Monday, January 25, 2016

[Herpetology • 2016] Frankixalus, A New Rhacophorid Genus of Tree Hole Breeding Frogs with Oophagous Tadpoles


Frankixalus jerdonii (Günther, 1876) 

Genus Frankixalus [gen. nov.Biju, Senevirathne, Garg, Mahony, Kamei, Thomas, Shouche, Raxworthy, Meegaskumbura & Van Bocxlaer, 2016

 A male Frankixalus jerdonii emerges from a tree hole about 5 meters high. 

PHOTOGRAPH BY S.D. Biju || DOI: 10.1371/journal.pone.0145727

Abstract
Despite renewed interest in the biogeography and evolutionary history of Old World tree frogs (Rhacophoridae), this family still includes enigmatic frogs with ambiguous phylogenetic placement. During fieldwork in four northeastern states of India, we discovered several populations of tree hole breeding frogs with oophagous tadpoles. We used molecular data, consisting of two nuclear and three mitochondrial gene fragments for all known rhacophorid genera, to investigate the phylogenetic position of these new frogs. Our analyses identify a previously overlooked, yet distinct evolutionary lineage of frogs that warrants recognition as a new genus and is here described as Frankixalus gen. nov. This genus, which contains the enigmatic ‘Polypedatesjerdonii described by Günther in 1876, forms the sister group of a clade containing Kurixalus, Pseudophilautus, Raorchestes, Mercurana and Beddomixalus. The distinctiveness of this evolutionary lineage is also corroborated by the external morphology of adults and tadpoles, adult osteology, breeding ecology, and life history features.

Fig 1. Bayesian consensus phylogram showing phylogenetic relationships among 86 taxa representing all known rhacophorid genera and one outgroup species.
Numbers above the branches represent Bayesian Posterior Probabilities, numbers below the branches represent Maximum Likelihood bootstrap values. Clade representing Frankixalus gen. nov. is shown in red. The specimen that was assigned to “Theloderma moloch” by Li et al. [2009] is indicated by an asterisk. Colors of taxa labels represent the reproductive modes: blue, terrestrial foam-nesting, exotrophic tadpoles; orange, terrestrial gel-nesting, exotrophic tadpoles; green, terrestrial direct-developing, endotrophic tadpoles; cyan, aquatic gel-nesting, exotrophic tadpoles. The new genus Frankixalus is also a terrestrial gel-nesting form.

Fig 2. A–C, Frankixalus jerdonii in life.
(A) dorsolateral view of an adult male (BNHS 5976), (B) an adult male (SDBDU 2009.271) emerging from a tree hole, (C) frontal view of an adult male (BNHS 5977). D–H, A composite showing the breeding habitat of Frankixalus jerdonii. (D) Evergreen forest at Mawphlang in East Khasi Hills district of Meghalaya state, (E) close-up of a tree hole opening located 3.4 meters above the ground, (F) oviposition site with eggs adhered to the inner vertical walls of the tree hole above the water level, and arrow pointing towards an adult female found submerged about 1 cm below the water surface, (G) unpigmented gel-encapsulated eggs, (H) premetamorphic larva inside the water-filled tree hole.

Taxonomic treatment

Amphibia Linnaeus, 1758
Anura Fischer von Waldheim, 1813

Rhacophoridae Hoffman, 1932
Rhacophorinae Hoffman, 1932

Frankixalus gen. nov.

Etymology: The genus is named after Prof. Franky Bossuyt of the Vrije Universiteit Brussel (Belgium), as a token of appreciation for his contribution to amphibian research and herpetology education, and in particular for the valuable role he played in the scientific career of SDB and IVB. The generic epithet is derived from the name ‘Franky’ (used as a noun in the nominative singular) in conjugation with the genus name ‘IxalusDuméril & Bibron, 1841, often used as a suffix in rhacophorid generic names. For the purposes of nomenclature, the gender of this genus is male.

Suggested common name: Franky’s tree frogs

Type species: Polypedates jerdonii Günther, 1876

'Polypedates' jerdonii =  Frankixalus jerdonii (Günther, 1876)

Boulenger, G. A. 1882. Catalogue of the Batrachia Salientia s. Ecaudata in the collection of the British Museum. 2d ed.  archive.org/stream/catalogueofbatra00brituof




Diagnosis: We consider Frankixalus to consist of the most inclusive clade that contains Frankixalus jerdonii comb. nov. but not Kurixalus eiffingeri. Frankixalus currently contains two species, F. jerdonii (Günther, 1876) and a currently unidentified species.

Frankixalus can be distinguished from the other rhacophorid genera by the combination of the following characters: medium-sized adults (male SVL 37.1–42.1 mm, N = 11; female SVL 46.8 mm, N = 1), webbing medium (foot webbing: I2––2+II1+–21/4III1+–11/2IV11/2−1+V; hand webbing: I1–1+II1+–2+III2––1+IV); creamy-white, gel-encapsulated eggs without pigmentation are laid in tree holes (phytotelm-breeding) where they also undergo development. The tadpole is oophagous and lacks keratinized tooth rows. The two currently included species are geographically restricted to high altitudes (approximately 1100–1600 m asl) in Northeast India and adjoining regions in China.


Fig 5. Geographic distribution of Frankixalus in Northeast India and China.
 Circle = Frankixalus jerdonii, square = Frankixalus sp.

Fig 2. A–C, Frankixalus jerdonii in life. (A) dorsolateral view of an adult male (BNHS 5976), (B) an adult male (SDBDU 2009.271) emerging from a tree hole, (C) frontal view of an adult male (BNHS 5977). D–H, A composite showing the breeding habitat of Frankixalus jerdonii. (D) Evergreen forest at Mawphlang in East Khasi Hills district of Meghalaya state, (E) close-up of a tree hole opening located 3.4 meters above the ground, (F) oviposition site with eggs adhered to the inner vertical walls of the tree hole above the water level, and arrow pointing towards an adult female found submerged about 1 cm below the water surface, (G) unpigmented gel-encapsulated eggs, (H) premetamorphic larva inside the water-filled tree hole.

Description of the name-bearing type

Frankixalus jerdonii (Günther, 1876) comb. nov.

Common name: Jerdon’s tree frog

Name-bearing type: Lectotype, NHM 1947.2.7.84 (ex BMNH 72.4.17.189), an adult female.

Type locality: “Darjeeling”, West Bengal, India.

Geographic distribution: Frankixalus jerdonii is widely distributed in three Northeast Indian states (Meghalaya, Manipur and Nagaland), and in the “Darjeeling” region of West Bengal. Meghalaya: East Khasi Hills district, Wahlynkien (Marai Kaphon), Cherrapunjee (1337 m asl), and Mawphlang forest (1577 m asl); Manipur: Churachandarpur district, Zaraengtung, Raenghzaeng village (1392 m asl); Nagaland: Kohima district, Sechüma village, Zubza (1470 m asl), Meriema village (1425 m asl), Seukwehii, Tseminyu village (1340 m asl); West Bengal: Darjeeling district, “Darjeeling” (1600 m asl) (Fig 5).

Natural history and breeding ecology

All males in our study were found on arboreal vegetation in montane evergreen forest (Mawphlang, Meghalaya), or secondary forests (Zaraengtung, Manipur and Zubza, Nagaland); males from Zubza were collected from inside bamboo poles with slits. Breeding activities of Frankixalus jerdonii take place between May–August. Males of F. jerdonii were heard calling at night (between 18:00–22:00 hours) from tree holes located at heights ranging from 0.8–5.5 m at Mawphlang forest, Meghalaya (in June 2009) soon after sporadic rain showers. The habitat at this locality is composed of an evergreen forest with sparse undergrowth, consisting of scattered shrubs and herbs (Fig 2D). The trunks of hardwood trees in these montane evergreen forests usually have large growths of bryophytes (Fig 2E). Amplexus was not observed. Freshly laid egg clutches (unpigmented, gel-encapsulated) were found adhering on the inner walls of a tree hole about 5 m above the ground (Fig 2F and 2G). In total, nine nest sites were observed in tree hollows, with tree diameters of about 10–30 cm (measured at the height of the hole). Occupied tree holes had openings oriented both horizontally (N = 5) and vertically (N = 4), usually with narrow openings, and contained water that ranged in depth from about 5–50 cm (volume of water contained ranging from 30–160 ml, N = 3). A deep layer of organic debris was observed at the bottom of some tree holes, and at two nest sites a dormant male was found submerged under water (Fig 2F). When disturbed, one male tightly wedged itself into a crevice in the bottom of the hollow. At another nest site, a female (not collected) was observed submerged in water. Eggs were observed between 0.3–10 cm above the water surface, were round, diameter measuring 2.0 ± 0.1 mm, N = 18, with a thick jelly layer of about 0.2–0.4 mm. Clutch size varied from 16–30 eggs per mass (2.5–5.6 cm, N = 7). During repeated surveys at the same site between 27–29 June 2009, we also observed tadpoles of various sizes (stages 10–44) inside the water-filled tree holes

Tadepole of Frankixalus jerdonii, oral disc with papillae demarcating its margins, shown in frontal view of a stage 36 tadpole

Fig 3. Various life history stages of Frankixalus jerdonii.
 (A) lateral, (B) dorsal, (C) ventral views of a preserved stage 36 tadpole, (D) unfertilised “nutritive” eggs found inside the dissected larval gut (mean diameter = 1.0 mm), (E) oral disc with papillae demarcating its margins, shown in frontal view of a stage 36 tadpole, (F) dextral vent tube, in ventral view of a stage 26 tadpole, (G) sinistral spiracular tube, in ventral view of a stage 36 tadpole, (H) gel-encapsulated eggs (mean diameter = 2.0 mm) found on the inside wall of a tree hole, (I) dorsolateral view of a stage 44 tadpole, (J) oral disc of a live stage 36 tadpole having a bifurcated muscular tongue, shown in frontal view, (K) dorsal, (L) ventral views of a live stage 35 tadpole, (M) serrated, inverted upper jaw of a stage 37 tadpole in ventral view, (N) serrated, V-shaped lower jaw of a stage 37 tadpole in ventral view.

dorsal, ventral views of a preserved stage 36 tadpole of Frankixalus jerdonii,
unfertilised “nutritive” eggs found inside the dissected larval gut (mean diameter = 1.0 mm)



Conservation: 
The major threat for amphibians in Northeast India is disturbance of primary and secondary forests by ‘jhumming’ (slash and burn) with the purpose of cultivating crops. Several localities where Frankixalus jerdonii is reported to occur are highly disturbed and fragmented habitats. The population at Cheerapunjee in Meghalaya state was recorded from a secondary forest adjacent to a highly polluted Wahlynkien stream, individuals from Manipur were from tree stumps within a jhum field, and those from Nagaland were from a secondary forest. These threats are alarming, especially for species that have very specialized habitat requirements, such as availability of small water collections in tree holes that are crucial for their survival and reproductive success.

A male Frankixalus jerdonii emerges from a tree hole about 5 meters high. 
 PHOTOGRAPH BY S.D. Biju || DOI: 10.1371/journal.pone.0145727

Conclusion

Multiple lines of evidence from our study highlight the unique evolutionary position and life history features of Frankixalus. The description of this enigmatic lineage from the relatively unexplored northeast region of India not only emphasizes that part of this region’s biodiversity still remains poorly studied, but also underscores the need to replicate similar studies in other animal groups within this globally recognized biodiversity hotspot.

The description of this new rhacophorid genus adds to our knowledge on reproductive diversification in one of the most specious groups of neobatrachian amphibians. Such information is essential in understanding the evolution of reproductive strategies that allowed amphibians to occupy a broad variety of ecological niches. 


S. D. Biju, Gayani Senevirathne, Sonali Garg, Stephen Mahony, Rachunliu G. Kamei, Ashish Thomas, Yogesh Shouche, Christopher J. Raxworthy, Madhava Meegaskumbura and Ines Van Bocxlaer. 2016. Frankixalus, A New Rhacophorid Genus of Tree Hole Breeding Frogs with Oophagous Tadpoles. PLoS ONE. 11(1): e0145727. DOI: 10.1371/journal.pone.0145727


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