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.     

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.

     

Assessing stink bug resistance in soybean breeding lines containing genes from germplasm IAC-100

Sixty-five soybean, Glycine max (L.) Merr., breeding lines containing the stink bug resistant 'IAC-100' in their pedigrees were evaluated for their resistance to stink bug, primarily southern green stink bug, Nezara viridula L., feeding in replicated field trials from 2001 to 2005. Plots were sampled throughout the season for stink bug abundance, and, at harvest, seed samples were rated for stink bug-induced kernel damage. Individual seeds were categorized as having none, light, moderate, or heavy damage plus 100-seed wt and plot yields were determined. Both ground cloth and sweep net sampling procedures were used to compare stink bug densities between the soybean entries. Stink bug densities varied between years; however, in the years when populations exceeded four per row-meter or six per 25 sweeps, there were more damaged soybean seeds (>25%) in the entries with higher stink bug numbers. During the first 2 yr of evaluations, the mean stink bug-damaged soybean seeds ranged from 10.0 to 38.2%. From these differential responses, 28 entries were selected for continued study in 2003-2004. In 2003, stink bug-damaged soybean seeds were low, with damage ranging from 2.9 to 18.2%. In 2004, stink bug damage ranged from 8.8 to 53.2%. From these 28 lines, 12 entries were selected for an advanced field screening trial in 2005, including the IAC-100 and 'Hutcheson'. Damaged soybean seeds ranged from 18.5 to 54.1% among these 12 entries in 2005, under heavy stink bug pressure. From these evaluations, four breeding lines with either Hutcheson X IAC-100 or IAC-100 x 'V71-370' in their genealogy were identified as possible breeding material for future soybean stink bug resistance cultivar development.     

Feeding Activity, Salivary Amylase Activity, and Superficial Damage to Soybean Seed by Adult Edessa meditabunda (F.) and Euschistus heros (F.) (Hemiptera: Pentatomidae)

Greenhouse and laboratory studies were conducted to evaluate feeding activity and superficial damage to soybean seed by the brown-winged stink bug, Edessa meditabunda (F.), and the Neotropical brown stink bug, Euschistus heros (F.). Soybean plants (cv. BRS 282), at R6 stage of development were used. Thirty pairs of each species were used individually for 48?h. Two daily observations (9:00?AM and 3:00?PM) were taken to record the number of bugs (feeding/resting) on plant parts. Harvested seeds imbibed in tetrazolium solution were photographed for measurement of the damaged surface. Adult E. meditabunda significantly preferred soybean stems (19.7 bugs) to pods (2.7). Feeding/resting was similar at 9:00?AM (mean number of 28.0 bugs) and 3:00?PM (24.3). Euschistus heros equally fed/stayed on stems (7.3 bugs) and pods (6.9), although most bugs (12.3) remained on the cage net; feeding/resting on all plant structures amounted to 13.7 bugs at 9:00?AM and 17.7 bugs at 3:00?PM. Amylase activity was greater for E. heros (41.61?±?0.89?U/mg) and almost none for E. meditabunda (2.35?±?0.14?U/mg). The superficial damage to seeds was significantly greater for E. meditabunda (22. 9?mm²) compared to E. heros (12.5?mm²). However, E. meditabunda caused less shrinkage of the seed tegument, while E. heros damage was deeper and seeds showed reduction in size.     

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.     

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.     

Toxicity of insecticides in a glass-vial bioassay to adult brown, green, and southern green stink bugs (Heteroptera: Pentatomidae)

Adult brown, Euschistus servus (Say); green, Acrosternum hilare (Say); and southern green, Nezara viridula (L.), stink bugs were collected from soybean, Glycine max (L.) Merr., in fall 2001 and 2002 near Stoneville, MS, and Eudora, AR. A glass-vial bioassay was used to determine LC50 values for the three species of stink bugs for the pyrethroids bifenthrin, cypermethrin, cyfluthrin, lambda-cyhalothrin, and permethrin, and the organophosphates acephate, dicrotophos, malathion, and methyl parathion. Results confirmed findings of other researchers that the brown stink bug was less susceptible to pyrethroid and organophosphate insecticides than were green and southern green stink bugs. The susceptibility of all three stink bug species to the insecticides tested was very similar at both test locations. The study established baseline insecticide mortality data from two locations in the mid-South for three stink bug species that are pests of soybean and cotton, Gossypium spp. Data from the tests are valuable for future use in studies on resistance and in resistance monitoring programs.     

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.     

Field screening of experimental corn hybrids and inbred lines for multiple ear-feeding insect resistance

Identifying and using native insect resistance genes is the core of integrated pest management. In this study, 10 experimental corn, Zea mays L., hybrids and 10 inbred lines were screened for resistance to major ear-feeding insects in the southeastern Coastal Plain region of the United States during 2004 and 2005. Ear-feeding insect damage was assessed at harvest by visual damage rating for the corn earworm, Helicoverpa zea (Boddie), and by the percentage of kernels damaged by the maize weevil, Sitophilus zeamais Motschulsky, and stink bugs [combination of Euschistus servus (Say) and southern green stink bug, Nezara viridula (L.)]. Among the eight inbred lines and two control populations examined, C3S1B73-5b was resistant to corn earworm, maize weevil, and stink bugs. In contrast, C3S1B73-4 was resistant to corn earworm and stink bugs, but not to maize weevil. In a similar manner, the corn hybrid S1W*CML343 was resistant to all three ear-feeding insects, whereas hybrid C3S1B73-3*Tx205 was resistant to corn earworm and maize weevil in both growing seasons, but susceptible to stink bugs in 2005. The silk-feeding bioassay showed that corn earworm developed better on corn silk than did fall armyworm. Among all phenotypic traits examined (i.e., corn ear size, husk extension, and husk tightness), only corn ear size was negatively correlated to corn earworm damage in the inbred lines examined, whereas only husk extension (i.e., coverage) was negatively correlated to both corn earworm and maize weevil damage on the experimental hybrids examined. Such information could be used to establish a baseline for developing agronomically elite corn germplasm that confers multiple ear-feeding insect resistance.     

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.

     

Attraction of the stink bug egg parasitoid Telenomus podisi to defence signals from soybean activated by treatment with cis-jasmone

After herbivore attack or chemical activation, plants release a blend of volatile organic compounds (VOCs) that is qualitatively or quantitatively different to the blend emitted by an undamaged plant. The altered blend of VOCs is then usually attractive to the herbivore's natural enemies. Soybean, Glycine max (L.) (Fabaceae), when damaged by stink bug herbivory, has been shown to emit a blend of VOCs that attracts the stink bug egg parasitoid Telenomus podisi (Ashmead) (Hymenoptera: Scelionidae) to the plant. In this study, our aim was to investigate changes in the VOC profile of soybean (var. BR16) elicited by the naturally occurring plant activator cis -jasmone, and to determine whether these changes elicited the attraction of T. podisi . cis -Jasmone elicited chemical defence in soybean similar to that previously reported for stink bug damage. The main components induced by cis- jasmone were camphene, myrcene, ( E )-ocimene, methyl salicylate, and ( E , E )-4,8,12-trimethyltrideca-1,3,7,11-tetraene. In Y-tube behavioural bioassays, T. podisi preferred cis -jasmone treated plants over untreated plants. Thus, cis -jasmone appears to induce defence pathways in soybean similar to those induced by stink bug damage, and this phenomenon appears to be a promising tool for the manipulation of beneficial natural enemies in future sustainable stink bug control strategies. The delay in response demonstrates that cis -jasmone treatment is not directly causing the response, but, more importantly, that it is causing activation of induced defence, long after initial treatment.     

Delayed maturity associated with southern green stink bug (Heteroptera: Pentatomidae) injury at various soybean phenological stages

Delayed maturity in soybean, Glycine max (L.) Merr., occurred in response to infestation by southern green stink bug, Nezara viridula (L.), in 4 yr of field studies. Maturity delays followed stink bug infestation that occurred only during the pod set and filling stages (R3-R5.5), and infestations at R3-4 and R5 resulted in delayed maturity more consistently than did infestation at R5.5. Infestation levels of six stink bugs per 0.3 m of row for 7-14 d generally were required to delay soybean maturity. The greatest impact on seed yield and quality parameters followed stink bug infestations that occurred during R3-R5.5, which corresponded closely with the periods of infestation that resulted in delayed maturity. If both delayed maturity and yield reduction are considered, the pod elongation through late pod filling stages were most critical for protecting soybeans from southern green stink bugs.     

Attractiveness of conspecific stink bugs to adult stink bug-baited traps in soybean fields

The attractiveness of live adult stink bugs used as baits in traps in soybean fields, Milyang, Korea, to conspecific stink bugs was evaluated. Both sexes of bean bug, Riptortus pedestris Fabricius (Hemiptera: Alididae), and one-banded stink bug, Piezodorus hybneri Gmelin (Hemiptera: Pentatomidae), were attracted to conspecific male adults-baited traps. Likewise, both sexes of brown-marmorated stink bug, Halyomorpha halys Stål (Hemiptera: Pentatomidae), and sole bug, Dolycoris baccarum L. (Hemiptera: Pentatomidae), were attracted to traps baited with conspecific male stink bugs. However, in Nezara antennata Scott (Hemiptera: Pentatomidae), both male and female used as baits in traps were attractive to conspecific adults. Accordingly, these results suggest that the only male adults of H. halys and D. baccarum and both sexes of N. antennata are attractive to conspecific male stink bugs.     

Spatial distribution and sampling plan of the phytophagous stink bug complex in different soybean production systems

Phytophagous stink bugs are major soybean pests, and knowledge of spatial distribution models of the pest in the crop is fundamental to establishing an appropriate sequential sampling plan, and thus, allowing the correct utilization of control strategies. This work aimed to study the spatial distribution of phytophagous stink bugs in soybean grown in different cropping systems and determine a sequential sampling plan. The experiment was conducted in Maracaju, MS, Brazil, during the agricultural year of 2012/2013. Soybean cultivars BRS 284 and SYN 1163 RR were placed in an experimental area comprising six fields (two soybean cultivars × three cropping systems). Sampling was performed weekly, using a beat cloth per plot and counting the number of stink bugs found, virtually throughout the soybean reproductive period. Concerning the statistical analyses, we used the dispersion indexes (variance‐to‐mean ratio, Morisita's index, exponent k of the negative binomial and Green's coefficient) and probabilistic methods of frequency adjustment (negative binomial and Poisson). Adult and nymph phytophagous stink bugs showed aggregate disposition in the field regardless of the cropping system, and their numbers were adjusted to the negative binomial probability distribution. There was no difference in the behaviour of adult and nymphs considering the tested cultivars. We elaborated a practical sequential sampling plan for phytophagous stink bug complexes, considering crops intended for the production of grains and seeds.     

Duration of feeding and superficial and in-depth damage to soybean seed by selected species of stink bugs (Heteroptera: Pentatomidae)

Laboratory studies were conducted to compare duration of feeding and superficial and in-depth damage to soybean (Glycine max) seeds by the Southern green stink bug, Nezara viridula (L.), the Neotropical brown stink bug, Euschistus heros (F.), the red-banded stink bug, Piezodorus guildinii (Westwood), and the green-belly stink bug, Dichelops melacanthus (Dallas). Results indicated that feeding time was significantly longer for N. viridula (≈ 133 min) compared to E. heros and D. melacanthus (≈ 70 min), but not different from P. guildinii (≈ 103 min). There was a positive correlation between feeding time and the resulting damage for E. heros, N. viridula and P. guildinii (R2 > 0.80, P < 0.0001), but not for D. melacanthus (R2 = 0.1011, P = 0.1493). The deepest seed damage (2.0 mm) was made by P. guildinii and the shallowest (0.5 mm) by D. melacanthus. The depth of the seed damage by E. heros and N. viridula (0.8, 1.2 mm, respectively) was intermediate in comparison to the other species studied. Feeding damage to the seed endosperm caused variable cell disruption and protein body dissolution, particularly when P. guildinii fed on seeds, suggesting that the deleterious action of salivary enzymes was greater for this bug compared to the others.     

Treatment thresholds for stink bugs (Hemiptera: Pentatomidae) in cotton

The green stink bug, Acrosternum hilare (Say), the southern green stink bug, Nezara viridula (L), and the brown stink bug, Euschistus servus (Say), were predominant phytophagous Pentatomidae detected during 1995-1997 in cotton in South Carolina. These species occurred in similar numbers in conventional and transgenic cotton 'NuCOTN33B', containing the gene for expression of CryIA(c) delta-endotoxin of Bacillus thuringiensis Berliner variety kurstaki. Adult stink bugs moved into cotton from wild and cultivated alternate hosts during July, and reproducing populations usually were detected in cotton from late July into September. Applications of either methyl parathion (0.56 kg [AI]/ha) directed for stink bugs or lambda-cyhalothrin (0.037 kg [AI]/ha) or cyfluthrin (0.056 kg [AI]/ha) for control of cotton bollworm, Helicoverpa zea (Boddie), provided effective control of pentatomids in NuCOTN33B or conventional 'DP5415' and increased yields compared with untreated plots. Fiber quality did not differ among treated or untreated plots of NuCOTN33B. The ground-cloth technique was used to estimate populations of stink bugs, and data indicated that treatment at one bug per 2 m of row adequately protected cotton from yield loss due to stink bug damage. Observations on boll damage indicated that treatment might be necessary if >20-25% reveal internal symptoms of feeding injury during mid- to late season. More detailed damage thresholds should be developed to complement an approach based on population monitoring. This study validated current recommendations for management of pentatomids in cotton, demonstrated the necessity of threshold use for stink bugs in transgenic cultivars expressing endotoxin from B. thuringiensis, and provided insight into further development of management options for pentatomids in the crop.     

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.     

Dynamics and seasonal abundance of stink bugs (Heteroptera: Pentatomidae) in a cotton-soybean ecosystem

Two soybean varieties (early-maturing group V and late-maturing group VII) and two cotton varieties (conventional and transgenic (Bt) were grown in adjacent replicated large field plots (approximately 0.1 ha each) at two locations for 3 yr. The dynamics and relative abundance of phytophagous stink bugs within these two crops were observed. The most abundant pentatomid species in both crops for all 3 yr were Nezara viridula (L.), Acrosternum hilare (Say), and Euschistus servus (Say). Several other species also were commonly collected. This is the first record of Mormidea lugens (F.) on soybean and E. quadrator Rolston, E. obscurus (Palisot), Holcostethus limbolarius (St?l), and Oebalus pugnax (F.) on cotton. Stink bugs began arriving in soybean when plant growth stages ranged from pod formation to full seed development. Peak numbers of these insects were found in soybean from the time of full-size seeds in the pods until early maturity. The bugs were first attracted to the earlier maturing cultivar (group V), where they remained until plants began to mature (R7). The pentatomids then moved to the later-maturing cultivar (group VII) as it reached full pod to full seed. Stink bugs began arriving in cotton from the time of the earliest flowers until after the first bolls formed. Peak numbers in cotton occurred during the time when all stages of developing bolls were present. Stink bug numbers were much greater in soybean than in cotton over all three seasons. This preference for soybean over cotton indicates the potential use of soybean as a trap crop for attracting stink bugs away from cotton. Additionally, the coordinated use of early- and late-maturing soybean cultivars as a trap crop could minimize the area requiring insecticides, as well as the number of insecticide applications to cotton.     

A broad-spectrum, efficient and nontransgenic approach to control plant viruses by application of salicylic acid and jasmonic acid

Plant viruses cause many diseases that lead to significant economic losses. However, most of the approaches to control plant viruses, including transgenic processes or drugs are plant-species-limited or virus-species-limited, and not very effective. We introduce an application of jasmonic acid (JA) and salicylic acid (SA), a broad-spectrum, efficient and nontransgenic method, to improve plant resistance to RNA viruses. Applying 0.06?mM JA and then 0.1?mM SA 24?h later, enhanced resistance to Cucumber mosaic virus (CMV), Tobacco mosaic virus (TMV) and Turnip crinkle virus (TCV) in Arabidopsis, tobacco, tomato and hot pepper. The inhibition efficiency to virus replication usually achieved up to 80-90%. The putative molecular mechanism was investigated. Some possible factors affecting the synergism of JA and SA have been defined, including WRKY53, WRKY70, PDF1.2, MPK4, MPK2, MPK3, MPK5, MPK12, MPK14, MKK1, MKK2, and MKK6. All genes involving in the synergism of JA and SA were investigated. This approach is safe to human beings and environmentally friendly and shows potential as a strong tool for crop protection against plant viruses.