Neotibicen similaris apalachicola, Marshall, David C. & Hill, Kathy B. R., 2017

Marshall, David C. & Hill, Kathy B. R., 2017, A new Neotibicen cicada subspecies (Hemiptera: Cicadidae) from the southeastern USA forms hybrid zones with a widespread relative despite a divergent male calling song, Zootaxa 4272 (4), pp. 529-550 : 531-537

Neotibicen similaris apalachicola , n. subsp.

Neotibicen nr. similaris, Hill et al., 2015: 233 , 234, 235, 250. Neotibicen cf. similaris, Hill et al., 2015: 239 .

Type locality. Florida, Leon County, rest area on Interstate Highway 10, 0.6 miles east of the Ochlockonee River ; latitude 30.485° N, longitude 84.386° W.

Holotype male ( Fig. 1 ): WHITE LABEL: USA: Florida: Leon Co. \\Interstate 10 rest area, W side\\of Tallahassee. 0.6 mi E of the\\ Ochlockonee R. 21 July 2008 \\ 30°29.126'N 84° 23.137'W 198ft \\ K.Hill & D.Marshall US.FL.TRA. GREEN LABEL: HILL&MARSHALL VOUCHER\\pinned specimen, legs in EtOH\\08.US.FL.TRA.03\\ Neotibicen similaris apalachicola \\specimen recorded. Mature specimen attracted to light, recorded singing in cage on 21 July 2008 (see below). Pinned specimen deposited with the AMNH. Right midleg stored with C. Simon EtOH cold-storage tissue collection, University of Connecticut, Storrs, Connecticut, USA .

Paratype specimens: Florida: Gadsden Co. — 1♂, ~ 30 mi. W. of Tallahassee , 1 mi. SE of I10 on Rt270A, Flat Creek Rd., 30°36.56N 84°48.59W, 290ft. 0 2 Jul 2007. D. Marshall & K. Hill. DNA voucher 07.US.FL.FLK.01 (legs in EtOH). Mature male attracted to light. Jefferson Co. — 1♀, End of Depot St. , N. side of Lamont, NW of Aucilla R., 30°22.645'N 83°48.759'W, 80ft. 10 July 2008. K. Hill & D. Marshall. DNA voucher 08.US.FL.LMC.01 (legs in EtOH). Mature specimen . 1♂, Depot St., Lamont, NW of Aucilla River, 30°22.645'N 83°48.759'W, 80ft. 10 July 2008. K. Hill & D. Marshall. DNA voucher 08.US.FL.LMC.02 (legs in EtOH). Genitalic capsule removed and stored separately. Leon Co. — 1♂, type locality, Interstate 10 rest area, W. side of Tallahassee . 0.6 mi E of the Ochlockonee R., 30°29.126'N 84°23.137'W, 198ft. 10 July 2008. K. Hill & D. Marshall. DNA voucher 08.US.FL.TRA.01 (legs in EtOH). Crushed with abdomen on separate pin . 3♂, same location and collectors, 20 July 2008 (1♂ in WTD, 1♂ in USNM) . 1♀, same location and collectors, 20 July 2008, DNA voucher 08.US.FL.TRA.01 (legs in EtOH) . 1♀, same location and collectors, 20 July 2008, DNA voucher 08.US.FL.TRA.02 (legs in EtOH). Ecdysis incomplete . 2♀, same location and collectors, 20 July 2008 . 1♂, same location and collectors, 21 July 2008, voucher 08.US.FL.TRA.X , genitalic capsule labelled TIB22 removed and stored separately ( MSM) . 1♀, same location and collectors, 21 July 2008 . 2♂, 4♀, same location and collectors, 23 July 2008 (1♂ in AFS, 1♂ 1♀ in FAC, 1♀ in USNM, 1♀ in AMNH) . 2♀, same location and collectors, 4 Sep 2008 . 2♀, same location, 9 Aug 2010, Rondel Veal . 1♂, 3♀, same location, 13 Aug 2010, K. Hill & D. Marshall . Wakulla Co. — 1♂, 4.3 mi. NW of US319 on Rt. 267, NW of Hilliardville , 30°18.026'N 84°25.065'W, 83ft. 5 Sep 2008. K. Hill & D. Marshall. US.FL.LEC . Mature males collected singing. All pinned material stored in KHDM collection unless otherwise noted; for collection abbreviations see Methods.

Locations where only recordings or aural records were taken are listed in Supplementary Table 1 along with the specimen records. Note that all type locality specimens except the holotype were collected while emerging and allowed to mature for only 1–2 days before pinning.

Etymology. Named for the Apalachicola River of the Florida panhandle. The subspecies epithet is a noun in apposition and need not agree in gender with its genus following the Code of Zoological Nomenclature ( ICZN, 1999), articles 11.9.1.2 and 31.2.1.

Description, holotype male ( Fig. 1 A–D ). An overall large and dark-colored Neotibicen , with black background color and muted brown and green patterning, except where covered in white wax underneath. Small golden or silvery hairs can be seen, where they have not been rubbed off, in various crevices on the dorsal surface and to a lesser extent ventrally.

Head. Mostly black, with small brown patches extending between postclypeus and compound eyes and near ocelli. Compound eyes, viewed dorsally, as wide as or slightly wider than pronotal collar, dark brown or black, with a fringe of short hairs posteriorly. Underside of head covered in white wax except for center of the postclypeus. Postclypeus mostly black with a small brown spot at the top and along the anterior midline, with nine ridges and a central groove. Anteclypeus covered with wax except for brown central midline. Lorum covered with wax. Proboscis light brown at base tending darker towards tip, extending to midway between hind coxae.

Thorax. Pronotum mostly dark brown. Median sulcus muted yellow-green, bordered with black triangleshaped patches widening anteriorly and with a yellowish brown mark on either side posteriorly, just above the pronotal collar. Pronotal collar black, extreme lateral edges dull green. Mesonotum mostly black, with a thin “crown” pattern varying brown to green, and with the central portion above the cruciform element combining the two inner sigilla to form a large black patch. Lateral color patches, to the outer sides of the lateral sigillas, dark rusty brown. Cruciform elevation light brown, with the center notch black; metanotum brown. Underside of pronotum and mesonotum covered in white wax, this wax at least partially covering the coxae, trochanters and femora.

Legs. With trochanters pale greenish brown, femora mostly brown. Base of tibia pale green on mid and hind legs, pale brown on forelegs, all tips dark brown. Tarsi pale and dark brown with black tarsal claws. Foreleg primary spine angled but not lying flat, secondary spine larger and more erect.

Wings. Slightly longer than body, mainly hyaline. Forewing with basal cell mostly yellow-green, clear near vein CuA, flaps grey, and with only the faintest hint of yellow infuscation otherwise in the membranes. Dark brown infuscations present at the veins joining forewing cells u1/a2 and u2/a3. Basal half of forewing costa green, distal costa brown, ventrally with a black internal border. Vein CuP in forewing green, M and CuA in forewing and CuA and CuP in hindwing greenish brown, otherwise veins mostly black. Hindwing with veins 2A and 3A edged in brownish grey, flaps white.

Abdomen. Tergites glossy black, with bright white wax spots on tergite II on either side above the timbal cover and centrally. Timbal covers black. Underside of abdomen with white wax coating the lateral edges of the sternites and the opercula, especially the lateral and basal edges. Sternites mostly black, with posterior margins of sternites III–VII medium brown, especially laterally. Sternite VIII forming an upright V-shape in posterior view. Opercula pale brownish green, overlapping for more than half their length. Opercula slightly pointed at tips, reaching the 4th sternite, lateral edges bowed inward slightly where they meet the timbal covers.

Genitalia ( Figs. 1B, 1D , 2 A). Pygofer black, becoming brown towards base, in ventral view widest at about mid length, with widest width at base less than width of posterior margin of sternite VI; dorsal beak forming a sharp spine; distal shoulders weakly developed and rounded; basal lobes well-developed and visible in lateral view, in ventral view straight with rounded apices, not quite reaching to uncus. Median lobe of uncus black, broadest at base and narrowing evenly to a blunt apex that is almost divided by a deep dorsal suture; laterally with a large pair of black spines either side directed dorsally, their tips just visible dorsally (easily seen laterally). Aedeagus a sclerotized tube with a slightly flared, unsclerotized apex, at rest reaching just beyond the paired uncal spines. Anal styles dark brown.

Song. The following describes a single recorded phrase of the holotype male numbered 08.US.FL.TRA.03 found in voucher recording 08.US.FL.TRA.03.T02.WAV which will be deposited at the online repository BioAcoustica ( Baker et al., 2015) and at www.insectsingers.com ( Marshall and Hill, 2010). The holotype song phrase consists of approximately 20 s of timbal sound with a frequency range of approximately 2–19 kHz (approximately the limit of the microphone used), containing the following three sections: (1) a leading section consisting of a uniform buzz of increasing intensity approximately 1–2 s long (noted in the field, the holotype recording begins just after this section); (2) a main phrase that alternates sharply and seamlessly between shorter, higher amplitude, high-pitched echemes (0.08–0.13 s each) with sound frequencies mainly from 9–13 kHz and longer, lower amplitude, low-pitched echemes (0.35–0.38 s each) with sound frequencies mainly from 5.5–9.0 kHz (plus a secondary peak near 2.7 kHz) — the single low-pitched echeme could also be described as a series of seamlessly repeated four-pulse echemes; (3) a trailing buzz with sound energy mainly below 9 kHz. The rate of alternation between high- and low-pitched echemes in the main phrase is 2.1 cycles per second. Details of the waveform structures for the latter two parts of the song are as follows: Section (2) above, the main phrase, contains pulses repeated at about 370/sec in the shorter high-pitched echemes and pulses repeated at about 625/sec in the longer low-pitched echemes, the latter visibly grouped into fours based on amplitude patterns. Section (3) contains two-pulse echemes produced at about 240/sec and sometimes alternating in amplitude. In the holotype male phase, a subtle “rattle” lasting about 0.175 s appears near the beginning of the trailing section, suggesting the song pattern of the main phrase of N. similaris similaris (see below). The holotype recording is slightly distorted due to the short distance between the specimen and the microphone, which causes an exaggeration and smearing of the frequency spectrum at values over ca. 19 kHz; the important features of the song remain visible. The amplitude decreases at about 2.5 s into the track because the recorder gain was decreased. This recording was made on 21 July 2008 in the rear of an open car following a playback stimulus; ambient temperature was not recorded. Figure 3 shows an example phrase from a higher-quality recording made at a different location.

Morphological variation in male paratypes. Most paratype specimens were not individually recorded singing and some were not collected at the type locality. Subspecies identification in these cases was made on the basis that only Neotibicen similaris apalachicola songs were heard at and near those locations (see section on Distributions below). Many of the paratypes were preserved only one or two days post-ecdysis and so have only a light covering of wax and fine hairs coating much of the dorsal surface.

Although the male paratypes are overall dark-colored, some have slightly brighter green and brown patterning, and in some the pronotal "crown" is more complete than in others. Many individuals have the veins in the basal half of the forewing and many hind wing veins green or brown (especially on faded specimens). Legs of some specimens are mostly pale green with the tip of each segment tending dark brown. Opercula vary considerably in size and degree of pointedness at the tip, many being almost triangular, some with the tip and lateral portions appearing flattened compared to the inner part which appears to bulge outwards slightly. In all male paratypes the opercula extend at least half-way down the 3rd sternite, and in most they reach at least to the anterior edge of the 4th sternite. The tip of the forewing at the tip of veins R1a and R1b is often lightly infuscated with black, this infuscation sometimes reaching to the apex and slightly around the wing margin. Size measurements are given in Table 1.

Song variation. Measurements of song characters from 13 phrases from throughout the range of Neotibicen similaris apalachicola are found in Table 2 (see Supplementary Table 1 for source locations). Occasional song phrases from throughout the range, including at the holotype locality, exhibited brief rattles of a small fraction of a second in duration in the transition from the alternating section of the song phrase to the trailing buzz. These features resemble the rapidly alternating section of the song of the nominate subspecies (see below).

Females. Overall similar to males, but tending paler in color with more brown and green, especially ventrally, and with the basal half of the forewing veins usually green or brown (Supplementary Fig. 2 ). Ovipositor brown to dark brown, not extending beyond sheath. Abdominal sternites variable in color, commonly brown or greenish brown rather than black, sometimes with black centers, and with epipleurites brown to greenish brown. Ninth tergites varying from black adjacent to ovipositor to brown or tan laterally. Size measurements in mm for a sample of 13 female specimens are given in Table 1.

ZooBank registry. urn:lsid:zoobank.org:act:7E149853-51EB-4D61-A96F-B95E34E985C2

Neotibicen similaris similaris (15♂)

Main phrase length (s) 10.7** 6.3 17.3 Length of part I of main phrase (s) 3.2 1.2 5.8 Rate of alternation between high and low echemes, part I (Hz) 21.7 14.9 24.8 Length of part II of main phrase (s) 7.4 4.6 11.9 Rate of alternation between high and low echemes, part II (Hz) 34.5** 21.9 41.1 High pitched echeme duration (s) 0.01** 0.008 0.015 High pitched echeme dominant pitch (kHz) 8.6** 7.9 9.6 Low pitched echeme duration (s) 0.02** 0.007 0.1 Low pitched echeme dominant pitch (kHz) 5.2* 2.4 7.9

Figures

FIGURE 1. A – D, Neotibicen similaris apalachicola, n. subsp., dorsal view, ventral view, pygofer ventral view, pygofer lateral view (holotype specimen 08. US. FL. TRA. 03). E – H, N. similaris similaris, dorsal view, ventral view, pygofer ventral view, pygofer lateral view (specimen 08. US. GA. HAH. 01). Scale bars = 12.5 mm.

FIGURE 2. Pygofer preparations showing aedeagus (ae) beneath uncus (u): A, Neotibicen similaris apalachicola, n. subsp., specimen 08. US. FL. LMC. 02; B, N. similaris similaris, specimen 08. US. FL. HSC. 20. White scale bar = 1 mm.

FIGURE 3. Neotibicen similaris apalachicola, n. subsp., field recording of male calling song from Wakulla Co., Florida (recording 08. US. FL. BXU. T 08. WAV). Each panel shows a waveform above a spectrogram; A, complete song phrase; B, partial zoom of the central portion of the phrase; C, further zoom of one of the four oscillations in B; D, segment of song that precedes the main phrase. Sound energy below 1.8 kHz has been removed.