Attachment ability of the southern green stink bug, <Emphasis Type="Italic">Nezara viridula</Emphasis> (L.), on plant surfaces

Traction forces of male and female southern green stink bugs Nezara viridula (L.) were measured on adaxial leaves of green beans (Phaseolus vulgaris L. cv. ‘Nagauzura’), peas (Pisum sativum L. cv. ‘Hakuryu’), rice (Oryza sativa L. cv. ‘Mac hin sung’), and soybean (Glycine max [L.] Merr. cv. ‘Enrei’), as well as on glass as a control surface. Bugs attached well on three-dimensionally structured surfaces covered with anti-adhesive epicuticular wax crystals. Strongest pulls were generated on adaxial green bean leaves, corresponding to safety factors (traction force/body weight) of 11.1 and 11.6 in males and females, respectively. These values were slightly lower on soybean (males: 7.4, females: 8.0) and rice leaves (males: 8.9, females: 10.6). Trichomes and papillae are assumed to promote pentatomid bug’s attachment. On tabular, wax-covered pea leaves, safety factors decreased significantly to 1.7 and 1.6, in males and females, respectively. Differently, on non-structured glass, safety factors resembled those on rice and soybean leaves (males: 9.6, females: 8.0). No statistical differences in traction force and safety factor between sexes were detected on any substrate. Surface wettability did not significantly affect the results. Both robust claws and tough adhesive pads enable the N. viridula bugs to grasp and adhere to a wide range of various plant substrates, including such ones covered with anti-adhesive wax crystals. However, tabular, pruinose pea leaves were detected to prevent the foothold of the southern green stink bugs, although pea is known as one of their common host plants.     

Peptide mediated,enhanced toxicity of a bacterial pesticidal protein against southern green stink bug

The damage caused by stink bugs that feed on agricultural crops accounts for such significant losses that transgenic plant resistance to stink bugs would be highly desirable. As the level of toxicity of the Bacillus thuringiensis-derived, ETX/Mtx2 pesticidal protein Mpp83Aa1 is insufficient for practical use against the southern green stink bug Nezara viridula, we employed two disparate approaches to isolate peptides NvBP1 and ABP5 that bind to specific proteins (alpha amylase and aminopeptidase N respectively) on the surface of the N. viridula gut. Incorporation of these peptides into Mpp83Aa1 provided artificial anchors resulting in increased gut binding, and enhanced toxicity. These peptide-modified pesticidal proteins with increased toxicity provide a key advance for potential future use against N. viridula when delivered by transgenic plants to mitigate economic loss associated with this important pest.     

Identification of Stink Bugs Using an Electronic Nose

Stink bugs are recognized as pests of several economically important crops, including cotton, soybean and a variety of tree fruits. The Cyranose 320 was used for the classified investigation of stink bug. Stink bugs including males and females of the southern green stink bugs, Nezara viridula, were collected from crop fields around College Station, TX. Results show that the released chemicals and chemical intensity are both critical factors, which determine the rate that the Cyranose 320 correctly identified the stink bugs. The Cyranose 320 shows significant potential in identifying stink bugs, and can classify stink bug samples by species and gender.     

Soybean seed damage by different species of stink bugs

Abstract

• 1 Damage caused by the three main species of stink bugs occurring on soybean Nezara viridula (Linnaeus), Piezodorus guildinii (Westwood) and Euschistus heros (Fabricius) was compared in field cages and in greenhouses. Infestation levels of 4 stink bugs/m row of plants (field cages) and 2 stink bug/plant (greenhouse) for 15 days during the pod filling stage are reported. At harvest, the yield and seed quality were evaluated.
• 2 In the field, there was no difference in yield between infested and insect‐free plants, but damage to seed quality varied with stink bug species. Plants damaged by P. guildinii had the lowest quality seeds. From 50 g seed samples harvested in the field, the mean weight of seeds classified as ‘good’ was 37.3 g in plants infested with P. guildinii, compared to 41.8, 44.2 and 46.6 g in plants infested with E. heros, N. viridula and the control, respectively.
• 3 Plants infested with P. guildinii showed the highest number of seeds damaged by stink bugs, whereas those infested with E. heros showed the lowest damage.
• 4 Plants infested with P. guildinii had 18.5% damaged seeds, higher than the 3.6% and 3.4% damaged seeds from plants infested with the two other species and 0.1% in control plants. The percentage of non‐viable seeds due to stink bug damage was 5.7% for P. guildinii but lower for the other two species.

     

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.     

Flight-related metabolism and its regulatory peptides in the spittle bug Locris arithmetica (Cicadomorpha: Cercopidae) and the stink bugs Nezara viridula (Heteroptera: Pentatomidae) and Encosternum delegorguei (Heteroptera: Tessaratomidae)

Three species of bugs (Order: Hemiptera) belonging to different suborders and different families were investigated with respect to flight-related metabolism, and the neuropeptide hormones that regulate metabolism in Encosternum delegorguei, Locris arithmetica and Nezara viridula were characterised. The concentration of two potential metabolic fuels in the haemolymph of these bugs (at rest) revealed that lipids were more abundant than carbohydrates and that lipids increased significantly when the bugs performed extensive exercise (flight) and in the resting period following the aerobic activity. Carbohydrate levels declined during flight but recovered to the pre-flight level during a 1 h resting period post-flight. Further experiments with N. viridula revealed greater lipid accumulation in the haemolymph after a 10 min flight than after a 2 min flight and significant activation of glycogen phosphorylase was recorded in the fat body immediately after flight activity. Crude extracts of corpora cardiaca (CC) from L. arithmetica and E. delegorguei were both active in mobilising carbohydrates in the cockroach Periplaneta americana. In conspecific assays, only L. arithmetica CC extract had a significant hypertrehalosaemic effect, while CC extracts from both E. delegorguei and L. arithmetica were hyperlipaemic. By a combination of liquid chromatography and mass spectrometry two octapeptides known as Peram-CAH-I and Pyrap-AKH were identified from the spittle bug, L. arithmetica, and two octapeptides known as Panbo-RPCH and Schgr-AKH-II were identified from the edible inflated stink bug, E. delegorguei. Injection of Panbo-RPCH into E. delegorguei and into the green stink bug, N. viridula had no effect on circulating carbohydrates, although glycogen phosphorylase was activated in the fat body. The circulating lipid concentration in N. viridula did not change significantly under artificially induced hypertrehalosaemia, suggesting that lipids were not being used or mobilised.     

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.     

Evaluating potential trap crops for managing leaffooted (Hemiptera: Coreidae) and phytophagous stink bug (Hemiptera: Pentatomidae) species in peaches

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荔枝蝽取食行为的研究

在越冬前和产卵期,荔枝蝽Tessaratoma papillosa Drury在寄主植物-荔枝树的花枝、嫩枝和老枝上都有取食行为。但在这两个不同时期, 其取食行为有显著差异。在越冬前,只有50%～70%的成虫在各类枝条上取食;而处于产卵期的荔枝蝽成虫,在各类枝条上,100%积极取食,且其取食前时间显著短于越冬前在同类枝条上的取食前时间。同一时期在不同枝叶上,荔枝蝽的取食行为也有显著差异。被置于嫩枝叶和花枝上的成虫取食前时间明显短于被置于老枝叶上者;在有选择的情况下,两个时期的成虫都明显地选择在花枝和嫩枝上取食。经分析测定：在不同生长时期,荔枝树的花枝和嫩枝的含水量与含氮量均较老枝叶中的高,可溶性糖含量的变化较大;组织结构也存在明显差异。     

Seeding Dates and Cultivars Effects on Stink Bugs Population and Damage on Common Bean <Emphasis Type="Italic">Phaseolus vulgaris</Emphasis> L

Fields experiments were conducted during two growing seasons (2010–2011 and 2012–2013) at three seeding dates to identify stink bug (Hemiptera: Pentatomidae) species and to determine their seasonal population density fluctuation and damage caused to three common bean (Phaseolus vulgaris L.) cultivars “Ica Pijao,” “Cubacueto 25–9,” and “Chévere.” Stink bug species observed were Nezara viridula (L.), Piezodorus guildinii (Westwood), Chinavia rolstoni (Rolston), Chinavia marginatum (Palisot de Beauvois), and Euschistus sp. The most prevalent species was N. viridula in both seasons. The largest number of stink bugs was found in beans seeded at the first (mid September) and third (beginning of January) seeding dates. Population peaked at BBCH 75 with 1.75, 0.43, and 1.25 stink bugs/10 plants in 2010–2011 and with 2.67, 0.45, and 1.3 stink bugs/10 plants in 2012–2013 in the fields seeded the first, second, and third seeding dates, respectively. The lowest numbers of stink bugs were found in beans seeded at the second (mid November) seeding date. A significant negative correlation between relative humidity and number of stink bugs was found in 2010–2011, and a similar tendency was observed in 2012–2013. The highest seed and pod damage levels occurred in cv. “Chévere” and the lowest in cv. “ICA Pijao” during both seasons. Results suggest that cv. “ICA Pijao” and the second (mid November) seeding date is the best choice to reduce stink bug damage.     

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.     

Waveform characterization of the soybean stem feeder Edessa meditabunda: overcoming the challenge of wiring pentatomids for EPG

Stink bugs (Hemiptera: Heteroptera: Pentatomidae) are in general robust and restless insects, which makes them difficult to wire for electropenetrograph (EPG) studies. In addition, cuticular lipids may reduce wire effectiveness, and their removal could improve success of wiring. We compared wiring effectiveness for three species of stink bugs, differing in walking behaviour and degree of cuticular waxiness, that is, Piezodorus guildinii (Westwood), Nezara viridula (L.), and Loxa deducta (Walker). Results indicated that removal of cuticular lipids by mechanical abrasion (via sanding) greatly improved attachment success with gold wire. Our hypothesis that heavier and bigger bugs would lose the wire attachment more quickly than lighter and smaller bugs was not confirmed, regardless of the sanding. In contrast, our hypothesis that greater movement of a bug would cause the wire to break more often was supported by extensive testing. Behaviour appears to be more relevant for successful wiring than body weight. We used the sanding and wiring technique to characterize and correlate direct current EPG waveforms for the large and restless stem‐feeding stink bug Edessa meditabunda (Fabricius) on soybean plants. This marks the first published example of pentatomid EPG waveforms. Edessa meditabunda recordings on soybean stems generated eight types of waveforms in three phases and two families, named as follows: non‐probing = Np and Z; pathway phase = Em1; X wave phase = X; ingestion phase, family I = Em2 and Em3; ingestion phase, family N = Em4 and Em5. These eight were described based on their frequencies, relative amplitudes, and level voltages. Histological studies of stylets within salivary sheaths correlated the Em1, Em2, and Em3 waveforms with specific penetration sites. The waveform with the longest duration when feeding was Em2, representing xylem sap ingestion; in addition, waveform Em3 (always preceded by an X wave) was correlated with phloem sap ingestion.     

Selective responses of Trissolcus basalis and Telenomus podisi to chemical footprints of preferred hosts

Chemical trails of the hosts (footprints) are important cues for the host searching behaviour of egg parasitoids of the family Scelionidae. The present study aims to determine the influence of the footprints of three neotropical stink bugs (Euchistus heros, Dichelops melacanthus and Nezara viridula) on the foraging behaviour of two parasitoids, Trissolcus basalis and Telenomus podisi, as well as a possible selective response to fooprints of their preferred hosts. Accordingly, Tr. basalis and Te. podisi females are allowed to forage on open arenas where E. heros, D. melacanthus or N. viridula had walked or on open arenas that had been treated with samples of an extract from each stink bug's footprints. Hexane extracts of stink bug footprints are obtained from solvent-washed Petri dishes where insects were allowed to walk for 24 h, and these extracts were analyzed by gas chromatography-flame ionization detection and gas chromatography-mass spectrometry. Each parasitoid responds selectively to the footprints of their preferred host (Tr. basalis to footprints of N. viridula and Te. podisi to footprints of E. heros). Twenty-six compounds comprising of C18 to C35 (saturated and unsaturated) and methyl branched hydrocarbons were identified in extracts of E. heros, D. melacanthus and N. viridula, respectively. There are significant differences in the total amount of the compounds identified in the footprint stink bug's extracts and also a difference in the amounts of individual compounds. In addition, the behavioural assays showed that footprints of stink bugs are stimuli that are used by egg parasitoids to search, discriminate and selectively locate their preferred host.     

On Heels and Toes: How Ants Climb with Adhesive Pads and Tarsal Friction Hair Arrays

Ants are able to climb effortlessly on vertical and inverted smooth surfaces. When climbing, their feet touch the substrate not only with their pretarsal adhesive pads but also with dense arrays of fine hairs on the ventral side of the 3^rd and 4^th tarsal segments. To understand what role these different attachment structures play during locomotion, we analysed leg kinematics and recorded single-leg ground reaction forces in Weaver ants (Oecophylla smaragdina) climbing vertically on a smooth glass substrate. We found that the ants engaged different attachment structures depending on whether their feet were above or below their Centre of Mass (CoM). Legs above the CoM pulled and engaged the arolia (‘toes’), whereas legs below the CoM pushed with the 3^rd and 4^th tarsomeres (‘heels’) in surface contact. Legs above the CoM carried a significantly larger proportion of the body weight than legs below the CoM. Force measurements on individual ant tarsi showed that friction increased with normal load as a result of the bending and increasing side contact of the tarsal hairs. On a rough sandpaper substrate, the tarsal hairs generated higher friction forces in the pushing than in the pulling direction, whereas the reverse effect was found on the smooth substrate. When the tarsal hairs were pushed, buckling was observed for forces exceeding the shear forces found in climbing ants. Adhesion forces were small but not negligible, and higher on the smooth substrate. Our results indicate that the dense tarsal hair arrays produce friction forces when pressed against the substrate, and help the ants to push outwards during horizontal and vertical walking.     

Locomotion in a sticky terrain

The mirid bug Pameridea roridulae lives mutalistically on the protocarnivorous plant Roridula gorgonias. The latter resembles an effective, three-dimensional flypaper trap which captures numerous flying insects. We have recently shown that P. roridulae bugs are not trapped by the plant, because they are covered with a layer of epicuticular grease, which is considerably thicker than in other insects. The present study demonstrates that the bugs’ morphology and locomotory characteristics also contribute to their specialisation for life on the adhesive plant surface. A structural analysis of the mirid bug’s attachment system, and an experimental study on its attachment ability were carried out. In traction force tests, maximum forces of 8.8 mN were measured on adaxial R. gorgonias leaves, corresponding to 126 times the bug’s body weight. On smooth surfaces, generated forces were only 47 times the bug’s body weight. Compared to closely related mirid bug species avoiding contact with plant adhesive secretion, P. roridulae is distinctly stronger and heavier, and holds its body close to the plant substrate. Two locomotion strategies on the glandular hairy plant surfaces are suggested for mirid bug species from the tribus Dicyphini: (1) avoidance strategy, characterised by the slim body held at a large distance from the plant surface by using long, slender legs, and (2) defense strategy, where trapping of the heavy bugs, situated close to the plant surface, is overcome by generating strong forces during locomotion and by having a thick anti-adhesive epicuticular greasy layer on the bugs’ cuticle.     

Microstructure of pretarsal pulvilli in shield bug Acanthosoma spinicolle (Heteroptera: Acanthosomatidae)

Shield bugs effectively attach themselves on both rough and smooth surfaces, but their advanced biological attachment devices have not been studied closely. Our fine structural examination of the attachment devices in the shield bug A. spinicolle reveals a unique system to achieve extraordinary adhesion that allows vertical climbing. Each appendage has a pair of tarsal claws that attach to rough substrates and a pair of pretarsal pulvilli that attach to smooth surfaces. Similar to other heteropteran insects, the pulvilli of this bug are categorized as a wet adhesion system, which makes use of an adhesive fluid from the pad secretion. However, this deformable pad creates a regular pattern of contact with the mating surface with a compact array of microfolds and setae with filamentous distal protrusions. To date, this distinctive microstructure in pulvilli pads has never been reported. These microstructural characteristics should be further studied to understand biological adhesion as well as create biomimetic applications.     

Prevalence,damage, management and insecticide resistance of stink bug populations (Hemiptera: Pentatomidae) in commodity crops

1. Pest management of stink bugs (Hemiptera: Pentatomidae) in soybean [Glycine max (L.) Merr.], corn (Zea mays L.) and cotton (Gossypium spp.) agroecosystems has become a major concern in several countries of the Americas.
2. In this review, we report an overview on geographical distribution, injury, damage and methods used to control (plant resistance mechanisms, biological control) the most important stink bugs in the Americas, with an emphasis on Brazil, the implications of the trend towards decreased susceptibility of stink bug populations to insecticides and the current difficulties of the management of these insect pests.
3. Currently, the Neotropical brown stink bug Euschistus heros (Fabricius) is less susceptible to organophosphate insecticides than in the past. A slight reduction in E. heros susceptibility to pyrethroids and, to a lesser extent, to neonicotinoids has also been observed. In addition, the green‐belly stink bug [Dichelops melacanthus (Dallas)] is more tolerant to the three classes of insecticides (neonicotinoids, organophosphates and pyrethroids) than E. heros.
4. Metabolic detoxification is involved in organophosphate, neonicotinoid and pyrethroid differences in susceptibility. Restricted availability of insecticides with different modes of action could favour the selection of resistant phenotypes in stink bug populations.

     

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.     

Influence of corn on stink bugs (Heteroptera: Pentatomidae) in subsequent crops

In southeastern United States farmscapes, corn, Zea mays L., is often closely associated with peanut, (Arachis hypogaea L.), cotton, (Gossypium hirsutum L.), or both. The objective of this 3-yr on-farm study was to examine the influence of corn on stink bugs (Heteroptera: Pentatomidae), Nezara viridula (L.), and Euschistus servus (Say), in subsequent crops in these farmscapes. Adults of both stink bug species entered corn first, and seasonal occurrence of stink bug eggs, nymphs, and adults indicated that corn was a suitable host plant for adult survival and nymphal development to adults. Stink bug females generally oviposited on cotton or peanut near the interface, or common boundary, of the farmscape before senescence of corn, availability of a new food, or both. Adult stink bugs dispersed from crop to crop at the interface of a farmscape in response to senescence of corn, availability of new food, or both. In corn-cotton farmscapes, adult stink bugs dispersed from senescing corn into cotton to feed on bolls (fruit). In corn-peanut farmscapes, adult stink bugs dispersed from senescing corn into peanut, which apparently played a role in nymphal development in these farmscapes. In the corn-cotton-peanut farmscape, stink bug nymphs and adults dispersed from peanut into cotton in response to newly available food, not senescence of peanut. Stink bug dispersal into cotton resulted in severe boll damage. In conclusion, N. viridula and E. servus are generalist feeders that exhibit edge-mediated dispersal from corn into subsequent adjacent crops in corn-cotton, corn-peanut, and corn-peanut-cotton farmscapes to take advantage of suitable resources available in time and space for oviposition, nymphal development, and adult survival. Management strategies for crops in this region need to be designed to break the cycle of stink bug production, dispersal, and expansion by exploiting their edge-mediated movement and host plant preferences.     

Relative longevity of adult Nezara viridula in field cages of cotton,peanut, and soybean

Producers in the southeastern USA face significant crop losses from the stink bugs Nezara viridula (L.), Euschistus servus (Say), and Chinavia hilaris (Say) (all Hemiptera: Pentatomidae). Cotton, peanut, and soybean are major agronomic crops and host plants of stink bugs in the region. We conducted a field plot study to measure the relative longevity of adult, unmated N. viridula males and females caged on peanut, cotton, and soybean to test three hypotheses: (1) differences in mortality are associated with differences in host plant food suitability, (2) mortality rates increase with age, and (3) males have higher mortality than females. Using survival analysis, we found that the sex of the individual did not affect survival rates on any of the three host plants. Survival was significantly higher in cotton and soybean than in peanut. Mortality rates increased with age in peanut, but not in soybean or cotton. The frequency of canopy temperatures above 35 °C was higher in peanut than in soybean. Peanut appears to be a less than ideal habitat in terms of canopy temperature and/or food quality for N. viridula adults. Both, cotton and soybean were equally suitable food resources for N. viridula adults prior to maturation of the plants.