Tijdschrift voor Entomologie 155 (2012) 269–283 brill.com/tve

Taxonomy and song of the cicada Ayesha serva (Walker, 1850) from the coasts of northern Sundaland Hans Duffels & Tomi Trilar

The genus Ayesha belongs to the tribe Dundubiini and is distinguished from other genera of the tribe by the spatulate and strongly overlapping male opercula. The synonymy of three species, Cosmopsaltria vomerigera Breddin, 1901, Dundubia lelita Kirkaldy, 1902 and Cicada elopurina Distant, 1888, which are treated as junior synonyms of A. serva (Walker, 1850) in the literature, is confirmed. Two other species, A. spathulata Stål, 1870 and A. operculissima Stål, 1870, are synonymized here with A. serva,sothatAyesha now becomes a monotypic genus. Ayesha serva is redescribed and recorded from Greater Natuna Island, the northern parts of Borneo and Sulawesi and the southern Philippines; the species is mainly found in trees on the beach, in mangroves and other coastal forests. The broad band long lasting monotonous calling song has a very simple and constant pattern. It consists of a fast repetition of many echemes of duration from 41.7 to 79.0 ms, which are composed of 8 to 19 pulses with a repetition rate of 240 pulses per second. Hans Duffels*, Naturalis Biodiversity Center, Department of Terrestrial Zoology, P.O. Box 9517, NL-2300 RA Leiden, The Netherlands. [email protected] Tomi Trilar, Slovenian Museum of Natural History, Prešernova 20, P.O. Box 290, SI-1001 Ljubljana, Slovenia. [email protected]

Introduction Ayesha serva and provides a description of the species Ayesha serva (Walker, 1850) is known from Greater and an analysis of its calling song. Natuna Island between the Malayan Peninsula and Borneo, from the coasts of North Borneo (Malaysia: Sabah and Sarawak; Brunei) and North Sulawesi, History of the genus and the southern Philippines. It can be found in The genus Ayesha was described by Distant (1905) shrubs and trees on the beach, in mangroves and for Cosmopsaltria spathulata from the Philippines. other coastal forests. The cicadas are difficult to spot In 1906, Distant synonymized three species with and to catch but the monotonous sound of the males Ayesha spathulata: Cosmopsaltria vomerigera from Su- and the high number of their nymphal skins on the lawesi, and Dundubia lelita and Cicada elopurina, tree trunks may betray their presence. Since its de- both from Borneo. In the same publication Distant scription as Dundubia serva by Walker (1850), the (1906) transferred two species to Ayesha: Dundubia species has been described five times under differ- serva described from Korea and Cosmopsaltria op- ent names, viz., Cosmopsaltria spathulata Stål, 1870, erculissima from Borneo. Moulton (1923) followed Cosmopsaltria operculissima Stål, 1870, Cicada elop- Distant and distinguished two species of Ayesha in his urina Distant, 1888, Cosmopsaltria vomerigera Bred- ‘Cicadas of Malaysia’: A. spathulata from the Philip- din, 1901 and Dundubia lelita Kirkaldy, 1902. The pines, Borneo, Greater Natuna Island and Sulawesi present paper synonymizes all these names with and A. operculissima from Borneo. Ayesha serva from

Tijdschrift voor Entomologie 155: 269–283, Figs 1–20. [ISSN 0040-7496]. brill.com/tve © Nederlandse Entomologische Vereniging. Published by Koninklijke Brill NV, Leiden. Published 10 December 2012. DOI 10.1163/22119434-00002016

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Korea was mentioned by Moulton (1923) as another Malaysia, Kota Kinabalu, Tanjung Aru, 05°54 N species of the genus, but it was not discussed. 116°04 E, 6.iii.2003, 5 m, T. Trilar & K. Pros- enc Trilar and deposited in the collection of the Slovenian Museum of Natural History (PMSL) Material and methods in Ljubljana, Slovenia. All sound recordings are The institutions listed below are the depositories of stored in the Slovenian Wildlife Sound Archive the material studied. The abbreviations have been housed in the Slovenian Museum of Natural His- used in the lists of material and throughout the text. tory (PMSL). Samples of the song are available on the web page Asian cicadas (http://www2.pms-lj.si/ BMNH Natural History Museum, London staff/bioacoustics/asian.html). MCZ Museum of Comparative Zoology, Cam- Data on the distribution of the species were de- bridge, MA rived from the authors’ ‘Biodiversity Database of MZS Museé Zoologique de la Ville de Stras- the Cicadas of South East Asia and the West Pa- bourg, Strasbourg cific’, and plotted on maps of ADC-Worldmap ver- NHRS Naturhistoriska Riksmuseet, Stockholm sion 2.0 vol. 4 Southern Asia & Australia with the NHMW Naturhistorisches Museum, Wien program MapInfo version 11 for Windows XP. The PMSL Prirodoslovni muzej Slovenije (Slovenian localities and other data from the specimen labels Museum of Natural History), Ljubljana in the database are filed in the program FileMaker RMNH Naturalis Biodiversity Center (former Ri- Pro 6.0. Geographical information has been re- jksmuseum van Natuurlijke Historie), Lei- trieved from the following sources: ‘Malaysia, Travel den and Holiday Planner’ (Anonymous 1996), ‘The SAM South Australian Museum, Adelaide, SA Times Comprehensive Atlas of the World’ (Anony- UZMK Universitets Zoologisk Museum, Copen- mous 1999) and from Global Gazetteer Version 2.2 hagen (www.fallingrain.com). ZMAN Zoological Museum, Amsterdam The terminology adopted in this paper for ex- Songs of A. serva were recorded in the field using ternal features of the body and the male genitalia a parabolic mono microphone Telinga Pro 3M (in follows that of Duffels (1977, 1983) and Moulds the year 1996) and a parabolic stereo microphone (2005). Telinga Pro V (in 1999 and 2003) (parabola diameter 57 cm) connected to Sony DAT-recorder TCD-D3 (sampling rate 48 kHz, 16 Bit dynamic range). In Taxonomy the lab, DAT recordings were transferred to the Hard Genus Ayesha Distant Disk of a Power Macintosh G4 computer through Ayesha Distant, 1905: 63. Type species by original an Audiomedia III sound card using Pro-Tools 5.0 designation: Ayesha spathulata (Stål, 1870). (Digidesign, Avid Technology) software. Afterwards Ayesha; Moulton 1923: 96; Metcalf 1963: 560, 561; the song files were transferred to a PC computer Nast 1972: 142; Duffels & Van der Laan 1985: and the software used for analysing the song signals 131; Moulds 2005: 391, 432; Lee 2009: 2630; was Raven 1.2.1 (Cornell Lab of Ornithology) and Lee & Hill 2010: 299, 300, 302. Seewave package (Sueur et al. 2008) as a part of R software platform (R Development Core Team Description of genus 2008). For statistical evaluation we used Excel 2000 Medium sized cicadas, body length male: 25– (Microsoft). 28 mm, female 24–29 mm. Head slightly broader The recordings were made on the island of Bor- than pronotum and distinctly broader than mesono- neo: at Tanjung Aru beach near Kota Kinabalu, tum. Postclypeus moderately produced. Vertex with rd Sabah, on July, 3 1996 around 13:00 h and March, median black spot. Rostrum reaching just beyond 6th 2003 around 16:00 h, at Telok Assam in Bako trochanter of middle legs. Pronotum with a pair of National Park, Sarawak, on June, 6th 1996 around fairly narrow, black to black-brown, central fasciae. 15:30 h and on Pulao Sapi in Tunku Abdul Rahman Mesonotum with narrow median fascia, which is National Park, just offshore Kota Kinabalu, Sabah, widened at half its length, a pair of paramedian fas- on April, 8th 1999 around 15:30 h (Fig. 16). The du- ciae, which are very variable in width, a pair of black, ration of the recordings was between 40 s and 2 min round spots in front of anterior angles of cruciform 31 s, while altogether was measured 17 min 4 s of A. elevation and a pair of, often indistinct, lateral fas- serva calling songs. ciae. Male operculum spatulate, strongly narrowed Two males o f A. serva from Tanjung Aru, which at one third of its length and strongly widened at were first recorded and then collected, are labelled: two thirds of length; apical part broadly rounded

Downloaded from Brill.com10/08/2021 08:43:37AM via free access Duffels & Trilar: Taxonomy and song of the cicada Ayesha serva 271 and oblique with broad, dark brown coloration along Lectotype designation for Ayesha spathulata apical and medial margins; lateral part of opercu- (Stål) lum with white wax. Apical parts of both opercula Dr Gunvi Lindberg (NHRS) kindly sent us pho- strongly overlapping. Tergites of male and female tographs of the type specimens of Ayesha spathulata, shiny brown without distinct marking. Timbal cov- viz., one male labelled ‘Typus’ (Figs 1–3), one fe- erings dark brown and not shiny. Ventral side of male male labelled ‘Allotypus’ (Figs 4–6) and one female and female abdomen ochraceous to light brown. labelled ‘Paratypus’. She also wrote at an earlier oc- Duffels & Van der Laan (1985), Moulds (2005) casion (Duffels 2010): ...’all curators seem to agree and Lee & Hill (2010) placed Ayesha in the tribe that the [type] labels are from the 20th century’. In Dundubiini Atkinson, 1886. order to establish the identity of A. spathulata,we designate the male specimen labelled ‘Typus’ as the Ayesha serva (Walker, 1850) lectotype of A. spathulata. Figs 1–16 Dundubia serva Walker, 1850: 60, Holotype : Synonymy ‘Dundubia/serva, W. type’, ‘Type’ [round label For the present paper we have studied the holotype with green circle; print] [locality label ‘Corea’ of Ayesha serva from Korea and the holotypes of A. missing; head missing] (BMNH) [examined]. operculissima and A. elopurina, both described from Cosmopsaltria spathulata Stål, 1870: 709, Lectotype Borneo, and photographs of the lectotype and par-  (designated here): ‘Ins./Philipp.’, ‘Semper’, alectotypes of A. spathulata.Wehavenotexamined ‘Cosmopsaltria/spathulata/Stål.’, ‘Typus’ [print in types of Cosmopsaltria vomerigera from Sulawesi, and black in black cadre on red paper], ‘NHRS- Dundubia lelita from North Borneo. Examination HEMI/000000006’ (NHRS). [examined pho- of the holotype of C. elopurina confirms the syn- tographs of lectotype and paralectotypes]. onymy of this species to A. spathulata as already es- Cosmopsaltria operculissima Distant, 1881: 641, Ho- lotype : ‘N. Borneo/Pryer’, ‘operculis-/sima tablished by Distant (1906). Study of Ayesha mate- Dist.’, ‘Type’ [round label with red circle; print], rial from Borneo and Sulawesi (see list of material ‘Distant Coll./1911-383’ [print] [the type is miss- examined) sustains the synonymy of Dundubia lelita ing the locality label Sandakan] (BMNH) [exam- from Borneo, and Cosmopsaltria vomerigera from Su- ined]; Distant 1891: 61, pl. v Figs 5, 5a-b. lawesi to A. spathulata, as was also proposed by Dis- Cicada elopurina Distant, 1888: 297, Holotype tant (1906). : ‘Elopura/[two other lines of label illegi- Moulton (1923) distinguished two species of ble]’, ‘elopurina/Dist.’, ‘Distant Coll./1911-383’, Ayesha: A. spathulata from the Philippines, Borneo, ‘Type’ [round label with red circle; print] Greater Natuna Island and Sulawesi with short male (BMNH) [examined]. opercula reaching the 6th abdominal segment and Cosmopsaltria spathulata; Distant 1890: 61, pl.vi A. operculissima from Borneo with long male oper- Figs 3a, b; cula reaching the tip of the abdomen. However, our Cicada elopurina; Distant 1892: 98, pl.xii Figs 5, 5a. study demonstrates that the relative length of the Cosmopsaltria vomerigera Breddin, 1901: 105, Holo- male operculum in Ayesha cannot be used to sep-  type : Nord Celebes, Buol, vii.1894, Sarasin arate species. Due to telescoping of the abdominal [not examined].  segments, specimens may differ in the relative length Dundubia lelita Kirkaldy, 1902: 54, Holotype : of abdomen and operculum, though it is not the op- British Borneo [not examined]. erculum, but the male abdomen in the first place, Ayesha spathulata; Distant 1905: 63; Distant 1906: that shows variability in length. Examination of spec- 57 (= Cicada elopurina Distant, Dundubia lelita imens with a normal and a more or less telescoped Kirkaldy, Cosmopsaltria vomerigera Breddin); Dis- tant 1912: 46, pl. 5 Figs 39, 39a-c; Moulton abdomen among a series of Ayesha from Toli Toli, 1923: 72, 96, 97, 167; Metcalf 1963: 561, 562; Sulawesi proved that these specimens are conspecific. Lee 2009: 2630, Fig. 8, 2631. Ayesha serva from Korea was mentioned by Moul- Ayesha operculissima; Distant 1906: 58; Moulton ton (1923) as another species of the genus, but it 1923: 96, 97, 167; Metcalf 1963: 560. was not discussed. Dundubia serva was originally de- Ayesha serva; Distant 1906: 57, 58; Distant 1890: 60, scribed from Korea by Walker (1850). In his pub- 61; Distant 1891: pl. xi, Fig. 3b; Moulton 1923: lications on the cicadas of Korea, Lee (1995, 1999, 97; Metcalf 1963: 560, 561; Nast 1972: 142; 2008), concluded that the type specimen was misla- Duffels & Van der Laan 1985: 131; Lee 1995: belled and that Ayesha serva does not occur in Korea. 7, 8, 12; Lee 1999: 13; Lee 2008: 462. Two other species also described by Walker (1850)

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Figs 1–3. Ayesha serva, male lectotype of A. spathulata. – 1, dorsal view; 2, labels; 3, ventral view (Copyright Swedish Museum of Natural History, Stockholm (NHRS)). from Korea, Cryptotympana aquila and Orientopsal- Description (Figs 1–9) tria phaeophila, do not occur in Korea either (Lee Ground colour of head and pronotum ochraceous 1995), both are Sundaland species (Hayashi 1987; to greenish, mesonotum dark brown to castaneous, Duffels & Zaidi 2000). It is most likely that the holo- abdomen of male and female light to dark brown. type of Dundubia serva also originates from Sunda- Underside of head and thorax covered with short and land. fairly long white setae. Study of the external morphology, body marking Head. Vertex with median, round, black spot enclos- and male genitalia of the types of A. serva and ing ocelli, anterior margin of median spot convex A. operculissima, the photographs of the types of and reaching to frontoclypeal suture, posterior part A. spathulata, and additional material from Greater of median spot broadly connected with black col- Natuna Island, Borneo, Sulawesi and the Philippines oration along posterior margin of head; a median (see list of material examined) lead to the conclusion lanceolate, ochraceous spot extends from median that the latter two species are junior synonyms of ocellus to posterior head margin. A pair of triangular A. serva. Since Dundubia serva is the oldest available black-brown marks covers the supra-antennal plates name among the six synonymous names discussed and small parts of the vertex lobes. Proximal apices of above, Ayesha serva should be the valid name. In our these triangular marks may be connected with a pair opinion all specimens of Ayesha studied belong to of squarish black-brown marks, which are attached to this species. lateral parts of posterior margin of head and broadly

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Figs 4–6. Ayesha serva, female allotype of A. spathulata.–4,dorsalview;5,labels;6,ventralview(Copyright Swedish Museum of Natural History, Stockholm (NHRS)). connected with a fairly broad, black fascia extend- imens with pair of faint brownish marks between ing along whole margin of eye. Anterior part of post- anterior and posterior oblique fissures. Pronotal fis- clypeus with upper 5–7 transverse grooves of either sures unmarked or light brownish. Posterior margin side usually more or less black but sometimes brown; of pronotum and margin of lateroproximal bend of a black to brown quadrangular mark often covers the pronotum collar black to black-brown. upper 2–4 transverse grooves of each side; quadran- Mesonotum. Marking only slightly darker than gular marks separated by a median, yellow, oval spot. ground colour. Median fascia reaching from anterior A median brown to black fascia extends, and usually margin of mesonotum to level of anterior angles of widens, from this oval spot to clypeal suture. Ante- cruciform elevation; the fascia is very narrow in ante- clypeus black but median keel and anterior margin rior one third, widens to 4–5 times its anterior width yellow. Gena with triangular, black to brown mark at half or two thirds of its length and slightly narrows narrowing from eye margin to antenna. Basal half or again to the posterior. two-thirds of lorum black. Rostrum with brownish Paramedian fasciae very variable in width, ante- apex and reaching just beyond trochanter of middle riorly equally broad to many times as broad as an- legs. terior end of median fascia, and slightly converging Thorax. Pronotum. Central fasciae fairly narrow, from anterior margin of mesonotum to two fifths black to black-brown, strongly widened and fused of mesonotum length, in some specimens parame- at black to black-brown anterior pronotum mar- dian fasciae widest at half their length but apical part gin; proximal ends kidney-shaped and almost fused always narrowing to the apex that is sometimes re- at anterior margin of pronotal collar. Some spec- curved. A pair of black, round spots in front of ante-

Downloaded from Brill.com10/08/2021 08:43:37AM via free access 274 Tijdschrift voor Entomologie, volume 155, 2012 rior angles of cruciform elevation. Lateral fasciae of- Male ten very vague, brownish, either more or less contin- Operculum (Fig. 7). Spatulate, strongly narrowed at uous from just below anterior mesonotum margin to one third of its length to 0.7 times its basal width anterior angles of cruciform elevation or broken up and strongly widened in the apical part to 2.5 times in several spots or consisting of only one short line its basal width. Lateral and medial margins strongly or completely lacking. A pair of dark brown to black- concave at one third of their length, lateral mar- brown, sometimes fairly long and narrow, triangles at gin strongly convex and medial margin very strongly anterior mesonotal margin between paramedian and convex at two thirds of their length. Apical margin lateral fasciae. broadly rounded and oblique and reaching to one Legs. Ochraceous to brownish. Under-ridge of fore third of abdominal segment 6 or to half-length of femur with a fairly long and narrow, semi-erect, segment 7. Apical parts of opercula strongly over- brown spine at one third of its length, a shorter, lapping. Surface brown with broad, dark brown col- triangular spine at three-fourths of length and a very oration along apical and medial margins; lateral part small spine next to the latter; spines connected by of operculum covered with white wax from base of black line. Tibiae of all legs more brownish to their operculum to the dark brown coloration. distal ends. Tarsi of fore and middle legs brown to Abdomen. Tergites shiny brown, timbal coverings black, those of hind legs ochraceous. dark brown and not shiny. Tergite 3 with a pair of Tegmina and wings. Hyaline without spots, venation dark brown, more or less round, lateral spots. Ter- ochraceous to brownish. gites 5–7 with a pair of smaller, often less distinct,

Figs 7, 8. Ayesha serva, male, Tanjung Aru. – 7, abdomen with opercula in ventral view; 8, male pygofer with pair of claspers in ventral view (drawing Dick Langerak).

Downloaded from Brill.com10/08/2021 08:43:37AM via free access Duffels & Trilar: Taxonomy and song of the cicada Ayesha serva 275 lateral spots. Ventral side of abdomen ochraceous to as a reversed triangle (Fig. 9). Apex of tibia of hind light brown. leg with four strong spines. Male segment 10 with Genitalia (Fig. 8). Pygofer ochraceous to light brown- a pair of proximal protrusions. Length exuviae (4 ish; lateral pygofer lobes rounded. Uncus lobes with a 3): male: 23.6–26.5 mm, female: 25.5–26.5 mm. pair of juxtaposed or somewhat apart, lobes, apically taper to a laterodistal sharp apex; lateral margins of Description of the song uncus lobes weakly concave, medial margin convex. Altogether