Invasive behaviour of oak lace bug in forest ecosystems: a comparative analysis between thermophilous and mesophilous oak forests

Abstract

Forest ecosystems provide invaluable ecological, economic, and social benefits,
making them essential for global well-being. However, these ecosystems face
various threats, including biological invasions by alien species. Among these,
the oak lace bug (OLB), an invasive North American insect, has rapidly spread
in Europe, impacting oak forests and raising concerns about its adaptation
to new environments. OLB feeds on the undersides of oak leaves, extracting
sap and causing chlorotic discoloration. Severe infestations lead to premature
defoliation, increased susceptibility to diseases or pests and can also result in
a substantial reduction in photosynthesis activity. This study aims to analyse
OLB’s invasive behaviour in Romanian forest ecosystems, with a specific focus
on the differences between thermophilous and mesophilous oak forests. The
analysis covers 6 years of data and reveals critical insights. In the initial 4 years,
OLB predominantly inhabited the extracarpathian regions of Romania, with
concentrated presence in the southern, western, and northwestern areas.
Forest ecosystems mainly affected between 2017 and 2020 were characterized
by thermophilous oak forests in southern and western regions. However, in
the last 2 years (2021–2022), OLB presence increased, particularly in lowland
ecosystems, albeit with reduced damage intensity. The analysis also unveiled an
adaptation and expansion of OLB in mesophilous forest ecosystems. Climatic
factors, specifically temperature and precipitation, significantly influenced OLB’s
behaviour, points with severe attacks exhibiting specific climatic conditions. In
summary, this study provides crucial insights into OLB’s behaviour, emphasizing
the role of climatic and environmental factors in its invasive tendencies.

Full text

Frontiers in Forests and Global Change 01 frontiersin.org
Invasive behaviour of oak lace
bug in forest ecosystems: a
comparative analysis between
thermophilous and mesophilous
oak forests
FlaviusBălăcenoiu 1, ConstantinNețoiu
1, DragoșToma
1,2* and
IonCătălinPetrițan 2
1 National Institute for Research and Development in Forestry “Marin Dracea”, Voluntari, Romania,
2 Faculty of Silviculture and Forest Engineering, Transilvania University of Brașov, Brașov, Romania
Forest ecosystems provide invaluable ecological, economic, and social benefits,
making them essential for global well-being. However, these ecosystems face
various threats, including biological invasions by alien species. Among these,
the oak lace bug (OLB), an invasive North American insect, has rapidly spread
in Europe, impacting oak forests and raising concerns about its adaptation
to new environments. OLB feeds on the undersides of oak leaves, extracting
sap and causing chlorotic discoloration. Severe infestations lead to premature
defoliation, increased susceptibility to diseases or pests and can also result in
a substantial reduction in photosynthesis activity. This study aims to analyse
OLB’s invasive behaviour in Romanian forest ecosystems, with a specific focus
on the dierences between thermophilous and mesophilous oak forests. The
analysis covers 6 years of data and reveals critical insights. In the initial 4 years,
OLB predominantly inhabited the extracarpathian regions of Romania, with
concentrated presence in the southern, western, and northwestern areas.
Forest ecosystems mainly aected between 2017 and 2020 were characterized
by thermophilous oak forests in southern and western regions. However, in
the last 2 years (2021–2022), OLB presence increased, particularly in lowland
ecosystems, albeit with reduced damage intensity. The analysis also unveiled an
adaptation and expansion of OLB in mesophilous forest ecosystems. Climatic
factors, specifically temperature and precipitation, significantly influenced OLB’s
behaviour, points with severe attacks exhibiting specific climatic conditions. In
summary, this study provides crucial insights into OLB’s behaviour, emphasizing
the role of climatic and environmental factors in its invasive tendencies.
KEYWORDS
biological invasions, forest health, oak forests, habitat disruption, ecological resilience
1 Introduction
Forest ecosystems have immeasurable value for our planet, providing a multitude of
ecological, social, and economic benets. In terms of ecological benets, forests play a vital
role in climate regulation at both local and global levels, contributing to the mitigation of
weather phenomena, regulating the hydrological cycle, and safeguarding watersheds. Forest
ecosystems hold signicant ecological importance due to the diversity of functional groups
OPEN ACCESS
EDITED BY
Miglena Zhiyanski,
Bulgarian Academy of Sciences, Bulgaria
REVIEWED BY
Muhammad Waheed,
University of Okara, Pakistan
Jovan Dobrosavljević,
University of Belgrade, Serbia
*CORRESPONDENCE
Dragoș Toma
dragost93@gmail.com
RECEIVED 24 October 2023
ACCEPTED 22 December 2023
PUBLISHED 08 January 2024
CITATION
Bălăcenoiu F, Nețoiu C, Toma D and
Petrițan IC (2024) Invasive behaviour of oak
lace bug in forest ecosystems: a comparative
analysis between thermophilous and
mesophilous oak forests.
Front. For. Glob. Change 6:1326929.
doi: 10.3389/gc.2023.1326929
COPYRIGHT
© 2024 Bălăcenoiu, Nețoiu, Toma and
Petrițan. This is an open-access article
distributed under the terms of the Creative
Commons Attribution License (CC BY). The
use, distribution or reproduction in other
forums is permitted, provided the original
author(s) and the copyright owner(s) are
credited and that the original publication in
this journal is cited, in accordance with
accepted academic practice. No use,
distribution or reproduction is permitted
which does not comply with these terms.
TYPE Original Research
PUBLISHED 08 January 2024
DOI 10.3389/gc.2023.1326929

Bălăcenoiu et al. 10.3389/gc.2023.1326929
Frontiers in Forests and Global Change 02 frontiersin.org
within them (Haq et al., 2023a), as well as for their capacity to
sequester carbon (Haq etal., 2023b). ey serve as habitats for a
remarkable diversity of species and constitute reservoirs of genetically
important information, with many of these species yet to bediscovered
(Pearce, 2001). Some of these ecosystem services, such as climate
regulation, soil formation, water resource management, and water
supply, make signicant contributions to human society, even in the
absence of direct monetary valuation (Costanza et al., 1997).
Furthermore, the total annual value of ecosystem services globally
averages around 33 trillion USD, with global forests contributing
approximately 969 USD per hectare (Costanza etal., 1997).
From an economic standpoint, forests are fundamental for
poverty eradication and economic development, providing food, ber,
wood, and other essential forest products for sustenance and income
generation (Jenkins and Schaap, 2018). In terms of the social benets
of ecosystem services provided by forests, they manifest in ensuring
human health and well-being, providing a high-quality living
environment, oering outdoor recreation and tourism opportunities,
aesthetic values, facilitating outdoor education, and promoting
knowledge about forests and the environment. Additionally, forests
serve as sources of intellectual and spiritual inspiration, contributing
to cultural identity and our cultural heritage (de Groot etal., 2010).
Disturbances caused by factors such as insect outbreaks,
phytopathogens, wind, precipitation, or wildres can aect the ability
of forest ecosystems to fulll multiple functions. In addition to these
factors, forest ecosystems are threatened by various phenomena,
including pollution, climate change (Lindner etal., 2010) and most
notably, biological invasions caused by alien species (Trumbore etal.,
2015). In the context of the global expansion of invasive species,
accelerated by processes of globalization, it is evident that invasions of
foreign species have generated diverse consequences for the
environment, economy, and human health (Pimentel etal., 2000;
Lovell etal., 2006; Meyerson and Mooney, 2007; Vilà etal., 2010, 2011;
Jeschke etal., 2013; Simberlo etal., 2013; Blackburn etal., 2014;
Hulme, 2014; Schindler etal., 2015). rough the forecast of forest
ecosystem health, the results could aid in the assessment and
evaluation of ecosystem goods and services (Haq etal., 2022). is, in
turn, might support the development of forest conservation plans,
aiming to restore the ecology in areas aected by invasions (Haq
etal., 2023c).
Among alien species with a signicant impact on ecosystems in
Europe and, consequently, Romania, Corythucha arcuata (Say, 1832)
(Hemiptera, Tingidae) stands out as an invasive insect of particular
relevance. Also known as the oak lace bug (OLB), this North
American-origin insect was rst reported in Europe in 2000, in Italy
(Bernardinelli and Zandigiacomo, 2000). is insect species feeds on
the underside of host leaves, typically oaks, by piercing the epidermis
and extracting cellular sap material (Mutun etal., 2009), resulting in
chlorotic discoloration of the leaves (Bernardinelli, 2006; Mutun etal.,
2009; Paulin etal., 2020). In cases of severe infestation, this pest can
cause premature defoliation of the host or increase its susceptibility to
various diseases or pests (Connell and Beacher, 1947), as well as aect
photosynthesis activity by up to 58.8% (Nikolic etal., 2019). Although
the general public and stakeholders in the forestry sector of countries
facing the invasion caused by OLB believe that the insect’s attack can
lead to tree mortality (Bălăcenoiu etal., 2021a) to our knowledge,
there is no research on the impact of the insect on local ecosystems
and biodiversity.
Regarding its invasion into the Eurasian territory, within just
2 years following its rst report, in 2002, the species was recorded in
both Switzerland (Forster etal., 2005), and Turkey (Mutun, 2003).
Due to its potential to cause signicant damage and its rapid spread,
OLB was included on the Alert List of the European and
Mediterranean Plant Protection Organization in March 2001 (EPPO,
2001) and remained on this list until 2007 (EPPO, 2007), when it
became evident that administrative eorts could not halt its expansion.
In 2012, the species was rst reported in Bulgaria (Dobreva etal.,
2013) and in 2013, its presence was conrmed in three other countries:
Hungary (Csóka etal., 2013), Croația (Hrašovec etal., 2013) și Serbia
(Pap etal., 2015; Poljaković-Pajnik etal., 2015). Furthermore, its
presence is currently documented in various other European countries
as a result of its invasion, including Russia (Neimorovets etal., 2017),
Romania (Don etal., 2016; Chireceanu etal., 2017), Albania (Csóka
etal., 2019), Slovenia (Jurc and Jurc, 2017), BosniaandHerzegovina
(Dautbašić et al., 2018), France (Streito et al., 2018), Ukraine
(Meshkova, 2022), Greece (Csóka etal., 2019), Slovakia (Zúbrik etal.,
2019), and Austria (Sallmannshofer etal., 2019).
Following the rst recording of the insect in several countries,
including Turkey, Hungary, Bulgaria, and Romania, the phenomenon
did not remain limited to the stage of appearance, with subsequent
reports conrming the other phases of a biological invasion, namely,
its spread and establishment within the respective territories (Mutun
etal., 2009; Csepelényi etal., 2017; Simov etal., 2018; Tomescu etal.,
2018). e invasion in many European countries is likely due to the
fact that the majority of European and Asian forests provide favourable
conditions for its establishment (Csóka etal., 2019). In 2019, the oak
lace bug infested an estimated combined area of over 1.7 million
hectares of oak forests in just ve European countries: Croatia,
Hungary, Romania, the European part of Russia, and Serbia (Paulin
etal., 2020). However, the chemical control method has not yielded
ecient results (Bălăcenoiu et al., 2021b). Nevertheless, trials
conducted in Turkey (Sönmez etal., 2016) and Croatia (Kovač etal.,
2020, 2021) provide a glimmer of hope for a potential future biological
control program for the insect.
Considering that oak forests in Romania constitute 16% of the
country’s forested area (NFI, 2018), their susceptibility to the invasive
oak lace bug (OLB) is of paramount importance. e scale of these
ecosystems makes them a critical component of Romania’s biodiversity
and ecological balance. Given the ndings of Tomescu etal. (2018),
which demonstrated that OLB had reached altitudes of 534 meters in
Romania just 2 years aer its initial report and had shown survival
inlocations where the average temperature of the coldest month was
0.8°C, this situation could potentially pose future challenges to
montane forest ecosystems. e aim of this study is to analyse the
invasive behaviour of the oak lace bug in the forest ecosystems of
Romania, with a particular focus on the dierences between
thermophilous oak forests and mesophilous oak forests. erefore, the
study aims to address two crucial questions: (i) Are there signicant
dierences in the invasive behaviour of the oak lace bug between these
environments (thermophilous and mesophilous), and if so, what are
these dierences? (ii) What role do climatic factors play in the
expansion and intensication of the oak lace bug invasion in the forest
ecosystems of Romania? By examining how this insect has evolved in
these distinct environments, our goal is to contribute to a deeper
understanding of the dynamics of biological invasion and its impact
on forest ecosystems.

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Frontiers in Forests and Global Change 03 frontiersin.org
2 Material and method
2.1 Data collection
To study the invasive behaviour of the Oak Lace Bug (OLB) in
the forest ecosystems of Romania, wefocused on monitoring the
temporal evolution of damage in the oak forests of Romania. Given
that the OLB was rst reported in the national forest fund starting
in 2016 (Tomescu etal., 2018), weestablished the reference period
for understanding the temporal evolution of damage caused by the
insect in oak forests in Romania as the interval between 2017
and 2022.
Information regarding the location and damage intensity
during this period was extracted from the internal databases of
the National Research and Development Institute for Forestry
“Marin Drăcea” pertaining to the status of attacks produced by
C. arcuata in Romanian oak forests. We employed the
methodology outlined in Tomescu et al. (2018) to gauge the
extent of insect attack. This involved a visual assessment of the
extent of foliage discoloration relative to the typical colour of oak
leaves on the host trees. The damage intensity was quantified
using percentages of discoloration in multiples of 5, with a range
spanning from 0% (indicating no attack) to 100% (indicating a
severe attack). To ensure clarity and consistency in our
assessments, weestablished a standardized scale with five degrees
of damage intensity (Figure1).
2.2 Mapping attacks produced by OLB
To highlight the relationship between the intensity of attacks and
the invaded ecosystem units, weconducted the mapping of damage
caused by OLB on the Forest Map of Romania – based on forest
ecosystem types (Doniţă etal., 2008).
In this manner, each forest where the damage caused by C. arcuata
was recorded was assigned a point of a specic colour corresponding
to the level of attack (See Figure1).
Maps throughout this paper were created using ArcGIS® 10.3
soware by Esri.
2.3 Description of studied forest ecosystem
formations
Our study focused on the analysis and characterization of a set of
forest ecosystems in Romania where OLB is present. ese ecosystem
formations were initially described by Doniţă et al. (2008) and
represent a diverse range of forest habitats that are of particular
importance to the biodiversity and ecological functioning of the
region. e ecosystem formations in which OLB was identied in
Romania are presented in Table1.
2.4 Climatic data
Due to the incompleteness of local climate data, weused gridded
climatic data (annual monthly temperature and average daily
precipitation) to generate the annual mean temperature, annual winter
temperature, overwinter temperature, annual total precipitation,
winter precipitation and overwinter precipitation, but also temperature
and precipitation during the growing season for each monitoring
point for each year of the 2017–2022 period. is dataset was
downloaded from the KNMI Climate Explorer (E-OBS, https://
climexp.knmi.nl/) and corresponds to interpolated data obtained from
measured values recorded by a dense network of local meteorological
stations, and gridded onto a 0.25° network (0.25° 1950-now: E-OBS
v25.0e Tg (Europe), 0.25° 1950-now: E-OBS v25.0e precip (Europe)).
E-OBS is a daily gridded observational dataset for main climatic
parameters (e.g., precipitation and temperature, used in current
research) in Europe based on ECA&D (European Climate Assessment
& Dataset) information and currently it is maintained and by the
Copernicus Climate Change Services. Weacknowledge the E-OBS
dataset from the Copernicus Climate Change Service (C3S, https://
surfobs.climate.copernicus.eu) and the data providers in the ECA&D
project.
1
More detail on interpolation method could be found in
Cornes etal. (2018). Wehave decided to use E-OBS dataset mainly
1 https://www.ecad.eu
FIGURE1
Standardized scale for assessing damage intensity through leaf discoloration.

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Frontiers in Forests and Global Change 04 frontiersin.org
due to higher provided resolution (0.25°) compared to of that other
similarly products existed on Europe level (>0.5°).
2.5 Data analysis
To comprehensively evaluate the climatic conditions leading to
signicant attacks by OLB in all the examined ecosystems,
we conducted a 2D scatterplot frequency analysis. is analysis
primarily concentrated on severe attacks, which encompassed strong
and very strong instances (refer to Figure1), considering two pivotal
climatic factors: (i) the average annual temperature and annual
precipitation, and (ii) the average temperature during the growing
season (May–October) and the corresponding precipitation.
To determine the key factors inuencing the migration of OLB
into mesophilous forest ecosystems, we employed Principal
Components Analysis (PCA), using the following variables: damage
intensity, the year in which it occurred, altitude, average annual
temperature and precipitation, average temperature and precipitation
during the growing season (May–October), average temperature and
precipitation during the insect’s overwintering period (November–
April), and average temperature and precipitation during winter
(December–February).
Although the important factors (temperature and precipitation)
inuencing insect damages are well represented by Principal
Component Analysis, a quantitative analysis (e.g., correlation analysis
or regression analysis) of their impact on insect damages should
beconsidered to obtain a deeper explanation of such variables. Finally,
a correlation analysis was preferred over regression analysis or GLM
analysis mainly due to the presence of autocorrelation between
dierent climatic variables that cannot beincluded as explanatory
variables in the same model simultaneously. us, a Spearman
correlation coecient was calculated between insect damages and
every climatic variable (average annual temperature and precipitation,
overwintering temperature and precipitation but also during growing
season temperature and precipitation). Spearman rank correlation
coecient calculation was performed because the assumptions
necessary for Pearson correlation coecients were violated (lack of
data normality and discrete character of damage values).e
relationship between climatic factors and severe attacks caused by
OLB (2D scatterplot frequency analysis), but also principal component
analysis and correlation analysis was performed using STATISTICA
8.0 soware (StatSo Inc., 2007).
3 Results
3.1 Analysis of oak lace bug spread:
concentration and expansion in forest
ecosystems
e study, conducted from 2017 to 2022, focused on analysing
the spread of the OLB in Romanian forest ecosystems (Figure2).
e data analysis reveals that in the rst 4 years of observation, the
spread of the oak lace bug was predominantly conrmed to the
extra Carpathian regions of Romania, concentrating in the
southern, western, and northwestern parts of the country, with a
recent expansion into the eastern region. During the period of
2017–2020, the most aected forest ecosystems were characterized
by termophilous Turkey oak and Hungarian oak forests,
termophilous pedunculate oak forests, as well as alluvial and
wetland deciduous broad-leaved forests (where there are also grey
oak forests), located mainly at low altitudes in the southern and
western regions of Romania. In the nal 2 years of the analysis
(2021–2022), there is a noticeable increase in the frequency of
insect presence, especially in lowland ecosystems, accompanied by
a decline in damage intensity in these forests. During this period,
attacks with severe leaf damage have been reported in forest
ecosystems consisting of mesophilous sessile oak forests and mixed
beech-oak forests, located mainly at high altitudes. Additionally,
during this period, the insect was reported within the forested area
of the Carpathian arc for the rst time, albeit with a very low
damage intensity. Notably, in the last year of the study, data analysis
indicates that most points (55%) with very high damage intensity
are situated in forest ecosystems consisting of mesophilous sessile
oak forests and mixed beech-oak forests.
3.2 Assessing the climatic range and major
OLB attacks
e analysis of the climate data reveals that most of the
locations where OLB caused signicant damage can becharacterized
by average annual temperatures ranging between 10 and 14°C and
annual precipitation between 300 and 700 mm. Additionally, the
most frequent severe damage were situated between 12 and 13°C
and 450–600 mm of annual precipitation (Figure3A). Regarding
the analysis of climate characteristics during the growing season,
TABLE1 Characterization of forest ecosystems with oak lace bug.
Forest ecosystem formation Number of
OLB points
Altitude
range (m)
Code [According to
Doniţă etal., 2008]Name
4 Mesophilous hill beech (Fagus sylvatica L.) forests 82 91–984
5 Mesophilous and thermophilous sessile oak (Quercus petraea (Matt.) Liebl)forests 75 75–618
6 Mesophilous and thermophilous oak (Quercus robur L.,) forests 74 29–526
7 ermophilous Turkey oak (Quercus cerris L.) and Hungarian oak (Quercus frainetto Ten.) forests 139 59–462
8 ermophilous grayish oak (Quercus pedunculiora K. Koch) and downy oak (Quercus pubescens
Wild.) forests
42 0–207
9 Alluvial and wetland deciduous broad-leaved forests 64 7–375

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Frontiers in Forests and Global Change 05 frontiersin.org
the data analysis indicates that most points where OLB caused
major damages can be characterized by average temperatures
during the vegetation season ranging between 17 and 21.5°C and
precipitation between 150–450 mm during the vegetation season
(Figure3B). e most frequent severe attacks are produced around
values of 19 and 20.5°C and 300–400 mm of precipitation during
the growing season.
3.3 Impact trends in varying ecosystem
contexts
As for the analysis of each ecosystem individually, it is noted that
forest ecosystems in which oak lace bug was present during the
analysed period can bedivided into two main clusters: thermophilous
FIGURE2
Yearly distribution patterns of oak lace bug (2017–2022) in Romanian forest ecosystems.

Bălăcenoiu et al. 10.3389/gc.2023.1326929
Frontiers in Forests and Global Change 06 frontiersin.org
located mainly at low altitudes in the lowland regions and mesophilous
forest ecosystems that are mainly found at higher altitudes, in
mountainous areas (Figure4).
Within thermophilous forest ecosystems, the dynamics of damage
intensity during the period of 2017–2022 exhibit an oscillating
pattern, where the number of points with strong and very strong
attacks showed an increase until the year 2019, when it reached its
peak. Subsequently, starting from 2020, a steady decrease was
observed, and by 2022, oak lace bug caused very few attacks with
strong intensity. In parallel, within mesophilous forest ecosystems, a
distinct pattern of damage intensity dynamics during the period of
2017–2023 becomes evident. is can bedescribed as an increase in
the number of points where the insect caused major attacks,
concurrently with a decrease in the number of points where the insect
caused weak damages as time progressed. is trend suggests a
signicant adaptation and expansion of the oak lace bug in
mountainous environments, exerting an increasingly pronounced
impact on forest ecosystems in this area.
3.4 Determinants factors on the migration
of oak lace bug in mesophilous forest
ecosystems
e PCA results provide a profound insight into the inuence of
climatic factors on the invasive behaviour of the insect, highlighting a
direct correlation between rising temperatures, decreasing
precipitation, and the increasing number of recorded points with
severe attacks in both ecosystem 4 (Figure 5A) and ecosystem 5
(Figure5B). Data analysis suggests that, as the number of recorded
points with major attacks increases, there is a noticeable upward trend
in temperature-related factors, while precipitation rates exhibit a
decreasing trend in the mesophilous ecosystems over the study period
(2017–2022). In particular, the average winter temperature and the
annual precipitation mean to bedeterminants in this evolution.
Furthermore, altitude plays a crucial role in the insect’s attack
pattern. e higher the altitude, the fewer attacks seem to occur. is
observation suggests that OLB appears to favour lower areas within
mesophilous ecosystems, where climatic and altitude conditions may
bemore favourable for its development and survival.
e correlation analysis (Table2) revealed that the average annual
temperature and the average temperature during the growing season
positively inuenced the intensity of insect damage. Meanwhile, the
altitude and annual precipitation had a signicant negative impact on
insect damage intensity. Spearman values did not indicate any
signicant relationship between insect damage intensity and
precipitation during the growing season, overwintering temperature,
overwintering precipitation, average winter precipitation, and average
winter temperature.
4 Discussions
is study aimed to investigate the invasive behaviour of the oak
lace bug in the forest ecosystems of Romania, with a focus on the
dierences between thermophilous and mesophilous environments.
During the study period, a distinctive pattern of OLB invasion
emerges, predominantly in the extra-Carpathian regions of Romania,
with recent expansion into the eastern region. In contrast, the central
part of the country has remained relatively protected from this
invasion. An intriguing aspect to highlight is how the Carpathian
Mountain range has played a crucial role in shaping the spatial
distribution of OLB. ese major geographical features have acted as
natural barriers, delimiting the distribution of native insects and
posing signicant obstacles to the invasion of alien insects (Haran
etal., 2015). ese geographical barriers have created environmental
variability, which, in turn, can inuence the adaptability and
invasiveness of species. A relevant example of this phenomenon is the
dierent climate in mountainous areas, which can inhibit the activity
and development of insects (Mellanby, 1939; Bale, 2002; Sinclair etal.,
2003; Jaworski and Hilszczański, 2013). Temperature, in particular,
has proven to bea key factor in the success or failure of invasion by
several alien species (Kang etal., 2009; Ju etal., 2017; Ward etal.,
2019). In the same context, another important aspect that could
FIGURE3
The relationship between climatic factors and severe attack caused by OLB: (A) analysis of annual mean temperatures and precipitation (B) analysis of
mean temperatures and precipitation during the growing season. The ellipse represents 95% confidence.

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Frontiers in Forests and Global Change 07 frontiersin.org
berelevant to the inuence of the mountain range on OLB invasion is
related to landscape heterogeneity, including habitat composition and
conguration (With, 2002; O’Reilly-Nugent etal., 2016). Furthermore,
the host species range should not beunderestimated in its inuence
on OLB invasion, primarily represented by oak species (Tom es cu
etal., 2018; Csóka etal., 2019; Paulin etal., 2020). In the Carpathian
region, the food resources available to this insect are limited, which
may signicantly contribute to the creation of a natural barrier to
OLB’s spread, at least for the time being.
Regarding forest ecosystems, in the initial years of the study
(2017–2020), thermophilous forest ecosystems, especially those
featuring termophilous Turkey oak and Hungarian oak forests,
termophilous pedunculate oak forests, and grey oak forests, proved to
bethe most aected. is nding aligns with the results of a Eurasian
study (Csóka etal., 2019), which identied Quercus cerris L., Q. petraea
(Matt.) Liebl., Q. pubescens Willd. and particularly Q. robur L. as the
species that suered the most signicant attacks across all the
countries studied. Furthermore, Marković etal. (2021) demonstrated
that by studying OLB’s preference for dierent oak species in eld
conditions, the insect exhibited the greatest preference for the
Hungarian oak and the least for pedunculate oak. Additionally, in
terms of the spatial distribution of the invasion, it is evident that
FIGURE4
Assessing oak lace bug damage trends (2017–2022) in Romanian thermophilous and mesophilous ecosystems.
FIGURE5
Assessing factors influencing oak lace bug attack patterns in mesophilous forest ecosystems: (A) Ecosystem 4 – Mesophilous hill beech forests;
(B) Ecosystem 5 – Mesophilous and thermophilous sessile oak forests.

Bălăcenoiu et al. 10.3389/gc.2023.1326929
Frontiers in Forests and Global Change 08 frontiersin.org
during this period, the forests in the western part of the country,
particularly in the south, experienced more severe impacts than other
regions. is trend can beattributed to the initial reports of the insect
in these two regions (Don etal., 2016; Chireceanu etal., 2017), making
the southern part of the country one of the most severely aected
areas in Romania (Tomescu etal., 2018).
In the last years of the study period, weobserve an expansion
of locations where the insect is present in thermophilous
ecosystems, coupled with a reduction in the severity of damage in
the forests of these regions. is suggests that the areas with strong
attacks are diminishing in intensity, while the number of areas with
mild damage is increasing. Simultaneously, wenotice that OLB has
extended its range to higher altitudes, inltrating montane
environmentals and predominantly establishing in mesophilic oak
forests. In the nal year of the study, most of the points with very
strong attacks are in sessile oak forests or mixed beech-oak forests.
is phenomenon might indicate a potential adaptation of OLB to
new conditions, including the insect’s ability to colonize and explore
new environments, progressively overcoming natural barriers.
ese results are consistent with another study (Paulin etal., 2023),
which suggests that OLB is adapted to surviving Central European
winter conditions, with low winter temperatures not being a major
limiting factor for its expansion in the invaded regions, as supported
by previous observations in Hungary (Csepelényi et al., 2017;
Paulin etal., 2021).
It is worth noting that these ndings align with research by
Robinet and Roques (2010), which posits that climate change can
play a pivotal role in the rapid spread of invasive insects. Rising
temperatures enable the introduction of species into areas where
they could not survive previously (Walther et al., 2009). For
instance, Régnière etal. (2009) provide a compelling example of the
invasive species Lymantria dispar (Linnaeus, 1758) (Lepidoptera,
Erebidae) in Canada, showcasing its close correlation with
favourable climatic conditions. Increasing temperatures have
allowed this insect to expand its population north-westward in the
country. Moreover, research by Jaworski and Hilszczański (2013)
suggests that invasive species such as Parectopa robiniella Clemens,
1863 and Phyllonorycter robiniella (Clemens, 1859), (both
Lepidoptera: Gracillariidae), introduced in Southern Europe from
North America during the latter half of the 20th century, have
extended their range northward on the continent primarily due to
temperature increases. ese examples underscore the importance
of considering climate change when assessing the behaviour of
invasive species like OLB.
Overall, the analysis of major attacks in forest ecosystems
suggests that climate changes can play a crucial role in the expansion
and intensication of the OLB invasion in mesophilous forest
ecosystems in Romania. Increasing temperatures and decreasing
precipitation in these ecosystems may have contributed to increased
stress on host trees, rendering them more susceptible to OLB attacks.
Furthermore, based on prior observations (Bălăcenoiu etal., 2021c),
wehave highlighted that the daily and seasonal dynamics of the OLB
population are signicantly inuenced by climatic factors. In this
context, it becomes increasingly plausible that OLB is developing
adaptive capabilities and thriving in mountainous environments,
establishing itself as a remarkable and challenging invasive species
for the forest ecosystems of Romania. “Studies have shown that
rising winter temperatures have allowed some species to extend their
ranges. For example, rising winter temperatures allowed the
southern pine beetle Dendroctonus frontalis Zimmermann, 1868
(Coleoptera, Curculionidae) to extend its range to northern latitudes
(Ungerer et al., 1999). Similarly, warmer winters enabled the
expansion of species like Operophtera brumata (Linnaeus, 1758) and
Epirrita autumnata (Borkhausen, 1794) (both Lepidoptera,
Geometridae) northward into Scandinavia (Jepsen etal., 2008).
Certainly, temperature increases not only lead to latitudinal range
extensions but also to altitudinal ones. A striking example is the
Mediterranean species, the pine processionary moth aumetopoea
pityocampa (Denis and Schiermüller, 1775) (Lepidoptera,
Notodontidae), which expanded its range into the mountainous
regions of the Alps, reaching altitudes exceeding 1,400 meters due
to the rising temperatures in both the winter and the ight period of
females (Battisti etal., 2006).
e PCA analysis reveals a signicant inuence of climatic factors
on the expansion and intensication of the Oak Lace Bug (OLB)
invasion in the Romanian mesophilous ecosystems. e substantial
increase in temperatures and the decrease in precipitation are closely
associated with the heightened intensity of attacks, suggesting
increased activity of the insect in these ecosystems and enhanced
eciency in attacking their hosts. ese climatic factors may lead to
a drier environment in mountainous ecosystems, potentially
contributing to the water stress experienced by host trees. By the end
of the century, European forests could undergo remarkable changes
due to the climate change phenomenon, which will substantially alter
the current distribution of climatically suitable areas for the majority
of European tree species (Buras and Menzel, 2019; Mauri etal., 2022).
In this context, harmful eects for several insect guilds, such as the
OLB, can beexpected, as the new microclimates may also become
more favorable for certain insect groups (Sallé etal., 2021). Regarding
our results, this additional climatic stress renders the trees more
vulnerable to OLB attacks, which can explain the notable rise in the
attack levels under these conditions. ese ndings align with the
results of another study (Ju etal., 2011), which indicates an increase
in both average fecundity and the success rate of passing through all
developmental stages in Corythucha ciliata (Say, 1832) (Hemiptera,
Tingidae), a closely related species to the one studied here, in response
to rising temperatures. Additionally, similar conclusions have been
drawn by Lu etal. (2019), who observed a signicant impact of air
TABLE2 Correlation analysis of insect damage with altitudinal and
climatic variables.
Pair of variables Spearman
R value
Value of
p
Damage & altitude −0.2486 0.0000
Damage & average year temperature 0.0648 0.0031
Damage & average winter temperature 0.0232 0.2909
Damage & average overwinter temperature 0.0247 0.2601
Damage & annual precipitation −0.0444 0.0427
Damage & winter precipitation 0.0342 0.1190
Damage & overwinter precipitation −0.0063 0.7755
Damage & average growing season temperature 0.0857 0.0001
Damage & growing season precipitation 0.0125 0.5704
Bold values indicate statistically signicant correlations.

Bălăcenoiu et al. 10.3389/gc.2023.1326929
Frontiers in Forests and Global Change 09 frontiersin.org
temperature on the ight distance of C. ciliata. Our research primarily
focuses on the study of select climatic and environmental factors that
inuence the invasion of the oak lace bug, as it is essential to gain a
deeper understanding of this invasion’s dynamics in Romania and to
formulate eective management strategies for this invasive species.
While human-mediated introduction of potentially invasive species
is a well-recognized factor (Brockerho etal., 2006; Skarpaas and
Økland, 2009), our present work dedicates particular attention to
elucidating the critical ecological and climatic aspects of this invasion.
It is worth noting that invasive species’ movement and establishment
can beinuenced by a complex interplay of factors beyond climate,
environment, and human activities (e.g., habitat availability, host tree
diversity, predator–prey relationships, and more). erefore, our
study underscores the importance of continued monitoring and
research eorts to comprehensively grasp the evolution of the OLB’s
presence in Romania and to devise robust strategies for
its management.
Nevertheless, it is essential to acknowledge certain limitations in
our study that may impact the robustness and generalizability of the
ndings. Firstly, the relatively short duration of the study period,
spanning from 2017 to 2022, might limit our ability to conclusively
assert the inuence of climatic factors on the behaviour of the
OLB. Climate patterns exhibit long-term trends, and our study may
not capture the full spectrum of these inuences. Recognizing this,
weintend to continue monitoring OLB behaviour in subsequent years
to enhance our understanding of its relationship with climatic
conditions. Secondly, the reliance on visual assessment for
determining the extent of foliage discoloration introduces potential
biases in data collection. While visual inspections are a widely used
method, the subjectivity inherent in human judgment may lead to
variations in assessing the severity of OLB damage. e current study
attempted to mitigate this limitation by categorizing the damage
caused by OLB into ve distinct levels. However, it is essential to
recognize that advancements in Articial Intelligence data processing
may enhance the objectivity of remote sensing technologies in the
future. Exploring these technological advancements could further
rene and standardize the methodology for quantifying OLB-induced
foliage discoloration, addressing concerns about potential biases
associated with visual assessments.
5 Conclusion
Geographical spread: initially, oak lace bug was mainly observed
in the extra Carpathian regions of Romania, particularly in the
southern, western, and northwestern parts. However, there has been
a recent expansion into the eastern region.
Change in attack patterns: in recent years (2021–2022), OLB
presence has become more frequent, especially in thermophilous
ecosystems, coinciding with a decrease in damage intensity.
Mountain environment impact: in the last year of the study, most
points with very strong OLB attacks were observed in mountain
environments, particularly within mesophilous sessile oak and mixed
beech-oak forests.
Climate inuence: climate analysis indicated that OLB’s major
attacks were associated with specic temperature and precipitation
ranges, suggesting that climatic factors play a signicant role in
its behaviour.
Altitude: there was an inverse relationship between altitude and
OLB attacks, with lower elevations in mesophilous ecosystems
being more prone to severe attacks. is relationship may
beassociated with both abiotic factors such as precipitation and
temperature, as well as the distribution of oak species in those
specic altitudinal ranges.
Data availability statement
e original contributions presented in the study are included in
the article/supplementary material, further inquiries can bedirected
to the corresponding author.
Author contributions
FB: Conceptualization, Formal analysis, Investigation,
Methodology, Writing – original dra. CN: Conceptualization,
Funding acquisition, Methodology, Project administration, Writing
– review & editing. DT: Conceptualization, Data curation,
Investigation, Writing – review & editing. IP: Formal analysis,
Writing – review & editing.
Funding
The author(s) declare financial support was received for the
research, authorship, and/or publication of this article. This work
was supported by the projects PN 23090102, and
34PFE./30.12.2021 “Increasing the institutional capacity and
performance of INCDS “Marin Drăcea” in the activity of RDI –
CresPerfInst” funded by the Ministry of Research, Innovation
and Digitalization of Romania.
Acknowledgments
e authors acknowledge the partial nancial support provided
by Transilvania University of Brașov to cover the article
publishing charges.
Conflict of interest
e authors declare that the research was conducted in the
absence of any commercial or nancial relationships that could
beconstrued as a potential conict of interest.
Publisher’s note
All claims expressed in this article are solely those of the
authors and do not necessarily represent those of their affiliated
organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteed or
endorsed by the publisher.

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Frontiers in Forests and Global Change 10 frontiersin.org
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