Ghost frogs, hyloids, arcifery.. what more could you want?

Welcome again to Frog Blog, as Tet Zoo is now affectionately known. In the previous froggy article we got through the so-called transitional anurans, and I finished by introducing the largest, most speciose, most diverse anuran clade: Neobatrachia Reig, 1958. It contains about 96% of all extant anuran species: most of these belong to one of two great assemblages (conventionally dubbed hyloids and ranoids). My aim here - mostly an effort to avoid discussing all the myriad groups that belong to Neobatrachia - was to briefly dash through all of neobatrachian diversity in just one article, but I failed. If you're bored with anurans you might want to go away and ignore Tet Zoo for a while... hey: you could read Loren Coleman's article about my toy collection (here). It's not everyday you get to see the phrase "A television interviewer plays with Darren's plesiosaur" (even more so when that television interviewer is Judy Finnigan). To business. Parts I (here) and II (here) on anurans are essential reading.

Two obscure anuran groups, composed of small-bodied cryptic species that have relictual, Southern Hemisphere distributions, are almost certainly close to - or at - the base of Neobatrachia. They are the Seychelles frogs (or sooglossids) and kin, and the ghost frogs (or heleophrynids). The fact that these anurans are restricted to the Seychelles, India and southern Africa - combined with the fact that other basal neobatrachian lineages are restricted to the southern continents - strongly suggests that Neobatrachia originated in Gondwana prior to its breakup.

Ghost frogs (so named because one species comes from Skeleton Gorge in South Africa) are a small group (6 species) of southern African species, specialised for clinging to rock surfaces along mountain streams [adjacent image shows Table Mountain ghost frog Heleophryne rosei]. Their tadpoles have an oral sucker-like disc and lack keratinous beaks (though they do possess denticles). Suggested at times to be close relatives of the Australasian myobatrachids (more on this group later), ghost frogs were found by Haas (2003) to be outside of Neobatrachia, and by Frost et al. (2006) to the sister-taxon to the rest of Neobatrachia (a taxon they named Phthanobatrachia). Genetic data led Van der Meijden et al. (2007) to link ghost frogs with the cannibal frogs* (Lechriodus), conventionally classified within Myobatrachidae, and the Chilean helmeted water toad (Caudiverbera caudiverbera) [a species I covered briefly here], conventionally - and probably erroneously - included within Leptodactylidae.

* It's a dumb name, given that cannibalism is not exactly rare among anurans.

While Seychelles frogs have (virtually) always been regarded as neobatrachians, workers have disagreed as to whether they are closer to hyloids or ranoids, and this is still an area of contention. The four extant species of Seychelles frogs (the newest was named in 2002) are all tiny (SVL 10-40 mm) terrestrial frogs of leaf litter or arboreal habitats in high altitude forest [adjacent image shows tiny Gardiner's Seychelles frog Sechellophryne gardineri*]. They all lay their eggs on land; the young either undergo direct development, or the non-feeding tadpoles are carried on the back of the mother. They lack external vocal sacs and middle ear ossicles, so should be both voiceless and deaf... but they aren't, as at least some species make calls (Gerlach & Willi 2002). The recently discovered, bizarre, blackish fossorial Indian frog Nasikabatrachus sahyadrensis has been identified in several studies as the sister-taxon to Sooglossidae (Biju & Bossuyt 2003, Frost et al. 2006, Van der Meijden et al. 2007), but these studies have disagreed as to where the Nasikabatrachus + Sooglossidae clade should fit within Neobatrachia. They might be basal members of the hyloid clade (as shown in the cladogram above). Interestingly, Nussbaum & Wu (2007) expressed scepticism about a link between Nasikabatrachus and Seychelles frogs, and suggested that the former might be a hemisotid or a relative of the microhylids (more on those two groups later). I'll be saying more about Seychelles frogs (and Nasikabatrachus) in a later article - all of this is just an introduction.

* Yes, I know I know. I'm going to discuss it later (see Chris Taylor's article here).

Neobatrachians have usually been divided into two major assemblages: Hyloidea (aka Bufonoidea) and Ranoidea, both traditionally differentiated on the basis of different pectoral girdle types. Hyloids have what is known as an arciferal pectoral girdle [see image below]: this is where the epicoracoid cartilages overlap on the ventral midline (the epicoracoid cartilages are two cartilaginous bars, each located near the ventral midline of the pectoral girdle, that connect the subparallel clavicles and coracoids). Ranoids have what is known as a firmisternal pectoral girdle: this is where the epicoracoid cartilages fuse along the ventral midline. However, an intermediate condition (the arcifero-firmisternal condition) also exists, and phylogenetic studies looking at other lines of evidence show that firmisterny has evolved from arcifery on multiple different occasions (Emerson 1983), including within some hyloid groups! Taxa traditionally identified as hyloids also tend to have simple, procoelous vertebrae only, whereas ranoids are generally diplasiocoelous: that is, they possess both procoelous and amphicoelous vertebrae (procoely describes the condition where vertebral centra are concave anteriorly and convex posteriorly; amphicoely is where both faces of the centra are concave).

If the 'key characters' used to identify hyloids are primitive within neobatrachians - as they seem to be - you might wonder whether hyloids really are a clade or not, and indeed some people have argued that a hyloid is simply any neobatrachian that is not a ranoid. However, molecular studies have generally supported the monophyly of a neobatrachian clade that includes most of the 'hyloid' taxa: the southern frogs (myobatrachids), treefrogs (hylids), paradox frogs (pseudids), glass frogs (centrolenids), the American leptodactylids, poison-arrow frogs (denodrobatids) and toads (bufonids) (Hay et al. 1995, Darst & Cannatella 2004, Frost et al. 2006). This clade could be called Hyloidea, but the new name Hyloides was used by Frost et al. (2006).

Two large, Southern Hemisphere groups included in the hyloid clade - the myobatrachids of Australia and New Guinea and the leptodactylids of the American tropics - have always lacked identified synapomorphies and have often been accused of being artificial assemblages. Myobatrachids in the traditional sense should probably be split up into several distinct clades, all of which seem to belong somewhere near the base of Hyloides (Ford & Cannatella 1993, Darst & Cannatella 2004, Frost et al. 2006). Members of these groups include some of the most fantastic of anurans: the gastric-brooding frogs (Rheobatrachus), the surreal turtle frog Myobatrachus gouldii, and the Pseudophryne toadlets, best known for the tiny Corroboree frog P. corroboree [shown in adjacent image].

Leptodactylidae (in the traditional sense) also lacks synapomorphies and could be described as including all those non-myobatrachid hyloids that lack the diagnostic characters of such distinctive groups as toads, treefrogs and glass frogs. At least some taxa conventionally included in Leptodactylidae (like the Helmeted water toad) probably belong somewhere near myobatrachids within Hyloides, but other 'leptodactylids' (like the eleutherodactylines, horned frogs and Darwin's frogs) may instead be more closely related to treefrogs, poison-arrow frogs and toads. Among these diverse 'leptodactylids' are foam-nesting species, direct-developers, viviparous forms, and arboreal, fossorial and entirely aquatic taxa.

Fossils indicate that some of the groups formerly included within Leptodactylidae were around in the Palaeocene or even the Cretaceous: Baurubatrachus pricei from the Upper Cretaceous of Minas Gerais in Brazil has been allied by many workers with the horned frogs, and Estesiella boliviensis from the Palaeocene of Tiupampa in Bolivia has also generally been considered a 'leptodactylid'. The presence of these early members of Hyloides in South America makes sense in view of what we think we know about neobatrachian biogeography, which is why Thaumastosaurus from the Eocene of France and England - suggested by some to be related to horned frogs (Rage & Roček 2007) - has always been such a headache [excellent Thaumastosaurus images from Roček's projects page]. Was Thaumastosaurus actually the product of weird convergence, or does it indicate some Eocene link between Europe and South America? You'll know, of course, that the various other fossil tetrapods once used as evidence for such a link have now been reidentified (for the specifics see this ver 1 article on phorusrhacids).

More soon, you know you love it.

Refs - -

Biju, S. D. & Bossuyt, F. 2003. New frog family from India reveals an ancient evolutionary link with the Seychelles. Nature 425, 711-714.

Darst, C. R. & Cannatella, D. C. 2004. Novel relationships among hyloid frogs inferred from 12S and 16S mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 31, 462-475.

Emerson, S. 1983. Functional analysis of frog pectoral girdles. The epicoracoid cartilages. Journal of Zoology 201, 293-308.

Ford, L. S. & Cannatella, D. C. 1993. The major clades of frogs. Herpetological Monographs 7, 94-117

Frost, D. R., Grant, T., Faivovich, J., Bain, R. H., Haas, A., Haddad, C. F. B., De Sá, R. O., Channing, A., Wilkinson, M., Donnellan, S. C., Raxworthy, C. J., Campbell, J. A., Blotto, B. L., Moler, P., Drewes, R. C., Nussbaum, R. A., Lynch, J. D., Green, D. M. & Wheeler, W. C. 2006. The amphibian tree of life. Bulletin of the American Museum of Natural History 297, 1-370.

Gerlach, J. & Willi, J. 2002. A new species of frog, genus Soglossus (Anura, Sooglossidae) from Silhouette Island, Seychelles. Amphibia-Reptilia 23, 445-458.

Haas, A. 2003. Phylogeny of frogs as inferred from primarily larval characters (Amphibia: Anura). Cladistics 19, 23-90.

Hay, J. M., Ruvinsky, I., Hedges S. B. & Maxson L. R. 1995. Phylogenetic relationships of amphibian families inferred from DNA sequences of mitochondrial 12S and 16S ribosomal RNA genes. Molecular Phylogenetics and Evolution 12, 928-937.

Nussbaum, R. A. & Wu, S.-H. 2007. Morphological assessments and phylogenetic relationships of the Seychellean frogs of the family Sooglossidae (Amphibia: Anura). Zoological Studies 46, 322-335.

Rage, J.-C. & Roček, Z. 2007. A new species of Thaumastosaurus (Amphibia: Anura) from the Eocene of Europe. Journal of Vertebrate Paleontology 27, 329-336.

Van der Meijden, A., Boistel, R., Gerlach, J., Ohler, A., Vences, M. & Meyer, A. 2007. Molecular phylogenetic evidence for paraphyly of the genus Sooglossus, with the description of a new genus of Seychellean frogs. Biological Journal of the Linnean Society 91, 347-359.