Spread and potential host range of the invasive oak lace bug [Corythucha arcuata (Say, 1832) – Heteroptera: Tingidae] in Eurasia

Abstract

The North American oak lace bug feeds on leaves of ‘white oaks” in its native range. In Europe, it was first discovered in northern Italy in 2000. In recent years, it has subsequently spread rapidly and population outbreaks have been observed in several European countries. In the present study, we summarize the steps of its expansion.
To predict its potential host range, we checked 48 oak species in 20 sentinel gardens in seven countries between 2013 and 2018.
In total, 27 oak species were recorded as suitable hosts; 13 of them are globally new ones, 23 out of the 29 in section Quercus (∼ white oaks, an intrageneric taxonomic unit within genus Quercus ), including Asian oaks, native to Japan, Korea and China, and four out of five in section Cerris (another intrageneric unit of the same genus), were accepted as hosts. None of the species in section Lobatae (red oaks) or in the Ilex group was accepted.
Host records were also collected in forest stands of 10 countries. We found 11 oak species that were infested. Outbreak populations were most commonly found on Quercus robur , Quercus frainetto , Quercus petraea and Quercus cerris , comprising widespread and outstandingly important oaks species in Europe.
Based on our findings, we conclude that suitable hosts for oak lace bug are present in most of Europe and Asia. This means that a lack of hosts will likely not restrict further range expansion.

Full text

Agricultural and Forest Entomology (2019), DOI: 10.1111/afe.12362
Spread and potential host range of the invasive oak lace bug
[Corythucha arcuata (Say, 1832) – Heteroptera: Tingidae] in Eurasia
György Csóka∗,AnikóHirka
∗, Serap Mutun†, Milka Glavendeki ´
c‡, Ágnes Mikó∗, Levente Sz ˝
ocs∗,
Márton Paulin∗, Csaba Béla Eötvös∗, Csaba Gáspár∗, Mariann Csepelényi§, Ágnes Szénási§, Milivoj Franjevi ´
c¶,
Yuri Gninenko∗∗, Mirza Dautbaši ´
c††, Osman Muzejinovi ´
c††, Milan Zúbrik‡‡ , Constantin Netoiu§§ ,Andrei
Buzatu§§ , Flavius B ˘
al ˘
acenoiu§§ ,MajaJurc
¶¶, Dušan Jurc∗∗∗, Iris Bernardinelli†††, Jean-Claude Streito‡‡‡ ,
Dimitrios Avtzis§§§ and Boris Hrašovec¶
∗Department of Forest Protection, NARIC Forest Research Institute, Hegyalja 18, 3232 Mátrafüred, Hungary, †Faculty of Arts and Science,
Department of Biology, Bolu Abant ˙
Izzet Baysal University, 14030 Bolu, Turkey, ‡Faculty of Forestry, Department of Landscape Architecture and
Horticulture, University of Belgrade, Belgrade, Kneza Višeslava 1, 11030 Belgrade, Serbia, §Institute of Plant Protection, Szent István University,
Páter K. 1, 2100 Gödöll˝
o, Hungary, ¶University of Zagreb Faculty of Forestry, Institute of Forest Protection and Wildlife Management, Svetošimunska
cesta 25, 10000 Zagreb, Croatia, ∗∗Department for Forest Protection, All-Russian Research Institute of Silviculture and Mechanization of Forestry,
Pushkino, Institutskaya ul. 15, 141200 Pushkino Moskow oblast, Russia, ††Faculty of Forestry, University of Sarajevo, Sarajevo, Zagrebacka 20, 71000
Sarajevo, Bosnia and Herzegovina, ‡‡National Forest Centre, Forest Protection Service, Banská Štiavnica, Lesnícka 11, 96901 Banská Štiavnica,
Slovak Republic, §§National Institute for Research and Development in Forestry “Marin Dr˘
acea” Bucharest. Bulevardul Eroilor 128, 077190
Voluntari, Romania, ¶¶Department of Forestry and Renewable Forest Resources, University of Ljubljana, Jamnikarjeva ulica 101, SI-1000 Ljubljana,
Slovenija, ∗∗∗The Tree Institute, Institute for the Development and Research of Forest and Trees, Polje XXII/4, 1260 Ljubljana-Polje, Slovenia,
†††Servizio tosanitario e chimico, ricerca, sperimentazione e assistenza tecnica, Pozzuolo del Friuli, Via Sabbatini 5, 33050 Pozzuolo del Friuli, Italy,
‡‡‡INRA-CBGP, Montferrier sur Lez, France and §§§Forest Research Institute, Hellenic Agricultural Organisation Demeter, Vassilika, 57006
Thessaloniki, Greece
Abstract 1 The North American oak lace bug feeds on leaves of ‘white oaks” in its native
range. In Europe, it was rst discovered in northern Italy in 2000. In recent years,
it has subsequently spread rapidly and population outbreaks have been observed
in several European countries. In the present study, we summarize the steps of its
expansion.
2 To predict its potential host range, we checked 48 oak species in 20 sentinel gardens
in seven countries between 2013 and 2018.
3 In total, 27 oak species were recorded as suitable hosts; 13 of them are globally new
ones, 23 out of the 29 in section Quercus (∼white oaks, an intrageneric taxonomic
unit within genus Quercus), including Asian oaks, native to Japan, Korea and China,
and four out of ve in section Cerris (another intrageneric unit of the same genus),
were accepted as hosts. None of the species in section Lobatae (red oaks) or in the Ilex
group was accepted.
4 Host records were also collected in forest stands of 10 countries. We found 11 oak
species that were infested. Outbreak populations were most commonly found on
Quercus robur,Quercus frainetto,Quercus petraea and Quercus cerris, comprising
widespread and outstandingly important oaks species in Europe.
5 Based on our ndings, we conclude that suitable hosts for oak lace bug are present in
most of Europe and Asia. This means that a lack of hosts will likely not restrict further
range expansion.
Keywords Corythucha arcuata, host plants, non-native species, Quercus spp,
sentinel gardens.
Introduction
Insects are among the most numerous invaders worldwide (Kenis
& Branco, 2010; Brockerhoff & Liebhold, 2017) and make
Correspondence: György Csóka. Tel.: +36 30 3050747; e-mail:
csokagy@erti.hu
up approximately 87% of the non-native arthropods introduced
in Europe (Roques, 2010). Non-native insect species have
appeared at an alarmingly increasing rate in Europe in recent
decades (Roques, 2010; Kenis & Branco, 2010; Csóka et al.,
2012; Tuba et al., 2012; Csóka et al., 2017; Smith et al., 2018).
Although some non-native insects spread slowly and do not
cause detectable economic/ecological damage, others become
© 2019 The Royal Entomological Society

2G. Csóka et al.
Table 1 North American host records of oak lace bug based on literature sources: (Morrill [1903]; Osborn & Drake [1917]; Connell & Beacher [1947];
Drake & Ruhoff [1965]; Connor [1988]; Torres-Miller [1995]; Drew & Arnold [1997]; Trieff [2002]; Kay et al. [2007]; Barber [2010])
Name Common name Native range*
Section Quercus – white oaks
Quercus alba L. 1753 White oak Eastern North America
Quercus bicolor Willd 1801 Swamp white oak North-eastern U.S.A.; southern Canada
Quercus macrocarpa Michx. 1801 Bur oak Eastern North America
Quercus montana Willd. 1805 Chestnut oak Southern and eastern U.S.A.
Quercus muehlenbergii Engelm. 1887 Chinkapin oak Eastern and central U.S.A.; Canada; north-eastern Mexico
Quercus prinoides Willd. 1801 Dwarf chinkapin oak Eastern U.S.A.
Quercus stellata Wangenh. 1787 Post oak Central and south-eastern U.S.A.
Native ranges are taken from Web link (2019). Common names of the oaks follow Miller & Lamb (1985).
invasive, rapidly expand their range and subsequently have rather
severe effects within newly invaded area. Examples of recent
rapid spreads within Europe are provided amongst many oth-
ers by Obolodiplosis robiniae (Skuhrava et al., 2007), Har-
monia axyridis (Roy et al., 2016), Leptoglossus occidentalis
(Lesieur et al., 2018) and Halyomorpha halys (Vétek et al.,
2018). Non-native species, in addition to their potential to cause
signicant economic losses, may have impacts on natural pro-
cesses in ecosystem functions (Simberloff, 2001, 2011; Kenis
et al., 2009; Wardle & Peltzer, 2017; Liebhold et al., 2017).
One of the major determinants regarding a non-native insect’s
potential to become invasive is the availability of its hosts. If
suitable hosts are absent or very rare in the newly invaded
territory, the non-native insect species has limited chance to
establish and become invasive.
The oak lace bug (Corythucha arcuata Say, 1832 –
Heteroptera: Tingidae; herein abbreviated as ‘OLB’) is native
and widespread in the eastern part of the U.S.A. and across
southern Canada (Barber, 2010). The known host records from
its native range are listed in Table 1. Surprisingly, only seven
oak species out of more than 40 native to North America are
named at the species level (Table 1). Most literature sources
refer to the hosts of OLB as oaks, or slightly more accurately
white oaks (section Quercus in genus Quercus). Morrill (1903)
also recorded ‘English oak’ (Quercus robur) as a preferred host
in Massachusetts, although he used the scientic name of this
species incorrectly (he gave Quercus rubra instead of Q. robur).
Non-oak hosts include Castanea dentata,Acer spp., Malus
spp., Pyrus spp. and Rosa spp. without accurate species names
(Connell & Beacher, 1947; Drake & Ruhoff, 1965; Drew &
Arnold, 1977).
OLB was rst discovered in Europe, in northern Italy in
2000 (Bernardinelli, 2000; Bernardinelli & Zandigiacomo, 2000)
(Fig. 1.). Recognizing its potential importance, OLB was put on
the EPPO Alert List in March 2001 and it remained until 2007,
when it became clear that administrative efforts could not stop
its further spread. Between April and July 2002, two specimens
of OLB were caught in a ight interception trap in southern
Switzerland (Forster et al., 2005). In the same year, OLB was
found for the rst time in Turkey, approximately 200km east
of Istanbul (Mutun, 2003). One specimen was found in Iran
(Western Azerbaidjan) in 2005 (Samin & Linnavuori, 2011).
By the summer of 2008, the distribution expanded signicantly,
reaching 28 000 km2only in Turkey (Mutun et al., 2009). This
population build-up in western Asia most likely acted as a prolic
source for the spread north through the Balkans. However, a
human-mediated accidental introduction from northern Italy to
other countries could not be excluded.
In July 2012, OLB was found in Bulgaria (Dobreva et al.,
2013). One year later, it appeared in Hungary (Csóka et al.,
2013), and was recorded at two distant (140 km in a straight line)
locations almost at the same time. In 2013, it was also discovered
in Croatia (Hrašovec et al., 2013) and Serbia (Poljakovi´
c-Pajnik
et al., 2015; Pap et al., 2015; Glavendeki´
c, 2017). In Russia,
OLB was rst found in Krasnodar in 2015 (Neimorovets et al.,
2017). OLB was detected for the rst time in 2016, again in
several countries: Albania (E. Cota, personal communication),
at two locations in Romania, rather far (at least 400 km) from
each other (Don et al., 2016; Chireceanu et al., 2017). In autumn
2016, Jurc & Jurc (2017) also recorded it in Slovenia, close
to the Croatian border (Jurc & Jurc, 2017). In Bosnia and
Herzegovina, the rst observation dates from 2017 (Glavendeki´
c
& Vukovic-Bojanovi´
c, 2017; Dautbaši´
cet al., 2018). In the
same year, it was detected in southwestern France (Streito
et al., 2018). In 2017, it was also found in southern Ukraine
(V. Meshkova, personal communication). In May 2018, OLB
has been recorded in north-eastern Greece (D. Avtzis, personal
communication) and in June 2018, in southern Slovakia (Zúbrik
et al., 2019). A screening in south-eastern Austria in September
2019 conrmed its occurrence at 21 sites (Sallmannshofer et al.,
2019). Subsequent to the rst records, fast range expansions
were reported from almost all the countries (Csepelényi et al.,
2017a; Simov et al., 2018). It should also be noted that the
temporal sequence of the rst records in different countries does
not necessarily reect a real pattern of the spread relating to
time. It is more likely related to the timing of the intensive
search after the species appeared in the given country. The
countries where and the years when OLB was detected rst are
shown in Fig. 1. The northernmost known record (N48.510889;
E22.051056) in September 2018 is from eastern Slovakia (Zúbrik
et al., 2019). Population genetic studies may clarify the starting
point and routes of the invasion (Estoup & Guillemaud 2010;
Cristescu 2015). Although OLB adults can actively y and they
can also be passively dispersed by wind, their long-term dispersal
is generally related to international road and rail trafc. The
rst infested locations in a given region were often found at
resting places near motorways or along rail lines (Gy. Csóka, B.
Hrasovec, D. Jurc & M. Jurc, unpublished observations).
By autumn 2016, the total area of invaded oak forests was
about one million hectares in Russia, of which approximately 0.4
© 2019 The Royal Entomological Society, Agricultural and Forest Entomology, doi: 10.1111/afe.12362

Area expansion and host range of the oak lace bug 3
Figure 1 Countries where the invasion of OLB has been detected with the year of the first records. [Colour figure can be viewed at wileyonlinelibrary.com].
million was severely infested (oak crowns in large groups or in
whole forest blocks suffered early discoloration exceeding 50%
level). The total extent of the outbreak areas in 2017 exceeded
1.3 million hectares in the oak forests of the Krasnodar Territory
and the Republic of Adygea. Currently, the bug has spread to
all the oak forests of the Black Sea coast, of the Krasnodar Krai
region, from Anapa to the state border. There is still no indication
that OLB has reached its potential distribution limits in Europe
and Asia.
In the present study, we summarize the present information
available on the range expansion in Europe and the host range of
the accidentally introduced and rapidly spreading invasive North
American oak lace bug. To predict its further potential regarding
hosts use in the invaded range, and the risk of its further area
expansion, we checked 48 oak species in 20 sentinel gardens
in seven countries between 2013 and 2018. These gardens can
provide valuable data on the host range of non-native pests or
pathogens (Roques et al., 2017; Vettraino et al., 2017). The data
on potential host use are very important with respect to evaluating
and predicting the potential to spread and cause damage.
Materials and methods
We have been collecting data intensively on host use from 2013
onwards in 20 sentinel gardens (i.e. botanical gardens and arbore-
tums) in seven countries (Croatia, Hungary, Italy, Romania, Ser-
bia, Slovakia, Slovenia) and forest stands in eleven ones (Bosnia
and Herzegovina, Bulgaria, Croatia, Hungary, Italy, Romania,
Russia, Serbia, Slovakia, Slovenia and Turkey). A list of the
sentinel gardens is provided in Table 2 and illustrated in Fig. 2.
In total, 15 sentinel gardens were located in an area already
invaded by the oak lace bug, and ve of them were outside of
the presently known range. These ve (two in Hungary, two
in Slovakia and one in Slovenia) were also checked for the
presence of OLB because we consider arboretums and botanical
gardens as potential ‘hot spots” of non-native insects and early
detection points. We assumed that invasive OLB might appear
in such places even far from the core invaded area. We also
collected information from the oak stands of the countries where
the presence of OLB was known for at least 2years. Although
the discolouration of the infested leaves is typical, we always
checked the affected trees for presence of adults, moulted skins of
larvae and egg clusters. Together, these can provide unequivocal
signs of a plant being utilized as a host. We did not consider a
tree species as a host if only adults were found on it. As an easily
and passively spreading species, OLB can often land and exist
on plants that are not suitable hosts.
The overwintered adults can be found on the underside of
leaves from April. Egg bunches are present from early May, with
larvae appearing later in May. Because OLB may have three
overlapping generations per season, all developmental stages are
noted on the foliage from June until October.
The arboretums and botanical gardens in Hungary were visited
two to six times, most of the sentinel gardens outside this
country were visited once (Table 2). The surveys (both in sentinel
gardens and autochthonous oak stands) were made once a year
from mid-July to late September. By this time, the symptoms
become easily noticeable and unambiguous. Sample branches
were regularly cut using long-handled loppers to check the
presence of the different developmental stages.
© 2019 The Royal Entomological Society, Agricultural and Forest Entomology, doi: 10.1111/afe.12362

4G. Csóka et al.
Table 2 List of the sentinel gardens (botanical gardens and arboretums) surveyed between 2013 and 2018 in seven countries
Number Name Coordinates Year(s) visited
Croatia
1Lisi
ˇ
cine N45.656667; E17.501944 2017
2 Zagreb N45.805000; E15.970556 2017
Hungary
3 Alcsútdoboz N47.423333; E18.591944 2017
4 Budapest N47.480833; E19.038333 2017
5Erd
˝
otelek N47.689722; E20.313611 2017
6 Gödöll ˝
o N47.567500; E19.383889 2015– 2018
7 Kecskemét N46.915833; E19.655556 2015 –2017
8 Püspökladány N47.334444; E21.090833 2015– 2018
9Sárvár N47.253119; E16.941489 2016– 2018
10 Sopron N47.680161; E16.573414 2016– 2018
11 Szarvas N46.875556; E20.529444 2013– 2017
12 Tiszaigar N47.527500; E20.806111 2017– 2018
13 Tiszakürt N46.888611; E20.118889 2014–2017
14 Vácrátót N47.707778; E19.234444 2013– 2017
Italy
15 Padua N45.399167; E11.880278 2017
Romania
16 Macea N46.382222; E21.307222 2015– 2016
Serbia
17 Belgrade N44.815833; E20.473333 2017
Slovakia
18 Malacky N48.439028; E17.030639 2017
19 Topolcianky N48.422306; E18.413917 2017
Slovenia
20 Vol ˇ
cji Potok N46.191178; E14.612783 2017
aHighlighted rows indicate locations where oak lace bug has not yet been found.
Figure 2 Locations of the 20 sentinel gardens surveyed. Black dots represent locations where oak lace bug has been found, empty circles represent
locations where oak lace bug has not yet been found. For site numbers, see Table 1.
© 2019 The Royal Entomological Society, Agricultural and Forest Entomology, doi: 10.1111/afe.12362

Area expansion and host range of the oak lace bug 5
The number of locations and of trees from different oak species
varied depending on the species. The oaks native in the region
were regularly sampled (>10) and, at many locations (>10), the
most exotic ones were generally rare and restricted to few places.
Although specimens of Q. robur, for example, were present as
a number of individual trees in most of the botanical gar-
dens/arboretums surveyed, only single individual trees of some
other species (i.e. Quercus aliena,Quercus gambelii,Quercus
imeretina, etc.) were available at one site only. This would make
the statistical analysis of host preference rather difcult.
Oak stands were also surveyed in 10 countries (Bosnia and
Herzegovina, Bulgaria, Croatia, Hungary, Italy, Romania, Rus-
sia, Serbia, Slovenia and Turkey). The levels of infestation were
classied as described below. The number of oak stands that
were surveyed cannot be given precisely, although the total area
reaches several thousand hectares. In different native oak stands,
regularly no survey of single trees was necessary because, in
most cases, larger groups of them or even whole stands were
severely infested, providing easily detectable symptoms. We
categorized the infestation level on a 0–3 scale. The scale is
described as:
0: No symptoms.
1: Symptoms/different developmental stages of OLB are spo-
radic, restricted to single leaf or smaller groups of them and can
only be found with targeted, intensive search.
2: Symptoms/different developmental stages of OLB are found
along whole branches that can easily be spotted on the tree.
3: Symptoms/different developmental stages of OLB cover
whole trees or groups of them, sometimes even extensive stands
of many hectares. Heavily infested trees/stands can be safely
spotted from larger distance, or for instance with drones.
Results
Oak hosts
We checked 48 different oak species in 20 sentinel gardens
in seven countries. The presence of OLB was recorded at 15
locations in ve countries (Croatia, Hungary, Italy, Romania
and Serbia). In total, 27 out of 48 oak species were proved
to be suitable OLB hosts. They are listed in Table 3. Only the
locations with recorded presence of OLB are included. Of these
27, 15 were globally new host records for OLB, as underlined
in Table 3. The share of each intrageneric taxonomic unit from
genus Quercus can be seen in Fig. 3. Out of 29 species surveyed
in section Quercus (white oaks), 23 (79.3%) can be hosts of
the OLB, four out of the ve ones (80%) belonging to section
Cerris are suitable for it and three of them were heavily infested
at almost all locations. No symptoms were recorded on any of
the North American red oaks within the section Lobatae and no
species in the Ilex group (Mediterranean evergreen oaks) showed
some infestation (Table 3).
In forest stands of the 10 countries involved in the present
study, we found 11 species of oaks (autochthonous in the given
country) infested by OLB at different levels (Fig. 4 and Table 4).
All species showed signs of heavy infestation in some countries.
So far, outbreak populations have most often been detected in Q.
robur,Quercus frainetto,Quercus petraea and Quercus cerris
stands.
Non-oak hosts
Thirty-three species of non-oak woody hosts belonging to 10
plant families have been recorded in eight countries. These host
records are provided in Table 5. Many of them are new host
records.
Discussion
The widely accepted host species of OLB belong to the two
major sections of the genus Quercus (Quercus and Cerris).
The taxonomic relatedness of the oak species included in the
present study appears to be a more important factor than their
native ranges. White oaks (section Quercus) were infested
almost independently from their native ranges, except for the
North American ones, naturally present on the western coast
of the U.S.A. One species (Q. gambelii) showed a low level of
infestation, the other one (Quercus garryana) was not attacked.
However, it should be noted that these species were represented
by only single (and small) tree at only one botanical garden
(Vácrátót, Hungary). Heavily infested species can be found both
among the North American (Quercus alba,Quercus macrocarpa,
etc.), European (Q. robur,Q. petraea, etc.) and even species with
Far East origin (Quercus dentata,Quercus mongolica). Only one
species from the section Cerris (Quercus acutissima –nativeto
Eastern Asia) was unattacked, although this species was only
surveyed at one place (Vácrátót, Hungary).
From our observations, it is quite clear that the red oaks
(section Lobatae) are not suitable hosts for OLB. None of these
species (with one exception, see below) showed any signs of
infestation, although most of them grow in a rather exposed
environment, surrounded by heavily infested suitable hosts. We
found only a very small (less than 1 cm2) spot with symptoms
on Quercus imbricaria (Szarvas, Hungary, 2015), although dead
larvae were surrounding it; therefore, we do not consider this
oak species as a suitable host. These results coincide with the
observations of Morrill (1903), who reported three species of
red oaks (Quercus coccinea,Quercus ilicifolia and Quercus
laurifolia) remained unaffected ‘although they stood so near to
badly infested trees that their branches touched in some cases’.
Trieff (2002) found OLB adults in the canopy of Q. rubra during
a knockdown fogging experiment in the U.S.A. However, the
presence of adults itself does not conrm that Q. rubra is a
suitable host, as noted earlier. Our results are also similar to
those of Bernardinelli (2006a, b) who found the North American
Q. rubra as unsuitable versus native European oaks that are
suitable.
None of the three oak species belonging to the Ilex group had
any feeding symptoms in the arboretums and botanical gardens
visited. However, in a sentinel experiment in Croatia (seedlings
were placed under a heavily infested Q. robur stand), even these
species (Quercus ilex and Quercus coccifera) showed sporadic
small symptoms of sucking. Therefore, it can be concluded
that OLB’s preferred hosts are present in the majority of the
Europe. It should also be noted again that many central and
even eastern Asian oaks (including natives of Japan, Korea
and China) are suitable OLB hosts. These are globally new
host records for OLB, meaning that eastbound range expansion
of OLB is unlikely to be restricted by host availability. In
surveys at the stand level, not surprisingly, Q. cerris,Q. petraea,
© 2019 The Royal Entomological Society, Agricultural and Forest Entomology, doi: 10.1111/afe.12362

6G. Csóka et al.
Table 3 Oak lace bug oak hosts recorded in 15 sentinel gardens (arboretums and botanical gardens) in five countries
Country
Croatia Hungary
Location
Oak (Quercus)
species Native range Lisi ˇ
cine Zagreb Alcsútdoboz Budapest Erd ˝
otelek Gödöll ˝
o Kecskemét Püspökladány Szarvas Tiszaigar Tiszakürt Vácrátót
Italy
Padua
Romania
Macea
Serbia
Belgrade
Section Quercus
Quercus alba L.
1753*
Eastern North
America
−−− − 3−− − 32 −3−− −
Quercus aliena
Blume 1850
Central China,
Korea, Japan
−−− − − − − − − − − 2−− −
Quercus bicolor
Wild 1801*
North-eastern
U.S.A.,
Southern
Canada
−−− − − − − − − 2−12+−
Quercus dentata
Thunb. 1784
Japan, Korea,
China
0−− − − − 3−−−−2−− −
Quercus faginea
Lam. 1783
Spain, Portugal,
the Baleares,
Algeria,
Morocco
−−− − − − − − − − − 1−− −
Quercus frainetto
Ten. 1813
Southern Italy, The
Balkans, south
of the Black Sea
11−2−−3−−−32−− 2
Quercus gambelii
Nutt. 1848
South-western
U.S.A., northern
Mexico
−−− − − − − − − − − 1−− −
Quercus garryana
Dougl. ex Hook.
1839
Western U.S.A.
(Pacific coast)
−−− − − − − − − − − 0−− −
Quercus
hartwissiana
Steven 1857
Southern and
eastern
Bulgaria, Asia
Minor,
Caucasus
−−− − − − − − − 3−0−− −
Quercus iberica
Steven ex Bieb.
1808
Transcaucasus,
Balkans,
north-western
Turkey, Crimea,
northern Iran
−−− − − − − − − − − 3−− −
Quercus imeretina
Steven ex
Woronov 1936
Western
Caucasus
−−− − − − − − − − − 3−− −
© 2019 The Royal Entomological Society, Agricultural and Forest Entomology, doi: 10.1111/afe.12362

Area expansion and host range of the oak lace bug 7
Table 3 Continued
Country
Croatia Hungary
Location
Oak (Quercus)
species Native range Lisi ˇ
cine Zagreb Alcsútdoboz Budapest Erd ˝
otelek Gödöll ˝
o Kecskemét Püspökladány Szarvas Tiszaigar Tiszakürt Vácrátót
Italy
Padua
Romania
Macea
Serbia
Belgrade
Quercus lobata
Née 1801
California −−− − − − − − − − − 0−− −
Quercus lyrata
Walt. 1788
South-eastern
U.S.A., from New
Jersey to Texas
−−− − − − − − − − − 3−− −
Quercus
macranthera
Fisch. & C.A.Mey
ex Hohen 1838
Caucasus, northern
Iran, south of
Caspian Sea,
Armenia
−−− − − 33 −33 −1−+ −
Quercus
macrocarpa
Michx. 1801*
Eastern North
America
−−3−3−33 −233−+ 3
Quercus mannifera
Lindl. 1840
From eastern Turkey
to northern Iran
−−− − − − − − − − − 0−− −
Quercus mongolica
Fisch. ex Ledeb.
1850
China, Japan,
Korea, Mongolia,
eastern Russia,
Sachaline Islands
−−− − − − − − − 3−3−− −
Quercus
muehlenbergii
Engelm. 1887*
Eastern and central
U.S.A., Canada,
north-eastern
Mexico
−−− − − − − − − − − 0−− −
Quercus
pedunculiflora
K.Koch 1849
Asia Minor,
Caucasus,
Balkans
−−2−−−− − 3−−−−−−
Quercus petraea
(Matt.) Liebl.
1784
Europe, western
Asia,
112 −32−− −−33−+ −
Quercus
polymorpha
Schltdl. & Cham.
1830
Atlantic slope of
Mexico,
Guatemala,
south-western
Texas
−−− − − − − − − − − 0−− −
Quercus pontica
K.Koch 1849
Caucasus, Armenia,
around Black
Sea, northern
Tur k e y
−−− 3−−2−3−32−− −
© 2019 The Royal Entomological Society, Agricultural and Forest Entomology, doi: 10.1111/afe.12362

8G. Csóka et al.
Table 3 Continued
Country
Croatia Hungary
Location
Oak (Quercus)
species Native range Lisi ˇ
cine Zagreb Alcsútdoboz Budapest Erd ˝
otelek Gödöll ˝
o Kecskemét Püspökladány Szarvas Tiszaigar Tiszakürt Vácrátót
Italy
Padua
Romania
Macea
Serbia
Belgrade
Quercus prinoides
Willd. 1801*
Eastern U.S.A. −−− − − − − − − − − 1−− −
Quercus
pubescens Willd.
1805
Southern Europe,
western Asia,
Caucasus
−−− 0−−− − −3−−−−−
Quercus pyrenaica
Willd. 1805
Atlantic Coast
(France, Spain,
Portugal,
Morocco)
−−− − − − − − − − − − −+ −
Quercus robur L.
1753
Europe,
south-western
Asia, northern
Africa
333 −333 3 33333+3
Quercus serrata
Murray 1784
China, Taiwan,
Japan, Korea
−−− − − − − − − − − 0−− −
Quercus stellata
Wangenh. 1787*
Central and
south-eastern
U.S.A.
−−− − − − − − − 2−0−− −
Quercus virgiliana
Ten. 1835
Southern Europe,
eastern Corsica,
Italy, to the Black
Sea
−−1−−−− − −−−−−−−
Section Cerris
Quercus acutissima
Carruth. 1861
Japan, northern
China, Korea,
Himalaya,
Cambodia,
Vietnam, Thailand
−−− − − − − − − − − 0−− −
Quercus cerris L.
1753
Southern and
south-eastern
Europe, Asia
Minor
−13 3 3 2 2 3 3 3 3 3 −+ −
Quercus libani
G.Olivier 1801
Syria, Lebanon, Asia
Minor
−−− − − − 33 −− 31−− −
Quercus trojana
Webb 1839
South-western Italy,
Balkans, Asia
Minor
−−− − − − − − 3−−−−−3
© 2019 The Royal Entomological Society, Agricultural and Forest Entomology, doi: 10.1111/afe.12362

Area expansion and host range of the oak lace bug 9
Table 3 Continued
Country
Croatia Hungary
Location
Oak (Quercus)
species Native range Lisi ˇ
cine Zagreb Alcsútdoboz Budapest Erd ˝
otelek Gödöll ˝
o Kecskemét Püspökladány Szarvas Tiszaigar Tiszakürt Vácrátót
Italy
Padua
Romania
Macea
Serbia
Belgrade
Quercus variabilis
Blume 1851
Japan, China, Korea,
Taiwan, Tibet
0−− − − − − − − − − 1−− −
Section Lobatae
Quercus buckleyi
Nixon & Dorr 1985
Texas, Oklahoma −−− − − − − − − 0−0−− −
Quercus coccinea
Münchh. 1770
Eastern U.S.A. −−0−00−− 0−00−− −
Quercus ilicifolia
Wangenh. 1787
Eastern U.S.A. −−− − − − − − 0−−−−−−
Quercus imbricaria
Michx. 1801
South-eastern and
central U.S.A.
−−− − 00−− −000−− −
Quercus laurifolia
Michx. 1801
South-eastern Virginia
to southern Florida
and Texas
−−− − − − − − − 0−−−−−
Quercus laurina
Humb. & Bonpl.
1809
Mexico, Guatemala −−− − − − − − − − − 0−− −
Quercus palustris
Münchh. 1770
North-eastern U.S.A. 0 0 0 0 0 0 0 0 0 0 0 0 −− 0
Quercus phellos L.
1753
South-eastern U.S.A. 0 0 −−−−−− −−0−−− −
Quercus rubra L.
1753
South-eastern
Canada, eastern
U.S.A.
000 0 0 0 0 0 0 0 0 0 −− −
Quercus shumardii
Buckley 1860
Southern Ontario;
eastern and central
U.S.A.
−−− − − − − − − − 0−−− −
Quercus velutina
Lam. 1785
Eastern U.S.A. −−− − − − − − − 00−−− −
Ilex group
Quercus coccifera L.
1753
Mediterranean region 0 −− 0−−− − −−−−−−0
Quercus ilex L. 1753 Southern Europe −−− 0−−− − 0−− −0−−
Quercus
phillyreoides
A.Grey 1859
Southern Japan;
central China;
Korea
−−− − − − − − − 0−−−−−
Oak names and native ranges are taken from http://oaks.of.the.world.free.fr. The oaks recorded as host in a native range are marked with an asterisk (*). The globally new host records are underlined. +,
a recorded host but with no information on the infestation level. The Romanian data are based on Don et al. (2016).
© 2019 The Royal Entomological Society, Agricultural and Forest Entomology, doi: 10.1111/afe.12362

10 G. Csóka et al.
Figure 3 Number of oak species in different intrageneric classifications with/without oak lace bug (OLB) records in 15 sentinel gardens in five countries.
Figure 4 Number of countries (out of 10), where a given oak species was recorded in forest stands with different infestation levels (1– 3). Data are
extracted from Table 4.
Quercus pubescens and particularly Q. robur were recorded as
being most heavily attacked in all countries. These species are
widely distributed and are among the most abundant on trees
in the surveyed region. Summed up, only these four species are
covering together more than 10 million hectares of forested land
in Europe.
Climate may inuence signicantly the establishment and
further spread of the non-native invasive insects. The milder and
shorter winters could affect the higher overwintering survival and
the timing of spring emergence, resulting more generations per
year (Berzitis et al., 2017; Papp et al., 2018; Smith et al., 2018;
War d et al., 2018). Bernardinelli (2006b) compared climatic
conditions of the native North American range and Europe and
concluded that most of the latter is likely to provide suitable
conditions for the establishment of OLB. A recent study by
Csepelényi et al. (2017b) found that the relatively cold winter
of 2016/2017 did not cause high overwintering mortality (not
exceeding 50%) at two locations in south-eastern Hungary.
The long-term impact of the OLB damage is not yet known,
although there are good reasons to assume that the ‘chronic’
© 2019 The Royal Entomological Society, Agricultural and Forest Entomology, doi: 10.1111/afe.12362

Area expansion and host range of the oak lace bug 11
Table 4 Oak host records in forest stands in 10 countries (data collected by the authors)
Country oak species
Bosnia and
Herzegovina Bulgaria Croatia Hungary Italy Romania Russia Serbia Slovenia Turkey
Quercus castaneifolia C.A.Meyer 1831 ------3
a-- -
Quercus cerris L. 1753 -323233
a3- -
Quercus frainetto Ten. 1813 -3--22----
Quercus hartwissiana Steven 1857 -3----3
a-- -
Quercus infectoria G.Olivier 1801 ---------3
Quercus macranthera Fisch. & C.A.Mey. ex Hohen 1838 ---------3
Quercus pedunculiflora K.Koch 1849 -3---2----
Quercus petraea (Matt.) Liebl. 1784 33-22233-3
Quercus polycarpa Schur 1851 -3--------
Quercus pubescens Willd. 1805 -3112-3
a-- 3
Quercus robur L. 1753 3333333
a32 3
aData from Neimorovets et al. (2017).
Table 5 Non-oak woody hosts recorded in eight countries with different levels (1– 3) of infestation (data collected by the authors)
Country
Species Bulgaria Croatia Hungary Italy Romania Russia Serbia Turkey
Sapindaceae
Acer campestre L. 1753 - 1 1 - - - - -
Koelreuteria paniculata Laxm. 1772 - - 1 - - - - -
Cannabaceae
Celtis occidentalis L. 1753 - - - - - - 2 -
Fagaceae
Castanea sativa Mill. 1768 2 - - - - - - -
Fagus sylvatica L. 1753 - 1 1 - - - - -
Betulaceae
Carpinus betulus L. 1753 - 1 1 - - - - -
Corylus avellana L. 1753 - 1 2 3 - - 2 -
Corylus colurna L. 1753 - 1 2 - - - - -
Cornaceae
Cornus sanguinea L. 1753 - 1 - - - - - -
Rosaceae
Chaenomeles japonica (Thunb). Lindl. Ex Spach 1834 - - - - - - 2 -
Crataegus coccinea L. 1753 - - - 2 - - - -
Crataegus monogyna Jacq. 1775 - - - - - - 2 -
Crataegus spp. - - - - - - - -
Kerria japonica (L.) DC. 1818 - - 1 - - - - -
Prunus lusitanica L. 1753 - - - 1 - - - -
Prunus serotina Ehrh. 1784 - 1 3 - - - - -
Prunus serrulata Lindl. 1830 - - 2 - - - 2 -
Prunus spinosa L. 1753 - - 2 - - - - -
Prunus subhirtella Miq. 1865 - - - 1 - - - -
Pyrus communis L. 1753 - 1 - - - - 2 -
Rosa canina L. 1753 1 - 1 - - - - -
Rosa spp. 1 - 1 - - - - 1
Rubus caesius L. 1753 1 2 3 - - - 3 -
Rubus spp. 1 - - - - - - -
Sorbus aria (L.) Crantz 1763 - - 1 - - - - -
Sorbus scandica Fr. 1817 - - - - - - 3 -
Sorbus torminalis (L.) Crantz 1763 - 1 - - - - - -
Ulmaceae
Ulmus glabra Huds. 1762 - - 2 - - - - -
Ulmus minor Mill. 1768 - 2 2 - - - - -
Ulmus spp. - - - - 1 3 - -
Malvaceae
Tilia cordata Mill. 1768 - - 2 - - - - -
Tilia platyphyllos Scop. 1771 - - 3 - - - 1 -
Tilia spp. - - - - 1 - - -
New host records are underlined.
© 2019 The Royal Entomological Society, Agricultural and Forest Entomology, doi: 10.1111/afe.12362

12 G. Csóka et al.
infestations will negatively inuence, in a signicant manner,
the growth, health status and fecundity of the oak stands that
already suffer from both the direct and indirect effects of cli-
mate change (Csóka, 1997; Csóka et al., 2009). The heavily
attacked leaves lose most of the chlorophyll in their upper
surface, whereas the one in their underside tissues remains
relatively unharmed. This is particularly important in terms
of photosynthesis because approximately 80% of this process
takes place in the palisade clorenchyma of the leaf upper
surface (Lambers et al., 1998). According to a recent Ser-
bian study, the rate of photosynthetic and transpiration activ-
ity, as well as the stomatal conductance, decreased by 58.84%,
21.66% and 35.71%, respectively, compared with non-infested
plants (Nikoli´
cet al., 2019). An unpublished study in Hun-
gary resulted in a similar loss regarding the photosynthetic
activity in late June, at above 50% of the degree of leaf dis-
colouration (I. Mészáros, personal communication). Further tar-
geted experiments should be established to clarify the long-term
impact of OLB on the health, growth and fecundity of the
infested oaks.
It is also still unknown how the mass presence of OLB
will inuence the extremely species-rich herbivorous insect
communities thriving on European oaks. Only in Hungary, at
least 650 herbivore insect species were recorded feeding on oaks
and more than 40% of them are strictly specialists (Csóka, 1998,
2006; Csóka & Szabóky, 2005). Mitchell et al. (2019) reported
2300 species associated with Q. petraea/robur in the U.K., of
which 326 were found to be obligate associates (only found on
these two oak species). It has already been reported in Hungary
that larvae of oak specialist notodontids (Harpya milahuseri and
Drymonia querna) starve and then die on leaves severely infested
by OLB (unpublished observations).
Our survey in sentinel gardens and forest stands must be
considered as an early but evidently ‘snapshot’ warning. By
this, we mean that both the number of affected oak species and
the level of infestation are likely to grow in the near future,
particularly in most recently invaded areas. The host range,
based on our results, could be considered as a ‘minimum’ one.
The datasets collected during our survey allow us to predict a
further large-scale spread and even a wider host range within both
Europe and Asia.
Insect outbreaks sometimes provoke otherwise unexpected
host shifting together with range expansion (Castagneyrol et al.,
2016). As a consequence, we recorded 28 plant species within
eight families as occasional hosts of OLB in eight recently
invaded countries (Table 5). The family of Rosaceae was repre-
sented by 15 species; Betulaceae by three; Fagaceae, Ulmaceae,
Sapindaceae and Malvaceae by two; and the other two families
(Cannabaceae and Cornaceae) by one each. Genera Corylus and
Rubus were infested in the highest number of countries, and reg-
ularly with highest infestation rates. New host records are under-
lined in Table 5. However, the infestation levels were much lower
on a regular basis than those on oaks at the same locations. Nev-
ertheless, host shifting may further facilitate the spread of OLB
even where the landscape is strongly fragmented and the oak
forests do not adjoin each other.
The recent explosive spreads and outbreaks of OLB in several
European countries show that the dispersal ability and the
potential damage by the species cannot be properly evaluated
upon its arrival as a non-native. Some species do not show
immediate invasiveness, and they start to spread rapidly only
after a latent period of different lengths (Crooks 2005; Jaric et al.,
2018). The favourable weather conditions (likely mild winters
allowing high overwintering survival) in several consecutive
years may play a ‘triggering’ role in the acceleration of the
expansion and the fast increase in abundance, as also assumed
in the case of OLB.
As a result of large-scale and potentially severe effects of
OLB in the Eurasian oak forests, further studies, preferably
international, are necessary.
Acknowledgements
The work of the Hungarian participants was supported by
the COST Action FP1401 – ‘Global Warning’ and the OTKA
128008 research project sponsored by the National Research,
Development and Innovation Ofce. Research in Croatia was by
the two projects funded by Croatian forests LLC. The Ministry
of Education, Science and Technological Development gave sup-
port to the work in Serbia, Grant number III43002. In Slovenia,
the research was conducted through the project V4-1439 Devel-
opment of new methods of detection, diagnostics and prognosis
for non-native organisms harmful to forest 2014–2017 and pro-
gramme groups P4-0059 Forest, forestry and renewable forest
resources and P4-0107 Forest biology, ecology and technology.
Special thanks are given regarding the Bulgarian data provided
by Georgi Georgiev, Plamen Mirchev, Margarita Georgieva (For-
est Research Institute), Snezhana Grozeva (Institute of Biodi-
versity and Ecosystem Research) and Nikolay Simov (National
Museum of Natural History). The authors thank Dominique
Fournier from Services Linguistiques DF (Canada) for linguis-
tic and editorial improvements made to the manuscript submitted
for publication.
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Accepted 21 October 2019
© 2019 The Royal Entomological Society, Agricultural and Forest Entomology, doi: 10.1111/afe.12362