A re-examination of the of the Chorthippus albomarginatus group in Europe on the basis of song and morphology (: )

Varvara Yu. Vedenina & Otto von Helversen

A study of European sibling species of the Chorthippus albomarginatus group shows that the males could be well distinguished on the basis of the number and density of the stridulatory pegs. We recorded and analysed the calling and courtship songs of the males, as well as the stridulatory movements of the hind legs. Analysis of the stridulatory leg movements allowed us to reveal more differences between both the courtship songs and the calling songs of the European species of this group. On the basis of the morphology, calling and courtship song analysis, we describe a new species, Ch. ferdinandi sp. n., from Greece (Peloponnesus) and a new subspecies, Ch. oschei pusztaensis ssp. n., from the Balkans, Hungary, Moldova and Ukraine. Ch. bruttius Fontana & La Greca, 1999 is classified as a subspecies of Ch. karelini. We describe the phylogenetic relations between the European species of the Ch. albomarginatus group based on the courtship song complexity and courtship visual display. Varvara Yu. Vedenina*, Institute for Information Transmission Problems, Russian Academy of Sciences, Bolshoi Karetnyi per. 19, 127994 Moscow, Russia. [email protected] Otto von Helversen**, Institut für Zoologie, Universität Erlangen-Nürnberg, Staudtstrasse 5, D-91058 Erlangen, Germany.

Introduction south-eastern part of European Russia, Kazakhstan Closely related species belonging to the and Middle Asia, eastward reaching Irkutsk region Chorthippus albomarginatus group are difficult to of Russia; Ch. lacustris La Greca & Messina, 1975 distinguish morphologically. Thus, for a long time, endemic to a very small area around the lake of Joan- they were named as subspecies of Ch. albomarginatus nina in northern Greece; Ch. bruttius Fontana & (De Geer, 1773) (Bei-Bienko & Mishchenko 1951, La Greca, 1999 described from southern Italy and Harz 1975). Recording and analysis of the acoustic Ch. labaumei Ramme, 1926 described from north- signals allowed several authors to distinguish more western Anatolia. Four species, Ch. albomarginatus, species of this group (Helversen 1986, Fontana & Ch. oschei, Ch. karelini and Ch. lacustris, have quite La Greca 1999). To date, the following sibling spe- similar calling songs (the songs produced spontane- cies are reported to inhabit Europe: Ch. albomar- ously by an isolated male) that are relatively simple ginatus (De Geer, 1773) inhabiting northern and in their temporal structure (Helversen 1986, Ragge central Europe, eastward reaching western Siberia & Reynolds 1998, Fontana & La Greca 1999, and Yakutia; Ch. oschei Helversen, 1986 inhabiting Vedenina & Bukhvalova 2001, Benediktov 2005). In the Balkans, Moldova and south-western Ukraine; contrast, their courtship songs (the songs produced Ch. karelini (Uvarov, 1910) occurring in Asia Minor, by a male when close to a female) are very different

Tijdschrift voor Entomologie 152: 65–97, Figs 1–81. [ISSN 0040–7496]. http://www.nev.nl/tve © 2009 Nederlandse Entomologische Vereniging. Published 1 August 2009.

* Corresponding author ** We announce with deep regret the death of the junior author on March 2, 2009. 66 Tijdschrift voor Entomologie, volume 152, 2009

and extremely complex in temporal pattern, and in Morphology of the stridulatory files was studied with three species, Ch. oschei, Ch. karelini and Ch. lacus- a CamScan MV2300 scanning electron microscope. tris, the songs are accompanied by species-specific Specimens examined in this study are deposited in movements of the hind legs and antennae (Helversen Zoological Institute, Russian Academy of Sciences, 1986). Two species of this group, Ch. albomargina- St.-Petersburg (ZIN), Zoological Museum of Mos- tus and Ch. oschei, were found to hybridize in a cow State University (ZMMU), Department of contact zone in Ukraine and Moldova (Vedenina & Entomology, Moscow State University (EDMU), in Helversen 2003). The hybrids can be easily produced the personal collections of V. Vedenina in Moscow under no-choice conditions; however, in choice mat- (CV) and of Fer Willemse in Eygelshoven, The Neth- ing experiments, females of the both species demon- erlands, a public collection in due time (CW), in the strated a strong assortative mating. Comparison of Zoological Museum of Akdeniz University, Antalya, the parental and hybrid viability revealed a reduced Turkey (AUZM), in the Museum für Naturkunde hatching and increased larval mortality in F1 and F2 der Humboldt-Universität, Berlin (MNHU), and in hybrids (Vedenina et al. 2007 a). This indicated that the British Museum of Natural History (BMNH). reproductive isolation between Ch. albomarginatus and Ch. oschei was incomplete and mainly ethologi- Song recordings cal isolating mechanisms evolved between the two The calling song was recorded from isolated males; species. It is generally agreed that the Ch. albomar- the courtship song was recorded when a male was ginatus group in Europe is an assemblage of phyloge- sitting close to a female. Most of the song record- netically young species. ings (from 185 males) were made in the laborato- The existent literature does not contain a clear diag- ries of Zoological Institute in Erlangen and Insti- nosis for all European species of the Ch. albomar- tute for Information Transmission Problems in ginatus group. On the other hand, more recent Moscow. During stridulation of the males studied studies show that to distinguish the species of this in laboratory, both the sound and the movements group one can use the morphology of the stridula- of the hind legs were recorded with a custom-built tory pegs situated on the inner side of the male hind opto-electronic device (Helversen & Elsner 1977, femur. Thus the morphology of the stridulatory Hedwig 2000). A piece of reflecting foil was glued to pegs was shown to be different in Ch. bruttius and the distal part of each hind leg femur of a male and Ch. albomarginatus (Fontana & La Greca 1999). two opto-electronic cameras were focused on the illu- Two species, Ch. albomarginatus and Ch. oschei, may minated reflecting dots. Each camera was equipped be well recognized on the basis of the stridulatory with a position-sensitive photodiode that converted file structure and the number of the stridulatory pegs the upward and downward movements of the hind as well (Vedenina et al. 2007 b). Moreover, recently legs into voltage signals. These signals, together with collected material on the calling and courtship songs the microphone (½’’ Brüel and Kjaer) recordings of allows us to re-examine the European species of the the sounds, were A/D-converted with a custom-built group. As a result of this study: (i) the species of the PC card. The sampling rate was 2 kHz for record- Ch. albomarginatus group are reviewed on the basis of ing the stridulatory movements and 100 kHz for morphology and song parameters, (ii) a description sound recordings. The ambient temperature near of a new species and a new subspecies is given, (iii) a singing male was 30–32° C. The smaller number one species is downgraded to the level of subspecies, of the song recordings (from 63 males) was made in (iv) the phylogenetic relations between the European the field with the cassette recorders; the upper fre- species of the group are clarified and a hypothesis on quency limit was 14 kHz. During the field record- their biogeography is presented. ings, the ambient temperature near a singing male varied in a range of 24–42° C; however, the record- ings made at 30–32° C were only chosen to measure Methods the song parameters and to show the oscillograms of Morphological measurements the calling songs. All recordings were analyzed with a Morphological studies of the specimens were done Turbolab 4.0 program (Germany, Bressner Tech- with a MBS-9 light microscope at 8–56 magni- nology). Courtship behaviour of 25 males was also fication using an ocular micrometer. The following recorded with a Sony DCR-TRV 355E digital video morphological features were measured: the number camera; the video signals were transferred to a PC for of stridulatory pegs, the length and width of tegmen, analysis of visual display. the length and width of hind femur, the length of The courtship song analysis allowed us to compare pronotum and prozona. Figures were obtained using the homologous temporal song features. Earlier, a Sony DSC-W17 digital camera. we identified the homologous song elements in