Study of the overwintering ecology of the hazelnut pest, Palomena prasina (L.) (Hemiptera: Pentatomidae) in a perspective of Integrated Pest Management

Abstract

Palomena prasina, the green shield bug (GSB), is widely distributed in the Eurosiberian region. In the Southwest of France, it is considered as a serious pest of hazelnuts, its feeding punctures lead to blank hazelnuts and kernel necrosis, causing heavy losses in commercial orchards. To date, no Integrated Pest Management strategy is available to control P. prasina. Control strategies often focus on the pests' spring-summer ecology, when they are in the field or in the vicinity of crops. However, the abundance of pest populations in crops is also related to their autumn-winter ecology. The present work focussed on the autumn-winter ecology of P. prasina to identify new opportunities for this pest suppression. We investigate (i) where P. prasina overwinters, (ii) if it aggregates in its overwintering sites and (iii) if it mates while overwintering. Samples were collected over a 2-year period in different ecosystems (forests, hedges, orchards), in human made structures and habitats (litter, bushes/trees, dead trees). The reproductive status of GBS individuals was monitored in winter, and in spring when they emerged from overwintering sites. Our results show that 97% P. prasina adults overwinter in the leaf litter of orchards and natural ecosystems and that 70% overwinter individually. The abundance of GSB in those sites is negatively correlated with litter temperature and positively correlated with humidity levels. Furthermore, adults only mate after leaving their overwintering site. Finally, unexpectedly, there was an important number of over-wintering adults hosting endoparasitoids (32%). The fact that GSB overwinters alone in the leaf litter means controlling its populations by destroying the overwintering sites is not a solution. All the same, our results point out some promising lines of research for developing methods to control P. prasina. First, the emergence traps, in particular the cone traps, proved efficient for collecting emerging adults and could be considered for monitoring. Moreover, our observations suggest the existence of long-range mating signals that could be exploited for trapping. Last but not least, the important number of overwintering parasitised adults is a potential biocontrol avenue.

Full text

J Appl Entomol. 2023;00:1–15.
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1wileyonlinelibrary.com/journal/jen
Received: 14 June 2023
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Revised: 30 October 2023
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Accepted: 1 November 2023
DOI: 10.1111/jen.13206
ORIGINAL ARTICLE
Study of the overwintering ecology of the hazelnut pest,
Palomena prasina (L.) (Hemiptera: Pentatomidae) in a
perspective of Integrated Pest Management
Laetitia Driss1,2 | Rachid Hamidi1 | Christophe Andalo2 | Alexandra Magro2,3
1Association Nationale des Producteurs
de Noisettes (ANPN), Cancon, France
2Laboratoire Évolution et Diversité
Biologique, UMR 5174 CNRS/UPS/IRD,
Université Toulouse III – Paul Sabatier,
Toulouse, France
3Université Toulouse – ENSFEA , Castanet-
Tolosan, France
Correspondence
Laetitia Driss, Association Nationale des
Producteurs de Noiset tes (ANPN), 150 0
route de Monbahus, Cancon, France.
Email: laetitia.driss@univ-tlse3.fr
Abstract
Palomena prasina, the green shield bug (GSB), is widely distributed in the Eurosiberian
region. In the Southwest of France, it is considered as a serious pest of hazelnuts, its
feeding punctures lead to blank hazelnuts and kernel necrosis, causing heavy losses in
commercial orchards. To date, no Integrated Pest Management strategy is available to
control P. pra sina . Control strategies often focus on the pests' spring–summer ecology,
when they are in the field or in the vicinity of crops. However, the abundance of pest
populations in crops is also related to their autumn-winter ecology. The present work
focussed on the autumn-winter ecology of P. pra sina to identify new opportunities for
this pest suppression. We investigate (i) where P. pr asina overwinters, (ii) if it aggregates
in its overwintering sites and (iii) if it mates while overwintering. Samples were col-
lected over a 2-year period in different ecosystems (forests, hedges, orchards), in hu-
man-made structures and habitats (litter, bushes/trees, dead trees). The reproductive
status of GBS individuals was monitored in winter, and in spring when they emerged
from overwintering sites. Our results show that 97% P. prasin a adults overwinter in the
leaf litter of orchards and natural ecosystems and that 70% overwinter individually. The
abundance of GSB in those sites is negatively correlated with litter temperature and
positively correlated with humidity levels. Furthermore, adults only mate after leaving
their overwintering site. Finally, unexpectedly, there was an important number of over-
wintering adults hosting endoparasitoids (32%). The fact that GSB overwinters alone in
the leaf litter means controlling its populations by destroying the overwintering sites is
not a solution. All the same, our results point out some promising lines of research for
developing methods to control P. pras ina. First, the emergence traps, in particular the
cone traps, proved efficient for collecting emerging adults and could be considered
for monitoring. Moreover, our observations suggest the existence of long-range mating
signals that could be exploited for trapping. Last but not least, the important number of
overwintering parasitised adults is a potential biocontrol avenue.
KEYWORDS
abiotic conditions, green shield bug, overwintering behaviour, overwintering habitat,
reproductive status
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction
in any medium, provided the original work is properly cited and is not used for commercial purposes.
© 2023 The Authors. Journal of Applied Entomology published by Wiley-VCH GmbH.

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DRISS et a l.
1 | INTRODUC TION
Understanding the ecology and evolution of insect herbivores is
key to designing efficient Integrated Pest Management programmes
(Peterson et al., 2018; Sentis et al., 2022). However, existing pest
control strategies often focus on the spring—early summer ecology
of pests, when the pests are in the field or in the vicinity of crops.
To reduce pest pressure on the crop, we need to better account for
the overall temporal and landscape ecological dynamics of pests
(Schellhorn et al., 2015).
In temperate regions, insects spend a large proportion of their
lifetime in diapause in the autumn–winter season (Delinger, 2022).
Although diapause is an adaptive advantage for surviving this critical
period (Hahn & Denlinger, 2007), it still has an important impact on
the life history of insects, and strongly influences their population
dynamics (Delinger, 2022). As such, some pest control strategies do
account for the overwintering ecology of insect herbivores.
Trapping strategies based on knowledge of overwintering be-
haviour, for instance, have been tested with success for the con-
trol of Eucryptorrhynchus scrobiculatus (Motschulsky) and E. brandti
(Harold) (Coleoptera: Curculionidae), which attack Alianthus al-
tissima (Simaroubaceae). Late in the season, adults of these pests
crawl down their host trees to overwinter in the soil nearby (Guo
et al., 2021). Based on this knowledge, Yang and Wen (2021) de-
signed bottle traps they buried in the soil close to the host trees
that efficiently reduced the density of the pests in the orchard.
Another strategy based on overwintering trap plants was devel-
oped to control the cotton pest Lygus lineolaris (Palisot de Beauvois)
(Hemiptera: Miridae) (Dumont & Provost, 2022). The adults of this
species overwinter in different plants (Hanny et al., 1977; Villavaso
& Snodgrass, 2004) and Verbascum thapsus L. (Scr oph ulariace ae) was
used to attract the bugs, as they tend to converge on it. In the fol-
lowing winter, these plants are sprayed with insecticides (Dumont
& Provost, 2022). Overwintering aggregation may also occur inde-
pendently of the spatial distribution of resources and could be used
to develop control strategies. Indeed, to increase their survival rate,
some species aggregate during diapause, a strategy thought to con-
tribute to their thermoregulation (Schowalter, 1986), as protection
against predators (Delinger, 2022; Wolda & Denlinger, 1984), to
improve the metabolic rate (Szejner-Sigal & Williams, 2022; Tanaka
et al., 1988) or is part of species' mating systems (Susset et al., 2018).
Thus, for species with overwintering aggregation behaviour, control
strategies could target the aggregation sites and hence a large num-
ber of insects simultaneously (Kenis et al., 2008; Lee et al., 2014).
Palomena prasina (L.) (Hemiptera: Pentatomidae), the green
shield bug (GSB), is a widely distributed species in the Eurosiberian
region (Lupoli & Dusoulier, 2015). The feeding punctures of this po-
lyphagous stink bug lead to kernel necrosis or to empty hazelnuts
(Romero et al., 2009) with type of damage depending on the feed-
ing period (Hamidi et al., 2022). As a consequence, P. prasina causes
heavy crop losses in commercial orchards in Europe (e.g. Saruhan
et al., 2023; Ateş & Kaçar, 2021, for Turkey, and Bosco et al., 2018,
for Italy). In southern France, P. prasina is a major pest of hazelnuts
(Hamidi et al., 2022) and a minor pest of other crops including apples
and kiwis (Blanc, 1988).
Pyrethroid insecticides are applied to the crop in summer when
the hazelnuts are most vulnerable to P. prasina attacks, but with lim-
ited success and with negative environmental impacts (Ceuppens
et al., 2015; Liu et al., 2012). Although biological control strate-
gies using entomopathogenic fungus (Ozdemir et al., 2021), bacte-
ria (Ozsahin et al., 2014) or parasitoids are under study (Ozdemir
et al., 2023), to date, no comprehensive IPM strategy for the control
of P. prasina is available. There is thus a need to advance our knowl-
edge of the overall temporal and landscape ecology of the GSB.
In the present study, we focussed on the overwintering ecol-
ogy of P. prasina. In Southern Europe, GSB is univoltine and, at the
adult stage, it enters obligate diapause in the autumn-winter sea-
son, which lasts between 3 and 4 months (Musolin & Saulich, 1996;
Saulich & Musolin, 2014). However, its overwintering ecology re-
mains mostly unknown. The information available on the pentato-
mid family is scattered but suggests a diversity of overwintering
behaviours (Table 1), and this knowledge has been used to design
control strategies for some pests. For instance, traps based on ag-
gregation pheromones (Leskey et al., 2015) or particular building ma-
terials (Lee et al., 2013) are used to attract the overwintering brown
marmorated stink bug, Halyomorpha halys (Stal) to help monitor its
populations and have also been considered as possible trap-and-kill
devices (Weber et al., 2017). Moreover, the potential of entomo-
pathogenic fungi and parasites as biocontrol agents of overwinter-
ing individuals of this species has been evaluated (Chen et al., 2020;
Hajek et al., 2023).
The aim of this study was to advance our knowledge of the over-
wintering ecology of P. prasina to identify new opportunities for
pest management. We focused on the following questions: (i) where
does P. prasina over winter, that is, in which ecosys tems, specif ic ha b-
itats and abiotic conditions? (ii) does it aggregate in the overwin-
tering sites? (iii) does it mate while overwintering? The answers to
these questions are discussed both from an ecological and an IPM
perspective.
2 | MATERIALS AND METHODS
2.1 | Characterisation of overwintering sites
A field study was conducted in a zone with a radius of 20 km around
the city of Cancon, France (44°32′09.7 ″ N, 0°37′30.1″ E, 160 m a.s.l.)
from December to February (10 weeks), both in 2021 and 2022.
In 2021, three different types of ecosystems were studied: ha-
zelnut orchards, linear hedges and woods. The hazelnut orchards
were over 20 years old, at least 1 ha in size, and most of them were
planted with the Pauetet cultivar, which is sensitive to P. prasina.
They were all commercial orchards with no cultural practices or pes-
ticide spraying during the study period (the last management prac-
tices before that period correspond to pesticide spraying in July).
The linear hedges were lines of trees and bushes that separated two

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DRISS et al.
TAB LE 1 Diapause characteristics and overwintering sites of Pentatomidae.
Tri be Species
Diapause
program
Diapause
stage
Aggregation
behaviour Overwintering site
Studied region/
country References
Aeliini Aelia rostrata Boheman Obligatory Adult ? Leaf litter Tur key Memişoğlu et al. (1996); Cakmak
et al. (2008)
Atestiini Plautia stali Scott Facultative Adult ?Asia Kotaki and Yagi (1989)
Cappaeini Halyomorpha halys (Stäl) Facultative Adult Present Bark of trees; Human-made
structures
North America and
Asia
Toyama et al. (2006); Inkley (2012);
Leskey et al. (2012); Lee
et al. (2014); Hancock et al. (2019)
Carpocorini Dolycoris baccarum (L.) Facultative Adult ? Leaf litter; bark of trees Asia et Europe Jung and Lee (2018); Mutlu
et al. (2018); Sabuncu et al. (2021)
Graphosomatini Graphosoma lineatum (L.) Adult ? Leaf litter Europe Tullberg et al. (2008)
Halyini Erthesina fullo (Thunberg) Facultative Adult Present Human-made structures; bark of
tree; leaf litter
Northern Asia Mi et al. (2020)
Pentatomini Euschistus heros
(Fabricius)
Facultative Adult ? Leaf litter South America Panizzi and Niva (1994); Mourão and
Panizzi (2000)
Oebalus poecilus (Dallas) Facultative Adult ? Leaf litter South America Albuquerque (1993); Santos
et al. (2003, 2007)
Oebalus pugnax
(Fabricius)
Facultative Adult ?Grasses South America Nilakhe (1976)
Oebalus mexicana Sailer Unknown Adult Present Leaf litter South America Cortez-Madrigal et al. (2022)
Pentatoma rufipes (L.) Obligate Nymphal ? Bark of trees Europe Powell (2020)
Piezodorini Piezodorus guildinii
(Wes twood)
Facultative Adult ? Leaf litter, alfalfa, pittosporum South America Zerbino et al. (2020)
Piezodorus hybneri
(Gmelin)
Facultative Adult ? ? Asia Higuchi (1994)
Piezodorus lituratus
(Fabricius)
Unknown Adult ? Leaf litter; bushes Europe Mutlu et al. (2018); Laterza
et al. (2023)
Strachiini Bagrada hilaris
(Burmeister)
Unknown Adult ?Soil North America Reed et al. (2013)
Rhynchocorini Biprorulus bibax (Breddin) Facultative Adult Present ?Europe James (1990)
Menidini Menida disjecta (Puton)
(=M. scotti)
Obligate Adult Present ?Asia Koshiyama et al. (1994)
Nezarini Palomena prasina (L.) Obligate Adult ? ? Northern Europe Musolin and Saulich (1996)
Nezara viridula (L.) Facultative Adult ? Leaf litter; bark of trees; human-
made structures
North America and
Australia
Jones and Sullivan (1981);
Coombs (2000); Ehler (2002);
Laterza et al. (2023)
Abbreviation: ?, no information available.

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DRISS et a l.
fields and were more than 116 m in length. The woods were at least
0.68 ha in size. The hedges and the woods were mainly composed of
local deciduous trees, different species of oak, chestnut, hornbeam,
checker tree and some shr ubs includin g dogwood and hawthorn; ev-
ergreen bushes included wild blackberr y, butcher's broom and wild
madder (Badeau et al., 2017; Bonneaud, 2014). In 2022, apple or-
chards were added to the above-mentioned ecosystems. The apple
orchards were at least 3.36 ha in size. All the orchards were managed
conventionally and most were surrounded by crops, mainly hazelnut,
plum and apple orchards. Ten sites representing each ecosystem, lo-
cated at least 8 km apart, were selected for the study. Each week,
one site of each ecosystem type was prospected (i.e. each site was
prospected only once per year).
Three main types of habitats were sampled in each ecosystem:
leaf litter, the bark of trees and the foliage of evergreen bushes. Five
samples were collected at 10-m intervals along a 50 m transect in
the hedges and at the edges of orchards and woods starting at 0 m
and continuing to 40 m. A further five samples were collected at the
centre of the orchards and woods, at a distance of between 10 and
50 m from the edge.
A total of 600 leaf litter samples were collected, of 1 m2 each
(250 and 350 samples were collected in 2021 and 2022 respec-
tively). For each sample, four abiotic parameters were recorded at
the surface of the litter using a TR-74Ui Series data logger (TandD
corporation, Japan): temperature, relative humidity, illuminance and
UV. The depth of the leaf litter was also measured. After the mea-
sure ment s were co mplete , the leaf litter cove ring each 1 m2 area was
collected separately, placed in a black plastic bag and transported
to the laboratory. The contents of each bag were placed under a
photo-eclector trap (Soil photo-eclector Ø1 m2, ecoTech Umwelt-
Meßsysteme GmbH, Germany) for 24 h at 25°C under constant light
(Philips Master TDL 18 W/840 Cool white), after which the presence
of insects was checked in each trap. At the end of the 24-h period,
the photo-eclector traps were removed, and leaf litter was carefully
inspected for any remaining insects.
We then defined an area with a radius of 2 metres around each
leaf litter sampling area. In this area, the bark of one dead or standing
tree was inspected visually for 2 minutes, and one evergreen bush
was prospected for 10 seconds using a beating tray.
Finally, during the same monitoring period, a survey was con-
ducted of potential overwintering sites in human-made structures
(buildings and houses) based on a call for witnesses broadcast by
radio, on Internet, and using flyers. Witnesses were asked to take
photos of stink bugs present in their houses and buildings and to
send them to the laboratory by email together with information on
the general geographical location, plus the exact place and date of
collection. Thirty-seven volunteers in the Cancon region responded
to the call.
All the individuals belonging to the Pentatomoidea collected in
the above-mentioned samples were identified to species level.
The abundance of P. prasina in the 600 leaf litter samples was
analysed. We fitted a gGeneralised linear mixed model (GLMM)
with a Poisson error distribution and the following fixed effects:
type of ecosystem (categorial factors: hedge, woods, apple and
hazelnut orchards), zone (categorial factors: interface and cen-
tre; interface corresponds to samples collected in the hedges and
edges of woods and orchards), abiotic parameters of the leaf litter
(continuous factors: litter depth, temperature, humidity, light and
UV), study year (categorial factors: 2021 and 2022). To consider
the spatial autocorrelation, we added the sampling site as a ran-
dom effect (Table 2).
Th e goo dnes s of fi t was evalu ate d thro ugh th e rand omi sed qu an-
tile residuals calculated using the DHARMa package (version 0.4.6;
(Hartig, 2022). The GLMM was performed with the HLfit function of
the spaMM package (version 3.13.0; Rousset & Ferdy, 20 14) using
R software version: 4.1.2.; (R Developmental Core Team, 2021).
P-values were calculated using the type II log likelihood ratio test
(hereafter L.R.). We started with a model including all the double
interactions between the zone and the other seven independent
variables and removed them when they were not significant. This
first model is called ‘Full model’.
The same statistical procedure was applied to two partial mod-
els focused on P. prasina abundance in the 250 samples collected in
the centre of woods and orchards (called the ‘Centre model’) and in
TAB LE 2 Description of the variables used in the overwintering site characterisation models.
Variable name Description of the variable Scale Code
Abundance of Palomena prasina Absence or presence of P. prasina in a m2 of leaf
litter
0–5 Ab
Ecosystem type Woods, hedges, apple and hazelnut orchards Eco
Zone Sampling area Interface and Centre Zone
Litter depth Depth of the leaf litter (cm) 0.5–9 D
Temperature Surface temperature (°C) of leaf litter −2 to −17 Ts
Humidity Relative humidity (%) inside the leaf litter 70 –1 0 0 HR
Light intensity Light above the leaf litter (Lux) 369–94,361 L
UV UV (mW/cm2) above the leaf litter 0.019–0.99 UV
Years Study years 2021 and 2022 Year
Study sites All the sampling sites 10 sites Site

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DRISS et al.
the 350 samples collected at the edge of woods and orchards and
in the hedges (called the ‘Interface model’). The effect ‘zone’ was
removed from each of those GLMM and the remaining fixed and
random effects were tested. Using the two final partial models and
the ‘predict’ function in R, we calculated the predicted number of
P. prasina individuals. We computed predictions and their 95% con-
fidence intervals according to each type of ecosystem and for the
year in which the largest number of individuals was recorded, ex-
cept the apple orchard ecosystem which was only sampled in 2022.
Furthermore, the quantitative predictive variables with no signifi-
cant effect were set to their average value and the random effect
was not included in the calculation.
Next, a qualitative variable with two categories correspond-
ing to high and low values of the parameter was created for the
quantitative abiotic parameters which showed a significant effect
in the partial models. The threshold for defining these categories
was determined by selecting a value that minimised the P-value of
the effect associated with this new qualitative variable in the par-
tial model. In simple terms, this threshold represents a value above
which the number of P. prasina individuals in our leaf litter samples
changed significantly.
2.2 | Reproductive status
The reproductive status of P. prasina was assessed for the overwin-
tering adults collected in the leaf litter, as described in the previous
section, plus adults emerging from overwintering sites at the end of
the hibernation period, captured as described below. The study was
performed in 2021–2022.
From the end of February to the end of April 2022, adults of
P. prasina newly emerged from overwintering sites were collected
in two ecosystems: a 2.3 ha hazelnut orchard surrounded by lakes
and other hazelnut orchards, located near the village of Moulinet
(44°31′23.9” N, 0°36′00.5″ E, 117 m a.s.l.), and a 2.25 ha wood sur-
rounded by buildings, crop fields and hazelnut orchards, located
close to the city of Cancon (44°32′34.6″ N, 0°35′34.2″ E, 97 m a.s.l.).
As no information was available concerning the most efficient traps
to catch P. prasina emerging from overwintering sites, we used
two different kinds of traps. The first was a homemade Cone trap
(Raney, 1969) adapted from a pop-up mosquito transparent net tent
measuring 1.8 m × 2 m × 1.5 m (LxWxH, ®GLKEBY). The adaptation
consisted of cutting off the floor of each tent and placing a plastic
cone collector, with a1.5 cm Ø entrance at the top of the tent. The
tent was kept in place by a 1.50 m wooden pole inserted into the
ground at the centre of the tent. The second trap was a homemade
trap based on the Circle trap design (Mulder Jr et al., 2012), modified
and adapted for P. prasina by enlarging the opening at the top of the
trap top from Ø 0.80 cm to 1.50 cm, and by reducing the width of the
trap from 81 cm to 66 cm so it fitted the circumference of the tree
trunks better.
Ten cone traps and 20 Circle traps were installed at each site. The
cone traps were spaced about 20 m apart and the Circle traps were
fixed to trees growing about 10 m apart. The presence of P. prasina in
the traps was checked three times every day in the morning (at 9 am,
at noon and at 5 pm), to avoid leaving emerging individuals together
which could bias the evaluation of mating status (see below).
We checked the sexual maturity of both male and female P.
prasina collected weekly in the overwintering sites between
De cem ber an d Febr uary, in 2020–21 and 20 21–22, and in the con e
and Circle traps between the end of February and the end of April
2022. All parasitised individuals were excluded from the analyses,
as they could interfere with reproductive status (De Salles, 1992).
First, we observed the colour of the individuals, which is consid-
ered as a proxy for reproductive status in the close species Nezara
viridula (L.) and Plautia stali Scott (Kotaki & Yagi, 1989; Musolin &
Numata, 2003): russet or reddish brown during the winter repro-
ductive diapause and green during the period of active reproduc-
tion. The insects were then killed by freezing at −20°C for 2 min,
dissected and the sexual organs extracted in distilled water under
a stereo microscope (Nikon, SMZ1270). Ovarian development was
assessed using a scale starting at 0 (previtellogenic females) and
going up to 4 (post-reproductive females) (Kiritani, 1963; Nielsen
et al., 2017). The mated status of females was evaluated by the
presence of spermatozoids in the spermatheca (Golec & Hu, 2015;
Hamidi et al., 2021) obser ved under the microscope. In males, sex-
ual maturit y was assessed through the presence of living (i.e. mov-
ing) spermatozoids in the testes.
3 | RESULTS
3.1 | Characterisation of overwintering sites
Table 3 lists the results of sampling Pentatomoidea in overwinter-
ing sites. A to t a l of 47 1 in dividuals be l o n g ing to fi ve Pe n t ato moidae
families were collected during the two-year survey: Pentatomidae
(87%), Coreidae (12%), Acanthosomatidae (0.4%), Scutelleridae
(0.4%) and Reduviidae (0.2%). The three most abundant species
belonging to the Pentatomidae family were P. prasina (38.1%), N.
viridula (26.2%) and H. halys (9.2%). Coreidae were mainly repre-
sented by Gonocerus acuteangulatus (Goez) (86%). With 159 indi-
viduals, P. prasina was the most abundant true bug found among
the samples.
No GSB were found in human-made structures as it is the case for
G. acuteangulatus and in contr as t to H. halys or N. viridula which were
only found in human-made structures (Table 3). In natural ecosys-
tems, P. prasina is extr emely rare in app le orch ards but is consis tently
present in hazelnut orchards, hedges and woods. Ninety-seven per-
cent of P. prasina individuals were found in the leaf litter, while the
remaining 3% were present in evergreen foliage. No individuals were
found overwintering in the bark of trees. Henceforth, our analysis
focuses on the litter samples.
The ‘Full model’ (Table 4) reveals significant interactions be-
twe en zo n e and tempe rat ure an d be t ween zon e and li g ht. Howe ver,
the p-values and estimates obtained from the partial models show

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DRISS et a l.
TAB LE 3 Total and relative abundance (%) of the Pentatomoidea species collected in the different ecosystems and habitats during the 2-year study.
Tax on Species
Relative abundance (%)
Tot al
abundance
Apple orch. Hazelnut orch. Hedge Wood
Human-
made
structures
L.I T. L.I T. B. L.I T. B. L.I T.
i. c. i. c. i. c. i. c. i. c. i. c. i. c.
Acanthosomatidae:
Acanthosomatinae
Acanthosoma
haemorrhoidale
1.4 1.1 2
Coreidae: Coreinae
Anisoscelini Leptoglossus sp. 25 2
Coreini Coreus marginatus 3.2 11.8 2.9 1.1 6
Gonocerini Gonocerus
acuteangulatus
240 35.3 25 21.7 24. 5 49
Pentatomidae:
Pentatominae
Aelinii Aelia acuminata 6.5 10 3.6 5.9 8.7 8.5 23
Cappaeini Halyomorpha halys 22.3 37
Carpocorini Chlorochroa pinicola 0.6 1
Carpocoris
purpureipennis
3.2 23.6 1.4 4
Dolycoris baccarum 6.5 43.6 11.8 12 .5 2.9 4.3 14
Peribalus strictus 12.9 810.7 4.3 5.3 19
Nezarini Palomena prasina 100 100 61.3 74 50 11. 8 37. 5 46.4 52.1 159
Nezara viridula 63.9 106
Pentatomini Rhaphigaster
nebulosa
60 5.9 1.4 12 25
Piezodorini Piezodorus lituratus 3.2 28.6 17. 6 7.2 2.1 19
Strachiini Eurydem a sp. 3.2 1.1 2
Scutelleridae:
Eurygastrinae
Eurygaster maura 1.4 0.6 2
Reduviidae:
Harpactorinae
Nagusta goedelii 0.6 1
Total abundance 1 2 31 50 528 17 869 94 166 471
Abbreviations: B, bushes; c, centre; I, interface; L, leaf litter; orch., orchard; T, tree.

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DRISS et al.
that these effects are not significant within each zone and exhibit
inconsistency between zones (Table 4). No other effect was sig-
nificant. The two partial models, ‘Interface’ and ‘Centre’, used to
analyse the two zones separately, show that the abundance of P.
prasina in the samples is explained by relative humidity and tem-
perature: the ‘Interface’ model reveals a positive effect of the rel-
ative humidity of the leaf litter on P. prasina abundance (Table 4,
Figure 1), whereas the ‘Centre’ model shows a negative effect of
the temperature at the litter surface on the abundance of P. prasina
(Table 4, Figure 2).
The relative humidity threshold above which the majority of P.
prasina were observed in the ‘Interface’ zone was 69% and the tem-
perature threshold under which the most P. prasina were observed
in the ‘Centre’ zone was 7.5°C.
Concerning aggregation during overwintering, 70% of the leaf
litter samples in which P. prasina were found contained only one in-
dividual, and a maximum of five individuals were present in less than
1% of the samples (Figure 3).
3.2 | Reproductive status
A total of 72 P. prasina were collected in the overwintering sites, 53
in Cone traps and 42 in Circle traps. There were, 2.7 and 1.1 indi-
viduals per cone and Circle trap respectively (Figure 4). There was a
significant difference between the total abundance collected in the
two types of traps (χ2 = 3.69, p < 0.05, df = 2) as well as in the abun-
dance at the two different sites (χ2 = 5.24, p < 0.05, df = 1) (Figure 4).
Twenty-nine adults collected in the overwintering sites and 24
adults collected in the emergence traps hosted endoparasitoids,
that is, a total of 32% overwintering individuals were parasitised.
Analyses of the reproductive status were performed exclusively on
non-parasited individuals, that is, 23 females and 20 males collected
in the overwintering sites and 22 females and 13 males collected
during the following emergence period. From December to the end
of March, all the females presented an ovarian development in rank
zero (Figure 5) and none was fecundated (Figure 6). During the emer-
gence period, although more than 65% of the females still presented
an ovarian development rank of 0, some were already at a more
advanced stage of ovarian development (rank 1 or 3) and also had
spermatozoids in the spermatheca (Figures 5 and 6). In contrast, the
testes of all the males were full of living spermatozoids in both the
overwintering and the spring emergence periods.
Almost all the overwintering P. prasina colle c ted, wh ethe r male or
female, were brown, with less than 20% remaining green (Figure 7).
In contrast, more than 80% of the emerging male and female P. pr a-
sina collected were green (Figure 7).
4 | DISCUSSION
Overwintering is an important driver of arthropod population dy-
namics (Lawton et al., 2022) and may be pivotal to developing al-
ternative management programmes for insect pests. In this study,
we investigated the almost unknown overwintering ecology of P.
prasina, to explore new avenues for the development of IPM strate-
gies against this important hazelnut pest.
Our results show that P. prasina overwintered almost exclusively
in the leaf litter in all the natural ecosystems studied. Leaf litter is
often used as an overwintering habitat by Pentatomidae species
(McPherson et al., 2018; Table 1), but apparently varies between
populations of the same species. For instance, N. viridula, a spe-
cies phylogenetically close to P. prasina (Roca-Cusachs et al., 2022)
which shares the same habitat in spring- and summer (wild plants
and hazelnut trees, personal observ.), in the present study was only
found in human-made structures, as also reported by other authors
(Musolin, 2012), although Jones and Sullivan (1982) and Laterza
et al. (2023) observed this stink bug overwintering in leaf litter.
Leaf litter is a common overwintering habitat for insects be-
cause it helps them survive the harsh winter season in several ways
(Danks, 2006; Lee, 1989), such as by protecting them against natu-
ral enemies, but also against cold temperatures by improving their
supercooling capacity (Wagner et al., 2012), or preventing marked
TAB LE 4 Results of the three best fitting models (GLMM)
used to test the effect of the type of ecosystem, zone and abiotic
parameters on the abundance of Palomena prasina in leaf litter.
Model/variable Loglike- ratio Df p value
1) Full model
D5.45 10.020
Eco 2.27 30 . 518
HR 2.25 10.13 4
L0.45 10.500
Ts 1.71 10.192
UV 3.35 10.067
Year 0.82 10.364
Zone 0.07 10.795
Zone: Ts 4.50 1<0.050
Zone: L 4.52 1<0.050
2) Interface
D2.32 10.128
Eco 1.06 30.788
HR 6.41 1<0.050
L1.92 10.165
Ts 0.10 10.754
UV 1.42 10.233
Year 0.00 10.977
3) Centre
D2.14 10.144
Eco 1.08 20.581
HR 0.42 10.51 5
L3.17 10.075
Ts 9.3 4 1<0.010
UV 1.42 10.233
Year 0.00 10.977

8
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DRISS et a l.
temperature variations (Parajulee et al., 1996) Thus, abiotic param-
eters play an essential role for insects that overwinter in leaf litter.
This is also the case for P. prasina: our results show that GSB prefers
humidity levels above 69% and temperatures below 7.5°C, which
broadly corresponds to the climate characteristics of woods, the
natural environment of hazelnut trees (Al-Khayri et al., 2019) and to
which they are therefore more adapted.
Our study, based on a large sample, shows that P. prasina does
not aggregate in the overwintering sites. Adults of several pentato-
mid species aggregate at different periods of their cycle (Musolin &
Saulich, 2018), including during diapause (e.g. Table 1). Aggregation
behaviour may be related to mating, as is the case of the pentatomid
species Menida disjecta (Ulher), where mating was observed within
overwintering aggregations (Koshiyama et al., 1994). However, ag-
gregation is more generally considered to be a defence strategy
(Gamberale & Tullberg, 1996; Parrish & Edelstein-Keshet, 1999), for in-
stance, in the Spined citrus bug Biprorulus bibax (Breddin), whose win-
ter aggregations form a prickly mass hypothesised to repel predators
(Panizzi et al., 2000). In contrast, the overwintering defence strategy
of P. prasina may rely on hiding and being camouflaged by the leaf lit-
ter, as our results show that overwintering individuals were brown and
difficult to spot in the leaf litter, whereas they turned green after the
diapause period. Cryptic coloration in winter is often used by insects
to avoid predation. In the genus Chrysoperla, lacewings living in decid-
uous forests change colour from green to yellowish in autumn, while
those living in coniferous forests remain green, in each case to blend
FIGURE 1 Prediction of the abundance
of Palomena prasina in leaf litter in the
Interface zone of the four ecosystem
types, according to relative humidity.
Dashed line: CI; solid line: prediction
curve; ◇ 2021; ▲2022.
FIGURE 2 Prediction of the abundance
of Palomena prasina in the leaf litter at the
Centre zone of three ecosystem types,
according to temperature. Dashed line:
CI; solid line: prediction curve; ◇ 2021;
▲2022.

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DRISS et al.
in with the corresponding forest foliage and thereby avoid predation
(Duelli et al., 2014; Macleod, 1967). Winter defence strategies based
on colour changes have also been demonstrated in Pentatomidae. For
instance, Graphosoma lineatum (L.) is a usually red-striated species in
spring and summer whereas in late summer, individuals become pale-
brown striated and overwinter among dried grasses on the ground
(Tullberg et al., 2008). Johansen et al. (2010) showed that avian pred-
ators of G. lineatum need longer to find the pale-brown adults in the
dried grasses than the red ones. Colour changes during the winter
diapause have also been observed in N. viridula, where, in autumn,
prior to overwintering, adults turn from green to reddish brown, be-
come brown in winter and become green again at the beginning of
spring (Musolin, 2012; Musolin & Numata, 2003).
In the case of P. prasina, not only winter aggregation behaviour is
absent, but mating does not occur before the adults leave the over-
wintering sites in early spring. Indeed, although males of P. prasina
have active spermatozoids in their testes during the overwintering
period, the females remain sexually immature and do not mate during
that period. In many adult insects, diapause corresponds to the ar-
rested development of ovaries, testes, accessory glands and repro-
ductive structures, and mating behaviour is absent (Delinger, 2022).
The reproductive status of pentatomid species in winter and once
they emerge from their winter habitats, differs between species.
Although Oebalus poecilus (Dallas) and N. viridula behave in a similar
way to P. prasina (Santos et al., 2003), that is, do not mate in the
overwintering sites, species such as M. disjecta do mate just before
emergence (Koshiyama et al., 1993, 1994).
Colour changes during the winter often match diapause. This is
the case for N. viridula (Musolin & Numata, 2003) but also, for in-
stance, for Lygus Hesperus Knight (Hemiptera: Miridae) (Brent, 2012).
In our study, the changes in colour by P. prasina from green to brown
also correspond to diapause in females. Concerning males, although
active spermatozoids were present throughout the sampling period,
they could have been produced in autumn before the beginning of
FIGURE 3 Percentage of leaf litter samples hosting 1 to 5
Palomena prasina individuals (n = 600).
FIGURE 4 Abundance of Palomena prasina adults emerging from the leaf litter that were collected in the cone traps (20) and the Circle
traps (20) at both sites, (a wood and a hazelnut orchard).

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DRISS et a l.
diapause, meaning we were unable to resolve the diapause status of
males in our study.
The main objecti ve of the pre sent work was to exp loit the knowl-
edge gathered on the overwintering ecology of P. prasina, in order to
design new pe st ma nagement stra tegie s. Th e fac t that GSB over win-
ters in the le af lit ter of seve r al di ffer ent ecos yste ms an d that , in ad di-
tion, individuals overwinter alone, means controlling its populations
by destroying the overwintering sites is not a solution, in contrast
FIGURE 5 Stage of ovarian development (ranked 0 to 4) of Palomena prasina females collected weekly (a) at the overwintering sites, and
(b) in the cone and Circle traps.
FIGURE 6 Number of virgin and mated Palomena prasina females collected weekly (a) at the overwintering sites, and (b) in the cone and
Circle traps.

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DRISS et al.
to other species (e.g. Seiter et al., 2013). All the same, our results
do open new perspectives for the control of P. prasina. In particular,
the fact that no mating was found to take place in the overwintering
sites strongly suggests that mating takes place after overwintering
and thereby raises the question of how individuals that emerge sin-
gly from their overwintering site manage to find each other. Beyond
the framework of the present study, in several years, we observed
from April to May many large aggregations of post-overwintering P.
prasina indi vid ual s on th e bar k of willow an d bla ck po pla r tre es grow-
ing next to one of our sampling sites. Many mating events were tak-
ing place in these aggregations, which could mean sex pheromones
are involved in the attraction of partners. Sex pheromones have
been identified in several pentatomid species (Weber et al., 2017)
and have for instance been used for monitoring Euschistus heros
(F.) (Borges et al., 2011). However, group mating communication in
pentatomid species is generally multimodal, involving both long and
short-range signals (Čokl et al., 2019). Although short-range vibra-
tional signals have been reported for P. prasina (Polajnar et al., 2013),
long-range communication with chemical signals still requires inves-
tigation for this species.
It is also noteworthy that both cone and Circle traps succeeded
in collecting post-overwintering individuals, and cone traps proved
to be particularly efficient. As such, cone traps could be used to es-
tablish a Biofix, either for the first emerging individuals or for the
time they consistently emerge from diapause (Pak et al., 2022). This
could then be used to construct degree-day models to predict the
future presence of GBS at particular developmental stages in the
crop, as suggested for H. halys (Bergh et al., 2017 ).
Finally, unexpectedly, we found a large number of parasitised
individuals in the overwintering sites, corresponding to 32% of all
the individuals collected. Identification of these natural enemies of
P. prasina is still ongoing, but strategies to favour the presence of
parasitoids close to overwintering sites to enhance biological control
of pests is a promising option which now requires further study.
To conclude, our work on the overwintering ecology of P. prasina
points out three promising lines of research for developing meth-
ods to control this pest, in particular the use of emergence traps for
monitoring, the identification of long-range mating signals as attrac-
tants for traps, and the study of winter endoparasitoids as potential
biocontrol agents.
AUTHOR CONTRIBUTIONS
Laetitia Driss: Conceptualization; methodology; investigation;
writing – original draft; visualization; formal analysis; data cura-
tion. Rachid Hamidi: Conceptualization; methodology; project ad-
ministration; supervision; writing – review and editing. Christophe
Andalo: Formal analysis; methodology; visualization; writing – re-
view and editing. Alexandra Magro: Conceptualization; methodol-
ogy; supervision; project administration; validation; writing – review
and editing.
FIGURE 7 Proportion of brown and green Palomena prasina collected (a) at the overwintering sites, and (b) in the cone and Circle traps.

12
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DRISS et a l.
ACKNO WLE DGE MENTS
We thank L. Tournier for her invaluable assistance on the monitor-
ing of Cone and Circle traps, and S. Papillon, A. Jagueneau and G.
Vincent for general help during field work. We are also grateful to
all the farmers that provided access to their orchards, and the con-
tributors who responded to our call for witnesses. This work was
supported by Unicoque, the ANPN, in particular M. Thomas, and
the European Community [FEDER FSE 2019 7838010 (REPLIK)].
The laboratory ‘Evolution et Diversité Biologique’ is part of the
‘Laboratoire d'Excellence’ LABEX TULIP (ANR-10-LABX-41) and
LABEX CEBA (ANR-10-LABX- 25-01).
CONFLICT OF INTEREST STATEMENT
All the co-authors declare that they have no conflict of interest.
DATA AVAIL AB ILI T Y STATE MEN T
Raw data are available on the following link: h t t p s : / / d o i . o r g / 1 0 .
5 0 6 1 / d r y a d . z c r j d f n j t .
ORCID
Laetitia Driss https://orcid.org/0000-0003-2437-9599
Rachid Hamidi https://orcid.org/0000-0002-1651-8440
Christophe Andalo https://orcid.org/0000-0001-5528-3800
Alexandra Magro https://orcid.org/0000-0002-7043-0845
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How to cite this article: Driss, L., Hamidi, R., Andalo, C., &
Magro, A. (2023). Study of the overwintering ecology of the
hazelnut pest, Palomena prasina (L.) (Hemiptera:
Pentatomidae) in a perspective of Integrated Pest
Management. Journal of Applied Entomology, 00, 1–15.
https://doi.org/10.1111/jen.13206