Thrips Settling, Oviposition and IYSV Distribution on Onion Foliage.

Thrips tabaci Lindeman (Thysanoptera: Thripidae) adult and larval settling and oviposition on onion (Allium cepa L.) foliage were investigated in relation to leaf position and leaf length at prebulb plant growth stages under controlled conditions. In the laboratory, four and six adult females of T. tabaci were released on onion plants at three-leaf stage and six- to eight-leaf stage, respectively, and thrips egg, nymph, and adult count data were collected on each of the three inner most leaves at every 2-cm leaf segment. Thrips settling and oviposition parameters were quantified during the light period on the above ground portion of onion plants from the distal end of the bulb or leaf sheath "neck" through the tips of the foliage. Results from studies confirmed that distribution of thrips adults, nymphs, and eggs were skewed toward the base of the plant. The settling distributions of thrips adults and nymphs differed slightly from the egg distribution in that oviposition occurred all the way to the tip of the leaf while adults and nymphs were typically not observed near the tip. In a field study, the foliage was divided into three equal partitions, i.e., top, middle, basal thirds, and thrips adults by species, primarily Frankliniella fusca (Hinds) and T. tabaci, were collected from each partition to determine if there was a similar bias of all adult thrips toward the base of the plant. The results suggested that adults of different species appear to segregate along leaf length. Finally, thrips oviposition on 2-cm segments and Iris yellow spot virus positive leaf segments were quantified in the field, irrespective of thrips species. Both variables demonstrated a very similar pattern of bias toward the base of the plant and were significantly correlated.

Evaluation of Wild Peanut Species and Their Allotetraploids for Resistance against Thrips and Thrips-Transmitted Tomato Spotted Wilt Orthotospovirus (TSWV).

Thrips-transmitted tomato spotted wilt orthotospovirus (TSWV) causes spotted wilt disease in peanut (Arachis hypogaea L.) and limits yield. Breeding programs have been developing TSWV-resistant cultivars, but availability of sources of resistance against TSWV in cultivated germplasm is extremely limited. Diploid wild Arachis species can serve as important sources of resistance, and despite ploidy barriers (cultivated peanut is tetraploid), their usage in breeding programs is now possible because of the knowledge and development of induced interspecific allotetraploid hybrids. This study screened 10 wild diploid Arachis and six induced allotetraploid genotypes via thrips-mediated TSWV transmission assays and thrips' feeding assays in the greenhouse. Three parameters were evaluated: percent TSWV infection, virus accumulation, and temporal severity of thrips feeding injury. Results indicated that the diploid A. stenosperma accession V10309 and its derivative-induced allotetraploid ValSten1 had the lowest TSWV infection incidences among the evaluated genotypes. Allotetraploid BatDur1 had the lowest thrips-inflicted damage at each week post thrips release, while diploid A. batizocoi accession K9484 and A. duranensis accession V14167 had reduced feeding damage one week post thrips release, and diploids A. valida accession GK30011 and A. batizocoi had reduced feeding damage three weeks post thrips releasethan the others. Overall, plausible TSWV resistance in diploid species and their allotetraploid hybrids was characterized by reduced percent TSWV infection, virus accumulation, and feeding severity. Furthermore, a few diploids and tetraploid hybrids displayed antibiosis against thrips. These results document evidence for resistance against TSWV and thrips in wild diploid Arachis species and peanut-compatible-induced allotetraploids.

Standardized Field Trials in Cotton and Bioassays to Evaluate Resistance of Tobacco Thrips (Thysanoptera: Thripidae) to Insecticides in the Southern United States.

Foliar-applied insecticide treatments may be necessary to manage thrips in cotton (Gossypium hirsutum L.) under severe infestations or when at-planting insecticide seed treatments do not provide satisfactory protection. The most common foliar-applied insecticide is acephate. Field observations in Tennessee suggest that the performance of acephate has declined. Thus, the first objective was to perform leaf-dip bioassays to assess if tobacco thrips, Frankliniella fusca (Hinds) (Thysanoptera: Thripidae), in cotton production regions have evolved resistance to foliar-applied insecticides. A second objective was to assess the performance of commonly applied foliar insecticides for managing thrips in standardized field trials in Arkansas, Tennessee, Mississippi, and Texas. For both objectives, several insecticides were evaluated including acephate, dicrotophos, dimethoate, lambda-cyhalothrin, imidacloprid, and spinetoram. Field trials and bioassays were completed from 2018 to 2021. Dose-response bioassays with acephate were performed on tobacco thrips field populations and a susceptible laboratory population. Bioassay results suggest that tobacco thrips have developed resistance to acephate and other organophosphate insecticides; however, this resistance seems to be most severe in Arkansas, Tennessee, and the Delta region of Mississippi. Resistance to other classes of insecticides were perhaps even more evident in these bioassays. The performance of these insecticides in field trials was variable, with tobacco thrips only showing consistent signs of resistance to lambda-cyhalothrin. However, it is evident that many populations of tobacco thrips are resistant to multiple classes of insecticides. Further research is needed to determine heritability and resistance mechanism(s).

Virulence of Entomopathogenic Nematodes to Pupae of Frankliniella fusca (Thysanoptera: Thripidae).

Tobacco thrips, Frankliniella fusca (Hinds) is an economically significant pest. Entomopathogenic nematodes (EPNs) have shown promise as biocontrol agents against certain thrips species, but they have not been explored for suppression of F. fusca. We investigated the potential of EPNs to manage F. fusca by conducting three different bioassays: 1) a small cup dose-response bioassay (25, 50, and 100 IJs cm-2) with four EPN species, 2) a broad virulence bioassay with eight EPN species at 100 IJs cm-2, and 3) a potted soil bioassay testing with four EPN species (100 IJs cm-2). In the dose-response bioassay, all treatments showed relatively lower adult emergence when compared with the control group, but the minimum adult emergence (30%) was observed at 7 d post-treatment when Heterorhabditis bacteriophora (FL1-1) was applied at the highest rate (100 IJs cm-2). In the broad virulence study, all EPN treatments caused significant reductions in F. fusca adult emergence (18.3-75.0%) in comparison with the control. H. bacteriophora (Fl1-1) was more virulent than other nematode treatments but statistically not different from Steinernema feltiae and Steinernema riobrave, while Steinernema rarum was the least virulent. In the potted soil bioassay, the lowest emergence (10.6%) was observed in H. bacteriophora (Fl1-1) treatment, followed by S. feltiae (SN), S. riobrave (355), and Heterorhabditis indica (HOM1) treatments. These results indicate that EPNs have the ability to suppress the soil dwelling stage of F. fusca and should be explored further under greenhouse and field conditions for biocontrol potential within an integrated pest management (IPM) context.

Impact of Host Resistance to Tomato Spotted Wilt Orthotospovirus in Peanut Cultivars on Virus Population Genetics and Thrips Fitness.

Thrips-transmitted tomato spotted wilt orthotospovirus (TSWV) is a major constraint to peanut production in the southeastern United States. Peanut cultivars with resistance to TSWV have been widely used for over twenty years. Intensive usage of resistant cultivars has raised concerns about possible selection pressure against TSWV and a likelihood of resistance breakdown. Population genetics of TSWV isolates collected from cultivars with varying levels of TSWV resistance was investigated using five TSWV genes. Phylogenetic trees of genes did not indicate host resistance-based clustering of TSWV isolates. Genetic variation in TSWV isolates and neutrality tests suggested recent population expansion. Mutation and purifying selection seem to be the major forces driving TSWV evolution. Positive selection was found in N and RdRp genes but was not influenced by TSWV resistance. Population differentiation occurred between isolates collected from 1998 and 2010 and from 2016 to 2019 but not between isolates from susceptible and resistant cultivars. Evaluated TSWV-resistant cultivars differed, albeit not substantially, in their susceptibility to thrips. Thrips oviposition was reduced, and development was delayed in some cultivars. Overall, no evidence was found to support exertion of selection pressure on TSWV by host resistance in peanut cultivars, and some cultivars differentially affected thrips fitness than others.

Novel mechanism of thrips suppression by Cry51Aa2.834_16 Bt toxin expressed in cotton.

BACKGROUND: Genetically engineered (GE) crops that express insecticidal traits have improved the sustainability of insect pest management worldwide, but many important pest orders are not controlled by commercially available toxins. Development of the first transgenic thysanopteran- and hemipteran-active Bacillus thuringiensis (Bt) Cry51Aa2.834_16 toxin expressed in MON 88702 cotton will significantly expand the diversity of pests controlled in the crop. Here, we examined MON 88702 cotton activity against two thrips species within the same genera, Frankliniella fusca and Frankliniella occidentalis. We used a multi-component cotton tissue assay approach to understand effects on adult longevity, fecundity, and larval development. RESULTS: We found that in no-choice assays, cotton plants expressing MON 88702 suppress oviposition, when compared to a non-Bt cotton. MON 88702 did not kill a large proportion of F. fusca larvae or adults but killed most F. occidentalis larvae. Time series experiments with F. occidentalis larvae documented significant developmental lags for MON 88702 exposed individuals. We also found that female thrips preferred to oviposit on non-Bt cotton when provided a choice. CONCLUSION: Together these results describe the activity of MON 88702 against thrips. They document clear differences in toxin performance between different thrips species and throughout the insects' life cycle. Most importantly, we show that MON 88702 was associated with reduced oviposition via behavioral avoidance to the toxin. This is a novel mechanism of action for pest control for a Bt crop plant. Together, these results provide a basis to describe the mechanism of population control for MON 88702 cotton. © 2019 Society of Chemical Industry.

Cotton thrips infestation predictor: a practical tool for predicting tobacco thrips (Frankliniella fusca) infestation of cotton seedlings in the south-eastern United States.

BACKGROUND: Thrips (order Thysanoptera) infestations of cotton seedlings result in plant injury, increasing the detrimental consequences of other challenges to production agriculture, such as abiotic stress or infestation by other pests. Using Frankliniella fusca as a thrips species of focus, we empirically developed a composite model of thrips phenology and cotton seedling susceptibility to predict site-specific infestation risk so that monitoring and other resources can be allocated efficiently, to optimize the timing of thrips control measures to maximize effectiveness, and to inform stakeholders about the dynamics of thrips infestation and cotton seedling injury at a time when thrips are evolving resistance to commonly-used pesticides. RESULTS: A mixture distribution model of thrips infestation potential, fit to data describing F. fusca adult dispersal in time, proved best for predicting infestations of F. fusca on cotton seedlings. Thrips generations occurring each year as a function of weather are represented as a probability distribution. A model of cotton seedling growth was also developed to predict susceptibility as a function of weather. Combining these two models resulted in a model of seedling injury, which was validated and developed for implementation as a software tool. CONCLUSIONS: Experimental validation of the implemented model demonstrated the utility of its output in predicting infestation risk. Successful implementation and use of the software tool derived from this model was enabled by close cooperation with university extension personnel, agricultural consultants, and growers, underscoring the importance of stakeholder and expert input to the success of applied analytical research. © 2020 Society of Chemical Industry.

Specific and Spillover Effects on Vectors Following Infection of Two RNA Viruses in Pepper Plants.

Mixed infection of plant viruses is ubiquitous in nature and can affect virus-plant-vector interactions differently than single virus infection. While several studies have examined virus-virus interactions involving mixed virus infection, relatively few have examined effects of mixed virus infection on vector preference and fitness, especially when multiple vectors are involved. This study explored how single and mixed viral infection of a non-persistently transmitted cucumber mosaic virus (CMV) and propagative and persistently-transmitted tomato spotted wilt orthotospovirus (TSWV) in pepper, Capsicum annum L., influenced the preference and fitness of their vectors, the green peach aphid, Myzus persicae (Sulzer), and the tobacco thrips, Frankliniella fusca (Hinds), respectively. In general, mixed infected plants exhibited severe symptoms compared with individually infected plants. An antagonistic interaction between the two viruses was observed when CMV titer was reduced following mixed infection with TSWV in comparison with the single infection. TSWV titer did not differ between single and mixed infection. Myzus persicae settling preference and median developmental were not significantly different between CMV and/or TSWV-infected and non-infected plants. Moreover, M. persicae fecundity did not differ between CMV-infected and non-infected pepper plants. However, M. persicae fecundity was substantially greater on TSWV-infected plants than non-infected plants. Myzus persicae fecundity on mixed-infected plants was significantly lower than on singly-infected and non-infected plants. Frankliniella fusca fecundity was higher on CMV and/or TSWV-infected pepper plants than non-infected pepper plants. Furthermore, F. fusca-induced feeding damage was higher on TSWV-infected than on CMV-infected, mixed-infected, or non-infected pepper plants. Overall, our results indicate that the effects of mixed virus infection on vectors were not different from those observed following single virus infection. Virus-induced host phenotype-modulated effects were realized on both specific and non-specific vectors, suggesting crosstalk involving all vectors and viruses in this pathosystem. The driving forces of these interactions need to be further examined. The effects of interactions between two viruses and two vectors towards epidemics of one or both viruses also need to be examined.

Effects of Planting Date on Thrips (Thysanoptera: Thripidae) in Cotton.

At-plant applications of insecticides are the most common method to manage thrips in upland cotton, Gossypium hirstutum L. Because the primary pest species, tobacco thrips, Frankliniella fusca (Hinds), has developed resistance to commonly used neonicotinoid insecticides used in producing cotton, alternative control options are needed for sustainable thrips management programs. A 3-year study (2015-2017) showed that densities of thrips, feeding injury from thrips, cotton growth, and yield varied among 10 planting dates. Densities of thrips were lowest in seedling cotton planted after mid-May in all years. Thrips injury ratings in all years were highest in cotton planted in April, lowest in cotton planted in June, and below intermediate injury (intermediate corresponded to a 3 on the 0-5 scale) levels in cotton planted after mid-May. Cotton planted during May, rather than in April or June, had the highest yield potential, regardless of variety. Results of the study indicated that altering planting date could potentially be useful in mitigating injury and losses from thrips in upland cotton.

Resistance to Thrips in Peanut and Implications for Management of Thrips and Thrips-Transmitted Orthotospoviruses in Peanut.

Thrips are major pests of peanut (Arachis hypogaea L.) worldwide, and they serve as vectors of devastating orthotospoviruses such as Tomato spotted wilt virus (TSWV) and Groundnut bud necrosis virus (GBNV). A tremendous effort has been devoted to developing peanut cultivars with resistance to orthotospoviruses. Consequently, cultivars with moderate field resistance to viruses exist, but not much is known about host resistance to thrips. Integrating host plant resistance to thrips in peanut could suppress thrips feeding damage and reduce virus transmission, will decrease insecticide usage, and enhance sustainability in the production system. This review focuses on details of thrips resistance in peanut and identifies future directions for incorporating thrips resistance in peanut cultivars. Research on thrips-host interactions in peanut is predominantly limited to field evaluations of feeding damage, though, laboratory studies have revealed that peanut cultivars could differentially affect thrips feeding and thrips biology. Many runner type cultivars, field resistant to TSWV, representing diverse pedigrees evaluated against thrips in the greenhouse revealed that thrips preferred some cultivars over others, suggesting that antixenosis "non-preference" could contribute to thrips resistance in peanut. In other crops, morphological traits such as leaf architecture and waxiness and spectral reflectance have been associated with thrips non-preference. It is not clear if foliar morphological traits in peanut are associated with reduced preference or non-preference of thrips and need to be evaluated. Besides thrips non-preference, thrips larval survival to adulthood and median developmental time were negatively affected in some peanut cultivars and in a diploid peanut species Arachis diogoi (Hoehne) and its hybrids with a Virginia type cultivar, indicating that antibiosis (negative effects on biology) could also be a factor influencing thrips resistance in peanut. Available field resistance to orthotospoviruses in peanut is not complete, and cultivars can suffer substantial yield loss under high thrips and virus pressure. Integrating thrips resistance with available virus resistance would be ideal to limit losses. A discussion of modern technologies such as transgenic resistance, marker assisted selection and RNA interference, and future directions that could be undertaken to integrate resistance to thrips and to orthotospoviruses in peanut cultivars is included in this article.

Within-Plant Distribution and Dynamics of Thrips Species (Thysanoptera: Thripidae) in Cotton.

A 2-yr study in cotton (Gossypium hirsutum L.) was conducted to determine the abundance and species composition of thrips (Thysanoptera: Thripidae) on different plant parts throughout the season in Alabama, Georgia, North Carolina, South Carolina, and Virginia. Plant parts sampled included seedlings, terminals with two expanded leaves, leaves from the upper, middle, and lower sections of the canopy, white flowers, and medium-sized bolls. Adult thrips were significantly more abundant on seedlings and flowers in 2014, and on flowers followed by seedlings and leaves from the middle canopy in 2015. Immature thrips were significantly more abundant on seedlings, followed by flowers in 2014, and on seedlings followed by leaves from the lower canopy and flowers in 2015. Across locations and plant parts, thrips consisted of Frankliniella tritici (Fitch) (46.8%), Frankliniella fusca Hinds (23.5%), Frankliniella occidentalis (Pergande) (17.1%), Neohydatothrips variabilis (Beach) (7.4%), Thrips tabaci (Lindeman) (1.8%), and other species (3.4%). Frankliniella fusca represented 86.7% of all thrips on seedlings, while F. tritici was more abundant on terminals (51.6%), squares (57.5%), and flowers (75.1%). Across all leaf positions, F. fusca was the most abundant species (28.8%), followed by F. tritici (19.2%), N. variabilis (18.8%), F. occidentalis (12.9%), and T. tabaci (5.2%), as well as other species (15.0%). As neonicotinoid insecticides remain a primary tool to manage seedling infestations of F. fusca, our data indicate that mid- to late-season applications of neonicotinoid insecticides targeting other insect pests will intensify selection pressure for resistance on F. fusca, the primary pest of seedling cotton.

Three decades of managing Tomato spotted wilt virus in peanut in southeastern United States.

Southeastern states namely Georgia, Florida, and Alabama produce two-thirds of the peanuts in the United States. Thrips-transmitted Tomato spotted wilt virus (TSWV), which causes spotted wilt disease, has been a major impediment to peanut production for the past three decades. The cultivars grown in the 1980s were extremely susceptible to TSWV. Early yield losses extended to tens of millions of dollars each year (up to 100% loss in many fields). This situation led to the creation of an interdisciplinary team known as "SWAT: Spotted Wilt Action Team". Initial efforts focused on risk mitigation using a combination of chemical and cultural management practices along with a strong investment in breeding programs. Beginning in the mid 1990s, cultivars with field resistance were developed and integrated with cultural and chemical management options. A Risk Mitigation Index (Peanut Rx) was made available to growers to assess risks, and provide options for mitigating risks such as planting field resistant cultivars with in-furrow insecticides, planting after peak thrips incidence, planting in twin rows, and increasing seeding rates. These efforts helped curtail losses due to spotted wilt. The Peanut Rx continues to be refined every year based on new research findings. Breeding efforts, predominantly in Georgia and Florida, continue to develop cultivars with incremental field resistance. The present-day cultivars (third-generation TSWV-resistant cultivars released after 2010) possess substantially greater field resistance than second-generation (cultivars released from 2000 to 2010) and first-generation (cultivars released from 1994 to 2000) TSWV resistant cultivars. Despite increased field resistance, these cultivars are not immune to TSWV and succumb under high thrips and TSWV pressure. Therefore, field resistant cultivars cannot serve as a 'stand-alone' option and have to be integrated with other management options. The mechanism of resistance is also unknown in field resistant cultivars. Recent research in our laboratory evaluated field resistant cultivars against thrips and TSWV. Results revealed that some resistant cultivars suppressed thrips feeding and development, and they accumulated fewer viral copies than susceptible cultivars. Transcriptomes developed with the aid of Next Generation Sequencing revealed differential gene expression patterns following TSWV infection in susceptible than field resistant cultivars. Results revealed that the upregulation of transcripts pertaining to constitutive and induced plant defense proteins in TSWV resistant cultivars was more robust over susceptible cultivars. On the flipside, the long-term effects of using such resistant cultivars on TSWV were assessed by virus population genetics studies. Initial results suggest lack of positive selection pressure on TSWV, and that the sustainable use of resistant cultivars is not threatened. Follow up research is being conducted. Improvements in TSWV management have enhanced sustainability and contributed to increased yields from <2800kg/ha before 1995 to ∼5000kg/ha in 2015.

The Tomato Spotted Wilt Virus Genome Is Processed Differentially in its Plant Host Arachis hypogaea and its Thrips Vector Frankliniella fusca.

Thrips-transmitted tospoviruses are economically important viruses affecting a wide range of field and horticultural crops worldwide. Tomato spotted wilt virus (TSWV) is the type member of the Tospovirus genus with a broad host range of more than 900 plant species. Interactions between these viruses and their plant hosts and insect vectors via RNAi pathways are likely a key determinant of pathogenicity. The current investigation, for the first time, compares biogenesis of small RNAs between the plant host and insect vector in the presence or absence of TSWV. Unique viral small interfering RNA (vsiRNA) profiles are evident for Arachis hypogaea (peanut) and Frankliniella fusca (thrips vector) following infection with TSWV. Differences between vsiRNA profiles for these plant and insect species, such as the relative abundance of 21 and 22 nt vsiRNAs and locations of alignment hotspots, reflect the diverse siRNA biosynthesis pathways of their respective kingdoms. The presence of unique vsiRNAs in F. fusca samples indicates that vsiRNA generation takes place within the thrips, and not solely through uptake via feeding on vsiRNAs produced in infected A. hypogaea. The study also shows key vsiRNA profile differences for TSWV among plant families, which are evident in the case of A. hypogaea, a legume, and members of Solanaceae (S. lycopersicum and Nicotiana benthamiana). Distinctively, overall small RNA (sRNA) biogenesis in A. hypogaea is markedly affected with an absence of the 24 nt sRNAs in TSWV-infected plants, possibly leading to wide-spread molecular and phenotypic perturbations specific to this species. These findings add significant information on the host-virus-vector interaction in terms of RNAi pathways and may lead to better crop and vector specific control strategies.

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.

Thripenema fuscum n. sp. (Tylenchida: Allantonematidae), a Parasite of the Tobacco Thrips, Frankliniella fusca (Thysanoptera).

Thripenema fuscum n. sp., a parasite of the tobacco thrips, Frankliniella fusca, is described and illustrated from material collected from peanut (Arachis hypogaea) in Marianna, Florida. Thripenema fuscura can be distinguished from all other previously described Thripenema spp. by the dorsal curvature of the male and the presence of a stylet in the male. Highest parasitism rates of F. fusca by T. fuscum in peanuts were 51% in 1995 and 68% in 1996.