Tuesday, October 9, 2018

[Herpetology • 2018] Micryletta nigromaculata • A New Limestone-dwelling Species of Micryletta (Anura: Microhylidae) from northern Vietnam


Micryletta nigromaculata 
Poyarkov, Nguyen, Duong, Gorin & Yang, 2018

DOI: 10.7717/peerj.5771 

Abstract
We report on a new species of the genus Micryletta from limestone karst areas in northern Vietnam, which is described on the basis of molecular and morphological evidence. Micryletta nigromaculata sp. nov. is restricted to narrow areas of subtropical forests covering karst massifs in Cat Ba National Park (Hai Phong Province) and Cuc Phuong National Park (Ninh Binh Province) at elevations of 90–150 m a.s.l. In the phylogenetic analyses, the new species is unambiguously positioned as a sister lineage to all remaining species of Micryletta. We also discuss genealogical relationships and taxonomic problems within the genus Micryletta, provide molecular evidence for the validity of M. erythropoda and discuss the taxonomic status of M. steinegeri. We suggest the new species should be considered as Endangered (B1ab(iii), EN) following the IUCN’s Red List categories. A discussion on herpetofaunal diversity and conservation in threatened limestone karst massifs in Southeast Asia is provided.


Figure 4: Holotype of Micryletta nigromaculata sp. nov. (ZMMU A5934), male, in situ in dorsolateral view.
Photo by Nikolay A. Poyarkov.

Figure 6: Color variation of Micryletta nigromaculata sp. nov. in life. Cat Ba National Park:
 (A) Male paratype ZMMU A5945; (B) male paratype ZMMU A5935 in situ; Cuc Phuong National Park; (C) male DTU 302 in situ; (D) female DTU 303 in situ.
Photos A–B by Nikolay A. Poyarkov; C–D by Tan Van Nguyen.

Figure 3: Holotype of Micryletta nigromaculata sp. nov. (ZMMU A5934), male, in life.
(A) Dorsal view; (B) ventral view; (C) lateral view of head; (D) volar view of left hand; (E) plantar view of right foot.
Photos by Nikolay A. Poyarkov.

Micryletta nigromaculata sp. nov.

Diagnosis. The new species is assigned to the genus Micryletta by the following combination of morphological features: small body size; vomerine teeth absent; tympanum small, rounded, externally visible; very prominent subarticular tubercles on fingers and toes; three well-developed metacarpal tubercles; distinct supernumerary palmar and metatarsal tubercles posterior to base of digits; first finger not reduced; digit tips expanded to very small disks and webbing on fingers and toes totally absent (Dubois, 1987; Fei et al., 2009). Micryletta nigromaculata sp. nov. is distinguished from all of its congeners by a combination of the following morphological characters: body size small (SVL 18.5–23.0 mm in males, 24.2–25.9 mm in females); body habitus moderately slender; head wider than long; snout obtusely rounded in profile; EL equal to or shorter than SL; IOD two times wider than UEW; tibiotarsal articulation of adpressed limb reaching the level of eye center; dorsal surface slightly granular with small round flattened tubercles; supratympanic fold present, thick, glandular; outer metatarsal tubercle absent; dorsum coloration brown to reddish-brown; dorsum with dark-brown irregular hourglass-shaped pattern edged with orange; body flanks brown with dark-brown to black patches or spots edged with white, a large black blotch in inguinal area on each side; lateral sides of head immaculate reddish brown lacking white patches; venter whitish with indistinct gray pattern; and throat in males whitish with light-gray marbling.

Figure 2: Phylogenetic BI tree of Micryletta reconstructed on the base of 947 bp of 16S rRNA gene. Values on the branches correspond to BI PP/ML BS, respectively. For specimen, locality and GenBank accession number information see Table 1.
Photos by Nikolay A. Poyarkov (Micryletta nigromaculata sp. nov. M. erythropoda, M. cf. inornata) and Chung-Wei You (M. steinegeri).

Figure 1: Distribution of the genus Micryletta and the new species.
(A) Map of Southeast Asia with approximate range of the genus Micryletta shown in red. Black circles indicate type localities of the currently recognized taxa within Micryletta. Yellow stars show distribution of Micryletta nigromaculata  sp. nov. black dot in the center of icon indicates the type locality (Cat Ba Island). Black square indicates the inset shown in detail in B.
 (B) Map of northern Vietnam, showing distribution of Micryletta nigromaculata sp. nov. and the Red River basin; 1—Cat Ba National Park, Hai Phong Province (type locality); 2—Cuc Phuong National Park, Ninh Binh Province. Photo by Nikolay A. Poyarkov.

Etymology: Specific epithet “nigromaculata” is an adjective in the nominative case, feminine gender, derived from Latin words “niger” for “black” and “maculatus” for “spotted,” in reference the characteristic black blotches on flanks in the new species.

Recommended vernacular names: We recommend “Black-spotted Paddy Frog” as the common English name of the new species and the common name in Vietnamese as “Nhái bầu hông đen.”


Distribution and biogeography: The presently known distribution of Micryletta nigromaculata sp. nov. is shown in Fig. 1. To date, the new species is known from limestone karst areas covered by primary tropical forest in Cat Ba N. P., Hai Phong Province, and by secondary tropical forest in Cuc Phuong N. P., Ninh Binh Province at elevations 90–150 m a.s.l. Northern Vietnam has one of the world largest areas of limestone landscapes, covered by specific limestone vegetation (Fenart et al., 1999; Day & Urich, 2000). The currently known range of Micryletta nigromaculata sp. nov. is divided by the vast lowlands of the Red River valley, an important biogeographic border in Indochina (Bain & Hurley, 2011; Yuan et al., 2016); our phylogenetic analysis estimates genetic divergence between the Cat Ba and Cuc Phuong populations at 0.7% (see Table 1). It is anticipated that Micryletta nigromaculata sp. nov. also occurs in the adjacent limestone karsts of northern Vietnam; in particular, records from Quang Ninh, Lang Son and Bac Giang provinces of northeastern Vietnam, as well as from Hoa Binh, Ha Nam and Thanh Hoa provinces of northwestern Vietnam are anticipated.

Natural history notes: Our knowledge on the biology of Micryletta nigromaculata sp. nov. is scarce; the species appears to be closely associated with karstic habitats. In Cat Ba N. P. (Hai Phong Province) during a 2-week survey in October 2011, specimens were only recorded from a small patch of limestone outcrops ca. 20 m in diameter, near a large limestone karst cliff and a small temporary body of water. Frogs were observed from 16:00 to 20:00 h hiding between small pieces of limestone rocks. Despite intensive search from 10 to 22 of October 2013, no additional specimens of the new species were recorded from other areas in Cat Ba N. P. In Cuc Phuong N. P. (Ninh Binh Province) specimens were found at night between 19:00 and 23:30 h near cave entrances and in valleys surrounded by limestone cliffs, relatively near to water sources. Surrounding habitat was limestone karst covered with primary polydominant tropical forest with multilayered canopy and an abundance of lianas, with occasional trees of Streblus macrophyllus (Moraceae), Terminalia myriocarpa (Combretaceae), Parashorea chinensis (Dipterocarpaceae) and Tetrameles nudiflora (Tetramelaceae) (in Cat Ba N.P.) or secondary forest (in Cuc Phuong N.P.). Reproduction biology, including advertisement call, tadpole morphology, as well as diet of the new species remains unknown.

Other species of anurans recorded syntopically with the new species at the type locality included Polypedates megacephalus Hallowell, P. mutus (Smith), Theloderma albopunctatum (Liu & Hu), Liuixalus calcarius Milto, Poyarkov, Orlov & Nguyen, Philautus catbaensis Milto, Poyarkov, Orlov & Nguyen, Hyla chinensis Günther, Microhyla butleri Boulenger, M. heymonsi Vogt and Micryletta cf. inornata. In Cuc Phuong National Park (Ninh Binh Province) the new species was recorded in sympatry with Occidozyga martensii (Peters), Leptobrachium guangxiense Fei, Mo, Ye & Jiang, Ophryophryne microstoma Boulenger, Glyphoglossus (formerly Calluella) guttulatus (Blyth), Microhyla heymonsi Vogt, Micryletta cf. inornata (Boulenger); Rana johnsi Smith; Sylvirana cf. annamitica Sheridan & Stuart; Raorchestes cf. menglaensis (Kou); Theloderma albopunctatum (Liu & Hu) and T. annae Nguyen, Pham, Nguyen, Ngo & Ziegler.


Conclusions: 
Limestone karst areas are recognized as arks of highly endangered though still insufficiently studied biodiversity. Unique geological structure of karst massifs, formed by erosion and subterranean water drainages create numerous humid microrefugia with stable environmental conditions, which serve as an important environmental buffer for small vertebrates during periods of climate change (Clements et al., 2006; Glaw, Hoegg & Vences, 2006). The complex terrain of isolated karstic hills and caves create multiple ecological niches what along with their highly fragmented habitat-island nature result in high degrees of site-specific endemism within, and diversity among them (Oliver et al., 2017; Grismer et al., 2018). Limestone karsts are also known as important “biodiversity arks” for both surface and cave faunas, yet karstic regions are rapidly becoming some of the most imperiled ecosystems on the planet (Clements et al., 2006; Grismer et al., 2016a, 2016b, 2018; Luo et al., 2016; Suwannapoom et al., 2018). South-east Asia harbors more limestone karsts than anywhere else on earth (Day & Urich, 2000) with numerous new species including relic lineages of amphibians and reptiles being discovered from limestone areas (e.g. see discussions in Milto et al., 2013; Grismer et al., 2014; Grismer & Grismer, 2017; Grismer et al., 2016a, 2016b, 2017, 2018; Nazarov et al., 2014, 2018; Connette et al., 2017; Suwannapoom et al., 2018 and references therein). Ironically, though acting as major biodiversity hotspots, limestone karsts are critically endangered due to unregulated quarrying mostly for cement manufacturing, which is the primary threat to the survival of karst-associated species (Grismer et al., 2018); their continued exploitation for limestone cannot be stopped (Clements et al., 2006). Until karst habitats in Vietnam are thoroughly investigated, a significant portion of this country’s herpetological diversity will remain underestimated and unprotected. Our study thus calls for urgent focused survey and conservation efforts on karst herpetofauna in Southeast Asia and in Vietnam in particular.



Nikolay A. Poyarkov, Tan Van Nguyen, Tang Van Duong, Vladislav A. Gorin and Jian-Huan Yang. 2018. A New Limestone-dwelling Species of Micryletta (Amphibia: Anura: Microhylidae) from northern Vietnam. PeerJ. 6:e5771.  DOI: 10.7717/peerj.5771

   

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