Direct and indirect effects of a thrips‐transmitted Tospovirus on the preference and fitness of its vector,Frankliniella fusca

Phytoviruses including tospoviruses are known to affect the behavior and fitness of their vectors both positively and negatively. In this study, we investigated the effects of Tomato spotted wilt virus (TSWV) (family Bunyaviridae, genus Tospovirus) infection on the fitness and feeding ability of tobacco thrips, Frankliniella fusca (Hinds) (Thysanoptera: Thripidae) using peanut, Arachis hypogaea L. (Fabaceae), as a host. Potentially viruliferous F. fusca laid more eggs than non‐viruliferous F. fusca. In contrast, fewer potentially viruliferous F. fusca developed into adults and required a longer developmental time than non‐viruliferous F. fusca, indicating a direct negative effect of the virus on thrips fitness. In addition, no‐choice feeding tests indicated that non‐viruliferous F. fusca fed more rapidly than potentially viruliferous F. fusca. Typically, phytovirus infections are known to enhance the availability of vital nutrients such as free amino acids in infected host plants and to affect other important physiological processes negatively. Free amino acids are known to play a vital role in egg production and development. Further investigations in this study revealed that leaflets of infected plants had ca. 15 times more free amino acids than non‐infected leaflets. TSWV‐infected leaflets were used to rear potentially viruliferous thrips. Higher amino acid levels in TSWV‐infected leaflets than in non‐infected leaflets could have contributed to increased oviposition by potentially viruliferous F. fusca compared to non‐viruliferous F. fusca. Taken together, these results suggest that increased concentrations of free amino acids in TSWV‐infected plants might serve as an incentive for thrips feeding on otherwise unsuitable hosts, thereby facilitating TSWV acquisition and transmission.     

Effects of tomato spotted wilt virus (TSWV) isolates, host plants, and temperature on survival, size, and development time of Frankliniella fusca

The effects of different isolates of the tomato spotted wilt tospovirus (TSWV), host plants, and temperatures on Frankliniella fusca (Hinds) (Thysanoptera: Thripidae), the most important vector of TSWV in North Carolina, were measured in the laboratory. Thrips were reared at either 18.3, 23.9, or 29.4 °C until adult eclosion on excised leaves of Datura stramonium L. or Emilia sonchifolia (L.). Plants were either infected with the TSWV isolates CFL or RG2, or left uninfected (control). The results revealed a positive relationship between larval survival and temperature, regardless of host plant or TSWV isolate. Both survival to adult and percentage transmission of TSWV by F. fusca were significantly affected by the interaction between host plant and TSWV isolate. The consequence of this interaction was that the cohort‐based percentage transmission from infected E. sonchifolia plants for CFL was 1.3‐fold greater than that of RG2, whereas the percentage transmission from infected D. stramonium plants for RG2 was twice that of CFL. Both host plant and TSWV isolates showed significant effects on thrips development time to adult and head capsule width of adult thrips, as well as on the incidence of thrips infection with TSWV. The infection status of these thrips was determined by ELISA for the NSs viral protein. Infected thrips reared on infected host foliage took longer to develop to adult and were smaller than non‐infected thrips which had also been reared on infected host foliage, demonstrating a direct effect of the TSWV on thrips. However, non‐infected thrips reared on non‐infected leaves took longer to develop than non‐infected thrips reared on infected leaves, suggesting an effect of the plant tissue on thrips. In addition, adult thrips reared on TSWV‐infected D. stramonium at 29.4 °C developed smaller head capsules than thrips developing on infected foliage at lower temperatures and on non‐infected leaves of D. stramonium or E. sonchifolia. Both TSWV isolates and host plants differentially affected females more than males. In conclusion, both the infection of thrips by TSWV and TSWV‐mediated changes in host plant quality were found to have significant biological effects on F. fusca.     

Does natural deposition of pine pollen affect the ovipositional behavior of Frankliniella occidentalis and Frankliniella fusca?

Tree pollen, especially Pinus spp. (Pinaceae), is shed in large quantities every spring in North America. Pine pollen deposition onto leaves was found to significantly influence the ovipositional behaviors of certain thrips species (Thysanoptera: Thripidae) in peanut and tomato leaf choice and no‐choice tests. Pine pollen (Pinus elliottii Engelm.) increased the oviposition rate 2.9‐fold for Frankliniella occidentalis (Pergande) (western flower thrips) and 1.6‐fold for Frankliniella fusca (Hinds) (tobacco thrips) in choice tests averaged over both plant species. These results support the idea that pollen has a greater impact on F. occidentalis behavior than on F. fusca behavior. The most dramatic increase was in peanut, where F. occidentalis only oviposited on leaves dusted with pollen, suggesting that the addition of pollen stimulated this flower thrips to lay eggs on a poor host‐plant part. The impact of pollen on the rate of oviposition by thrips is important because it is the early‐instar nymphs that acquire tomato spotted wilt virus (TSWV), which these two thrips species vector. In a laboratory bioassay, the addition of pine pollen to TSWV‐infected peanut foliage increased the percentage of infected F. fusca after one generation.     

Variation in thrips species composition in field crops and implications for tomato spotted wilt epidemiology in North Carolina

Thrips were surveyed in tomato spotted wilt-susceptible crops in five areas across North Carolina. Tomato, pepper, and tobacco plants in commercial fields were sampled and 30 species of thrips were collected over a 3-year period. The most common species overall was Frankliniella tritici (Fitch). The most common thrips species that are known to vector Tomato Spotted Wilt Virus (TSWV) were F. fusca (Hinds), and F. occidentalis (Pergande). Relatively low numbers of Thrips tabaci Lindeman, another reported vector, were collected. The spatial and temporal occurrence of vectors varied with sampling method, crop species, region of North Carolina, and localized areas within each region. In a laboratory experiment, no difference was detected between the ability of F. fusca and F. occidentalis to acquire and transmit a local isolate of TSWV. Based on vector efficiency and occurrence, F. fusca is considered the most important vector of TSWV in tobacco, whereas both F. fusca and F. occidentalis are important vectors of TSWV in tomato and pepper.     

Effects of tomato spotted wilt virus isolates, host plants, and temperature on survival, size, and development time of Frankliniella occidentalis

Tomato spotted wilt virus (TSWV) replicates in both its plant hosts and its thrips vectors. Replication of TSWV within thrips suggests the potential for pathological effects that could affect the fitness of its vectors directly, whereas infection of the plant may alter its suitability as a host for thrips development. This study was undertaken to examine the influence of TSWV isolate, host plant, and temperature on potential direct and host-mediated effects of virus infection of the thrips and the plant on Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), an important vector of TSWV. Neonate F. occidentalis were reared to adult eclosion on excised foliage of Datura stramonium (L.) (Solanaceae) or Emilia sonchifolia (L.) (Compositae) infected with either the CFL or RG2 isolate of TSWV, or not infected. Effects of the TSWV isolates and host plants on thrips were measured at 18.3, 23.9, and 29.4 °C. Results demonstrate significantly improved survival and a small but significant decrease in development time of F. occidentalis on TSWV-infected plants. These effects resulted from the combined influence of the direct effects of the virus on infected thrips and plant-mediated effects resulting from virus infection of the thrips’ host plant. Our results extend previous findings and help to explain inconsistencies among previously published reports by demonstrating that the manifestation and magnitude of effects of TSWV on F. occidentalis are dependent on host plant, virus isolate, and temperature.     

Obstructor,a Frankliniella occidentalis protein,promotes transmission of tomato spotted wilt orthotospovirus

Tomato spotted wilt orthotospovirus (TSWV) causes substantial economic losses to vegetables and other crops. TSWV is mainly transmitted by thrips in a persistent and proliferative manner, and its most efficient vector is the western flower thrips, Frankliniella occidentalis (Pergande). In moving from the thrips midgut to the salivary glands in preparation for transmission, the virions must overcome multiple barriers. Although several proteins that interact with TSWV in thrips have been characterized, we hypothesized that additional thrips proteins interact with TSWV and facilitate its transmission. In the current study, 67 F. occidentalis proteins that interact with G_N (a structural glycoprotein) were identified using a split-ubiquitin membrane-based yeast 2-hybrid (MbY2H) system. Three proteins, apolipoprotein-D (ApoD), orai-2-like (Orai), and obstructor-E-like isoform X2 (Obst), were selected for further study based on their high abundance and interaction strength; their interactions with G_N were confirmed by MbY2H, yeast β-galactosidase and luciferase complementation assays. The relative expressions of ApoD and Orai were significantly down-regulated but that of Obst was significantly up-regulated in viruliferous thrips. When interfering with Obst in larval stage, the TSWV acquisition rate in 3 independent experiments was significantly decreased by 26%, 40%, and 35%, respectively. In addition, when Obst was silenced in adults, the virus titer was significantly decreased, and the TSWV transmission rate decreased from 66.7% to 31.9% using the leaf disk method and from 86.67% to 43.33% using the living plant method. However, the TSWV acquisition and transmission rates were not affected by interference with the ApoD or Orai gene. The results indicate that Obst may play an important role in TSWV acquisition and transmission in Frankliniella occidentalis.     

Vector and virus induce plant responses that benefit a non-vector herbivore

The negative cross-talk between induced plant defences against pathogens and arthropod herbivores is exploited by vectors of plant pathogens: a plant challenged by pathogens reduces investment in defences that would otherwise be elicited by herbivores. This negative cross-talk may also be exploited by non-vector herbivores which elicit similar anti-herbivore defences in the plant. We studied how damage by the thrips Frankliniella occidentalis and/or infection with Tomato spotted wilt virus (TSWV) affect the performance of a non-vector arthropod: the two-spotted spider mite Tetranychus urticae, a parenchym feeder just like F. occidentalis. Juvenile survival of spider mites on plants inoculated with TSWV by thrips was higher than on control and on thrips-damaged plants. However, thrips damage did not reduce spider-mite survival as compared to the control, suggesting that the positive effect of TSWV on spider-mite survival is independent of anti-thrips defence. Developmental and oviposition rates were enhanced on plants inoculated with TSWV by thrips and on plants with thrips damage. Therefore, spider mites benefit from TSWV-infection of pepper plants, but also from the response of plants to thrips damage. We suggest that the positive effects of TSWV on this non-vector species cannot be explained exclusively by cross-talk between anti-herbivore and anti-pathogen plant defences.     

Temporal and spatial dynamics of Tomato spotted wilt virus and its vector in a potato crop in Argentina

The nature of spatial and temporal dynamics of Tomato spotted wilt virus (TSWV) and its vector in a potato crop cv. Innovator without insecticide application is analysed. Seed tuber was analysed for the presence of TSWV as a source of initial inoculum. The presence of plants with symptoms of TSWV was evaluated by visual observation and DAS‐ELISA analysis to confirm the virus infection. Thrips species were collected from leaves and inflorescences and identified under stereomicroscope. The distribution of symptomatic plants and thrips species was recorded five times at 14 days intervals. The initial seed tuber infection was of 1.1%. Disease incidence was 0% at 29 days after planting (DAP), 0.2% at 43 DAP, 2.2% at 56 DAP, 11.6% at 70 DAP and 14.6% at 84 DAP. The progress of the disease was adequately described by a Logistic model [y = 0.15/(1 + 1205372.93 × exp (?0.22 × DAP))]. Thrips vector species identified as resident in the crop during the whole cycle were Thrips tabaci (n = 423), Frankliniella occidentalis (n = 141) and as occasional species, F. schultzei (n = 34) and F. gemina (n = 5) were found. At 43 and 56 DAP a random distribution pattern was observed and the thrips species found were T. tabaci (n = 188) and F. occidentalis (n = 105). An aggregated pattern was determined at 70 and 84 DAP. Spatial patterns of the disease spread suggest a polycyclic epidemic with TSWV secondary spread in the potato crop. Multiple control measures were deduced from these epidemiological results like virus testing in tubers, removal of external virus infection sources and thrips control.     

Pine pollen dehiscence relative to thrips population dynamics

A two‐part study related tree pollen dehiscence and thrips population dynamics in the field, and directly evaluated effects of pine pollen deposition on Frankliniella spp. (Thysanoptera: Thripidae) reproduction on tobacco, Nicotiana tabacum L. (Solanaceae), under laboratory conditions. Ambient pollen and thrips were monitored in Tift County, GA, USA, from early spring to late summer/early fall from 2005 to 2008. Correlation analyses were conducted using weekly means of thrips collected on sticky traps compared to weekly pollen counts from a Burkard air sampler and pollen deposition sheets. There were significant positive correlations between pollen and thrips counts on later dates, suggesting that if a relationship exists between pine pollen dehiscence and thrips population dynamics, it will be delayed. Over all years combined, the first spring time peak in Frankliniella fusca (Hinds) counts on sticky traps occurred at 227 accumulated degree days (dd) after the first peak in pine pollen, approximately the dd required to complete a single F. fusca generation. Two subsequent thrips peaks occurred at approximately one and two F. fusca generations following the first peak. After 10 weeks following the final peak in pollen, there appears to be no more effect of pollen on thrips population dynamics. A tobacco leaf, lightly dusted with Slash pine [Pinus elliottii Engelmann (Pinaceae)] pollen to mimic natural deposition, showed a significant increase in the number of offspring produced per Frankliniella occidentalis (Pergande) and F. fusca female. The total offspring produced increased five‐fold in F. fusca and 22‐fold in F. occidentalis in 15 days on the pollen‐treated leaves over the untreated leaves.     

Weed species in tomato production and their role as alternate hosts of Tomato spotted wilt virus and its vector Frankliniella occidentalis

Tomato spotted wilt virus (TSWV) is an important plant virus that infects a wide range of hosts including weeds making its management difficult. A survey was undertaken to establish the occurrence of weed species in tomato production systems in Kenya and their role as hosts of TSWV and its vectors. Selected weed species were further evaluated for their reaction to TSWV, transmission efficiency by Frankliniella occidentalis and ability to support thrips reproduction. Of the 43 weed species identified in the field, 29 species had been reported as hosts of TSWV, two were non‐hosts and 11 had no record of their status. Among the more common species, Amaranthus hybridus, Solanum nigrum, Tagetes minuta and Datura stramonium were susceptible to the virus and supported high levels of thrips reproduction. The TSWV could not be transmitted to Galinsoga parviflora and Sonchus oleraceus by F. occidentalis despite them being highly susceptible in mechanical transmission tests. There was a significant correlation between feeding damage and number of larvae of F. occidentalis on different weeds. Occurrence of weeds that support thrips reproduction and are good hosts of TSWV is a clear indicator of their role in epidemiology and the importance of their management for disease control.     

Midgut infection by tomato spotted wilt virus and vector incompetence of Frankliniella tritici

Abstract:  The mechanism leading to vector competence of thrips species to transmit tomato spotted wilt virus (TSWV) is not well characterized. We investigated the interaction of TSWV and the non-vector species Frankliniella tritici . A monoclonal antibody to the non-structural protein (NSs) of the TSWV was used to detect TSWV replication within the thrips by immunofluorescence microscopy and enzyme-linked immonosorbent assay (ELISA). TSWV was acquired by F. tritici , replicated and moved within the alimentary canal of F. tritici similar to a known vector of TSWV, Frankliniella occidentalis . However, virus was not found in the salivary glands of F. tritici , which is a prerequisite to virus transmission. Thus, movement to the salivary glands may determine vector incompetence of F. tritici .     

Specific Insect-Virus Interactions Are Responsible for Variation in Competency of Different Thrips tabaci Isolines to Transmit Different Tomato Spotted Wilt Virus Isolates

Local adaptation between sympatric host and parasite populations driven by vector genetics appears to be a factor that influences dynamics of disease epidemics and evolution of insect-vectored viruses. Although T. tabaci is the primary vector of Tomato spotted wilt virus (TSWV) in some areas of the world, it is not an important vector of this economically important plant virus in many areas where it occurs. Previous studies suggest that genetic variation of thrips populations, virus isolates, or both are important factors underlying the localized importance of this species as a vector of TSWV. This study was undertaken to quantify variation in transmissibility of TSWV isolates by T. tabaci, in the ability of T. tabaci to transmit isolates of TSWV, and to examine the possibility that genetic interactions and local adaptation contribute to the localized nature of this species as a vector of TSWV. Isofemale lines of Thrips tabaci from multiple locations were tested for their ability to transmit multiple TSWV isolates collected at the same and different locations as the thrips. Results revealed that the probability of an isofemale line transmitting TSWV varied among virus isolates, and the probability of an isolate being transmitted varied among isofemale lines. These results indicate that the interaction of T. tabaci and TSWV isolate genetic determinants underlie successful transmission of TSWV by T. tabaci. Further analysis revealed sympatric vector-virus pairing resulted in higher transmission than allopatric pairing, which suggests that local adaptation is occurring between T. tabaci and TSWV isolates.     

Preference of the vector thrips Frankliniella occidentalis for plants infected with thrips‐non‐transmissible Tomato spotted wilt virus

The effect of a thrips‐non‐transmissible Tomato spotted wilt virus (TSWV) on insect–host interactions between thrips and Arabidopsis thaliana was analysed. A wild‐type TSWV virulent isolate and a TSWV isolate that induces mild symptoms on inoculated plants (TSWV‐Mo) were used in this study, and TSWV‐Mo isolate was obtained by single local lesion isolation using Petunia x hybrid after several passages on Nicotiana rustica plants. In transmission test, although wild‐type TSWV (TSWV‐wt) was transmitted by two thrips species (transmission ratio; Frankliniella occidentalis, 25%; Thrips tabaci, 10%; and T. palmi, 0%), none of the thrips transmitted TSWV‐Mo. Feeding damage by F. occidentalis in A. thaliana plants was more extensive on TSWV‐wt‐infected plants than on TSWV‐Mo‐infected plants, despite comparable preference. Among the markers of plant defences, salicylic acid‐regulated genes were upregulated threefold to sixfold by TSWV‐wt or TSWV‐Mo infection. In contrast, jasmonate‐regulated genes and jasmonate/ethylene‐regulated genes were not affected by the infections. Pull assays showed that adjacent TSWV‐Mo‐infected plants were preferred over uninfected plants. In conclusion, our results showed that the transmissibility by thrips of TSWV is not related to preference of vector thrips and suggested that TSWV‐Mo‐infected plants may be used as attractants for behaviour control of thrips.     

A new record of the tobacco thrips <Emphasis Type="Italic">Frankliniella fusca</Emphasis> (Hinds) (Thysanoptera: Thripidae) from Japan

The tobacco thrips, Frankliniella fusca, which is known as a vector of TSWV and Pantoea ananatis causing center rot of onion, and a serious pest of tobacco, cotton and groundnuts in North America, is newly recorded from the bulbs of Narcissus pseudonarcissus in Honshu, mainland Japan. Two strains were found in Shimane Prefecture. One strain was collected from a bulb produced in Niigata Prefecture in the winter of 2002, and the other was collected from bulbs produced in Fukushima Prefecture in the autumn of 2002. F. fusca can be easily distinguished from other members of this genus in Japan.     

Fine structure and distribution of three types of virus-like particles in the sheep blowfly,Lucilia cuprina and associated cytopathic effects

The ultrastructure is described for three types of virus-like particles (VLP 1–3) found in thin sections of the sheep blowfly Lucilia cuprina and, in the case of one type (VLP 1), in negatively stained preparations. VLP 1 appears to be morphologically similar to the particles of chronic bee paralysis virus and RS virus of Drosophila and causes a highly characteristic vesiculation of mitochondria. VLP 2 has two forms, spherical and filamentous; these are seen mainly in the gut where the filaments proliferate in the apical parts of the cells and resemble reovirus-like particles found in the gut of Musca domestica. The third type of particle (VLP 3) is intranuclear and seen only rarely. It is arrayed in quasi-crystalline inclusions which resemble inclusions reported in cells and tissues of Drosophila.     

Relationships between Tospovirus Incidence and Thrips Populations on Tomato in Mendoza, Argentina

The objectives of this work were to estimate the capability of local populations of thrips as vectors of groundnut ringspot virus (GRSV) and tomato spotted wilt virus (TSWV), and to determine the species composition of vectors in tomato crops. Transmission assays were performed. Incidence of tospoviruses was estimated in commercial crops. Random samples of flowers were taken from tomato for identification of thrips. Of the five species of thrips tested, Frankliniella gemina (first record), F. occidentalis and F. schultzei transmitted GRSV and TSWV. F. schultzei was a significantly more efficient vector of GRSV than F. occidentalis under controlled assay conditions. The thrips were identified on flowers from six surveyed tomato crops. F. occidentalis was the most frequently identified species (43.0%), followed by F. schultzei (35.6%) and Thrips tabaci (10.1%). The incidence of tospoviruses was low (1.1–2.8%) in crops planted during August–September and greater (9.5–61.1%) in crops planted in December. GRSV was prevalent (85%) over TSWV (11%).     

Patterns of spread of Tomato spotted wilt virus in field crops of lettuce and pepper: spatial dynamics and validation of control measures

Patterns of spread of Tomato spotted wilt virus (TSWV) were examined in lettuce and pepper plantings into which thrips vectors spread the virus from external virus sources. These plantings were: 1) seven separate field trials into which TSWV ‘infector’ plants of tomato were introduced alongside or near to plantings of lettuce or pepper, and 2) three commercial lettuce plantings into which spread from nearby external infection sources was occurring naturally. The vector thrips species were Frankliniella occidentalis, F. schnitzel and Thrips tabaci, at least two of which were always present. Spatial data for plants with TSWV infection collected at different stages in the growing period were assessed by plotting gradients of infection, and using Spatial Analysis by Distance IndicEs (SADIE) and maps of spatial pattern. Despite the persistent nature of TSWV transmission by thrips vectors, in both lettuce and pepper plantings there was a steep decline in TSWV incidence with distance from external infection sources that were alongside them. The extent of clustering increased over time and was greatest closest to the source. The relationship between percentage infection and assessment date suggested that spread was predominantly monocyclic with only limited polycyclic spread. Development of isolated clusters of infected plants distant from TSWV sources within both crops was consistent with only limited polycyclic spread. Spread to lettuce was greater downwind than upwind of virus source, with magnitude and proximity of source determining the amount of spread. When 15 m wide fallow or non-host (cabbage) barriers separated TSWV sources from lettuce plantings, spread was slower and there was much less clustering with the latter. In commercial lettuce plantings, spread was favoured by TSWV movement within successive side-by-side plantings. The spatial data from the diverse scenarios examined enabled recommendations to be made over ‘safe’ planting distances between external infection sources of different magnitudes and susceptible crops that were short-lived (e.g. lettuce) or long-lived (e.g. pepper). They also helped validate the inclusion of isolation and ‘safe’ planting distances, planting upwind, prompt removal of virus sources, avoidance of side-by-side plantings, and deploying intervening non-host barrier crops as control measures within an integrated disease management strategy for TSWV in field vegetable crops.     

Seasonal dispersal patterns of Frankliniella fusca (Thysanoptera: Thripidae) and tomato spotted wilt virus occurrence in central and eastern North Carolina

The seasonal abundance and temporal pattern of Frankliniella fusca Hinds dispersal were monitored from 1996 to 2000 at 12 locations in central and eastern North Carolina. The predominant vector species of tomato spotted wilt virus (TSWV) captured across all locations was F. fusca (98%). The temporal patterns of F. fusca dispersal observed during spring seasons varied among locations in all years except 2000. Regression analysis estimated that times of first flight in the spring seasons varied among locations, whereas flight duration intervals were similar. Temporal patterns of F. fusca captured varied significantly between aerial traps placed 0.1 and 1.0 m above the soil surface. Fewer total thrips were captured at 0.1 m, although thrips dispersal occurred earlier and over a greater time interval compared with 1.0-m traps. Temporal patterns of TSWV occurrence differed among locations in the spring seasons of 1999 and 2000, whereas patterns of virus occurrence were similar during the fall seasons. Patterns of F. filsca dispersal and subsequent TSWV occurrence were synchronous at locations in 1999 and 2000 where the greatest number of TSWV lesions was recorded. Knowledge of the temporal patterns of F. fiasca dispersal and TSWV occurrence may be a useful indicator for describing the time when susceptible crops are at highest risk of TSWV infection.