The first extensive analysis of species composition and abundance of stink bugs (Hemiptera: Pentatomidae) on soybean crops in Brazil.

BACKGROUND: Soybean is the third-greatest global commodity crop with respect to grain production, Brazil is the largest soybean producer in the world. We performed the first extensive survey including all the five main soybean cultivation regions in Brazil over three seasons (2018/2019, 2019/2020, and 2020/2021). A total of 2386 localities were sampled, corresponding to 145 municipalities in 11 states. Sampling was carried out between the R1 and R8 soybean growth stages, using a beating sheet. RESULTS: Fifteen species were recorded, with five species accounting for more than 99% of the sampled insects. The Neotropical brown stink bug, Euschistus heros (F.), was the most abundant species (82.4% of the adults and 84.1% of the nymphs overall), with differences in the mean abundance between soybean macroregions. The melacanthus green belly stink bug, Diceraeus melacanthus Dallas was the second most abundant species overall, followed by the brown winged stink bug, Edessa meditabunda (F.), the furcatus green belly stink bug, Diceraeus furcatus (F.) and the red-banded green stink bug, Piezodorus guildinii (Westwood). The relative abundance of each species differed between soybean macroregions. The mean abundance of nymphs and adults of Euschistus heros at different soybean reproductive stages showed an increase from early reproductive stages to the beginning of the late reproductive stages (R5 or R6). CONCLUSION: This large-scale assessment of stink bugs provides a basis for outlining integrated pest management programs and drives the development of monitoring and control strategies, as well as future studies investigating population dynamics over time and space in soybean fields. © 2024 Society of Chemical Industry.

Molecular characterization and demographic insights into soybean bud borer (Lepidoptera: Tortricidae) in Brazil.

The soybean bud borer, a soybean pest in Brazil, was initially identified as Crocidosema aporema (Walsingham 1914) (Lepidoptera: Tortricidae). Outbreaks of this species have recently increased, but identification of this pest remains uncertain, and the historical factors associated with its geographic distribution in Brazil are little known. Here, we conducted a species characterization and phylogeographic analysis based on molecular and morphological evidence. Ninety individuals of bud-borers Lepidoptera were collected in different regions of Brazil. We sequenced COI and COII mitochondrial genes and examined wing patterns and male genital morphology. DNA barcoding approach revealed that 10 individuals were Argyrotaenia sphaleropa (Meyrick 1909) (Lepidoptera: Tortricidae) and 80 were a species of the genus Crocidosema Zeller. The morphology of the adult genitalia and wings proved to be insufficient to confirm the identification of Brazilian individuals as C. aporema, a species originally described from a high-elevation site in Costa Rica. Furthermore, the genetic distance between putative C. aporema specimens from Brazil and Costa Rica (ranging from 5.2% to 6.4%) supports the hypothesis that the Brazilian specimens are not referable to C. aporema. Our analysis revealed a single genetic strain (i.e., species) with low genetic diversity on soybean crops. We found no indication that the genetic structure was related to geographic distance among populations or edaphoclimatic regions. The population expansion of the soybean bud borer coincides with the increase in the area of soybean production in Brazil, suggesting that expanded soybean farming has allowed a significant increase in the effective population size of this pest.

Molecular insights on the historical dispersion of Piezodorus guildinii (Hemiptera: Pentatomidae) in Brazil.

Piezodorus guildinii (Westwood, 1837) (Hemiptera: Pentatomidae) is an important arthropod pest of soybean (Glycine max (L.) Merr.) throughout American continents. However, the historical events associated with its dispersion are poorly understood. In this study, we employed a phylogeographic approach to investigate the origin and demographic history of P. guildinii in Brazil. We analyzed the cytochrome c oxidase subunit I and Cytb gene sequences of P. guildinii individuals collected in Brazil's 5 soybean production macro-regions and cross-referenced this information with sequences available in public databases. Our findings support an older Caribbean basin establishment for the current genealogical strains of P. guildinii, with subsequent dispersion to Brazil around 0.97 Mya. No secondary dispersion of this species from the Caribbean region to soybean areas in Brazil was identified. The Brazilian populations of P. guildinii are genetically structured across the country's soybean macro-regions and show strong signals of continuous demographic and spatial expansion in Brazil, which may be accelerated by the soybean cropping landscape in the country. The populations from the northern region (MR5) are older than the Central and South populations. The signs of demographic expansion indicate that P. guildinii populations are increasing their effective size in soybean regions, which could reflect its importance as a soybean pest in the coming years.

Establishment of Sinoxylon anale Lesne (Coleoptera, Bostrichidae) in Brazil: Identification, Host Plants, Distribution, and Damage.

Damage from Sinoxylon anale Lesne, a woodboring beetle not previously known to be established in Brazil, was observed in young jabuticaba trees (Plinia cauliflora, Myrtaceae) in a nursery in the municipality of Laranjal Paulista, state of São Paulo. We immediately advised MAPA ("Ministério da Agricultura, Pecuária e Abastecimento") and collected samples from the nursery and from different hosts in nearby areas, to identify the specimens and investigate the dynamics of the infestation in the jabuticaba trees. Sinoxylon anale was also collected in ethanol-baited and ultraviolet-light traps and in dry branches of the native species pau-jacaré (Piptadenia gonoacantha, Fabaceae) and inga (Inga vera, Fabaceae), and the exotic pau-d'água (Dracaena fragrans, Asparagaceae) in the municipality of Piracicaba, state of São Paulo. These collections established that S. anale larvae and adults develop in dead branches of four new host plants. Taxonomic studies using morphological parameters and DNA barcoding confirmed the identification of S. anale. An illustrated key to the three Sinoxylon species now recorded in Brazil is provided, and the COI gene sequences have been made available in a public database. Sinoxylon anale probably attacked the young jabuticaba trees after they were killed by larvae of long-horned beetles (Cerambycidae). So far, S. anale has been found established only in two locations in the same area of the state of São Paulo.

A Molecular Marker to Identify Spodoptera frugiperda (JE Smith) DNA in Predators' Gut Content.

Spodoptera frugiperda is a serious pest of maize and other crops worldwide. The integration of control tactics is recommended for S. frugiperda suppression because reports of insecticide and Btplant-resistance are frequent. Biological control agents would be an alternative to improve S. frugiperda control in agricultural areas. We constructed a species-specific molecular marker to detect S. frugiperda DNA in predators' gut content and estimated the predation rates of ladybugs and earwigs on S. frugiperda in maize crops. Predators were sampled in Pirassununga, São Paulo state, Brazil, in 2020 and 2021. Using the species-specific molecular marker in laboratory conditions, we estimated the half-life time to detect S. frugiperda DNA in the gut contents of Hippodamia convergens as 6.16 h and Doru luteipes as 25.72 h. The weekly predation rate of S. frugiperda by predators in maize crop varied from 0 to 42.1% by ladybugs and from 0 to 9.2% by D. luteipes. Predation events on S. frugiperda by predators were more frequent during the maize reproductive stage. Our results confirmed that predators might contribute to S. frugiperda suppression in maize fields. However, further studies of prey-predator interactions and agricultural landscapes are essential for a better understanding of predator dynamics in crops.

"Unmasking the Villain": Integrative Taxonomy Reveals the Real Identity of the Key Pest (Thysanoptera: Thripidae) of Peanuts (Arachis hypogaea L.) in South America.

The peanut thrips, Enneothrips enigmaticus sp. n., is the key pest of Arachis hypogaea L. in South America, where it can cause yield losses of up to 85%. This species has historically been identified as Enneothrips flavens, but access to the holotype of this species and freshly collected material from southeastern and northern Brazil revealed that specimens commonly collected on peanut crops are not conspecific with E. flavens. Biological, molecular, and morphological assessments were carried out and led to the conclusion that the key pest of A. hypogaea belongs to a previously undescribed species: Enneothrips enigmaticus sp. n.

Reproductive Patterns Drive the Gene Flow and Spatial Dispersal of Euschistus heros (Hemiptera: Pentatomidae).

Euschistus heros (Hemiptera: Pentatomidae) has two allopatric strains with a hybrid zone in central Brazil. Asymmetric dispersal and gene flow between these strains of E. heros have been observed, where the South strain (SS) moves more quickly to the northern regions of the country than the North strain (NS) to the southern areas. In addition, SS generally has a bigger body size and presents dark brown coloration, and NS is usually smaller in size and presents light brown coloration. Here, we studied the reproductive behavior and tested for the presence of assortative mating and reproductive barriers between the two allopatric strains of E. heros. Nonrandom mating was observed in the SS strain based on mating choice trials and the reproductive isolation indexes. SS females and males prefer to mate with their co-specific (same strain) partner, while NS insects showed no mating preference. The insect's pronotum width was positively associated with the mating choice suggesting size-assortative mating in E. heros. Reciprocal crosses between strains yielded similar reproductive outputs when compared with pure strain crosses, suggesting similar fitness of hybrid pure strains. The asymmetric gene flow in the hybridization zone that favors SS seems to be associated with the reproductive behavior of the species, which favors the typical phenotype found in the SS populations.

Euschistus crenator (Fabricius) (Hemiptera: Pentatomidae): a New Invasive Species on Soybean Fields in Northern Brazil.

The expansion of soybean Glycine max (L.) Merrill in South America has provided an abundant host to the native arthropod fauna. Stink bugs (Heteroptera: Pentatomidae) are severe pests on soybean crops due to their feeding activities. Several native species have been recorded on this crop, with the widespread Neotropical brow stink bug Euschistus heros (Fabricius) recognized as the key pest in most of its distribution. Here, we report for the first time Euschistus crenator (Fabricius) as a new invasive species on soybean fields in Northern Brazil. We collected the species at Pará state (2°38'32.2″S 54°55'56.1″W and 4°06'31.2″S 54°55'01.9″W) and Roraima state (2°39'41.3″N 60°46'58.9″W and 3°00'44.6″N 60°22'32.9″W). The latter represents a new state record, and the first represents new locality records, however, both representing the first soybean host record for the species. The distribution of E. crenator ranges from southern US (AZ, CA, FL, and TX) to north South America, mostly between the Tropics of Cancer and Capricorn. Despite overlap in distribution, we did not find E. crenator and E. heros simultaneously on soybean crops in the North region (Amazon Forest) of Brazil. Euschistus crenator was able to complete its life cycle and had viable offspring on soybean plants, with development parameters similar to E. heros.

Integrating data to redescribe Euschistus taurulus Berg (Hemiptera: Pentatomidae).

The genus Euschistus Dallas includes 67 species restricted to the New World, and several species are registered on cultivated plants in the Nearctic and Neotropical regions. In South America, most Euschistus species are completely overlooked due to the lack of information to allow accurate identification. Here, we redescribed Euschistus taurulus Berg, including for the first time, characterization of the internal and external genitalia of both sexes. We also report original information on bionomics, review and update information on geographical distribution and host plants records. Additionally, we provide DNA barcoding sequences for E. taurulus and three other morphologically similar key-agriculture pest species in South America: Euschistus heros (Fabricius), Dichelops melacanthus (Dallas), and Dichelops furcatus (Fabricius). We discuss means for correct identification of E. taurulus and its phylogenetic position within Euschistus and other similar stink bugs; the potential economic importance of the E. taurulus is also addressed.

Invasion origin, rapid population expansion, and the lack of genetic structure of cotton bollworm (Helicoverpa armigera) in the Americas.

In 2013, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) was officially declared as present in Brazil and, after two years, the species was detected in the Caribbean and North America. Information on genetic features and accurate distribution of pests is the basis for agricultural protection policies. Furthermore, such knowledge is imperative to develop control strategies, understand the geographical range, and genetic patterns of this species in the Americas. Here, we carried out the widest sampling of H. armigera in the South American continent and Puerto Rico, after we estimated the diversity, demographic parameters, and genetic structure. The Internal Transcribed Spacer 1 (ITS1) nuclear marker was used to investigate the presence of putative hybrids between H. armigera and H. zea, and they were observed at a frequency of 1.5%. An ABC analysis, based in COI gene fragment, suggested Europe as the origin of South America specimens of H. armigeraand following a movement northward through the Caribbean. Three mtDNA genes and three nDNA markers revealed high genetic diversity distributed without the defined population structure of H. armigera in South America. Most of the genetic variation is within populations with a multidirectional expansion of H. armigera among morphoclimatic regions. High genetic diversity, rapid population expansion, and hybridization have implications for pest management since they suggest that adaptive alleles are spread through wide areas in South America that favor rapid local adaptation of H. armigera to new and disturbed environments (e.g., in agricultural areas).

A Phylogeographic Approach to the Drosophila suzukii (Diptera: Drosophilidae) Invasion in Brazil.

Biological invasions have reached large parts of the globe, due to human actions across the planet. Drosophila suzukii (Matsumura, 1931) is a globally invasive species, always associated with enormous and costly damage to agricultural crops. Native to Southeast Asia, D. suzukii recently (i.e., 2013) invaded and is dispersing through South America. Here, we used a phylogeographic approach based on the cytochrome c oxidase subunit I gene fragment to explore the invasion dynamics of D. suzukii populations in Brazil. We identified five haplotypes and moderate genetic diversity in Brazilian populations, which are undergoing demographic and spatial expansion. The analyses of molecular variance indicated a high genetic structure among the populations, which is partially explained by their morphoclimatic origin and invasion history. Drosophila suzukii expanded from southern to southeastern Brazil, aided by human-mediated transport of fruits from region to region. The sharing of haplotypes among Brazilian and other invaded regions of the world suggests a single invasion event of D. suzukii in Brazil, originating from previously invaded areas (e.g., North America and Europe). The rapid geographic dispersal and wide variety of fruits attacked by of D. suzukii require immediate implementation of control strategies (legal and phytosanitary) to manage this pest in Brazil.

Comparative cytogenetics and derived phylogenic relationship among Sitophilus grain weevils (Coleoptera, Curculionidae, Dryophthorinae).

Cytogenetic characteristics and genome size are powerful tools for species characterization and identification of cryptic species, providing critical insights into phylogenetic and evolutionary relationships. Sitophilus Linnaeus, 1758 grain weevils can benefit from such tools as key pest species of stored products and also as sources of archeological information on human history and past urban environments. Moreover, the phylogenetic relationship among these weevil species remains controversial and is largely based on single DNA fragment analyses. Therefore, cytogenetic analyses and genome size determinations were performed for four Sitophilus grain weevil species, namely the granary weevil Sitophilus granarius (Linnaeus, 1758), the tamarind weevil S. linearis (Herbst, 1797), the rice weevil S. oryzae (Linnaeus, 1763), and the maize weevil S. zeamais Motschulsky, 1855. Both maize and rice weevils exhibited the same chromosome number (2n=22; 10 A + Xyp). In contrast, the granary and tamarind weevils exhibited higher chromosome number (2n=24; 11 A + Xyp and 11 A + neo-XY, respectively). The nuclear DNA content of these species was not proportionally related to either chromosome number or heterochromatin amount. Maize and rice weevils exhibited similar and larger genome sizes (0.730±0.003 pg and 0.786±0.003 pg, respectively), followed by the granary weevil (0.553±0.003 pg), and the tamarind weevil (0.440±0.001 pg). Parsimony phylogenetic analysis of the insect karyotypes indicate that S. zeamais and S. oryzae were phylogenetically closer than S. granarius and S. linearis, which were more closely related and share a more recent ancestral relationship.

High frequency of CYP337B3 gene associated with control failures of Helicoverpa armigera with pyrethroid insecticides in Brazil.

Control failures with the use of pyrethroid insecticides have been reported frequently for populations of Helicoverpa armigera (Hübner) in Brazil, since its detection in 2013. Here, we confirmed and investigated the metabolic mechanisms of pyrethroid resistance in H. armigera populations from Brazil. Mortality of H. armigera populations was lower than 50% at the highest dose (10µg a.i./3rd instar larva) of the pyrethroids deltamethrin and fenvalerate in dose-response bioassays. Very low mortality (10 to 40%) was obtained at a diagnostic dose of 10µg a.i./larva for each pyrethroid in H. armigera populations collected from different agricultural regions in Brazil, from 2013 to 2016. In synergist bioassays, when larvae were treated with PBO synergist, the mortality of all populations tested was 100%. The frequency of the cytochrome P450 CYP337B3 gene was above 0.95 in all populations of H. armigera. We found only fourteen heterozygous H. armigera out of 497 individuals tested for this gene subfamily. Our results indicated that H. armigera populations from Brazil have different degrees of susceptibility to deltamethrin and fenvalerate, but all populations can be considered tolerant to pyrethroid insecticides. The chimeric P450 CYP337B3 enzyme is one of the main mechanisms of pyrethroid resistance in Brazilian H. armigera populations.

Mesoamerican origin and pre- and post-columbian expansions of the ranges of Acanthoscelides obtectus say, a cosmopolitan insect pest of the common bean.

An unprecedented global transfer of agricultural resources followed the discovery of the New World; one consequence of this process was that staple food plants of Neotropical origin, such as the common bean (Phaseolus vulgaris), soon expanded their ranges overseas. Yet many pests and diseases were also transported. Acanthoscelides obtectus is a cosmopolitan seed predator associated with P. vulgaris. Codispersal within the host seed seems to be an important determinant of the ability of A. obtectus to expand its range over long distances. We examined the phylogeographic structure of A. obtectus by (a) sampling three mitochondrial gene sequences (12s rRNA, 16s rRNA, and the gene that encodes cytochrome c oxidase subunit I (COI)) throughout most of the species' range and (b) exploring its late evolutionary history. Our findings indicate a Mesoamerican origin for the current genealogical lineages of A. obtectus. Each of the two major centers of genetic diversity of P. vulgaris (the Andes and Mesoamerica) contains a highly differentiated lineage of the bean beetle. Brazil has two additional, closely related lineages, both of which predate the Andean lineage and have the Mesoamerican lineage as their ancestor. The cosmopolitan distribution of A. obtectus has resulted from recent expansions of the two Brazilian lineages. We present additional evidence for both pre-Columbian and post-Columbian range expansions as likely events that shaped the current distribution of A. obtectus worldwide.

Does the aggressiveness of the prey modify the attack behavior of the predator Supputius cincticeps (Stål) (Hemiptera, Pentatomidae)? / A agressividade da presa altera o comportamento de ataque do predador Supputius cincticeps (Stål) (Hemiptera, Pentatomidae)?

Does the aggressiveness of the prey modify the attack behavior of the predator Supputius cincticeps (Stål) (Hemiptera, Pentatomidae)? The stink bug Supputius cincticeps (Stål) (Hemiptera, Pentatomidae) is a predator found in several Brazilian regions, which possesses desirable attributes as a natural control agent and in biological control programs. The aim of this study was to test if the attack behavior and predation success of S. cincticeps were affected by prey species. Larvae of Tenebrio molitor (L.) (Coleoptera, Tenebrionidae), Spodoptera frugiperda (J. E. Smith) (Lepidoptera, Noctuidae), and Thyrinteina arnobia (Stoll) (Lepidoptera, Geometridae) were offered to S. cincticeps in laboratory bioassays where predatory attack and prey defensive behaviors were observed for 2-hour periods. The attack behavior of S. cincticeps changed with the prey species offered. More than 25% of T. molitor and S. frugiperda larvae were immediately attacked, but T. arnobia was not immediately attacked by S. cincticeps. Successful attack (i.e., successful insertion of the predator stylets into the prey) depends on the region of the body attacked, with a greater proportion of successful attacks in the anterior than in the median or posterior regions. Larvae of T. arnobia and S. frugiperda displayed a sequence of abrupt head and body movements in response to S. cincticeps attack. Attempts of predation were more successful on T. molitor and S. frugiperda than on T. arnobia. Information about the differential attack behavior of S. cincticeps on different prey species is important for designing successful biological control programs using this hemipteran predator.

A agressividade da presa altera o comportamento de ataque do predador Supputius cincticeps (Stål) (Hemiptera, Pentatomidae)? O percevejo Supputius cincticeps (Stål) (Hemiptera, Pentatomidae) é um predador encontrado em várias regiões brasileiras, que possui atributos desejáveis como agente de controle natural ou em programas de controle biológico. O objetivo deste trabalho foi testar se diferentes espécies de presa podem afetar o comportamento de ataque e o sucesso de predação de S. cincticeps. Larvas de Tenebrio molitor (L.) (Coleoptera, Tenebrionidae), Spodoptera frugiperda (J. E. Smith) (Lepidoptera, Noctuidae) e Thyrinteina arnobia (Stoll) (Lepidoptera, Geometridae) foram oferecidas a S. cincticeps, em bioensaios de laboratório, onde o comportamento de ataque do predador e o comportamento de defesa das presas foram observados por período de duas horas. O comportamento de ataque de S. cincticeps às presas apresentou variações nas frequências dos atos predatórios. O sucesso da inserção dos estiletes na presa depende da parte do corpo que é atacada (anterior, mediana ou posterior), apresentando maior sucesso quando o ataque ocorre na região anterior. As larvas de T. arnobia e S. frugiperda apresentaram maior frequência de movimentos bruscos quando atacadas por S. cincticeps, enquanto as de T. molitor não exibiram tais reações. Consequentemente, o sucesso da predação de S. cincticeps foi maior sobre T. molitor e S. frugiperda e consideravelmente menor em T. arnobia. Essas informações sobre as diferenças no comportamento de ataque de S. cincticeps a diferentes presas são úteis para os programas de controle biológico envolvendo hemípteros predadores.