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Case Study 2: Halyomorpha halys (Stål) in Europe
Abstract
First discovered in Switzerland in 2004, the brown marmorated stink bug (BMSB) Halyomorpha halys (Stål) is now present in 80% of European countries. A few years after its introduction, BMSB has caused severe losses, particularly in fruit and hazelnut orchards in southern and eastern Europe, and is currently a serious threat to agricultural production. Due to its bio-ecological characteristics, BMSB is difficult to control. The use of broad-spectrum insecticides has been inconclusive in reducing damage, and has disrupted integrated pest management programmes with negative economic and environmental impacts. Some countries have approved classical biological control programmes, such as the one launched in Italy in 2020, as an environmentally sustainable long-term solution to managing the invasive pest. This chapter provides a comprehensive overview of studies carried out in Europe covering the history of its invasion, biology, natural enemies, ecology and behaviour. Integrated management options, with particular emphasis on biocontrol is also covered, including innovative approaches for monitoring and control.
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BACKGROUND
Halyomorpha halys is one of the most damaging invasive agricultural pests in North America and southern Europe. It is commonly monitored using pheromone traps, which are not very effective because few bugs are caught and some escape and/or remain outside the trap on surrounding plants where they feed, increasing the damage. Other monitoring techniques are based on visual sampling, sweep‐netting and tree‐beating. However, all these methods require several hours of human labor and are difficult to apply to large areas. The aim of this work is to develop an automated monitoring system that integrates image acquisition through the use of drones with H. halys detection through the use of artificial intelligence (AI).
RESULTS
The study results allowed the development of an automated flight protocol using a mobile app to capture high‐resolution images. The drone caused only low levels of disturbance in both adult and intermediate instars, inducing freezing behavior in adults. Each of the AI models used achieved very good performance, with a detection accuracy of up to 97% and recall of up to 87% for the X‐TL model.
CONCLUSION
The first application of this novel monitoring system demonstrated the potential of drones and AI to detect and quantify the presence of H. halys. The ability to capture high‐altitude, high‐resolution images makes this method potentially suitable for use with a range of crops and pests. © 2024 Society of Chemical Industry.
The brown marmorated stink bug Halyomorpha halys (Heteroptera:
Pentatomidae) is a harmful polyphagous species that recently became a key pest of hazelnut. Its rapid spread in different areas worldwide is causing yield losses. For this reason, several studies have focused on low-impact control strategies in an integrated pest management (IPM) framework. The reduction of pesticide use is the main goal of IPM, and for this the prediction of H. halys population development is an important part of setting up innovative strategies. Currently, projections are empirically based on data from field monitoring. In addition to the estimates being rough, monitoring takes time and resources and requires expert technicians. Mathematical models may support monitoring, more precisely predicting potential pest outbreaks. This study is the first part of a general ordinary differential equation (ODE) model describing insect pest populations in the case of H. halys. Accordingly, we analyzed the current literature on the species looking for quantitative biological data that support the model application. The resulting model has the potential for describing H. halys populations over time and through its life stages, considering the interaction between the species and the external environment, as well. Moreover, this feasibility analysis provided promising results for further field validation experiments.
Simple Summary
The brown marmorated stink bug, Halyomorpha halys (Stål), is a highly polyphagous invasive species in Europe. This species can puncture fruits, causing fruit deformations and abscissions. Recently, H. halys was detected on olives in Greece and Italy. Injuries are being attributed to this pest by olive growers in northern and central Italy, but studies are necessary to confirm feeding and describe the damage. Here, we evaluated the effect of the artificial infestation of olive trees with different densities of H. halys on fruit drop and characterized the phenolic composition in injured vs. healthy fruits.
Abstract
The brown marmorated stink bug, Halyomorpha halys (Stål), is an invasive species causing economic crop losses. This species was recently detected attacking olive fruits. The aim of this study was to characterize feeding damage. Olive samples were initially collected from a field where H. halys was reported to cause damage to olive fruits. Hence, we conducted a field trial on the Moraiolo variety using sleeve cages to test the effect of H. halys feeding pressure on olive fruit drop and evaluated the effect of feeding on fruit quality. We tested two densities of H. halys (two or eight adults/cage) at two different stages of olive development, pre- and post-pit hardening. High pressure of H. halys before pit hardening caused a significant fruit drop compared to the control. In addition, chemical analysis of damaged and infested fruits revealed higher levels of total phenols compared to healthy fruits. These findings indicate that feeding by H. halys induced a stress response in the plants that could translate in quality variations in the olive drupes.
Die Marmorierte Baumwanze (Halyomorpha halys) wurde 2004 zum ersten Mal in der Schweiz nachgewiesen. Seither hat sie sich als Schädling im Obstanbau etabliert. Zuletzt kam es 2019 in verschiedenen Ländern Europas, vor allem in Italien, zu erheblichen Ernteausfällen. Mit ihrem breiten Wirtsspektrum, das alle gängigen Obstkulturen in der Schweiz umfasst, stellt die eingeschleppte Wanze eine grosse Herausforderung für Produzentinnen und Produzenten dar.
In this paper, we present a case study on the transition to informed automated decision-making processes in smart agriculture. Our focus is on addressing the challenges posed by the new invasive global pest, Halyomorpha halys (HH), which causes significant economic damage to fruit orchards. Specifically, we aim to automate the time-and labor-intensive process of HH scouting, which is traditionally performed by phytosanitary operators. Our objective is to demonstrate the pipeline of technological and methodological decisions necessary for automating the scouting process. To gather images from the orchard, we utilized a drone equipped with an RGB camera as well as other devices such as smartphones. Despite the suboptimal quality of the images captured by the drone's camera, our computer vision algorithm for HH detection yields promising results. These findings serve as an encouragement to further explore the possibilities of technology transfer to the agriculture.
This paper explores the utilization of innovative technologies such as RGB cameras, drones, and computer vision algorithms, for monitoring pests in orchards, with a specific focus on detecting the Halyomorpha halys (HH), commonly known as the "brown marmorated stink bug". The integration of drones and machine learning (ML) into integrated pest management shows promising potential for effectively combating HH infestations. However, challenges arise from relying on vision models solely trained using high-quality images from public datasets. To address this issue, we create an ad hoc dataset of on-site images mainly captured with the help of a drone as well as other devices. We initially conduct an in-depth analysis of the captured images, considering factors such as blurriness and brightness, to possibly improve the performance of the ML algorithms. Afterwards, we undertake the training and evaluation of diverse ML models using distinct approaches within the YOLO framework. We employ a range of metrics to compare their performance and ultimately achieve a satisfactory outcome. Through the optimization of ML models and the correction of image imperfections, we contribute to advancing automated decision-making processes in pest insect monitoring and management, specifically in HH monitoring.
The Brown marmorated stink bug (BMSB) [Halyomorpha halys (Hemiptera: Pentatomidae)] is a polyphagous pest causing significant damage to approximately 300 crops, such as nuts, vegetables, and ornamentals. In 2017, the BMSB was discovered for the first time in Türkiye. There is currently no published data available on the biology of the pest in Türkiye. This preliminary study was carried out in Sakarya province, where the BMSB has observed a low population since 2021. In this study, some biological parameters such as voltinism, mortality rates, egg hatching rates, and egg-adult developmental times of the 1st and 2nd generations of the insect populations were determined. The study was carried out under semi-field conditions and laboratory. Considering the BMSB's minimum temperature threshold, which has yet to be determined in Turkey, the accumulation of degree days was calculated using the references to four possible thresholds (DD12, 12.5, 13, 13.5) and was determined to be between 536.91 - 608.69 DD. The average egg-adult developmental time was 47.85 days for the 1st generation at naturally fluctuating temperatures and 47.13 days for the 2nd generation under laboratory conditions at 25 ֯C. The hatching rate of egg masses was determined to 90.63% in the 1st generation and 57.75% in the 2nd generation. Total mortality in the first generation was 22.97% and 90.24% in the second generation. It was revealed that the insect could produce two generations in Türkiye, but the number of egg-producing adults and eggs laid in the second generation was significantly lower than that in the first. This preliminary study was carried out with a limited number of samples due to the initial infesting in the region and, therefore more comprehensive research is needed to reveal the the biology of BMSB in the country.
Urban areas are often populated by specific species of insects, some colorful and appealing, such as ladybugs and butterflies, and others irritating as nuisance bitters or as vectors of pathogens of public health importance. Mosquitoes in urban areas often utilize habitats adjacent to human residences, while phytophagous insect species such as stink bugs often colonize ornamental plants and utilize human-made structures including houses as overwintering shelters. This article discusses the early detection and the current distribution of two invasive mosquito species, Aedes albopictus Skuse 1894 and Ae. japonicus (Theobald 1901), in Serbia, introduced in 2009 and 2018, respectively. From the first findings until today, regular monitoring has been carried out and the establishment of both species in the newly invaded areas has been confirmed. Both species can become nuisance species, especially at high population densities, but more importantly, they are capable of transmitting a wide variety of arboviruses of public health importance. This article also discusses two invasive stink bug species Halyomorpha halys Stål 1855 and Nezara viridula Linnaeus 1758, introduced in Serbia in 2015 and 2008, respectively. These two stink bug species have also been monitored, and the establishment of their populations in the country has been confirmed. Both species have caused damage to a wide range of crops and ornamental plants and sometimes become nuisance pests in urban areas.
The brown marmorated stink bug Halyomorpha halys is an Asian species that has become a major agricultural pest in North America and Europe. Ants from the genus Crematogaster are predators of H. halys nymphs in Asia, as well as in the Mediterranean, where known native predators are still few. At the same time, ants usually do not harm H. halys eggs, which are the target of the main biological control agents, the scelionid parasitoids of the genus Trissolcus. However, ants, as generalist predators and territorial organisms, may kill or displace a variety of other insects, potentially interfering with parasitoids and biological control programmes. We conducted laboratory experiments to investigate the interactions between the Mediterranean ant Crematogaster scutellaris and the parasitoids T. japonicus and T. mitsukurii, evaluating the possibility that the ants could damage the parasitized eggs, attack the parasitoids during emergence or interfere with the egg-laying behaviour of female parasitoids. Our results demonstrate that C. scutellaris is not able to damage parasitized eggs and is not aggressive towards adult parasitoids at any stage. The presence of ants can slow down the parasitization rate in T. mitsukurii females in the smallest laboratory setups; however, this has not been observed in a more natural setting. We suggest that ants may play a complementary role together with egg-parasitoids in the control of H. halys without interfering with each other.
Female egg parasitoids must optimize their ability to find a suitable host for reproduction in a limited foraging time. Odorant cues associated with the plant–host complex play an essential role in guiding females toward the host. However, parasitoid response is not always identical within the same genotype, and it could be influenced by the environment. This phenotypic plasticity affects parasitoid behavior and morphology and is directly linked to rearing conditions. Yet, how plasticity influences olfactory responses of egg parasitoids toward plant–host odors is largely unexplored. Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) is an effective biocontrol agent of the invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). Laboratory no-choice and choice tests showed T. japonicus potential to develop in eggs of non-target Pentatomidae. In Y-tube olfactometer we evaluated the olfactory responses of T. japonicus reared on different hosts toward plant–host derived volatiles associated with H. halys and two other stink bug species. Parasitoids reared on the main host H. halys positively responded only to odors from V. faba–H. halys complex. When reared on alternative hosts, T. japonicus was smaller and did not exhibit attraction to any stimuli, although egg load was only partially affected. Host-induced phenotypic plasticity should be considered when evaluating parasitoids for classical biological control.
Halyomorpha halys (Stål), the brown marmorated stink bug, is a highly invasive insect species that causes significant agricultural losses, especially to orchard fruits, vegetables, herbaceous and ornamental plants. It is also a nuisance pest that seeks shelter in indoor spaces during the winter months. Harnessing H. halys virome can result in new environmentally sustainable approaches to contain its populations and its relatated agricultural damages. In this study, RNA-seq data were used to explore the virome associated to ten field populations collected in the Lombardy region in Northern Italy. We identified six complete viral genomes, three of which were previously unknown, belonging to the orders Reovirales, Articulavirales, Ghabrivirales, Durnavirales, and Picornavirales. The prevalence of the six viruses was evaluated by Real-time reverse transcription-quantitative PCR on eighty individuals. Halyomorpha halys ifla-like virus 2 turned out to be the most geographically widespread virus, as it was found in more than 50% of the analyzed insects and in nine out of the ten sampling locations. Moreover, in some individuals, this iflavirus was found in association with each of the other viruses in various combinations that involved up to four viruses. Further studies on such virus-virus interactions and their relationships with the insect host may open the possibility to exploit these naturally occurring viruses as specific and targeted biocontrol agents of H. halys.
The main purpose of the study was to examine the potential of crops, such as soybeans (Glycine max), sunflowers (Helianthus annuus), alfalfa (Medicago sativa), and sorghum (Sorghum bicolor), as trap crops for Halyomorpha halys. We monitored the abundance and seasonal dynamics of H. halys (egg clusters, larvae, and adults) on a selected number of various crops at 10-day intervals. The experiment was performed in two different regions of Slovenia (western and central) and in two different years (2021, 2022). The results varied depending on the location and the year. In the first experiment, data from the entire year showed that sorghum was the most attractive for H. halys adults (1.56 ± 0.12), followed by sunflowers (0.61 ± 0.05), soybeans (0.37 ± 0.03) and alfalfa (0.41 ± 0.21). In the second experiment, the abundance numbers of the pest were significantly lower compared to those of the first experiment [sorghum and soybeans (0.003 3 ± 0.002), sunflowers (0.000 3 ± 0.000 3)]. In both cases, the abundance numbers increased when all the crops entered the fruit development stage (BBCH 70+). Overall, the lower density of the H. halys population and the experimental design could also be some of the factors for such a low incidence of stink bugs in the central region of the country. More research will be needed to further develop effective control methods for this invasive pest.
The brown marmorated stink bug (BMSB), Halyomorpha halys, is a phytophagous invasive pest native to south-eastern Asia, and it is now distributed worldwide. This species is considered to be one of the most damaging insect pests in North America and in Europe. In agriculture, the predominant approach to managing BMSB is based on the use of insecticides, specifically pyrethroids and neonicotinoids. Unfortunately, the biology of the species and its facility to develop mechanisms of resistance to available pesticides has induced farmers and scientists to develop different, least-toxic, and more effective strategies of control. In a territorial area-wide approach, the use of a classical biological control program in combination with other least-toxic strategies has been given prominent consideration. Following exploratory surveys in the native range, attention has focused on Trissolcus japonicus, a small scelionid egg parasitoid wasp that is able to oviposit and complete its larval development in a single egg of H. halys. A common method for detecting egg parasitoids in the native range involves the placement of so-called ‘sentinel’ egg masses of the pest in the environment for a short period, which are then returned to the laboratory to determine if any of them are parasitized. Outside of the area of origin, the use of fertile sentinel eggs of the alien species may lead to the further release of the pest species; an alternative is to use sterile sentinel eggs to record the presence of new indigenous egg parasitoids or to detect the dispersal of alien species (in this case, T. japonicus) released in a new environment to control the target insect pest species. This study evaluated the performance of three types of sterile sentinel eggs as a suitable substrate for the oviposition and larval development of the egg parasitoid T. japonicus in a context of combining classical biological control with a Sterile Insect Technique (SIT) approach.
The brown marmorated stink bug (Halyomorpha halys) is an invasive pest insect species, which was recently introduced from Asia to America and then to Europe. Besides causing serious damage in agriculture, this species also represents a source of intense annoyance for humans in residential areas, because large amounts of individuals can aggregate on buildings while seeking shelter before overwintering. Taking into account the need for pesticide-free pest management methods, for example light trapping, we measured the spectral sensitivity of the compound eyes of H. halys with electroretinography (ERG). In behavioural experiments, we also quantified the attraction of H. halys to 14 quasi-monochromatic light stimuli in the 368–743 nm spectral range. The dark-adapted compound eyes were mostly sensitive to the green range, but a minor sensitivity peak in the UV region was also identified. Recordings on chromatic-adapted eye preparations unequivocally revealed the presence of only a green- and a UV-sensitive photoreceptor type, with sensitivity maxima at 519 nm and 367 nm, respectively. No sign of any blue-sensitive receptor was detected, and thus only a receptor set allowing dichromatic vision was found. Based on the results of the behavioural experiments, we established that the attraction of H. halys to light is increasing with decreasing wavelength, and thus we emphasize the importance of short wavelength lights (368–455 nm) when phototactic attraction of H. halys is the aim.
Halyomorpha halys (Stål) (Hemiptera, Pentatomidae) was accidentally introduced to North America and Europe, becoming a key pest of many important crops. In its native range, it is attacked by egg parasitoids, including Trissolcus japonicus (Ashmead), considered to be the main species, and T. mitsukurii (Ashmead) (Hymenoptera, Scelionidae). Trissolcus japonicus was detected in North America in 2014 and Europe in 2017, while T. mitsukurii was detected in Australia in the early 20 th century and in Europe in 2016. Both species now appear established in the new areas. The present study used the MaxEnt algorithm to clarify the geographic dimension of the potential interaction between H. halys and these two parasitoid species, and to indicate where the release of one or the other parasitoid species is more likely to be effective. We found that the suitability for the two parasitoids overlaps the H. halys native range completely. In invaded areas, T. japonicus showed higher potential habitat suitability at the global scale, compared to T. mitsukurii , and also higher potential suitability at lower latitudes at continental and national scales. These results can substantially improve the effectiveness of biological control against H. halys , by targeting the releases of parasitoids to the areas where each species is most likely to succeed.
Over the past decade, Halyomorpha halys has become one of the main threats to hazelnut production. Its trophic activity makes kernels inedible due to strongly detrimental effects on the organoleptic quality. Its management in Italy is still tricky due to the lack of effective native biocontrol agents and authorized and effective insecticides. A field test was performed on San Giovanni (SG) and Tonda Romana (TR) cultivars (early and late ripening, respectively) to assess the intensity of cimiciato damage with different pest management approaches (no insecticide and integrated pest management, IPM). Moreover, phenological analysis of fruits and the monitoring of stink bug species by traps and plant beating were carried out. In the untreated plots, the SG cv showed a higher cimiciato incidence with respect to the late TR cv (40% SG-NI vs. 23% TR-NI). This was probably due to the different phenological phases in which stink bugs injured the fruits. In fact, stink bug bites provoke different kinds of injuries (blanks, shriveled, and cimiciato) according to the fruit's development period. Indeed, in the period of highest insect occurrence in the field, the fruits of the early cv (SG) were in kernel expansion, a phenological phase in which bug injuries are more likely in cimiciato defects. Lastly, the IPM did not provide sufficient fruit protection (19% SG-IPM vs. 11% TR-IPM). The interaction between the phenological development of hazelnuts and the brown marmorated stink bug represents a critical aspect in understanding and implementing effective strategies for controlling this key pest on hazelnut trees.
Es confirma la presència de l'espècie Halyomorpha halys a les Illes Balears a partir d'un exemplar capturat a Palma (Mallorca). Es compara amb l'espècie autòctona propera Rhaphigaster nebulosa. La confirmació és d'importància al tractar-se d'una possible plaga agrícola. Paraules clau: Hemiptera, Pentatomidae, Halyomorpha halys, Rhaphigaster nebulosa, espècie invasora, Illes Balears. CONFIRMATION OF THE PRESENCE OF Halyomorpha halys (STÅL, 1855) (HEMIPTERA: PENTATOMIDAE) IN THE BALEARIC ISLANDS. The presence of the species Halyomorpha halys in the Balearic Islands is confirmed from a specimen captured in Palma (Mallorca). It is compared with the nearby autochthonous species Rhaphigaster nebulosa. This confirmation is important as it is a possible agricultural pest.
The brown marmorated stink bug, Halyomorpha halys Stål (Hemiptera: Pentatomidae), is native to Japan, China, Taiwan, and Korea. Its dispersion from Asia to the United States of America and Europe caused serious damage to fruit, vegetables, and high-value crops. In Greece, damages are reported in kiwi orchards in the regions of Pieria and Imathia, which are the main production areas of kiwifruit. Greek kiwifruit production is expected to increase twofold within the next years. The aim of this research is to study the terrain and canopy properties that may have an impact on the development of H. halys populations. Thus, five kiwi orchards in total were selected in the regions of Pieria and Imathia. Τen traps were installed from early June to late October within each selected kiwi orchard–two types of traps at every side of the orchards and the center. The installed traps were examined weekly and the number of the captured H. halys was recorded. During the same days, sentinel satellite images were analyzed to calculate the vegetation index, NDVI (Normalised Difference Vegetation Index), and NDWI (Normalised Difference Water Index). The results showed population variability within the kiwi orchards since the population of H. halys was higher in areas with high NDVI and NDWI values. Additionally, our research revealed that H. halys prefers to develop populations at higher altitudes at both regional and field scales. The results of this research can be used to reduce damages by H. halys in kiwi orchards using different rates of pesticides depending on the prediction of the population size. There are multiple benefits of the proposed practice, such as a reduction in the production cost of kiwifruits, an increase in farmers’ profit, and environmental protection.
Materials to the distribution of true bugs (Hemiptera: Heteroptera) in selected localisations of southern and eastern Poland]. New faunistic data on the occurrence of true bugs in 9 zoogeographical regions of southern and eastern Poland: the Bieszczady Mts., the Eastern Beskids Mts., the Western Beskids Mts., the Pieniny Mts., the Sandomierz Lowland, the Wielkopol-ska-Kujawy Lowland, the Roztocze, the Lublin Upland and the Mazurian Lakeland are presented. The paper includes the data concerning 171 true bugs species from 32 families collected in 80 localities within 58 10x10 km UTM squares. Aellopus atratus, Campylosteira verna, Chilacis typhae, Coriomeris denticulatus, Dufouriellus ater, Loricula elegantula, Odontoscelis fuliginosa, Peri-trechus nubilus, Pseudoloxops coccineus, Salicarius roseri and Velia caprai are found for the first time in the region of the Eastern Beskids Mts., Acalypta carinata, Aradus bimaculatus, Dufouriellus ater, Grypocoris sexguttatus, Lasiosomus enervis, Physatocheila dumetorum, Plinthisus pusillus, Polymerus nigrita and Stalia boops are found for the first time in the Sandomierz Lowland, Rhy-parochromus vulgaris is new to the Roztocze, Cimex lectularius is new to the Lublin Upland, while Aneurus avenius and Prostemma aeneicolle are first detected in the Mazurian Lakeland. Additionally, new data on invasive species Leptoglossus occidentalis and Nezara viridula were also provided.
Unintentional introduction of natural enemies has increased in recent years due to a massive rise in global trade and tourism. One such natural enemy is the Asian egg parasitoid Trissolcus japonicus, a promising agent for classical biological control of Halyomorpha halys. In Europe, adventive T. japonicus populations have been detected in Switzerland, Italy and Germany. Host specificity testing demonstrated that its fundamental host range is fairly broad; however, it is unclear whether spatial or temporal refuges reduce parasitism of non-target species in the field. To address this, the realized host range of T. japonicus was assessed over three years by exposing sentinel egg masses of H. halys and 18 non-target species and collecting naturally-laid egg masses in Switzerland and Italy. In total, 15 of 18 non-target species were successfully parasitized by T. japonicus in the field, confirming its broad fundamental host range. However, most non-target species were less parasitized by T. japonicus than H. halys, profiting from either partial temporal or spatial refuges from parasitism. Species with an unusual life cycle and the same ecological niche as H. halys, such as Pentatoma rufipes, which was the most parasitized non-target species in both countries, potentially face an increased risk of parasitism. In contrast, beneficial non-target effects may occur for the invasive pest, Nezara viridula, which suffered high non-reproductive mortality induced by T. japonicus. In both cases, life table studies will be needed to determine the impact of non-target parasitism, and the potential consequences at the population level.
The brown marmorated stink bug, Halyomorpha halys, is a pentatomid bug of Eastern Asian origin that became an economically relevant pest in the Eurasian and American continents. Management of this species is limited to use of chemical insecticides: an inefficient method due to the strong adaptability of the target pest. The sterile insect technique (SIT) is potentially a valid tactic in the search for nontoxic alternatives. In this work, we investigated the suitability of mass-trapped overwintering males, collected during the aggregation phase before the winter diapause, for their release as competitive sterile males in an SIT programme. Differently from previous studies, irradiation was applied with a linear accelerator device that produced high-energy photons. Following a similar scientific protocol with newly emerged irradiated males, the effects of X-ray irradiation on physiological parameters (longevity, fecundity and fertility) were assessed. In addition, behavioural bioassays were carried out in no-choice conditions to evaluate if irradiation interferes with mating processes. The results are very encouraging; the effects of the irradiation at 32 Gy did not differ from the controls in the longevity or fecundity of the exposed overwintering adults. The hatching rate of the eggs laid by the fertile females that had mated with the irradiated males was less than 5%. The results of behavioural bioassays showed that the irradiation did not cause a significant impact on the quality of the sterile males. More research is warranted to evaluate the mating competitiveness of sterile males in semi-field and field conditions.
Among the invasive insect species, Halyomorpha halys (Stål) (Heteroptera: Pentatomidae), has been causing significant damages in many parts of the world, particularly in vegetables, field crops and tree fruits. In the scientific studies conducted in Türkiye and the world so far, egg parasitoids of H. halys have been found, but adult parasitoids have not been detected. Two specimens of Cylindromyia bicolor were reared from an adult of H. halys collected in northern Türkiye (Borçka, Artvin). Adults of H. halys is reported for the first time as a host of Cylindromyia bicolor (Olivier) (Diptera: Tachinidae) in Türkiye as well as the rest of the world. Özet İstilacı böcek türlerinden Halyomorpha halys (Stål) (Heteroptera: Pentatomidae), başta sebzeler, tarla bitkileri ve ağaç meyveleri olmak üzere dünyanın birçok yerinde önemli zararlara neden olmaktadır. Şimdiye kadar ülkemizde ve dünyada yapılan bilimsel çalışmalarda, H.halys'ın yumurta parositoidleri bulunmuş fakat ergin parasitoidleri tespit edilmemiştir. Cylindromyia bicolor'un iki örneği, Türkiye'nin kuzeyinden (Artvin, Borçka) toplanan Halyomorpha halys ergininden elde edilmiştir. Halyomorpha halys erginlerinin ilk kez Cylindromyia bicolor'un (Olivier) (Diptera: Tachinidae) konukçusu oldukları belirlenmiştir.
The highly destructive Asian brown marmorated stink bug (Halyomorpha halys, BMSB) invaded Europe, Caucasus region, and North and South America. Efforts to control it are ongoing in the Palearctic European-Mediterranean Basin and North America by introducing and redistributing two Asian stenophagous scelionid egg parasitoids (Trissolcus japonicus and T. mitsukurii) that are attacked by an adventive oligophagous pteromalid Asian hyperparasitoid (Acroclisoides sinicus). Large BMSB nymphs and adults may be parasitized by new associations of oligophagous tachinid flies and immature stages by egg parasitoids and predators. The terms stenophagous and oligophagous are commonly used to define narrow and wider ranges, respectively, of food eaten, but here they refer to the range of hosts attacked by adult female parasitoids. A holistic weather-driven physiologically based demographic model (PBDM) of the tritrophic interactions was developed to evaluate prospectively the impact of natural enemies on the biological control of BMSB under current and climate change weather. Our study focuses on the European-Mediterranean region, with the results for the USA, Mexico, and Central America reported as supplementary information. The PBDM analysis suggests that biotypes of the egg parasitoids T. japonicus and T. mitsukurii with high search capacity could suppress BMSB regionally, but the requisite levels of parasitism by these parasitoids for economic control are not observed in their native range nor in invaded areas. The model suggests that the action of T. japonicus is greater than that of T. mitsukurii, but that joint interactions of the two egg parasitoids would provide higher mortality of BMSB. Field data and model results suggest that the egg hyperparasitoid A. sinicus has a modest negative impact on the suppression of BMSB. Moreover, tachinid parasitoids of adults could have an important supplemental role in suppressing BMSB densities. Analysis suggests that new biotypes of egg parasitoids and species of tachinid parasitoids of large nymphs and adults be sought.
In addition to recently published checklists of Heteroptera from the Canary Islands, new records of Dieuches schmitzi Reuter, 1893 (Heteroptera: Rhyparochromidae), Cydnus aterrimus (Forster, 1771) (Heteroptera: Cydnidae) and Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) are reported.
Brown marmorated stink bug (BMSB), Halyomorpha halys, is a polyphagous invasive pest whose spread and damage are
increasing with global commercial activities. In this study, following the invasion of Black Sea Region in 2018, spread, population density and change of the pest were investigated in the years 2019, 2020, and 2021, possible causes of spread and measures to be taken were evaluated. Course of population was monitored with pheromone traps placed in 141, 120, and 162 locations in 8 provinces along the coastline of Black Sea Region. High population density was detected at all locations of Artvin and Rize provinces. Since the population interactions continued near the Georgian border, about 98% of the total population in the region was seen in these two provinces. Weekly average population level was 7.36 adults/traps in Artvin and 9.11 adults/traps in Rize Province; spread of the pest continued from east to west and irregular and further-apart local populations were detected at some points. It was determined that it caused population density-dependent economic damage on different hosts including hazelnut, kiwi, citrus, maize and beans. This research examined the H. halys population distribution in Türkiye, potential problems associated to that too, ways that it spreads, and possible solutions.
Resumen: Se aporta la primera cita de Halyomorpha halys (Stål, 1855) (Hemiptera, Pentatomidae) para Navarra, especie ya conocida en la península ibérica de toda Cataluña, Guipúzcoa, Zaragoza y Portugal. Debido a su creciente expansión, se prevé una rápida dispersión por el resto del territorio peninsular. Abstract: Halyomorpha halys (Stål, 1855) (Hemiptera, Pentatomidae), new record for the Foral Community of Navarra (Spain). The first record of Halyomorpha halys (Stål, 1855) (Hemiptera, Pentatomidae) for Navarra, species already known in the Iberian Peninsula throughout Catalonia, Guipúzcoa, Zaragoza, and Portugal, is provided. Due to its increasing expansion, a fast spreading throughout the rest of the Iberian territory is expected.
Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae), new record for Aragon (NE Spain).
BACKGROUND
Classical biological control has been identified as the most promising approach to limit the impact of the invasive pest species Halyomorpha halys (Heteroptera: Pentatomidae). This study investigated the parasitism rate at sites where the biocontrol agent Trissolcus japonicus (Hymenoptera: Scelionidae) was released and where its unintentional introduction took place, in the Trentino–South Tyrol region. The effect of land‐use composition was studied to understand which factors favor the establishment of hosts and parasitoids, including native and exotic species.
RESULTS
The released T. japonicus were detected a year after the start of the program, with a significant parasitoid impact and discovery, compared to control sites. Trissolcus japonicus was the most abundant H. halys parasitoid, and Trissolcus mitsukurii and Anastatus bifasciatus were recorded also. The efficacy of T. mitsukurii was lower in sites where T. japonicus was successfully established, suggesting a possible competitive interaction. Parasitism level by T. japonicus at the release sites was 12.5% in 2020 and 16.4% in 2021. The combined effect of predation and parasitization increased H. halys mortality up to 50% at the release sites. Landscape composition analysis showed that both H. halys and T. japonicus were more likely to be found at sites with lower altitude and with permanent crops, whereas other hosts and parasitoids preferred different conditions.
CONCLUSION
Trissolcus japonicus showed a promising impact on H. halys, at release and adventive sites, with minor nontarget effects, mediated by landscape heterogeneity. The prevalence of T. japonicus in landscapes with permanent crops could support IPM in the future. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
Halyomorpha halys (Stal, 1855) (Hemiptera: Heteroptera: Pentatomidae) invasion in Georgia territory first observed in 2015 year. In
2016-2019 an outbreak of H. halys resulting huge economic losses which negatively affected to the income of small-scale farmers as
well as the Georgian economy. The article reviews the bioecological characteristics of the insect at various locations, such as in Georgia,
other invaded areas and its natural distribution range of H. halys . This article describes the life history, food specialization, economic
importance of H. halys. Also the recent results of studies on H. halys natural enemies, control tools and management strategies are
incorporated to the article. In the face of climate change, the risks of insect outbreaks increase from year to year. Invasive agricultural
pests such as H. halys pose a major threat to agriculture crop production and food security. To have a comprehensive information about
H. halys has a huge importance to effectively plan and implement measures without or with minimal adverse environmental impact.
The presence of the invasive species Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae), the brown marmorated stink bug (BMSB), was first confirmed in Portugal in late 2018. In this note, an update to the known distribution in the Portuguese territories, including the first record in the Madeiran Archipelago, is presented. In Portugal, the BMSB has now been detected 51 times more, including six new districts, with increasing records registered in the last two years that envisage an exponential outspread in this territory. Also, the re-occurrence of individuals in the same localities in past years and the detection of a high number of individuals in some of them suggest that small stable populations may already exist, at least in some regions.
The invasive stink bug species Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae), a dangerous pest of many agricultural plants, is recorded from Uzbekistan for the first time. Several imagi- nes and larvae were found in the Khorezm and Ferghana provinces in 2020 and 2022.
Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae), the brown marmorated stink bug (BMSB), is an alien invasive pest that originated from South Asia (China, Japan, Taiwan, Korea) (Hoebeke and Carter 2003). Many studies have shown that the number of invasions by pests has increased significantly in the last 5 centuries and the reason for this situation is directly related to human activities. (Pascal, Le Guyader et al. 2010). Halyomorpha halys is considered to be a dangerous pest insect species due to economic losses in agricultural areas of the countries where it is distributed. It has been observed that the pest can have 1–2 generations per year (Rice, Bergh et al. 2014) and each egg mass contains of an average of 26 eggs and, furthermore, causes significant losses in many crops such as bean, hazelnut and pear. This study was conducted between July and August in 6 different areas and a total of 18 egg masses that were thought parasitized were collected from BMSB infested fields and kept in tubes to determine if they had parasitoids. Emerged parasitoids were fed with the honey solution and bred in tubes. The specimens were identified as Anastatus bifasciatus morphologically, however, they were sent for molecular identification to the USA, and the molecular test confirmed the identification. In this study, Anastatus bifasciatus was reported as the first parasitoid recorded on Halyomorpha halys in Turkiye.
The brown marmorated stink bug Halyomorpha halys is a polyphagous insect, which has a devastating impact on agricultural production in many countries. The alteration of symbiont vertical transmission, by removing symbionts from stink bug eggs (symbiotic control), has been recently introduced in control programmes against this insect. A major advantage of this strategy is the compatibility with natural enemies, since it allows an insecticide-free approach that is not harmful to other agroecosystem components. However, the effect of anti-symbiont products on parasitism by egg parasitoids is still unexplored. Here, we investigated the impact on parasitism by native (Anastatus bifasciatus, Ooencyrtus telenomicida and Trissolcus kozlovi) and exotic (Trissolcus japonicus and Trissolcus mitsukurii) parasitoids that attack H. halys eggs, after treatment with the micronutrient biocomplex Dentamet®, used for symbiotic control. The native wasp species were tested in no-choice bioassays, showing that treatment of the egg masses did not affect emergence percentages, but the non-reproductive effects were often reduced by the biocomplex. The exotic species T. japonicus and T. mitsukurii were used in no-choice and paired choice bioassays, showing an opposite influence of Dentamet® on emergence percentage and preference in the two species. No-choice tests indicated the highest successful parasitoid emergence on biocomplex-treated egg masses for T. japonicus, while no preference in the paired comparison with eggs treated with water or untreated. In contrast, T. mitsukurii displayed the lowest parasitism after Dentamet® treatment in no-choice tests, and preferred egg masses without Dentamet® in paired choice tests. We did not record any natural symbiont acquisition by the parasitoids emerged from H. halys egg masses, indicating that the wasp fitness is very unlikely to be altered by dysbiotic effects resulting from treatments. Therefore, our results support a further implementation of symbiotic control in different crops in combination with biological control, as sustainable options for H. halys integrated pest management.
In the last decade, the invasive brown marmorated stink bug Halyomorpha halys, native to East Asia, has become one of the most serious pests for agricultural crops worldwide. First detected in Europe (in Switzerland), the insect is now widely found across the European continent and many Eurasian countries. Since its first appearance in Slovenia in 2017 it has caused considerable damage to fruit and vegetable production. Understanding the biology and behavior in the local environmental conditions is of key importance for an effective pest management. Knowledge of the voltinism of the species is crucial to anticipate critical phases of pest development and for adapting control measures that target the vulnerable life stages of the pest. A 3-year study (2019–2021) of H. halys biological parameters was performed outdoors in Nova Gorica (western Slovenia), confirming that in the sub-Mediterranean climate this pest has two overlapping generations per year. The net reproductive rates observed in the studied period indicate growing populations. The highest population growth was recorded in 2019, when the net reproductive rate of increase (R0) reached 14.84 for the summer generation and 5.64 for the overwintering generation. These findings match the current situation in Slovenia, where increasing populations of H. halys and severe crop damage have been observed since 2019.
Your article is protected by copyright and all rights are held exclusively by Deutsche Phytomedizinische Gesellschaft. This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com". Abstract The brown marmorated stink bug, Halyomorpha halys (Stål), is a pest of many annual and perennial agricultural products. The species is native to Asia. It is an awful highly polyphagous invasive pest. This study is the first comprehensive study on Halyomorpha halys (Stål) (Heteroptera: Pentatomidae), which is an invasive species in Turkey, and was conducted to determine the spread, intensity, population change and hosts of it in the Black Sea Region in 2018. In the present study, pheromone traps were placed for the pest in 6 cities, 49 counties and 149 locations between May and October, and were followed periodically. According to the results, it was determined that H. halys spread between Kemalpaşa (Artvin) and Hayrat (Trabzon). According to the number of the adults that were caught by the pheromone traps, the areas where the pest was at the highest intensity were: Hopa, Kemalpaşa, Borçka, Arhavi (Artvin) and Fındıklı (Rize). It was determined in the area where the study was conducted that many cultivated plants especially hazelnut, kiwi, corn, orange, blueberry, beans and tomato were the hosts of the pest, and recommendations were given on the precautions that must be taken against the pest.
The presence of the invasive stink bug species Halyomorpha halys in the Bordeaux vineyards since 2020 has raised concerns among wine growers in the Pomerol and Saint-Emilion AOC regions. These production areas are characterised by manual harvesting and the production of high value-added wines, whose quality is likely to be altered by the aromatic deviations generated by the presence of harvested insects. To evaluate the risk faced for these wine-growing areas, we monitored the abundance of H. halys nymphs and adults in selected vineyards. Monitoring was carried out in 2021 on a few plots (n = 5) using the beating technique for 20 vines per plot every two weeks from the beginning of the vegetative phase of vines in April to the end of harvest in September. It showed that H. halys was present in the vineyard plots, that at least one generation was occurring on grapevines and that adults were detected on vines as soon as fruit set was reached, followed by nymphs from the bunch closure stage. In 2022, a much comprehensive sampling (n = 26) was conducted to characterise the abundance of the insect, taking into account the type of landscape surrounding vineyard plots. Five beating sessions of 20 vines per plot on a monthly schedule were carried out from before fruit set to maturation. We found that 92 % of the plots were infested. Halyomorpha halys individuals was detected earlier and in higher abundance in plots surrounded by semi-natural habitats, with significantly higher abundances of nymphs. At harvest, the assessment of three transport crates for each of the 12 plots (several hundred bunches depending on the crates) showed a very low level of infestation per bunch: on average, H. halys were detected in 2 % of bunches during the manual harvesting operation. After transport, when the harvest was being received in the winery, the rate of infestation of these same bunches decreased to less than 1 %. Finally, in the winery, after the bunch processing line, no insect was observed in the optical sorting machine before these bunches were put into the fermentation tank. These observations indicate that the current population levels of H. halys may probably pose no considerable risk to the wine quality in the Pomerol and Saint-Emilion AOCs. However, this study only applies to this area of manual harvesting and cannot be extrapolated to mechanical harvesting, which is characterised by other equipment in the winery. An assessment of the risks for mechanical harvesting should therefore be conducted. Despite the findings of this survey, the quantitative evolution of populations should be monitored to anticipate any new outbreaks of this invasive insect recently arrived in the Bordeaux region.
The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), native to eastern Asia, has become one of the most serious pests of fruit orchards worldwide. This invasive species is highly polyphagous and capable of moving across the agricultural matrix at long distances. However, comprehensive studies exploring how landscape characteristics influence H. halys colonization of orchards are still lacking. Here, we investigated the impact of landscape composition on the trap captures of H. halys in 113 orchards of different fruit tree crops (i.e., apple, pear, peach, walnut and kiwi) in northern Italy. We found that landscapes rich in semi-natural habitats and vineyards and poor in annual crops supported a higher abundance of H. halys juveniles in traps. This pattern became more evident towards the end of the growing season as the abundance of juveniles increased. Adults were instead not affected by the landscape. The invasive stink bug best responded to landscape processes at large spatial scales (3000 m) confirming its high dispersal ability. Moreover, H. halys did not display a strong preference among fruit orchards, although fewer individuals were caught in walnut orchards. Our findings suggest that the habitat composition of agricultural landscapes is a key factor driving the dynamics of this pest in agroecosystems and that semi-natural habitats might be important in supporting H. halys populations and crop colonization. These effects are however limited to juveniles while adult density was similar even in landscapes with very contrasting structures.
Brown marmorated stink bug Halyomorpha halys (Stål, 1855) is an invasive and polyphagous stink bug native to Asia. It has recently invaded Europe and Bosnia and Herzegovina. It is highly polyphagous pest of many economically important commodities including tree fruit, nut crops, field crops, vegetables and ornamentals. Moreover, it is an important nuisance pest because large numbers of adults seek out artificial structures for overwintering. Monitoring of population dynamics of H. halys during two years (2020 and 2021) was performed in Banja Luka, Bosnia and Herzegovina. The pest was present through monitoring period April–October with the highest abundance in the third decade of July when all life stages were present. More individuals were caught on pyramid trap (845) compared to sticky trap (156) favoring pyramid trap for future monitoring. Total number of caught individuals was 6.5 folds higher in the second year of the monitoring indicating population increase that presents threat to agricultural production.
The emission of volatile organic compounds (VOCs) from plants is associated with biotic and abiotic stress and depends on the plant species, organs, and developmental stage. Insects use VOCs to locate their host plants and their behavior is heavily influenced by the chemical profile of each at its current phenological stage. The brown marmorated stink bug Halyomorpha halys (Hemiptera: Pentatomidae) is a highly polyphagous pest that causes significant damage to tree, vegetable, and ornamental crops worldwide. The volatile profiles of five hosts of H. halys were compared for common substances to provide insight into this insect's extreme polyphagy. Headspace collection of volatile substances was performed for five hosts of H. halys by gas chromatography-mass spectrometry (GC-MS), and their VOC profiles were compared. The results show that, although the volatile profiles of the host plants differ substantially, 13 out of the 68 identified compounds were shared. These results suggest that host recognition by H. halys is likely driven by a combination of attractive and possibly repellent compounds that work synergistically which is the first step toward decoding this pest's polyphagous nature.
Double-stranded (ds) RNA-based technologies could provide novel and potential tool for pest management with efficiency and specificity of action. However, before applying this technique in the field, it is necessary to identify effective delivery methods and evaluate the non-target effects that may occur. In this article, we evaluated the effectiveness of dsRNA by topical delivery on a species of great agricultural interest, Halyomorpha halys. The specificity of action of the dsRNA was also investigated in Rhodnius prolixus, an insect phylogenetically close to H. halys. Of the three investigated genes (putative ATPase N2B, ATPase, serine/threonine-protein phosphatase PP1-β catalytic subunit, PP1, and IAP repeat-containing protein 7-B-like, IAP), IAP and ATPase were able to induce higher mortality in H. halys nymphs compared to the control, with specific concentrations for each gene targeted. However, when the same RNAs were topically delivered to both R. prolixus 2nd and 3rd instar nymphs, no gene silencing and mortality were observed. For this reason, to assess dsRNA application-mediated non-target effects, we injected both H. halys and R. prolixus specific dsRNA in R. prolixus 5th instar nymphs. When the dsRNA targeting H. halys IAP was microinjected into R. prolixus 5th instar nymphs, no mortality was observed, suggesting a strong RNAi specificity. Together, these data suggest that the topical delivery could be suitable for the dsRNA to control H. halys population. Furthermore, its specificity of action would allow treatments towards single harmful species with limited non-target effects.
The data on the first findings of the southern green stink bug Nezara viridula (Linnaeus, 1758) in Armenia are presented. The species was found in three localities in the north-eastern part of the country, characterized by subtropical climatic conditions. The species is thought to have spread naturally from neighboring regions of Georgia or Azerbaijan.
The invasive stink bug Halyomorpha halys, native to east Asia, is a severe agricultural pest of worldwide importance and biocontrol is a promising method for its long-term management. The two Asian egg parasitoids Trissolcus japonicus and Trissolcus mitsukurii are considered to be effective candidates as biological control agents. These species can co-occur in the same habitats and interspecific competition for hosts could therefore have an important role in natural control. We assessed the foraging behavior and the progeny production of both species under laboratory conditions with three different interspecific competition scenarios. With indirect competition, H. halys egg masses previously parasitized by the female of one species were offered to the competitor females after 0, 3, 5, or 7 days. With direct extrinsic competition, females of each species were tested in arenas either when introduced simultaneously (synchronous release) or when half of the host egg mass had already been parasitized by the other species (asynchronous release). Both Trissolcus species were able to parasitize host eggs already para-sitized by the other species, although the progeny production always favored the species that arrived first on the host egg mass. However, in the synchronous releases scenario, T. mitsukurii displayed more aggressive behavior and spent more time defending the host egg mass than T. japonicus, resulting in a higher progeny production. Our results showed that multiparasitism among T. japonicus and T. mitsukurii, at least under laboratory conditions, resulted in a general waste of searching time, energy, eggs laid, and a lower reproductive potential by the second-arriving species on the host egg mass.