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The western conifer seed bug, Leptoglossus occidentalis, is an alien invasive species of North American origin. Leptoglossus occidentalis was recorded for the first time in Arsoun-Metn, Lebanon in 2015. Adults and nymphs of L. occidentalis were collected by the authors from various locations in Lebanon and observed on two species of pine, Pinus pinea and Pinus brutia, on Juniperus excelsa and even on Cedrus libani. This could indicate its successful integration in the country and its presence on many coniferous tree species. Studies to investigate the behaviour and the economic impact of this alien insect species in Lebanon are recommended.
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Research Article
First records of the invasive species Leptoglossus occidentalis Heidemann (Hemiptera:
Coreidae) on dierent coniferous species including the cedars of Lebanon
Primeras citas de la especie invasora Leptoglossus occidentalis Heidemann (Hemiptera: Coreidae) en
diferentes especies de coníferas incluyendo los cedros del Líbano
Nabil Nemer1*, Yara El Khoury2, Elise Noujeim3, Yara Zgheib1, Eustachio Tarasco2 and
Torsten van der Heyden4
1Department of Agriculture and Food Engineering, Holy Spirit University of Kaslik, P.O. Box 446, Jounieh,
Lebanon. *E-mail: nabilnemer@usek.edu.lb
2Department of Soil Plants and Food Sciences, University of Bari Aldo Moro, Via Amendola 165/A, I-70126
Bari, Italy.
3National Center for Marine Sciences, National Council for Scientic Research - CNRS, P.O. Box 11-8281,
Ryad El Solh 1107 2260, 59, Zahia Selman street, Beirut, Lebanon.
4Immenweide 83, D-22523 Hamburg, Germany.
ZooBank: urn:lsid:zoobank.org:pub: DD0F3806-90B6-41E0-BB61-C438282C3951
https://doi.org/10.35249/rche.45.4.19.01
Abstract. The western conifer seed bug, Leptoglossus occidentalis, is an alien invasive species of North
American origin. Leptoglossus occidentalis was recorded for the rst time in Arsoun-Metn, Lebanon
in 2015. Adults and nymphs of L. occidentalis were collected by the authors from various locations in
Lebanon and observed on two species of pine, Pinus pinea and Pinus brutia, on Juniperus excelsa and
even on Cedrus libani. This could indicate its successful integration in the country and its presence on
many coniferous tree species. Studies to investigate the behaviour and the economic impact of this
alien insect species in Lebanon are recommended.
Key words: Cedrus libani, distribution, Heteroptera, western conifer seed bug.
Resumen. La chinche de las coníferas occidental, Leptoglossus occidentalis, es una especie exótica
invasora de origen norteamericano. Leptoglossus occidentalis se registró por primera vez en Arsoun-
Metn, Líbano en 2015. Los autores recolectaron adultos y ninfas de L. occidentalis en varios lugares
de este país y los observaron en dos especies de pino, Pinus pinea y Pinus brutia, en Juniperus excelsa e
incluso en Cedrus libani. Esto podría indicar su establecimiento y naturalización en el país y su presencia
en diversas especies de coníferas. Se recomiendan estudios para investigar el comportamiento y el
impacto económico de esta especie invasora en el Líbano.
Palabras clave: Cedrus libani, chinche de las coníferas occidental, distribución, Heteroptera.
Introduction
The adult of Leptoglossus occidentalis Heidemann, 1910 is a large, reddish brown bug
measuring 15 to 20 mm, having white zigzag band across the middle of the hemelytra,
deltoid pronotum and lanceolate foliaceous metatibial dilations (Fent and Kment 2011).
Received 10 September 2019 / Accepted 30 September 2019 / Published online 16 October 2019
Responsible Editor: José Mondaca E.
Nemer et al.: First records of Leptoglossus occidentalis on dierent coniferous species.
508
The bug attacks conifers and during winter hides in holes of barks, in litter, or inside
houses, even causing damage to plumbing materials and biting humans (Fent and Kment
2011; Ingels and Haviland 2014; Faúndez et al. 2019). About 40 species of conifers (family
Pinaceae) can be hosts to the western conifer seed bug, mainly in the genera of Pinus,
Pseudotsuga, Abies, and Picea (McPherson et al. 1990; Barta 2009; Fent and Kment 2011).
Leptoglossus occidentalis is native to the western areas of North America and started to
spread out of the country after World War II. In 1992, it was reported in Pennsylvania
after a period of silence and its range started to extend around the world (van der Heyden
2019a). The western conifer seed bug reached Europe in 1999 by invading Italy and was
reported later from Albania, Austria, Belgium, Bosnia and Herzegovina, Bulgaria, Croatia,
the Czech Republic, Denmark, France, Georgia, Germany, Greece, Hungary, Ireland, the
Isle of Man, Kosovo, Liechtenstein, Luxembourg, Malta, Moldova, Monaco, Montenegro,
the Netherlands, North Macedonia, Norway, Poland, Portugal, Romania, Russia, Serbia,
Slovakia, Slovenia, Spain, Sweden, Switzerland, Turkey, Ukraine and the United Kingdom
as well as Morocco and Tunisia in Africa, China, Japan, Kazakhstan and South Korea in
Asia, Costa Rica in Central America and Argentina and Chile in South America (van der
Heyden 2017, 2018b, 2018c, 2019a, 2019b, 2019d; Kun and Masciocchi 2019). It was found
near Lebanon in 2016 in eastern Turkey (Özgen et al. 2017) and has been recently reported
in the northern part of the Golan Heights (van der Heyden 2018a) and in the western
Galilee (van der Heyden 2019c). In February 2015, the presence of this new alien invasive
insect in Lebanese stone pine woods in Arsoun in Mount Lebanon was conrmed (Nemer
2015).
Leptoglossus occidentalis feeds on seeds of conifers and can cause severe damages
especially in pine stands. Starting 1999, a sudden decrease in pine nut production was
observed in Italy and later on in many other Pinus pinea L. nuts producing countries (Bates
et al. 2002). Aected cones were associated with remnants of saliva, puncture holes on the
seed’s pericarps and the presence of L. occidentalis on the trees (Strong et al. 2001). In fact, L.
occidentalis bugs, both adults and nymphs, have long sucking piercing mouthparts they use
to suck out the seed endosperm causing depletion and infertility of the seeds (Klass 2009;
Ingels and Haviland 2014) leading to nut yield decrease (Nemer 2015). In Italy, serious
losses in commercial pine nut production were recorded after L. occidentalis introduction
in 1999 (Roversi 2009). Dried seeds and cones induce conelets abortion and loss of nut
production. In several US states, Bates et al. (2000a, 2000b, 2002) reported the eect of L.
occidentalis on abortion of cones of Douglas r trees, Pseudotsuga menziesii (Mirb.) Franco,
as well as its direct damage by depletion of the lipid and protein content of the seed up
to its complete emptying. Also, their mouthparts carry fungal yeast, Eremothecium coryli
Kurtzman, which cause discolouration of seeds (Ingels and Haviland 2014). Equally, Luchi
et al. (2012) veried the ability of L. occidentalis of vectoring Diplodia pinea (Desm.) J.J. Kickx
conidia, an endophytic fungus that colonize green tissues. The western conifer seed bug
could spread the pathogen to new host plants. In addition, it can directly infect new cones
and shoots (Tamburini et al. 2012).
Following the rst record of L. occidentalis in Lebanon, this study aims to provide the
distribution and occurrence of this insect and its host trees range in the country.
Materials and Methods
The study area expended over Lebanon from the south to the north where coniferous
plantations exist. The distribution of L. occidentalis in Lebanon was studied all over the year
from 2015 until 2018.
The insects were searched for on dierent coniferous plants, mainly Pinaceae family and
to a lesser extent the Cupressaceae. Adults and nymphs were expected to be found around
Revista Chilena de Entomología 45 (4) 2019
509
the cones, thus trees bearing newly formed cones were exclusively chosen for insect’s
collection. Sweep netting and knocking on branches techniques including the Japanese
umbrella were used to catch the insects. During overwintering when the temperature
decreases, adults were searched in old and dead trees, among litter, barks and shrubs. The
insects we encountered over the years were morphologically identied according to Fent
and Kment (2011). All insects caught were deposited at the entomological collection of the
entomology laboratory at the Faculty of Agricultural and Food Sciences of the Holy Spirit
University of Kaslik.
Results
The presence of L. occidentalis in Lebanon was conrmed shortly after its rst detection
in 2015. However, starting 2012 a major threat was encountered in stone pine stands,
referred to as the dry cone syndrome associated with empty pine seed. For this reason,
invasive western conifer seed bug could have been introduced and established for years
before its rst detection. Considering the rapid spreading of the species, being recorded in
Turkey in 2009 reinforces this hypothesis.
Adults and nymphs of L. occidentalis were found in 25 other localities (Figs. 1, 2): Bkassine,
Qaitouli, Ras El Matn, Salima Baabda, Qsaybeh Baabda, Deir El Harf, Bzebdine, Qortada,
Jouret Arsoun, Zandouka and Bhamdoun. Additionally, other specimens were collected
from Ehden nature reserve, North Lebanon and Dlebta in Mount Lebanon, and lately one
adult insect was found in the nature reserve of Tannourine (Fig. 1). Several ndings of
specimens indicate that L. occidentalis is now well implemented in the three main regions
of pines forests in Lebanon, namely Bkassine (south Lebanon), Mount Lebanon and the
North.
Figure 1. Distribution map of Leptoglossus occidentalis Heidemann in Lebanon.
1
Nemer et al.: First records of Leptoglossus occidentalis on dierent coniferous species.
510
Most specimens in Lebanon were collected from P. pinea, then Pinus brutia Ten., while in
North of Lebanon individual adults as well as nymphal stages were captured in Ehden on
Juniperus excelsa M. Bieb. (Cupressaceae) and on Cedrus libani A. Rich (Pinaceae). This insect
has never been reported on the two latter tree species, therefore C. libani and J. excelsa are
reported as new host plants of L. occidentalis.
Discussion
The species P. pinea is well established in Lebanon and is the second emblematic tree
after C. libani. This invasive bug can aect natural regeneration of the rst two emblematic
trees in the country, in addition to the reduced pine nut yield and conelet losses that
pine growers are suering of during the past six years (Mutke et al. 2017). However, bug
establishment is still limited to P. pinea stands as the highest insect population was found in
stone pine stands. In Lebanon, stone pine extends over around 12,740 ha which represent
9.33% of the total forest cover in Lebanon (FAO 2005). Therefore, this insect pest has greater
impact since it is aecting the yield production of pine nuts, one of the major economical
commodities in non-wood forest products and which contribute to the living of at least
1000 families (Nemer 2015).
In North America, the native country of L. occidentalis, a single generation was observed
per season (Jacobs 2002). Overwintering adults emerge from their shelters between mid-
spring (1st of May) and early June to mate, feed and lay eggs (Fent and Kment 2011); they
live until early August (FGC 2011). Females lay their barrel shaped eggs on needles between
Figure 2. Adult specimen of the western conifer seed bug, Leptoglossus occidentalis Heidemann, from
Arsoun, Lebanon, caught in 2015 (Photograph: Staan Kyrk). Scale: 5 mm.
2
Revista Chilena de Entomología 45 (4) 2019
511
mid-June and early August. Depending on weather conditions, eggs hatch in 10-15 days
(Klass 2009; Jacobs 2002; Fent and Kment 2011) pass through ve nymphal stages and
become adults in 35-40 days (Fent and Kment 2011). However, the insect has an ability to
adapt, population density and number of generations vary depending on rainfall, food
availability, natural enemies and many other factors. Even though the bug is univoltine in
North America, observations show the presence of three generations in Mexico (Mitchell
2000) and two generations in Sicily (Maltese et al. 2009). Also, Tamburini et al. (2012)
estimated that L. occidentalis is multivoltine in Canada. In Lebanon, the warm weather
may result in increase in the number of generations during the year, therefore higher
damage level on pines. Adults were found in January, March, July, August, September,
October and November in the surveys conducted. These records that extend along the
aforementioned months imply the presence of two generations per year, conrmed by the
presence of nymphal stages one and two in the same location in the months of May and
June and then in August. The prevalence of a warm weather most of the year strengthens
this hypothesis too.
According to its spatiotemporal distribution in Lebanon there may be a strong possibility
that the western conifer seed bug has established a vital population and we should be alert
of the economic and ecological consequences of this event on the cedars of Lebanon and
the coniferous forests in general.
Acknowledgements
This work was funded partially through TCP/LEB/3501BABY funded by FAO. The
authors would also like to acknowledge the National Council for Scientic Research of
Lebanon (CNRS-L) for granting a doctoral fellowship to Yara El Khoury.
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... Recently, L. occidentalis has been reported from Costa Rica in Central America (van der Heyden, 2019a), from Argentina (Kun & Masciocchi, 2019), Chile (Faúndez et al., 2017) and Uruguay (Faúndez & Silvera, 2019) in South America as well as from the Golan Heights (van der Heyden, 2018), Israel (van der Heyden, 2019c), Lebanon (Nemer, 2015;Nemer et al., 2019) and Palestine (Handal & Qumsiyeh, 2019) in the Middle East. The species occurs in Iran, too (Hassan Ghahari, personal communication). ...
... Recientemente, L. occidentalis ha sido reportada desde Costa Rica en América Central (van der Heyden, 2019a), hasta Argentina (Kun & Masciocchi, 2019), Chile (Faúndez et al., 2017) y Uruguay (Faúndez & Silvera, 2019) en América del Sur, así como en los Altos del Golán (van der Heyden, 2018), Israel (van der Heyden, 2019c), Líbano (Nemer, 2015;Nemer et al., 2019) In the Maghreb, L. occidentalis has been reported from Morocco (Gapon, 2015;van der Heyden, 2019b) and Tunisia (Ben Jamâa et al., 2013) so far. On 8.XII.2019, a photograph of a dead adult specimen of L. occidentalis was taken in the area of Algiers at the Mediterranean coast of Algeria. ...
... Originària de la costa est d'Estats Units, actualment aquesta espècie està distribuïda àmpliament per Europa, i Amèrica Central i del Nord (Figura 12.2). L'espècie ha estat citada a l'oest d'Àfrica (Nemer et al., 2019). El 2020, es va detectar per primera vegada a Finlàndia, Xipre, Guatemala i Argentina. ...
... From 2012, similar symptoms have been detected in Lebanon; dry cone syndrome (DCS), associated with empty pine seeds and dried conelets, has been found in many stone pine stands across the country [12]. These symptoms are reported to be caused either by the invasive conifer seed bug Leptoglossus occidentalis [18][19][20][21][22][23], or by other biotic and abiotic factors as a result of climate change and droughts, as reported by others [2,4,[24][25][26]. Additionally, Pinus pinea is threatened by the fungus Diplodia pinea, and an association between L. occidentalis and this fungus was detected in Mediterranean forests [27]. ...
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The family Coreidae is distributed worldwide, but these phytophagous bugs are most abundant in the tropics and subtropics. In the Neotropical region, all of the subfamilies and 16 tribes are represented. In tropical ecosystems, these bugs feed on herbs and shrubs in open areas of forests as well as at the forest edge. Some species are spectacularly colored, and unusual expansions of antennae, humeral angles, femora, or tibiae occur in many groups. Some of them move lazily even when disturbed and hardly fly to escape; others are extremely nimble, fast flying away when disturbed. They are frequently encountered in crops, representing important pests in several commodities. No one common name is universally accepted for the family, and none of the frequently used names (e.g., squash bug, leatherbug, leaf-footed bug, Randwanzen) are collectively appropriate for all members of the family. © Springer Science+Business Media Dordrecht 2015. All rights reserved.
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