EPPO Datasheet: Aleurocanthus spiniferus
Taxonomic position: Animalia: Arthropoda: Hexapoda: Insecta: Hemiptera: Sternorrhyncha: Aleyrodidae
Other scientific names: Aleurocanthus cheni Young, Aleurocanthus citricola (Newstead), Aleurocanthus rosae Singh, Aleurodes citricola Newstead, Aleurodes spinifera Quaintance
Common names in English: citrus mealywing, citrus spiny whitefly, orange spiny whitefly, spiny blackfly
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Notes on taxonomy and nomenclature
Aleurocanthus spiniferus grouped two different taxa for several years, until the description of Aleurocanthus camelliae Kanmiya & Kasai in Kanmiya et al. (2011) was published. Thus, previous records of A. spiniferus may include records of A. camelliae, especially for populations infesting tea (Camellia sinensis).
EU Categorization: A2 Quarantine pest (Annex II B)
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EPPO Code: ALECSN
Citrus spp. are the main hosts of economic importance but A. spiniferus has been recorded on other crops, for example grapes (Vitis vinifera), guavas (Psidium guajava), pears (Pyrus spp.), persimmons (Diospyros kaki) and roses (Rosa spp.). A. spiniferus occurs throughout much of the Asian range of A. woglumi and possibly shares many of its hosts.
The potential host range in the EPPO region would be essentially citrus, with some possibility of establishment on other woody plantation crops growing in the southern part of the region in climatic conditions suitable for the pest.Host list: Ailanthus altissima, Akebia longiracemosa, Akebia trifoliata, Alnus formosana, Annona muricata, Annona reticulata, Annona squamosa, Annona x atemoya, Aphananthe philippinensis, Arbutus unedo, Barringtonia acutangula, Bauhinia championii, Boehmeria virgata var. densiglomerata, Boehmeria zollingeriana var. blinii, Casearia aculeata, Ceratonia siliqua, Cinnamomum camphora, Citrus aurantium, Citrus limon, Citrus medica, Citrus reticulata, Citrus sinensis, Clematis vitalba, Cocos nucifera, Cupaniopsis anacardioides, Cydonia sp., Diospyros kaki, Diospyros maritima, Entada phaseoloides, Eriobotrya japonica, Erycibe henryi, Fatsia sp., Ficus carica, Ficus racemosa, Ficus sp., Ficus sur, Flindersia sp., Fortunella, Ganophyllum falcatum, Gardenia jasminoides, Gossypium sp., Hedera helix, Hibiscus cannabinus, Hibiscus rosa-sinensis, Hibiscus tiliaceus, Laurus nobilis, Liquidambar formosana, Macaranga tanarius, Machilus zuihoensis, Maesa perlarius, Malus sp., Malva sp., Manihot esculenta, Maranthes corymbosa, Meliosma rigida, Morella rubra, Morus alba, Murraya koenigii, Mussaenda pubescens, Parthenocissus tricuspidata, Persea americana, Phoebe formosana, Piper kadsura, Pistacia vera, Plumeria rubra, Prunus armeniaca, Prunus avium, Prunus cerasus, Prunus domestica, Prunus persica, Prunus serotina, Psidium guajava, Punica granatum, Pyracantha coccinea, Pyrus communis, Pyrus pyraster, Pyrus pyrifolia, Rhododendron latoucheae, Rollinia mucosa, Rosa banksiae, Rosa chinensis, Rosa indica, Rosa x damascena, Rosa, Salix sp., Scolopia oldhamii, Senna siamea, Sloanea dasycarpa, Streblus sp., Synedrella nodiflora, Syzygium samarangense, Toona ciliata, Triadica sebifera, Urena lobata, Vigna unguiculata subsp. sesquipedalis, Vitis vinifera, Xylosma congesta, Zanthoxylum nitidum
GEOGRAPHICAL DISTRIBUTION 2020-09-15
Aleurocanthus spiniferus originated in tropical Asia and has spread widely into the Indian Ocean, Africa and the Pacific. Its range overlaps that of A. woglumi in many regions, but it has not been introduced into the American continent. In the EPPO region, it has been recorded in Southeast Europe where populations remain low. It was first recorded in Italy in 2008 (Porcelli, 2008) in the area of Supersano (Puglia region). Since then, it has also been found on Citrus spp. in the Campania, Lazio and Basilicata regions in Italy (EPPO, 2017/19). It has been found in Croatia (first record 2012) (Šimala et al., 2015) with a severe outbreak reported in Split Dalmatia County in 2019 (EPPO, 2020). A. spiniferus was first recorded in Greece (Corfu) in 2016 (Kapantaidaki et al., 2019). It has also been recorded from Montenegro (first record 2013: Radonjić et al., 2014) and Albania (first report 2020: Nugnes et al., 2020).EPPO Region: Albania, Croatia, Greece (mainland), Italy (mainland), Montenegro
Africa: Kenya, Mauritius, Nigeria, Reunion, South Africa, Swaziland, Tanzania, Uganda
Asia: Bangladesh, Bhutan, Brunei Darussalam, Cambodia, China (Anhui, Aomen (Macau), Fujian, Guangdong, Guizhou, Hainan, Hubei, Hunan, Jiangsu, Jiangxi, Shandong, Shanxi, Sichuan, Xianggang (Hong Kong), Yunnan, Zhejiang), India (Andaman and Nicobar Islands, Assam, Bihar, Karnataka, Maharashtra, Tamil Nadu, Uttar Pradesh), Indonesia (Java, Sumatra), Iran, Japan (Honshu, Kyushu, Ryukyu Archipelago, Shikoku), Korea Dem. People's Republic, Korea, Republic, Lao, Malaysia (Sabah, Sarawak, West), Myanmar, Pakistan, Philippines, Sri Lanka, Taiwan, Thailand, Viet Nam
North America: United States of America (Hawaii)
Oceania: Australia (Northern Territory, Queensland), Guam, Micronesia, Northern Mariana Islands, Palau, Papua New Guinea
In tropical conditions all stages of A. spiniferus may be found throughout the year, but very limited breeding occurs during cold periods. In Asia, the stages that overwinter (eggs and early-instar larvae or pupa) vary with the region and the year. The biology of A. spiniferus is essentially similar to that of A. woglumi (EPPO/CABI, 1996). A. spiniferus has six developmental stages: the egg stage, four nymphal instars and the adult. All stages are found on the leaves. Eggs are laid in a spiral pattern on the underside of the leaf in batches of 12-22 (USDA, 1982; Byrne & Bellows, 1991). Eggs hatch in 4 to 15 days depending on environmental conditions. The first instar nymphs are active, brown to black, with a flattened body and six legs. Upon hatching, the 1st instar nymphs disperse by crawling for a short time, staying mainly on abaxial leaf surface to avoid strong sunlight. They then insert their mouthparts into the leaves and begin sucking phloem sap. Following this, the nymphs moult, losing their legs in the process, and become minute, flattened, oval bodies which attach to the leaf by their mouthparts. Immature stages often form dense colonies of up to several hundred individuals on a single leaf. After two more moults, the adults emerge from the last instar (called puparium). In Croatia, egg development takes 12-15 days (11-22 in Japan), the development of the stages 1 to 3 takes 36-43 days and development of the last instar (puparium) takes 12-17 days (7-34 in Japan) (Gyeltshen et al., 2017; Paladin Soče et al., 2020). Both sexes are winged and feed by sucking phloem sap. Depending on climatic conditions (mild temperatures and high relative humidity being optimal), the life cycle generally takes 2-4 months but there can be four (Japan) to six (Guam) overlapping generations a year (Gyeltshen et al., 2017).
In the very similar species A. woglumi, development is favoured by temperatures of 20-34°C (optimum 25.6°C) and relative humidities of 70-80%. The species does not survive at temperatures below freezing and is not found in areas with temperatures of 43°C or over. The occurrence of A. woglumi and A. spiniferus on citrus in Kenya, at lower and higher altitudes respectively, suggests these species may differ in their ecological tolerances (CABI, 2018). It may also be noted that A. spiniferus occurs further north in Asia than A. woglumi (Jiangsu and Shandong provinces in China; Japan, Korean peninsula) (EFSA Plant Health Panel, 2018).
DETECTION AND IDENTIFICATION 2020-09-15
Dense colonies of immature stages develop on leaf undersides, mainly on the lower parts of the trees; the adults fly actively when disturbed. Leaves and fruit have spots of sticky, transparent honeydew, which become covered in black sooty mould fungus. A heavy infestation gives trees an almost completely black appearance.
Elongate-oval to kidney-shaped, 0.2 mm long, laid in a very characteristic spiral pattern, attached to the underside of leaves by a short pedicel; yellowish at first, turning darker to brown and black as the embryo develops.
1st instar: 6-legged, elongate, 0.315 x 0.153 mm, brown to black, with 2 long and several shorter, radiating spiny filaments.
2nd instar: no legs, ovate-convex, 0.4 x 0.3 mm, dark-brown to pale-black with yellow markings, with easily distinguished, radiating spiny filaments and a crenulated marginal edge.
3rd instar: more ovate,
4th instar = ‘puparium’: ovate, shiny-black, females 1.08-1.28 mm long x 0.8-1 mm wide, males smaller 0.75-0.8 x 0.52-0.58 mm. Dorsal surface with many long, acute glandular spines; insect surrounded by a white fringe of waxy secretion. Exuviae of earlier instars often remain stacked up on median area of immature insect.
Authoritative identification of Aleurocanthus spp. involves detailed microscopic study of external puparial morphology by a specialist. A. spiniferus and A. woglumi can be confused with each other since they only differ from one another in subtle characteristics. They might also be confused with several similar species of Aleurocanthus that occur on citrus, including A. citriperdus, and A. husaini (Schrader et al., 2018). Microscopic differences between puparia of A. spiniferus, A. woglumi and A. camelliae are given in Jansen & Porcelli (2018).
Females about 1.33-1.7 mm in length, males 0.96-1.33 mm long: at rest, the general appearance is metallic grey-blue, being the colour of the wings which cover most of the body; light markings on the wings appear to form a band across the middle of the red abdomen. The eyes are reddish-brown and the antennae and legs are white with pale-yellow markings.
Two haplotypes of A. spiniferus from Italy, based on mtCOI partial gene, are described in Nugnes et al. (2020). Primers used to amplify a 682bp fragment of the same gene are given in Uesugi & Sato (2011) and PCR conditions in Uesugi et al. (2016). A slightly modified protocol has been used by Kapantaidaki et al. (2019).
The EPPO Standard PM 7/7 Aleurocanthus spiniferus (EPPO, 2002) is under revision (EPPO, 2011) and the revised version will describe the characters to be used to distinguish species of interest within this taxonomically difﬁcult genus.
Detection and inspection methods
Yellow sticky traps can be used to capture adults, mainly in the citrus orchards. However, since adults and immature stages are present on above ground plant parts, Aleyrodidae can be detected more efficiently by visual observation (presence of sooty mould on leaves and fruits) and plant sampling (spiral egg masses and the three last larval instar stages being sessile), especially targeting the black puparia surrounded by a fringe of white wax and the adults with metallic grey-blue wings with white markings.
Infested samples showing the presence of various stages or debris of the insects (e.g. adults, pre-imaginal whitefly stages, puparia or pupal cases) should be collected and placed in a labelled plastic bag together with a piece of slightly damp absorbent paper, kept in cool conditions and sent to a diagnostic laboratory as soon as possible (EPPO, 2018).
PATHWAYS FOR MOVEMENT 2020-09-15
Adults of Aleurocanthus spp. are capable of limited down-wind flight but this is not a major means of long-range dispersal (Meyerdink et al., 1979). The whiteflies are most likely to be moved between countries on planting material of citrus or other host species, or possibly on fruits (CABI, 2018). Species of Aleurocanthus have been intercepted on the leaves of infested host plants moving in international trade (e.g. USDA, 1988).
PEST SIGNIFICANCE 2020-09-15
Aleurocanthus spiniferus excretes copious amounts of sugary honeydew, which coats leaf and fruit surfaces. Sooty mould fungus develops on the honeydew, reducing respiration and photosynthesis and rendering plants and fruit unsightly and unsaleable (USDA, 1982). Badly affected foliage may drop and fruit set may be reduced (Radonjić et al., 2014). Nitrogen levels in infested leaves are reduced and young leaf growth is damaged by heavy infestations. Eventual death of heavily infested plants owing to sap loss and development of sooty mould may occur (USDA, 1982). It is one of the most destructive Aleyrodids attacking citrus in tropical Asia (USDA, 1982; Kapantaidaki et al., 2019). In Australia, A. spiniferus is occasionally a pest on Annona and Citrus, and also on several ornamental trees (Mifsud et al., 2010; Gillespie, 2012). In India, A. spiniferus can be a serious pest of roses (David & Subramaniam, 1976; Cioffi et al., 2013).
It has not been demonstrated that chemical control was effective on A. spiniferus but biological control, using hymenopteran parasites, has proved to be more economical and effective in several parts of the world (Lin et al., 1975; Clausen, 1978). Encarsia smithi (Silvestri) has been used to control A. spiniferus in Japan, in Hawaii (Clausen, 1978; Cioffi et al., 2013), in Pohnpei, Federated States of Micronesia (Muniappan et al., 1992) and in Southern Africa (van den Berg & Greenland, 1997). The same parasitoid, together with Amitus hesperidum Silvestri, has also been used to successfully control A. spiniferus in Guam on citrus, but it was less successful on rose and grape (Clausen, 1978).
Aleurocanthus spiniferus presents a risk to citrus in Mediterranean countries. It has a well-documented history of spread to new continents from its south-east Asian origin. Due to its small size and the potential of it moving and spreading via planting material and fruit further and repeated introductions are likely. For example, genetic analysis of samples of A. spiniferus suggests that multiple introductions have occurred in Corfu (Kapantaidaki et al., 2019).
Based on its current distribution and the distribution of citrus species in the EPPO region, it is predicted that the limits of the potential distribution of A. spiniferus is the southern part, in particular the Mediterranean region. There is also a risk of establishment on other woody plantation crops growing in the southern part of the region in climatic conditions suitable for the pest.
Aleurocanthus spiniferus appears to be fairly well restricted by natural enemies in its native range, but is liable to cause damage if introduced into new areas.
PHYTOSANITARY MEASURES 2020-09-15
Aleurocanthus spiniferus is on the EPPO A2 list and has recently been added to the EU Annex II B. The measures recommended by EPPO for A. woglumi would also be appropriate for A. spiniferus (EPPO/CABI, 1996). This would include that all host plants imported as planting material and as cut branches come from a nursery found to be free from the pest during the previous growing season. Additionally, plant material and cut branches of host plants shipped from countries where A. spiniferus occurs should be fumigated. Fresh fruit of host plants should be imported with a phytosanitary certificate.
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Gillespie PS (2012) A review of the whitefly genus Aleurocanthus Quaintance & Baker (Hemiptera: Aleyrodidae) in Australia. Zootaxa 3252, 1-42
Gyeltshen J, Hodges A, Hodges GS (2017) Orange Spiny Whitefly, Aleurocanthus spiniferus (Quaintance) (Insecta: Hemiptera: Aleyrodidae). Department of Entomology and Nematology, UF/IFAS Extension, Gainesville (USA), pp. 1-4.
Jansen M, Porcelli F (2018) Aleurocanthus camelliae (Hemiptera: Aleyrodidae), a species possibly new for the European fauna of a genus in great need of revision. Tijdschrift voor Entomologie 161, 63–7
Kanmiya K, Ueda S, Kasai A, Yamashita K, Sato Y, Yoshiyasu S Yoshiyasu Y (2011) Proposal of new specific status for tea-infesting populations of the nominal citrus spiny whitefly Aleurocanthus spiniferus (Homoptera: Aleyrodidae). Zootaxa 2797, 25-44. https://doi.org/10.11646/zootaxa.2797.1.3
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Lin HC, Wei HL, Tao CC (1975) Integrated control of citrus spiny white fly, Aleurocanthus spiniferus, Quaintance & Baker (Homoptera: Aleyrodidae). Journal of Agricultural Research of China 24, 55–61.
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Muniappan R, Marutani M, Esguerra N (1992) Establishment of Encarsia smithi (Silvestri) (Hymenoptera: Aphelinidae) on Pohnpei for control of the orange spiny whitefly, Aleurocanthus spiniferus (Quaintance) (Homoptera: Aleyrodidae). Proceedings of the Hawaiian Entomological Society 31, 243.
Nugnes F, Laudonia S, Jesu G, Jansen MGM, Bernardo U, Porcelli F (2020) Aleurocanthus spiniferus (Hemiptera: Aleyrodidae) in some European countries: diffusion, hosts, molecular characterization, and natural enemies. Insects 11(1), 42.
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Porcelli F (2008) First record of Aleurocanthus spiniferus (Homoptera: Aleyrodidae) in Apulia, Southern Italy. OEPP/EPPO Bulletin 38(3), 516-518.
Radonjić S, Hrnčić S, Malumphy C (2014) First record of Aleurocanthus spiniferus (Quaintance) (Hemiptera Aleyrodidae) in Montenegro. Redia 77, 141-145.
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Uesugi R, Sato Y (2011) Differentiation of the tea-infesting population of citrus spiny whitefly Aleurocanthus spiniferus (Homoptera: Aleyrodidae) from the citrus-infesting population in Japan on the basis of differences in the mitochondrial cytochrome c oxidase subunit I gene. Japanese Journal of Applied Entomology and Zoology 55, 155-161. https://doi.org/10.1303/jjaez.2011.155
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This datasheet was extensively revised in 2020 by David Ouvrard. His valuable contribution is gratefully acknowledged.
How to cite this datasheet?
Datasheet history 2020-09-15
This datasheet was first published in the second edition of 'Quarantine Pests for Europe' in 1997 and revised 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 (1997) Quarantine Pests for Europe (2nd edition). CABI, Wallingford (GB).