Preferred name: Aleurocanthus woglumi
Authority: Ashby
Taxonomic position: Animalia: Arthropoda: Hexapoda: Insecta: Hemiptera: Sternorrhyncha: Aleyrodidae
Other scientific names: Aleurocanthus formosana (Takahashi), Aleurocanthus punjabensis Corbett, Aleurodes woglumi (Ashby)
Common names in English: blue grey fly, citrus blackfly, citrus spring whitefly
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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: ALECWO

Citrus spp. are the main hosts of A. woglumi but it can be found on a wide range of crops, mostly fruit trees, including avocados (Persea americana), bananas (Musa spp.), cashews (Anacardium occidentale), coffee (Coffea arabica), ginger (Zingiber officinale), grapes (Vitis spp.), guavas (Psidium guajava), lychees (Litchi chinensis), mangoes (Mangifera indica), papaws (Carica papaya), pears (Pyrus spp.), pomegranates (Punica granatum), and quinces (Cydonia oblonga). In Mexico, 75 species in 38 families have been reported as hosts on which A. woglumi can complete its life cycle (Shaw, 1950).

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: Actinidia sp., Anacardium occidentale, Annona cherimola, Annona muricata, Annona sp., Annona squamosa, Antigonon leptopus, Ardisia compressa, Ardisia revoluta, Ardisia solanacea, Artocarpus altilis, Artocarpus heterophyllus, Atalantia buxifolia, Begonia sp., Bouvardia multiflora, Bursera simaruba, Buxus sempervirens, Byrsonima crassifolia, Callerya atropurpurea, Canna indica, Capparis roxburghii, Capparis spinosa, Capsicum frutescens, Cardiospermum sp., Carica papaya, Cedrela sp., Cestrum diurnum, Cestrum nocturnum, Chrysophyllum cainito, Citrus maxima, Citrus medica, Citrus reticulata, Citrus x aurantiifolia, Citrus x aurantium var. deliciosa, Citrus x aurantium var. paradisi, Citrus x aurantium var. sinensis, Citrus x aurantium, Citrus x latifolia, Citrus x limon, Citrus x limonia var. jambhiri, Clausena lansium, Coffea arabica, Cordia alba, Crataegus sp., Crescentia cujete, Croton sp., Cryosophila nana, Cupania juglandifolia, Cydonia oblonga, Diospyros ebenum, Diospyros kaki, Diospyros sp., Duranta erecta, Elaeis guineensis, Eugenia uniflora, Fortunella sp., Fraxinus sp., Guaiacum officinale, Guazuma ulmifolia, Gymnosporia diversifolia, Hibiscus rosa-sinensis, Hibiscus schizopetalus, Hibiscus sp., Hura polyandra, Inga jinicuil, Inga sp., Ixora thwaitesii, Jatropha curcas, Jatropha urens, Lagerstroemia indica, Laurus nobilis, Loranthus sp., Machilus zuihoensis, Madhuca longifolia var. latifolia, Magnolia x soulangeana, Malpighia glabra, Mammea americana, Mangifera indica, Manilkara zapota, Melia azedarach, Melicoccus bijugatus, Monstera deliciosa, Morinda coreia, Morus sp., Murraya koenigii, Murraya paniculata, Musa x paradisiaca, Parmentiera edulis, Passiflora edulis, Persea americana, Philodendron sp., Plumeria rubra f. acutifolia, Plumeria rubra, Populus sp., Pouteria caimito, Pouteria campechiana, Pouteria sapota, Prunus domestica, Psidium cattleyanum, Psidium guajava, Psidium oligospermum, Punica granatum, Pyracantha koidzumii, Pyrus communis, Salacia reticulata, Sapindus mukorossi, Sapium macrocarpum, Scolopia oldhamii, Sideroxylon palmeri, Solandra guttata, Spondias mombin, Strelitzia sp., Struthanthus flexicaulis, Swinglea glutinosa, Syzygium cumini, Syzygium jambos, Syzygium malaccense, Tabebuia riparia, Trichilia spondioides, Triphasia trifolia, Vitis sp., Wallenia laurifolia, Washingtonia robusta, Zingiber clarkei

A. woglumi originated in south-east Asia and it has spread widely in tropical and subtropical regions, overlapping the distribution of A. spiniferus in some regions. It was first detected in India in 1910, and in 1915 it was reported in other parts of Asia (Vieira et al., 2017). 

In the Western Hemisphere, A. woglumi was first recorded in Jamaica in 1913 and it has spread throughout the Caribbean region into Central America (Hoelmer and Grace, 1989; Vieira et al., 2017). By 1940 it had become a serious threat to citrus in Mexico where it may have been introduced on shipments of mango cuttings from India or from boats from Central America (Smith et al., 1964). A. woglumi was recorded in Florida in 1934, where it is now widespread throughout the north-central and southern parts of the state, and Texas (1955) (Smith et al., 1964; Hoelmer and Grace, 1989; Ngugen et al., 1998). In Brazil, A. woglumi was first detected in 2001, in Belém, Pará state in the north, and has now become widespread in the country (Silva et al., 2011; Monteiro et al., 2012; Alvim et al., 2016). A. woglumi was also, discovered near Durban, South Africa in January 1959, and is established in and around Durban on the Natal coast (Bedford and Thomas, 1965).

Africa: Eswatini, Kenya, Nigeria, Seychelles, South Africa, Tanzania, Uganda
Asia: Bangladesh, Bhutan, Cambodia, China (Guangdong, Hainan, Xianggang (Hong Kong)), Christmas Island, India (Andhra Pradesh, Assam, Bihar, Delhi, Goa, Gujarat, Karnataka, Madhya Pradesh, Maharashtra, Punjab, Sikkim, Tamil Nadu, Telangana, Uttar Pradesh, West Bengal), Indonesia (Irian Jaya, Java, Kalimantan, Sulawesi, Sumatra), Iran, Laos, Malaysia (Sabah, Sarawak, West), Maldives, Myanmar, Nepal, Oman, Pakistan, Philippines, Singapore, Sri Lanka, Taiwan, Thailand, United Arab Emirates, Vietnam, Yemen
North America: Mexico, United States of America (Florida, Hawaii, Texas)
Central America and Caribbean: Antigua and Barbuda, Bahamas, Barbados, Belize, Bermuda, Cayman Islands, Costa Rica, Cuba, Dominica, Dominican Republic, El Salvador, Guadeloupe, Guatemala, Haiti, Jamaica, Netherlands Antilles, Nicaragua, Panama, Puerto Rico, Saint Lucia, St Kitts-Nevis, Trinidad and Tobago, Virgin Islands (British)
South America: Argentina, Brazil (Amapa, Amazonas, Bahia, Ceara, Espirito Santo, Goias, Maranhao, Mato Grosso do Sul, Para, Paraiba, Parana, Pernambuco, Piaui, Rio de Janeiro, Rio Grande do Norte, Rio Grande do Sul, Rondonia, Roraima, Santa Catarina, Sao Paulo, Sergipe, Tocantins), Colombia, Ecuador, French Guiana, Guyana, Suriname, Venezuela
Oceania: Papua New Guinea

In tropical conditions all stages of A. woglumi may be found throughout the year, but little breeding occurs during cold periods (EFSA, 2018). Laboratory experiments found that the optimal temperature for development is 25±3˚C (Moraes et al., 2014), relative humidity 70-80% (CABI, 2018), and survival was greatest at 25.6˚C (Dowell and Fitzpatrick, 1978). A. woglumi persists in temperatures often exceeding 44˚C in the Middle East or areas such as the Sindh and Punjab provinces in Pakistan and Maharastra in India, where long-term monthly average maximum temperatures can exceed 42˚C (Akrivou et al., 2021).

Females opt for oviposition sites in tree canopies with high humidity as this influences egg hatch and nymph survival (Raga et al., 2016; Lima et al., 2017). Each female lays 35-100 or more eggs (average 38) in a spiral pattern on leaf undersides in batches adhered by a short pedicel (Quezada, 1974; Lima et al., 2017), and hatch in 4 to 12 days depending on conditions (Dietz & Zetek, 1920). In the field it has been observed that on sunny days the eggs are laid in the morning, or in the late afternoon, when the relative humidity is highest. On cloudy days, when the relative humidity is almost constant, egg laying may take place at any time during the day (Dietz and Zetek, 1920). Active, first instars (crawlers) emerge. They disperse for a short time (3 or 4 hours) (Medina-Gaud et al., 1991), staying mainly on lower leaf surfaces to avoid strong sunlight and begin feeding on plant sap (CABI, 2018). They then moult, losing their legs and remain attached to the leaf by their mouthparts (Bell et al., 2014). The four instar stages last 7-16, 7-30, 6-20, 16-50 days, respectively (EFSA, 2018), and the adult lifespan is 6 to 12 days (Dietz & Zetek, 1920). 

The life cycle generally takes 2-4 months and there are up to six generations annually (CABI, 2018; EFSA, 2018). Hoelmer and Grace (1979) reported three to four generations annually in South Florida, Clausen and Berry (1932) observed five generations each year in Kuala Lumpur, while in the Panama Canal Zone a maximum number of five generations were reported (during the dry season at least one generation is lost) (Dietz and Zetek, 1920).

Symptoms

Dense colonies of immature stages develop on the undersides of the leaves, and are more common on the lower half of citrus trees. Direct damage by A. woglumi is caused by continuous sucking of leaf sap by both immature and adult stages (Gomes et al. 2019). Plants weaken, the leaves wither and drop (Clausen and Berry, 1932), and the fruit-bearing capacity of the tree is also badly affected. The leaf organic nitrogen content is reduced below 2.2%, which is the minimum prerequisite for successful fruit set (Rao and George, 2018). Additional damage is associated with honeydew egestion by nymphs and the development of a sooty mould (Capnodium sp.) on leaves and fruits, causing negative physiological changes to plants (Gomes et al. 2019; Lima et al. 2017) which decrease leaf respiration and photosynthesis (Raga et al., 2013). A heavy infestation gives trees an almost completely black appearance.

Morphology

The genus Aleurocanthus has been described based on the puparium. Details for identification are provided in the EPPO Diagnostic Protocol PM 7/007 Aleurocanthus citriperdus, Aleurocanthus spiniferus and Aleurocanthus woglumi (EPPO, 2022).

Egg

Elongate-oval, 0.2 mm long (CABI, 2018), cream-white to pale yellow at first, turning darker toward advanced stages of maturation (Silva et al., 2015), laid in a very characteristic spiral pattern (Quezada, 1974), attached to the underside of leaves by a short pedicel (CABI, 2018) which is an extension of the chorion fixed to abaxial surface (Raga et al., 2016).

Larval stage

Descriptions of the pre-adult stages are given in PM 7/007 (EPPO, in press).

1st instar (crawler): Elongate-oval, 0.30 mm long x 0.15 mm wide (CABI, 2018), with reddish eye spots, short antennae, and rather short legs (Dietz and Zetek, 1920) with 2 long and several shorter, radiating spiny filaments. Colour rather dark brown under the microscope, almost black on the leaf (Dietz and Zetek, 1920).

2nd instar: Legs are reduced but present, ovate-convex, 0.42-0.45 mm long, dark brown to pale black with yellow markings, with the exception of a large, more or less circular spot on the anterior part of the dorsum, which remains a dull green (Dietz and Zetek, 1920) with easily distinguished, radiating spiny filaments.

3rd instar: More convex and much longer, 0.57-0.65 mm long, generally black with a rounded, greenish spot on the anterior part of the abdomen, spiny filaments obvious (CABI, 2018). Dimorphism is also visible in this stage as the female third instars possess an extra pair of cephalic spines (14) in contrast to male third instars that have only 13 pairs (Dubey and Ko, 2012). 

4th instar (puparium or pupal case): Ovate, shiny-black, females about 1.24 mm long, males slightly shorter, up to 1 mm in diameter (CABI, 2018). Submedian spines on the cephalothorax do not reach beyond the margin, except the anterior two pairs. Longitudinal and transverse moulting sutures reach the margin. The eye spots are evident (Dubey and Ko, 2012).  

Adult

Females about 1.7 mm in length, males up to 1.35 mm long (Nguyen et al., 1998). At emergence, the head is pale yellow, legs are whitish, and eyes are reddish-brown (Dietz and Zetek, 1920). 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 (CABI, 2018). 

Detection and inspection methods

Aleurocanthus woglumi infestations are detected by looking for populations and damage symptoms. Honeydew, sooty mould, and honeydew-seeking ants are general signs of phloem feeding insect infestations (CABI, 2018; Carvalho and Francelli, 2021); they can be used to pinpoint the areas where plants may be inspected for the presence of the pest. 

To monitor A. woglumi, translucent fluorescent yellow traps are suggested (Meyerdirk et al., 1979; Summy et al., 1986). Furthermore, fluorescent yellow with a reflectance of 500-550 nm proved to be the most attractive shade of yellow (Meyerdirk et al., 1979; Dowell and Cherry 1981). Visual inspections were more efficient than sticky traps for detecting A. woglumi at low densities (<5% leaves infested) on citrus trees in urban areas (Dowell and Cherry, 1981; EFSA 2019). 

All stages are found on the leaves and several useful taxonomical keys and guides are available in the literature described by Dietz & Zetek (1920), Bink-Moenen (1983), Nguyen et al. (1998) & Dubey and Ko (2012). Moreover, a revised EPPO diagnostic protocol is in press. One GenBank accession is available for A. woglumi mitochondrial COI gene for cytochrome oxidase subunit I: https://www.ncbi.nlm.nih.gov/nuccore/JX281760.1

Aleurocanthus woglumi is liable to be locally spread by natural dispersal. It can disperse by crawling (first instars), and wind (Dietz & Zetek, 1920; EFSA, 2018) but dispersion will be slow (Hoelmer and Grace, 1989). Specific spread rates for this pest have been reported by Dowel and Fitzpatrick (1978) and Oliveira et al. (2001). Adults of A. woglumi are capable of limited down-wind flight (up to 187 m in 24 h) (Oliveira et al., 2001) and, according to theoretical estimates, the natural dispersion of the pest can occur between 200 and 300 km annually, mainly along roads (Carvalho and Francelli, 2021). Plants for planting, fruits, vegetables and cut flowers are the main pathways of spread of A. woglumi over long distances (Raga et al., 2016; Vieira et al., 2017; EFSA, 2018). The fast spread rates detailed in the literature may be due to river and road transport, especially via the transport of citrus fruits from infested areas to areas where juice production occurs (Vieira et al., 2017). Until April 2022, six records of A. woglumi interceptions are listed in the EUROPHYT database on Citrus sp., Citrus hystrix, Annona reticulata, and Musaceae.

Economic impact

Aleurocanthus woglumi egests abundant amounts of sugary honeydew, which covers leaf and fruit surfaces, causing foliage drop and making fruits unmarketable. In Mexico and Florida, short-term (less than one-year) infestations were found to reduce fruit production by up to 50%, and longer-term infestations regularly resulted in almost total loss of production. In Pakistan, losses due to citrus blackfly infestations have been estimated at 5 to 10% with occasional losses of 50 to 60% (Hoelmer and Grace, 1989). Severe infestations cause reduction of citrus yield of about 80% (Aruna et al., 2017; Gomes et al., 2019). Aleurocanthus woglumi is a constant threat to citrus and other crops in the USA and Venezuela. It has not been recorded as a glasshouse pest (Aruna et al., 2017).

Control

The production and economic losses caused by A. woglumi have led to several studies being conducted to identify the most effective strategies for the pest control.

Chemical control of A. woglumi is possible but the reduction of pest population is only temporary (Vieira et al., 2017). Several pesticides have been evaluated for the management of A. woglumi under field conditions and on nursery citrus (Watts et al., 1973; Ba-Angood, 1977; French and Meagher, 1992; Aruna et al., 2017). 

In Texas, organic farmers apply treatments such as sulphur, oils, and microbials to control A. woglumi (Thomas, 2007; Vieira et al., 2017). The application of mineral and vegetable oils, or derivatives may result in improved control strategies for agricultural pests and associated diseases and can cause minimal adverse effects on populations of biological agents (Silva et al., 2012; Vieira et al., 2017). Oils from Eucalyptus globulus, Allium sativum, Gossypium hirsutum, Sesamum indicum, Ricinus communis are alternative control treatments against A. woglumi eggs (90-100% mortality) (Vieira et al., 2017). In Brazil, vegetable oils of Glycine max, Zea mays, Helianthus annuus, Gossypium hirsutum, and extract of neem were evaluated on the fourth-instar nymphs and the mortality rate of puparia was above 90% for all vegetable oils (Silva et al., 2012). Also, the methanolic extract of Mimosa tenuiflora root bark caused significant mortality of A. woglumi nymphs in concentrations above 5 mg/L (Souza et al., 2021). Gamma radiation against citrus blackfly eggs caused egg mortality up to 100% and was recommended as a quarantine treatment (Villavicencio et al., 2009; Vieira et al., 2017).

For biological control, hymenopteran parasitoids such as Encarsia perplexa and Amitus hesperidum have proved economical and effective; they kept A. woglumi below economically damaging levels in much of its distribution range in several parts of the world such as Southern Florida, Trinidad & Tobago, Texas, Mexico, and Dominica (Akrivou et al., 2021). According to Thompson et al. (1987) in Florida, both E. opulenta and A. hesperidum were released and control of A. woglumi was mainly due to E. opulenta. On Merritt Island (Florida), in addition to the two aforementioned parasitoids a hyperparasite (Encarsia smithi) was also released, and although at the beginning of the study A. hesperidum was the dominant parasitoid, ultimately E. opulenta became and remained dominant until the end of the study. Based on field data obtained by Nguyen et al. (1983) E. smithi was ineffective when it was released alone, and a delayed reduction of A. woglumi populations was observed when E. smithi was released together with A. hesperidum and E. opulenta. It was concluded that the delay was due to activity of E. smithi as a hyperparasite of E. opulenta. In Southern Texas, E. opulenta has held population densities of A. woglumi at very low population densities (Summy et al., 1983). As part of a classical biological control programme against A. woglumi in Trinidad, A. hesperidum parasitoids were released, and citrus blackfly populations declined by more than 98% at all sites while parasitism increased to 60-90% (White et al., 2005). In El Salvador, the introduction of E. opulenta brought about the successful biological control of A. woglumi (Quezada 1974). Similar results from the release of E. opulenta were presented by Dowell et al. (1979) in Southern Florida. In Dominica, after four years of the release of A. hesperidum and E. perplexa it was found that A. woglumi populations declined, the parasitoids were present, and no nontarget effects on other Aleyrodidae or their natural enemies were noted (Lopez et al., 2009). In Florida, it has been found that insecticide sprays against other orchard pests can be used without disrupting the parasites of A. woglumi, providing the pesticides used are highly water-soluble (Fitzpatrick & Dowell, 1981); this implies that integrated pest management of citrus orchards should be possible.

Finally, control strategies such as the use of silicon forms (e.g. potassium silicate) to induce citrus defence mechanisms with the increased activity of peroxidase and polyphenol oxidase (Vieira et al., 2016; 2017) and the use of Fusarium volatile in combination with Ricinus communis extract for the control of A. woglumi (Barbosa et al., 2021) are promising.

Phytosanitary risk

Aleurocanthus woglumi mainly presents a risk to citrus in Mediterranean countries. It has a well-documented history of spread around the world from its South-East Asian origin.

EFSA (2018) used the Köppen Geiger climate classification system to determine that A. woglumi occurs in climatic zones that also occur in European countries, making them potentially suitable for establishment. Furthermore, Akrivou et al. (2021) used CLIMEX - a process-oriented climatic niche model - to model the potential global distribution of A. woglumi under an historical climate scenario (centred on 1995), including a spatially explicit irrigation scenario and found that there are current and emerging risks in every continent, including a potential invasion in the Mediterranean Basin. Moreover, CLIMEX simulation under the RCP 8.5 climate change scenario for 2050, indicates that the risk of A. woglumi establishing in Europe is high, making citrus-growing countries a potential hotspot for A. woglumi.

The import of some host plants of A. woglumi for planting from third countries is prohibited (Regulation 2021/2285, Annex VI), while banana (Musa spp.) which is a host for A. woglumi, is exempt by Regulation 2021/2285, Annex XI, Part C. There are many other hosts that can be imported to the EU with a phytosanitary certificate. A phytosanitary certificate should guarantee absence of the pest from consignments of fruit (EFSA, 2018) although a tolerance for A. woglumi may be acceptable during the winter months. It is recommended (EFSA, 2018) that all imported host plants, as planting material and as host cut flowers or branches, should come from a nursery found free from A. woglumi during the previous growing season. Planting material and cut flowers or branches of host plants shipped from countries where A. woglumi occurs are required to be fumigated (EFSA, 2018).

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CABI and EFSA resources used when preparing this datasheet

CABI Datasheet on Pest Aleurocanthus woglumi. Available from: https://www.cabi.org/isc/datasheet/4137 [accessed on 02 March 2022]

EFSA Pest survey card on Aleurocanthus spiniferus and Aleurocanthus woglumi. EFSA supporting publication 2019: EN-1565. 17 pp. https://doi.org/10.2903/sp.efsa.2019.EN-1565   

This datasheet was extensively revised in 2022 by Antigoni Akrivou, Benaki Phytopathological Institute (GR). Her valuable contribution is gratefully acknowledged.

EPPO (2024) Aleurocanthus woglumi. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-04-27)

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

EPPO (1981) Data sheets on quarantine organisms No. 103, Aleurocanthus woglumi. EPPO Bulletin 11(1), 4 pp. https://doi.org/10.1111/j.1365-2338.1981.tb01737.x