The exact origin of the MED species of Bemisia tabaci, and the reasons why it became such an important pest are still not fully known. MED species has been identified as a distinct member within the B. tabaci species complex (...
The exact origin of the MED species of Bemisia tabaci, and the reasons why it became such an important pest are still not fully known. MED species has been identified as a distinct member within the B. tabaci species complex (Tay et al., 2012). MED species is also an effective vector of many different plant viruses which, in conjunction with its high level of polyphagy, make it extremely problematic within agricultural regions where crops may be susceptible to viruses acquired from indigenous plants. Despite Bemisia in general being a tropical/sub-tropical whitefly species, MED species can easily be transported on plant species to temperate regions of the world (Cuthbertson and Vänninen, 2015). Within these cooler regions, MED species can survive within a protected environment and could feasibly spread virus diseases to new locations. It is for this reason that B. tabaci and members of its species complex, including MED species are on EPPO A2 Alert list.
The pest status of B. tabaci insects is complicated and through the comparison of mitochondrial cytochrome oxidase 1 (mtCO1) gene it is generally accepted that, rather than one complex species, B. tabaci is a complex of 11 genetic groups. These genetic groups are composed of at least 34 morphologically indistinguishable species, which are merely separated by a minimum of 3.5% mtCOI nucleotide divergence (Dinsdale et al., 2010; De Barro et al., 2011; Boykin and De Barro, 2014). The MED species, which was originally described in Greece as Aleyrodes tabaci in 1889 by Gennadius, was recently confirmed using molecular markers as the Mediterranean species (Tay et al., 2012). Within the B. tabaci complex, the Middle East-Asia Minor 1 (MEAM1) cryptic species, formerly referred to as 'B biotype', and Mediterranean (MED) cryptic species, formerly referred to as 'Q biotype' are the two most widely distributed, and as a result, best known of the species. These two species present the greatest threat to glasshouse crops worldwide (Bethke et al., 2009). The damaging MEAM1 is described as an aggressive coloniser and is an effective vector of many viruses, whereas the MED species characteristically shows strong resistance to novel insecticides (Jones et al., 2008; McKenzie et al., 2009).
Eggs are pear shaped with a pedicel spike at the base, approximately 0.2 mm long.
A flat, irregular oval shape, about 0.7 mm long, with an elongate, triangular vasiform orifice. On a smooth leaf the puparium lacks enlarged dorsal setae, but if the leaf is hairy, 2-8 long, dorsal setae are present.
Adults are approximately 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 in colour.
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
The B. tabaci Mediterranean species is currently increasing its global presence. It is continually being distinguished from Middle East-Asia Minor 1 species of the B. tabaci complex around the world (Powell et al., 2012; Cavalieri et al., 2014).
The risk to the EPPO region is primarily to the glasshouse industry in northern countries, and mainly concerns MED species and also MEAM1 species. Present legislation relates to B. tabaci, so reference to B. argentifolii should be avoided to prevent confusion in these areas. Since the recent introduction of this whitefly 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 (Prabhaker et al., 1985; Della Giustina et al., 1989; Mushtaq Ahmad et al., 2002).
Countries that already contain many begomoviruses that infect indigenous plants and weeds, and are associated with localized populations of B. tabaci that exhibit narrow host ranges may be particularly at risk from MED species. Should MED species become established in these countries its polyphagous feeding activities could enable viruses to move into new susceptible host plants, causing new crop protection problems.
MED species is documented as being polyphagous, having a host range of around 600 different plant species. This includes many glasshouse and field crops, as well as weeds. However, a study by de Courcy Williams et al. (1996) indicated that only a small number of individuals within a population can readily change host plants. It is the progeny of these particular individuals that lead to the species as a whole being highly polyphagous.
Early indication of infestation may consist of chlorotic spots caused by larval feeding, which may also be disfigured by honeydew and associated sooty moulds. Leaf curling, yellowing, mosaics or yellow-veining may also indicate the presence of whitefly-transmitted viruses. These symptoms are also observed in B. tabaci infestations, however phytotoxic responses such as a severe silvering of courgette and melon leaves, mis-ripening of tomato fruits, stem whitening of brassicas and yellow veining of some solanaceous plants may also be seen (Costa et al., 1993; Secker et al., 1998).
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 underside of leaves and can cause a reduction in photosynthetic potential when colonized by moulds. Honeydew can also disfigure flowers and, in cotton, can cause problems in lint processing. Following heavy infestations, plant height, the number of internodes, and yield quality and quantity can be affected, for example, in cotton.
Phytotoxic responses in many plant and crop species caused by larval feeding include 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 honeysuckle (Lonicera) (Bedford et al., 1994a,b).
A close observation of leaf undersides will show tiny, yellow to white larval scales. In severe infestations, when the plant is shaken, numerous small and white adult whiteflies will emerge in a cloud and quickly resettle. These symptoms do not appreciably differ from those of Trialeurodes vaporariorum, the glasshouse whitefly, which is common throughout Europe.
Eggs are usually laid in circular groups on the underside of leaves, with the broad end 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 plant tissue, and not into stomata as is the case with many other members of the Aleyrodidae. Eggs are whitish in colour when first laid, but gradually turn brown. Hatching occurs after 5-9 days at 30°C but this depends very much on host species, temperature and humidity.
On hatching, the first instar, or 'crawler', is flat, oval and scale-like in shape. The first instar is the only larval stage of this whitefly which is mobile. It moves from the egg site to a suitable feeding location on the lower surface of the leaf, after which its legs are lost in the next moult and the larva becomes sessile. It does not move again throughout the remaining nymphal stages. The first three nymphal stages each last 2-4 days, according to temperature. The fourth nymphal stage is termed the puparium, and is approximately 0.7 mm long. True pupation within the whitefly life-cycle does not occur, although the last (fourth) nymphal instar is typically referred to as a pupa after apolysis has been completed. Metamorphosis to adult occurs over about 6 days.
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 hours after emergence and takes place several times throughout the life of the adult. The lifespan of the female can extend to 60 days. The life of the male is generally much shorter, being between 9 and 17 days. Each female can oviposit over 300 eggs during her lifetime, these are often arranged in an arc around the female as she rotates on her stylet. Some 11 to 15 generations can occur within 1 year.
MED species is also responsible for vectoring many plant viruses in the genera Geminivirus, Closterovirus, Nepovirus, Carlavirus and Potyvirus. Whitefly-transmitted geminiviruses, now designated begomoviruses (Mayo and Pringle, 1998), are the most important of these agriculturally, causing yield losses to crops of between 20 and 100% (Brown and 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. Mansoor et al. (1993) reported that 1 million hectares of cotton were decimated in Pakistan by Cotton leaf curl virus (CLCuV) and important African subsistence crops such as cassava are affected by begomoviruses such as African cassava mosaic virus (ACMV) (see datasheet on African cassava mosaic disease). Tomato crops throughout the world are particularly susceptible to many different begomoviruses, and in most cases exhibit yellow leaf curl symptoms. This has caused their initial characterization as Tomato yellow leaf curl virus (TYLCV). A number of different species of TYCLV have now been recorded from within both the New World and Old World where MED occur (Jones, 2003). MED species has also been associated with transmission of several other begomoviruses such as Tomato mottle virus, Tobacco leaf curl virus (TLCV), Sida golden mosaic virus (SiGMV), Squash leaf curl virus (SLCV), Cotton leaf crumple virus (CLCV), Bean golden mosaic virus (BGMV) and Cotton leaf curl virus (Simon et al., 2003), some of which cause heavy yield losses in their respective hosts. Dual infections have also been shown to occur (Bedford et al., 1994c).
Natural enemies of whiteflies will, in most cases, have co-evolved with their prey and may, in some regions, be more efficient at controlling their native prey than an introduced one.
Various species of predatory mites have also been shown to be effective in feeding upon Mediterranean species of B. tabaci populations, including; Amblyseius limonicus, A. swirskii and Transeius montdorensis (Cuthbertson, 2014). No doubt they will also feed on other Bemisia species. A large range of natural enemies of B. tabaci have been recorded in China (Li et al., 2011). Their specificity to individual members of the B. tabaci species complex is unknown.
Entomopathogenic nematodes and fungi have been shown to offer much potential in controlling what has now been determined as MEAM1 species Bemisia populations (Cuthbertson et al., 2003a, 2005a, 2007a,b; Cuthbertson and Walters, 2005). The impact of these agents upon MED species has yet to be determined.
Adults do not fly very efficiently, but once airborne, can be transported long distances by convection or by wind. The greater dispersive capacity of MED species has been instrumental in its greater economic importance. All stages of this whitefly are likely to be transported within the international trade of ornamental plants and cut flowers. The international trade in poinsettia and gerbera has played a significant role in the dispersal of Bemisia (Cuthbertson, 2013) to all continents.
As with other species of whitefly and biotypes of B. tabaci, MED species can easily disperse over short distances. This dispersal can occur in vast numbers when host plants become heavily infested and begin to senesce. Large 'clouds' comprising many millions of individuals have been recorded leaving a dying host crop. Dispersal is almost certainly assisted by wind.
Physical movement of infested plants, whether it be through plant care, harvesting or spraying, can result in adult MED species dispersal from an infested plant.
Movement in trade
Any susceptible plant or crop, where leafy material is produced for distribution and export, can act as a means of dispersing MED species. Seasonal plants such as poinsettia, bedding plants, grafted crop plants and cut flowers are all potential means for MED species distribution. However, this usually involves dispersal of whitefly larvae and pupae rather than adults.
The appearance of MED species within new areas is in most cases, the result of movement of infested plant material. The movement and establishment of MED species populations through this route brings along the possibility of insecticide resistance genes. This invariably leads to an increase in the use of insecticides as whitefly control becomes increasingly more difficult. This in turn can produce an ever increasing spiral in the levels of insecticide resistance and insecticide use, having a direct impact on the environment.
Numerous chlorotic spots develop on the leaves of affected plants, which may also be disfigured by honeydew and associated sooty moulds. Leaf curling, yellowing, mosaics or yellow veining could indicate the presence of whitefly-transmitted viruses, and phytotoxic responses such as a severe silvering of courgette and melon leaves indicate the presence of MED species, the immature stages being mainly responsible for this symptom (Costa et al., 1993). Other phytotoxic responses to themed species include mis-ripening of tomato fruits (Maynard and Cantliffe, 1989), white streaking of Brassica leaves (Brown et al., 1992) and yellow veining of some solanaceous plants (Bedford et al., 1998).
Close observation of the undersides of the leaves will show the tiny, yellow/white larval scales and in severe infestations, when the plant is shaken, numerous small, white adult whiteflies will flutter out and quickly resettle.
B. tabaci is now widely regarded to be a multi-species complex. Consisting of as many as 34 species that are morphologically indistinguishable from each other. They can however, be distinguished molecularly (De Barro et al., 2011; Tay et al., 2012; Boykin and De Barro, 2014).
Differentiation of MED species from other whitefly species on the basis of adult morphology is often difficult, although close observation of adult eye morphology may often show differences in ommatidial arrangements between some species. At rest, MED species has wings more closely pressed to the body than Trialeurodes vaporariorum, which is a larger whitefly and more triangular in appearance.
The fourth instar or puparium can also be used to distinguish MED species from T. vaporariorum as a glasshouse pest. T. vaporariorum is 'pork-pie shaped', regularly ovoid, has straight sides (viewed laterally) resulting from the vertical wax pallisade surrounding each puparium, and in most instances, 12 large setae. MED species has an irregular, 'pancake-like' oval shape, oblique sides and shorter, finer setae. Although the number of enlarged setae in the MED species and wax rods in T. vaporariorum can vary according to host plant morphology, the two caudal setae are always stout and nearly always as long as the vasiform orifice in the B biotype. The length of caudal setae can be used to distinguish some Bemisia species.
For more information on the identification of B. tabaci from slide-mounted pupae, see Martin (1987).
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
Intercropping practices using non-hosts have been used in many countries aiming to reduce numbers of whiteflies on specific crops. However, intercropping with susceptible crops can promote whitefly populations, by offering a greater leaf area for feeding.
Weed species can play an important role in harbouring whiteflies between crop plantings and attention should be paid to removing these in advance of planting susceptible crops. Weeds also often harbour whitefly-transmitted viruses (Bedford et al., 1998) and may be a major source of crop virus epidemics, especially where MED species is present, due to its polyphagous nature.
Cultural control is generally much more effective where whiteflies are physical pests rather than virus vectors.
The development of transgenic resistant plant and crop species through genetic engineering must be considered and accepted as a future method of control where whitefly-transmitted viruses are already endemic and causing severe crop losses (Wilson, 1993; Raman and Altman, 1994). Traditional sources of resistance have been used successfully for the control of other whitefly species.
The following active ingredients have been reported as effective in controlling MED species worldwide: bifenthrin, buprofezin, imidacloprid, fenpropathrin, amitraz, fenoxycarb, deltamethrin, azadirachtin, pymetrozine. Chemical resistance is an ever increasing concern within the B. tabaci species complex. The MED species is widely considered to evolve stable resistance to the neonicotinoid insecticides commonly used for Bemisia control more rapidly than MEAM1 (Nauen, 2005). Hence, MED species neonicotinoid resistance is becoming increasingly widespread and problematic, with numerous cases being reported worldwide (Horowitz et al., 2005; Fernandez et al., 2009; Dennehy et al., 2010; Luo et al., 2010; Wang et al., 2010). However sequential chemical treatments have been shown under laboratory conditions to offer excellent potential in eradicating MED species on poinsettia plants (Cuthbertson et al., 2012).
A rotation of insecticides that offer no cross-resistance must therefore be used to control infestations.
A new group of environmentally safer insecticides that effectively kill whitefly by a physical mode of action are appearing on the market in many countries (Cuthbertson and Collins, 2015). These products do not have a specific active ingredient, but appear to utilise surfactant-like properties to overcome the protective waxes on whitefly larvae and adults.
The increased fecundity and polyphagous habit of MED species has exacerbated many control problems in field and glasshouse crops worldwide, compounded by insecticide resistance. It appears that no single control treatment can be used on a long-term basis against this pest, and that approaches should be integrated to achieve an effective level of control.
IPM appears to offer the best option for controlling MED species infestations without causing contamination of the environment. Beneficial insects are used alongside chemicals that offer a high level of selectivity, such as insect growth regulators. However, if whitefly-transmitted viruses are present, it is unlikely that the threshold of whitefly vectors would ever be reduced to a level where virus transmission would cease by using these methods, because MEAM1 is such an efficient viral vector. Plant and crop species that exhibit a high level of resistance to both vector and virus must also be considered when designing an IPM system.
Entomopathogenic nematodes and fungi have been shown to be successfully tank-mixed with several chemical products for use in eradication programmes against what has now been deemed as MEAM1 species in the UK (Cuthbertson et al., 2003b, 2005b, 2007b). Their impact upon MED species populations has not been fully determined. Cuthbertson et al. (2012) devised a sequential treatment programme that successfully eradicated MED species on poinsettia plants under laboratory conditions using both chemicals and entomopathogenic fungi.
In countries where MED species is not already present, the enforcement of strict phytosanitary regulations as required for B. tabaci in general, may help to reduce the risk of this whitefly becoming established (Cuthbertson and Vänninen, 2015).
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 (OEPP/EPPO, 1990). Particular attention is needed for consignments from countries where certain B. tabaci-listed viruses, now on the EPPO A1 or A2 quarantine lists, are present. These viruses can also be transmitted by MED species.
Bedford ID; Briddon RW; Markham PG; Brown JK; Rosell RC, 1993. A new species of Bemisia or biotype of Bemisia tabaci (Genn) as a future pest of European agriculture. Plant Health and the European Single Market, BCPC Monograph, 54., UK: BCPC, 381-386.
Cathrin PB; Ghanim M, 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. Amsterdam, The Netherlands: Elsevier, 79-103.
Horoxitz R; Kontsedalov S; Khasdan V; Breslauer H; Ishaaya I, 2008. The biotypes B and Q of Bemisia tabaci in Israel - Distribution, resistance to insecticides and implications for pest management. Journal of Insect Science, 8:23-24.
Simon B; Cenis JL; Beitia F; Khalid S; Moreno IM; Fraile AY; Garcia-Arenal F, 2003. Genetic structure of field populations of begomoviruses and of their vector Bemisia tabaci in Pakistan. Phytopathology, 93:1422-1429.
Horoxitz R, Kontsedalov S, Khasdan V, Breslauer H, Ishaaya I, 2008. The biotypes B and Q of Bemisia tabaci in Israel - Distribution, resistance to insecticides and implications for pest management. In: Journal of Insect Science, 8 23-24.