Bemisia tabaci Grennadius Homoptera Aleyrodidae

Natural History

Distribution. Silverleaf whitefly and sweet-potato whitefly are closely related whitefly species, or possibly strains of the same species. They cannot be distinguished easily by appearance, though there are some biological differences. Much literature from tropical and subtropical environments around the world referring to sweetpotato whitefly probably pertains to silverleaf whitefly and other closely related species. Until the identities of these species are accurately determined, their distribution will remain unknown and some aspects of their biologies will remain confused. It appears, however, that sweet-potato whitefly has been in Florida since at least 1900, but it was not considered as a serious pest in the United States until about 1981 when it became very abundant in Arizona and southern California.

Silverleaf whitefly gained access to the southern United States in the 1980s; the first serious problem occurred in Florida in 1986 followed soon thereafter by similar problems in California, Arizona, and Texas. In the desert southwest, where both whiteflies occurred as serious vegetable and field crop pests, sweetpotato whitefly was displaced by silverleaf whitefly. Thus, sweetpotato whitefly appears to have been returned to insignificant pest status, but is often confused with the serious pest, silverleaf whitefly. The states of Arizona, California, Florida, and Texas are particularly affected by silverleaf whitefly because these are locations where silverleaf whitefly successfully overwinters and where crop and weed hosts persist throughout the year. Cooler climates do not experience major problems with silverleaf whitefly except when overwintering in greenhouses occurs or vegetable transplants originate from whitefly-infested areas.

Host Plants. Silverleaf whitefly has a very wide host range. In Florida alone, over 50 hosts have been reported, and there may be 500 worldwide. Sweet potato, cucumber, cantaloupe, watermelon, squash, eggplant, pepper, tomato, lettuce, broccoli and many other crops are hosts, but suitability varies. For example, sweet potato, cucumber, and squash are much more favorable for whitefly than broccoli and carrot (Coudriet et al., 1985). Tsai and Wang (1996) rated suitability of five vegetable crops for whitefly population development as eggplant > tomato > sweet potato > cucumber > snap bean. Various weeds and field crops may favor survival of whiteflies during vegetable-free periods (Coudriet et al., 1986). Wild lettuce, Lactuca serriola, and sowthistle, Sonchus spp., are examples of suitable weed hosts. Cotton, soybean, and to a lesser extent alfalfa and peanut are field crop hosts. (See color figure 10.)

Sweetpotato whitefly has a narrower host range than silverleaf whitefly. For example, silverleaf white-fly oviposits more readily on cabbage (Blua et al., 1995), which is an important factor in overwintering.

As with most insects, host preference and suitability for whitefly growth and survival are highly, but not perfectly, correlated (Zalom et al., 1995). Despite the lack of suitability among certain hosts for whitefly growth and reproduction, even less suitable vegetable crops such as lettuce can sometimes be damaged when large numbers of dispersing whiteflies feed and oviposit. This is especially likely to happen when suitable crops supporting numerous whiteflies senesce or are harvested, forcing the whiteflies to disperse in search of food. Survival of whitefly may be enhanced by feeding on virus-infected plants, relative to healthy plants (Costa et al., 1991). Deterioration of host-plant quality will often prompt dispersal of adults.

Weather. Silverleaf whitefly thrives under hot and dry conditions. Rainfall seems to decrease populations though the mechanism is not known. Silverleaf whitefly is not a strong flier, normally moving only short distances in search of young plant tissue. However, under proper weather conditions dramatic, longdistance flights involving millions or billions of insects are observed. Such flights normally occur in the morning as the sun heats the ground, and most insects move downwind.

Natural Enemies. Numerous predators, parasi-toids, and fungal diseases of silverleaf whitefly are known (Gerling, 1990; Cock, 1993). The general predators usually associated with Homoptera such as minute pirate bugs (Hemiptera: Anthocoridae), green lacewings (Neuroptera: Chrysopidae), and lady beetles (Coleoptera: Coccinellidae) are important, as are many parasitic wasps, particularly in the genera Encar-sia and Eretmocerus (both Hymenoptera: Aphelinidae) (Polaszek et al., 1992). While these agents exert considerable control on whitefly populations in weedy areas or on crops where insecticide use is minimal or absent, they do not survive well in the presence of most insecticides.

Life Cycle and Description. Silverleaf whitefly can complete a generation in about 20-30 days under favorable weather conditions (Gerling et al., 1986). In tropical countries up to 15 generations per year have been reported, and in the southwestern United States 12-13 generations occur annually.

  1. The egg is about 0.2 mm long, elongate, and tapers distally; it is attached to the plant by a short stalk. The whitish eggs turn brown before hatching, which occurs in 4-7 days. The female deposits 9095% of her eggs on the lower surfaces of young leaves (Simmons, 1994).
  2. All instars are translucent, and somewhat shiny. The flattened first instar is mobile, and is commonly called the "crawler" stage. It measures about 0.27 mm long and 0.15 mm wide. Its movement is usually limited to the first few hours after hatch, and to a distance of 1-2 mm (Price and Taborsky, 1992).

Duration of the first instar is usually 2-4 days. The feeding site is normally the lower surface of a leaf, but sometimes more than 50% of the nymphs are found on the upper surface, and feeding location seems not to affect survival (Simmons, 1999). The second and third instars are similarly flattened, but their leg segmentation becomes reduced and the legs nonfunctional. Duration of these instars is about 2-3 days for each. Body length and width are 0.36 and 0.22 mm, and 0.49 and 0.29 mm, for the second and third instar, respectively. Although the early portion of the fourth instar is similar to instars 2-3, the latter portion is sessile and called the "pupa." This term is not technically correct because some feeding occurs during this instar. The appearance of the fourth instar is variable, depending on the food plant; this stage tends to be spiny when develops on a hairy leaf but has fewer filaments or spines when feeding on smooth leaves. The fourth instar measures about 0.7 mm long and 0.4 mm wide. Duration of the fourth instar is about 4-7 days. Total pre-adult development time averages 15-18 days in the temperature range of 25-32°C, but increases markedly at lower temperatures. The lower-and upper-developmental thresholds are considered to be about 10° and 32°C (Natwick and Zalom, 1984). (See color figure 175.)

The form of the pupa is used to distinguish among whitefly species, and can be used to separate greenhouse whitefly from the similar-appearing greenhouse whitefly, Trialeurodes vaporariorum (Westwood), from the Bemisia spp. Greenhouse whitefly is straight-sided when viewed laterally, ovoid, and lacks a groove near the anal end of the body. In contrast, the Bemesia spp. are oblique-sided, irregularly oval, and possess a groove in the anal region.

Adult. The adult is white and measures about 1.01.3 mm long. The antennae are pronounced and the

Bemisia Tabaci Crawlers Images
Silverleaf whitefly nymph.

eyes red. Oviposition begins 2-5 days after emergence of the adult, often at about 5 eggs per day. Adults typically live 10-20 days and may produce about 50-150 eggs, though there are records of over 300 eggs per female. Females may produce male offspring without fertilization but males are common, so most females are probably fertilized. (See color figure 174.)

The biology and management of "sweetpotato" whitefly were comprehensively reviewed by Butler et al. (1986) and Cock (1986, 1993). A study of sweet-potato whitefly developmental biology on tomato was published by Salas and Mendoza (1995). Silverleaf whitefly was described by Bellows et al. (1994). The specific status of these whiteflies was discussed by Brown et al. (1995).

Another whitefly that easily can be confused with Bemisia spp. is greenhouse whitefly, Trialeurodes vapor-ariorum Westwood. They can be distinguished in the field by the manner in which they hold their wings. Bemisia spp. hold their wings roof-like over their body while at rest, whereas greenhouse whitefly holds its wings horizontally when at rest.

Damage

The adult and nymphal whiteflies use their piercing-sucking mouthparts to feed on the phloem of host plants. This results in direct damage, which is manifested in localized spotting, yellowing, or leaf drop. Under heavy feeding pressure wilting and severe growth reduction may occur.

Systemic effects also are common, with uninfested leaves and other tissue being severely damaged by whitefly feeding on other areas of the plant. A trans-

Bemisia Tabaci Antenna
Adult silverleaf whitefly.

located toxicogenic secretion by nymphs, but not by adults, is implicated (Yokomi et al., 1990). The young and developing tissue is damaged by whiteflies while feeding on older tissue. Once the whiteflies are removed, new plant growth is normal if a disease is not transmitted. Damaged foliar tissue, however, does not recover once injured. Among leafy vegetables and crucifers, white streaking or discoloration, especially of veins, is common (Brown et al., 1992; Costa et al., 1993). In Texas, population densities of three adult whiteflies per leaf are estimated to inflict 10% yield reduction in cantaloupe (Riley and Sparks 1993). Other studies in Texas and Arizona (Riley and Palumbo, 1995a,b) demonstrated similar losses, and indicated that yields could be optimized if plants were treated with insecticide at whitefly densities of three adults per leaf or 0.5 large nymphs per 7.6 sq cm of leaf area.

A disorder called irregular ripening affects tomato fruit when whiteflies feed on tomato foliage (Schuster et al., 1990). Although the tomato foliage is not damaged, the internal portions of the fruit do not ripen properly and the surface is blotched or streaked with yellow.

Squash silverleaf, a disorder responsible for the common name of B. argentifolli, has been known from Israel since 1963 but did not occur in the United States until about 1986, when silverleaf whitefly first became abundant in Florida. Silverleaf symptomology includes blanching of the veins and petioles, and eventually the interveinal areas of the leaf. The fruit of both yellow- and green-fruited varieties also may be blanched (Yokomi et al, 1990; Schuster et al., 1991).

In addition to direct damage, silverleaf whitefly also causes damage indirectly by transmitting plant viruses. Over 60 plant viruses, most belonging to a group called geminiviruses, are known to be transmitted to crops by silverleaf and sweetpotato white-flies (Markham, 1994). Some viruses, such as tomato yellow leaf curl virus, cause more damage than the insect feeding alone, so the effects are devastating. Unfortunately, unlike the case with the phyo-toxemia caused by the whitefly salivary secretions, once viruses are inoculated into the plant there is no recovery by the host even if the whiteflies are eliminated.

Lastly, whiteflies cause injury by excreting excess water and sugar in the form of honeydew. This sticky substance accumulates on the upper surface of leaves and fruit, and provides a substrate for growth of a fungus called sooty mold. The dark mold inhibits photo-synthetic activity of the foliage, and may also render the fruit unmarketable unless it can be washed thoroughly and the residues are removed.

Management

  1. The distribution of whitefly life stages on cantaloupe was studied by Tonhasca et al. (1994) and Gould and Naranjo (1999). The eggs tend to be concentrated on young foliage and mature larvae on older foliage. Large nymphs are a considered good stage for population assessment, because they cannot move and are large enough to see without magnification. Adults sometimes are concentrated on lower leaves, but they move to young foliage during ovipo-sition. Such distributions must be considered in population assessment before initiating management practices. Ohnesorge and Rapp (1986) recommended yellow sticky traps rather than direct visual counts for population estimates when insect densities were low. However, when Palumbo et al. (1995) evaluated several sampling methods in cantaloupe, they found that visual observation of the lower-leaf surface and vacuum sampling were less time consuming, and sometimes more precise, than yellow sticky traps. Sampling techniques were reviewed by Butler et al. (1986) and Naranjo (1996).
  2. In southern states, where silverleaf whitefly can be the most important insect problem on some vegetable crops, frequent applications of insecticides are often made to minimize the direct and indirect effects of whitefly feeding. Whitefly resistance to nearly all classes of insecticides is known, and rotation of insecticide classes is encouraged. Mixtures of insecticides are often used, which is indicative of high levels of resistance. Most agriculturalists suggest that whitefly numbers be maintained at low levels because once they become abundant they are difficult to suppress; this, of course, exacerbates development of insecticide resistance. The phytotoxemia and disease transmission potential of this insect exaggerates its damage potential, further justifying frequent application of insecticides. Often the most effective approach to effective management involves regional or area-wide suppression based on a combination of insecticides, weed management, and crop management.

Silverleaf whitefly feeds on the lower surface of foliage and is sessile throughout most of its life—habits that minimize contact with insecticides. Frequent insecticide application also disrupts naturally occurring biological control agents. In an attempt to minimize the cost and disruptive effects of insecticides, and to reduce the evolution of insecticide resistance, soaps and oils have been extensively studied for whitefly control. The mechanism of control by surfactants such as soaps and oils is not clearly understood, but disruption of the insect cuticle, physical damage, and repellency are postulated. In any event, mineral and vegetable oils alone, or in combination with soaps and detergents, can provide some suppression of whiteflies. Combination of insecticide and oil often enhances whitefly control (Horowitz et al., 1997). Suppression usually increases with concentration of the surfactants, but 0.5% detergent plus 0.5% vegetable oil, or 0.5% detergent alone, or 1% insecticidal soap alone, or 0.75-1.0% light-mineral oil are often recommended initially until the phytotoxicity potential is known. Oil has more residual activity than soaps or detergents; the former is also more repellent to adults (Liu and Stansly, 1995). Cucurbits and crucifers seem especially prone to foliage damage by surfactants, and damage occurs frequently under high-temperature conditions. High gallonage enhances coverage and pest population reduction, but increases cost of control (Butler and Henneberry, 1990a,b; Butler et al., 1993). Neem products and other growth regulators affect immature insect survival only (Price and Schuster, 1991).

Biological Control. Although many predators, parasitoids, and fungal diseases are known to attack silverleaf and sweetpotato whitefly, no biotic agents are known to provide adequate suppression alone. Under greenhouse conditions, parasitoids can be released at high enough densities to provide some suppression, especially when insecticidal soap and other management techniques are also used (Parrella et al., 1991). Under natural field conditions, parasitism does not usually build to high levels until late in the growing season (Cock, 1993). Insecticides often interfere with parasitoids and predators, of course, and effective use of biological control agents will probably be limited to cropping systems where broad-spectrum insecticide use is minimized, and other management techniques used which favor action of predators, para-sitoids, and disease agents. Some new insecticides are quite selective, killing whiteflies and yet preserving most natural enemies. Verticillium, Paecilomyces, and other fungi similarly show some promise under greenhouse conditions, but are limited by low humidity under field conditions (Meade and Byrne, 1991; Cock, 1993).

Cultural Practices. Cultural controls can be vitally important in managing silverleaf whitefly. Incorrect crop management, in particular, can create or exacerbate whitefly problems. Whiteflies can move from crop to crop, and area-wide crop-free periods help diminish populations. Thus, prompt tillage of land and destruction of crop residues after crop maturity is recommended. Similarly, weeds can harbor whiteflies, whitefly-transmitted diseases, and white-fly parasitoids, so weed management is a consideration.

Row covers and other physical barriers can decrease infestation of crops, and infection with disease (Cohen and Berlinger, 1986). Screen hole sizes of about 0.19 sq mm or smaller are required to successfully exclude silverleaf whitefly (Bethke et al., 1994). Colored and aluminum mulches provide only temporary reduction in whitefly abundance and disease transmission (Cohen and Berlinger, 1986) or none at all (Powell and Stoffella, 1993). Orozco-Santos et al. (1995) reported effective whitefly exclusion on cantaloupe by using row covers, and reduction in whitefly population levels with transparent mulch.

Host-Plant Resistance. Host-plant resistance offers considerable potential, but currently it is difficult to put into practice. Both very hairy and hairless culti-vars are perhaps less suitable for parasitoid activity than plants with intermediate densities of plant hairs. Resistance to the toxic saliva and to viruses transmitted by whiteflies also are being sought among commercially acceptable hybrids. For example, McCreight and Kishaba (1991) evaluated numerous cucurbit species and cultivars for susceptibility to squash leaf curl virus. Susceptibility varied among and within cultivated species, but overall susceptibility among species was: Cucurbita maxima > C. pepo > C. mixta > C. moschata. All cultivated species and cultivars were at least moderately susceptible to squash leaf curl virus, and most were severely damaged in field tests. In contrast, many wild cucurbit species were unaffected. Among commercial tomato cultivars, there was less oviposition by whiteflies on plants with low trichome densities, but this relationship was not apparent for wild tomatoes (Heinz and Zalom, 1995). As the basis for resistance is understood, there is good possibility of incorporating at least partial resistance into commercial cultivars.

Disease Transmission. Growers generally rely on whitefly suppression to manage disease incidence. This is not entirely satisfactory, however, and roguing of virus-infected plants is often suggested to minimize within-field spread of viruses. As whiteflies may transmit disease from one crop to another, or from weeds to crops, vegetation management is important. As noted above, reflective mulches have not produced consistent economic benefits. Mineral and vegetable oils may inhibit virus transmission. Application of 10-15% commercial whitewash solution is reported to be as effective as mineral oil, and more effective than some pyrethroid insecticides, in reducing virus disease incidence; however, phytotoxicity is sometimes a problem (Marco, 1993). Row covers or other physical barriers can substantially prevent disease transmission (Costa et al., 1994), but often they are not economical. Ultraviolet (UV) light-absorbing plastic has been suggested as a preferred medium for plastic greenhouses (Antignus et al., 1996). Apparently, the elimination of UV light decreases the attraction of plants to whiteflies, or changes their feeding behavior, thereby suppressing feeding and disease transmission.

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