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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.
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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
Table 1. Differences in external morphology between Halyomorpha halys and two similar European species, Rhaphigaster nebulosa (Poda, 1761)
and Pentatoma rufipes (Linneaus, 1758).
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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.
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Invasive Halyomorpha halys in Croatia 5
ª 2018 The Authors. Journal compilation ª 2018 OEPP/EPPO, EPPO Bulletin 0, 1–6
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I. Sapina Jelaska
and L. S.
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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