ANNALES ■ Ser. hist. nat. ■ 25 ■ 2015 ■ 1 Original scientific article UDK 595.74(497) Received: 2015-02-12 TWO SIBLING GREEN LACEWING SPECIES, CHRYSOPA PALLENS AND CHRYSOPA GIBEAUXI (INSECTA: NEUROPTERA: CHRYSOPIDAE) IN SLOVENIA AND WESTERN BALKAN COUNTRIES1 Dušan DEVETAK Department of Biology and Institute of Biology, Ecology and Nature Conservation, Faculty of Natural Sciences and Mathematics, University of Maribor, SI-2000 Maribor, Koroška cesta 160, Slovenia E-mail: dusan.devetak@guest.arnes.si Predrag JAKŠIC Department for Biology and Ecology, Faculty of Natural Science and Mathematics, University of Niš, RS-18000 Niš, Višegradska 33, Serbia Toni KOREN Institute of Biodiversity Studies, Science and Research Centre, University of Primorska, SI-6310 Izola, Giordana Bruna 6, Slovenia Danijel IVAJNŠIČ Department of Biology and Institute of Biology, Ecology and Nature Conservation, Faculty of Natural Sciences and Mathematics, University of Maribor, SI-2000 Maribor, Koroška cesta 160, Slovenia ABSTRACT Green lacewing species, Chrysopa gibeauxi (Leraut, 1989), was recently reinstated as a valid species, and closely related to Chrysopa pallens (Rambur, 1838). Evaluation of morphological diagnostic characters of the two sibling species justified the separation of the two species. After re-examination the available insect material from Slovenia and western Balkan countries it was revealed that Chrysopa pallens is widely distributed in the area, whilst Chrysopa gibeauxi is a rare green lacewing, recorded in Slovenia, Croatia and Serbia (Kosovo). The distribution of the latter species is for sure larger than appearing. Some details concerning morphology and habitat of the species are provided. The erroneous citations given for Slovenia, assigned now to Chrysopa gibeauxi, are corrected. Key words: Neuroptera, Chrysopa gibeauxi, Chrysopa pallens, sibling species, new records, Slovenia, Balkan DUE SPECIE GEMELLE DI CRISOPIDI, CHRYSOPA PALLENS E CHRYSOPA GIBEAUXI (INSECTA: NEUROPTERA: CHRYSOPIDAE) IN SLOVENIA E NEI PAESI DEI BALCANI OCCIDENTALI SINTESI Il crisopide Chrysopa gibeauxi (Leraut, 1989) è stato recentemente ripristinato come specie valida, strettamente correlata a Chrysopa pallens (Rambur, 1838). La valutazione dei caratteri diagnostici morfologici delle specie gemelle ha giustificato la separazione delle due specie. Dopo un nuovo esame del materiale entomologico proveniente dalla Slovenia e dai paesi dei Balcani occidentali è stato concluso che Chrysopa pallens è una specie ampiamente diffusa nell'area in questione, mentre Chrysopa gibeauxi è un crisopide raro, trovato in Slovenia, Croazia e Serbia (Kosovo). La distribuzione della seconda specie è sicuramente più ampia di quanto al momento appaia. L'articolo fornisce alcuni dettagli riguardanti la morfologia e l'habitat delle specie considerate. Le citazioni erronee fornite per la Slovenia sono state corrette e ora assegnate a Chrysopa gibeauxi. Parole chiave: Neuroptera, Chrysopa gibeauxi, Chrysopa pallens, specie gemelle, nuove segnalazioni, Slovenia, Balcani 1 Dedicated to the memory of Jan Carnelutti (1920-2012) 47 ANNALES ■ Ser. hist. nat. ■ 25 ■ 2015 ■ 1 Dušan DEVETAK et al.: TWO SIBLING GREEN LACEWING SPECIES, CHRYSOPA PALLENS AND CHRYSOPA GIBEAUXI ..., 47-54 INTRODUCTION Green lacewings (Chrysopidae) are neuropteran insects used as biological pest control agents of insect and mite pests in agriculture and gardens (e.g., McEwen & Senior, 1998; Senior & McEwen, 2001; for reviews see Stelzl & Devetak, 1999; Canard, 2001; McEwen et al., 2001). The family Chrysopidae comprises more than 1,200 described species in approximately 80 valid genera world-wide (Brooks & Barnard, 1990). Green lace-wing genus Chrysopa Leach in Brewster, 1815 is distributed in Holarctic, with 11 valid species occurring in North America and approx. 50 in Europe, North Africa and Asia. Among them, 17 are recorded from Europe (Brooks & Barnard, 1990; Aspock et al., 2001). From specimens captured in the French Alps, Leraut (1989) described a new green lacewing subspecies, Me-tachrysopa pallens ssp. gibeauxi Leraut, 1989. It was later raised as bona species (Leraut, 1992), but in 2001 it was synonymized with Chrysopa pallens (Rambur, 1838) by Aspock et al. (2001). A decade and a half later, the species Chrysopa gibeauxi (Leraut, 1989) was con- firmed and its valid status reinstated in a comprehensive study by Tillier et al. (2014). Tillier et al. (2014) provided diagnostic characters separating the two species. In Ch. gibeauxi is the pro-notum covered with numerous thick black hairs, whilst in Ch. pallens there are slender blond and blackish brown hairs (Figs. 1, 2). In forewings of Ch. gibeauxi is first costal cross-veinlet black, and other costal cross-veinlets are fully black except in pterostigma, whilst in Ch. pallens is first costal cross-veinlet green, and other costal cross-veinlets are partly blackened, i.e. in the very distal part the veinlets are bright (Figs. 3, 4). On the head of Ch. gibeauxi seven black spots are larger and more intensively marked than in Ch. pallens. (Figs. 1, 2) (Tillier et al., 2014). Furthermore, examination of the male genitalia of Ch. pallens from France and Romania, and of Ch. gibeauxi from France showed differences justifying the separation of the two species (Tillier et al., 2014). In the past, when the existence of Ch. gibeauxi has not yet been confirmed, Chrysopa pallens sensu lato was considered a common species in Slovenia and western Figs. 1, 2: Dorsal view of the head and the prothorax: 1 - Chrysopa pallens (Rambur) (Hrastovlje, Slovenia), 2 - Chrysopa gibeauxi (Leraut) (Šempeter pri Gorici, Slovenia). (Photo: D. Devetak) Sl. 1,2: Glava in predprsje dorzalno: 1 - Chrysopa pallens (Rambur) (Hrastovlje, Slovenija), 2 - Chrysopa gibeauxi (Leraut) (Šempeter pri Gorici, Slovenija) (Foto: D. Devetak) 48 ANNALES ■ Ser. hist. nat. ■ 25 ■ 2015 ■ 1 Dušan DEVETAK et al.: TWO SIBLING GREEN LACEWING SPECIES, CHRYSOPA PALLENS AND CHRYSOPA GIBEAUXI ..., 47-54 Balkan countries (reviews in Aspock et al., 1980, 2001; Devetak, 1992a). As we now know, two closely related species occur in Europe (Tillier et al., 2014), consequently it was necessary to re-examine material in the first author's collection to reinstate the knowledge of the occurrence of the both species in the area. MATERIAL AND METHODS Green lacewings were collected using a sweep net. Pinned individuals and lacewings preserved in alcohol are deposited in the first author's collection. Insects were photographed under a stereoscopic zoom microscope Nikon SMZ800 with a mounted digital camera Nikon DS-Fi1, and processed with NIS-Elements F 3.0 software. Digital images captured at different focal planes were assembled using the application Helicon Focus 4.62 Lite. A map of the studied area was created using ArcGIS 9.3 software (ESRI, 2010) and the free available DIVA-GIS database (http://www.diva-gis.org/gdata, accessed on 9.2.2015). RESULTS Distribution of Chrysopa pallens (Rambur) and Ch. gibeauxi (Leraut) in the studied area Chrysopa pallens (Rambur, 1838) In older literature (e.g., Klapalek, 1898, 1899, 1900; Živojinovic, 1950; Zeleny, 1964; Devetak, 1984, 1991, 1992b), the species is cited as Chrysopa septempunc-tata Wesmael, 1841. After re-inspection the first author's collection the presence of the species was confirmed for Slovenia, Croatia, Montenegro, Serbia, Serbia: Kosovo, and Macedonia (=FYROM) (Fig. 5). Klapalek (1898, 1899, 1900) reported Ch. pallens in Bosnia and Herzegovina, Živojinovic (1950) in Serbia, Zeleny (1964) in Albania, and a series of papers in Croatia (for a review see Devetak, 1992 b), but due to the lack of preserved individuals it was impossible to verify the identity of species cited in the papers for these countries. Slovenia Literature records Verified citations: Devetak (1984): Bohinj; Črni Kal; Ljubljana; Maribor; Maribor: Meljski hrib; Sečovlje; Šempeter pri Gorici; Škocjan pri Divači. Erroneous citations - Ch. gibeauxi mistaken for Ch. pallens in the following collecting places: Devetak (1984): Dravograd; Maribor: Starše; Kidričevo; Devetak (2011): Predoslje: grad Brdo. Re-examined individuals: Bohinj, jezero, 9. VIII. 1975 1 S 1 ?, 1. VIII. 1976 1 S, D. Devetak leg.; Črni Kal, Predloka, 24. VI. 1990 1 ?; Haloze: Belski vrh, 14. VII. 1986 1 S, F. Janžekovič leg.; Ljubljana, VI. 1968 1 ?, VI. 1971 1 S 1 ?, 1.-23. IX. 1971 1 Ç, I. Sivec leg., 8. VIII. 1976 7 S 1 ?, D. Devetak leg.; Makole: Šega, 13. VII. 1984 1 S, C. Krušnik leg.; Maribor, 24. VII. 1975 1 S, 28. VIII. 1976 3 S 1 ?, 10. IX. 1986 1 Ç, 14. IX. 1986 1 S, D. Devetak leg.; Maribor: Kalvarija, 16. VIII 1991 1 S 1 ?, D. Devetak & Barbara Senegačnik leg.; Maribor: Kamnica, Kamniška Graba-Medič, 12. IX. 1992 1 S, Nataša Kočev leg.; Maribor, Meljski hrib, 22. VII. 1978 1 S, D. Devetak leg.; Nazarje, 23. VIII. 1986 1 Ç, D. Devetak leg.; Nova Gorica: Šempeter pri Gorici, 6. VII. 1973 1 Ç, 14. IX. 1973 1S 1?, I. Sivec leg.; Obalno-kraška regija: Hrastovlje, 13. IX. 1980 1?; 13. IX. 1990 1S 1 ?, D. Devetak leg.; Ptuj: Gorišnica, 26. VIII. 1988 1 S, F. Janžekovič leg.; Rižana, izvir, 24. VII. 1990 1 Ç, C. Krušnik leg.; Sečovlje, VIII. 1973, 1 ?, 19. VIII. 1983 1 S, D. Devetak leg.; Škocjan pri Divači, Škocjanske jame, 22. V. 1976 1 S, D. Devetak leg. Croatia Literature records Verified citations: Devetak (1992b): Biograd na Moru; Istra, Premantura; O. Brač, Bol; O. Brač, Vidova gora; O. Rab, Lopar. Re-examined individuals: Biograd na Moru, 19. VIII. 1973 1 S, D. Devetak leg.; Istra, Premantura, 20. VII. 1984 1 Ç, D. Devetak leg.; O. Brač, Bol, 12. VII. 1987 1 S, 25.-30. VII. 1997 1 Ç, all D. Devetak leg.; O. Brač, Vidova gora, 9. VII. 1990 1 S, D. Devetak leg.; O. Rab, Lopar, 21. VI. 1976 2 Ç, D. Devetak leg. Montenegro Literature records Verified citations: Devetak (1991): National Park Durmitor: Crno jezero: Celine, Drenova gora, Komar-nica - Nevidio, Mlinski potok, Tara - Tepca. Re-examined individuals: Budva, 25. VIII. 1988 1 Ç, F. Janžekovič leg.; National Park Durmitor, Crno jezero: Celine, 11. VIII. 1988 1 S, P. Jakšic leg.; Durmitor, Drenova gora, 20. VIII. 1987 4 S 3 Ç, F. Janžekovič leg.; Durmitor, Komarnica, Nevidio, 1100 m, 6. VII. 1986 1 S, P. Jakšic leg.; Durmitor, Mlinski potok, 17. VIII. 1987 1 S, F. Janžekovič leg.; Durmitor, Tara - Tepca, 4. VIII. 1984 1 Ç, 13. VIII. 1988 1 Ç, both P. Jakšic leg.; Tuzi, 5.-17. IX. 1982, 2 Ç, F. Janžekovič leg. Serbia Re-examined individuals: Kopaonik: Jošanička Banja, 6. VIII. 1986 5 S, P. Jakšic leg.; Raška: Raška, Razdolje, 500 m, 29. VII. 1987 1 Ç, P. Jakšic leg. Serbia: Kosovo Literature records Verified citations: Devetak & Jakšic (2003): Ibarska klisura: Košutovac, Košutovački potok; Mt. Grmija; Mt. Goleš; Mt. Šar planina, Prizrenska Bistrica; Priština; Prizren; Slatina. 49 ANNALES ■ Ser. hist. nat. ■ 25 ■ 2015 ■ 1 Dušan DEVETAK et al.: TWO SIBLING GREEN LACEWING SPECIES, CHRYSOPA PALLENS AND CHRYSOPA GIBEAUXI ..., 47-54 Figs. 3, 4: The forewing of both species: 3 - Ch. pallens (Hrastovlje, Slovenia), 4 - Ch. gibeauxi (Šempeter pri Gorici, Slovenia). (Photo: D. Devetak) Sl. 3, 4: Sprednje krilo: 3 - Ch. pallens (Hrastovlje, Slovenija), 4 - Ch. gibeauxi (Šempeter pri Gorici, Slovenija). (Foto: D. Devetak) 50 ANNALES ■ Ser. hist. nat. ■ 25 ■ 2015 ■ 1 Dušan DEVETAK et al.: TWO SIBLING GREEN LACEWING SPECIES, CHRYSOPA PALLENS AND CHRYSOPA GIBEAUXI ..., 47-54 Re-examined individuals: Ibar (Iber): Ibarska klisura: Košutovac, Košutovački potok, 510 m, 24. VII. 1987 1 S 5 ?, P. Jakšic leg.; Kosovska Mitrovica (Mitrovice) /former: Titova Mitrovica/, Ribariče, 1. VII. 1987 1 ?, P. Jakšic leg.; Mt. Goleš (Golesh), 5. VI. 1979 1 S, D. Devetak leg.; Mt. Grmija (Germia), 21. VII. 1979 1 S, D. Devetak leg.; Mt. Šar planina (Malet e Sharrit), Prizrenska Bistrica, 530 m, 22. VII. 1986 1 S, P. Jakšic leg.; Priština (Prishtine), from V. to IX. 1979 41 S 11 ?, D. Devetak leg.; 21. VIII. 1980 5 S 2 ?, P. Jakšic leg.; Prizren (Prizren), 22. VII. 1986 1 ?, P. Jakšic leg.; Slatina (Sllatine), 25. VII. 1979 1 ?, D. Devetak leg. Macedonia (=FYROM) Re-examined individuals: Demir Kapija, 21. V. 1988 1 S, P. Jakšic leg.; Dojran-sko Ezero, N part, 7. VIII. 1978 6 S 2 ?, F. Janžekovič leg.; Sv. Naum, Ohridsko Ezero, 5. VIII. 1988 1 S, F. Janžekovič leg.; Zrnovci, Kochani, 8. VI. 1985 1 S, I. Sivec & M. Štangelj leg. Chrysopa gibeauxi (Leraut, 1989) Distribution of re-examined individuals (Fig. 5): Slovenia Črni Kal, Predloka, 2. VII. 1990 1 ?; Dravograd, 1. VII. - 6. VIII. 1975 38 ind.; Ig, Kremenica, 3. VIII. 1980 2 ?, S. Brelih leg.; Kidričevo, 26. VI. 1983 1 ?, D. Devetak leg.; Maribor, 4. VII. 1975 1 S, 16.-23. VII. 1975 5 S 1 $, D. Devetak leg.; Mt. Pohorje, Pameče: Jesen-kov vrh, 25. VII. 1985 1 $, M. Jež leg.; Nova Gorica: Šempeter pri Gorici, 6. VII. 1973 1 S, I. Sivec leg.; Pre-doslje: grad Brdo, 31. V. 2007 1 S, D. Devetak leg.; Starše, VIII. 1974, 2 ?. Croatia Baranja: Ilok, 26. VIII. 2013 1 S, T. Koren leg. Serbia: Kosovo Priština (Prishtine), 9. VIII. 1979 1 $, D. Devetak leg. Diagnostic differences between the two species Both sibling species observed in this study are - like Polish green lacewings studied by Tillier et al. (2014) - unambiguously separated. The key characters separating the two species are colouration of hairs on the pro-notum (Ch. pallens: slender blond and blackish brown hairs, Ch. gibeauxi: thick black hairs) (Figs. 1, 2) and colouration of first costal cross-veinlet in forewings (Ch. pallens: green cross-veinlet, Ch. gibeauxi: black cross-veinlet) (Figs. 3, 4). Colouration of second antennal segment is not clearly visible in individuals preserved in alcohol, because, after a few years, it loses its colour. Most of the abdomen and the legs of Ch. pallens are covered only with blond (light) hairs, whilst in Ch. gibeauxi there are black hairs. Black spots on the head are in most individuals (but not in all) of Ch. gibeauxi larger than in Ch. pallens. In male genitalia, the gonocristae (central group) are smaller and more numerous in Ch. pallens than in Ch. gibeauxi. Plant substrate specificity The two sibling species differ according to their preference for plant substrate. Whilst Ch. gibeauxi was found on conifers (Picea, Pinus) or in coniferous forests, Ch. pallens occurred on a variety of deciduous trees. Twelve tree species were noted in Slovenia and western Balkan countries as plant substrates for Ch. pallens (Tab. 1). Plant substrate species Country Slovenia Croatia Serbia: Kosovo Montenegro Pinus nigra J.F. Arnold X Acer monspessulanum L. X Acer campestre L. X Acer negundo L. X Acer platanoides L. X Acer pseudoplatanus L X Fagus sylvatica L. X X Prunus avium L. X Quercus pubescens Willd. X Quercus virgiliana (Ten.) Ten. X Robinia pseudacacia L. X Tilia cordata Mill. X 51 Tab. 1: Plant substrate species for Chrysopa pallens in Slovenia and western Balkan countries. Tab. 1: Rastlinske vrste, na katerih je bila najdena Chrysopa pallens v Sloveniji in deželah zahodnega Balkana ANNALES ■ Ser. hist. nat. ■ 25 ■ 2015 ■ 1 Dušan DEVETAK et al.: TWO SIBLING GREEN LACEWING SPECIES, CHRYSOPA PALLENS AND CHRYSOPA GIBEAUXI ..., 47-54 Fig. 5: Known distribution of Ch. pallens (circles) and Ch. gibeauxi (triangles) in Slovenia and western Balkan countries. BH - Bosnia and Herzegovina, CRO - Croatia, KO - Serbia: Kosovo, MAC - Macedonia, MTG -Montenegro, SLO - Slovenia, SRB - Serbia. (Author of the map: D. Ivajnšič) Sl. 5: Znana razširjenost vrst Ch. pallens (krogi) in Ch. gibeauxi (trikotniki) v Sloveniji in deželah zahodnega Balkana. BH - Bosna in Hercegovina, CRO - Hrvaška, KO - Srbija: Kosovo, MAC - Makedonija, MTG - Črna Gora, SLO - Slovenija, SRB - Srbija. (Avtor risbe: D. Ivajnšič) Szentkiralyi, 2001a, b). In this study, the occurrence of Ch. pallens is confirmed for Slovenia and western Balkan countries, and the presence of Ch. gibeauxi is noted for the first time in Slovenia, Croatia and Serbia: Kosovo. A series of papers containing data on the Balkan distribution of Ch. pallens published before 1989 exists, e.g., for Serbia (Zivojinovic, 1950), Bosnia and Herzegovina (Klapalek, 1898, 1899, 1900), Albania fZeleny, 1964), and Croatia (Novak, 1891; Mocsary, 1899; Klapalek, 1906; Esben-Petersen, 1925; Saure, 1989). However, these papers have no value in these particular cases, considering the fact that they were published before 1989, when Ch. gibeauxi has not yet been known. When morphological characters are considered, the both sibling species are unambiguously separated, as was already pointed out by Tillier et al. (2014). The association of green lacewings with particular tree species in Europe was reviewed extensively by Monserrat & Marin (2001) and Szentkiralyi (2001b). The two species in the studied area differ in their ecological preference - whilst Ch. gibeauxi is found mainly on conifers, Ch. pallens prefers deciduous trees (Tab. 1). It may be possible that Ch. gibeauxi is in Europe more frequent than it appears until now (Tillier et al., 2014) and is probably relatively common also in Balkan countries. ACKNOWLEDGEMENTS DISCUSSION Species of the green lacewing taxon, Ch. pallens sensu lato, are known as beneficial predatory insects, feeding on crop pests, mainly small arthropods (e.g., Grimal & Canard, 1990; Canard, 2001). The species play role in vegetables, forests, field, fruit and nut crops (Duelli, 2001; We are grateful to field entomologists for collecting the insects. This research was supported partly by the Research Project Biodiversity of the Neuropterida in the Balkan (RP BioDiv Neuropterida Balkan - ALBH 2013) and partly by the Research Project Biodiversity of the green lacewings (Neuroptera: Chrysopidae) in Serbia (RP BioDiv CHRYSER 2015). 52 ANNALES ■ Ser. hist. nat. ■ 25 ■ 2015 ■ 1 Dušan DEVETAK et al.: TWO SIBLING GREEN LACEWING SPECIES, CHRYSOPA PALLENS AND CHRYSOPA GIBEAUXI ..., 47-54 VRSTI TENČIČARIC, CHRYSOPA PALLENS IN CHRYSOPA GIBEAUXI (INSECTA: NEUROPTERA: CHRYSOPIDAE), V SLOVENIJI IN DEŽELAH ZAHODNEGA BALKANA Dušan DEVETAK Oddelek za biologijo in Inštitut za biologijo, ekologijo in varstvo narave, Fakulteta za naravoslovje in matematiko, Univerza v Mariboru, SI-2000 Maribor, Koroška cesta 160 E-mail: dusan.devetak@guest.arnes.si Predrag JAKŠIC Departman za biologiju i ekologiju, Prirodno-matematički fakultet, Univerzitet u Nišu, RS-18000 Niš, Višegradska 33, Srbija Toni KOREN Inštitut za biodiverzitetne študije, Znanstveno-raziskovalno središče, Univerza na Primorskem, SI-6310 Izola, Giordana Bruna 6 Danijel IVAJNŠIČ Oddelek za biologijo in Inštitut za biologijo, ekologijo in varstvo narave, Fakulteta za naravoslovje in matematiko, Univerza v Mariboru, SI-2000 Maribor, Koroška cesta 160 POVZETEK Tenčičarico vrste Chrysopa gibeauxi (Leraut, 1989) so v novejšem času ponovno ovrednotili kot veljavno vrsto, ozko sorodno vrsti Chrysopa pallens (Rambur, 1838). Na osnovi ovrednotenja morfoloških diagnostičnih znakov so utemeljili razlikovanje dveh sestrskih vrst. Ob ponovnem pregledu dostopnega materiala iz Slovenije in držav zahodnega Balkana smo ugotovili, da je vrsta Chrysopa pallens na območju splošno razširjena, medtem ko je Chrysopa gibeauxi redka, prvič zabeležena v Sloveniji, na Hrvaškem in Kosovem. Prav gotovo je slednja vrsta bolj razširjena, kot nakazujejo najdbe. Navajamo podatke o morfologiji in habitatu obeh vrst. Popravljeni so napačni citati za Slovenijo, ki se nanašajo na Chrysopa gibeauxi. Ključne besede: Neuroptera, Chrysopa gibeauxi, Chrysopa pallens, sestrske vrste, nove najdbe, Slovenija, Balkan REFERENCES Aspöck, H., U. Aspöck & H. Hölzel (unter Mitarbeit von H. Rausch) (1980): Die Neuropteren Europas. 2 Vols. Goecke & Evers, Krefeld. Aspöck, H., H. Hölzel & U. Aspöck (2001): Kommentierter Katalog der Neuropterida (Insecta: Raphidi-optera, Megaloptera, Neuroptera) der Westpaläarktis. Denisia, 2, 1-606. Brooks, S. 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