Cicadetta sibillae, 2015

Hertach, Thomas, Trilar, Tomi, Wade, Elizabeth J., Simon, Chris & Nagel, Peter, 2015, Songs, genetics, and morphology: revealing the taxonomic units in the European Cicadetta cerdaniensis cicada group, with a description of new taxa (Hemiptera: Cicadidae), Zoological Journal of the Linnean Society (Zool. J. Linn. Soc.) 173 (2), pp. 320-351 : 326-334

CICADETTA SIBILLAE HERTACH & TRILAR SP. NOV.

Cicadetta cerdaniensis s.l. ( Hertach, 2007)

Cicadetta cerdaniensis ( Trilar & Hertach, 2008, Hertach, 2011, Hertach & Pollini Paltrinieri, 2012)

Cicadetta sp. aff. cerdaniensis ( Hertach & Nagel, 2013)

Type material

The type series consists of 25 males and three females representing the Central Apenninian (3), Northern Apenninian (9), Western Alpine (2), and Insubrian

metapopulations (14). It is kept in the NHMB (holotype), MCSN, NMBE, PMSL, and in two private collections.

Holotype male

Verbatim label information: ‘nördl. Campigna , EMIL, I/ 43.8854° / 11.7567°, 950 m asl / 3.7.2012, leg. T. Hertach / Collection Code No. 5.020’ (label rectangular, white, printed) and ‘HOLOTYPUS ♂ / Cicadetta sibillae sp. n. / Hertach & Trilar 2014’ (label rectangular, light red with dark red margin, printed) ( NHMB).

Paratypes

All paratypes with labels ‘ PARATYPUS XX Y, Cicadetta sibillae sp. n. Hertach & Trilar 2014’ (label rectangular, white with red margin, printed) at which ‘XX’ is the number of the paratype and ‘Y’ is the sex of the specimen. Numbers ‘20’ and ‘24’ do not exist.

Paratype males: Monte San Giorgio, TI, CH, 45.9123°/ 8.9478°, 1040 m asl, 6.6.2005, leg. T. Hertach (paratype 1, coll. MCSN) ; Monte San Giorgio, TI, CH, 45.9123°/ 8.9478°, 1040 m asl, 27.6.2007, leg. T. Hertach (paratype 2, coll. Hertach) ; Monte San Giorgio, TI, CH, 45.9100°/ 8.9516°, 1000 m asl, 27.6.2007, leg. T. Hertach (paratype 3, coll. MCSN) ; Monte San Giorgio, TI, CH, 45.9100°/ 8.9516°, 1000 m asl, 27.6.2007, leg. T. Hertach (paratype 4, coll. Hertach) ; Pontinvrea, LIGU, I, 44.4267°/8.4250°, 550 m asl, 1.8.2008, leg. T. Hertach (paratype 5, coll. Hertach) ; Monte Bré, Sassa, TI, CH, 46.0084°/8.9851°, 880 m asl, 6.7.2009, leg.A. Rey (paratype 7, coll. Hertach) ; Lodrino, LOMB, I, 45.7043°/10.2808°, 930 m asl, 18.6.2010, leg. T. Hertach (paratypes 8 and 9, coll. Hertach) ; Monte Caslano, TI, CH, 45.9611°/8.8799°, 460 m asl, 24.6.2010, leg. T. Hertach (paratype 10, coll. MCSN) ; Monte San Giorgio, TI, CH, 45.9100°/8.9503°, 970 m asl, 11.7.2004, leg. T. Hertach (paratype 11, coll. MCSN) ; Rocca di Cambio/Rocca di Mezzo, ABRU, I, 42.2140°/13.4812°, 1390 m asl, 7.7.2011, leg. T. Hertach (paratypes 12 and 13, coll. Hertach) ; Verrecchie, ABRU, I, 42.0384°/13.2459°, 1010 m asl, 8.7.2011, leg. T. Hertach (paratype 14, coll. Hertach) ; E Celle, Susa, PIEM, I, 45.1304°/7.3548°, 870 m asl, 16.6.2012, leg. T. Hertach (paratype 15, coll. Hertach) ; Lottulo, Maira , PIEM, I, 44.4944° / 7.2351°, 780 m asl, 18.6.2012, leg. T. Hertach (paratype 16, coll. NMBE) ; Mte. Tugello/Mte. Tobbio, LIGU, I, 44.5775°/8.7869°, 540 m asl, 21.6.2012, leg. T. Hertach (paratype 17, coll. Hertach) ; NE Vobbia , LIGU, I, 44.6074° / 9.0495°, 520 m asl, 21.6.2012, leg. T. Hertach (paratype 18, coll. NMBE) ; Castello di Comano, TOSC, I, 44.3039°/10.1152°, 770 m asl, 24.6.2012, leg. T. Hertach (paratype 19, coll. Hertach) ; N Pregola, LOMB, I, 44.7548°/ 9.2915°, 1120 m asl, 18.7.2012, leg. T. Hertach (paratype 22, coll. Hertach) ; Monte Caslano, TI, CH, 45.9612°/8.8801°, 470 m asl, 22.6.2013, leg. T. Hertach (paratype 23, coll. Hertach) ; Monte d’Alpe, LOMB, I, 44.8022°/9.3149°, 1050 m asl, 3.7.2013, leg. T. Hertach (paratype 26, coll. Hertach) ; SW Brallo di Pregola, LOMB, I, 44.7341°/9.2759°, 970 m asl, 4.7.2013, leg. T. Hertach (paratype 27, coll. Hertach) ; Monte Bré, Sassa, TI, CH, 46.0085°/8.9853°, 880 m asl, 20.6.2009, leg. A. Rey (paratype 28, coll. Rey) ; Rasa, Monte Chiusarella, LOMB, I, 45.8660°/8.8133°, 700 m asl, 14.6.2007, leg. T. Trilar, T. Hertach (paratype 29, coll. PMSL).

Paratype females: Monte Bré, Sassa, TI, CH, 46.0085°/ 8.9853°, 880 m asl, 20.6.2009, leg. A. Rey (paratype 6, coll. Hertach); N Campigna , EMIL, I, 43.8854° / 11.7567°, 950 m asl, 3.7.2012, leg. T. Hertach (paratype 21, coll. NMBE); Monte Caslano, TI, CH, 45.9612°/8.8801°, 470 m asl, 22.6.2013, leg. T. Hertach (paratype 25, coll. Hertach).

MORPHOLOGY

Diagnosis

The morphological distinction between the species of the C. montana complex is very difficult, and is not

possible for all specimens. Cicadetta sibillae sp. nov. specimens are separated from the very closely related C. cerdaniensis s.str. with high probability by the predominantly dark basal junction of anal veins (92.3 versus 5.0%). From C. montana s.str., many specimens are distinguished by the outer rim of costa darker than the inner rim and the radial/subcostal veins in the forewing (87.5 versus 9.5%, chi-square contingency test, χ 2 = 42.3, P <0.001), or by the cubitus anterior vein brighter than the median vein in the hindwing (85.7 versus 8.3%, chi-square contingency test, χ 2 = 42.2, P <0.001). Cicadetta sibillae sp. nov. has on average slender forewings and a significantly lower wing ratio (length to width) than C. a. anapaistica ( Fig. 5A , only males considered, Wilcoxon rank sum test, W = 79, P = 0.004).

Description

Measurements

Body length: 18.0 mm in holotype specimen; 17.2 ± 0.7 mm (mean ± SD) in male paratypes; 18.5 ± 1.3 mm in female paratypes. Body width (abdomen, tergite 2): 5.8 mm in holotype specimen; 5.6 ± 0.2 mm in male paratypes; 5.8 ± 0.5 mm in female paratypes. Forewing length: 19.7 mm in holotype specimen; 18.9 ± 1.1 mm in male paratypes; 20.6 ± 1.0 mm in female paratypes. Forewing width: 8.2 mm in holotype specimen; 7.7 ± 0.5 mm in male paratypes; 8.3 ± 0.4 mm in female paratypes.

Male holotype with remarks on the variability in the paratype series ( Fig. 4A )

Head: Black with ochre patch on epicranial suture. Postclypeus with longitudinal narrow groove, black with lateral margins yellowish (paratypes sometimes additionally with a yellowish triangular patch at postclypeus towards the frontoclypeal suture), anteclypeus black. Rostrum reaching mid trochanter, labrum and mentum predominantly dark brown (paratypes often lighter), labium dark brown to black. Compound eyes and ocelli brownish. Antennae dark brown to black with lighter margins of scapes.

Thorax: Pronotum generally black with posterior margin of pronotal collar and its lateral angles yellowish (paratypes sometimes completely black, sometimes additionally with central suture partly marked yellowish). Lateral angles of pronotal collar pronounced but margin frontal to the lateral angles scarcely turned up and steadily narrowed towards the head in dorsal view (paratypes often turned up more strongly and convex in shape, compare Fig. 5B ). Scutum, cruciform elevation, and metanotum black, the latter with yellowish margins (paratypes sometimes with paired lighter spots on the cruciform elevation, rarely also on the scutum). Ventral side generally black, except membranes at bases of legs orange to brown and broad yellowish margin of episternum 2 (rarely missing in paratypes). Opercula not overlapping, kidney-shaped with black base and yellowish to brownish distal part. Meracanthus with spike of medium size, directed mainly caudally (paratypes very variable in shape and size).

Abdomen: Abdomen triangular in cross section. Tergites I and II black, first with orange to red brown marked ribs anterad to timbals. Tergites III–VIII frontal black and caudal red brown (some paratypes and fresh specimens orange). Sternites III–VII red brown with darker sectors frontal in the centre (paratypes sometimes orange or ochre instead of red brown, and dimensions and colour intensity of dark sectors highly variable). Epipleurites caudally orange brown, frontally darker. Timbals with three main ribs, two long and one shortened (the latter optionally interrupted in paratypes), and timbal plate.

Legs: All legs with yellow to orange and black fasciae and dots. Front femora with one longer and two shorter spines.

Wings: Forewing hyaline except for slightly yellowish basal cell and for brownish to reddish pterostigma. Basal membrane orange to red. Median and cubitus anterior vein originating in one point at basal cell (five paratypes with median and cubitus anterior vein fused, on one or both sides, for approximately 1 mm). Coloration of basal veins ranging from ochre to dark brown (paratypes rarely and partly even black). Costal vein with darker exterior and lighter inner rim, radial/ subcostal veins and median vein lightest (paratypes rarely other colour combinations). Basal junction of anal veins predominantly dark brown to black ( Fig. 4C, D , one paratype yellowish). Distal veins with eight apical cells (paratypes also seven or nine), dark or even black. Hindwing transparent, except for orange base of costal cell, orange margins of jugum and plaga, and darkbrown spotted apical vannus margin. Veins dark, especially in distal part with six apical cells. Radius and cubitus anterior vein lighter than median vein (paratypes sometimes same colour, especially in radius).

Genitalia: Pygofer very dark (paratypes lateral often with important orange brown portions) with rounded dorsal beak and rounded blunt upper lobes. Median lobe of uncus dark brown and curved upwards, rounded and broad. Claspers hooked and dark brown, hooks pointed. Pseudoparameres flattened, especially in the central part, and with sharp end. Basal lobe of pygofer dark brown (in paratypes often lighter ochre or red brown), touching main capsula. Anal tube and anal style reddish.

Female paratypes ( Fig. 4A )

Female body and wing coloration is close to the lightest paratype males. On the thorax, all three females with paired lighter spots on the cruciform elevation and its lateral depressions and fine drawings along the parapsidal sutures. On the abdomen, dark spots on the sternites highly variable in dimensions and intensity. On forewings, the basal veins less variable in coloration, from ochre to brown, and never black, one specimen even with basal junction of anal veins yellowish instead of dark. Ratio of body length to ovipositor length (including sheath) 3.2 ± 0.2.

ACOUSTIC BEHAVIOUR

Diagnosis

The calling song of C. sibillae sp. nov. is very similar to C. cerdaniensis s.str. in qualitative aspects ( Fig. 6B, C ); however, it is best distinguished by the speed of the fast phrase (phrase 3), which is slower in the new species, and by the number of timbal movements of the ungrouped, short echemes forming this phrase (> 6.5 syllables, valid for 93% of investigated individuals in C. sibillae sp. nov., 0% in C. cerdaniensis s.str.). Other species of the C. cerdaniensis species group differ qualitatively in the fast phrase 3: in C. cantilatrix the fast phrase is missing in the calling song and in C. anapaistica echemes of the fast phrase are grouped.

Composition of calling song

Recordings of 22 individuals of C. sibillae sp. nov. were analysed in detail in a perch temperature range of 23– 28°C (T mean = 25.4 °C). They were compared with eight recordings of C. cerdaniensis s.str. in the same temperature range (T mean = 25.0 °C). Cicadetta sibillae sp. nov. recordings originate from all five metapopulations (with a minimum of two and a maximum of six recordings), and the C. cerdaniensis s.str. recordings come from the most important local populations known in Osseja and Py ( Puissant, 2006, Eastern Pyrenees, Fig. 2 ). Another 62 sound samples of C. sibillae sp. nov. and 16 of C. cerdaniensis s.str. were analysed for at least one variable in a broad temperature range.

The song structure is composed of two clearly distinct phrases ( PH 2 and PH 3). A typical phrase 1 ( PH 1) as in C. cerdaniensis s.str. ( Puissant & Boulard, 2000) and as in C. a. anapaistica ( Hertach, 2011) is very rare. Slow phrase 2 ( PH 2) consists of a longer series of echemes composed of a low-intensity part (FP 2) and a completely connected loud short part (SP 2), which is comparable with the main phrases in C. cantilatrix , C. cerdaniensis s.str., and C. anapaistica . Typical echemes slightly differ in qualitative or quantitative aspects between some taxa ( Fig. 6 , right). Phrase 3 ( PH 3) is a faster repetition of evenly distributed short single echemes, which is similar to the pattern in C. cerdaniensis s.str. Phrase 2 and phrase 3 are alternating, but the song never starts or ends with phrase 3 ( Fig. 6C ). Interestingly, phrase 3 is almost equal in mean duration for all investigated taxa of this species group ( PH 3; Table 2 ).

Measurements of the calling song characters within the defined temperature range in C. sibillae sp. nov. are reported in comparison with C. cerdaniensis s.str. in Table 2 . The box plots of important time variables measured and the linear discriminant analysis show significant differences between the two taxa ( Fig. 7 ; Table 3 ).

We tested in detail the assumptions from the fieldwork that phrase 3 is emitted with different rates in C. cerdaniensis s.str. and C. sibillae sp. nov. ( Fig. 8C– F ). In fact, rates and durations are specific and correlate to the perch temperature. G 3 but also ED 3 are highly significant between species [ Fig. 8A , ANCOVA; F temp (1, 85) = 38.8, P temp <0.001, F species (1, 85) = 66.8, P species <0.001 for G 3; F temp (1, 85) = 14.0, P temp <0.001, F species (1, 85) = 103.9, P species <0.001 for ED 3]. Cicadetta sibillae sp. nov. echemes have approximately the same duration as C. cerdaniensis s.str. when the temperature is shifted by +10 °C. Looking for a less temperaturedependent character, we counted the timbal movements of 20 short echemes for each individual, which turned out to be very constant within species and different between them: 5.40 ± 0.59 syllables in C. cerdaniensis s.str. and 7.64 ± 0.89 in C. sibillae sp. nov. [ Fig. 8B , ANCOVA, F temp (1, 73) = 2.8, P temp = 0.097, F species (1, 73) = 113.6, P species <0.001]. The mean values of the five metapopulations in C. sibillae sp. nov. vary in a very small range from 7.5 syllables (Campanian, Insubrian, and Northern Apenninian) to 7.8 (Western Alpine) and 7.9 (Central Apenninian), and are not correlated with latitude ( Table 4 ). Out of 79 individuals investigated, only four of each species fall into the category with mean values between 6.0 and 6.4, and are impossible to separate.

Song variables are constant and without disruption between the different metapopulations in C. sibillae sp. nov., with one clear exception ( Table 4 ). A spatial gradient is recognizable for the echeme durations in phrases 1 and 2 (ED 1+2) from north to south, with echemes of double durations on average in the Campanian and Central Apenninian metapopulations, compared with the northern echemes. The high correlation with latitude indicates a cline. ED 1+2 and IED 1+2 are well and positively correlated in most individuals (linear regressions, R 2 median = 0.54, n ind = 22), which is stronger than in any other taxa of the group (compare with Hertach, 2011).

Echeme power (EP) is slightly reduced from that in phrases 1 and 2 (E 1+2) to that in phrase 3 (E 3) in both species being compared [1.3 ± 1.3 dB for C. sibillae sp. nov. (mean values for 39 individuals) and 1.1 ± 1.2 dB for C. cerdaniensis s.str. (mean values for 14 individuals)]. The frequency domain (EF) is comparable with others from the Cicadetta montana complex, with a broad intraspecific variability, and is not suitable for species delimitation within the investigated group ( Table 2 and 3 ).

The song pattern of C. sibillae sp. nov. is very stable. No qualitative song variability and aberrations have been detected.

ETYMOLOGY

The species name ‘ sibillae ’ is genitive of ‘ sibilla ’, and is derived from the locality name ‘Monte Sibilla’ in the Monti Sibillini mountain group (Marche Region). The geographically closest local population is situated at the northern edge of the Central Apenninian metapopulation. In addition, the name is indicative to the wife of the first author, with her first name being ‘Sibille’. Finally, we hope that subsequent researchers judge our taxonomic conclusions in accordance with the origin of the word, which designates a wise or a truth-speaking woman.

DISTRIBUTION AND ECOLOGY

Cicadetta sibillae sp. nov. is one of the most widely distributed cicadas in Italy, and reaches the southernmost parts of Switzerland and probably also France in the Maritime Alps, close to the Italian border (S. Puissant, pers. comm.). Our database consists of 267 locations, with observations of more than one thousand individuals (Appendix S3). The distribution range is well known and is split into at least five disjunct areas ( Figs 2 , 9 ). The Insubrian metapopulation in the north reaches from Lake Garda and Bolzano to Lake Maggiore, and contains all Swiss populations in the southern Ticino and the Mesocco Valley. Populations are scattered over relatively small suitable habitats but some local populations are very rich in individuals, as is the case at Monte San Giorgio (Meride, Ticino; Fig. 10B ), Monte Chiusarella (Varese), or Lodrino (Trompia Valley). The Western Alpine metapopulation is a relictual fragment in very few locations around Lanzo, the Susa Valley, the Monferrato Hills, and the Maira Valley. The most important occurrences are found in the Northern Apennine, where the new species is generally the most frequent cicada. This metapopulation reaches at least from the Ormea region (Piedmont) in the west to the Monte Falterona and Campigna forest (Tuscany and Emilia-Romagna) in the east. Southwards, Cicadetta sibillae sp. nov. is abruptly replaced by C. brevipennis . The new species itself competitively excludes C. brevipennis in a Central Apenninian metapopulation from the Sibillini Mountains south- and westwards to the Simbruini Mountains. The southernmost metapopulation in Campania contains only a few scattered observations.

The altitudinal range of C. sibillae sp. nov. is from 20 m asl (Terme di Suio, Lazio) to 1430 m asl (Denti della Vecchia, Lombardy/Ticino), with a maximum abundance between 400 and 900 m asl. In peripheral metapopulations, the species is a habitat specialist. The Insubrian metapopulation prefers sparsely or semi- open woodland characterized by Downy Oak ( Quercus pubescens ), Turkey Oak ( Quercus cerris ), Hop Hornbeam ( Ostrya carpinifolia ), and Manna Ash ( Fraxinus ornus ) ( Fig. 10B ). Western alpine cicadas are often found in sparse woods of the Black Pine ( Pinus nigra ) and the Scots Pine ( Pinus sylvestris ). The Central Apenninian and Campanian metapopulations are normally restricted to habitats with mesophilous, mountainous conditions, often on slopes or floors of smaller valleys. Conversely, the species is more of a generalist in the Northern Apenninian metapopulation (compare Fig. 10A ). It has been found in Mediterranean shrub land influenced by fire near the coast as well as in vigorous Beech forests ( Fagus sylvatica ). Nevertheless, the majority of populations are found in ecotone habitats with sparse oak woods and a well-developed grass layer. Individuals sing in a broad vertical range from a few centimetres up to 10 m above ground, but with a clear maximum between 2 and 5 m.

Cicadetta sibillae sp. nov. was observed syntopically with up to seven other cicada species in sparse oak forests ( Quercus spp. ) in the Apennine (Santerno Valley, Tuscany). Conversely, in the Alps and mesophilous, temperate habitats of the Apennine Mountains, it is sometimes the single cicada species. The new species was phenologically first recorded on 27 May (2005 and 2006, Ticino) and last on 1 August (2008, Liguria).

Figures

Figure 2. Chorological pattern of seven undetermined metapopulations in the Cicadetta cerdaniensis song group and distribution areas of described species in Southern Europe. Preliminary classifications with informal names according to qualitative song patterns. Map with locations of analysed data: G, genetics; M, morphology; s, some key variables of the song analysed; S, detailed song analyses (recordings between 23 °C and 28 °C perch temperature only).

Figure 4. A, Cicadetta sibillae sp. nov. type series with holotype specimen (above) and female paratype (below). B, Cicadetta anapaistica lucana ssp. nov. type series with holotype specimen (above), light morph paratype (centre), and female paratype (below). Basal junction of anal veins (red line) dark in C. sibillae sp. nov. (C, D) and light in Cicadetta cerdaniensis s.str. (E, F). Males of (D) C. sibillae sp. nov., (F) C. cerdaniensis s.str., and (H) C. a. lucana ssp. nov. in natural conditions. G, dorsofrontal view of head and pronotum in (dried) light morph paratype of C. a. lucana ssp. nov.

Figure 5. Morphometry of Cicadetta sibillae sp. nov. and Cicadetta anapaistica: box plots of some significant but not diagnostic differences in sizes and ratios.

Figure 6. Oscillograms (time versus amplitude) of typical calling songs in the Cicadetta cerdaniensis group (20-s sections of different phrases on the left, 2-s sections of phrase 2 on the right, with terms of variables): A, Cicadetta cantilatrix (phrases 2–1, Basel-Land, Switzerland); B, Cicadetta cerdaniensis s.str. (phrases 1–3–1–2, Eastern Pyrenees, France); C, Cicadetta sibillae sp. nov. (phrases 2–3–2, Tuscany, Italy); D, Cicadetta anapaistica lucana ssp. nov. (phrases 2– 3–2, Basilicata, Italy); E, Cicadetta anapaistica anapaistica (phrases 2–3–2, Calabria, Italy); F, Cicadetta brevipennis song pattern for comparison. Triangles indicating the beginning of the phrases: ▲, typically clear transitions, with phrase 3 involved; △, smooth transitions between phrases 1 and 2. For more details of phrase 3, see Figures 8C–F and 11.

Figure 7. Box plots of important song duration variables in Cicadetta cerdaniensis s.str. (eight individuals) and Cicadetta sibillae sp. nov. (22 individuals), and of the linear discriminant analysis (LDA) between 18 song variables for a 23– 28 °C perch temperature range; ED, echeme durations; FP, first echeme part; IED, inter-echeme durations; SP, second echeme part.

Figure 8. Echemes of phrase 3 in Cicadetta cerdaniensis s.str. (△) and Cicadetta sibillae sp. nov. (◆). A, duration of echemes as a function of perch temperature, with linear regression trend lines and standard errors (grey areas). B, box plot of the number of syllables per echeme given as mean values of 20 echemes for each individual. C–F, oscillograms (time versus amplitude) close to the linear regression trend lines of (A): C, C. sibillae sp. nov. at 23 °C perch temperature (with measured duration terms, Northern Apenninian metapopulation); D, C. sibillae sp. nov. at 28 °C (Western Alpine metapopulation); E, C. cerdaniensis s.str. at 23 °C (Eastern Pyrenees); F, C. cerdaniensis s.str. at 28 °C (Eastern Pyrenees).

Figure 9. Distribution map of the species of the Cicadetta cerdaniensis song group (15 × 15-km2 grid cells). Notes: cells recently checked in the framework of the Swiss and Italian projects of the first author without detection of a taxon of this group are brownish. The Cicadetta cantilatrix distribution range is not completely visible. Published records of Cicadetta cantilatrix by Sueur & Puissant (2007), Trilar & Holzinger (2004), Hertach (2007), Brua & Hugel (2008), Trilar & Gogala (2012), and Hertach & Nagel (2013).

Figure 10. Habitats of Cicadetta sibillae sp. nov. in Tiglieto (Liguria, A) and at the Monte San Giorgio (Ticino, B), and most important location of Cicadetta anapaistica lucana ssp. nov. in the mountainous Pollino National Park (C). Threatened core population habitat of Cicadetta anapaistica anapaistica in the Madonie Mountains as a result of overgrazing and soil erosion (D).