciones Agrarias (IVIA), Moncada, Valencia, Spain. His valuable contribution is gratefully acknowledged.
How to cite this datasheet?
Datasheet history 2020-08-28
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 (1st and 2nd 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.