Food habits of 3 myrmecophilous bug species on myrmecophytic Macaranga (Malpighiales: Euphorbiaceae) vary from herbivory to predation.

Myrmecophytes have mutualistic relationships with symbiotic ants. Although myrmecophytic Macaranga (Malpighiales: Euphorbiaceae) species are well protected by aggressive Crematogaster (Hymenoptera: Formicidae) ants, some bug species occur on the myrmecophytes. To clarify the associations of these bugs with the plants and the ants, we studied the food habits of 3 bug species, Pilophorus lambirensis Nakatani et Komatsu, 2013 (Hemiptera: Miridae: Phylinae), Phylinae sp. 1, and Arbela sp. 1 (Hemiptera: Nabidae). We conducted field observations in a Bornean rainforest. First, we located these bugs and studied their behavioral responses to the ants on Macaranga species; we then conducted stable isotope analyses. All bugs avoided direct contact with ants, but they occurred only on trees with active ants. Pilophorus lambirensis and Phylinae sp. 1 were most commonly observed on the apical parts of host trees, whereas Arbela sp. 1 was mainly in areas distant from the apical parts where ants were sparse. The stable isotope ratios indicated that Phylinae sp. 1 fed on food bodies, which are nutrient-rich spherical bodies produced by Macaranga trees on the apical parts for ants. Although the main diet of the other 2 species remains unclear, nitrogen isotopic signatures demonstrated that P. lambirensis is herbivorous, whereas Arbela sp. 1 is carnivorous. However, the distant location from ants and its isotopic signatures indicated that Arbela sp. 1 rarely fed on the ants. At least 2 mirid bug species might obtain enemy-free space in addition to the food provided by the myrmecophytes.

Revisiting the Taxonomy of Cylapocoris Carvalho, 1954 (Hemiptera: Miridae: Cylapinae) with Descriptions of Five New Species and Morphology-Based Phylogenetic Analysis of the Genus.

This paper provides descriptions of five new species of the Neotropical genus Cylapocoris Carvalho, 1954 (C. bimaculatus n. sp., C. brooksi n. sp., C. carvalhoi n. sp., C. scutellatus n. sp., and C. simplexoides n. sp.). Cylapocoris and Cylapocoroides Carvalho, 1989 are redescribed and rediagnosed. Illustrations of male genitalia, scanning electron micrographs of selected structures of certain taxa, and an identification key to species are provided. Female genitalia are described and illustrated for the first time for Cylapocoris in nine out of 19 known species. A cladistic analysis of the genus, based on 62 morphological characters, is presented as a contribution to the understanding of relationships within Cylapocoris and its relationships with other groups of Cylapinae. The analysis comprises 16 ingroup species and 15 outgroup taxa. Both equal and implied weighting parsimony analyses were used in the phylogenetic reconstruction. We confirm the monophyly of Cylapocoris and its sister-group relationship with Cylapocoroides. Additionally, we identify subgroupings within Cylapocoris. Intertribal relationships within Cylapinae are briefly discussed.

A Revision of the Genus Argolis (Hemiptera: Reduviidae: Stenopodainae) from Asia.

The assassin bug genus Argolis Stål, 1861 (Hemiptera: Reduviidae: Stenopodainae) has a disjunct distribution in Sub-Saharan Africa and Asia. In the present study, the Asian species of Argolis are revised. Two species are recognized, redescribed, and illustrated, with the following new subjective synonyms and new combination proposed: Argolis Stål, 1861 = Bardesanes Distant, 1909, syn. nov. = Neoklugia Distant, 1919, syn. nov.; A. farinator (Reuter, 1882) = N. typica Distant, 1919, syn. nov. = B. sericenotatus Livingstone & Ravichandran, 1989, syn. nov.; A. signata (Distant, 1909), comb. nov. (transferred from Bardesanes) = Caunus noctulus Hsiao, 1977, syn. nov. Lectotypes for C. farinator, B. signatus, and N. typica are designated. A key to separate the two Asian species of Argolis is provided. The sexual dimorphism, systematic relationships, and distribution of Argolis are discussed. Argolis is newly recorded from Laos, Pakistan, and Vietnam.

The spread of satellite DNAs in euchromatin and insights into the multiple sex chromosome evolution in Hemiptera revealed by repeatome analysis of the bug Oxycarenus hyalinipennis.

Satellite DNAs (satDNAs) are highly repeated tandem sequences primarily located in heterochromatin, although their occurrence in euchromatin has been reported. Here, our aim was to advance the understanding of satDNA and multiple sex chromosome evolution in heteropterans. We combined cytogenetic and genomic approaches to study, for the first time, the satDNA composition of the genome in an Oxycarenidae bug, Oxycarenus hyalinipennis. The species exhibits a male karyotype of 2n = 19 (14A + 2 m + X1 X2 Y), with a highly differentiated Y chromosome, as demonstrated by C-banding and comparative genomic hybridization, revealing an enrichment of repeats from the male genome. Additionally, comparative analysis between males and females revealed that the 26 identified satDNA families are significantly biased towards male genome, accumulating in discrete regions in the Y chromosome. Exceptionally, the OhyaSat04-125 family was found to be distributed virtually throughout the entire extension of the Y chromosome. This suggests an important role of satDNA in Y chromosome differentiation, in comparison of other repeats, which collectively shows similar abundance between sexes, about 50%. Furthermore, chromosomal mapping of all satDNA families revealed an unexpected high spread in euchromatic regions, covering the entire extension, irrespective of their abundance. Only discrete regions of heterochromatin on the Y chromosome and of the m-chromosomes (peculiar chromosomes commonly observed in heteropterans) were enriched with satDNAs. The putative causes of the intense enrichment of satDNAs in euchromatin are discussed, including the possible existence of burst cycles similar to transposable elements and as a result of holocentricity. These data challenge the classical notion that euchromatin is not enriched with satDNAs.

A Faboideae-Specific Floral Scent Betrays Seeds to an Important Granivore Pest.

Seed predation by insect herbivores reduces crop production worldwide. Foraging on seeds at pre-dispersal generally means that females need to find the suitable host plant within a relatively short timeframe in order to synchronize larval development with seed production. The mechanistic understanding of host finding by seed pests can be harnessed for more sustainable pest management strategies. We here studied the chemical communication between the bean bug Riptortus pedestris, a major pest of legumes, and several crop species and cultivars in the Fabaceae. Via a comparative chemical analysis, we found that 1-octen-3-ol is the principal constituent of the floral scents of most species tested in the subfamily Faboideae, including soybean and faba bean. With field trapping and laboratory bioassays, including electroantennography, we further revealed that this compound can be perceived, and stimulate attraction responses, by R. pedestris nymphs and adults. The addition of 1-octen-3-ol to pheromone traps might therefore improve trapping efficacy for controlling populations of this important granivore pest on legumes.

Ontogenetic change in effectiveness of chemical defence against different predators in Oxycarenus true bugs.

Many prey species change their antipredator defence during ontogeny, which may be connected to different potential predators over the life cycle of the prey. To test this hypothesis, we compared reactions of two predator taxa - spiders and birds - to larvae and adults of two invasive true bug species, Oxycarenus hyalinipennis and Oxycarenus lavaterae (Heteroptera: Oxycarenidae) with life-stage-specific chemical defence mechanisms. The reactions to larvae and adults of both true bug species strikingly differed between the two predator taxa. The spiders were deterred by the defences of adult bugs, but the larval defences were ineffective against them. By contrast, birds attacked the larvae considerably less often than the adult bugs. The results indicate a predator-specific ontogenetic change in defence effectiveness of both Oxycarenus species. The change in defence is likely linked to the life-stage-specific composition of secretions in both species: whereas secretions of larvae are dominated by unsaturated aldehydes, secretions of adults are rich in terpenoids, which probably serve dual function of defensive chemicals and pheromones. Our results highlight the variation in defence between different life stages and the importance of testing responses of different types of predators.

Characterization of two new Pylorgus mitogenomes (Hemiptera, Lygaeidae, Ischnorhynchinae) and a mitochondrial phylogeny of Lygaeoidea.

Lygaeidae is a large family of Hemiptera (Heteroptera) currently separated into three subfamilies, Ischnorhynchinae, Lygaeinae, and Orsillinae. In this research, the complete mitogenomes of the iscnorhynchines Pylorgusporrectus Zheng, Zou & Hsiao, 1979 and Pylorgussordidus Zheng, Zou & Hsiao, 1979 were sequenced, and the phylogeny of Pylorgus and the Lygaeidae with known complete mitogenomes were examined. The mitogenomes are 15,174 bp and 15,399 bp in size, respectively, and comprised of 13 protein-coding genes (PCGs), 22 transfer RNA genes (tRNAs), two ribosomal RNA genes (rRNAs), and a control region (D-loop). Nucleotide composition is biased toward A and T, and the gene order is identical to that of the putative ancestral arrangement of insects. Eleven PCGs begin with a typical ATN, and the remaining two PCGs begin with TTG (cox1 and nad4l). All tRNAs had a typical cloverleaf secondary structure, but some of them had individual base mismatches. The phylogenetic analyses based on the concatenated nucleotide sequences of the 13 PCGs, using Bayesian inference and maximum likelihood, support the monophyly of Lygaeidae. The results show that P.porrectus and P.sordidus clustered with nine other Lygaeidae. This study includes the first complete sequencing of the mitochondrial genomes of two Pylorgus species, which will provide important data for studying the phylogenetic position of Lygaeidae in Lygaeoidea and reconstructing the phylogenetic relationships within Pentatomomorpha.

First record of the predatory stink bug species Picromerusgriseus (Dallas) (Hemiptera, Heteroptera, Pentatomidae, Asopinae) in Japan, with an illustrated key to the Japanese species of the genus Picromerus Amyot & Serville.

Background: The predatory stink bug genus Picromerus Amyot & Serville, 1843 (Hemiptera, Heteroptera, Pentatomidae, Asopinae) comprises 11 species found in the Northern Hemisphere. In Japan, two species have been recorded to date. However, an easy-to-understand identification method, such as an illustrated key, is lacking. Currently, Picromerusgriseus (Dallas, 1851) has been recorded in Bangladesh, Bhutan, China, Indonesia, Myanmar, Pakistan and Taiwan, but not in Japan. New information: Picromerusgriseus was recorded in Japan for the first time, based on a single individual collected from grasslands around the fields of Ishigaki Island of the Ryukyu Islands, which belong to the Oriental Region. This discovery represents the easternmost record of the species. An illustrated key to the species of Picromerus occurring in Japan is also provided.

Reproductive biology of overwintering leaffooted bug Leptoglossus zonatus (Hemiptera: Coreidae) in California.

Leptoglossus zonatus (Dallas) (Hemiptera: Coreidae) is a polyphagous insect pest attacking a wide variety of crops. In California's Central Valley, it is now the dominant leaffooted bug on almonds, pistachios, and pomegranates. Leptoglossus zonatus pest status depends largely on overwintering adult survival and reproductive potential, which determines its population size in spring and early summer when nut crops are particularly susceptible to bug damage. Here, we investigated the overwintering reproductive biology of L. zonatus in laboratory and field experiments to gain information about its ovary development, time of mating, and the impact of low temperatures on egg hatch. With dissections of laboratory-reared L. zonatus, we established a baseline for ovarian development and determined that the size of the spermathecal reservoir is larger in mated than in unmated females. Dissections and behavioral experiments of field-collected material provided evidence of mating events before dispersal from overwintering sites. Laboratory trials showed that temperature significantly impacted L. zonatus egg hatch. Leptoglossus zonatus reproductive biology presented provides valuable information on its population dynamics and dispersal from overwintering sites, and will contribute to the development of monitoring and management tools.

Molecular Phylogeny of Cimicoidea (Heteroptera: Cimicomorpha) Revisited: Increased Taxon Sampling Reveals Evolution of Traumatic Insemination and Paragenitalia.

The molecular phylogeny of the Cimicoidea was reconstructed from an expanded sampling based on mitochondrial (16S, COI) and nuclear (18S, 28SD3) genes. The data were analyzed using maximum likelihood (ML), maximum parsimony (MP), and Bayesian inference (BI) phylogenetic frameworks. The phylogenetic relationships inferred by the model-based analyses (ML and BI) were largely congruent with those inferred by the MP analysis in terms of the monophyly of most of the higher taxonomic groups and the species-level relationships. The following clades were recovered in all analyses: Cimiciformes; Nabidae: Prostemmatinae; Nabidae: Nabinae; Plokiophilidae; Microphysidae; Lasiochilidae; Cimicidae: Cacodminae; Cimicidae; Lyctocoridae; Anthocoridae s. str.; Cardiastethini excluding Amphiareus; Almeidini; Scolopini; Anthocorini; Oriini; Curaliidae + Lasiochilidae; Almeidini + Xylocorini; Oriini + Cardiastethini; and Anthocorini + Amphiareus. Reconstructions of ancestral copulation states based on Bayesian and parsimony inference indicated that at least one shift from standard insemination (SI) to traumatic insemination (TI) occurred within Cimicoidea, and an investigation of the evolutionary correlation between TI and paragenitalia (PG) revealed that the acquisition of PG in cimicoid females was correlated with the TI habit. Additionally, our morphological examination of various types of PG suggested that even the same PG type may not constitute a homologous feature at various taxonomic levels, indicating the convergent evolution of female morphology to adapt to TI.

Juvenile hormone identification in the cabbage bug Eurydema rugosa.

Juvenile hormone (JH) plays a pivotal role in almost every aspect of insect development and reproduction. The chemical structure of the JH in heteropteran species has long remained elusive until methyl (2R,3S,10R)-2,3;10,11-bisepoxyfarnesoate, commonly named as juvenile hormone III skipped bisepoxide (JHSB3), was isolated from Plautia stali (Hemiptera: Heteroptera: Pentatomidae). Recently, several groups reported the presence of JHSB3 in other heteropteran species. However, most of the studies paid no attention to the determination of the relative and absolute structure of the JH. In this study, we investigated the JH of the cabbage bug Eurydema rugosa (Hemiptera: Heteroptera: Pentatomidae), known as a pest for wild and cultivated crucifers. JHSB3 was detected in the hexane extract from the corpus allatum (CA) product using a chiral ultraperformance liquid chromatography-tandem mass spectrometer (UPLC-MS/MS) which can inform the absolute stereochemistry of the JH. Its stereoisomers were not detected. Topical application of the synthetic JHSB3 to the last instar nymphs inhibited their metamorphosis and induced nymphal-type colouration of the dorsal abdomen in a dose-dependent manner. Additionally, the topical application of JHSB3 effectively terminated summer and winter diapauses in females. These results indicate that the JH of E. rugosa is JHSB3. Although individuals in summer and winter diapauses are physiologically distinct in E. rugosa, the results suggest that the physiological differences between these diapauses are based, not on the responsiveness to JH, but on the processes governing activation of the CA or on its upstream cascades.

Phytoremediation of crude oil-contaminated sediment using Suaeda heteroptera enhanced by Nereis succinea and oil-degrading bacteria.

A 150-day experiment was performed to investigate the stimulatory effect of a promising phytoremediation strategy consisting of Suaeda heteroptera (S. heteroptera), Nereis succinea (N. succinea), and oil-degrading bacteria for cleaning up total petroleum hydrocarbons (TPHs) in spiked sediment. Inoculation with oil-degrading bacteria and/or N. succinea increased plant yield and TPH accumulation in S. heteroptera plants. The highest TPH dissipation (40.5%) was obtained in the combination treatment, i.e., S. heteroptera + oil-degrading bacteria + N. succinea, in which the sediment TPH concentration decreased from an initial value of 3955 to 2355 mg/kg in 150 days. BAF, BCF, and TF confirmed the role of N. succinea and oil-degrading bacteria in the amelioration and translocation of TPHs. In addition, TPH toxicity of S. heteroptera was alleviated by N. succinea and oil-degrading bacteria addition through the reduction of oxidative stress. Therefore, S. heteroptera could be used for cleaning up oil-contaminated sediment, particularly in the presence of oil-degrading bacteria + N. succinea. Field studies on oil-degrading bacteria + N. succinea may provide new insights on the rehabilitation and restoration of sediments contaminated by TPHs.

Our study attempted to investigate the stimulatory effect of a promising phytoremediation strategy consisting of Suaeda heteroptera (S. heteroptera), Nereis succinea (N. succinea), and oil-degrading bacteria for cleaning up TPH in spiked sediment. Planting S. heteroptera can greatly increase sediment TPH removal, and its removal was enhanced greater after inoculation with oil-degrading bacteria and/or N. succinea. Moreover, the promising phytoremediation strategy developed in the current work can serve as an efficient, novel approach to removal TPH in sediment/soil. In our opinions, these findings provide insights into the assessment of their ecological risks in the environments that are of interest to broad readership of International Journal of Phytoremediation.

Prey-mediated effects of mCry51Aa2-producing cotton on the predatory nontarget bug Orius majusculus (Reuter).

Genetically engineered (GE) cotton, MON 88702, is protected against certain sucking pests, such as plant bugs and thrips, by producing mCry51Aa2, a modified protein from Bacillus thuringiensis (Bt). Predatory pirate bugs (Orius spp.), natural enemies contributing to biological pest control, are also sensitive to the insecticidal protein when exposed continuously to high concentrations. We evaluated effects of MON 88702 on Orius majusculus when fed prey types with different mCry51Aa2 concentrations. When neonates were provided exclusively Tetranychus urticae spider mites reared on MON 88702 (high mCry51Aa2 content), adverse effects on predator survival and development were confirmed, compared with specimens fed prey from near-isogenic non-Bt cotton. When fed a mixture of T. urticae and Ephestia kuehniella eggs (mCry51Aa2-free), predator life table parameters were similar to the treatment where eggs were fed exclusively. When mCry51Aa2-containing spider mites were provided for a limited time at the beginning or the end of juvenile development, effects were less pronounced. While pirate bug nymphs showed similar consumption rates for prey from Bt and non-Bt cotton, choice experiments revealed a preference for E. kuehniella eggs over spider mites. Lepidopteran larvae (Spodoptera littoralis, high mCry51Aa2 content) or cotton aphids (Aphis gossypii, mCry51Aa2-free) reared on MON 88702 as alternative prey did not result in adverse effects on O. majusculus. Our study suggests limited risk of mCry51Aa2-producing cotton for O. majusculus, because its sensitivity for the Bt protein is relatively low and its natural food consists of diverse prey species with varying concentrations of Bt protein.

Biology of Glyphepomis dubia Campos & Souza, 2016 (Hemiptera: Pentatomidae) and the parasitoids Telenomus podisi Ashmead, 1893 and Trissolcus basalis (Wollaston, 1858) (Hymenoptera: Platygastridae) on rice / Biologia de Glyphepomis dubia Campos & Souza, 2016 (Hemiptera: Pentatomidae) e dos parasitoides Telenomus podisi Ashmead, 1893 e Trissolcus basalis (Wollaston, 1858 (Hymenoptera: Platygastridae) em arroz

Abstract The life cycle of stink bug, Glyphepomis dubia and the development of two egg parasitoids (Telenomus podisi and Trissolcus basalis) were studied at the Federal University of Maranhão, at 26 ± 2oC, relative humidity (RH) of 60 ± 10% and 12h photophase. Individuals used in the study were collected from seven rice fields located around the municipality of Arari, Maranhão, Brazil, and maintained in greenhouse and laboratory for the life cycle studies. From egg to adult, G. dubia took 35.2 days to complete the life cycle. The oviposition period was 37 days, with egg masses of about 12 eggs each and viability of 93.1%. Longevity was 53 and 65 days for females and males, respectively. The egg parasitoids Te. podisi and Tr. basalis parasitized and developed in G. dubia eggs; however, the biological characteristics of Tr. basalis were affected. Emergence of the parasitoids was higher for Te. podisi (83.5%) compared to the records for Tr. basalis (50.4%). Therefore, G. dubia may potentially achieve a pest status and Te. podisi is a promising biological control agent for G. dubia management in Brazil due to its higher longevity and better reproductive parameters.

Resumo O ciclo de vida do percevejo, Glyphepomis dubia e a biologia de dois parasitoides de ovos (Telenomus podisi e Trissolcus basalis) foram estudados na Universidade Federal do Maranhão, a 26 ± 2oC, umidade relativa (UR) de 60 ± 10% e fotofase de 12h. Sete indivíduos de G. dubia foram coletados em lavoura de arroz localizada no município de Arari, Maranhão, Brasil e mantidos em casa de vegetação e laboratório para estudos de ciclo de vida. Do ovo ao adulto, G. dubia levou 35.2 dias para completar o ciclo de vida. O período de oviposição foi de 37 dias com massas de ovos com cerca de 12 ovos/massa e viabilidade de 93.1%. A longevidade foi de 53 e 65 dias, respectivamente, para fêmeas e machos. Os parasitoides de ovos, Te. podisi e Tr. basalis parasitaram e se desenvolveram em ovos de G. dubia, no entanto as características biológicas de Tr. basalis foi afetada. A emergência dos parasitoides foi maior para Te. podisi (83.5%) em comparação com o registrado para Tr. basalis (50.4%). Portanto, G. dubia poderá apresentar potencial para atingir o status de praga e Te. podisi é um promissor agente de controle biológico para ser utilizado no manejo de G. dubia no Brasil, pois apresentou maior longevidade e os melhores parâmetros reprodutivos.

Biology of Glyphepomis dubia Campos & Souza, 2016 (Hemiptera: Pentatomidae) and the parasitoids Telenomus podisi Ashmead, 1893 and Trissolcus basalis (Wollaston, 1858) (Hymenoptera: Platygastridae) on rice / Biologia de Glyphepomis dubia Campos & Souza, 2016 (Hemiptera: Pentatomidae) e dos parasitoides Telenomus podisi Ashmead, 1893 e Trissolcus basalis (Wollaston, 1858) (Hymenoptera: Platygastridae) em arroz

The life cycle of stink bug, Glyphepomis dubia and the development of two egg parasitoids (Telenomus podisi and Trissolcus basalis) were studied at the Federal University of Maranhão, at 26 ± 2oC, relative humidity (RH) of 60 ± 10% and 12h photophase. Individuals used in the study were collected from seven rice fields located around the municipality of Arari, Maranhão, Brazil, and maintained in greenhouse and laboratory for the life cycle studies. From egg to adult, G. dubia took 35.2 days to complete the life cycle. The oviposition period was 37 days, with egg masses of about 12 eggs each and viability of 93.1%. Longevity was 53 and 65 days for females and males, respectively. The egg parasitoids Te. podisi and Tr. basalis parasitized and developed in G. dubia eggs; however, the biological characteristics of Tr. basalis were affected. Emergence of the parasitoids was higher for Te. podisi (83.5%) compared to the records for Tr. basalis (50.4%). Therefore, G. dubia may potentially achieve a pest status and Te. podisi is a promising biological control agent for G. dubia management in Brazil due to its higher longevity and better reproductive parameters.

O ciclo de vida do percevejo, Glyphepomis dubia e a biologia de dois parasitoides de ovos (Telenomus podisi e Trissolcus basalis) foram estudados na Universidade Federal do Maranhão, a 26 ± 2oC, umidade relativa (UR) de 60 ± 10% e fotofase de 12h. Sete indivíduos de G. dubia foram coletados em lavoura de arroz localizada no município de Arari, Maranhão, Brasil e mantidos em casa de vegetação e laboratório para estudos de ciclo de vida. Do ovo ao adulto, G. dubia levou 35.2 dias para completar o ciclo de vida. O período de oviposição foi de 37 dias com massas de ovos com cerca de 12 ovos/massa e viabilidade de 93.1%. A longevidade foi de 53 e 65 dias, respectivamente, para fêmeas e machos. Os parasitoides de ovos, Te. podisi e Tr. basalis parasitaram e se desenvolveram em ovos de G. dubia, no entanto as características biológicas de Tr. basalis foi afetada. A emergência dos parasitoides foi maior para Te. podisi (83.5%) em comparação com o registrado para Tr. basalis (50.4%). Portanto, G. dubia poderá apresentar potencial para atingir o status de praga e Te. podisi é um promissor agente de controle biológico para ser utilizado no manejo de G. dubia no Brasil, pois apresentou maior longevidade e os melhores parâmetros reprodutivos.

Biology of Glyphepomis dubia Campos & Souza, 2016 (Hemiptera: Pentatomidae) and the parasitoids Telenomus podisi Ashmead, 1893 and Trissolcus basalis (Wollaston, 1858) (Hymenoptera: Platygastridae) on rice

Abstract The life cycle of stink bug, Glyphepomis dubia and the development of two egg parasitoids (Telenomus podisi and Trissolcus basalis) were studied at the Federal University of Maranhão, at 26 ± 2oC, relative humidity (RH) of 60 ± 10% and 12h photophase. Individuals used in the study were collected from seven rice fields located around the municipality of Arari, Maranhão, Brazil, and maintained in greenhouse and laboratory for the life cycle studies. From egg to adult, G. dubia took 35.2 days to complete the life cycle. The oviposition period was 37 days, with egg masses of about 12 eggs each and viability of 93.1%. Longevity was 53 and 65 days for females and males, respectively. The egg parasitoids Te. podisi and Tr. basalis parasitized and developed in G. dubia eggs; however, the biological characteristics of Tr. basalis were affected. Emergence of the parasitoids was higher for Te. podisi (83.5%) compared to the records for Tr. basalis (50.4%). Therefore, G. dubia may potentially achieve a pest status and Te. podisi is a promising biological control agent for G. dubia management in Brazil due to its higher longevity and better reproductive parameters.

Resumo O ciclo de vida do percevejo, Glyphepomis dubia e a biologia de dois parasitoides de ovos (Telenomus podisi e Trissolcus basalis) foram estudados na Universidade Federal do Maranhão, a 26 ± 2oC, umidade relativa (UR) de 60 ± 10% e fotofase de 12h. Sete indivíduos de G. dubia foram coletados em lavoura de arroz localizada no município de Arari, Maranhão, Brasil e mantidos em casa de vegetação e laboratório para estudos de ciclo de vida. Do ovo ao adulto, G. dubia levou 35.2 dias para completar o ciclo de vida. O período de oviposição foi de 37 dias com massas de ovos com cerca de 12 ovos/massa e viabilidade de 93.1%. A longevidade foi de 53 e 65 dias, respectivamente, para fêmeas e machos. Os parasitoides de ovos, Te. podisi e Tr. basalis parasitaram e se desenvolveram em ovos de G. dubia, no entanto as características biológicas de Tr. basalis foi afetada. A emergência dos parasitoides foi maior para Te. podisi (83.5%) em comparação com o registrado para Tr. basalis (50.4%). Portanto, G. dubia poderá apresentar potencial para atingir o status de praga e Te. podisi é um promissor agente de controle biológico para ser utilizado no manejo de G. dubia no Brasil, pois apresentou maior longevidade e os melhores parâmetros reprodutivos.

Comparative analysis of detoxification-related gene superfamilies across five hemipteran species.

BACKGROUND: Hemiptera is one of the most speciose orders of insects, and the most speciose considering Hemimetabola. Through their evolutive history, hemipterans with different feeding habits have adapted to deal with different chemical challenges. Three major gene families are involved in xenobiotic detoxification in insects: the cytochromes P450 (CYPs), carboxyl/cholinesterases (CCEs), and glutathione transferases (GSTs). Here we perform a comparative analysis on the complement of these gene superfamilies across five hemipteran species; four heteropterans (the pentatomid plant feeders Nezara viridula and Halyomorpha halys; the hematophagous Cimex lectularius, Cimicidae, and Rhodnius prolixus, Reduviidae), and one Auchenorrhyncha plant feeder (Nilaparvata lugens). RESULTS: Our results point to an expansion of several enzyme families associated with xenobiotic detoxification in heteropterans with respect to other species and the existence of a dynamic evolution pattern including CYP3 clan, hormone and pheromone processing class in the CCE superfamily, and sigma class in GST superfamily. Other detoxification-related families are reduced in the hemipteran species analyzed here: reduction or even absence of epsilon class and reduced delta class in GST superfamily; absence of mitochondrial CYP12 family; absence of CYP9 family in CYP3 clan; and reduction or even absence of some dietary/detoxification groups of CCEs. Interestingly, the most polyphagous species analyzed here (H. halys) is also the one that presents the largest repertoire of detoxification enzymes. Gene cluster analysis suggests that this could be due to gene duplication events. CONCLUSIONS: The evolutionary analysis performed here reveals characteristics that are both common and particular for heteropterans. The composition and organization of detoxification-related gene families could shed light on evolutionary forces that shaped their divergence. These families are important for both the detoxification of diet products and for conferring tolerance or resistance to synthetic insecticides. Furthermore, we present the first comprehensive analysis of detoxification gene superfamilies in N. viridula, an understudied species in spite of its economic relevance as a crop pest. The information obtained is of interest for basic insect science as well as for the control of harmful species and the management of insecticide resistance.

Symbiotic Microorganisms and Their Different Association Types in Aquatic and Semiaquatic Bugs.

True bugs (Hemiptera, suborder Heteroptera) constitute the largest suborder of nonholometabolous insects and occupy a wide range of habitats various from terrestrial to semiaquatic to aquatic niches. The transition and occupation of these diverse habitats impose various challenges to true bugs, including access to oxygen for the aquatic species and plant defense for the terrestrial phytophagans. Although numerous studies have demonstrated that microorganisms can provide multiple benefits to terrestrial host insects, a systematic study with comprehensive higher taxa sampling that represents aquatic and semiaquatic habitats is still lacking. To explore the role of symbiotic microorganisms in true bug adaptations, 204 samples belonging to all seven infraorders of Heteroptera were investigated, representing approximately 85% of its superfamilies and almost all known habitats. The symbiotic microbial communities of these insects were analyzed based on the full-length amplicons of the bacterial 16S rRNA gene and fungal ITS region. Bacterial communities varied among hosts inhabiting terrestrial, semiaquatic, and aquatic habitats, while fungal communities were more related to the geographical distribution of the hosts. Interestingly, co-occurrence networks showed that species inhabiting similar habitats shared symbiotic microorganism association types. Moreover, functional prediction analyses showed that the symbiotic bacterial community of aquatic species displayed richer amino acid and lipid metabolism pathways, while plant-feeding true bugs benefited more from the symbiont-provided xenobiotics biodegradation pathway. These results deepened the recognition that symbiotic microorganisms were likely to help heteropterans occupy diverse ecological habitats and provided a reference framework for further studies on how microorganisms affect host insects living in various habitats. IMPORTANCE Symbiotic bacteria and fungi generally colonize insects and provide various benefits for hosts. Although numerous studies have investigated symbionts in terrestrial plant-feeding insects, explorations of symbiotic bacterial and fungal communities in aquatic and semiaquatic insects are rare. In this study, the symbiotic microorganisms of 204 aquatic, semiaquatic, and terrestrial true bugs were explored. This comprehensive taxon sampling covers ~85% of the superfamilies of true bugs and most insect habitats. Analyses of the diversity of symbionts demonstrated that the symbiotic microbial diversities of true bugs were mainly affected by host habitats. Co-occurrence networks showed that true bugs inhabiting similar habitats shared symbiotic microbial association types. These correlations between symbionts and hosts together with the functions of bacterial communities indicated that symbiotic microbial communities may help true bugs adapt to (semi)aquatic habitats.

The mouthparts of the Aradidae (Insecta: Hemiptera: Heteroptera).

The flat bugs, Aradidae, have exceptionally long piercing-sucking stylets coiled up at rest in the anterior part of the head. Previous studies suggested that the majority of aradids can be divided into two groups by the direction of stylet coiling, clockwise or anticlockwise. Detailed reconstruction of the head skeleton and musculature from series of polished sections, examined in SEM, of epon-embedded specimens of three species has shown that these groups represent two disparate modifications of the head groundplan. In Aradus betulae (L.), the stylet coil is accommodated inside the greatly enlarged anteclypeus within an expansible membranous diverticulum of its epipharyngeal cuticle. In contrast, in Isodermus planus Erichson and Carventus brachypterus Kormilev, the coil lies freely underneath the anteclypeus between the extended maxillary lobes (in I. planus fused with the extended gular lobe). The intraclypeal coils occur in the subfamilies Aradinae, Calisiinae, and Chinamyersiinae and the subclypeal coils in Isoderminae, Carventinae, Mezirinae, Aneurinae, Prosympiestinae, and possibly in the closely related family Termitaphididae. Each method of stylet coiling is associated with a suite of divergently specialized structural traits, suggesting that the two groups have independently evolved from ancestors endowed with regular stylets. Functional mechanics of the coiled stylet bundles are discussed.

The Impact of Environmental Habitats and Diets on the Gut Microbiota Diversity of True Bugs (Hemiptera: Heteroptera).

Insects are generally associated with gut bacterial communities that benefit the hosts with respect to diet digestion, limiting resource supplementation, pathogen defense, and ecological niche expansion. Heteroptera (true bugs) represent one of the largest and most diverse insect lineages and comprise species consuming different diets and inhabiting various ecological niches, even including underwater. However, the bacterial symbiotic associations have been characterized for those basically restricted to herbivorous stink bugs of the infraorder Pentatomomorpha. The gut microbiota associated with the megadiverse heteropteran lineages and the implications of ecological and diet variance remain largely unknown. Here, we conducted a bacterial 16S rRNA amplicon sequencing of the gut microbiota across 30 species of true bugs representative of different ecological niches and diets. It was revealed that Proteobacteria and Firmicute were the predominant bacterial phyla. Environmental habitats and diets synergistically contributed to the diversity of the gut bacterial community of true bugs. True bugs living in aquatic environments harbored multiple bacterial taxa that were not present in their terrestrial counterparts. Carnivorous true bugs possessed distinct gut microbiota compared to phytophagous species. Particularly, assassin bugs of the family Reduviidae possessed a characterized gut microbiota predominantly composed of one Enterococcus with different Proteobacteria, implying a specific association between the gut bacteria and host. Overall, our findings highlight the importance of the comprehensive surveillance of gut microbiota association with true bugs for understanding the molecular mechanisms underpinning insect-bacteria symbiosis.