Nanohyla Poyarkov, Gorin & Scherz, 2021

Gorin, Vladislav A., Scherz, Mark D., Korost, Dmitriy V. & Poyarkov, Nikolay A., 2021, Consequences of parallel miniaturisation in Microhylinae (Anura, Microhylidae), with the description of a new genus of diminutive South East Asian frogs, Zoosystematics and Evolution 97 (1), pp. 21-54 : 21

Nanohyla Poyarkov, Gorin & Scherz gen. nov. Figs 10 , 11 ; Suppl. material 5: Table S5

Chresonymy.

Microhyla (partim)- Boulenger 1900; Smith 1923; Inger and Frogner 1979; Inger 1989; Bain and Nguyen 2004; Poyarkov et al. 2014; Hoang et al. 2020.

Microhyla (Microhyla) (partim)- Dubois 1987 (as a part of the subgenus Microhyla Microhyla ).

Type species.

Microhyla annectens Boulenger, 1900.

Etymology.

The genus name is derived from the Greek νᾶνος (nanos), meaning “dwarf”, “pygmy”, and the mythological figure, Hylas (Ancient Greek: Ὕλας), which is probably derived from the Ancient Greek verb " ὕλαω " meaning "to bark" ( Bourret 1942). In classical mythology, Hylas, son of King Theiodamas, was a youth who served as Heracles’ companion, lover, and servant. Heracles took Hylas with him on the Argonauts’ expedition, during which Hylas was kidnapped by nymphs of the spring in Pegae, Mysia, and turned into an echo. Heracles left the ship and was searching for Hylas for a great length of time, calling his name: " His adjunxit Hylan nautae quo fonte relictum / Clamassent ut littus Hyla! Hyla! omne sonaret " ("The mariners cried on Hylas till the shore / Then Re-echoed Hylas! Hylas! soothed..."; Virgil 1916, Ecl. 6, 43). The genus name refers to the small body size (< 25 mm) of all known Nanohyla species, while maintaining resemblance to its sister genus Microhyla , from which it is separated herein. The new genus name is feminine in gender.

Suggested common name.

Pygmy Narrow-mouthed Frogs.

Taxonomic content.

Nine species, including: Nanohyla annamensis comb. nov. (Smith, 1923); Nanohyla annectens comb. nov. (Boulenger, 1900); Nanohyla arboricola comb. nov. (Poyarkov, Vassilieva, Orlov, Galoyan, Tran, Le, Kretova & Geissler, 2014); Nanohyla hongiaoensis comb. nov. (Hoang, Nguyen, Luong, Nguyen, Orlov, Chen, Wang & Jiang, 2020); Nanohyla marmorata comb. nov. (Bain & Nguyen, 2004); Nanohyla nanapollexa comb. nov. (Bain & Nguyen, 2004); Nanohyla petrigena comb. nov. (Inger & Frogner, 1979); Nanohyla perparva comb. nov. (Inger & Frogner, 1979); and Nanohyla pulchella comb. nov. (Poyarkov, Vassilieva, Orlov, Galoyan, Tran, Le, Kretova & Geissler, 2014). Photos of Nanohyla gen. nov. members are presented in Fig. 11 .

Diagnosis.

The new genus is assigned to the subfamily Microhylinae on the basis of phylogenetic affinities and the following combination of morphological character states: vomers small, confined to the anterior and medial margins of choanae; clavicles and, in most cases, procoracoids absent, maxillary arcade edentate ( Parker 1934). Nanohyla gen. nov. differs from other Microhylinae genera by the following combination of osteological character states: (1) frontoparietals fused with exoccipitals; (2) exoccipitals fused with each other (incomplete fusion in N. pulchella ); (3) neopalatines present; (4) sphenethmoids completely fused with parasphenoid (incomplete fusion in N. pulchella ); (5) crista parotica entirely cartilaginous; (6) otic ramus of squamosal well-developed; (7) tympanic annulus well-developed; (8) transverse processes of presacral vertebrae with the following orientation: IV and V posterolaterally, II, VII and VIII anterolaterally, III and VI at right angle to body axis; (9) clavicles absent; (10) omosternum present, cartilaginous; (11) prehallux cartilaginous; (12) terminal phalanges of longest fingers and toes T-shaped. The combination of diagnostic external morphological characters includes: (13) small to extremely small frogs (adult SVL 11.8-25.8 mm); (14) snout rounded or pointed in profile; (15) supratympanic fold present; (16) ridge on posterior sides of choanae absent; (17) first finger (FI) length less than ½ FII or reduced to a nub; (18) finger discs present, at least on FII-FIV; (19) dorsal median longitudinal grooves on finger discs generally present (with the exception of N. perparva ); (20) toes dorsolaterally flattened, prominent discs present; (21) dorsal median longitudinal grooves on toe discs present; (22) metatarsal tubercle single (inner metatarsal tubercle present, outer absent); (23) dorsomedial line absent; (24) superciliary tubercles absent; (25) tibiotarsal articulation of adpressed hindlimb reaching well beyond snout; (26) toe webbing well-developed (at least one-half webbed); (27) skin on dorsum feebly granular to tubercular; (28) tympanum externally distinct at least in males ( N. annamensis , N. annectens , N. arboricola , N. marmorata , N. nanapollexa , N. pulchella ) or barely distinct ( N. hongiaoensis , N. perparva , N. petrigena ); (29) terrestrial or scansorial semi-arboreal microhabitat preference.

Phylogenetic definition.

The genus Nanohyla gen. nov. includes all species sharing a more recent common ancestor with Nanohyla annectens than with Microhyla achatina and Glyphoglossus molossus .

Distribution.

The distribution area of Nanohyla gen. nov. covers montane forests of the Annamite (Truong Son) Mountains in Vietnam, eastern Laos, and north-eastern Cambodia, the Titiwangsa Mountain Range in the southernmost Thailand and peninsular Malaysia, mountains of Borneo (including Sabah and Sarawak of Malaysia, Brunei, and Kalimantan of Indonesia) and the Sulu Archipelago of the Philippines (see Fig. 1 ). The occurrence of Nanohyla gen. nov. in Cardamom Mountains in eastern Thailand (the record of " M. annamensis " from Khao Sebab by Taylor [1962], see Fig. 1 ) is questionable (see Poyarkov et al. 2014, 2020a).

Morphological comparison.

The new genus Nanohyla gen. nov. differs from its sister genus Microhyla Tschudi, 1838 s. str. by the well-developed (vs poorly-developed) otic ramus of the squamosal, frontoparietals and exoccipitals fused (vs separated or slightly fused), exoccipitals fused with each other (vs always separated), omosternum present (vs usually absent), sphenethmoid and parasphenoid fused completely or partially (vs separated), cartilaginous crista parotica (vs mineralized posteriorly), cartilaginous prehallux (vs mineralized), tympanum externally visible or barely visible (vs concealed beneath skin), inner metatarsal tubercle well-developed, outer generally absent (vs two metatarsal tubercles well-developed), and in having digits dorso ventrally flattened, FI often reduced to a nub or shortened (vs variably longer). The new genus differs from the closely related genus Glyphoglossus Günther, 1869 by its smaller adult size with SVL < 25mm (vs SVL > 25mm), skull longer than wide or almost equal (vs wider than long), alary process of premaxilla oriented slightly anteriorly (vs posteriorly), neopalatines present (vs obscured by vomers), vomers small, indistinct (vs large, well-developed), omosternum present (vs absent), terminal phalanges T-shaped (vs simple), tibio-tarsal articulation reaching well beyond snout (vs to the anterior border of the eye, or less), by body habitus short, triangular-shaped (vs stout, balloon-shaped), and by inner metatarsal tubercle not enlarged (vs enlarged, shovel-shaped). Nanohyla gen. nov. differs from Kaloula Gray, 1831 by its much smaller adult body size SVL < 25 mm (vs SVL > 38 mm), procoracoids absent (vs present), postchoanal portion of vomer absent (vs present), neopalatines present (vs obscured), prehallux formed by two elements (vs one), tibio-tarsal articulation reaching well beyond snout (vs to shoulder), absence (vs presence) of ridge on posterior margin of choanae, inner metatarsal tubercle not enlarged (vs enlarged and spatulate), and by body habitus short, triangular-shaped (vs robust). The new genus can be distinguished from Uperodon Duméril & Bibron, 1841 by its smaller adult size, SVL < 25 mm (vs SVL > 34 mm), postchoanal portion of vomer absent (vs present), neopalatines present (vs obscured), tibio-tarsal articulation reaching well beyond snout (vs posterior border of eye, or less), absence (vs presence) of ridge on posterior margins of choanae, inner metatarsal tubercle not enlarged (vs enlarged or spatulate), and by body habitus short, triangular-shaped (vs robust and globular). Nanohyla gen. nov. differs from Phrynella Boulenger, 1887 by its smaller adult size, SVL < 25 mm (vs SVL > 30 mm), medial process of the prechoanal part of vomer absent (vs present), neopalatines present (vs absent), procoracoids absent (vs present), vertebral column diplasiocoelus (vs procoelus), metatarsal tubercules separate (vs united), by tibio-tarsal articulation reaching well beyond snout (vs to tympanic region), by body habitus short, triangular-shaped (vs robust and flattened), and by generally dull brownish coloration of inguinal and dorsal surfaces (vs greenish coloration of dorsum and bright-red coloration of inguinal area, and ventral surfaces of limbs). The new genus further differs from Metaphrynella Parker, 1934 by its smaller adult size, SVL < 25 mm (vs SVL > 25 mm), skull longer than wide or almost equal (vs wider than long), neopalatines present (vs absent), omosternum present (vs absent), vertebral column diplasiocoelus (vs procoelus), tibio-tarsal articulation reaching well beyond snout (vs to tympanic region), absence (vs presence) of a ridge on posterior margins of choanae, metatarsal tubercules separate (vs united and enlarged), and by finger webbing absent (vs present). The new genus differs from Mysticellus Garg & Biju, 2019 by its short triangular-shaped body habitus (vs slender), supratympanic fold present (vs absent), finger and toe tips enlarged with prominent discs (vs slightly enlarged), toe webbing well-developed (vs rudimentary), supernumerary carpal tubercles absent (vs prominent subarticular tubercles alternating with additional smaller tubercles), and the two prominent blackish-brown ‘false-eye’ inguinal spots absent (vs present). Nanohyla gen. nov. differs from Micryletta Dubois, 1987 by its snout longer than eye diameter, and having eye less (vs more) prominent in lateral and dorsal aspects, finger and toe tips enlarged with prominent discs (vs slightly enlarged), toe webbing well-developed (vs rudimentary or absent), supernumerary carpal tubercles absent (vs present), omosternum present (vs absent), neopalatines present (vs absent), tibio-tarsal articulation reaching well beyond snout (vs to anterior border eye, or less), supratympanic fold present (vs absent), and body habitus short, triangular-shaped (vs slender). Finally, the new genus is distinguished from Chaperina Mocquard, 1892 by clavicles and procoracoids absent (vs present), postchoanal portion of vomer absent (vs present), omosternum present (vs absent), terminal phalanges T-shaped (vs simple), tibiotarsal articulation reaching well beyond snout (vs anterior border of eye), belly dull-colored (vs bright saffron-yellow belly with dark pattern), and by absence of spine-like projections on limbs (vs a long, narrow dermal spine projecting from calcaneus).

Larval morphology.

Description of the larval stages of the Nanohyla gen. nov. members are sparse and often not detailed. Poyarkov et al. (2014) provided descriptions, photos and illustrations of tadpole morphology for N. annamensis , N. arboricola and N. pulchella . Vassilieva et al. (2017) provided a detailed description of development, larval morphology and anatomy for N. arboricola . Le et al. (2016) provided a brief description of tadpole morphology of N. marmorata . Leong (2004) provided a short description and photographs of larval and metamorph morphology for N. annectens . Brief descriptions and figures depicting larvae of N. petrigena and N. perparva are found in the original description of these species by Inger and Frogner (1979), as well as in Inger and Steubing (2005) and Haas et al. (2020). Larval stages of N. hongiaoensis and N. nanapollexa remain unknown.

As with almost all larvae in Microhylidae , labial teeth and mandibles are absent from the oral discs of Nanohyla tadpoles. Most species of Nanohyla have larval morphology resembling that of many pond-breeding Microhyla species ( Poyarkov et al. 2014) with rather short-tailed transparent or semi-transparent Orton’s type II tadpoles ( Orton 1953), that are mid-water column (neustonic) feeders with comparatively unexpanded lower labium and anteriorly directed terminal mouths, lateral orientation of eyes, spiraculum located in a medial position on the venter, spiracular flap with crenulate margins, and tail lacking terminal filament ( Altig and Johnston 1989; Donnelly et al. 1990; Leong 2004). In contrast, many species of Microhyla s. str. are surface suspension feeders, and demonstrate greatly expanded lower labium and dorso-terminal mouth orientation; they may have terminal filament on tail and smooth margins of spiracular flap (e.g., Leong 2004; Hendrix et al. 2008; Poyarkov et al. 2014).

A peculiar exception is the case of N. arboricola , which is an obligate phytotelm-breeding species that reproduces in water-filled tree hollows ( Vassilieva et al. 2017). The oophagous tadpoles of this species differ from larvae of pond-dwelling Microhyla and Nanohyla species in many aspects, including external morphology (extremely long tails, dorsolateral position of the eyes, dark pigmentation), morphology of digestive tract (large, extensible stomach with comparatively short intestine), and characteristic oral morphology ( Vassilieva et al. 2017). Nanohyla nanapollexa was suggested as phytotelm-breeder as a single specimen of this species was recorded in a water-filled tree hollow ( Gorin et al. 2020), although the details of reproductive biology and tadpole morphology of this species are still unknown.

Taxonomic comment.

Microhyla pulverata Bain & Nguyen, 2004 was considered a junior synonym of N. marmorata based on the phylogenetic results of Gorin et al. (2020); the same study also reported on three putative candidate species within N. arboricola , N. perparva , and N. petrigena , indicating that our knowledge on diversity of Nanohyla is still incomplete.

Certain variation in diagnostically important characters of Nanohyla gen. nov. requires further comments. Bain and Nguyen (2004) reported on significant variation in size and shape of the outer metatarsal tubercle in N. marmorata which was reported to vary from almost indistinct to “conical.” We have examined a large series of N. marmorata (see Poyarkov et al. 2014; Nguyen et al. 2019) and found that in this species the outer metatarsal tubercle usually is not discernable or is indistinct; we assume that this discrepancy might be explained with the differences in preservation of specimens examined by us and by Bain and Nguyen (2004). Hoang et al. (2020) reported two metatarsal tubercles in their diagnosis of N. hongiaoensis , however in the holotype description they refer to the outer metatarsal tubercle as “indistinct;” it is also not discernable in their photo of holotype’s foot ( Hoang et al. 2020:fig. 3F). In all the remaining species of Nanohyla gen. nov. it is absent, and we therefore consider this state to be diagnostic for the genus (in comparison to Microhyla s. str., which has two metatarsal tubercles in all species but M. maculifera , see comment below). It is not clear why Bain and Nguyen (2004), or Poyarkov et al. (2014; and other preceding studies) did not recognize the presence of externally visible tympanum in most of species of the genus (Fig. 11 ). In species of Nanohyla gen. nov., smaller tubercles and other dermal structures of the skin become flattened and less distinct after fixation and preservation; this has also been reported in other anurans ( Poyarkov et al. 2015, 2017, 2019; Nguyen et al. 2018, 2019, 2020). It is likely that the presence of the tympanum was artifactually concealed from Bain and Nguyen (2004), since their description was based exclusively on museum specimens. In some species of Nanohyla gen. nov., we were not able to detect an externally visible tympanum ( N. hongiaoensis , N. perparva , N. petrigena ). It is not clear whether this reflects an actual character state in these species, or if this apparent state relates to the small sample size of specimens and photographs available to us. Further studies are needed to clarify variation of the external tympanum in Nanohyla gen. nov.

Figures

Figure 1. Distribution ranges of the three clades of the Microhyla - Glyphoglossus assemblage. Distribution area of Microhyla I is shown in yellow, of Microhyla II in red, and of Glyphoglossus in blue. Distributional data from Gorin et al. (2020). Question mark denotes the unconfirmed record of " Microhyla annamensis " from Khao Sebab in eastern Thailand by Taylor (1962).

Figure 10. Palmar views of hands (above) and thenar views of feet (below) of the representative Microhyla s. str. and Nanohyla gen. nov. species: N. annamensis (A, B), N. arboricola (C, D), M. minuta (E, F), and M. tetrix (G, H). Arrow indicates outer metatarsal tubercle. Not to scale. Line drawings by Valentina D. Kretova.

Figure 11. Members of the new genus Nanohyla gen. nov. in life (males): N. annectens from Genting Highlands, Pahang, Malaysia (A), N. annamensis from Bidoup - Nui Ba N. P., Lam Dong, Vietnam (B), N. arboricola from Chu Yang Sin N. P., Dak Lak, Vietnam (C), N. hongiaoensis from Bidoup - Nui Ba N. P., Lam Dong, Vietnam (D), N. marmorata from Kon Chu Rang N. R., Gia Lai, Vietnam (E), N. nanapollexa from Kon Plong, Kon Tum, Vietnam (F), N. perparva from Gunung Mulu, Sarawak, Malaysia (G), N. petrigena from Gunung Mulu, Sarawak, Malaysia (H), and N. pulchella from Bidoup - Nui Ba N. P., Lam Dong, Vietnam (I). Insets show tympanic area of the each species; white arrow points at the tympanic rim of the external tympanum. Photos by Nikolay A. Poyarkov (A-S, D-F, I), Vu Dang Hoang Nguyen (D), and Indraneil Das (G, H).