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Russian Entomol. J. 15(3): 275-278

ї RUSSIAN ENTOMOLOGICAL JOURNAL, 2006

Song of Cicadetta flaveola Brullй (Auchenorrhyncha: Cicadoidea: Tibicinidae) from Greece Песня Cicadetta flaveola Brullй (Auchenorrhyncha: Cicadoidea: Tibicinidae) из Греции Matija Gogala1 & Sakis Drosopoulos М. Гогала1 и С. Дрозопулос
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Slovenian Academy of Sciences and Arts, Novi trg 3, 1000 Ljubljana, Slovenia. E-mail: matija.gogala@guest.arnes.si , 3, 1000 , . Agricultural University of Athens, Department of Agricultural Biotechnology, Iera odos 75, Votanikos, 11855 Athens, Greece. E-mail: drosop@ aua. gr , , 75, , 11855 , .

KEY WORDS: Cicadetta flaveola, song, bioacoustics, singing cicadas. : Cicadetta flaveola, , , . ABSTRACT. B rullй described in his b ook [183 2] Cicadetta flaveola fro m Pelopo nnesus (Mistras, Sparta) and later it has been reported from various Med iterranean countries. Nevertheless, the song of this species has not been described until no w. W e fo und this sp ecies on Pelo ponnesus (Greece) in four different lo calities and recorded its so ng. It is characterized by three different patterns or p hrases, a basic one comprising equally long echemes (A) and two other phrases (B and C), comp osed of characteristic sequences of short and long echemes, with d urations of a few seconds, which fo llow each other without interrup tions fo r a few minutes. A b asic aco ustic unit is a gro up o f 4 tymb al clicks with a duratio n of 7-9 ms and all other echemes are composed o f different numb ers of such 4-click units. . [Brullй, 1832] Cicadetta flaveola (, ). . , . () . . (A) (B C), , . 4 7-9 4- .

Introduction
In the recent years it has been shown, that singing cicadas of Europe are not known to such extent as supposed previously. Bioacoustic investigations, combined with morphological and molecular approaches shed new light on the taxonomy of this group of insects. By acoustic methods it is much easier to single out singing animals in vegetation and recognize their identity. This is true also for the fauna of Cicadoidea of Greece. Our aim was to search especially for the small singing cicadas in Greece, which were previously not studied in detail. In this paper we are describing the song characteristics of Cicadetta flaveola (Brullй, 1832) described from Peloponnesus (Mistras near Sparti). The song of this species has not been previously investigated [Sueur, 2001; Puissant & Boulard, personal communication].

Materials and Methods
In the years 2004 and 2005 both authors made field trips to the eastern part of Peloponnesus in the time periods of May 19-26, 2004 and June 9-12, 2005. Material collected during our field trips: (2) Fteri, Peloponnesus, (~1200 m elev.), 9.VI.2005, (2) Kastanitsa, Peloponnesus (~1000 m) 9.VI.2005. For acoustic detection and recording of songs we used following equipment: the ultrasonic detector PETTERSSON D-200 with a detached microphone, mounted in front of a TELINGA reflector and a solid state recorder MARANTZ PMD-670 with compact flash card 1 and 2 GB. In the year 2004 also a SONY DAT recorder


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Matija Gogala & Sakis Drosopoulos

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Figs 1-2. Cicadetta flaveola Brullй: 1 -- prepared specimen from the locality near Fteri, Peloponnesus; 2 -- live animal from the same locality. Рис. 1-2. Cicadetta flaveola Brullй: 1 -- наколотый экземпляр из окрестностей Фтери, Пелопоннес; 2 -- живой экземпляр из той же местности.

TCD-D10 was used. For analyses of sound we used RAVEN 1.2, CANARY 1.4 and AMADAEUS software and for statistical evaluation MICROSOFT EXCELL on an APPLE iMac G4 computer. Cicadas were first localized acoustically and then collected with entomological net. The dry prepared animals are in the collection of the Slovenian Museum of Natural History in Ljubljana (PMSL) and in the collection of S. Drosopoulos. All sound recordings are stored in the Sound Archive of the Slovenian Museum of Natural History in Ljubljana. The samples of the song are available on the web page: http://www2.pms-lj.si/ european-cicadas/.

Results
In various collections we found specimens of C. flaveola from Peloponnesus and some other localities in Greece, often with wrong determination labels. Comparing the morphology of the specimens with the original description it became clear that these specimens belong to the taxon mentioned above and described by Brullй from Mistra(s) near Sparti. During our field trip in 2004 we recorded in the locality Ag. Andreas a characteristic cicada song, recognized by one of us (S.D.) as a specific one for C. flaveola. One year later (2005) we visited Peloponnesus and near the village Fteri (~ 1200 m above sea level) on June the 9th acoustically detected and recorded and later also collected some cicadas of this species (Figs 1, 2). It turned out that the song differs from all previously known song patterns of European singing cicadas. The next locality, where the species has been found, recorded and collected was above the village of Kastanitsa on the slopes of the Parnon Mountain (~ 1000 m a.s.l.). During the following day we recorded the species also near the village of Kastri (800 m). After a comparison of songs it became very likely that also our recordings from the previous year in Ag. Andreas were produced by males of the same species. However, those males were singing in small trees or shrubs and not in grasses.

Description of the song pattern TIME PARAMETERS. The calling song of this species consists of repetition of short echemes (S) of similar duration (phrase A) as a basic pattern and of two different parts (phrases B and C) with more or less regular sequences of longer (L) and shorter echemes (S) (Fig. 3). In the phrase B the echemes follow the pattern: L S S L S S L... (Fig. 3a) and in the phrase C the pattern is simpler L S L S L... (Fig. 3b). Sometimes this pattern is also changing during a phrase (last phrase B- C in Fig. 3b). Singing animals switch without interruption between these rhythmic patterns or phrases. They may interrupt singing in any phase of their song, but usually during the basic repetition of the echemes of equal length i.e. phrase A. The duration of phrases B is typically 2-3 s and between these phrases there are 3 to 5 s long sequences of short echemes (phrase A) (Figs 3a, 5). The phrases C are usually longer, 3-5 s, separated by "A" phrases of approximately 1 s duration (Figs 3b, 7). In the Figs 5 and 7 one can see that the short echemes can last for about 8 + 1 ms, 16-18 ms or 25-29 ms and there is a reason for this. The shortest echemes in all three phrases comprise a basic pattern of 4 tymbal clicks (Fig. 4a). Such shortest echemes occur most often in the phrase B and sometimes in A and C. Looking at this pattern in more detail one can actually recognize 4 double clicks: the inward movement of a tymbal producing a very soft click and the outward movement a loud one (Fig. 4a). From the pictures 4, 5 and 7 it is evident that short echemes in the basic phrase A are often composed from 3 and sometimes 2 of such basic 4-click units. Also the long echemes, typical for phrase B and C usually contain 8 (6-9) 4-click units (Figs 4b, 5, 7). Therefore, the duration of echemes is distributed stepwise as shown clearly in Figs 5 and 7. The intervals between echemes and the repetition rate of echemes differ slightly from case to case, being in phrases A and C between 70 and 110 ms and change also within phrases, as shown in Fig. 6 during phrase B. The repetition rate of echemes in a phrase A is typically 7-11 echemes per second.


Song of Cicadetta flaveola (Auchenorrhyncha: Cicadoidea: Tibicinidae) from Greece

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Echeme duration [ms]

Time [s]

Fig. 3. Oscillograms of the calling a -- phrases B, A, B; b -- phrases Рис. 3. Осциллограммы пр flaveola Brullй: a -- фразы B, смешанные фразы B-C.

song of Cicadetta flaveola Brullй: C, A and mixed phrase B-C. изывного сигнала Cicadetta A, B; b -- фразы C, A и

Fig. 5. Graph showing echeme durations during phrase A and B of the song of Cicadetta flaveola Brullй. Duration of shortest echemes is about 8 to 9 ms, higher values of short echeme durations are two to three times higher than the "4click unit". Long echemes in phrases B are in this recording composed by 7-8 basic units. Рис. 5. График, показывающий продолжительность серий в течение фраз A и B песни Cicadetta flaveola Brullй. Продолжительность самых коротких серий -- приблизительно от 8 до 9 мс, более высокие значения продолжительностей коротких серий в 2-3 раза выше чем "4-щелчковая единица". Длинные серии во фразах B этой записи состоят из 7-8 основных единиц.

Fig. 4. Oscillograms showing pulse structures of Cicadetta flaveola Brullй: a -- sample of the shortest echeme with 4 double pulses, soft "in" and loud "out" clicks representing the basic "4-click unit"; b -- 2 long echemes comprising 6 and 7 "4-click units" and 3 short echemes comprising 2 and 1 unit. Note a different time scale in Fig. 4b! Рис. 4. Осциллограммы показывают пульсирующие структуры Cicadetta flaveola Brullй: a -- пример самой короткой серии с 4 двойными пульсами, тихие щелчки "прогибания тимбала" и громкие "выгибания тимбала" представляют собой основную "4-щелчковую единицу"; b -- 2 длинные серии, состоящие из 6 и 7 "4-щелчковых единиц" и 3 короткие серии, состоящие из 2 и 1 единиц. Обратите внимание, что на Рис. 4b другая временная шкала!

Interval between echemes [ms]

Time [s]

Fig. 6. Graph showing intervals between echemes during the same song sequence of Cicadetta flaveola Brullй as in Fig. 5. During B-phrases every third interval substantially shorter compared with others in both phrases. Ри с. 6. Гр афи к, показыв аюший и нтервалы между сер иями в том же фрагменте сигнала Ci cad ett a fl ave ola Brullй, как на Р ис. 5. В течени е фразы B каждый третий интерв ал существ енно к ор оче по срав нению с други ми в о бо их фр аза х.

FREQUENCY RANGE. The frequency spectrum of the Cicadetta flaveola calling song has a wide range. There is a main peak of frequencies between 13.5 and 16 kHz with a secondary peak or plateau in the range of 6 to 8 kHz. The -20 dB range of the main peak covers the frequencies between 8 and 19 kHz. Such frequency characteristics can be expected from the size of these singing cicadas [Bennet-Clark & Young, 1994]. Due to the high frequency content of this song it makes sense to use the ultrasonic or "bat" detector for listening, detecting and recording these cicadas in the field.

ECOLOGY. As mentioned before we found this species in localities between 100 and 1200 m. They usually sit and sing on grass or other green plants in meadows or forest clearings. They are active at daytime and call at temperatures between 16 and 25њC or higher. The single male is singing periodically at the same spot for one or a few minutes, then, when it stops, another male starts to sing a few meters away, then the next one or again the first one. Therefore and due to the cryptic green to yellow coloration it is not easy to spot the singing males in the field.


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Matija Gogala & Sakis Drosopoulos distribution of this species reported by some authors is much wider. Nast [1972] and Duffels & van der Laan [1985] mention in addition to Greece the following countries: Algeria, Italy (Sicily), Morocco, Portugal, Spain, Georgia, Kazakhstan, Tadzhikistan and Turkmenia. Nevertheless, Sueur et al. [2004] could not find this species during recent field work in Portugal. Even for Greece there are data not only for Peloponnesus but also for East Macedonia and the island of Kalymnos (Dodekanesos) [Drosopoulos, unpublished data]. Now, with the knowledge of its calling song, the distribution of C. flaveola will be much easier to check.
ACKNOWLEDGEM ENTS . We are than kfull to Dr. Andrej Gogala, who did the preparations of collected specimens for the PMSL collection. We are also grateful to Stйphane P uissant (P erpignan), Michel Boulard (P aris) and J. P . Duffels (Amsterdam) for advice in determination and additional literature. This research has been financially supported by the Slovenian Academy of Sciences and Arts, Ljubljana. This paper is dedicated to the renowned Russian hemipterologists Prof. Alexander F. Emelyanov and P rof. Izyaslav M. Kerzhner.

Echeme duration [ms]

Time [s]

Fig. 7. Graph showing echeme durations during phrase A and C of the song of Cicadetta flaveola Brullй. The last phrase in the graph is a mixed one with elements of B and C. One can see the regular sequence of one long and one short echeme during the C phrase. Phrases C are separated by phrases A with short echemes composed by 3 basic "4-click units". Рис. 7. График показывает продолжительность серии в течение фраз A и C песни Cicadetta flaveola Brullй. Последняя фраза на графике представляет собой смесь элементов фраз B и C. Можно видеть регулярную последовательность одной длинной и одной короткой серий в течение фразы C. Фразы C разделены фразами A с короткими сериями, состоящими из 3 основных "4-щелчковых единиц".

Discussion
First we have to mention that according to Boulard and Puissant (pers. comm.) the taxon Cicadetta flaveola should be placed, by some morphological characters especially the wing venation (5 apical cells in the hind wings and a common root of M and CuA vein in front wings), into the genus Cicadivetta [Boulard, 1982]. Since this opinion is not published yet we did not change the name of the genus. A song pattern closest to the one of Cicadetta flaveola described above is probably the song of Euryphara contentei Boulard, 1982 [Quartau & Simхes, 2004]. The ecology and behaviour of the E. contentei is similar to the eco-ethology of the C. flaveola since both are singing on grass or herbaceous plants [compare Sueur et al., 2004]. Another species with similar ecology from Europe is Cicadetta mediterranea Fieber 1876. Also in this species one phrase (phrase II) consists of very short echemes (11-17 ms) with high repetition rate and long echemes [Gogala & Popov, 1997]. This could be an adaptation to the acoustic conditions in such habitats but such a hypothesis should be supported by exact acoustic measurements. Terra typica of C. flaveola is, as mentioned before, Peloponnesus, Greece. Nevertheless, the geographic

References
Bennet-Clark H.C. & Young D. 1994. The scaling of song frequency in cicadas // Journal of Experimental Biology. Vol .191 . P.2 91-2 94. Boulard M. 1982. Taxa nouveaux pour la faune des Cigales de France (Hom.) // Bull. Soc. ent. France. T.87. No.1-2. P.49-5 0 . Brullй M.A. 1832. Expedition scientifique de Moree. Section des Sciences physiques. T.3. Pt.1. Zoologie, Paris. Duffels J.P. & van der Laan P.A. 1985. Catalogue of Cicadoidea (Homoptera, Auchenorrhyncha) 1956-1980. Dr. W. Junk Publishers, Dordrecht, Boston, Lancaster. Gogala M. & Popov A.V. 1997. Bioacoustics of singing cicadas of the Western Palaearctic: Cicadetta mediterranea Fieber 1 87 6 (Cicado id ea: Tib icini dae) // Acta entomol og ica slovenica. Vol.5. No.1. P.11-24. Nast J. 1972. Palaearctic Auchenorrhyncha (Homoptera). An annotated checklist. Warszawa: Polish scientific publishers. Quartau J.A. & Simoes P.C. 2004. First description of the calling song produced by Euryphara contentei Boulard, 1982 (Insecta, Hemiptera, Cicadoidea) in Portugal // Arquivos do Museu Bocage, Nova Serie. Vol.3. No.22. P.563-572. Sueur J. 2001. Audiospectrographical analysis of cicada sound production: a catalogue (Hemiptera: Cicadidae) // Deutsche Entomologische Zeitschrift. T.48. Ht.1. S.33-51. Sueur J., Puissant S., Simoes P.C., Seabra S., Boulard M. & Quartau J.A. 2004. Cicadas from Portugal: revised list of species with eco-ethological data (Hemiptera: Cicadidae) // Insects Systematics and Evolution. Vol.35. No.2. P.177- 1 8 7.