Ischnocnema crassa, Silva-Soares & Ferreira & Ornellas & Zocca & Caramaschi & Cruz, 2021

Silva-Soares, Thiago, Ferreira, Rodrigo Barbosa, Ornellas, Iago Silva, Zocca, Cássio Z., Caramaschi, Ulisses & Cruz, Carlos Alberto Gonçalves, 2021, A new species of Ischnocnema (Anura: Brachycephalidae) from the mountainous region of Atlantic Forest, southeastern Brazil, with a new phylogeny and diagnose for Ischnocnema parva series, Zootaxa 5082 (3), pp. 201-222 : 204-214

Ischnocnema crassa sp. nov.

Ischnocnema aff. parva sp. 2– Ferreira et al. (2016, 2019a)

( Figs 1–4A )

Holotype. MNRJ 93647, adult male, SVL 18.6 mm ( Fig. 1 ), collected at Sítio do Sr. Darci and Nelda Cherque (19º49’27,3” S; 40º32’19,6”W, datum WGS84; 850 m above sea level), district of Nova Lombardia, municipality of Santa Teresa, state of Espírito Santo, southeastern Brazil, collected by Cássio Zocca, Fernanda C. Lirio Ferreira, Marcio M. Mageski, and Rodrigo Barbosa Ferreira, on 24 June 2013.

Paratypes. Four males and four females collected in the municipality of Santa Teresa, state of Espírito Santo, southeastern Brazil: MNRJ 93648, adult male, collected at Sítio do Sr. Paulinho (19º54’33,05” S; 40º34’53,02” W; WGS 84, 868 m a.s.l.), by Cássio Zocca, Fernanda C. Lirio Ferreira, and Rodrigo Barbosa Ferreira, on 12 September 2012 ; MNRJ 93649, subadult female, collected at Sítio dos Irmãos Picolli (19º56’7,7” S; 40º32’56,2” W; WGS 84, 865 m a.s.l.), district of Penha, by Cássio Zocca, Fernanda C. Lirio Ferreira, Gustavo Milanezi, and Rodrigo Barbosa Ferreira, on 30 October 2012 ; MNRJ 93650, adult male, collected at Sítio do Sr. Darci Cherque (19º49’27,3” S; 40º32’19,6” W; WGS84, elev. 850 m a.s.l.), district of Nova Lombardia, by Cássio Zocca, Fernanda C. Lirio Ferreira, Marcio M. Mageski, and Rodrigo Barbosa Ferreira, on 24 June 2013 ; MNRJ 93651, adult female, collected at Cachoeira Country Club (19º55’21,53” S; 40º38’03,55” W; WGS84, elev. 964 m a.s.l.), Parque Municipal São Lourenço, by Cássio Zocca, João Victor de Andrade Lacerda, Juliana Teixeira and João Pedro Kloss-Degen, on 29 June 2019 ; MNRJ 93652, adult male, and MNRJ 93653, adult female, collected at Cachoeira Country Club (19º55’20,75” S; 40º38’05,51” W; WGS84, elev. 904 m a.s.l.), Parque Municipal São Lourenço, by Cássio Zocca, João Victor de Andrade Lacerda, João Pedro Kloss-Degen, and Juliana Teixeira, on 29 June 2019 ; MBML 11847, adult male, collected at a site near Vale do Tabocas (19º56’11,1” S; 40º40’44,13” W; WGS84, elev. 876 m a.s.l.), by Cássio Zocca, João Pedro Kloss-Degen, Leonardo Nevares, and Juliana Teixeira, on 02 November 2019 ; MBML 11848, subadult female, collected at Sítio do Sr. Pedro (19º54’11,99” S; 40º38’21,41” W; WGS84, elev. 964 m a.s.l.), by Cássio Zocca, João Victor de Andrade Lacerda, Fernanda C. Lirio Ferreira, and Rodrigo Barbosa Ferreira, on 20 November 2019 .

Species Diagnosis. Ischnocnema crassa sp. nov. belongs to the Ischnocnema parva series by phylogenetic placement (see discussion), and it is diagnosed by the following combination of characters: (1) moderate size with adult males SVL 18.1–19.1 mm; adult females SVL 20.2–22.7 mm; (2) body robust with short legs, tibia length <50% SVL; (3) skin lightly rugose with small tubercles and granules sparsely distributed on dorsum and lateral surfaces; (4) head wider than long; (5) snout nearly rounded in dorsal and lateral views; (6) venter and gular region smooth; (7) vocal sac single, subgular, not expanded; (8) presence of webbing between Fingers I, II, and III; (9) Fingers I and II approximately the same size, with relative lengths I≈II<IV<III; (10) finger discs pointed, except in Finger III, which is rounded and slightly expanded; (11) single glandular-appearing nuptial pad covers dorsal surface of Finger I; (12) toes relative lengths I<II<V<III<IV; (13) calcar tubercle absent; (14) distinctive black stripe on tarsus, feet, and perianal region.

Comparisons with other species. Ischnocnema crassa sp. nov. differs from all species of Ischnocnema by the presence of webbing between Fingers I, II, and III ( Fig. 2 ; webbing absent in all other Ischnocnema ), and it also differs from most Ischnocnema species by having pointed discs of fingers I, II, and IV ( Fig. 3C ; not pointed in I. manezinho and I. sambaqui neither in the series of I. guentheri , I. lactea , and I. verrucosa ). Ischnocnema nanahallux , former member of I. parva series, however, currently unassigned to any species series, also has pointed finger discs.

Ischnocnema crassa sp. nov. is most similar to I. parva , I. pusilla , and I. nanahallux , and distinguishes by having webbing between fingers, body robust (moderate in I. parva ) and venter distinctly areolate (uniformly beige in I. parva , and with conspicuous large white blotches on a black background in I. pusilla ), absence of calcar tubercle (well-developed in I. nanahallux ), Finger I and II approximately of the same size (Finger I is shorter I. nanahallux ), disc of Finger III rounded, not pointed and slightly expanded (pointed in I. parva , I. pusilla , and I. nanahallux ). A comparison of diagnostic characters amongst species currently belonging to I. parva series is presented in Table 1 .

From species in the I. guentheri series, I. crassa sp. nov. differs by its smaller size (only overlapping the 17 mm SVL of I. oea ); shorter legs, with tibia length <50% of SVL (long legs, with tibia length>60% of SVL); head wider than long, with snout nearly rounded in dorsal view (head longer than wide, with snout acuminate in dorsal view in I. guentheri series); pointed discs of Fingers I, II, and IV (not pointed in the I. guentheri series).

From I. lactea series, Ischnocnema crassa sp. nov. differs by having head wider than long, with snout nearly rounded in lateral view (head longer than wide, with snout acuminate in lateral view in I. lactea series); by having Finger I approximately the same size as Finger II (fingers relative lengths I<II<IV<III in I. lactea series); pointed discs of Fingers I, II, and IV (discs expanded, T-shaped truncate, indented with a notch on Fingers II–IV in I. lactea series).

From the I. verrucosa series, Ischnocnema crassa sp. nov. differs by its smooth dorsum (very tuberculate in the I. verrucosa series); absence of a W-shaped mark on dorsum at the level of shoulders with one tubercle at each posterior point (present in I. verrucosa series); pointed discs of Fingers I, II, and IV (not pointed in I. verrucosa series). From I. manezinho and I. sambaqui , both species currently unassigned to any series, Ischnocnema crassa sp. nov. differs by its smaller size and by lacking a W-shaped mark on dorsum at the level of shoulders with one tubercle at each posterior point (both adults males of I. manezinho [SVL> 23 mm] and I. sambaqui [SVL> 32 mm] are larger, and with a W-shaped pattern on dorsum). Variation in size and proportions for adults are presented in Table 2 .

Description of holotype. Adult male, 18.6 mm SVL. Texture of dorsal surface of body smooth; lateral surface with few scattered granules; few small globular palpebral tubercle present; ventral surfaces smooth; discoidal fold conspicuous; two dorsal curved folds originate behind the eyes forming a dorsal stripe. Head wider than long; head width 38.5% of SVL; head length 32.8% of SVL; snout nearly rounded in dorsal and lateral views; nostrils elliptical, protruding in dorsal and lateral views, posterolaterally directed, posterior to the anterior end of the mandible; internarial distance slightly larger than eye diameter and eye to nostril distance, and 27.6% of head width; canthus rostralis distinct, curved; loreal region dorsolaterally directed, concave; eyes large, prominent, with diameter 88.5% of interorbital distance, and 26.9% of head width; tympanic membrane and annulus rounded, underneath the skin, with upper half undifferentiated; its diameter corresponds to 47% of eye diameter; supratympanic fold distinct, curved, ending before the arm insertion; white stripe containing postrictal tubercles between tympanum and arm insertion; vocal sac single, subgular, not externally expanded; vocal slits present, posterolaterally located on the mouth floor, moderately conspicuous, posterior to the tongue notch, anterolaterally directed; choanae rounded, largely apart from each other; prevomerine odontoids in two elongated dentigerous processes, twice the size of choanae, narrowly separated, between and very posterior to choanae, with five odontoids lined-up on each side; premaxillary teeth present; maxillary teeth present, small; the thick, large-sized tongue covers almost all mouth floor, notched posteriorly.

Arms short; forearm more robust and longer than upper arms; discs of Finger III rounded, slightly expanded, with grooves present distally, both indented with a notch; discs of Fingers I and II pointed; disc pads follow disc covers shape, surpassing the anterior limits of disc covers; relative lengths of Fingers I≈II<IV<III; fringes narrowly developed; broad webbing between Fingers I, II, and III, originating medially from both subarticular tubercle; webbing among other fingers absent. Finger I with a translucent or slightly whitish nuptial pad with glandular appearance; it covers all dorsal surface of the Finger I until the base of the last phalange, extending to the base of the inner metacarpal tubercles; thenar tubercle ovoid, well developed; palmar tubercle elliptical, less developed than thenar tubercle; poorly defined and irregularly shaped supernumerary globular tubercles; subarticular tubercles globular, well developed.

Legs moderately robust, small; thigh slightly smaller than tibia; sum of thigh and tibia lengths slightly smaller than SVL; tibia length 48.7% of SVL; foot not webbed, foot length 45.8% of SVL; toes narrowly fringed; toes discs conspicuously indented, pointed in toes I, II, and V, and rounded in toes III and IV. Relative lengths of toes I<II<V<III<IV; inner metatarsal tubercle well developed, elliptical; outer metatarsal tubercle conical, moderately developed; supernumerary metatarsal tubercles absent; subarticular tubercles globular or conical, well developed; no tarsal fold nor calcar tubercle present.

Color pattern ( Figs 4–5 ). Dorsum varies from light brown to dark or nut-brown. Lateral surfaces are darker, contrasting to dorsum, varying in tones according to dorsum: individuals light brown may have lateral surfaces slightly darker (MNRJ 93650–93651; Figs 5A and 5D , respectively), while individuals brown or nut-brown may have heavily dark lateral surfaces (MNRJ 93649, 93652 [ Fig. 5B ]). There may be a large triangular shaped mark on the loreal region, from eye to posterior lips. In life, iris marbled in golden, with a golden band circling the black pupil. Postrictal tubercles white. Dark interorbital bar conspicuously shown in some individuals (MNRJ 93651, 93653; Figs 5A and 5C , respectively). Bands and blotches on loreal region and dorsal surface of snout are randomly disposed and colored. Dorsum has a large band that goes from the tip of the snout to inguinal region, indenting inward behind the head. Some small white-tipped warts on lateral surfaces. Knees may present a dark blotch. Distinctive black stripe on perianal region in triangular shape. A dark stripe is also present on the posterior part of tarsus and feet. Ventral surface of belly, arms, and legs are dark black, areolate in several small golden irregular blotches on a black background.

In preservative, the background color faints varying from grayish to beige or dark brown. Ventral surfaces become opaque, maintaining areolate pattern. In general, all specimens maintained former patterns of blotches, dots, and stripes in all surfaces; iris became darker.

Variation. In general, specimens are congruent with respect to morphological characters. Color and pattern variation are described above. Nevertheless, some minor considerations regarding morphology are noteworthy, as the vocal sac in MNRJ 93648, which is somewhat externally expanded. Subadult female MNRJ 93649 has webbing between Fingers I and II reduced, but still present.

Geographic distribution. Ischnocnema crassa is known from the Reserva Biológica Augusto Ruschi (3591 hectares), Parque Natural Municipal de São Lourenço (22 hectares) and surrounding private properties in the municipality of Santa Teresa, state of Espírito Santo, southeastern Brazil ( Fig. 6 ). It occurs in montane forests with ca. 850 m elevation.

Natural History. Ischnocnema crassa is a nocturnal leaf-litter frog inhabitant of the forest interior. Two individuals were found along transects inside the forest and seven individuals were found across the 507 plots of 5 m x 5 m sampled in Santa Teresa. Nine individuals were inside the forest at 50 m (N=1), 150 m (N=1), 200 m (N=4), and 300 m (N=3) from the forest edge. No individuals of I. crassa were in the 100 plots sampled at the forest edge and in the 84 plots inside the matrix of abandoned pasture, coffee plantation, or Eucalyptus plantation, and thus the population density estimate excluded these 184 plots. By assuming the probability of detection = 1 across the used habitats (323 plots inside the forest), the estimated population density of I. crassa is 0.11 individual/ 100m 2 in Santa Teresa.

Males called during rainy nights under the leaf litter inside the forest. In a laboratory aquarium, a pair of I. crassa displayed acoustic and tactile courtship signals. During courtship on 16 July 2019, a male MNRJ 93652 (SVL 1.95 mm) vocalized by inflating the single, median and subgular vocal sac. The amplexus of I. crassa is axillary ( Fig. 4F ), similar to that reported for I. verrucosa ( Lirio et al. 2018) and I. lactea ( Silva-Soares et al. 2018) . For 10 min in amplexus, the male performed head movements by rubbing the chin from left-to-right direction on the female’s dorsum. The adult female MNRJ 93653 (SVL 22.2 mm) collected on 29 June 2019 had 13 mature eggs (xÞ= 3.0 ± 0.2, 2.4–3.1 mm) and two immature eggs. Observations of calling males, amplexus, and eggs in oviducts during May to August suggest I. crassa breeds during colder and drier season.

On the field, I. crassa displayed seven antipredator mechanisms and nine variations: camouflage (variation: background matching; Fig. 7C ), immobility ( Fig. 7A and 7C ), interrupt calling, aposematism (variation: hidden), posture (variations: body elevation [ Fig. 7B ], body inflation [ Figs 7A–B, and 7D ], death feigning, mouth gape), escape (variations: hide and jump away [ Fig. 7C ]), cloacal discharge, and aggression (variation: kick). Ischnocnema crassa camouflages on the leaf litter due to the dorsal coloration similar to a decomposing leaf ( Fig. 7A and 7C ). During our approach, a male and a female adults jumped and hid on the leaf-litter. During capture attempts, adults jumped and remained motionless on the leaf litter.Adults have contrasting coloration on venter that ranges from dark brown (male) to dark gray (female) distinctively areolate with small golden irregular blotches. During handling and manipulation, adults inflated the body, elevated the body and death feigned showing the hidden aposematism, opened the mouth, kicked with posterior limbs, and released cloacal discharge. No individual released skin secretion.

Five species co-occurred with Ischnocnema crassa within the 5 m X 5 m plots: one individual was found with Euparkerella tridactyla Izecksohn, 1988 (N=1) and Ischnocnema aff. parva sp. 1 (N=1). Another individual was found with Adelophryne glandulata Lourenço-de-Moraes, Ferreira, Fouquet & Bastos, 2014 (N=1) and Haddadus binotatus (N= 1). The other two individuals were found with A. glandulata (N= 1), H. binotatus (N= 1), I. aff. parva sp. 1 (N= 4), and I. verrucosa (N= 1). We did not observe any interspecific interaction.

Etymology. The specific epithet “ crassa ” ( crassa = fat) is a Latin name here used as an adjective in allusion to its rounded body shape in general view. Typically, Ischnocnema parva series are usually more elongated.

Common name. Due to its rounded and robust body shape of this little inhabitant of the Brazilian Atlantic Rainforest, we designate to Ischnocnema crassa the common name of “rã gordinha de Santa Teresa”, which, in English, stands for “Santa Teresa’s Chubby Rain Frog.”

Figures

FIGURE 1. Ischnocnema crassa sp. nov., holotype, adult male (MNRJ 93647; SVL 18.6 mm): dorsal (left) and ventral (right) views.

FIGURE 2. Ischnocnema crassa sp. nov.: (A) holotype MNRJ 93647 and (B) paratype MNRJ 93650 evidencing webbing between Fingers I, II, and III.

FIGURE 3. Ischnocnema crassa sp. nov., holotype, adult male (MNRJ 93647): dorsal and lateral views of head; ventral views of right hand, and left foot. Measurements: HL 6.1 mm; HW 7.2 mm; HAL 4.1; FL 8.5.

FIGURE 4. Ischnocnema crassa sp. nov., color and dorsolateral patterns in life of type series: (A) holotype adult male MNRJ 93647, and paratypes (B) adult male MNRJ 93650; (C) subadult female MNRJ 93649; (D) adult female MNRJ 93651; (E) adult male MNRJ 93652; and (F) couple in amplex MNRJ 93651-52.

FIGURE 5. Dorsal and ventral color patterns of Ischnocnema crassa sp. nov. paratypes in preservative: (A) adult female MNRJ 93651; (B) adult male MNRJ 93652; (C) adult female MNRJ 93653; (D) adult male MNRJ 93650; (E) adult male MNRJ 93648; and (F) subadult female MBML 11848.

FIGURE 6. Distribution of Ischnocnema crassa (stars): holotype (yellow star) and paratypes (unfilled stars). Closely related species: Ischnocnema pusilla (circle), I. parva (cross), and I. nanahallux (triangle).

FIGURE 7. Ischnocnema crassa sp. nov. displaying antipredator mechanisms: (A) body inflation; (B) body elevation; (C) hiding and; (D) death feigning and body inflation with hidden aposematism.