Zootaxa, Diversity of small Amazonian ...

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ISSN 1175-5326 (print edition)

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ZOOTAXA

Diversity of small Amazonian Dendropsophus (Anura: Hylidae): another new species from northern Bolivia JIŘÍ MORAVEC1,5, JAMES APARICIO2, MARCELO GUERRERO-REINHARD3, GONZALO CALDERON3 & JÖRN KÖHLER4 1

Department of Zoology, National Museum, 115 79 Praha 1, Czech Republic. E-mail: [email protected] Museo Nacional de Historia Natural – Colección Boliviana de Fauna, Casilla 8706, La Paz, Bolivia 3 Universidad Amazónica de Pando, Av. 9 de Febrero No. 001, Cobija, Bolivia. E-mail: [email protected]; [email protected] 4 Department of Natural History, Zoology, Hessisches Landesmuseum Darmstadt, Friedensplatz 1, 64283 Darmstadt, Germany. E-mail: [email protected] 5 Corresponding author 2

Abstract A new small species of Dendrospsophus is described from lowland Amazonia of the Departamento Pando, northern Bolivia. The new species is mainly characterized by smooth dorsal skin with scattered minute tubercles, relatively large distal subarticular tubercle on first toe, lack of tarsal folds, light brown to dark reddish or purple brown dorsum with numerous small dark markings and spots, dark colouration of loreal-tympanic region sharply outlined and contrasting against dorsal head colouration, one or two small white spots below the eye, yellow vocal sac in life, and advertisement call consisting of two notes with strong amplitude modulation. The new species is tentatively grouped with species placed in the Dendropsophus microcephalus group. It has rather arboreal habits and occurs in the tree canopy along swampy or flooded shores of smaller streams running through terra firme rainforest. Key words: Amphibia, Anura, Hylidae, Dendropsophus reichlei, new species, Bolivia

Introduction Small species of the hylid genus Dendropsophus may represent one of the most species-rich groups of frogs in Neotropical rainforests, including the vast lowlands of the Amazon. However, research in the last few decades have revealed that the present state of knowledge (nearly 100 known species) underestimates the actual diversity in this group, as demonstrated by the description of several new species, new country records, as well as reports of many populations with uncertain taxonomic status (e.g. De la Riva et al. 2000, Duellman 2005). The reasons for this situation are manifold, and could be summarized as follows: (a) the small size and superficial morphological similarity among species makes it difficult to reach reliable identification, particularly in preserved specimens; (b) many lowland species were described from one or very few localities only, although they are probably more widespread, and (c) the type specimens are scattered over many museum collections in America and Europe. This partly hampers necessary comparisons and consequently, several nominal taxa of small hylids were confused in the literature (e.g. De la Riva & Duellman 1997) and probably many are still. In addition, various small species of Dendropsophus seem to be highly seasonal in their activity and/or are undergoing dramatic changes in population size, being observed in hundreds of individuals at one place and then not recollected for years (own unpubl. data). This means, researchers have to be at the right place at the right time, suggesting that more species are awaiting their discovery even at “well studied” tropical sites.

Accepted by M. Vences: 16 Sept. 2008; published: 29 Oct. 2008

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One Amazonian region of apparently high diversity in Dendropsophus species is the Departamento Pando in northern Bolivia. It is situated in the south-western Amazonian basin within the zone of tall evergreen lowland rainforest and holds a species-rich amphibian fauna. The present list of anuran species of Pando comprises at least 108 species including 50 hylids (own unpubl. data). Among them are at least 19 presently known species of Dendropsophus. Field work in this area resulted in recent descriptions and new records of species in this genus (e.g. De la Riva et al. 2000, Köhler & Lötters 2001, Moravec & Aparicio 2005, Moravec et al. 2006). Despite the mentioned difficulties connected with the taxonomy of this group, we discovered another small species of Dendropsophus for which we found distinguishing characters convincing enough to describe it as new herein.

Material and methods The collected specimens were fixed and stored in 70 % ethanol. Tissue samples for DNA analyses were preserved in 99.8 % ethanol. Measurements are given in millimetres (mm) and were taken to the nearest 0.1 mm under a dissecting microscope using digital callipers. Notes on colour in life were taken from field notes and colour images. Webbing formulae follow the standards of Myers & Duellman (1982), whereas all other terminology is that of Duellman (1970). Measurement abbreviations used throughout the text are: EN, eye to nostril distance; ED, horizontal eye diameter; ELW, upper eyelid width; FL, foot length as the distance from the heel to the tip of the fourth toe; HL, head length as the straight line distance from the posterior edge of the jaw articulation to the tip of the snout; HW, greatest head width at midlevel of eyes; IOD, interorbital distance; SVL, snout-vent length; TD, horizontal tympanum diameter; and TL, tibia length. Specimens examined are listed in the Appendix. Institutional abbreviations used are those listed in Leviton et al. (1985) with the following additions and corrections: CBF, Colección Boliviana de Fauna, La Paz; NMP6V, National Museum Prague (vertebrates); and HLMD-RA, Hessisches Landesmuseum Darmstadt (reptiles and amphibians). Advertisement calls were recorded using a Marantz PMD660 compact flash recorder, a Stage Line ECM950 directional microphone, and saved on Compact Flash Type 1 SanDisk 512 MB as uncompressed files. Air temperature during recording was 24.5°C. Recordings were analyzed with the sound analysis software Cool Edit 96 (Syntrillium Software Corp.) on personal computers and were resampled at a rate of 44 kHz and 16-bit resolution. Frequency information was obtained through Fast Fourier Transformation (FFT, width 1024 points); the audiospectrogram was obtained at Hanning window function with 256 bands resolution and linear energy plot. Terminology in call descriptions follows Köhler (2000).

Results 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. GuerreroReinhard, G. Calderon and J. Moravec. Paratypes. CBF 6074–6075, NMP6V 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. GuerreroReinhard.

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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

DIVERSITY OF AMAZONIAN DENDROPSOPHUS

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(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).

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.

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).

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FIGURE 2. Adult male paratype of Dendropsophus reichlei sp. n. (NMP6V 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. (NMP6V 73618/1) from Palmira (Bolivia, Pando) in life.

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