Euparkerella cryptica, Hepp, Fábio, De Carvalho-E-Silva, Sergio P., Telles De Carvalho-E-Silva, Ana M. P. & Folly, Manuella, 2015

Hepp, Fábio, De Carvalho-E-Silva, Sergio P., Telles De Carvalho-E-Silva, Ana M. P. & Folly, Manuella, 2015, A fifth species of the genus Euparkerella (Griffths, 1959), the advertisement calls of E. robusta Izecksohn, 1988 and E. tridactyla Izecksohn, 1988, and a key for the Euparkerella species (Anura: Brachycephaloidea: Craugastoridae), Zootaxa 3973 (2), pp. 251-270 : 255-264

Euparkerella cryptica sp. nov.

( Figures 4 and 5 )

Holotype. ZUFRJ 13281, adult male, collected in a rainforest fragment (22°29'1.53''S, 42°15'11.82''W; ca. 70 m above sea level) at Sítio Igarapê, municipality of Silva Jardim, state of Rio de Janeiro, Brazil, on 19 May 2011 by F. Hepp, S.P. de Carvalho-e-Silva, J. Kirchmeyer, M. Folly, and D. de Goes. The area is near the Reserva Biológica Poço das Antas.

Paratopotypes. ZUFRJ 12645, 12648–12649, MNRJ 85756–85757 collected on 11 November 2010 by F. Hepp, S.P. de Carvalho-e-Silva, J. Kirchmeyer, P. Bragança, A.M.P.T. de Carvalho-e-Silva and D. de Goes; ZUFRJ 12683 collected on 24 November 2010 by F.F. Hepp, S.P. de Carvalho-e-Silva, J. Kirchmeyer; ZUFRJ 12849– 12855 collected on 15 April 2011 by F. Hepp, S.P. de Carvalho-e-Silva, J. Kirchmeyer, M. Folly, and D. de Goes; ZUFRJ 13449 collected on 2011 by F. Hepp, S.P. de Carvalho-e-Silva, J. Kirchmeyer, and D. de Goes; ZUFRJ 13524–13527 collected in 2011 by F. Hepp, S.P. de Carvalho-e-Silva, J. Kirchmeyer, and D. de Goes; ZUFRJ 13282, 13283, 13285, 13286 collected on 26 August 2011 by F. Hepp, S.P. de Carvalho-e-Silva, J. Kirchmeyer and D. de Goes.

Etymology. The species epithet “ cryptica ” is used as an adjective in feminine. The Latin word crypticus means “covered” or “concealed,” and it is used in reference to the morphological similarity of some individuals of this species to Euparkerella brasiliensis or E. cochranae .

Diagnosis. A species of Euparkerella , according to its globular body, head narrower than body, lateral surfaces of the head darker than dorsal surface, forming a masklike facial pattern, a pair of ventrolateral grooves along body, slender arms, short fingers and toes, terminal digits pointed with small pads with no circumferential grooves, large inner and outer metatarsal tubercles, and no tarsal tubercles. Euparkerella cryptica sp. nov. is diagnosed as follows: (1) medium size (adults SVL: x = 15.7 ± 2.1; 12.5–19.5 mm); (2) slender body (BW: x = 7.4 ± 1.0; 5.7–9.0 mm); (3) narrow head (HW: x = 6.6 ± 0.8; 5.5–8.0 mm); (4) long Finger IV, Toes I and V; (5) all plantar tubercles protuberant; (6) duration of advertisement call longer than 3 s (x = 4.7; Mo = 5.0; 3.4– 6.2 s); (7) Pulse-Section Rate slower than two sections/s (x = 1.5; Mo = 1.8; 1.2–1.9 sections/s); and (8) exhibiting pulse clusters made up two or three pulses grouped in a single pulse section.

Comparisons with the other species. Euparkerella cryptica sp. nov. is smaller than E. robusta and E. tridactyla (SVL: x = 15.7 ± 2.1; 12.5–19.5 mm in E. cryptica vs. x = 18.5 ± 1.0; 17.2–21.5 mm and = 18.3 ± 1.8; 16.0– 20.7 mm in E. robusta and E. tridactyla , respectively). The new species differs from E. robusta by its slender body (BW: x = 7.4 ± 1.0; 5.7–9.0 mm in E. cryptica vs. x = 10.3 ± 1.2; 9.0– 13.5 mm in E. robusta ) and its narrower head (HW: x = 6.6 ± 0.8; 5.5–8.0 mm in E. cryptica vs. x = 8.3 ± 0.6; 7.4–10.0 mm in E. robusta ). Euparkerella cryptica sp. nov. differs from E. tridactyla in having long completely developed Finger IV, and Toes I and V (vs. vestigial Finger IV, and Toes I and V in E. tridactyla ; Table 3); tubercles of the hand and foot protuberant (vs. not protuberant, large and flat in E. tridactyla ). Acoustically, E. cryptica differs from all other species of Euparkerella in having a longer call (3.4– 6.2 s in E. cryptica vs. 0.4– 2.2 s in the other 4 species; Table 4 ); presence of pulse clusters (vs. absence in the other species); and slower repetition rate (1.2–1.9 pulse sections/s in E. cryptica vs. 3–45 pulse sections/s in the other species).

Measurements E. brasiliensis E. cochranae E. cryptica sp. nov. E. robusta E. tridactyla (N = 21) (N = 20) (N = 19) (N = 17) (N = 7)

SVL 14.9 ± 1.7 (12.1– 14.6 ± 1.8 (11.5– 15.7 ± 2.1 (12.5–19.5) 18.5 ± 1.0 18.3 ± 1.8

18.6) 17.7) (17.2–21.5) (16.0–20.7) ......continued on the next page Measurements E. brasiliensis E. cochranae E. cryptica sp. nov. E. robusta E. tridactyla (N = 21) (N = 20) (N = 19) (N = 17) (N = 7) Description of holotype. Slender robust. Head slightly longer than wide (HW/HL = 0.9); HL 43% of the SVL. Snout rounded, slightly protuberant in ventral view. Interorbital distance slightly greater than 1.5× upper eyelid width (IOD/UEW = 1.7). Eye diameter slightly greater than 1.5× eye–nostril distance (ED/ END = 1.7). Tympanic membrane indistinct externally. Supratympanic fold pronounced and glandular. Vomerine teeth absent. A single, small toothlike process at anterior margin of lower jaw that fits in a single, small socket between premaxillae. Tongue long, free posteriorly, unnotched. Skin almost smooth, slightly granulated on lateral and dorsolateral surfaces. A median dorsal glandular fold. A pair of deep ventrolateral grooves along body. An area with large granules on ventral surface of thighs, corresponding to less than half of the ventral thigh surface. A slight midventral groove.

Arms slender; forearm long, slender; fingers short; finger lengths: IV <I ≅ II <III. Number of subarticular tubercles of Fingers I, II, III, and IV—1, 1, 2, and 1, respectively. Subarticular tubercles present on all fingers. Subarticular tubercle partially overlapping digital pad of Finger IV ( Fig. 6 A). Palmar subarticular tubercles large and protuberant. Finger tips conical (especially on Finger III). Three large, rounded accessory tubercles on hand; tubercles aligned with Fingers II, II and IV. Carpal tubercles large, elliptical or rounded; outer carpal tubercle slightly larger than the inner one. Legs robust. Toe lengths: I <II ≅ V <III <IV; tip of Toe V reaching top of proximal tubercle of Toe IV. Numbers of subarticular tubercles of Toes I, II, III, IV, and V – 1, 1, 2, 3, and 2, respectively. Tips of longer toes conical, especially that of Toe IV. Subarticular tubercles large, elliptical or rounded. Many small, elliptical or rounded accessory tubercles on foot aligned with Toes II, III, IV, and V. Metatarsal tubercles large, elliptical and of similar size. Tarsi without tubercles.

Measurements of holotype (mm). SVL 14.3; HL 6.2; HW 5.9; IOD 2.2; UEW 1.3; ED 1.8; END 1.0; NSD 1.0; IND 1.7; BW 1.7; UAL 3.2; FAR 3.1; HAL 2.6; FIL1 0.6; FIL2 0.7; FIL3 1.3; FIL4 0.5; THL 6.4; TIL 6.2; TAL 3.9; FL 5.2; TL1 0.6; TL2 0.9; TL3 1.4; TL4 2.5; TL5 1.1.

Color of holotype in life. Dorsum brown, with a dark Y-shaped mark. Two pairs of dark straight marks on the dorsolateral region, all marks with anterior end slanted to the body midline. One pair is in the anterior and the other in the posterior region of dorsum near inguinal and axillary regions, respectively. Upper eyelid slightly darker than dorsum. Posterior upper surface of head with inverted triangular mark, slightly darker than dorsum. Lateral surfaces of head slightly darker than dorsum, resulting in a mask-like pattern. Upper edge of mask formed by two narrow bands, one dark and one light; the upper one is twice the width of the ventral. No longitudinal median light stripe on dorsum. A pair of transversal narrow light stripes on the posterior surface of each thigh; stripes ending at the posterior end of the urostyle. Two symmetrical dark blotches on posterior part of dorsum (coccyx region, one on each side); dark transverse bars on thighs and shanks. Venter and throat purplish-brown. Throat darker than abdomen, with small, dispersed light marks. Narrow pale brown or beige fragmented stripe traversing abdomen and throat longitudinally along ventral groove. Peri-cloacal region pigmented. Pupil elliptical, horizontal; iris with numerous gold dots on black background.

Color of holotype in preservative. Coloration similar to that in life, but darker and pattern less evident. Dorsum and flanks dark brown. Venter brown, vermiculated or marbled with pale brown or beige. Ventral surfaces of thighs lacking unpigmented patches.

Variation of morphology among paratopotypes. Euparkerella cryptica sp. nov. is highly polymorphic. Frequently, individuals vary bilaterally (e.g., different features observed on right and left hands or feet). Head as long as wide (HW/HL: x = 1.0 ± 0.0). Mean head length is 43% (SD = 2%) of snout–vent length. Snout in dorsal aspect varies from rounded to subovoid, slightly acuminated to protuberant in lateral profile. In ventral view, mandible prognathous or not. Interorbital distance usually slightly longer than 1.5× width of upper eyelid (IOD/ UEW: x = 1.7 ± 0.2). Eye diameter slightly greater than 1.5× eye–nostril distance (ED/ END: = 1.7 ± 0.1). Tympanic membrane indistinct. Supratympanic fold may be less pronounced than observed in holotype. In most specimens (75%), skin granulate (especially darker specimens); some individuals with nearly smooth skin, with granules on body sides only. Middorsal glandular fold frequently pronounced and elevated, but sometimes present as a depression. Ventral thigh area with large granules about 25–50% of the ventral thigh surface. Slight medial ventral groove on thighs present or absent. Inguinal, ventrolateral, axillary, and cephalic glands (near anterior insertion of the arm in body) variably present, lumped and highlighted, or sparse and less prominent. More highly pigmented specimens with less obvious glands.

Finger lengths: I ≅ IV <II <III, or IV <I <II <III, or IV <I ≅ II <III. Five paratypes (ZUFRJ 12645–12648, 12854) lacking subarticular tubercle on Finger IV, only the digital pad ( Fig. 6 B) at least on one hand. Specimen MNRJ 85756 with subarticular tubercle clearly isolated from digital pad on Finger IV only on one hand ( Fig. 6 C). Frequently (in the holotype and 8 paratypes), subarticular tubercle partially overlapping digital pad on Finger IV ( Fig. 6 A). Outer carpal tubercle commonly rounded and inner elliptical (45%) or both elliptical (45%); sometimes both rounded (only on one hand, specimen ZUFRJ 13449). Outer and inner carpal tubercles similar in size in MNRJ 85756. Toe lengths: I <II <V <III <IV or I <II ≅ V <III <IV or I <V <II <III <IV. Frequently (55%), top of Toe V not reaching distal limit of proximal tubercle of Toe IV ( Fig. 6 D); sometimes (25%) reaching or extending beyond tubercle (10%; Fig. 6 E). Number of subarticular tubercles of Toes I, II, III, IV, and V – 0, 1, 2, 3, and 1, respectively, in ZUFRJ 12645 and 13449 (only one foot). Variation of morphometric data in Table 3.

Variation in color among paratopotypes. In preservative, much of the dorsum and flanks of some paratypes is grayish brown, brown, or light brown. There is a dark M-shaped mark on the dorsum; the central angle of the M is connected posteriorly to a triangle or arrow. A pair of inverted V-shaped marks may be present, one on each side of the dorsum. The inner end of each mark is connected to one upper angle of the M, configuring a pattern resembling two, partially overlapped, M-shaped marks. Frequently, the dorsal pattern is incomplete, with a larger V or Y-shaped mark located dorsomedially. Five paratypes (ZUFRJ 12645, 12854–55, 13449 and 13526) have a pair of light brown, circular blotches in scapular region. The upper eyelids may present the same color as the dorsum. The posterodorsal part of the head may lack a dark mark. The dark and light bands of the dorsolateral edge of mask can have the same width. A longitudinal median light stripe may be present posterior to the dorsal fold, not pronounced, starting from the posterior end of the urostyle (connected to the light stripes of the thighs) and ending at the level of the interorbital region. The two light stripes on the posterior surface of the thighs may be fragmented and connected to the dorsal light stripe at end of the urostyle. The dark marks on the posterior part of the trunk may be absent or well developed and connected to the other M-shaped mark of the dorsum. The venter may be more or less vermiculated, or marbled with pale brown or beige. The ventral stripe may traverse the whole or only the posterior half of the abdomen. The peri-cloacal region may have a slightly depigmented or clear patch.

Advertisement call. Thirteen calls of five individuals of Euparkerella cryptica sp. nov. were analyzed in detail. The advertisement call ( Fig. 7 A–C) consists of a single note comprising five to twelve sections of pulses (x = 7.4 ± 1.9; N = 13), in which one, two, or three pulses are present. Seventy of 96 pulse sections (73%) have two pulses; 25 (26%) have a single pulse, and one (<1%) has three pulses. Only one call lacked a pulse cluster (i.e., pulse sections with more than one pulse). The intervals between pulse sections are regular, as are the intervals between the pulses within the sections. All pulses show the attack shorter than the decay. There are 9–19 (x = 13 ± 3; Mo = 11; N = 13) pulses per call. The amplitude varies irregularly throughout the call, except for the first section, which always has the lowest amplitude. However, second pulses tend to have lower (ca. 50%) amplitude than the first ones within each section. Call Duration ranges from 3.393– 6.184 s (x = 4.472 ± 0.697; Mo = 5.015; N = 13). Although the pulses have a wide frequency band, between 2000 and 21000 Hz, a harmonic series is notable (frequency bands more energetic in spectrogram), with up to seven harmonics. The Fundamental Frequency ranges from 2756.2–3703.7 Hz (x = 3067.6 ± 236.3; Mo = 3000.0; N = 13). The Dominant Frequency corresponds to the Fundamental Frequency in 12 of the 13 calls, ranging from 2756.2–3617.6 Hz (x = 3193.5 ± 535.7; Mo = 3000.0; N = 13); in another call, the Dominant Frequency corresponds to the second harmonic with a value of 4823.4 Hz. The Pulse-Section Periods decrease throughout the call, and range from 0.656– 1.246 s (x = 0.978 ± 0.206; N = 13) for the first period and 0.464– 0.721 s (x = 0.618 ± 0.069; N = 13) for the last period. The Pulse Periods within the sections range from 0.057– 0.101 s (x = 0.078 ± 0.013; Mo = 0.062; N = 71). The Pulse- Section Rate ranges from 1.232–1.940 pulse sections per second (x = 1.545 ± 0.227; Mo = 1.795; N = 13). Pulse ……continued on the next page PulsePeriοd(s) Pulse-Sectiοn Pulse Duratiοn (s) Pulse-Grοup Pulse-Sectiοn Pulse Repetitiοn Number οf Periοd (s) Duratiοn (s) Repetitiοn Rate Rate (pulse⁄s) visible

(sectiοn⁄s) Harmοnics

brasiliensis 0.065 ± 0.005 (0.066) 0.065 ± 0.005 0.007 ± 0.002 ---- 17 ± 0.7 (*) 17 ± 0.7 (*) 5.9 ± 0.6 (6) 5‾7

0.053‾0.084 (0.066) (0.008) 15.9‾17.8 15.9‾ 17.8 N = 10 N = 82 0.053‾0.084 0.002‾ 0.010 N = 10 N = 10

N = 82 N = 92

cochranae 0.030 ± 0.004 (0.028) 0.030 ± 0.004 0.005 ± 0.001 ---- 35 ± 4.3 (*) 35 ± 4.3 (*) 6.3 ± 1.1 (7) 0.021‾0.041 (0.028) (0.005) 30.2‾45.1 30.2‾45.1 4‾7 N = 129 0.021‾0.041 0.002‾ 0.008 N = 10 N = 10 N = 7

N = 129 N = 135

cryptica sp. nov. 0.078 ± 0.013 (0.062) 0.730 ± 0.183 0.007 ± 0.001 0.088 ± 0.013 1.5 ± 0.2 (1.8) 23.2 ± 3.1 (22.7) 7 ± 0 (7) 7 0.057‾0.101 (0.581) (0.007) (0.088) 1.2‾1.9 18.5‾ 29.4 N = 4 N = 71 0.464‾1246.000 0.003‾0.011 0.068‾ 0.143 N = 13 N = 71

N = 83 N = 168 N = 71

robusta 0.329 ± 0.042 (0.293) 0.329 ± 0.042 0.077 ± 0.011 ---- 3.5 ± 0.2 (*) 3.5 ± 0.2 (*) 6.5 ± 0.8 (7)

0.261‾0.498 (0.293) (0.073) 3.0‾3.9 3.0‾3.9 5‾8 N = 82 0.261‾0.498 0.043‾ 0.116 N =17 N=17 N=17

N = 82 N = 99

tridactyla 0.050 ± 0.004 (0.052) 0.050 ± 0.004 0.007 ± 0.001 ---- 20.7 ± 1.0 (*) 20.7 ± 1.0 (*) 6.6 ± 1.0 (6) 5‾8

0.039‾0.063 (0.052) (0.008) 19.1‾22.7 19.1‾ 22.7 N =12 N = 352 0.039‾0.063 0.001‾ 0.010 N = 12 N= 12

N = 352 N = 364

Duration ranges from 0.003– 0.011 s (x = 0.007 ± 0.001; Mo = 0.007; N = 168). The Pulse Rate within pulse sections ranges from 18.5–29.4 pulses per second (x = 23.1 ± 3.0; Mo = 22.7; N = 71). Frequently, the first pulse section is cryptic and barely noticed because of its low amplitude.

Distribution and natural history. Euparkerella cryptica sp. nov. is known only from the type locality ( Fig. 8 ). Specimens were collected mainly at night. Advertisement calls were emitted more frequently just after sunset and just before sunrise. Most specimens were found covered in leaf litter on the ground, frequently at the bottom of small ravines. Although some males were observed exposed on top of the leaves or on the bare ground at the side of ravines, most males called in short choruses, hidden and dispersed across the forest (this behavior is similar in Euparkerella brasiliensis and E. cochranae [ Hepp & Carvalho-e-Silva 2011]). Frequently, specimens exhibited thanatotic behavior after jumping, remaining motionless in relaxed positions until they were captured. In captivity, frogs moved slowly in the terrarium, rarely jumping. They frequently hid inside rolled leaves. The slow motion of E. cryptica sp. nov. resembles that of the other species of Euparkerella .

Figures

FIGURE 4. Euparkerella cryptica sp. nov. from Silva Jardim, RJ, Brazil, holotype (ZUFRJ 13281, adult male, SVL 14.30 mm), in life. Frontal (A) and (B) dorsal views.

FIGURE 5. Euparkerella cryptica sp. nov. from Silva Jardim, RJ, Brazil, holotype (ZUFRJ 13281). Dorsal (A) and lateral (B) views of the head. Ventral views of the right hand (C) and foot (D).

FIGURE 6. (A – E) Euparkerella cryptica sp. nov. from Silva Jardim, RJ, Brazil. (A) Ventral view of the left hand, holotype (ZUFRJ 13281). The arrow indicates the presence of digital pad and partially overlapped subarticular tubercle. (B) Ventral view of the left hand (MNRJ 85756). The arrow indicates the presence of a single digital pad. (C) Ventral view right hand (ZUFRJ 12851). The arrow indicates the presence of a digital pad and a subarticular tubercle. (D) Ventral view of the left foot (ZUFRJ 12645). The arrow and dashed line indicate the tip of the Toe V reaching near the middle of proximal subarticular tubercle of the Toe IV. (E) Ventral view of the right foot (ZUFRJ 12852). The arrow and dashed line indicate the tip of the Toe V extending beyond the proximal subarticular tubercle of the Toe IV. (F) Euparkerella tridactyla from Santa Teresa, ES, Brazil. Ventral view of the left hand (ZUFRJ 1928). Hand greatly reduced, with triangular fingers; Finger IV vestigial; digital tubercles and pads weakly developed and planar.

FIGURE 7. (A – C) Euparkerella cryptica sp. nov. from Silva Jardim, RJ, Brazil. (A) Oscillogram, (B) audiospectrogram (C) and power spectrum of an advertisement call (ASEC 17678). Note the long duration and the presence of pulse clusters. (D – F) Euparkerella tridactyla from Santa Maria de Jetibá, ES, Brazil. (D) Oscillogram, (E) audiospectrogram (F) and power spectrum of an advertisement call (ASEC 17704). Note the long duration and high number of pulses. Audiospectrograms and power spectrums with window function Hann, amplitude logarithmic, window size 256 (B, C) and 512 (E, F) samples, overlap 99 %.

FIGURE 8. Distribution of the species of Euparkerella. Euparkerella brasiliensis (circle); E. cryptica sp. nov. (white star); E. cochranae (triangle); E. robusta (pentagon); E. tridactyla (square). White symbols represent type localities; black symbols indicate the provenances of the specimens examined from zoological collections; symbols marked with a cross indicate the provenances of the acoustically recorded specimens. The type locality of E. brasiliensis is not precisely known (Izecksohn 1988) and therefore, not shown.

Tables

TABLE 4. Numerical values οf call parameters fοr five species οf Euparkerella. Mean ± standard deviatiοn is fοllοwed by mοde in parentheses, fοllοwed by range. * mοde nοt available; - nοt applicable. Nοte that in all calls the dοminant frequency cοrrespοnds with the fundamental frequency.

. brasiliensis	DοminantFrequency (Hz) 2793.8 ± 59.3 (2812.5) 2625.0‾2812.5 N = 10	Call Duratiοn (s) 0.543 ± 0.037 (*) 0.506‾0.630 N = 10	Τοtal Number οf Pulses 9.2 ± 0.4 (9) 9‾10 N = 10	Number οf Cryptic Pulses 1.2 ± 0.4 (1) 1‾2 N = 10	Number οf Pulse Sectiοns 9.2 ± 0.4 (9) 9‾10 N = 10	Number οf Pulses Grοup 0 N = 10	Number οf Pulses per Grοup -
. cochranae	3259.6 ± 91.0 (3187.5) 3187.5‾3375.5 N = 9	0.509 ± 0.093 (*) 0.375‾0.633 N = 10	17.5 ± 1.8 (18) 14‾20 N = 10	1.4 ± 0.8 (2) 0‾2 N = 7	17.5 ± 1.8 (18) 14‾20 N = 10	0 N = 10	-
. cryptica sp. nov.	3193.5 ± 535.7 (3000.0) 2756.2‾4823.4 N = 13	4.742 ± 0.697 (5.015) 3.393‾6.184 N = 13	13.0 ± 3.0 (11) 9‾19 N = 13	1.3 ± 0.8 (2) 0‾2 N = 13	7.4 ± 1.9 (7) 5‾12 N = 13	5.5 ± 2.3 (6) 0‾9 N = 13	2.0 ± 0.0 (2) 2‾3 N = 71
. robusta	3033.1 ± 95.3 (3000.0) 2906.2‾3187.5 N = 17	1.700 ± 0.200 (*) 1.300‾2.200 N = 17	5.8 ± 0.8 (6) 5‾8 N = 17	0 N = 17	5.8 ± 0.8 (6) 5‾8 N = 17	0 N = 17	-
. tridactyla	2648.5 ± 53.5 (2670.1) 2584.0‾2756.2 N = 12	1.468 ± 0.141 (*) 1.240‾1.711 N = 12	30.3 ± 2.5 (28) 27‾34 N = 12	1.4 ± 2.5 (1) 1‾2 N =12	30.3 ± 2.5 (28) 27‾34 N = 12	0 N = 12	-