Crossodactylodes itambe, Barata, Izabela M., Santos, Marcus T. T., Leite, Felipe S. F. & Garcia, Paulo C. A., 2013

Barata, Izabela M., Santos, Marcus T. T., Leite, Felipe S. F. & Garcia, Paulo C. A., 2013, A new species of Crossodactylodes (Anura: Leptodactylidae) from Minas Gerais, Brazil: first record of genus within the Espinhaço Mountain Range, Zootaxa 3731 (4), pp. 552-560 : 553-559

Crossodactylodes itambe sp. nov.

Itambe’s Bromeliad Frog ( Fig. 1 )

Holotype: UFMG 11239, adult male, Parque Estadual do Pico do Itambé , 18º23'53.1''S, 43º20'39.6''W, 1921 m above sea level (a.s.l.), municipality of Santo Antônio do Itambé , State of Minas Gerais, Brazil, collected by I.M. Barata, C.M. Correia, and R. Alcântara on 13 January 2010.

Paratypes: UFMG 11236–11238, three adult females, and UFMG 11240–11242, one adult female and two juvenile males, collected by I.M. Barata, R. Alcântara, and I.P. Reis on 6 October 2011; UFMG 11244, one male (probably an adult), UFMG 11243 and UFMG 11245, two adult female, collected by I.M. Barata, and M. Viotti on 15 February 2012; UFMG 11246–11247 one male and one female; UFMG 11248, a female collected by I.M. Barata, and R. Alcântara on 0 1 September 2011; UFMG 13375–13387, five adult males, seven adult female and one juvenile, collected by M.T.T. Santos, P.C. Rocha, and L. O. Drummond on 20–21 November 2012, all collected at the type-locality between 18º23'55.7''S, 43º20'26.5''W and 18º23'56.6''S, 43º20'54.8''W, ranging from 1836–2060 m a.s.l.

Diagnosis. Following Cochran (1938, 1955) and Lynch (1971), we allocated the new species in the genus Crossodactylodes , by the following combination of characters: 1) head and body flattened; 2) tympanum absent; 3) males with cluster of spines on thumbs; 4) first finger shorter than second; 5) fingers and toes without web or fringes; 6) discs on fingers II–IV and toes moderately expanded; 7) life cycle in bromeliads. Additionally, the new species is diagnosed by: 8) snout short, rounded in dorsal view, sloping in lateral view; 9) vocal sac and vocal slits absent in males; 10) vomerine teeth absent; 11) males with upper arms and forearms hypertrophied; 12) cloacal flap prominent, simple; 13) dorsal skin coarsely granular.

Comparison with other species. Crossodactylodes itambe sp. nov. can be separated from C. izecksohni by its slightly larger size (SVL males 11.8–14.3 mm, n = 18; SVL females 11.2–13.7, in C. izecksohni ; SVL males 14.0– 17.6 mm and SVL females 13.5–18.0 mm, in Crossodactylodes itambe sp. nov.), and absence of marks on the dorsal surface of the hands and body (presence of X mark on dorsum and brownish transversal bands on hands in C. izecksohni ). Thumb is robust in C. izecksohni males and slightly less robust in Crossodactylodes itambe sp. nov. males. Inner metacarpal tubercle is lateral and developed on C. izecksohni and weakly developed on Crossodactylodes itambe sp. nov. Hand length proportions of Crossodactylodes itambe sp. nov. are larger (HAL/ SVL males 0.27–0.33 mm, mean 0.29, n=10; HAL/SVL females 0.26–0.31 mm, mean 0.27, n=15) when compared to C. izecksohni (HAL/SVL males 0.23–0.25 mm, mean 0.24 mm, n=18; HAL/SVL females 0.20–0.24 mm, mean 0.23, n=24). Iris is yellow with reticulate brown pattern and separated by a brown horizontal line in the base of the pupil in C. izecksohni , and differs from iris completely black in Crossodactylodes itambe sp. nov.. Crossodactylodes itambe sp. nov. differs from C. pintoi by the absence of vocal sac and simple cloacal flap (median subgular vocal sac and bilobed cloacal flap in C. pintoi ; Peixoto 1982). Crossodactylodes itambe sp. nov. differ from C. bokermanni by the absence of vocal sac and vocal slit (present in C. bokermanni ), discs on finger and toes sizes moderately expanded (expanded in C. bokermanni ), dorsal skin of body coarsely granular (smooth in C. bokermanni ), absence of vomerine teeth (present in C. bokermanni ), and absence of marks on the dorsal surface of the legs and body (presence of marks on dorsum and dark transversal bands on legs in C. bokermanni ). Thumb is robust in Crossodactylodes itambe sp. nov. males when compared to discrete enlargement of thumb in C. bokermanni males.

Description of the holotype. UFMG 11239, adult male, SVL 17.0 mm ( Fig. 1 ). Head 1.1 times wider than long (HW/HL); head width is one quarter of snout vent length (HW/SVL=0.4); and head length 0.4 SVL (HL/ SVL). Head flat. Snout short, rounded in dorsal view, sloping in lateral view. Canthus rostralis indistinct. Loreal region slightly concave. Nares protuberant, directed laterally. Eye prominent, antero-laterally oriented, its diameter 0.3 times head length. Tympanum absent. Vomerine teeth indistinct. Choanae rounded, separated by a distance larger than five times maximum diameter. Tongue not notched, attached overall, narrowly free around lateral and posterior margin, medium-sized, occupying half of oral cavity. Vocal slits absent; vocal sac indistinct. A single, small toothlike process in front of lower jaw, with socket in between premaxillae. Low elongated tubercle on upper eyelid margin. Arms robust and forearms hypertrophied. Fingers with elliptical discs, slighting expanded. Relative lengths of fingers I <II <IV<III. Fingers not webbed, with a few developed dermal fringe. Subarticular tubercles rounded; two tubercles on fingers III and IV, absent on fingers I and II. Outer metacarpal tubercles large and rounded; inner metacarpal tubercle weakly developed. Cluster of 16 spines on right and left thumbs. Tibia length 0.4 SVL; foot length 0.4 SVL. Inner metatarsal tubercle distinct, elliptical; outer metatarsal tubercle small and conical. Toes relative length I <II <III ≈ V <IV; disc width V <I <II ≈ III ≈ IV. Subarticular tubercles distinct, rounded, large and flat; three on fingers V, III, and IV, one on fingers II and I. Cloacal opening directed posteriorly at level of thighs; cloacal flap present. Dorsal and ventral skin granular; chest and gular region smooth. Pectoral fold absent.

Color of the holotype in preservative. Dorsum and venter are dark gray with no distinguished marks.

Measurements of the holotype (mm). SVL 17.0; HL 6.2; HW 7.1; ED 1.8; END 1.4; NSD 1.1; IND 1.3; EW 1.4; AMD 3.4; FAL 3.6; HAL 4.8; 3FD 0.7; THL 6.7; TBL 6.2; TAL 3.9; FL 6.0; 4TD 0.7; FAB 1.8.

Variation. The type-series includes 15 adult females and 10 adult males. Males and females are distinguished by the presence of spines on males’ thumbs, which varies in number and aggregation: large adult males have clustered spines and smaller adult males (probably juveniles) have few isolated spines. Spines on males’ thumb on Crossodactylodes itambe sp. nov., varies from 6̶16 spines by thumb, which is similar to C. izecksohni , 3–12 spines and C. bokermanni , 3–8 spines (Peixoto 1982). We examined the gonads of six males and four females, all males possessing spines on thumbs. Crossodactylodes itambe sp. nov. seems not to have sexual dimorphism in SVL (males 16.2 ± 1. 3; females 16.2 ± 1.0), but males have forearms more robust than females (FAB/FAL 0.48– 0.69 in males; FAB/FAL 0.34–0.46 in females; Table 2 ). All adults are similar in coloration varying the presence of a light brown rectangle shape at the dorsum, but there is no color distinguishing between sexes. Color in preservative varies from dark gray to black.

Color in life. Dorsum and venter are dark to light brown. During daylight specimens are dark brown (sometimes even black) and color pattern is uniform ( Fig. 2 A). At night specimens are light brown, with variable pattern which includes darker marble marks on dorsal surface of arms and legs and a dorsal light brown rectangle shape in some specimens. When exposed to flashlight a variable number of small white spots are apparent and spread in the dorsum, arms, and legs of some specimens, and these white spots are quite imperceptible when examined without accuracy. Palmar and plantar surfaces of hand and foot are darkly pigmented. Iris black.

Etymology. The specific epithet itambe , derives from the type-locality were individuals were collected at Parque Estadual do Pico do Itambé , municipality of Santo Antônio do Itambé , within the Espinhaço Range, State of Minas Gerais. The Itambé summit is the highest point at the Espinhaço Range in the State of Minas Gerais (2062 m a.s.l.), and from the Tupi-Guarani language Itambé means “sharp rock”. The epithet is noun in apposition.

Geographic Distribution. Crossodactylodes itambe sp. nov. is known only from type-locality, in Itambé summit, within the Pico do Itambé State Park, at the municipality of Santo Antônio do Itambé , state of Minas Gerais, Southeastern Brazil. Crossodactylodes itambe sp. nov. extends the genus distribution for about 325 km northwest from where it was currently known ( Fig. 3 ).

Natural history. Crossodactylodes itambe sp. nov. occurs in high-elevation (in altitudes ranging from 1836– 2062 m a.s.l.) rocky mountain meadows called campos rupestres (Rapini et al. 2008), a typical phytophysiognomy of the Espinhaço Range. Individuals of the new species were found in open field (exposed to the sun) rupicolous bromeliads. The species is active by night and most individuals were found during this period inside bromeliads’ tanks and leafs usually with half of their body inside the water line. No records were made inside dry bromeliads. Despite our efforts we did not hear species vocalizations, if there is any (males do not have vocal slits). To date, no Crossodactylodes species have been registered in vocal activity despite C. pintoi and C. bokermanni have vocal slits. Considering monthly field samples done from January and October 2011 (except April and July) Crossodactylodes itambe sp. nov. was found in every sampled month except in May and August, but was most abundant in September and October 2011 (61.3% of 235 records). Egg masses contained only one egg ( Fig. 2 B), and were laid attached to lateral leaves of bromeliad tanks, at the water level. Clutches were found in February and November 2012.

Four species of Crossodactylodes are known to date: Crossodactylodes pintoi , C. bokermanni , and C. izecksohni occur in forested habitats located in the coastal mountains of the States of Rio de Janeiro (Serra do Mar) and Espírito Santo. Crossodactylodes itambe sp. nov. is the only one which occurs in open field habitats (campos rupestres), in very high altitudes of a non-costal mountain range (the Espinhaço Range). Because of its distance to the ocean and its proximity to the savanna-like Cerrado biome, the Espinhaço Range is likely drier and more seasonal than the coastal mountains of eastern Brazil. However, the Itambé summit with its 2062 m a.s.l. acts as a barrier blocking Atlantic moisture-laden winds, making it one of the wettest part of the Espinhaço Range (Leite 2012). The orographic effects lead to enhanced rainfall amounts and to thick banks of orographic fog that cover the upper parts of the Itambé summit for much of the year, even during seasonal drought (from April to September), providing the humid microclimate required by Crossodactylodes species, which are always associated to highly humid areas of eastern Brazil.

Conservation. If considered the total area above 1800 m a.s.l. of the Itambé summit Crossodactylodes itambe sp. nov. would have an extent of occurrence (EO, sensu IUCN 2001) smaller than ca. 0.5 km 2. However, the species EO is fully located within the Pico do Itambé State Park a small (4,696 ha) strictly protected reserve (equivalent to IUCN categories I and II; IUCN 1994). Anthropogenic fires, grazing, and selective removal of plant species with economic value (including bromeliads) are the main potential threats to Crossodactylodes itambe sp. nov. These impacts are not expected to be extirpated but are likely to be avoided since the creation of the reserve in 1998. Even with the mentioned pre and post reserve potential negative impacts, Crossodactylodes itambe sp. nov. was found relatively easily and in a high abundance (n = 78 in September; n = 66 in October, during one night survey). Even though the current scenario suggests a stable population trend, species with very small ranges are expected to be more vulnerable to adverse natural events and anthropogenic activities and therefore most prone to extinction, stressing the need of protection of its habitat.

Based on the insular pattern of distribution of some Espinhaço Range endemic anurans and the degree of isolation of its highland islands Leite et al. (2008) hypothesized that the inventory of the unexplored isolated plateaus and summits of this mountain range would lead to the discovery of new narrowly endemic species. The recent description of the narrowly endemics Bokermannohyla sagarana from Serra do Cabral, State of Minas Gerais (Leite et al. 2011), B. flavopicta which is restricted to the highlands of southwestern Chapada Diamantina, State of Bahia (Leite et al. 2012), and Crossodactylodes itambe sp. nov. (present study) corroborate the importance of the highlands to the diversification and conservation of the Brazilian biota.

Remarks. Until recently there was no cladistics analysis including the genus Crossodactylodes . Thereby, Frost et al. (2006) based on Lynch (1971), included Crossodactylodes in the tribe Cycloramphini of Cycloramphidae , while Pyron and Wiens (2011) left Crossodactylodes as genera incertae sedis within Hyloidea. For the first time Fouquet et al. (2013), included the genus in a cladistics analysis, and Crossodactylodes was unambiguously grouped with Rupirana , Paratelmatobius and Scythrophrys . For this clade the authors introduced the new nomen Crossodactylodinae , but as explained by Dubois (2013) this nomen is a junior synonym of Paratelmatobiinae Ohler & Dubois, 2012. Fouquet et al. (2013) also present a new species, not yet described, of Crossodactylodes occurring in Southern Bahia.

Figures

FIGURE 1. Holotype of Crossodactylodes itambe sp. nov., UFMG 11239, adult male from Parque Estadual do Pico do Itambé, municipality of Santo Antônio do Itambé, State of Minas Gerais, Southeastern Brazil. SVL 17.0 mm. (A) body in dorsal and (B) ventral views (horizontal line equals 5, 0 mm), (C) head in lateral view (scale 2.0 mm), and (D) details of the left hand and the left foot in ventral view (scale 2.0 mm). (photos: B. Fehlberg; M. T. Santos).

FIGURE 2. Paratype UFMG 13384 of Crossodactylodes itambe sp. nov. (A) living adult male and (B) egg clutch attached to a bromeliad from Parque Estadual do Pico do Itambé, municipality of Santo Antônio do Itambé, State of Minas Gerais, Southeastern Brazil. (photos: L. O. Drummond; M. Viotti).

FIGURE 3. Geographic distribution of Crossodactylodes itambe sp. nov. from Parque Estadual do Pico do Itambé, municipality of Santo Antônio do Itambé, State of Minas Gerais, Southeastern Brazil. Star, C. itambe sp. nov., cross, C. pintoi; close circle, C. bokermanni; and black and white circle, C. bokermanni and C. izecksohni.

Tables

TABLE 2. Measurements of adult specimens (min, minimum; max, maximum; and mean, in mm) of Crossodactylodes itambe sp. nov., type-series from Parque Estadual do Pico do Itambé, municipality of Santo Antônio do Itambé, Espinhaço Range, State of Minas Gerais, Southeastern Brazil. (see Materials and methods for abbreviations).

Measurements	Males (n = 10)		Females (n = 15)
	Min Max	Mean	Min Max	Mean
HL/SVL	0.36 0.40	0.38	0.36 0.40	0.37
HW/SVL	0.38 0.44	0.41	0.37 0.44	0.40
FAL/SVL	0.20 0.25	0.22	0.20 0.24	0.22
HAL/SVL	0.27 0.33	0.29	0.26 0.31	0.27
THL/SVL	0.37 0.46	0.41	0.38 0.44	0.40
TBL/SVL	0.37 0.45	0.39	0.36 0.40	0.38
TAL/SVL	0.22 0.25	0.23	0.21 0.24	0.23
FL/SVL	0.34 0.40	0.36	0.33 0.38	0.35
FAB/SVL	0.10 0.14	0.12	0.08 0.10	0.09
FAB/FAL	0.48 0.69	0.56	0.34 0.46	0.39
HW/HL	1.01 1.14	1.08	1.04 1.12	1.06
ED/HL	0.25 0.30	0.28	0.24 0.31	0.29
END/HL	0.22 0.26	0.23	0.20 0.24	0.23
NSD/HL	0.15 0.18	0.17	0.16 0.19	0.17
IND/HL	0.19 0.23	0.21	0.19 0.23	0.21
EW/HL	0.19 0.23	0.21	0.18 0.24	0.21
AMD/HL	0.53 0.60	0.56	0.52 0.59	0.55
3FD/HAL	0.13 0.15	0.13	0.12 0.17	0.14
4TD/FL	0.10 0.13	0.12	0.10 0.14	0.12
4TD/3FD	0.97 1.22	1.08	0.94 1.33	1.12