Genetics of spinosad resistance in Frankliniella occidentalis (Thysanoptera: Thripidae)

The genetic basis of spinosad resistance was investigated in the western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). The resistant strain, selected in the laboratory for spinosad resistance from a pool of thrips populations collected in Almeria (southeastern Spain), showed a very high resistance to spinosad (356,547-fold based on LC50 values) compared with the laboratory susceptible strain. Mortality data from reciprocal crosses of resistant and susceptible thrips indicated that resistance was autosomal and not influenced by maternal effects. Analysis of probit lines from the parental strains and reciprocal crosses showed that resistance was expressed as an almost completely recessive trait. To determine the number of genes involved, a direct test of monogenic inheritance based on the backcrosses suggested that resistance to spinosad was probably controlled by one locus. Another approach, which was based on phenotypic variances, showed that nE, or the minimum number of freely segregating genetic factors for the resistant strain, equaled 0.59.     

Mechanisms associated with methiocarb resistance in Frankliniella occidentalis (Thysanoptera: Thripidae)

Biochemical mechanisms associated with methiocarb resistance were examined in laboratory-selected and field populations of the western flower thrips, Frankliniella occidentalis (Pergande). Seven populations were examined and they differed in their susceptibility to methiocarb by 30 times. Including the synergists piperonyl butoxide, a cytochrome P-450 monooxygenase inhibitor, or S,S,S-tributylphosphorotrithioate, an esterase inhibitor, in the methiocarb bioassays partially suppressed resistance in the most resistant populations. In vitro assays of general esterase, glutathione S-transferase, and acetylcholinesterase activities showed increased activity in some of the resistant populations and increased activity of the enzymes after methiocarb selection on one of the populations. Assays of acetylcholinesterase sensitivity to inhibition by methiocarb, dichlorvos, and eserine suggested insensitive acetylcholinesterase in two of the resistant populations. These results indicate that methiocarb resistance in F. occidentalis was polyfactorial and involved detoxification and altered target site. None of the biochemical assays showed interpopulation enzymatic differences strongly correlated with the level of methiocarb resistance. The possibilities for developing rapid biochemical diagnostic assays to detect methiocarb resistance in F. occidentalis are discussed.     

Chemical Control System of Frankliniella occidentalis (Thysanoptera: Thripidae) in Greenhouse Eggplant

Systems of chemical control were implemented in a plastic greenhouse to control mainly Frankliniella occidentalis (Pergande) in eggplant with several effective eligible groups of insecticides, spraying insecticide singly with new mode of action or in sequence with conventional. The system consisted of three phase of strategy to cope with initial population build up, sporadic pests and F. occidentalis population control. To check the effectiveness of the control system it was evaluated phytotoxicity, the residual toxicity, spraying frequency, insecticidal spectrum against Tetranychus urticae Koch, and Liriomyza trifolii (Burgess), and marketable quality and yield. Spraying singly with abamectin or imidacloprid gave high yields with low damage to the eggfruits. Furthermore abamectin 1.8 emulsifiable concentrate (Ec) showed wide range of insecticidal activity against T. urticae and L. trifolii with slightly less spraying frequency.     

Management of Frankliniella occidentalis (Thysanoptera: Thripidae) with granular formulations of entomopathogenic fungi

Western flower thrips (WFT), Franklinella occidentalis, is a major pest of ornamentals. Mycotized millet grains with entomopathogenic fungi applied to soil of potted marigold plants were tested to target the soil-dwelling stages of thrips. Two experimental fungal isolates, (Beauveria bassiana [ARS7060] and Metarhizium anisopliae [ERL1171]), were compared with the registered B. bassiana strain GHA [commercialized as BotaniGard®] and untreated controls in greenhouse caged trials. Mycotized millet grains were mixed into the upper surface of the potting soil in pots of flowering ‘Hero Yellow’ marigolds (4 g/pot). One week after application five mated WFT females were released onto each plant (four plants per cage). At 8 weeks post-infestation, the mean total number of thrips per plant was 81% and 90% less in the ERL1171 and ARS 7060 treatments, respectively, than in the control. The mean numbers of thrips per plant for the control and GHA treatments were not significantly different. Plant damage was 60% less on plants treated with the experimental fungi than the control and GHA treatments. At 10 weeks post-application, 75–90% of WFT collected from the treatments of the experimental fungi were infected with the fungal species applied. These results demonstrate that soil applications of entomopathogenic fungi can reduce WFT populations significantly and prevent major damage.     

The ultrastructure of Malpighian tubules and hindgut of Frankliniella occidentalis (Pergande) (Thysanoptera : Thripidae)

The ultrastructure of the western flower thrips, Frankliniella occidentalis (Pergande) (Order : Thysanoptera), has 4 Malpighian tubules that are free of the intestine as they leave their junction at the pyloric region. The tubules consist of an epithelium with a single type of microvillated cells; proximally, the cells are lined by a thin cuticle. Numerous mitochondria, basal infoldings of the plasma membrane and vesicles with varying densities suggest active transit of fluid in the cell for osmoregulation. Two of the Malpighian tubules are bent posteriorly and closely adhere to the hindgut in the region of the rectal pads where the 2 epithelia are separated only by a basal lamina. The ultrastructure of this region suggests possible fluid reabsorption from the gut lumen.     

Olfactory Cues Used in Host Selection by Frankliniella occidentalis (Thysanoptera: Thripidae) in Relation to Host Suitability

Olfactory responses of Frankliniella occidentalis (Pergande) to odors from six vegetable host plants-cabbage (Brassica oleracea), lettuce (Lactuca sativa), cucumber (Cucumis sativus), eggplant (Solanum melongena), celery (Apium graveolens) and garlic (Allium sativum) - were measured in choice tests in a Y-tube olfactometer, while host suitability of these same plants was assessed based on life table parameters-development time, survival rates, fertility, offspring sex ratio, female longevity, and an index of population change (I) - measured on leaf disks. Olfactory response was measured on both undamaged and mechanically-damaged plants. Regardless of plant damaged, female F. occidentalis responded positively to the odors of cabbage, lettuce, cucumber, and eggplant, but showed negative responses to celery and garlic, when offered a choice of plant odor or clean air. When female thrips were offered choices between each possible pairing of undamaged plants, or pairings of mechanically-damaged plants, the order of preference was cabbage = lettuce = cucumber > eggplant > celery = garlic. Male thrips responded differently, males responded positively only to undamaged lettuce and eggplant compared to clean air, while among mechanically-damaged plants only cucumber elicited a positive response. Given a choice between all possible pairings of undamaged plants, male thrips preferred lettuce to celery, and eggplant to garlic, whereas among pairings of mechanically-damaged plants male thrips preferred lettuce to celery, and cucumber to eggplant. The order of suitability of the six host plants based on life table parameters for F. occidentalis was essentially the same as the order of preference by female thrips. These results indicate that host plant odor is an important cue for female F. occidentalis in recognizing hosts suitable for oviposition. Information on plant attraction and repellency may be useful in thrips pest management. In addition, the correspondence of preference and performance that we found suggests that evolution of local host adaptation and, perhaps, host specialization, is possible.     

Imidacloprid effects on probing and settling behavior of Frankliniella fusca and Frankliniella occidentalis (Thysanoptera: Thripidae) in tomato

The effects of tomato, Lycopersicum spp., leaves treated with imidacloprid on probing and settling behavior of Frankliniella fusca (Hinds) and Frankliniella occidentalis (Pergrande) were examined using an electrical penetration graph technique and an intact leaf bioassay. For each experiment, thrips were subjected to nontreated plants and plants treated with either of two rates of imidacloprid: 7.81 and 41.55 microg [(AI)] per plant. F. fusca probed less frequently on plants treated with the high rate of imidacloprid compared with the nontreated plants. The duration of F. fusca noningestion probing waveforms and ingestion was shorter on plants treated with the high rate of imidacloprid compared with that on nontreated plants. In contrast, F. occidentalis probed longer and more frequently on plants treated with either the low or high imidacloprid rates compared with nontreated plants. They also ingested more frequently and for longer durations on plants treated with the high rate compared with nontreated plants. The duration and frequency of noningesting probing waveforms were greater on the imidacloprid-treated plants compared with the nontreated plants. F. occidentalis probed and ingested more frequently and for a longer duration than F. fusca on plants treated with the high rate of imidacloprid. F. fusca ingested more frequently and the duration of ingestion was longer than F. occidentalis in untreated plants. F. fusca and F. occidentalis settling behavior differed within the first 30 min in a choice bioassay. F. fusca preferred settling on leaves of nontreated plants, whereas F. occidentalis showed no preference in an intact leaf choice bioassay.     

Systemic effects of neem on western flower thrips,Frankliniella occidentalis (Thysanoptera: Thripidae)

The systemic effects of neem on the western flower thrips, Frankliniella occidentalis (Pergande), were investigated in laboratory trials using green bean, Phaseolus vulgaris L., in arena and microcosm experiments. In arena experiments, systemic effects of neem against western flower thrips larvae on primary bean leaves were observed with maximum corrected mortality of 50.6%. In microcosm experiments using bean seedlings, higher efficacy in the control of western flower thrips were observed with soil applications of neem on a substrate mixture (i.e., Fruhstorfer Erde, Type P, and sand) in a 1:1 ratio (93% corrected mortality) compared with application on the commercial substrate only (76% corrected mortality). However, longer persistence of neem was observed with soil application on the commercial substrate, which showed effects against thrips for up to 6 d after application. In addition to systemic effects observed on all foliage-feeding stages of western flower thrips, mortality on contact and repellent effects were observed on soil-inhabiting stages after soil applications of neem. Finally, bean seedlings grown from seeds pregerminated for 3 d in neem emulsion were also toxic to western flower thrips.     

Variation in preference and performance of Frankliniella occidentalis (Thysanoptera: Thripidae) on three strawberry cultivars

Western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), is a major pest of strawberry, causing substantial yield loss through direct feeding on the flowers and fruit. Insecticides are the main method used for its control; however, F. occidentalis has developed resistance to insecticides from all major chemical classes. Chemical control is not a long-term strategy and integrated pest management is required. This study determined whether F. occidentalis damage could be reduced by host plant resistance or tolerance in three commercial strawberry cultivars (Fragaria X ananassa [Rosaceae]: 'Albion', 'Camarosa', and 'Camino Real'). Determination of resistance or tolerance to F. occidentalis was based on olfactory response, feeding damage, ovipositional preference, and host suitability for reproduction on leaves. F. occidentalis adults preferred to feed on Camarosa; however, if leaves had been fed on previously by conspecifics, there was no difference in feeding preference. Camarosa was the most preferred cultivar for oviposition, and more eggs were laid by F. occidentalis on Camarosa than either Albion or Camino Real. More larvae hatched and adults were reared from Camarosa than either Albion or Camino Real. The percentage of unhatched eggs, larvae, and pupae that died was highest on Camino Real. Survival rate was highest on Camarosa. Egg incubation, prepupation, pupation, and total developmental periods were shortest on Camarosa, but the larval period was longest on Camarosa. Camarosa was the most favorable cultivar for F. occidentalis population growth on leaves.     

Impact of production system on development of insecticide resistance in Frankliniella occidentalis (Thysanoptera: Thripidae)

The western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), has become one of the most difficult insects to control in the intensive agriculture of southeastern Spain. However, resistance problems are quite different in two neighboring areas, Murcia and Almeria, with distinct production systems. Thirty-six field populations of western flower thrips from sweet pepper crops were collected in two different dates in Murcia and Almeria in 2005 and 2006. Western flower thrips populations collected were exposed to a diagnostic concentration of spinosad, methiocarb, acrinathrin, and formetanate. The results allowed the recognition of higher levels of resistance in Almeria compared with Murcia throughout the growing season. The mortality at the diagnostic concentration for spinosad (120 ppm) in western flower thrips populations ranged from 34 to 81% in Almeria, and from 73 to 100% in Murcia. The mortalities at the diagnostic concentration to acrinathrin (800 ppm) and formetanate (8000 ppm) were 17-31% in Almeria and 77-100% in Murcia, and 14-41% in Almeria and 48-99% in Murcia, respectively, indicating large geographic variations. Toxicity of methiocarb was higher for western flower thrips populations from both areas. However, mortality at the diagnostic concentration of methiocarb (2000 ppm) varied from 56 to 90% in Almeria, and it was from 94 to 100% in Murcia. The impact of production systems and agricultural practices of each area on the development and stability of insecticide resistance is discussed.     

西花蓟马取食对菜豆防御基因表达的诱导作用

为探讨菜豆对西花蓟马Frankliniella occidentalis取食的防御反应分子机制, 本实验利用荧光定量PCR（RT-qPCR）研究了西花蓟马取食、 机械损伤及外源水杨酸甲酯（MeSA）和茉莉酸（JA）处理对菜豆叶片防御相关基因（LOX, AOS, PAL及PR-2）相对表达量的影响。结果表明： 脂氧合酶基因（LOX）的相对表达量在外源JA和机械损伤诱导后分别在24 h和48 h时达到最大值, 但与对照相比差异不显著（P>0.05）, 外源MeSA处理后LOX几乎没有表达, 西花蓟马取食后LOX的相对表达量在24 h显著升高, 约为对照的41.9倍, 且明显高于其余3个处理（P<0.05）。不同诱导处理后丙二烯氧化物合成酶基因（AOS）的相对表达量较低, 其中外源MeSA处理后在整个诱导时间内几乎没有表达。苯丙氨酸解氨酶基因（PAL）在机械损伤和外源JA处理后在整个诱导时间内几乎没有表达, 外源MeSA处理后PAL的表达量在24 h时最高, 为对照的1.9倍左右。PAL的相对表达量在遭受蓟马取食诱导后迅速升高, 在24 h时约为CK的4.3倍, 显著高于其他3种处理诱导的（P<0.05）。β-1, 3-葡聚糖酶基因（PR-2）的相对表达量在蓟马取食和外源JA处理的整个诱导时间内受到抑制, 机械损伤诱导后PR-2的表达水平在24 h时有所升高, 之后诱导期间内受到抑制。外源MeSA诱导后菜豆叶片中PR-2的相对表达量在24 h就急剧升高, 达到对照的6.63倍, 且显著高于其余3种处理诱导的（P<0.05）, 但48 h后却几乎检测不到。研究结果提示, 西花蓟马取食不仅能够诱导SA和JA介导的信号传导途径, 且两通路间存在交互作用。     

Summer weeds as hosts for Frankliniella occidentalis and Frankliniella fusca (Thysanoptera: Thripidae) and as reservoirs for tomato spotted wilt Tospovirus in North Carolina

In North Carolina, Tomato spotted wilt tospovirus (family Bunyaviridae, genus Tospovirus, TSWV) is vectored primarily by the tobacco thrips, Frankliniella fusca (Hinds), and the western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). TSWV overwinters in winter annual weeds from which it is spread to susceptible crops in spring. Because most susceptible crops are destroyed after harvest before winter weeds emerge in the fall, infected summer weeds are thought to be the principal source for spread of TSWV to winter annual weeds in fall. A survey of summer weeds associated with TSWV-susceptible crops in the coastal plain of North Carolina conducted between May and October revealed that relatively few species were commonly infected with TSWV and supported populations of F. fusca or F. occidentalis. F. occidentalis made up > 75% of vector species collected from 15 summer weed species during 2002. The number of F. occidentalis and F. fusca immatures collected from plant samples varied significantly among plant species. Ipomoea purpurea (L.) Roth, Mollugo verticillata L., Cassia obtusifolia L., and Amaranthus palmeri S. Wats supported the largest numbers of immature F. occidentalis. Richardia scabra L., M. verticillata, and Ipomoea hederacea (L.) supported the largest numbers of F. fusca immatures. TSWV was present at 16 of 17 locations, and naturally occurring infections were found in 14 of 29 weed species tested. Five of the TSWV-infected species have not previously been reported as hosts of TSWV (A. palmeri, Solidago altissima L., Ipomoea lacunosa L., I. purpurea, and Phytolacca americana L.). Estimated rates of infection were highest in I. purpurea (6.8%), M. verticillata (5.3%), and I. hederacea (1.9%). When both the incidence of infection by TSWV and the populations of F. occidentalis and F. fusca associated with each weed species are considered, the following summer weed species have the potential to act as significant sources for spread of TSWV to winter annual weeds in fall: I. purpurea, I. hederacea, M. verticillata, A. palmeri, C. obtusifolia, R. scabra, Ambrosia artemisiifolia L., Polygonum pensylvanicum L., and Chenopodium album L.     

Mechanisms of resistance to spinosad in the western flower thrip, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae)

Cross‐resistance, resistance mechanisms, and mode of inheritance of spinosad resistance were studied in the western flower thrip, Frankliniella occidentalis (Pergande). Spinosad (naturalyte insecticide) showed low cross‐resistance to prothiophos (organophosphorus insecticide) and chlorphenapyr (respiratory inhibitor) showed some cross‐resistance to thiocyclam (nereistoxin). The synergists PBO (piperonyl butoxide), DEM (diethyl maleate), and DEF (s, s, s‐tributyl phosphorotrithioate) did not show any synergism on the toxicity of spinosad in the resistant strain (ICS), indicating that metabolic‐mediated detoxification was not responsible for the spinosad resistance, suggesting that spinosad may reduce sensitivity of the target site: the nicotinic acetylcholine receptor and GABA receptor. Following reciprocal crosses, dose‐response lines and dominance ratios indicated that spinosad resistance was incompletely dominant and there were no maternal effects. The results of backcross showed that spinosad resistance did not fit a single‐gene hypothesis, suggesting that resistance was influenced by several genes.     

Monitoring insecticide resistance in Australian Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) detects fipronil and spinosad resistance

Abstract  Insecticide resistance monitoring using a Potter precision spray tower with discriminating concentration and log dose probability techniques underpins the Australian insecticide management strategy for Frankliniella occidentalis Pergande. Abamectin, acephate, chlorpyrifos, dichlorvos, dimethoate, endosulfan, fipronil, malathion, methamidophos methidathion, methiocarb, methomyl, pyrazophos and spinosad are recommended for use against F. occidentalis but abamectin, methiocarb and pyrazophos are the only chemicals where insecticide resistance has not been detected. Although not registered, chlorfenapyr was effective against F. occidentalis and should be pursued for that purpose. In contrast, chlorpyrifos, dichlorvos and malathion resistance were detected at low to moderate levels throughout the study period putting their sustainable use for F. occidentalis control in doubt . Although it appears that acephate, dimethoate, endosulfan, fipronil, methamidophos, methidathion and spinosad remain effective, some populations contained a small percentage of thrips that survived exposure to a concentration that killed 100% of the susceptible strain. Subsequent laboratory selection of one such population separately with fipronil and spinosad caused an increase in resistance to these insecticides. These products must now be considered at risk. This is the first report of fipronil or spinosad resistance in populations of F. occidentalis.     

Host plant, temperature, and photoperiod effects on ovipositional preference of Frankliniella occidentalis and Frankliniella fusca (Thysanoptera: Thripidae)

Host plant effects of tomato, Lycopersicon esculentum Mill., and chickweed, Stellaria media (L.) Vill., foliage infected and uninfected with Tomato spotted wilt virus (family Bunyaviridae, genus Tospovirus, TSWV) on the ovipositional preferences of western flower thrips, Frankliniella occidentalis (Pergande), and tobacco thrips, Frankliniella fusca (Hinds), were investigated for whole plants in the greenhouse. In addition, the preference for leaf disks from the same host plants was investigated under a range of temperatures, 15-30 degrees C at a photoperiod of 12:12 (L:D) h, and at three photoperiods, 6:18, 12:12, and 18:6, at 20 degrees C in no-choice and choice studies conducted in growth chambers. In a choice test, F. fusca oviposited significantly more eggs per whole plant foliage over a 7-d period than F. occidentalis by an average ratio of 3:1 over both tomato and chickweed. The optimum temperature for oviposition of F. occidentalis and F. fusca was 24.5 and 24.9 degrees C, respectively. Both species laid significantly more eggs under the longest daylight hours tested, 18:6, in the choice study. Temperature and photoperiod did not significantly interact in terms of thrips ovipositional preference. Ovipositional preference for chickweed or tomato foliage was different for each thrips species in the choice and no-choice tests. However, both thrips species laid significantly more eggs per square centimeter of leaf area in chickweed than in tomato in the whole plant choice test.     

Insecticide resistance in Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) collected from horticulture and cotton in Turkey

Abstract  The sensitivity of three reference strains of the western flower thrips Frankliniella occidentalis from Australia, Israel and Turkey was evaluated and their response did not differ significantly and so they are considered typical of susceptible F. occidentalis . Field strains of F. occidentalis from Antalya, Turkey were tested for resistance against five classes of insecticide during the years 2001–2003. Difference in the field strains response to abamectin, endosulfan, malathion and methomyl was low (<3.0-fold) and in many cases not significant. However, all strains were likely resistant to cypermethrin (1.6- to 12.2-fold at LC₅₀ (lethal concentration)). The established agricultural practices and ecosystem patterns in the Antalya province are assumed to contribute to delay in insecticide resistance in F. occidentalis .     

Pyrethroid resistance in Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) and implications for its management in Australia

Abstract  The study was conducted to characterise the underlying resistance mechanisms responsible for high levels of pyrethroid resistance in Frankliniella occidentalis (Pergande) in Australia. Seven commercially available pyrethroids (acrinathrin, alpha-cypermethrin, bifenthrin, deltamethrin, esfenvalerate, permethrin and tau-fluvalinate) were evaluated against seven F. occidentalis strains collected from ornamentals, fruit and vegetables in three states of Australia. A Potter spray tower was used to test for pyrethroid resistance and all field strains were found to be resistant, with resistance ratios ranging from 15-fold deltamethrin to 1300-fold tau-fluvalinate. The two most resistant strains were further tested for detoxification enzymes that could be involved in resistance. Three synergists, piperonyl butoxide (PBO), diethyl maleate (DEM) and profenofos, which, respectively, inhibit the enzymes cytochrome P-450 monooxygenases, glutathione S -transferases and esterases, were used. The synergism data indicate that multiple mechanisms may be involved in pyrethroid resistance in Australian populations of F. occidentalis . Among the three synergists, PBO considerably reduced pyrethroid resistance in the selected strains compared with DEM and profenofos. The practical implication for PBO use to suppress pyrethroid resistance in F. occidentalis is elaborated.     

入侵昆虫西花蓟马的潜在适生区分析

本文在分析西花蓟马生物学特性及其世界分布的基础上,采用CLIMEX软件及提供的气候匹配性分析和位置比较分析两种分析模型,结合我国634个气象站点的数据,预测西花蓟马在我国的潜在分布区。结果表明,西花蓟马在生态气候指数EI≥3的地区爆发危害风险性较大。西花蓟马在我国的广东、海南、安徽、福建、江苏、山东、广西、贵州、河南、湖北、陕西、四川、云南、重庆等省市具有广泛的适生区; 其适宜生存的北界分布在中国年平均温度10℃等温线、1月份平均温度-8℃等温线以及年平均极端最低温度-20℃等温线附近; 而新疆、青海、西藏、黑龙江、吉林、辽宁、内蒙古等省或自治区为不适应生存区。     

Tomato plant and leaf age effects on the probing and settling behavior of Frankliniella fusca and Frankliniella occidentalis (Thysanoptera: Thripidae)

The effect of tomato, Solanum lycopersicum L., plant and leaf age on the probing and settling behavior of Frankliniella fusca (Hinds) and F. occidentalis (Pergande) was studied using electrical penetration graph technique and whole plant bioassays. Male and female F. fusca probed and ingested more and for longer periods of time on 3- and 4-wk-old plants compared with 6- and 8-wk-old plants. Female F. fusca probed and ingested more frequently than males in the plant age experiment, but not in the leaf age experiment. F. fusca probed and ingested more frequently on 2- and 4-wk-old leaves compared with 1-wk-old leaves. Plant age did not affect the probing frequency or duration of F. occidentalis; however, males probed and ingested 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-wk-old plants. F. fusca preferred to settle on 4-wk-old leaves after settling randomly for an hour. F. occidentalis showed no settling preference relative to leaf age. The preference of F. fusca for young plants suggests that this species could attack tomato plants at a very early stage, which is important for understanding its role as a vector in the transmission of Tospovirus in the field.