Reproductive behaviour and vibratory communication of the neotropical predatory stink bug Podisus nigrispinus

Vibratory communication during reproductive behaviour is less well described in predatory (Asopinae) than in phytophagous (Pentatominae) stink bugs. Different steps in the mating behaviour of the predatory stink bug Podisus nigrispinus (Dallas) (Hemiptera: Pentatomidae; Asopinae) are described in the present study, together with vibratory signals emitted on artificial and natural substrate during courtship and copulation. Vibratory signals in Podisus nigrispinus have a decisive role in copulation success and are produced in both sexes by abdominal vibration and tremulation. In P. nigrispinus, one species‐specific female and two male songs, which do not show the calling function typically found in phytophagous stink bugs, are produced by abdominal vibration and are emitted during reproductive behaviour. Additionally, P. nigrispinus produces tremulatory signals that have no species or sex specificity. Tremulatory signals emitted spontaneously on a plant as a sequence of readily repeated pulses are similar to the calling songs of the Pentatominae stink bug. These signals may carry information on the presence of a mate; however, in other behavioural contexts, they may have a different function, such as advertisement or even alarm signals. Plants transmit vibratory signals produced by both mechanisms as a low‐pass filter, increasing the amount of low‐frequency components. The results of the present study raise important questions about the interaction between chemical and vibratory signals in the mating behaviour of predatory stink bugs.     

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.

     

Vibratory Communication and its Relevance to Reproductive Isolation in two Sympatric Stink Bug Species (Hemiptera: Pentatomidae: Pentatominae)

Communication is in phytophagous stink bugs of the subfamily Pentatominae related to mating behavior that among others includes location and recognition of the partner during calling and courting. Differences in temporal and frequency parameters of vibratory signals contributes to species reproductive isolation. Chinavia impicticornis and C. ubica are two green Neotropical stink bugs that live and mate on the same host plants. We tested the hypothesis that differences in temporal and spectral characteristics of both species vibratory signals enable their recognition to that extent that it interrupts further interspecific communication and copulation. To confirm or reject this hypothesis we monitored both species mating behaviour and recorded their vibratory songs on the non-resonant loudspeaker membranes and on the plant. The level of interspecific vibratory communication was tested also by playback experiments. Reproductive behavior and vibratory communication show similar patterns in both Chinavia species. Differences observed in temporal and spectral characteristics of female and male signals enable species discrimination by PCA analyses. Insects that respond to heterospecific vibratory signals do not step forward to behaviors leading to copulation. Results suggest that species isolation takes place in both investigated Chinavia species at an early stage of mating behavior reducing reproductive interference and the probability of heterospecific mating.     

Vibrational communication and mating behaviour of Dichelops melacanthus (Hemiptera: Pentatomidae) recorded from loudspeaker membranes and plants

Vibrational communication is important for successful mating in various stink bugs species. The vibrational signals from males and females of Dichelops melacanthus Dallas (Hemiptera: Pentatomidae) are recorded from a nonresonant substrate (i.e. a loudspeaker membrane) to characterize the temporal and spectral properties of these vibrational signals, as well as on a resonant substrate (i.e. bean plants) to obtain information about how these signals are altered when they are transmitted through the plants. On the loudspeaker membrane, D. melacanthus males and females emit only one male or one female song, respectively. However, when the insects are placed on bean leaves, a more complex repertoire is recorded, with three different songs for each sex. The first female and male songs appear to have calling functions and the third male and female songs are emitted during courtship. The second female and male songs are emitted after the first song, although their functions in mating behaviour are not clear. The identified repertoire is similar to those of other Neotropical stink bugs, starting with songs 1 and 2 and developing into song 3. Frequency modulation is observed in the female songs recorded from the loudspeaker membrane and the plants. The signals recorded from plants present higher harmonic peaks compared with the signals recorded from the loudspeaker membrane. The presence of species and sex‐specific songs during mating confirms the important role of vibrational communication in mate location and recognition. The temporal and spectral characteristic signals are influenced by the substrate used to record the songs emitted by D. melacanthus.     

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.     

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.     

Stink bug rostrum length vs. stylet penetration potential

Stink bugs (Hemiptera: Pentatomidae) and related species continue to plague cotton, Gossypium hirsutum L. (Malvaceae), worldwide. Stink bugs utilize their stylets (housed within the rostrum) to feed upon cotton bolls and transmit pathogens that cause seed and boll rot of cotton. Stylet penetration potential of stink bugs is influenced by species and recent observations indicated a phenomenon whereby stink bugs with shorter rostra yielded deeper stylet penetration estimates. The objective of this study was to elucidate the relationship between rostrum length and known stylet penetration estimates for two pairs of similar‐sized pentatomid species: Chinavia hilaris (Say) vs. Euschistus servus (Say), and Oebalus pugnax (Fabricius) vs. Piezodorus guildinii Westwood. For each species, individual rostral segments were measured to yield total lengths, and measurements were compared against known stylet penetration estimates. Chinavia hilaris and P. guildinii have longer rostra than E. servus and O. pugnax, respectively, yet E. servus and O. pugnax yielded deeper stylet penetration estimates. Deeper stylet penetration by species with shorter rostra can be attributed to differences in the lengths of rostral segments 1 and 2. Euschistus servus and O. pugnax each had significantly longer rostral segments 1 and 2 than C. hilaris and P. guildinii, respectively. Also, the cumulative lengths of rostral segments 1 and 2 comprised a higher overall proportion of the entire rostrum length in E. servus and O. pugnax vs. C. hilaris and P. guildinii, respectively. Rostral segments 1 and 2 are instrumental in the feeding mechanics of these phytophagous species; it is clear that their greater length and their role in stylet penetration model calculations – including the lengths of segments 3 and 4 – override the presumption that total rostrum length equates to stylet penetration potential. This novel finding contributes to the general knowledge of stink bug feeding mechanics.     

Comparison of Substrate-Borne Vibrational Signals of Two Congeneric Stink Bug Species, Thyanta pallidovirens and T. custator accerra (Heteroptera: Pentatomidae)

Vibrational signals (songs) were recorded and compared for two stink bug species, Thyanta pallidovirens and T. custator accerra. Females of both species produced two songs. Male T. pallidovirens also produced two songs, whereas male T. c. accerra produced four. Songs emitted by females of both species were comparable in structure and function, as was one of the male-produced songs. During the courtship phase of mating behavior, males of both species emitted a song with similar function but different temporal and spectral properties. Basic properties of songs, such as the dominant frequencies, were similar to those of songs of other pentatomid species, but the extensive use of frequency modulation and overlapping duets were novel. Differences in songs, combined with differences in male-produced pheromones, may play a role in the reproductive isolation of these congeners.     

The structure and function of songs emitted by southern green stink bugs from Brazil, Florida, Italy and Slovenia

Nezara viridula (L.) (Pentatomidae: Heteroptera) from Brazil, Florida, Italy and Slovenia, communicate by vibratory songs associated with long‐range calling and close‐range courting, rivalry and repelling. Each song is composed of spectrally and temporally different units. Spectrally different pulses of duration less than 300 ms are present in the male calling song. The female calling song is characterized by pulse trains composed of pulses shorter than 150 ms and pulse trains composed of a longer (> 700 ms) and shorter (< 250 ms) pulse. Shorter and longer pulses have different spectral characteristics. The male and female courtship songs are characterized by fusion of shorter (< 150 ms) pulses into a pulse train usually followed by a shorter (< 200 ms) postpulse in the case of the male courtship song. The female repelling song is a several seconds long vibration of irregular temporal structure. The short (< 400 ms) male rival song pulses are frequency modulated. The dominant frequency peaks of the songs investigated lie between 70 and 130 Hz. The dominant frequency and the microstructure of song spectra show no population specificity. The average duration varies more in calling than in courtship songs. The repetition time varies extensively in songs of different populations. Normal communication followed by copulation was observed between mates from Slovenia and Brazil and between mates from Florida and Italy. The potential role of different temporal and spectral parameters for species recognition and mate location is discussed in view of the expected distortion of the characteristic signal structure during transmission through plants.     

Female competition for availability of males in insects: the Nezara viridula (Linnaeus, 1758) model

Multimodal communication in solitary stinkbugs enables them to meet, mate and copulate. Many plant‐dwelling species exchange information during the calling phase of mating behavior using substrate‐borne vibratory signals. A female‐biased gender ratio induces rivalry and competition for a sexual partner. Female competition for males, first described among Heteroptera in three stinkbug species, revealed species specific differences and opened the question of plasticity in individually emitted temporal and frequency signal characteristics during calling and rival alternation. To address this question and gain an insight into the mechanisms underlying stinkbug female rivalry, we compared the characteristics of alternated signals in the southern green stinkbug Nezara viridula (Linnaeus, 1758) (Hemiptera: Pentatomidae). Compared to male rivalry, female rivalry is more complex, lasts longer and runs through successive phases by a combination of different song types. The male pheromone triggers alternation between females, producing song pulses that occasionally overlap each other. One female initiates the rivalry by changing individual pulses into pulse trains of three different types. The competing female alternates with pulses of changed temporal characteristics at lower levels of rivalry and by varying the frequency characteristics of pulse trains at higher levels. During female rivalry, the male either stops responding or occasionally emits calling and courtship signals in response to the female that has produced signals of steady temporal characteristics. Female rivalry shows complex and species specific patterns of information exchange at different levels with a broad‐range variation of temporal and frequency characteristics of, until now, unidentified vibratory emissions.     

Tremulatory and Abdomen Vibration Signals Enable Communication through Air in the Stink Bug Euschistus heros

Communication by substrate-borne mechanical signals is widespread among animals but remains one of their least understood communication channels. Past studies of vibrational communication in insects have been oriented predominantly to communication during mating, showing that species- and sex-specific vibrational signals enable recognition and localization of potential mates on continuous solid substrates. No special attention has been paid to vibrational signals with less obvious specificity as well as to the possibility of vibrational communication across substrates that are not in physical contact. We aimed to reinvestigate emission of the aforementioned vibrational signals transmitted through a plant in the stink bug Euschistus heros (Pentatomidae: Pentatominae) and to check whether individuals are able to communicate across adjecent, physically separated substrates. We used laser vibrometry for registration of substrate-borne vibrational signals on a bean plant. Using two bean plants separated for 3 to 7 cm between two most adjacent leaves, we investigated the possibility of transmission of these signals through air. Our study showed that males and females of E. heros communicate using tremulatory, percussion and buzzing signals in addition to the previously described signals produced by vibrations of the abdomen. Contrary to the latter, the first three signal types did not differ between sexes or between pentatomid species. Experiments with two physically separated plants showed significant searching behaviour and localization of vibrational signals of an E. heros male or a female, in response to abdominal vibration produced signals of a pair duetting on the neighbouring plant, in comparison to control where no animals were on the neighbouring plant. We also confirmed that transmission through air causes amplitude and frequency decay of vibrational signals, which suggests high-amplitude, low-frequency tremulatory signals of these stink bugs their most plausible way of communication across discontinuous substrates.     

Rivalry between Stink Bug Females in a Vibrational Communication Network

In the field, male pheromone attracts stink bugs to meet on the same plant and triggers females to call a male by the emission of the calling song. As first among Pentatomidae we describe female rivalry in Chinavia impicticornis, C. ubica and Euschistus heros. Rivalry starts in C. impicticornis by synchronized exchange of the first type of the female calling song pulse trains and proceeds by one of them either to change pulse trains from the first to the second type or to produce readily repeated single pulses. Both reactions either inhibit calling of the rival female or trigger her to respond by alternation with the second type of the calling song pulse trains. Female rivalry in C. ubica differs by the emission of the rival song that replaces alternation with the second type of the calling song typical for C. impicticornis. E. heros females synchronize pulses of the calling song duets and induce emission of the female rival song by one of them that partly inhibits singing of the other. These competitive interactions in Chinavia species reduce the proportion of couples when compared with single couples on a plant. Contrary to both Chinavia species, E. heros female rivalry does not inhibit male response, male signals overlap female emissions and create complex vibrations with modified amplitude modulation pattern caused by interference.     

Vibratory signals of the harlequin bug and their transmission through plants

Abstract. Males of the harlequin bug, Murgantia histrionica (Hahn), produce five different vibrational songs, whereas females produce one song. Songs differ from those of other stink bugs primarily in their species‐specific temporal characteristics. The broad band male courtship songs of M. histrionica are achieved by a combination of different frequency modulated and/or narrow band subunits, with several higher harmonic frequencies. Males rather than females initiate substrate‐borne vibrational communication, and the longer‐range calling songs found typically in other pentatomid species are lacking. Interindividual differences in song temporal and spectral characteristics are discussed. Transmission of vibrational songs through a cabbage head is more efficient along veins than along lamina. Attenuation of signals transmitted through veins is low and similar to that reported previously for plant stalks. On the leaf vein, distances between peak amplitude minima and maxima are different for the dominant and subdominant frequencies. At any distance from the vibration source, a different relationship between spectral peak amplitudes can be recorded. Resolution of these differences, together with velocity differences between signals recorded on the vein and lamina, may help small stink bugs to estimate distance and to locate each other on a plant.     

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.     

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.     

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.     

Stink bug interaction with host plants during communication

In solitary plant-dwelling stink bug species, success depends crucially on efficient mate location and recognition, mediated by signals transmitted through the plant. All stink bugs investigated so far communicate with species and sex-specific narrow-band calling and courtship song signals produced by abdomen vibration. Calling songs of lower specificity are characterized by readily repeated units emitted with regular repetition rate from the same place on a plant, while courtship songs take place at shorter distances in the process of species and sex recognition, together with signals of other modalities. Signal spectra with about 100Hz fundamental frequency and harmonics below 1000Hz are tuned to the resonant properties of their green host plants. The majority of the identified leg vibratory receptor cells and the underlying ventral cord interneurons respond best in the frequency range below 500Hz. Green plants with low pass filtering properties transmit optimally signals with a dominant frequency around 100Hz and strongly attenuate vibrations above 600Hz. Accurate tuning of signal spectral properties with the plant's mechanical characteristics enables communication over several meter distances, with dispersive bending waves running through the plant's rod-like structures under standing wave conditions.     

Vibrational directionality in the southern green stink bug, Nezara viridula (L.), is mediated by female song

We tested the hypothesis that male southern green stink bugs, Nezara viridula (L.), use substrate-borne songs to locate females. We recorded the responses of bugs on plants to the vibrations caused by a prerecorded female song and by an artificial sound. The female song caused males to walk, to respond with the calling and courtship songs and to approach the source of the song with characteristic search behaviour at junctions between branches on the plants. At a junction, a searching male stopped, stretched his legs and antennae and compared the vibratory signals on the two branches, with different combinations of legs and antennae. The males then left the junction and approached the source of the vibration. Males located the loudspeaker significantly more frequently in the presence than in the absence of vibratory stimuli on cyperus, Cyperus alternifolius L., and beans, Phaseolus vulgaris L. Vibrational directionality was also elicited by artificial pure tones whose spectral and temporal parameters were similar to those of natural female song. Females showed no reaction to vibratory stimulation and no vibrational directionality. We discuss possible mechanisms underlying vibrational directionality in the light of expected signal changes during transmission through plants. Copyright 1999 The Association for the Study of Animal Behaviour.     

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.

     

Female choice for male gregariousness in a Stink bug,Megacopta punctissimum (Montandon) (Heteroptera,Plataspidae)

Adults of a stink bug,Megacopta punctissimum, form mating aggregations on their host plants, based on the gregarious habit of males. A female was released on a stem on which there was an aggregation of 2 mating pairs and 1 bachelor male. Next, the bachelor male was released on a stem on which no bugs were present, and the same female was released there. Sequences of courtship behavior were compared between them. This experiement was repeated for 41 pairs of males and females, and about half (20 cases) of these experiments were made in the reverse order. Males were the active sex in courtship, whilst females either accepted the courtship, or escaped from courting males. Females accepted courtship with a higher probability when males courted in aggregations (73%) compared to solitary conditions (22%). This was because the escape behavior of females from the males was reduced if females detected the presence of other bugs near the males. It was concluded that female choice is a selective force for gregariousness in males.