Tachiramantis, Heinicke, Matthew P., Barrio-Amorós, César L. & Hedges, S. Blair, 2015

Heinicke, Matthew P., Barrio-Amorós, César L. & Hedges, S. Blair, 2015, Molecular and morphological data support recognition of a new genus of New World direct-developing frog (Anura: Terrarana) from an under-sampled region of South America, Zootaxa 3986 (2), pp. 151-172 : 160-166

Tachiramantis gen. nov.

( Figs. 3–7 )

Type species. Eleutherodactylus prolixodiscus Lynch, 1978 (Holotype: KU 132726)

Diagnosis. Species of Tachiramantis are moderately small craugastorid frogs (SVL 20–30 mm). The head is wider than long, with a moderately pointed snout; cranial crests absent; canthus rostralis well-defined; tympanum welldefined and large, approximately 2/5 to 3/4 diameter of eye; dentigerous processes of vomers well-developed, arranged obliquely, with few teeth. Overall body form is moderately robust, with limbs of moderate length; skin on the dorsum varies from smooth to finely granular, that on the venter is smooth to areolate or granular; dorsolateral folds are poorly-developed or absent; discoidal folds are present or absent; anal sheath or cloacal folds are absent. Males have vocal slits but only some species have an external vocal sac; nuptial pads are present in at least some species. Digits bear pads which are moderately dilated; digital fringes narrow or absent; circumferential grooves present; webbing is absent. Finger I is shorter than Finger II, Finger IV is much shorter than Finger III, and Toe III is shorter than Toe V. Tarsal folds present or absent; the inner metatarsal tubercle is larger than the outer, metacarpal tubercles are small. The color pattern is variable but usually includes white spots on the posterior surfaces of the thighs. In skull, the frontoparietals are fused to the prootics; a large fontanelle exists between posterior (not anterior) portions of frontoparietals in at least one species; vomers are strongly-developed and nearly surround choanae; the parasphenoid is broad, does not narrow anteriorly, reaches palatines, and has alary processes angled slightly backward obliquely. There are eight presacral vertebrae; no vertebrae are fused and neural spines are absent. Terminal phalanges are conical with minute, delicate T-shaped tips; intercalary elements on digits are absent.

Content. Tachiramantis prolixodiscus ( Figs. 3–7 ), T. douglasi (Lynch) , T. lentiginosus ( Fig. 3 ).

Distribution. Known from both sides of the Táchira depression in the Cordillera de Mérida of Venezuela and adjacent portions of the Cordillera Oriental in Colombia ( Fig. 8 ). Tachiramantis prolixodiscus has also been reported from the Sierra de Perijá along the Venezuela-Colombia border ( Barrio-Amorós et al., 2010).

Etymology. Tachira refers to the Táchira depression, which lies between the Andean ranges in which all referred species occur. The word Táchira is ultimately derived from the Timoto-Cuica word tachure, which refers to a medicinal plant that grows in this region. The word mantis, from Greek, means treefrog. The name is masculine.

Remarks. In external morphology Tachiramantis can be readily distinguished from most craugastorid genera ( Hedges et al. 2008) by the combination of having a broad head, well-developed tympanum, and expanded digital tips with pads separated by circumferential grooves. Among craugastorid genera sharing these characteristics, Noblella differs from Tachiramantis in lacking dentigerous processes of the vomers and having terminal phalanges minimally expanded, and the genera Yunganastes and Strabomantis differ from Tachiramantis in having Finger I longer than Finger II and Toe III longer than Toe V. In addition, Strabomantis species are typically large (SVL 30– 106 mm), heavy-bodied, and have cranial crests.

As might be expected given the constituent species were previously placed in Pristimantis , there are no obvious external characteristics that universally distinguish Tachiramantis from Pristimantis . However, compared to the ~25 recognized Pristimantis occurring in adjacent regions of Venezuela and Colombia, Tachiramantis does differ from most in having finger IV much shorter than (about 2/3 the length of) finger III. The lack of welldeveloped dorsolateral or pre-cloacal folds, lack of cranial crests, presence of vocal slits, and lack of extremely expanded digital discs distinguishes Tachiramantis from most other Pristimantis in adjacent Venezuela and Colombia except for P. melanoproctus (Rivero) , P. monodolfi (Rivero) , P. ni c ef o r i, and P. tubernasus .

Osteological characters more readily distinguish Tachiramantis from Pristmantis and other terraranan genera ( Figs. 5–7 ; see morphobank project for data matrix). Most notably, investigation of the osteology of T. prolixodiscus revealed a suite of characters that are rare or absent in Pristimantis : presence of a posterior frontoparietal fontanelle ( Fig. 5 A), frontoparietal-prootic fusion ( Fig. 5 A), parasphenoid shape (broad, does not narrow anteriorly, and reaches forward to level of palatines; Fig. 5 B), and vomers that nearly surround the choanae ( Fig. 5 B). The large fontanelle between the posterior portions of the frontoparietals was not otherwise observed in a sampling of 45 Pristimantis species and only occurred in one of 53 other sampled terraranans ( Elutherodactylus intermedius ). In other terraranans characterized by the presence of a frontoparietal fontanelle, such as species in the Pristimantis orcesi group ( Guayasamin 2004b), the opening is between the anterior portions of the frontoparietals. A brief description of the cranial osteology of Eleutherodactylus chlorosoma (= T. prolixodiscus ) by Rivero (1984) states that there is no frontoparietal fontanelle. However, this statement apparently only refers to a typical anterior opening: the same description states that the rear of the skull is shrunken (“apergaminado”), exposing parts of the telencephalon and optic lobes of the brain, the same region of the brain left uncovered by the fontanelle we observe in specimen KU 132729.

The other three skull characters listed in the preceding paragraph are all shared with Tachiramantis douglasi , which occurs sympatrically with T. prolixodiscus in Colombia. Vomers that nearly surround the choanae were not otherwise documented in Pristimantis , and among all Terrarana were observed in only three species of Eleutherodactylus (subgenus Euhayas). The paraspenoid shape shared by T. prolixodiscus and T. douglasi is found in only one sampled Pristimantis : P. tayrona . This species from the Sierra Nevada de Santa Marta is externally similar to and was confused with T. prolixodiscus until being named by Lynch and Ruiz-Carranza (1985), but given differences in vomer shape and lack of frontoparietal/prootic fusion, we refrain from referring P. tayrona to Tachiramantis at this time. Fusion of the frontoparietal and prootics occurs in Pristimantis , but more rarely than in other terraranan genera, as only seven of 45 Pristimantis show this condition. In combination, these three skull characters distinguish Tachiramantis from all other sampled terraranans. The terminal phalanges of T. prolixodiscus also differ from the typical T-shaped condition described for most Pristimantis and other terraranans: rather than narrowing gradually from the proximal to distal end before broadening at the terminal expansions, the phalanges narrow dramatically before broadening at the delicate terminal expansions, such that the overall width of the terminal expansions of each phalanx is less than the width of the base of the phalanx ( Fig. 7 ). Assuming the genus-level phylogeny of Terrarana presented in Fig. 2 , fusion of the frontoparietals to the prootics and vomers that nearly surround the choanae are unambiguous osteological synapomorphies for Tachiramantis . The parasphenoid shape characters are not synapomorphic of Tachiramantis , although they do serve to distinguish the genus from Pristimantis . The shape of the terminal phalanges may represent an additional osteological synapomorphy, but requires additional investigation for confirmation. None of the examined external morphological characters represent unambiguous synapomorphies.

Several other Pristimantis species, in addition to P. tayrona , have at one time or another also been considered closely related to species we refer to Tachiramantis . Rivero (1984) suggested a close relationship between T. prolixodiscus (includes synonym Eleutherodactylus chlorosoma Rivero ) and the externally similar, sympatric species P. tubernasus (Rivero) (includes synonym Eleutherodactylus pulidoi Rivero ). A close relationship between these two species was argued against by Lynch (2003), who considered their similar morphologies to be adaptations for living in bromeliads, and justified treating them as not closely related based on the two species having differently-shaped tympani. Rivero (1984) also recognized a lentiginosus complex, including the species P. melanoproctus (Rivero) , P. mondolfii (Rivero) , and P. vanadise (La Marca) , based on all four species having a color pattern that includes white spots on the rear of the thighs ( T. douglasi also shares this pattern); subsequent genetic and morphological data show that P. vanadise , at least, is not closely related to Tachiramantis ( Barrio-Amorós et al. 2013) . While we have no genetic or skeletal data for melanoproctus or mondolfii , they bear a striking external resemblance to T. lentiginosus . We suspect both species are referable to Tachiramantis , but refrain from making this change until molecular or osteological data become available.

Osteology of Tachiramantis prolixodiscus . The skull of T. prolixodiscus ( Fig. 6 ) is broad, with the length of the skull only 86% the greatest width of the skull. The skull narrows quite gradually anteriorly, with the head width at the level of the palatines being 91% the width at the level of jaw articulation. The rostrum is short (27% of skull lenth), which, in combination with the skull’s width, gives an overall blunt appearance.

The braincase combines well- and poorly ossified elements. The anterior portion of the braincase is fully enclosed by the sphenethmoid, which broadly overlaps the frontoparietals and nasals dorsally and the parasphenoid ventrally, but only extends posteriorly to approximately the level of the midpoint of the orbit, resulting in enlarged optic fenestrae. The posterior portion of the braincase is also fully enclosed, by the fused prootics and exoccipitals. These, in turn, are fused to the frontoparietals. The frontoparietals are relatively large, and narrowly separated anteriorly; there is a broad, non-ossified fontanelle between the posterior third of the frontoparietals, leaving the optic tectum of the brain exposed. At the floor of the braincase, the parasphenoid is large and quite broad. Anteriorly, it does not narrow appreciably and reaches to the level of the palatines. Posteriorly, the alary processes are well-developed, and directed somewhat posteriorly at an oblique angle.

The nasals are large, nearly triangular in shape, and narrowly separated from one another and from the robust pars facialis of the maxillae. The maxillae broadly articulate with the quadratojugal, and bear large, peglike teeth. The premaxillae bear a small number (7) of similarly-shaped teeth; vomerine teeth are also few in number. The vomers themselves are large with broad pre- and post-choanal processes that combine to almost fully enclose the choanae. In contrast, the dentigerous processes of the vomers are relatively narrow, though elongate. The palatines are long, narrow, and pointed, and angled posteriorly, terminating adjacent to the dentigerous processes of the vomers. The pterygoids are triradiate, each with a long, thin anterior ramus articulating with the maxilla just anterior to the level of the midpoint of the orbit, a short, stout medial ramus broadly articulating with the prootic, and a more gracile, short posterior ramus articulating with the squamosal. Each squamosal is itself robust, with a long, narrow, pointed zygomatic ramus, and a similarly-shaped otic ramus that deflects medially but remains quite distant of the prootic. In the mandible, the angulosplenials are very well-developed and sigmoidal in shape, articulating broadly with the relatively small dentaries anterior of the level of the orbits and are only narrowly separated from the mentomeckelian bones. The only ossified portions of the hyoid apparatus are the two posteromedial processes, which are slightly expanded anteriorly and posteriorly and are moderately separated from one another at their anterior ends.

There are eight presacral vertebrae, none of which are fused. All presacral vertebrae save the atlas have welldeveloped transverse processes; those on vertebrae 4–6 are deflected posteriorly. Transverse processes on vertebrae 4–8 are similar in size, with those on vertebra 3 being larger and those on vertebra 2 being smaller. Neural spines are absent. The sacral diapophyses are relatively narrow and are uniform in width. The sacrum has a bicondylar articulation with the urostyle, which is 89% of the length of the presacral vertebral column and extends posteriorly to the ischium. In the pectoral girdle, the clavicles are long and curved, moderately separated from one another medially. Coracoids are stout and hourglass-shaped, with the sternal ends more broadly expanded than the scapular end. The scapulae are narrow, while each cleithrum is long and very slender, broadly articulating with a partially mineralized suprascapula. Ossification of the suprascapula is concentrated in the areas of articulation with the scapula and cleithrum, resulting in an “L” shaped appearance of the suprascapula + cleithrum. There is no mineralized sternum or omosternum. The remainder of the appendicular skeleton is well-ossified, with the exception of some phalanges, which apparently have remained partially cartilaginous. The phalangeal formulae are 2/2/3/3 (manus) and 2/2/3/4/3 (pes); relative digital lengths are IV>V>III>II (manus; frogs do not have digit I) and IV>V>III>II>I (pes). Terminal phalanges are conical in shape, each narrowing to a minute terminus with delicate T-shaped expansions that do not reach the width of the base of the terminal phalanges.

Figures

FIGURE 2. Maximum likelihood phylogeny of Terrarana, based on analysis of the genes 12 S, tRNA-Val, 16 S, RAG 1, and TYR. Support values (Bayesian posterior probabilities / ML bootstrap support / MP bootstrap support) are indicated for nodes bearing on intergeneric relationships (i. e., at or above the genus level) with ML bootstrap support ≥ 50 %.

FIGURE 3. Tachiramantis species in life. (A) Tachiramantis prolixodiscus specimen CBA 7510, adult female from Calderas, Barinas, Venezuela. (B) Tachiramantis lentiginosus specimen CVULA 9100, adult male from Guaraque, Mérida, Venezuela.

FIGURE 4. Tachiramantis prolixodiscus specimen KU 132729, adult male paratype of the type species of Tachiramantis.

FIGURE 5. High resolution X-ray computed tomography of Tachiramantis prolixodiscus (KU 132729, adult male); dorsal view.

FIGURE 6. High resolution X-ray computed tomography of skull of Tachiramantis prolixodiscus (KU 132729, adult male); (A) dorsal view, (B) ventral view, (C) side view.

FIGURE 7. High resolution X-ray computed tomography of digits of Tachiramantis prolixodiscus (KU 132729, adult male); (A) manus, (B) pes.

FIGURE 8. Distribution of Tachiramantis in the Cordillera de Mérida of Venezuela and the Cordillera Oriental of Colombia. The range gap corresponds to the relatively low-elevation Táchira Depression. Known point localities of each species are indicated, based on specimens listed in the Appendix, as well as those listed in Rivero (1984), and those with data on GBIF (www. gbif. org).