Biodiversity Data Journal :
Taxonomic Paper
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Corresponding author: Tomi Trilar (ttrilar@pms-lj.si), Ilia Gjonov (gjonov@cicadina.com), Matija Gogala (matija.gogala@guest.arnes.si)
Academic editor: Ben Price
Received: 18 May 2020 | Accepted: 30 Sep 2020 | Published: 09 Oct 2020
© 2020 Tomi Trilar, Ilia Gjonov, Matija Gogala
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Trilar T, Gjonov I, Gogala M (2020) Checklist and provisional atlas of singing cicadas (Hemiptera: Cicadidae) of Bulgaria, based on bioacoustics. Biodiversity Data Journal 8: e54424. https://doi.org/10.3897/BDJ.8.e54424
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The singing cicadas (Hemiptera: Cicadidae) of Bulgaria were poorly known. There are published records for 14 species: Cicada orni, Lyristes plebejus, Cicadatra atra, Cicadatra hyalina, Cicadatra persica, Cicadetta montana, Cicadetta mediterranea, Dimissalna dimissa, Oligoglena tibialis, Tympanistalna gastrica, Pagiphora annulata, Saticula coriaria, Tibicina haematodes and Tibicina steveni.
Two species from this list were doubtful in the beginning of our study, since Tympanistalna gastrica is distributed in central and southern Portugal and Saticula coriaria is a north African species.
We checked three major institutional collections housed in Sofia, Bulgaria: the National Museum of Natural History (SOFM), the Institute of Zoology (ZISB) and the Biology Faculty of Sofia University "St. Kliment Ohridski" (BFUS). We confirmed 11 of the species mentioned in literature, except Cicadetta mediterranea and found two additional species: Cicadatra platyptera and Cicadetta macedonica (the specimens in BFUS were bioacoustically confirmed).
Based on this knowledge, we further investigated the singing cicadas of Bulgaria with the use of morphological and bioacoustic methods in the years 2008, 2009, 2010, 2012, 2016, 2018 and 2019. We were not able to confirm the presence of Cicadatra persica and Cicadetta mediterranea, but found three additional species: Cicadetta brevipennis s. lat., Cicadetta cantilatrix and Tettigettula pygmea. Using the bioacoustic methods, we also detected unknown singing patterns, which could belong to three or four additional taxa, which need to be described.
The Bulgarian fauna of singing cicadas at the moment consists of 16 confirmed and 3-4 potential species.
Hemiptera, Cicadoidea, singing cicadas, fauna, bioacoustics, distribution, Bulgaria
The singing cicadas (Hemiptera: Cicadidae) of Bulgaria were poorly known and have received little attention until recently. There are published records for 14 species (
The present paper provides an overview of the literature, data from the major collections housed in Bulgaria and new faunistic data collected mainly with bioacoustic methods, which significantly extend the earlier knowledge about the fauna of singing cicadas in this part of Europe.
Between 2008 and 2019, we investigated the singing cicadas (Hemiptera: Cicadidae) of Bulgaria with morphological and bioacoustic methods. In the periods from 22nd to 27th July 2008, from 15th to 24th June 2009, from 23rd to 30th July 2010, from 27th June to 7th July 2012, from 18th to 28th June 2016, from 29th June to 11th July 2018 and from 26th June to 9th July 2019 we carried out the joint fieldwork (in 2010 and 2012, the first author could not participate in the fieldwork).
For the sound recordings, we used microphones which are sensitive in the sonic range (Telinga Pro 6 stereo and Telinga Pro Science - parabola diameter 57 cm, frequency response 40-20,000 Hz) and in the ultrasonic range (ultrasonic detector Pettersson D-200 (frequency range 10-120 kHz) with microphones mounted in front of a Telinga reflector (57 cm diameter), Wildtronics Pro Mini Parabolic Dish (29 cm diameter), smaller metal reflector (15 cm diameter) and self made parabolas (diameters 12 cm, 20 cm and 40 cm) in combination with the Solid State recorders Marantz PMD660, PMD661 and PMD670, Tascam DR-600mkII, Zoom H2 and H4. For sound analysis, we used Raven 1.3 to 1.5 (Cornell Lab of Ornithology), Amadeus Pro 2.4.5. (HairerSoft), Wave Pad (NHC Software) and Seewave package (
We first localised the cicadas acoustically, recorded them and then, if possible, collected them with an entomological net. Morphological studies were carried out on dry prepared specimens. Higher classification and morphological terminology are according to
The specimens collected during the joint fieldwork are preserved in the collections of the Biology Faculty, Sofia University "St. Kliment Ohridski" (BFUS) in Sofia, Bulgaria and the Slovenian Museum of Natural History (PMSL) in Ljubljana, Slovenia. The audio recordings are stored at the Slovenian Wildlife Sound Archive of Slovenian Museum of Natural History (PMSL) in Ljubljana, Slovenia and at the file-hosting service of the Department of Zoology and Anthropology, Biology Faculty, Sofia University "St. Kliment Ohridski" (BFUS) in Sofia, Bulgaria. Selected sound samples are also available on the web pages Songs of the European singing cicadas (
The following information is given for each locality: metadata of the locality (province and municipality), name of the locality, coordinates, altitude (a.s.l.), date, type of data (song recorded, species recorded in the background, song heard, photographed or collected), number of specimens, if collected, repository or source and collectors of the data. Geographic coordinates are given in decimal degrees (datum WGS84). The number of decimal places depends on the accuracy of the data.
To describe the distribution of the singing cicadas in Bulgaria, we used the geographical subdivision of Bulgaria (Fig.
In addition to the fieldwork, records of the cicadas from the public collections of the National Museum of Natural History (SOFM), the Institute of Zoology (ZISB) and the Biology Faculty of Sofia University "St. Kliment Ohridski" (BFUS), all located in Sofia, Bulgaria, were checked for usable data.
We also tried to check all potentially-relevant regional, national and international zoological journals or series for references of cicadas from Bulgaria.
ACRONYMS
Collections (see http://hbs.bishopmuseum.org/codens/codens-inst.html)
BFUS – Biology Faculty, Sofia University "St. Kliment Ohridski", Sofia, Bulgaria
MZPW – Museum and Institute of Zoology, Polish Academy of Science, Warszawa, Poland
PMSL – Slovenian Museum of Natural History, Ljubljana, Slovenia
SOFM – National Museum of Natural History, Sofia, Bulgaria
ZISB – Institute of Zoology, Sofia, Bulgaria
Some material that is in the public collections of the National Museum of Natural History (SOFM), the Institute of Zoology (ZISB) and the Biology Faculty of Sofia University "St. Kliment Ohridski" (BFUS), located in Sofia, have been collected by different collectors. We have examined, reviewed, evaluated and re-determined all the material in the collections. In addition to 11 species already mentioned in literature, with the exception of Cicadetta mediterranea, Tympanistalna gastrica and Saticula coriaria, we found two additional species: Cicadatra platyptera Fieber, 1876 and Cicadetta macedonica Schedl, 1999. In collections, we also found Pagiphora annulata, which was falsely identified as Tympanistalna gastrica.
In the joint fieldwork, we mapped singing cicadas at 250 localities using morphological and bioacoustic methods (Figs
Faunistic data for single species are presented below.
Cicada orni (Fig.
General distribution: Southern Europe: Albania, Bulgaria, Croatia, France (including Corsica), Greece, Italy (including Sardinia and Sicily), Montenegro (Trilar & Gogala, unpublished data), North Macedonia, Portugal, Romania, Serbia, Slovenia, Spain (including Balearic Islands); Central Europe: Austria, Hungary, Germany, Slovakia, Switzerland; Eastern Europe: Russia (South European Russia), Ukraine; Middle East: Cyprus, Iran, Israel, Jordan, Lebanon, Turkey; Transcaucasia: Armenia, Azerbaijan, Georgia, Russia (Chechnya); Northern Africa: Algeria, Egypt, Tunisia; Central Asia: Turkmenistan (all data except for the countries with the citation in brackets are summarised by
Cicada orni is in older literature cited also for the Greek island Crete (
Cicada orni is on the eastern side of Rechinger's line in the Aegean Sea replaced by Cicada mordoganensis Boulard, 1979 (
Distribution in Bulgaria: Cicada orni is a very abundant and widespread species of singing cicadas distributed in Bulgaria. Data are available for 74 localities (Fig.
In Bulgaria, Cicada orni is distributed all over the country: in eastern Danubian Plane, northern lowest hills of the Pre-Balkan, southern Lower Mountain Pre-Balkan, northern Balkan Mts., southern Balkan Mts., Eastern Sub-Balkan valleys, Kraishte-Ichtiman, Kyustendil-Blagoevgrad Middle Struma valley, Sandanski-Petrich Middle Struma valley, Pirin Mt., Prespa-Chernatitsa Western Rhodope Mts., Upper Thracian Plain, Tundzha-Burgas Valley, Eastern Rhodope Mts. and Strandzha Mt. (Fig.
In this survey the majority of the populations were found between sea level and 800 metres (95% of the population) (Fig.
Acoustic behaviour: The song was described by
The males of Cicada orni can sing for hours without interruption from a single spot, sometimes chorusing with other males. The calling song is a pattern of regular repetitions (5-8 times per second) of echemes and interecheme intervals, where the echemes are composed of a variable number of groups of pulses (Fig.
Calling song of Cicada orni. (A) spectrogram (time vs. frequency vs. amplitude, amplitude scale is given on the right) and oscillogram (time vs. amplitude) of the selected part of the calling song; (B) oscillogram of six echemes corresponding to the inverted window in (A); (C) oscillogram of one echeme corresponding to the inverted window in (B).
Selected sound samples of Cicada orni are available on the web pages Songs of the European singing cicadas (
Materials: Suppl. material
Lyristes plebejus (Fig.
General distribution: Southern Europe: Albania, Bulgaria, Croatia (
There is a doubtful citation of Lyristes plebejus for Germany (
Lyristes plebejus is on the eastern side of Rechinger's line in the Aegean Sea replaced by Lyristes gemellus Boulard, 1988 (
Distribution in Bulgaria: In Bulgaria, data are available for 76 localities (Fig.
In Bulgaria, Lyristes plebejus is distributed all over the country with the known data in eastern Danubian Plane, northern lowest hills of the Pre-Balkan, eastern Sub-Balkan valleys, Ograzhden-Vlachina Mts., Sandanski-Petrich Middle Struma valley, Pirin Mt., Dabrash-Batak western Rhodope Mts., Prespa-Chernatitsa western Rhodope Mts., Upper Thracian Plain, Tundzha-Burgas Valley, eastern Rhodope Mts., Haskovo Hills Land and Strandzha Mt. (Fig.
In this survey, the majority of the population was found between sea level and 800 m (93% of the population) (Fig.
Acoustic behaviour: The song was described by
The song of Lyristes plebejus has a very complex structure (Fig.
Selected sound samples of Lyristes plebejus can be found on the web pages Songs of the European singing cicadas (
Materials: Suppl. material
Cicadatra atra (Fig.
General distribution: Southern Europe: Albania, Bulgaria, Croatia, France, Greece, Italy (including Sicily), Montenegro (Trilar & Gogala, unpublished data), North Macedonia, Romania, Serbia, Slovenia, Spain; Eastern Europe: Russia (South European Russia), Ukraine; Middle East: Cyprus, Iran, Israel, Lebanon, Palestine, Syria, Turkey; Transcaucasia: Armenia, Azerbaijan, Georgia, Russia (Chechnya) (all data except for the countries with the citation in brackets are summarised by
There are dubious citations of Cicadatra atra for Czech Republic (
Distribution in Bulgaria: Cicadatra atra is abundant throughout Bulgaria and data are known for 79 localities (Fig.
In Bulgaria, it is distributed all over the country with the known data in western Danubian Plane, eastern Danubian Plane, northern lowest hills of the Pre-Balkan, Kraishte-Ichtiman, Kyustendil-Blagoevgrad Middle Struma valley, Sandanski-Petrich Middle Struma valley, Rila Mt., Pirin Mt., Dabrash-Batak western Rhodope Mts., Prespa-Chernatitsa western Rhodope Mts., Upper Thracian Plain, Tundzha-Burgas Valley, eastern Rhodope Mts., Haskovo Hills Land, Sakar Mt. and Strandzha Mt. (Fig.
In this study, the majority of the population was found between sea level and 600 m a.s.l. (86% of the population) (Fig.
Acoustic behaviour: The song was described by
Four types of songs are registered in Cicadatra atra: continuous calling song, intermittent calling song, courtship song and alarm song (rivalry song or distress call) (
Continuous calling song consists of a sound with a constant amplitude, which is up to several minutes long and resembles a smooth high-frequency buzz (Fig.
Continuous and intermittent calling song of Cicadatra atra. (A) spectrogram and oscillogram of the song showing the transition from continuous song to the calling song with short echemes; (B) oscillogram of the enlarged part of the transition from the continuous song to the calling song with short echemes corresponding to the inverted window in (A).
Intermittent calling song consists of short echemes (duration 95-129 ms) and the interecheme periods of approximately equal length (Fig. 15). During the short echemes, the intensity of the song rises smoothly and ends steeply at the end. Each echeme consists of successive sequences of pulses whose frequency increases by 1/3 towards the end of the echeme. The frequency characteristics are almost the same as in the continuous calling song (Popov 1975).
Courtship song (Fig.
Selected sound samples of Cicadatra atra are available on the web pages Songs of the European singing cicadas (
Materials: Suppl. material
General distribution: Southern Europe: Greece, North Macedonia, Romania; Eastern Europe: Russia (South European Russia), Ukraine; Middle East: Iran, Israel, Jordan, Palestine, Syria, Turkey; Transcaucasia: Armenia, Azerbaijan, Georgia; Central Asia: Turkmenistan (summarised by
Distribution in Bulgaria: In Bulgaria, data are known for four localities from eastern Danubian Plane, Sandanski-Petrich Middle Struma valley and Upper Thracian Plain (Fig.
Acoustic behaviour: Four types of songs are registered in Cicadatra hyalina: continuous calling song, intermittent calling song, courtship song and alarm song (rivalry song or distress call) (
Continuous calling song (Fig.
The intermittent calling song resembles a rumbling noise and consists of echemes of 0.8-1.6 s in length and the interecheme periods of approximately the same length (Fig.
The courtship song is a sequence of pulses that is regularly repeated at a frequency of 54-59 Hz. It has a similar rumbling sound as the intermittent calling song with the same spectral characteristics, but it lacks the segmentation in echemes and is much quieter than the intermittent calling song (
Selected sound samples of Cicadatra hyalina are available on the web pages Songs of the European singing cicadas (
Materials: Suppl. material
General distribution: Southern Europe: Bulgaria (this study), North Macedonia; Eastern Europe: Russia (south European Russia); Middle East: Iran, Israel, Syria, Turkey; Transcaucasia: Armenia, Azerbaijan, Georgia; Central Asia: Pakistan (summarised by
According to
Distribution in Bulgaria: Two male and one female specimen of Cicadatra persica from Sliven are kept in the collections of SOFM and MZPW (Figs
Cicadatra persica is also mentioned for Bulgaria in literature by
Using bioacoustic methods, we searched in Sliven and its surroundings under ideal weather conditions for singing cicadas and in suitable habitat (based on our own field experiences from North Macedonia (
Acoustic behaviour: The song with intensive wing clicking was described by
Like many other Cicadatra species, Cicadatra persica also has two types of songs: continuous calling song and courtship song with wing clicks. It is obvious that many species of this genus combine the normal tymbal sounds with clicks produced by wing beats against the body or substrate during their courtship song (
The phrases of a continuous calling song can last for many minutes without interruption (Fig.
Courtship song (Fig.
In addition to these two types of song, a few irregular tymbal echemes are recorded with the same spectrum as the continuous song, usually before the cicadas flew away. This may be an alarm song (rivalry song or distress call) by animals singing or courting too close together (
Selected sound samples of Cicadatra persica are available on the web pages Songs of the European singing cicadas (
Materials: Suppl. material
General distribution: Southern Europe: Greece, North Macedonia; Middle East: Iran, Israel, Jordan, Lebanon, Palestine, Syria, Turkey (summarised by
The citation of the distribution in Italy (
Distribution in Bulgaria: Cicadatra platyptera was found for the first time in Bulgaria at seven localities in eastern Danubian Plane, Upper Thracian Plain and Tundzha-Burgas Valley (Fig.
Acoustic behaviour: In Cicadatra platyptera three types of songs are registered: calling song, courtship song and alarm song (rivalry song or distress call) (
Calling song (Fig.
Courtship song consists of echemes, produced by the tymbal and clicks, produced by wing flapping (Fig.
Selected sound samples of Cicadatra platyptera are available on the web pages Songs of the European singing cicadas (
Materials: Suppl. material
Singing activity is a very important mechanism used by male cicadas to attract females and is therefore species-specific (e.g. Gogala & Trilar 2004). Recent bioacoustic studies have shown that Cicadetta montana (Scopoli 1772), once thought to be a single widespread Palearctic cicada species, is, in fact, a complex of morphologically-similar sister species that are best characterised by their song patterns. With the help of bioacoustic methods, we find four species from this complex in Bulgaria: Cicadetta montana s. str. (Scopoli, 1772), Cicadetta brevipennis Fieber, 1876, Cicadetta cantilatrix Sueur and Puissant, 2007 and Cicadetta macedonica Schedl, 1999.
General distribution: Northwest Europe: Denmark, Estonia, Finland, Lithuania, Luxembourg, Norway, Sweden; Southern Europe: Bulgaria, Croatia, France, Greece, Italy (including Sicily), Montenegro, North Macedonia, Romania, Slovenia, Serbia, Spain; Central Europe: Austria, Belgium, Czech Republic, Germany, Hungary, Netherlands, Poland, Slovakia, Switzerland; British Isles: United Kingdom; Eastern Europe: Moldavia, Russia, Ukraine; Middle East: Iran, Palestine, Turkey; Transcaucasia: Azerbaijan, Georgia, Russia (Dagestan); Central Asia: Kazakhstan, Kyrgyzstan, Russia (Bashkiria, Chuvashia), Tajikistan; Siberia: Russia (Southern Siberia); Eastern Asia: China (Heilongjiang, Sichuan), Korea, Russia (Primorsky Krai, Sakhalin) (summarised by
Distribution in Bulgaria: In addition to a single literature citation by
Materials: Suppl. material
Cicadetta montana s. str. (Fig.
General distribution (only acoustically-validated data): Southern Europe: Croatia (Trilar & Gogala, unpublished data), France (
Distribution in Bulgaria: These are the first bioacoustically verified data for Cicadetta montana s. str. in Bulgaria. This mountain species was found in Bulgaria at 40 localities in the northern lowest hills of the Pre-Balkan, southern Lower Mountain Pre-Balkan, northern Balkan Mts., southern Balkan Mts., Kraishte-Ichtiman, Vitosha Mt., Sarnena Sredna Gora Mt., Osogovo Mt. and Rila Mt. (Fig.
In this survey, the majority of the population was found between 600 and 1400 m (90% of the population) (Fig.
Acoustic behaviour: The song was described by
The calling song (Fig.
Selected sound samples of Cicadetta montana s. str. are available on the web pages Songs of the European singing cicadas (
Materials: Suppl. material
General distribution (only acoustically-validated data): Southern Europe: Bulgaria, Croatia, Italy, Romania, Serbia, Slovenia; Central Europe: Austria, Hungary (summarised by
Distribution in Bulgaria: During our research, Cicadetta brevipennis s. lat. was found for the first time in Bulgaria and some of the song recordings were used in the research of
In this survey, the majority of the population was found between sea level and 600 m (97% of the population) (Fig.
Acoustic behaviour: The song was described by
The calling song (Fig.
Selected sound samples of Cicadetta brevipennis are available on the web pages Songs of the European singing cicadas (
Materials: Suppl. material
General distribution (only acoustically-validated data): Southern Europe: Bulgaria, France, Italy, Montenegro, North Macedonia, Romania, Serbia, Slovenia; Central Europe: Austria, Czech Republic (
Distribution in Bulgaria: In our survey Cicadetta cantilatrix was found for the first time in Bulgaria. The species was found in four localities in southern Lower Mountain Pre-Balkan, southern Balkan Mts., Kraishte-Ichtiman and Kyustendil-Blagoevgrad Middle Struma valley (Fig.
Acoustic behaviour: The song was described by
The calling song is a sequence of repeated two-phase echemes (Fig.
The courtship song and the alarm song (rivalry song or distress call) were described by
Selected sound samples of Cicadetta cantilatrix are available on the web pages Songs of the European singing cicadas (
Materials: Suppl. material
Cicadetta macedonica (Fig.
General distribution: Southern Europe: Greece, North Macedonia, Romania, Serbia (
Distribution in Bulgaria: Cicadetta macedonica was found for the first time in Bulgaria in 50 localities in northern lowest hills of the Pre-Balkan, southern Lower Mountain Pre-Balkan, northern Balkan Mts., southern Balkan Mts., Kraishte-Ichtiman, Pirin Mt., Dabrash-Batak western Rhodope Mts., Prespa-Chernatitsa western Rhodope Mts., eastern Rhodope Mts. and Strandzha Mt. (Fig.
Acoustic behaviour: The song was described by
The many-minutes lasting calling songs of Cicadetta macedonica consist of a series of short echemes (SE) with a single long echeme (LE) at the end (Fig.
Selected sound samples of Cicadetta macedonica are available on the web pages Songs of the European singing cicadas (
Materials: Suppl. material
Dimissalna dimissa (Fig.
General distribution: Southern Europe: Albania, Bosnia (
The records from Kazakhstan and Central Asia are doubtful as they could refer to unidentified Central-Asiatic closely-related species (Tishechkin, personal communication). There are doubtful records for Sicily (
Distribution in Bulgaria: Dimissalna dimissa is the second most common and widespread species of singing cicada distributed in Bulgaria. Data are known for 122 localities (Fig.
In Bulgaria, Dimissalna dimissa is a generally distributed species with known data in western Danubian Plane, eastern Danubian Plane, northern lowest hills of the Pre-Balkan, southern Lower Mountain Pre-Balkan, northern Balkan Mts., Kraishte-Ichtiman, Osogovo Mt., Belasitsa Mt., Osogovo Mt., Kyustendil-Blagoevgrad Middle Struma valley, Sandanski-Petrich Middle Struma valley, Pirin Mt., Gotse Delchev Mesta valley, Dabrash-Batak western Rhodope Mts., Prespa-Chernatitsa western Rhodope Mts., Upper Thracian Plain, Tundzha-Burgas Valley, Eastern Rhodope Mts., Haskovo Hills Land, Sakar Mt. and Strandzha Mt. (Fig.
In this survey, the majority of the population was found between sea level and 1000 m (98% of the population) (Fig.
Acoustic behaviour: The song was described by
The first type of song (Fig.
The second type (Fig.
Second type of song of Dimissalna dimissa. (A) spectrogram and oscillogram of the second type of song; (B) oscillogram of one sequence of the second type of song corresponding to the inverse window in (A); (C) oscillogram of the first and second segments; (D) oscillogram of the third segment and final long echeme (LE).
Selected sound samples of Dimissalna dimissa are available on the web pages Songs of the European singing cicadas (
Materials: Suppl. material
Oligoglena tibialis (Fig.
General distribution: Southern Europe: Albania, Bosnia, Bulgaria, Croatia, France, Greece, Italy, North Macedonia, Portugal, Romania, Slovenia, Serbia, Spain; Central Europe: Austria, Czech Republic, Hungary, Poland, Slovakia; Eastern Europe: Moldova, Russia (South European Russia), Ukraine; Middle East: Iran, Israel, Jordan, Lebanon, Turkey; Transcaucasia: Azerbaijan, Georgia, Russia (Chechnya); Central Asia: Kyrgyzstan, Uzbekistan; Northern Africa: Morocco, Tunisia (summarised by
There is a doubious citation of Oligoglena tibialis for Germany (
Distribution in Bulgaria: This small cicada is the most abundant and most widespread species of singing cicadas found in Bulgaria. The data for 125 localities are known (Fig.
In Bulgaria, it is distributed all over the country with known data in western Danubian Plane, eastern Danubian Plane, northern lowest hills of the Pre-Balkan, southern Lower Mountain Pre-Balkan, northern Balkan Mts., western Sub-Balkan valleys, Kraishte-Ichtiman, Vitosha Mt., True Sredna Gora Mt., Ograzhden-Vlachina Mts., Kyustendil-Blagoevgrad Middle Struma valley, Sandanski-Petrich Middle Struma valley, Pirin Mt., Dabrash-Batak western Rhodope Mts., Prespa-Chernatitsa western Rhodope Mts., Upper Thracian Plain, Tundzha-Burgas Valley, eastern Rhodope Mts., Haskovo Hills Land, Sakar Mt. and Strandzha Mt. (Fig.
In this study, the majority of the population of Oligoglena tibialis was found between sea level and 800 m (91% of the population) (Fig.
Acoustic behaviour: The song was described by
The calling song contains two types of phrases (Fig.
Calling song of Oligoglena tibialis. (A) spectrogram and oscillogram of the calling song, showing the transition from the first phrase to the second; (B) oscillogram of the enlarged part of the transition from the first phrase to the second one corresponding to the inverted window in (A).
Selected sound samples of Oligoglena tibialis are available on the web pages Songs of the European singing cicadas (
Materials: Suppl. material
Tettigettula pygmea (Fig.
General distribution: Southern Europe: Albania, Austria (
It was not found in Spain (
Distribution in Bulgaria: Tettigettula pygmea was found for the first time in Bulgaria at three localities in Strandzha Mt. (Fig.
Acoustic behaviour: The song was described by
The calling song consists of two phrases with repeating patterns (Figs
Selected sound samples of Tettigettula pygmea are available on the web pages Songs of the European singing cicadas (
Materials: Suppl. material
General distribution: Southern Europe: Albania, Bulgaria, Greece, Moldova, North Macedonia, Romania, Serbia, Spain; Central Europe: Hungary, Slovakia; Middle East: Turkey (summarised by
The populations from north Africa (Algeria, Tunisia) (
One of the biodiversity hotspots for the genus Pagiphora is in Turkey, where at least three species can be found. Pagiphora annulata (Brullé, 1832) is distributed in the northwest at least in Hatay Province (
Distribution in Bulgaria: In Bulgaria, data are available for 45 localities (Fig.
In Bulgaria, Pagiphora annulata is scattered all over the country, with the known data in eastern Danubian Plane, northern lowest hills of the Pre-Balkan, northern Balkan Mts., eastern Sub-Balkan valleys, Kyustendil-Blagoevgrad Middle Struma valley, Rila Mt., Tundzha-Burgas Valley, eastern Rhodope Mts., Haskovo Hills Land and Strandzha Mt. (Fig.
In this survey, the majority of the population was found between sea level and 600 m (93% of the population) (Fig.
Acoustic behaviour: The characteristic of the song emission of Pagiphora annulata (the same applies to all other species of the genus Pagiphora) is a surprisingly low frequency band for such relatively-small animals. According to
The song was described by
The calling song consists of phrases (duration 2.1-2.9 s), consisting of 7 to 10 echemes, whose duration and intensity increases towards the end of a phrase (Fig.
The second part of the last 3 to 5 echemes is accompanied by wing movements and the sound is louder and sharper. The spectrograms show a wider spectrum and oscillograms show the additional short sound pulses (repetition frequency 130-140 Hz) only roughly synchronised with the regular tymbal pulses (Fig.
Selected sound sample of Pagiphora annulata is available on the web pages Songs of the European singing cicadas (
Materials: Suppl. material
Tibicina haematodes (Fig.
General distribution: Southern Europe: Albania, Bulgaria, Croatia, France, Greece, Italy, Moldova, North Macedonia, Portugal, Romania, Serbia, Slovenia, Spain; Central Europe: Austria, Czech Republic, Germany, Hungary, Slovakia, Switzerland; Eastern Europe: Russia (south European Russia), Ukraine; Middle East: Iran, Palestine, Turkey; Transcaucasia: Armenia, Azerbaijan, Georgia (summarised by
There are dubious citations for Corsica (
Distribution in Bulgaria: This colourful cicada was found in many localities in Bulgaria and the data are known for 45 localities (Fig.
In Bulgaria, it is generally distributed with known data in western Danubian Plane, eastern Danubian Plane, northern lowest hills of the Pre-Balkan, southern Lower Mountain Pre-Balkan, northern Balkan Mts., western Sub-Balkan valleys, eastern Sub-Balkan valleys, Kraishte-Ichtiman, Sandanski-Petrich Middle Struma valley and eastern Rhodope Mts. (Fig.
In this survey, the majority of the population was found between sea level and 600 m (91% of the population) (Fig.
Acoustic behaviour: The song recorded during our fieldwork in Bulgaria does not differ from the pattern recorded, analysed and described by
The calling song (Fig.
Calling song of Tibicina haematodes. (A) spectrogram and oscillogram of the calling song; (B) oscillogram of the beginning of the calling song with four introductory echemes corresponding to the inverse window in (A); (C) detailed oscillogram showing subgroups of pulses corresponding to the inverse window in (B); (D) detailed oscillogram showing pulses corresponding to the inverse window in (C).
Selected sound samples of Tibicina haematodes are available on the web pages Songs of the European singing cicadas (
Materials: Suppl. material
General distribution: Southern Europe: Bulgaria, France, Greece (
Distribution in Bulgaria: This species is reported for Bulgaria as literature data, but without the citation of the source, by
In Bulgaria, data are known for 32 localities (Fig.
Acoustic behaviour: The song was described by
The calling song (Fig.
Calling song of Tibicina steveni. (A) spectrogram and oscillogram of the selected part of the calling song; (B) oscillogram of the enlarged part corresponding to the inverted window in (A); (C) detailed oscillogram showing subgroups of pulses corresponding to the inverted window in (B); (D) detailed oscillogram showing pulses corresponding to the inverted window in (C).
Selected sound sample of Tibicina steveni is available on the web pages Songs of the European singing cicadas (
Materials: Suppl. material
Due to extensive field research and the use of bioacoustic methods, the number of known cicada species in Bulgaria has increased in recent years and the knowledge about ecology and distribution has improved.
The three ubiquitous, loudest and largest singing cicadas with spectacular songs, Cicada orni, Lyristes plebejus and Tibicina haematodes, were recorded acoustically and also collected in many localities in Bulgaria. Some other species were not so easy to detect and locate acoustically and especially for the Cicadetta montana group of sister species, ultrasonic detectors were needed to confirm their presence.
During the fieldwork for this survey, we recorded and/or collected 15 species: Cicada orni, Lyristes plebejus, Cicadatra atra, Cicadatra hyalina, Cicadatra platyptera, Cicadetta montana s. str., Cicadetta brevipennis s. lat., Cicadetta cantilatrix, Cicadetta macedonica, Dimissalna dimissa, Oligoglena tibialis, Tettigettula pygmea, Pagiphora annulata, Tibicina haematodes and Tibicina steveni.
There are published records for 10 of them: Cicada orni (
In the public collections of the National Museum of Natural History (SOFM), the Institute of Zoology (ZISB) and the Biology Faculty of Sofia University »St. Kliment Ohridski« (BFUS), which are all located in Sofia, we found, besides the nine species already mentioned in literature, three more species: Cicadatra persica, Cicadatra platyptera and Cicadetta macedonica. For all three species, the occurrence in Bulgaria has not yet been published.
Table
Number of provinces and localities where cicada species were found in Bulgaria
Species |
No of provinces |
No of localities |
Oligoglena tibialis |
23 |
125 |
Dimissalna dimissa |
19 |
122 |
Lyristes plebejus |
17 |
76 |
Tibicina haematodes |
17 |
45 |
Cicadetta macedonica |
16 |
50 |
Cicada orni |
15 |
74 |
Cicadatra atra |
14 |
79 |
Pagiphora annulata |
12 |
45 |
Cicadetta montana s. str. |
9 |
40 |
Cicadetta brevipennis s. lat. |
7 |
33 |
Tibicina steveni |
4 |
32 |
Cicadatra hyalina |
4 |
4 |
Cicadatra platyptera |
3 |
7 |
Cicadetta cantilatrix |
3 |
4 |
Tettigettula pygmea |
1 |
3 |
Cicadatra persica |
1 |
1 |
Cicadas are not evenly distributed in Bulgaria. Figs
Distribution of cicadas by province in Bulgaria. Pink - 1-4 species per province, orange - 5-8, red - 9-11. Source of the map
1 - Blagoevgrad Province, 2 - Burgas Province, 3 - Dobrich Province, 4 - Gabrovo Province, 5 - Haskovo Province, 6 - Kardzhali Province, 7 - Kyustendil Province, 8 - Lovech Province, 9 - Montana Province, 10 - Pazardzhik Province, 11 - Pernik Province, 12 - Pleven Province, 13 - Plovdiv Province, 14 - Razgrad Province, 15 - Ruse Province, 16 - Shumen Province, 17 - Silistra Province, 18 - Sliven Province, 19 - Smolyan Province, 20 - Sofia Province, 21 - Stara Zagora Province, 22 - Targovishte Province, 23 - Varna Province, 24 - Veliko Tarnovo Province, 25 - Vidin Province, 26 - Vratsa Province, 27 - Yambol Province
The Provinces with a moderate number of species, which are marked orange (5-8 species per Province), have a lower altitudinal range and probably a lower habitat diversity. The Dobrich Province is a lowland area rich in steppe habitats and the mountain cicada species are missing. In contrast, Smolyan Province has mostly high mountains and the steppe cicada species are missing. Additionally, some areas in the Danube plain, such as Silistra, Razgrad and Pleven Province are lowland areas with a considerable amount of wetland habitats, which are not suitable for the development of the underground cicada larvae.
We found that the richest cicada biodiversity is found in areas with a greater diversity of relief, ranging from lowlands to low mountain ranges and high mountains. These areas are the Struma Valley with the Kresna Gorge and Pirin Mountain, Eastern Rhodopes, Balkan Mountains and Strandzha Mountain, in Figs
In total, during this investigation, we discovered seven new species in the collections or in the field for the fauna of Bulgarian singing cicadas, namely Cicadatra persica, Cicadatra platyptera, Cicadetta montana s. str., Cicadetta brevipennis s. lat., Cicadetta cantilatrix, Cicadetta macedonica and Tettigettula pygmea. Amongst these species, Cicadetta montana s. str., Cicadetta brevipennis s. lat. and Cicadetta macedonica are relatively common and well distributed. All other species, including Cicadatra hyalina and Cicadatra persica, are rare and have a very limited distribution. In Bulgaria, we have data for Cicadatra hyalina from only four localities, Cicadatra platyptera from seven localities, Cicadatra persica from one locality, Cicadetta cantilatrix from four localities and for Tettigettula pygmea from three localities. This raises the question of the protection of these species and their habitats. There is also an urgent need for further research on the localities described in the above-mentioned literature and collections to confirm the recent occurrence of these rare species, to determine the state of their habitats and to propose conservation measures.
In literature, we also find the records for four additional species: Cicadatra persica (
The specimen of Cicadatra persica from Sozopol on the Black Sea coast cited by
Cicadetta mediterranea was collected (one female) by V. Pelov in August 1957 on dry open slopes north of the village of Podkova (41.398°N, 25.401°E; Kardzhali Province: Kirkovo Municipality) and published with the note that it was determined according to Melichar 1896 (
Tympanistalna gastrica is distributed in central and southern Portugal (
Saticula coriaria is a north African species (
We propose to exclude both species, Tympanistalna gastrica (Stål 1854) and Saticula coriaria Stål 1866, from the list of Bulgarian cicadas.
We also solved the riddle with the literature quote from Tibicina steveni from Petrich, cited by
Using bioacoustic methods, we also discovered unknown song patterns similar to the songs of Cicadetta montana species complex, which could belong to three or four additional taxa. From a population with undescribed song patterns, we were also able to collect a reasonable number of specimens and the description of the species is in preparation. The second singing pattern shows cline changes in the time parameters from west to east with a step change at the middle of the geographical distribution, which could indicate two separate taxa. However, we could collect only four males from both distribution margins and a few females from one location, for which we are not convinced that they belong to the males recorded and collected. In the population of the third song pattern, we could not collect any specimens because the animals live high up in the treetops. Therefore, we need additional specimens and recordings to confirm this hypothesis.
The Bulgarian fauna of the singing cicada currently consists of 16 confirmed and 3-4 potential species. Twenty species from Bulgaria show the richness of the Mediterranean cicada fauna, which can be compared with the neighbouring countries. In Greece, 33 species (Gogala and Trilar, unpublished data) and 15 in North Macedonia (
The Slovenian Academy of Sciences and Arts and the Bulgarian Academy of Sciences have financially supported the fieldwork of the TT and MG in Bulgaria in 2016, 2018 and 2019.
TT research was part of the programme “Communities, relations and communications in the ecosystems” (No. P1-0255) financed by the Ministry of Education, Science and Sports of the Republic of Slovenia.
IG was supported by the National Programme "Young scientists and postdocs" of the Bulgarian Ministry of Education and Science, contract No. РД-22 1025 / 17.04.2019.
We are grateful to Dr. Andrej Gogala (Slovenian Museum of Natural History, Ljubljana), who made the preparations of the material for the PMSL collection. We also appreciated the great help of our wives, M.Sc. Katarina Prosenc Trilar, who joined us during the fieldwork in 2018 and Assoc. Prof. Dr. Albena Lapeva-Gjonova for the great hospitality and logistic support.
We are grateful for the very useful comments and suggestions by the reviewers, Thomas Hertach, Benjamin Price and Kiran Marathe.