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1.  Arabidopsis-thrips system for analysis of plant response to insect feeding 
Plant Signaling & Behavior  2008;3(7):446-447.
Insect feeding retards plant growth and decreases crop productivity. Plants respond to insect feeding at the molecular, cellular and physiological levels. The roles of the plant hormones jasmonic acid (JA), ethylene (ET) and salicylic acid (SA) in plant responses to insect feeding have been studied. However, these studies are focused on the plant responses to feeding by well-studied caterpillar type insects or aphid pests. In contrast, we have focused on a minute insect pest, the western flower thrips (Frankliniella occidentalis). Analyses of the responses of hormone-related mutants of Arabidopsis (i.e., JA-insensitive mutant coi1-1, ET-insensitive mutants ein2-1 and ein3-1, and SA-deficient mutant eds16-1) and transcriptome-based comparative analyses indicate the central role of JA in plant responses to thrips feeding. Our work clearly shows that JA signaling, but not JA/ET signaling, is involved in plant tolerance to thrips feeding. We intend to examine the utility and suitability of the Arabidopsis-thrips system in studies of plant responses to insect feeding.
PMCID: PMC2634423  PMID: 19704479
Arabidopsis thaliana; ethylene; Frankliniella occidentalis; insect feeding; jasmonate; western flower thrips
2.  Prey Preference of the Predatory Mite, Amblyseius swirskii between First Instar Western Flower Thrips Frankliniella occidentalis and Nymphs of the Twospotted Spider Mite Tetranychus urticae  
The prey preference of polyphagous predators plays an important role in suppressing different species of pest insects. In this study the prey preference of the predatory mite, Amblyseius swirskii (Athias-Henriot) (Acari: Phytoseiidae) was examined between nymphs of the twospotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae) and first instar larvae of the western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), as well as between active and chrysalis spider mite protonymphs and active and chrysalis spider mite deutonymphs. The study was done in the laboratory on bean leaf discs at 25 ± 1° C and 70 ± 5% RH. Amblyseius swirskii had a clear preference for thrips compared to both spider mite protonymphs and deutonymphs. About twice as many thrips as spider mites were consumed. Amblyseius swirskii did not show a preference between active and chrysalis stages of spider mites.
doi:10.1673/031.010.14109
PMCID: PMC3016914  PMID: 21070175
polyphagous; biological control
3.  The Green Lacewing, Chrysoperla carnea: Preference between Lettuce Aphids, Nasonovia ribisnigri, and Western Flower Thrips, Frankliniella occidentalis 
This study investigated the prey preference of 3rd instar green lacewing, Chrysoperla carnea Stephens (Neuroptera: Chrysopidae), between western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), and lettuce aphids, Nasonovia ribisnigri (Mosley) (Hemiptera: Aphididae) in laboratory experiments at 25 ± 1° C and 70 ± 5% RH with five prey ratios (10 aphids:80 thrips, 25 aphids:65 thrips, 45 aphids:45 thrips, 65 aphids:25 thrips, and 80 aphids:10 thrips). Third instar C. carnea larvae readily preyed upon both thrips and aphids, with thrips mortality varying between 40 and 90%, and aphid mortality between 52 and 98%. Chrysoperla carnea had a significant preference for N. ribisnigri at two ratios (10 aphids:80 thrips, 65 aphids:25 thrips), but no preference for either prey at the other ratios. There was no significant linear relationship between preference index and prey ratio, but a significant intercept of the linear regression indicated an overall preference of C. carnea for aphids with a value of 0.651 ± 0.054. The possible implications of these findings for control of N. ribisnigri and F. occidentalis by C. carnea are discussed.
doi:10.1673/031.013.9401
PMCID: PMC3835039  PMID: 24205864
Aphididae; biological control; Chrysopidae; prey ratios; Thripidae
4.  Foraging on Individual Leaves by an Intracellular Feeding Insect Is Not Associated with Leaf Biomechanical Properties or Leaf Orientation 
PLoS ONE  2013;8(11):e80911.
Nearly all herbivorous arthropods make foraging-decisions on individual leaves, yet systematic investigations of the adaptive significance and ecological factors structuring these decisions are rare with most attention given to chewing herbivores. This study investigated why an intracellular feeding herbivore, Western flower thrips (WFT) Frankliniella occidentalis Pergande, generally avoids feeding on the adaxial leaf surface of cotton cotyledons. WFT showed a significant aversion to adaxial-feeding even when excised-cotyledons were turned up-side (abaxial-side ‘up’), suggesting that negative-phototaxis was not a primary cause of thrips foraging patterns. No-choice bioassays in which individual WFT females were confined to either the abaxial or adaxial leaf surface showed that 35% fewer offspring were produced when only adaxial feeding was allowed, which coincided with 32% less plant feeding on that surface. To test the hypothesis that leaf biomechanical properties inhibited thrips feeding on the adaxial surface, we used a penetrometer to measure two variables related to the ‘toughness’ of each leaf surface. Neither variable negatively co-varied with feeding. Thus, while avoiding the upper leaf surface was an adaptive foraging strategy, the proximate cause remains to be elucidated, but is likely due, in part, to certain leaf properties that inhibit feeding.
doi:10.1371/journal.pone.0080911
PMCID: PMC3829965  PMID: 24260510
5.  Pyrethrins Protect Pyrethrum Leaves Against Attack by Western Flower Thrips, Frankliniella occidentalis 
Journal of Chemical Ecology  2012;38(4):370-377.
Pyrethrins are active ingredients extracted from pyrethrum flowers (Tanacetum cinerariifolium), and are the most widely used botanical insecticide. However, several thrips species are commonly found on pyrethrum flowers in the field, and are the dominant insects found inside the flowers. Up to 80 % of western flower thrips (WFT, Frankliniella occidentalis) adults died within 3 days of initiating feeding on leaves of pyrethrum, leading us to evaluate the role of pyrethrins in the defense of pyrethrum leaves against WFT. The effects of pyrethrins on WFT survival, feeding behavior, and reproduction were measured both in vitro and in planta (infiltrated leaves). The lethal concentration value (LC50) for pyrethrins against WFT adults was 12.9 mg/ml, and pyrethrins at 0.1 % (w/v) and 1 % (w/v) had significantly negative effects on feeding, embryo development, and oviposition. About 20-70 % of WFT were killed within 2 days when they were fed chrysanthemum leaves containing 0.01-1 % pyrethrins. Chrysanthemum leaves containing 0.1 % or 1 % pyrethrins were significantly deterrent to WFT. In a no-choice assay, the reproduction of WFT was reduced significantly when the insects were fed leaves containing 0.1 % pyrethrins, and no eggs were found in leaves containing 1 % pyrethrins. Our results suggest that the natural concentrations of pyrethrins in the leaves may be responsible for the observed high mortality of WFT on pyrethrum.
doi:10.1007/s10886-012-0097-7
PMCID: PMC3324680  PMID: 22456949
Pyrethrum; Pyrethrins; Western flower thrips; Frankliniella occidentalis; Natural pesticide; toxicity; Tanacetum cinerariifolium; Crop pest
6.  Selenium hyperaccumulation offers protection from cell disruptor herbivores 
BMC Ecology  2010;10:19.
Background
Hyperaccumulation, the rare capacity of certain plant species to accumulate toxic trace elements to levels several orders of magnitude higher than other species growing on the same site, is thought to be an elemental defense mechanism against herbivores and pathogens. Previous research has shown that selenium (Se) hyperaccumulation protects plants from a variety of herbivores and pathogens. Selenium hyperaccumulating plants sequester Se in discrete locations in the leaf periphery, making them potentially more susceptible to some herbivore feeding modes than others. In this study we investigate the protective function of Se in the Se hyperaccumulators Stanleya pinnata and Astragalus bisulcatus against two cell disrupting herbivores, the western flower thrips (Frankliniella occidentalis) and the two-spotted spider mite (Tetranychus urticae).
Results
Astragalus bisulcatus and S. pinnata with high Se concentrations (greater than 650 mg Se kg-1) were less subject to thrips herbivory than plants with low Se levels (less than 150 mg Se kg-1). Furthermore, in plants containing elevated Se levels, leaves with higher concentrations of Se suffered less herbivory than leaves with less Se. Spider mites also preferred to feed on low-Se A. bisulcatus and S. pinnata plants rather than high-Se plants. Spider mite populations on A. bisulcatus decreased after plants were given a higher concentration of Se. Interestingly, spider mites could colonize A. bisulcatus plants containing up to 200 mg Se kg-1 dry weight, concentrations which are toxic to many other herbivores. Selenium distribution and speciation studies using micro-focused X-ray fluorescence (μXRF) mapping and Se K-edge X-ray absorption spectroscopy revealed that the spider mites accumulated primarily methylselenocysteine, the relatively non-toxic form of Se that is also the predominant form of Se in hyperaccumulators.
Conclusions
This is the first reported study investigating the protective effect of hyperaccumulated Se against cell-disrupting herbivores. The finding that Se protected the two hyperaccumulator species from both cell disruptors lends further support to the elemental defense hypothesis and increases the number of herbivores and feeding modes against which Se has shown a protective effect. Because western flower thrips and two-spotted spider mites are widespread and economically important herbivores, the results from this study also have potential applications in agriculture or horticulture, and implications for the management of Se-rich crops.
doi:10.1186/1472-6785-10-19
PMCID: PMC2940900  PMID: 20799959
7.  Invasion Genetics of the Western Flower Thrips in China: Evidence for Genetic Bottleneck, Hybridization and Bridgehead Effect 
PLoS ONE  2012;7(4):e34567.
The western flower thrips, Frankliniella occidentalis (Pergande), is an invasive species and the most economically important pest within the insect order Thysanoptera. F. occidentalis, which is endemic to North America, was initially detected in Kunming in southwestern China in 2000 and since then it has rapidly invaded several other localities in China where it has greatly damaged greenhouse vegetables and ornamental crops. Controlling this invasive pest in China requires an understanding of its genetic makeup and migration patterns. Using the mitochondrial COI gene and 10 microsatellites, eight of which were newly isolated and are highly polymorphic, we investigated the genetic structure and the routes of range expansion of 14 F. occidentalis populations in China. Both the mitochondrial and microsatellite data revealed that the genetic diversity of F. occidentalis of the Chinese populations is lower than that in its native range. Two previously reported cryptic species (or ecotypes) were found in the study. The divergence in the mitochondrial COI of two Chinese cryptic species (or ecotypes) was about 3.3% but they cannot be distinguished by nuclear markers. Hybridization might produce such substantial mitochondrial-nuclear discordance. Furthermore, we found low genetic differentiation (global FST = 0.043, P<0.001) among all the populations and strong evidence for gene flow, especially from the three southwestern populations (Baoshan, Dali and Kunming) to the other Chinese populations. The directional gene flow was further supported by the higher genetic diversity of these three southwestern populations. Thus, quarantine and management of F. occidentalis should focus on preventing it from spreading from the putative source populations to other parts of China.
doi:10.1371/journal.pone.0034567
PMCID: PMC3317996  PMID: 22509325
8.  Onion Thrips, Thrips tabaci, Have Gut Bacteria That are Closely Related to the Symbionts of the Western Flower Thrips, Frankliniella occidentalis  
It has been shown that many insects have Enterobacteriaceae bacteria in their gut system. The western flower thrips, Frankliniella occidentalis Pergande [Thysanoptera: Thripidae], has a symbiotic relation with Erwinia species gut bacteria. To determine if other Thripidae species have similar bacterial symbionts, the onion thrips, Thrips tabaci, was studied because, like F. occidentalis, it is phytophagous. Contrary to F. occidentalis, T. tabaci is endemic in Europe and biotypes have been described. Bacteria were isolated from the majority of populations and biotypes of T. tabaci examined. Bacteria were present in high numbers in most individuals of the populations studied. Like F. occidentalis, T. tabaci contained one type of bacterium that clearly outnumbered all other types present in the gut. This bacterium was identified as an Erwinia species, as was also the case for F. occidentalis. However, its biochemical characteristics and 16S rDNA sequence differed from the bacteria present in F. occidentalis.
doi:10.1673/031.008.2301
PMCID: PMC3061595  PMID: 20298113
symbiosis; 16S rDNA; bacterial taxonomy; Erwinia; Pantoea agglomerans; API 20E; insect gut
9.  Phytophagous Arthropods and a Pathogen Sharing a Host Plant: Evidence for Indirect Plant-Mediated Interactions 
PLoS ONE  2011;6(5):e18840.
In ecological systems, indirect interactions between plant pathogens and phytophagous arthropods can arise when infestation by a first attacker alters the common host plant so that although a second attacker could be spatially or temporally separated from the first one, the former could be affected. The induction of plant defense reactions leading to the production of secondary metabolites is thought to have an important role since it involves antagonistic and/or synergistic cross-talks that may determine the outcome of such interactions. We carried out experiments under controlled conditions on young rose plants in order to assess the impact of these indirect interactions on life history traits of three pests: the necrotrophic fungus Botrytis cinerea Pers.: Fr. (Helotiales: Sclerotiniaceae), the aphid Rhodobium porosum Sanderson (Hemiptera: Aphididae) and the thrips Frankliniella occidentalis Pergande (Thysanoptera: Thripidae). Our results indicated (i) a bi-directional negative interaction between B. cinerea and R. porosum, which is conveyed by decreased aphid growth rate and reduced fungal lesion area, as well as (ii) an indirect negative effect of B. cinerea on insect behavior. No indirect effect was observed between thrips and aphids. This research highlights several complex interactions that may be involved in structuring herbivore and plant pathogen communities within natural and managed ecosystems.
doi:10.1371/journal.pone.0018840
PMCID: PMC3097179  PMID: 21611161
10.  Can Mass Trapping Reduce Thrips Damage and Is It Economically Viable? Management of the Western Flower Thrips in Strawberry 
PLoS ONE  2013;8(11):e80787.
The western flower thrips Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) is a cosmopolitan, polyphagous insect pest that causes bronzing to fruit of strawberry (Fragaria x ananassa). The main aim of this study was to test whether mass trapping could reduce damage and to predict whether this approach would be economically viable. In semi-protected strawberry crops, mass trapping of F. occidentalis using blue sticky roller traps reduced adult thrips numbers per flower by 61% and fruit bronzing by 55%. The addition of the F. occidentalis aggregation pheromone, neryl (S)-2-methylbutanoate, to the traps doubled the trap catch, reduced adult thrips numbers per flower by 73% and fruit bronzing by 68%. The factors affecting trapping efficiency through the season are discussed. Damage that would result in downgrading of fruit to a cheaper price occurred when bronzing affected about 10% of the red fruit surface. Cost-benefit analysis using this threshold showed that mass trapping of thrips using blue sticky roller traps can be cost-effective in high-value crops. The addition of blue sticky roller traps to an integrated pest management programme maintained thrips numbers below the damage threshold and increased grower returns by a conservative estimate of £2.2k per hectare. Further work is required to develop the F. occidentalis aggregation pheromone for mass trapping and to determine the best timing for trap deployment. Mass trapping of thrips is likely to be cost-effective in other countries and other high-value crops affected by F. occidentalis damage, such as cucumber and cut flowers.
doi:10.1371/journal.pone.0080787
PMCID: PMC3839998  PMID: 24282554
11.  Taqman real-time quantitative PCR for identification of western flower thrip (Frankliniella occidentalis) for plant quarantine 
Biology Letters  2010;6(4):555-557.
Western flower thrip (Frankliniella occidentalis) is a major global pest of agricultural products. It directly damages crops through feeding, oviposition activity or transmission of several plant viruses. We describe a Taqman real-time quantitative PCR detection system, which can rapidly identify F. occidentalis from thrips larvae to complement the traditional morphological identification. The data showed that our detection system targeted on the ribosomal RNA gene regions of F. occidentalis has high sensitivity and specificity. The rapid method can be used for on-site testing of samples at ports-of-entry in the future.
doi:10.1098/rsbl.2009.1060
PMCID: PMC2936211  PMID: 20129946
Frankliniella occidentalis; real-time quantitative PCR; plant quarantine
12.  Analysis of the Salivary Gland Transcriptome of Frankliniella occidentalis 
PLoS ONE  2014;9(4):e94447.
Saliva is known to play a crucial role in insect feeding behavior and virus transmission. Currently, little is known about the salivary glands and saliva of thrips, despite the fact that Frankliniella occidentalis (Pergande) (the western flower thrips) is a serious pest due to its destructive feeding, wide host range, and transmission of tospoviruses. As a first step towards characterizing thrips salivary gland functions, we sequenced the transcriptome of the primary salivary glands of F. occidentalis using short read sequencing (Illumina) technology. A de novo-assembled transcriptome revealed 31,392 high quality contigs with an average size of 605 bp. A total of 12,166 contigs had significant BLASTx or tBLASTx hits (E≤1.0E−6) to known proteins, whereas a high percentage (61.24%) of contigs had no apparent protein or nucleotide hits. Comparison of the F. occidentalis salivary gland transcriptome (sialotranscriptome) against a published F. occidentalis full body transcriptome assembled from Roche-454 reads revealed several contigs with putative annotations associated with salivary gland functions. KEGG pathway analysis of the sialotranscriptome revealed that the majority (18 out of the top 20 predicted KEGG pathways) of the salivary gland contig sequences match proteins involved in metabolism. We identified several genes likely to be involved in detoxification and inhibition of plant defense responses including aldehyde dehydrogenase, metalloprotease, glucose oxidase, glucose dehydrogenase, and regucalcin. We also identified several genes that may play a role in the extra-oral digestion of plant structural tissues including β-glucosidase and pectin lyase; and the extra-oral digestion of sugars, including α-amylase, maltase, sucrase, and α-glucosidase. This is the first analysis of a sialotranscriptome for any Thysanopteran species and it provides a foundational tool to further our understanding of how thrips interact with their plant hosts and the viruses they transmit.
doi:10.1371/journal.pone.0094447
PMCID: PMC3988053  PMID: 24736614
13.  Juvenile prey induce antipredator behaviour in adult predators 
Experimental & Applied Acarology  2012;59(3):275-282.
It is generally assumed that the choice of oviposition sites in arthropods is affected by the presence of food for the offspring on the one hand and by predation risk on the other hand. But where should females oviposit when the food itself poses a predation risk for their offspring? Here, we address this question by studying the oviposition behaviour of the predatory mite Amblyseius swirskii in reaction to the presence of its counterattacking prey, the western flower thrips Frankliniella occidentalis. We offered the mites a choice between two potential oviposition sites, one with and one without food. We used two types of food: thrips larvae, which are predators of eggs of predatory mite but are consumed by older predator stages, and pollen, a food source that poses no risk to the predators. With pollen as food, the predators preferred ovipositing on the site with food. This might facilitate the foraging for food by the immature offspring that will emerge from the eggs. With thrips as food, female predators preferred ovipositing on the site without thrips. Predators that oviposited more on the site with thrips larvae killed more thrips larvae than females that oviposited on the site without food, but this did not result in higher oviposition. This suggests that the females killed thrips to protect their offspring. Our results show that predators display complex anti-predator behaviour in response to the presence of counter-attacking prey.
doi:10.1007/s10493-012-9601-6
PMCID: PMC3557378  PMID: 22923143
Phytoseiids; Thrips; Oviposition site selection; Role reversals; Predator–prey interactions; Counterattacking prey; Amblyseius swirskii
14.  The Species Composition of Thrips (Insecta: Thysanoptera) Inhabiting Mango Orchards in Pulau Pinang, Malaysia 
A field study was conducted at two localities on Pulau Pinang, Malaysia, during two consecutive mango flowering seasons in 2009 to identify variations in the species composition of thrips infesting treated and untreated mango (Mangifera indica L.) orchards. The CO2 immobilisation technique and the cutting method were used to recover different thrips species from mango panicles and weed host plants, respectively. The mango panicles and various weed species within the treated orchard were found to harbour four thrips species from the family Thripidae. These species were identified as Thrips hawaiiensis (Morgan), Scirtothrips dorsalis (Hood), Frankliniella schultzei (Trybom) and Megalurothrips usitatus (Bagnall). The weed species Mimosa pudica, Cleome rutidosperma, Echinochloa colonum, Borreria laevicaulis, Veronia cinerea and Asystasia coromandeliana served as additional hosts to these thrips. Six thrips species were found in the untreated orchard. These species included Thrips palmi (Karny), Haplothrips sp. (Amyot and Serville) and the four thrips species found in the treated orchard. A brief description of the larvae for each genus is provided.
PMCID: PMC3799398  PMID: 24575225
Thrips; Mangifera indica; Weed; Malaysia
15.  Variation within and between Frankliniella Thrips Species in Host Plant Utilization 
Anthophilous flower thrips in the genus Frankliniella (Thysanoptera: Thripidae) exploit ephemeral plant resources and therefore must be capable of successfully locating appropriate hosts on a repeated basis, yet little is known of interspecific and intraspecific variation in responses to host plant type and nutritional quality. Field trials were conducted over two seasons to determine if the abundance of males and females of three common Frankliniella species, F. occidentalis (Pergande), F. tritici (Fitch) and F. bispinosa (Morgan), their larvae, and a key predator, Orius insidiosus (Say) (Hemiptera: Anthocoridae) were affected by host plant type and plant nutritional quality. Two host plants, pepper, Capsicum annuum L. (Solanales: Solanaceae) and tomato, Solanum lycopersicum L. that vary in suitability for these species were examined, and their nutritional quality was manipulated by applying three levels of nitrogen fertilization (101 kg/ha, 202 kg/ha, 404 kg/ha). F. occidentalis females were more abundant in pepper than in tomato, but males did not show a differential response. Both sexes of F. tritici and F. bispinosa were more abundant in tomato than in pepper. Larval thrips were more abundant in pepper than in tomato. Likewise, O. insidiosus females and nymphs were more abundant in pepper than in tomato. Only F. occidentalis females showed a distinct response to nitrogen fertilization, with abundance increasing with fertilization. These results show that host plant utilization patterns vary among Frankliniella spp. and should not be generalized from results of the intensively studied F. occidentalis. Given the different pest status of these species and their differential abundance in pepper and tomato, it is critical that scouting programs include species identifications for proper management.
doi:10.1673/031.011.0141
PMCID: PMC3281448  PMID: 21539418
fertilization; flower thrips; Frankliniella occidentalis; Frankliniella tritici; Frankliniella bispinosa; host selection; Orius insidiosus; pepper; tomato
16.  Herbivore benefits from vectoring plant virus through reduction of period of vulnerability to predation 
Oecologia  2008;156(4):797-806.
Herbivores can profit from vectoring plant pathogens because the induced defence of plants against pathogens sometimes interferes with the induced defence of plants against herbivores. Plants can also defend themselves indirectly by the action of the natural enemies of the herbivores. It is unknown whether the defence against pathogens induced in the plant also interferes with the indirect defence against herbivores mediated via the third trophic level. We previously showed that infection of plants with Tomato spotted wilt virus (TSWV) increased the developmental rate of and juvenile survival of its vector, the thrips Frankliniella occidentalis. Here, we present the results of a study on the effects of TSWV infections of plants on the effectiveness of three species of natural enemies of F. occidentalis: the predatory mites Neoseiulus cucumeris and Iphiseius degenerans, and the predatory bug Orius laevigatus. The growth rate of thrips larvae was positively affected by the presence of virus in the host plant. Because large larvae are invulnerable to predation by the two species of predatory mites, this resulted in a shorter period of vulnerability to predation for thrips that developed on plants with virus than thrips developing on uninfected plants (4.4 vs. 7.9 days, respectively). Because large thrips larvae are not invulnerable to predation by the predatory bug Orius laevigatus, infection of the plant did not affect the predation risk of thrips larvae from this predator. This is the first demonstration of a negative effect of a plant pathogen on the predation risk of its vector.
doi:10.1007/s00442-008-1027-9
PMCID: PMC2469278  PMID: 18392858
Tritrophic interactions; Preference; Prey size; Frankliniella occidentalis; Tomato spotted wilt virus
17.  Innate Responses to Putative Ancestral Hosts: Is the Attraction of Western Flower Thrips to Pine Pollen a Result of Relict Olfactory Receptors? 
Journal of Chemical Ecology  2014;40:534-540.
Pollinophagy is widely documented in the order Thysanoptera, with representative individuals from six of the nine divergent families known to feed on pollen. Various pollens of the genus Pinus increase the development time, fecundity, longevity, and settling preference of Western Flower Thrips (WFT), Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Certain species of flower thrips discriminate among pollen types, but no studies have elucidated the olfactory cues that play a role in their pollen preferences. In this study, the volatile organic compounds emitted by pollens of the genus Pinus were elucidated. Various chemicals from pollen headspace elicited electrophysiological responses from WFT antennae. The compound (S)-(-)-verbenone, identified in pollen headspace, attracted WFT in a 4-arm olfactometer. This compound has potential for use in integrated pest management programs against the pest. We present the hypothesis that this polyphagous insect may have retained ancestral ‘relict’ olfactory receptors through the course of evolution, to explain this attraction to pine pollen. This attraction has allowed the insect to find and exploit an unusual nutrient source that significantly increases its fitness. The study demonstrates how fossil record analysis and subsequent evolutionary knowledge can aid in explaining possibilities as to why some insects sense and respond to chemicals that would otherwise seem peculiar to their ecology, allowing insight into the evolutionary forces that may shape insect olfactory systems over time.
Electronic supplementary material
The online version of this article (doi:10.1007/s10886-014-0450-0) contains supplementary material, which is available to authorized users.
doi:10.1007/s10886-014-0450-0
PMCID: PMC4090808  PMID: 24879603
Frankliniella occidentalis; Thrips; Pine pollen; Semiochemical; (S)-(-)-Verbenone; Electroantennogram; Insect pest
18.  Development and Characterization of 18 Novel EST-SSRs from the Western Flower Thrips, Frankliniella occidentalis (Pergande) 
The western flower thrips, Frankliniella occidentalis (Pergande), is an invasive species and the most economically important pest within the insect order Thysanoptera. For a better understanding of the genetic makeup and migration patterns of F. occidentalis throughout the world, we characterized 18 novel polymorphic EST-derived microsatellites. The mutational mechanism of these EST-SSRs was also investigated to facilitate the selection of appropriate combinations of markers for population genetic studies. Genetic diversity of these novel markers was assessed in 96 individuals from three populations in China (Harbin, Dali, and Guiyang). The results showed that all these 18 loci were highly polymorphic; the number of alleles ranged from 2 to 15, with an average of 5.50 alleles per locus. The observed (HO) and expected (HE) heterozygosities ranged from 0.072 to 0.707 and 0.089 to 0.851, respectively. Furthermore, only two locus/population combinations (WFT144 in Dali and WFT50 in Guiyang) significantly deviated from Hardy–Weinberg equilibrium (HWE). Pairwise FST analysis showed a low but significant differentiation (0.026 < FST < 0.032) among all three pairwise population comparisons. Sequence analysis of alleles per locus revealed a complex mutational pattern of these EST-SSRs. Thus, these EST-SSRs are useful markers but greater attention should be paid to the mutational characteristics of these microsatellites when they are used in population genetic studies.
doi:10.3390/ijms13032863
PMCID: PMC3317692  PMID: 22489130
Frankliniella occidentalis; EST-SSRs; expressed sequence tags; microsatellite; population genetics
19.  Effects of kinship or familiarity? Small thrips larvae experience lower predation risk only in groups of mixed-size siblings 
In many species of insects, larvae are distributed in an aggregated fashion. As they may differ in size and size matters to predation risk, small larvae may be less likely to fall prey to predators when near large and therefore better-defended larvae. We hypothesize that the small larvae may profit even more when these large larvae are siblings. We tested this hypothesis on kinship-dependent survival in groups of larvae of the Western flower thrips (Frankliniella occidentalis) exposed to a predatory mite (Iphiseius degenerans). Our experiments showed that small larvae in sibling groups survive significantly better than in non-sibling groups, but only when such groups consisted of a mixture of small and large larvae. To test whether the survival effect we found is due to familiarity of thrips larvae growing up together (i.e. on one leaf), we also measured survival in sibling groups of larvae grown up on different leaves and in non-sibling groups of larvae grown up on the same leaf. These experiments showed an increased survival of small thrips larvae only in groups of sibling larvae from the same leaf. Non-sibling larvae did not show an increased survival when they come from the same leaf. Our results indicated that the increased survival in sibling groups was only partly due to the familiarity effect we tested. Growing up together did not return the same survival effect for non-siblings as it did for siblings. We conclude that growing up together is a necessary but not sufficient condition for discrimination in thrips larvae.
doi:10.1007/s00265-014-1715-x
PMCID: PMC4018515  PMID: 24833813
Frankliniella occidentalis; Iphiseius degenerans; Kin discrimination; Predation risk; Size structure; Non-social insects
20.  Genome-wide analysis of the AP2/ERF transcription factor superfamily in Chinese cabbage (Brassica rapa ssp. pekinensis) 
BMC Genomics  2013;14:573.
Background
Chinese cabbage (Brassica rapa ssp. pekinensis) is a member of one of the most important leaf vegetables grown worldwide, which has experienced thousands of years in cultivation and artificial selection. The entire Chinese cabbage genome sequence, and more than forty thousand proteins have been obtained to date. The genome has undergone triplication events since its divergence from Arabidopsis thaliana (13 to 17 Mya), however a high degree of sequence similarity and conserved genome structure remain between the two species. Arabidopsis is therefore a viable reference species for comparative genomics studies. Variation in the number of members in gene families due to genome triplication may contribute to the broad range of phenotypic plasticity, and increased tolerance to environmental extremes observed in Brassica species. Transcription factors are important regulators involved in plant developmental and physiological processes. The AP2/ERF proteins, one of the most important families of transcriptional regulators, play a crucial role in plant growth, and in response to biotic and abiotic stressors. Our analysis will provide resources for understanding the tolerance mechanisms in Brassica rapa ssp. pekinensis.
Results
In the present study, 291 putative AP2/ERF transcription factor proteins were identified from the Chinese cabbage genome database, and compared with proteins from 15 additional species. The Chinese cabbage AP2/ERF superfamily was classified into four families, including AP2, ERF, RAV, and Soloist. The ERF family was further divided into DREB and ERF subfamilies. The AP2/ERF superfamily was subsequently divided into 15 groups. The identification, classification, phylogenetic reconstruction, conserved motifs, chromosome distribution, functional annotation, expression patterns, and interaction networks of the AP2/ERF transcription factor superfamily were predicted and analyzed. Distribution mapping results showed AP2/ERF superfamily genes were localized on the 10 Chinese cabbage chromosomes. AP2/ERF transcription factor expression levels exhibited differences among six tissue types based on expressed sequence tags (ESTs). In the AP2/ERF superfamily, 214 orthologous genes were identified between Chinese cabbage and Arabidopsis. Orthologous gene interaction networks were constructed, and included seven CBF and four AP2 genes, primarily involved in cold regulatory pathways and ovule development, respectively.
Conclusions
The evolution of the AP2/ERF transcription factor superfamily in Chinese cabbage resulted from genome triplication and tandem duplications. A comprehensive analysis of the physiological functions and biological roles of AP2/ERF superfamily genes in Chinese cabbage is required to fully elucidate AP2/ERF, which provides us with rich resources and opportunities to understand crop stress tolerance mechanisms.
doi:10.1186/1471-2164-14-573
PMCID: PMC3765354  PMID: 23972083
Chinese cabbage; AP2/ERF; Stress tolerance; Gene expression; Interaction network; Protein annotation
21.  The Plant Virus Tomato Spotted Wilt Tospovirus Activates the Immune System of Its Main Insect Vector, Frankliniella occidentalis 
Journal of Virology  2004;78(10):4976-4982.
Tospoviruses have the ability to infect plants and their insect vectors. Tomato spotted wilt virus (TSWV), the type species in the Tospovirus genus, infects its most important insect vector, Frankliniella occidentalis, the western flower thrips (WFT). However, no detrimental effects on the life cycle or cytopathological changes have been reported in the WFT after TSWV infection, and relatively few viral particles can be observed even several days after infection. We hypothesized that TSWV infection triggers an immune response in the WFT. Using subtractive cDNA libraries to probe WFT DNA macroarrays, we found that the WFT's immune system is activated by TSWV infection. The activated genes included (i) those encoding antimicrobial peptides, such as defensin and cecropin; (ii) genes involved in pathogen recognition, such as those encoding lectins; (iii) those encoding receptors that activate the innate immune response, such as Toll-3; and (iv) those encoding members of signal transduction pathways activated by Toll-like receptors, such as JNK kinase. Transcriptional upregulation of these genes after TSWV infection was confirmed by Northern analysis, and the kinetics of the immune response was measured over time. Several of the detected genes were activated at the same time that viral replication was first detected by reverse transcription-PCR. To our knowledge, this is the first report of the activation of an insect vector immune response by a plant virus. The results may lead to a better understanding of insects' immune responses against viruses and may help in the future development of novel control strategies against plant viruses, as well as human and animal viruses transmitted by insect vectors.
doi:10.1128/JVI.78.10.4976-4982.2004
PMCID: PMC400384  PMID: 15113877
22.  The Relationship between Structurally Different Pyrrolizidine Alkaloids and Western Flower Thrips Resistance in F2 Hybrids of Jacobaea vulgaris and Jacobaea aquatica 
Journal of Chemical Ecology  2011;37(10):1071-1080.
Segregating plant hybrids often have more ecological and molecular variability compared to parental species, and are therefore useful for studying relationships between different traits, and the adaptive significance of trait variation. Hybrid systems have been used to study the relationship between the expression of plant defense compounds and herbivore susceptibility. We conducted a western flower thrips (WFT) bioassay using a hybrid family and investigated the relationship between WFT resistance and pyrrolizidine alkaloid (PA) variation. The hybrid family consisted of two parental (Jacobaea vulgaris and Jacobaea aquatica) genotypes, two F1 genotypes, and 94 F2 hybrid lines. The J. aquatica genotype was more susceptible to thrips attack than the J. vulgaris genotype, the two F1 hybrids were as susceptible as J. aquatica, and susceptibility to WFT differed among F2 hybrid lines: 69 F2 lines were equally susceptible compared to J. aquatica, 10 F2 lines were more susceptible than J. aquatica and 15 F2 lines were as resistant as J. vulgaris or were intermediate to the two parental genotypes. Among 37 individual PAs that were derived from four structural groups (senecionine-, jacobine-, erucifoline- and otosenine-like PAs), the N-oxides of jacobine, jaconine, and jacoline were negatively correlated with feeding damage caused by WFT, and the tertiary amines of jacobine, jaconine, jacoline, and other PAs did not relate to feeding damage. Total PA concentration was negatively correlated with feeding damage. Among the four PA groups, only the total concentration of the jacobine-like PAs was negatively correlated with feeding damage. Multiple regression tests suggested that jacobine-like PAs play a greater role in WFT resistance than PAs from other structural groups. We found no evidence for synergistic effects of different PAs on WFT resistance. The relationship between PA variation and WFT feeding damage in the Jacobaea hybrids suggests a role for PAs in resistance to generalist insects.
Electronic supplementary material
The online version of this article (doi:10.1007/s10886-011-0021-6) contains supplementary material, which is available to authorized users.
doi:10.1007/s10886-011-0021-6
PMCID: PMC3197926  PMID: 21969251
Hybridization; Jacobaea vulgaris; Jacobaea aquatica; Secondary metabolite diversity; Chemical defense; Frankliniella occidentalis
23.  Behavioural responses of Frankliniella occidentalis Pergande larvae to methyl jasmonate and cis-jasmone 
Journal of Pest Science  2013;87:53-59.
The larval stages of Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) cause more direct feeding damage to plants than the adults. We, therefore, investigated the behaviour-modifying effects on second instar larvae of two jasmonic acid derivatives. The artificial application of methyl jasmonate and cis-jasmone, both at 1 % concentration, deterred the larvae from settling in a dual choice bean leaf disc assay. We observed a dose-dependent feeding deterrence of both jasmonates and calculated the concentration required to reduce the feeding damage by 50 % relative to the control treatment (FDC50) for each jasmonate. The feeding damage was reduced by the application of cis-jasmone at 1 % concentration, but not by the jasmonates at the respective FDC50 in no-choice leaf disc bioassays. However, significantly more larvae left jasmonate-treated whole potted bean plants by migrating to the soil compared with control plants. Our results may be exploited extending behavioural manipulation by using plant compounds in thrips control programmes to the full lifecycle of the pest. Plant compounds could be used in integrated and biological pest management strategies against F. occidentalis in combination with the application of various above and below ground control measures.
doi:10.1007/s10340-013-0532-8
PMCID: PMC3925295  PMID: 24563647
Thrips; Second instar; Secondary plant compounds; Jasmonates; Feeding deterrent; Leaving behaviour
24.  How Predictable Are the Behavioral Responses of Insects to Herbivore Induced Changes in Plants? Responses of Two Congeneric Thrips to Induced Cotton Plants 
PLoS ONE  2013;8(5):e63611.
Changes in plants following insect attack are referred to as induced responses. These responses are widely viewed as a form of defence against further insect attack. In the current study we explore whether it is possible to make generalizations about induced plant responses given the unpredictability and variability observed in insect-plant interactions. Experiments were conducted to test for consistency in the responses of two congeneric thrips, Frankliniella schultzei Trybom and Frankliniella occidentalis Pergrande (Thysanoptera: Thripidae) to cotton seedlings (Gossypium hirsutum Linneaus (Malvales: Malvaceae)) damaged by various insect herbivores. In dual-choice experiments that compared intact and damaged cotton seedlings, F. schultzei was attracted to seedlings damaged by Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), Tetranychus urticae (Koch) (Trombidiforms: Tetranychidae), Tenebrio molitor Linnaeus (Coleoptera: Tenebrionidae), F. schultzei and F. occidentalis but not to mechanically damaged seedlings. In similar tests, F. occidentalis was attracted to undamaged cotton seedlings when simultaneously exposed to seedlings damaged by H. armigera, T. molitor or F. occidentalis. However, when exposed to F. schultzei or T. urticae damaged plants, F. occidentalis was more attracted towards damaged plants. A quantitative relationship was also apparent, F. schultzei showed increased attraction to damaged seedlings as the density of T. urticae or F. schultzei increased. In contrast, although F. occidentalis demonstrated increased attraction to plants damaged by higher densities of T. urticae, there was a negative relationship between attraction and the density of damaging conspecifics. Both species showed greater attraction to T. urticae damaged seedlings than to seedlings damaged by conspecifics. Results demonstrate that the responses of both species of thrips were context dependent, making generalizations difficult to formulate.
doi:10.1371/journal.pone.0063611
PMCID: PMC3653804  PMID: 23691075
25.  Jasmonic Acid-Induced Changes in Brassica oleracea Affect Oviposition Preference of Two Specialist Herbivores 
Journal of Chemical Ecology  2007;33(4):655-668.
Jasmonic acid (JA) is a key hormone involved in plant defense responses. The effect of JA treatment of cabbage plants on their acceptability for oviposition by two species of cabbage white butterflies, Pieris rapae and P. brassicae, was investigated. Both butterfly species laid fewer eggs on leaves of JA-treated plants compared to control plants. We show that this is due to processes in the plant after JA treatment rather than an effect of JA itself. The oviposition preference for control plants is adaptive, as development time from larval hatch until pupation of P. rapae caterpillars was longer on JA-treated plants. Total glucosinolate content in leaf surface extracts was similar for control and treated plants; however, two of the five glucosinolates were present in lower amounts in leaf surface extracts of JA-treated plants. When the butterflies were offered a choice between the purified glucosinolate fraction isolated from leaf surface extracts of JA-treated plants and that from control plants, they did not discriminate. Changes in leaf surface glucosinolate profile, therefore, do not seem to explain the change in oviposition preference of the butterflies after JA treatment, suggesting that as yet unknown infochemicals are involved.
doi:10.1007/s10886-006-9245-2
PMCID: PMC1915630  PMID: 17334923
Host plant selection; Glucosinolates; Pieris rapae; Pieris brassicae; Cabbage; Performance; Octadecanoid pathway

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