Ecologica Montenegrina 13: 25-29 (2017) This journal is available online at: www.biotaxa.org/em

Three new assassin bug records (: : ) for the Balkan Peninsula

NIKOLAY SIMOV1*, DENIS GRADINAROV2, LEONIDAS-ROMANOS DAVRANOGLOU3

1National Museum of Natural History, 1 Tsar Osvoboditel Blvd., 1000 Sofia, Bulgaria 2Faculty of Biology, Sofia University, 8 Dragan Tsankov Blvd., 1164 Sofia, Bulgaria. E-mail: [email protected] 3Department of Zoology, University of Oxford, OX1 3PS, United Kingdom. E-mail: [email protected] *Corresponding author: E-mail: [email protected]

Received: 9 September 2017│ Accepted by V. Pešić: 7 October 2017 │ Published online: 12 October 2017.

Assassin bugs are one of the largest and most diverse families of Heteroptera. So far, the reduviid fauna of the Balkan Peninsula comprises of only 52 species (Putshkov & Putshkov1996; Putshkov & Moulet 2009, Davranoglou 2011; Petrakis & Moulet 2011). In the present paper we add some new records of rare and invasive assassin bugs for some Balkan countries and the Balkan Peninsula as a whole. tabellarius Ribes & Putshkov, 1992 is reported for the first time for the Balkan Peninsula and novaki Horváth, 1888 for Greece and Macedonia, respectively. Zelus renardii Kolenati, 1857 was established for the first time in natural habitats for the Balkan Peninsula in Greece. An extra-European origin of E. tabellarius is herein suggested. Material was collected by sweeping net, light traps, pitfall traps, sifting leaf litter and searching under bark and stones. Digital images of the head, prothorax, hemelytra and male genitalic structures were taken with an Olympus SZ61 microscope equipped with CMEX-5 DC.5000c digital camera. Specimens examined in the course of this study are deposited at the collections of the National Museum of Natural History, Sofia, Bulgaria (SOFM), the Faculty of Biology of Sofia University ―St. Kliment Ohridski‖, Sofia, Bulgaria (BFUS) and the private collection of L.R. Davranoglou (DPC). Two paratypes of Empicoris maeharai Ishilawa, 2008 from the collections of the Laboratory of Resources, Faculty of Agriculture, Tokyo University of Agriculture, Atsugi, Japan (TUA) were also examined.

List of species

Empicoris tabellarius Ribes & Putshkov, 1992

Material examined: Bulgaria: Black Sea Coast, State Hunting Area ―Ropotamo‖, 42.331067°N, 027.716983°E, 23 m a.s.l., sparse longose forest with Fraxinus angustifolia, 02 September 2015, B. Zlatkov, O. Sivilov leg.; light trapping with both MBFT 160W and UV 8W lamps, 2 males, 4 females, N. Simov & D. Gradinarov det. (1 male and 3 females in SOFM, 1 male and 1 female in BFUS).

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NEW ASSASSIN BUG RECORDS FOR THE BALKAN PENINSULA

Figure 1. Empicoris tabellarius from Bulgaria: A — head and pronotum; B — hemelytron; C, D — end of male abdomen - ventral and dorsal view. Scale bares: A, B = 1 mm; C, D = 300 μm.

Our specimens are characterized by long and slender profemora, ventral spines on the profemora, which are small and hidden by pubescence (Fig. 1 A), and the hemelytral pterostigma exceeding the apex of the discal cell and decorated with only one brown spot, which is subdivided transversely (Fig. 1 B), and the first and second antennal segments are subequal. The above-mentioned characters fit in the diagnosis of E. discalis species group of Empicoris Wolff, 1811 (Putshkov et al. 1999; Ishikawa, 2008). Based on additional characters such as the apophysis of the pygophore being broadly notched apically and the simple paramere being very long and crook-ended (Fig. 1 C, D), our specimens are determined as E. tabellarius. Our specimens are similar in general habitus, coloration and shape of profemora and protibia, as well as shape and coloration of pterostigma to E. maeharai Ishikawa, 2008 and also in the coloration of the hemelytra and shape of its discal cell to E. okinawanus Ishikawa, 2008, both from E. discalis group of Empicoris (Ishikawa

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2008). Bulgarian specimens of E. tabellarius can be easily distinguished from the latter by the different shape of the paramere – strongly hooked with curved apical part longer and truncate apex (Figs. 1 C, D) and shape of the lateral carina of the posterior pronotal lobe (Fig. 1 A), and shape and size of the eyes. The two species (E. maeharai and E. okinawanus) could be classified as the closest relatives of E. tabellarius.

Distribution. The thread-legged bug Empicoris tabellarius Ribes & Putshkov, 1992 was described from a few localities in the southern parts of France and Spain and more than ten years later was considered endemic to the region (Putshkov & Putshkov 1996; Putshkov et al. 1999). When this species was recorded in Hungary in 2000, Rédei (2004) commented on the peculiarity of such a finding. The record of this species from the Balkan Peninsula is also curious. The true bug fauna of Bulgaria and especially of the Bulgarian Black Sea Coast is very well studied (Josifov 1974; Hubenov 2008) and it is unlikely that a thread-legged bug has been overlooked for nearly a century until our study. Perhaps it is spreading and the last two European records could be considered as a result of invasion. On the other hand, several alien true bugs were described from invaded areas and later discovered in their native range (e.g. rhododendri (Dolling, 1972), Stephanitis rhododendri Horváth, 1895) (Rabitsch 2008). Empicoris tabellarius belongs to E. discalis species group of the genus Empicoris Wolff, 1811. All the species of this group except E. tabellarius, are distributed in tropical, subtropical and southern parts of temperate regions of the Old World, excluding Europe (Rédei 2004). The probable closest relatives of E. tabelllarius are from East Asia (Japan). It is thus possible that E. tabellarius is an extra-European species which is now spreading. If this is the case, then E. tabellarius, should be registered as an alien species, as was the case with E. rubromaculatus (Blackburn, 1889). Our record of the species is the first for Bulgaria and the Balkan Peninsula, respectively.

Stenolemus novaki Horváth, 1888

Material examined: Bulgaria: Black Sea Coast, Varna, Sofia University Botanical Garden in St. Konstantin and Elena resort, 43.23830°N, 028.00140°E, 74 m a.s.l., termophilous deciduous woodland, March 2015, under bark, 1 nymph, P. Mitov leg., N. Simov det. (SOFM). Greece: Cyclades, Naxos, June 2014, 37.076261°N, 025.420244°E, 135 m a.s.l. pitfall trap in phrygana, 20 June, 2014, 1 female, leg. Aris Vellianitis, det. L.R. Davranoglou (DPC). Macedonia: Pchinya River Valley, Badarska Klisura protected site, Sveta Bogoroditsa Monastery, 41.82894°N, 021.68642°E, 229 m a.s.l., Mediterranean riparian woodand, 13 May 2014, under stones, 1 female, S. Hristovski & N. Simov leg., N. Simov det. (SOFM).

Distribution. To date, this species was known from the Balkan Peninsula only from its terra typica in Island of Hvar (Croatia) (Putshkov & Putshkov 1996) and from foothills of the Western Rhodopes Mts. near Asenovgrad in Bulgaria (Simov & Josifov 2004). Our findings significantly extend the range of the species. Finding this species in the central Cyclades suggests that it is almost certainly more widely distributed in this country, but has been overlooked due to its cryptic habits. Our specimens represent the first records from Greece, Macedonia and the Black Sea Coast of Bulgaria.

Zelus renardii Kolenati, 1857

Material examined: Greece: Pelion Peninsula, Papa Nero Beach, close to Agios Ioanis vill., 39.407239°N, 023.172648°E, 5 m a.s.l., 9 September 2015, 1 female, leg. & det. N. Simov (SOFM); Attica, Tatoi Royal Estate, 38.157167°N, 023.796075°E, 460 m a.s.l., 27 September 2015, swept from Quercus ilex, together with Nagusta goedelii (Kolenati, 1857), 1 male, 1 female, leg. & det. L.R. Davranoglou (DPC); Attica, Helidonous stream, 38.102167°N, 023.797397°E, 209 m a.s.l., 19 June 2015 (1 female)-27 September 2015 (1 male, 1 female), semi natural xerothermic pasture, swept from Daucus carota, leg. & det. L.R. Davranoglou (DPC); Attica, Adames, 38.099539°N, 023.793650°E, 230 m a.s.l., 20 July 2015, semi natural pasture, swept from ruderal vegetation, 1 V instar larva, leg. & det. L.R. Davranoglou (DPC); Attica, Schinias, Karavi beach parking lot, 38.134825°N, 024.011700°E, 3 m a.s.l., 3 July 2017, swept from Pittosporum tobira, 1 V instar larva, leg. & det. L.R. Davranoglou (DPC); Achaea, Rion, Platani village, 38.295228°N, 021.822575°E, 189 m a.s.l., 20 June 2014, olive grove, swept from ruderal vegetation, including Daucus carota, 1 V instar larva, 1 male, leg. & det. L.R. Davranoglou (DPC); Aetolia-Acarnania,

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NEW ASSASSIN BUG RECORDS FOR THE BALKAN PENINSULA road from Missolonghi to Astakos, 38.410692°N, 021.397603°E, 7 m a.s.l., 28 July 2015, small clearing next to river, swept from ruderal vegetation, 1 female, leg. & det. L.R. Davranoglou (DPC).

Distribution. The native range of the leafhopper assassin bug Zelus renardii includes North and Central America. In the 20th century Z. renardii spread to Hawaii and other tropical areas in the Pacific Region (Weirauch et al. 2012). Since then, the species has reached Chile (2001), and the Mediterranean (Greece: 2010; Italy: 2013; Spain: 2011; European Turkey: 2016; Albania: 2016) by human-assisted introductions (Davranoglou 2011; Weirauch et al. 2012; Dioli 2013; Vivas 2012; Faúndez 2015; Çerçi & Koçak 2016; Heyden 2017). From the Balkan Peninsula, the species has so far been found only in man-made environments in Greece (Attica and Crete) (Davranoglou 2011; Petrakis & Moulet 2011; Heyden 2015). The locality in Pelion is typical for the coastal maquis and arborescent matorral region (EUNIS types –F5.1 and F5.2) (see Fig. 2). Throughout Greece, the species exhibits high adaptability and has been collected from a range of disturbed and semi natural habitats in Mediterranean forests, olive groves, lagoons and xerothermic pastures. The relatively great invasive potential of Z. renardii due to its high abundance in man-made and disturbed environments, high reproductive success and its predatory behavior may be a problem for the local insect communities in case of establishment of large populations. Indeed, Z.renardii has been frequently found in habitats shared by the native N.goedelii (LR.Davranoglou, personal observation); it would be interesting to investigate whether competition between the two species takes place. Our specimens represent the first records from natural habitats in Greece and the Balkan Peninsula, respectively.

Figure 2. The locality of Zelus renardii in Pelion Peninsula in the typical for the region coastal maquis and arborescent matorral.

Acknowledgements The authors wish to thank to Tadashi Ishikawa (Laboratory of Insect Resources, Faculty of Agriculture, Tokyo University of Agriculture, Japan), Slavco Hristovski (Faculty of Natural Sciences and Mathematics, ―Ss. Cyril and Methodius‖ University, Skopje, Macedonia), Plamen Mitov, Boyan Zlatkov and Ognyan Sivilov (Sofia University ―St. Kliment Ohridski‖, Bulgaria) for providing material and assistance in the field. We would also like to thank David Redei (Nankai University, Tianjin, China) for encouragement and for valuable comments on an earlier version of this manuscript. The study was supported by the Financial

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Mechanism of the European Economic Area (2009–2014), Programme BG03 Biodiversity and Ecosystem Services, Projects ESENIAS-TOOLS, D-33-51/30.06.2015 and IBBIS, D-33-72/20.07.2015.

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