Oviposition preference of western flower thrips for cucumber leaves from different positions along the plant stem

While the distribution of herbivorous insects over leaves along the stem often shows a peak at some distance from the apex this does not necessarily reflect an innate preference as alternative explanations can be provided such as impact of predators and inter- or intraspecific competitors. It is of interest to determine which factors shape the distribution of insects over the leaves of a plant. Do leaves from different positions differ in suitability for insects and is that reflected in the insect's preference, or are other factors involved? In this paper we assess how the herbivorous insect western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), chooses among leaves from different positions relative to the apex of cucumber, Cucumis sativus (L.) plants. On leaf discs of a susceptible and three partially resistant cucumber accessions, thrips reproduction was highest on apical leaves and lowest on basal leaves. In dual-choice essays thrips females preferred younger leaves over older leaves for oviposition in all cucumber accessions tested, as was predicted from the no-choice assay. This indicates that differences in leaf suitability are an important factor in determining thrips distribution on cucumber plants.     

Engineered multidomain cysteine protease inhibitors yield resistance against western flower thrips (Frankliniella occidentalis) in greenhouse trials

Western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), cause very large economic damage on a variety of field and greenhouse crops. In this study, plant resistance against thrips was introduced into transgenic potato plants through the expression of novel, custom-made, multidomain protease inhibitors. Representative classes of inhibitors of cysteine and aspartic proteases [kininogen domain 3 (K), stefin A (A), cystatin C (C), potato cystatin (P) and equistatin (EIM)] were fused into reading frames consisting of four (K-A-C-P) to five (EIM-K-A-C-P) proteins, and were shown to fold into functional inhibitors in the yeast Pichia pastoris. The multidomain proteins were expressed in potato and found to be more resistant to degradation by plant proteases than the individual domains. In a time span of 14-16 days, transgenic potato plants expressing EIMKACP and KACP at a similar concentration reduced the number of larvae and adults to less than 20% of the control. Leaf damage on protected plants was minimal. Engineered multidomain cysteine protease inhibitors thus provide a novel way of controlling western flower thrips in greenhouse and field crops, and open up possibilities for novel insect resistance applications in transgenic crops.     

Optimization of dietary RNA interference delivery to western flower thrips Frankliniella occidentalis and onion thrips Thrips tabaci

In insect reverse genetics, dietary delivery of interfering RNAs is a practical approach in nonmodel species, such as thrips, whose small size, and feeding behavior restricts the use of other delivery methods. In a laboratory context, an unsuitable diet could confound the interpretation of an RNA interference (RNAi) phenotype, however well-formulated artificial diets can minimize experimental variability, reduce the need for insect handling, and can further be used for roles, such as delivering double-strand RNA (dsRNA)-expressing recombinant bacteria. In this study, artificial diets for oral delivery of dsRNA were developed for two important pest thrips species, western flower thrips (Frankliniella occidentalis) and onion thrips (Thrips tabaci), with the goal of (a) stimulating feeding behavior, (b) supporting optimal growth rates of dsRNA-expressing symbiotic bacteria, and (c) nutritionally supporting the thrips for sufficient periods to observe RNAi phenotypes. The efficacy of artificial diets for ingesting “naked” dsRNA or dsRNA-expressing symbionts and dsRNA delivery via host plant uptake was evaluated. Compared with previously published diet formulations, new combinations based on tryptone, yeast, and soy were superior for enhancing feeding and longevity. However, simply adding “naked” dsRNA to an artificial diet was an unreliable form of RNAi delivery in our hands due to dsRNA degradation. Delivery via host plants was more successful, and the new diet formulation was suitable for symbiont-mediated dsRNA delivery, which we believe is the most convenient approach for large-scale knockdown experiments. This study, therefore, provides alternative methodologies for thrips rearing, dietary RNAi delivery, and insights into the challenges of performing dietary RNAi in nonmodel insects.     

Intraspecific larval competition in two solitary parasitoids, Apoanagyrus (Epidinocarsis) lopezi and Leptomastix dactylopii

Analysis of total aromatic amino acid (free and bound) in some cucumber accessions selected previously for resistance to western flower thrips, Frankliniella occidentalis (Pergande) [Thysanoptera: Thripidae], indicated that low concentrations of these essential nutrients, relative to total leaf protein, were correlated with a reduction in damage by the insect. Further analysis of samples of four important horticultural crops (lettuce, tomato, pepper and cucumber) with unknown levels of resistance to thrips showed a significant genotypic variation in the concentrations of total aromatic amino acids relative to the total leaf protein. Accessions from each crop with low or high concentrations of aromatic amino acids in proteins were exposed to thrips larvae. Regression analysis showed a highly significant positive correlation between aromatic amino acid concentration in leaf protein and thrips damage, regardless of crop species. It is concluded that higher concentrations of aromatic amino acids in plant proteins are important for successful thrips development. These results provide plant breeders with a promising tool for indirect selection without using undesirable insect bioassays.     

Influence of salicylaldehyde and methyl salicylate on post-landing behaviour of Frankliniella occidentalis Pergande

This study investigates behavioural responses of adult western flower thrips (Frankliniella occidentalis Pergande; Thysan., Thripidae) females to direct contact with repellent phenylpropanoid plant compounds (salicylaldehyde and methyl salicylate) applied on bean and cucumber leaves. The residence time of F. occidentalis females until take off was significantly shorter on bean or cucumber leaf discs treated with salicylaldehyde at 1% concentration compared with control leaf discs. A methyl salicylate (1%) treatment of cucumber resulted in shorter time periods until thrips took off the treated leaf discs compared with the control leaf discs. In a choice experiment thrips avoided to settle on a 1% salicylaldehyde treatment of bean and cucumber leaf discs for a maximum of 3 h, on a 1% methyl salicylate treatment for a 5‐h period. Within a 24‐h period neither the egg‐laying nor the feeding activity of F. occidentalis was affected after salicylaldehyde application (0.1%, 1%) on bean or cucumber. In contrast, methyl salicylate (1%) applied on bean and cucumber significantly prevented thrips females from oviposition and reduced the percentage of damaged area caused by their feeding activity for 24 h. As olfactory repellent plant volatiles applied on crop plants may elicit diverse post‐landing responses of F. occidentalis, short‐ and long‐term effects should be considered when evaluating the factual applicability of secondary plant compounds in a successful thrips management strategy.     

Specific cysteine protease inhibitors act as deterrents of western flower thrips, Frankliniella occidentalis (Pergande), in transgenic potato

In this study, the effects of the accumulation of cysteine protease inhibitors on the food preferences of adult female western flower thrips, Frankliniella occidentalis (Pergande), were investigated. Representative members of the cystatin and thyropin gene families (stefin A, cystatin C, kininogen domain 3 and equistatin) were expressed in potato (Solanum tuberosum) cv. Impala, Kondor and Line V plants. In choice assays, a strong time- and concentration-dependent deterrence from plants expressing stefin A and equistatin was observed. Cystatin C and kininogen domain 3 were not found to be active. All tested inhibitors were equally or more active than stefin A at inhibiting the proteolytic activity of thrips, but, in contrast with stefin A, they were all expressed in potato as partially degraded proteins. The resistance of cysteine protease inhibitors against degradation in planta by endogenous plant proteases may therefore be relevant in explaining the observed differences in the deterrence of thrips. The results demonstrate that, when given a choice, western flower thrips will select plants with low levels of certain cysteine protease inhibitors. The novel implications of the defensive role of plant cysteine protease inhibitors as both deterrents and antimetabolic proteins are discussed.     

Abundances of thrips on plants in vegetative and flowering stages are related to plant volatiles

Western flower thrips (WFTs), Frankliniella occidentalis Pergrande, and onion thrips (OTs), Thrips tabaci Lindeman, are two cosmopolitan insect pests of agricultural and horticultural plants. Understanding the occurrence and development of thrips on plants is crucial for identifying suitable plants that can be used for developing a “push-pull” strategy against thrips. In this study, the dynamics of WFTs and OTs on plants (Allium fistulosum L., Medicago sativa L., Luffa cylindrica (L.) Roem., Ocimum basilicum L., and Schizonepeta tenuifolia (Benth.) Briq.) were investigated for two consecutive years (2018–2019). Throughout the survey, the abundances of both thrips species were strongly associated with plant species and plant phenology; both thrips species were present at relatively high densities on M. sativa but very low densities on O. basilicum and S. tenuifolia. Populations of both thrips species greatly increased during plant flowering. A Y-tube olfactory test was used to study the effects of plant volatiles in mediating thrips behaviour and showed that volatiles of M. sativa were attractive to both thrips species whether emitted by the plant in the vegetative or flowering stage, while volatiles of O. basilicum and S. tenuifolia were repellent to thrips. Additionally, because of the presence of a high number of floral chemicals, both thrips species exhibited a greater preference for volatiles emitted by plants in the flowering period over those emitted by plants in the vegetative period. Our observations indicate that plant species and flowering status play an important role in the abundance dynamics of thrips and that the volatiles of flowering plants attract thrips more strongly than volatiles emitted by vegetative plants. These findings can facilitate the screening of attractive/unattractive plants for developing push-pull strategies to control thrips.     

Variation in performance of western flower thrips populations on susceptible and partially resistant cucumber

Biotypic variation is of major concern in breeding for host plant resistance to insects. The existence or development of aggressive biotypes can lead to a rapid break-down of host plant resistance. Therefore the study of biotypic variation should be included in breeding programs for resistance to insects. In the present study we measured the reproduction of randomly collected females of ten different populations of the insect herbivore Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) on one susceptible and two resistant cucumber (Cucumis sativus L.) accessions. Significant differences between thrips populations were observed on all three cucumber accessions. None of the populations had a significantly higher reproduction than the Dutch reference population NL1. For three populations, the Dutch population NL1, a population from New Zealand (NZ), and an Italian population (IT), partial life history parameters, such as reproduction rate, developmental time and survival were determined and the relative rate of increase r _r was calculated. On all three cucumber accessions the r _r-value of population NZ was lower than of populations NL1 and IT. It is concluded that there is biotypic variation in F. occidentalis with regard to performance on cucumber plants with different levels of resistance. Reproduction is a good criterion for differentiating biotypes of F. occidentalis on cucumber.     

Management of thrips (Thysanoptera: Thripidae) in Australian strawberry crops: within-plant distribution characteristics and action thresholds

Abstract  Management of thrips in a hydroponic strawberry crop near Sydney, New South Wales, was studied from 1999 to 2002. The main species present were western flower thrips, Frankliniella occidentalis (Pergande), plague thrips, Thrips imaginis Bagnall, and, occasionally, onion thrips, Thrips tabaci Lindeman. Their within- and between-plant distribution and the degree and type of damage caused are described, and used to recommend action thresholds. Flowers are identified as the primary monitoring site, and young green fruit as the key damage site. Action thresholds of approximately 45% of flowers with 5 or more adult western flower thrips, or 40% of flowers with 10 or more adult plague thrips are recommended. Alternative thresholds using all motile stages are given for flowers, and for young green and red berries. A higher tolerance is recommended during cool, wet periods.     

西花蓟马在6种蔬菜寄主上的实验种群生命表

自西花蓟马Frankliniella occidentalis传入我国后,该虫对蔬菜寄主的危害趋于严重,组建了25℃条件下,西花蓟马在黄瓜、甘蓝、莴苣、茄子、芹菜和大蒜叶片的实验种群生命表,以研究西花蓟马的危害差异性,为西花蓟马的防治提供基础数据。结果表明西花蓟马的生长发育、繁殖和生命表参数等在不同寄主之间有明显差异。西花蓟马在黄瓜上发育最快,其未成熟期为11.43 d,同时在黄瓜上最先开始产卵,产卵前期为1.22 d,在芹菜上发育最慢,为16.11 d。其每雌每天在甘蓝上和莴苣上产卵量最大,分别为2.88粒和2.48粒,在大蒜上最小,为0.77粒;每雌每天产雌率、子代雌性比在甘蓝和莴苣上都大于其他寄主。雌虫寿命在甘蓝上最长(29.06 d)、雄虫寿命在莴苣上最长(13.22 d)。西花蓟马在黄瓜、莴苣、茄子、甘蓝、芹菜和大蒜上的内禀增长力rm值分别为0.1318、0.1228、0.1154、0.1197、0.0860和0.0791;净增殖率R0分别为19.1248、30.8523、17.9322、34.5322、8.9491和8.3536。种群趋势预测指数(I)在甘蓝(34.17)、莴苣(30.09)上明显高于其它寄主,在芹菜(8.00)和大蒜(8.22)上最低。     

Beetle pollination of Shorea parvifolia (section Mutica, Dipterocarpaceae) in a general flowering period in Sarawak, Malaysia

Pollination ecology of an emergent tree species, Shorea (section Mutica) parvifolia (Dipterocarpaceae), was studied using the canopy observation system in a lowland dipterocarp forest in Sarawak, Malaysia, during a general flowering period in 1996. Although the species has been reported to be pollinated by thrips in Peninsular Malaysia, our observations of flower visitors and pollination experiments indicated that beetles (Chrysomelidae and Curculionidae, Coleoptera) contributed to pollination of S. parvifolia in Sarawak. Beetles accounted for 74% of the flower visitors collected by net-sweeping, and 30% of the beetles carried pollen, while thrips accounted for 16% of the visitors, and 12% of the thrips carried pollen. The apical parts of the petals and pollen served as a reward for the beetles. Thrips stayed inside the flower almost continuously after arrival, and movements among flowers were rare. Fruit set was significantly increased by introduction of beetles to bagged flowers, but not by introduction of thrips. Hand-pollination experiments and comparison of fruit set in untreated, bagged, and open flowers suggested that S. parvifolia was mainly outbreeding.     

Initial verification of the resistance management strategy for Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) in Australia

Shortly after the initial detection of western flower thrips (WFT), Frankiniella occidentalis (Pergande), in Australia during 1993 a resistance management strategy based on the alternation of chemical groups was implemented. This study aimed to verify this strategy by field testing α-cypermethrin against WFT with and without chemical alternation. Up to 114 times α-cypermethrin resistance (at LC50) was detected and resistance increased with and without chemical alternation; however, chemical alternation did significantly reduce numbers of thrips compared with a nonalternation strategy. Resistance has the potential to undermine the sustainable use of those chemicals to which there is no current detectable resistance. Consequently, chemicals with a high frequency and level of resistance against WFT need to be identified through monitoring and quickly eliminated from WFT chemical control recommendations.     

Management of western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), in hydroponic strawberry crops: using yellow sticky traps to determine action thresholds

Abstract  The relationship between western flower thrips (WFT) populations in flowers and catches on yellow sticky traps was investigated in a hydroponic strawberry crop in the Sydney area in 1999–2000. The thrips population was initially dominated by males, but by mid-summer it was composed primarily of females. At a point when approximately 60–65% of WFT on traps were female (approximately 20–30 females per trap), the overall density of thrips on traps and in the crop increased rapidly, resulting in severe damage to immature fruit. The sex ratio of 0.60–0.65 females corresponded very closely to a mean of five adult WFT per flower at the start of the trapping week, which was an infestation level previously calculated as the action threshold to prevent damage to young green fruit.     

The role of floral structure and biotic factors in determining the occurrence of florivorous thrips in a dystilous shrub

Elucidating the factors determining the occurrence of florivorous organisms is an essential step for comprehending arthropod–plant interactions, especially when considering florivores that use flowers/inflorescences as microhabitats. In this study, we characterize the interaction between florivorous thrips (Thysanoptera) and Palicourea rigida (Rubiaceae), a distylous hummingbird-pollinated shrub. We investigated the relative role of different factors in determining thrips occurrence in the flower and inflorescence microhabitats. Furthermore, we experimentally examined the protective role of corolla influencing thrips exploration of floral buds. Frankliniella musaeperda (Thripidae) was the only species recorded on P. rigida, feeding on floral tissue, pollen and nectar. Thrips occurrence was not related to distyly, but rather to floral stage. Open flowers presented the highest abundance of thrips, followed by senescent flowers and then buds. The experimental opening of buds translated in increased thrips occurrence, indicating that F. musaeperda manage to explore the microhabitat offered by the floral chamber, as long as there is an opening in the corolla. In inflorescences, thrips abundance was negatively related to the number of ants visiting extrafloral nectaries. We found that the marked difference between floral morphs of distylous plants is not necessarily reflected in the abundance of florivores. Thrips seek for floral cavities, preferentially those with fresh tissue, which may confer nutrient-rich food and protection. Buds also provide this; however, the enclosed petals are an effective barrier against F. musaeperda entrance. At inflorescence scale, presence of mutualistic ants in high numbers can drive away these flower-feeding insects. Despite the abundance of thrips in the flowers, there was no evidence of any functional relationship, either of pollination for flowers or of breeding for insects. We demonstrate here that in the flower/inflorescence microhabitat, structural and biotic factors play a key role in the exploitation and occupation by insect florivores.     

Sex determination in the monoecious species cucumber is confined to specific floral whorls

In unisexual flowers, sex is determined by the selective repression of growth or the abortion of either male or female reproductive organs. The mechanism by which this process is controlled in plants is still poorly understood. Because it is known that the identity of reproductive organs in plants is controlled by homeotic genes belonging to the MADS box gene family, we analyzed floral homeotic mutants from cucumber, a species that bears both male and female flowers on the same individual. To study the characteristics of sex determination in more detail, we produced mutants similar to class A and C homeotic mutants from well-characterized hermaphrodite species such as Arabidopsis by ectopically expressing and suppressing the cucumber gene CUCUMBER MADS1 (CUM1). The cucumber mutant green petals (gp) corresponds to the previously characterized B mutants from several species and appeared to be caused by a deletion of 15 amino acid residues in the coding region of the class B MADS box gene CUM26. These homeotic mutants reveal two important concepts that govern sex determination in cucumber. First, the arrest of either male or female organ development is dependent on their positions in the flower and is not associated with their sexual identity. Second, the data presented here strongly suggest that the class C homeotic function is required for the position-dependent arrest of reproductive organs.     

Host-plant species modifies the diet of an omnivore feeding on three trophic levels

The diet choice of omnivores feeding on two adjacent trophic levels (either plants and herbivores or herbivores and predators) has been studied extensively. However, omnivores usually feed on more than two trophic levels, and this diet choice and its consequences for population dynamics have hardly been studied. We report how host-plant quality affects the diet choice of western flower thrips feeding on three trophic levels: plants (cucumber or sweet pepper), eggs of spider mites and eggs of a predatory mite that attacks spider mites. Spider mites feed on the same host plants as thrips and produce a web that hampers predator mobility. To assess the indirect effects of spider mites on predation by thrips, the thrips were offered spider-mite eggs and predatory-mite eggs on cucumber or sweet pepper leaf discs that were either clean, damaged by spider mites but without spider-mite web, or damaged and webbed. We show that, overall, thrips consumed more eggs on sweet pepper, a plant of low quality, than on cucumber, a high quality host plant. On damaged and webbed leaf discs (mimicking the natural situation), thrips killed more predator eggs than spider-mite eggs on sweet pepper, but they killed equal numbers of eggs of each species on cucumber. This is because web hampered predation on spider-mite eggs by thrips on sweet pepper, but not on cucumber, whereas it did not affect predation on predatory-mite eggs. We used the data obtained to parameterize a model of the local dynamics of this system. The model predicts that total predation by the omnivore has little effects on population dynamics, whereas differential attack of predator eggs and spider-mite eggs by the omnivore has large effects on the dynamics of both mite species on the two host plants.     

Jasmonate-dependent plant defense restricts thrips performance and preference

Background  

The western flower thrips (Frankliniella occidentalis [Pergande]) is one of the most important insect herbivores of cultivated plants. However, no pesticide provides complete control of this species, and insecticide resistance has emerged around the world. We previously reported the important role of jasmonate (JA) in the plant's immediate response to thrips feeding by using an Arabidopsis leaf disc system. In this study, as the first step toward practical use of JA in thrips control, we analyzed the effect of JA-regulated Arabidopsis defense at the whole plant level on thrips behavior and life cycle at the population level over an extended period. We also studied the effectiveness of JA-regulated plant defense on thrips damage in Chinese cabbage (Brassica rapa subsp. pekinensis).     

Damage to nectarines by the western flower thrips (Thysanoptera: Thripidae) in the interior of British Columbia, Canada

The phenology of damage by the western flower thrips, Frankliniella occidentalis (Pergande), on nectarines was investigated using sticky cards and direct sampling of buds between 1993 and 1995 in the interior of British Columbia, the most susceptible period for damage by western flower thrips to nectarines. The life stage responsible for damage and variation in susceptibility to damage of 11 different nectarine varieties were determined. To evaluate the predictive ability of 2 sampling methods, thrips were counted from both buds and sticky cards before petal fall and correlated to damage levels at husk drop. Damage to nectarines was caused almost entirely by larval feeding at petal fall. No predictive relationships between adult or larval densities of western flower thrips and subsequent damage to fruit were apparent. Varieties did not differ in terms of larval densities at petal fall or the subsequent damage to fruit. Female western flower thrips oviposit in nectarine buds from dormant through bloom stages primarily in sepal tissues in the early buds, and in filaments and petals as these become available.     

Intraguild predation among plant pests: western flower thrips larvae feed on whitefly crawlers

Omnivores obtain resources from more than one trophic level, and choose their food based on quantity and quality of these resources. For example, omnivores may switch to feeding on plants when prey are scarce. Larvae of the western flower thrips Frankiniella occidentalis Pergande (Thysanoptera: Thripidae) are an example of omnivores that become predatory when the quality of their host plant is low. Western flower thrips larvae usually feed on leaf tissue and on plant pollen, but may also attack eggs of predatory mites, their natural enemies, and eggs of the two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae), one of their competitors. Here, we present evidence that western flower thrips larvae prey on Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae), another competitor for plant tissue. We tested this on two host plant species, cucumber (Cucumis sativa L.), considered a host plant of high quality for western flower thrips, and sweet pepper (Capsicum annuum L.), a relatively poor quality host. We found that western flower thrips killed and fed especially on whitefly crawlers and that the incidence of feeding did not depend on host-plant species. The developmental rate and oviposition rate of western flower thrips was higher on a diet of cucumber leaves with whitefly crawlers than on cucumber leaves without whitefly crawlers, suggesting that thrips do not just kill whiteflies to reduce competition, but utilize whitefly crawlers as food.     

The Mirid Bug Dicyphus tamaninii as a Greenhouse Whitefly and Western Flower Thrips Predator on Cucumber

Dicyphus tamaninii Wagner is a polyphagous predator that also feeds on plants. Its effectiveness against several pests has been tested and good results have been obtained on tomato, but not on cucumber. This paper reports the results of three exclusion cage experiments. The first was carried out to evaluate the effectiveness of D. tamaninii for reducing greenhouse whitefly and western flower thrips populations on cucumber. The second experiment examined the safety of the mirid bug in terms of the potential for damaging cucumber fruits even at very low prey densities. Two predator (3 and 18 insects/plant) and variable prey release rates were used. The predator was able to reduce whitefly populations greatly, even at high initial pest infestation levels, especially at the higher release rate. Western flower thrips populations were maintained at very low densities a few weeks after the predator had been introduced into cages at the two release rates tested. The mirid bug was barely able to reproduce on cucumber in the absence of prey. Mirid feeding punctures on cucumber fruit or yield decrease due to the action of mirids were not observed. The potential of this mirid bug for inoculative and conservation biological control is discussed.