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.     

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.     

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 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.     

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.

     

The role of Acanthospermum hispidum in the phenology of Euschistus heros and of Nezara viridula

Laboratory, greenhouse, and field studies with Euschistus heros (F.) and Nezara viridula (L.) (Heteroptera: Pentatomidae) in northern Paraná, Brazil, demonstrated greater survival and longevity with E. heros than N. viridula when fed the weed Acanthospermum hispidum DC. (Compositae). E. heros was better adapted to A. hispidum than N. viridula but neither species reproduced on this plant. Stink bugs moved from soybean to A. hispidum mainly during mid-March to mid-April when soybean plants matured. The infestation reached 60 and 100% with a maximum of ca. 3 and 10 stink bugs/plant in 1988 and 1989, respectively. Surprisingly, E. heros and N. viridula, which are normally seed-feeders, strongly preferred the high moisture stems of A. hispidum. Both species demonstrated similar feeding frequencies. These results suggest that in northern Paraná, the common weed, A. hispidum functions as a temporary host providing water and nutrients to those two pentatomid pests of soybean. Finally, both species do not seem to recognize A. hispidum as an unsuitable or perhaps toxic plant.     

Gripping ease in southern green stink bugs Nezara viridula L. (Heteroptera: Pentatomidae): Coping with geometry,orientation and surface wettability of substrate

The southern green stink bug Nezara viridula L. (Heteroptera, Pentatomidae) is highly polyphagous, preferring apically situated seeds and fruits on more than 150 plant species belonging to over 30 plant families all over the world. This forces them to move over highly variable terrains, including plant stems, leaves, pods and buds, which requires efficient attachment. Stink bugs have long slender legs and feet (tarsi) equipped with paired curved claws, paired soft adhesive pads (pulvilli), and flattened lanceolate hairs (setae), which arise ventrally on the first and second foot segments (tarsomeres). To characterize their attachment abilities on well‐defined test substrates, here we comparatively measured and analyzed the traction forces of bugs walking horizontally and vertically on hydrophilic (water attractive) and hydrophobic (water repellent) glass plates and rods. The latter correspond to the geometry of preferred feeding sites of stink bugs in the field. The results show a clear contribution of tarsal flattened lanceolate hairs to the stink bug's attachment. Higher traction forces are generated on a glass rod than on a glass plate, corresponding to up to individual maximum of 43 times the stink bug's body weight. Substrate hydrophobicity promotes the attachment, while the measured forces are up to eight times lower when tarsal hairs are disabled. The combination of smooth and hairy tarsal pads results in a remarkable attachment ability, which enables N. viridula to climb unstable apical plant parts, and supports their invasive behavior and global dispersion.     

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.     

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.     

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.     

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.     

Seasonal body weight, lipid content, and impact of starvation and water stress on adult survivorship and longevity ofNezara viridula andEuschistus heros

Fresh and dry body weights (FW, DW) were greater for adult southern green stink bug,Nezara viridula (L.) than for the brown stink bug,Euschistus heros F. throughout the year in southern Brazil. FemalesN. viridula significantly increased FW and DW in late summer-early autumn, and during mid-spring; femaleE. heros did not show the same rates of increase in FW and DW. FemaleN. viridula were heavier than males, particularly during summer; however, female and maleE. heros were generally similar in weight.E. heros contained significantly greater amounts of lipid thanN. viridula, during mid-autumn to early-spring (April–September). Survivorship (%) and total longevity ofE. heros adults provided water only was greater (34.6–24.6 days, for females and males) than that forN. viridula (14.8–13.0 days); without water and food, longevity was drastically reduced (<7 days) for both species.     

Estimating potential stylet penetration of southern green stink bug – a mathematical modeling approach

Southern green stink bugs, Nezara viridula (L.) (Hemiptera: Pentatomidae), and related species are significant pests of cotton, Gossypium hirsutum L. (Malvaceae), in the USA Cotton Belt. Using their stylets, adults introduce pathogens of cotton into cotton bolls, and preliminary data indicate nymphs can also ingest these pathogens. However, data are lacking regarding stylet penetration potential of N. viridula nymphs, and records of stylet penetration by adults are typically determined after damage has occurred. In this study, rostral segments of all developmental stages of N. viridula were measured to estimate potential stylet penetration depth using a novel mathematical model. Overall mean stylet penetration estimates for all stages ranged from 135.3 μm for first instars to 2 389.3 μm for adult females. Potential stylet penetration significantly increased as the insect progressed through nymphal stages. Penetration was also significantly affected by insect posture while feeding. Overall minimum and maximum observed lengths of rostrum ranged from 835.3 μm (first instars) to 7 088.2 μm (adult females), and mean rostral lengths were significantly different between all stages. This report establishes conservative baselines of potential stylet penetration depths by all nymphal stages and both adult sexes of N. viridula. Additionally, the model presented here can be used to estimate potential stylet penetration for other Hemiptera and closely related insects with similar modes of feeding. In conjunction with crop phenology data, accurate estimates of potential stylet penetration will allow more proactive approaches to pest management in a wide range of high‐value cash crops affected worldwide by N. viridula.     

Interaction of the Bacillus thuringiensis delta endotoxins Cry1Ac and Cry3Aa with the gut of the pea aphid, Acyrthosiphon pisum (Harris)

Hemipteran pests including aphids are not particularly susceptible to the effects of insecticidal Cry toxins derived from the bacterium Bacillus thuringiensis. We examined the physiological basis for the relatively low toxicity of Cry1Ac and Cry3Aa against the pea aphid, Acyrthosiphon pisum (Harris). Cry1Ac was efficiently hydrolyzed by aphid stomach membrane associated cysteine proteases (CP) producing a 60 kDa mature toxin, whereas Cry3Aa was incompletely processed and partially degraded. Cry1Ac bound to the aphid gut epithelium but showed low aphid toxicity in bioassays. Feeding of aphids on Cry1Ac in the presence or absence of GalNAc, suggested that Cry1Ac gut binding was glycan mediated. In vitro binding of biotinylated-Cry1Ac to gut BBMVs and competition assays using unlabeled Cry1Ac and GalNAc confirmed binding specificity as well as glycan mediation of Cry1Ac binding. Although Cry3Aa binding to the aphid gut membrane was not detected, Cry3Aa bound 25 and 37 kDa proteins in aphid gut BBMV in ligand blot analysis and competition assays confirmed the binding specificity of Cry3Aa. This, combined with low toxicity in feeding assays, suggests that Cry3Aa does bind the gut epithelium to some extent. This is the first systematic examination of the physiological basis for the low efficacy of Cry toxins against aphids, and analysis of Cry toxin-aphid gut interaction.     

Effect of C-terminus site-directed mutations on the toxicity and sensitivity of Bacillus thuringiensis Vip3Aa11 protein against three lepidopteran pests

The insecticidal activities and specificities of the Vip3Aa proteins derived from different Bt strains are very different, although the similarities between these proteins are higher than 95%. In this study, we hypothesised that the differences in Vip3Aa11 and Vip3Aa39 C-terminal amino acids determine their differences in insecticidal activity against three Lepidoptera insects. To find the amino acid residues associated with insecticidal activity, nine different amino acid residues of Vip3Aa11 were substituted with the corresponding amino acid residues from Vip3Aa39 by site-directed mutagenesis. The toxicity of each protein was estimated by bioassays, and the results demonstrated that the mutant Y784N lost its insecticidal activity against three insects (Agrotis ipsilon, Helicoverpa armigera, and Spodoptera exigua). The insecticidal activity of S543N, I544L, and S686R against S. exigua increased 5-fold, 2.65-fold, and 8.98-fold, while the toxicity to H. armigera and A. ipsilon slightly decreased compared with that of the Vip3Aa11 protein. These findings indicate that the amino acid residues Ser⁵⁴³, Ile⁵⁴⁴, Thr⁶⁸⁵, Ser⁶⁸⁶, Arg⁷⁰⁴, Ile⁷⁸⁰, and Tyr⁷⁸⁴ may be insecticidal activity-related residues. Additionally, the trypsin activation of the four mutants indicated that all proteins can form a 62-kDa core fragment, except Y784N. A possible association between the insecticidal activity and trypsin sensitivity of Vip3A proteins is suggested.     

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

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Localization of selected pathogens of cotton within the southern green stink bug

Southern green stink bugs, Nezara viridula (L.) (Hemiptera: Pentatomidae), are pests of cotton recently shown to ingest, retain, and introduce some pathogens of cotton into bolls. The objective of this study was to determine where pathogen colonization occurs in N. viridula after ingestion. Laboratory‐reared adult N. viridula were fed sterile green beans soaked in water (control) or beans previously soaked in a suspension of one of three opportunistic bacterial pathogens [Pantoea agglomerans (Ewing & Fife), Pantoea ananatis (Serrano) Truper & De’Clari, or Klebsiella pneumoniae (Schroeter)] or a yeast [Nematospora coryli (Peglion)]. The insect rostrum, head, and alimentary canal were subsequently processed to determine the presence of pathogenic organisms. Overall, the alimentary canal exhibited significantly more bacterial colony forming units per g tissue (mean ± SEM = 4 806.3 ± 397.2) than the head (443.4 ± 397.2) and rostrum (46.0 ± 397.2); concentrations in the head and rostrum did not differ significantly. All four pathogens were detected in the alimentary canal, but only P. agglomerans and N. coryli were detected in the rostrum and head. Although P. ananatis and K. pneumoniae were only detected in the alimentary canal, their ranges of concentrations were similar to those of P. agglomerans and N. coryli in this tissue. Non‐selective media indicated that other bacterial fauna was also detected in all study insects. Thus, N. viridula does not discriminate with regard to ingestion of pathogens. The observed distribution pattern of tested bacteria and yeast in certain tissues of N. viridula clarifies the propensity for transmission of P. agglomerans and N. coryli. Results are discussed in relation to future research avenues examining selective colonization of certain pathogens and frequency of host infection by adults harboring the pathogenic organisms.     

Insects in a warmer world: ecological, physiological and life-history responses of true bugs (Heteroptera) to climate change

Focusing on the southern green stink bug, Nezara viridula (Pentatomidae), in central Japan the effects of climate change on true bugs (Insecta: Heteroptera) are reviewed. In the early 1960s, the northern edge of the species's distribution was in Wakayama Prefecture (34.1°N) and distribution was limited by the +5°C coldest month (January) mean temperature isothermal line. By 2000, N. viridula was recorded 70 km further north (in Osaka, 34.7°N). Historical climate data were used to reveal possible causes of the northward range expansion. The increase of mean and lowest winter month temperatures by 1–2°C in Osaka from the 1950s to the 1990s improved potential overwintering conditions for N. viridula. This promoted northward range expansion of the species. In Osaka, adult diapause in N. viridula is induced after mid‐September, much later than in other local seed‐feeding heteropterans. This late diapause induction results in late‐season ineffective reproduction: some females start oviposition in autumn when the progeny have no chance of attaining adulthood and surviving winter. Both reproductive adults and the progeny die. A period from mid‐September to early November represents a phenological mismatch: diapause is not yet induced in all adults, but it is already too late to start reproduction. Females that do not start reproduction but enter diapause in September have reduced postdiapause reproductive performance: they live for a shorter period, have a shorter period of oviposition and produce fewer eggs in smaller egg masses compared with females that emerge and enter diapause later in autumn. To some extent, N. viridula remains maladapted to Osaka environmental conditions. Ecological perspectives on establishment in recently colonized areas are discussed. A review of available data suggests that terrestrial and aquatic Heteroptera species respond to climate change by shifting their distribution ranges, changing abundance, phenology, voltinism, physiology, behaviour, and community structure. Expected responses of Heteroptera to further climate warming are discussed under scenarios of slight (<2°C) and substantial (>2°C) temperature increase.     

Colonization preference of Euschistus servus and Nezara viridula in transgenic cotton varieties,peanut, and soybean

Producers of Bt cotton, Gossypium hirsutum L. (Malvaceae), in the southeastern USA face significant losses from highly polyphagous stink bug species. These problems may be exacerbated by crop rotation practices that often result in cotton, peanut, Arachis hypogaea L., and soybean, Glycine max (L.) Merrill (both Fabaceae), growing in close proximity to one another. Because all of these crops are hosts for the major pest stink bug species in the region, we experimentally examined colonization preference of these species among the crops to clarify this aspect of their population dynamics. We planted peanut, soybean, Bt cotton, and glyphosate‐tolerant (RR) non‐Bt cotton at three sites over 3 years in replicated plots ranging from 192 to 1 323 m² and calculated odds ratios for colonization of each crop for Nezara viridula (L.) and Euschistus servus (Say) (both Hemiptera: Pentatomidae). In four of five experiments, both E. servus and N. viridula preferred soybean significantly more often than Bt cotton, non‐Bt cotton, and peanut. Neither N. viridula nor E. servus showed any preference between non‐Bt and Bt cotton in any experiment. Both species had higher numbers in Bt and non‐Bt cotton relative to peanut; this was not significant for any single experiment, but analyses across all experiments indicated that N. viridula preferred Bt and non‐Bt cotton significantly more often than peanut. Our results suggest that soybean in the landscape may function as a sink for stink bug populations relative to nearby peanut and cotton when the soybean is in the reproductive stage of development. Stink bug preference for soybean may reduce pest pressure in near‐by crops, but population increases in soybean could lead to this crop functioning as a source for later‐season pest pressure in cotton.