Of short-heads, shovel-snouters and squeakers: an afrobatrachian's tale (part I)

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Within the immense anuran clade termed Neobatrachia, we've so far gotten through the hyloids (see previous anuran article here: you'll need to read also the articles on basal anurans, transitional anurans, and ghost frogs and so on). All we have left is Ranoidea, but this is the biggest, most diverse, and most complex (and perhaps most interesting) anuran group. So here we go: we are at the beginning of the end...

Ranoidea has always been understood to include ranids ('typical frogs') and all the anurans closer to them than to hyloids, and several derived characters of the skeleton and musculature are shared by all ranoid groups. Ranoidea was defined as a node-based clade by Ford & Cannatella (1993), and proposed by them to include reed and lily frogs (hyperoliids), rhacophorid treefrogs, ranids, poison-arrow frogs (dendrobatids), shovel-snouted frogs (Hemisus), squeakers (arthroleptids), microhylids, and all other taxa that descend from the common ancestor of this lot.

The main character that's been used to unite ranoids is firmisterny (the condition where the epicoracoid cartilages meet along the ventral midline, rather than overlap: see the article on transitional anurans for explanation). This is somewhat problematical however because firmisterny seems to have evolved multiple times from different arciferal lineages. A diplasiocoelous vertebral column (viz, where both procoelous and amphicoelous vertebrae are present) has also been used as a distinctive derived character state of ranoids, but this is also problematical because some ranoids are entirely procoelous. Anyway, other characters uniting ranoids are present, and molecular studies consistently unite members of the group. While members of several lineages have certainly invaded and diversified within the New World, ranoids are mostly Old World neobatrachians.

Oh, another problem with ranoid monophyly is Ford & Cannatella's (1993) inclusion of poison-arrow frogs (Dendrobatidae) as a specifier within Ranoidea: as we saw in the previous article on hyloids, molecular data strongly indicates that poison-arrow frogs are hyloids. If we stick with Ford & Cannatella's (1993) phylogenetic definition of Ranoidea, this name would now be applied to a far more inclusive clade: this is so contrary to traditional usage that it's probably best to ignore their proposal and go with a more stable definition (Darst & Cannatella 2004). Frost et al. (2006) used the name Ranoides for the clade that most workers have called Ranoidea. There's an awful lot more that could be said about the historical usage of the term Ranoidea, but I think that discussion might be rather too specialised even for Tet Zoo readers.

Narrow-mouthed frogs

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Among ranoids, one of the biggest groups is the narrow-mouth frogs, or Microhylidae. Phylogenetic studies indicate that microhylids are somewhere round the base of Ranoidea, and they may belong in a clade that also includes the Afro-Madagascan hyperoliids, the squeakers, and an assortment of African anurans that we'll get to in a minute (Emerson et al. 2000, Cannatella & Hillis 2004, Bossuyt et al. 2006, Frost et al. 2006)... more on hyperoliids and squeakers later. Frost et al. (2006) coined the name Allodapanura for the ranoid clade that includes all of these diverse anurans [adjacent image shows the gastrophrynine microhylid Gastrophryne carolinensis of the eastern USA and Caribbean].

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Few people outside of lissamphibian research are familiar with microhylids, but this is one of the most diverse and widespread anuran groups: as of 2007, over 420 species in about 70 genera are recognized. They occur across the Americas, tropical Africa and Asia, Madagascar and Australasia. Most are smallish (SVL 10-50 mm), relatively short-legged, stout-bodied terrestrial, fossorial or arboreal frogs, and reasonably well known members of the group include the American narrow-mouthed toads Gastrophryne, the Asian painted frog Kaloula pulchra [shown in adjacent image], and the Red-banded rubber frog Phrynomantis bifasciatus [shown in image below]. Some Madagascan cophyline microhylids have rows of little horns over their eyes. Chris Mattison (1987) points out that the group includes some of the coolest names among anurans: wonders such as Relictovomer, Stereocyclops and Dasypops.

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All Australasian microhylids (representing the traditional subfamilies Asterophryinae and Genyophryninae) are direct-developers (the babies hatch from eggs as mini-adults, skipping the tadpole phase). But, in those microhylid species that do have tadpoles, the tadpoles are odd (and reminiscent of those of non-neobatrachians like pipoids) in lacking the keratinous beak and denticles that are typical of neobatrachian larvae, and in having a median spiracle. These are the 'Type II' tadpoles of Orton's classification scheme (see the previous article on transitional anurans for elaboration). Microhylid tadpoles also share several cranial characters that have been regarded as synapomorphies (Ford & Cannatella 1993) but, other than that, it's difficult to find derived characters that unite the 70-odd genera, and there is of course the problem that these larval characters can't be identified in the groups that exhibit direct development. Accordingly, microhylid monophyly has been doubted by some. Having said that, microhylid monophyly hasn't fared that badly in recent studies: of the 13 subfamilies traditionally recognised within the group (Scaphiophryninae, Asterophryinae, Genyophryninae, Brevicipitinae, Dyscophinae, Cophylinae, Gastrophryninae, Hoplophryninae, Kalophryninae, Otorphryninae, Melanobatrachinae, Microhylinae and Phrynomerinae), only brevicipitines have been found to be outside of Microhylidae (Blommers-Schlösser 1993, Van der Meijden et al. 2004, 2007, Frost et al. 2006).

The afrobatrachians

Arguably one of the most interesting discoveries within neobatrachian systematics is that microhylids are allied to a mostly African assemblage of ranoids: the reed and lily frogs (hyperoliids), the squeakers (arthroleptids), the pig-nosed or shovel-nosed frogs (hemisotids or hemisotines), and the short-headed or rain frogs (brevicipitines or brevicipitids) (Darst & Cannatella 2005, Bossuyt et al. 2006, Frost et al. 2006, Van der Meijden et al. 2003, 2005, 2007). A list of larval characters might be synapomorphies for this group, but the evidence which has mostly led to its recognition has been genetic. Van der Meijden et al. (2005) used the name Arthroleptoidae for this clade; Frost et al. (2006) named the clade Afrobatrachia.

Various anuran workers have loosely allied some or all of these taxa over the years, but the idea that they represent a clade restricted to the Seychelles, Madagascar and sub-Saharan Africa is now well supported. This supports the idea that ranoids (and hyloids, and neobatrachians in general) probably originated in the Southern Hemisphere, and indicates that the deep divergences within ranoids were driven by Cretaceous or early Cenozoic vicariance events (Bossuyt et al. 2006). In the case of afrobatrachians, it appears to have been the Cretaceous separation of Africa from the rest of Gondwana that resulted in their divergence.

Short-headed and shovel-nosed frogs: the xenosyneunitanurans (!!)


Probably near the base of the afrobatrachian radation are the short-headed or rain frogs (brevicipitines or brevicipitids), a group of five genera of round-bodied, short-limbed, fossorial African frogs. These frogs swell up when it rains and end up looking ridiculous - the adjacent picture shows a rain-holding Breviceps adspersus [an unswollen B. rosei can be seen in the top image at bottom left]. Like some round-bodied microhylids and southern frogs (myobatrachids), some short-headed frogs are the wrong shape to indulge in amplexus, and males and females instead adhere to each other by way of a secretion produced in the male's abdominal region. Says Mattison (1987, p. 82): 'the attachment is said to be so effective that any attempt to separate the frogs would result in damage'. The eggs are laid in a burrow and, guarded by the female, develop directly into froglets.

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Hemisotids - the nine species of pig-nosed or shovel-nosed frogs (Hemisus) - are odd little ant- and termite-eating afrobatrachians that possess fused vertebrae, lack a sternum, burrow head-first (highly unusual for anurans) using a bullet-shaped skull, and have a unique prehensile tongue that is 'telescoped' out of the mouth and has two muscular finger-like organs at its tip (Ritter & Nishikawa 1995) [you can watch a video of tongue action in Hemisus at Kiisa Nishikawa's website here: adjacent image taken from her site]. Males and females don't indulge in amplexus, and females dig an underground chamber where they lay their eggs. When the tadpoles hatch, the female excavates a tunnel that connects the chamber to a nearby pool, and the tadpoles then follow her to the water. If you can recall what the recently discovered purple Indian frog Nasikabatrachus sahyadrensis looks like (go here), you might understand why some anuran workers have suggested that it might be allied with hemisotids rather than with Seychelles frogs.

Frost et al. (2006) united brevicipitids with hemisotids in a new clade that has to have one of the most hideous names I've seen for a higher taxon: Xenosyneunitanura. The etymology is nice however (Xenosyneunitanura essentially means 'strange bed-fellow frogs'), and you have to commend the authors for naming a taxon that starts with 'Xeno-'. As we all know, names that start with 'Xeno-' are pretty much among the coolest in existence, and any authors bold and clever enough to name a taxon starting with 'Xeno-' are due immense accolade; they are the champions of their peers (all will become clear).

The rest of the afrobatrachians are to be covered next - well, in the next anuran article anyway. Huh, so much for getting through all neobatrachians in a single article.

Refs - -

Blommers-Schlösser, R. M. A. 1993. Systematic relationships of the Mantellinae Laurent 1946 (Anura Ranoidea). Ethology Ecology & Evolution 5, 199-218.

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.

Darst, C. R. & Canatella, 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. B., Richards, C., Drewes, R. C. & Kjer, K. M. 2000. On the relationships among ranoid frogs: a review of the evidence. Herpetologica 56, 209-230.

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.

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

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

Ritter, D. A. & Nishikawa, K. C. 1995. The kinematics and mechanism of prey capture in the African pig-nosed frog (Hemisus marmoratum): the description of a radically divergent anuran tongue. Journal of Experimental Biology 198, 2025-2040.

Van der Meijden, A., Kosuch, J., Glaw, F., Böhme, W. & Veith, M. 2003. Molecular phylogeny of hyperoliid treefrogs: biogeographic origin of Malagasy and Seychellean taxa and re-analysis of familial paraphyly. Journal of Zoological, Systematic and Evolutionary Research 41, 205-215.

- ., Vences, M., Hoegg, S., Boistel, R., Channing, A. & Meyer, A. 2007. Nuclear gene phylogeny of narrow-mouthed toads (Family Microhylidae) and a discussion of competing hypotheses concerning their biogeographical origins. Molecular Phylogenetics and Evolution 44, 1017-1030.

- ., 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. & Meyer, A. 2004. Novel phylogenetic relationships of the enigmatic brevicipitine and scaphiophrynine toads as revealed by sequences from the nuclear Rag-1 gene. Proceedings of the Royal Society B (Suppl.) 271, S378-S381.

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Does the 'Xeno-' rule apply to Xenonomia? That insect clade was named by Terry & Whiting (2005) to include the Mantophasmatodea and Grylloblattodea. The name means 'strange names' and refers to the fact that both these two small orders were named as combinations of two other orders ('mantis-stick insect' and 'cricket-cockroach', and neither is closely related to either one of the two orders it is named after.

[i]Ranoidea has always been understood to include ranids ('typical frogs') and all the anurans closer to them than to hyloids.... [A]nother problem with ranoid monophyly is Ford & Cannatella's (1993) inclusion of poison-arrow frogs (Dendrobatidae) as a specifier within Ranoidea: as we saw in the previous article on hyloids, molecular data strongly indicates that poison-arrow frogs are hyloids. If we stick with Ford & Cannatella's (1993) phylogenetic definition of Ranoidea, this name would now be applied to a far more inclusive clade: this is so contrary to traditional usage that it's probably best to ignore their proposal and go with a more stable definition (Darst & Cannatella 2004).[/i]

This seems like a textbook example of where a branch-modified node-based definition would be apropos. Why not this?:

"[i]Ranoidea[/i] is the final common ancestor of all extant* organisms sharing closer ancestry with [i]Rana temporaria[/i] Linnaeus 1758 than with [i]Hyla arborea[/i] (Linnaeus 1758), and all descendants of that ancestor."

* The exact meaning of "extant" would have to be clarified, of course.

Xenosyneunitanura - rolls off the tongue doesn't it :)

I notice you listed it's author(s) as Frost et al. (2006) - I just checked and I can see why you went with 'et al' - it seems this one was authored by half the planet - Frost, Grant, Faivovich, Bain, Haas, Haddad, de Sa, Channing, Wilkinson, Donnellan, Raxworthy, Campbell, Blotto, Moler, Drewes, Nussbaum, Lynch, Green & Wheeler, 2006

Regarding the node based definitions and the like - as far as I am concerned 'Death to the Phylocode and long live Linnaean binomials'!

Now I'll take cover - :)

[from Darren: at this point I'll mention that I'm a coauthor on two papers in the upcoming PhyloCode volume :) ]

By Mark Lees (not verified) on 12 Nov 2007 #permalink

Death to the Phylocode and long live Linnaean binomials

Ummm ... the PhyloCode uses Linnaean binomials (which would still be governed by the rank-based codes). See Arts 11 and (especially) 21.

By Mike Keesey (not verified) on 12 Nov 2007 #permalink

Dammit, I used BBCode instead of HTML in my first comment. The perils of frequenting multiple forums....

By Mike Keesey (not verified) on 12 Nov 2007 #permalink

The word monster should of course have been Xenosynunitanura, without the vowel cluster.

Phylogenetic definitions and binominals are orthogonal.

When the tadpoles hatch, the female excavates a tunnel that connects the chamber to a nearby pool, and the tadpoles then follow her to the water.

:-o Fantastic.

[from Darren: I've seen 'tadpoles follow mother' given as an autapomorphy of Hemisus.]

By David Marjanović (not verified) on 12 Nov 2007 #permalink

That name reminds me of Ritgen's (1829, I think) classification of "amphibians" (incl. reptiles), which included such wonderful names as Atryptodontopholidophides. For some reason, nobody else used this classification...

By Lars Dietz (not verified) on 13 Nov 2007 #permalink

(gad, hope I've finally figured out how to link properly)

You did! Unfortunately, comments are closed over there, so I'll have to lament over here that there are no chamaeleons in South America.

By David Marjanović (not verified) on 14 Nov 2007 #permalink

David wrote:

The word monster should of course have been Xenosynunitanura, without the vowel cluster.

Nope. In this case, the eu is a diphthong: Gk syneunetes 'bedfellow', from eune 'bed'. The clade name is misspelled, though; it should be Xenosyneunetanura.

Oh. I thought there was a mangled Latin unitas in there. Oops...

By David Marjanović (not verified) on 21 Nov 2007 #permalink