ORIGINAL PAPER

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

Darren J. Kriticos1 • John M. Kean2,3 • Craig B. Phillips2,3 • Senait D. Senay3,4 •

Hernando Acosta5 • Tim Haye6

Received: 17 February 2017 / Revised: 17 April 2017 / Accepted: 21 April 2017

� Her Majesty the Queen in Right of Australia 2017

Abstract The brown marmorated stinkbug, Halyomorpha

halys is a highly polyphagous invasive insect, which has

more than 300 reported hosts, including important horti-

cultural crops. It has spread to every Northern Hemisphere

continent, most recently to Europe. Whilst there have been

no reports of incursions into Southern Hemisphere coun-

tries, there have been many interceptions associated with

trade and postal goods. We modelled the potential distri-

bution 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 dis-

tribution 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, Scandi-

navia 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 Hemi-

sphere; most recently Europe.

• It is essential for biosecurity agencies to better under-

stand 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 horticul-

tural zones.

Communicated by M. Traugott.

Special issue: The brown marmorated stink bug Halyomorpha halys

an emerging pest of global concern.

& Darren J. Kriticos

Darren.Kriticos@csiro.au

John M. Kean

http://www.b3nz.org

Craig B. Phillips

http://www.b3nz.org

Senait D. Senay

http://www.b3nz.org

1 CSIRO, GPO Box 1700, Canberra, Australia

2 AgResearch, Forage Systems,

Private Bag 4749, Christchurch 8140, New Zealand

3 Better Border Biosecurity, Wellington, New Zealand

4 International Science & Technology Practice & Policy

(InSTePP), Deptartment of Applied Economics, University of

Minnesota, 1994 Buford Ave., 248E Ruttan Hall, St. Paul,

MN 55108, USA

5 Ministry for Primary Industries,

PO Box 2526, Wellington 6140, New Zealand

6 CABI, Rue des Grillons 1, 2800 Delemont, Switzerland

123

J Pest Sci

DOI 10.1007/s10340-017-0869-5

Introduction

Halyomorpha halys Stal (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; Seat 2015; Simov 2016; Vetek

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 dis-

colouration (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 condi-

tions 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 pre-

sented 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 infer-

entially, relying mostly upon geographical distribution data

and phenological observations, as well as deductively,

drawing upon experimental observations of species beha-

viour 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 inde-

pendent 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

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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 west-

ern 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.

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 theoreti-

cally 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. 1–4).

EI ¼ GIA � SI� SX ð1Þ

GIA ¼ 100X52

i¼1

TGIWi=52 ð2Þ

SI ¼ 1� CS=100ð Þ 1� DS=100ð Þ 1� HS=100ð Þ1�WS=100ð Þ ð3Þ

SX ¼ 1� CDX=100ð Þ 1� CWX=100ð Þ 1� HDX=100ð Þ1� HWX=100ð Þ ð4Þ

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 require-

ments for species persistence such as an obligate or fac-

ultative 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 inte-

gral 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 maxi-

mum 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

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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-west-

ern-most records to barely persist. A degree-day cold stress

mechanism was also explored, but all resulting models

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

J Pest Sci

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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) reviewedH. 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 �Cwithmost

rapid development at 25–30 �C. Similarly, Haye et al. (2014)

observed no development atB15 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).

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.

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

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PDD

Nielsen et al. (2008a) estimated that the degree-day

requirements of H. halys were 537.6 �C days above 14 �Cfor 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 develop-

ment. 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 tem-

perature 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. Haly-

omorpha halys enters a state of reproductive diapause

before overwintering (Niva and Takeda 2003; Watanabe

et al. 1978), though the degree of cold tolerance this con-

fers 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, thehighest 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 com-

plicated 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 sup-

port 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

Fig. 3 Modelled climate suitability (CLIMEX Ecoclimatic Index) for Halyomorpha halys in Europe, including reported distribution locations

J Pest Sci

123

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 geo-

graphically 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 temper-

ature and soil moisture conditions in this region are asyn-

chronous, and hence the modelled climate suitability here

is relatively low. The modelled climate suitability in North

America highlights the potential for further spread west-

wards 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, Min-

nesota, USA and Nova Scotia, Canada appear to receive an

insufficient heat sum to support a single univoltine gener-

ation 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 cam-

pervan, recently returned from the USA.

Europe

The infestation in Europe has had relatively little time to

spread compared with North America. The modelled cli-

mate 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 con-

ditions. The UK and Ireland appear to be marginally suit-

able 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 sit-

uation 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

Table 1 CLIMEX parameter values fitted for Halyomorpha halys

Parameter Mnemonic Unit

Temperature requirements

Limiting low temperature DV0 12 �CLower optimal temperature DV1 27 �CUpper optimal temperature DV2 30 �CLimiting high temperature DV3 33 �CDegree-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 �CDiapause termination temperature DPT1 5 �CDiapause development days DPD 0 days

Diapause summer (1) or winter (0) DPSW 0

Cold stress

Temperature threshold TTCS -18 �CStress accumulation rate THCS -0.01 Week-1

Heat stress

Temperature threshold TTHS 33 �CStress 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 �CStress accumulation rate PHW 0.007 Week-1

Values without units are dimensionless indices of plant available soil

moisture

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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 estab-

lishment are to Australia’s vegetable bowl between

Bundaberg and Bowen (Fig. 5).

In New Zealand, most of the North Island appears cli-

matically 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 con-

tinent 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 man-

agement 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 juris-

dictions. 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 Ameri-

can 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

Fig. 4 Modelled climate suitability (CLIMEX Ecoclimatic Index) for

Halyomorpha halys globally, including reported distribution loca-

tions. Note the three outlying distribution records in the USA and

Canada have been investigated and found to be transient populations

associated with human transportation

J Pest Sci

123

models in the aforementioned studies, with qualitatively

better sensitivity and specificity: the MaxEnt model indi-

cating infeasibly large regions of northern Europe as being

suitable, and the GARP model being excessively conser-

vative. 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 100

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 biosecu-

rity threat to agricultural development in Africa should H.

halys (and other significant agricultural pests) be intro-

duced. Curiously, however, the proportion of recent inter-

ceptions 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.

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).

Fig. 5 Modelled climate suitability (CLIMEX Ecoclimatic Index) for Halyomorpha halys in Australasia

J Pest Sci

123

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 individ-

ual participants included in the study.

Research involving human participants and/or animals This

article does not contain any studies with human participants or ani-

mals (vertebrates) performed by any of the authors.

References

Arnold K (2009) Halyomorpha halys (Stal, 1855), Eine fur die

europaische Fauna neu nachgewiesene Wanzenart (Insecta:

Heteroptera: Pentatomidae: Cappaeini). Mitt Thuringer Entomol

16

Bergmann EJ, Venugopal PD, Martinson HM, Raupp MJ, Shrewsbury

PM (2016) Host plant use by the invasive Halyomorpha halys

(Stal) on woody ornamental trees and shrubs. PLoS ONE

11:e0149975

Callot H, Brua C (2013) Halyomorpha halys (Stal, 1855), la Punaise

diabolique, nouvelle espece pour la faune de France (Heteroptera

Pentatomidae). L’Entomologiste 69:69–71

Cesari M, Maistrello L, Ganzerli F, Dioli P, Rebecchi L, Guidetti R

(2015) A pest alien invasion in progress: potential pathways of

origin of the brown marmorated stink bug Halyomorpha halys

populations in Italy. J Pest Sci 88:1–7. doi:10.1007/s10340-014-

0634-y

Chamberlin TC (1965) The method of multiple working hypotheses.

Science 148:754–759. doi:10.1126/science.148.3671.754

Cira TM, Venette RC, Aigner J, Kuhar T, Mullins DE, Gabbert SE,

Hutchison W (2016) Cold tolerance of Halyomorpha halys

(Hemiptera: Pentatomidae) across geographic and temporal

scales. Environ Entomol 45:484–491

De Villiers M et al (2016) The potential distribution of Bactrocera

dorsalis: considering phenology and irrigation patterns. Bull

Entomol Res 106:19–33

Dioli P, Leo P, Maistrello L (2016) Prime segnalazioni in Spagna e in

Sardegna della specie aliena Halyomorpha halys (Stal, 1855) e

note sulla sua distribuzione in Europa (Hemiptera, Pentatomi-

dae). Revista gaditana de Entomologıa 7:539–548

Duthie C (2012) Risk analysis of Halyomorpha halys (brown

marmorated stink bug) on all pathways. Ministry for Primary

Industries, Wellington

Elith J, Phillips SJ, Hastie T, Dudik M, Chee YE, Yates CJ (2011) A

statistical explanation of MaxEnt for ecologists. Div Distrib

17:43–57

Gapon DA (2016) First records of the brown marmorated stink bug

Halyomorpha halys (Stal, 1855) (Heteroptera, Pentatomidae) in

Russia, Abkhazia, and Georgia. Entomol Rev 96:1086–1088

Gariepy TD, Haye T, Fraser H, Zhang J (2014) Occurrence, genetic

diversity, and potential pathways of entry of Halyomorpha halys

in newly invaded areas of Canada and Switzerland J. Pest Sci

87:17–28. doi:10.1007/s10340-013-0529-3

Gariepy TD, Bruin A, Haye T, Milonas P, Vetek G (2015) Occurrence

and genetic diversity of new populations of Halyomorpha halys

in Europe J. Pest Sci 88:451–460. doi:10.1007/s10340-015-

0672-0

Haye T, Abdallah S, Gariepy T, Wyniger D (2014) Phenology, life

table analysis and temperature requirements of the invasive

brown marmorated stink bug, Halyomorpha halys, in Europe.

J Pest Sci 87:407–418. doi:10.1007/s10340-014-0560-z

Haye T, Gariepy T, Hoelmer K, Rossi JP, Streito JC, Tassus X,

Desneux N (2015) Range expansion of the invasive brown

marmorated stinkbug, Halyomorpha halys: an increasing threat

to field, fruit and vegetable crops worldwide. J Pest Sci

88:665–673. doi:10.1007/s10340-015-0670-2

Heckmann R (2012) Erster Nachweis von Halyomorpha halys

(STAL, 1855) (Heteroptera: Pentatomidae) fur Deutschland.

Heteropteron 36:17–18

Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very

high resolution interpolated climate surfaces for global land

areas. Int J Climatol 25:1965–1978

Hiruki C (1997) Paulownia witches’-broom disease important in East

Asia. In: International symposium on urban tree health 496,

pp 63–68. doi:10.17660/ActaHortic.1999.496.6

Hoebeke ER, Carter ME (2003) Halyomorpha halys (Stal) (Hetero-

ptera: Pentatomidae): a polyphagous plant pest from Asia newly

detected in North America. Proc Entomol Soc Wash

105:225–237

Hoffman WE (1931) A pentatomid pest of growing beans in South

China. Peking Nat Hist Bull 5:25–26

Jones JR, Lambdin PL (2009) New county and state records for

Tennessee of an exotic pest, Halyomorpha halys (Hemiptera:

Pentatomidae), with potential economic and ecological implica-

tions. Fla Entomol 92:177–178. doi:10.1653/024.092.0132

Julien MH, Skarratt B, Maywald GF (1995) Potential geographical

distribution of alligator weed and its biological control by

Agasicles hygrophila. J Aquat Plant Manag 33:55–60

Kiritani K (2007) The impact of global warming and land-use change

on the pest status of rice and fruit bugs (Heteroptera) in Japan.

Glob Change Biol 13:1586–1595

Kriticos DJ (2016) Climex publications up until April 2015. CSIRO,

Canberra

Kriticos DJ, Randall RP (2001) A comparison of systems to analyse

potential weed distributions. In: Groves RH, Panetta FD, Virtue

JG (eds) Weed risk assessment. CSIRO Publishing, Melbourne,

pp 61–79

Kriticos DJ, Leriche A (2009) The effects of spatial data precision on

fitting and projecting species niche models. Ecography

33:115–127. doi:10.1111/j.1600-0587.2009.06042.x

Kriticos DJ, Brunel S (2016) Assessing and managing the current and

future pest risk from water hyacinth, (Eichornia crassipes), an

invasive aquatic plant threatening food and water security. PLoS

ONE 11:e0120054

Kriticos DJ, Sutherst RW, Brown JR, Adkins SA, Maywald GF

(2003) Climate change and biotic invasions: a case history of a

tropical woody vine. Biol Invasions 5:145–165

Kriticos DJ, Webber BL, Leriche A, Ota N, Bathols J, Macadam I,

Scott JK (2012) CliMond: global high resolution historical and

future scenario climate surfaces for bioclimatic modelling.

Methods Ecol Evol 3:53–64. doi:10.1111/j.2041-210X.2011.

00134.x

Kriticos DJ, Maywald GF, Yonow T, Zurcher EJ, Herrmann NI,

Sutherst RW (2015a) CLIMEX Version 4: exploring the effects

of climate on plants, animals and diseases. CSIRO, Canberra

Kriticos DJ et al (2015b) The potential distribution of invading

Helicoverpa armigera in North America: Is it just a matter of

time? PLoS ONE 10:e0119618. doi:10.1371/journal.pone.

0119618

Lee DH, Short BD, Joseph SV, Bergh JC, Leskey TC (2013) Review

of the biology, ecology, and management of Halyomorpha halys

(Hemiptera: Pentatomidae) in China, Japan, and the Republic of

Korea Environmental. Entomology 42:627–641. doi:10.1603/

En13006

Leskey TC et al (2012a) Pest status of the brown marmorated stink

bug, Halyomorpha halys in the USA. Outlooks Pest Manag

23:218–226

J Pest Sci

123

Leskey TC, Lee DH, Short BD, Wright SE (2012b) Impact of

insecticides on the invasive Halyomorpha halys (Hemiptera:

Pentatomidae): analysis of insecticide lethality. J Econ Entomol

105:1726–1735

Macavei L, Baetan R, Oltean I, Florean T, Varga M, Costi E,

Maistrello L (2015) First detection of Halyomorpha halys, a new

invasive species with a high potential of damage on agricultural

crops in Romania. Lucrari Stiintifice Seria Agronomie

58:105–108

Mesgaran MB, Cousens RD, Webber BL (2014) Here be dragons: a

tool for quantifying novelty due to covariate range and

correlation change when projecting species distribution models.

Div Distrib. doi:10.1111/ddi.12209

Milonas P, Partsinevelos G (2014) First report of brown marmorated

stink bug Halyomorpha halys Stal (Hemiptera: Pentatomidae) in

Greece. EPPO Bull 44:183–186

Mitchell TD, Carter TR, Jones PD, Hulme M, New M (2004) A

comprehensive set of climate scenarios for Europe and the globe:

the observed record (1900–2000) and 16 scenarios (2000–2100).

University of East Anglia, Norwich

Mityushev IM (2016) First record of marmorated bug detection in

Russia. Zashchita Karantin Rasteniı 3:48

Nielsen AL, Hamilton GC (2009) Life history of the invasive species

Halyomorpha halys (Hemiptera: Pentatomidae) in northeastern

United States. Ann Entomol Soc Am 102:608–616. doi:10.1603/

008.102.0405

Nielsen AL, Hamilton GC, Matadha D (2008a) Developmental rate

estimation and life table analysis for Halyomorpha halys

(Hemiptera: Pentatomidae). Environ Entomol 37:348–355

Nielsen AL, Shearer PW, Hamilton GC (2008b) Toxicity of

insecticides to Halymorpha halys (Hemiptera: Pentatomidae)

using glass-vial bioassays. J Econ Entomol 101:1439–1442

Niva CC, Takeda M (2003) Effects of photoperiod, temperature and

melatonin on nymphal development, polyphenism and repro-

duction in Halyomorpha halys (Heteroptera: Pentatomidae).

Zool Sci 20:963–970. doi:10.2108/zsj.20.963

Nystrom Santacruz E, Venette R, Dieckhoff C, Hoelmer K, Koch RL

(2017) Cold tolerance of Trissolcus japonicus and T. cultratus,

potential biological control agents of Halyomorpha halys, the

brown marmorated stink bug. Biol Control 107:11–20. doi:10.

1016/j.biocontrol.2017.01.004

Pigato M, Tang W (2015) China and Africa: expanding economic ties

in an evolving global context. World Bank, Washington

Rice KB et al (2014) Biology, ecology, and management of brown

marmorated stink bug (Hemiptera: Pentatomidae). J Integr Pest

Manag 5:A1–A13

Seat J (2015) Halyomorpha halys (Stal, 1855) (Heteroptera: Pentato-

midae) a new invasive species in Serbia. Acta Entomologica

Serbica 20:167–171

Shelford VE (1963) The ecology of North America. University of

Illinois Press, Urbana

Simov N (2016) The invasive brown marmorated stink bug

Halyomorpha halys (Stal 1855 (Heteroptera: Pentatomidae)

already in Bulgaria. Ecologica Montenegrina 9:51–53

Sutherst RW, Maywald GF (1985) A computerised system for

matching climates in ecology Agriculture. Ecosyst Environ

13:281–299

Sutherst RW, Bourne AS (2009) Modelling non-equilibrium distri-

butions of invasive species: a tale of two modelling paradigms.

Biol Invasions 11:1231–1237

Teulon DAJ, Leskey TC, Duthie C (2016) Brown marmorated stink

bug—current or planned research to prevent its establishment

and to reduce its impact in New Zealand. NZ Plant Prot 69:323

van der Ploeg RR, Bohm W, Kirkham MB (1999) On the origin of the

theory of mineral nutrition of plants and the law of the minimum.

Soil Sci Soc Am J 63:1055–1062

Vetek G, Papp V, Haltrich A, Redei D (2014) First record of the

brown marmorated stink bug, Halyomorpha halys (Hemiptera:

Heteroptera: Pentatomidae), in Hungary, with description of the

genitalia of both sexes. Zootaxa 3780:194–200

Vink CJ, Derraik JGB, Phillips CB, Sirvid PJ (2011) The invasive

Australian redback spider, Latrodectus hasseltii Thorell 1870

(Araneae: Theridiidae): current and potential distributions, and

likely impacts. Biol Invasions 13:1003–1019. doi:10.1007/

s10530-010-9885-6

Watanabe M, Kamimura K, Koizumi Y (1978) The annual life cycle

of Halyomorpha mista and ovarian development process.

Toyama J Rural Med 9:95–99

Watanabe M, Arakawa R, Shinagawa Y, Okazawa T (1994) Anti-

invading methods against the brown marmorated stink bug,

Halyomorpha mista, in houses. Jpn J Sanit Zool 45:311–317

Watt MS, Ganley RJ, Kriticos DJ, Manning LK (2011) Dothistroma

needle blight and pitch canker: the current and future potential

distribution of two devastating diseases of Pinus species. For

Ecol Manag 41:412–424. doi:10.1139/X10-204

Webber BL et al (2011) Modelling horses for novel climate courses:

insights from projecting potential distributions of native and

alien Australian acacias with correlative and mechanistic mod-

els. Div Distrib 17:978–1000. doi:10.1111/j.1472-4642.2011.

00811.x

Wermelinger B, Wyniger D, Forster B (2008) First records of an

invasive bug in Europe: Halyomorpha halys Stal (Heteroptera:

Pentatomidae), a new pest on woody ornamentals and fruit trees?

Mitteilungen-Schweizerische Entomologische Gesellschaft 81:1

Wiman NG, Walton VM, Shearer PW, Rondon SI, Lee JC (2015)

Factors affecting flight capacity of brown marmorated stink bug,

Halyomorpha halys (Hemiptera: Pentatomidae). J Pest Sci

88:37–47

Yonow T, Kriticos DJ, Medd RW (2004) The potential geographic

range of Pyrenophora semeniperda. Phytopathology 94:805–812

Yonow T, Hattingh V, de Villiers M (2013) CLIMEX modelling of

the potential global distribution of the citrus black spot disease

caused by Guignardia citricarpa and the risk posed to Europe.

Crop Prot 44:18–28. doi:10.1016/j.cropro.2012.10.006

Yonow T, Kriticos DJ, Ota N, Van den Berg J, Hutchison WD (2016)

The potential global distribution of Chilo partellus, including

consideration of irrigation and cropping patterns. J Pest Sci.

doi:10.1007/s10340-016-0801-4

Yu G, Zhang J (2007) The brown marmorated stink bug, Halyomor-

pha halys (Heteroptera: Pentatomidae) in PR China. In: Inter-

national workshop on biological control of invasive species of

forests. Beijing, China, Citeseer, pp 58–62

Zhu G, Bu W, Gao Y, Liu G (2012) Potential geographic distribution

of brown marmorated stink bug invasion (Halyomorpha halys).

PLoS ONE 7:e31246. doi:10.1371/journal.pone.0031246

Zhu G, Gariepy TD, Haye T, Bu W (2016) Patterns of niche filling

and expansion across the invaded ranges of Halyomorpha halys

in North America and Europe. J Pest Sci. doi:10.1007/s10340-

016-0786-z

J Pest Sci

123