Raúl A. Laumann

Induced volatiles in soybean and pigeon pea plants artificially infested with the neotropical brown stink bug, Euschistus heros, and their effect on the egg parasitoid, Telenomus podisi

Herbivory is known to increase the emission of volatiles, which attract natural enemies to herbivore‐damaged plants in laboratory and agricultural systems. We report on signalling through volatiles induced by Euschistus heros (F.) (Heteroptera: Pentatomidae) in two legumes that influence the attraction and retention of the egg parasitoid Telenomus podisi (Ashmead) (Hymenoptera: Scelionidae). Air‐borne extracts obtained from two host plants of E. heros, soybean, Glycine max, and pigeon pea, Cajanus cajan (Leguminosae), produce a different blend of emitted volatiles when attacked by adult males or females and nymphs of the pest species, compared with the undamaged plants. The same results were obtained when the plants were treated with extracted saliva of E. heros which had been mechanically introduced into the plants. This indicates that some substance in the saliva contributed to the release of the volatiles. Bioassays in a Y‐tube olfactometer with female T. podisi and treated plants confirmed the significant preference of the egg parasitoid for plants attacked by either males, females, or fourth instar nymphs of the pest species. On the other hand, volatile extracts obtained from soybean subjected to the velvetbean caterpillar, Anticarsia gemmatalis, a non‐host species for T. podisi, showed a different blend of volatiles compared to those obtained from plants subjected to E. heros. Additionally, the volatiles obtained from this plant–host complex were not attractive to T. podisi. These results indicate that E. heros causes an increase in the emission of specific plant volatiles, and that the induction is possibly caused by an elicitor present in the pest saliva. The possibility that these plant volatiles play an important role in the attraction and retention of the egg parasitoid T. podisi is discussed.

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 herbivores 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.

Volatiles Mediating a Plant-Herbivore-Natural Enemy Interaction in Resistant and Susceptible Soybean Cultivars

Several studies have shown that herbivore-induced plant volatiles act directly on herbivores and indirectly on their natural enemies. However, little is known about the effect of herbivore damage on resistant and susceptible plant cultivars and its effect on their natural enemies. Thus, the aim of this study was to evaluate the attraction of the herbivorous pentatomid bug Euschistus heros and its egg parasitoid Telenomus podisi to two resistant and one susceptible soybean cultivars with different types of damage (herbivory, herbivory+oviposition, and oviposition). In a Y-tube olfactometer, the parasitoids were attracted to herbivory and herbivory+oviposition damaged soybean plants when compared to undamaged soybean plants for the resistant cultivars, but did not show preference for the susceptible cultivar Silvânia in any of the damage treatments. The plant volatiles emitted by oviposition-damaged plants in the three cultivars did not attract the egg parasitoid. In four-arm-olfactometer bioassays, E. heros females did not show preference for odors of damaged or undamaged soybean plants of the three cultivars studied. The Principal Response Curves (PRC) analysis showed consistent variability over time in the chemical profile of volatiles between treatments for the resistant cultivar Dowling. The compounds that most contributed to the divergence between damaged soybean plants compared to undamaged plants were (E,E)-α-farnesene, methyl salicylate, (Z)-3-hexenyl acetate, and (E)-2-octen-1-ol.

The chemical volatiles (Semiochemicals) produced by neotropical stink bugs (Hemiptera: Pentatomidae)

In recent years the growing concern about environmental changes and how we are using the natural resources have triggered a search for natural products as alternatives to synthetic pesticides. The stink bugs produce a wide variety of chemical compounds (semiochemicals) that show potential to manage these insects. The stink bugs Chinavia impicticornis (Stål), C. ubica (Rolston), Dichelops melacanthus (Dallas), Euschistus heros (F.), Piezodorus guildinii (Westwood), Thyanta perditor (Westwood) and Tibraca limbativentris (Stål) had their blends of defensive compounds evaluated both qualitative and quantitatively. The main compounds identified on the glands of Brazilian stink bugs are: 2-alkenals, mainly the E isomer; saturated aliphatic hydrocarbons; and 4 oxo-(E)-2-alkenals. The first sex attractant determined from a stink bug was obtained from Nezara viridula L., and consists on a mix of two isomers cis - and trans bisabolene-epoxides. Later the soybean stink bug E. heros was also studied and its sex attractant was identified as three esters methyl: 2,6,10-trimethyldecanoate, methyl 2,6,10-trimethyldodecanoate, and methyl E2, Z4-decadienoate. Recently, three new Brazilian sting bugs were studied and had their sex attractant elucidated. Males of T. perditor produce the ester, methyl 2E,4Z,6Z-decatrienoate. Whereas, the stink bug, P. guildinii has as sexual pheromone, the sesquiterpene beta-sesquiphellandrene, and the stink bug T. limbativentris produces as sex attractant the zingiberenol. In this review we discuss the advances obtained on the behaviour and identification of sex and defensive compound of stink bugs from Brazilian crops and the application of this knowledge to manage the stink bugs.

Vibratory signals of four Neotropical stink bug species

Abstract.  The stink bugs Acrosternum impicticorne, Euschistus heros, Piezodorus guildinii and Thyanta perditor (Heteroptera: Pentatomidae) feed and mate on the same host plants and constitute major components of the soybean pest complex in Brazil. During mating, they communicate with species and sex‐specific vibratory signals whose spectral properties are characteristic of the subfamily Pentatominae. Songs differ between species in the time structure and amplitude modulation of their units. The repertoire of A. impicticorne, E. heros and T. perditor fits into the scheme described for most investigated stink bugs: females call with a sequence of pulses that differ between species in their duration and repetition rate, and males respond with courtship songs of species‐specific temporal structure and amplitude modulation of complex pulse trains. Female calling and male courtship songs are the main constituents of vibratory communication between sexes in the mating period. The other vibratory emissions appear to represent either transitional songs, support recognition during close‐range courtship, or are involved in male rivalry. The first recorded vibratory emissions of P. guildinii confirm that the genus Piezodorus represents an exception within the Pentatominae. Irregularly repeated female vibratory signals of P. guildinii do not trigger typical male courtship responses as they would in the small stink bugs Holcostethus strictus and Murgantia histrionica. On the other hand, complex rivalry with extensive frequency modulation of pulses, as also described in Piezodorus lituratus, opens a new insight into the role of vibratory communication in stink bugs.

Response of the egg parasitoids Trissolcus basalis and Telenomus podisi to compounds from defensive secretions of stink bugs.

We tested the hypotheses that host-searching behavior of the egg parasitoids Telenomus podisi and Trissolcus basalis may be differentially influenced by the different blends of volatiles released from the metathoracic glands of adult stink bug host species. We further studied whether such a differential response is due to different individual components of these glands and whether these responses reflect host preferences. Y-tube olfactometer bioassays were carried out with crude extracts of metathoracic glands of five different host species of neotropical stink bugs. Additionally, we tested the parasitoids’ responses to synthetic standards of individual compounds identified in these stink bug glands. Results showed that females of T. basalis and T. podisi responded differentially to crude gland extracts of the different species of host stink bugs and to the compounds tested. The parasitoid T. basalis showed a positive taxic behavior to Nezara viridula methathoracxic gland extracts of a host species preferred in the field, i.e., N. viridula. Furthermore, T. basalis responded positively to 4-oxo-(E)-2-hexenal and (E)-2-decenal, two components of N. viridula glandular secretion. Higher residence time, reduced linear velocity, and higher tortuosity in the arm of the olfactometer supplied with 4-oxo-(E)-2-hexenal showed that this compound modifies the kinetics of some traits of T. basalis walking pattern and suggests that it might stimulate the searching behavior of this parasitoid. The parasitoid T. podisi was attracted to crude gland extracts of the preferred host (Euschistus heros) and also to 4-oxo-(E)-2-hexenal. Additionally, this parasitoid responded positively to (E)-2-hexenal and to the hydrocarbon tridecane, both of which are defensive compounds released from the metathoracic glands by several stink bugs. The results indicate some degree of specialization in the response of two generalist parasitoid species toward defensive secretions of stink bugs.

Response of the parasitoid Telenomus podisi to induced volatiles from soybean damaged by stink bug herbivory and oviposition

Abstract Egg parasitoids have a short time frame in which their host eggs are suitable for parasitism, and in several systems these parasitoids respond to plant volatiles induced by oviposition on the plant (either in isolation or in combination with feeding damage) as a means of finding suitable hosts. It is known that the parasitoid of pentatomid eggs Telenomus podisi responds to damage done to soybeans by female Euschistus heros, its preferred host. In this study our aim was to determine the type of E. heros damage to soybean (herbivory, oviposition or a combination of both) necessary for attraction of T. podisi. In a Y-tube olfactometer the parasitoid has shown to respond to the undamaged plant over clean air and herbivory-damaged plants over undamaged plants. However, the parasitoids did not respond to the treatments where oviposition occurred, either in isolation or in combination with herbivory. Analysis of volatile blends revealed that herbivory plus oviposition damage to soybean induced a volatile blend different to those induced when herbivory or oviposition occurred separately. These results, along with other results from this system, suggest that T. podisi uses plant volatile cues associated with female E. heros damage in order to be present when E. heros lays its eggs, and thus ensure its resource is optimal for parasitism.

Semiochemicals from Herbivory Induced Cotton Plants Enhance the Foraging Behavior of the Cotton Boll Weevil, Anthonomus grandis

The boll weevil, Anthonomus grandis, has been monitored through deployment of traps baited with aggregation pheromone components. However, field studies have shown that the number of insects caught in these traps is significantly reduced during cotton squaring, suggesting that volatiles produced by plants at this phenological stage may be involved in attraction. Here, we evaluated the chemical profile of volatile organic compounds (VOCs) emitted by undamaged or damaged cotton plants at different phenological stages, under different infestation conditions, and determined the attractiveness of these VOCs to adults of A. grandis. In addition, we investigated whether or not VOCs released by cotton plants enhanced the attractiveness of the aggregation pheromone emitted by male boll weevils. Behavioral responses of A. grandis to VOCs from conspecific-damaged, heterospecific-damaged (Spodoptera frugiperda and Euschistus heros) and undamaged cotton plants, at different phenological stages, were assessed in Y-tube olfactometers. The results showed that volatiles emitted from reproductive cotton plants damaged by conspecifics were attractive to adults boll weevils, whereas volatiles induced by heterospecific herbivores were not as attractive. Additionally, addition of boll weevil-induced volatiles from reproductive cotton plants to aggregation pheromone gave increased attraction, relative to the pheromone alone. The VOC profiles of undamaged and mechanically damaged cotton plants, in both phenological stages, were not different. Chemical analysis showed that cotton plants produced qualitatively similar volatile profiles regardless of damage type, but the quantities produced differed according to the plant’s phenological stage and the herbivore species. Notably, vegetative cotton plants released higher amounts of VOCs compared to reproductive plants. At both stages, the highest rate of VOC release was observed in A. grandis-damaged plants. Results show that A. grandis uses conspecific herbivore-induced volatiles in host location, and that homoterpene compounds, such as (E)-4,8-dimethylnona-1,3,7–triene and (E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene and the monoterpene (E)-ocimene, may be involved in preference for host plants at the reproductive stage.

Monitoring the Neotropical brown stink bug Euschistus heros (F.) (Hemiptera: Pentatomidae) with pheromone‐baited traps in soybean fields

The effectiveness of the synthetic sex pheromone of the Neotropical brown stink bug, Euschistus heros, was evaluated both in laboratory and in field assays. Lures loaded with 1 mg of methyl 2,6,10‐trimethyltridecanoate (TMTD) continuously attracted female bugs for more than 30 days to pheromone‐baited traps in field trials. The pheromone‐baited traps were effective in field tests even at low bug population densities, as compared with the usual monitoring technique, shake cloth sampling. Traps around borders or in the centre of soybean fields caught similar numbers of bugs. Trap captures showed a positive relationship with field populations, as monitored with the shake cloth technique, during the reproductive phase of the soybean crop, i.e. from the R1–R5 developmental stage (pod formation to pod fill). The physiological state of the trapped migrating insects was determined. The first insects arriving in the field had fewer eggs in the reproductive tract compared to later arrivals. Some cross‐attraction was also observed, with Piezodorus guildinii and Edessa meditabunda also being caught in pheromone‐baited traps, suggesting that these insects respond to the sex pheromone or to the defensive compounds released by E. heros captured in traps. In brief, the results showed that traps baited with 1 mg of the sex pheromone efficiently caught bugs, that the lures lasted for more than 1 month under field conditions and that placement of traps around the borders of the crop area was as effective as placement inside the crop area. Border‐placed traps were effective at a density of one trap every 200 m.

Odour masking of tomato volatiles by coriander volatiles in host plant selection of Bemisia tabaci biotype B

The silverleaf whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), is one of the most important pest insects in tomato crop systems worldwide. It has been previously demonstrated that intercropping tomato [Solanum lycopersicum L. Mill. (Solanaceae)] with coriander [Coriandrum sativum L. (Apiaceae)] reduces the incidence and severity of damage caused by B. tabaci. However, it is not yet known how coriander affects the insect′s behaviour. We evaluated the attractiveness of tomato constitutive volatiles to B. tabaci and what effect coriander constitutive volatiles have on the insect′s behaviour. To this end, we conducted three bioassays in a multiple‐choice four‐arm olfactometer (‘×’ type), measuring B. tabaci behaviour when offered tomato and coriander constitutive volatiles presented alone as well as together. We also evaluated the colonisation and establishment of B. tabaci in experimental plots with only single tomato plants and tomatoes intercropped with coriander in a greenhouse. Bemisia tabaci males and females recognised tomato constitutive volatiles as a positive stimulus (kairomonal effect), indicating that semiochemicals from this plant can play an important role in the insect’s host plant selection. Coriander constitutive volatiles reduced the attractiveness of tomato volatiles but no repellency to these volatiles was observed. Greater numbers of adults and nymphs of B. tabaci per plant were observed in tomato monoculture plots than in tomato intercropped with coriander. We suggest that coriander constitutive volatiles have an odour masking effect on tomato volatiles, thus interfering in the host plant selection of B. tabaci.