The North American species Belonochilus numenius (Say, 1832) (Hemiptera: Heteroptera: Lygaeidae: Orsillinae) was first recorded in Europe in 2008, and is now present in most of the countries of Southern and Central Europe. The first specimen of B. numenius in Serbia was found in 2011 in Sremska Kamenica; it was later recorded in Zasavica, Mokrin and Novi Sad

Protić, Ljiljana

Šeat, Jelena

NEUROSURGERY ENTHUSIASTIC WOMEN SOCIETY

FIRST RECORDS OF THE ALIEN SYCAMORE SEED BUG BELONOCHILUS NUMENIUS IN SERBIA (HETEROPTERA: LYGAEIDAE)

University of Belgrade - Faculty of Biology: Open Journal Systems

 Acta entomologica serbica, 2016, 21: 13-19 UDC 595.754(497.11) DOI: 10.5281/zenodo.198280   FIRST RECORDS OF THE ALIEN SYCAMORE SEED BUG BELONOCHILUS NUMENIUS IN SERBIA (HETEROPTERA: LYGAEIDAE)   LJILJANA PROTIĆ1 and JELENA ŠEAT2  1 Natural History Museum in Belgrade, Njegoševa 51, 11000 Belgrade, Serbia E-mail: ljilja.protic@gmail.com 2 HabiProt, Bulevar Oslobođenja 106/34, 11040 Belgrade, Serbia E-mail: jelena@habiprot.org.rs    Abstract  The North American species Belonochilus numenius (Say, 1832) (Hemiptera: Heteroptera: Lygaeidae: Orsillinae) was first recorded in Europe in 2008, and is now present in most of the countries of Southern and Central Europe. The first specimen of B. numenius in Serbia was found in 2011 in Sremska Kamenica; it was later recorded in Zasavica, Mokrin and Novi Sad.  KEY WORDS: Belonochilus numenius, Hemiptera, invasive species, true bug    Introduction  The sycamore seed bug, Belonochilus numenius (Say, 1832) is a Nearctic invasive species with a continuously expanding range. Its native area of distribution is in Canada, the United States of America and Mexico (Slater, 1964; Wheeler, 1984; Ashlock & Slater, 1988; Maw et al., 2000; Sweet, 2000).  In recent years, the species has continuously expanded its range in Europe and has been found in thirteen South and Central European countries, as well as on Madeira (Fig. 1) (Aukema et al., 2013; Werner, 2014; Rabitsch & Heiss, 2015; Riba et al., 2015; Gogala et al., 2016).  Belonochilus numenius is a granivorous species and its primary hosts are trees of the genus Platanus, but it was also occasionally recorded on other deciduous trees in its native area (Wheeler, 1984). In Europe, individuals of B. numenius have been recorded exclusively on or near ornamental plane trees, mostly found in parks and tree allées, often on Platanus × acerifolia or London plane, which is a widely used hybrid in the 14 LJ. PROTIĆ & J. ŠEAT  urban areas of Europe (Matocq, 2008; Gessé et al., 2009; Küchler & Strauß, 2010; Hradil, 2011; Rabitsch et al., 2011; Torma 2012; Dusoulier et al., 2013; Kment & Cunev, 2013; Küchler & Kehl, 2013; Rabitsch & Heiss, 2015; Riba et al., 2015). The adults and nymphs of B. numenius have similar ecological needs; they spend most of their time feeding on plane seeds, rarely leaving globular fruits. In its native range, the species overwinters mostly in the egg stage on ripe fruits, but in the southern parts of the USA, adults may also survive winter hidden under the bark of plane trees. Wheeler (1984) investigated the biology of the species on populations from Pennsylvania, and the B. numenius in this area is multivoltine with 3-4 generations that overlap. The first generation of nymphs hatches in April-May, and the cycle of the last generation ends in September-October (Wheeler, 1984).     Figure 1. Distribution of Belonochilus numenius (Say) in Europe with the year of the first record in each country.   In most of the European countries where B. numenius is present, specimens are rarely noticed because they spend most of their lifetime on plane fruits, and this inconspicuous behavior, together with small population size, could adversely influence the recording of the species in new areas and countries. Thus far, there are no records of sycamore seed bug causing economic losses or aesthetically affecting urban plants (Steinmöller et al., 2014; Sweet, 2000). Nonetheless, there are indications that B. numenius could become a serious urban pest. In July 2015, species outbreaks were recorded at a few locations in northeastern Spain, and reports of public nuisance have forced local authorities to treat urban greenery with insecticides. These incidents designated B. numenius as an urban pest for the first time (Riba et al., 2015). How the species was introduced into Europe is still unclear, but there is certain probability that it was brought in with host plants and other goods, or by vehicles (Kment & Cunev, 2013; Küchler & Strauß, 2010; Matocq, 2008; Rabitsch & Heiss, 2015). Also, Carapezza & Cusimano (2014) suggest that wind could play an important role in passive dispersion, and the species spread throughout the continent. Belonochilus numenius in Serbia 15  Results and Discussion  1. Sremska Kamenica [UTM DR00] 24.05.2011. Photo Dragiša Savić (Fig. 2), det. Jelena Šeat, confirmed by Petr Kment. The first specimen from Serbia was just photographed, and the photo is posted on the personal website of the author (www.naturefg.com).  2. Zasavica: Ravnje [UTM CQ87] 10.09.2011. 1m, leg. Mihajlo Stanković, det. Ljiljana Protić.  3. Mokrin [UTM DR58] 13.10.2012. Photo Ivan Pančić, det. Andrej Gogala. The specimen was not collected, only photographed, and the photo is posted in the gallery of online Alciphron database (Šeat, 2014).  4. Novi Sad [UTM DR01]  20.03.2013. 1m; 06.04.2013. 1m, leg. Marko Šćiban, det. Ljiljana Protić. 29.06.2014. 1m, leg. Radislav Mirić, det. Ljiljana Protić.  All specimens are stored at the Entomological Collection of the Natural History Museum in Belgrade.   According to records from Serbia and the description of the species’ biology in its natural range (Wheeler, 1984), the adult individuals collected or photographed in Serbia may belong to at least two generations. The individuals recorded by Marko Šćiban in March and April may be overwintering adults surviving from the previous calendar year. The individual recorded by Radislav Mirić in June would be of the “first” generation, while the autumnal records by Mihajlo Stanković and Ivan Pančić would belong to the “second” generation. As the biology of European populations of B. numenius remains unstudied, our conclusions are based on Wheeler’s research (1984) on native populations and should be taken with caution.  As B. numenius was recorded only individually, at this stage it is not causing any damage to plane trees. It is necessary to monitor the species for several years and record its abundance. The individuals spend most of their life cycle inside the plane tree fruits, and this hidden life may adversely influence its recording in new areas.  Belonochilus numenius can be easily distinguished from European Orsillus species by the host plants (the genus Orsillus is trophically linked to conifers) and also externally visible characters (Gessé et al., 2009; Küchler & Strauß, 2010). Consequently, identification of the species by photos is often feasible, and photo-sharing websites and online databases could play an important role in the monitoring of B. numenius in Europe and Serbia.   Acknowledgments  The authors are grateful to colleagues Mihajlo Stanković, Marko Šćiban and Radislav Mirić for providing specimens; Dragiša Savić and Ivan Pančić for allowing us to use their photos of Belonochilus numenius; Andrej Gogala and Petr Kment for photo identification; Dietrich  Werner, François Dusoulier, Wolfgang Rabitsch and Attila Torma for sharing their papers with us. 16 LJ. PROTIĆ & J. ŠEAT    Figure 2. Records of Belonochilus numenius (Say) in Serbia (dots/codes indicate 10 x 10 km plots):   1 − Sremska Kamenica (DR00), 2 − Zasavica (CQ87), 3 − Mokrin (DR58), 4 − Novi Sad (DR01).  Belonochilus numenius in Serbia 17    Figure 3. The first recorded specimen of Belonochilus numenius (Say) from Serbia (photo by Dragiša Savić).   References  Ashlock, P. D. & Slater, A. (1988). Family Lygaeidae Schilling, 1829. Pp. 167-245. In: Henry, T. J. & Froeschner, R. C. (eds.) Catalog of the Heteroptera, or True Bugs, of Canada and the Continental United States. E. J. Brill, Leiden-New York-Københaven-Köln, 958 pp. Aukema, B., Rieger, Ch. & Rabitsch, W. (2013). Catalogue of the Heteroptera of the Palaearctic Region. 6, Supplement. The Netherlands Entomological Society, Amsterdam 629 pp. Carapezza, A. & Cusimano, C. (2014). Heteroptera in the aeroplancton of Palermo town, with two new records for Italy (Hemiptera Heteroptera). Il Naturalista Siciliano, 38(2): 367-380. Dusoulier, F., Maillot, R. & Dereumaux, V. (2013). Belonochilus numenius (Say, 1832): état de la progression de l’espèce et nouvelles localités dans le Sud de la France (Hemiptera Lygaeidae). L’Entomologiste, 69(3): 185-190. Gessé, F., Ribes, J. & Goula, M. (2009). Belonochilus numenius, the sycamore seed bug, new record for the Iberian fauna. Bulletin of Insectology, 62(1): 121-123. Gogala, A., Kamin, J. & Zdešar, M. (2016). Three new records of Heteroptera in Slovenia. Acta Entomologica Slovenica 24(1): 55-58. Hradil, K. (2011). Faunistic records from the Czech Republic – 315. Heteroptera: Lygaeidae: Belonochilus numenius (Say, 1831). Klapalekiana, 47: 261-262. Kment, P. & Cunev, J. (2013). First record of the alien seed bug Belonochilus numenius (Hemiptera: Heteroptera: Lygaeidae) in Slovakia. Entomofauna Carpathica, 25(2): 15-20. Küchler, S. & S. Kehl (2013). Erstfund für Belonochilus numenius Say, 1932 (Heteroptera: Lygaeidae) in Deutschland. Mitteilungen des Entomologischen Vereins Stuttgart 48: 89-90. 18 LJ. PROTIĆ & J. ŠEAT  Küchler, S. & Strauss, G. (2010). Belonochilus numenius (Say, 1832) (Heteroptera: Lygaeidae) – bald auch in Mitteleuropa? Beiträge zur Entomofaunistik, 11: 27-33. Matocq, A. (2008). Presence en France et en Corse d’un Heteroptere nearctique, Belonochilus numenius (Say, 1831) (Hemiptera, Lygaeidae, Orsillinae). Bulletin de la Societe Entomologique de France, 113: 533-534. Maw, H. E. L., Foottit, R. G., Hamilton, K. G. A. & Scudder, G. G . E. (2000). Checklist of the Hemiptera of Canada and Alaska. NRC Research Press, Ottawa, 220 pp. Rabitsch, W. (2010). True Bugs (Hemiptera, Heteroptera). Chapter 9.1. In: Roques, A., Kenis, M., Lees, D., Lopez-Vaamonde, C., Rabitsch, W., Rasplus, J.-Y. & Roy, D. B. (eds.): Alien terrestrial arthropods of Europe. BioRisk, 4(1): 407-433.  Rabitsch, W., Bräu, M. & Friess, T. (2011). Belonochilus numenius (Say, 1832) (Heteroptera: Lygaeidae) has reached Austria! Beiträge zur Entomofaunistik, 12: 148-149. Rabitsch, W. & Heiss, E. (2015).   Belonochilus numenius (Say, 1832), the sycamore seed-bug (Hemiptera: Heteroptera: Lygaeidae): new to Madeira. Heteropterus Revista de Entomología, 15(1): 83-86. Riba, J. M., Martí, I. & Goula, M. (2015). Updatig data on the sycamore bug Belonochilus numenius (Say, 1832) (Hemiptera: Lygaeidae) in Spain. Butlletí de la Institució Catalana d'Història Natural, 79: 157-163.  Savić, D. (2002). Fauna: Insecta: Hemiptera. http://www.naturefg.com Slater, J. A. (1964). A catalogue of the Lygaeidae of the world. Vol. I. University of Connecticut, Storrs, 778 pp. Steinmöller, S., Schrader, G. & Baufeld, P. (2014). Express-PRA zu Belonochilus numenius. Auftreten. Julius Kühn-Institut, Institut für nationale und internationale Angelegenheiten der Pflanzengesundheit am: 27.08.2014. (http://www.Pflanzengesundheit.jki.bund.de/dokumente/upload/.c155d_belonochilis_numenius_express_pra.pdf) [Consulted on 17 November 2015]. Sweet, M. H. (2000). Seed and chinch bugs (Lygaeoidea). Pp. 143-264. In: Schaeffer, C. W. & Panizzi, A. R. (eds.): Heteroptera of economic importance. CRC Press, Boca Raton, 828 pp. Šeat, J. (ed.) (2014). Alciphron - database on insects of Serbia (Heteroptera), HabiProt. alciphron.habiprot.org.rs [last visit 04/11/2016] Torma, A. (2012). A Belonochilus numenius (Heteroptera: Lygaeidae) adventiv polskafaj elso magyarorszagi elofordulasa. [First record of the alien sycamore seed bug Belonochilus numenius (Heteroptera: Lygaeidae) in Hungary]. Novenyvedelem, 48: 467- 468. Werner, D. J. (2014). Die amerikanische Platanen-Samen-Wanze Belonochilus numenius (Say, 1831) (Heteroptera: Lygaeidae, Orsillinae) als Neozoon in Europa und in Deutschland: Verbreitung und Biologie. Andrias 20, 245-250. Werner, D. J., Brandner, J., Muller, A. & Zapf, M. (2013). Ein Fund von Belonochilus numenius (Say, 1831) in Deutschland (Heteroptera: Lygaeidae) mit Diskussion zum Jahr der Erstbeschreibung der Art. Heteropteron, 39: 37 – 39. Wheeler, A. G. Jr. (1984). Seasonal history, habits and immature stages of Belonochilus numenius (Hemiptera: Lygaeidae). Proceedings of the Entomological Society of Washington, 86: 790-796.           Belonochilus numenius in Serbia 19  НАЛАЗИ АЛОХТОНЕ СТЕНИЦЕ BELONOCHILUS NUMENIUS  У СРБИЈИ   ЉИЉАНА ПРОТИЋ и ЈЕЛЕНА ШЕАТ    Извод  Неарктичка врста Belonochilus numenius (Say, 1832) 2008. године је први пут забележена на европском континенту и већ је регистрована у већини земаља Централне и Јужне Европе (Rabitsch & Heiss, 2015; Riba et all., 2015; Werner, 2014). Домаћини врсте B. numenius су различите врсте и хибриди платана (род Platanus), на чијим лоптастим плодовима ове стенице проводе највећи део времена, хранећи се семенима. Присуство врсте B. numenius у Србији је потврђено на неколико локација (Сремска Каменица, Засавица, Мокрин, Нови Сад), а прве јединке су забележене 2011. године. На основу налаза из Србије и описа биологије врсте у нативном ареалу (Wheeler, 1984), адулти који су ухваћени или фотографисани у Србији могли би да припадају најмање двема генерацијама. С обзиром на појединачне налазе, врста B. numenius у Србији за сада не представља опасност по урбано зеленило нити домаћинства.     Received: May 30th, 2016 Accepted: July 7th, 2016 

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FIRST RECORDS OF THE ALIEN SYCAMORE SEED BUG BELONOCHILUS NUMENIUS IN SERBIA (HETEROPTERA: LYGAEIDAE)

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NEUROSURGERY ENTHUSIASTIC WOMEN SOCIETY

University of Belgrade - Faculty of Biology: Open Journal Systems

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