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. 2023 Jul 6;21(7):e08074. doi: 10.2903/j.efsa.2023.8074
Taxonomic information

Current valid scientific name: Bemisia tabaci

Synonyms: Aleurodes inconspicua, Aleurodes tabaci, Bemisia achyranthes, Bemisia bahiana, Bemisia costa‐limai, Bemisia emiliae, Bemisia goldingi, Bemisia gossypiperda, Bemisia gossypiperda mosaicivectura, Bemisia hibisci, Bemisia inconspicua, Bemisia longispina, Bemisia lonicerae, Bemisia manihotis, Bemisia minima, Bemisia minuscula, Bemisia nigeriensis, Bemisia rhodesiaensis, Bemisia signata, Bemisia vayssieri

Name used in the EU legislation: Bemisia tabaci Genn. (European populations)

Order: Hemiptera

Family: Aleyrodidae

Common name: cassava whitefly, cotton whitefly, silver‐leaf whitefly, sweet‐potato whitefly, tobacco whitefly

Name used in the Dossier: –

Group Insects
EPPO code BEMITA
Regulated status

The pest is listed in Annex III as protected zone quarantine pest Bemisia tabaci Genn. (European populations) for Ireland and Sweden.

Bemisia tabaci is included in the EPPO A2 list (EPPO, online_a).

The species is a quarantine pest in Belarus, Moldova, Norway and New Zealand. It is on A1 list of Azerbaijan, Chile, Georgia, Kazakhstan, Ukraine and the UK. It is on A2 list of Bahrain, East Africa, Southern Africa, Russia, Türkiye and EAEU (= Eurasian Economic Union – Armenia, Belarus, Kazakhstan, Kyrgyzstan and Russia) (EPPO, online_b).

Pest status in the UK

Bemisia tabaci (European populations) is present in the UK, with few occurrences (CABI, online; EPPO, online_c) and it is continuously intercepted to the UK. The intercepted populations were identified as B biotype Middle East‐Asia Minor 1 (=MEAM1) and Q biotype Mediterranean (=MED) (Cuthbertson, 2013).

From 1998 to 2015, there were between 7 and 35 outbreaks per year of B. tabaci in the UK and all the findings were subject to eradication. The UK outbreaks of B. tabaci have been restricted to greenhouses and there are no records of the whitefly establishing outdoors during summer (Cuthbertson and Vänninen, 2015; Bradshaw et al., 2019).

According to the Dossier Section 5.0, B. tabaci is present: not widely distributed and under official control, restricted to four outbreak sites in 2022–2023 in contained environments (glasshouses). Many interceptions and outbreaks (356 in total in 2021), but all outbreaks subject to eradication measures. Not known outdoors (i.e. not under protection) and not thought to be able to establish outdoors.

Pest status in the EU

Bemisia tabaci (European populations) is widespread in the EU – Austria, Belgium, Bulgaria, Croatia, the Republic of Cyprus, Czechia, Finland, France, Germany, Greece, Hungary, Italy, Luxembourg, Malta, the Netherlands, Poland, Portugal, Romania, Slovenia and Spain (CABI, online; EPPO, online_c).

It is absent from Denmark, Estonia, Ireland, Latvia, Lithuania, Slovakia and Sweden (CABI, online; EPPO, online_c).

In the EU, B. tabaci is mainly present in the greenhouses, with exception of Mediterranean coastal region (Cyprus, Greece, Malta, Italy, south of France, certain parts of Spain and Portugal), where the whitefly occurs also outdoors (EFSA PLH Panel, 2013).

Host status on Acer

Acer palmatum is reported host of Bemisia tabaci in China (Li et al., 2011; CABI, online). Other reported hosts are A. buergerianum (Li et al., 2011) and A. macrophyllum (Yassin and Bendixen, 1982).

There is no information on whether B. tabaci can also attack Acer pseudoplatanus.

PRA information Available Pest Risk Assessments:
  • Scientific Opinion on the risks to plant health posed by Bemisia tabaci species complex and viruses it transmits for the EU territory (EFSA PLH Panel, 2013);

  • Scientific Opinion on the commodity risk assessment of Persea americana from Israel (EFSA PLH Panel, 2021);

  • Scientific report on the commodity risk assessment of specified species of Lonicera potted plants from Turkey (EFSA PLH Panel, 2022a);

  • Scientific Opinion on the commodity risk assessment of Jasminum polyanthum unrooted cuttings from Uganda (EFSA PLH Panel, 2022b);

  • Scientific Opinion on the commodity risk assessment of Berberis thunbergii potted plants from Turkey (EFSA PLH Panel, 2022c);

  • Scientific Opinion on the commodity risk assessment of Ligustrum delavayanum topiary plants grafted on Ligustrum japonicum from the UK (EFSA PLH Panel, 2022d);

  • UK risk register details for Bemisia tabaci non‐European populations (DEFRA, online_a);

  • UK risk register details for Bemisia tabaci European populations (DEFRA, online_b).

Other relevant information for the assessment
Biology

Bemisia tabaci is a cosmopolitan whitefly present on all continents except for Antarctica (CABI, online; EPPO, online_c). In the literature, it is reported as either native to Africa, Asia, India, North America or South America (De Barro et al., 2011). However, based on mtCO1 (mitochondrial cytochrome oxidase 1) sequence, its origin is most likely to be sub‐Saharan Africa (De Barro, 2012).

Bemisia tabaci is a complex of at least 40 cryptic species that are morphologically identical but distinguishable at molecular level (Khatun et al., 2018). The species differ from each other in host association, spread capacity, transmission of viruses and resistance to insecticides (De Barro et al., 2011).

Bemisia tabaci develops through three life stages: egg, nymph (four instars) and adult (Walker et al., 2010). Nymphs of Bemisia tabaci mainly feed on phloem in minor veins of the underside leaf surface (Cohen et al., 1996). Adults feed on both phloem and xylem of leaves (Walker et al., 2010, citing others). Honeydew is produced by both nymphs and adults (Davidson et al., 1994). Bemisia tabaci is multivoltine with up to 15 generations per year (Ren et al., 2001). The life cycle from egg to adult requires from 2.5 weeks up to 2 months depending on the temperature (Norman et al., 1995) and the host plant (Coudriet et al., 1985).

In the southern California desert on field‐grown lettuce (from 27 October 1983 to 4 January 1984), B. tabaci completed at least one generation (Coudriet et al., 1985). In Israel, the reproduction of B. tabaci was much reduced in winter months, but adults emerging in December survived and started ovipositing at the end of the cold season (Avidov, 1956). The most cold‐tolerant stage are eggs (at temperatures of −2°, −6°, −10°C) and the least tolerant are large nymphs. Short periods of exposure in 0° to −6°C have little effect on mortality. As the temperature lowers to −10°C, the duration of time required to cause significant mortality shortens dramatically (Simmons and Elsey, 1995).

Females can lay more than 300 eggs (Gerling et al., 1986), which can be found mainly on the underside of the leaves (CABI, online). Females develop from fertilised and males from unfertilised eggs (Gerling et al., 1986). Eggs are yellowish white and with age turn golden brown. Their size is about 0.19–0.20 mm long and 0.10–0.12 mm wide. First‐instar nymph (=crawler) is scale‐like, elliptical, darker yellow in colour and about 0.26 mm long and 0.15 mm wide. Crawlers have legs and crawl actively on leaves before they settle down and moult through second‐ (0.38 mm long and 0.24 mm wide), third‐ (0.55 mm long and 0.35 mm wide)

and fourth‐instar nymph (0.86 mm long and 0.63 mm wide) (Hill, 1969). Fourth‐instar nymph (=pupa) stops feeding and moults into an adult (Walker et al., 2010, citing others). Adult emerges through a ‘T'‐shaped rupture in the pupal case (El‐Helaly et al., 1971). Adults are pale yellow and have two pairs of white wings dusted with a white waxy powder (Hill, 1969). Female is approximately 1 mm long. Males are smaller about 0.8 mm long (EFSA PLH Panel, 2013).

Out of all life stages, only first‐instar nymph (= crawler) and adults are mobile. Movement of crawlers by walking is very limited, usually within the leaf where they hatched (Price and Taborsky, 1992) or to more suitable neighbouring leaves. The average distance was estimated within 10–70 mm (Summers et al., 1996). For these reasons, they are not considered to be good colonisers. On a contrary, adults can fly reaching quite long distances in a search of a permanent host. According to a study done by Cohen et al. (1988), some of the marked individuals were trapped 7 km away from the initial place after 6 days. Long‐distance passive dispersal by wind is also possible (Byrne, 1999).

Bemisia tabaci is an important agricultural pest that is able to transmit more than 121 viruses (belonging to genera Begomovirus, Crinivirus, Ipomovirus, Carlavirus and Torradovirus) and cause significant damage to food crops such as tomatoes, cucurbits, beans and ornamental plants (EFSA PLH Panel, 2013). However, these viruses are not reported to infect Acer species.

Possible pathways of entry for B. tabaci are plants for planting including cuttings and rooted ornamental plants; cut flowers and branches with foliage; fruits and vegetables; human‐assisted spread; natural spread such as wind (EFSA PLH Panel, 2013).

Symptoms Main type of symptoms Main symptoms of B. tabaci on plants are chlorotic spotting, decrease of plant growth, deformation of fruits, deformation of leaves, intervein yellowing, leaf yellowing, leaf curling, leaf crumpling, leaf vein thickening, leaf enations, leaf cupping, leaf loss, necrotic lesions on stems, plant stunting, reduced flowering, reduced fruit development, silvering of leaves, stem twisting, vein yellowing, wilting, yellow blotching of leaves, yellow mosaic of leaves, presence of honeydew and sooty mould. These symptoms are plant responses to the feeding of the whitefly and to the presence of transmitted viruses (EPPO, 2004; EFSA PLH Panel, 2013; CABI, online).
Presence of asymptomatic plants Symptoms of B. tabaci being present on the plants are usually visible. However, B. tabaci is a vector of several viruses and their infection could be asymptomatic.
Confusion with other pests

Bemisia tabaci can be easily confused with other whitefly species such as B. afer, Trialeurodes lauri, T. packardi, T. ricini, T. vaporariorum and T. variabilis. A microscopic slide is needed for morphological identification (EPPO, 2004).

Different species of B. tabaci complex can be distinguished using molecular methods (De Barro et al., 2011).

Host plant range

Bemisia tabaci has a wide host range, including more than 1,000 different plant species (Abd‐Rabou and Simmons, 2010).

Some of the many hosts of Bemisia tabaci are Abelmoschus esculentus, Amaranthus blitoides, Amaranthus retroflexus, Arachis hypogaea, Atriplex semibaccata, Bellis perennis, Borago officinalis, Brassica oleracea var. botrytis, B. oleracea var. gemmifera, B. oleracea var. italica, Bryonia dioica, Cajanus cajan, Capsella bursa‐pastoris, Capsicum annuum, Citrus spp., Crataegus spp., Cucumis sativus, Cucurbita pepo, Erigeron canadensis, Euphorbia pulcherrima, Gerbera jamesonii, Glycine max, Gossypium spp., G. hirsutum, Hedera helix, Ipomoea batatas, Lactuca sativa, L. serriola, Lavandula coronopifolia, Ligustrum lucidum, L. quihoui, L. vicaryiis, Manihot esculenta, Melissa officinalis, Nicotiana tabacum, Ocimum basilicum, Origanum majorana, Oxalis pes‐caprae, Phaseolus spp., Phaseolus vulgaris, Piper nigrum, Potentilla spp., Prunus spp., Rosa spp.,

Rubus fruticosus, Salvia officinalis, S. rosmarinus, Senecio vulgaris, Sinningia speciosa, Solanum lycopersicum, S. melongena, S. nigrum, S. tuberosum, Sonchus oleraceus, Stellaria media, Tagetes erecta, Taraxacum officinale, Thymus serpyllum, Urtica urens, Vitis vinifera and many more (Li et al., 2011; EFSA PLH Panel, 2013; CABI, online; EPPO, online_d). Acer palmatum and A. buergerianumare are reported hosts in China (Li et al., 2011; CABI, online).

For a full host list, refer to Li et al. (2011), EFSA PLH Panel (2013); CABI (online) and EPPO (online_d).

Reported evidence of impact Bemisia tabaci (European populations) is EU protected zone quarantine pest.
Evidence that the commodity is a pathway Bemisia tabaci is continuously intercepted in the EU on different commodities including plants for planting (EUROPHYT/TRACES‐NT, online). Therefore, the commodity is a pathway for B. tabaci. Plants can carry leaves at the time of export which can host all life stages of the pest.
Surveillance information

Bemisia tabaci is regulated quarantine pest in the UK. As such, the policy for any outbreak is to eradicate the population. The UK makes many interceptions of B. tabaci and experiences a few outbreaks each year (356 interceptions and outbreaks in 2021), but all outbreaks are under protection and subject to eradication measures. This pest has never established outdoors in the UK (Dossier Section 3.0).

As part of an annual survey at ornamental retail and production sites (frequency of visits determined by a decision matrix), B. tabaci is inspected for on common host plants. In addition, all tomato and pepper production sites subject to annual inspection (Dossier Sections 3.0 and 5.0).