Bemisia tabaci(BEMITA)
EPPO Datasheet: Bemisia tabaci
IDENTITY
Authority: (Gennadius)
Taxonomic position: Animalia: Arthropoda: Hexapoda: Insecta: Hemiptera: Sternorrhyncha: Aleyrodidae
Other scientific names: Aleurodes tabaci Gennadius, Bemisia achyranthes Singh, Bemisia argentifolii Bellows & Perring, Bemisia bahiana Bondar, Bemisia emiliae Corbett, Bemisia goldingi Corbett, Bemisia gossypiperda Misra & Lamba, Bemisia hibisci Takahashi, Bemisia inconspicua (Quaintance), Bemisia longispina Priesner & Hosny, Bemisia lonicerae Takahashi, Bemisia manihotis Frappa, Bemisia minima Danzig, Bemisia minuscula Danzig, Bemisia nigeriensis Corbett, Bemisia rhodesiaensis Corbett, Bemisia vayssieri Frappa
Common names in English: cassava whitefly, cotton whitefly, silverleaf whitefly, sweet-potato whitefly, tobacco whitefly
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Notes on taxonomy and nomenclature
The genus Bemisia contains 37 species and is thought to have originated from Asia (Mound & Halsey, 1978). B. tabaci, being possibly of Indian origin (Fishpool & Burban, 1994), was described under numerous names before its morphological variability was recognized. For a full list of synonyms see Mound & Halsey (1978). Three distinct groups of B. tabaci have been identified by comparing their mitochondrial 16S ribosomal subunits. These are: 1) New World, 2) India/Sudan, 3) remaining Old World (Frohlich & Brown, 1994).
The first reports of a newly evolved biotype of B. tabaci, the B biotype, appeared in the mid-1980s (Brown et al., 1995b). Commonly referred to as the silverleaf whitefly or poinsettia strain, the B biotype has been shown to be highly polyphagous and almost twice as fecund as previously recorded strains, and has been documented as being a separate species: B. argentifolii (Bellows et al., 1994). The B biotype is able to cause phytotoxic disorders in certain plant species, e.g., silverleaf in squashes (Cucurbita sp.) and this is an irrefutable method of identification (Bedford et al., 1992, 1994a). A distinctive non-specific esterase banding pattern is also helpful in identification (Brown et al., 1995a), but not infallible (Byrne et al., 1995).
One may note that the presence or absence of spines on the 'puparium' is known to be determined by the smoothness or hairiness of the leaves of the host plant (Bedford et al., 1994a), yet the absence of a small anterior submarginal seta on the 4th larval instar/puparium stage has been described as one of the identifying morphological features of so-called B. argentifolii. No European populations of B. tabaci studied so far can be distinguished from so-called B. argentifolii by this or other morphological features, although these populations do not induce phytotoxic disorders or exhibit B biotype esterase banding patterns. It may be noted, finally, that several other biotypes (up to K) have been described (Brown et al., 1995b), which supports the idea of a species complex, rather than of a number of distinct species such as B. argentifolii. Several important taxonomic problems exist because, as a result of morphological studies of Bemisia species and others, it appears that morphological characteristics of many whitefly species are very poorly understood (Martin, 2003). Molecular techniques appear to solve some problems in whitefly phylogenies and they should be studied in synchrony with more thorough morphological studies of at least pupae and adults. This is indeed a fruitful field for further research (Gill and Brown, 2010).
Bemisia tabaci is known for its genetic diversity and is considered a complex of biotypes (Brown et al., 1995b; Perring, 2001; Xu et al., 2010) or, as suggested, a complex of distinct cryptic species (De Barro et al., 2011). Recent report suggested that B. tabaci is considered a complex of at least 40 morphologically indistinguishable species (Bertin et al., 2021). The biotypes and species are largely differentiated based on biochemical or molecular polymorphism markers and differ in their biological characteristics such as host plant range, the capacity to cause plant disorders, attraction to natural enemies, expression of resistance and plant virus-transmission capabilities (e.g., Bedford et al., 1994b; Sanchez-Campos et al. , 1999; Horowitz et al., 2005). The B biotype is the most widespread biotype on a worldwide scale (it belongs to the Middle East Asia Minor 1—MEAM1 group) and is hypothesized to originate from the Middle East–Asia Minor region (De Barro et al., 2011). The confirmation of the identity of this (previously reported) biotype occurred in the late 1980s (Costa et al., 1993), following extensive outbreaks of B. tabaci in the South-West USA. An additional common biotype Q (belonging to the Mediterranean—MED group), which possibly originated in the Iberian Peninsula, has since spread globally (Horowitz et al., 2003; Chu et al., 2010). So far, the genetic group of B. tabaci MEAM1 (biotype B) is considered the most common B. tabaci species, and it has probably been dispersed throughout the world by international trade, mainly with ornamentals.
Early reports have indicated that invasions of a new biotype can result in the displacement of indigenous biotypes as a result of competition or possibly other reasons for example: B biotype displaced A biotype in the USA (Brown et al., 1995b); the displacement of B by non-B populations such as the Q biotype (Guirao et al., 1997); Q biotype displaced B when insecticide selection occurred (Horowitz et al. 2005). Since then, many reports have shown similar changes in biotypes/species of B. tabaci elsewhere, apparently due to frequent use of insecticides and development of insecticide resistance. Since 2005, a shift of biotype B to Q occurred in many locations in China (e.g., Teng et al., 2010). The opposite phenomenon has been observed on cotton fields in Israel, where since 2009, a significant shift in the biotype ratios has been observed: the B biotype replaced the Q biotype in cotton as well as in other crops.
EU Categorization: A1 Quarantine pest (Annex II A), PZ Quarantine pest (Annex III)
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EPPO Code: BEMITA
HOSTS 2023-01-11
Until the 1990s, B. tabaci was mainly known as a pest of field crops in tropical and sub-tropical countries: cassava (Manihot esculenta), cotton (Gossypium sp.), sweet potatoes (Ipomoea batatas), tobacco (Nicotiana sp.) and tomatoes (Solanum lycopersicum). Its host plant range within any particular region was small, yet B. tabaci had a composite range of around 300 plant species within 63 families (Mound & Halsey, 1978). With the evolution of the highly polyphagous B biotype, B. tabaci has now become a pest of protected crops in many parts of the world, especially Capsicum sp., courgettes (Cucurbita pepo), cucumbers (Cucumis sativus), Hibiscus sp., Gerbera sp., Gloxinia sp., lettuces (Lactuca sp.), poinsettia (Euphorbia pulcherrima) and tomato. B. tabaci moves readily from one host species to another and has more recently been estimated as having a host range of more than 1000 species (mainly belonging to the families: Asteraceae, Brassicaceae, Convolvulaceae, Cucurbitaceae, Euphorbiaceae, Fabaceae, Malvaceae, Solanaceae) (Basu, 1995; Oliveira et al., 2001; Simmons et al. ,2008; Li et al., 2011; EFSA, 2013).
According to EFSA, it is often difficult to distinguish between true hosts of B. tabaci (i.e., insects feed and complete its entire life cycle) and incidental hosts. The presence of B. tabaci on a particular plant species is not proof of host suitability. Feeding behaviour or oviposition are also unreliable host indicators because whiteflies can check a plant several times before rejecting it or laying eggs. For the purpose of risk assessment, the more suitable a plant is as a host (feeding and successful nymphal development), the higher the risk it presents as a commodity.
Various literature sources (e.g., Simmons et al., 2008; Li et al., 2011) suggest three categories of host plants of B. tabaci: (i) host plant status (full life cycle supported – confirmed by experiments); (ii) host plant status confirmed from field observations; (iii) unconfirmed data. Due to its extensive host plant range, suitable hosts for B. tabaci are found in almost every environment, including agricultural and horticultural crops and among wild plants (EFSA, 2013; CABI, 2021).
Host list: Abelmoschus esculentus, Amaranthus blitoides, Amaranthus retroflexus, Asteraceae, Atriplex semibaccata, Borago officinalis, Brassica rapa subsp. sylvestris, Brassicaceae, Bryonia dioica, Capsella bursa-pastoris, Capsicum annuum, Convolvulaceae, Cucumis sativus, Cucurbita pepo, Cucurbitaceae, Erigeron canadensis, Euphorbia pulcherrima, Euphorbiaceae, Fabaceae, Gerbera jamesonii, Glycine max, Gossypium hirsutum, Hibiscus, Ipomoea batatas, Lactuca sativa, Lactuca serriola, Lavandula coronopifolia, Malvaceae, Manihot esculenta, Melissa officinalis, Mentha, Nicotiana tabacum, Ocimum basilicum, Oxalis pes-caprae, Phaseolus vulgaris, Salvia officinalis, Salvia rosmarinus, Senecio vulgaris, Sinningia, Solanaceae, Solanum lycopersicum, Solanum melongena, Solanum nigrum, Sonchus oleraceus, Stellaria media, Tagetes erecta, Thymus serpyllum, Urtica urens, plants, vegetable plantsGEOGRAPHICAL DISTRIBUTION 2023-01-11
B. tabaci has a global presence. However, certain areas within Europe are still free from the pest or it is transient, e.g., Finland, Sweden, Republic of Ireland and the United Kingdom (Cuthbertson and Vänninen, 2015) as they have protected zones against this invasive pest.
In Canada, B. tabaci is a glasshouse pest; it is not established outdoors (Broadbent et al., 1989; Howard et al., 1994; CFIA Canada, 2005, per J.A. Garland).
In the USA, the MEAM1 species is frequent outdoors and the MED species used to be found just in protected crops (McKenzie et al., 2012); however, recently, the MED species was observed especially on hibiscus plants located in residential areas in Florida (McKenzie & Osborne 2017).
EPPO Region: Algeria, Austria, Azerbaijan, Belgium, Bosnia and Herzegovina, Bulgaria, Croatia, Cyprus, Czech Republic, Finland, France (mainland, Corse), Georgia, Germany, Greece (mainland, Kriti), Hungary, Israel, Italy (mainland, Sardegna, Sicilia), Jordan, Kyrgyzstan, Malta, Montenegro, Morocco, Netherlands, Norway, Poland, Portugal (mainland, Madeira), Romania, Russia (Southern Russia), Slovenia, Spain (mainland, Islas Baleares, Islas Canárias), Switzerland, Tunisia, Türkiye, Ukraine, United Kingdom (England), UzbekistanAfrica: Algeria, Angola, Benin, Burkina Faso, Cameroon, Cape Verde, Central African Republic, Chad, Congo, Congo, Democratic republic of the, Cote d'Ivoire, Egypt, Equatorial Guinea, Eritrea, Ethiopia, Gambia, Ghana, Guinea, Guinea-Bissau, Kenya, Libya, Madagascar, Malawi, Mauritius, Mayotte, Morocco, Mozambique, Nigeria, Reunion, Rwanda, Senegal, Seychelles, Sierra Leone, Somalia, South Africa, Sudan, Tanzania, Togo, Tunisia, Uganda, Zimbabwe
Asia: Afghanistan, Bahrain, Bangladesh, Brunei Darussalam, Cambodia, China (Anhui, Beijing, Fujian, Guangdong, Guangxi, Guizhou, Hainan, Hebei, Heilongjiang, Henan, Henan, Hubei, Hunan, Jiangsu, Jiangxi, Liaoning, Neimenggu, Shaanxi, Shandong, Shanghai, Shanxi, Sichuan, Tianjin, Xianggang (Hong Kong), Xinjiang, Yunnan, Zhejiang), India (Andaman and Nicobar Islands, Andhra Pradesh, Assam, Bihar, Delhi, Gujarat, Haryana, Himachal Pradesh, Jammu & Kashmir, Karnataka, Kerala, Lakshadweep, Madhya Pradesh, Maharashtra, Meghalaya, Odisha, Punjab, Rajasthan, Tamil Nadu, Telangana, Tripura, Uttar Pradesh, West Bengal), Indonesia (Java, Sulawesi, Sumatra), Iran, Iraq, Israel, Japan (Honshu, Shikoku), Jordan, Korea, Republic, Kuwait, Kyrgyzstan, Laos, Lebanon, Malaysia (Sarawak, West), Maldives, Myanmar, Nepal, Oman, Pakistan, Philippines, Saudi Arabia, Singapore, Sri Lanka, Syria, Taiwan, Tajikistan, Thailand, Turkmenistan, United Arab Emirates, Uzbekistan, Vietnam, Yemen
North America: Canada (Alberta, British Columbia, New Brunswick, Nova Scotia, Ontario, Québec), Mexico, United States of America (Alabama, Arizona, California, Connecticut, District of Columbia, Florida, Georgia, Hawaii, Illinois, Indiana, Kentucky, Louisiana, Maine, Maryland, Massachusetts, Michigan, Mississippi, New Hampshire, New Jersey, New York, North Carolina, Ohio, Oregon, Pennsylvania, South Carolina, Tennessee, Texas, Vermont, Washington)
Central America and Caribbean: Antigua and Barbuda, Bahamas, Barbados, Belize, Bermuda, Costa Rica, Cuba, Dominica, Dominican Republic, El Salvador, Grenada, Guadeloupe, Guatemala, Haiti, Honduras, Jamaica, Martinique, Montserrat, Netherlands Antilles, Nicaragua, Panama, Puerto Rico, Saint Lucia, St Kitts-Nevis, Trinidad and Tobago, Virgin Islands (British)
South America: Argentina, Bolivia, Brazil (Bahia, Distrito Federal, Goias, Maranhao, Mato Grosso, Mato Grosso do Sul, Minas Gerais, Parana, Pernambuco, Rio de Janeiro, Rio Grande do Sul, Sao Paulo), Colombia, French Guiana, Guyana, Paraguay, Peru, Uruguay, Venezuela
Oceania: American Samoa, Australia (New South Wales, Northern Territory, Queensland, South Australia, Tasmania, Western Australia), Cook Islands, Fiji, French Polynesia, Guam, Kiribati, Marshall Islands, Micronesia, Nauru, New Caledonia, New Zealand, Niue, Northern Mariana Islands, Palau, Papua New Guinea, Samoa, Solomon Islands, Tonga, Tuvalu, Vanuatu
BIOLOGY 2023-01-11
Biological characteristics of B. tabaci can be summarized based on Byrne & Bellows, 1991; De Barro, 1995; Stansly & Naranjo, 2010 and EFSA, 2013.
Eggs (pear shaped with a pedicel point at the base) are usually laid in circular groups, on the underside of leaves, touching the surface and the long axis perpendicular to the leaf. They are anchored by a pedicel which is inserted into a fine slit made by the female in the tissues, and not into stomata, as in the case of many other aleyrodids. Eggs are whitish when first laid but gradually turn brown. Hatching occurs after 5-9 days at 30°C but, like many other developmental rates, this depends very much on host species, temperature and humidity.
On hatching, the first instar, or 'crawler', is flat, oval and scale-like. This first instar is the only larval stage of this insect which is mobile. It moves from the egg site to a suitable feeding location on the lower surface of the leaf where its legs are lost in the ensuing moult and the larva becomes sessile. It does not therefore move again throughout the remaining nymphal stages. The first three nymphal stages last 2-4 days each (this could however vary with temperature). The fourth nymphal stage, called the puparium, lasts about 6 days and it is within the latter period of this stage that the metamorphosis to adult occurs.
The adult emerges through a 'T'-shaped rupture in the skin of the puparium and spreads its wings for several minutes before beginning to powder itself with a waxy secretion from glands on the abdomen. Copulation begins 12-20 h after emergence and takes place several times throughout the life of the adult.
In general, the life span of the female is two to three weeks (Drost et al., 1998; Henneberry & Castle, 2001) but can extend to 60 days. The life of the male is generally much shorter, being between 9 and 17 days. Each female lays up to 300 eggs during her lifetime, although the B biotype has been shown to lay more eggs. Each group of eggs is laid in an arc or a circular around the female. Eleven to fifteen generations can occur within one year.
Bemisia tabaci is a vector of more than 400 plant viruses (Jones, 2003; Hogenhout et al., 2008, Ghosh and Ghanim, 2021), and in some cases, viral diseases reduce yield and may cause total crop loss. It is a vector of viruses in the genera of Begomovirus, Crinivirus, Potyviridae, Torradovirus, Carlavirus and Cytorhabdovirus (Ghosh & Ghanim, 2021).
The begomoviruses (formerly geminiviruses) transmitted by B. tabaci are by far the most important viruses agriculturally, causing yield losses to crops of between 20 and 100% (Brown & Bird, 1992; Cathrin and Ghanim, 2014). Begomoviruses cause a range of different symptoms which include yellow mosaics, yellow veining, leaf curling, stunting and vein thickening. Begomoviruses associated with Cotton leaf curl Disease (CLCuD) cause severe losses to cotton crop, worldwide. Five species of begomovirus complexes i.e., cotton leaf curl Multan virus (CLCuMuV), cotton leaf curl Bangalore virus (CLCuBaV), cotton leaf curl Kokhran virus (CLCu-KoV), cotton leaf curl Gezira virus (CLCuGeV) and cotton leaf curl Alabad virus (CLCuAlV) are presently associated with CLCuD (Saleem et al., 2016). Tomato crops throughout the world are particularly susceptible to many different begomoviruses, and in most cases exhibit yellow leaf curl symptoms. Most of these epidemics in the Middle East and Europe are attributed to tomato yellow leaf curl virus (TYLCV) but may also be caused by other begomoviruses (Sánchez-Campos et al., 1999). TYLCV has also recently been recorded in the Americas, but several other, exclusively American, tomato begomoviruses have now been described, e.g. tomato mottle virus (EPPO/CABI 1996). Begomoviruses also cause heavy yield losses in their respective hosts. Dual infections have also been shown to occur. Several of these viruses are now quarantine pests for the EPPO region (e.g., bean golden mosaic, squash leaf curl, tomato mottle viruses, and lettuce infectious yellows closterovirus; tomato yellow leaf curl virus (EPPO/CABI, 1996).
The emergence of the B biotype of B. tabaci, with its ability to feed on many different host plants has given whitefly-transmitted viruses the potential to infect new plant species. This has already been shown to have occurred in the Americas.
Five begomoviruses are known to be present in Europe. Some of them have been shown to no longer be transmissible by B. tabaci: e.g. abutilon mosaic virus (Bedford et al., 1994a, Banks et al., 1999), possibly through many years of vegetative propagation of their ornamental host plants. The others are two different transmissible TYLCVs that are causing major crop losses within the tomato industries of Spain (mainland and the Canary Islands), Portugal and Italy. Indigenous weed species such as Solanum nigrum and Datura stramonium have also been shown to be field reservoirs for these tomato viruses (Bedford et al., 1994a) and may be the source of others yet to be identified within Europe. Two B. tabaci-transmitted belong to genus Crinivirus, are also now affecting European crops, including those in the Canary Islands. Cucurbit yellow stunting disorder is causing severe damage to cucumbers and melons in southern Europe (Celix et al., 1996), along with tomato chlorosis virus (Navas-Castillo et al., 1999). There are also reports of a third Crinivirus, tomato infectious chlorosis virus, in Europe (Duffus et al., 1996) although this virus currently appears not to be of economic significance. In addition, a Bemisia-transmitted potyvirus, cucumber vein yellowing virus (CVYV), appeared in cucumber crops in southern Spain for the first time in 2000 (Cuadrado et al., 2001). Despite a crop destruction programme to eradicate this virus, it has recently spread to melon crops in the region. Protected zones (e.g., the United Kingdom and Finland) within Europe remain free from damaging begomoviruses (Cuthbertson & Vänninen, 2015).
There is a recent knowledge of whitefly-mediated transmission (B. tabaci MEAM1) of two recombinant poleroviruses (Luteoviridae), a virus group with an ssRNA genome that was only known to be associated with aphids (Ghosh & Ghanim, 2021).
DETECTION AND IDENTIFICATION 2023-01-11
Symptoms
The feeding of adults and nymphs causes chlorotic spots to appear on the surface of the leaves. Depending on the level of infestation, these spots may coalesce until the whole of the leaf is yellow, apart from the area immediately around the veins. Such leaves are later shed. The honeydew produced by the feeding of the nymphs covers the surface of the leaves and can cause a reduction in photosynthetic potential when colonized by moulds. Honeydew can also disfigure flowers and, in the case of cotton, can cause problems in processing the lint. With heavy infestations, plant height, number of internodes and quality and quantity of yield can be affected. The larvae of the B biotype of B. tabaci are unique in their ability to cause phytotoxic responses to many plant and crop species. These include a severe silvering of courgette leaves, white stems in pumpkin, white streaking in leafy brassica crops, uneven ripening of tomato fruits, reduced growth, yellowing and stem blanching in lettuce and kai choy (Brassica campestris) and yellow veining in carrots and Lonicera spp. (Bedford et al., 1994a; 1994b).
Morphology
Eggs
Pear-shaped with a pedicel spike at the base, about 0.2 mm long.
Nymphal stages
The early first instar, or 'crawler', is flat, oval and scale-like. Other three nymphal stages are yellow-white 'scales', 0.3-0.6 mm long.
Puparium
Flat, irregular oval shape, 0.7 mm long. On a smooth leaf the 'puparium' lacks enlarged dorsal setae but, if the leaf is hairy, two to eight long dorsal setae are present.
Adult
About 1 mm long; the male slightly smaller than the female. The body and both pairs of wings are covered with a powdery, waxy secretion, white to slightly yellowish. Differentiation of whitefly species by means of the adults is difficult, although close observation of adult eye morphology will often show differences in ommatidial arrangements between species. However, at rest B. tabaci has wings more closely pressed to the body than Trialeurodes vaporariorum which is larger and more triangular in appearance.
The fourth instar/puparium is used to distinguish between B. tabaci and T. vaporariorum as glasshouse pests. T. vaporariorum is 'pork-pie shaped', being regularly ovoid, with straight sides (viewed laterally) and in most instances, 12 large, wax setae; B. tabaci has an irregular 'pancake- like' oval shape, oblique sides and shorter, finer setae. The numbers of enlarged setae vary with the morphology of the host plant, however, and the two caudal setae are always stout and nearly always as long as the vasiform orifice. The length of caudal setae can be used to identify some Bemisia species.
See Martin (1987) and Gill & Brown (2010) for more information on the identification of B. tabaci.
Diagnostic protocols for B. tabaci as well as some common viral diseases, which the whiteflies transmit are available. PM 7/35 (EPPO 2004) describes a diagnostic protocol for Bemisia tabaci. Bemisia tabaci is an unresolved species complex. The revision of the diagnostic protocol will be initiated when the taxonomy is resolved but in the meantime the experts from the EPPO Panel on Diagnostics in Entomology agreed that the current protocol was appropriate regarding morphology.
PM 7/050 (EPPO 2005) describes a diagnostic protocol for tomato yellow leaf curl begomovirus (TYLCV) and tomato mottle begomovirus (ToMoV) and PM 7/118 (EPPO 2013) describes a diagnostic protocol for tomato chlorosis virus and tomato infectious chlorosis virus (criniviruses)
Detection and inspection methods
Large numbers of chlorotic spots are seen on the leaves of infested plants, which may also be stained by honeydew and associated sooty moulds. Leaf curling, yellowing, mosaics or yellowing-veins could indicate the presence of whitefly-transmitted viruses and phytotoxic responses such as a severe silvering of courgette and melon leaves indicating the presence of a B biotype B. tabaci infestation, the immature stages being mainly responsible for this symptom (Costa et al., 1993). A close observation of the underside of the leaves will show the tiny yellow/white larval instars (immature stages, nymphs) and in severe infestations, when the plant is shaken, numerous small white adult-whiteflies will flutter out and quickly resettle. These symptoms do not appreciably differ from those of Trialeurodes vaporariorum, the glasshouse whitefly, which is common throughout Europe.
For sampling and identification, the underside of the leaves should be inspected carefully to detect different life stages of the pest (eggs, larvae, pupae) or signs of it and honeydew (see also EPPO, 2016 and CABI, 2021). In addition to direct observations on plants, the use of yellow sticky traps for whitefly monitoring is common (Gerling & Horowitz, 1984; Pinto-Zevallos & Vänninen, 2013).
PATHWAYS FOR MOVEMENT 2023-01-11
Adults of B. tabaci do not fly very efficiently but, once airborne, they can be transported quite large distances by the wind (Byrne, 1999; Isaacs et al., 1999). All stages of the pest are liable to be carried on planting material and cut flowers of host species. Ornamental trade, primarily the poinsettia pathway, was considered as the main route of introduction and spread of B. tabaci MEAM1 and Med in the United States (Dalton, 2006) and New Zealand (Drayton et al., 2009). Thus, the international trade in poinsettia is considered to have been a major means of dissemination within the EPPO region of the B biotype of B. tabaci (see also EPPO 2011 and EFSA 2013).
PEST SIGNIFICANCE 2023-01-11
Economic Impact
B. tabaci has been known as a pest of cotton and other tropical or semi-tropical crops in Asia, Africa, South America and the warmer parts of Europe and, has been effectively controlled by insecticides. However, in the southern states of the USA in 1991, due to invasion of biotype B, it was estimated to have caused combined losses of 500 million USD to the winter vegetable crops (Perring et al., 1993). Economic losses due to B. tabaci are enormous mainly in Africa, the Americas, Australia, Asia and Middle East (Horowitz et al., 2020). Henneberry & Faust (2008) summarized some reports related to economic losses, which estimated approximately 10 billion USD during the years 1980 to 2000. In India it was estimated that the losses in 1991 to various bean crops were approximately 300 million USD (Henneberry & Faust, 2008). Nevertheless, losses due to virus diseases transmitted by B. tabaci were considered the most damaging: Briddon (2003) reported that Cotton leaf curl disease caused 5 billion USD losses to cotton in Pakistan from 1992 to 1997, and Legg et al. (2014) estimated that cassava mosaic disease (CMD) and cassava brown streak disease (CBSD) caused annual production losses of more than 1 billion USD in Africa.
Control
Following outbreaks of B. tabaci in fields and greenhouses, the use of insecticides has increased rapidly. However, difficulties with its effective control on many crops are now being experienced worldwide due to insecticide resistance. Insecticide resistance in B. tabaci is widespread to the most used insecticides (Horowitz et al., 2020). Among the common cryptic species, MED (biotype Q) is considered more resistant than the MEAM1 (biotype B) to insecticides such as pyriproxyfen and neonicotinoids (e.g., Horowitz et al., 2005). However, in recent years, there are other species of Bemisia including MEAM1, Asia I and Asia II-1 that have developed high resistance levels to various groups of insecticides (e.g., Naveen et al., 2017; Dângelo et al., 2018). It appears that no single control treatment can be used on a long-term basis against this pest and that the integration of a number of different control agents needs implementing for an effective Integrated Pest Management (IPM) strategy. Each area where B. tabaci is occurring needs assessing individually and an appropriate IPM programme should be specifically designed. For example, the use of biological control agents such as the entomopathogenic fungi, Lecanicillium lecanii, Beauveria bassiana; the predatory mite Amblyseius swirskii some predatory Mirid species, and parasitoids belonging to Eretmocerus and Encarsia spp) is recommended (Horowitz et al., 2020). However, these agents can never bring infestation levels of B. tabaci down to a level that stops virus transmission. The use of virus- resistant crops should be investigated. Future control methods involving a disruption of the vector-virus-host plant cycle and the use of the RNA-interference method are presently under investigation.
Phytosanitary risk
The risk to the EPPO region is primarily to the glasshouse industry in northern countries, and mainly concerns the B and Q biotypes (MEAM1 and Med). Since its recent introduction to several of these countries, the pest has proved particularly difficult to combat because of its polyphagy, its resistance to many insecticides and its disruption of biological control programmes (Della Giustina et al., 1989). Very few countries remain free from B. tabaci, illustrating the difficulty of preventing its movement in international trade. Furthermore, it is likely that it is already present, but unreported, as a pest of field crops, in other countries in the south of the EPPO region. In addition, the Q biotype may now displace other biotypes on outdoor crops in Southern Europe and cause much greater damage.
PHYTOSANITARY MEASURES 2023-01-11
Because of the difficulty of detecting low levels of infestation in consignments, it is best to ensure that the place of production is free from the pest. Particular attention is needed for consignments from countries where certain B. tabaci transmitted viruses, listed in quarantine lists, are present.
In EPPO Standard PM 10/13 (EPPO 2009) a treatment programme aimed at eradication of B. tabaci is suggested. It might be done in those parts of the EPPO region where the pest is not established, or for eradication of new and invasive biotypes (or species). It is proposed to treat ornamental production sites with insecticides and use various methods of applications (e.g., spray, fogs, space treatment, soil drench and granular). A treatment schedule is detailed in the EPPO Standard and applications of various insecticides have been found successfully in eradicating outbreaks of B. tabaci on ornamental nurseries in the United Kingdom.
Poinsettias are imported as cuttings and this is the most common pathway for the introduction of B. tabaci to ornamental nurseries in a number of EPPO countries. An eradication programme is suggested in EPPO Standard PM 10/17 (EPPO, 2011) and treatment involves dipping the cuttings in insecticides before the cuttings are propagated. Mineral oil or other types of oils were found effective treatments against all stages of B. tabaci.
REFERENCES 2023-01-11
Basu AN (1995) Bemisia tabaci (Gennadius) crop pest and the principal whitefly vector of plant viruses. First published 1995 by Westview Press; Published 2018 by Routledge, New York, USA.
Bedford ID, Briddon RW, Markham PG, Brown JK & Rosell RC (1992) Bemisia tabaci - biotype characterisation and the threat of this whitefly species to agriculture. Proceedings 1992 British Crop Protection Conference - Pests and Diseases 3, 1235-1240.
Bedford,ID, Briddon RW, Brown JK, Rosell RC & Markham PG (1994a) Geminivirus transmission and biological characterisation of Bemisia tabaci (Gennadius) biotypes from different geographic regions. Annals of Applied Biology 125, 311-325.
Bedford ID, Pinner, M, Liu S & Markham PG (1994b) Bemisia tabaci - potential infestation, phytotoxicity and virus transmission within European agriculture. Proceedings 1994 British Crop Protection Conference - Pests and Diseases 2, 911-916.
Bellows TS, Perring TM, Gill RJ & Headrick DH (1994) Description of a species of Bemisia (Homoptera: Aleyrodidae). Annals of the Entomological Society of America 87, 195-206.
Bertin S, Parrella G, Nannini M, Guercio G, Troiano E & Tomassoli L (2021) Distribution and genetic variability of Bemisia tabaci cryptic species (Hemiptera: Aleyrodidae) in Italy. Insects 12, 521. https://doi.org/10.3390/insects12060521
Briddon RW (2003) Cotton leaf curl disease, a multicomponent begomovirus complex. Molecular Plant Pathology 4, 427–434.
Broadbent, A., Foottit, R., & Murphy G (1989) Sweetpotato whitefly Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae), a potential insect pest in Canada. The Canadian Entomologist 121(11), 1027-1028. https://doi.org/10.4039/Ent1211027-11
Brown JK, & Bird J (1992) Whitefly-transmitted geminiviruses and associated disorders in the Americas and the Caribbean Basin. Plant Disease 76, 220-225.
Brown JK, Coats SA, Bedford ID, Markham PG, Bird J & Frohlich DR (1995a) Characterization and distribution of esterase electromorphs in the whitefly, Bemisia tabaci (Genn.) (Homoptera: Aleyrodidae). Biochemical Genetics 33, 205-214.
Brown JK, Frohlich DR, & Rosell RC (1995b) The sweetpotato or silverleaf whiteflies. Biotypes of Bemisia tabaci or a species complex. Annual Review of Entomology 40, 511-534.
Byrne DN (1999) Migration and dispersal by the sweet potato whitefly Bemisia tabaci. Agricultural and Forest Meteorology 97, 309-316.
Byrne DN & Bellows Jr TS (1991) Whitefly biology. Annual Review of Entomology 36, 431-457.
Byrne FJ, Bedford ID, Devonshire AL & Markham PG (1995) Esterase variation and squash silverleaf induction in 'B' biotype Bemisia tabaci (Homoptera; Aleyrodidae). Bulletin of Entomological Research 85, 175-179.
Cathrin PB & Ghanim G (2014) Recent advances on interactions between the whitefly Bemisia tabaci and begomoviruses, with emphasis on tomato yellow leaf curl virus. In Plant Virus–Host Interaction Molecular Approaches and Viral Evolution (eds Gaur RK, Hohn T & Sharma P), PP. 79-103. Academic Press, Amsterdam.
Celix A, Lopez-Sese A, Almarza N, Gomez-Guillamon ML & Rodriguez-Cerezo E (1996) Characterization of cucurbit yellow stunting disorder virus, a Bemisia tabaci transmitted closterovirus. Phytopathology 86, 1370-1376.
Chu D, Wan FH, Zhang YJ & Brown JK (2010) Change in the biotype composition of Bemisia tabaci in Shandong Province of China from 2005 to 2008. Environmental Entomology 39:1028–1036
Costa HS, Ullman DE, Johnson MW & Tabashnik BE (1993) Squash silverleaf symptoms induced by immature, but not adult, Bemisia tabaci. Phytopathology 83, 763-766.
Cuadrado IM, Janssen D, Velasco L, Ruiz L & Segundo E (2001) First report of cucumber vein yellowing virus in Spain. Plant Disease 85, 336.
Cuthbertson AGS & Vänninen I (2015) The importance of maintaining Protected Zone status against Bemisia tabaci. Insects 6, 432-441.
Dalton R (2006) Whitefly infestations: the Christmas invasion. Nature 443, 898-900.
Dângelo RAC, Michereff-Filho M, Campos MR, da Silva PS & Guedes RNC (2018) Insecticide resistance and control failure likelihood of the whitefly Bemisia tabaci (MEAM1; B biotype): a neotropical scenario. Annals of Applied Biology 172, 88–99.
De Barro PJ (1995) Bemisia tabaci biotype B: a review of its biology, distribution and control. CSIRO Australia Division of Entomology Technical Paper 1-55.
De Barro PJ, Liu SS, Boykin LM & Dinsdale AB (2011) Bemisia tabaci: a statement of species status. Annual Review of Entomology 56, 1-19.
Della Giustina W, Martinez M & Bertaux F (1989) Bemisia tabaci : le nouvel ennemi des cultures sous serres en Europe. Phytoma 406, 48-52.
Drayton GM, Teulon DAJ, Workman PJ & Scott IAW (2009) The Christmas dispersal of Bemisia tabaci (Gennadius) in New Zealand. New Zealand Plant Protection 62, 310-314.
Drost Y, Van Lenteren J & Van Roermund H (1998) Life history parameters of different biotypes of Bemisia tabaci (Hemiptera, Aleyrodidae) in relation to temperature and host plant: a selective review. Bulletin of Entomological Research 88, 219-230.
Duffus J, Liu HY, Wisler G & Li, R (1996) Lettuce chlorosis virus: a new whitefly transmitted closterovirus. European Journal of Plant Pathology 102, 591-596.
EPPO (2004) EPPO Standards PM 7/35(1) Bemisia tabaci. EPPO Bulletin 34, 281–288.
EPPO (2005) EPPO Standards PM 7/50(1) Tomato yellow leaf curl and Tomato mottle begomoviruses. EPPO Bulletin 35, 319–325.
EPPO (2008) EPPO Standards PM 4/34 (1) Production of pathogen-tested herbaceous ornamentals. EPPO Bulletin 38, 31–52.
EPPO (2009) EPPO Standards PM 10/13 Disinfestation of production site against Bemisia tabaci. EPPO Bulletin 39, 478–479.
EPPO (2011) EPPO Standards PM 10/17 (1) Treatment of plants for planting (cuttings) of Euphorbia pulcherrima for eradication of Bemisia tabaci. EPPO Bulletin 41, 404–405.
EPPO (2013) EPPO Standards PM 7/118 (1) Tomato chlorosis virus and Tomato infectious chlorosis Virus. EPPO Bulletin 43(3), 462–470
EPPO (2016) EPPO Standards PM 3/77 (1) Vegetable plants for planting under protected conditions – inspection of places of production. EPPO Bulletin 46(1), 40–48.
Fishpool LDC & Burban C (1994) Bemisia tabaci the whitefly vector of African cassava mosaic geminivirus. Tropical Science 34, 55-72.
Frohlich DR & Brown JK (1994) Mitochondrial 16S ribosomal subunit as a molecular marker in Bemisia tabaci and implications for population variability. Bemisia Newsletter 8, 3.
Gerling D & Horowitz AR (1984) Yellow traps for evaluating the population levels and dispersal patterns of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae). Annals of the Entomological Society of America 77, 753-759.
Gill RJ & Brown JK (2010) Systematics of Bemisia and Bemisia relatives: Can molecular techniques solve the Bemisia tabaci complex conundrum – a taxonomist's viewpoint. In Bemisia: bionomics and management of a global pest (eds Stansly PA & Naranjo SE), pp, 5– 29. Springer, Dordrecht, The Netherlands.
Ghosh S & Ghanim M (2021) Factors determining transmission of persistent viruses by Bemisia tabaci and emergence of new virus-vector relationships. Viruses 13, 1808.
Guirao P, Beitia F, Cenis JL (1997) Biotype determination of Spanish populations of Bemisia tabaci (Hemiptera: Aleyrodidae) Bulletin of Entomological Research 87(6), 587 - 593.
Henneberry TJ & Castle SJ (2001) Bemisia: Pest status, economics, biology and population dynamics. In Virus-Insect-Plant Interactions, (eds Harris, KF, Smith, OP & Duffus, JE), pp. 247-278. Academic Press, New York.
Henneberry TJ & Faust RM (2008) Introduction. In Classical biological control of Bemisia tabaci in the United States (eds Gould J, Hoelmer K & Goolsby J), pp, 1-16. Springer, Dordrecht.
Hogenhout SA, Ammar ED, Whitfield AE & Redinbaugh MG (2008) Insect vector interactions with persistently transmitted viruses. Annual Review of Phytopathology 46, 327–359.
Horowitz AR, Denholm I, Gorman K, Cenis JL, Kontsedalov S & Ishaaya I (2003) Biotype Q of Bemisia tabaci identified in Israel. Phytoparasitica 31, 94–98.
Horowitz AR, Kontsedalov S, Khasdan V & Ishaaya I (2005) Biotypes B and Q of Bemisia tabaci and their relevance to neonicotinoid and pyriproxyfen resistance. Archives of Insect Biochemistry and Physiology 58, 216-225.
Horowitz AR, Ghanim M, Roditakis E, Nauen R &Ishaaya I (2020) Insecticide resistance and its management in Bemisia tabaci species. Journal of Pest Science 93, 893-910.
Isaacs R, Willis MA & Byrne DN (1999) Modulation of whitefly take-off and flight orientation by wind speed and visual cues. Physiological Entomology 24, 311–318.
Jones DR (2003) Plant viruses transmitted by whiteflies. European Journal of Plant Pathology 109, 195–219.
Legg JP, Shirima R, Tajebe LS, Guastella D, Boniface S, Jeremiah S, Nsami E, Chikoti P & Rapisarda C (2014) Biology and management of Bemisia whitefly vectors of cassava virus pandemics in Africa. Pest Management Science 70, 1446–1453.
Li SJ, Xue X, Ahmed MZ, Ren SX, Du YZ, Wu JH, Cuthbertson AGS & Qiu BL (2011) Host plants and natural enemies of Bemisia tabaci (Hemiptera, Aleyrodidae) in China. Insect Science 18, 101-120.
Martin JH (1987) An identification guide to common whitefly pest species of the world (Homoptera, Aleyrodidae). Tropical Pest Management 33, 298-322.
Martin JH (2003) Whiteflies (Hemiptera: Aleyrodidae) - their systematic history and the resulting problems of conventional taxonomy, with special reference to descriptions of Aleyrodes proletella (Linnaeus, 1758) and Bemisia tabaci (Gennadius, 1889). Entomologist's Gazette 54, 125–136.
McKenzie CL & Osborne LS (2017) Bemisia tabaci MED (Q biotype) (Hemiptera: Aleyrodidae) in Florida is on the move to residential landscapes and may impact open-field agriculture. Florida Entomologist 100, 481-484.
McKenzie CL, Bethke JA, Byrne FJ, Chamberlin JR, Dennehy TJ, Dickey AM, Gilrein D, Hall PM, Ludwig S, Oetting RD, Osborne LS, Schmale L & Shatters Jr RG (2012) Distribution of Bemisia tabaci (Hemiptera: Aleyrodidae) biotypes in North America following the Q invasion. Journal of Economic Entomology 105, 753–766.
Mound LA & Halsey SH (1978) Whiteflies of the world, a systematic catalogue of the Aleyrodidae (Homoptera) with host plant and natural enemy data. British Museum (Natural History), London, UK.
Navas-Castillo J, Sanchez-Campos S, Diaz JA, Saez-Alonso E & Moriones E (1999) Tomato yellow leaf curl virus - is causes a novel disease of common bean and severe epidemics in tomato in Spain. Plant Disease 83, 29-32.
Naveen NC, Chaubey R, Kumar D, Rebijith KB, Rajagopal R, Subrahmanyam B & Subramanian S (2017) Insecticide resistance status in the whitefly, Bemisia tabaci genetic groups Asia-I, Asia-II-1 and Asia-II-7 on the Indian subcontinent. Scientific Reports 7, 40634.
Oliveira M, Henneberry T & Anderson P (2001) History, current status and collaborative research projects for Bemisia tabaci. Crop Protection 20, 709-723.
Perring TM (2001) The Bemisia tabaci species complex. Crop Protection 20, 725-737.
Perring TM, Cooper A., Rodriguez RJ, Farrar CA & Bellows TS (1993) Identification of a whitefly species by genomic and behavioural studies. Science 259, 74-77.
Pinto-Zevallos DM & Vänninen I (2013) Yellow sticky traps for decision-making in whitefly management: what has been achieved? Crop Protection 47, 74–84.
Saleem H, Nahid N, Shakir S, Ijaz S, Murtaza G, Khan AA, Mubin M & Shah Nawaz-ul-Rehman M (2016) Diversity, mutation and recombination analysis of cotton leaf curl geminiviruses. PLoS ONE 11(3), e0151161. https://doi.org/10.1371/journal.pone.0151161
Sánchez-Campos S, Navas-Castillo J, Camero R, Soria C, Diaz J & Moriones E (1999) Displacement of tomato yellow leaf curl virus (TYLCV)-Sr by TYLCV-Is in tomato epidemics in Spain. Phytopathology 89, 1038-1043.
Simmons AM, Harrison HF & Ling KS (2008) Fortynine new host plant species for Bemisia tabaci (Hemiptera, Aleyrodidae). Entomological Science 11, 385-390.
Stansly PA & Naranjo S (2010) Bemisia: bionomics and management of a global pest. Springer, Dordrecht, Netherlands, 540 pp.
Teng X, Wan FH & Chu D (2010) Bemisia tabaci biotype Q dominates other biotypes across China. Florida Entomologist 93, 363–368.
Xu J, De Barro P & Liu S (2010) Reproductive incompatibility among genetic groups of Bemisia tabaci supports the proposition that the whitefly is a cryptic species complex. Bulletin of Entomological Research 100, 359-366.
CABI and EFSA resources used when preparing this datasheet
CABI Datasheet on Bemisia tabaci (CABI Datasheet 12/2021). https://www.cabidigitallibrary.org/doi/10.1079/cabicompendium.8927
CIE (1986) Distribution Maps of Pests, Series A No. 284. CAB International, Wallingford, UK.
EFSA Panel on Plant Health (PLH) (2013) Scientific Opinion on the risks to plant health posed by Bemisia tabaci species complex and viruses it transmits for the EU territory. EFSA Journal 11, 3162, 302 pp. https://doi.org/10.2903/j.efsa.2013.3162
EPPO/CABI (1996) Bean golden mosaic bigeminivirus; Lettuce infectious yellows closterovirus; Squash leaf curl bigeminivirus; Tomato mottle bigeminivirus; Tomato yellow leaf curl bigeminivirus. In Quarantine pests for Europe 2nd edition (ed Smith IM, McNamara DG, Scott PR & Holderness M). CAB INTERNATIONAL, Wallingford, UK.
ACKNOWLEDGEMENTS 2023-01-11
This datasheet was extensively revised in 2023 by A. Rami Horowitz, Agricultural Research Organization (the Volcani Center) and Katif Research Center (Israel). His valuable contribution is gratefully acknowledged.
How to cite this datasheet?
Datasheet history 2023-01-11
This datasheet was first published in the EPPO Bulletin in 1989 and revised in the two editions of 'Quarantine Pests for Europe' in 1992 and 1997, as well as in 2023. 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 (1989) EPPO data sheet on quarantine organisms no 178: Bemisia tabaci. EPPO Bulletin 19(4), 733-738. https://doi.org/10.1111/j.1365-2338.1989.tb01170.x