Welcome back, err, me! And, while I could have started with ‘here are the things I saw on holiday’, I became concerned that my list of bats and raptors might seem a bit mundane in comparison to what certain of my friends have encountered (wait until you see what Carel got to see). Anyway, to business. Tet Zoo regulars will know that I’ve had a thing about anurans (frogs and toads) recently (go here, here or here); the reasons for this will become clear soon enough. And to make things easier in the articles that will follow, I thought it might be a good idea to produce a short article on anuran phylogeny and diversity. That didn’t work, and it soon became a series of long articles. I will try to avoid all the family-level groups, otherwise things will certainly not be so short. Anurans have to be among the most incredible, charismatic and jaw-droppingly ridiculous of all tetrapods. Why? Well…
Consider how bizarre their skeletons are: anurans have (at most) nine presacral vertebrae, and some have as few as five; ribs are either highly reduced or absent; the radius and ulna are fused (forming the radioulna); the bones of the pectoral girdle are highly reduced and complimented by an assortment of new weird bits; the pelvis consists of a rod-like central unit (the urostyle) surrounded by two super-long, shaft-like ilia; and in their (generally) elongate hindlimbs, the tibia and fibula are fused (forming the tibiofibula) while the ankle bones are elongated to form a long ‘extra’ limb segment. This is one of the most modified skeletal plans in the whole of Tetrapoda: it is, we think, highly specialised for jumping, and the inheritance and retention of this bauplan means that anurans are, as a group, astoundingly uniform.
The diversity seen in anuran reproductive biology beggars belief. It’s true that the majority of anurans reproduce and develop in the manner that’s most familiar to us: pair mates and lays eggs in water, tadpoles emerge from eggs, tadpoles grow into little frogs, frogs leave water. But about 20 anuran lineages have evolved direct development where a free-swimming tadpole phase is skipped and a terrestrial egg develops into a terrestrial froglet. Others make bubble nests (these might be on the water surface, or in terrestrial vegetation), others carry their eggs wound round their hindlimbs, or carry their tadpoles, or their froglets, on their backs, others retain the developing babies in a pouch, submerged in specially grown skin on the back, in a vocal sac, or in the stomach (yes, stomach: adjacent image shows gastric-brooding frog Rheobatrachus silus in the act of ‘giving birth’. Discovered in 1973, it is apparently now extinct). Some exhibit parental care of eggs, tadpoles and/or froglets: some feed their babies on unfertilized eggs, and in some species males and females are pair-bonded and provide extended biparental care (Caldwell 1997). Individuals in some aquatic-spawning species practise clutch piracy: males actually grab freshly-laid egg masses and fertilize them (Vieites et al. 2004).
Amplexus – the behaviour in which a male grabs hold of a female in order to fertilize her eggs when they are expelled – is often assisted by special spiny nuptial pads on the hands, arms or chest; some round-bodied species use a secreted glue to remain in contact; in some of the South American harlequin toads (Atelopus), couples may remain in amplexus for several months. Internal fertilization has evolved in the North American tailed frogs (hey, that ain’t no tail baby), in some African bufonids (Nectophrynoides and perhaps Mertensophryne) and in some Caribbean leptodactylids (some Eleutherodactylus species). Most male anurans use vocal displays to attract females, but some indulge in combat, and the males of some anuran species exhibit curved spines on the hands or arms; members of many clades have evolved enlarged tooth-like structures in the lower jaws (these are called odontoids: with the exception of Gastrotheca, no anuran has a mandibular dentition) (Emerson & Ward 1998, Fabrezi & Emerson 2003). In contrast to the majority of anurans, the males of these spiny or fanged species are larger than the females.
Tadpoles aren’t all the same. Some [like the Xenopus tadpoles shown in the adjacent image] are filter-feeders with paired barbels at the corners of the mouth (or even multiple barbel-like structures [properly called barbellae], as in the burrowing toad Rhinophrynus); most possess keratinized beaks surrounded by rows of black, comb-like labial teeth and fleshy papillae. Species that inhabit fast-flowing water adhere to rocks with sucker-like discs on their mouths or bellies, and some cling to vertical waterfalls using these organs. Some tadpoles complete metamorphosis in a couple of weeks; others take years, and grow to a size that rivals that of their parents. And there’s so much more stuff to say about anurans… their ears, their vocal displays, their repeated evolution of skin toxicity, their repeated crossings of marine barriers, their excursions into arboreal and fossorial lifestyles, their sometimes projectile tongues, and so on and on. I’m telling you, there’s no end to the frickin’ awesomeness of frogs and toads.
While there have been occasional suggestions that some basal anurans (Ascaphus and Leiopelma) might have arisen separately from the other anuran groups, it is clear from their extremely characteristic anatomy that anurans are monophyletic. A few fossil ‘proto-anurans’ are known, the most basal of which are the Early Triassic taxa Triadobatrachus massinoti from Madagascar and Czatkobatrachus polonicus from Poland. These animals share a list of derived characters with extant anurans, including a short body, strongly reduced tail and elongate hindlimbs, but lack many others, including the radioulna, tibiofibula, reduced compliment of dorsal vertebrae and urostyle. The name Anura is currently used for the node-based clade that includes all extant anuran species, whereas the stem-based clade that includes Anura and all taxa closer to anurans than to other lissamphibians is termed Salientia (Ford & Cannatella 1993, Evans & Borsuk-Bia?ynicka 1998, Cannatella & Hillis 2004). The aim of the article here (and the following two or so) is to quickly review anuran diversity: I’ve tried to avoid getting into the highly complex historical stuff. Good historical reviews of anuran classification are provided by Ford & Cannatella (1993), Pugener et al. (2003), Cannatella & Hillis (2004) and Frost et al. (2006). Particularly good non-technical reviews of anuran diversity include those provided by Arak (1986), Mattison (1987) and Zweifel (2000). The standard work on the anuran fossil record is Sanchiz (1998).
Generally regarded as the most basal of anurans (although wait for the next article) are the North American tailed frogs (Ascaphus: adjacent pic shows A. truei) and the New Zealand frogs (Leiopelma). Whether the members of these groups should be classified together (in a group usually termed Ascaphidae, although Leiopelmatidae Mivart, 1869 has priority and Amphicoela was used in some of the older literature), or as entirely distinct, has proved controversial. Leiopelma shares derived characters with other aurans that aren’t present in Ascaphus (including long bony processes on the sternum and the route of the facial nerve), and Ford & Cannatella (1993) coined Leiopelmatanura for a clade that included Leiopelma and other anurans but not Ascaphus. Recent molecular evidence and a reassessment of the morphological data has led some authors to unite the two again (Gao & Wang 2001, Roelants & Bossuyt 2005, Frost et al. 2006). Despite their basal position within anuran phylogeny, both Ascaphus and Leiopelma are specialised and unusual, with such unique features as a male intromittent organ (in Ascaphus).
Also universally regarded as basal within anuran phylogeny are the fire-bellied toads, midwife toads, painted frogs and jungle toads or barbourulas, sometimes called the disk-tongued frogs for the obvious reason. Distributed across Eurasia and parts of northern Africa, these smallish (SVL 30-70 mm) anurans include both predominantly aquatic species (like the fire-bellied Bombina species, famous for exposing their vividly coloured undersides in a distinctive anti-predator display) as well as terrestrial forms (like the midwife toads Alytes, a group of European species that may mate away from water: the males then carry the strings of eggs wrapped around their hindlimbs, eventually depositing the tadpoles in water. See adjacent image).
Traditionally united as the Discoglossidae, synapomorphies uniting these species had never been identified until recently, and consequently it has been widely suspected that discoglossids are not monophyletic. Ford & Cannatella (1993) argued that fire-bellied toads and barbourulas should be classified in a distinct group, Bombinatoridae, and that discoglossids were more closely related to all ‘higher’ anurans, forming with them the clade Discoglossanura. However, monophyly of discoglossids (sensu stricto) and bombinatorids has been strongly supported by other studies (Haas 2003, Roelants & Bossuyt 2005, Frost et al. 2006) and Gao & Wang (2001) argued that characters of the vomers, clavicles, facial foramina and the elongate coracoid provided support for the monophyly of the traditional Discoglossidae. Some workers prefer the name Alytidae for discoglossids.
So that’s part I done, part II to follow next of course…
Refs – –
Arak, A. 1986. Frogs. In Halliday, T. & Adler, A. (eds) Animals of the World: Reptiles and Amphibians. The Leisure Circle (Wembley, UK), pp. 36-51.
Caldwell, J. P. 1997. Pair bonding in spotted poison frogs. Nature 385, 211.
Cannatella, D. C. & Hillis, D. M. 2004. Amphibians: leading a life of slime. In Cracraft, J. and Donoghue, M. (eds), Assembling the Tree of Life. Oxford University Press (Oxford), pp. 430-450.
Emerson, S. B. & Ward, R. 1998. Male secondary sexual characteristics, sexual selection, and molecular divergence in fanged ranid frogs of southeast Asia. Zoological Journal of the Linnean Society 122, 537-553.
Evans, S. E. & Borsuk-Bia?ynicka, M. 1998. A stem-group frog from the Early Triassic of Poland. Acta Palaeontologica Polonica 43, 573-580.
Fabrezi, M. & Emerson, S. B. 2003. Parallelism and convergence in anuran fangs. Journal of Zoology 260, 41-51.
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.
Gao, K.-Q. & Wang, Y. 2001. Mesozoic anurans from Liaoning Province, China, and phylogenetic relationships of archaeobatrachian anuran clades. Journal of Vertebrate Paleontology 21, 460-476.
Haas, A. 2003. Phylogeny of frogs as inferred from primarily larval characters (Amphibia: Anura). Cladistics 19, 23-90.
Mattison, C. 1987. Frogs & Toads of the World. Blandford, London.
Pugener, L. A., Maglia, A. M. & Trueb, L. 2003. Revisiting the contribution of larval characters to an analysis of phylogenetic relationships of basal anurans. Zoological Journal of the Linnean Society 139, 129-155.
Roelants, K. & Bossuyt, F. 2005. Archaeobatrachian paraphyly and pangaean diversification of crown-group frogs. Systematic Biology 54, 111-126.
Sanchiz, B. 1998. Salientia. Handbuch der Paläoherpetologie, Teil 4. Verlag Dr. Friedrick Pfeil, München.
Vieites, D. R., Nieto-Román, S., Barluenga, M., Palanca, A., Vences, M. & Meyer, A. 2004. Post-mating clutch piracy in an amphibian. Nature 431, 305-308.
Zweifel, R. G. 2000. Frogs and toads. In Cogger, H. G., Gould, E., Forshaw, J., McKay, G. & Zweifel, R. G. (consultant eds) Encyclopedia of Animals: Mammals, Birds, Reptiles, Amphibians. Fog City Press (San Francisco), pp. 516-545.