Thrips tabaci Lindeman Thysanoptera Thripidae

Natural History

Distribution. Onion thrips is believed to have originated near the eastern end of the Mediterranean Sea, or perhaps India. It was first observed in North America in 1872, and by the early 1900s had spread throughout the United States and southern Canada. It is easily transported on plant material, and redistribution of onion thrips occurs frequently with commercial shipment of bulbs and plants. It is now found throughout the world. (See color figure 181.)

Host Plants. Onion thrips has a wide host range, reportedly feeding on over 300 plants. In Hawaii, for example, 66 plants from 25 families were found to support onion thrips (Sakimura, 1932). It has been found to infest such vegetables as asparagus, bean, beet, cabbage, cantaloupe, carrot, cauliflower, celery, cowpea, cucumber, garlic, kale, leek, mustard, onion, parsley, pea, pepper, pigeon pea, potato, pumpkin, spinach, squash, sweet potato, tomato, and turnip. Under field conditions, the most serious problems occur on onion, followed by cosmetic injury to cabbage and edible-podded pea. In greenhouse cultivation of vegetables, onion thrips sometimes causes severe injury to tomato and cucumber. Field crops such as alfalfa, cotton, oat, soybean, sugarbeet, wheat, and tobacco also may support onion thrips. Ornamental crops such as rose and carnation may be injured, especially when grown under greenhouse conditions. Many common weeds support onion thrips, including amaranth, Amaranthus palmeri; dandelion, Taraxacum officinale; mullein, Ver-bascum thapsus; goldenrod, Solidago canadensis; ragweed, Ambrosia spp.; kochia, Kochia scoparia; sage, Salvia sp.; sunflower, Helianthus annuus; smartweed, Polygonum spp.; and yellow nutgrass, Cyperus esculen-tus (Chittenden, 1919; Doederlein and Sites, 1993). (See color figures 13,14, and 15.)

Onion thrips is the most important insect pest of onion, and the dominant thrips species on onion. However, it is not the only species attacking onion, and in the southern states it is sometimes a relatively small component of the thrips fauna, being supplanted by western flower thrips, Frankliniella occidentalis (Per-gande) (Bender and Morrison, 1989; Doederlein and Sites, 1993), and possibly by tobacco thrips, Frankliniella fusca (Hinds) (D.G. Riley, personal communication).

Natural Enemies. No natural enemies of significance are known. Numerous species of lady beetles (Coleoptera: Coccinellidae), lacewings (Neuroptera: Chrysopidae), and flower flies (Diptera: Syrphidae) have been observed attacking onion thrips, but none regularly are effective enough to provide suppression. Insidious plant bug, Orius insidiosus (Say), and minute pirate bug, O. tristicolor (White) (both Hemiptera: Anthocoridae), are among the most effective of the predators, because their small size allow them to pursue the thrips between the closely appressed leaves of the onion plant, but these predators are rarely abundant enough to suppress thrips populations. Parasi-toids have been introduced from Southeast Asia, where they parasitize a high proportion of onion thrips and other thrips species. In Hawaii, Ceranisus brui (Vuillet) (Hymenoptera: Eulophidae) was successfully introduced, but introductions of other Ceranisus spp. failed (Clausen, 1978).

Weather. Weather is reported by many authors to be important in determining thrips abundance and damage. The combination of abnormally high temperature and low precipitation stimulates thrips reproduction and/or enhances survival. High temperature speeds up the life cycle, increasing the biotic potential of populations. Heavy rain is considered to be an important mortality factor, and is easy to observe large decreases in thrips abundance following significant rainfall events (Harding, 1961).

Life Cycle and Description. The life cycle of onion thrips is completed rapidly. Based on field work conducted in Iowa, development time from the egg to adult stages is estimated at only 10 days in July, and 20 days in September. Similar values were obtained by Watts (1934) in South Carolina. Sakimura (1932) studied this insect in Hawaii, and observed longer developmental periods, but these studies were conducted during the relatively cool winter months. In any event, the potential number of generations is great under ideal conditions. The actual number of generations is estimated at ten per year in southern climates but only two in the north. In temperate areas, overwintering occurs in the adult stage. Adults survive on winter wheat, alfalfa, clover, other crops and weeds, but not on soil in the absence of living plants (Chambers and Sites, 1989). Some of these crops, particularly wheat, are also favorable for oviposition and larval development in the spring, and provide inoculum for nearby vegetables (Shirck, 1951; North and Shelton, 1986b). In warmer climates nymphs may survive the winter, or reproduction may continue throughout the year.

  1. The female cuts slits in the foliage and deposits eggs just beneath the epidermis, with one end of the egg protruding slightly. The egg is colorless or yellowish white. It measures about 0.26 mm long and 0.12 mm wide, a size that is quite large considering the small size of the female. The egg is bean-shaped, with one side being strongly concave whereas the opposite side is strongly convex. Duration of the egg stage is estimated at 5-7 days when held at 21 °C, but only three days at 25°C.
  2. The larvae of thrips (sometimes called nymphs) resemble the adults in appearance, though the larvae are colorless or yellowish-white. There are two instars. The first instar measures about 0.4 mm long, whereas the second instar measures about 0.9 mm long. The larvae can be differentiated by the tarsal arrangement—first instars bear tarsi with two claws, but these are absent from second instars. A less reliable, but more convenient, character for distinguishing the instars is their color; first instars tend to be colorless to white, whereas second instars tend to be yellowish. Both the first and second instars bear antennae with four segments. Larval duration varies from 3-11 days, with about 8-10 days required for development at 21°C and 5-6 days required at 25°C. Watts (1934) reported development times of 2.0 and 2.8 days, respectively, for the first and second instars. Larvae usually confine their feeding on onion to the youngest foliage at the center of the plant, but are more widely distributed on cabbage.
  3. After feeding for the first two instars, the larva almost always leaves the foliage and descends to the soil, where it constructs a small earthen chamber. Occasionally, it descends only to some vegetative structure such as a leaf axil. The active larval stages are followed by relatively inactive prepupal and pupal instars, which may last about 1.0 and 2.5 days, respectively, at warm temperature. This non-feeding period requires about 5-7 days at 21 °C, and 4-6 days at 25°C. These stages are colorless to yellow, and measure about 0.7mm long. Setae are much more abundant on the prepupal and pupal stages than in the larvae, and their wing pads are visible. The wing pads of the prepupae extend back to the second abdominal segment. The wing pads of the pupae are considerably larger, extending back to the eighth abdominal segment. Antennae of the prepupal stage project forward, whereas those of the pupal stage orient back over the thorax.
  4. The adults do not occur in an equal sex ratio. Male thrips are relatively rare, and seem to be more plentiful in the autumn (Sakimura, 1932) and in the western hemisphere (Kendall and Capinera, 1990). Females generally reproduce parthenogeneti-cally. Females are about 1.0-1.2 mm long, and yellowish or yellowish-brown. Patches of dark-brown occur on the thorax and abdomen. The overall body color is lighter in the summer and darker in the winter. The wings are colorless, and extend back to about the sixth abdominal segment. As is typical of thrips, there are two pairs of long, narrow wings, each bearing a fringe of hairs. Male onion thrips are slightly smaller than females, and have nine abdominal segments instead of the ten found in females. A pre-ovi-position period in adults of about three days was noted by Watts (1934), but it was estimated at 5-7 days by Sakimura (1932). Adult females live about a month, and typically deposit an average of 30-40 eggs (maximum of about 100 eggs) at 1.5-2.5 per day.

Differentiation of onion thrips from other common vegetable-infesting thrips requires close examination. The adult female of onion thrips has seven antennal segments, a character that is useful to distinguish this species from co-occuring Frankliniella thrips; females of western flower thrips, F. occidentalis, and tobacco thrips, F. fusca, have eight antennal segments. To distinguish onion thrips from melon thrips, which also has seven antennal segments, it is helpful to examine the ocelli. There are three ocelli on the top of the head, in a triangular formation. In onion thrips a pair of setae originate from within this triangular formation, unlike the arrangement found in melon thrips, where the setae do not originate within the triangle. The ocelli also tend to be gray in onion thrips, but bear red pigment in melon thrips. Although the body color of onion thrips is quite variable, some gray or brown is usually present on the body of adults in addition to yellow, whereas in melon thrips the body is uniformly yellow. Melon thrips has a very resticted geographic range, and so should infrequently be confused with onion thrips.

Good accounts of onion thrips biology were given by Chittenden (1919) and Horsfall and Fenton (1922). Developmental parameters were given by Sakimura (1932), Watts (1934), and Edelson and Magaro (1988). Quaintance (1898b) provided a useful morphological description. A key for identification of common thrips was given by Palmer et al. (1989). This species also is included in a key to common vegetable-infesting thrips in Appendix A.

Damage

The principal form of damage caused by onion thrips results from the piercing of cells and removal of cell contents by larvae and adults. In onions, this leads to an irregular or blotchy whitening of the leaves, a condition sometimes termed "blast." Heavy levels of feeding injury disrupt the hormonal balance of the plant, causing the leaves to curl and twist, and the foliage to be stunted (Kendall and Bjostad, 1990).

Adult female onion thrips.

Thrips Tabaci

Anterior region of onion thrips.

Adult female onion thrips.

Anterior region of onion thrips.

Such damage decreases onion bulb size, and may even lead to death of the plant. Silvering or whitening of the pods on edible-podded peas also is attributed to onion thrips (Shelton and North, 1987). On cabbage, feeding by thrips causes a bronze discoloration and rough texture, and the cabbage heads may fail fresh market standards (North and Shelton, 1986a).

Crops such as cabbage also may fail processing standards due to contamination of products such as sauerkraut with thrips bodies (Shelton et al., 1982). As happens with onion, the thrips feed in sheltered locations, here between the leaves that form the cabbage head. The tips of asparagus spears may be heavily infested with thrips following dispersal from nearby weeds or crops. Careful management of weeds and crop borders can alleviate such problems (Ban-ham, 1968).

The relationship between thrips numbers and onion yield has been the subject of much study. Although Mayer et al. (1987) found no relationship between thrips abundance and yield of dry onions in Washington, studies in Colorado (Kendall and Capinera, 1987), Texas (Edelson et al., 1986, 1989), and Quebec (Four-nier et al., 1995) demonstrated yield decreases associated with thrips feeding. For thrips injury to be signifícant, feeding must occur during the mid-season period of rapid bulb expansion; early and late season feeding has little or no effect on yield. Also, there is a threshold effect. Thrips densities of 1-2 per leaf or 30 per plant generally must be reached for injury to occur. To complicate matters further, however, onion responses are modifíed somewhat by weather, particularly moisture, and by onion variety. Sweet onions are particularly susceptible to bulb size reduction. Unlike the situation with storage onions, there is virtually no tolerance of thrips on scallions (green onions) because the tops as well as the developing bulb are marketed and consumed (Kawate and Couglin 1995).

Onion thrips may also affect plant disease incidence. The fungus Alternaría porri causes a foliar disease of onions called purple blotch. Although the fungus does not depend on thrips for transport or inoculation, feeding wounds can serve as a penetration site for the purple blotch fungus, and disease incidence is increased in the presence of thrips (McKenzie et al., 1993). Onion thrips is also implicated in the transmission of tomato spotted wilt virus to several vegetable crops (Greenough and Black, 1990). Tomato spotted wilt virus is acquired by thrips during the larval stage, but the insects remain infected and capable of transmitting the virus for the duration of their life (Sakimura, 1963).

Management

Sampling. Edelson et al. (1986) studied the dispersion of thrips among onion plants and reported a clumped distribution. Distribution within plants also is non-uniform. Thrips densities are normally determined by visual examination of plants. Although there is variation among counts attributable to different observers (Theunissen and Legutowska, 1992) there is a strong correlation between visual estimates and actual population densities (Edelson, 1985a). Onion thrips is normally found at the basal area of onion leaves or in the leaf folds, and it is necessary to pull the leaves apart slightly to observe the entire population. This is especially true early in the season and early in thrips development, while later the thrips are more prone to move apically. Sunny weather, maturity, and the need for flight are reputed to account for the change in thrips distribution (Sites et al., 1992). Sequential sampling (Shelton et al., 1987) and binomial (presence-absence) sampling (Fournier et al., 1994) plans have been developed to reduce the effort associated with thrips sampling on onion.

Thrips are active and are readily dispersed by wind when they fly. Because thrips readily disperse from crop to crop, it is useful to employ sticky traps to monitor thrips flights, or to monitor their densities in crops that provide potential inoculum. White- or yellow-sticky traps can be used for monitoring thrips in flight, and thrips on foliage can also be sampled by using heat to drive than from the foliage, as with a Berlese funnel (Shelton and North, 1986; Doederlein and Sites, 1993).

Insecticides. Insecticides are frequently used for thrips suppression, especially during the period of rapid bulb expansion when plants are most susceptible to injury, or late in the season when thrips have the potential to reach very high levels of abundance and feeding injury is obvious. Foliar applications are made as frequently as twice per week in commercial onion production. It is difficult to obtain excellent control because of the cryptic nature of thrips feeding. Many onion and cabbage producers, concerned that they will be unable to eliminate thrips from sheltered feeding locations, apply insecticides as a preventive measure, in advance of potential problem development. Especially for cabbage, once the leaves begin to cup and form a head, effective insect control is difficult. Insecticides that produce toxic fumes are desirable, because they penetrate into crevices where thrips hide, but these materials are limited in availability. On occasion, insecticides are applied to the soil or plastic mulch beneath plants because the thrips descend to the soil to pupate, where they contact the insecticide (Pickford, 1984). Some, but not all, systemic insecticides effectively suppress thrips for at least part of the season (Getzin, 1973; Sinha et al., 1984). Insecticide resistance occurs in many locations.

Biological Control. Introduction of exotic eulo-phid parasitoids has had some success (see above, natural enemies), but this approach to biological control has not been fully exploited. Release of predators that are easily cultured, particularly lacewings (Neurop-tera: Chrysopidae), has not been very successful in the field. Predatory mites (Acari: Phytoseiidae) have been found to provide suppression of onion thrips in greenhouse culture (Bakker and Sabelis, 1989), as have releases of Orius spp. (Hemiptera: Anthocoridae). It is important to release adequate numbers of predators at the first sign of thrips infestations.

Cultural Practices. Crop management can influence the nature of thrips injury in several ways. For example, the proximity of susceptible crops to thrips sources is important. Damage sometimes occurs when thrips disperse in large numbers into susceptible crops. This often results when an early season crop such as oats or wheat reaches maturity, or when a crop is cut at mid-season, as is the case with alfalfa and clover (Banham, 1968; Shelton and North, 1986).

Mulches can influence the abundance of thrips and the transmission of plant viruses. In studies conducted in Louisiana, aluminum-surfaced mulch reduced the incidence of tomato-spotted wilt transmission by thrips to tomato and pepper by about 60-80% (Greenough and Black, 1990). This approach toward disease management has been studied much more with aphid vectors (see section on Melon Aphid), but most of this technology is probably applicable to thrips-transmitted diseases.

Intercropping can have some benefit for onion thrips management. Despite its wide host range, there are clearly preferred hosts, principally onion. For example, Uvah and Coaker (1984) alternated rows of onion with various ratios of carrot rows, and found that the presence of carrots decreased abundance of thrips. This occurred despite the fact that carrot is a nominal host of thrips.

Sanitation is very important. Long ago, Horsfall and Fenton (1922) noted the ability of thrips to disperse from contaminated overwintering plants left in the field, or from transplanted onion bulbs taken from storage, to newly seeded onions. Now, with the availa-bilty of rapid transportation, thrips are often moved with plant material, and then inadvertently inoculated into fields. For example, Schwartz et al. (1988) found that nearly all batches of onion transplants shipped from Texas to Colorado were contaminated with thrips. Sporadic incidence of insecticide resistance among Colorado onion fields apparently was related to different sources of onions and thrips, and different pesticide exposure histories. Also, in some northern areas greenhouses are a source of thrips in the spring.

Host-Plant Resistance. The cryptic nature of thrips feeding on onion has long made chemical control difficult, and has stimulated the search for resistant varieties. Characteristics associated with resistance are round leaves and open or spreading plant architecture, attributes sometimes found in white onion varieties. It has been speculated that this plant architecture affords less opportunity for thrips to hide between leaves, hastening their predation by other insects (Jones et al., 1935; Coudriet et al., 1979). However, differences in plant chemistry have also been suggested (Saxena, 1975) to account for this difference. Indeed, differences in the ratio of adult and larval thrips among onion varieties (Coudriet et al., 1979) could indicate physiological differences in suitability for thrips growth and survival. Some studies, however, report that the basis for resistance to onion thrips is feeding tolerance by some onion cultivars.

Resistance has also been identified among cabbage varieties (Shelton et al, 1983a;1988; 1998; Hoy and Kretchman, 1991), but the basis for resistance is uncertain, and no clear patterns have emerged that would allow prediction of resistant types of cabbage. It is interesting to note, however, that some "resistant" cul-tivars support as many thrips as the susceptible culti-vars, but on resistant plants the thrips feed principally on the outer leaves that are discarded at harvest, thus causing little damage (Stoner and Shelton, 1988). Whereas insecticide treatments alone sometimes fail to keep thrips from damaging thrips injury-susceptible cabbage in New York, when insecticides are used with varieties moderately susceptible to thrips injury, the combination is effective at preventing damage (Shelton et al., 1998).

Tobacco Thrips

Frankliniella fusca (Hinds) (Thysanoptera: Thripidae)

Natural History

Distribution. Tobacco thrips is widely distributed in eastern Canada and the United States, west to about the Rocky Mountains. However, it is most abundant, and most often recorded as a pest, in the southeastern states. It is a native species.

Host Plants. Vegetable hosts include bean, beet, cantaloupe, carrot, corn, cowpea, cucumber, onion, pea, pepper, potato, tomato, and watermelon. Because tobacco thrips can vector tomato spotted wilt virus, among vegetable crops it is known principally as a pest of tomato. Tobacco thrips is better known as a field crop-infesting insect, infesting alfalfa, barley several types of clover, cotton, lespedeza, peanut, rye, tobacco, vetch, wheat, and occasionally corn and oats. Winter grains such as rye and wheat, and volunteer peanut, apparently are suitable overwintering hosts. Several weeds have been reported to support tobacco thrips, such as Bermudagrass, Cynodon dactylon; blue toadflax, Linaria canadensis; broomsedge, Andropogon virginicus; buttercup, Ranunculus sp.; cocklebur, Xanthium sp; crabgrass, Digitaria sp.; cutleaf evening primrose, Oenothera laciniata; dandelion, Taraxacum officinale; dog fennel, Eupatorium capillifolium; false dandelion, Pyrrhopappus carolinianus; feathergrass, Leptochloa filiformis; Johnsongrass, Sorghum halepense; little barley, Hordeum pusillum; rabbit tobacco, Gnapha-lium obtusifolium; sand blackberry, Rubus cuneifolius; shepherdspurse, Capsella bursa-pastoris; spiny sowthis-tle, Sonchus asper; wild lettuce, Lactuca sp.; wild radish, Raphanus raphanistrum; wood sorrel, Oxalis spp.; and a grass, Brachiaria extensa.

Natural Enemies. The natural enemies of tobacco thrips have not been well documented, but likely are the same as those associated with western flower thrips, Frankliniella occidentalis. A nematode, Thripe-nema fuscum (Tylenchida: Allantonematidae), was observed to parasitize up to 68% of thrips in Florida, suggesting that this may be an important mortality factor in some cropping systems (Tipping et al., 1998). Insidious flower bugs, Orius insidiosus (Say) (Hemiptera: Anthocoridae), also have been observed to be important, and heavy rainfall is detrimental.

Life Cycle and Description. Tobacco thrips tend to be abundant in a crop during the spring and summer (McPherson et al., 1992). In Florida, tomato blossoms are infested during April-June (Salguero Navas et al., 1991a), but the thrips are abundant later further north. Several generations are present annually in Florida, including about three during the winter months (Toapanta et al., 1996). Eddy and Livingstone (1931) reported five generations annually from South Carolina. Unlike the situation in Florida, where reproduction occurs during the winter months, in Georgia, South Carolina, and Louisiana overwintering occurs only in the adult form. The life cycle requires about 15-21 days for completion.

  1. The egg is inserted into the foliage with an end protruding slightly. The egg measures about 0.25 mm long, is white, and bean-shaped. Mean duration of the egg stage is 6.7 days (range 3-10 days).
  2. The immature stages consist of two larval and two pupal instars. Only the larval instars feed on foliage. The first instar measures about 0.23 mm long, the second instar 0.60-1.17 mm. Both instars are yellowish or whitish. Mean duration of the first larval instar is about 1.1 and 1.0 days at 25° and 35°C, respectively. Mean duration of the second larval instar is about 4.7 and 2.6 days at 25° and 35°C, respectively. Larvae tend to feed in cryptic habitats such as blossoms and terminal growth, and rarely in open, exposed areas.
  3. At the completion of the larval instars the mature larva drops to the soil to pupate. The prepupa is 0.5-0.6 mm long, the pupa 0.6-1.2 mm. The color of these latter instars is yellow, but unlike the larval instars they display wing pads. Mean duration of the prepupa is about 1.1 and 0.8 days at 25° and 35°C, respectively. Mean duration of the pupa is about 1.4 days at both 25° and 35°C.
  4. The adult stage is variable but often has two pairs of fringed wings. The fringe on the anterior edge of the wings is markedly shorter than the fringe on the posterior edge. The adults measure 1.0-1.3 mm long. The head and thorax are light brown or yellowish-brown, but the abdomen is dark-brown. The antennae consist of eight segments. Long-winged (macropterous) and short-winged (brachypterous) forms occur, with brachypterous forms dominant during the winter months. The wings of the macropterous form usually do not attain the tip of the abdomen, but wing length is quite variable. Wings of the brachypter-ous forms barely extend to the first abdominal segment. Feeding behavior of the adults is similar to that of the larvae. The mean pre-oviposition period is about 2.6 days (range 2-6 days). Lowry et al. (1992) reported adult female longevity of about 6-10 days, and fecundity of 13-24 eggs per female, but these values seemed small and might reflect a poor host or suboptimal rearing conditions. When fed cotton, mean longevity of mated females is 27-47 days and fecundity about 20-60 eggs per female (Eddy and Livingstone, 1931). Fertilized females produce both female and male offspring, though females are favored; unfertilized females produce only males.

Distinguishing tobacco thrips from other vegetable-infesting thrips requires careful examination. Anten-nal structure can be used to separate the Thrips spp. because their antennae consist of seven segments, whereas in Frankliniella there are eight segments. Separation of western flower thrips from tobacco thrips is accomplished by examining the eighth dorsal plate on the abdomen. In western flower thrips there is row of short hairs of approximately equal length along the posterior edge, whereas in tobacco thrips the hairs at the center of the posterior edge are shorter or absent.

The biology of tobacco thrips was presented by Hooker (1907) and Eddy and Livingstone (1931), but additional observations were made by Newsom et al. (1953), Chamberlin et al. (1992) and Chellemi et al. (1994). Developmental data were given by Watts (1934) and Lowry et al. (1992). Culture methods were described by Kinzer et al. (1972). Keys for identification were included by Palmer et al. (1989) and Oetting et al. (1993). Also, this species is included in a key to common vegetable-infesting thrips in Appendix A.

Thysanoptera Indent Indent
Adult female tobacco thrips.
Tobacco Thrip
Anterior region of tobacco thrips.

Damage

Vegetable seedlings can be damaged by this thrips when they disperse to young annual crops from maturing perennial crops such as alfalfa or clover. Thrips feed and deposit eggs into the young tissue, causing young leaves to curl upward and older leaves to acquire a silvery or speckled, and crinkled, appearance (Webb, 1995). Buds and other young tissue may be killed, giving the seedling a scorched or burnt appearance. Destruction of terminal growth may disrupt apical dominance, producing an excessively bushy, branched growth form. Tobacco thrips may be found in blossoms, but unlike its co-occurring species western flower thrips, it is primarily a leaf feeder. Direct feeding injury has been studied best in peanuts, where insect suppression has been shown to increase yields slightly or not at all (Tappan and Gorbet 1981, Tappan 1986, Lynch et al., 1984a). Similarly, direct injury to vegetables in infrequent, but because tobacco thrips now transmits tomato spotted wilt virus, its importance as a vegetable pest has escalated greatly. As happens with western flower thrips, virus acquisition occurs in the larval stage. After a latent period of 4-18 days, adults remain capable of transmitting tomato spotted wilt throughout their life (Sakimura, 1963). Weeds are important in the overwintering of both the thrips and virus (Hobbs et al., 1993; Johnson et al., 1995).

Management

  1. Distribution of tobacco thrips in tomato blossoms was studied by Salguero Navas et al. (1994). Populations were aggregated or randomly dispersed, varying with year of sampling. A binomial (presence or absence) sampling protocol was developed and shown to be useful for populations with less than an average of two thrips per blossom. These authors recommended collecting 16-18 flowers to assess the need for population suppression. Washing of plant material with a dilute sodium hypochlorite and soap solution produced higher thrips estimates than visual searches (Burris et al., 1990)
  2. Management of this species is normally accomplished in conjunction with western flower thrips suppression, because Frankliniella occi-dentalis is generally more numerous and damaging (see the discussion under western flower thrips for more detail), they are similar in ecology, and because they occur together in mixed populations. Other thrips species, particularly flower thrips, Frankliniella tritici (Fitch), also may be present, but because they are not an important vectors of tomato spotted wilt virus they are considered to be of little importance.

Western Flower Thrips

Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae)

Natural History

Distribution. Formerly restricted mostly to the western United States and Canada, by 1980 this native thrips had spread east to Georgia. Subsequently, it has spread throughout the United States and into southern Canada, and to other continents. It also has become a serious pest in Hawaii. Range expansion has undoubtedly been enhanced by movement of ornamental plants and vegetable seedlings from southern nurseries. It survives best in warm climates, and overwinters outdoors on growing plants along the west coast and throughout the southeastern states. Normally it is not thought to overwinter in very cold climates, but to re-invade these areas annually from greenhouses, or via introduction of seedlings from southern areas. However, the report of overwintering in Pennsylvania under leaf debris and in bare soil (Felland et al., 1993) suggests a significant degree of cold hardiness. (See color figure 182.)

Host Plants. Western flower thrips apparently has an exceedingly wide host range. However, plant suitability varies seasonally and even geographically. Also, from an economic perspective the most important hosts are those that support both thrips reproduction and virus disease multiplication. Western flower thrips occurs on several vegetable crops, including cucumber, onion, pepper, potato, lettuce, and tomato. Tomato is most seriously injured directly by the thrips, through oviposition, but both lettuce and tomato are seriously damaged by tomato spotted wilt virus transmitted by thrips. Under greenhouse conditions, cucumber and pepper also are readily damaged. Field crops on which western flower thrips occurs include alfalfa, canola, crimson and white clover, millet, peanut, rye, vetch, and wheat. Several fruit crops have been reported to serve as hosts, such as apple, blackberry, blueberry, peach, pear, and plum. Among the weeds that serve as good hosts are such common species as black nightshade, Solanum nigrum; cheese weed, Malva palviflora; daisy fleabane, Erigeron annuus; dandelion, Taraxacum officinale; false dandelion, Pyr-rhopappus carolinianus; jimson weed, Datura stramonium; galinsoga, Galinsoga parciflora; lambsquarters, Chenopodium album; lantana, Lantana camara; pigweed, Amaranthus spp.; prickly lettuce, Lactuca serriola; sorrel, Oxalis spp.; sowthistle, Sonchus oleraceus; and wild radish, Raphanus raphanistrum (Stewart et al., 1989; Yudin et al., 1986; Chamberlin et al., 1992; Bautista and Mau, 1994; Chellemi et al., 1994), but numerous other species also can serve as hosts. In Hawaii, the blossoms of woody legumes growing near cultivated fields serve as a major source of thrips.

Natural Enemies. Considering the abundance of western flower thrips and the severity of their injury to plants, surprisingly little is known about natural enemies. Minute pirate bugs, particularly Orius tristi-color (White), feed voraciously on western flower thrips, and there is good evidence that they suppress thrips populations in vegetable crops (Salas-Aguilar and Ehler, 1977; Letourneau and Altieri, 1983). Cerani-sus spp. (Hymenoptera: Eulophidae) parasitize the immature stages, but are not generally abundant. Fungal epizootics caused by Verticillium and Entomophthora have been observed in moist climates. Nematodes in the genus, Thripenema (Howardula) (Nematoda: Allan-tonematidae), appear to be frequent associates of western flower thrips (Wilson and Cooley, 1972; Heinz et al., 1996), and induce sterility in their hosts (Poinar, 1979). Impact of these nematodes has been inadequately studied, but an incidence of 88% has been reported from California (Heinz et al., 1996).

Life Cycle and Description. In mild climates these thrips readily overwinter as adults and nymphs on many crops and weeds. However, in relatively cold climates such as northern Texas they overwinter on hardy crops such as alfalfa and winter wheat (Chambers and Sites, 1989). As noted above, they apparently can also survive in leaf debris and soil under the cold-weather conditions of Pennsylvania (Felland et al., 1993). Toapanta et al. (1996) estimated 3-5 generations per year in north Florida, with populations highest in spring and a smaller peak in autumn. They can complete one generation in 15 days, so under ideal conditions many more generations are possible. A temperature of about 30°C seems to be optimal for population growth.

  1. The eggs are deposited in young vegetative tissue, with one end protruding slightly. They are shaped like a bean, white in color, and measure about 0.25 mm long. Duration of the egg stage is reported to require 5-15 days in the field, but mean duration is only 2.6 days at 25°C. Females were reported by Gaum et al. (1994) to produce about 9-10 eggs during their life span when cultured on cucumber, and Lowry et al. (1992) reported that fecundity was 14-23 eggs per female when fed peanut. Because western flower thrips have preferred hosts, and usually include pollen in their diet, the aforementioned estimates of egg production may be artificially low. Thus, Lublinkhof and Foster (1977), recorded 43-95 eggs per female cultured on bean, and Trichilo and Leigh (1988) observed fecundity of about 130 eggs per female on cotton but 190 eggs on cotton supplemented with pollen.
  2. Development of the immature thrips requires two larval instars (also sometimes called nymphs), which are feeding stages, followed by non-feeding prepupal and pupal stages. The temperature threshold for larval development is about 9.4°C. Larval development time may require 9-12 days in the field, extending to 60 days during the winter. However, when reared at a constant temperature of 25°C, the first and second larval instars require only 2.3 and 3.7 days, respectively. Larvae and adults are somewhat gregarious, often feeding together in small groups. At maturity, the larvae drop to the ground to pupate.
  3. The prepupal and pupal stages are reported to require 1-3 and about 3-10 days, respectively, under field conditions. At a constant temperature of 25°C, however, thrips complete their pupal development in an average of 1.1 and 2.7 days, respectively. The prepupa is distinguished by the presence of short-wing pads and erect antennae. The pupae have long wing pads that reach almost to the tip of the abdomen, and antennae that are bent backward along the head. Prepupae and pupae may be found on the surface, under debris, or in cracks and crevices to a depth of 7-10 cm.
  4. The adults have fully formed, fringed wings and measure 1.2-1.9 mm long, averaging 1.5 mm. The fringe along the anterior edge is markedly shorter than the posterior edge. Body color varies from yellow to brown. The antennae bear eight segments. The adults commonly live about 20-30 days, but some persist providing 40-70 days. Females may mate, or reproduce parthenogenetically. Unmated females produce only males, whereas mated females produce both sexes. The offspring of mated females are female-biased, usually on the order of 2:1. Females mate immediately upon emergence, and repeatedly over the course of their life. Dispersal by adults usually occurs when their food plants become unsuitable, which commonly results from drought, maturity, or harvesting.

Distinguishing western flower thrips from other vegetable-infesting thrips requires careful examination. Antennal structure can be used to separate the Thrips spp., because their antennae consist of seven segments, whereas the antennae in Frankliniella bear eight segments. Separation of western flower thrips from tobacco thrips, Frankliniella fusca (Hinds), is accomplished by examining the eighth dorsal plate on the abdomen. In western flower thrips there is row of short hairs of approximately equal length along the posterior edge, whereas in tobacco thrips the hairs at the posterior edge of the plate are shorter or absent centrally.

Both nymphs and adults produce an alarm phero-mone, and respond to it by moving away from the source of the pheromone, and usually by dropping from the plant. The pheromone is released in droplets of anal fluid (Teerling et al., 1993).

Thrips biology was given by Bailey (1933b), Bryan and Smith (1956), Lublinkhof and Foster (1977), Gaum et al. (1994), and van Rijn et al. (1995). Rearing techniques were described by Teulon (1992) and Doane et al. (1995). Keys that included western flower thrips were presented by Palmer et al. (1989) and Oetting et al. (1993). Also, this species is included in a key to common vegetable-infesting thrips in Appendix A.

Damage

This species, as its common name suggests, prefers an interstitial habitat such as within flowers or in leaf clusters; only rarely is it found in exposed locations. It typically feeds on pollen grains and on the ovary of flowers, resulting in malformed, stunted, or discolored fruit. In cucumber, for example, western flower thrips feeding causes silvery, web, or streak-like scarring, which may be accompanied by fruit malformation (Rosenheim et al., 1990). When they feed on foliage, they cause distortion of expanding leaves and mottling or speckling of mature leaves. On onion, their

Adult female western flower thrips.
Anterior region of western flower thrips.

feeding injury is similar to the effects of feeding by onion thrips, Thrips tabaci Lindeman.

Thrips also deposit eggs in small fruits, inducing deformities. In the absence of flowering plants, however, they oviposit readily on such plants as non-flowering lettuce. Salguero Navas et al. (1991a) documented the damage to tomato fruit caused by ovi-position, typically reflected by a dimple or indentation surrounded by a light-colored halo. Western flower thrips was much more damaging than some other tomato-infesting thrips at comparable densities. In southern Texas, western flower thrips has been reported to damage onions along with onion thrips (Bender and Morrison, 1989). These thrips also are found associated with onion blossoms, where they enhance pollination and seed set. Only at very high densities, approximately 9,000-10,000 thrips per onion seed head, is damage likely to occur (Carlson, 1964).

There is a strong association between the prevalence of western flower thrips and tomato spotted wilt virus. In this thrips species, oviposition preference is as important as feeding preference, because only nymphs are capable of virus acquisition. Thus, selection of oviposition sites by females determines the likelihood of the thrips developing into a virus vector. Once infected, the thrips remain capable of transmitting the virus for the remainder of their life. Tomato spotted wilt virus-infected weeds are the major host of virus in vegetable fields unless susceptible crops are cultivated continuously (Cho et al., 1986,1987).

Western flower thrips has become a particularly serious pest of vegetable and ornamental greenhouse crops. Its short development time, wide host range, cryptic feeding habits, and particularly its tendency to evolve insecticide resistance rapidly, make it well suited for inhabiting commercial greenhouses.

Despite the severity of the western flower thrips-virus disease problem on some crops, these thrips are not entirely detrimental. The thrips also feed on mites, and serve as important alternate hosts for some larger predators. Thus, in cropping systems that are not particularly susceptible to thrips or virus injury, the presence of low to moderate numbers of thrips can be beneficial (Gonzalez et al., 1995a).

Management

Sampling. Thrips densities in blossom samples are often made in the field, by visual examination of the plant or by shaking the blossom or other vegetative material over a tray, but the precision of this type of population estimate is quite low. A better estimate is gained by submerging the plant sample in 70% etha-nol, or in sodium hypochlorite and soap solution, and shaking it to dislodge the insect. Rummel and Arnold (1989), for example, found that thrips counts were 5-6 times higher when sampled by washing vegetation. A sample unit of 10 blossoms from each of five areas in a field is considered optimal (Cho et al., 1995). Thrips densities can also be estimated with the use of sticky traps. Yellow, white, and blue traps are generally most attractive to western flower thrips (Yudin et al., 1987; Vernon and Gillespie, 1990). Trap efficiency is increased by highly contrasting background color; yellow in front of a violet background, for example, is highly attractive (Vernon and Gillespie, 1995). Thrips can also be captured in water traps, and higher captures are made when certain volatile chemicals are added to the trap (Teulon et al., 1993). Sampling has been reviewed by Shipp (1995).

In tomato, western flower thrips are most abundant in blossoms on the upper half of plants, and at field margins. Nymphs are more abundant in blossoms in the lower regions of plants (Salguero Navas et al., 1991a). Thrips populations, especially nymphal populations, are aggregated. A binomial, or presence-absence, sampling program has been developed for tomato when thrips densities average less than 1.4 per blossom; 16-18 blossom samples are used to estimate abundance and suppression is initiated only when greater than 50% of the blossoms are infested (Salguero Navas et al., 1994).

Insecticides. Insecticides are commonly applied to the foliage and blossoms of vegetables to minimize feeding and oviposition damage and to limit disease transmission. However, insecticide resistance is a widespread phenomenon (Zhao et al., 1995). The severity of the resistance problem in the field is exacerbated by the ability of thrips to infest and escape from greenhouses, where insecticide use is frequent. Rotation of insecticide classes is frequently recommended to forestall development of resistance. If insecticides are used, a common practice is to apply two treatments about five days apart because the eggs are within the plant tissue and the prepupal and pupal stages are beneath the soil, and thus relatively immune.

Cultural Practices. Barriers are sometimes recommended for insect exclusion, including such small species as thrips. However, the small size of western flower thrips (width of males is about 184 microns; width of females about 245 microns) requires extremely fine screen if thrips are to be denied access to plants. This fact excludes most standard materials from consideration as screens (Bethke and Paine, 1991). However, low barriers can be used under fíeld conditions to limit thrips dispersal and invasion of crops (Yudin et al., 1991). Also, walk-in tunnels or greenhouses covered with ultraviolet light-absorbing plastic are less infested by thrips than ultraviolet light-reflecting coverings, apparently due to reduced attraction of plants grown in flitered light or to modifíed thrips feeding behavior (Antignus et al., 1996).

Sanitation is an important element in thrips management. Weeds can serve as important alternate hosts of both thrips and virus diseases, and their presence should be minimized. Also, if seedlings are used to initiate a crop, care should be taken to assure that they are free from thrips. The proximity of greenhouses is another consideration, as this may be a principal source of crop infestation by thrips, especially in cold climates where overwintering success by thrips is limited.

Biological Control. Considerable emphasis has been placed on development of biological control agents for thrips-infesting greenhouses, including western flower thrips. Such benefícial organisms as the parasitic wasp Ceranisus menes (Hymenoptera: Eulo-phidae) (Loomans et al., 1995); the minute pirate bug, Orius laevigatus (Hemiptera: Anthocoridae) (Chambers et al., 1993); the foliage-dwelling predatory mites Amblyseius cucumeris (Oudemans) and A. degenerans Berlese (Acari: Phytoseiidae) (van Houten and van Stratum, 1995); the soil-dwelling predatory mites Geo-laelaps sp. (Acari: Laelapidae) (Gillespie and Quiring, 1990); and entomopathogenic nematodes (Nematoda: Heterorhabditidae and Steinernematidae) (Chyzik et al., 1996) have been studied. Some beneficial organisms, particularly the mite A. cucumeris, are used in commercial greenhouse vegetable production. Factors such as temperature, photoperiod, and crop type sometimes limit success, even under greenhouse conditions. For example, mite predators are much more effective in suppressing western flower thrips on pepper than on cucumber, presumably due to interference with mite searching behavior by the numerous tri-chomes found on cucumber leaves (Shipp and Whit-fíeld 1991). Several common entomopathogenic fungi such as Beauveria bassiana, Metarhizium anisopliae, Paeci-lomyces fumosroseus, and Verticillium lecanii also have been used, but the level of suppression is only moderate. The expense and dispersal tendencies of most benefícial organisms thus far have limited their use to greenhouses.

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