Redescription of the Planthopper Bursinia genei (Dufour, 1849), with a New Record from Greece (Hemiptera: Fulgoromorpha: Dictyopharidae)

© 2022 Academia Sinica, Taiwan Open Access Redescription of the Planthopper Bursinia genei (Dufour, 1849), with a New Record from Greece (Hemiptera: Fulgoromorpha: Dictyopharidae) Leonidas-Romanos Davranoglou1,*,§ , Igor Malenovský2,3,§ , Zestin Wen Wen Soh4, Christian M. Schlepütz5, and Michael R. Wilson6 1Oxford University Museum of Natural History, University of Oxford, Oxford, United Kingdom. *Correspondence: E-mail: [email protected] (Davranoglou) 2Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, Brno, CZ-61137, Czech Republic. E-mail: [email protected] (Malenovský) 3Department of Entomology, Moravian Museum, Zelný trh 6, Brno, CZ-65737, Czech Republic 4Singapore Botanic Gardens, National Parks Board, 1 Cluny Road, Singapore 259569. E-mail: [email protected].sg (Soh) 5Swiss Light Source, Paul Scherrer Institute, 5232 Villigen, Switzerland. E-mail: [email protected] (Schlepütz) 6Department of Natural Sciences, National Museum of Wales, Cardiff, CF10 3NP, United Kingdom. E-mail: [email protected] (Wilson) §LRD and IM contributed equally to this work. Received 8 April 2022 / Accepted 15 June 2022 / Published 27 September 2022 Communicated by Y. Miles Zhang Bursinia genei (Dufour, 1849) is the most widespread species of the planthopper subfamily Orgeriinae (Hemiptera: Fulgoromorpha: Dictyopharidae) in Europe, found from the Iberian Peninsula to the Western Balkans. However, its diagnostically important genitalia and biology have been insufficiently described. We employ state-of-the-art synchrotron X-ray microtomography and photomicrography to re-describe B. genei, and to study the morphology of both its sexes in unprecedented detail. By examining specimens from across the distribution of B. genei, we find that they probably belong to a single, broadly distributed morphospecies. Our morphological examination allowed us to make inferences on its jumping mechanism and capacity for vibrational communication. We also record B. genei for the first time from Greece, further extending the range of this elusive species. Detailed information on the habitat of B. genei is also provided. Key words: Auchenorrhyncha, Orgeriinae, Snapping organ, Balkans, Taxonomy, X-ray tomographic microscopy. BACKGROUND The planthopper genus Bursinia Costa, 1862 (Hemiptera: Dictyopharidae: Orgeriinae: Almanini) comprises 18 species with a largely West Mediterranean distribution, whose centre of diversity is in the Iberian Peninsula, where 11 species are endemic (Horváth 1910 1913 1936; Emeljanov 1972 1980 2003; Emeljanov and Drosopoulos 2004; Bourgoin 2022). Bursinia is split into two subgenera: Bursinia sensu stricto, distributed primarily in southern Europe, and Struthionia Emeljanov, 2009, which is found exclusively in North Africa (Algeria, Morocco, Tunisia), Spain, Sicily and Malta (Emeljanov 2003 2009; Linnavuori 1965). However, the validity of the various Bursinia spp. is ambiguous, as the genus has not been revised since the work of Horváth (1910), and most species descriptions are short, with few to no illustrations of diagnostic features such as the genitalia. An updated taxonomic revision of all described taxa in this biogeographically interesting genus is urgently required. As a first step towards the abovementioned objective, we studied the taxonomy of the most widespread species of the genus, B. (Bursinia) genei Citation: Davranoglou LR, Malenovský I, Soh ZWW, Schlepütz MC, Wilson MR. 2022. Redescription of the planthopper Bursinia genei (Dufour, 1849), with a new record from Greece (Hemiptera: Fulgoromorpha: Dictyopharidae). Zool Stud 61:51. doi:10.6620/ZS.2022.61-51. Zoological Studies 61:51 (2022) doi:10.6620/ZS.2022.61-51 1 © 2022 Academia Sinica, Taiwan (Dufour, 1849), which was described from Sardinia and later recorded from Spain, Portugal, France (including Corsica), mainland Italy, Croatia, Bosnia and Hercegovina, and Montenegro (Horváth 1910; Melichar 1912; Metcalf 1946; Emeljanov 2003). Like most of its congeners, B. genei is an elusive species that has seldom been collected, and almost nothing is known regarding its biology. Furthermore, the genitalia of this species have only been illustrated partly and schematically (Emeljanov 1980), which makes it difficult to distinguish it from its congeners. It is also possible that being flightless, different subpopulations may have been isolated for millennia, leading to the evolution of multiple related cryptic species. In the present study, we use conventional and state-of-the-art techniques to redescribe the morphology of B. genei, providing the first detailed description of its genitalia based on material from across the species’ distribution. We used synchrotron X-ray microtomography (SR-μ-CT) to reconstruct the internal morphology of B. genei, which allowed us to make inferences regarding aspects of its jumping and vibrational behaviour. We also record B. genei from the Pindus mountain range in Epirus, Greece, for the first time, further extending its distribution to south-eastern Europe. MATERIALS AND METHODS Photomicrographs of the habitus of B. genei were taken using a Leica M165c binocular microscope equipped with a Leica DFC490 camera at the Oxford University Museum of Natural History (OUMNH), or a Keyence VHX-5000 digital microscope with VHZ20T and and VH-ZST objectives at the Department of Botany and Zoology, Masaryk University, Brno. The latter equipment was also used to image the snapping organ and genitalia of B. genei. All photomicrographs were stacked and combined using Helicon Focus or Keyence VHX-5000 software. For examination of male and female genitalia, abdomina were detached from specimens and cleared in a 10% solution of warm KOH for approximately two hours. Dissections were made in distilled water. A few drops of chlorazol black (CAS No. 1937–37–7) were later added to water to dye the female ectodermic genital ducts (Carayon 1969; Bourgoin 1993). X-ray tomographic microscopy scans of a criticalpoint dried male specimen of B. genei from Greece were obtained at the TOMCAT beamline, Swiss Light Source (SLS), Paul Scherrer Institut, Switzerland, at an X-ray beam energy of 15.99 keV with final pixel size of 1.625 μm. Three-dimensional image processing and segmentation was carried out using Amira 6.1 software (Mercury Systems). Image labelling and illustrations were generated in Adobe Illustrator CC/CS6 (Adobe Systems Incorporated, San Jose, California, USA). As we did not have the opportunity to study the type material of B. genei or any other specimen from Sardinia, the species’ type locality, we used the works of Horváth (1910), Melichar (1912), Emeljanov (1969 1972 1980 2009) and Emeljanov and Drosopoulos (2004) for the identification of the examined material. The identification of the specimens from Greece as B. genei was also kindly confirmed by Prof. Alexander F. Emeljanov (Zoological Institute, Russian Academy of Sciences, St. Petersburg) based on habitus photographs. The morphological terminology in the description follows Song et al. (2018) for the general morphology and male genitalia, Bourgoin (1993) for the female genitalia, and Davranoglou et al. (2019) for the vibrational (snapping) organ. The examined specimens were deposited at the Natural History Museum in London (BMNH) and the Moravian Museum in Brno (MMBC). RESULTS TAXONOMY Class Insecta Linnaeus, 1758 Order Hemiptera Linnaeus, 1758 Suborder Auchenorrhyncha Duméril, 1806 Infraorder Fulgoromorpha Evans, 1946 Family Dictyopharidae Spinola, 1839 Subfamily Orgeriinae Fieber, 1872 Tribe Almanini Kusnezov, 1936 Genus Bursinia Costa, 1862 Bursinia genei (Dufour, 1849) (Figs. 1–10) Dyctiophora [sic] senegalensis nec Spinola, 1839 – Spinola 1839: 296 (misidentification, not conspecific with the type of D. senegalensis, now Philotheria senegalensis (Spinola, 1839), according to Melichar 1912: 93 and Metcalf 1946: 189). Dyctiophora [sic] genei Dufour, 1849: 101 (original description). Almana genei – Stål 1861: 150 (new combination, listed). Bursinia genei – Horváth 1910: 180, 183, fig. 5 (new combination, in key, redescription); Melichar 1912: 185, 188 (in key, redescription); Metcalf 1946: 189 (catalogue); Emeljanov 1980: 27, 29, figs. 113, 126 (drawings of female gonapophysis VIII and male phallotheca). Bursinia genei var. dispar Horváth, 1910: 180, 184, fig. 6. Synonymy according to Nast 1972: 93. Bursinia (Bursinia) genei – Emeljanov 2009: 48 (listed). Material examined: Spain: Sierra de Guadarrama, page 2 of 15Zoological Studies 61:51 (2022) © 2022 Academia Sinica, Taiwan viii.1927, Uvarov leg., 1 m*, 1 f* (BMNH); Espinar, viii.1894, I. Bolivar leg., 1 f* (MMBC). France: AlpesMaritimes, Théoule, 14.vii.1955, P. Hervé leg., 1 m*; Alpes-Maritimes, Sospel env., Albaria, Mt Razit, 700 m, 31.vii.1955, P. Hervé leg., 1 m*; Serres, 8.vii., F. Lombard leg., 2 m*m*; same data but ix., 1 m* 1 f* (all MMBC). Croatia: Murter, Slanica, 25.viii.1983, I. Vavřínová leg., 1 m*; Dalmatia, Ragusa, 2 m* m* (all MMBC). Greece: Epirus, Konitsa Municipality, outskirts of Konitsa, 40°2'56.80"N, 20°45'50.53"E, 818 m, 24.vii.2015, L.-R. Davranoglou & Z.W.W. Soh leg., 2 m*m* (BMNH). Redescription: Colouration (same in both sexes). General body colour light ochreous; tegmina ochreous to dark brown, often darker than rest of body (Fig. 1A–D); cephalic process with a dark brown-greyish suffusion that runs along most of its length, becoming lighter at level of eyes (Fig. 1B–E); a dark brown band extending from paranotal lobe of pronotum to the head at the level of antennae, often reaching clypeal area Fig. 1. Dorsal habitus of male B. genei. (A) Specimen from Epirus, Greece. (B) Close-up view of head. (C) Specimen from Murter, Croatia. (D) Specimen from Serres, France. (E) Close-up view of head of specimen from Serres, France. Abbreviations: ica = intermediate carina of abdomen; mca = median carina of abdomen; mcv = median carina of vertex. page 3 of 15Zoological Studies 61:51 (2022) © 2022 Academia Sinica, Taiwan (Fig. 2A–C); thorax, legs, and abdomen light ochreous, mottled with dark brown spots throughout their surface (Figs. 1, 2); fore and mid coxae and tarsi, and apices of fore and mid tibiae and metatibial spines all distinctly dark brown (Fig. 1A). Structure: Head: vertex slightly elevated from plane of pronotum in lateral view (Figs. 2A, B; 3A, B), its base 1.65–1.85 times wider than maximum width of eye in dorsal view (Fig. 1A–C); median carina of vertex distinct basally and apically, faint in the middle on cephalic process in front of eyes (Fig. 1B, E); head, in dorsal view, 2.3–3.7 times longer than vertex width at anterior eye margin); base of vertex tapered, its posterior margin straight, apex or cephalic process, in dorsal view, narrowly rounded (Fig. 1); frons with sharply delimited lateral, intermediate and median carinae (Fig. 2C); lateral carinae of frons joining lateral carinae of vertex subapically, at a clear distance from apex of cephalic process; apex of cephalic process, in lateral view, broadly, asymmetrically rounded (Fig. 2A–C), in frontal view, apical swelling (apical callus) of cephalic process longer than broad; area between intermediate and lateral carinae apically with three rows of sensory pits reaching the very apex of cephalic process, only one or two rows continue downward to level of eyes and beyond (Figs. 2C, 3B); postocular swelling (callus postocularis) well developed, distinctly concave in lateral view (Fig. 3B–D); ocelli rudimentary, only present as a small brown spot in front of eye (Fig. 2C: black arrow); antenna small: scape shortly circular; perdicel bulbous, bearing ca 25 plate organs (sensilla placodea) spread over most of its surface. Pronotum: Distinctly raised in lateral view (Figs. 2A, B; 3A–C); in dorsal view, anterior margin tapered, nearly straight (Figs. 1, 3A), with distinctly ridged median and intermediate carinae; discal area enclosed by inner margin of intermediate carina with three sensory pits (Fig. 3A, C), remainder of disk bare; lower lateral carina distinct, arc-shaped in dorsal view, enclosing about 14 sensory pits (Fig. 3A–C); area enclosed by lower lateral carina and paranotal lobe of pronotum with two sensory pits (Fig. 3B, D); paranotal lobe of pronotum expanding ventrally into a rounded plate, with a distinct carina and a single sensory pit (Fig. 3D); posterior margin of pronotum only slightly concave, with a nearly indistinct median notch (Fig. 3A). Mesonotum: broad, 1.65–1.77 times longer than maximum length of pronotum; median carina distinct, almost reaching scutellar apex (Figs. 1B–D; 3A); lateral carinae of mesonotum short, straight, diverging laterally (Figs. 1C, 3A); part of mesonotum enclosed by the external margin of the lateral carina with six sensory pits (Fig. 3A–C). Tegmina: micropterous, coriaceous, firmly interlocked, not reaching (Fig. 1A, D) or slightly surpassing (Fig. 1C) posterior margin of tergum III; apical margin truncate (Fig. 1A, C, D); wing surface glabrous, reticulation very faint (Fig. 1D) or entirely absent (Fig. 1A, C); hind wings absent. Legs: femora on all legs unarmed; hind tibia with 3–6 lateral spines and 6–10 apical teeth; each hind Fig. 2. Lateral habitus of male B. genei. (A) Specimen from Murter, Croatia. (B) Specimen from Serres, France. (C) Specimen from Epirus, Greece. Abbreviations: icf = intermediate carina of frons; lcf = lateral carina of forns; mcf = median carina of frons. page 4 of 15Zoological Studies 61:51 (2022) © 2022 Academia Sinica, Taiwan tarsomere with 12–14 platellae ventrally and a pair of apical teeth laterally. Pregenital abdomen: short and broad (Fig. 1A, C, D), 1.15–1.3 times longer than maximum width, with a distinct median carina on each tergite, and an intermediate one, towards the junction between tergum and sternum (Fig. 1C, D); terga IV–VI with 3+3 and terga VII and VIII usually with 4+4 (sometimes 4+3 or 3+4), sensory pits laterally (mediad of intermediate carinae), arranged in transversal rows. Snapping organ of the fulgorid-dictyopharid type (Fig. 10). Male genitalia: Dorsal margin of pygophore (segment IX), in profile, with a deep emargination (Figs. 4F, 5A, 6B); ratio of ventral to dorsal profile length 3.8; upper process of gonostyle short, rounded, hooklike process of gonostyle short, subtriangular, with a rounded apex (Figs. 4A–C, F; 5A; 6A–C); segment X (anal tube) in dorsal view short and broad, rounded (Figs. 4A, 6A), ratio of length to width about 1.5; anal style short, not reaching apex of segment X by its about half its length (Figs. 4A, 6A); base of phallotheca broad and trapezoid, remaining portion very long and slender (Figs. 4B: white arrow; 6D: black arrow); distal margin of phallotheca with a distinct emargination medially (Fig. 4B: black arrow); each dorsolateral lobe of phallotheca split into two subconical lobes, unarmed (Fig. 4A, B, E, F); ventral lobe of phallotheca strongly developed downwards, split in the middle (Fig. 4C–E), with a sawlike dorsal margin (Fig. 4F), without any sclerotised spines or denticles; endosomal processes strongly inflated, each with a single row of denticles, interrupted in the middle by unarmed surface (Figs. 4A, C, E, F; 5C, D); endosomal processes ending in an acute spine (Fig. 5D). Uninflated phallotheca as in figure 6B, F. Note: The genitalia of the male specimen from Pindos, Greece, were damaged during maceration, but Fig. 3. Three-dimensional reconstruction of synchrotron microtomographic scans of male specimen of B. genei from Greece. (A) Head, proand mesonotum, dorsal view. (B) Same, lateral view. (C) Same, dorsolateral view. (D) Frontolateral view, with emphasis on paranotal lobe. page 5 of 15 Zoological Studies 61:51 (2022) © 2022 Academia Sinica, Taiwan Fig. 4. Male genitalia of B. genei from Serres, France. (A) Dorsal view, blue arrows indicating gap between row of spines on endosomal process of phallotheca. (B) Same, with segment X raised, black arrow indicating the emargination of the phallothecal apex. (C) Ventral view. (D) Same, close-up of ventral lobe of phallotheca. (E) Ventral view, emphasising on the dorsolateral lobes of phallotheca. (F) Lateral view. Abbreviations: gs = gonostyle; ep = endosomal processes; dll = dorsolateral lobe of phallotheca; hpg = hook-like process of gonostyle; upg = upper process of gonostyle; pt = phallotheca; vl = ventral lobe of phallotheca. page 6 of 15Zoological Studies 61:51 (2022) © 2022 Academia Sinica, Taiwan they possess all the diagnostic characters found in other examined specimens of B. genei, namely in the overall shape and proportions of the pygophore and gonostyles (Fig. 5A), the trapezoid base of phallotheca (Fig. 5B, white arrow), and endosomal processes with a single row of denticles that are interrupted in the middle (Fig. 5D, black arrow). The morphology of the external male genitalia of the Spanish specimens is largely the same with the other populations, although the endosomal processes possess a single row of spines that are confined only towards their apex, are not interrupted, and are somewhat larger (Fig. 6A, B, E). More samples should be studied to determine whether these slight differences are fixed in most of the Spanish populations of B. genei. The Spanish populations, are however, likely conspecific with the remaining European ones, as all other features are largely identical. Female genitalia: external view of female genitalia as in figure 7A, B; segment X (anal tube) as in figure 7C, ratio of length to width about 1.2; posterior lobe Gp1 of gonoplac (valvula 3) simple, rounded, more than three times thicker than posterior lobe Gp2, without any spines, apex subtriangular (Fig. 7D); gonapophysis IX (valvula 2) with posterior connective lamina symmetrical in ventral view, completely fused at base, apex of sclerotised part harpoon-shaped (Fig. 7E); gonocoxa VIII (valvifer VIII) with anterior connective lamina consisting of six gradually enlarging, blunt teeth (Fig. 7F); endogonocoxal process largely membranous, subtriangular (Fig. 7F); bursa copulatrix with a single pouch, almost globular in dorsal (Fig. 8A) and lateral (Fig. 8B, C) views, its entire surface with distinct pitFig. 5. Male genitalia of B. genei from Epirus, Greece. (A) Pygophore, lateral view. (B) Same, caudal view, white arrow indicating trapezoid base of phallotheca. (C) Low resolution image of endosomal process, lateral view. (D) Same, with outline traced, black arrow indicating unarmed area between row of spines of endosomal process. page 7 of 15Zoological Studies 61:51 (2022) © 2022 Academia Sinica, Taiwan Fig. 6. Male genitalia of B. genei from Guadarrama, Spain. (A) Dorsal view. (B) Lateral view. (C) Ventral view. (D) Ventrocaudal view, black arrow indicating trapezoid shape of base of phallotheca. (E) Extracted endosomal process of phallotheca. (D) Phallotheca with uninflated lobes. Abbreviations: dll = dorsolateral lobe of phallotheca; ep = endosomal process of phallotheca; sp = spine at apex of endosomal process; vl = ventral lobe of phallotheca. page 8 of 15Zoological Studies 61:51 (2022) © 2022 Academia Sinica, Taiwan Fig. 7. Female genitalia of B. genei from Serres, France. (A) External genitalia, dry-mounted, ventral view. (B) Same, lateral view. (C) Segment X, macerated, dorsal view. (D) Gonoplac, outer lateral view. (E) Gonapophysis IX, ventral view. (F) Gonocoxa and gonapophysis VIII, outer lateral view. Abbreviations: acl = anterior connective lamina; gp1, gp2 = posterior lobes of gonoplac; gxVIII = gonocoxa VIII; gxp = endogonocoxal process; pcl = posterior connective lamina. page 9 of 15 Zoological Studies 61:51 (2022)