Hemiptera: Heteroptera: Pentatomidae

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https://doi.org/10.11646/zootaxa.4347.2.13 http://zoobank.org/urn:lsid:zoobank.org:pub:512C8885-E166-4F26-8F68-31A4E16D1D95

Acrosternum heegeri Fieber, 1861 (Hemiptera: Heteroptera: Pentatomidae), another Mediterranean bug expanding to the north BALÁZS KÁROLYI1 & DÁVID RÉDEI2,3 1

Királyok útja 184. 2/7, H-1039 Budapest, Hungary. E-mail: [email protected] Institute of Entomology, College of Life Sciences, Nankai University, Weijin Rd. 94, 300071 Tianjin, China. E-mail: [email protected] 3 Department of Zoology, Hungarian Natural History Museum, Baross u. 13, H-1088 Budapest, Hungary 2

Abstract Acrosternum heegeri Fieber, 1861 (Hemiptera: Heteropera: Pentatomidae: Pentatominae: Pentatomini), a Holomediterranean-Turanian shield bug species, is recorded for the first time from Hungary, representing the first known occurrence of the species in Central Europe. The species is illustrated, its geographic distribution is reviewed. The occurrence of A. heegeri in two localities in Budapest, regular records from one of the localities in the years 2015 and 2016, and the finding of an overwintering individual indicate the presence of a stable population in the city; the species is probably already established and it is locally abundant. Its further spread in Europe is expected. Key words: Heteroptera, Pentatomidae, Acrosternum heegeri, new locality, area expansion, biological invasion, Europe

Introduction Acrosternum Fieber, 1860, is a moderately species-rich genus of shield bugs (Hemiptera: Heteroptera: Pentatomidae) distributed in the Afrotropical, Palaearctic and Oriental Regions. The genus was defined in different ways over the last century; particularly its separation from the closely related Nezara Amyot & Serville, 1843, and Chinavia Orian, 1965, has been a subject of disagreement (Freeman 1940, Linnavuori 1972, 1982). Rolston (1983) reviewed the problem and offered a reclassification which has been accepted by the overwhelming majority of subsequent authors. Fourteen species are currently recognized; the West Palaearctic fauna was treated by Wagner (1959) and Ribes & Pagola-Carte (2013), the Afrotropical fauna by Linnavuori (1972, 1982) (defining Acrosternum broadly, including members of Chinavia), and the fauna of the Arabian Peninsula by Linnavuori & Al-Safadi (1993). Acrosternum heegeri Fieber, 1861, is a species distributed in the Mediterranean Basin and the Middle East (Fig. 3). As its northernmost stable populations were known to occur in the coastal region of Slovenia and Croatia (Protić 2001, Gogala 2008, Ribes & Pagola-Carte 2013), its occurrence in the present area of Hungary was not expected. For our considerable surprise several individuals were collected and observed in different localities of Budapest during 2015 and 2016. The present paper provides the first record of this species from Hungary and in the same time from Central Europe, with illustrations and a review of the distribution of the species. The circumstances of finding the species in Hungary and the significance of this new record are also discussed.

Material and methods Most of the individuals of A. heegeri examined during the present study were collected from or observed on a white sheet illuminated by a 125 W Mercury bulb, set on the balcony of a 2nd floor flat in an apartment building

392 Accepted by D. Rider: 14 Sept. 2017; published: 13 Nov. 2017

situated in the Békásmegyer suburban area of northern Budapest. The locality is an urban habitat densely intermixed with fragments of green patches, particularly extensive remnants of the former riverine forest vegetation along the river Danube at a distance of about 300 m. The first specimens were observed during late August and early September of 2015 (more precise dates are not available, no voucher specimens have been preserved). During 2016 the light was operated on 22.vi., 24.vi., 22.vii., 24.vii. and 18.viii., approximately between 10 pm to 1 am of the next day. Individuals were observed in all of these nights; voucher specimens have been collected and deposited in the Hemiptera collection of the Hungarian Natural History Museum (HNHM), Budapest. Besides specimens attracted to light, a reddish brown, obviously overwintering individual was found hiding in a box on the same balcony on 8.iv.2016, and an individual sitting on a wall and another one on a planted forsythia shrub (Forsythia × intermedia Zabel, Oleaceae) were observed. Digital photographs (Figs. 1–2) were taken with a Nikon D90 camera equipped with an AF-S Micro Nikkor 60 mm f/2.8G ED lens.

Taxonomy Acrosternum heegeri Fieber, 1861 (Figs. 1–3) Acrosternum heegeri Fieber, 1861: 331. Syntypes: südliches Europa [= southern Europe]; Muséum National d’Histoire Naturelle, Paris (Orian 1965). The nomenclatural history and synonyms of the species were reviewed by Rider (2006).

Proposed Hungarian name. Rőtcsápú vándorpoloska Material examined. Hungary, Budapest, Békásmegyer, Királyok útja, 47°35'51.9"N 19°3'59.4"E, 2nd floor balcony, at light, 24.vii.2016, leg. B. Károlyi (six males and eight females deposited in the HNHM). New record to Hungary. Diagnosis. Body rather uniformly green, with pronotum, costal margin of fore wing, and connexivum narrowly pale, without contrasting markings on scutellum; membrane uniformly whitish; integument smooth; head about 1.2 times as broad as its length along midline, clypeus anteriorly free; antenna contrastingly bicolorous, scape and basipedicellite green, distipedicellite and basiflagellum red except of their bases, distiflagellum red; apex of labium generally surpassing middle of abdominal ventrite III (Figs. 1–2). Genitalia of the male were accurately illustrated by Linnavuori (1972), Fuente (1975), Josifov & Heiss (1989), and Ribes & Pagola-Carte (2013), and less accurately by a number of other authors. Intraspecific variability. Overwintering individuals are reddish brown. Individuals with the head and anterior portion of pronotum being pale yellow occur sporadically in all populations in low frequency. Bionomics, economic importance. The species is apparently polyphagous, feeding on both gymnosperms and angiosperms. Published data on its host plants were summarized by Ribes & Pagola-Carte (2013) and Ghahari et al. (2014). Mehrnejad (2010) claimed that it is a significant pest of the pistachio, Pistacia vera L. (Anacardiaceae) in Iran; besides its direct damage, it is also a vector of Eremothecium coryli (Peglion) Kurtzman (Saccharomycetaceae), a plant pathogen fungus causing stigmatomycosis (Ershad & Barkhordary 1974). Distribution. A Holomediterranean-Turanian species (Carapezza 1997, Ribes & Pagola-Carte 2013). Its distribution was summarized by Rider (2006), Aukema et al. (2013b) and Ribes & Pagola-Carte (2013); a rather incomplete distribution map was provided by Tamanini (1981: 135, fig. 45) which is updated now (Fig. 3). In the Mediterraneum the distribution of the species strictly follows the vegetational zone of Mediterranean forests, woodlands and scrub; in the Middle East, however, it extends far into the zone of temperate deciduous and mixed forests eastwards. The species has been recorded from Iraq by Al-Ali (1968, 1977) and a few subsequent authors; all of these records are doubtful, some of them, e.g. the one by Augul et al. (2015: 125, fig. 2a) are evidently based on misidentification and pertain to other species, most probably A. breviceps (Jakovlev, 1889). Records from “Arabien” [= Arabia, referring either to Saudi-Arabia or the Arabian Peninsula] and Socotra (Distant 1903, Stichel 1961) are erroneous and at least partly pertain to A. arabicum Wagner, 1959 (Linnavuori & Al-Safadi 1993); the voucher specimen referred to by Distant could not be found in the Natural History Museum, London, and the ACROSTERNUM HEEGERI EXPANDING TO THE NORTH

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species was not collected during a recent thorough faunistic exploration of Socotra (A. Carapezza & P. Kment, pers. comm.).

FIGURES 1–3. Acrosternum heegeri Fieber, 1861. Fig. 1, a male collected in Budapest, dorsal view; Fig. 2, same, ventral view (scale bar in mm); Fig. 3, geographic distribution in the Palaearctic Region. Localities in the Arab Peninsula are omitted. White circles represent previous literature records, red circle indicate the new record. The zone of Mediterranean forests, woodlands and scrub is marked with red.

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The species has been recorded from Madagascar (Signoret 1861, as Rhaphygaster incerta), but no subsequent author confirmed this record (Cachan 1952), therefore its occurrence in the island is considered as doubtful; Signoret’s record is probably based on mislabelled or misidentified specimens and it potentially pertains to Chinavia bergrothi (Horváth, 1904). Old records from Belgian Congo, now Democratic Republic of the Congo (Schouteden 1909), British and Dutch East Africa, now Kenya ad Tanzania (Jeannel 1913) were considered as questionable by Linnavuori (1972). The figure of the genital capsule drawn after a male from East Africa (Kilimanjaro, Tanzania) (Cachan 1952: 442, fig. 525) is apparently different from the condition found in A. heegeri (posterior margin distinctly concave at midline, not nearly transversely truncate as in A. heegeri) and therefore probably shows another species. Therefore we consider all Afrotropical records, including those listed above as well as those provided by Distant (1901), Schouteden (1905, 1929), Villiers (1950, 1952, 1954, 1956) and Robertson (2009) as in need of confirmation. The records from the Seychelles (Distant 1913, Orian 1965, Roche 1977, Gerlach 2003, Gerlach et al. 2006) are controversial and data published by different authors are conflicting, therefore we consider the presence of the species in the Seychelles and the Mascarene Archipelago as in need of verification. The available information on the distribution of the species is summarized below. For countries for which comprehensive faunistic studies summarizing earlier literature are available, e.g. Italy (Servadei 1967), the former Yugoslav countries (Protić 2001), Iran (Ghahari et al. 2014), Spain and France (Ribes & Pagola-Carte 2013), earlier references are not cited. EUROPE. Spain: numerous localities in Navarra, Aragón, Catalunya, Valencia, Madrid, Andalucia, Baleares: Eivissa Is., Mallorca Is., Menorca Is., Cabrera Is. (Ribes & Pagola-Carte 2013). Portugal: Beja (Oliveira 1895), Alfeite (Seabra 1926), Várzea da Orada, Serra de Monchique (Pissarro 1951). France: numerous localities in the Departments of Pyrénées-Orientales, Aude, Hérault, Gard, Ardèche, Vaucluse, Bouches-du-Rhône, AlpesMaritimes, Alpes de Haute Provence, and Corse (Ribes & Pagola-Carte 2013). Monaco (Ponel et al. 2013). Italy: Liguria, Emilia Romagna, Toscana, Umbria, Lazio, Puglia, Basilicata, Calabria, Sicilia, Sardegna, Giglio Is., Tremiti Is., Pantelleria Is. (Servadei 1967, Tamanini 1981, Carapezza 1995). Slovenia: Dragonja, Pišine (Gogala 2008). Croatia: Rijeka, Sveta Jelena, Vrana, Kaštel Stari, Sućurac, Split, Janjina, Dubrovnik, Korčula Is., Trstenik Is., Lopud Is. (Protić 2001), Lošinj Is. (Furlan & Gogala 1995). Bosnia and Herzegovina: Domanovići (Protić 2001). Montenegro: Stari Bar, Kotor (Protić 2001). Albania: Lushnjë (Misja 1973). Hungary: Budapest (new record). Romania: Moldova Nouă (Kis 1984). Bulgaria: Sandanski (Göllner-Scheiding & Arnold 1988), Kresna Gorge (Simov 2001). Macedonia: Udovo, Stari Dojran (Protić 2001). Greece: Kalambaka (Günther 1990), Argolis (Ribes & Pagola-Carte 2013), Crete: several localities (Heiss 1983, Heckmann et al. 2015). Ukraine: Yalta, Alushta (Jakovlev 1906); earlier records from Kharkiv are erroneous (Putshkov & Putshkov 1996). Russia: Caucasus (Kerzhner & Jaczewski 1964). Turkey (European part): Karaağaç (Fent & Aktaç 2007). — ASIA. Turkey (Asian part): Adana, Antalya, Diyarbakır, Gaziantep, Hatay, İzmir, Manisa, Mersin, Muğla, Kayseri, Şanlıurfa Provinces (Önder et al. 2006), Manavgat, Posof, Artvin, Şenkaya, Erenköy, Kemaliye, Datça, Trabzon (Külekçi et al. 2009), Osmangazi (Gençer et al. 2004), Tapan, Ekbaz (Hoberlandt 1956), Atabey (Karsavuran et al. 2008), Bursa (Kaya & Kovanci 2004), Mardin (Özgen et al. 2005), Aksu, Kepez, Serik, Karacabey, İspir, Kahramanmaraş (Yazici et al. 2014), Bodrum (Tezcan et al. 2013), Kayseri (Ribes & Pagola-Carte 2013). Cyprus: Akrotiri (Lindberg 1948). Syria (Frey-Gessner 1881). Israel: env. of Jericho (Hoberlandt 1952), Rehovot (Linnavuori 1960). Jordan: several localities around Amman (Katbeh et al. 2000). Georgia: Sukhumi (Kiritshenko 1939). Azerbaijan: Aresch [= Agdash] (Sienkiewicz 1964), Absheron, Agdzhabedin [= Aghjabadi] Shamkhor [= Shamkir] Distr., Kirovabad [= Ganja] (Gidayatov 1982). Iraq? (Al-Ali 1968, 1977). Iran: Ardabil, Bushehr, Fars, Hormozgan, Khuzestan, Lorestan, East Azarbaijan, Golestan, Guilan, Mazandaran, Kerman, Khorasan, Sistan & Baluchestan, Tehran (Ghahari et al. 2014). Afghanistan: Sarobi [= Surobi] (Hoberlandt 1984). Pakistan: Rahim Yar Khan (Ahmad & Rana 1989). — NORTH AFRICA. Madeira (Ribes & Heiss 2008). Canary Islands: Tenerife (Aukema et al. 2006), La Palma (Aukema et al. 2013a). Morocco: Debdou, Oudja, Berkane, Ras Foughal, Fès [= Fez], Asni, Dar Drius (Vidal 1937, 1949), Marrakech [= Marrakesh] (Ribes & Pagola-Carte 2013). Algeria: Biskra (Lethierry 1889, Deghiche-Diab et al. 2015), Tahount Arak, Mouydir, Imarera, Amguid (Bergevin 1934), Oued R[h]iou, Chellala, Teniet el Haad [= Theniet el Had], Mt. Ouarsenis, Tiaret (Sienkiewicz 1964), Oued Marsa (Wagner 1965), Boufarik (Ribes & Pagola-Carte 2013). Tunisia: Hadjeb el Aioun [= Hajeb El Ayoun], Porto Farina [= Ghar al Milh], Kairouan (Sienkiewicz 1964), Korbous, Téboursouk, Tabarka, Barrage Mellègue, Ousseltia, Thala, Gafsa (Carapezza 1997). Libya: Tripoli, Mellaha, El Giofra

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(Mancini 1937), Serti [= Sirte], Jebel Akhdar Messa, El Merj [= Marj], Tobruck [= Tobruk] (Eckerlein & Wagner 1970). Egypt: Cairo, Meadi, Siwa (Linnavuori 1964), Zaranik Protectorate (El-Moursy et al. 2001). — AFROTROPICAL REGION. Senegal? (Villiers 1956). Mali? (Robertson 2009). Niger? (Villiers 1950, 1954). Benin? (Villiers 1952). Nigeria? (Robertson 2009). Sudan? (Villiers 1956). Ethiopia? (Schouteden 1905, 1929). Eritrea? (Robertson 2009). Gabon? (Distant 1901). Democratic Republic of the Congo? (Schouteden 1909). Kenya? (Jeannel 1913). Tanzania? (Jeannel 1913). Madagascar? (Signoret 1861). Rodrigues Is.? (China 1926). Seychelles?: Mahé Is.?, Silhouette Is.?, Aride Is.? (Roche 1977, Gerlach 2003, Madl 2006).

Discussion Species of the genus Acrosternum are of subtropical and tropical distribution. Accordingly, in Europe they are restricted to the Mediterranean Basin, and no species are native in the neighbouring continental areas. A single individual of a closely related congener, A. millierei (Mulsant & Rey, 1866), was recorded from western Hungary a few years ago (Kondorosy 2005), but as it has not been collected again, this record was considered as due to accidental introduction or immigration (Kondorosy 2012). So far A. heegeri has been strictly restricted to the Mediterranean climatic zone in Europe. The single record conspicuously falling outside of this range is the occurrence in Caraș-Severin County, southwestern Romania (Kis 1984), an area of humid subtropical climate. As the Romanian fauna of true bugs is poorly known, it is unclear whether the species is native in this region, or the above record is due an isolated event of introduction or immigration. The first Hungarian specimens of A. heegeri were observed during late August and early September of 2015. During five collecting events between late June and mid-August in 2016, approximately ten, sometimes even more individuals were observed on each occasion. Besides of the specimens observed and captured at the locality in Királyok útja, two individuals were found in Montevideo street of Békásmegyer suburban area of Budapest, at a distance of about 5 km south of the previous one (M. Lukátsi, pers. comm.). The way of arrival of A. heegeri to Hungary is unknown. Considering that the newly discovered localities in Budapest are situated at a distance of about 430 km from the nearest area where native populations are known to exist in the coastal region of Slovenia and Croatia, direct spread seems unlikely. As Budapest is a major node of national and international transportation, passive human-assisted dispersal seems the most probable. The ability of the species to spread long distances via human transport is also indicated by interceptions in the USA in shipments originating from Israel (Hunt 1959) and Spain (Mumford 1967). The abundance of the species in two consecutive years and the finding of an overwintering individual in early April indicates that the species is able to overwinter in central Hungary, it has apparently already established and it is abundant in the habitats surrounding the site. A rapid area expansion of a taxonomically related pentatomid, Nezara viridula (Linnaeus, 1758), has recently been documented (Rabitsch 2008). This circumtropical species has been restricted to the Mediterranean Basin until the early 2000s when it started to spread to the north; reproducing populations were reported from Hungary (Rédei & Torma 2003, Rédei & Vétek 2005), the United Kingdom (Barclay 2004, Shardlow & Taylor 2004), southwestern Germany and northern Switzerland (Werner 2005), and most recently from Slovakia (Vétek & Rédei 2014, Hemala & Kment 2017), the Netherlands (Aukema 2016), Austria (Rabitsch 2016), and Romania (Grozea et al. 2016). Stable populations of A. heegeri in Budapest indicate that similarly to N. viridula it also has the potential to establish in Central Europe, and due to the impending climatic change its further expansion in temperate regions of Europe is anticipated as well.

Acknowledgements We are grateful to Márk Lukátsi (Budapest) for sharing his observations on A. heegeri in Budapest, to Attilio Carapezza (University of Palermo), Petr Kment (National Museum, Prague), and Előd Kondorosy (University of Pannonia, Keszthely) for several comments which considerably improved our manuscript, to the latter three colleagues and David A. Rider (North Dakota State University) for providing references, and to Mária Höhn (Szent

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István University, Budapest) for assistance in plant identification. This study received financial support from the National Natural Science Foundation of China (grant no. 31472024) and the One Hundred Young Academic Leaders Program of Nankai University to D. Rédei.

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