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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 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.
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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. ...
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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.
... 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. ...
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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.
... 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 ...
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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.
... 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] . ...
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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.
... 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). ...
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Full-text available
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.
... Originally from Asia, but now widespread in much of North America and Europe, as well as Chile [7], H. halys has the capacity for long-distance flight [8,9], enabling a high dispersal capability. Because of its association with human-modified habitats and its tendency to shelter in enclosed locations, it has become a superb international hitchhiker, making it an important invasive species [7,10]. Attributes that favour its ability to become invasive also include being a long-lived species with high reproductive output [11], extreme polyphagy (including many crops of economic significance) and an overwintering clustering behaviour potentially involving hundreds of tightly packed individuals of both sexes which is enabled by sheltering within human-made structures [7,12,13]. ...
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... In autumn, several species aggregate in buildings and other artificial shelters to hibernate. Overwintering H. halys adults have been transported while hidden inside many types of material Nixon et al., 2019). This has affected international trade due to the mandatory phytosanitary importation measures required by some countries (e.g., New Zealand and Australia). ...
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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.
Article
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.