Stink bug rostrum length vs. stylet penetration potential

Stink bugs (Hemiptera: Pentatomidae) and related species continue to plague cotton, Gossypium hirsutum L. (Malvaceae), worldwide. Stink bugs utilize their stylets (housed within the rostrum) to feed upon cotton bolls and transmit pathogens that cause seed and boll rot of cotton. Stylet penetration potential of stink bugs is influenced by species and recent observations indicated a phenomenon whereby stink bugs with shorter rostra yielded deeper stylet penetration estimates. The objective of this study was to elucidate the relationship between rostrum length and known stylet penetration estimates for two pairs of similar‐sized pentatomid species: Chinavia hilaris (Say) vs. Euschistus servus (Say), and Oebalus pugnax (Fabricius) vs. Piezodorus guildinii Westwood. For each species, individual rostral segments were measured to yield total lengths, and measurements were compared against known stylet penetration estimates. Chinavia hilaris and P. guildinii have longer rostra than E. servus and O. pugnax, respectively, yet E. servus and O. pugnax yielded deeper stylet penetration estimates. Deeper stylet penetration by species with shorter rostra can be attributed to differences in the lengths of rostral segments 1 and 2. Euschistus servus and O. pugnax each had significantly longer rostral segments 1 and 2 than C. hilaris and P. guildinii, respectively. Also, the cumulative lengths of rostral segments 1 and 2 comprised a higher overall proportion of the entire rostrum length in E. servus and O. pugnax vs. C. hilaris and P. guildinii, respectively. Rostral segments 1 and 2 are instrumental in the feeding mechanics of these phytophagous species; it is clear that their greater length and their role in stylet penetration model calculations – including the lengths of segments 3 and 4 – override the presumption that total rostrum length equates to stylet penetration potential. This novel finding contributes to the general knowledge of stink bug feeding mechanics.     

Effect of deltamethrin-incorporated nets on mobility and survivorship of Halyomorpha halys (Hemiptera: Pentatomidae) adults and nymphs in the laboratory

The brown marmorated stink bug, Halyomorpha halys Stål (Hemiptera: Pentatomidae), is an invasive pest that attacks specialty and row crops in North America and Europe. There has been a concerted effort to reduce frequent broad-spectrum insecticide applications made on vulnerable crops. One tool that has emerged recently is the use of long-lasting insecticide-treated nets (LLINs) as a killing agent. Here, we conducted bioassays to evaluate the effect of direct contact on deltamethrin-impregnated LLINs on the behaviour and survivorship of H. halys nymphs and adults in the laboratory. Following exposure at three different durations (1.25, 4.25 or 7.25 min), vertical and horizontal mobility of adults and nymphs and the flight capacity of adults were recorded and compared with individuals that were not exposed (control). Exposure to LLINs reduced the horizontal distance and velocity and increased the angular velocity of adults only but reduced vertical mobility of adults and nymphs. Adult flights were not significantly affected by LLIN exposure. Mortality of adults and nymphs at 7-day post-exposure ranged from 73% to 77% regardless of exposure time. We discuss our findings within the context of the potential for and limitations of deploying LLINs in vulnerable crops to manage H. halys populations.     

Landscape Factors Facilitating the Invasive Dynamics and Distribution of the Brown Marmorated Stink Bug,Halyomorpha halys (Hemiptera: Pentatomidae), after Arrival in the United States

The brown marmorated stink bug, Halyomorpha halys, a native of Asia, has become a serious invasive pest in the USA. H. halys was first detected in the USA in the mid 1990s, dispersing to over 41 other states. Since 1998, H. halys has spread throughout New Jersey, becoming an important pest of agriculture, and a major nuisance in urban developments. In this study, we used spatial analysis, geostatistics, and Bayesian linear regression to investigate the invasion dynamics and colonization processes of this pest in New Jersey. We present the results of monitoring H. halys from 51 to 71 black light traps that were placed on farms throughout New Jersey from 2004 to 2011 and examined relationships between total yearly densities of H. halys and square hectares of 48 landscape/land use variables derived from urban, wetland, forest, and agriculture metadata, as well as distances to nearest highways. From these analyses we propose the following hypotheses: (1) H. halys density is strongly associated with urban developments and railroads during its initial establishment and dispersal from 2004 to 2006; (2) H. halys overwintering in multiple habitats and feeding on a variety of plants may have reduced the Allee effect, thus facilitating movement into the southernmost regions of the state by railroads from 2005 to 2008; (3) density of H. halys contracted in 2009 possibly from invading wetlands or sampling artifact; (4) subsequent invasion of H. halys from the northwest to the south in 2010 may conform to a stratified-dispersal model marked by rapid long-distance movement, from railroads and wetland rights-of-way; and (5) high densities of H. halys may be associated with agriculture in southern New Jersey in 2011. These landscape features associated with the invasion of H. halys in New Jersey may predict its potential rate of invasion across the USA and worldwide.     

Repellent activity of essential oils on adults of Halyomorpha halys (Heteroptera: Pentatomidae) in different physiological-behavioural phases

The brown marmorated stink bug Halyomorpha halys is an invasive agricultural pest in North America and Europe, and also a dwelling nuisance in autumn, due to the overwintering adults aggregating inside buildings. The repellent potential of ginger, clove, vetiver and turmeric essential oils (EOs) was tested on H. halys adults of three different physiological-behavioural phases: exiting overwintering (EXOV), active during summer (SUMM) and entering overwintering (ENOV). In a two-choice apparatus, fresh food was used as an attractant in both sides, together with three males when testing ENOV individuals. A filter paper with different concentrations of the EOs was the treatment side, and a filter paper with ethanol acted as control. The position of the individually tested bugs was recorded after 1, 6 and 24 hr. All tested EOs were repellent at concentrations higher than 3%, independent of sex or length of exposure. Turmeric and clove were the most repellent EOs, whereas ginger and vetiver showed on average a medium-to-low repellency. Significant differences emerged among the physiological-behavioural phases, with SUMM individuals showing a greater repellency to many of the tested concentrations, and EXOV individuals being overall the least susceptible to these substances. The response to vetiver oil was ambiguous, as at 25%, it elicited both a strong repellency in SUMM and a strong attraction in EXOV. Turmeric and clove EOs are promising candidates in integrated pest management strategies to reduce attacks by H. halys to susceptible crops especially during summer, as well as to prevent the entrance of overwintering bugs in buildings in autumn.     

Adjacent Habitat Influence on Stink Bug (Hemiptera: Pentatomidae) Densities and the Associated Damage at Field Corn and Soybean Edges

The local dispersal of polyphagous, mobile insects within agricultural systems impacts pest management. In the mid-Atlantic region of the United States, stink bugs, especially the invasive Halyomorpha halys (Stål 1855), contribute to economic losses across a range of cropping systems. Here, we characterized the density of stink bugs along the field edges of field corn and soybean at different study sites. Specifically, we examined the influence of adjacent managed and natural habitats on the density of stink bugs in corn and soybean fields at different distances along transects from the field edge. We also quantified damage to corn grain, and to soybean pods and seeds, and measured yield in relation to the observed stink bug densities at different distances from field edge. Highest density of stink bugs was limited to the edge of both corn and soybean fields. Fields adjacent to wooded, crop and building habitats harbored higher densities of stink bugs than those adjacent to open habitats. Damage to corn kernels and to soybean pods and seeds increased with stink bug density in plots and was highest at the field edges. Stink bug density was also negatively associated with yield per plant in soybean. The spatial pattern of stink bugs in both corn and soybeans, with significant edge effects, suggests the use of pest management strategies for crop placement in the landscape, as well as spatially targeted pest suppression within fields.     

Contrasting Role of Temperature in Structuring Regional Patterns of Invasive and Native Pestilential Stink Bugs

Objectives

Assessment and identification of spatial structures in the distribution and abundance of invasive species is important for unraveling the underlying ecological processes. The invasive agricultural insect pest Halyomorpha halys that causes severe economic losses in the United States is currently expanding both within United States and across Europe. We examined the drivers of H. halys invasion by characterizing the distribution and abundance patterns of H. halys and native stink bugs (Chinavia hilaris and Euschistus servus) across eight different spatial scales. We then quantified the interactive and individual influences of temperature, and measures of resource availability and distance from source populations, and their relevant spatial scales. We used Moran’s Eigenvector Maps based on Gabriel graph framework to quantify spatial relationships among the soybean fields in mid-Atlantic Unites States surveyed for stink bugs.

Findings

Results from the multi-spatial scale, multivariate analyses showed that temperature and its interaction with resource availability and distance from source populations structures the patterns in H. halys at very broad spatial scale. H. halys abundance decreased with increasing average June temperature and distance from source population. H. halys were not recorded at fields with average June temperature higher than 23.5°C. In parts with suitable climate, high H. halys abundance was positively associated with percentage developed open area and percentage deciduous forests at 250m scale. Broad scale patterns in native stink bugs were positively associated with increasing forest cover and, in contrast to the invasive H. halys, increasing mean July temperature. Our results identify the contrasting role of temperature in structuring regional patterns in H. halys and native stink bugs, while demonstrating its interaction with resource availability and distance from source populations for structuring H. halys patterns.

Conclusion

These results help predicting the pest potential of H. halys and vulnerability of agricultural systems at various regions, given the climatic conditions, and its interaction with resource availability and distance from source populations. Monitoring and control efforts within parts of the United States and Europe with more suitable climate could focus in areas of peri-urban developments with deciduous forests and other host plants, along with efforts to reduce propagule pressure.     

Effect of resistant and susceptible soybean cultivars on the attraction of egg parasitoids under field conditions

The association of resistant crop varieties and biological pest control has great potential for pest management, as resistant cultivars may affect herbivore population dynamics by interfering with their biology and search behaviour for host plants. In addition, resistant varieties can also affect the efficiency of natural enemies. The aims of this work were to evaluate the influence of the soybean cultivars Dowling (resistant), IAC 100 (resistant) and Silvânia (susceptible) under field conditions on: (i) the abundance of parasitoids in the Platygastridae family and the stink bug Euschistus heros and (ii) the parasitism of stink bug eggs by these natural enemies. There was no difference between cultivars in stink bug distribution in the field. The parasitoids Telenomus podisi, Trissolcus teretis, Tr. urichi and Tr. brochymenae emerged from the sentinel eggs of E. heros, and T. podisi was the most abundant species observed during the reproductive stage R6. The cultivars Dowling and IAC 100 attracted a higher number of Platygastridae parasitoids, T. podisi and Tr. teretis, and the abundance of these parasitoids during the period from R1 to R7 might have being sufficient to control the stink bug population. These results suggest that the cultivars Dowling and IAC 100 have important attributes that should be taken into account in the implementation and development of new cultivars in breeding programmes that aim to obtain plants more resistant to stink bugs and more attractive to natural enemies.     

Behavioural response of the invasive Halyomorpha halys (Hemiptera: Pentatomidae) to host plant stimuli augmented with semiochemicals in the field

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A modified DNA barcode approach to define trophic interactions between native and exotic pentatomids and their parasitoids

The establishment of invasive Halyomorpha halys (Stål) outside of its native range may impact native species assemblages, including other pentatomids and their scelionid parasitoids. This has generated interest in defining species diversity and host‐parasitoid associations in this system to better understand the impact of invasive alien species on trophic interactions in invaded regions. Information on scelionid–pentatomid associations in natural habitats is lacking, and species‐level identification of these associations can be tenuous using rearing and dissection techniques. Naturally occurring pentatomid eggs were collected in areas where H. halys has established in Canada and were analysed using a modified DNA barcoding approach to define species‐level trophic interactions. Identification was possible for >90% of egg masses. Eleven pentatomid and five scelionid species were identified, and trophic links were established. Approximately 70% of egg masses were parasitized; parasitism and parasitoid species composition were described for each species. Telenomus podisi Ashmead was the dominant parasitoid and was detected in all host species. Trissolcus euschisti Ashmead was detected in several host species, but was significantly more prevalent in Chinavia hilaris (Say) and Brochymena quadripustulata (Fabricius). Trissolcus brochymenae Ashmead and Tr. thyantae Ashmead were recorded sporadically. Parasitism of H. halys was 55%, and this species was significantly less likely to be parasitized than native pentatomids. The scelionid species composition of H. halys consisted of Te. podisi, Tr. euschisti and Tr. thyantae. Although these species cannot develop in fresh H. halys eggs, we demonstrate that parasitoids attempt to exploit this host under field conditions.     

Insight into Salivary Gland Proteomes of Two Polyphagous Stink Bugs: Nezara viridula L. and Halyomorpha halys Stål

The invasive brown marmorated stink bug (BMSB), Halyomorpha halys Stål, and the southern green stink bugs (SGSBs), Nezara viridula L., are widely distributed in Europe, even if the date of introduction and the diet differ. Saliva of Hemipteran pests plays essential roles in the interaction between insects and their host plants. The salivary proteomes of several aphid species have been studied and found to differ according to the species, while no comparative investigation between phytophagous stink bugs has been performed yet. Here, the salivary proteins from two bugs, BMSB and SGSB, are analyzed using LC‐MS/MS. Data are available via ProteomeXchange with identifiers PXD011920 and PXD011976. A total of 238 and 305 proteins are identified in salivary glands of BMSB and SGSB, respectively. In comparison with salivary proteome from other Hemiptera, the most striking feature of the salivary gland proteomes of SGSB and BMSB is the similar pattern of protein functions between both species. Some of the proteins are speculated to play a significant role in plant–insect interactions. The results herein provide a framework for future research to elucidate the molecular basis of differential impact of piercing–sucking insects on host plants.     

Characterization of Overwintering Sites of the Invasive Brown Marmorated Stink Bug in Natural Landscapes Using Human Surveyors and Detector Canines

Halyomorpha halys is an invasive species from Asia causing major economic losses in agricultural production in the mid-Atlantic region of the United States. Unlike other crop pests, H. halys is also well-known for nuisance problems in urban, suburban, and rural areas, as massive numbers of adults often invade human-made structures to overwinter inside protected environments. Research efforts have focused on populations in human-made structures while overwintering ecology of H. halys in natural landscapes is virtually unknown. We explored forested landscapes in the mid-Atlantic region to locate and characterize natural overwintering structures used by H. halys. We also evaluated the use of detector canines to locate overwintering H. halys to enhance the accuracy and efficiency of surveys. From these studies, we indentified shared characteristics of overwintering sites used by H. halys in natural landscapes. Overwintering H. halys were recovered from dry crevices in dead, standing trees with thick bark, particularly oak (Quercus spp.) and locust (Robinia spp.); these characteristics were shared by 11.8% of all dead trees in surveyed landscapes. For trees with favorable characteristics, we sampled ∼20% of the total above-ground tree area and recovered 5.9 adults per tree from the trees with H. halys present. Two detector canines were successfully trained to recognize and detect the odor of adult H. halys yielding >84% accuracy in laboratory and semi-field trials. Detector canines also found overwintering H. halys under field conditions. In particular, overwintering H. halys were recovered only from dead trees that yielded positive indications from the canines and shared key tree characteristics established by human surveyors. The identified characteristics of natural overwintering sites of H. halys will serve as baseline information to establish crop economic risk levels posed by overwintering populations, and accordingly develop sustainable management programs.     

Performance of Ooencyrtus kuvanae (Hymenoptera: Encyrtidae) on two host species,Halyomorpha halys and Philosamia ricini

The brown marmorated stink bug, Halyomorpha halys, is an invasive agricultural pest of fruit trees and vegetables. Egg parasitoids play a key role in the reducing of H. halys populations. Ooencyrtus kuvanae (Howard) (Hymenoptera: Encyrtidae) can parasitize H. halys and complete its life cycle in this host species. Many factors can influence this parasitoid–host relationship. Of these factors, we evaluated the effect of female age, exposure time, and host species on the biological characteristics and fecundity of O. kuvanae reared on eggs of H. halys as well as another previously known host Philosamia ricini (Lepidoptera: Saturniidae). In this study, we used a 3-year-old laboratory colony of O. kuvanae. Parasitism rates positively affected by exposure time in P. ricini. The highest parasitism rates were obtained in 5- and 7-day-old females of both hosts. The highest emergence rates were recorded on P. ricini for 5- and 7-day-old female P. ricini (81.8% and 84.8%, respectively). The development time of O. kuvanae ranged from 18.4 to 19.1 days on H. halys and 17.7 to 18.3 days on P. ricini. The longevity of O. kuvanae that were provided honey was 38.5 and 47.8 days on H. halys and P. ricini, respectively. The longevity of O. kuvanae that were not provided honey was 2.3 and 2.8 days on H. halys and P. ricini, respectively. The sex ratio was male-biased (36.5% female) on H. halys and female-biased (55.2% female) on P. ricini. Fecundity of O. kuvanae was 37.7 and 59.6 progeny per female for H. halys and P. ricini, respectively. The performance of O. kuvanae was lower when compared with its performance on the host P. ricini. Our results suggest that O. kuvanae has potential as new biological control agent for H. halys.     

Biological control of soybean stink bugs by inoculative releases of Trissolcus basalis

Field studies of inoculative releases of Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) in early-maturing soybean, used as a trap crop, were conducted during four consecutive seasons to evaluate the parasitoid's potential as an IPM tactic for use against stink bug (Pentatomidae) species. Fifteen thousand adults of the parasitoid were released per hectare in the trap crop when the first stink bugs were detected in the experimental area. The stink bug population density was reduced by an average of 54% in the trap crop and by 58% in the main crop. The inoculative releases produced a reduction and delay in the stink bug population peak, mainly represented by Nezara viridula (L.), Piezodorus guildinii (Westwood) and Euschistus heros (Fabr.), which were held below economic threshold levels during the most critical stages of stink bug attack on soybean (pod and seed fill, R3–R6). As a result, seed quality was better in areas where T. basalis was released, demonstrating the efficacy of inoculative releases of this egg-parasitoid which could be an important component of the soybean IPM program in Brazil.     

Effects of Rag1 aphid‐resistant soybean on mortality,development, and preference of brown marmorated stink bug

The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), poses a new threat to soybean, Glycine max (L.) Merrill (Fabaceae), production in the north central USA. As H. halys continues to spread and increase in abundance in the region, the interaction between H. halys and management tactics deployed for other pests must be determined. Currently, the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is the most abundant and damaging insect pest of soybean in the region. Aphid‐resistant soybean, mainly with the Rag1 gene, is commercially available for management of A. glycines. Here, experiments were performed to evaluate the effects of Rag1 aphid‐resistant soybean on the mortality, development, and preference of H. halys. In a no‐choice test, mortality of H. halys reared on Rag1 aphid‐resistant soybean pods was significantly lower than when reared on aphid‐susceptible soybean pods (28 vs. 53%). Development time, adult weight, and proportion females of surviving adults did not differ when reared on Rag1 aphid‐resistant or aphid‐susceptible soybean pods. In choice tests, H. halys exhibited a preference for Rag1 aphid‐resistant over aphid‐susceptible soybean pods after 4 h, but not after 24 h. Halyomorpha halys exhibited no preference when tested with vegetative‐stage or reproductive‐stage soybean plants. The preference by H. halys for Rag1 aphid‐resistant soybean pods and the decreased mortality when reared on these pods suggests that the use of Rag1 aphid‐resistant soybean may favor this emerging pest in the north central USA.     

Stink Bug Feeding Induces Fluorescence in Developing Cotton Bolls

Background

Stink bugs (Hemiptera: Pentatomidae) comprise a critically important insect pest complex affecting 12 major crops worldwide including cotton. In the US, stink bug damage to developing cotton bolls causes boll abscission, lint staining, reduced fiber quality, and reduced yields with estimated losses ranging from 10 to 60 million dollars annually. Unfortunately, scouting for stink bug damage in the field is laborious and excessively time consuming. To improve scouting accuracy and efficiency, we investigated fluorescence changes in cotton boll tissues as a result of stink bug feeding.

Results

Fluorescent imaging under long-wave ultraviolet light showed that stink bug-damaged lint, the inner carpal wall, and the outside of the boll emitted strong blue-green fluorescence in a circular region near the puncture wound, whereas undamaged tissue emissions occurred at different wavelengths; the much weaker emission of undamaged tissue was dominated by chlorophyll fluorescence. We further characterized the optimum emission and excitation spectra to distinguish between stink bug damaged bolls from undamaged bolls.

Conclusions

The observed characteristic fluorescence peaks associated with stink bug damage give rise to a fluorescence-based method to rapidly distinguish between undamaged and stink bug damaged cotton bolls. Based on the fluorescent fingerprint, we envision a fluorescence reflectance imaging or a fluorescence ratiometric device to assist pest management professionals with rapidly determining the extent of stink bug damage in a cotton field.     

Biological control of invasive stink bugs: review of global state and future prospects

Invasive stink bugs (Hemiptera: Pentatomidae) are responsible for high economic losses to agriculture on a global scale. The most important species, dating from recent to old invasions, include Bagrada hilaris (Burmeister), Halyomorpha halys (Stål), Piezodorus guildinii (Westwood), Nezara viridula (L.), and Murgantia histrionica (Hahn). Bagrada hilaris, H. halys, and N. viridula are now almost globally distributed. Biological control of these pests faces a complex set of challenges that must be addressed to maintain pest populations below the economic injury level. Several case studies of classical and conservation biological control of invasive stink bugs are reported here. The most common parasitoids in their geographical area of origin are egg parasitoids (Hymenoptera: Scelionidae, Encyrtidae, and Eupelmidae). Additionally, native parasitoids of adult stink bugs (Diptera: Tachinidae) have in some cases adapted to the novel hosts in the invaded area and native predators are known to prey on the various instars. Improving the efficacy of biocontrol agents is possible through conservation biological control techniques and exploitation of their chemical ecology. Moreover, integration of biological control with other techniques, such as behavioural manipulation of adult stink bugs and plant resistance, may be a sustainable pest control method within organic farming and integrated pest management programs. However, additional field studies are needed to verify the efficacy of these novel methods and transfer them from research to application.     

Essential oils as spatial repellents for the brown marmorated stink bug,Halyomorpha halys (Stål) (Hemiptera: Pentatomidae)

The brown marmorated stink bug (BMSB), Halyomorpha halys (Stål), native to Northeastern Asia, is a serious invasive pest in the United States, Canada, Switzerland, Germany and France. Several common essential oils and their compositions were tested against BMSBs as potential repellents. All the tested individual essential oils and a ternary oil blend showed significant repellency to both BMSB nymphs and adults. Clove oil, lemongrass oil, spearmint oil, ylang‐ylang oil, and the ternary oil mixture (clove, lemongrass and spearmint) almost completely blocked attraction of BMSBs to the stink bug attractant‐baited traps; whereas wintergreen oil, geranium oil, pennyroyal oil and rosemary oil resulted in 60–85% trap catch reductions. Over 20 BMSB antennally active compounds were identified from SPME headspace samples of the eight repellent essential oils using GC‐EAD and GC‐MS techniques. Among the synthetic EAD‐active compounds tested in the field, eugenol, l‐carvone, p/l‐menthone, pulegone, methyl salicylate, trans/cis‐citral, methyl benzoate and β‐caryophyllene significantly reduced trap catches of BMSBs by 72–99%; these compounds are likely responsible for the repellency of their corresponding essential oils. Surprisingly, a synthetic mixture of the predacious spined soldier bug (SSB) [Podisus maculiventris (Say)] aggregation pheromone (trans‐2‐hexenal, α‐terpineol and benzyl alcohol) also showed a significant inhibition of BMSB response to its attractants. These repellent essential oils and their active compounds, as well as the synthetic SSB pheromone, are potentially useful as part of an efficient, environmentally sound semiochemical‐based IPM programme to combat this serious invasive stink bug.     

Presence of the invasive brown marmorated stink bug Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) on home exteriors during the autumn dispersal period: Results generated by citizen scientists

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