Flying frogs, goliath frogs, and the one who can eat 16-and-a-half baby cobras

We returned late last night: it was a journey involving koalas, Pallas' cat and Asian golden cat, wolverines, rhinos, anteaters, Ceratosaurus, a toy armadillo, and yet again those bloody ichthyosaurs. Thanks to those who've been leaving comments in my absence, I'll address some of the points in due course. Anyway.. so, Tet Zoo has recently played host to articles on deer and carnivorans and, all too briefly, to weird turtles and red bats. But you know that, eventually, we had to return to anurans right?

Yes, finally, we come to the last group of ranoids, last group of neobatrachians, and indeed last group of aurans - the... well, what name do we use for them?

I'll start by saying that this is the ranoid clade that includes Rana and all ranoids closer to it than to, say, the hyperoliid Hyperolius or the microhylid Gastrophryne (the senior synonym of Microhyla) [that's actually not a bad phylogenetic definition, but I haven't seen it proposed in the literature]. Members of this group tend to have a notched tongue, fusion of some of the wrist and ankle bones, and a bony style on the metasternum. You might recall (from the article on ghost frogs and hyloids: here) that their pectoral girdles are firmisternal.

Some authors - like Bossuyt et al. (2006) - have included all the members of this group in an immense, highly diverse 'family' Ranidae, subdivided into as many as 14 'subfamilies' (from hereon this concept of Ranidae is termed 'inclusive Ranidae'). Others restrict the name Ranidae to the clade that includes Rana and similar forms, and treat all those 'subfamilies' as 'families'. Frost et al. (2006) used the new name Natatanura* for 'inclusive Ranidae'. Either way it makes no real difference, but I personally find it more useful to recognise multiple distinct 'families' given the diversity and sheer number of distinct groups within this clade, and hence I'm going to refer to these frogs as natatanurans (if you want the obligatory cladogram, it's coming in the next article). Ranids in the strictest sense of the term appear to be one of the youngest and most morphologically derived natatanuran clades, but also one of the most geographically widespread and speciose.

* This name means 'swimming frogs'. I think it's a pretty dumb name given that anurans in many other clades are equally, if not more, aquatic.

Slippery frogs and pyxi frogs: another African radiation

Arguably among the more interesting of the rather less well known natatanuran clades are the conrauines, or slippery frogs, a tropical African group that famously includes the immense Goliath frog Conraua goliath (shown with kids in adjacent photo. Big, no). Frost et al. (2006) united slippery frogs with the African water frogs (Petropedetes and Arthroleptides) and the Indian frogs (Indirana) in a clade that they termed Pedropedetidae: an arrangement they noted as initially surprising but well supported by molecular data.

The reason this affinity would be surprising is that all the other pedropedetids - and all the members of all the other natatanuran clades that seem closely related to them - are endemic to sub-Saharan Africa. In fact, we now have good evidence from several molecular studies that natatanuran lineages owe their distribution to the Late Cretaceous fragmentation of Gondwana, with strong endemism being the result. More on this later (in another article). An affinity of Indirana with the pedropedetids was outright rejected (on molecular grounds) by Van Bocxlaer et al. (2006); they instead found this taxon to be allied to the Indian micrixalids, as did Bossuyt et al. (2006) (what are micrixalids? I'll explain later).

Possibly closely related to pedropedetids are the pyxicephalids (sometimes called pyxi frogs, especially in the pet trade) and the obscure phrynobatrachids (Van der Meijden et al. 2005, Bossuyt et al. 2006, Frost et al. 2006). Again, these frogs are all endemic to sub-Saharan Africa, and Frost et al. (2006) named the phrynobatrachid-pyxicephalid-pedropedetid clade Africanura (not to be confused with Afrobatrachia!). About the only well known member of this lot is the South African bullfrog Pyxicephalus adspersus, a huge, stout-bodied, semi-fossorial pyxicephalid (SVL up to 200 mm) that possesses bony pseudo-teeth (aka odontoids) in the lower jaw [shown nicely in the image at the top of the article]. Males guard the shoaling tadpoles. This frog is famous for being an incredible glutton: a specimen that somehow got into a cobra enclosure at Pretoria Zoo managed to eat 16.5 baby cobras before someone stopped it (Mattison 1987).

Flying frogs and kin

Rhacophorids, sometimes called flying frogs, Old World treefrogs, or Afro-Asian treefrogs, are a reasonably large group (about 290 species... though read on) of mostly arboreal ranoids that occur across sub-Saharan Africa, India, China, Indonesia, Japan, the Philippines and Sulawesi. Some (like the foam-nest frogs Chiromantis and most Rhacophorus species) manufacture large arboreal foam nests; some (like the Indian Philautus species) are direct-developers. The best known rhacophorid, and the only one ever shown on TV or written about in books, is the famous Wallace's flying frog R. nigropalmatus from Indonesia, Thailand and adjacent countries. With its enormous fully webbed hands and feet and flaps of skin on its arms, body and legs, it is able to glide diagonally for over 7 m. You might think that it's unique in this regard, but it's not as lots of other Rhacophorus species are highly similar and can do the same trick. The adjacent painting of a flying frog is, again, by Carel Brest van Kampen (blog here, website here).

About that number of species... Meegaskumbura et al. (2006) reported how phylogenetic analysis of newly discovered Sri Lankan rhacophorids revealed the presence of a previously unrecognised endemic radiation. The big deal is that this radiation consists of over 100 new Sri Lankan rhacophorid species (18 were known prior to their work), making Sri Lanka on par with Madagascar, New Guinea and Borneo in terms of anuran diversity. As you'll hopefully have noticed while reading these anuran articles, the number of recognised lissamphibian species has sky-rocketed in recent years, and this really is because of newly discovered species, not just the result of splitting, taxonomic elevation of subspecies, or the recognition of cryptic species that can only be distinguished genetically. The great paradox is that lissamphibians are in chronic global decline at the same time, and many species can no longer be located at all. Despite Meegaskumbura et al.'s 100+ new species, they were unable to find many that had been described in the 19th century, a discovery which implies that the species concerned have gone extinct. As you surely know, lissamphibian species are currently being 'lost' on a regular and worrying basis, and I'll be talking more about the global amphibian crisis next year.

Golden mantellas and their Madagascan relatives

Rhacophorids appear to be particularly closely related to the mantellids, a group of Madagascan frogs (though with two species on Mayotte Islands in the Comores*); both share bifurcate (usually T-shaped) distal phalanges, intercalary elements, and a few muscle characters. Intercalary elements, you'll recall, are also present in true treefrogs (hylids) and are clearly convergent between these different arboreal neobatrachians. Of the 170 or so mantellid species, most are smallish arboreal or terrestrial frogs, most of which lay their eggs away from water (the tadpoles appear to undergo metamorphosis in hidden nests, and don't feed during development). Some of the arboreal taxa (like the species in the Boophis majori group) are very rhacophorid-like and in fact were regarded as rhacophorids as recently as the 1970s: Bossuyt & Milinkovitch (2000) showed how striking this convergence was, and discussed other cases of convergence between mantellids and neobatrachians from elsewhere. Mantellids don't engage in normal amplexus; instead, a male will press the ventral surfaces of his thighs directly against the back of a female, and it is almost certainly not coincidental that the males of many mantellid species possess large glands on the undersides of their thighs (Glaw et al. 2000). The exact function of the femoral glands remains uncertain, last I heard. Because they don't practice amplexus, male mantellids lack nuptial pads (what are nuptial pads? They're horny or spiky pads on the hands and/or arms of male anurans. They help the males stay attached to the females) [adjacent image shows, I think, Mantella aurantiaca].

* Mayotte Island never had a terrestrial connection with any of the adjacent landmasses, so the two endemic mantellids must have crossed marine barriers to get there. Vences et al. (2003) confirmed the island-endemic status of the Mayotte mantellids and also argued that several other island-dwelling anurans probably also underwent overseas dispersal. Lissamphibians thus can cross marine barriers, presumably by taking refuge on drifting rafts**.

** Remind me to explain one time why the term 'raft' is so annoying and inappropriate. We are not talking about floating logs, with desperate animals clinging to the sides.

Recent work, predominantly by Miguel Vences, Frank Glaw and their colleagues, has shown that mantellids include a particularly high number of cryptic species: populations that are morphologically highly similar but, on the basis of advertisement calls and genetics, appear to be distinguishable as species (e.g., Glaw et al. 2000, 2001, Glaw & Vences 2002a, b, Vallan et al. 2003). Of all the mantellids, the best known are very brightly coloured and poisonous: they convergently resemble the South American poison-arrow frogs and are sometimes called Malagasy poison frogs. Members of both groups apparently sequester their toxins in the same way: by ingesting toxic insects and then co-opting their poisons. Recent studies indicate that some South American poison-arrow frogs are becoming less poisonous over time, perhaps because their toxic insect prey are declining. The adjacent photo, taken by my good friend Mary Blanchard (of indri and sifaka fame), shows the Painted mantella Mantella madagascariensis. It might not surprise you to find that this rather variable species has recently been suggested to actually be a complex of several similar species.

And talking of being surprised, this isn't the last article in this now very long-running series. But the next one might be the last. And therein we find the purpose of this strange episode in Tet Zoo's history. I'll have some other things to deal with before then, however, as one of those personally-relevant publications is just about to appear. Stay tuned.

Refs - -

Bossuyt, F., Brown, R. M., Hillis, D. M., Cannatella, D. C. & Milinkovitch, M. C. 2006. Phylogeny and biogeography of a cosmopolitan frog radiation: Late Cretaceous diversification resulted in continent-scale endemism in the family Ranidae. Systematic Biology 55, 579-594.

- . & Milinkovitch, M. C. 2000. Convergent adaptive radiations in Madagascan and Asian ranid frogs reveal covariation between larval and adult traits. Proceedings of the National Academy of Sciences 97, 6585-6590.

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.

Glaw, F. & Vences, M. 2002a. A new sibling species of the anuran subgenus Blommersia from Madagascar (Amphibia: Mantellidae: Mantidactylus) and its molecular phylogenetic relationships. Herpetological Journal 12, 11-20.

- . & Vences, M. 2002b. A new cryptic frog species of the Mantidactylus boulengeri group with a divergent vocal sac structure. Amphibia-Reptilia 23, 293-304.

- ., Vences, M., Andreone, F. & Vallan, D. 2001. Revision of the Boophis majori group (Amphibia: Mantellidae) from Madagascar, with descriptions of five new species. Zoological Journal of the Linnean Society 133, 495-529.

- ., Vences, M. & Gossmann, V. 2000. A new species of Mantidactylus (subgenus Guibemantis) from Madagascar, with a comparative survey of internal femoral gland structure in the genus (Amphibia: Ranidae: Mantellinae). Journal of Natural History 34, 1135-1154.

Mattison, C. 1987. Frogs & Toads of the World. Blandford, London.

Meegaskumbura, M., Bossuyt, F., Pethiyagoda, R., Manamendra-Arachchi, K., Bahir, M., Milinkovitch, M. C. & Schneider, C. J. 2002. Sri Lanka: an amphibian hotspot.
Science 298, 379.

Vallan, D., Vences, M. & Glaw, F. 2003. Two new species of the Boophis mandraka complex (Anura, Mantellidae) from the Andasibe region in eastern Madagascar. Amphibia-Reptilia 24, 305-319.

Van Bocxlaer, I., Roelants, K., Biju, S. D., Nagaraju, J. & Bossuyt, F. 2006. Late Cretaceous vicariance in Gondwanan amphibians. PLoS ONE 1 (1): e74. doi:10.1371/journal.pone.0000074

Van der Meijden, A., Vences, M. Hoegg, S. & Meyer, A. 2005. A previously unrecognized radiation of ranid frogs in Southern Africa revealed by nuclear and mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 37, 674-685.

Vences, M., Vieites, D. R., Glaw, F., Brinkmann, H., Kosuch, J., Veith, M. & Meyer, A. 2003. Multiple overseas dispersal in amphibians. Proceedings of the Royal Society of London B 270, 2535-2442.