Pristimantis crepitaculus, Fouquet & Peloso & Jairam & Lima & Mônico & Ernst & Kok, 2022

Fouquet, Antoine, Peloso, Pedro, Jairam, Rawien, Lima, Albertina P., Mônico, Alexander T., Ernst, Raffael & Kok, Philippe J. R., 2022, Back from the deaf: integrative taxonomy revalidates an earless and mute species, Hylodes grandoculis van Lidth de Jeude, 1904, and confirms a new species of Pristimantis Jiménez de la Espada, 1870 (Anura: Strabomantidae) from the Eastern Guiana Shield, Organisms Diversity & Evolution (New York, N. Y.) 22 (4), pp. 1065-1098 : 1075-1081

Pristimantis crepitaculus sp. nov.

Pristimantis marmoratus Lescure & Marty, 2000 Pristimantis marmoratus Fouquet et al., 2007 Pristimantis marmoratus Dewynter et al., 2008 Pristimantis marmoratus Fouquet et al., 2012 Pristimantis sp. 1 Fouquet et al., 2013

Pristimantis sp. 1 Kok et al., 2018

Pristimantis sp. 1 Fouquet et al., 2019

Pristimantis cf. marmoratus Vacher et al., 2020

Holotype. MNHN-RA-2020.0102 (field no. AF2786 ), an adult male, collected by Antoine Fouquet, Maël Dewynter & Nicolas Vidal on 26 February 2015 at Mitaraka , French Guiana (2.2358 N 54.4493 W,~ 200 m asl; Fig. 5 ).

Paratypes. Twenty-seven specimens (23 males and four females) from French Guiana and the state of Amapá, Brazil: MNHN-RA-2020.0092–0112; MPEG 41819–41825 (Appendix 2) .

Etymology. The specific epithet is a latinised adjective referring to the call structure of the new species, which sounds like a rattle (crepitaculum).

Definition. The new species is characterized by the following unique combination of characters: (1) SVL small, adult males 17.0± 0.8 mm (range 15.7–18.3 mm, n = 24) and adult females 23.4 ± 0.5 mm (range 22.9–23.9 mm, n =4) ( Table 1); (2) dorsal skin tuberculate, two pairs of enlarged tubercles on the scapular region embedded in a W-shaped scapular fold, ventral skin granular particularly on the femoral region; (3) tympanum visible, tympanic membrane not or only poorly differentiated, tympanic annulus partially visible externally obscured by supratympanic fold on the posterodorsal edge of tympanum, tympanum c.a. 1/3 of eye length; (4) pharyngeal ostia present; (5) columella present; (6) tibia length 48–54% of SVL; (7) snout broadly rounded in profile and slightly acuminate in dorsal view; (8) each upper eyelid with two prominent tubercles; (9) choanae round and small (0.5 mm for the holotype), dentigerous processes of vomers oblique, narrowly separated, each bearing 2–4 small odontophores; (10) vocal slits present, vocal sac median, subgular; (11) one unpigmented whitish nuptial pad located on the preaxial side of the thenar tubercle on each thumb in male; (12) FI slightly shorter than FII, reaching disc of FII; (13) fingers without lateral fringes; (14) finger discs broadly expanded, elliptical, thenar tubercle ovoid, palmar tubercle ill-defined; (15) three enlarged ulnar tubercles often flat and barely visible; (16) axillary tubercles (sensu Myers & Donnelly, 2001) absent; (17) small tarsal tubercles present; (18) toes without lateral fringes but with weak lateral keels, webbing rudimentary basal between TII–V; (19) calcars absent, inner metatarsal tubercle oval, much larger than the round outer tubercle; (20) dorsal colouration highly variable from greenish to brownish with various patterns, ventral colouration light grey with small black spots denser on throat and legs; (21) iris reddish to copper with a darker horizontal band and a black vertical streak; (22) posterior surface of thighs and groin dark grey in life and brown in preservative, lack of yellow circumscribed spot on groin; (23) anterior surface of arms, posterior surface of flanks and dorsal surface of thighs often yellow in reproductive males; (24) advertisement call characterized by series (0.50– 0.75 s long) of 6–12 very short notes (0.02– 0.05 s long) with a dominant frequency ranging between 3.2–3.6 kHz and emitted every 5.4– 8.6 s; (25) male calling activity exclusively crepuscular, usually upside down on tree trunks of low diameter.

Morphological comparisons with other Guiana Shield lowlands Pristimantis of the “ unistrigatus group”. Pristimantis crepitaculus sp. nov. can mainly be distinguished from P. espedeus by its smaller body size (SVL range in males = 15.7–18.3 mm vs. 20.7–24.8 in P. espedeus ); dark grey groin colouration in life (vs. reddish in P. espedeus ); and advertisement call composed of more notes and higher dominant frequency (> 6 notes and> 3.1 kHz).

Pristimantis crepitaculus sp. nov. can mainly be distinguished from P. inguinalis by dark grey groin colouration in life (vs. bright yellow inguinal mark in P. inguinalis ); light grey ventral colouration with small black spots (vs. entirely black in P. inguinalis ); and advertisement call composed of series of notes (vs a single note in P. inguinalis ).

Pristimantis crepitaculus sp. nov. can mainly be distinguished from P. grandoculis by visible tympanum (external tympanum absent in P. grandoculis ); more tuberculate dorsal skin; enlarged tubercles on eyelids being equally distant from the eye (vs. posterior tubercles closer to the eye in P. grandoculis ); fingers and toes without fringes (fringed in P. grandoculis ), smaller tibia length (48–54% of SVL vs. 58–60%); and presence of vocal slits in males (absent in P. grandoculis ).

All the other species of the unistrigatus group known from the Guiana Shield occur in the Pantepui region and are generally associated with highlands (i.e.> 700 m elevation; Fouquet et al., 2013; Kok et al., 2018). One of these Pantepui species, P. marmoratus , is possibly its closest relative. Pristimantis crepitaculus sp. nov. can mainly be distinguished from P. marmoratus by its fingers and toes without fringes (fringes present in P. marmoratus ) and its advertisement call composed of a series of notes (vs. a single note in P. marmoratus ). Among the other Pristimantis species found at mid-elevation in Pantepui, P. crepitaculus sp. nov. can mainly be distinguished from P. jester ( Means & Savage, 2007) by the presence of a tympanum (absent in P. jester ), from P. saltissimus ( Means & Savage, 2007) by iris colour in life (black vertical streak running across the iris in P. crepitaculus vs. no such streak in P. saltissimus ), from P. guaiquinimensis ( Schlüter & Rödder, 2007) by its smaller body size (females 32.4–33.6 mm in P. guaiquinimensis [see Kok & Barrio-Amorós, 2013] vs. 22.9–23.9 mm in P. crepitaculus sp. nov.), a distinct tympanum (weakly distinct in Pristimantis crepitaculus sp. nov.), from P. sarisarinama ( Barrio-Amorós & Brewer-Carías, 2008) by iris colour in life (black vertical streak running across the iris in P. crepitaculus sp. nov. vs. no such streak in P. sarisarinama ), and distinct vocalization (1–2, rarely 3 notes in P. sarisarinama vs. 6–12 notes in P. crepitaculus sp. nov.), from P. pulvinatus ( Rivero, 1968) by its smaller body size (males 23.0– 26.1 mm in P. pulvinatus vs. 15.7–18.3 mm in P. crepitaculus sp. nov.) and distinct vomerine teeth (indistinct or absent in P. pulvinatus ), from P. memorans ( Myers & Donnelly, 1997) by iris colour in life (black vertical streak running across the iris in P. crepitaculus sp. nov. vs. no such streak in P. memorans ), a shorter inter-note interval (0.05– 0.12 s in P. crepitaculus sp. nov. vs. 0.20– 0.29 s in P. memorans ), and by the posterior thigh surface being dark grey in life (vs. blackish with yellow flecking in P. memorans ).

Description of the holotype. An adult male, SVL 15.8 mm. Head only slightly longer than wide, widest at corner of the mouth; snout slightly acuminate in dorsal and round in lateral views; canthus rostralis distinctly concave; nostrils nearly elliptical, directed almost completely laterally; interorbital region flat, loreal area slightly concave. Eyes large and protuberant, directed laterally, diameter of eyes much larger than tympanum diameter (ED/TD = 3.0), pupil elliptical. Supratympanic fold slightly distinct; tympanum small, ovoid, tympanic membrane completely covered by skin, but tympanic annulus distinct anteriorly and ventrally, covered by the M. depressor mandibulae posteriorly and dorsally. Vocal sac present, single, subgular, extending towards pectoral region between forearms. Choanae small (0.5 mm), round, not concealed by palatal shelf, larger than vomerine odontophores; a pair of small vomerine odontophores present; tongue ovoid, posteriorly free; vocal slits present, extending diagonally from lateral base of tongue to almost to the angle of the jaw.

Arms slender, not hypertrophied; lateral margins of arm and forearm free of fringes, folds, but with three tubercles; finger discs elliptical, expanded in all fingers, disc on FI the smallest, on FIII the largest; relative lengths of fingers I<II <IV <III; subarticular tubercles round, narrower than finger width; fringes absent on all fingers. Subarticular tubercles present on all fingers, one on FI and FI, two on FIII and FIV; all subarticular tubercles round and about the same size; inner metacarpal (thenar) tubercle present, oval; outer metacarpal tubercle large, W-shaped, ill-defined. Webbing between fingers absent.

Legs relatively long and slender, with rows of large and flat tubercles on tarsus and postaxially on foot (but lacking fringes or folds). All toes well developed, with expanded, elliptical, medium sized discs; discs on TIV and TV the largest, those on TI and TII the smallest; relative lengths of toes I<II <III <V <IV. Toes lacking fringes. Subarticular tubercles present on all toes; one tubercle present on TI, TII, and TV, two tubercles on TIII, three on TIV; all subarticular tubercles round, similar in size. Inner metatarsal tubercle oval; outer metatarsal tubercle small, round.

Skin on dorsum, head, dorsal surfaces of limbs, flanks, and groin tuberculate with enlarged tubercles on the scapular region and on eyelids, posterior surface of the dorsum, and dorsal surface of hindlimbs. Skin on the gular region smooth; chest, belly and undersurfaces of limbs granular. Cloacal opening directed posteriorly; cloacal region lacking tubercles.

Colour of holotype in life. Dorsal colour dark brown with V-shaped black band on the scapular region, a large middorsal black blotch and an ill-defined black blotch near groin ( Fig. 5 ). Black bands and blotches located in the interorbital region, on the loreal region, the nasal region, below the eyes and the tympanic region. Interorbital region and V-shaped scapular mark delimited anteriorly by reddish bands. Lower flank as dorsum with a black blotch. Axillary region and upper arm yellow. Lower arm as dorsum with two black transversal bands. Dorsal colouration of legs as dorsum with four black transversal bars on thigh, four on tibia and three on tarsus. Throat background grey covered with minute black melanophores; belly skin grey covered with small cream spots and by black melanophores that become sparse near groin; ventral surfaces of thighs and arms as throat. Iris with copper metallic pigmentation and pupil ring interrupted dorsally and ventrally by transversal pigmentation ( Fig. 5 ).

Colour of holotype in preservative. After four years in 70% ethanol, colours of the specimen faded, notably glandular supracarpal pad and throat pigmentation ( Fig. 5 ). The snout is dorsally dark brown and well-delimited by a transversal light grey interorbital band extending on half of the eyelids. Posteriorly, the interorbital region is covered by a dark brown band. A V-shaped dark brown mark is well-defined on the scapular region posteriorly followed by two oblique traversal dark brown bands. Similar, transversal dark brown bands are present on the arms, hands and legs and feet (for more details see Fig. 5a ).

Variation in the type series. Proportions vary little among the 21 paratypes. Males are smaller than females (15.7–18.3 mm vs. 22.9–23.9). The amount of tuberculation on the skin varies, especially on the dorsum and flanks. Outer metatarsal tubercle is always present, but its size/visibility vary among specimens.

Colour pattern is highly variable among specimens and several patterns are observed. A pattern similar to the holotype (middorsal and interobital bands) is present in female MNHN-RA-2020.0104 and in males MNHN- RA-2020.0110 and MPEG 41821 . A white band between the anterior corner of the eyes is present in most individuals but some specimens have less conspicuous markings (e.g. MNHN-RA-2020.0102, MNHN-RA-2020.0107). The scapular V-shaped mark is light grey in a few specimens (MNHN-RA-2020.0101, MNHN-RA-2020.094) or reddish (MNHN-RA-2020.0102, MNHN-RA-2020.0109) and display brightly coloured upper arms and posterior portions of flanks in life. Two specimens (MNHN-RA-2020.0098 and MPEG 41825 ) have a large well-defined cream spot on top of the snout and another one (MNHN-RA-2020.0100) has a light brown scapular mark posteriorly prolonged along the back forming a Y-shaped pattern delimited by darker flanks. Two specimens, one male ( MPEG 41823 ) and one female ( MPEG 41821 ) have large cream blotches on the dorsum .

Osteology of the holotype (MNHN-RA-2020.0102). Cranium ( Fig. 6 ). Shape and proportions. The skull is widest posterior to the orbit at the level of the articulation of the maxilla with the quadratojugal. The rostrum is moderate, the braincase is broad.

col—columella, den—dentary, exo—exoccipital, fro—frontal, max— maxillary, men—mentomeckelian, nas—nasal, neo—neopalatine, par—parasphenoid, pre—premaxillary, pro—prootic, pte—pterygoid, qua—quadratojugal, sep—septomaxilla, sph—sphenethmoid, squ— squamosal, vom—vomer

Neurocranium and dorsal investing bones. The nasals are broadly separated from one another and from the sphenethmoid; they cover most of the nasal capsules dorsally. The frontoparietals are well developed, co-ossified with the sphenethmoid. Frontoparietal crests are absent and the frontoparietal fontanelle (T-shaped) is exposed. The parasphenoid and neopalatines are co-ossified with the sphenethmoid. The frontoparietal and prootic are fused. Ventrally, the prootics are fused with the parasphenoid alae. The exoccipitals are fused. The dorsal surface of the otic capsule is mostly ossified. The septomaxilla is roughly spiralled, the medial ramus extending posterodorsal to the posterior ramus; the anterior ramus is thick; the lateral ramus is oblique with a long acuminate posterolateral extension; the posterior ramus extends from the middle of the lateral ramus ventromedially. The columellae (stapes) are well ossified, formed by the synostotic fusion of the long, thin pars media plectri (stylus) and the pars interna plectri (baseplate), which is curved.

Ventral investing bones. The parasphenoid cultriform process extends anteriorly from the anterior edge of the otic capsule and is co-ossified with the sphenethmoid. The parasphenoid alae are moderately long (about half of the length of the cultriform process), perpendicular to the anteroposterior body axis, broadening slightly laterally. The vomers are in narrow contact with the sphenethmoid; each vomer is composed of an arcuate bone bordering the anteromedial, medial, and posterior margins of the choana. The prechoanal ramus is expanded medially and anteriorly and bears a ventral flange along its medial edge. The postchoanal process is narrow and acuminate, slightly anteriorly curved. Well-developed dentigerous processes extend posteromedially from the union of the pre- and postchoanal processes, left process bears two small odontophores. Each dentigerous process is broadly separated from its counterpart medially. The neopalatine is narrowly in contact with the maxilla distally. This complex is fused with the parasphenoid medially.

Maxillary arcade. The maxillary arcade bears many small teeth on the premaxilla and maxilla. The arcade is complete and connected to the slender quadratojugal. The premaxillae are separated medially, and their anterodorsal alary process is weakly divergent from the midline. The pars palatina is broad, with two well-defined processes: the medial (palatine) process is relatively narrow and runs roughly parallel toward its contralateral; the lateral process is broader. The premaxilla and maxilla are in lateral contact via a simple juxtaposition. The maxilla is long, with a broad pars palatina along its lingual margin and a moderately developed pars facialis.

Suspensory apparatus. The triradiate pterygoid bears a slightly curved anterior ramus with a sculpted ventrolateral face, oriented anterolaterally toward the maxilla, with which it articulates at approximately the mid-length of the orbit. This pterygoid is fused to the maxilla. The medial and posterior face of the medial rami of the pterygoid are about equal in length. The medial ramus is broader than the posterior and its posterior face is strongly sculpted. The lateral end of the medial ramus overlaps the lateral edge of the prootic. The quadratojugal is long, laterally curved, and slender, articulating anteriorly with the maxilla. It has a bulbous posteroventral process and articulates dorsally with the ventral ramus of the squamosal. The squamosal is dorsally bifurcated, broad, and sculpted, extending anterodorsomedially from the quadratojugal to the level of the otic capsule; the zygomatic ramus is very short, whereas the otic ramus is long, almost reaching the posterior end of the skull.

Mandible. The mandible is slim and edentate. The mentomeckelians are small and arcuate in ventral view, medially and laterally broadened, and medially separated. The dentary is short and thin, posteriorly acuminate, and overlaps the angulosplenial for about a quarter of its length. Dentary is not in contact with the angulosplenial posteriorly. The angulosplenial is long and arcuate, laterally slightly grooved. The coronoid process is weak.

Hyoid. The bony posteromedial processes of the hyoid are expanded proximally and separated from one another. No ossified parahyoid is present.

Axial skeleton ( Fig. 6 ).

Vertebral column. The vertebral column has eight procoelous, presacral vertebrae. The vertebrae have complete neural arches and low neural processes. Atlas (presacral I) and presacral II are fused medially and laterally. The transverse processes of presacrals II–III are slightly expanded distally, thicker, and broader than those of other presacrals. The transverse processes of presacrals II and III are oriented ventrolaterally (II anteriorly, III slightly posteriorly), whereas those of presacrals IV–VIII extend dorsolaterally (IV–V posteriorly, VI–VIII anteriorly). The relative lengths of the transverse processes and sacral diapophyses are: Sacrum> III> IV> V ≈ VI ≈ VII ≈ VIII> II. The sacral diapophyses are slightly expanded distally. The urostyle has a well-developed dorsal ridge that extends along most of its length.

Pectoral girdle. The zonal portion has well-ossified coracoids, clavicles, scapulae, and cleithra. The clavicles are long, slender, and oriented anteromedially; the medial tips are in contact and located anteriorly from the level of anterolateral end of the clavicle that articulates with the scapula; the coracoid is long and flared, with its sternal end slightly broader than its glenoid end. The coracoids overlap medially. The scapula is long with a prominent pars acromialis that is not separated from the pars glenoidalis. The scapula is about one and a half the length of the clavicle. The cleithrum is ossified, well-developed, anteriorly thicker, thinning posteriorly. The suprascapula is unossified.

Pelvis girdle. The long, slender iliac shafts bear dorsolateral crests throughout their length. The overall length of the girdle is more than two times the width between the anterior ends of the iliac shafts. The iliac prominence is broad and low, and pubes mineralized.

Manus and pes. The phalangeal formulae for the hand and foot are standard, 2–2–3–3 and 2–2–3–4–3, respectively. Terminal phalanges strongly T-shaped. Ossified prepollex and prehallux visible.

Advertisement call. Six specimens calling from the underwood vegetation were recorded from about 2 m away at air temperatures between 23 ‒ 25 °C and 90 ‒ 100% relative humidity. Descriptive statistics of call parameters are presented in Table 2. Pristimantis crepitaculus sp. nov. emits every 7.04 s on average (range 5.44–8.62) series (call length mean = 0.59, range 0.50– 0.75 s) of 6–12 short notes (note length mean= 0.004 s; range 0.003 –0.006 s). These notes are emitted with increasing inter-note intervals within the call (mean1 st interval = 0.068 s; range 0.054 –0.085 s; mean 2nd interval = 0.102 s; range 0.078 –0.125 s). The notes have a clear harmonic structure (i.e. with extensive amount of energy in the harmonics). The dominant frequency is 3.50 kHz on average (range 3.16–3.91 kHz) with a slight upward modulation within the call (ca. 0.2 kHz) ( Fig. 7 , Table 2).

Natural history. Pristimantis crepitaculus sp. nov. is a scansorial species. Males were found calling perched on low vegetation (0.5–2.0 m above the ground). Calling activity was limited to a short period (about 1 h) at dawn and early night. Calling males often adopt a position head down along the trunks, small twigs, or leaves. They form groups of 2– 10 males usually spaced by at least 2 m between individuals. Juveniles and females are very rarely found, but at least one female (MPEG 41825) was collected very close to a calling male (MPEG 41824, calling from a leaf at about 2 m above ground). The species inhabits terra firme forests from 50 to 700 m asl and seems to particularly thrive near ecotones, such as tree falls, clear-cuts, roads, rivers, maybe because the penetrating light allows denser understory cover and thus more abundant calling sites.

Distribution. The species is apparently endemic to the easternmost part of the Guiana Shield lowlands, i.e. throughout the Amapá state of Brazil and French Guiana (at the exception of the northwest part of the territory). It occurs in the upper Maroni region, which corresponds to the border with Suriname, and probably extends at least in southeastern Suriname, like other species that are also endemic to the easternmost part of the Guiana Shield (e.g. Amazophrynella teko , Boana dentei , Pristimantis gutturalis ). However, it is unlikely that the range of P. crepitaculus sp. nov. extends to the Coppename river.

Figures

Fig. 5 a Holotype of Pristimantis crepitaculus sp. nov. in dorsal, ventral views. b Hand, foot and lateral view of the head. c Photographs of the holotype in life.d Several photographs of additional specimens in life

Fig. 6 Volumetric renderings of µ-CT scans of the skeleton of the holotype of Pristimantis crepitaculus (MNHN-RA-2020.0102). a Full skeleton in dorsal (left), ventral (middle), and lateral (right) views. b Skull in dorsal (left), ventral (middle), and lateral (right) views. Columellae are highlighted in red. Abbreviations: ang—angulosplenial,

Fig. 7 Sonograms and oscil- lograms on a 0.7-s window of a characteristic call of Pristi- mantis crepitaculus sp. nov. from Oiapoque, Amapá, Brazil (paratype, MPEG 41823)