Spiraling whitefly Aleurodicus dispersus Russell, 1965 Hemiptera:Aleyrodidae

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Islamic Republic Of Iran Ministry of Jihad-e-Agriculture Plant Protection Organization A Guide for Diagnosis & Detection Of Quarantine Pests Spiraling

1 Islamic Republic Of Iran Ministry of Jihad-e-Agriculture Plant Protection Organization A Guide for Diagnosis & Detection Of Quarantine Pests Spiraling whitefly Aleurodicus dispersus Russell, 1965 Hemiptera:Aleyrodidae Edited by: Ahmad cheraghian Bureau of Plant Pest Surveillance and Pest Risk Analysis 2015

2 Aleurodicus dispersus Russell, 1965 Hemiptera:Aleyrodidae Common name: Spiraling whitefly Synonyms: Economic impact: The economic impact of A. dispersus infestations is due to a combination of three factors. Direct feeding damage results from the extraction of sap from leaves, mainly by larval stages but with adults also contributing. Direct feeding can cause premature leaf drop, reduces plant vigour and yields, but rarely kills plants outright. Indirect damage is due to excreted honeydew that encourages the development of sooty moulds, which hinder photosynthesis and reduce yields. Finally, cosmetic damage is due both to sooty moulds and to the white flocculence secreted by immature stages, which reduces the market-value of crops. Wind-borne flocculence can be unsightly, and may also contribute to asthma attacks (Waterhouse and Norris, 1989). A. dispersus is not usually an economic pest within its native range of Central America and the Caribbean. In Florida, USA, where A. dispersus has been collected from avocados, citrus, guavas and palms, it was initially suspected of being a vector of the mycoplasma causing coconut lethal yellowing disease (Russell, 1965). Lethal yellows was first recorded a short time after A. dispersus became established, and has in the past been responsible for the loss of over 90% of the coconut palms in the Florida Keys (Russell, 1965; Weems, 1971). However, a planthopper is now suspected of being the lethal yellowing disease vector (Waterhouse and Norris, 1989). A. dispersus is currently only a minor pest in Florida. A. dispersus is a recently discovered economic pest in both southern India and west Africa. In India, for example, it has reached pest status on cassava, where up to 580 insects per leaf have been observed (Palaniswami et al., 1995). A range of susceptible crops has been catalogued in Kerala, India, by Ranjith et al. (1996) and in Nigeria by Akinlosotu et al. (1993). It has also recently been recorded on soyabean in Indonesia, where it is a potential economic pest (Kajita et al., 1991). Since its accidental introduction into Taiwan in 1988, it has posed a serious threat to fruit trees, forest trees, food crops, ornamentals and shade trees throughout the country (Wen et al., 1997). A. dispersus currently presents a major threat to Australian agriculture, as it has recently entered Queensland via the Torres Strait islands (Lambkin, 1998). Hosts: Major hosts:citrus, Cocos nucifera (coconut), Glycine max (soyabean), Manihot esculenta (cassava), Musa x paradisiaca (plantain),persea americana (avocado),prunus (stone fruit),psidium guajava (guava) Minor hosts: Acacia (wattles), Acalypha (Copperleaf), Agave americana (american agave), Amaranthus (grain amaranth), Annona squamosa (sugarapple), Arachis hypogaea (groundnut), Areca catechu (betelnut palm), Artocarpus (breadfruit trees), Bauhinia (camel's foot), Begonia, Bougainvillea, Canna, Capsicum (peppers), Carica papaya (papaw), Cassia (sennas), Celtis (nettle tree), Cestrum (jessamine), Chrysalidocarpus lutescens (butterfly palm), Chrysanthemum (daisy), Cinnamomum camphora (camphor laurel), Coffea (coffee), Coleus, Colocasia esculenta (taro), Cucumis (melons, cucuimbers, gerkins), Cucumis melo (melon), Dahlia pinnata (garden dahlia), Eugenia, Euphorbia (spurges), Euphorbia pulcherrima (poinsettia), Ficus, Gossypium (cotton), Hedera (Ivy), Hibiscus (rosemallows), Ipomoea (morning glory), Ipomoea batatas (sweet potato), Jasminum (jasmine), Lactuca sativa (lettuce),

Luffa aegyptiaca (loofah), Lycopersicon esculentum (tomato), Macadamia, Mangifera indica (mango), Manilkara zapota (sapodilla), Monstera deliciosa (ceriman), Morus (mulberrytree), Musa (banana),

3 Luffa aegyptiaca (loofah), Lycopersicon esculentum (tomato), Macadamia, Mangifera indica (mango), Manilkara zapota (sapodilla), Monstera deliciosa (ceriman), Morus (mulberrytree), Musa (banana), Osmanthus fragrans, Phaseolus (beans), Physalis (Groundcherry), Plumeria (frangipani), Pongamia pinnata (Indian beech), Rhododendron (Azalea), Ricinus communis (castor bean), Rorippa indica (indian marshcress), Rosa (roses), Rubus (blackberry, raspberry), Salvia (sage), Schinus terebinthifolius (Brazilian pepper tree), Solanum (nightshade), Solanum melongena (aubergine), Sorghum bicolor (sorghum), Strelitzia, Terminalia catappa (Singapore almond), Vigna (cowpea), Zingiber zerumbet (wild ginger) Geographic distribution: A.dispersus is of Neotropical origin, and is native to Central America and the Caribbean region. It is naturally found in Central and South America, the West Indies and southern Florida, USA. It has been present in the Canary Islands since During the 1970s it began a rapid expansion of its range. It established in Hawaii in 1978 (Paulson and Kumashiro, 1985). It was first reported in the Philippines in 1982, and during the 1980s it spread throughout the islands of the Pacific (Waterhouse and Norris, 1989). More recently, it has been reported in India, Sri Lanka, Africa, Indonesia, Thailand, Taiwan and northern Australia (Wijesekera and Kudagamage, 1990; Martin, 1990; Kajita et al., 1991; Akinlosotu et al., 1993; Wen et al., 1994b; Palaniswami et al., 1995; Carver and Reid, 1996). Asia:Bangladesh, Brunei Darussalam, China, Taiwan, India, Indonesia, Laos, Malaysia, Maldives, Myanmar, Philippine, Singapore, Sri Lanka, Thailand, Vietnam Europe:Portugal, Spain Africa:Benin, Cameroon, Congo, Ghana, Mauritius, Nigeria, Sao Tome and Principe, Togo Central America:Bahamas, Barbados, Belize, Cayman Islands, Costa Rica, Cuba, Dominica,Dominican Republic, Guadeloupe, Guatemala, Haiti, Martinique, Nicaragua, Panama, Puerto Rico. South America:Brazil, Colombia, Ecuador, Peru, Venezuela. North America: U.S.A. Australia and Pacific Island: American Samoa, Australia, Belau, Cook Islands, Federated states of Micronesia, Fiji, French Polynesia, Guam, Kiribati, Marshall Islands, Nauru, New Caledonia, Northern Mariana Islands, Papua New Guinea, Samoa, Solomon Islands, Tokelau, Tonga World distribution map of Aleurodicus dispersus

4 Morphology: Adult female A. dispersus lay a few to several elliptical, smooth-surfaced, yellow-totan coloured eggs (0.3 mm long). The eggs have a short pedicel or subterminal stalk, which is inserted into the host plant during oviposition (Waterhouse and Norris, 1989). The eggs are laid, along with deposits of waxy secretions, in a spiraling pattern. The first larval stage ('crawler') is the only mobile immature stage (0.32 mm long). During the second larval stage (0.5 mm long), a row of mid-back waxy tufts form on the anterior of the body. During the third larval stage (0.65 mm long), short, evenlyspaced, glass-like, waxy rods emanate from distinctive compound pores along the side of the body (Waterhouse and Norris, 1989). Russell (1965) described the pore structure in detail for each immature stage. During the early pupal stage (fourth larval stage), sedentary feeding continues (Russell, 1965; Waterhouse and Norris, 1989). Copious amounts of white, cottony flocculent wax, extending from the dorsum, are then secreted by the pupae; more so than for the larval stages. Young pupae are nearly flat dorsally and flat ventrally. Mature pupae (1.06 mm long) have a swollen ventral surface and are surrounded by a band of wax. The waxy rods emanating from each of the large compound pores, which occur in five subdorsal pairs, extend upward and outward from the back. The waxy rods can be up to 8 mm in length (Waterhouse and Norris, 1989). Pupae are colourless or yellowish, nearly oval and mm long and mm wide (Russell, 1965). Fully mobile adults emerge from the pupae. The pupal cases or puparia are used for identification purposes. Martin (1987, 1996) provided keys to tropical pest species based on pupal morphology. Adult A. dispersus are white and coated with a fine dust-like waxy secretion. Body length of males 2.28 mm, and females 1.74 mm. Both sexes are winged. Wings are clear soon after emergence, but turn white due to the wax coating after a few hours. Pale or dark spots may occasionally occur on the forewings. Antennae have seven segments and eyes are dark reddish-brown (Waterhouse and Norris, 1989). Adult females do not have pores, while males have numerous circular pores on the abdomen (Russell, 1965). The following characters and diagram, should enable accurate identification: abdomen with four pairs of large compound pores, all approximately the same size abdominal compound pores situated on segments III-VI abdominal compound pores each normally with a finger-like projection at its centre vasiform orifice slightly wider than long central area of dorsum with scattered `Saturn-like' pores, each pore divided by a fine septum across its centre

5 The line drawing, by Arthur Cushman, that accompanied the original description of the puparium of Aleurodicus dispersus

7 Eggs of Aleurodicus dispersus

Biology and ecology: Females, collected in the field in Sri Lanka and studied in the laboratory, each laid 14-26 eggs in a loose spiral on the underside of leaves. The common name of A.

The eggs hatched after 7-10 days, the first and second larval instars lasted for 6-9 days in total, the third instar for 5-13 days and the fourth (pupae) 5-16 days.

The leaf structure of the host plant appears to affect feeding preference (Wen et al., 1994a). The larval stages and adults feed by sucking phloem sap from leaves.

11 Biology and ecology: Females, collected in the field in Sri Lanka and studied in the laboratory, each laid eggs in a loose spiral on the underside of leaves. The common name of A. dispersus, the spiralling whitefly, is derived from this characteristic egg-laying pattern, although other species of aleurodicine whitefly also lay eggs in spiral patterns (Martin, 1990). The eggs hatched after 7-10 days, the first and second larval instars lasted for 6-9 days in total, the third instar for 5-13 days and the fourth (pupae) 5-16 days. Adults lived for about 2 weeks (Wijesekera and Kudagamage, 1990). The immature stages of A. dispersus are found on the lower leaf surface of host plants. The leaf structure of the host plant appears to affect feeding preference (Wen et al., 1994a). The larval stages and adults feed by sucking phloem sap from leaves. Copious honeydew is excreted which coats surrounding surfaces and often develops a layer of sooty mould when colonies are poorly controlled. Wen et al. (1994b) described the effects of temperature on development rate and fecundity. Adults were active between C and maximum female fecundity occurred at 25 C. A. dispersus populations were found all year round in southern Taiwan, building up rapidly in October, reaching a peak in November, and then declining gradually after December. The developmental time (from oviposition to eclosion) of the pest at 25 C on poinsettia, canna, guavas and pawpaws was 26.1, 25.0, 29.4 and 26.1 days; immature mortality was 26.9, 24.5, 33.3 and 27.8%; and fecundity was 65.2, 35.8, 51.3 and 58.0 eggs per female, respectively (Wen et al., 1996). Females begin laying eggs within a few days of emergence, and continue to lay throughout their lifetime. The rate of population growth can be rapid. In one experiment, 20 pairs produced 1549 individuals in 37 days (Waterhouse and Norris, 1989). Unmated females produce only male progeny, while mated females produce a mixture of male and female progeny. Adults are most active in the morning, but mate in the afternoon (Waterhouse and Norris, 1989). In the USA, A. dispersus is limited to southern coastal areas in Florida where mild winter temperatures occur. Extreme mortality occurs at low temperatures (below 10 C), which limits the northward spread of A. dispersus in the Americas (Cherry, 1979). Aleurodicus dispersus

curled. Infestation spread from the bottom leaves to the top (Palaniswami et al.

12 Symptoms: In cassava, A. dispersus infestation caused yellowish speckling of the leaves, and in severe infestation the leaves crinkled and curled. Infestation spread from the bottom leaves to the top (Palaniswami et al., 1995) Copious honeydew is excreted which coats surrounding surfaces and often develops a layer of sooty mould. Symptoms by affected plant part Fruits/pods : Leaves: abnormal colours; honeydew or sooty mould. Damage of Aleurodicus dispersus

13 Damage of Aleurodicus dispersus

Means of movement and dispersal: The eggs and larvae of A. dispersus may be transported on leaves, and these early insect stages are often cryptic.

Plant parts liable to carry the pest in trade/transport - Fruits (inc. Pods): Eggs; borne externally. - Leaves: Eggs, Larvae; borne externally.

Roots/ - Stems (above Ground)/Shoots/Trunks/Branches - True Seeds (inc. Grain)/ - Wood. Phytosanitary significance: A.

Quarantine areas have been declared in Queensland, Australia.

14 Means of movement and dispersal: The eggs and larvae of A. dispersus may be transported on leaves, and these early insect stages are often cryptic. The eggs may also be transported on fruit. Newly-dead foliage may harbour puparia, which are usually detected by the presence of woolly secretions. Plant parts liable to carry the pest in trade/transport - Fruits (inc. Pods): Eggs; borne externally. - Leaves: Eggs, Larvae; borne externally. Plant parts not known to carry the pest in trade/transport - Bark/ - Bulbs/Tubers/Corms/Rhizomes - Growing Medium Accompanying Plants - Flowers/Inflorescences/Cones/Calyx - Roots/ - Stems (above Ground)/Shoots/Trunks/Branches - True Seeds (inc. Grain)/ - Wood. Phytosanitary significance: A. dispersus presents a serious phytosanitary risk to tropical and subtropical areas on the edges of its current range. Quarantine areas have been declared in Queensland, Australia. The movement of plants, plant material, and fruits out of quarantine areas can only proceed after official inspections (Lambkin, 1998). The spread of A. dispersus on citrus is of particular concern, in Australia, Mexico and other countries. Only the climatic limitations will ultimately determine the final distribution of this highly invasive and polyphagous pest. It has not stopped moving yet (2003). A. disperses is quarantine pest for Iran. Detection and inspection host for Aleurodicus dispersus

15 Detection and inspection: When A. dispersus are abundant they are conspicuous on leaves due to the white flocculence that covers their bodies (Russell, 1965). They are found on the undersides of leaves, often associated with sticky honeydew and sometimes sooty mould growth. A.dispersus were found in significantly higher numbers in the upper canopy than in the middle and the lower canopy on guava (Shah Alam et al., 1997). Detection and inspection host for Aleurodicus dispersus

16 References: Abai, M. (1984).List of forest trees and shrubs of Iran. Plant pests and Diseases Rech. Inst.,Tehran, 147p. Barouti,S.,A.alavi,2004,Plant Nematology,Principles, Parasitic and Quarantine Nematode in Iran., p. Behdad,E.,1984.Pests of Fruit Crops in Iran,Sepehr pub,tehran,822p. Esmaile,M.1983, Pests of Fruit Crops in Iran, Sepehr pub,tehran,366p. CAB International Crop Protection Compendium Edition. CAB International. Wallingford, Oxon, UK. Modarres Awal, M.2012.List of Agricultural pests and Their Natural Enemies in Iran. Revised Edition, Ferdowsi university Prss,877p. Salavatean, Mer.1996, Plant quarantine in Iran, Research Institute,Ministey of Agriculture pub,279p. eol.org/pages/

World distribution map of Aleurocanthus spiniferus (Quaintance, 1903)

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