Annales de la Société entomologique de France (N.S.), 2020 https://doi.org/10.1080/00379271.2020.1756911

A new unexpected species of Chrysopa Leach from Cyprus with biogeographic remarks (Neuroptera: Chrysopidae) Davide Badano a,b* & Christodoulos Makrisc aDISTAV, University of Genoa, Corso Europa 26 I-16132, Genoa, Italy; bDepartment of Biology and Biotechnology “Charles Darwin”, Sapienza University of Rome, Piazzale A. Moro 5 I-00185, Rome, Italy; cEthnikis Antistaseos 21 C-3022, Lemesós, Cyprus (Accepté le 14 avril 2020; publié en ligne le 18 mai 2020)

Summary. Cyprus is rich in endemics; however, all but two lacewing species are shared with the mainland. Thus, the discovery of a new morphologically distinct species of chrysopid belonging to the extensively studied genus Chrysopa, Chrysopa niki n. sp., appears remarkable. While most Chrysopa species differ in relatively subtle morphological characters, the new taxon is set apart from all Western Palaearctic congeners due to a unique combination of pattern, venational, leg and genital characters. The characteristics of C. niki n. sp. suggest that it might be an endemic to Cyprus, not strictly related to other congeners, underlining the importance of the discovery. The biogeography of Cypriot Neuroptera is discussed in light of this new finding.

Résumé. Une nouvelle espèce inattendue de Chrysopa Leach de Chypre avec des remarques biogéographiques (Neuroptera : Chrysopidae). Chypre est riche en espèces endémiques, mais tous les névroptères à l’exception de deux sont partagés avec le continent. À cet égard, la découverte d’une nouvelle espèce de chrysope morphologiquement distincte appartenant au genre Chrysopa, Chrysopa niki n. sp., est remarquable. Tandis que la plupart des espèces de Chrysopa se distinguent par des caractères morphologiques relativement subtils, le nouveau taxon se differencie de tous ses congénères du Paléarctique occidental grâce à une combinaison unique de caractères de coloration, des nervures et des genitalia. Les caractéristiques de C. niki n. sp. suggèrent qu’il s’agit d’une espèce endémique de Chypre, non strictement affine d’autres congénères, soulignant l’importance du nouveau taxon. La biogéographie des névroptères chypriotes est discutée en fonction de cette découverte. http://www.zoobank.org/urn:lsid:zoobank.org:act:C6E3397B-19BA-431A-8F3A-4B872A72CED1 Keywords: Neuropterida; green lacewings; Mediterranean; biogeography; endemics; new species

(Navás, 1932) and the myrmeleontid Delfimeus limasso- Mediterranean islands are biodiversity hotspots (Myers et licus (Navás, 1931) (Aspöck & Hölzel 1996; Aspöck et al. 2000) and among them Cyprus, the third largest, had a al. 2001; Kral & Devetak 2016). Chrysopidae, or green long geologic history with important biogeographic lacewings, are the most diverse family in Cyprus, with 17 implications. Cyprus originated from the uplift of the reported species, four of which are in the genus Chrysopa sea bed during the Late Cretaceous but reached its actual Leach in Brewster, 1815, i.e. C. dubitans McLachlan, shape and extension only in the Late Pliocene– 1887, C. pallens (Rambur, 1838), C. viridana Schneider, Pleistocene (Robertson 1977; Hadjisterkotis et al. 2000; 1845 and C. walkeri McLachlan, 1893 (Tjeder 1958; Kinnaird et al. 2011). A direct connection between Aspöck & Hölzel 1996; Hölzel & Ohm 1999; Canard Cyprus and the mainland is debated (see Hadjisterkotis 2007; Kral & Devetak 2016). et al. 2000), although geological data suggest a union The genus Chrysopa has a largely Holarctic distribu- with the Asian coast during the Late Messinian (Jolivet tion, including more than 60 described species, although et al. 2006; Bache et al. 2012). Probably the first wave of the affinities of some non-Holarctic species need further colonizers reached the island at that time, while during investigations as this taxon was once a “waste basket” the Pliocene and Pleistocene Cyprus was not connected to including most species of Chrysopinae (Brooks & the mainland; this history may help explain the relatively Barnard 1990). Phylogenomic analyses corroborate mor- high number of endemic species (Poulakakis et al. 2013). phological clues, strongly supporting a close relationship The Neuropterida of Cyprus comprise 54 species, among Chrysopa and the smaller genera Plesiochrysa belonging to the orders Raphidioptera (2 species) and Adams, 1982 and Ceratochrysa Tjeder, 1966, suggesting Neuroptera (52 species), only two of which are endemic that they might be merged within a broader Chrysopa to the island: the chrysopid Pseudomallada cyprinus (Tauber et al. 2001 ; Winterton et al. 2019). On

*Corresponding author. Email: [email protected]

© 2020 Société entomologique de France Published online 18 May 2020 2 D. Badano & C. Makris morphological grounds, the species of Chrysopa are often chlorazol black and alcohol to enhance the contrast of the recognizable at a first glance due to their head and thor- sclerites. The specimens and their genitalia were preserved in acic pattern, although the genus monophyly relies on alcohol. Terminology for genitalia follows the interpretation of – the homology of genital sclerites of Aspöck & Aspöck (2008); genital and larval characters (Principi 1940 1941; however, traditional terminology, i.e. following Adams & Penny Brooks & Barnard 1990; Tsukaguchi 1995; Penny & (1985) and Tauber (2010), is given in square brackets to ease Tauber 2000). The adults of Chrysopa are characterized comparisons with previous literature. Wing venation largely by unusual traits for green lacewings, being predatory (in follows Breitkreuz et al. (2017), also taking account of recent contrast to most green lacewings, which feed on nectar updates (Tauber 2019). and pollen) and secreting skatole from the prothoracic Type specimens were deposited in the following collections: glands for defense (Principi 1947, 1954; Canard et al. 1984; Canard 2001; Aldrich & Zhang 2016). The larvae MSNG Museo Civico di Storia Naturale “G. Doria”, Genoa, of Chrysopa are mostly “naked” (i.e. not camouflaging Italy with debris) with a few exceptions, such as the North MZUR Museum of Zoology, Sapienza Università di Roma, Rome, Italy American C. slossonae Banks, 1924 (Principi 1947, 1954; DBRC Davide Badano Research Collection, Taggia (IM), Italy Eisner et al. 1978; Tsukaguchi 1995; Penny & Tauber 2000; Monserrat & Díaz-Aranda 2012; Tauber et al. 2014). Taxonomy The Western Palaearctic contains 25 species (taking Family Chrysopidae Schneider, 1851 into account the recently revised status of some taxa), Subfamily Chrysopinae Schneider, 1851 including some of the most common European chrysopids, Tribe Chrysopini Schneider, 1851 and these species are mostly widespread in the region, with Genus Chrysopa Leach in Brewster, 1815 rare exceptions such as the Iberian endemic C. nierembergi Diagnosis Navás, 1908 (Aspöck et al. 1980, 2001). The European Male genitalia without gonocoxites 11 [tignum]; species of this genus are relatively well known, while a gonapophyses 9 [entoprocessus] with gonocornua; dorsal few Middle Eastern species belonging to the C. formosa apodeme of the ectoproct curved upward; sternite 8 and 9 Brauer, 1851 and C. phyllochroma Wesmael, 1841 species- not fused; ventral apodeme of sternite 9 protruding apically; groups are in need of revision (Aspöck et al. 2001). Most apex of sternite 9 with gonosetae. European Chrysopa species were described in the nine- teenth and in the first decades of the twentieth century, while several Iranian species were named in the 1960s Chrysopa niki n. sp. (Hölzel 1967); the most recent described species are C. nigrescens Hölzel & Ohm, 1983 and the recently re-eval- Type material uated C. gibeauxi Leraut, 1992. Given this information, the Holotype: ♂, CYPRUS/Koilani, Agia Mavri, 722 m/34° fi nding of a new Chrysopa species from Cyprus is note- 50ʹ43.56ʺN 32°52ʹ8.56ʺE/2.VIII.2018/C. Makris leg.// worthy and unexpected. The aim of the present paper is to HOLOTYPUS/Chrysopa niki Badano & Makris, sp. describe the morphology of this new species and compare nov./D. Badano det. 2020. Dissected, alcohol preserved it with other Western Palaearctic congeners. (MZUR) (Figures 3 and 5A). Paratypes: 1♂,1♀, CYPRUS/Koilani, Agia Mavri, 722 m/34°50ʹ43.56ʺN 32°52ʹ8.56ʺE/2.VIII.2018/C. Materials and methods Makris leg.//PARATYPUS/Chrysopa niki Badano & Specimens were examined and measured with a Leica® Makris, sp. nov./D. Badano det. 2020. Alcohol preserved (Wetzlar, Germany) MZ 9.5 stereomicroscope equipped with ♂ ♀ an optical micrometer. Photographs were taken with a Canon® (MZUR). 1 ,1 , CYPRUS/Koilani, Agia Mavri, 722 m/ (Tokyo, Japan) EOS 600D digital camera equipped with 34°50ʹ43.56ʺN 32°52ʹ8.56ʺE/2.VIII.2018/C. Makris leg.// Canon® (Tokyo, Japan) lens MP-E 65 mm; the resulting images PARATYPUS/Chrysopa niki Badano & Makris, sp. nov./ were then processed and focus-stacked with the software D. Badano det. 2020. Alcohol preserved (MSNG). 2♂, Zerene® (Richland, WA, USA) Stacker. The color and pattern 2♀, CYPRUS/Koilani, Agia Mavri, 722 m/34°50ʹ43.56ʺN of chrysopids quickly fade after death; therefore, photos of live ʹ ʺ specimens are provided to show the habitus of the new species 32°52 8.56 E/2.VIII.2018/C. Makris leg.//PARATYPUS/ in life. Measurements were taken following the protocol of Chrysopa niki Badano & Makris, sp. nov./D. Badano Tauber (2010): vertex width (V), pronotum length (PrL), pro- det. 2020. Alcohol preserved (DBRC). 1♂,2♀ (of notum width (PrW), forewing length (FL), forewing width which one dissected), CYPRUS/near Pera Pedi village (FW), hind wing length (HL), hind wing width (HW); body and Pano Platres, 920 m/34°50ʹ43.56ʺN 32°52ʹ8.56ʺE/4. length (BL) was taken from vertex to abdomen tip. Genitalia were cleared in a solution of 10% KOH (potassium hydroxide) VIII.2018, C. Makris leg.//PARATYPUS/Chrysopa niki at room temperature and later rinsed in a solution of glacial Badano & Makris, sp. nov./D. Badano det. 2020. acetic acid and water. Finally, they were stained in a solution of Alcohol preserved (DBRC). 1♀, Pafos Panagia, 800 m/ Annales de la Société entomologique de France (N.S.) 3

6.VI.2010, light trap/C. Makris leg.//Pafos Panagia, basal trapezoidal dilatation. Wing veins largely dark 800 m; 6.VI.2010; light trap; C. Makris leg.; brown. PARATYPUS/Chrysopa niki Badano & Makris, sp. nov./D. Badano det. 2020. Dry pinned (DBRC). Description All specimens were collected in Mediterranean mid- Measurements (in mm). Males (6 specimens measured): mountain biotopes in the western part of the island. body length mean 7.73 (min–max 5.87–9.37); vertex width 0.68 (0.50–0.85); pronotum length 0.39 (0.35–0.40); pro- Diagnosis notum width 0.92 (0.75–1.00); forewing length 9.82 (7.75– Relatively small-sized Chrysopa with boldly marked 10.62); forewing width 3.64 (3.12–4.00); hind wing length body (Figure 1). Head with reddish brown x-shaped 8.69 (7.25–9.75); hind wing width 3.21 (2.75–3.75). interantennal marking; vertex yellow with a pair of Females (5 specimens measured): body length mean 9.25 reddish brown stripes; gena and labrum with black (min–max 8.37–10); vertex 0.75 (0.75–0.75); pronotum stripe (Figure 2). Thorax with a pair of transverse length 0.46 (0.40–0.50); pronotum width 1.01 (0.85– dark brown bands (Figure 2). Pretarsal claws with 1.10); forewing length 11.42 (10.75–12.25); forewing

Figure 1. Chrysopa niki n. sp., live specimens, habitus. A, ♂ (Cyprus, Kalo Chorio, 17.VI.2016, not collected). B, ♂ paratype, pale morph (Koilani, Agia Mavri). C, ♀ paratype (Koilani, Agia Mavri). All photos by C. Makris. 4 D. Badano & C. Makris

Figure 2. Chrysopa niki n. sp., live specimens, details of head and thorax. A, ♂ paratype, pale morph (Koilani, Agia Mavri). B, ♀ paratype (Koilani, Agia Mavri). All photos by C. Makris.

width 4.07 (3.75–4.25); hind wing length 10.52 (9.75– Torulus creamy white. Scape creamy, with a small dark 11.12); hind wing width 3.61 (3.50–3.75). marking along the internal side. Pedicel creamy. Flagellum pale brown. Maxillary palp brown externally. Head. Base coloration pale green with prominent black Labial palp pale (Figure 4A). and reddish markings (Figures 2, 3, 4A). Vertex slightly raised, smooth, without setae (Figure 4A). Frons smooth, Thorax. Base coloration pale yellowish green with dor- shiny throughout. Clypeus flat, unsculptured. Labrum flat, salpaireddarkbands(Figure 2). Pro-, meso- and surface smooth; distal margin straight. Vertex yellow with metanotum with a pair of lateral dark brown stripes two paired, faded reddish stripes. Frons creamy with a running for their entire length (Figures 3 and 4B). reddish brown, x-shaped marking darker between the Pronotum with short, brown setae. Mesoscutellum antennae, surrounding the anterior and posterior margins with sparse brown setae. Pleurae pale green. Legs of the toruli and bordering the anterior margin of the pale, unmarked, covered with short black setae. vertex. Gena and clypeus marked with a lateral dark Pretarsal claws curved, base with trapezoidal dilatation black stripe reaching the compound eye. Labrum brown. (Figure 4C). Annales de la Société entomologique de France (N.S.) 5

Figure 3. Chrysopa niki n. sp., ♂ holotype with labels (abdomen and genitalia in Figure 5A) (Koilani, Agia Mavri). Scale bar: 1 mm.

Wings. Membrane hyaline, stigmas slightly opaque apically (Figure 5B–F). Gonosaccus ventral to the genital (Figure 4D). Forewing rounded apically. RP relatively sclerites, laterally bearing clusters of gonosetae rising straight; first crossvein between RP and MA almost from elevated bases (Figure 5B, C). touching the apex of the first intermedial cell; first inter- medial cell triangular; inner gradate series touching pseu- Female genitalia. Genitalia as for genus (Figure 6). domedia (i.e. amalgamation of radial and medial veins), Variability. In some specimens the dark pattern of the with 2–3 crossveins; outer gradate series with 5–6 cross- body is brown instead of blackish (Figures 1B and 2A), veins. Costal margin, Sc, RA, MP pale; all other long- thus the new species has distinct dark and pale morphs. itudinal veins, costal veinlets and crossveins dark brown. Hind wing rounded apically. Inner gradate series with 2 Etymology crossveins. Outer gradate series with 5–6 crossveins. The new species is named after Niki Makri, the daughter Costal margin, Sc and RA pale; all the other longitudinal of one of the authors, C. Makris. The specific name is a veins and crossveins pale brown (Figure 4D). noun in apposition.

Abdomen. Base coloration pale green. Tergites green with Comparative notes faint paired lateral brown markings, ventral margin Chrysopa niki n. sp. is unmistakable among western slightly tinged with brown. Sternites green, with slightly Palaearctic chrysopids because of its combination of brown dorsal margins (especially on the anterior seg- pale green body color, reddish brown x-shaped ments). Abdomen covered with short black setae. interantennal marking and vertex with reddish-brown stripes and thorax with transversal dark bands (Figure Male genitalia. Ectoproct relatively short, apically 1). Several Western Palaearctic Chrysopa species, such rounded (Figure 5A). Sternite 9 with ventral apodeme as C. perla (Linnaeus, 1758), C. walkeri, C. dorsalis extending dorsally in a sub-apical projection with Burmeister, 1839, C. nigrescens, C. hungarica Klapálek, rounded apex (Figure 5A); gonocoxites 9 [gonarcus] 1899 and C. fuscostigma Esben-Petersen, 1933 have arch-like in dorsal view, with a pair of lateral distal broad x-shaped black interantennal markings (Figure 7), projections and a pair of median distal subtriangular while they are narrow and reddish-brown in the new projections; gonapophyses 9 [entoprocessus] with distal species. Moreover, all these species usually have a black horn-like projections and with ventral wing-like or darkened pedicel (Figure 7), in contrast to the entirely projections converging medially (Figure 5B–F). green antenna of C. niki n. sp.(Figure 2). These Gonocoxite 10 [pseudopenis] hook-like, gently tapered Chrysopa species also share largely black abdominal 6 D. Badano & C. Makris

Figure 4. Chrysopa niki n. sp., details of head and thorax. A, ♂ paratype (Koilani, Agia Mavri), head in frontal view. B, ♀ paratype (Koilani, Agia Mavri), head and thorax, dorsal view. C, ♀ paratype (Koilani, Agia Mavri), pretarsal claw. D, ♂ paratype (Koilani, Agia Mavri), wings. Scale bars: 1 mm. Abbreviations: C = costa; Sc = subcosta; RA = radius anterior; RP = radius posterior; MA = media anterior; MP = media posterior; CuA = cubitus anterior; CuP = cubitus posterior; A = anal field; ig = inner gradates; og = outer gradates; psm = pseudomedia; psc = pseudocubitus; im = intramedian cell. tergites and sternites, while the abdomen is green (and crossveins in the forewing inner gradate than in the without bands) in C. niki n. sp. In contrast to the above outer series. Finally, at a first glance, C. niki n. sp. species with dark markings, all the remaining Western might resemble the small-sized, brownish and strongly Palaearctic Chrysopa species (see Aspöck et al. 2001 patterned species of the genera Pseudomallada for a complete list) have just a small dot between the Tsukaguchi, 1995 and Suarius Navás, 1914, but it is set antennae and inconspicuous head and body markings (see apart by the venational and genital characters of Monserrat 2016: figs 98, 102, 103, 105) or are completely Chrysopa. unmarked (see Monserrat 2016: figs 98, 106). C. niki n. sp., the totally green C. viridana and the sparsely spotted Life history C. sogdianica McLachlan in Fedchenko, 1875 are the Chrysopa niki n. sp. was mainly collected on only Western Palaearctic Chrysopa species with fewer Mediterranean oak trees, although it was also found Annales de la Société entomologique de France (N.S.) 7

Figure 5. Chrysopa niki n. sp., male abdomen and genitalia. A, Holotype (Koilani, Agia Mavri), abdomen with partly everted genitalia in lateral view. B–D, Paratype (Koilani, Agia Mavri), genitalia in B, lateral, C, ventrolateral and D, ventral views. E, F, Genitalia, schematic drawing. Scale bars, A: 0.5 mm, B–F: 0.2 mm. Abbreviations: ect = ectoproct; dap = dorsal apodeme; gs = genital sclerites; vap = ventral apodeme; gp9 = gonapophyses 9; gx9 = gonocoxites 9; gx10 = gonocoxites 10; gnsc = gonosaccus; gnst = gonosetae; T = tergite; S = sternite; sp = spiracle. on conifers. In the site of Agia Mavri (34°50ʹ43.56ʺN L. and Rubus sanctus Schreb. In another locality, near 32°52ʹ8.56ʺE), located at 722 m asl, specimens of the Pera Pedi (34°52ʹ31.25ʺN 32°52ʹ0.91ʺE, 722 m asl), C. new species were found on Quercus infectoria veneris niki n. sp. was collected on the endemic Quercus (A.Kern.) Meikle heavily infested with aphids, near a alnifolia PoechinapineforestwithPinus brutia river valley with a riparial vegetation of Alnus Ten., Quercus alnifolia, Arbutus andrachne L. and orientalis Decne., Platanus orientalis L., Salix alba Cistus creticus L. Only one specimen was found on 8 D. Badano & C. Makris

Coniopterygidae (3 species), Hemerobiidae (4 species) and most species of Chrysopidae and Myrmeleontidae. (Aspöck & Hölzel 1996; Aspöck et al. 2001). Several species are Eastern Mediterranean faunal elements, including the only species of Berothidae and Mantispidae present on the island, i.e. Isoscelipteron ful- vum Costa, 1863 and Mantispa scabricollis McLachlan in Fedchenko, 1875, one chrysopid, Suarius nanus (McLachlan, 1893), and some Myrmeleontidae and Ascalaphidae, such as Nemoleon poecilopterus (Stein, 1863), Neuroleon assimilis (Navás, 1914), Libelloides rhomboideus (Schneider, 1845), and Deleproctophylla variegata (Klug in Ehrenberg, 1834) (Aspöck et al. 2001; Kral & Devetak 2016; Badano et al. 2018). Figure 6. Chrysopa niki n. sp., ♀ paratype (Koilani, Agia Myrmeleontiformia are the only group of Cypriot lacew- Mavri), abdomen, lateral view. Scale bars: 0.5 mm. ings comprising Middle Eastern elements such