Dendropsophus reichlei, Moravec, Ji Ř Í, Aparicio, James, Guerrero-Reinhard, Marcelo, Calderon, Gonzalo & Köhler, Jörn, 2008

Moravec, Ji Ř Í, Aparicio, James, Guerrero-Reinhard, Marcelo, Calderon, Gonzalo & Köhler, Jörn, 2008, Diversity of small Amazonian Dendropsophus (Anura: Hylidae): another new species from northern Bolivia, Zootaxa 1918, pp. 1-12 : 2-8

Dendropsophus reichlei sp. n.

Figs. 1 (A–D), 2(Α −C)

Holotype. CBF 6073, adult male, from the vicinity of the settlement of Limón, 11°44’ S, 68°34’ W, ca. 260 m a.s.l., Provincia Manuripi, Departamento Pando, Bolivia, collected on 29 November 2007 by M. Guerrero- Reinhard, G. Calderon and J. Moravec.

Paratypes. CBF 6074–6075, NMP 6 V 73617/1–2, HLMD-RA-3065, adult males, from the surroundings of the settlement San Antonio de Filadelfia, 11°18’ S, 67°23’ W, collected on 23 November 2007 by M. Guerrero-Reinhard, G. Calderon and J. Moravec.

Referred material. An adult female in a private collection of Marcelo Guerrero-Reinhard, from the vicinity of Estacion Biológica Tahuamanu, 11°24’ S, 69°01’ W, collected in 2005 by G. Calderon and M. Guerrero- Reinhard.

Diagnosis. A species of the genus Dendropsophus , based on preliminary comparisons of a sequence of the 16S rRNA gene (J. Faivovich, unpubl.), distinguished from other species of Dendropsophus by the following combination of characters: (1) small size, SVL 17.7–19.0 mm in males, 21.5 mm in female, head slightly narrower than body; (2) snout short, rounded in dorsal view, truncate in lateral view; (3) canthus rostralis distinct, rounded in cross-section; loreal region slightly concave; (4) tympanum evident, round, about one third of eye length, tympanic annulus indistinct; supratympanic fold distinct; (5) vomerine odontophores small, barely prominent, separated medially, between posterior halves of choanae; (6) skin on dorsal surfaces smooth, with minute scattered low tubercles; (7) tarsal fold and tubercles on outer edge of tarsus absent; ulnar folds and tubercles absent; (8) axillary membrane extensively developed; (9) fingers about one third webbed; toes about three fourth webbed; (10) bifid distal subarticular tubercle under fourth finger; (11) pectoral glands lacking; (12) generally, darker colouration of loreal-tympanic region contrasting to lighter dorsal head colouration, one or two small white to cream spots below the eye; (13) in life, dorsum tan to pale brown at night to reddish or purple brown by day, with numerous small irregular dark brown markings; head dark brown laterally; flanks ventrally and posteriorly translucent pink without chromatophores; hidden surfaces of thighs yellowish brown to orange brown with numerous dark melanophores; (14) in life, throat yellow; belly bright yellow in pectoral and central part, translucent pink in posterior and lateral parts; ventral surfaces of thighs translucent fleshy pink; (15) in life, iris periphery silver brown to reddish brown with dark brown mottling, inner iris dark reddish brown with darker mottling; bones white; (16) advertisement call consisting of two moderately long high-pitched notes with distinct amplitude modulation and an internote-interval of 152–163 ms; each note containing 16–29 pulses.

Comparisons. External morphology and preliminary comparisons of a sequence of the 16S rRNA gene (J. Faivovich, unpubl.) indicate that Dendropsophus reichlei is related to species currently placed in the D. microcephalus group (sensu Faivovich et al. 2005), although this species group is probably paraphyletic. Comparing external habitus, the new species is most similar to D. coffea (Köhler, Jungfer & Reichle) , D. cruzi (Pombal & Bastos) , D. juliani Moravec, Aparicio & Köhler , D. meridianus (B. Lutz) and D. minusculus (Rivero) by sharing dark loreal-tympanic region sharply outlined and contrasting against lighter dorsal head colouration. However, D. reichlei differs from these five species by exhibiting a clear white subocular spot, indistinct or absent in the mentioned species, details of ventral colouration ( Murphy 1997, Pombal & Bastos 1998, Köhler et al. 2005, Moravec et al. 2006), and mainly advertisement call characteristics (see Discussion). Dark loreal-tympanic region and a different advertisement call distinguish D. reichlei from D. joannae (Köhler & Lötters) and D. leali (Bokermann) , the former differing also by smaller size, tuberculate dorsal skin and a red inner iris in life ( Köhler & Lötters 2001). Three other small species, D. nanus (Boulenger) , D. sanborni (Schmidt) and D. walfordi (Bokermann) , differ from D. reichlei by having numerous thin brown lines on a yellowish dorsum, a longer, more pointed snout and a different advertisement call ( Martins & Jim 2003). Brazilian D. bipunctatus (Spix) and D. studerae (Carvalho-e-Silva, Carvalho-e-Silva & Izeckson) mainly differ from D. reichlei by having a loreal region with numerous white blotches ( Carvalho-e-Silva et al. 2003).

Other small Amazonian species of Dendropsophus associated with the D. microcephalus group, the weakly defined D. minimus group or not associated with any of the species groups (see Faivovich et al. 2005) include: D. aperomeus (Duellman) , D. haraldschultzi (Bokermann) , D. mathiassoni (Cochran & Goin) , D. microcephalus (Cope) (including the subspecific form D. m. miserus (Werner)), D. minimus (Ahl) , D. miyatai (Vigle & Goberdhan-Vigle) , D. rhodopeplus (Günther) , D. riveroi (Cochran & Goin) and D. tintinnabulum (Melin) . All of these species differ from D. reichlei by morphological and/or bioacoustical characters: D. aperomeus exhibits a white supracloacal stripe (Duellman 1982), lacking in D. reichlei ; D. haraldschultzi has a more slender body with thin longitudinal lines on dorsum ( Rodríguez & Duellman 1994); D. mathiassoni has a dorsum without any pattern and dorsolateral lymphatic sacs visible through the skin ( Cochran & Goin 1970); males of D. microcephalus are larger in size ( Savage 2002); D. minimus has a concealed tympanum ( Köhler & Lötters 2001, Köhler et al. 2005), D. miyatai exhibits red markings on dorsum and a pink venter ( Rodríguez & Duellman 1994); D. rhodopeplus has a yellow dorsum with red markings and a red lateral stripe (Duellman 1974); D. riveroi lacks contrasting colouration and a sharp canthus rostralis in cross-section ( Köhler et al. 2005; see also Discussion); and D. tintinnabulum has a high-pitched bell-like advertisement call ( Lutz 1973).

Species in the D. rubicundulus clade of the D. microcephalus group (sensu Faivovich et al. 2005) mainly differ from the new species by a green dorsum in life, a regular dorsal stripe pattern and longer more pointed snouts ( Napoli & Caramaschi 1998, 1999). From species of the D. decipiens clade (sensu Faivovich et al. 2005), D. reichlei differs by colour pattern and advertisement call ( Lutz 1973, Carvalho-e-Silva et al. 2003). Species of the D. minutus group (sensu Faivovich et al. 2005) differ by the presence of a white supracloacal stripe and mostly a white line on heel, lacking in D. reichlei . Members of the Amazonian D. leucophyllatus , D. marmoratus and D. parviceps species groups differ by general colour pattern, body proportions and call characters (e.g. Duellman & Crump 1974, De la Riva & Duellman 1997).

Description of holotype. Body moderately robust; head slightly narrower than body, shorter than wide, widest below eyes; snout rounded in dorsal view, truncate in lateral view; distance from nostril to eye shorter than diameter of eye; canthus rostralis distinct, rounded; loreal region slightly concave; lips slightly flared; internarial area slightly depresed; nostrils barely protuberant, directed dorsolaterally; interorbital area flat, IOD 158.9% of ELW; eye large, strongly protuberant, its diameter about four times depth of lip below eye; tympanic membrane small, round, clearly evident, its diameter about one third of eye length, separated from eye by ca.135% of its diameter; tympanic annulus distinct ventrally, indistinct anteriorly and posteriorly; supratympanic fold evident, slightly obscuring upper edge of tympanum. Arm slender, not hypertrophied; axillary membrane extending to second third of upper arm; ulnar folds and tubercles absent; fingers of medium length, bearing small, round discs; relative length of fingers 1<2<4<3; diameter of disc on third finger about the size of tympanum; subarticular tubercles small to medium sized, ovoid, distal ones of first and fourth fingers prominent, bifid in fourth finger; supernumerary tubercles barely evident; palmar tubercle medium sized, flat, elliptical; prepollical tubercle large, flat, elliptical, lacking nuptial excrescences and glands; fingers about one third webbed; webbing basal between fingers one and two; webbing formula of fingers II1 3/4—2 3/ 4III 2—2+IV. Legs moderately long, slender; heels overlapping when limbs flexed perpendicular to axis of body; tarsal fold and tarsal tubercles absent; toes moderately long, bearing round discs slightly smaller than those of fingers; relative length of toes 1<2<5<3<4; outer metatarsal tubercle small, obscure, round; inner metatarsal tubercle large, flat, elliptical; distal subarticular tubercle of the first toe large, ovoid, ca. 80% of the length of inner metatarsal tubercle, extending distally under the second phalange; remaining subarticular tubercles small, prominent, ovoid; supernumerary tubercles obscure; toes three fourth webbed; webbing formula of toes I1—2 – II1 +— 2III 1 1/4— 2IV 2—1 1/ 3V. Skin on dorsum, head, and dorsal surfaces of limbs smooth, with few scattered minute tubercles; skin on flanks smooth; skin on venter coarsely granular; skin on throat smooth; skin on lower surfaces of thighs slightly granular. Cloacal opening directed posteriorly at upper level of thighs; moderately long simple cloacal sheath covering cloacal opening; cloacal folds and tubercles absent. Tongue nearly round, slightly notched posteriorly, posterior and lateral margins not attached to floor of mouth; vomerine odontophores small, barely evident, separated medially, between posterior halves of choanae; choanae medium sized, oval; vocal slits long, extending from anterior third of lateral base of tongue to angle of jaws; vocal sac large, single, median, subgular. Measurements: SVL 18.7; HL 6.7; HW 6.8; EN 1.5; ED 2.6; TD 0.9; ELW 1.9; IOD 2.0; TL 9.6; FL 13.4.

In alcohol, dorsal surfaces of head, body, and limbs purple brown with numerous small inconspicuous scattered dark brown flecks and markings. An indistinct interorbital streak containing a round darker spot situated asymmetrically at the right upper eyelid, small dark round spot in prescapular region, and three obscure irregular dark bars on shanks are obvious. Flanks whitish; supratympanic fold dark brown; upper lip whitish, with scattered melanophores and distinct white spot below the eye; loreal-tympanic region dark brown; region around nostrils dark brown, tip of snout white with two small irregular white spots laterally; dorsal surfaces of hands, feet, and webbing covered by melanophores (melanophores reduced on inner two fingers and toes); posterior surfaces of thighs whitish with densely scattered melanophores; cloacal sheath dark brown; lower lip whitish, posterior third with scattered melanophores; throat yellowish, with several melanophores scattered anteriorly; belly, and ventral surfaces of limbs whitish; palmar and plantar surfaces covered by melanophores.

In life, dorsum reddish brown with a similar pattern of dark markings and spots as in the preserved specimen; head dark brown laterally; flanks ventrally and posteriorly translucent pink without chromatophores; finger tips yellow dorsally, hidden surfaces of thighs yellowish brown with numerous dark melanophores; throat yellow; axillar region translucent pink; belly bright yellow in pectoral and central part, translucent pink in posterior and lateral parts; ventral surfaces of thighs translucent fleshy pink; palmar and plantar surfaces yellowish, scattered with dark melanophores; iris reddish brown with dark brown mottling; bones white.

Variation. Variation of measurements of male type specimens is given in Table 1 . The single known female (referred material) has the following measurements: SVL 21.5; HL 7.1; HW 7.6; EN 1.8; ED 2.5; TD 0.9; ELW 1.8; IOD 2.5; TL 11.6. Body proportions of six adult males are as follows: HL/SVL 0.35–0.36; HW/ SVL 0.35–0.37; HW/HL 1.00–1.02; EN/ED 0.52–0.65; ED/HL 0.34–0.43; ED/HW 0.37–0.43; TD/ED 0.29– 0.37; ELW/IOD 0.77–1.00; IOD/ED 0.62–0.85; TL/SVL 0.43–0.51; FL/SVL 0.67–0.72. Photographs of the paratypes NMP 6 V 73617/1 and CBF 6074 are shown in Fig. 2 A–C. Dendropsophus reichlei exhibits considerable variation in presence of vomerine teeth. They are barely evident in the holotype and paratypes CBF 6074 and HLMD-RA-3065, but distinct in the remaining paratypes (2–4 small teeth on each vomerine odontophore). Some variation seems to be evident in the size and distinctiveness of subarticular tubercles. The length of the distal subarticular tubercle of the first toe reaches ca. 0.60 mm in holotype and paratypes NMP 6 V 73617/2 and HLMD-RA-3065 and ca. 0.45 mm in the paratypes CBF 6074–6075 and NMP 6 V 73617/1. The finger and toe webbing formulae vary as follows: II (1 2/3−2–)—(2 1/2−3) III (2)—(2−2+) IV and I (1−1 3/4)—(2–− 2) II (1−1+)—(2−−2) III (1−−1 1/4)—(2) IV (2)—(1−1 1/3) V. The axillary membrane extends along nearly the whole upper arm in CBF 6074 and NMP 6 V 73617/1–2.

General dorsal colouration in alcohol varies from light brown with purple tint to purple brown. Dorsal pattern varies mostly regarding density and distinctness of the scattered irregular small dark flecks and markings (“pepper-and-salt” pattern). A distinct dark interorbital streak and small transverse mark in scapular region is present in NMP 6 V 73617/2 and HLMD-RA-3065 (barely distinct in CBF 6074–6075 and NMP 6 V 73617/1). A more or less obvious pattern of 1-3 dark transverse bars on forearm and 3–4 transverse bars on shanks is evident in all paratypes. One distinct white subocular spot is present below the eyes of all paratypes, except CBF 6075. The latter specimen possesses a clear subocular spot below the right eye and an inconspicuous trace of a spot below the left eye. The female has two small white spots below each eye.

Vocalization. The advertisement call of well-motivated males ( Fig. 3 ) consists of two moderately long, high-pitched notes repeated in fast succession. If less motivated, males emit single notes at irregular intervals. Notes are distinctly pulsed and lack an obvious frequency modulation. Amplitude modulation within the note is emphasized with the maximum call energy occurring at its beginning followed by a rapid decrease and continuing with relatively low energy for most of the note's duration. Generally, call energy is distributed within a very wide frequency band with recognizable frequencies from approximately 2000 up to 21000 Hz. Numerical call parameters are as follows (range followed by mean ± standard deviation in parentheses): note duration, 68–112 ms (92.6 ± 13.1; n=21); inter-note interval in motivated two-note calls, 152–163 ms (n=2); pulses/note, 16–29 (23.6 ± 6.1; n=12); maximum call energy at 6212–6634 Hz (6363 ± 114; n=20); secondary frequency peaks at approximately 12400 and 19500 Hz. Calls were repeated at an approximate rate of 12–35 calls per minute, but repetition rate is highly variable and strongly depends on male motivation.

Distribution, ecology and threat status. The known range of Dendropsophus reichlei covers western and central parts of the Departamento Pando, northern Bolivia ( Fig. 4 ) and is entirely located in the southwestern Amazon basin within the zone of tall evergreen lowland rainforest. At all known localities, D. reichlei inhabited very humid swampy or flooded shores of smaller streams running through undisturbed terra firme forest. These places were densely overgrown with herbaceous plants (mostly family Araceae ), ferns and palms. Abundant herbaceous lianas climbing higher tree strata were another typical character in the D. reichlei habitat. During wet nights, unmotivated males were heard calling from the canopy of high trees. In cases of long or heavy rains, males descended to 2–4 m above the inundated ground and emitted motivated calls while hidden on horizontally oriented leafs. Density of D. reichlei was rather low, as observed local assemblages of calling males did not exceed 4–6 individuals. Other hylid species found in sympatry with D. reichlei include Dendropsophus minutus (Peters) , Hypsiboas cinerascens (Spix) , H. geographicus (Spix) , Osteocephalus buckleyi (Boulenger) , Phyllomedusa bicolor (Boddaert) , P. c a m b a De la Riva, P. vaillantii Boulenger. Reproductive mode and larvae are unknown. According to the sparse data available and its partly secretive habits, we here classify D. reichlei as “Data Deficient” according to the IUCN criteria.

Etymology. The specific name is a patronym for our colleague and friend Steffen Reichle in recognition of his important contributions to the knowledge and conservation of the Bolivian fauna and his assistance leading to the discovery of this new species.

Figures

FIGURE 1. Drawings of holotype of Dendropsophus reichlei sp. n. (CBF 6073). (A) Lateral, and (B) dorsal views of the head; (C) palmar, and (D) plantar views of left hand and foot. Scale bars equal 1 mm.

FIGURE 2. Adult male paratype of Dendropsophus reichlei sp. n. (NMP 6 V 73617 / 1) in life, (A) dorsal, and (B) ventral views. (C) Adult male paratype of Dendropsophus reichlei sp. n. (CBF 6074) in life, showing thigh and flank colouration. (D) Adult male of Dendropsophus sp. (NMP 6 V 73618 / 1) from Palmira (Bolivia, Pando) in life.

FIGURE 3. Audiospectrogram (A), corresponding waveform (B), and expanded waveform (C) of the advertisement call of Dendropsophus reichlei sp. n. Recording obtained on 29 November 2006. Air temperature 24.5 ° C.

FIGURE 4. Schematic map of northern Bolivia showing known distribution of Dendropsophus reichlei sp. n.: (1) Estacion biológica Tahuamanu, (2) Limón (the type locality), (3) San Antonio de Filadelfia.

Tables

TABLE 1. Variation of measurements (in mm) of the type series of Dendropsophus reichlei sp. n. (adult males, N = 6). See text for abbreviations.

Measurement	Mean ± SD	Range
SVL	18.6 ± 0.45	17.7–19.0
HL	6.6 ± 0.12	6.4–6.7
HW	6.7 ± 0.12	6.5–6.8
EN	1.6 ± 0.08	1.5–1.7
ED	2.7 ± 0.16	2.4–2.9
TD	0.9 ± 0.10	0.7–1.0
ELW	2.0 ± 0.15	1.6–1.9
IOD	2.4 ± 0.08	1.8–2.2
TL	9.3 ± 0.27	9.0–9.6
FL	12.9 ± 0.41	12.4–13.4