Pristimantis grandoculis ( van Lidth de Jeude, 1904 )

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 : 1070-1075

Pristimantis grandoculis ( van Lidth de Jeude, 1904)

Hylodes grandoculis van Lidth de Jeude, 1904 Eleutherodactylus marmoratus Hoogmoed , in Frost, 1985 Eleutherodactylus marmoratus Avila-Pires et al., 2010 Pristimantis marmoratus Ouboter & Jairam, 2012 Pristimantis sp. 4 Jairam, 2019

Pristimantis sp. “Guianas” Vacher et al., 2020

Holotype. RMNH 4467 . Type locality: “the basin and the sources of the Coppename”, interior of Surinam. van Lidth de Jeude stated that the specimen was collected “ Sept. 10th 1901 ” during the Coppename expedition ( Anonymous, 1903). The expedition took place between August and late November 1901 “we went up the Coppename then the two rivers that form it until they become unseaworthy even for the korjales (boats) of the natives (3°57 N)”. These indications suggest that the specimen was collected at the farthest point reached by the expedition and that 3.9500°N 56.7543°W are plausible coordinates for the type locality.

Referred specimens. MNHN-RA-2020.0118 (field no. AF3435 ), an adult male collected by A. Fouquet, S. Cally and R. Jairam on 30 April 2015 at Bakhuis Mountains , Suriname (4.7246°N 56.7638°W, ~ 200 m asl; Fig. 3 ). NZCS A1212 , an adult male collected by P. Ouboter and V. Kadosoe on 20 August 2013 at Tafelberg, Suriname (3.8049°N 56.1539°W ~ 500 m asl) ; NZCS A1210–11 , two adult males collected by R. Jairam and D. Baêta on 23 June 2016 at Lely Mountain , Suriname (4.4158°N 54.6498°W, ~ 600 m asl) .

Definition. Pristimantis grandoculis is characterized by the following unique combination of characters: (1) SVL small, adult males 16.5 ± 1.1 mm (range 14.7–17.9 mm, n = 5) ( Table 1), female unknown; (2) dorsal skin tuberculate, with 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) external tympanum absent, tympanic membrane not differentiated and obscured by supratympanic fold on the posterodorsal edge of tympanum, tympanic annulus indistinct; (4) pharyngeal ostia absent; (5) columella absent; (6) tibia length 55–59% of SVL; (7) snout broadly rounded in profile and dorsal view; (8) each upper eyelid with two prominent tubercles; (9) choanae round and small (0.3 mm for MNHN-RA-2020.0118), dentigerous processes of vomers oblique, narrowly separated, each bearing 3–5 odontophores; (10) vocal slits absent, vocal sac absent; (11) one unpigmented whitish nuptial pad located on the preaxial side of the thenar tubercle on each thumb in male; (12) FI much shorter than FII, reaching subarticular tubercle of FII; (13) fingers with preaxial fringes on FII and III; (14) finger discs broadly expanded, elliptical, thenar tubercle oval, palmar often broken in three distinct tubercles; (15) three enlarged ulnar tubercles often flat and barely visible; (16) axillary tubercles (sensu Myers & Donnelly, 2001) absent; (17) tarsal fold absent but tubercles present; (18) toes basally webbed between TII –IV with preaxial fringes on TII – V; (19) calcars absent, inner metatarsal tubercle oval, outer metatarsal tubercle round; (20) dorsal specimen of P. grandoculis (MNHN-RA-2020.0118) from Bakhuis, Suriname. c A photograph in life of another recently collected specimen P. grandoculis (NZCS A1210)

colouration mostly chestnut brown, but highly variable in colour and pattern, ventral colouration translucent brownish grey with small cream spots, mostly on chest, throat suffused with black melanophores and scattered with small irregular cream blotches; (21) iris golden with a copper horizontal band, absence of vertical streak; (22) posterior surface of thighs and groin dark grey in life and brown in preservative, absence of yellow spot on groin.

Morphological comparisons with other Guiana Shield lowlands Pristimantis of the “ unistrigatus group”. Pristimantis grandoculis can mainly be distinguished from P. espedeus by its smaller body size ( SVL range in males= 14.7–17.9 mm vs. 20.7–24.8 in P. espedeus ); external tympanum absent (vs. visible in P. espedeus ) and dark grey groin colouration in life (vs. reddish in P. espedeus ).

Pristimantis grandoculis can mainly be distinguished from P. inguinalis by dark grey groin colouration in life (vs. bright yellow inguinal mark in P. inguinalis ); external tympanum absent (vs. visible in P. inguinalis ) and translucent brownish grey ventral colouration with small cream spots (vs. entirely black in P. inguinalis ).

All the other known Guiana Shield species of the “ unistrigatus group” occur in the Pantepui region and are generally associated with highlands (i.e.> 700 m elevation; Fouquet et al., 2013; Kok et al., 2018). Pristimantis grandoculis was previously confused (and considered a synonym) with P. marmoratus , one of these Pantepui species, from which it can immediately be distinguished by iris colour in life (black vertical streak running across the iris in P. marmoratus vs. no such streak in P. grandoculis ) and absence of columella and vocal slits (vs. present in P. marmoratus ). Among the other Pristimantis species found at mid-elevation in Pantepui, P. grandoculis can mainly be distinguished from P. jester ( Means & Savage, 2007) by having preaxial fringes on FII and III (absent in P. jester ), toes basally webbed between TII –IV with preaxial fringes on TII – V (webbing and fringes on toes absent in P. jester ) and by iris colour in life (golden to copper in P. grandoculis vs. upper 2/5 of iris blue-grey in P. jester ); from P. saltissimus ( Means & Savage, 2007) by tympanum condition (external tympanum absent, with indistinct tympanic annulus in P. grandoculis vs. distinct with distinct tympanic annulus in P. saltissimus ), by having preaxial fringes on FII and III (absent in P. saltissimus ) and toes basally webbed between TII –IV with preaxial fringes on TII – V (webbing and fringes on toes absent in P. saltissimus ); from P. guaiquinimensis ( Schlüter & Rödder, 2007; see also Kok & Barrio-Amorós, 2013) mostly by tympanum condition (external tympanum absent, with indistinct tympanic annulus in P. grandoculis vs. distinct with distinct tympanic annulus in P. guaiquinimensis ); from P. sarisarinama ( Barrio-Amorós & Brewer-Carías, 2008) mostly by the absence of vocal slits in males (present in P. sarisarinama ); from P. pulvinatus ( Rivero, 1968) mostly by smaller body size in males (14.7–17.9 mm in P. grandoculis vs. 23.0– 26.1 mm in P. pulvinatus ) and distinct vomerine teeth (indistinct or absent in P. pulvinatus ); and from P. memorans ( Myers & Donnelly, 1997) mostly by the absence of vocal slits in males (present in P. memorans ), and tympanum condition (external tympanum absent, with indistinct tympanic annulus in P. grandoculis vs. distinct with distinct tympanic annulus in P. memorans ).

Variation. The holotype is relatively well preserved. However, it is highly discoloured, and overall tuberculation is difficult to assess. Proportions are similar among the five specimens examined; the amount of tuberculation on the skin varies, especially on the dorsum and lateral surfaces of the body. Colour pattern is variable across the recently collected specimens. NZCS A1210 has a dark band running along the canthus rostralis which is absent in the other specimens ( Fig. 2c). The W-shaped scapular mark is well-developed anteriorly but less so posteriorly compared to the other specimens. An interorbital band darker than the dominant background is often present as well as dark bands on the arms and legs but all these markings are variable in sharpness across specimens.

Osteology of the holotype (RMNH 4467). Cranium ( Fig. 4 ). Shape and proportions. The skull is well ossified, 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.

Neurocranium and dorsal investing bones. The nasals (separated medially from one another and covering all the nasal capsules dorsally), frontoparietals, 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 ossified. Frontoparietal crests are absent and the frontoparietal fontanelle is exposed. 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 absent.

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 fused 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 posteriorly curved. Well-developed dentigerous processes extend posteromedially from the union of the pre- and postchoanal processes. Each dentigerous process bears three teeth and is broadly separated from its counterpart medially. The neopalatine is fused 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 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 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. The 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 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 in narrow contact medially. The dentary is short and thin, posteriorly acuminate, and overlaps the angulosplenial for about a quarter of its length. Dentary is 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. 4 ).

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 posteriorly), whereas those of presacrals IV–VIII extend dorsolaterally (IV–VII posteriorly, VIII anteriorly). The relative lengths of the transverse processes and sacral diapophyses are: III> IV> Sacrum> V ≈ VI ≈ VII ≈ VIII> II. The sacral diapophyses are slightly expanded distally. The urostyle has a well-developed dorsal ridge that extends along half 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 narrowly separated from one another 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 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.

Natural history. Our data suggest that Pristimantis grandoculis is terrestrial and scansorial. Males were often found perched on low vegetation (0.5–1.5 m above the ground), at dusk, in a position suggesting calling activity. However, acoustic activity has never been observed neither in Suriname nor in French Guiana for P. sp. “Guianas” East (despite being locally abundant). It is noteworthy that both groups of populations also lack a columella and that external tympanum is absent in all specimens examined. Juveniles have been found on the leaf litter during the day, and this is also where juveniles, females and amplectant pairs of P. sp. “Guianas” East have been found in French Guiana suggesting that the reproduction takes place there. The species inhabits pristine terra firme forests from 50 to 700 m asl, generally along the slopes of small massifs.

Distribution. Pristimantis grandoculis occurs throughout the interior of Suriname (not along the coastal band), on the southern border of Guyana with Brazil (Acari mountains), and along the border between the Brazilian states of Pará and Amapá. The species probably extends further in southern Suriname and northern Pará state, Brazil. Phylogenetically related populations occur in French Guiana ( Pristimantis sp. “Guianas” East), the Maroni River separating these two groups of genetically divergent populations. The taxonomic status of this group of populations needs to be clarified when additional material becomes available. In French Guiana, P. sp. “Guianas” East occurs throughout the territory except the Approuague-Oyapock interfluvium and is probably absent from northern Amapá state in Brazil. This pattern of distribution strikingly mirrors that of Anomaloglossus surinamensis ( Vacher et al., 2017) and Pipa aspera ( Vacher et al., 2020) , both species displaying similar geographical boundaries and deep genetic structures across the Maroni River. Interestingly, Pristimantis sp. “Guianas” East only overlaps with P. cf. marmoratus ( Pristimantis sp. 1 ) in the southern half of French Guiana. Likewise, the distribution of A. surinamensis only weakly overlaps with that of A. blanci ( Fouquet et al., 2018) . Both are pairs of sister species with similar ecology and body size.

Figures

Fig. 3 a Dorsal, ventral, and lateral (head) views of the holotype (RMNH 4467) of P. grandoculis from Coppename River, Suriname. b Dorsal and ventral views and hand and foot of a recently collected

Fig.4 Volumetric renderings of µ-CT scans of the skeleton of the holotype of Pristimantis grandoculis (RMNH 4467). a Full skeleton in dorsal (left), ventral (middle), and lateral (right) views. b Skull in dorsal (left), ventral (middle), and lateral (right) views. Abbreviations: ang—angulosplenial, den—dentary, dp—dentigerous process, exo—