Bemisia tabaci (Gennadius)

Taxonomic placing: Insecta, Hemimetabola, Hemiptera, Sternorrhyncha, Aleyrodidae.

Common names: Tobacco whitefly; cotton whitefly; sweetpotato whitefly; silverleaf whitefly. These common names reflect major hosts and symptoms, and in some cases also denote different biotypes or even species.

Geographical distribution: At least 24 sibling species within the Bemisia tabaci species complex occur in most parts of the world, with different centers of origin. They differ from each other by causing different plant disorders, by transmiting different virus diseases, by supporting different parasitoids, by different flight patterns and by molecular markers. The North American form is known as Biotype A. Biotype B, the silverleaf whitefly, initially named Bemisia argentifolii Bellows and Perring, is thought to have originated in the area encompassing Sudan, Israel and Yemen, whence it invaded North America. Biotype Q, another sibling species, is widely distributed in the Mediterranean region. Other biotypes have not yet been named. Biotypes B and Q occur in Israel, often in mixed populations. Due to the differential dynamics and distribution of the various biotypes, assisted by the development and application of more discriminating molecular identification methods, the reader should seek the most current information available on local populations. CIE Maps #284, 1999 (revised) and #591, 1999, which may be somewhat outdated.

Morphology: The different biotypes of the tobacco whitefly complex cannot be differentiated by the usual morphological features, but may be separated by molecular means. All adult whiteflies are small, approximately 1.0 mm in length, with a yellow body and two pairs of white wings covered with a white waxy powder. The compound eyes are red. At rest the wings are held in a Λ (inverted V) position. The legless nymphs are initially semi-transparent, later becoming creamy yellow to pale-green. The pupae (or fourth nymphal stage) bear 7 pairs of setae on their dorsum.

Host plants: These pests have a wide host range, occurring on more than 500 plant species assignable to over 60 plant families. Cotton and tomato are especially damaged in the Middle East. Otherhost plants include weeds, which often serve as alternate hosts when commercial crops are not available.

Life history: These whiteflies mate shortly after emergence, reproduction being by arrhenotoky. Eggs are inserted into the underside of leaves, but during heavy infestations the upper leaf surfaces, and even the pedicels, may be covered with eggs. As females prefer to place their eggs on the young, apical foliage, its nymphs are age-distributed vertically on the host plant, the older stages being located on the older and lower leaves. The emerging crawlers move away until setlling, losing their legs at the first molt and excreting copious amounts of honeydew throughout their feeding stages. When feeding on cotton at 30°C, a life cycle is completed in 17 days, whereas in the field development and fecundity vary according to host plants and season, and can last 25-70 days. To complete its development the pest requires 225 to 370 day-degrees. Females live for a fortnight in summer, several months during winter, producing 80-300 eggs. In the Middle East the pest raises 10-15 annual generations. Pest survival is constrained by climatic factors. Adults (but not the feeding nymphs) suffer heavy mortality during khamsin periods, and development ceases below 12°C. Dispersal between plants in the field or for long distances is by drifting on winds.

Economic importance: Members of the B. tabaci complex have become key pests of a number of agricultural systems throughout the world. Although recognized as pests for at least 80 years, they attained major pest status only in the last two decades, possibly through the indiscriminate use of pesticides. It is estimated that since 1991 annual crop value losses exceed $500 million in the USA alone.

The pest damages plants in various ways. By piercing and sucking nutrients, their feeding causes leaf withering and premature drop, weakens plants, reduces growth and yield, and may bring about plant death. In tomatoes, infestations are associated with irregular ripening. Indirect damage is due to the honeydew, which serves as substrate for sootymold that affects photosynthesis, reducing the quantity and quality of the product, whether fruit or fiber. The third type of damage is caused by the transmission of over 100 plant disease viruses; this pest complex is considered to be the most important whitefly vector of plant viruses worldwide. In addition, it is the only whitefly vector of geminivirus virus diseases, reducing yield of certain crops by 20-100%. Major viral plant diseases associated with the pest include tomato yellow leaf curl virus (TYLCV), lettuce necrotic yellows (LNYV), cucumber vein yellowing virus (CVYV), lettuce infections yellows virus (LIYV) and others.

Management: Due to the rapid development of the pest, high fecundity, its ability to transmit plant viruses, propensity to become resistant to many pesticides and lack of enough efficient natural enemies, the control of these pests is very difficult and an integrated effort is usually recommended.

Cultural control: Barriers, including row covers, repellent mulches (such as peanuts), screens with very fine mesh, yellow polyethylene sheets or those that absorb UV (“UV-deficient”) can reduce infestations. Other methods include the removal of host-weeds near cultivated fields, avoiding the growth of pest-sensitive crops near infested fields, and trap plants. Intercrops are used for he hosting natural enemies and to allow their population build-up. The intercrops are planted earlier than the specific crop, so that a suite of natural enemies will be in place before or when the pest arrives.

Plant resistance: Certain tomato cultivars suffer fewer attacks than others, probably due to a thick coat of glandular trichomes. Cotton resistance is associated with morphological features of the plant leaves. A recent approach is the creation of transgenic tomato plants resistant to TYLCV.

Chemical control: Tobacco whitefly populations in Egypt and Israel have developed high levels of resistance to most currently-used pesticides, including organophosphates, pyrethroids and insect growth regulators. This has led to the implementation of a resistance-management program in Israel, within which the use of pesticides with different modes of action is rotated during the season in cotton fields. Other pesticides in use are neem compounds, various oils and petroleum. Due to the pests’ tendency to live mostly on lower leaf surfaces, they are little affected by sprayed contact pesticides, exacerbating the difficulties of chemical control.

Biological control: Many predators attack the tobacco whitefly, including Anthocoridae, Miridae, Coccinellidae, Neuroptera, various flies, ants, spiders and mites. Most are opportunistic predators, although a few may be specific predators of whiteflies. However, little information is available on the impact of most of these predators under field conditions. Several Aphelinid parasitoids in the genera Encarsia and Eretmocerus, attack the pest and often control it. Their overall effect (especially in the field) may sometimes be limited due to the rapid development of the pest which often overtakes that of its enemies. Then, the fact that even a few whiteflies can transmit pernicious plant viruses, a situation that requires a pest-free crop environment, which in turn promotes the use of pesticides. Finally, chemicals that are applied against other major cotton and tomato pests usually kill the enemies. Some entomophatogenic fungi infect B. tabaci, but their overall effect in the field or in greenhouse is not known.

International cooperation: The world literature on what at the time were known as Bemisia tabaci and Bemisia argentifolii has been cataloged since 1992 and can be found at the email address snaranjo@wcrl.ars.usda.gov. The Annual Progress Reviews of the Silverleaf Whitefly Research and Technology Transfer Plans may also be obtained.

References

Al-Zyoud, F.A. 2014. The most common predators of Bemisia tabaci (Genn.): Biology, predation, preferences, releases, alternative food resources, combined use, current efforts and future perspectives. Journal of Biological Control 28: 1–16.

Anonymous, 2004. Diagnostic protocols for regulated pests. Bemisia tabaci. EPPO Bulletin 34: 281-288.

Antignus, Y. (and 6 co-authoirs). 2004. Truncated Rep gene originated from tomato yellow leaf curl virus-Israel [Mild] confers strain-specific resistance in transgenic tomato. Annals of Applied Biology 144: 39-44.

Antignus, Y., Nestel, D., Cohen, S. and Lapidot, M. 2001. Ultraviolet-deficient greenhouse environment affects whitefly attraction and flight-behavior. Environmental Entomology 30: 394-399.

Boykin, L.M. and de Barro, P.J. 2014. A practical guide to identifying members of the Bemisia tabaci species complex: And other morphologically identical species. Frontiers of Ecology and Evolution 45:1-5.

Dinsdale, A., Cook, L., Riginos, C., Buckley, Y.M. and De Barro, P. 2010. Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Annals of the Entomological Society of America 103: 196–208.

El Kady, H. and Devine, G.J. 2003. Insecticide resistance in Egyptian populations of the cotton whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Management Science 59: 865-871.

Frohlich, D.R., Torres-Jerez, I, Bedford, I.D., Markham, P.G. and Brown, J. K. 1999. A phylogeographical analysis of the Bemisia tabaci species complex based on mitochondrial DNA markers. Molecular Ecology 8: 1683-1691.

Gerling, D., Alomar, O. and Arno, J. 2001. Biological control of Bemisia tabaci using predators and parasitoids. Crop Protection 20: 779–799.

Gerling, D. and Mayer, R.T. (Eds) 1996. Bemisia: 1995. Taxonomy, Biology, Damage, Control and Management_. Intercept, Andover, UK.

Horowitz, A.R., Denholm, I., Gorman, K., Cenis, J.L., Kontsedalov, S. and Ishaaya, I. 2003. Biotype Q of Bemisia tabaci identified in Israel. Phytoparasitica 31: 94-98.

Horowitz, A.R., Forer, G, and Ishaaya, I. 1994, Managing resistance in Bemisia tabaci in Israel with emphasis on cotton. Pesticide Science 42: 113-122.

Horowitz, A.R. and Ishaaya, I. 2014. Dynamics of biotypes B and Q of the whitefly Bemisia tabaci and its impact on insecticide resistance. Pest Management Science 70: 1568–1572.

Morales, F.J.1. 2007. Tropical whitefly IPM project. Advances in Virus Research 69: 249-311.

Naranjo, S. E., Butler, G. D. Jr. and Henneberry, T. J. 2002. Complete bibliography of Bemisia tabaci and Bemisia argentifolii. Pp. 227-415. In Silverleaf Whitefly: National Research, Action and Technology Transfer Plan, 1997-2001; Fourth Annual Review of the Second 5-year Plan and Final Report for 1992-2002. USDA, ARS, Beltsville, USA.

Naranjo, S.E., Hagler, J.R. and Ellsworth, P.C. 2003. Improved conservation of natural enemies with selective management systems for Bemisia tabaci (Homoptera: Aleyrodidae) in cotton. Biocontrol Science and Technology 13: 571-587.

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