Introduction

Bushcrickets (katydids) of the family Phaneropteridae are well known for their complicated male calling songs (e.g., Walker & Dew 1972, Walker et al. 2003, Hemp et al. 2010). In this family typically not only do the males produce sounds, but the females also respond acoustically to the male song.

By far the largest genus of the family is Poecilimon Fischer, 1853. All of its more than 150 named species and subspecies occur nearly exclusively in a relatively small area, the East Mediterranean. Within the genus, two different types of acoustical communication systems and a large variety of different song patterns are found (Heller 1990). The genus thus offers excellent opportunities to study the evolution of song patterns and possible factors responsible for divergence. While within subgroups this approach has been successfully applied (e.g., Lehmann 1998; Heller et al. 2006, 2008; Chobanov & Heller 2010), for the genus as a whole, the evolution of the song patterns could not be traced and understood properly, partly because of a lack of information about the songs of some groups and partly because of missing knowledge about relationships between different subgroups and species.

After some initial phylogenetic studies (Ramme 1933, Heller 1984), the situation has been greatly improved by a recent molecular study by Ullrich et al. (2010). One important result of this study was that a group of species, the Poecilimon hamatus group, seems to be the sister group to all other Poecilimon (including some related small genera). The members of the group had already previously been identified as closely related, but the relationship to their congeners remained unsolved (see phylogenetic scheme in Warchalowska-Sliwa et al. 2000).

In this paper we review morphology and distribution and present new data on the acoustical behavior of all species of the P. hamatus group. Both males and females are acoustically active and communicate with each other using very short time intervals (< 100 ms) for reaction (responding and recognition time-windows). While the songs are quite short, they are surprisingly complicated. Without registration of the wing movement their structure would be hard to understand. The song patterns of all species (except of two sister forms) are distinct, but share some important characters.

Methods

Depositories of material are abbreviated as follows: CH - Collectio Heller, Magdeburg; ITZ - Instituut voor taxonomische Zoologie, Amsterdam; NHM - The Natural History Museum, London; NMW Naturhistorisches Museum, Vienna; ZMB - Museum für Naturkunde der Humboldt-Universität, Berlin.

All described species are mentioned in the databanks of the Orthoptera Species File (OSF, Eades et al. 2010), mostly with quite incomplete reference lists; they are also in Fauna Europaea ( http://www.faunaeur.org/) and The Orthoptera of Europe ( http://www.ortheur.org/); selected species are also at  http://members.tripod.com/Cesa88/orthtr.htm (hamatus, unispinosus) and DORSA/SYSTAX ( http://www.biologie.uni-ulm.de/systax/daten/index.html).

The stridulatory files of the males were studied after removal of the left tegmen using a scanning electron microscope (SEM HITACHI S-450, Bielefeld).

The songs were recorded with a Uher tape recorder 42001C, with microphone Uher M 645 (frequency response flat up to 20 kHz) or a Sony WM-3D Walkman with microphone Sony ECM-121 or a Sony WM-GX688 Walkman with a stereo microphone (flat up to 18 kHz) (distance to microphone 5 to 10 cm). Additional sound recordings were made with a Racal store 4-D tape recorder, with microphones Brüel & Kjær 4133 and 4135 (frequency response flat up to 40 and 70 kHz respectively; all frequency measurements were made on animals without reflective tape; see below) and a Pettersson D240 bat-detector (P. klausgerhardi). After digitizing the songs on a PC or an Apple computer, oscillograms (after filtering) and sound analyses were made using the programs Turbolab, Amadeus and Canary (Apple).

Wing movements were registered by an opto-electronic device (Helversen & Eisner 1977, modified as in Heller 1988). Due to the heating effect of the registration lamp, only a lower limit for body temperature can be given [see Heller 1988; in the oscillogram figures which follow these measurements are marked by “>”; for correction of temperature effects [see below] degrees have been added to the measurements of air temperature].

Table 1.

Bioacoustical data.

Fig. 1.

A. Poecilimon hamatus, male (Rhodos). B. P. paros, male (Paros, paratype). C. P. unispinosus, male (Chios). D. P. ikariensis, male (Ikaria). E. P. deplanatus, male (Karpathos). F. P. ikariensis, female (Ikaria). For color version, see Plate V.

To get song data comparable between different species, the influence of temperature had to be eliminated. This has been done (1) using a van't Hoff temperature coefficient (Q 10) of 2 (despite some limitations as discussed by Walker 1975). As a second independent estimate (2) we ran an analysis of variance with temperature as linear covariate (ANCOVA; SPSS v 16.0, Chicago, Illinois). The data from both approaches were similar (see Table 1), although some species slightly differed.

The maps were produced using the program Versamap ( http://www.versamap.com/). Localities with sound records are characterized by ‘SR’ in the text.

Song terminology. — Calling song: song produced by an isolated male. Syllable: the sound produced by one complete up (opening) and down (closing) stroke of the wing. For “simple” and “complex” syllables see Results. Echeme: a first-order assemblage of syllables. Impulse: a simple, undivided, transient train of sound waves (here: the highly damped sound impulse arising as the impact of one tooth of the stridulatory file; see Eisner 1974). Recording session: all sound files of one animal obtained at the same date and the same temperature.

Results

Characteristics

Molecular results.—Molecular analyses (Ullrich 2007, Ullrich et al. 2010) clearly show that Hamatopoecilimon has to be placed close to the root of the genus Poecilimon, separated from all congeners. Both the sequences of mitochondrial DNA and that of nuclear DNA indicate the same pattern. In the nuclear data the placement as a sister group to all other Poecilimon species was statistically well supported, but in the faster evolving mt-DNA this old bifurcation could not be traced with the same certainty (Ullrich et al. 2010). There is only one unexplained point in the nuclear dataset at the moment: that is the inclusion of P. ersisi within the group. Regarding its morphology, bioacoustics and mt-DNA (and in a combined DNA-tree, Ullrich 2007) this species belongs to the P. syriacus-group (Heller et al. 2008) and is also geographically quite distant from the species discussed here. Considering the fact that species of several small genera like Parapoecilimon, Phonochorion and even Polysarcus are grouped together with Poecilimon, the basal position of Hamatopoecilimon becomes even more striking.

Morphology

Coloration.— The members of the P. hamatus group are easily recognised by their coloration, a feature already used by Ramme (1933) as the most important character to consider as closely related the three species known at that time. Typically the body color is not green, but yellowish-white to light brown (yellow in P. deplanatus) with many dark brown and black markings (Fig. 1. See also e.g., jacket picture of Heller 1988, Willemse & Willemse 2008: 55; Kleukers in  http://www.ortheur.org/). Male tegmina are largely covered by the pronotum, the free parts black, distolaterally bordered with an ivory-white band. The metazona of the pronotum is always reddish-brown to black and the eyes are typically red. These data refer mainly to males. In many populations, besides varicolored females (like males), more or less green ones are also found (Fig. 1), quite rarely also yellow-green males (e.g., Willemse & Willemse 2008: 56). Nymphs are also quite often green. Black and white tegmina are found in other Poecilimon species (e.g., P. thoracicus), but not in combination with an unusual body coloration. Body colors other than green are, to our knowledge, not mentioned for other Poecilimon species. However, at high densities individuals with many black markings, as described above, can sometimes be found (see e.g., Chobanov & Heller 2010). In Hamatopoecilimon the coloration seems not to be correlated with population density, since in localities where a species was rare, nearly exclusively non-green individuals were also found.

Cerci.— Three of the six species of the group have cerci with a quite unusual bifurcate shape (Fig. 2). From the other three, however, only P. unispinosus might be considered as a prestage to the bifid type: the other two show no similarities.

Stridulatory file.— The species differ only slightly concerning shape (Fig. 3), number of teeth (range 83–128), intervals between teeth (range 16–23 µm in the middle of the file) and file length (range 1.06–1.79 mm; Table 1).

Other characters.— Ramme (1933) mentioned unusually short hind legs as typical for the group, but did not present any quantification. According to our data (Table 2) and in comparison to the measurements given by Harz (1969), neither absolute nor relative dimensions (in relation to pronotum length) are strikingly different from other species of the genus.

Song.— In all species of the group the male calling song consists of small groups of short syllables (echemes), which are repeated at intervals of about one to several seconds. The number of syllables per echeme differs between species. Except for P. bilgeri (see Discussion) such song types have not been found in any other Poecilimon species with responding females (see Heller 1984, Heller 2004, Heller & Sevgili 2005, Heller et al. 2006, Chobanov & Heller 2010). In all species of the group, syllables are known which are produced by a continuous closing movement of the tegmina (“simple syllables”). Except for the closely related P. paros and P. Mausgerhardi, the other species also produce echemes partly or entirely containing more complex acoustical signals, in addition to echemes consisting of only simple syllables. Here the closing movement shows steps (changes in closing speed) that result in isolated impulses (Figs 4, 6, 8). Often these impulses are followed by similar ones, produced by stridulatory movement cycles with small amplitude. These units might therefore also be called microsyllables. Since there is a continuous transition by partial wing openings (see e.g. Fig. 8) and since the exact state can only be determined by simultaneous recording of the tegmen movement, for simplicity we will call all these elements ‘complex syllables’ (normal syllable together with following impulses).

Fig. 2.

Left male cercus. A, B according to Heller & Reinhold 1992, C Fontana 2004, D, F Ramme 1933, E Willemse 1982.

Table 2.

Body dimensions [length in mm; using data from Brunner von Wattenwyl 1878, Fontana 2004, Harz 1969 (all outgroup data), Heller & Reinhold 1992, Willemse 1982, own data] of the species of Hamatopoecilimon and some representatives from other Poecilimon groups.

Fig. 3.

Male stridulatory file, tegmen articulation at the bottom. A. P. hamatus. B. P. paros. C. P. klausgerhardi. D. P. deplanatus. E. P. ikariensis. F. P. unispinosus.

In frequency composition the songs of all species are quite similar (Table 3) with the maximum of sound energy at about 30 kHz, in the females perhaps slightly higher.

Taxonomic remarks

The other previously described subgenus of Poecilimon, Eupoecilimon Tarbinsky 1932, seems to refer to a group at the top of the tree (see Ullrich et al. 2010). It was redefined and elevated to genus rank by Ramme (1951), but considered as a synonym by Bey-Bienko (1954) and most later authors. Other genera later synonymized with Poecilimon never included a member of Hamatopoecilimon (see also Ünal 2010). According to present knowledge, all other species of Poecilimon thus belong to the nominal subgenus Poecilimon, with the type species P. jonicus (containing as subspecies P. superbus, the taxon Poecilimon is based on; Fischer 1853).

Fig. 4.

Overview of calling songs. Oscillograms of stridulatory movements and song [synchronous registration of left tegmen movement (upward deflection represents opening, downward closing) and sound]. A. P. hamatus. B. P. paros. C. P. klausgerhardi (sound only). D. P. deplanatus. E. P. ikariensis. F. P. unispinosus.

Fig. 5.

Lateral view of the basal fold of the dorsal margin of the lower ovipositor valve. A. P. hamatus. B. P. unispinosus. Scale 1 mm. Arrows indicate the notch in P. hamatus.

Identification of species

Males of the six species can easily be identified by the shape of their cerci (Fig. 2), except for P. hamatus and P. paros. These two species are separated easily only by song. Females are more difficult to discriminate. However, the species are by and large allopatric — only the ranges of the P. hamatus and P. unispinosus overlap. Females of these two species can be differentiated by the deep notch in the basal fold of the ovipositor of P. hamatus (see Fig. 5).

Species account

Fig. 6.

Expanded oscillograms of stridulatory movements and song [synchronous registration of left tegmen movement (upward deflection represents opening, downward closing) and sound]. Two types of echemes in P. hamatus; in P. paros and P. klausgerhardi (sound only) only one type observed.

Fig. 7.

Oscillograms of female response song [in P. hamatus and P. unispinosus synchronous registration of left tegmen movement (upward deflection represents opening, downward closing) and sound; middle and lower track] with the simultaneously recorded male song (upper line). In the female sound track often the male sound can also be seen.

Table 3.

Frequency characteristics of male and female song (single measurements or means).

Fig. 8.

Circadian activity pattern of P. paros' singing.

Fig. 9.

Expanded oscillograms of stridulatory movements and song [synchronous registration of left tegmen movement (upward deflection represents opening, downward closing) and sound]. All three species show two different types of echemes.

Fig. 10.

Female imitation in male song. Comparison of the latency of female response (histograms on the left, measured from beginning of male trigger syllable to beginning of response) and time period to first isolated impulse in complex syllable of male song (histograms on the right, measured from beginning of male syllable to beginning of impulse).

Discussion

Phylogeny and biogeography.—At first glance the occurrence of a basal group of the widespread genus Poecilimon on some small islands in the Aegean Sea does not seem very plausible. However, another large bush-cricket genus with a supposed similar history, the genus Eupholidoptera, shows some striking resemblances.

Both genera have their origins probably on the Aegeid plate, as can be concluded from the present distribution of their species (see Figs 8, 9 in Ciplak 2004). Eupholidoptera seems to have evolved in the southern part of this plate in or near an area which now forms the island of Crete (Ciplak et al. 2010). The most basal species and species groups of Eupholidoptera are found in Crete. Poecilimon may have evolved in an area a little bit more northern than that of Eupholidoptera and did not reach Crete before it became an island for the first time, 10 million years before the present (Ciplak et al. 2010).

During the appearance of the Aegean Sea by the formation of the Mid-Aegean Trench (which started 12 Mya and was completed 9 Mya, see Allegrucci et al. 2009) some islands (and/or the Eastern border of the trench) in this postulated area of origin may have remained. Here an ancestral line of Poecilimon survived and could colonize the areas becoming available during the Messinian salinity crisis when the sea level dropped (about 5 Mya). Today only the Kiklades, Karpathos and the East Aegean islands are still available and inhabited by Hamatopoecilimon. Surprisingly, the ancestor of the group did not reach Crete nor the Greek mainland at the time of low sea level as it has been postulated for cave crickets of the genus Dolichopoda (Allegrucci et al. 2009), which may have had a similar distribution. In this respect the Aegean/Anatolian Eupholidoptera prasina group (and partly E. smyrnensis) and some other groups of animals and plants show the same pattern as Hamatopoecilimon (see Ciplak et al. 2010). The single Poecilimon species in Crete (P. cretensis) may have reached the island from the East, from Southern Anatolia (see data in Heller 2004, Ulrich et al. 2010) possibly during the same period (Messinian salinity crisis).

Fig. 11.

Distribution map.

At present the distribution of the ancestral population of Hamatopoecilimon cannot be located more exactly. The relationship between all of its members is not fully resolved. There is a well-supported southern group containing P. hamatus, P. paros and P. klausgerhardi, which share the strongly bifid cerci. P. hamatus and P. paros are also sister species in the mt-DNA tree (Ullrich et al. 2010; P. klausgerhardi not studied), while P. paros and P. klausgerhardi are the only species which do not differ in song. The islands, where the latter two occur, became disconnected only 20,000 years ago (Perissoratis & Conispoliatis 2003). Future molecular studies may give hints, if both species separated just at that time. P. deplanatus may also belong to the southern group (Ullrich et al. 2010), while the two northern species P. ikariensis and P. unispinosus — closely related to each other according to both nuclear and mitochondrial DNA data — have split off earlier. P. hamatus and P. unispinosus are the only species which are found on islands as well as on the Anatolian mainland. The distribution of P. hamatus has similarities to that of P. sanctipauli (Heller & Sevgili 2005) and Eupholidoptera smyrnensis (Ciplak et al. 2009). All three occur on the island of Rhodes and the Anatolian mainland and have also been found (by v. Oertzen on 10–11 June 1887) on the volcanic island of Nisyros.

However, despite the similarities it is difficult to draw any firm conclusions. Nisyros has probably never been connected with the mainland, while Rhodes, which is separated from the mainland by relatively deep water, has had terrestrial connections, but not during the last glaciation (see Perissoratis & Conispoliatis 2003). P. sanctipauli has a distribution similar to P. hamatus, but it extends in the North only up to the region of Izmir, while E. smyrnensis is spread up to Makedonia on the European mainland. Like P. hamatus, E. smyrnensis has not been found on the island of Chios, where P. unispinosus occurs together with Eupholidoptera prasina (Ciplak et al. 2009). P. deplanatus lives on Karpathos, together with a third Eupholidoptera species, E. uvarovi, which is not closely related to either of the other two according to morphology (Ciplak et al. 2010).

Song evolution and sexual selection.—Many of the Poecilimon species which use the typical phaneropterid communication system (the male calls, the female responds acoustically) produce a calling song consisting of isolated syllables (e.g., Heller 1984). Often these syllables are modulated in their amplitude by variation of the impulse rate or by different intensity of the impulses (e.g., Chobanov & Heller 2010). There are, however, also Poecilimon species which produce quite short isolated syllables, which are in duration comparable to Hamatopoecilimon. Some of these species also use simple, as well as complex, syllables as described above. Representatives with this song type are mainly found in the P. inflatus group and in species near P. jonicus (Heller 2004). According to Ullrich et al. (2010) they all belong to one group, not closely related to Hamatopoecilimon, but with some species occurring in Southwest Anatolia nearly touching the range of P. hamatus. In addition there is one species, P. bilgeri, which is even more similar in song to Hamatopoecilimon than the above-mentioned forms. From the song it was considered to be related to P. inflatus (Heller 2004). Its DNA sequence data are ambiguous (Ullrich et al. 2010), but in any case neither near P. hamatus nor P. jonicus. This species is also found in Southwest Anatolia.

Under the assumption that the DNA tree is correct, the occurrence of such a song pattern or at least of short syllables in three different groups could be an indication that it might be ancestral for the whole genus.

All species of Hamatopoecilimon produce echemes. They can be very short containing two syllables only, as in P. hamatus or P. ikariensis, or consist of longer syllable groups (up to 14 elements). Both extremes are found in the northern and the southern groups, so that independent reductions or amplifications in syllable number must be assumed. Reasons for such song changes may be found either on an inter- or an intraspecific level. Species recognition by song seems to make no sense in allopatric insular species, but it cannot be completely excluded. In Anatolia the ranges of P. unispinosus and P. hamatus overlap and both species differ strongly in syllable number per echeme. The other species with short echemes, P. ikariensis, is at present restricted to the island of Ikaria, but theoretically may have been in contact with P. unispinosus only 20,000 years ago (see Perissoratis & Conispoliatis 2003). Even P. deplanatus may have had contact with P. hamatus if it occurs on Kos (but see species account).

On the other side, sexual selection seems to have strong influence on song structure in any case. The temporal structure of a complex syllable exactly mimics a male-female duet (see Fig. 10). These presumed duet imitations are known from many phaneropterid species (e.g., Zhantiev & Korsunovskaya 1986, Heller 1990, Stumpner & Meyer 2001, Bailey et al. 2006), but they mostly or preferentially occur during male-female interactions. In Hamatopoecilimon they are produced seemingly indiscriminately by isolated males as well as in duets. There are several possibilities to explain such behaviour (see e.g., Stumpner & Meyer 2001, Bailey et al. 2006), but for confirmation they all require specifically designed experiments. In any case, the males of the two species with two types of polysyllabic echemes produce long series of such imitations, whereas the female typically responds only once and the male stops its syllable series after having heard a response. During a long interaction, a female of P. unispinosus responded to the male song regularly but stopped as soon as the male produced complex syllables, and responded again to simple syllables. The complex signals may be directed to females, e.g., with the meaning to attract a female more quickly by imitating another responding female competing for the nutritious spermatophore (McCarthey et al. 2009). They may be also or additionally directed against other males, e.g., by making the localization of a responding female more difficult for eavesdropping males. At present we cannot decide between these hypotheses concerning the evolutionary context of the complicated sound signals, as their function remains unexplored.

Sexual selection may not only shape the song pattern, but also morphological structures which can give information about the quality of the mating partners. In tettigoniids, the most important morphological character in this respect, the cerci, typically evolve even faster than songs (Heller 2006, Ciplak et al. 2009). However, P. paros and P. hamatus were cited (loc. cit.) as one of the few examples with an opposite tendency. Looking on all species of the subgenus it becomes obvious that here both structures evolved quite fast. P. paros and P. klausgerhardi differ only in morphology, possibly as the result of a very fast change (see above). The remaining three species differ in song as well as in genital morphology. Thus the subgenus represents a group of species quite suitable for a comparison of the speed in ethological and morphological evolution and the build-up of reproductive isolation.