[Herpetology • 2016] Unearthing the Fossorial Tadpoles of the Indian Dancing Frog Family Micrixalidae, Micrixalus herrei

Fig 1. Habitat preference and characteristic features of various life history stages of Micrixalus herrei.
 (A) Adult male (SDBDU 2012.2452, SVL 17.40 mm), found on the surface of emergent wet rocks along the stream; (B) metamorphosed larva, near shallow water, closer to the stream bank (stage 44, SVL 17.20 mm); (C) stream margin habitat of metamorphs (stages 43–44); (D) anguilliform bodied tadpoles on the gravel bed (stages 30–35), after being exposed from depths of about 30 cm; (E) egg clutch (N = 20) buried under sand in shallow water; (F) fossorial tadpoles after being exposed, at stages 26 (1), 28 (2), and 29 (3), having eel-like, dorsoventrally flattened bodies, dorsal eyes, and well-developed muscular tails with reduced fins; (G) lateral profile of a tadpole, observed amongst exposed gravel (stage 27).

DOI: 10.1371/journal.pone.0151781

Abstract

Tadpoles of the monotypic Indian dancing frog family Micrixalidae have remained obscure for over 125 years. Here we report the discovery of the elusive tadpoles of Micrixalus herrei from the sand beds of a forested stream in southern Western Ghats, and confirm their identity through DNA barcoding. These actively burrowing tadpoles lead an entirely fossorial life from eggs to late metamorphic stages. We describe their internal and external morphological characters while highlighting the following features: eel-like appearance, extensively muscularized body and tail, reduced tail fins, skin-covered eyes, delayed development of eye pigmentation in early pre-metamorphic stages (Gosner stages 25–29), prominent tubular sinistral spiracle, large transverse processes on vertebrae II and III, ankylosed ribs on transverse processes of vertebra II, notochord terminating before the atlantal cotyle-occipital condyle junction, absence of keratodonts, serrated well-formed jaw sheaths, and extensive calcified endolymphatic sacs reaching sacrum posteriorly. The tadpole gut contains mostly fine sediments and sand. We discuss the eel-like morphology and feeding habits of M. herrei in the context of convergence with other well-known fossorial tadpoles. This discovery builds the knowledge base for further comparative analyses and conservation of Micrixalus, an ancient and endemic lineage of Indian frogs.

Discussion

This description of the external morphology, osteology and ecological adaptations, of Micrixalus herrei provides the first confirmed report of a tadpole from the ancient anuran family, Micrixalidae. The present study also bridges a significant gap by documenting the life history of at least one representative species from each of the world’s 54 anuran families, which facilitates comparative studies across many disciplines, including development, evolution, and ecology.

There is a single report of Micrixalus tadpoles by Smith[14] based on “two poorly preserved specimens said to belong to M. opisthorhodus” (currently M. phyllophilus). According to the basic description provided by Smith[14], these tadpoles bear a single row of keratodonts, which subsequently were considered “characteristic” of micrixalid tadpoles without further investigation[15–17]. This observation is contrary to our finding that M. herrei tadpoles, along with three other micrixalid species (currently being studied in detail), lack keratodonts (tooth rows). Given that many features of the tadpoles described by Smith are synapomorphies with larvae of many other groups, we presume that this description is erroneous. Furthermore, Smith does not mention the fossorial habitat of the two tadpoles, which is their most conspicuous feature. Unfortunately, Smith’s description could not be validated due to the loss of his specimens. We have failed to recover them from any potential museum collections (Natural History Museum, London and Zoological Survey of India, Kolkata).

The unusual morphological characters of Micrixalus herrei show convergence with the fossorial forms that are currently known globally. Here we discuss some of the unique features and morphological adaptations of Micrixalus herrei tadpoles that correlate with a fossorial habit.

Gayani Senevirathne, Sonali Garg, Ryan Kerney, Madhava Meegaskumbura and S. D. Biju. 2016. Unearthing the Fossorial Tadpoles of the Indian Dancing Frog Family Micrixalidae. PLoS ONE. DOI: 10.1371/journal.pone.0151781

Indian dancing frog's secretive tadpoles unearthed from sand beds
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