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Journal of Pest Science

, Volume 90, Issue 4, pp 1033–1043 | Cite as

The potential global distribution of the brown marmorated stink bug, Halyomorpha halys, a critical threat to plant biosecurity

  • Darren J. Kriticos
  • John M. Kean
  • Craig B. Phillips
  • Senait  D. Senay
  • Hernando Acosta
  • Tim Haye
Original Paper

Abstract

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, sub-tropical, Mediterranean and warm-temperate climates appear to be at substantial risk on each continent. The threats are greatest in prime horticultural production areas.

Keywords

Bioclimatic model Climatic suitability CLIMEX Cold stress Ecoclimatic Index Heat stress Niche model Pest risk 

Key message

  • The brown marmorated stinkbug can damage more than 300 hosts.

  • It has invaded every continent in the Northern Hemisphere; most recently Europe.

  • It is essential for biosecurity agencies to better understand the extent of the threat to the remainder of Europe, and to countries in the Southern Hemisphere.

  • The potential threat in Europe and the Southern Hemisphere extends throughout most of the horticultural zones.

Introduction

Halyomorpha halys Stål (Hemiptera: Pentatomidae) (syn. H. mista), commonly known as the brown marmorated stink bug, is highly polyphagous, with more than 300 reported hosts (Bergmann et al. 2016; Hoffman 1931; Lee et al. 2013). Originally from north-eastern Asia, H. halys has invaded extensive areas across North America, and more recently Europe (Austria, Bulgaria, France, Germany, Greece, Hungary, Italy, Liechtenstein, Romania, Serbia, Spain and Switzerland) (Arnold 2009; Callot and Brua 2013; Cesari et al. 2015; Dioli et al. 2016; Heckmann 2012; Hoebeke and Carter 2003; Macavei et al. 2015; Milonas and Partsinevelos 2014; Šeat 2015; Simov 2016; Vétek et al. 2014; Wermelinger et al. 2008). Halyomorpha halys continues to spread further east in Europe and is now also present in Abkhazia, Georgia and Russia (Gapon 2016; Mityushev 2016).

In northern China, Japan, Europe and North America, one or two generations of H. halys commonly occur (Haye et al. 2014; Lee et al. 2013; Nielsen and Hamilton 2009), and four to six generations are assumed to occur in southern China (Hoffman 1931). Halyomorpha halys is considered to be a pest in both its native and introduced ranges (Hoffman 1931; Lee et al. 2013; Leskey et al. 2012a). It is perhaps most notorious for its overwintering activity, where non-reproductive adults aggregate in favourable protected microhabitats such as beneath bark and within buildings (Rice et al. 2014). This behaviour leads to a variety of pest impacts, interfering with building functions as well as causing a nuisance when disturbed as they emit a foul-smelling scent (Watanabe et al. 1978, 1994). However, its most important economic impacts are likely due to the problems that it causes to agricultural, horticultural and silvicultural hosts (Haye et al. 2015). Feeding damage to plants can cause wilting and reduced yield, and feeding on fruits can render the fruit unacceptable for markets due to deformity and discolouration (Nielsen et al. 2008b). Halyomorpha halys also transmits Paulownia tomentosa witches’ broom disease caused by a phytoplasma, which reduces growth and vigour of ornamental trees and may cause early tree death (Hiruki 1997). Halyomorpha halys may also transmit damaging phytoplasmas to other ornamental tree and shrub species (Jones and Lambdin 2009).

Halyomorpha halys is able to travel long distances as a hitchhiker associated with host material, and as a stowaway on ground transport vehicles (Gariepy et al. 2014, 2015; Hoebeke and Carter 2003). Consequently, H. halys has been frequently intercepted by border and post-border officials in many countries (Gariepy et al. 2014, 2015, and citations within), but it has also led to misleading distribution records, when single adults were found in high latitude northern areas and in xeric regions, where conditions during winter are excessively cold, and it is infeasible that they could survive or establish, e.g. Alberta (Canada) and Alaska (USA).

There have been several previous attempts to estimate the potential distribution of H. halys (Haye et al. 2015; Zhu et al. 2012, 2016). These projects employed correlative species distribution models, which have been shown to be unreliable when applied to novel environments such as those encountered when species invade new continents or regions (Kriticos and Randall 2001; Sutherst and Bourne 2009; Webber et al. 2011). To deal with this, software tools have been developed to identify where correlative models are being projected into novel environments (Elith et al. 2011; Mesgaran et al. 2014). Zhu et al. (2016) prepared and presented two models, one using MaxEnt and one using GARP. The MaxEnt model presented in the main paper displays poor specificity, projecting an excessive capacity of H. halys to cope with cold climates, such as those found in Canada and Russia. In contrast, the GARP model presented in the Supplementary Materials in Zhu et al. (2016) appears excessively conservative in relation to both the warm-wet and cold range limits. The model of Rossi and Streito (unpublished) presented in Haye et al. (2015) appears conservative in the native range and in North America in relation to the cold tolerance limits, and excessively liberal in relation to H. halys ability to tolerate cold and dry conditions in novel climates in the Southern Hemisphere.

CLIMEX (Kriticos et al. 2015a; Sutherst and Maywald 1985) is a niche modelling package specifically developed to explore the effects of climate on invasive species, and to estimate their potential distributions in novel climates. It is widely used by invasion biologists and risk assessors, with more than 630 publications (Kriticos 2016). A major advantage of CLIMEX is its ability to be calibrated inferentially, relying mostly upon geographical distribution data and phenological observations, as well as deductively, drawing upon experimental observations of species behaviour under laboratory conditions to inform parameter selection. CLIMEX allows the modeller to compare the modelling implications of information from each of these knowledge domains and to apply the method of multiple competing hypotheses to resolve conflicts (Chamberlin 1965).

In this study, we fit a CLIMEX model for H. halys using the known distribution throughout its native range in Asia and project it globally, validating the model using independent distribution data in the USA and Europe. In fitting the model, we draw upon published literature to inform the selection of model parameters. This model is intended as a platform to undertake pest risk analyses, with a particular focus on modelling economic impacts. These impacts are likely to be related to inter alia the length and favourability of the growing season, the number of generations, the value of production and favourability of the host crops.

Methods

The present known distribution of Halyomorpha halys

Halyomorpha halys is native to parts of China, Japan, Myanmar, Taiwan, Vietnam and the Korean peninsula (Yu and Zhang 2007, and citations within). The large number of distribution records in South Korea and the records in the North of Honshu Island in Japan, and some to the north and west in China suggest that the lack of records in North Korea (which lies between these sets of records) does not indicate the absence of H. halys from this region, but rather a lack of reporting from North Korea. Similarly, there may be an absence of reports from South-east Asian countries such as Laos and the Philippines.

Halyomorpha halys was first detected in North America in 1996 (Hoebeke and Carter 2003), and the oldest records from Europe date back to 2004 (Arnold 2009; Haye et al. 2014). Following the introduction to these continents, it has spread rapidly (Figs. 1, 2, 3) (reviewed by Haye et al. 2015). Reports of H. halys detections in central and western provinces of Canada (Alberta and Saskatchewan) have been associated with human-mediated transport from the USA and do not represent established populations. The H. halys distribution record from near Kenai in Alaska would appear to also represent a vagrant observation, most likely associated with aerial transport.
Fig. 1

Modelled climate suitability (CLIMEX Ecoclimatic Index) for Halyomorpha halys in Asia, including reported distribution locations. The three outlying records in Western China appear to be located in infeasibly cold locations above 3000 m A.S.L

Fig. 2

Modelled climate suitability (CLIMEX Ecoclimatic Index) for Halyomorpha halys in North America, including reported distribution locations. Note the three outlying distribution records in the USA and Canada have been investigated and found to be transient populations associated with human transportation

Fig. 3

Modelled climate suitability (CLIMEX Ecoclimatic Index) for Halyomorpha halys in Europe, including reported distribution locations

CLIMEX modelling

CLIMEX (Kriticos et al. 2015a; Sutherst and Maywald 1985) is a process-oriented climate-based niche modelling package. It enables users to project the climatic potential distribution of poikilothermal organisms based primarily on their current distribution. However, it is unique amongst climate-based niche modelling packages in that a combined inductive–deductive method can be used to fit models. CLIMEX has been widely used to model the potential distribution of many invasive arthropod pests (De Villiers et al. 2016; Kriticos et al. 2015b; Vink et al. 2011; Yonow et al. 2016), weeds (Julien et al. 1995; Kriticos and Brunel 2016; Kriticos et al. 2003) and plant diseases (Watt et al. 2011; Yonow et al. 2004, 2013).

CLIMEX uses a set of fitted growth and stress functions to assess the potential for a species to persist and grow at each location for which relevant climatic data are available. CLIMEX calculates an annual index of overall climate suitability, the Ecoclimatic Index (EI), which is theoretically scaled between 0 (unsuitable) and 100 (climatically perfect all year round). In practice, a score of 100 is rarely achieved, and then only in locations with high climatic stability such as some equatorial regions. The EI represents the net effect of the opportunity for growth as indicated by the annual Growth Index (GIA), discounted by the Stress Index (SI) and the interaction Stress Index (SX) (Eqs. 14).
$${\text{EI }} = {\text{ GI}}_{\text{A}} \times {\text{SI}} \times {\text{SX}}$$
(1)
$${\text{GI}}_{\text{A}} = 100\sum\limits_{i = 1}^{52} {{\text{TGI}}_{{{\text{W}}_{i} }} } /52$$
(2)
$${\text{SI }} = \, \left( {1 - {\text{CS}}/100} \right)\left( {1 - {\text{DS}}/100} \right)\left( {1 - {\text{HS}}/100} \right)\left( {1 - {\text{WS}}/100} \right)$$
(3)
$${\text{SX }} = \, \left( {1 - {\text{CDX}}/100} \right)\left( {1 - {\text{CWX}}/100} \right)\left( {1 - {\text{HDX}}/100} \right)\left( {1 - {\text{HWX}}/100} \right)$$
(4)
where CS, DS, HS and WS are the annual cold, dry, heat and wet stress indices, respectively, and CDX, CWX, HDX and HWX are the annual cold-dry, cold-wet, hot-dry and hot-wet Stress Interaction indices. In addition to the growth and stress indices, it is possible to add additional requirements for species persistence such as an obligate or facultative diapause, or a minimum annual heat sum required to complete a generation. The weekly growth index GIW is composed of a separate soil moisture index (MI) and a temperature Index (TI), which are formulated using three-segment linear equations, varying between 0 (no growth) and 1 (optimal growth) to comply with Shelford’s Law of Tolerance (reviewed in Shelford 1963). By combining MI and TI together multiplicatively, GIW and its annual integral GIA satisfy the Sprengel–Liebig Law of the Minimum (reviewed in van der Ploeg et al. 1999).

The CLIMEX Compare Locations model was fitted to the known distribution of H. halys in Asia, verified using the North American records and validated against the European presence records. The CliMond CM10 World (1975H V1.1) climate dataset was used for model fitting (Kriticos et al. 2012). This global climatological dataset has a spatial resolution of 10 arc minutes and consists of long-term monthly averages of daily minimum and maximum temperature, relative humidity at 09:00 and 15:00 h and monthly rainfall totals. The averages are centred on the year 1975. The sample period for the temperature and relative humidity variables is 1961–1990, and for the rainfall the sampling period was extended to 1951–2000 for some stations that were otherwise poorly sampled (Hijmans et al. 2005).

The Compare Locations/Years model was used to explore the meaning of a number of locations near the range boundary that were modelled as being unsuitable. For this analysis, the CRU time-series dataset was run using data from 2000 to 2013 (Mitchell et al. 2004).

Stresses

Halyomorpha halys is a chill intolerant species (Cira et al. 2016). In order to survive in temperate climates, it must employ several strategies: diapause, aggregation, shelter and acclimation. Halyomorpha halys individuals collected from, and acclimated in Minnesota during fall and spring have shown mean supercooling points as low as −16.85 ± 0.08 °C, and mortality, presumably due to cold stress, commencing at temperatures as high as 4 °C (Cira et al. 2016). A threshold temperature cold stress was fitted to the northern Chinese records. A temperature threshold of −18 °C (TTCS) and a stress accumulation rate of −0.01 week−1 (THCS) allowed the north and north-western-most records to barely persist. A degree-day cold stress mechanism was also explored, but all resulting models fitted the known distribution patterns poorly. The stresses in this model are set to be active during diapause, a new option in CLIMEX Version 4 (Kriticos et al. 2015a).

Hot-wet stress is likely to be limiting the expansion of H. halys into the wet tropics. A combination of a threshold temperature (TTHW) of 28 °C, a threshold soil moisture index (MTHW) of 1.5, and a stress accumulation (PHW) of 0.007 week−1 gave results that reduce the potential range of H. halys in southern Asia without impacting on its known range in northern Asia.

Growth indices

Kiritani (2007) reviewed H. halys development studies from Asia and cited values for the lower threshold for development in the range 11–13.8 °C. Nielsen et al. (2008a) observed incomplete development at 15 and 35 °C with most rapid development at 25–30 °C. Similarly, Haye et al. (2014) observed no development at ≤15 or >35 °C, with most rapid development at 30 °C. Therefore, the CLIMEX parameters for the Temperature Index were set as DV0 = 12 °C, DV1 = 27 °C, DV2 = 30 °C, DV3 = 33 °C, and PDD = 595 °C day (Table 1).
Table 1

CLIMEX parameter values fitted for Halyomorpha halys

Parameter

Mnemonic

 

Unit

Temperature requirements

Limiting low temperature

DV0

12

°C

Lower optimal temperature

DV1

27

°C

Upper optimal temperature

DV2

30

°C

Limiting high temperature

DV3

33

°C

Degree-days per generation

PDD

595

°C days

Soil moisture

Limiting low soil moisture

SM0

0.1

 

Lower optimal soil moisture

SM1

0.5

Upper optimal soil moisture

SM2

1

Limiting high soil moisture

SM3

1.5

Diapause

Diapause induction day length

DPD0

12

h light

Diapause induction temperature

DPT0

5

°C

Diapause termination temperature

DPT1

5

°C

Diapause development days

DPD

0

days

Diapause summer (1) or winter (0)

DPSW

0

 

Cold stress

Temperature threshold

TTCS

−18

 °C

Stress accumulation rate

THCS

−0.01

Week−1

Heat stress

Temperature threshold

TTHS

33

°C

Stress accumulation rate

THHS

0.01

Week−1

Dry stress

Threshold soil moisture

SMDS

0.1

 

Stress accumulation rate

HDS

−0.01

Week−1

Wet stress

Threshold soil moisture

SMWS

1.5

 

Stress accumulation rate

HWS

0.002

Week−1

Hot-wet stress

Threshold soil moisture

TTHW

28

 

Threshold temperature

MTHW

1.5

°C

Stress accumulation rate

PHW

0.007

Week−1

Values without units are dimensionless indices of plant available soil moisture

Because H. halys is dependent on fresh plant material for sustenance, a lower soil moisture level for growth (SM0) was set to 0.1, which equates to permanent wilting point for plants with moderate rooting depth. In southern Asia, H. halys can apparently withstand conditions leading to a small amount of water-logging. Accordingly, SM3 was set to 1.5, allowing growth in these areas.

PDD

Nielsen et al. (2008a) estimated that the degree-day requirements of H. halys were 537.6 °C days above 14 °C for egg–adult development, plus an additional 147.6 °C days for the pre-oviposition period of females. Similarly, Haye et al. (2014) found a requirement of 588.24 °C days above 12.24 °C for egg–adult development. Studies in Asia (reviewed in Kiritani 2007) suggest degree-day requirements ranging from 467.8 to 649 °C days.

Diapause

In CLIMEX, a winter diapause is triggered when day length is less than DPD0 h, daily minimum temperature is less than DPT0, and day length is decreasing (Kriticos et al. 2015a). It is switched off when the daily minimum temperature is greater than DPT1, day length is increasing, and any minimum number of days (DVP) have been spent in diapause. For facultative diapause, DPD is set to 0. Halyomorpha halys enters a state of reproductive diapause before overwintering (Niva and Takeda 2003; Watanabe et al. 1978), though the degree of cold tolerance this confers on the insect is not known experimentally (Cira et al. 2016). For the H. halys model, the threshold day length was set to 12 h and both DPT0 and DPT1 were set to 5 °C, the highest temperature assessed by Cira et al. 2016. DPD was set to 0 because diapause in H. halys is facultative. Stresses were set to accumulate during diapause.

Results

Asia

Overall, in the native range the fit of the model is good, with very high sensitivity and specificity (Fig. 1). The modelled range boundary in the north of China closely matches the known distribution points in this region, with the range boundary following logical topographic patterns (Fig. 1). The fit of the model in Western China was complicated by the high degree of topographic relief, which created a mismatch between the distribution data and the climate surface near the modelled range boundary. Further to the west of the modelled range boundary (near the western edge of Sichuan Province), three records were apparently from infeasibly cold locations, where H. halys would be expected to enter into diapause and never emerge because maximum temperatures are never sufficient to break diapause. In addition, the annual heat sum at these high-altitude locations (>3000 m) was insufficient to support H. halys completing a generation. In Japan, on the Island of Honshu, only two distribution records did not fall in cells modelled as being climatically suitable. These locations are only one cell away from the modelled suitable area, lying in the central part of the island where there is great topographic relief. It is likely that in addition to topographic complexity within a grid cell, this misfit may also be due to errors in the climate surface, or the records may represent transient populations.

North America

The known distribution of H. halys in the USA is quite extensive and provides independent data for a good test of the model (Fig. 2). The region of highest modelled climate suitability accords strongly with the region of highest density of location records in the east. The modelled climatic suitability patterns agreed perfectly with the geographically restricted range of H. halys for regions along the west coast of the USA, where it is well established (e.g. Washington, Oregon, California). The favourable temperature and soil moisture conditions in this region are asynchronous, and hence the modelled climate suitability here is relatively low. The modelled climate suitability in North America highlights the potential for further spread westwards and southwards, and for significant range infill in the central states.

The model did not accord with four aberrant records in North America. The record from Anchorage, Alaska, was a hitchhiker and does not represent an establishment risk. Records from northern locations such as Duluth, Minnesota, USA and Nova Scotia, Canada appear to receive an insufficient heat sum to support a single univoltine generation of H. halys. A southern record was recorded from Wadell, in Maricopa County, Arizona. This location is extremely hot and dry. It is infeasible that H. halys could over-summer in such a climate due to excessive heat stress. A record in Alberta, Canada, was traced back to a campervan, recently returned from the USA.

Europe

The infestation in Europe has had relatively little time to spread compared with North America. The modelled climate suitability patterns accord very strongly with the present known invasion patterns (Fig. 3). There are some minor anomalies in Switzerland where a 10’ lattice of points does not capture the topographic relief patterns and pest risks very well (Kriticos and Leriche 2009). The model further agrees with the current spread of H. halys into the Caucasus regions of Russia and Georgia and projects that H. halys could spread northwards into Poland, whereas Scandinavia and the Baltic states of Estonia, Latvia and Lithuania appear unsuitable under historical climatic conditions. The UK and Ireland appear to be marginally suitable under historical climate, with only a few climate grid cells appearing suitable. In considering these risks, we should be mindful that even small amounts of inter-annual climate variability or climate warming could see this situation change substantially. Similarly, urban heat island effects could perhaps extend the potential range of H. halys into otherwise excessively cold climates.

Southern Hemisphere

Since H. halys is spreading rapidly worldwide, notably through human activities, it is likely that regions in the Southern Hemisphere will be invaded in the near future. For South America, the current model indicates that regions in south eastern Brazil, Uruguay and North-eastern Argentina are highly climatically suitable (Fig. 4). In Africa, the most suitable climates for H. halys appear to be in central Africa (e.g. Uganda, Tanzania, Kenya, Angola) and the sub-tropical eastern areas of South Africa (Fig. 4). In Australia, the highest risk for H. halys establishment would be along the east coast of the continent, and the north of Tasmania, where most horticulture is practised (Fig. 5). The greatest climatic risks from H. halys establishment are to Australia’s vegetable bowl between Bundaberg and Bowen (Fig. 5).
Fig. 4

Modelled climate suitability (CLIMEX Ecoclimatic Index) for Halyomorpha halys globally, including reported distribution locations. Note the three outlying distribution records in the USA and Canada have been investigated and found to be transient populations associated with human transportation

Fig. 5

Modelled climate suitability (CLIMEX Ecoclimatic Index) for Halyomorpha halys in Australasia

In New Zealand, most of the North Island appears climatically suitable, including the Bay of Plenty and Hawke’s Bay horticultural regions (Fig. 5). On the South Island, the northern part of Marlborough and the eastern Canterbury Plains appear to be climatically suited to H. halys.

Discussion

The CLIMEX model of H. halys indicates the potential for substantial range expansion and infill in Europe and North America (Figs. 2, 3), and doubtless increased economic and amenity impacts. The rapid rate of spread in North America and from Italy into other European countries indicates that attempts to control its spread within a continent are ineffective. The difficulties of managing this pest with its potentially large number of generations (Hoffman 1931; Lee et al. 2013) and its multi-pesticide resistance (Leskey et al. 2012b) makes H. halys a formidable threat to plant biosecurity. The ineffectiveness of local-scale management techniques means that invasion pathway management is likely to be the only effective means of managing the invasion risks into the Southern Hemisphere. Sadly, the best that may be hoped for in the Southern Hemisphere may be to buy extra time with freedom from this pest, and to prepare management responses should it become established. Investigations in the USA and Europe are continuing into the effects of natural enemies on H. halys. The forewarning provided by this study to Southern Hemisphere jurisdictions could be used to decide whether it is worthwhile co-investing in researching the feasibility of classical or other biological control solutions (Nystrom Santacruz et al. 2017) that could be applied if H. halys were to be detected in Southern Hemisphere jurisdictions. Such an approach is being pursued in New Zealand (Teulon et al. 2016).

Compared with the MaxEnt model of Rossi and Streito presented in Haye et al. (2015), the current model fits the known distribution better in the native range in China, and in North America, defining the cold tolerance boundaries clearly. The present model also defines the dry range limits more credibly. This is most apparent in the North American and Middle-Eastern desert regions where the CLIMEX model indicates climatic unsuitability and the MaxEnt model indicates suitable climate. The curious arced zone of modelled climate suitability across north-western China in the MaxEnt model (most likely a modelling artefact) is absent from the CLIMEX model.

The high-altitude records in western China that were not fitted using the CLIMEX method here were also not fitted by either of the MaxEnt models, nor the GARP model presented in Zhu et al. (2012). The CLIMEX model appears substantially more skilful than either of these models in the aforementioned studies, with qualitatively better sensitivity and specificity: the MaxEnt model indicating infeasibly large regions of northern Europe as being suitable, and the GARP model being excessively conservative. For example, south eastern China and Taiwan experience a sub-tropical climate, and yet the sub-tropics in Africa and Australia are modelled as unsuitable in the GARP model. The GARP model also did not fit the known suitable locations in northern China and Japan.

In Europe, the CLIMEX model fitted almost all known locations records. The exceptions were in Switzerland, where extreme topographic relief appears to render the 10′ climate grid used here unable to satisfactorily simulate the climates at all known locations. The distribution pattern throughout the rest of Europe is logically consistent.

Halyomorpha halys adults are capable of long-distance flight (approximately 100 km), particularly during summer (Wiman et al. 2015). This only partly explains why H. halys spread so quickly in North America and Europe. Clearly, this species is also capable of being transported very long distances via automotive and air transportation, as appears to have been the case with detections in northern Canada and Alaska. Shipping and sea freight also pose introduction pathway threats for H. halys (Duthie 2012). Considering the difficulties with eradicating established populations, their rapid spread, and the significant impacts to horticulture and human amenity, strenuous efforts to manage importation pathways would seem most prudent. Intuitively, the expanding trade between China and Africa (Pigato and Tang 2015) could pose a substantial biosecurity threat to agricultural development in Africa should H. halys (and other significant agricultural pests) be introduced. Curiously, however, the proportion of recent interceptions of H. halys in Australia and New Zealand were far greater from the USA than from the native range in China and Japan (Duthie 2012), even though trade volumes are similar. Clearly, there is a need for biosecurity authorities throughout most of Africa and the Southern Hemisphere to be extremely vigilant to the invasion threats posed by H. halys.

Author contributions

DK, JK, CP, SS and HA conceived and designed research. DK, JK and HA developed the model. CP, SS and TH provided data. DK, JK and TH wrote the MS. All authors read and approved the manuscript.

Notes

Acknowledgements

All authors read and approved the manuscript. This project is a component of the International Pest Risk Research Group’s “Project Stinky” (www.pestrisk.org/project_stinky).

Compliance with ethical standards

Conflict of interest

The authors have declared that no conflict of interest exists.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Research involving human participants and/or animals

This article does not contain any studies with human participants or animals (vertebrates) performed by any of the authors.

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Copyright information

© Her Majesty the Queen in Right of Australia 2017

Authors and Affiliations

  • Darren J. Kriticos
    • 1
  • John M. Kean
    • 2
    • 3
  • Craig B. Phillips
    • 2
    • 3
  • Senait  D. Senay
    • 3
    • 4
  • Hernando Acosta
    • 5
  • Tim Haye
    • 6
  1. 1.CSIROCanberraAustralia
  2. 2.AgResearch, Forage SystemsChristchurchNew Zealand
  3. 3.Better Border BiosecurityWellingtonNew Zealand
  4. 4.International Science & Technology Practice & Policy (InSTePP), Deptartment of Applied EconomicsUniversity of MinnesotaSt. PaulUSA
  5. 5.Ministry for Primary IndustriesWellingtonNew Zealand
  6. 6.CABIDelémontSwitzerland

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