Invasion Biology, Ecology, and Management of Western Flower Thrips.

Western flower thrips, Frankliniella occidentalis, first arose as an important invasive pest of many crops during the 1970s-1980s. The tremendous growth in international agricultural trade that developed then fostered the invasiveness of western flower thrips. We examine current knowledge regarding the biology of western flower thrips, with an emphasis on characteristics that contribute to its invasiveness and pest status. Efforts to control this pest and the tospoviruses that it vectors with intensive insecticide applications have been unsuccessful and have created significant problems because of the development of resistance to numerous insecticides and associated outbreaks of secondary pests. We synthesize information on effective integrated management approaches for western flower thrips that have developed through research on its biology, behavior, and ecology. We further highlight emerging topics regarding the species status of western flower thrips, as well as its genetics, biology, and ecology that facilitate its use as a model study organism and will guide development of appropriate management practices.

Natural Enemies of the Frankliniella Complex Species (Thysanoptera: Thripidae) in Ataulfo Mango Agroecosystems.

A field survey was conducted in Ataulfo mango (Mangifera indica L.) orchards in Chiapas, Mexico, with the objective of determining the natural enemies of the Frankliniella complex species (Thysanoptera: Thripidae). Seven species of this genus feed and reproduce in large numbers during the mango flowering. Two representative orchards were selected: the orchard "Tres A" characterized by an intensive use of agrochemicals directed against thrips, and the orchard "La Escondida" that did not spray insecticides. During mango flowering, five inflorescences were randomly collected every 5 d in both orchards, for a total of 18 sampling dates. Results revealed the presence of 18 species of arthropods that were found predating on Frankliniella. There were 11 species in the families Aeolothripidae, Phlaeothripidae, Formicidae, Anthocoridae and Chrysopidae; and seven species of spiders in the families Araneidae, Tetragnathidae, and Uloboridae. Over 88% of predators were anthocorids, including, Paratriphleps sp. (Champion), Orius insidiosus (Say), Orius tristicolor (White), and O. perpunctatus (Reuter). The orchard that did not spray insecticides had a significantly higher number of predators suggesting a negative effect of the insecticides on the abundance of these organisms.

The α6 nicotinic acetylcholine receptor subunit of Frankliniella occidentalis is not involved in resistance to spinosad.

Insects evolve resistance which constrains the sustainable use of insecticides. Spinosyns, a class of environmentally-friendly macrolide insecticides, is not an exception. The mode of inheritance and the mechanisms of resistance to spinosad (the most common spinosyn insecticide) in Frankliniella occidentalis (Western flower thrips, WFT) were investigated in this study. Resistance (170,000-fold) was autosomal and completely recessive. Recent studies showed that deletion of the nicotinic acetylcholine receptor α6 subunit gene resulted in strains of Drosophila melanogaster, Plutella xylostella and Bactrocera dorsalis that are resistant to spinosad, indicating that nAChRα6 subunit maybe important for the toxic action of this insecticide. Conversely, a G275E mutation of this subunit in F. occidentalis was recently proposed as the mechanism of resistance to spinosad. We cloned and characterized nAChRα6 from three susceptible and two spinosad resistant strains from China and the USA. The Foα6 cDNA is 1873bp and the open reading frame is 1458bp which encodes 485 amino acid residues with a predicted molecular weight of 53.5-kDa, the 5' and 3' UTRs are 121 and 294bp, respectively. There was no difference in the cDNA sequence between the resistant and susceptible thrips, suggesting the G275E mutation does not confer resistance in these populations. Ten isoforms of Foα6, arising from alternative splicing, were isolated and did not differ between the spinosad-susceptible and resistant strains. Quantitative real time PCR analysis showed Foα6 was highly expressed in the first instar larva, pupa and adult, and the expression levels were 3.67, 2.47, 1.38 times that of the second instar larva. The expression level was not significantly different between the susceptible and resistant strains. These results indicate that Foα6 is not involved in resistance to spinosad in F. occidentalis from China and the USA.

Characterization of Frankliniella occidentalis and Frankliniella bispinosa (Thysanoptera: Thripidae) Injury to Strawberry.

Frankliniella flower thrips are pests of numerous fruit and vegetable crops as they feed and reproduce in the flowers and fruits. The invasive Frankliniella occidentalis (Pergande) from the Southwestern United States, an economic pest in Florida since 2005, and the native Frankliniella bispinosa Morgan are both found in Florida strawberries. The objective of this research was to characterize injury to strawberry fruit from these species. Densities of 0, 2, 4, 8, 16, or 32 adult females of each species were caged on a strawberry plant with one flower. The cages were removed after 2, 5, or 10 d, and the number of surviving adults and the number of larvae determined. Injury was quantified on the mature fruit 21 d after thrips were introduced onto the experimental plant. Initial densities as low as two adult F. occidentalis females per flower decreased fruit set and increased cat-facing on the fruits that developed. There were no significant effects on fruit set and cat-facing by any initial density of F. bispinosa. Feeding by thrips on the small, green fruit affected the size and shape of the mature fruit: the diameters were decreased as a linear function of increased feeding by F. bispinosa, and the weights were decreased as a linear function of increased feeding by F. occidentalis. Overall, results showed that F. occidentalis was more damaging to strawberry than F. bispinosa. The differences in pest status between these common flower thrips species in Florida presents challenges to management programs.

Population abundance of Frankliniella occidentalis (Thysanoptera: Thripidae) and natural enemies on plant hosts in central Chile.

Populations of the invasive Frankliniella occidentalis (Pergande) are serious pests of agricultural crops in the Aconcagua Valley of central Chile. An extensive survey was conducted of 55 plant species in 24 families to identify plant hosts of F. occidentalis and to determine its relative abundance on each host during each season. A more intensive study was conducted on selected plant species serving as reproductive hosts to determine the population dynamics of F. occidentalis and to evaluate the potential importance of Orius species and other natural enemies for controlling F. occidentalis. Adults of F. occidentalis were active during each season of the year inhabiting the flowers of 91% of the sampled plant species in 22 families, and 86% of these plant species in 19 families served as reproductive hosts. The number of host plant species used was greatest in the spring and least in the winter. All of the hosts except Medicago sativa L. were used only when flowering. Populations of F. occidentalis were significantly aggregated in M. sativa in the terminal buds over the leaves when the host was not flowering, and in the flowers, followed by the terminal buds, followed by the leaves when the host was flowering. Larvae were 1.3-2.3 times more abundant on dates when M. sativa was flowering. There were no identifiable patterns in plant hosts based on endemicity or plant family. Most of the plant species used by F. occidentalis were inferior quality hosts where populations either declined or were stable. Populations of F. occidentalis on low-quality hosts generally escaped predation by Orius species and competition by other species of thrips. Only 25% of the food hosts and 28% of the reproductive hosts for F. occidentalis in the extensive survey, respectively, were host plants for Orius. Parasitoids and other predators were not found to be important in suppressing thrips on any of the plant hosts. Populations of F. occidentalis increased on only a few hosts, including M. sativa and Sisymbrium officinale L. Scop. These apparently are major sources of F. occidentalis adults invading crops. We conclude that F. occidentalis is established in central Chile and that it has replaced and possibly displaced the native Frankliniella australis (Morgan) as the most common thrips species.

Population dynamics and within-plant distribution of Frankliniella spp. thrips (Thysanoptera: Thripidae) in cotton.

Thrips cause damage to seedling cotton, and they are associated with the spread of Fusarium hardlock, a serious disease affecting cotton bolls that reduces lint yield in the southern United States. The population dynamics and within-plant distribution of Frankliniella spp. thrips in cotton were determined in 2005, 2006, and 2007 in Quincy and in 2006 and 2007 in Marianna, FL. Frankliniella tritici (Fitch) was >98% of the adult thrips collected. The adults of F. bispinosa (Morgan), F. occidentalis (Pergande), and F. fusca (Hinds) also were collected. Populations of F. fusca inhabited the cotton leaves of vegetative-stage cotton. The other species were highly anthophilic, primarily inhabiting cotton during its reproductive growth stages. Densities of these species peaked during mid-season, which also coincided with peak bloom. The adult F. tritici and the thrips larvae were aggregated in the flowers over the other plant parts, with more collected in the upper than the lower canopies. These patterns of aggregation were observed at each location each year, and the numerical differences usually were significant (P < 0.05). Densities of adult F. tritici were low on the leaves, squares, and bolls. The population dynamics and with-plant distribution of individual thrips species has not previously been determined for cotton in the southern United States.

Flower-inhabiting Frankliniella Thrips (Thysanoptera: Thripidae), pesticides, and Fusarium hardlock in cotton.

Cotton hardlock caused by Fusarium verticillioides (Sacc. Nirenberg) can reduce cotton, Gossypium hirsutum L., yields > 70% in the southeastern United States. The spores infect flowers on the day of pollination, resulting in hardlock, which is the failure of the fiber to fluff as the boll opens at maturity. Frankliniella spp. Thrips (Thysanoptera: Thripidae) inhabiting the flowers are hypothesized to increase hardlock by spreading the conidia or by creating entranceways for the germinating Fusarium conidia. Experiments were conducted at Marianna and Quincy in Florida in 2006 and 2007 to determine whether there was a relationship between the number of adult and larval thrips inhabiting the flowers of cotton and the incidence of cotton hardlock. Frankliniella tritici (Fitch) was > 98% of the adult thrips in the samples at both locations each year. The adults of Frankliniella bispinosa (Morgan) and Frankliniella occidentalis (Pergande) also were collected. There were no significant regression relationships between weekly mean densities of thrips in the flowers and the incidence of cotton hardlock at harvest in any of the experiments. Additional experiments were conducted at each location in 2006 and 2007 to determine whether weekly applications during flowering of the insecticide lambda-cyhalothrin, the fungicide thiophanate methyl, and the combination of the two reduced the incidence of cotton hardlock at harvest. Applications of the insecticide significantly reduced the numbers of adult F. tritici, the number of thrips larvae, and the incidence of hardlock at harvest. Applications of the insecticide were as affective as applications of the insecticide plus fungicide. In one experiment, applications of the fungicide reduced the incidence of hardlock at harvest. Applications of the insecticide usually significantly increased the number of adult F. occidentalis. None of the pesticide treatments significantly affected the numbers of the key thrips predator Orius insidiosus (Say). We conclude that insecticidal control of the adults and larvae of F. tritici during flowering reduced the incidence of cotton hardlock. However, there were no significant regression relationships between the incidence of cotton hardlock at harvest and the number of thrips in the flowers.

Competitive exclusion of a worldwide invasive pest by a native. Quantifying competition between two phytophagous insects on two host plant species.

1. High competitive ability is believed to be an important characteristic of invasive species. Many animal studies have compared the competitive ability of invasive species with a native species that is being displaced, but few have looked at systems where an invasive species has failed to establish itself. These types of studies are important to determine if competition is relevant not only to invading species but also to the biotic resistance of a community. 2. The thrips species F. occidentalis is a highly invasive pest that has spread from its original range (the western states of the USA) to a worldwide distribution. Despite this, F. occidentalis is largely absent or occurs in low numbers in the eastern states of the USA, where the native F. tritici dominates. It is possible that F. tritici is competitively excluding F. occidentalis from this region. 3. Larval competition between these two thrips species was tested on two known plant hosts, Capsicum annuum (a crop plant), and Raphanus raphanistrum (an invasive weed), using a response surface design with number of larvae surviving as the response variable. The response surface design allowed competition models to be fit to data using maximum likelihood estimation, thus generating quantitative values for interspecific competition. 4. On both plant hosts, the native F. tritici did not experience significant interspecific competition from the invasive F. occidentalis. In contrast, F. occidentalis did experience significant interspecific competition from F. tritici. Competition from F. tritici larvae on F. occidentalis larvae was estimated to be 1.72 times (on C. annuum) and 1.76 times (on R. raphanistrum) the effect of intraspecific competition. The invasive F. occidentalis appears to be competitively excluded by the native F. tritici. 5. This study confirms the importance of competition in the biotic resistance of a community and is one of the few animal studies to not only test for competition in an apparently resistant ecosystem but also to quantify the level of interspecific competition between two animal species.

Evaluation of a Push-Pull System for the Management of Frankliniella Species (Thysanoptera: Thripidae) in Tomato.

A push-pull strategy for reducing populations of the thrips Frankliniella occidentalis (Pergande), F. bispinosa (Morgan) and F. tritici (Fitch) in tomato was evaluated. Push components consisted of ultraviolet (UV)-reflective mulch and foliar applications of kaolin and the pull component consisted of the companion plant Bidens alba (L.). Replicated field experiments were conducted in 2011 and 2012. Adult and larval thrips were reduced by UV-reflective mulch during early and mid-flowering of tomato. Spray applications of kaolin were effective in reducing adult and larval thrips during early, mid- and late-flowering. The pull effects of the B. alba companion plants were additive and sometimes interactive with the push effects of UV-reflective mulch and kaolin in reducing the adult males of each thrips species and the females of F. bispinosa. The strategy was not effective in reducing the adult females of F. tritici and F. occidentalis. In addition to attracting the Frankliniella species adults, the companion plants were hosts for the thrips predator Orius insidiosus (Say). The companion plants combined with UV-reflective mulch and kaolin proved effective as a push-pull system for suppressing flower thrips, including F. occidentalis which is a serious pest of tomato worldwide.

Biotic resistance limits the invasiveness of the western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae), in Florida.

The spread of the western flower thrips, Frankliniella occidentalis (Pergande), has resulted in the world-wide destabilization of established integrated pest management programs for many crops. It is hypothesized that frequent exposure to insecticides in intensive agriculture selected for resistant populations, which allowed invasive populations in the eastern USA to overcome biotic resistance from the native community of species. Research conducted in Florida to understand the role of biotic factors in limiting the abundance of the western flower thrips is reviewed. Orius spp. (Hemiptera: Anthocoridae) are effective predators that suppress populations of thrips on crop and non-crop hosts in southern and northern Florida. Orius are more effective predators of the western flower thrips than the native flower thrips, F. tritici (Fitch) and F. bispinosa (Morgan). The native species are competitors of the western flower thrips. Excessive fertilization and the use of broad-spectrum insecticides in crop fields further enhances populations of the western flower thrips. Interactions with native species clearly limit the abundance of western flower thrips in Florida, but populations are abundant in fertilized crop fields where application of insecticides excludes predators and competitor species.

Host-Parasite Biology of Thripinema fuscum (Tylenchida: Allantonematidae) and Frankliniella fusca (Thysanoptera: Thripidae).

Thripinema fuscum is a natural enemy of Frankliniella fusca in peanut. Laboratory experiments were conducted to determine the reproductive biology of T. fuscum as affected by gender and stage of development of the host and to determine the effects of parasitism on host longevity, fecundity, and mortality. The adult females of F. fusca were the most readily parasitized (P < 0.001) in the laboratory experiments followed by the second instars, the first instars, and the adult males. One generation of T. fuscum developed within the parasitized larvae and adults, with the males and females emerging only during the adult stage of the host. Parasitism did not cause mortality of the host. Parasitism affected male longevity (P < 0.001) but not female longevity. The adult female thrips that were parasitized as first or second instars did not lay eggs, and the adult females stopped laying eggs within 3 days of being parasitized. The female-to-male sex ratio of T. fuscum emerging from parasitized male and female F. fusca was 22 and 18 to 1, respectively. More T. fuscum emerged from female hosts than from male hosts (P < 0.001). More emerged from hosts parasitized as larvae compared with hosts parasitized as adults (P < 0.05). The intrinsic capacity of increase of T. fuscum ranged between 0.29 and 0.37 when parasitizing the adult males and females and between 0.18 and 0.21 when parasitizing the larval males and females. Percent parasitism of F. fusca was estimated in peanut fields. The flowers were the primary site for aggregation of the adults of F. fusca and for the free-living females of T. fuscum to parasitize new hosts. As under laboratory conditions, field parasitism of adult males was less than parasitism of adult females in 2001 and 2002 (P < 0.01 and 0.001, respectively). Our study indicates that T. fuscum is a potential biological control agent capable of suppressing F. fusca populations in peanut.

Population Dynamics of Frankliniella bispinosa (Thysanoptera: Thripidae) and the Predator Orius insidiosus (Hemiptera: Anthocoridae) as Influenced by Flower Color of Lagerstroemia (Lythraceae).

Crapemyrtle is a common landscape planting that is a resource subsidy for beneficial insects. Field studies were conducted to determine the influence of crapemyrtle flower color on the population abundances and predator-prey dynamics of the herbivorous Frankliniella species and the predator Orius insidiosus. Adults and immatures of predator and prey were highly anthophilous, preferring white 'Acoma' flowers compared with lavender 'Apalachee', red 'Carolina Beauty', and pink 'Choctaw'. The predator was aggregated with its prey in a density-dependent manner: the adults by preferring the crapemyrtle clones also preferred by the thrips and the nymphs by direct tracking or as a function of increased prey and fecundity. Acoma was best for preference and buildup of O. insidiosus populations, and it was the only clone where there was no buildup in thrips populations. Two species of Karnyothrips (Thysanoptera: Phlaoethripidae), predators of small insects, were common in Tillandsia usneoides, an epiphyte on the crapemyrtle. Crapemyrtle is a bridge to enhance populations of O. insidiosus during summer months when there are few other hosts in the southern USA.

The Scirtothrips dorsalis Species Complex: Endemism and Invasion in a Global Pest.

Invasive arthropods pose unique management challenges in various environments, the first of which is correct identification. This apparently mundane task is particularly difficult if multiple species are morphologically indistinguishable but accurate identification can be determined with DNA barcoding provided an adequate reference set is available. Scirtothrips dorsalis is a highly polyphagous plant pest with a rapidly expanding global distribution and this species, as currently recognized, may be comprised of cryptic species. Here we report the development of a comprehensive DNA barcode library for S. dorsalis and seven nuclear markers via next-generation sequencing for identification use within the complex. We also report the delimitation of nine cryptic species and two morphologically distinguishable species comprising the S. dorsalis species complex using histogram analysis of DNA barcodes, Bayesian phylogenetics, and the multi-species coalescent. One member of the complex, here designated the South Asia 1 cryptic species, is highly invasive, polyphagous, and likely the species implicated in tospovirus transmission. Two other species, South Asia 2, and East Asia 1 are also highly polyphagous and appear to be at an earlier stage of global invasion. The remaining members of the complex are regionally endemic, varying in their pest status and degree of polyphagy. In addition to patterns of invasion and endemism, our results provide a framework both for identifying members of the complex based on their DNA barcode, and for future species delimiting efforts.

Population dynamics of Frankliniella spp. and tomato spotted wilt incidence as influenced by cultural management tactics in tomato.

We investigated the effects of ultraviolet (UV)-reflective mulch and two rates of nitrogen fertilization on populations of Frankliniella spp. thrips and on the incidence of tomato spotted wilt in field-grown tomato in northern Florida. The higher of the two soil nitrogen fertilizer treatments significantly increased populations of Frankliniella occidentalis (Pergande), whereas mulch reflectance significantly decreased populations of F. occidentalis. Populations of Frankliniella tritici (Fitch) were decreased only by UV-reflective mulch. Decreased thrips populations in UV-reflective mulch plots were probably due to disruptions in host-finding behavior. Increased thrips populations in tomatoes treated with the higher nitrogen fertilization rate were probably due in part to increased nutrients available in flowers. Incidence of tomato spotted wilt was significantly decreased in tomatoes grown on UV-reflective mulch, whereas disease incidence was significantly greater in increased nitrogen-fertilized plots. This research reveals that cultural practices resulted in up to 45% reduction in the numbers of vector and nonvector species of flower thrips and up to 50% reduction in tomato spotted wilt.

Evaluation of a push-pull strategy for the management of Frankliniella bispinosa (Thysanoptera: Thripidae) in bell peppers.

A push-pull strategy for managing the anthophilous Frankliniella bispinosa (Morgan) in pepper and increasing conservation biological control was evaluated. Push components of ultraviolet (UV)-reflective mulch and foliar applications of kaolin and the pull component of sunflower companion plants were evaluated in replicated field experiments in 2011 and 2012. Adult F. bispinosa rapidly colonized and reproduced in the peppers and sunflowers during early flowering, but populations declined later, as numbers of the predatory Orius insidiosus (Say) and Orius pumilio (Champion) increased in both hosts. Numbers of F. bispinosa were reduced by kaolin during early pepper flowering. Thrips numbers were increased on some of the later sample dates, apparently due to reduced predation that resulted from negative effects of kaolin and UV-reflective mulch on Orius populations. Numbers of thrips increased in peppers with companion plants during the first week of flowering each year, followed by declines in thrips numbers during the next 2 wk in 2011. There was little effect each year of the companion plants on the numbers of Orius in the pepper flowers. There was one date in 2011 and no dates in 2012 in which UV-reflective mulch or kaolin acted in concert with the presence of the companion plants to reduce thrips numbers in the main crop of pepper. Yield effects were not attributed to thrips damage. We conclude that sunflower companion plants did not act additively or synergistically with kaolin or UV-reflective mulch to reduce thrips and increase Orius populations in pepper.

Frankliniella occidentalis (Pergande) integrated pest management programs for fruiting vegetables in Florida.

BACKGROUND: The spread of the western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), resulted in the worldwide destabilization of established integrated pest management programs for many crops. Efforts to control the pest and the thrips-vectored tospoviruses with calendar applications of broad-spectrum insecticides have been unsuccessful. The result has been a classic '3-R' situation: resistance to numerous insecticides; resurgence of the western flower thrips populations as a result of natural predators and native competitor thrips being eliminated; replacement by various other pests. This paper reports on integrated pest management programs for fruiting vegetables that are effective, economical, ecologically sound and sustainable. RESULTS: The components include the following: define pest status (economic thresholds); increase biotic resistance (natural enemies and competition); integrate preventive and therapeutic tactics (scouting, ultraviolet-reflective technologies, biological control, compatible insecticides, companion plants and fertility); vertically integrate the programs with other pests; continually communicate latest science-based management tactics with end-users. CONCLUSION: These programs have been widely implemented in Florida and have significantly improved the management of western flower thrips and thrips-transmitted viruses.