Sunteți pe pagina 1din 6

Bulletin OEPP/EPPO Bulletin (2018) 0 (0), 1–6 ISSN 0250-8052. DOI: 10.1111/epp.

12449

First report of invasive brown marmorated stink bug Halyomorpha


halys (St
al, 1855) in Croatia

I. Sapina  c
and L. Seri  Jelaska
Department of Biology, Faculty of Science, University of Zagreb, Rooseveltov trg 6,10000, Zagreb, (Croatia); e-mail: slucija@biol.pmf.hr

The brown marmorated stink bug, Halyomorpha halys (St al, 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 agri-
cultural 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
(St
al, 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.

(Cesari et al., 2015) and secondary invasions from estab-


Introduction
lished populations within Europe (Gariepy et al., 2015). In
The brown marmorated stink bug, Halyomorpha halys (St al, Croatia the entry of this pest species has been expected
1855), is a pentatomid polyphagous heteropteran, native to from the neighbouring countries, since it was reported in
the Korean peninsula, China, Taiwan and Japan (Hoebeke three out of six nearby countries: in Italy (Pansa et al.,
& Carter, 2003; La Mantia et al., 2017). It is considered to 2013; EPPO, 2014; Maistrello et al., 2014), Hungary
be an agricultural, urban and household pest and feeds on 
(Vetek et al., 2014) and Serbia (Seat, 2015), or from distant
up to 100 plant species (Rice et al., 2014). So far this stink sources via trading goods.
bug has been documented in several European countries Here, the authors report for the first time the finding of
(Fig. 1): Switzerland (Wermelinger et al., 2008), Liechten- six adult H. halys individuals in Croatia. The first individ-
stein (Arndt, 2009 in Hanselman, 2016), Germany (Heck- ual observed and collected was a female, found incidentally
mann, 2012), Italy (Haye & Wyniger, 2013; Pansa et al., by the first author on 15 January 2017, in a flat in a small
2013; EPPO, 2014; Maistrello et al., 2014), France (Callot building in the city of Rijeka in Western Croatia. In the
& Brua, 2013), the United Kingdom (Malumphy, 2014), same flat, a male individual was found incidentally and col-
Greece (Milonas & Partsinevelos, 2014), Hungary (Vetek lected by K. Vucinic, on 25 February 2017. Four individu-

et al., 2014), Serbia (Seat, 2015), Austria (Rabitsch & als, one female and three males, were collected by the
Friebe, 2015), Romania (Macavei et al., 2015) and Russia authors on 16 May 2017, using a sweep net on the
and Georgia (Gapon, 2016). This species was first docu- Ailanthus altissima trees surrounding the building [HTRS
mented in Europe in Liechtenstein in 2004 (Hanselman, 96/TM: E N 337511 5024271,125], [WGS 84: 45°200 22,45″
2016) and then in Switzerland in 2007 (Wermelinger et al., N 14°250 36,10″E] (72 m above sea level). COI sequences
2008). It probably spread from these countries to neigh- of newly found H. halys individuals have been obtained
bouring countries, for example Italy, (Rice et al., 2014; and compared with other sequences available in GenBank
Cesari et al., 2015), being introduced accidentally through in order to identify their haplotype and to try to elucidate
trade and transportation (e.g. Gariepy et al., 2014b, 2015; the pathway of this entry. This paper discusses the potential
Cesari et al., 2015; Macavei et al., 2015). In some of these spread and possible new entries to the country.
countries the populations were established soon after the
introduction with evident damage in fruits and vegetables
Material and methods
and reports of household nuisance when adult H. halys
enters residences for overwintering (Cesari et al., 2015; In three visits, 15 January, 25 February and 16 May 2017,
Macavei et al., 2015; Vetek & Koranyi, 2017). Genetic only six live H. halys adult individuals were observed and
data from recently established populations in Italy, France, collected by hand and using a sweep net, and then pre-
Greece, Hungary and Southern Switzerland indicate differ- served in absolute ethanol prior to DNA extraction, without
ent introduction pathways in Europe: multiple invasions any observations of eggs, juvenile forms or dead individu-
from Asia (Gariepy et al., 2015) and North America als. For identification the authors used the Wyniger &

ª 2018 The Authors. Journal compilation ª 2018 OEPP/EPPO, EPPO Bulletin 0, 1–6 1
2 
I. Sapina  Jelaska
and L. S.

Fig. 1 Distribution map of Halyomorpha halys across Europe, representing the first records in each country.

Kment (2010) key to separate H. halys from similar-appear- in one direction by Macrogen Inc. (Republic of Korea) using
ing pentatomids in Central Europe, and Hoebeke & Carter the LCO-1490 primer. Sequences are deposited in GenBank
(2003) which has a detailed morphological description of under accession numbers KY930699, KY930700 and
the species. For external examination a stereoscopic micro- KY930701. Novel sequences were aligned with other
scope (Zeiss Stemi 2000-C) with a cold light source (Zeiss sequences of the COI region of H. halys deposited in NCBI
KL 1500 Electronic) was used. The measurements of total GenBank using BioEdit 7.2.1. The Statistical Parsimony
body length (from the tip of the head to the tip of folded method (TCS) (Clement et al., 2000) within PopART soft-
forewings) and width across the humeral angles were taken ware (version 1.7) was used to construct a haplotype network
with a digital calliper (with accuracy of 0.01 mm). The based on novel data and those already available in GenBank
DNA was extracted from the middle leg muscles of two up to May 2017 (see the online Supporting Information).
individuals, one female collected on 15 January and one
male collected on 16 May 2017 using a DNeasy Blood and
Results
Tissue Kit (Qiagen), and amplified by PCR using general
invertebrate primers LCO-1490 (50 -GGTCAACAAATCA-
Material examined
TAAAGATATTGG-30 ) and HCO-2198 (50 -TAAACTT-
CAGGGTGACCAAAAAATCA-30 ), generating a 710-bp Two adult female (see Fig. 2) and four male Halyomorpha
fragment of the mitochondrial cytochrome oxidase I (COI) halys (Pentatominae: Cappaeini) were examined, with aver-
gene (Folmer et al., 1994) using the same conditions as in age total body length of 15.9 and 14.1 mm, respectively,
 c Jelaska et al. (2014). Polymerase chain reaction began
Seri and average length across the humeral angles of 8.36 and
with a 15-min initialization step at 95°C, followed by 35 8.13 mm, respectively.
cycles of denaturation for 90 s at 94°C, primer annealing
for 90 s at 45°C and fragment elongation for 1 min at
Identification
72°C. The programme ended with the final reaction of
DNA synthesis lasting 7 min at 72°C. PCR products were Since available keys for European insects or Heteroptera
purified using a Roche High Pure PCR Product Purification will lead to Pentatoma rufipes (Linneaus, 1758) if identify-
Kit, following the manufacturer’s instructions, and sequenced ing H. halys specimens (Wyniger & Kment, 2010), a

ª 2018 The Authors. Journal compilation ª 2018 OEPP/EPPO, EPPO Bulletin 0, 1–6
Invasive Halyomorpha halys in Croatia 3

only six specimens have been found, in January, February


and May 2017. Two specimens were found incidentally,
inside a flat, in January and February, and four specimens
were observed during an additional search of the surround-
ing A. altissima trees in May 2017. After genetic analysis it
has been shown that the specimens that were found in this
study are from a haplotype that is found in H. halys popu-
lations present in Asia, North America and Europe, and
according to Gariepy et al. (2015) and Cesari et al. (2015)
and is the most common haplotype within nearby Italian
and Hungarian populations.
The arrival of H. halys in Croatia was expected from
two different sources: from the populations from three
Fig. 2 Halyomorpha halys female found indoors, in Rijeka, Croatia.
neighbouring countries, Italy, Hungary and Serbia, since it
had already been reported there (EPPO, 2014; Vetek et al.,
simple comparison of distinct features for H. halys and the 
2014; Seat, 2015), and as a hitchhiker on goods from dis-
two most similar European species is presented in Table 1. tant areas (e.g. by the wood and plant trade through sea-
Two specimens generated three DNA sequences for the ports, by roads, etc.). Most of the first observations of this
50 end of the mitochondrial COI gene 703, 719 and 722 bp pest in Europe occurred in large urban areas and capital
long. cities [e.g. Athens (Milonas & Partsinevelos, 2014), Buda-
Genetic analyses showed that Croatian individuals share pest (Vetek et al., 2014) and Vienna (Rabitsch & Friebe,
the same haplotype (H5, node number 5, Fig. 3A,B) with 2015)], probably due to intensive trade and transportation
Hungarian and Italian populations. The same haplotype has that are also concentrated in the city of Rijeka as the prin-
also been reported in populations from three other European cipal seaport in Croatia.
countries, namely Switzerland, France and Greece. Along Although Italy has a sea border with Croatia, the Italian
with H5 that has been dominant in the Emilia Romagna terrestrial border is around 60 km away from Rijeka, and
Region in Italy (Cesary et al., 2015), Italian populations share intensive trade and transportation by roads, connecting North-
the H3 haplotype (placed within node 3, Fig. 3A) also present ern Italy and Western Croatia, might facilitate the spread of
in France and Switzerland Fig. 3B); Hungarian populations, this species from Italy. In Italy the first record of this species
along with H5, shared the H4 haplotype (node number 3, Fig. occurred more than 5 years ago, in 2012 (Haye & Wyniger,
3A), but according to Gariepy et al., (2015) with much lower 2013; EPPO, 2014; Maistrello et al., 2014), with evidence of
proportions than H5. Haplotype H4 is also present in France, population establishment in the Emilia Romagna Region 3
Switzerland and Greece. Haplotypes within nodes 8, 9, 22, years later (Cesari et al., 2015). In Hungary and Serbia, the
23 and 25 are present only in Greek populations and H12 species was observed for the first time in 2014 and 2015,
(node 12) in Switzerland (Fig. 3B). 
respectively (Vetek et al., 2014; Seat, 2015), with records of
serious damage to vegetables in Hungary (Vetek & Koranyi,
2017), so those populations can act as a source for new entry
Discussion
and spread towards Northern and Eastern Croatia.
The first record of H. halys for Croatia occurred in the Halyomorpha halys is polyphagous with preferences for
western part of the country, in the city of Rijeka. So far the invasive A. altissima (Miller) Swingle and non-native

Table 1. Differences in external morphology between Halyomorpha halys and two similar European species, Rhaphigaster nebulosa (Poda, 1761)
and Pentatoma rufipes (Linneaus, 1758).

Species H. halys R. nebulosa P. rufipes


*
Antennae coloration
2nd segment* Uniformly coloured, dark Base white, apex coloured Base uniformly coloured, apex white
4nd segment* Uniformly coloured, white Base white, apex coloured Base uniformly coloured, apex white
Antennae length
2nd segment Much shorter than the 3rd, Equal to the 4th or 5th segments Slightly shorter than the 3rd, 4th or
4th or 5th segments 5th segments
Head shape Rectangular Triangular Triangular
Membrane* Dark stripes Dark spots No markings
Trapezoidal white fields White mushroom-shaped fields White T-shaped fields
Frenum* Uniformly coloured Differently coloured Differently coloured
*
Variable in shape and size but consistent in general description.

ª 2018 The Authors. Journal compilation ª 2018 OEPP/EPPO, EPPO Bulletin 0, 1–6
4 
I. Sapina  Jelaska
and L. S.

(A)

(B)

B C

Fig. 3 (A) Phylogenetic network showing relationships among COI haplotypes from Halyomorpha halys populations recorded in Europe. The
numbers at the nodes denote different haplotypes and different colours within the circles denote the presence of the haplotypes in the six European
countries and their presence in other continents: Asia and North America. Black dots indicate evolutionary mutational steps. The diagram represents
only haplotype connectivity and does not provide a quantitative representation of these haplotypes. (B) Distribution map of nine haplotypes (H3, 4,
5, 8, 9, 12, 22, 23, 25) in Europe (A), North America (B) and Asia (C). Different haplotypes are represented in the pie charts with different colours.
Distribution data has been taken from NCBI GenBank and published literature (Gariepy et al., 2014a,b, 2015; Xu et al., 2014; Cesari et al., 2015;
Dhami et al., 2016; Zhu et al., 2016). The list of haplotypes screened for this study in May 2017 is listed in the online Supporting Information.

ª 2018 The Authors. Journal compilation ª 2018 OEPP/EPPO, EPPO Bulletin 0, 1–6
Invasive Halyomorpha halys in Croatia 5

Paulownia tomentosa (Thunberg) Steudel (Haye et al.,


Пepвoe cooбщeниe oб инвaзивнoм
2014; Rice et al., 2014). Ailanthus altissima is found in
кopичнeвoм мpaмopнoм щитникe Halyomorpha
Rijeka and P. tomentosa occurs outside the city (Flora
halys (St
al, 1855) в Xopвaтии
Croatica Database, Nikolic, 2017). Both plant species are
considered very important for the establishment of popula- C мoмeнтa пoявлeния пepвыx дoкyмeнтиpoвaнныx
tions of H. halys in areas where they are newly introduced, cooбщeний пoлyчeнныx из Лиxтeнштeйнa в 2004 гoдy и
especially in the final stages of their development (Rice из Швeйцapии в 2007 гoдy, кopичнeвый мpaмopный
et al., 2014). Unfortunately, urban habitats in Croatia suffer щитник Halyomorpha halys (St al, 1855) (Hemiptera:
from a strong invasion of A. altissima (Nikolic et al., Heteroptera: Pentatomidae) pacпpocтpaняли пo вceй
2013). This plant could facilitate the establishment of stable Eвpoпe. Oн cчитaeтcя вpeдитeлeм мнoгиx
H. halys populations in urban areas in Croatia, therefore ceльcкoxoзяйcтвeнныx кyльтyp и cyщecтвoм,
the authors suggest further monitoring of this area in order дoкyчaющим людям в дoмax. B 2017 гoдy этoт вид был
to check if populations will establish. Besides urban areas, впepвыe oбнapyжeн в Xopвaтии, в гopoдe Pиeкa нa
the arrival of H. halys could be expected in eastern and ceвepнoм пoбepeжьe Aдpиaтичecкoгo мopя. H. halys yжe
northern parts of Croatia in orchards and vegetable gardens, был зapeгиcтpиpoвaн в тpex coceдниx cтpaнax (Итaлии,
spreading from neighbouring Hungary. Beнгpии и Cepбии), и пoэтoмy пoявлeниe этoгo видa
The genus Halyomorpha Mayr, 1864 is represented by oжидaлocь либo из coceдниx пoпyляций, либo из
37 species (Rider, 2005), and only one species has been oтдaлeнныx иcтoчникoв чepeз тoвapы, пpи тopгoвлe. Для
recorded outside its native area. Still, the possibility that выявлeния пyти pacпpocтpaнeния, гaплoтипы ocoбeй H.
some other species of this genus will expand out of their al, 1855) были изyчeны пyтeм cpaвнeния чacти
halys (St
native range through human activities cannot be excluded, митoxoндpиaльнoгo гeнa COI c дpyгими гaплoтипaми
and thus a good identification key to Halyomorpha cyщecтвyющими в бaзe дaнныx GenBank.
should be made for easier monitoring and further predic- Индивидyaльныe ocoби имeли oбщий нaибoлee
tions. pacпpocтpaнeнный гaплoтип c coceдними итaльянcкими
и вeнгepcкими пoпyляциями.
Acknowledgements
The authors would like to thank to S. D. Jelaska for taking
References
photographs, J. Skejo and anonymous reviewers for helpful Callot H & Brua C (2013) Halyomorpha halys (St al, 1855), la Punaise
comments on the manuscript, V. Plazonic and L. Rucevic diabolique, nouvelle espece pour la faune de France (Heteroptera

for language editing and K. Vucinic for enabling I. Sapina Pentatomidae). Entomologiste (Paris) 69, 69–71.
to inspect the apartment and associated facilities in the Cesari M, Maistrello L, Ganzerli F, Dioli P, Rebecchi L & Guidetti R
(2015) A pest alien invasion in progress: potential pathways of origin
building where the specimens were found.
of the brown marmorated stink bug Halyomorpha halys populations
in Italy. Journal of Pest Sciences 88, 1–7. https://doi.org/10.1007/
s10340-014-0634-y.
Premier signalement de la punaise diabolique
envahissante Halyomorpha halys (St
Clement M, Posada D & Crandall KA (2000) TCS: a computer program
al, 1855) en to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
Croatie Dhami MK, Dsouza M, Waite DW, Anderson D & Li D (2016) Real-
Time PCR assay for the identification of the brown marmorated stink
La punaise diabolique Halyomorpha halys (St al, 1855)
bug (Halyomorpha halys). Frontiers in Molecular Biosciences 3, 5.
(Hemiptera: Heteroptera: Pentatomidae), se dissemine en https://doi.org/10.3389/fmolb.2016.00005.
Europe depuis les premiers signalements du Liechtenstein EPPO (2014) PQR database. Paris, France: European and
en 2004 et de la Suisse en 2007. Elle est consideree Mediterranean Plant Protection Organization. http://www.eppo.int/
comme un organisme nuisible a de nombreuses cultures DATABASES/pqr/pqr.htm [accessed on 12 June 2017]
agricoles, ainsi qu’une nuisance domestique. En 2017, Folmer O, Black M, Hoeh W, Lutz R & Vrijenhoek R (1994) DNA
l’espece a ete observee pour la premiere fois en Croatie, primers for amplification of mitochondrial cytochrome coxidase
subunit I from diverse metazoan invertebrates. Molecular Marine
dans la ville de Rijeka sur la c^ote nord de l’Adriatique. H.
Biology and Biotechnology 3, 294–299.
halys a deja ete signalee dans trois pays voisins (Italie, Gapon DA (2016) First records of the brown marmorated stink bug
Hongrie et Serbie). Par consequent, l’arrivee de cette Halyomorpha halys (St al, 1855) (Heteroptera, Pentatomidae) in
espece etait attendue depuis ces populations voisins, ou de Russia, Abkhazia, and Georgia. Entomological Review 96, 1086.
sources eloignees via le commerce de marchandises. Pour https://doi.org/10.1134/S001387381608011X.
identifier la filiere d’entree, les haplotypes des specimens Gariepy TD, Bruin A, Haye T, Milonas P & Vetek G (2015)
de H. halys (St al, 1855) ont ete analyses en comparant une Occurrence and genetic diversity of new populations of
Halyomorpha halys in Europe. Journal of Pest Sciences 88, 451–460.
partie du gene mitochondrial COI avec d’autres haplotypes
Gariepy TD, Fraser H & Scott-Dupree CD (2014a) Brown marmorated
presents dans la base de donnees GenBank. Les specimens stink bug (Hemiptera: Pentatomidae) in Canada: recent
partageaient l’haplotype le plus commun avec les establishment, occurrence, and pest status in southern Ontario. The
populations italiennes et hongroises voisines. Canadian Entomologist 146, 579–582.

ª 2018 The Authors. Journal compilation ª 2018 OEPP/EPPO, EPPO Bulletin 0, 1–6
6 
I. Sapina  Jelaska
and L. S.

Gariepy TD, Haye T, Fraser H & Zhang J (2014b) Occurrence, genetic Rabitsch W & Friebe GJ (2015) From the west and from the east? First
diversity, and potential pathways of entry of Halyomorpha halys in records of Halyomorpha halys (St al, 1855) (Hemiptera: Heteroptera:
newly invaded areas of Canada and Switzerland. Journal of Pest Pentatomidae) in Vorarlberg and Vienna, Austria. Beitr€ age zur
Sciences 87, 17–28. Entomofaunistik 16, 115–139.
Hanselman D (2016) Aliens and Citizens in Germany: Halyomorpha Rice KB, Bergh CJ, Bergmann EJ, Biddinger DJ, Dieckhoff C, Dively
halys (Stal, 1855) and Nezara viridula (Linnaeus, 1758) new to G et al. (2014) Biology, ecology, and management of brown
Rhineland-Palatinate, Oxycarenus lavaterae (Fabricius, 1787) new to marmorated stink bug (Hemiptera: Pentatomidae). Journal of
Saxony, Arocatus longiceps St al, 1872 new to Hesse. Mainzer Integrated Pest Management 5, A1–A13. https://doi.org/10.1603/
naturwissenschaftliches Archiv 53, 159–177. IPM14002.
Haye T, Abdallah S, Gariepy T & Wyniger D (2014) Phenology, life Rider DA (2005) Pentatomoidea home page. https://www.ndsu.
table analysis, and temperature requirements of the invasive brown edu/pubweb/~rider/Pentatomoidea/Genus_Cappaeini/Halyomorpha.htm
marmorated stink bug, Halyomorpha halys, in Europe. Journal of [accessed 01 September 2005]
Pest Sciences 87, 407–418. 
Seat J (2015) Halyomorpha halys (St al, 1855) (Heteroptera:
Haye T & Wyniger D (2013) Current distribution of Halyomorpha Pentatomidae) a new invasive species in Serbia. Acta Entomologica
halys in Europe. http://www.halyomorphalhalys.com/aktuelle-verbre Serbica 20, 167–171.
itungskarts-current-distribution.html [accessed on 30 March 2017]  c Jelaska L, Jambrosic Vladic Z,
Seri  Radovanovic H & Franjevic D
Heckmann R (2012) First evidence of Halyomorpha halys (Stal, 1855) (2014) Comparison of molecular and morphological systematic of
(Heteroptera: Pentatomidae) in Germany. Heteropteron 36, 17–18. Carabus species (Coleoptera: Carabidae) with emphasis on species
Hoebeke ER & Carter ME (2003) Halyomorpha halys (St al) from Dinaric karst. Periodicum Biologorum 116, 249–257.
(Heteroptera: Pentatomidae): a polyphagous plant pest from Asia Vetek G & Koranyi D (2017) Severe damage to vegetables by the
newly detected in North America. Proceedings of the Entomological invasive brown marmorated stink bug, Halyomorpha halys
Society of Washington 105, 225–237. (Hemiptera: Pentatomidae), in Hungary. Periodicum biologorum 119,
La Mantia MJ, Rouf Mian MA & Redinbaugh GM (2017) 131–135. https://doi.org/10.18054/pb.v119i2.4935.
Identification of soybean host plant resistance to brown marmorated Vetek G, Papp V, Haltrich A & Redei D (2014) First record of the
stink Bugs in Maturity Group III plant introductions. Journal of brown marmorated stink bug, Halyomorpha halys (Hemiptera:
Economic Entomology tox295. https://doi.org/10.1093/jee/tox295. Heteroptera: Pentatomidae), in Hungary, with description of the
Macavei LI, B^aetßan R, Oltean I, Florian T, Varga M, Costi E et al. genitalia of both sexes. Zootaxa 3780, 194–200.
(2015) First detection of Halyomorpha halys St al, a new invasive Wermelinger B, Wyniger D & Forster B (2008) First records of
species with a high potential of damage on agricultural crops in an invasive bug in Europe: Halyomorpha halys St al (Heteroptera:
Romania. Lucr ari Sßtiintßifice seria Agronomie 58, 105–108. Pentatomidae), a new pest on woody ornamentals and fruit trees?
Maistrello L, Dioli P, Vaccari G, Nannini R, Bortolotti P, Caruso S Mitteilungen-Schweizerische Entomologische Gesellschaft 81, 1–8.
et al. (2014) First records in Italy of the Asian stinkbug Wyniger D & Kment P (2010) Key for the separation of Halyomorpha
Halyomorpha halys, a new threat for fruit crops. ATTI Giornate halys (St
al) from similar-appearing pentatomids (Insecta: Heteroptera:
Fitopatologische 1, 283–288. Pentatomidae) occurring in Central Europe, with new Swiss records.
Malumphy C (2014) Second interception of Halyomorpha halys Mitteilungen der Schweizerischen Entomologischen Gesellschaft 83,
(St
al) (Hemiptera: Pentatomidae) in Britain. Het News, 3rd Series 261–270.
21, 4–5. Xu J, Fonseca DM, Hamilton GC, Hoelmer KA & Nielsen AL (2014)
Milonas PG & Partsinevelos GK (2014) First report of brown Tracing the origin of US brown marmorated stink bugs Halyomorpha
marmorated stink bug Halyomorpha halys Stal (Hemiptera: halys. Biological Invasions 16, 153–166.
Pentatomidae) in Greece. Bulletin OEPP 44, 183–186. Zhu GP, Ye Z, Du J, Zhang DL, Zhen YH, Zheng CG et al. (2016) Range
Nikolic T. ed. (2017) Flora Croatica database. Prirodoslovno- wide molecular data and niche modelling revealed the Pleistocene history
matematicki fakultet, Sveuciliste u Zagrebu. http://hirc.botanic.hr/fcd of a global invader (Halyomorpha halys). Scientific Reports 6, 23192.
[accessed on 22 February 2017]
Nikolic T, Mitic B & Milasinovic B (2013) Invasive alien plants in
Croatia as a threat to biodiversity of South-Eastern Europe: Supporting Information
Distributional patterns and range size. Comptes Rendus Biologies
336, 109–121.
Table S1. Accession numbers of the nucleotide
Pansa MG, Asteggiano L, Costamagna C, Vittone G & Tavella L sequences of the Halyomorpha halys taken from the NCBI
(2013) First discovery of Halyomorpha halys in peach orchards in Database on the 10th of May 2017 and used in the
Piedmont. (Primo ritrovamento di Halyomorpha halys nei pescheti analyses, with annotated haplotypes and geographical
piemontesi.). Informatore Agrario 69, 60–61. position (continent/country).

ª 2018 The Authors. Journal compilation ª 2018 OEPP/EPPO, EPPO Bulletin 0, 1–6

S-ar putea să vă placă și