ISSN 0013-8738, Entomological Review, 2016, Vol. 96, No. 3, pp. 288–293. © Pleiades Publishing, Inc., 2016. Original Russian Text © O.S. Korsunovskaya, 2016, published in Entomologicheskoe Obozrenie, 2016, Vol. 95, No. 2, pp. 301–308.

On the Distribution of the Bush Cricket albopunctata transiens Zeuner, 1941 (, ) in the South of European Russia and in Uzbekistan O. S. Korsunovskaya Faculty of Biology, Lomonosov Moscow State University, Moscow, 119234 Russia e-mail: [email protected] Received January 31, 2016

Abstract—Based on examination of the morphological characters and comparative analysis of the male calling acoustic signals, distribution of the subspecies transiens Zeuner, 1941 in the south of European Russia (Crimea and North Caucasus) and in Uzbekistan is proved. DOI: 10.1134/S0013873816030064

Species of the Palaearctic genus Platycleis Fieber, Platycleis intermedia differs from the preceding spe- 1853 are broadly distributed in Eurasia, from the Ibe- cies in the tooth positioned distal to the middle of the rian Peninsula to Transbaikalia. The following repre- cercus and in the presence of one or two more or less sentatives of the nominotypical subgenus have been distinct tubercles on abdominal sternite VII in females. recorded in Russia and adjacent countries: Its titillators are narrower and have a longer apical P. intermedia intermedia (Serville, 1838), P. albo- portion (Tarbinsky, 1948; Ramme, 1951; Harz, 1969). punctata grisea (Fabricius, 1781), P. escalerae This species, described from Montpellier (France), is Bolívar, 1899, and P. affinis Fieber, 1853 (Bey- distributed in the Mediterranean, from Spain and Mo- Bienko, 1964; Sergeev, 1986; Storozhenko, 2004). In rocco to Turkey, and also in Central Asia (Ragge, all the keys and taxonomic works (e.g., Zeuner, 1941; 1990; Benediktov, 2015). Within the territory of Rus- Tarbinsky, 1948; Ramme, 1951; Bey-Bienko, 1964; sia, it was recorded in the steppe zone, from the Cau- Harz, 1969; Ragge, 1990) these species are differenti- casus to Kazakhstan and Western Siberia (Bey- ated mostly by the structure of abdominal sternite VII Bienko, 1964; Storozhenko, 2004). Platycleis interme- in females, the position of the cercal tooth in males, dia reveals high variation of the main diagnostic char- and the shape of the titillators in the male genitalia. In acters, including those of the male genitalia, in par- ticular the curvature of the titillators, the length of addition, representatives of the genus Platycleis can be their distal portion, and the number and size of easily differentiated by the temporal and (partly) fre- spinules on it (Ramme, 1951; Kaltenbach, 1974). quency parameters of their calling signals (see, e.g., Transitional forms between P. albopunctata grisea Heller, 1988). The following morphological characters and P. intermedia exist in the mountains of Southern are typical of P. albopunctata: the cerci of males with Europe, being especially common in the Balkans (Ze- a tooth near the middle, the titillators with a relatively uner, 1941; Ramme, 1951; Ragge, 1990). Based on the massive basal part, and a smooth abdominal ster- presence of projections on abdominal sternite VII in nite VII in females. Platycleis albopunctata albopunc- females, resembling the tubercles of P. intermedia, tata differs from P. albopunctata grisea in the state Zeuner (1941) described the subspecies P. grisea tran- of the female’s proximal side sclerite (the lateral part siens Zeuner, 1941 from Greece; later, regarded this of the subgenital plate), which is separated from the form and P. albopunctata grisea Heller (1988) as two subgenital plate in the former subspecies and merged subspecies of P. albopunctata. with it in the latter. It is presently assumed that the nominotypical subspecies occurs in the western part of Thus, due to high variation and the existence of the range, from the Iberian Peninsula to the Alps, transitional forms, the known morphological charac- while P. albopunctata grisea occupies its eastern part, ters cannot serve as reliable criteria for identification as far as Crimea and the Caucasus (Ragge, 1990). of some species of Platycleis. At the same time, inten-

288 ON THE DISTRIBUTION OF THE BUSH CRICKET 289 sive studies of the acoustic signals of Orthoptera car- base of the elytra and consisting of the pars stridens on ried out in Western Europe and Russia (e.g., see re- the upper elytron and the plectrum on the lower views in Zhantiev, 1981; Heller, 1988; Ragge and elytron. The rhythmic pattern of the acoustic signals Reynolds, 1998) provide the means of solving compli- was described using the terminology proposed by cated taxonomic and biogeographic problems. In par- R.D. Zhantiev (1981). A pulse is an elementary sound ticular, they can be used to clarify the taxonomic posi- produced by the closing of the elytra; an interpulse is tion and distribution of bush crickets of the species a sound produced by the opening of the elytra; a series group P. albopunctata–P. intermedia. is a periodically repeated group of pulses.

MATERIALS AND METHODS RESULTS AND DISCUSSION To ensure exact identification, we used only those The examined specimens from Crimea, North Os- specimens whose signals are kept in the sound record setia, and Uzbekistan resemble P. intermedia in the collection of the Department of entomology, Lomo- complex of morphological characters (Figs. 1, 2): in nosov Moscow State University (MSU). males, the tooth on the cercus lies distal to its middle; in females, abdominal sternite VII has two small pro- Material. Hungary. Env. of Budapest, VII.2002 jections in its central and apical parts (Figs. 1a, 1b). (O.S. Korsunovskaya), 1 ♂. Russia. Crimea: env. of The basal portion of the titillators in the male genitalia Yalta, Mt. Krestovaya, VIII.1995 (R.D. Zhantiev), (Figs. 2b–2e) is narrower than in P. albopunctata al- 2 ♂; Sevastopol: VIII.1995 (V.V. Avdonin), 2 ♂, 1 ♀; bopunctata and P. albopunctata grisea (Fig. 2a) (see V.1996 (V.V. Avdonin), 1 ♀ ex larva. North Ossetia: Ragge, 1990, figs. 2–4). However, these specimens are Tseiskii Reserve, VIII.1990 (D.Yu. Tishechkin), 3 ♂. just as likely to belong to P. albopunctata transiens. Uzbekistan. Env. of Termez, VII.1991 (V.Yu. Sa- The male from Hungary, whose titillators have vitsky), 1 ♂. a shorter and more massive basal part, may be identi- Methods. Male genitalia were dissected from the fied as P. albopunctata grisea. Indeed, by the temporal ultimate abdominal segments and treated with 10% parameters of their calling signals (Fig. 3) the studied KOH solution for 15 h; the titillators were rinsed in specimens should be assigned to P. albopunctata, distilled water, embedded in glycerol, and documented whose signals were repeatedly described based on using a Canon EOS 6D digital camera with a Canon material from Western Europe (Samways, 1976; MP-E65 macro lens. Drawings were made from the Latimer, 1981; Heller, 1988; Ragge, 1990). Males of photos with a Wacom CTE-440 graphics tablet. this species emit series of 3–5 (very rarely 6 or 7) pulses, usually with no interpulses. The durations of The sounds emitted by the were recorded us- pulses and intervals between them decrease as the ing a Brüel & Kjær Type 4135 microphone with a temperature grows. According to the earlier publica- Type 2604 amplifier or an RFT MK-301 microphone tions (Samways, 1976; Latimer, 1981; Heller, 1988) with an RFT 00017 amplifier. The microphone with- and the records of Western European specimens of out a protection grid was positioned 5–10 cm from the P. albopunctata present in the Orthoptera Species File . The acoustic signals were recorded at a con- database (Eades et al., 2016), the pulse duration varies trolled temperature with a customized Jupiter-202 from 43–50 to 60–70 ms and the pulse repeat fre- Stereo tape recorder (tape speed 38 cm/s; frequency quency is about 11–14 s−1 (20–22°C). response nonlinearity ±1 dB within a range of 2–70 kHz); alternatively, the signal from the amplifier The calling signal of P. intermedia is a sequence of output was fed to an L305 or L-14440 analog-digital two-pulse series (Samways, 1976; Heller, 1989; converter (L-Card, Russia) and saved to a file. The Ragge, 1990). sampling frequencies were 30 303, 58 864, 142 857, The temporal parameters of some European and and 200 000 Hz. The taped signals were digitized off- Asian specimens of P. albopunctata are summarized line. The temporal and frequency parameters were in the table. analyzed using the CoolEditPro, Turbolab v.4.2, MiniAnalysis, and PowerGraph software. The temporal parameters of acoustic signals of bush crickets from different localities are very similar. The Terminology. Bush crickets are known to emit observed differences among them may result from the sounds with a stridulatory apparatus located at the temperature or intraspecific variation. The coefficient

ENTOMOLOGICAL REVIEW Vol. 96 No. 3 2016 290 KORSUNOVSKAYA

Fig. 1. Platycleis albopunctata transiens Zeuner, female (env. of Sevastopol): (1) abdominal sternite VII; (2) subgenital plate; (3) side sclerite: (a) ventral view; (b) lateral view.

Fig. 2. Platycleis albopunctata (Goeze), right titillators of the male genitalia: (a) P. albopunctata grisea (F.) (env. of Budapest); (b–e) P. albopunctata transiens Zeuner: (b) env. of Sevastopol; (c) env. of Yalta; (d) Tseiskii Reserve; (e) env. of Termez. of variation of the duration of signal elements varies in maximum or several peaks with slightly decreasing different specimens from 2.8 to 5.3 (duration of amplitudes at 15–22 kHz (Fig. 4). The dominant fre- pulses) and may reach 11.73 (duration of intervals quencies of P. albopunctata albopunctata from West- between pulses). The most stable parameter is the ern Europe are slightly shifted toward the higher fre- pulse period (Latimer, 1981). quencies (Heller, 1988). The frequency parameters of the calling signals of No individuals emitting signals with the temporal European and Central Asian bush crickets are also pattern corresponding to P. intermedia were revealed similar. The signal spectrum lies within the range of during long-term studies in Russia and the former 10–40 kHz; the dominant frequencies form a single USSR territory. The bush crickets distributed in Rus-

ENTOMOLOGICAL REVIEW Vol. 96 No. 3 2016 ON THE DISTRIBUTION OF THE BUSH CRICKET 291

Fig. 3. Oscillograms of the calling signals of Platycleis albopunctata (Goeze): (a) P. albopunctata grisea (F.) (env. of Budapest); (b–d) P. albopunctata transiens Zeuner: (b) env. of Sevastopol; (c) Tseiskii Reserve; (d) env. of Termez. Time bar: 100 ms.

Fig. 4. Amplitude-frequency spectra of the calling signals of Platycleis albopunctata (Goeze): (a) P. albopunctata grisea (F.) (env. of Budapest); (b–d) P. albopunctata transiens Zeuner: (b) env. of Sevastopol; (c) Tseiskii Reserve; (d) env. of Termez. sia and adjacent countries to the south and southeast similar to those of acridoid grasshoppers (see, e.g., obviously belong to P. albopunctata transiens, while von Helversen and von Helversen, 1975; Vedenina the range of P. intermedia is restricted to Western et al., 2012), are known in Platycleis; second, all Europe. The center of speciation of the group interme- the forms with intermediate morphological characters dia—albopunctata lies in Western Europe and emit calling signals with the temporal pattern of possibly in Western Asia (Zeuner, 1941; Ramme, P. albopunctata. By contrast, their genital morphology 1951; Kaltenbach, 1974). Cross between P. intermedia reveals a wide range of variation of such characters as and P. albopunctata occurs in the intergradation zone the shape of the titillators, the relative size of their east of the Alps, but the hybrids inherit the temporal basal and apical parts, and the number and position of signal pattern of only one of the two species, mostly spinules on them. Such diversity results either from P. albopunctata: first, no transitional signal variants, a high level of intraspecific variation or from hybridi-

ENTOMOLOGICAL REVIEW Vol. 96 No. 3 2016 292 KORSUNOVSKAYA

Temporal parameters of the calling signals in different subspecies of Platycleis albopunctata Goeze: mean ± standard de- viation (M ± SD) Number Temperature Frequency Duration Duration of intervals Subspecies of pulses during of series, s–1 of pulses, ms between pulses, ms per series recording, °C P. a. albopunctata (Germany, 4–5 1.6 ± 0.06 50 ± 2.9 20 ± 1.7 22 Baden-Württemberg, Mun- 55 ± 2.3 22 ± 1.8 zingen (Heller, 1978, cited 53 ± 2.6 25 ± 3.2 from Eades et al., 2016) 46 ± 3.7 28 ± 4.1 35 ± 7.7 P. a. grisea (Hungary, 4 1.1 ± 0.1 43 ± 6 23 ± 2.9 26 env. of Budapest) 46 ± 2.3 26 ± 1.7 46 ± 2.3 28 ± 2.7 40 ± 2.5 P. a. transiens (Crimea, 5 1.2 ± 0.05 67 ± 2.3 23 ± 2.9 21 env. of Sevastopol) 73 ± 2.2 22 ± 3.9 73 ± 3.9 22 ± 3.1 71 ± 2.9 28 ± 4.5 57 ± 9.3 P. a. transiens (North Ossetia, 3–5 1.9 ± 0.4 54 ± 4.7 26 ± 4.3 24 Tseiskii Reserve) 63 ±4.7 25 ± 2.5 53 ± 3.3 32 ± 6.3 47 ± 7.6 45 ± 4.3 39 ± 2.9 P. a. transiens (Uzbekistan, 5–6 1.9 ± 0.5 50 ± 9.8 28 ± 3.0 22 env. of Termez) 64 ± 2.8 27 ± 1.7 65 ± 3.8 29 ± 3.3 63± 5.5 32 ± 4.7 55 ± 5.4 37 ± 4.2 47 ± 7.5

zation. It may therefore be concluded that bush evolves at a lower and a more uniform rate due to ge- crickets of the species group P. albopunctata—P. in- netic drift. Correspondingly, it may be assumed that termedia present in the territory of Russia and adjacent speciation in these bush crickets starts with changes in countries cannot be reliably identified based on mor- the acoustic signals, which constitute the most labile phological characters alone. At the same time, the prezygotic isolation mechanism and form a fairly reli- temporal patterns of their acoustic signals provide able barrier against interspecific crossing. reliable diagnostic characters. These results agree well with the hypothesis of Gorochov (2014) on the pri- ACKNOWLEDGMENTS mary (stable) and secondary (variable) sexual charac- I am very grateful to R.D. Zhantiev, D.Yu. Tishech- ters with different modalities and functional roles dur- kin, V.V. Avdonin, and V.Yu. Savitsky for collecting ing reproduction. The male genital morphology in the the insects. species group P. albopunctata – P. intermedia evi- dently belongs to the first group of characters (unlike This work was carried out within the framework of the acoustic signal parameters), which relatively the research plan of Department of Entomology, MSU weakly depends on the environmental conditions and (“Theoretical Problems of General and Applied Ento-

ENTOMOLOGICAL REVIEW Vol. 96 No. 3 2016 ON THE DISTRIBUTION OF THE BUSH CRICKET 293 mology,” Federal Research Database No. АААА-А16- 9. Ragge, D.R., “The Songs of the Western European 116021660101-5). Morphological data were obtained Bush-Crickets of the Genus Platycleis in Relation to with financial support of the Russian Science Founda- Their (Orthoptera: Tettigoniidae),” tion (project 14-50-00029: “Scientific Basis of the Bull. Brit. Mus. Nat. Hist. Entomol. 59 (1), 1–35 National Biobank—Depository of the Living Sys- (1990). 10. Ragge, D.R. and Reynolds, W.J., The Songs of the tems”). Grasshoppers and Crickets of Western Europe (Harley Books, London, 1998). REFERENCES 11. Ramme, W., “Zur Systematik, Faunistik und Biologie 1. Benediktov, A.A., “The Possibility of Computer Analy- der Orthopteren von Südost-Europa und Vorderasien,” sis of the Twilight Soundscape of the Orthopteran (Tet- Mitt. Mus. Naturk. Berlin 27, 1–431 (1951). tigoniidae, Gryllidae) Community, by the Example of an 12. Samways, M.J., “Song Modification in the Orthoptera I. Proclamation Songs of Platycleis spp. (Tettigoniidae),” Agrocenosis in Eastern Bulgaria,” Zool. Zh. 94 (11), Physiol. Entomol. 1, 131–149 (1976). 1268–1275 (2015) [Entomol. Rev. 95 (9), 1174–1181 13. Sergeev, M.G., Distribution Trends in the Orthoptera (2015)]. of Northern Asia (Nauka, Novosibirsk, 1986) [in Rus- 2. Bey-Bienko, G.Ya., “Order Orthoptera,” in Keys to sian]. Insects of the European Part of the USSR in Five Vol- 14. Storozhenko, S.Yu., Long-Horned Orthopterans umes, Vol. 1: Apterygota, Archaeoptera, Hemime- (Orthoptera: ) of the Asian Part of Russia (Dal- tabola, Ed. by G.Ya. Bey-Bienko (Nauka, Moscow, nauka, Novosibirsk, 2004) [in Russian]. 1964), pp. 205–284 [in Russian]. 15. Tarbinsky, S.P., “Order Saltatoria (Orthoptera),” in 3. Eades, D.C., Otte, D., Cigliano, M.M., and Braun, H., Keys to Insects of the European Part of the USSR, Ed. Orthoptera Species File. Version 5.0/5.0 (2016). by S.P. Tarbinsky and N.N. Plavilstshikov (Selkhozgiz, http://orthoptera.speciesfile.org. Accessed January 1, Moscow, 1948), pp. 76–127 [in Russian]. 2016. 16. Vedenina, V., Sradnick, J., Kloepfel, A., and Elsner, N., 4. Gorochov, A.V., “Evolution and Taxonomic Signifi- “A Narrow Hybrid Zone between the Grasshoppers cance of the Copulatory Apparatus in Ensifera (Orthop- Stenobothrus clavatus and S. rubicundus: Courtship tera). Part 1: General Concepts and Origin,” Zoosyst. Song Analysis,” Biol. J. Linn. Soc. 107, 383–397 Ross. 23 (2), 197–209 (2014). (2012). 17. Von Helversen, D. and von Helversen, O., “Verhaltens- 5. Harz, K., Die Orthopteren Europas. Vol. I (Series genetische Untersuchungen am akustischen Kommuni- Entomologica, Vol. 5) (Dr. W. Junk, The Hague, 1969). kationssystem der Feldheuschrecken (Orthoptera, Ac- 6. Heller, K.-G., Bioakustik der europäischen Laub- rididae). I. Der Gesang von Artbastarden zwischen heuschrecken (Verlag Josef Margraf, Weikersheim, Chorthippus biguttulus und Ch. mollis,” J. Comp. 1988). Physiol. 104, 273–323 (1975). 7. Kaltenbach, A., “Decticinae aus Israel (Saginae und 18. Zeuner, F.E., “The Classification of the Decticinae Decticinae aus Israel II),” Ann. Naturhist. Mus. Wien Hitherto Included in Platycleis Fieb. or Metrioptera 78, 291–302 (1974). Wesm. (Orthoptera, Saltatoria),” Trans. R. Entomol. 8. Latimer, W., “Variation in the Song of the Bush Cricket Soc. London 91, 1–50 (1941). Platycleis albopunctata (Orthoptera, Tettigoniidae),” 19. Zhantiev, R.D., Insect Bioacoustics (Moscow State J. Nat. Hist. 15 (2), 245–263 (1981). Univ., Moscow, 1981) [in Russian].

ENTOMOLOGICAL REVIEW Vol. 96 No. 3 2016