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Volatile release, mobility, and mortality of diapausing Halyomorpha halys during simulated shipping movements and temperature changes

DOI:10.1007/s10340-019-01084-x
Authors:
Laura Nixon at United States Department of Agriculture
Laura Nixon
Amy Tabb at United States Department of Agriculture
Amy Tabb
William Morrison at United States Department of Agriculture
William Morrison
Kevin Rice at University of Missouri
Kevin Rice
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Abstract and Figures

The brown marmorated stink bug, Halyomorpha halys, is an agricultural and urban pest that has become widely established as an invasive species of major concern in the USA and throughout Europe. The insect forms large aggregations before entering diapause, and it is often these aggregations that are found by biosecurity officials conducting inspections of internationally shipped freight. Here, we aimed to gain insights into the potential volatile emissions, mobility, and mortality rates of the insects after undergoing a ship voyage across the equator (i.e. from northern hemisphere winter to southern hemisphere summer). Experiments were performed to simulate the effects on aggregations of diapausing H. halys of two variables associated with trans-Pacific voyages, i.e. ship and container movement and temperature changes within containers. Thus, H. halys aggregations were exposed to simulated shipping movement, using a 6-axis VS-6577G-B Denso robot arm, and emission of defence volatiles was measured repeatedly during the “voyage.” We also simulated temperature changes as they occur during a 26-day voyage from Baltimore, northeast USA, to Auckland, New Zealand, and assessed the effects on the mortality and mobility of the bugs. Aggregations that experienced movement were not found to be any more likely to release volatiles than stationary aggregations and neither did the movement affect bug mobility. Temperature changes had a significant effect on mobility. However, towards the end of the temperature simulation, most H. halys had died, probably from a lack of food and moisture. These findings are highly relevant for border biosecurity risk assessment and pathway risk management.
Experimental setup showing a 6-axis VS-6577G-B Denso Robot with 934 mm reach, with attached metal shelters containing diapausing H. halys colonies. a Metal cross-structure, b metal shelter (6 × 7.5 × 7 cm, H × L × W) C) Inserts constructed from seven 2-mm-thick metal sheets (7.5 × 6.5 cm, L × W) spaced 90 mm apart, affixed in place with three screws running the length of the box and a series of nuts
Experimental setup showing a 6-axis VS-6577G-B Denso Robot with 934 mm reach, with attached metal shelters containing diapausing H. halys colonies. a Metal cross-structure, b metal shelter (6 × 7.5 × 7 cm, H × L × W) C) Inserts constructed from seven 2-mm-thick metal sheets (7.5 × 6.5 cm, L × W) spaced 90 mm apart, affixed in place with three screws running the length of the box and a series of nuts
… 
Average temperatures extracted from Wallenius Wilhelmsen Logistics data, showing the temperature simulation mimicking the temperatures H. halys would experience during a cargo vessel voyage from Baltimore, USA, to Auckland, New Zealand, between the months of January and February
Average temperatures extracted from Wallenius Wilhelmsen Logistics data, showing the temperature simulation mimicking the temperatures H. halys would experience during a cargo vessel voyage from Baltimore, USA, to Auckland, New Zealand, between the months of January and February
… 
The number of occurrences of two target compounds. a(E)-2-decenal and b dodecane in diapausing H. halys populations undergoing movement simulation (n = 12) and remaining stationary (n = 12) represented by bars. T1 and T4 indicate sampling time points immediately after simulated loading and unloading, respectively. All other time points are associated with simulated ship movement. No significant differences in occurrence between moved and stationary bugs (Fisher’s exact test, p > 0.05) at any time point (T1–T5). Average amounts of compound per shelter per sampling period were calculated, only including the amounts when positively detected, shown on respective graphs by points
The number of occurrences of two target compounds. a(E)-2-decenal and b dodecane in diapausing H. halys populations undergoing movement simulation (n = 12) and remaining stationary (n = 12) represented by bars. T1 and T4 indicate sampling time points immediately after simulated loading and unloading, respectively. All other time points are associated with simulated ship movement. No significant differences in occurrence between moved and stationary bugs (Fisher’s exact test, p > 0.05) at any time point (T1–T5). Average amounts of compound per shelter per sampling period were calculated, only including the amounts when positively detected, shown on respective graphs by points
… 
Number of mobile H. halys during a 26-day simulation of temperatures experienced on a trans-Pacific cargo ship. Points represent mean counts (± SEM) of eight diapausing populations
Number of mobile H. halys during a 26-day simulation of temperatures experienced on a trans-Pacific cargo ship. Points represent mean counts (± SEM) of eight diapausing populations
… 
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Vol.:(0123456789)
1 3
Journal of Pest Science (2019) 92:633–641
https://doi.org/10.1007/s10340-019-01084-x
ORIGINAL PAPER
Volatile release, mobility, andmortality ofdiapausing Halyomorpha
halys duringsimulated shipping movements andtemperature
changes
LauraJ.Nixon1,2,7· AmyTabb2· WilliamR.Morrison2,3· KevinB.Rice2,4· EckehardG.Brockerho5,7,8·
TracyC.Leskey2· ChikakovanKoten6· StephenGoldson1,6· MichaelRostás1
Received: 6 August 2018 / Revised: 6 December 2018 / Accepted: 14 January 2019 / Published online: 2 February 2019
© Springer-Verlag GmbH Germany, part of Springer Nature 2019
Abstract
The brown marmorated stink bug, Halyomorpha halys, is an agricultural and urban pest that has become widely established as
an invasive species of major concern in the USA and throughout Europe. The insect forms large aggregations before entering
diapause, and it is often these aggregations that are found by biosecurity officials conducting inspections of internationally
shipped freight. Here, we aimed to gain insights into the potential volatile emissions, mobility, and mortality rates of the
insects after undergoing a ship voyage across the equator (i.e. from northern hemisphere winter to southern hemisphere sum-
mer). Experiments were performed to simulate the effects on aggregations of diapausing H. halys of two variables associated
with trans-Pacific voyages, i.e. ship and container movement and temperature changes within containers. Thus, H. halys
aggregations were exposed to simulated shipping movement, using a 6-axis VS-6577G-B Denso robot arm, and emission of
defence volatiles was measured repeatedly during the “voyage.” We also simulated temperature changes as they occur during
a 26-day voyage from Baltimore, northeast USA, to Auckland, New Zealand, and assessed the effects on the mortality and
mobility of the bugs. Aggregations that experienced movement were not found to be any more likely to release volatiles than
stationary aggregations and neither did the movement affect bug mobility. Temperature changes had a significant effect on
mobility. However, towards the end of the temperature simulation, most H. halys had died, probably from a lack of food and
moisture. These findings are highly relevant for border biosecurity risk assessment and pathway risk management.
Keywords Biological invasions· Biosecurity· Brown marmorated stink bug· Cargo· Diapause· Human-assisted
movement
Communicated by T. Haye.
* Laura J. Nixon
l_nixon@hotmail.co.uk
1 Bio-Protection Research Centre, Lincoln University,
Lincoln7674, Canterbury, NewZealand
2 USDA-ARS Appalachian Fruit Research Station, 2217
Wiltshire Rd, Kearneysville, WV25430, USA
3 USDA-ARS Center forGrain andAnimal Health, 1515
College Ave, Manhattan, KS66502, USA
4 Division ofPlant Science, University ofMissouri, Columbia,
MO, USA
5 Scion (New Zealand Forest Research Institute),
P.O. Box29237, Christchurch8440, NewZealand
6 AgResearch Ltd, Christchurch, NewZealand
7 Better Border Biosecurity Collaboration, Wellington,
NewZealand
8 Swiss Federal Research Institute WSL, Zürcherstrasse 111,
8903Birmensdorf, Switzerland
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Thus, understanding the physiology of individuals for which diapause has been induced by photoperiod alone is important for understanding the potential for accidental introduction of this species across climatic zones. In particular, during these dispersal events, we expect that dehydration and starvation tolerance likely determine survival more than low temperature exposure (Nixon et al., 2019), and we speculate that discontinuous gas exchange could reduce the efficacy of fumigants that cannot pass through the cuticle. ...
... Thus, H. halys could be susceptible to energy drain if temperatures are high (or there are warm spells) during winter. However, H. halys choose thermally-buffered environments, and they can move during winter (Nixon et al., 2019), which means that they could potentially behaviourally thermoregulate to reduce energy drain after they have selected their overwintering site. We would therefore predict that diapausing H. halys should prefer cooler and more thermally-stable habitats than those selected by their non-diapausing counterparts. ...
Cold tolerance, water balance, energetics, gas exchange, and diapause in overwintering brown marmorated stink bugs
Article
Halyomorpha halys (Hemiptera: Pentatomidae) is an emerging pest which established in Ontario, Canada, in 2012. Halyomporpha halys overwinters in anthropogenic structures as an adult. We investigated seasonal variation in the cold tolerance, water balance, and energetics of H. halys in southwestern Ontario. We also induced diapause in laboratory-reared animals with short daylength at permissive temperatures and compared cold tolerance, water balance, energetics, and metabolism and gas exchange between diapausing and non-diapausing individuals. Halyomorpha halys that overwintered outside in Ontario all died, but most of those that overwintered in sheltered habitats survived. We confirm that overwintering H. halys are chill-susceptible. Over winter, Ontario H. halys depressed their supercooling point to c. −15.4 °C, and 50% survived a 1 h exposure to −17.5 °C. They reduce water loss rates over winter, and do not appear to significantly consume lipid or carbohydrate reserves to a level that might cause starvation. Overall, it appears that H. halys is dependent on built structures and other buffered microhabitats to successfully overwinter in Ontario. Laboratory-reared diapausing H. halys have lower supercooling points than their non-diapausing counterparts, but LT50 is not enhanced by diapause induction. Diapausing H. halys survive desiccating conditions for 3–4 times longer than those not in diapause, through decreases in both respiratory and cuticular water loss. Diapausing H. halys do not appear to accumulate any more lipid or carbohydrate than those not in diapause, but do have lower metabolic rates, and are slightly more likely to exhibit discontinuous gas exchange.
View
... Such information is also essential to design and implement sustainable management strategies such as classical biological control programs [39,40]. In general, the origin of invasive species has been identified by tracking back routes of export goods from which the invasive species was found [6,21,34,41]. For example, Lymantria dispar asiatica (Vnukovskij), formerly called the Asian gypsy moth, was found to infest vessels departing from the Russia Far East, and upon arrival in North America eggs hatched into larvae ballooning to vegetation surrounding port areas [23]. ...
Survey of overwintering Halyomorpha halys (Hemiptera: Pentatomidae) in ports of export and natural landscapes surrounding the ports in Republic of Korea
Article
Full-text available
Halyomorpha halys (Hemiptera: Pentatomidae), an important agricultural and nuisance pest, is highly invasive with peculiar hiding behavior in human-made structures for overwintering. To evaluate the contamination risk of overwintering H . halys in non-agricultural export goods, we conducted a two-year field survey in Republic of Korea to locate overwintering H . halys in two major ports of export, Ulsan and Pyeongtaek ports, and monitored both active and overwintering H . halys population levels with varying distances from the ports ranging from 1 km to 48 km. First, we deployed wooden shelters in the two ports to catch dispersing H . halys for overwintering and conducted visual inspections for human-made structures in the ports to locate overwintering H . halys . In addition, we sampled dead trees to find overwintering H . halys in wooded areas. Second, we monitored active H . halys populations using pheromone traps with varying distances from the ports. From the survey of overwintering populations, no H . halys was collected from wooden shelters deployed in the two ports. However, we found four adults overwintering in human-made structures in Pyeongtaek port in the first year of survey. One dead adult was also found from a dead tree located in a wooded area adjacent to Pyeongtaek port in the second year. For active populations, results of pheromone trapping indicated that H . halys populations were present during autumn dispersal period not only in agricultural areas, but also in wooded areas adjacent to the two ports. This study reports for the first time that overwintering H . halys were found from the inside the port of export in its native areas with a low density. The results were discussed for evaluating contamination risk of overwintering H . halys in export goods shipping from the Republic of Korea.
View
... While the different life stages of BMSB can be associated with various trade goods, aggregations of adult BMSB pose a particular risk. These aggregations form at the onset of cooler temperatures in sheltered locations, including human dwellings and structures such as shipping containers and vehicles (Gariepy, Haye, Fraser, & Zhang, 2014;Nixon et al., 2019). If transported, these aggregations can result in large numbers of BMSB becoming fecund at one location in a new area. ...
An Integrated Biosecurity Risk Assessment Model (IBRAM) For Evaluating the Risk of Import Pathways for the Establishment of Invasive Species
Article
  • Dec 2021
An important aspect of analyzing the risk of unwanted organisms establishing in an area is understanding the pathways by which they arrive. Evaluating the risks of these pathways requires use of data from multiple sources, which frequently are uncertain. To address the needs of agencies responsible for biosecurity operations, we present an Integrated Biosecurity Risk Assessment Model (IBRAM) for evaluating the risk of establishment and dispersal of invasive species along trade pathways. The IBRAM framework consists of multiple linked models which describe pest entry into the country, escape along trade pathways, initial dispersal into the environment, habitat suitability, probabilities of establishment and spread, and the consequences of these invasions. Bayesian networks (BN) are used extensively to model these processes. The model includes dynamic BN components and geographic data, resulting in distributions of output parameters over spatial and temporal axes. IBRAM is supported by a web‐based tool that allows users to run the model on real‐world pest examples and investigate the impact of alternative risk management scenarios, to explore the effect of various interventions and resource allocations. Two case studies are provided as examples of how IBRAM may be used: Queensland fruit fly (Bactrocera tryoni) (Diptera: Tephritidae) and brown marmorated stink bug (Halyomorpha halys) (Hemiptera: Pentatomidae) are unwanted organisms with the potential to invade Aotearoa New Zealand, and IBRAM has been influential in evaluating the efficacy of pathway management to mitigate the risk of their establishment in the country.
View
... These included tridecane, (E)-2-decenal, 4-oxo-(E)-2-hexenal, and dodecane. Despite these efforts, the likelihood of using detection of these compounds as a biosurveillance method was determined to be unreliable as groups of diapausing adults were not found to release these compounds reliably based on typical movements experienced during simulated shipping voyages (Nixon et al., 2018(Nixon et al., , 2019. However, diapausing H. halys, often found in aggregations (Chambers et al., 2019;Cullum et al., 2020), did reliably release defensive compounds when held in groups and vigorously mechanically agitated (Nixon et al., 2018 ...
Behavioural responses of diapausing Halyomorpha halys (Hemiptera: Pentatomidae) to conspecific volatile organic compounds
Article
  • Nov 2021
The brown marmorated stink bug, Halyomorpha halys Stål (Hemiptera: Pentatomidae), is an invasive pest in America, Europe and Asia and causes serious economic loss to crops, and nuisance problems during overwintering. Uninvaded southern hemisphere countries, such as New Zealand and Australia, see an increase in H. halys border interceptions during the northern hemisphere populations’ overwintering period as large aggregations of H. halys can settle to diapause in items for export, e.g. vehicles, containers, etc. Here, we explored aspects of diapausing H. halys behaviour relative to release and perception of defensive odour compounds. First, to determine whether group size and agitation affect the release of defensive odours, diapausing H. halys were confined in glass tubes as individuals or in varying group sizes and mechanically agitated or remained stationary and the presence or absence of defensive odours was recorded. Using gas chromatography-mass spectrometry, we also established if exposure to individual defensive odour components (tridecane, (E)-2-decenal, 4-oxo-(E)-2-hexenal, and dodecane) induced individuals to release defensive compounds. Additionally, H. halys dispersal was measured in the laboratory following exposure to individual components of their defensive odour or their natural blend. We found that agitating individual bugs did not induce the release of defensive odours. The release of human-detectable odours was only found in groups of mechanically agitated H. halys, whereas non-agitated bugs did not emit odour. Exposure to 4-oxo-(E)-2-hexenal was the only odour component that resulted in individual H. halys releasing defensive compounds. Diapausing H. halys exposure to the natural blend of defensive compounds resulted in increased horizontal distance moved and velocity, while tridecane exposure increased distance moved, velocity and angular velocity, and (E)-2-decenal exposure increased distance moved. Our behavioural and chemical data suggest that defensive compounds released by diapausing H. halys act as an alarm pheromone, particularly when adults are in aggregations.
View
... The brown marmorated stink bug, Halyomorpha halys Stål (Hemiptera: Pentatomidae), is an economically important invasive pest of major concern worldwide [20] . Its aptitude to aggregate and hide in small spaces, e.g., shipping containers, facilitates its worldwide spread [21] . Indigenous of East Asia, this species was accidentally introduced in the US and detected rstly in 1996 [22] . ...
Olfactory Responses of Trissolcus Mitsukurii to Plants Attacked by Target and Non-target Stink Bugs Suggest Low Risk for Biological Control
Preprint
Full-text available
  • Sep 2021
In crop systems, successful management of invasive insect herbivores can be achieved through the introduction of exotic biocontrol agents, i.e. parasitoids or predators, having a coevolutionary history with the pest. To avert threats to local biodiversity, recent legislations require a risk assessment for the organism to be released. Evaluation of its ability to exploit, for host location, odours associated with target and non-target species is crucial for a better definition of its ecological host range. Using Y-tube olfactometer in quarantine laboratory, we investigated the ability of the Asiatic egg parasitoid Trissolcus mitsukurii (Hymenoptera: Scelionidae) to exploit odours associated with the global invader Halyomorpha halys (Hemiptera: Pentatomidae) and with non-target stink bugs native to Southern Europe. We demonstrated that T. mitsukurii is attracted by plants exposed to feeding and egg deposition of the coevolved H. haly s or the native Nezara viridula , while it is not attracted by physogastric females or eggs alone. Remarkably, T. mitsukurii is repelled by plants bearing eggs of the beneficial stink bug, Arma custos . Our results usefully contribute to a more thorough and nuanced assessment of the potential non-target risks in case of massive parasitoid release.
View
... The Brown Marmorated Stink Bug, Halyomorpha halys Stål (Hemiptera: Pentatomidae), is an economically important invasive pest of major concern worldwide (Leskey and Nielsen 2018). Its aptitude to aggregate and hide in small spaces, e.g., shipping containers, facilitates its worldwide spread (Nixon et al. 2019). Indigenous of East Asia, this species was accidentally introduced in the US and detected rstly in 1996 (Hoebeke and Carter 2003). ...
Olfactory responses of Trissolcus mitsukurii to plants attacked by target and non-target stink bugs suggest low risk for biological control
Preprint
Full-text available
  • Sep 2021
Field release of classical biocontrol agents requires prior risk assessment to ensure that non-target effects are averted. No-choice and choice bioassays can provide basic information on the physiological host range of the candidate agent. However, other experimental methods, like olfactometer bioassays of host-plant complexes, can depict more realistically the likelihood that the released biocontrol agent localizes non-targets in the field. Halyomorpha halys Stål (Hemiptera: Pentatomidae) is native to Asia and invasive in North America and Europe, where it represents a major threat for crops. The Asiatic egg parasitoid Trissolcus mitsukurii (Ashmead) is adventive in Italy and exhibits high parasitization ability on H. halys . In the light of evaluating T. mitsukurii for H. halys biocontrol, its physiological host range has been already partially explored. Here, we investigated the ability of the parasitoid to exploit odours associated with H. halys or with the following non-targets: Arma custos F., Dolycoris baccarum L. , Eurydema ventralis Kolenati, and Nezara viridula L. (all Hemiptera: Pentatomidae). Specifically, using a Y-tube olfactometer, we tested the response of parasitoid females to plants bearing naturally laid eggs, to physogastric females or eggs of the different species. We observed that T. mitsukurii is only attracted by plants challenged by eggs of H. haly s or N. viridula , while it is not attracted by physogastric females or eggs alone. Remarkably, T. mitsukurii was almost repelled by plants bearing eggs of the beneficial A. custos . Our results usefully contribute to a more valuable assessment of the potential non-target risks in case of parasitoid release.
View
... It is possible that these differing findings could be as a result of our standardization method skewing the NC results, as a lower rate of overall reproduction was found in the NC population. This lower reproductive rate could be a result of lower fitness of that population due to factors found within their environment (Taylor et al. 2017) or it is possible that fitness was reduced by storage conditions over winter, with the naturally fluctuating temperatures to which this cohort was exposed resulting in greater depletion of nutritional stores than that seen in the cohorts held at constant temperature (Nixon et al. 2019). The finding that the NC population had a significantly lower rate of reproduction at 16 h, while the WV and MD populations had identical rates, despite all three groups having been sourced from different areas, provides evidence in favor of this latter possibility. ...
Diapause Termination in Invasive Populations of the Brown Marmorated Stink Bug (Hemiptera: Pentatomidae) in Response to Photoperiod
Article
Understanding cues for diapause termination in insects can be valuable in predicting phenological events in their lifecycles. Once identified, such cues can be utilized as a biofix, the point at which the majority of individuals within a population begin to accumulate degree days. We investigated the impact of photoperiod on completion of reproductive diapause in the invasive eastern North American population of the brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), by exposing diapausing females to varying light regimes in otherwise identical environments. The critical photoperiod estimated to initiate reproductive development in at least 50% of the potential reproductive population was 13.0–13.5 h, with increasing photoperiods coinciding with increased probability of females reproducing, earlier time to first oviposition, and higher rates of fecundity. These data on the species’ response to photoperiod are in agreement with previous modeling that predicted the twin constraints of photoperiod and temperature on H. halys reproduction prevents populations that undergo diapause from producing more than two generations annually anywhere within the continental U.S. However, the facultative nature of diapause in H. halys leaves open the possibility that sub-populations may not enter diapause in some conditions, potentially allowing for additional annual generations.
View
Seasonal abundance of Halyomorpha halys (Hemiptera: Pentatomidae) in habitats surrounding international ports and mobility and reproductive status of the insect during autumn dispersal period in South Korea
Article
  • Oct 2022
We monitored the seasonal abundance of Halyomorpha halys (Hemiptera: Pentatomidae) in forested areas near international ports and agricultural landscapes in South Korea from April to November in 2020 and 2021. Furthermore, flight capacity and reproductive status of field-collected H. halys adults during autumn dispersal period were evaluated. A total of 2,395 adults and 259 nymphs were collected, and population dynamics of adults showed similar patterns in forested areas near the ports and agricultural landscapes. Mean and maximum flight distances of adults collected from October to November, 2021, were 229 ± 71 m and 2,802 m, respectively, and all adults were nonreproductive except one male.
View
Olfactory responses of Trissolcus mitsukurii to plants attacked by target and non-target stink bugs suggest low risk for biological control
Article
Full-text available
  • Feb 2022
In crop systems, successful management of invasive insect herbivores can be achieved through the introduction of exotic biocontrol agents, parasitoids or predators, having a coevolutionary history with the pest. To avert threats to local biodiversity, recent legislations require a risk assessment for the organism to be released. Evaluation of its ability to exploit, for host location, odours associated with target and non-target species is crucial for a better definition of its ecological host range. Using Y-tube olfactometer bioassays in a quarantine laboratory, we investigated the ability of the Asian egg parasitoid Trissolcus mitsukurii (Hymenoptera: Scelionidae) to exploit odours associated with the global invader Halyomorpha halys (Hemiptera: Pentatomidae) and with non-target stink bugs native to Southern Europe. We demonstrated that T. mitsukurii is attracted by plants exposed to feeding and egg deposition of the coevolved H. halys and the native Nezara viridula, while it is not attracted by physogastric (gravid) females or eggs alone. Remarkably, T. mitsukurii is repelled by plants bearing eggs of the beneficial Arma custos. Our results contribute to a more thorough and nuanced assessment of the potential non-target risks in the case of mass-release of parasitoids as part of a biological control programme for invasive stink bugs.
View
Greenhouse Rearing Methods for Brown Marmorated Stink Bug (Hemiptera: Pentatomidae) on Live Cowpea Plants
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Brown marmorated stink bug (BMSB), Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), is a pest of concern that must be controlled for market access of host material and regulated articles to certain countries. This work outlines a rearing system for BMSB on live cowpea plants, Vigna unguiculata (L.) Walp. (Fabales: Fabaceae), including methods to induce adults to both enter and exit diapause. This scalable system affords continuous access to >600 specimens per week of each life stage and/or age group, which is particularly advantageous when developing treatment efficacy data.
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New records of the invasive alien plant pest Halyomorpha halys (Stål, 1855) in the Iberian Peninsula (Heteroptera: Pentatomidae)
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The brown marmorated stink bug Halyomorpha halys (Stål, 1855) is reported in the province of Barcelona for the first time. Now locations are a hundred kilometer southwards from the first report in the Iberian Peninsula. An alert is made due to the economic importance that this plant pest species has on field, fruit and vegetable crops. Nuisance to people when insects congregate inside buildings to overwinter is not negligible either. Resum Nous registres de la plaga exòtica invasora Halyomorpha halys (Stål, 1855) a la península Ibèrica (Heteroptera: Pentatomidae) Se cita per primera vegada l'espècie invasora Halyomorpha halys (Stål, 1855) a la província de Barcelona. Les noves localitats són a un centenar de kilòmetres més al sud de la primera troballa de l'espècie a la península Ibèrica. S'alerta de la importància econòmica que com-porta aquesta plaga en cultius extensius, de fruiters o d'horta. No cal menysprear les molèsties per a la població quan l'insecte es congrega en els edificis per a hibernar-hi.
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FIRST RECORD OF BROWN MARMORATED STINK BUG (HALYOMORPHA HALYS (STÅL, 1855)) (HEMIPTERA: PENTATOMIDAE) IN SLOVENIA
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Full-text available
  • Jun 2018
Abstract - The brown marmorated stink bug Halyomorpha halys (Stål, 1855) was recorded for the first time in Slovenia in spring 2017. A single specimen was caught on the pheromone trap in Šempeter pri Gorici in mid-April 2017. A week later another specimen was accidentally found on the parking area of a shopping centre in Nova Gorica. During the summer 2017 the brown marmorated stink bug was discovered in some other localities in the area around Nova Gorica. The discovery of this new alien species is the result of methodical monitoring, which has been carried out in Primorska region since 2016. The new pest presents a severe threat for many agricultural important crops in the area, as well as in other parts of the country.
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Impact of the Invasive Brown Marmorated Stink Bug in North America and Europe: History, Biology, Ecology, and Management
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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.
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Identification of volatiles released by diapausing brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae)
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The brown marmorated stink bug, Halyomorpha halys, is an agricultural and urban pest that has become widely established as an invasive species of major concern in the USA and across Europe. This species forms large aggregations when entering diapause, and it is often these aggregations that are found by officials conducting inspections of internationally shipped freight. Identifying the presence of diapausing aggregations of H. halys using their emissions of volatile organic compounds (VOCs) may be a potential means for detecting and intercepting them during international freight inspections. Headspace samples were collected from aggregations of diapausing H. halys using volatile collection traps (VCTs) and solid phase microextraction. The only compound detected in all samples was tridecane, with small amounts of (E)-2-decenal found in most samples. We also monitored the release of defensive odors, following mechanical agitation of diapausing and diapause-disrupted adult H. halys. Diapausing groups were significantly more likely to release defensive odors than diapause-disrupted groups. The predominant compounds consistently found from both groups were tridecane, (E)-2-decenal, and 4-oxo-(E)-2-hexenal, with a small abundance of dodecane. Our findings show that diapausing H. halys do release defensive compounds, and suggest that volatile sampling may be feasible to detect H. halys in freight.
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Further contribution to the Heteroptera (Hemiptera) fauna of Turkey with a new synonymy
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  • Oct 2017
A total of 11 new Heteroptera species are recorded from Turkey for the first time: Amphiareus constrictus (Stål, 1860), Anthocoris simulans (Reuter, 1884), Halyomorpha halys (Stål, 1855), Engistus exsanguis (Stål, 1872), Campylomma unicolor Poppius, 1914, Campylomma vendicarinum Carapezza, 1991, Capsodes gothicus (Linnaeus, 1758), Leucodellus zagdani (Putshkov, 1970), Phytocoris scitulus scitulus Reuter, 1908, Psallus cruentatus (Mulsant and Rey, 1852) and Solenoxyphus punctipennis (Reuter, 1879). Additionally, Phytocoris (Phytocoris) malckyi Rieger, 1995 is synonymized with Phytocoris (Exophytocoris) parvuloides Wagner, 1961; Phytocoris (Exophytocoris) parvuloides = Phytocoris (Phytocoris) malckyi Rieger, 1995 syn. nov.
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Global invasion network of the brown marmorated stink bug, Halyomorpha halys
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  • Dec 2017
Human mediated transportation into novel habitats is a prerequisite for the establishment of non-native species that become invasive, so knowledge of common sources may allow prevention. The brown marmorated stink bug (BMSB, Halyomorpha halys) is an East Asian species now established across North America and Europe, that in the Eastern United States of America (US) and Italy is causing significant economic losses to agriculture. After US populations were shown to originate from Northern China, others have tried to source BMSB populations now in Canada, Switzerland, Italy, France, Greece, and Hungary. Due to selection of different molecular markers, however, integrating all the datasets to obtain a broader picture of BMSB's expansion has been difficult. To address this limitation we focused on a single locus, the barcode region in the cytochrome oxidase I mitochondrial gene, and analyzed representative BMSB samples from across its current global range using an Approximate Bayesian Computation approach. We found that China is the likely source of most non-native populations, with at least four separate introductions in North America and three in Europe. Additionally, we found evidence of one bridgehead event: a likely Eastern US source for the central Italy populations that interestingly share enhanced pest status.
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Phenology of brown marmorated stink bug described using female reproductive development
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  • Jul 2017
Temperature-based degree-day models describe insect seasonality and to predict key phenological events. We expand on the use of a temperature-based process defining timing of reproduction through the incorporation of female reproductive physiology for the invasive pentatomid species Halyomorpha halys, the brown marmorated stink bug. A five-stage ranking system based on ovary development was able to distinguish between the reproductive statuses of field-collected females. Application of this ranking method described aspects of H. halys’ seasonality, overwintering biology, and phenology across geographic locations. Female H. halys were collected in the US from NJ, WV, NC, OR, and two sites in PA in 2006–2008 (Allentown, PA only) and 2012–2014. Results identify that H. halys enters reproductive diapause in temperate locations in the fall and that a delay occurs in developmental maturity after diapause termination in the spring. Modification of the Snyder method to identify biofix determined 12.7-hr photoperiod as the best fit to define initiation of reproduction in the spring. Applying the biofix, we demonstrated significant differences between locations for the rate at which the overwintering generation transition into reproductive status and the factors contributing to this difference require further study. For example, after including abiotic variables influencing development such as temperature and photoperiod (critical diapause cue), reproduction occurred earlier in OR and for an extended period in NJ. This data describe a method to investigate insect seasonality by incorporating physiological development across multiple regions that can clarify phenology for insects with overlapping generations.
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Biological parameters of the invasive brown marmorated stink bug, Halyomorpha halys, in southern Europe
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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.
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Laboratory rearing of Halyomorpha halys: methods to optimize survival and fitness of adults during and after diapause
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Laboratory colonies are necessary to conduct year-round research on the invasive brown marmorated stink bug, Halyomorpha halys (Stål), a severe agricultural and nuisance pest in the USA. When adults are collected in the fall to either start or supplement colonies, they require a period of cold storage before they resume sexual development and egg production. There is a lack of understanding of how to collect and store diapause-triggered adults in the laboratory. A series of experiments in 2013–2015 assessed survival and fecundity of stink bugs collected from different locations and stored under different temperatures and durations. We found that a minimum of 7 weeks is necessary to break diapause and that a substantial proportion of adults can survive when stored at constant 9 °C, even for periods longer than needed to terminate diapause. Adults survived significantly better at 6 and 9 °C than at 3 °C in storage for 7 weeks. Longer durations up to 34 weeks in storage reduced adult survival and significantly affected survival rates, timing of first egg laying, and overall fecundity. Location where adults were collected at overwintering sites in the fall had a significant impact on survival in cold storage and colony performance. Adults collected from soybean fields in mid-September and fed in the laboratory for 2 weeks before storage had lower survival than adults collected in October at aggregation sites and stored immediately. The food sources available to H. halys adults at collection locations for nutrition and sequestration of sufficient energy reserves going into diapause are discussed.
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First report of invasive brown marmorated stink bug Halyomorpha halys (Stal, 1855) in Croatia
Article
  • Feb 2018
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.
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