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Tomato Spotted Wilt Virus: TSWV in Vegetable Crops: Tospoviruses
Tospoviruses In Solanaceae and Other Crops in The Coastal Plain of Georgia
Thrips Vectors of TSWV
David Riley, Robert McPherson, Lenny Wells
- Introduction
- General Biology
- Feeding
- Thrips Vector Species
- Thrips Vector Studies Relative to Plant Age
Thrips are minute, slender-bodied insects (around 1/16 inch long when fully grown, Fig. 2) that have become an important agricultural pest because of their ability to transmit plant viruses. In Georgia, TSWV has reduced tomato yields by an estimated $8.8 million in a single year in 2000 (Riley, 2000). Also, this virus has become a major yield-limiting factor to production of many other crops in Georgia, including pepper, peanut, and tobacco with total losses estimated at $100 million in 1996 (Bertrand, 1997; Pappu, 1997). Although TSWV is transmitted by multiple species of thrips (Ullman, 1997), thrips responsible for spotted wilt epidemics in Georgia and Florida can be largely attributed to western flower thrips, (Frankliniella occidentalis), tobacco thrips, (F. fusca), and possibly F. bispinosa (Salguero et al., 1991; Riley and Pappu, 2000, 2004; and Webb et al., 1997, respectively).
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Figure 2. Brachypterous tobacco thrips,Frankliniella fusca |
Possibly other species could be involved in vectoring tospoviruses, but these species are thought to be the most important. Because each generation of thrips must re-acquire the virus, as the virus in adult females is not passed on to her eggs, the frequency of viruliferous adults can vary greatly over time. However, even low percentages of viruliferous thrips can cause significant yield loss. Viruliferous thrips are usually <10 percent of the field population even in a severe TSWV year. The percentage tends to increase over time in the spring.
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Thrips belong to the insect order Thysanoptera (fringe-winged insects, their wings consisting of fine hairs rather than a membrane) and the main TSWV vector species all belong to the family Thripidae. In the Georgia solanaceous crops, TSWV is primarily transmitted by western flower thrips, (Frankliniella occidentalis, Pergande), and tobacco thrips, (F. fusca, Hinds) (Riley and Pappu, 2000, 2004; Salguero et al., 1991). Immatures are a cream to yellowish color and adults are either dark brown or yellow/orange depending on the species. Adults usually have wings but wings can be absent in tobacco thrips (brachypterous form, Fig. 2). When wings are present they are narrow and fringed with long hairs (Fig. 4, page 14). Eggs are laid singly and usually inserted in plant tissue (usually flower parts or young leaves). The eggs hatch in 3-4 days. There are two larval stages that last about 10-14 days, prepupa and pupa stages that last around 7 days, in which the thrips are inactive and do not feed, and then the adult stage. The only stages that can acquire TSWV are the two larval stages and this only occurs when larvae feed on an infected plant host. It is not passed from adults to eggs, so each generation of thrips must re-acquire the virus for the disease epidemic to continue. This is fortunate because thrips can reproduce parthenogenically. That is, if female thrips remain unmated then all male offspring are produced asexually. If thrips are mated, then they produce mostly female offspring.
It is important to note that once thrips acquire the virus, they remain viruliferous (infected with virus) throughout their life span. Several generations occur per year in Georgia, but only one or two generations in a single growing season of tobacco or tomato. Thrips overwinter on host plants, as adults or larvae (nymphs), and can be observed on winter weeds during warm periods throughout the winter months. Thrips extracted from weeds in Georgia have predominantly been in the larval stages. It has been observed that tobacco thrips can reproduce year-round in south Georgia in the winter onion crop and in weed hosts, even though winter populations are very low and the life cycle is greatly extended with the lower average temperatures. Infected thrips are capable of transmitting TSWV to a wide range of host plants spanning several hundred plant species from over 70 plant families. Thus, these winter populations of thrips are important for maintaining TSWV in the resident weed plant population. This sets the stage for TSWV epidemics in the following spring season.
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Figure 3. Illustration of thrips’ movement of TSWV in the spring. The nymphs acquire the virus from weeds before the fully developed adults transmit the virus to a springtime crop, like tomato.
Thrips feed on plant tissue with piercing and
sucking mouthparts. They produce an initial opening
by penetrating the plant cuticle with their single mandible
after rocking the head capsule downward and upward numerous times. Once an opening or food
channel is punched through the outer cell wall, then a
pair of maxillary stylets are extended into the plant
tissue. Saliva is injected into the plant and cellular
contents are drawn up through a pumping action. The
adults transmit TSWV as saliva is injected into the
plant tissue. Thrips feeding can damage plant tissue
directly. However, the greatest loss to agriculture is
caused by the species that vector (transmit) tospoviruses
like TSWV.
Since TSWV transmission occurs
with thrips feeding, understanding factors that affect
thrips feeding is critical for managing this pest. For
example, thrips vary greatly in their host preference
and, given a choice, they will lay eggs more in one
species of plant more than another (Chaisuekul and
Riley, 2005). Also, many factors can affect thrips feeding
and thus transmission efficiency. For example,
older plant age and treatment with the insecticide,
imidacloprid, has been shown to reduce feeding by
tobacco thrips (Joost, 2003). Unfortunately, imidacloprid
has been shown to increase settling in peanut
and feeding in tomato by western flower thrips, so it is
important to note that these effects can be specific for
the thrips species.
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Thrips have been found to be vectors of at least four plant virus groups (families), bunyaviruses, ilarviruses, sobemoviruses, and caroviruses (Ullman et al., 1997). Previously, eight species of thrips were reported to transmit TSWV (Wijkamp et al., 1995). Thrips tabaci Lindeman, T. setosus Moulton, T. palmi Karny, Frankliniella schultzei Trybom, F. occidentalis (Pergande), F. fusca (Hinds), and F. intonsa Trybom were reported to be vector of TSWV (Wijkamp et al., 1995, Ullman et al., 1997). Webb et al. (1997) also reported F. bispinosa (Morgan) as a vector of TSWV. Frankliniella tenuicornis (Uzel) and Scirtothrips dorsalis Hood had been previously reported to be vector of TSWV, but experimental verification had not been done for all species as has been done for F. occidentalis and T. tabaci (Ullman et al., 1997). Clearly, F. occidentalis and T. tabaci are common and important vectors of multiple plant viruses in many regions of the world (Ullman et al., 1997). In Georgia, western flower thrips, and tobacco thrips appear to be the most important species (Riley and Pappu, 2000, 2004).
A total of 43 species of thrips have been collected on flue-cured tobacco foliage and blooms in Georgia, and many of these same species are present on vegetables and other crops as well. However, only five species are commonly encountered during the growing season and include the tobacco thrips, the western flower thrips, the flower thrips, F. bispinosa (Morgan) and the grain thrips, Limothrips cerealium (Haliday). F. fusca is the predominate species on the foliage, and usually accounts for more than 90 percent of all the foliage thrips present, although L. cerealium can also be abundant on some sampling dates. Thrips are present at low densities (less than one per plant) on tobacco foliage soon after transplanting, and then steadily increase during the next 3-4 weeks after transplanting. They usually peak on foliage in early to mid-May, around six weeks after transplanting, before the tobacco flowering process begins. Peak populations of 50+ adult thrips per plant are common in Georgia in most growing seasons. Thrips movement within the field occurs between 9 a.m.-4 p.m. with almost no activity (captures on sticky cards) outside of this time range. Immature thrips (F. fusca) can be quite high (over 100 per plant) on some sampling dates in May.
In Georgia, the most common thrips in the tobacco blooms are F. tritici and F. bispinosa. Thrips can be collected from the blooms before the flowers fully open and continue to be present until the flowers dry up. Thrips peak in tobacco blooms in late May at over 100 adults per terminal floral branch (all blooms on single plant) plus immatures are very abundant. F. occidentalis are also present at relatively low populations in tobacco blooms every year. The thrips complex in tobacco flowers is probably of minor importance with regards to TSWV symptomatic plants in the crop, because they occur so late in the growing season. However, these same thrips species are also found on numerous flowering weeds in the tobacco farmscape throughout the summer, fall and winter. Many of the thrips in tobacco blooms do not complete one generation on the crop because the blooms are removed during the topping process. Many of the eggs and young larvae that are on these blooms that are removed from the plant do not survive to adulthood because the blooms dry up prematurely. Two other thrips species on weeds in the tobacco farmscape have also tested positive for a non-structural TSWV protein, indicating that these thrips also replicate the virus in their bodies and are potentially capable of transmitting TSWV. These other thrips include Haplothrips graminis Hood and Chirothrips spp. Both of these species are also present at low population densities on tobacco foliage.
Figure 5. Western flower thrips, Frankliniella
occidentalis
In the Georgia tomato crop, TSWV is primarily transmitted by western flower thrips, Frankliniella occidentalis (Pergande) (Fig. 5), and tobacco thrips, F. fusca (Hinds) (Fig. 1) (Riley and Pappu, 2000, 2004; Salguero et al., 1991). Of the individual species counted in tomato blossoms in 1997 and 1998 trials F. occidentalis represented 25 ± 2 percent and 31 ± 2 percent, respectively; and F. fusca represented 2 ± 0.7 percent and 7 ± 1 percent, respectively. The remainder consisted of other flower thrips (mainly F. tritici and F. bispinosa) and immature thrips (not identified to species). Frankliniella occidentalis was the predominant TSWV-vector species counted in the blossom sample in both years. Tobacco thrips have been found to be more prevalent than western flower thrips on preflowering tomato in Georgia (Joost and Riley, 2004) representing 74 percent of the adults collected. As in tobacco, thrips numbers on young tomato plants are low (less than one per plant), but this is sufficient to result in high incidence of TSWV. Once flowering occurs in the crop, thrips collected in blossoms are comprised mostly of flower thrips species and occur in much higher numbers. Relative to thrips species, two interesting correlations have been observed. Frankliniella occidentalis numbers in blossoms correlated better with percent TSWV as detected by ELISA than F. fusca and correlated well with percent TSWV based on plant symptoms. However, only F. fusca had a significant negative-correlation with marketable tomato yield and positive correlation with TSWV-affected fruit. The way we interpret these data is that although both thrips species are good vectors of TSWV, F. fusca occurs on tomato foliage in greater numbers earlier in the growing season during the preblossom< growth stages. TSWV inoculation of young vegetative tomato plants has been associated with significant negative effects on tomato yield (Chaisuekul et al., 2003) and so F. fusca tends to have Figure 5. Western flower thrips, Frankliniella occidentalis 16 Tospoviruses in Solanaceae and Other Crops in the Coastal Plain of Georgia more of an impact on yield than F. occidentalis. Even so, F. occidentalis is an excellent vector and occurs in greater numbers than F. fusca later in the season when tomato blossoms occur. In past studies, overall transmission of TSWV has been better correlated with F. occidentalis in tomato blossoms because F. occidentalis was more prevalent than F. fusca in flowers. The later the development of TSWV symptoms in the tomato plant, the lower the effect on the quality of tomato yield (Moriones et al., 1998). Thus, pre-blossom population of thrips early in the growing season could be important for correlating vector numbers to incidence of TSWV related damage to the crop.
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Thrips Vector Studies Relative to Plant Age
Recent thrips exclusion studies, using field cages to protect tobacco transplants, have concluded that the most critical time for thrips to transmit TSWV infection in flue-cured tobacco is during the first 6 weeks after transplanting. Plants protected from thrips feeding for the first two weeks following transplanting had 29.2 percent TSWV symptomatic plants compared to uncaged plants that had 36.3 percent. When plants were protected from thrips for 4 weeks and 6 weeks after transplanting, the seasonal incidence of TSWV symptomatic plants was lowered to 23.0 percent and 12.5 percent, respectively. None of the tobacco plants protected with thrips exclusion cages showed any TSWV symptoms until 2-4 weeks after the cages were removed, indicating that TSWV infection was occurring in the field after the plants were exposed to thrips infestation and not being brought into the field by TSWV infected plants obtained from the plant bed or greenhouse. Thus, thrips management practices need to focus on early-season control to be most beneficial in suppressing TSWV infection. Also, TSWV symptomatic plants that appear later in the season, 10-12 weeks after transplanting, usually have only minor reductions in plant height, leaves per plant and yield per plant compared to the non-symptomatic plants. When TSWV symptoms appear early in the season, 4- 8 weeks after transplanting, severe plant growth reductions and premature plant death usually occur.
In tomato cage and greenhouse vector studies at Tifton, tomato yield was lower as TSWV inoculation and TSWV symptoms occurred earlier (Chaisuekul et al., 2003). This effect was very dramatic in greenhouse studies where plants inoculated in the first few weeks after germination produced no marketable fruit. These results agree with that of Moriones et al. (1998) in that earlier symptomatic plants produce less yield than later symptomatic plants. A notable effect was that symptoms developed rapidly across all treatments after the screen cages were removed regardless of when thrips vectors were introduced into the field cages. We suspect that the cages often used in thrips vector studies are also a source of shading or temperature differences, which could potentially affect TSWV symptom expression (Diaz et al., 2003).
Only around 1-6 percent of all the thrips collected on tobacco throughout the growing season test positive for TSWV non-structural protein (using ELISA procedures) in any given year. Collections from a specific sampling date can have 10 percent or more thrips testing positive for TSWV, while other sampling dates have 0-1 percent testing positive. Groves et al.( 2001) reported no significant change in percentage of viruliferous F. fusca and F. occidentalis in the spring in North Carolina (possibly because of too little sample replication), but the highest percentage for both species from January to May occurred in April (14.7% and 11.6%, respectively) and ranged from 1.1 percent to 14.6 percent throughout this period. In conclusion, it appears that thrips species present, population density, time of infestation, and percent that are positive for TSWV (vectors capable of transmitting TSWV) all influence the cumulative infection rate of TSWV in flue-cured tobacco and other solanaceous crops. Most of these findings indicate the effect is related directly to plant age.
In recent studies, the effect of tomato, Lycopersicon esculentum (L.), plant and leaf age on the probing and settling behavior of Frankliniella fusca and F. occidentalis was studied using electrical penetration graph technique (EPG) and whole plant bioassays. Male and female F. fusca probed and ingested more and for longer periods of time on 3 and 4 week old plants compared to 6 and 8 week old plants. Female F. fusca probed and ingested more frequently than males in the plant age experiment but not in the leaf age experiment. Frankliniella fusca probed and ingested more frequently on 2 and 4 week old leaves compared to 1 week old leaves. Males did probe and ingest longer than females in the plant age experiment and on the oldest leaf in the leaf age experiment. Both thrips species preferred to settle on 3 week old plants. Frankliniella fusca preferred to settle on, 4 week old leaves after settling randomly for an hour. Thus, plant age does have an effect on F. fusca host selection and actual feeding with younger plants being preferred. We have observed in several studies that suppressing thrips early in the spring season on young plants 1-6 weeks in age with pre-plant, transplant and foliar insecticides or other tactics that reduce thrips present on young host crop plants can effectively reduce the incidence of TSWV.