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The invasive brown marmorated stink bug (Halyomorpha halys) is now widespread in Hungary
Abstract
The brown marmorated stink bug, Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae), is native to East Asia and was first detected in Europe in 2004 in Switzerland. In Hungary, it was first recorded in the capital, Budapest, in 2013. Halyomorpha halys is an invasive polyphagous species, which is able to cause severe damage to a wide range of crops, and it is also considered an urban pest in America and Europe. By 2018, the status of H. halys as an agricultural pest causing major damage to cultivated plants in Hungary has been confirmed only by a single study carried out in 2016 at a farm located in Budapest. In the past few years, the pest has received significant media coverage in Hungary due to the increasing nuisance problems. However, detailed and reliable information on its spread were still missing. Therefore, in 2016, an extensive survey was initiated to obtain data on the distribution of H. halys in the country. This study was primarily based on the use of citizen science, which was completed with information requests from the members of professional organizations as well as active data collection by the authors. The results of this first extensive survey revealed the wide distribution of H. halys in Hungary, with mass occurrence of the species at several locations throughout the country, especially in the region of Budapest. These data highlight the rapid dispersal of H. halys and call for attention to the threat the pest poses to Hungarian plant production. © 2018 E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, Germany.
... The international flight connections from this airport are available to many cities of continental Europe, such as Athens, Basel, Belgrade, Bucharest, Budapest, Milan and Zurich (Hermes Airports 2020). These are locations where the presence of large populations of H. halys has already been observed (Ciceoi et al. 2017;Gariepy et al. 2015;Haye et al. 2014;Maistrello et al. 2018;Vétek et al. 2018;Vétek personal observation). Also the airport of Paphos, which can be found a few kilometres away from the city harbour popular with tourists, is available from several of these towns (Hermes Airports 2020). ...
... Involvement of citizen scientists has been considered to be extremely useful for early detection of invasive pests ). In the case of H. halys, both approaches (i.e., targeted trapping and the involvement of the public in data collection) have already proved to be suitable for obtaining data quickly, broadly and even relatively inexpensively on the occurrence of this particular pest (Haye et al. 2014;Maistrello et al. 2016;Vétek et al. 2018;Tassini and Mifsud 2019). ...
... The involvement of CS as an additional tool for observing H. halys completed our study. Although this method has already been proved to be suitable for detecting and following the range expansion of this pest quickly and broadly (Haye et al. 2014;Maistrello et al. 2016;Vétek et al. 2018), it is difficult to predict how effective CS initiatives will be. On one hand, the communication channels and methods of information dissemination should be defined adequately so that data requests can reach the target groups effectively. ...
... The international flight connections from this airport are available to many cities of continental Europe, such as Athens, Basel, Belgrade, Bucharest, Budapest, Milan and Zurich (Hermes Airports 2020). These are locations where the presence of large populations of H. halys has already been observed (Ciceoi et al. 2017;Gariepy et al. 2015;Haye et al. 2014;Maistrello et al. 2018;Vétek et al. 2018;Vétek personal observation). Also the airport of Paphos, which can be found a few kilometres away from the city harbour popular with tourists, is available from several of these towns (Hermes Airports 2020). ...
... Involvement of citizen scientists has been considered to be extremely useful for early detection of invasive pests ). In the case of H. halys, both approaches (i.e., targeted trapping and the involvement of the public in data collection) have already proved to be suitable for obtaining data quickly, broadly and even relatively inexpensively on the occurrence of this particular pest (Haye et al. 2014;Maistrello et al. 2016;Vétek et al. 2018;Tassini and Mifsud 2019). ...
... The involvement of CS as an additional tool for observing H. halys completed our study. Although this method has already been proved to be suitable for detecting and following the range expansion of this pest quickly and broadly (Haye et al. 2014;Maistrello et al. 2016;Vétek et al. 2018), it is difficult to predict how effective CS initiatives will be. On one hand, the communication channels and methods of information dissemination should be defined adequately so that data requests can reach the target groups effectively. ...
... Anastatus japonicus Ashmead (Hymenoptera: Eupelmidae), an important egg parasitoid for biological control, has a wide range of hosts, with over 15 host species in two families of Hemiptera (Alydidae and Pentatomidae) and 5 families of Lepidoptera (Lasiocampidae, Lymantriidae, Notodontidae, Papilionidae, and Saturniidae) [1]. Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) feeds on many fruit crops and causes serious economic losses worldwide [2][3][4]. Releases of A. japonicus against H. halys have been used in an organic kiwifruit orchard with satisfactory effects [5]. Similarly, in recent years, Caligula japonica (Moore) (Lepidoptera: Saturniidae) is a significant pest of walnut, chestnut, plum, apple, pear, and persimmon fruit trees, and its egg parasitoids also include A. japonicus [6]. ...
... They use various physical and environmental cues to search for hosts in a multistage process, including host under conditions of 25 ± 1 • C, 70 ± 5% RH, and a 14:10 h L:D photoperiod. As previously studied, A. pernyi eggs were used as hosts [2]. ...
Anastatus japonicus Ashmead is an egg parasitoid wasp important for the biological control of fruit crop pests. The olfaction of parasitoids is crucial to searching for host pests in fruit crops. In this study, we sequenced and analyzed the antennal and abdominal transcriptomes of A. japonicus to better understand the olfactory mechanisms in this species. A total of 201 putative olfactory receptor genes were identified, including 184 odorant receptors (ORs) and 17 ionotropic receptors (IRs). Then, we assayed the tissue-specific and sex-biased expression profiles of those genes based on the transcriptional levels. In total, 165 ORs and 15 IRs had upregulated expression in the antennae. The expression levels of 133 ORs, including odorant receptor co-receptor (AjapORco), and 10 IRs, including AjapIR8a, were significantly different between the female and male antennae. Our results provide valuable information for further studies on the molecular mechanisms of the olfactory system in A. japonicus.
... The brown marmorated stink bug (Halyomorpha halys Stål, 1855) (Hemiptera: Pentatomidae) is an important, highly polyphagous invasive economic pest insect species (Vétek et al. 2018). It is native to Asia, primarily China, Korea and Taiwan (Hoebeke and Carter 2003;Lee et al. 2013), but it has been introduced also to America (Hoebeke and Carter 2003;Faúndez and Rider 2017) and recently to Europe (Haye et al. 2014). ...
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.
... They are small moths with a size between 6 and 7 mm, a silvery grey color, and present darker spots on their forewings as well as filiform antennas (Desneux et al. 2010 (Desneux et al. 2011;Mansour et al. 2018). Like all invasive species, T. absoluta is characterized by its high adaptive capacity in newly invaded areas (Gontijo et al. 2013;Vetek et al. 2018). This could explain its presence in almost the entire Ivorian territory only three years after its first detection. ...
The South American tomato pinworm, Tuta absoluta (Meyrick), is one of the major threats to tomato production. Larvae can cause losses of more than 80% of production. It was officially detected for the first time in West Africa in 2012, in Senegal, and was subsequently reported in most countries in this part of the continent. To identify infested vegetable production areas and determine reservoir plants in Côte d'Ivoire, surveys were carried out and pheromone traps set in the North, South, East, West and Center in the main tomato production areas of the country. The pest was detected in all surveyed areas, with the highest number of males (623 ± 19.5 insects/week) caught by pheromone traps in Bouaké in the Center of Côte d'Ivoire and a highest percentage of infested leaves, 96 ± 2.5%, was obtained in the locality of Agnibilékro in the East of the country. Tuta absoluta attacked all phenological stages of tomato plant in field. Larval mines were observed on the eggplant, Solanum melongena, the black nightshade, Solanum nigrum and the peppers, Capsicum annuum. Apart from tomato, T. absoluta seems to prefer S. melongena (41.64 ± 2.95% of infested leaves/plant; 4.88 ± 0.4 mine/plant) and S. nigrum (36.27 ± 3.42% of infested leaves/plant; 4.26 ± 0.6 mine/plant) more than C. annuum (13.48 ± 2.42% of infested leaves/plant and 1.38 ± 0.18 mine/plant). This study led to understanding that T. absoluta is well established in the main tomato production areas of Côte d’Ivoire, causing damage regardless of plant development stages and is present on other plant species.
... All three specimens reported here were captured and killed in ethanol in order to forestall the establishment any viable populations. The photos of the Hungarian specimen of M. vermiculata were discovered on a citizen science website, Fajbook.hu, which further emphasises the usefulness of such platforms for early detection and control of invasive species (Falk et al. 2016, Maistrello et al. 2016, Grason et al. 2018, véTek et al. 2018, Páll-GerGely et al. 2019, turóci et al. 2020). ...
The Mediterranean Massylaea vermiculata (O. F. Müller) is reported from Slovakia for the first time (two sites), and from Hungary for the first time since the 1980 record. There is a reason to suspect the existence of further, yet undetected, specimens or even populations in Central Europe. Based on the dynamics of similar invasions of terrestrial molluscs, we expect that in 2–3 decades the species may become locally abundant and widespread in both the Hungarian and the Slovak capitals.
... The number of exotic insect pests established in Europe is constantly increasing, mainly due to global trade and global warming [1][2][3][4][5][6][7]. These organisms often cause economic damage as well as an increase on pesticide applications with the consequent side effects toward non-target organisms, the environment and human health [8][9][10][11][12]. ...
Exotic ambrosia beetles are increasing in Europe due to global trade and global warming. Among these xylomycetophagous insects, Xylosandrus compactus (Eichhoff) (Coleoptera: Curculionidae) is a serious threat for several Mediterranean host plants. Carob trees growing in Sicily (Italy) have been extensively attacked by beetles leading to rapid tree decline. Although X. compactus has been found in Europe for several years, most aspects of its ecology are still unknown. We thus studied the population structure and dynamics of X. compac-tus, together with its twig size preference during a sampling of infested carob trees in south east Sicily. In addition, fungi associated with insects or galleries were isolated and characterized. The results showed that, in this newly-colonized environment and host plant, adult X. compactus overwinters inside twigs and starts to fly and reproduce in mid spring, completing five generations before overwintering in late fall. The mean diameter of carob twigs infested by the beetle varied significantly over the seasons, with the insect tending to infest larger twigs as season progresses. The mean number of adults/gallery was 19.21, ranging from 6 to 28. The minimum temperature significantly affected the overwintering adult mortality. Ambrosiella xylebori and Fusarium solani were the main symbionts associated with the pest in this study. Acremonium sp. was instead recorded for the first time in Europe inside X. compactus galleries. Several other fungi species were also found for the first time in association with X. compactus. Our findings provide useful insights into the sustainable management of this noxious pest.
... It is an invasive phytophagous pest, already recorded to feed on more than 170 plant species worldwide [5]. In Europe, the first H. halys was recorded outside its native range in the 2000s in Switzerland [6], and it is now widespread throughout many European countries [5,7,8]. In Italy, H. halys rapidly became an agricultural pest, resulting in damage to crops and causing nuisance problems for the human population [9][10][11]. ...
The invasive brown marmorated stink bug, Halyomorpha halys, is causing economic and ecological damage in invaded areas. Its overwintering behavior warrants mitigation practices in warehouses and shipping operations. The aim of this study was to characterize the mortality response curves of H. halys adults to short high-temperature exposure. Here we compared field-collected individuals entering (ENA) and exiting diapause (EXA). EXA adults displayed increased susceptibility to high temperatures compared to ENA individuals. Complete mortality of all tested individuals was obtained after 10 min exposure at 50.0 °C, and after 15 (EXA) or 20 min (ENA) at 47.5 °C. The nutritional status of these insects had no effect on high-temperature tolerance. The mortality curves obtained here may be used for the definition of cost-effective heat treatments aimed at the H. halys control.
... This invasive insect pest was first detected in North America (Allentown, Pennsylvania) in 2001 (Hoebeke & Carter 2003), and then in Virginia in 2004 (Day et al. 2011). Since then, it has been recorded in Liechtenstein (Arnold 2009), Germany (Heckmann 2012), France (Callot & Brua 2013), Italy (Pansa et al. 2013), Canada (Gariepy et al. 2014), Hungary (Vétek et al. 2018), Greece (Milonas & Partsinevelos 2014), Romania (Macavei et al. 2015) and more recently in Chile (Faúndez & Rider 2017). Its rapid spread makes it become a key pest that damage economically relevant agricultural crops (Kriticos et al. 2017, Bosco et al. 2018. ...
The brown marmorated stink bug, Halyomorpha halys Stål (Hemiptera: Pentatomidae) originates from Asia and has recently disseminated to America and Europe, where it is considered as an invasive pest of various crops. Developing biological control strategies is necessary, and egg parasitoids are among the best candidates. In this context, the objective of this study was to evaluate the fitness of the egg parasitoid Ooencyrtus pityocampae Mercet (Hymenoptera: Encyrtidae) reared on H. halys eggs, under laboratory conditions. We specifically investigated the impact of host age, host density and length of exposure on O. pityocampae life history traits. Host age × host density and host age × length of exposure affected the performance of O. pityocampae . The optimal emergence rate of the parasitoid was obtained from one-day-old H. halys eggs and 3 days of exposure. The parasitoid embryonic development ranged from 17.1 to 18.3 days. The mean longevity of O. pityocampae was 44.1 days. This species reproduces by thelytokous parthenogenesis and the female parasitoid produced an average of 42.6 progeny during their lifespan. Pre-oviposition, oviposition and post-oviposition periods were 1.9 days, 18.8 days and 24.8 days, respectively. These results suggest that H. halys is a suitable host for O. pityocampae , and may help for the development of a pest-management strategy against H. halys .
The invasive pentatomid true bug Halyomorpha halys is reported for the first time from the German state of Hamburg, along with records from several other locations in Northern Germany. Specimens collected by scientists were evaluated along with records from citizen science platforms. DNA barcode sequences of several H. halys specimens from Hamburg were evaluated along with 42 sequences of the species from across the world in a haplotype network analysis demonstrating that all specimens studied from Hamburg had the haplotype H3. The present state of distribution of H. halys in Germany, patterns of range extension, invasiveness, and possible economic impacts are discussed.
Halyomorpha halys (Stål, 1855) – a species native to south-eastern Asia was introduced to Europe and recently to Poland, where it was reported so far only from three sites located in the southern and central part of the country. This paper presents new records of Halyomorpha halys from south-eastern Poland. These are the first records of this invasive species in the Eastern Beskids and the Lower San Valley.
The North American oak lace bug feeds on leaves of ‘white oaks” in its native range. In Europe, it was first discovered in northern Italy in 2000. In recent years, it has subsequently spread rapidly and population outbreaks have been observed in several European countries. In the present study, we summarize the steps of its expansion.
To predict its potential host range, we checked 48 oak species in 20 sentinel gardens in seven countries between 2013 and 2018.
In total, 27 oak species were recorded as suitable hosts; 13 of them are globally new ones, 23 out of the 29 in section Quercus (∼ white oaks, an intrageneric taxonomic unit within genus Quercus ), including Asian oaks, native to Japan, Korea and China, and four out of five in section Cerris (another intrageneric unit of the same genus), were accepted as hosts. None of the species in section Lobatae (red oaks) or in the Ilex group was accepted.
Host records were also collected in forest stands of 10 countries. We found 11 oak species that were infested. Outbreak populations were most commonly found on Quercus robur , Quercus frainetto , Quercus petraea and Quercus cerris , comprising widespread and outstandingly important oaks species in Europe.
Based on our findings, we conclude that suitable hosts for oak lace bug are present in most of Europe and Asia. This means that a lack of hosts will likely not restrict further range expansion.
střední kontrolní a zkušební ústav zemědělský, Šlechtitelů 23, CZ-779 00 Olomouc, Abstract. The Brown Marmorated Stink Bug, Halyomorpha halys Stål, 1855 (Hemiptera: Heteroptera: Pentatomi-dae: Pentatominae: Cappaeini), is recorded from the Czech Republic for the first time based on a female collected with a light trap in Luková u Přerova (central Moravia) and a male collected indoor in Prague (central Bohemia). The current distribution, economic importance and biology of the species are briefly reviewed. The species is an important pest of a large number of crops and can cause considerable economic damage.
The brown marmorated stink bug (BMSB), Halyomorpha halys (Stål), is an invasive pentatomid introduced from Asia into the United States, Canada, multiple European countries, and Chile. In 2010, BMSB populations in the mid-Atlantic United States reached outbreak levels and subsequent feeding severely damaged tree fruit as well as other crops. Significant nuisance issues from adults overwintering inside homes were common. BMSB is a highly polyphagous species with a strong dispersal capacity and high reproductive output, potentially enabling its spread and success in invaded regions. A greater understanding of BMSB biology and ecology and its natural enemies, the identification of the male-produced aggregation pheromone, and the recognition that BMSB disperses into crops from adjacent wooded habitats have led to the development of behavior-based integrated pest management (IPM) tactics. Much is still unknown about BMSB, and continued long-term collaborative studies are necessary to refine crop-specific IPM programs and enhance biological control across invaded landscapes. Expected final online publication date for the Annual Review of Entomology Volume 63 is January 7, 2018. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Raising public awareness about invasive alien species (IAS) is essential and one step in citizen assumed
responsibility is represented by their willingness to cooperate and help the scientists. Recent citizen science
initiatives all around the world are bringing promising results, but in Romania almost no citizen-generated
data (CGD) projects on IAS were initiated. Mobile agriculture applications (apps) started to develop in
Romania and to be used by farmers, but not the IAS apps. The present article analyses the Romanian CGD
activities on IAS on EASIN, GBIF and iNaturalist web platforms and the citizen feedback on Halyomorpha
halys alert leaflets and public presentations. In the same direction, we initiated a questionnaire for reporting
on IAS, addressed to students and teachers of the University of Agronomic Sciences and Veterinary
Medicine in Bucharest. Report rates varied from 0.79% to 0.38% for web platforms, to 0.14% for e-mail
and phones, while the IAS survey received 21.2% answers from teachers and colleagues and 10.5% from
students. Face-to-face communication seemed to improve the participatory rate, but only when personal
commitment and passion of the researcher is shown.
Halyomorpha halys is a global invasive species, native to Southeast Asia, that is threatening agriculture
in invaded regions. Our objectives were to: 1) establish the attractiveness of semiochemical stimuli
paired with field-deployed traps in Europe (Greece, Hungary, Italy, and Switzerland), compared with
Maryland, USA, and 2) identify H. halys haplotypes recovered from traps at each location. We found
qualitatively identical patterns of capture between sites located across Europe and in Maryland,
USA. In both regions, captures of H. halys adults indicated a synergistic response to traps baited with
the two component H. halys aggregation pheromone, and pheromone synergist, methyl (2E, 4E, 6Z)-decatrienoate when compared with either individually. Haplotype diversity in Europe based on trapped specimens was much greater than the USA, with five new haplotypes described here, probably indicating ongoing invasion and re-introduction of H. halys. By contrast, a single, previously identified haplotype was trapped in Maryland, USA, representing a single introduction. All H. halys haplotypes responded to each semiochemical in apparent proportion to their frequency in the overall population based on independently derived information from prior work. Taken together, these data suggest that pheromone-based technology will be of global utility for the monitoring of this important invasive
species.
Halyomorpha halys is an invasive stink bug pest originating from East Asia. In Europe, it was first detected in Switzerland in 2004. It is now present in thirteen countries, and seems to be spreading throughout the continent. In Italy, where it has been recorded since 2012, other than being an urban nuisance, it is causing severe damage in commercial fruit orchards. An integrated approach, using current and previous observational data in space and time and molecular information, was used to identify the genetic diversity of this pest in Europe, its invasion history, and the potential pathways of entry and diffusion. The analysis of 1175 bp of mitochondrial DNA cytochrome c oxidase I and II genes (cox1, cox2) led to the identification of twenty previously unknown haplotypes. The European distribution of H. halys is the result of multiple invasions that are still in progress, and, in some cases, it was possible to identify the specific Asian areas of origin. Moreover, secondary invasions could have occurred among European countries by a bridgehead effect. In Italy, the data were more clearly related to their temporal occurrence, allowing for a clearer reading of the patterns of invasion and dispersion. After having successfully established in localized areas, H. halys further expanded its range by an active dispersion process and/or by jump dispersal events due to passive transport. The multiple introductions from different areas of the native range together with the different patterns of diffusion of H. halys, may hamper the pest management strategies for its containment.
The brown marmorated stink bug, Halyomorpha halys, is an invasive pest species, first detected in Italy in 2012. Only 2 years after this first detection, increasing damage was reported in fruit orchards in the Emilia Romagna region, the first invaded area, which is one of the most important regions for the Italian and European fruit production. In the present study, life table parameters of H. halys populations were investigated in Italy under typical temperate/Mediterranean climate conditions representative of southern Europe. Our findings indicate that in Italy H. halys has two generations/year and very high reproductive rates for both generations (R
0 = 24.04 and 5.44 for the overwintering and summer generation, respectively). The huge growth rates explain why in 2015 a massive outbreak of H. halys was observed in Italy, and these rates confirm that the pest is a threat for agricultural production in southern Europe. The parameters obtained in this study are essential for the development and optimization of sustainable management strategies.
Abstract Since the establishment of the brown marmorated stink bug, Halyomorpha halys (Sta°l) (Hemiptera:
Pentatomidae) in North America and Europe, there has been a large, multi-group effort to characterize the composition and impact of the indigenous community of arthropod natural enemies attacking this invasive pest. In this review, we combine 98 indigenous natural enemy datasets spanning a variety of sampling methods, habitats, and geographic areas. To date, the vast majority of H. halys biological control research has focused on the egg stage, using sentinel egg masses to characterize indigenous parasitoid and predator communities and their contribution to H. halys egg mortality. Although egg parasitism and predation levels by indigenous natural enemies are low (typically\10% each) in most surveys, total egg mortality attributable to natural enemies can be higher (typically between 5 and 25%; up to 83%)—even though these values were likely underestimated in most cases because some mortality due to biological control was not recognized. In North America, where the most data are available, it appears that the relative prevalence of different indigenous parasitoid species varies among habitat types, particularly between crop and non-crop habitats. Predator species responsible for
egg mortality are much less commonly identified, but appear to include a wide variety of generalist chewing and sucking predators. To date, studies of natural enemies attacking H. halys nymphs and adults are relatively rare. Based on our review, we identify a number of key research gaps and suggest several directions for future research.
The brown marmorated stink bug, Halyomorpha halys (Stål), is a serious invasive pest in the USA. Organic growers have limited options to effectively manage this pest. Several organically approved insecticides including pyrethrins, azadirachtin, spinosad, potassium salts of fatty acids, sabadilla, extract from Burkholderia sp., and two combination products were evaluated for toxicity to H. halys nymphs and adults using laboratory bioassays and evaluated in field experiments on tomatoes and peppers using weekly applications of the highest labeled rates of the products. In submersion bioassays, high mortality (>70%) of H. halys nymphs was achieved with pyrethrins, azadirachtin, azadirachtin + pyrethrins, potassium salts + spinosad, and sabadilla alkaloids. Using the same bioassay for adult H. halys, only pyrethrins, azadirachtin + pyrethrins, and potassium salts resulted in high mortality. In bean dip bioassays, only pyrethrins resulted in moderate mortality of nymphs and high mortality of adults. In field experiments, which included weekly insecticide applications, none of the insecticides that were tested significantly reduced stink bug feeding injury (from all species) to tomatoes or peppers with the exception of one harvest date of peppers in 2014, where pyrethrins + azadirachtin had less injury than the control. Our results confirm that several organically approved insecticides may demonstrate a high level of activity on H. halys in laboratory bioassays, but when applied in the field, none of the products that we tested appear to be consistently effective at reducing stink bug injury to peppers or tomatoes.
There have been notable and significant advances in elucidating the chemical ecology of the invasive Halyomorpha halys (Hemiptera: Pentatomidae), brown marmorated stink bug. This highly destructive and polyphagous pest is originally from Korea, China, and Japan, but was accidentally introduced into North America and Europe. Prior to its invasion into these regions, little was known about its chemical ecology. However, since then, researchers have identified and synthesized its aggregation pheromone, documented its synergism with the pheromone of another Asian stink bug, Plautia stali, developed monitoring traps of various designs, and lures with reliable attractants have become commercially available. Furthermore, plant volatiles have been shown to have attractive, neutral, and repellent effects on attraction and retention of H. halys, and H. halys-derived volatiles have been shown to play a role in recruiting natural enemies. Finally, management strategies based on pheromone-based technology have been evaluated, including insecticide applications based on a cumulative threshold of adult captures in pheromone-baited traps, and the use of intensively baited trees in an attract-and-kill strategy to manage this pest. This review summarizes the available literature on the chemical ecology of H. halys and concludes with several research areas that should be explored in future research.
The brown marmorated stink bug, Halyomorpha halys (Stål), is a highly polyphagous invasive pest. Increased use of broad-spectrum insecticides to manage H. halys has resulted in secondary pest outbreaks and disruptions to integrated pest management (IPM) programs. We evaluated H. halys mortality, molting, and feeding after exposure to insecticides in the laboratory. Five insecticides (four active ingredients), considered less risky to natural enemies, were compared to a pyrethroid insecticide and an untreated control. Compared to the control, only azadirachtin + pyrethrins significantly reduced egg hatch, while all insecticides caused significant direct mortality to 1st and 2nd instars 5 days after hatch (DAH). Bifenthrin quickly caused complete mortality of adults, and the only insecticide to statistically match this level of mortality was sulfoxaflor at 14 days after treatment (DAT). Azadirachtin + pyrethrins and sulfoxaflor significantly reduced the proportion of 1st instars that molted compared to the control. Adults that survived sulfoxaflor exposure produced significantly fewer feeding sites than the control. However, when taking into consideration both lethal and sublethal effects, all insecticides, except pyrethrins, resulted in significant reductions in feeding sites/individual compared to the control. This more complete estimate of efficacy (i.e., reduction in injury/insect), confirms the potential of several insecticides to reduce crop injury without the necessity of high direct mortality to H. halys.
The brown marmorated stinkbug, Halyomorpha halys is a highly polyphagous invasive insect, which has
more than 300 reported hosts, including important horticultural crops. It has spread to every Northern Hemisphere continent, most recently to Europe. Whilst there have been no reports of incursions into Southern Hemisphere countries, there have been many interceptions associated with trade and postal goods. We modelled the potential distribution of H. halys using CLIMEX, a process-oriented bioclimatic niche model. The model was validated with independent widespread distribution data in the USA, and more limited data from Europe. The model agreed with all credible distribution data. The few exceptions in the distribution
dataset appeared to be transient observations of hitchhikers, or were found at the edge of the range, in
regions with topographic relief that was not captured in the climatic datasets used to fit and project the model. There appears to be potential for further spread in North America, particularly in central and southern states of the USA. In Europe, there is substantial potential for further spread, though under historical climate the UK, Ireland, Scandinavia and the Baltic states of Estonia, Lithuania and Latvia appear not to be at risk of establishment of H. halys. In the Southern Hemisphere, regions with moist tropical, subtropical,
Mediterranean and warm-temperate climates appear to be at substantial risk on each continent. The
threats are greatest in prime horticultural production areas.
The brown marmorated stink bug, Halyomorpha halys (Stål), native to China, Japan, and Korea, has emerged as a harmful invasive pest of a variety of crops in North America and Europe. The Asian egg parasitoid Trissolcus japonicus has been identified as the most promising agent for classical biological control of invasive H. halys populations. A 4-year study evaluated the fundamental and ecological host ranges of T. japonicus as well as its phenology and impact on H. halys populations in fruit orchards in its native range in northern China. In laboratory no-choice tests, developmental suitability of eight non-target host species for T. japonicus was demonstrated by the successful production of progeny on the majority (>85%) of non-target host species tested. In field-collected, naturally laid egg masses, T. japonicus was the most abundant parasitoid associated with H. halys and Dolycoris baccarum, but was also sporadically found in Plautia crossota. Furthermore, it was regularly reared from sentinel egg masses of Menida violacea, Arma chinensis, and Carbula eoa. The only species that did not support development in the laboratory and field was Cappaea tibialis. Besides the benefit of having a high impact on H. halys populations in Northern China, the risk assessment conducted in the area of origin indicates that native Pentatomidae in North America and Europe could be negatively impacted by T. japonicus. Whether the benefits of T. japonicus outweigh the possible risks will have to be evaluated based on the outcome of additional host range studies in the two invaded regions.
The brown marmorated stink bug, Halyomorpha halys Stål, 1855 (Hemiptera: Heteroptera: Pentatomidae), is recorded from Slovakia for the first time based on a 5<sup>th</sup> instar larva collected in the town of Štúrovo, Slovakia. The current distribution, economic importance and biology of the species are briefly reviewed. During the visit to Štúrovo, a mass occurrence of adults and larvae of the southern green stink bug, Nezara viridula (Linnaeus, 1758) (Pentatomidae), so far captured in Slovakia in 2014 only as a single specimen, was also observed. This observation confirms the presence of N. viridula as an established species in southern Slovakia. Both species are important pests to a large number of crops (vegetables, fruit trees, decorative plants, etc.) and can cause considerable economic losses.
Long-lasting insecticide nets (LLINs), which have insecticide incorporated within the fibers, have been widely used for control of malaria and other insect-vectored diseases. Only recently have researchers begun exploring their use for control of agricultural pests. In this study, we evaluated the toxicity of a deltamethrin-incorporated LLIN, ZeroFly (Vestergaard–Frandsen, Washington, DC) for control of the brown marmorated stink bug, Halyomorpha halys (Stål). In the lab, exposure to the ZeroFly net for 10 s resulted in >90% mortality of H. halys nymphs and >40% mortality of H. halys adults. Longer exposure to the net resulted in higher mortality. In another experiment, a 15-cm 2 sheet of ZeroFly net placed inside of the stink bug trap provided long-lasting kill of H. halys adults equal to or better than standard dichlorvos kill strip. Potential for the use of ZeroFly nets for H. halys IPM is discussed.
Early detection of invasive alien species and the ability to track their spread are critical for undertaking appropriate management decisions. Citizen science surveys are potentially valuable tools for quickly obtaining information on biodiversity and species distributions. The Asian brown marmorated stink bug, Halyomorpha halys, is an invasive pest of agricultural crops and a dwelling nuisance. Halyomorpha halys was first recorded in Italy in 2012 in Emilia Romagna, one of the most important fruit producing regions of Europe. To rapidly obtain data on its distribution in the newly invaded area, a survey that combined citizen science and active search was set up using multimedia channels. Data concerning when, where and how the bugs were spotted were collected, together with photographs and specimens. The survey detected established breeding populations in different areas of Northern Italy and Southern Switzerland, indicating a potentially high risk for crop damage that extends beyond the territories of first detection. Furthermore, new data on H. halys phenology, host plants, voltinism and behaviour were obtained. The importance of citizen science in early detection of introduced pest species is highlighted. This paper also provides a picture-based key to recognize H. halys from similar pentatomids in the world.
en Since the first occurrence of Halyomorpha halys (Heteroptera: Pentatomidae) in Italy in 2012, the pest has spread in the Po Valley causing severe damage in summer 2015, particularly in pear orchards. At present, populations of H. halys have been reported in the regions of Emilia‐Romagna (Modena, Reggio Emilia and Bologna provinces), Piedmont, Lombardy, Veneto and Friuli. The damage caused by H. halys is typical of pentatomids and is aggravated by the pest's polyphagy and by the behaviour of adults which move continuously from plant to plant, from hedges or herbaceous crops to fruit orchards. The unpredictability of H. halys’ movements, along with the effect of the aggregating pheromone that concentrates the pest in certain areas of the orchards, therefore making chemical spraying complicated.
Distribution et impacts causés par Halyomorpha halys en Italie
fr Depuis la première détection de Halyomorpha halys (Heteroptera: Pentatomidae) en Italie en 2012, le ravageur s'est dispersé dans la plaine du Pô causant de nombreux dégâts, particulièrement sur poire, pendant l’été 2015. A présent, la punaise diabolique a été signalée dans les régions d'Emilia‐Romagna (provinces de Modena, de Reggio Emilia, et de Bologna), du Piedmont, de la Lombardia, de la Veneto, et du Friuli. Les dégâts causés par H. halys sont typiquement ceux d'un pentatomidé, et sont aggravés par la polyphagie de ce ravageur et le comportement des adultes qui se déplacent continuellement de plantes en plantes, depuis les haies et plantes herbacées, jusqu'aux vergers. L'impossibilité de prédire les mouvements d’H. halys, au même titre que les effets de leurs phéromones d'agrégation, concentre ce ravageur dans certaines zones des vergers, ce qui compliquent l'application de traitements phytosanitaires.
Pacпpocтpaнeннocть Halyomorpha halys в Итaлии и вызывaeмый eю yщepб
ru Haчинaя c пepвoй peгиcтpaции Halyomorpha halys (Heteroptera: Pentatomidae) в Итaлии в 2012 г. этoт вpeдный opгaнизм pacпpocтpaнилcя в дoлинe peки Пo, пpичиняя cepьeзный yщepб, ocoбeннo нa гpyшe, лeтoм 2015 г. B нacтoящee вpeмя пoпyляции этoгo вoнючeгo мpaмopнoгo клoпa были oтмeчeны в Эмилии‐Poмaньe (в пpoвинцияx Moдeнa, Peджиo‐Эмилия и Бoлoньe), в oблacтяx Пьeмoнт, Лoмбapдия, Beнeция и Фpиyли. Ущepб, нaнocимый H. halys, типичeн для пeнтaтoмид, oднaкo oн ycyгyблялcя мнoгoяднocтью вpeдитeля и пoвeдeниeм взpocлыx ocoбeй, кoтopыe нeпpepывнo пepeмeщaютcя oт pacтeния к pacтeнию c живыx изгopoдeй или тpaвяныx кyльтyp к плoдoвым caдaм. Heпpeдcкaзyeмocть пepeмeщeний H. halys в coчeтaнии c эффeктoм aгpeгиpyющeгo фepoмoнa, кoтopый oни иcпycкaют, пpивoдят к cocpeдoтoчeнию этoгo вpeднoгo opгaнизмa в oпpeдeлeнныx зoнax плoдoвыx caдoв, чтo ocлoжняeт xимичecкoe oпpыcкивaниe.
Halyomorpha halys (Stål, 1855) or the Brown Marmorated Stink Bug (BMSB) is an invasive species native to East Asia which was initially noted outside its native range about twenty years ago in the United States (Hoebeke & Carter, 2003). This species is present in Europe for more than a decade (Haye et al., 2014b), but the first published record on H. halys is from 2004 in Liechtenstein (Arnold, 2009). Since then, the species was recorded in 8 other European countries: Switzerland, Germany, France, Italy, Hungary, Greece, Austria and Romania (Haye et al., 2015; Lee, 2015; Macavei et al., 2015; Rabistch & Friebe, 2015) and first specimens were intercepted in England during border inspections (Malumphy, 2014). Worldwide, H. halys is recognized as pest of dozens of agricultural and ornamental plants, and a serious household nuisance. Damages caused by the species are mostly documented in the mid-Atlantic region of the USA (Leskey et al., 2012), but for the last few years it became a problem in a few European regions as well (Haye et al., 2014b, 2015). Aforementioned reasons rapidly accelerated researches and publishing of papers on species biology, distribution and management, which are briefly reviewed by Haye et al. (2014a, 2015) and Lee (2015).
Résumé. – Cet article signale les premières observations de Halyomorpha halys (Stål, 1855) (Punaise diabolique,
marmorated stink bug, Marmorierte Baumwanze) en France. ------
Summary. – Halyomorpha halys (Stål, 1855), the marmorated stink bug, new species for the fauna of France
(Heteroptera Pentatomidae). In this article the first observations of Halyomorpha halys (Stål, 1855)
(Punaise diabolique, marmorated stink bug, Marmorierte Baumwanze) in France are reported.
Keywords. – Halyomorpha halys, Rhaphigaster nebulosa, Pentatomidae, Alsace, France
The Asian pentatomid Halyomorpha halys (Stål) (Heteroptera) is reported for the first time in North America based on collection of specimens or confirmed sightings in five counties in eastern Pennsylvania. Known in the Asian literature as the yellow-brown or brown marmorated stink bug, H. halys is considered a significant horticultural pest in Japan; it has a broad host range that includes plants of economic importance such as pea, soybean, apple, peach, cherry, and various other fruit and ornamental trees. In Japan's northern regions it is regarded as a nuisance pest late in the season when adults aggregate and seek overwintering sites in and around houses and commercial establishments. Descriptions and photographs of the adult and immature stages are provided to help distinguish it from other North American pentatomids. Habits, seasonal history, and host plants, based on the Asian literature and our own observations, are summarized. Photographs of leaf-feeding damage are also provided. Halyomorpha halys may have been accidentally introduced with international commerce, i.e., via bulk freight containers from either Japan, Korea, or China.
Originating in East Asia, the brown marmorated stink bug, Halyomorpha halys, has established in North America and Europe where it has become an urban and agricultural pest. Although initial populations in Europe were only reported in Switzerland, H. halys has expanded its range to include areas in France, Greece, Hungary, and Italy. Analysis of a portion of the mitochondrial COI gene was used to evaluate the genetic diversity of these populations and to investigate the movement and spread of different COI haplotypes of this pest in Europe. A total of 9 haplotypes are now confirmed in Europe. Four of these haplotypes have not been previously reported elsewhere, and one of these haplotypes has not been previously reported in Europe but is known from Korea. The H. halys population in Greece was the most diverse, with 7 of the 9 haplotypes occurring in the area of collection. Haplotype H1, which is known from North America, Italy, and China, was also present in samples collected in France, Greece, Hungary, and Switzerland. In fact, the H1 haplotype was the dominant haplotype detected in Budapest, Hungary and also occurred frequently in the samples from Athens, Greece. Patterns of haplotype diversity indicate the movement of successful invasive populations to generate secondary invasions within Europe (‘bridgehead effect’), as well as the occurrence of multiple invasions from Asia. Scenarios regarding the movement and spread of particular haplotypes in Europe are discussed.
http://link.springer.com/article/10.1007/s10340-015-0670-2
The brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae), has emerged as a harmful invasive insect pest in North America and Europe in the 1990s and 2000s, respectively. Native to eastern Asia, this highly polyphagous pest (>120 different host plants) is spreading rapidly worldwide, notably through human activities. The increasing global importance of the pest suggests that more coordinated actions are needed to slow its spread and mitigate negative effects in invaded areas. Prevention of large-scale outbreaks will require accurate identification and effective mitigation tools to be rapidly developed and widely implemented. In this short review, we update the current distribution of H. halys, discuss potential geographic range expansion based on passive and active dispersal and provide insight on the economic, environmental and social impact associated with H. halys.
Halyomorpha halys (Stål 1855) in Ile de France (Hemiptera: Pentatomidae: Pentatominae): monitoring the Marmorated Brown Stink Bug. The Marmorated Brown Stink Bug Halyomorpha halys (Stal 1855) (Insecta: Hemiptera: Pentatomidae) has now been found on the Ile de France (Paris City and Lardy, Essonne) area in France at the end of 2013, after its first discovery in France the same year (Strasbourg city), near the German border. This is the fifth occurrence of this Asian-origin invasive species in Europe. This polyphagous and serious agricultural pest species for many crops, and potentially allergenic, needs to be surveyed to monitor its expanding distribution.
A public survey to determine the current distribution of the invasive brown marmortaed stink bug, Halyomorpha halys in Switzerland showed that by the end of 2013, it was present in 11 Cantons, including six newly invaded Cantons (Basel-Landschaft, Aargau, Genève, Solothurn, Ticino, Thurgau, and Bern). In total, H. halys was found in 76 locations in 38 cities across Switzerland with large breading populations being present in the cities Zurich, Basel, Bern, and Lugano. There is now evidence that H. halys was already present in 2004, three years before its first official detection in 2007. Although H. halys has been present in Switzerland for nearly 10 years, its natural spread can be considered slow. Large distribution gaps between Swiss cities Zurich, Basel and Bern indicate that founder populations from Zurich arrived in these locations through human activity and movement of goods along the main motorways connecting the cities. The new list of host plants in Europe contains 51 host plants in 32 families, including many exotic and native plants. High densities of nymphs and adults were observed on Catalpa bignonioides, Sorbus aucuparia, Cornus sanguinea, Fraxinus excelsior, and Parthenocissus quinquefolia. With growing populations in Switzerland, France and Italy H. halys may further extend its distribution and become a nuisance pest in many European cities.
The brown marmorated stink bug, Halyomorpha halys (Stål, 1855) (Hemiptera: Heteroptera: Pentatomidae) is recorded for the first time from Hungary. The circumstances of finding this species and a detailed description of both male and female genitalia are given. The currently known distribution, biology and significance of the species are briefly reviewed.
The brown marmorated stink bug, Halyomorpha halys, a native of Asia, has become a serious invasive pest in the USA. H. halys was first detected in the USA in the mid 1990s, dispersing to over 41 other states. Since 1998, H. halys has spread throughout New Jersey, becoming an important pest of agriculture, and a major nuisance in urban developments. In this study, we used spatial analysis, geostatistics, and Bayesian linear regression to investigate the invasion dynamics and colonization processes of this pest in New Jersey. We present the results of monitoring H. halys from 51 to 71 black light traps that were placed on farms throughout New Jersey from 2004 to 2011 and examined relationships between total yearly densities of H. halys and square hectares of 48 landscape/land use variables derived from urban, wetland, forest, and agriculture metadata, as well as distances to nearest highways. From these analyses we propose the following hypotheses: (1) H. halys density is strongly associated with urban developments and railroads during its initial establishment and dispersal from 2004 to 2006; (2) H. halys overwintering in multiple habitats and feeding on a variety of plants may have reduced the Allee effect, thus facilitating movement into the southernmost regions of the state by railroads from 2005 to 2008; (3) density of H. halys contracted in 2009 possibly from invading wetlands or sampling artifact; (4) subsequent invasion of H. halys from the northwest to the south in 2010 may conform to a stratified-dispersal model marked by rapid long-distance movement, from railroads and wetland rights-of-way; and (5) high densities of H. halys may be associated with agriculture in southern New Jersey in 2011. These landscape features associated with the invasion of H. halys in New Jersey may predict its potential rate of invasion across the USA and worldwide.
The invasive Halyomorpha halys was accidentally introduced into Switzerland around 2004 and has
recently established in the neighbouring countries of France and Italy. To better understand the population
dynamics of this pest in Europe, the phenology, reproductive biology and temperature requirements of Swiss H. halys populations were investigated. Overwintered adults became active in April, but peak oviposition was not observed before early July. Individual females laid on average 79 eggs (maximum of 160). The oviposition period lasted from mid-June to end of September. Eggs laid in August and September did not result in offspring due to the low temperatures in autumn. Under natural fluctuating temperatures, development from egg to adult lasted between 60 and 131 days. The first new generation of adults did not occur before mid-August when the photoperiodwas already below 15 h, which likely initiated diapause and suppressed the reproductive activity of new generation adults. Under controlled conditions of 20, 25 and 30 �C, Swiss H. halys populations developed within 75.8, 42.3 and 33.2 days from egg to adult, respectively.
No development was possible at or below 15 and at or above 35 �C. The number of degree days required for
completion of development from egg to adult was 588.24 DD. Under semi-natural conditions, total mortality of Swiss H. halys populations was 86.7 % with a net reproductive rate of 5.69, indicating growing populations. In Switzerland, H. halys is univoltine, but if it continues to spread into the Mediterranean area two generations per year could be expected.
The brown marmorated stink bug, Halyomorpha halys (Stål) is an invasive insect in the Mid-Atlantic region that is spreading rapidly across the United States. In this article, the authors document the pest potential of this bug to vegetable crops based on their observations in the Mid-Atlantic United States thus far.
Accepted for publication 20 April 2012. Published 23 May 2012.
The brown marmorated stink bug, Halyomorpha halys (Stål, 1855) (Hemiptera: Heteroptera: Pentatomidae), has been spreading over Europe since the first documented records from Liechtenstein in 2004 and Switzerland in 2007. It is considered to be a pest in many agricultural crops and a household nuisance. In 2017 the species was observed in Croatia for the first time, in the city of Rijeka on the north Adriatic coast. Halyomorpha halys has already been recorded in three nearby countries (Italy, Hungary and Serbia), and therefore the arrival of this species had been expected from neighbouring populations or from distant sources via trading goods. To identify the pathway of entry, the haplotypes of H. halys (Stål, 1855) individuals were analysed by comparing a part of the mitochondrial COI gene with other haplotypes present in the GenBank database. Individual specimens shared the most common haplotype with nearby Italian and Hungarian populations.
Halyomorpha halys is a polyphagous insect species with an original eastern Asiatic distribution, which was recently and accidentally introduced in the USA and Europe, where it became a serious agricultural pest. Chemicals have been widely used for its control leading often to failure of IPM programmes. Several approaches aimed at pest monitoring and control are currently under investigation, for example trapping, screening, border management and biological control. In the present work, we investigated the lethal and sublethal effects of the use of a long-lasting insecticide-treated net (LLIN with α-cypermethrin), focusing on the perspective to control H. halys in an integrated approach. All experiments were carried out in the laboratory either in small arenas, at five exposure times (5, 15, 30, 45 and 60 min) or in large cages at 8 hr exposure. In small arenas, the LLIN induced sublethal effects and/or effectively killed the adults. A higher adult mortality was observed after longer exposure times (LT90 was 51.64 min for females and 40.83 min for males). However, several specimens recovered from sublethal effects, with higher recovery rates after shorter exposure times. In the cage experiments, a significantly higher mortality (65% males and 75% of females) was recorded compared with controls. LLINs are physical barriers that can improve crop protection due to their insecticidal activity, and can be reasonably applied in various attract-and-kill systems both in glasshouses and in the field.
In autumn 2011, stink bugs were found causing a nuisance in houses in the centre of Athens, Greece. Specimens were identified by D.A. Rider at North Dakota State University as Halyomorpha halys Stål (Hemiptera: Pentatomidae). The species is native to Asia; it was detected in the USA in 1996 and has recently been introduced into Europe (2008). This paper provides the first report of the presence of H. halys (brown marmorated stink bug) in Greece. Some data on its phenology and economic impact are also provided.
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Az ázsiai márványospoloska (Halyomorpha halys (Stål,1855)) első észlelése Nyugat-Magyarországon
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Establishing the behavioral basis for an attract-and-kill strategy to manage the invasive Halyomorpha halys in apple orchards
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Key for the separation of Halyomorpha halys (Stål) from similarappearing pentatomids (Insecta: Heteroptera: Pentatomidae) occurring in Central Europe, with new Swiss records
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