A new species of the highland frog genus Holoaden (Amphibia, Strabomantidae) from cloud forests of southeastern Brazil Author Martins, Itamar A. Author Zaher, Hussam text Zootaxa 2013 3599 2 178 188 journal article 10.5281/zenodo.222736 59197a35-ca2a-4ed2-8a1b-f756ce67e1c5 1175-5326 222736 B04BEFE6-86E0-4F43-A578-DAEFCA7FCDB6 Holoaden suarezi sp. nov. Figs. 1 A, B; 2A, B; 3A; 4A Holotype . MZUSP 131872, adult female collected at Estação Ecológica de Bananal ( 22° 47’ 42” S , 44° 21’ 36” W , 1220 m above sea level), municipality of Bananal, State of São Paulo, Brazil , on 18 December 2003 by H. Zaher, A. P. Suarez, E. A. Domenico, T. Camolez, R. Clemente, R Masiero, and P. Nunes. Paratypes . MZUSP 23794, adult female collected at Estação Biológica de Boracéia ( 23° 38’ S , 45° 52’ W ), municipality of Salesópolis, State of São Paulo, on 23 March 1963 by A. S. Rand and P. Rand. MZUSP 94415, an adult male collected at Campo de Fruticultura da Bocaina (presently known as Ponte Alta, inside of Parque Nacional da Serra da Bocaina) ( 22° 42’ S , 44° 38’ W ), Municipality of São José do Barreiro, state of São Paulo, on 0 3 November 1965 by W. C. A. Bokermann (ex WCAB 37146); MZUSP 138348, adult male collected at Estação Biológica de Boracéia ( 23° 38’ S , 45° 52’ W ), Municipality of Salesópolis, State of São Paulo, Brazil , on 0 6 November 2003 by M. T. Rodrigues, V. Verdade, and M. C. Lange. Diagnosis . Holoaden suarezi can be recognized by the following combination of characters: (1) a moderate body size (female 42.6–44.2 mm SVL; male 37.2–38.5 mm SVL) indicating sexual dimorphism in size; (2) dorsum and head textures densely glandular (macroglands), with glands reaching the internasal region; (3) thigh and tibia with glandular texture; (4) forearms long and very slender; (5) legs and toes long and slender; (6) toe tips rounded, fingers not webbed nor fringed; (7) few supernumerary tubercles on the palmar region, (8) outer metatarsal tubercle elliptical, small; (9) texture of outer tarsal and sole of foot smooth; (10) iris black in living specimens; (11) tympanic membrane poorly or not visible. Comparisons with other species . Holoaden suarezi differs from H. bradei by a larger body size ( Holoaden suarezi = males 37.2–38.5 mm SVL; females 42.6–44.2 mm SVL; H. bradei = males 10.1–28.4 mm SVL; females 26.4–36.8 mm SVL) ( Table 1 ), longer limbs ( Holoaden suarezi = forearms 11.2–12.2 mm and 13.0– 13.1 mm , thighs 17.8–18.0 mm and 19.7–19.9 mm , tibia 16.9–17.7 mm and 18.3–18.7 mm in males and females, respectively; H. bradei = forearms 2.2–6.7 mm and 5.3–7.5 mm , thighs 4.3–11.9 mm and 5.9–12.1, tibia 3.6–10.9 mm and 6.0– 12.1 mm in males and females, respectively) ( Table 1 ), and a uniformly dark brown coloration (upper surface of dorsum olive brown with irregular and dispersed black marks in H. bradei ). Holoaden suarezi differs from H. luederwaldti by an uniformly dark brown coloration (dorsal surface brown to dark purple-brown or redbrown and ventral surface cream in H. luederwaldti ), longer forearms, thighs, and tibia ( Holoaden suarezi = forearms 11.2–12.2 mm and 13.0– 13.1 mm , thighs 17.8–18.0 mm and 19.7–19.9 mm , tibia 16.9–17.7 mm and 18.3–18.7 mm in males and females, respectively; H. luederwaldti = forearms 7.9–11.6 mm and 9.1–12.1 mm , thighs 11.7–17.5 mm and 15.5–18.2 mm , tibia 8.0–17.0 mm and 10.2–17.2 mm in males and females, respectively) ( Table 1 ), a longer length of the head that corresponds to 79% of its width (65% of head width in H. luederwaldti ), and a black iris coloration in live specimens (brown iris in H. luederwaldti ). Holoaden suarezi differs from H. pholeter an uniformly dark grey ventral surface of the body (ventral surface of the body dark brown with a light abdominal blotch of variable size in H. pholeter ) ( Fig. 1 ), dense glandular granules on the dorsal surface of the head and body that extend to the internasal region (glandular granules extend to the inter-orbital region in H. pholeter ), thigh and tibia also covered by glandular granules (thigh and tibia smooth in H. pholeter ) ( Fig. 1 ), a distinct and strait canthus rostralis (canthus rostralis weakly marked and slightly concave in H. pholeter ) ( Figs. 1 and 2 ), and a shorter length of the head that corresponds to 79% of its width (94% in H. pholeter ). FIGURE 1. Dorsal and ventral views of the body: A and B, holotype of Holoaden suarezi sp. nov. (SVL 42.6 mm, MZUSP 131872) C and D, holotype of Holoaden pholeter (SVL 44.6 mm, MNRJ 51475); E and F, lectotype of Holoaden luederwaldti (SVL 40.8 mm, MZUSP 87). FIGURE 2. Dorsal and lateral views of the head. A and B, holotype of Holoaden suarezi sp. nov. ; C and D, holotype of Holoaden pholeter ; E and F, lectotype of Holoaden luederwaldti . TABLE 1. Measurements (in millimeters) of Holoaden suarezi sp. nov. , Holoaden bradei , Holoaden luederwaldti , and Holoaden pholeter (Pombal et al ., 2008) . * Measurements include juveniles that were not sexed.

H. suarezi sp nov	H. bradei	H. luederwaldti	H. pholeter
Snout-vent length	Male Female (n=2) (n=2) 37.2; 38.5 42.6; 44.2	Male Female (n=134)* (n=18) 10.1–28.4 26.4–36.8	Male Female (n=26) (n=8) 27.1–39.9 39.3–42.8	Mal Female e (1) (n=2) 41.6 44.6; 47.7
Head width	14.6; 15.9 16.5; 17.1	3.7–10.3 8.5–12.2	10.1–16.0 13.7–16.3	16.4 16.3; 19.3
Head length	13.1; 13.6 13.0; 13.1	2.7–6.9 4.6–8.3	6.6–11.0 8.3–11.3	14.7 15.2; 18.4
Eye diameter	4,6; 4.8 5.1; 5.6	1.2–3.2 2.0–3.5	4.2- 6.1 5.1–6.2	4.7 5.4; 6.6
Eye-nostril distance	3.5; 3.5 3.9; 4.2	0.7–2.0 1.2–2.6	3.0–4.4 3.1–4.5	3.7 4.6; 4.4
Inter-orbital distance	6.0; 6.4 6.7; 6.9;	1.3–5.1 4.4–5.5	7.1–11.9 7.2–10.5	4.2 5.9; 6.2
Internasal distance	2.9; 3.0 3.1; 3.3	1.0–2.4 2.1–2.8	3.6–5.1 4.4–5.2	3.1 3.6; 3.4
Arm length	8.1; 9.5 9.0; 9.4	1.8–5.6 4.1–6.6	5.7–8.4 7.1–8.8	– –
Forearm length Femur length	11.2; 12.2 13.0; 13.1 17.8; 18.0 19.7; 19.9	2.2–6.7 5.3–7.5 4.3–11.9 5.9–12.1	7.9–11.6 9.0–12.1 11.7–17.5 15.5–18.2	11.9 12.9; 12.8 17.7 19.9; 20.6
Tibia length Foot length	16.9; 17.7 18.3; 18.7 16.6; 17.5 17.9; 18.2	3.6–10.9 6.0–12.1 3.7–12.7 10.9–14.5	8.0–17.0 10.2–17.2 10.6–16.9 14.9–17.5	18.0 19.0; 19.3 17.7 17.7; 19.5
Hand length	9.2; 10.4 10.7; 10.9	2.1–7.2 4.7–7.8	6.6–11.0 9.1–11.0	11.0 11.2; 12.0

Description of the holotype . Female with oocytes in the initial stage of development; The oocytes are unpigmented; Body robust; head large, wider than long ( Figs. 1 and 2 ), head length 30% of SVL and head width 38% of SVL; head length corresponds to 79% of head width; snout nearly rounded in dorsal view and almost rounded in lateral view ( Fig. 2 A, B); nostril elliptical and slightly protuberant, directed laterally; canthus rostralis distinct, straight; loreal region concave; eye large, protruding, lateral and slightly forward, eye diameter 30% of head length; pupil round; tympanic not visible externally or poorly visible; a glandular supratympanic fold extending from the corner of the eye to the insertion of the forearm ( Fig. 2 A); tongue large; two short transverse series of vomerine teeth behind and between choanae; choanae elliptical; numerous teeth on maxilla and premaxillae; arms very slender; forearms slender; fingers long and slender, forearm length 30% of SVL; finger lengths II≤IV<I<III; hand length 24% of SVL; finger tips rounded; fingers not webbed nor fringed; subarticular tubercles single, rounded; inner metacarpal tubercle large and nearly elliptical; outer metacarpal tubercle ovoid; few supernumerary tubercles on the palmar region ( Fig. 3 A); legs long and slender, thigh and tibia length 46% and 44% of SVL, respectively; toes very long and slender, toe lengths I<II<V<III<IV; toe tips rounded, with poorly expanded disc; toes not webbed nor fringed; subarticular tubercles single, elliptical or round; inner metatarsal tubercle elliptical; outer metatarsal tubercle elliptical, small; outer tarsal and sole of foot texture smooth ( Fig. 4 A); foot length 41.6% of SVL; thigh and tibia with glandular texture; dorsal surface of head and body with glandular texture; the glandular granulation extends to the internasal region ( Fig. 2 B); arm and forearm smooth; venter smooth ( Fig. 1 A, B). Color of the holotype in preservative . Dorsal surfaces of the head, dorsum, limbs, and flanks dark brown; lateral and ventral surfaces clear brown; palmar and plantar tubercles and tips of digits light brown, similar to ventral coloration ( Figs. 1–4 ). Measurements of the holotype . SVL 42.6; HL 13.1; HW 16.5; ED 5.1; IOD 6.7; END 3.9; IND 3.1; AL 9.4; FAL 13.0; HAL 10.7; FL 19.7; TL18.7; FOL 18.2. Color in life . Dorsal surfaces of the head, body, and limbs deeply dark brown. The glandular portion of the lateral surface dark brown; flanks and ventral surfaces of the body and limbs slightly lighter than dorsum; palmar and plantar tubercles and tips of digits light gray; eyes black ( Fig. 5 ). Variation . Males were smaller and with more robust forearms than females ( Tables 1 and 2 ). Otherwise, no conspicuous qualitative differences were found between the available specimens, which were very similar to the holotype in external morphology and color pattern. FIGURE 3. Ventral view of hands and fingers. (A) holotype of Holoaden suarezi sp. nov. ; (B) holotype of Holoaden pholeter ; (C) lectotype and (D) topotype of Holoaden luederwaldti . TABLE 2. Measurements (in millimeters) of paratypes of Holoaden suarezi sp. nov.

Male	Female
MZUSP-94415 MZUSP-138348	MZUSP-23794
Snout-vent length	38.5 37.2	44.2
Head width	15.9 14.6	17.1
Head length	13.6 13.3	13.0
Eye diameter	4.8 4.6	5.6
Eye-nostril distance	3.5 3.5	4.2
Inter-orbital distance	6.4 6.0	6.9
Internasal distance	3.0 2.9	3.3
Arm length	9.5 8.1	9.0
Forearm length	11.2 12.2	13.1
Femur length	17.8 18.0	19.9
Tibia length	16.9 17.7	18.3
Foot length	16.6 17.5	17.9
Hand length	10.4 9.2	10.9

FIGURE 4. Ventral view of feet and toes. (A) holotype of Holoaden suarezi sp. nov. ; (B) lectotype and (D) topotype of Holoaden luederwaldti ; (C) holotype of Holoaden pholeter . FIGURE 5. Living specimen of Holoaden suarezi sp. nov. (MZUSP 138348) (A) lateral, (B) ventral, (C) frontal and (D) dorsal views. Estação Ecológica de Boracéia, State of São Paulo, Brazil. Photo: Martha C. Lange. Distribution . So far, Holoaden suarezi was recorded in three localities of high altitude (between 900 and 1300 m ) in the State of São Paulo, situated in the Atlantic Forest Domain ( sensu Ab’Saber 1977) of the Serra do Mar mountain range. The three localities are situated in the municipalities of Bananal (Estação Ecológica de Bananal), São José do Barreiro (Parque Nacional da Serra da Bocaina), and Salesópolis (Estação Biológica de Boracéia) ( Fig. 6 ). Currently, Holoaden suarezi is endemic of the Serra do Mar in the State of São Paulo, and is geographically isolated from H. luederwaldti and H. bradei , which are endemic species of the Serra da Mantiqueira mountain range. Although H. pholeter also occurs in the Atlantic Forest Domain of the Serra do Mar mountain range, it is an endemic species of the Serra dos Órgãos that corresponds to a geographically isolated eastern portion of the Serra do Mar in the State of Rio de Janeiro (Pombal et al . 2008; Martins 2010 ). Etymology . A patronym honoring José Roberto Alves Suarez, Forest Ranger from the Instituto Florestal of São Paulo who dedicated most of his long-time career to the preservation of São Paulo’s high altitude Atlantic forest remnants and their fauna. Natural history . The holotype and paratype MZUSP 138348 were captured in pitfall traps during the months of highest precipitations ( November and December 2003 ). Heyer et al . (1990) mentioned that MZUSP 23794 was taken from the ground on a forest trail at night. MZUSP 23794 contained a small number of large and unpigmented eggs. Similar eggs were reported in H. bradei ( Lutz 1958 ) , H. luederwaldti ( Martins 2010 ) , and H. pholeter (Pombal et al. 2008) . Its vocalization is unknown.