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.     

Composition and abundance of stink bugs (Heteroptera: Pentatomidae) in corn

The species composition and abundance of stink bugs (Heteroptera: Pentatomidae) in corn, Zea mays L., was determined in this on-farm study in Georgia. Seven species of phytophagous stink bugs were found on corn with the predominant species being Nezara viridula (L.) and Euschistus servus (Say). All developmental stages of these two pests were found, indicating they were developing on the corn crop. The remaining five species, Oebalus pugnax pugnax (F.), Euschistus quadrator (Rolston), Euschistus tristigmus (Say), Euschistus ictericus (L.), and Acrosternum hilare (Say), were found in relatively low numbers. Adult N. viridula were parasitized by the tachinid parasitoid Trichopoda pennipes (F.). There was a pronounced edge effect in distribution of stink bugs in corn. Population dynamics of N. viridula and E. servus were different on early and late-planted corn. Oviposition by females of both stink bug species occurred in mid-to-late-May and again mid-to-late-June in corn, regardless of planting date. In early planted fields, if stink bug females oviposited on corn in mid-July, the resulting nymphs did not survive to the adult stage in corn because ears were close to physiological maturity and leaves were senescing. Density of stink bug adults in early planted corn was relatively low throughout the growing season. In late-planted corn, females of both stink bug species consistently laid eggs in mid-to-late-July on corn with developing ears. This habitat favored continued nymph development, and the resulting adult population reached high levels. These results indicate that corn management practices play a key role in the ecology of stink bugs in corn agroecosystems and provide information for designing management strategies to suppress stink bugs in farmscapes with corn.     

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.     

Parasitism and predation of stink bug (Heteroptera: Pentatomidae) eggs in Georgia corn fields

Nezara viridula L. and Euschistus servus (Say) are the predominant species of phytophagous stink bugs on corn, Zea mays L., in Georgia. Oebalus pugnax pugnax (F.) occurs in relatively low numbers, and the predatory stink bug Podisus maculiventris (Say) is commonly found. Limited information is available on natural biological control of these four stink bug species in Georgia corn fields; therefore, a 6-yr study of parasitism and predation of their eggs was initiated in 2003. Naturally occurring stink bug eggs were parasitized by six scelionid species, Trissolcus basalis (Wollaston), T. thyantae Ashmead, T. brochymenae (Ashmead), T. euschisti (Ashmead), Telenomus podisi Ashmead, Telenomus calvus Johnson, and one encyrtid species, Ooencyrtus sp. T. basalis was the most prevalent parasitoid of N. viridula, parasitizing E. servus and P. maculiventris eggs at low levels. T. podisi, the predominant parasitoid species emerging from eggs of E. servus and P. maculiventris, also parasitized O. p. pugnax eggs exclusively and parasitized N. viridula eggs at low levels. T. euschisti and T. thyantae parasitized E. servus egg masses. T. brochymenae parasitized eggs of both E. servus and P. maculiventris. T. calvus parasitized only P. maculiventris eggs. The same species of egg parasitoids that parasitized naturally occurring eggs of N. viridula and E. servus parasitized sentinel eggs of these bugs, except that no T. calvus and Ooencyrtus sp. were obtained from sentinel eggs, and T. thyantae and T. brochymenae emerged from sentinel eggs of N. viridula. Generally, parasitization of an egg mass was either greater than or equal to predation of sentinel eggs of N. viridula and E. servus. However, on some dates in late June and July, predation of sentinel egg masses was numerically approximately twice as high as parasitism. Results indicate stink bug egg parasitoids and predators are significant factors in the natural biological control of stink bugs in corn 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.     

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.

     

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.

     

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.     

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.     

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.     

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.     

Influence of non‐crop plants on stink bug (Hemiptera: Pentatomidae) and natural enemy abundance in tomatoes

We investigated the effects of weed hosts on stink bug density and damage (Euschistus conspersus Uhler and Thyanta pallidovirens Stal), and a nectar bearing plant on natural enemies of stink bugs in the Sacramento Valley of California. Stink bug density and fruit damage were evaluated in processing tomatoes adjacent to weedy and cultivated borders. The density of E. conspersus was significantly greater in tomatoes adjacent to weedy borders in July but not during August/September. Thyanta pallidovirens was less abundant overall (19%), but was found in significantly greater densities adjacent to cultivated borders in July but not in August/September. Mean percent fruit damage by stink bugs was greater adjacent to the weedy border than the cultivated border, but this difference was not significant. Stink bug egg parasitism and generalist predator density were evaluated in fresh market tomatoes adjacent to a sweet alyssum (Lobularia maritima L.) border and an unplanted control border at three sites. Egg parasitism was significantly greater in the alyssum treatment for the 9–12 September sampling period. Jalysus wickhami VanDuzee (Hemiptera: Berytidae) density was significantly greater in the alyssum treatment in mid‐June. No other significant differences in predator populations were detected. Results of these two studies show that habitat manipulations have the potential to reduce densities of E. conspersus in tomato, the first step in developing a farmscape management plan for stink bug control.     

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

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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.     

An invertebrate [hydroxyproline]-modified neuropeptide: further evidence for a close evolutionary relationship between insect adipokinetic hormone and mammalian gonadotropin hormone family

An octapeptide of the adipokinetic hormone (AKH) peptide family is identified in the corpora cardiaca of the stink bug, Nezara viridula, by ESI-MS^N (electrospray ionization multistage MS). This is the second AKH in N. viridula and it has a hydroxyproline residue at position 6, whereas the major AKH (known as Panbo-RPCH) has Pro as the sixth amino acid residue. The correct sequence assignment of [Hyp⁶]-Panbo-RPCH is confirmed by retention time and MS spectra of the synthetic peptide. Various extraction procedures were followed to ascertain whether the hydroxylation is an artefact of extraction, or whether it is due to a true post-translational modification at the prohormone level. The proline hydroxylation is unique for invertebrate neuropeptides, while it has been described in the vertebrate gonadotropin-releasing hormone (GnRH). The current finding is another piece of evidence that AKH and GnRH form a peptide superfamily and are closely related evolutionarily. Biologically, [Hyp⁶]-Panbo-RPCH is active in vivo as an AKH, causing hyperlipaemia in the stink bug at low doses, indicating again that it is an endogenous, mature and functional hormone in this insect species.     

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.     

Impact of brown stink bug (Heteroptera: Pentatomidae) feeding on corn grain yield components and quality

Brown stink bug, Euschistus servus (Say) (Heteroptera: Pentatomidae), damage on developing corn, Zea mays L., ears was examined in 2005 and 2006 by using eight parameters related to its yield and kernel quality. Stink bug infestations were initiated when the corn plants were at tasseling (VT), mid-silking (R1), and blister (R2) stages by using zero, three, and six in 2005 or zero, one, two, and four bugs per ear in 2006, and maintained for 9 d. The percentage of discolored kernels was affected by stink bug number in both years, but not always affected by plant growth stage. The growth stage effect on the percentage of discolored kernels was significant in 2006, but not in 2005. The percentage of aborted kernels was affected by both stink bug number and plant growth stage in 2005 but not in 2006. Kernel weight was significantly reduced when three E. sercus adults were confined on a corn ear at stage VT or R1 for 9 d in 2005, whereas one or two adults per ear resulted in no kernel weight loss, but four E. servus adults did cause significant kernel weight loss at stage VT in 2006. Stink bug feeding injury at stage R2 did not affect kernel damage, ear weight or grain weight in either year. The infestation duration (9 or 18 d) was positively correlated to the percentage of discolored kernels but did not affect kernel or ear weight. Based on the regression equations between the kernel weight and stink bug number, the gain threshold or economic injury level should be 0.5 bugs per ear for 9 d at stage VT and less for stage R1. This information will be useful in developing management guidelines for stink bugs in field corn during ear formation and early grain filling stages.     

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.     

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.     

The effect of vibratory disturbance on sexual behaviour of the southern green stink bug Nezara viridula (Heteroptera, Pentatomidae)

The effect of vibratory disturbance on sexual behaviour and substrate-borne sound communication of the southern green stink bug, Nezara viridula L. was studied. Disturbance signals do not change the time N. viridula males need to locate the source of vibratory signals, but decrease the number of males responding with the calling and courtship song to calling females. Female N. viridula proceed calling during stimulation with disturbance signals but some of them change the song rhythm by skipping one or more signal intervals or emitting the repelling signals. The number of females which change the dominant frequency of the calling song decreases proportionally with increasing differences between the dominant frequency of the disturbance signals and the emitted female calling song. Variation of the song dominant frequency probably serves females to avoid interference by increasing the signal to noise ratio. Signal duration and repetition rate do not change significantly when the female is stimulated with the disturbance signals. This indicates that frequency shift by calling females is the main strategy for reducing interference by competitive signalers in N. viridula vibrational communication.