Biodiversity Data Journal Biodiversity Data Journal Biodiversity Data Journal BDJ 1314-2836 1314-2828 Pensoft Publishers Biodiversity Data Journal 10.3897/BDJ.1.e978 2305 Cicadidae Faunistics & Distribution Spain First record of Tettigettalna mariae Quartau & Boulard, 1995 (Insecta: Hemiptera: Cicadoidea) in Spain Simões Paula C. Dr pcsimoes@fc.ul.pt 1 Nunes Vera L. Dr vlnunes@fc.ul.pt 1 Mendes Raquel Mr raquelgmendes@gmail.com 1 Quartau José A. Prof jaquartau@fc.ul.pt 1 Faculdade de Ciências da Universidade de Lisboa, Departamento de Biologia Animal e Centro de Biologia Ambiental, Computational Biology and Population Genomics Group, Edifício C2, Piso 3, Campo Grande, 1749-016 Lisboa, Portugal, Lisbon, Portugal

Corresponding author: Paula C. Simões (pcsimoes@fc.ul.pt).

Academic editor: Laurence Livermore

2013 16 9 2013 1 e978 1 8 2013 3 9 2013 Paula C. Simões, Vera L. Nunes, Raquel Mendes, José A. Quartau This is an open access article distributed under the terms of the Creative Commons Attribution License 3.0 (CC-BY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Tettigettalna mariae Quartau & Boulard 1995 is recorded for the first time in Spain. Thought to be endemic to Portugal (occurring in the southern province of Algarve), the present paper adds its distribution to southern Spain, being an Iberian endemism. The acoustic signals of the new specimens collected were recorded in different localities of Huelva province, in Andalusia during August 2012. According to their present known distribution, specimens of Tettigettalna mariae tend to be sparsely distributed in small range populations in southern Iberian Peninsula, favouring wooded areas with Pinus pinea.

Cicada first record Tettigettalna mariae Spain Project PTDC/BIA-BIC/115511/2009 of the Portuguese Foundation for Science and Technology (FCT)
Introduction

Cicadas (Hemiptera: Cicadoidea) constitute a successful group of insects where males typically communicate during pair formation and courtship through acoustic distinctive signals (Claridge 1985, Boulard and Mondon 1995, Simões et al. 2000, Quartau et al. 1999). Despite being common and with several thousands of species described worldwide, cicada’s biodiversity is still poorly known. Recent work has drawn some concern to the diversity of species in the Iberian Peninsula (Boulard 1982, Boulard 2000, Puissant and Sueur 2010, Sueur et al. 2004, Quartau and Fonseca 1988), showing that this region is an important hotspot for Mediterranean cicada diversity. Particular attention was given recently to smaller species in southern Iberia with nine species assigned to the genus Tettigettalna, seven of which are believed to be endemic to southern Iberia (Puissant and Sueur 2010). Three species (Tettigettalna mariae, Tettigettalna josei and Tettigettalna estrellae) have been described and recorded so far in Portugal only (Sueur et al. 2004) but their distribution range in other parts of the Iberia Peninsula has never been investigated before.

The current knowledge on the distribution boundaries of Tettigettalna species is far from being properly known and extensive field surveys for these cicadas are still missing. Moreover, some of these species are believed to have very restricted distribution ranges as is the case of Tettigettalna mariae, a new species that was recently described (Quartau and Boulard 1995) and was thought to be endemic to the Algarve, the southern province of Portugal.

Materials and methods

As an outcome of intensive fieldwork in Portugal and Spain for species of the genus Tettigettalna during the summer of 2012, we report here the discovery of a new populations of Tettigettalna mariae in Andalusia (Southern Spain). Identification was based on the collection of specimens and the recording of male acoustic signals typical of the species.

The field survey was conducted daily from 10:00 h to 19:00 h during sunny weather with temperatures ranging from 29° to 32° C. Searches were conducted by car while driving at a reduced speed, allowing the detection of the songs of calling males. Their acoustic signals were recorded at the collecting site using a Marantz PMD 661 Portable SD recorder (20 Hz – 24 kHz) connected to a Telinga Pro 7 Dat-mic microphone (Twin Science) following the procedures given in Simões et al. 2000. Specimens were then captured by hand or by means of a sweeping net.

Geographical coordinates were determined with a GPS (Garmin, Oregon series 550t) for each site where male songs were heard and where specimens were collected. Species confirmation was accomplished with time and frequency analysis of sound recordings using the software Avisoft Sas-Lab Pro (Specht 2012) as in previous analyses (e.g. Quartau et al. 1999, Simões et al. 2000). Acoustic recordings were analyzed with a sampling rate of 44.1 kHz and a resolution of 16 bits. Spectra were computed using FFT with a resolution of 512 points and a Hamming Window. For each male, recordings of about one minute were analysed. Song terminology follows that of Gogala and Trilar (1999) and Gogala and Trilar (2000). The examined material and acoustic recordings are deposited in the general data bank on insect data at the Department of Animal Biology in the

Faculty of Sciences, University of Lisbon

(FCUL). Collected specimens were stored dry and a front leg was preserved in 100% ethanol for DNA isolation.

Taxon treatments Rank: Species Type of treatment: Redescription or species observation extant Habitat: terrestrial Root classification: 8 Feeds on: feeding on xylem sap from several trees like Pinus pinaster, Pinus pinea and Olea europaea Tettigetalna mariae Quartau & Boulard, 1995 Materials

Occurrence: recordedBy: Raquel Mendes; individualCount: 3; sex: male; Location: country: Espana; stateProvince: Andaluzia; verbatimLocality: Cartaya; verbatimLatitude: 37°15\'44.2"N; verbatimLongitude: 7°07\'48.9"W; Event: samplingProtocol: Acoustic recording; eventDate: 2012-08-15T17:00Z; Record Level: collectionID: 3372;3373;3374; institutionCode: FCUL; collectionCode: Entomology_PCS

Occurrence: recordedBy: Raquel Mendes; Vera Nunes; individualCount: 3; sex: male; Location: country: Espana; stateProvince: Andaluzia; verbatimLocality: Cartaya; verbatimLatitude: 37°15\'44.2"N; verbatimLongitude: 7°07\'48.9"W; Event: samplingProtocol: Acoustic recording; eventDate: 2012-08-15T18:00Z; Record Level: collectionID: 3375;3376;3377; institutionCode: FCUL; collectionCode: Entomology_PCS

Occurrence: recordedBy: Vera Nunes; individualCount: 1; sex: male; Location: country: Espana; stateProvince: Andaluzia; verbatimLocality: Cartaya; verbatimLatitude: 37°15\'44.2"N; verbatimLongitude: 7°07\'48.9"W; Event: samplingProtocol: Sweep net capture; eventDate: 2012-08-15T17:45Z; Record Level: collectionID: 3378; institutionCode: FCUL; collectionCode: Entomology_PCS

Occurrence: recordedBy: Raquel Mendes; Vera Nunes; individualCount: 1; sex: male; Location: country: Espana; stateProvince: Andaluzia; verbatimLocality: Moguer; verbatimLatitude: 37°12\'30.7"N; verbatimLongitude: 6°46\'46.1"W; Event: samplingProtocol: Acoustic recording; eventDate: 2012-08-16T11:50Z; Record Level: collectionID: 3379; institutionCode: FCUL; collectionCode: Entomology_PCS

Occurrence: recordedBy: Raquel Mendes; Vera Nunes; individualCount: 1; sex: male; Location: country: Espana; stateProvince: Andaluzia; verbatimLocality: Moguer; verbatimLatitude: 37°12\'30.7"N; verbatimLongitude: 6°46\'46.1"W; Event: samplingProtocol: Acoustic recording; eventDate: 2012-08-16T14:40Z; Record Level: collectionID: 3380; institutionCode: FCUL; collectionCode: Entomology_PCS

Occurrence: recordedBy: Vera Nunes; individualCount: 1; sex: male; Location: country: Espana; stateProvince: Andaluzia; verbatimLocality: Almonte; verbatimLatitude: 37°13\'43.0"N; verbatimLongitude: 6°33\'51.1"W; Event: samplingProtocol: Acoustic recording; eventDate: 2012-08-16T15:45Z; Record Level: collectionID: 3382; institutionCode: FCUL; collectionCode: Entomology_PCS

Analysis

Our analysis of the morphological and acoustic data confirmed the presence of Tettigettalna mariae specimens in Spain.

Specimens were collected and recorded in different locations from Huelva province in Andalusia around the following localities: Cartaya, Aljaraque, Moguer, Mazagón, Almonte and Hinojos (Table 1). Records were sparse, even within large patches of suitable habitat, and match its current habitat preference, with Tettigettalna mariae tending to favour wooded areas of Pinus pinea near the sea in the southern Iberian Peninsula (Figs 1, 2).

Acoustic analysis (Table 2, Fig. 3) showed the profile of the calling song in agreement with previous studies (Quartau and Boulard 1995, Fonseca 1991, unpublished data). Tettigettalna mariae specimens have a broad spectrum near 6 - 16.5 kHz with maximum energy around 12 kHz. For time domain variables, our results indicated an echeme duration ranging from 0.02 to 0.10s, with an average value of 0.06s. For the echeme period we found a range of 0.16 to 0.54s and average of 0.32s.

Discussion

Previous studies suggested that Tettigettalna mariae was a Portuguese endemic cicada, seeming to be confined to central Algarve, close to the sea (Sueur et al. 2004) which is an area under increasing human pressure. The coastline of Algarve is heavily urbanized, with many touristic villages and golf courses covering most of Vilamoura, Vale do Lobo and Quinta do Lago. This raises concerns about the conservation of Tettigettalna mariae given the restricted habitat range of the known populations. The discovery of Tettigettalna mariae populations in Spain means that the species is not confined to the central wooded area of Algarve, close to the sea, having instead a wider distribution extending to Andalusia. The new populations of Tettigettalna mariae reported here constitute an important addition to the scarce knowledge of this rare species. However, Tettigettalna mariae distribution remains heavily fragmented and discontinuous. Consequently the species is still vulnerable to habitat loss caused by changes in land use or forest fires that often jeopardize Pinus pinea woods during the summer, when cicada adult males are active. These threats may cause the decline and eventual extinction of local populations of cicadas and are especially worrying for small range species such as Tettigettalna mariae (Quartau and Mathias 2010).

With the present data, obtained through our 2012 fieldwork, a new cicada species is listed for Spain and a new endemism for Iberia.

Moreover, the current species list available for the cicadas from Iberian Peninsula are likely to still be incomplete. As the male acoustic signals in cicadas are highly diagnostic for the separation of closely related species (Claridge 1985, Boulard and Mondon 1995, Gogala et al. 2008, Gogala et al. 2011), it is quite possible that to the same specific name may correspond in fact two or more independent sibling species as has happened in other genera, such as Cicadetta (e.g.Gogala et al. 2008, Gogala et al. 2011). All this suggests the presence of a larger number of species in the Iberian Peninsula than those already recorded and calls for further cicada surveys in the area, as well as a better knowledge of cicada biology and ecology, which is the key to the conservation of these interesting insects in the Mediterranean area.

Acknowledgements

This study was financially supported by the project PTDC/BIA-BIC/115511/2009 of the Portuguese Foundation for Science and Technology (FCT).

References Boulard M. 1982 Les cigales du Portugal, contribution à leur étude (Hom. Cicadidae). Annales de la Société entomologique de France 18 2 181 198 Boulard M. 2000 Description de quatre Tettigetta ibériques nouvelles (Auchenorhynca, Cicadidae, Tibicinae). EPHE Biologie et Évolution des Insectes 13 133 143 Boulard M. Mondon B. 1995 Vies et mémoires de cigales - Provence languedoc méditerranée. Équinoxe Barbentane 159 Claridge M. F. 1985 Acoustic signals in the Homoptera: behavior, taxonomy, and evolution. Annual Review of Entomology 30 297 317 10.1146/annurev.en.30.010185.001501 Fonseca P. 1991 Characteristics of the acoustica signals in nine species of cicadas (Homoptera, Cicadidae). Bioacoustics 3 173 192 10.1080/09524622.1991.9753178 Gogala M. Trilar T. 1999 The song structure of Cicadetta montana macedonica Schedl with remarks on songs of related singing cicadas (Hemiptera: Auchenorrhyncha: Cicadomorpha: Tibicinidae). Reichenbachia Staatliches Museum fur Tierkunde Dresden 33 11 91 97 Gogala M. Trilar T. 2000 Sound emissions of Pagiphora annulata (Homoptera: Cicadoidea: Tibicinidae) - A preliminary report. Acta Entomologica Slovenica 8 1 21 26 Gogala M Drosopoulos S. Trilar T. 2008 Cicadetta montana complex (Hemiptera, Cicadidae) in Greece - a new species and new records based on bioacoustics. Deutsche Entomologische Zeitschrift 55 1 91 100 10.1002/mmnd.200800006 Gogala M Trilar T. Drosopoulos S. 2011 Two new species and a new genus of Cicadettini (Hemiptera, Cicadidae) from the Greek island of Evia. Deutsche Entomologische Zeitschrift 58 1 105 117 10.1002/mmnd.201100007 Puissant S. Sueur J. 2010 A hotspot for Mediterranean cicadas (Insecta: Hemiptera: Cicadidae): new genera, species and songs from southern Spain. Systematics and Biodiversity 8 4 555 574 10.1080/14772000.2010.532832 Quartau J. A. Boulard M. 1995 Tettigetta mariae, nouvelle Cigale lusitanienne (HomopteraCicadoideaTibicinidae) EPHE Biologie et Évolution des Insectes 7/8 105 110 Quartau J. A. Fonseca P. 1988 Proceedings of the Sixth Auchenorrhyncha Meeting, Turin Sixth Auchenorrhyncha Meeting Italy 7-11 September 1987 Turin 267-375 Quartau J. A. Mathias M. L. 2010 Insects of the understorey in western mediterranean forest landscapes: a rich biodiversity under threat Harris E. L. Davies N. E. Eds Insect habitats: Characteristics, diversity and management. Nova Science Publishers Inc. New York 133 142 Quartau J. A. Rebelo M. T. Simões P. C. 1999 Cicadídeos (Insectos, Homópteros). Santos-Reis M. Correia A. I. Eds Caracterização da flora e fauna do montado da Herdade da Ribeira Abaixo (Grândola-Baixo-Alentejo). Centro de Biologia Ambiental Lisboa 69 74 Simões P. C Boulard M. M. Rebelo M. T. Drosopoulos S. Claridge M. F. Morgan J. C. Quartau J. A. 2000 Differences in the male calling songs of two sibling species of Cicada (Hemiptera: Cicadoidea) in Greece. European Journal of Entomology 97 437 440 Specht R 2012 Avisoft-SASLab Pro Sueur J Puissant S. Simões P. C. Seabra S. Boulard M. Quartau J. A. 2004 Cicadas from Portugal: revised list of species with eco-ethological data (Hemiptera: Cicadidae). Insect Systematics and Evolution 35 177 187 10.1163/187631204788912373 Supplementary files <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="genus">Tettigettalna</tp:taxon-name-part> <tp:taxon-name-part taxon-name-part-type="species">mariae</tp:taxon-name-part></tp:taxon-name> calling song

Authors: Raquel Mendes; Vera Nunes

Data type: sound file

Calling song of a Tettigettalna mariae specimen recorded in Cartaya (Huelva, Spain).

File: Tmariae.mp3

Habitat of Tettigettalna mariae in Cartaya (Huelva, Spain) corresponding to a typical wooded area of Pinus pinea. Males were usually singing on pine branches or leaves.

Map of occurrence of Tettigettalna mariae in the south of the Iberian Peninsula, showing former documented populations in Algarve (Portugal) according to Sueur et al. (2004) (white circles) and the new populations recorded in August 2012 (grey circles) in the province of Huelva, Andalusia (Spain).

Calling song profile of a Tettigettalna mariae specimen recorded in Cartaya (Huelva, Spain). A - Oscillogram (amplitude vs. time), B - sonagram or spectrogram (frequency vs. time) and C - mean amplitude spectrum (frequency vs. amplitude).

List of localities from the province of Huelva (Andalusia, Spain) where specimens of Tettigettalna mariae were detected. Type of observation: Ao = Audio only (sound heard but not recorded), Ar = Audio recording and C = Captured.

Locality GPS coordinates (degrees minutes seconds) Date Type of observation Specimen ID code DNA sample code
Cartaya 37°15\'44.2"N, 7°07\'48.9"W 15/08/2012 Ar 3372 __
Cartaya 37°15\'44.2"N, 7°07\'48.9"W 15/08/2012 Ar 3373 __
Cartaya 37°15\'44.2"N, 7°07\'48.9"W 15/08/2012 Ar 3374 __
Cartaya 37°15\'44.2"N, 7°07\'48.9"W 15/08/2012 Ar 3375 __
Cartaya 37°15\'44.2"N, 7°07\'48.9"W 15/08/2012 Ar 3376 __
Cartaya 37°15\'44.2"N, 7°07\'48.9"W 15/08/2012 Ar 3377 __
Cartaya 37°15\'44.2"N, 7°07\'48.9"W 15/08/2012 C 3378 Tma3378
Aljaraque 37°15\'50.1"N, 7°00\'29.6"W 17/08/2012 Ao __ __
Moguer 37°13\'55.2"N, 6°47\'48.7"W 16/08/2012 Ao __ __
Moguer 37°12\'30.7"N, 6°46\'46.1"W 16/08/2012 Ar 3379 __
Moguer 37°12\'30.7"N, 6°46\'46.1"W 16/08/2012 Ar 3380 __
Mazagón 37°09\'57.4"N, 6°48\'23.8"W 16/08/2012 Ao __ __
Almonte 37°13\'43.0"N, 6°33\'51.1"W 16/08/2012 Ar 3382 __
Hinojos 37°16\'59.4"N, 6°23\'36.1"W 16/08/2012 Ao __ __

Descriptive statistics of the acoustic variables for Tettigettalna mariae specimens. Time variables in seconds and frequency variables in Hz.

Ech/s Echeme duration Inter-echeme interval Eheme period Echeme rate Peak frequency Minimum frequency Maximum frequency
Average 4.41 0.06 0.26 0.32 0.27 12049 5808 16380
Minimum 1.86 0.02 0.14 0.16 0.14 11569 5195 15860
Maximum 8.98 0.10 0.46 0.54 0.42 12411 7741 17244