Did I mention that 2008 is Year of the Frog? Just kidding. In actuality, the conservation effort so many of us are now involved in doesn’t just concern anurans (frogs and toads), but all the living amphibian groups: as you’ll know, there are, besides anurans, two other such groups. We looked previously at the bizarre caecilians. This time round we get through the last group of the three: the caudates, or salamanders, of which there are about 560 living species. Again, these animals are anything but boring. Yes, this is that group that, believe it or don’t, includes species that have evolved beaks, are partially herbivorous, can be extremely tolerant to cold, and – in the big species – can easily bite open a human hand…
Most salamanders are small, but some species have approached or exceeded lengths of 2 m. Beaks, crushing teeth, claws, prehensile tails, reduced-limbed, eel-like body shapes, and ribs that literally protrude through the skin have all been evolved by caudates. Intra-uterine cannibalism, neoteny, the defensive shedding of tails and limbs, weird developmental shifts in digital development, bizarre warning displays, lekking and nuptial dancing, facultative herbivory and fungivory, dedicated cave-dwelling… it’s all here. The term caudate means ‘possessing a tail’ and, in contrast to anurans and caecilians, salamanders retain the body shape that seems to have been plesiomorphic for lissamphibians. Having said that, even salamanders exhibit a list of anatomical specialisations that make them unusual compared to other tetrapods: they’ve lost a long list of skull bones that are present in other amphibians (including the postorbitals, jugals, tabular, supraoccipital and ectopterygoids), and also lack a middle ear (though they’re not deaf). Bizarrely, salamanders have disproportionately large amounts of DNA [image at top shows a mole salamander in characteristic head-butting posture. More on all that later].
Salamanders are generally Laurasian and the groups that occur on the southern continents (there are plethodontids in South America and some salamandrids in northern Africa) have only gotten there comparatively recently. An important theme which has cropped up several times independently within different salamander clades is neoteny: the retention of juvenile characters into sexual maturity. It’s been widely suspected that neoteny results in the retention of confusing plesiomorphic characters, and in extensive convergence, so working out the relationships of neotenous salamander clades has been difficult (Wiens et al. 2005). Phylogenetic studies on salamanders have in fact differed pretty radically in the relationships they infer, though a rough consensus has started to emerge.
The oldest salamanders we know of are Middle Jurassic forms from central Asia (Kokartus honorarius) and England (two species of Marmorerpeton). What we know indicates that these basal forms looked superficially like stout-bodied living forms, but they lacked various bony and muscular characters present in the crown-group. The best known basal salamander – Karaurus sharovi from the Upper Jurassic of Kazakhstan [shown in adjacent image] – has been compared to living mole salamanders (ambystomatids) and probably lived in a similar manner (Estes 1981). Whether the name Urodela is restricted to the crown-group, with Caudata used for the total-group, or whether the name Caudata is restricted to the crown-group, with Urodela used for the total-group, depends on which authors you pay attention to. Evans & Milner (1996) argued that it made better sense to use Caudata for the total-group for several reasons, and this seems to have been mostly followed and is used here. So Marmorerpeton and the karaurids Kokartus and Karaurus are stem-caudates but not urodeles, and a few other Mesozoic taxa, like Pangerpeton and Jeholotriton from the Jurassic or Cretaceous of Liaoning Province in China, are too (Wang & Evans 2006).
It has been argued that, even by the Middle Jurassic, crown-group salamanders had appeared and started to diversity: this would be so if one recently named taxon, Chunerpeton tianyiensis, has been correctly interpreted (Gao & Shubin 2003), and if the sediments it comes from are Middle Jurassic in age and not younger as has been argued (Marjanovi? & Laurin 2007). Chunerpeton was described as a cryptobranchoid (explanation on that term below), in which case members of both of the youngest major salamander clades, Cryptobranchoidea and Salamandroidea (aka Salamandriformes, or Diadectosalamandroidei), had both appeared by this time (given that both are sister-taxa). Fossil members of Salamandroidea (or at least of its stem) are known from the Upper Jurassic: the best preserved being little Iridotriton hechti from the Morrison Formation (Evans et al. 2005). By the Upper Cretaceous, members of most or all of the living salamander ‘families’ had probably appeared.
In an effort to do the same thing I did with anurans (and have yet to complete!), here is a quick run-through of all the salamander clades (though not all the ones known only as fossils). You should see this as A Beginner’s Guide to Salamander Diversity, though a fairly advanced beginner’s guide if you get my meaning. I’ve tried desperately not to get distracted too much, nor to get into the minutiae like taxonomy, phylogeny or fossil history. Here we go.
Cryptobranchoids: giant salamanders and Asiatic salamanders
Two particularly primitive groups of salamanders are still around today: the hynobiids and the cryptobranchids. Hynobiids, generally just called Asiatic salamanders, are a poorly known group of about 50 species that occur from Afghanistan and Iran eastwards to Japan, though from the Miocene and into the Pleistocene they also occurred in Europe (Venczel 1999). Some hynobiids occur in cold parts of northern Asia and are particularly cold-tolerant, being able to withstand freezing at temperatures below -50°; C for months at a time (that is, they literally get frozen alive and stay dormant in a block of ice). Some species employ aquatic suction feeding while others have a projectile tongue, and some (like Onychodactylus) have evolved claw-like structures on their digit tips [in the adjacent image, the animal at the bottom is O. japonicus. You can just see its claws. The species at the top is Hynobius nigrescens]. A recent study of hynobiid phylogeny and biogeography indicated that, following its origin in China, the history and distribution of the group was mostly controlled by local geological effects like the desertification of Mongolia and the uplift of the Tibetan plateau (Zhang et al. 2006).
Grouped with hynobiids in the clade Cryptobranchoidea (or Cryptobranchiformes), are the giant salamanders, or cryptobranchids. There are only three extant species (the North American Hellbender Cryptobranchus alleganiensis, the Chinese giant salamander Andrias davidianus and Japanese giant salamander A. japonicus); all are salamanders of fast-flowing, well-oxygenated water (but this wasn’t the case for all fossil species). All possess dorsoventrally flattened bodies. Gills are absent in the adults and their lungs apparently don’t function in respiration, so all gas exchange occurs across the extensively folded, wrinkled skin. Eyelids are absent (a sure sign of aquatic habits in a caudate).
Giant salamanders are famous for, well, being giant, with record-holding specimens of the Chinese giant salamander reaching 1.8 m and 65 kg (some fossil species were bigger, with A. matthewi from Miocene North America reaching 2.3 m). Little known is that they have particularly vicious teeth, exude a foul smell which has been partially likened to ‘the rankest public urinal crossed with that of stale sweat’ (Brazil 1997, p. 64), and that the males brood the eggs. Giant salamanders can inflict massive wounds with their teeth: during territorial fights males frequently sever digits, limbs, and bits of tails of rivals, and massive fatal slices across the neck – sometimes resulting in decapitation – are apparently not uncommon. We’ll be coming back to giant salamanders in a later article.
Chunerpeton from the Jurassic of China (mentioned above) has been identified as a cryptobranchid, in which case both this group and its sister-taxon Hynobiidae have been around for a long time. Chunerpeton seems to have been reasonably large – about 200 mm long – but of course not ‘large’ by comparison with the Cenozoic species.
The amazing sirens
Several features support the view that cryptobranchoids are primitive relative to the other crown-group salamanders, the salamandroids. Unlike more derived salamanders, cryptobranchoids still possess an angular bone in the lower jaw, and they also practise external fertilization. Some studies indicate that cryptobranchoids are not alone in being outside of Salamandroidea (or Salamandriformes, or Diadectosalamandroidei), but that the bizarre sirens belong here too (Wiens et al. 2005). Sirens (Sirenidae) are perhaps the strangest salamanders: indeed, at times they’ve even been excluded from Caudata and put on their own as the Trachystomata, or Meantes. Superficially eel-like, neotenic animals that lack a pelvis and hindlimbs, they possess external gills, lack eyelids, are adept at burrowing in mud, and reach 95 cm in the largest species (Siren lacertina, the Greater siren: shown in adjacent pic, borrowed from USGS). The Cretaceous siren Habrosaurus reached 1.6 m.
The big surprise for many people is that sirens have a horny beak and pavements of teeth on the palate. The beak forms a broad platform inside the jaws, and the jaw joint is ventrally displaced relative to the rest of the skull. All of these features are adaptations for crushing, and field studies show that sirens specialize in feeding on gastropods and bivalves. Sirens also appear to be partially herbivorous, ingesting vascular plants and algae. They have enlarged hindguts that may house symbiotic microbes (Pryor et al. 2006). If this is correct it’s a big deal and would make them unique among caudates. They are also unusual in that they can survive desiccation by forming a sort of mucus cocoon in the mud, a habit very similar to that better known for lungfishes. Oh yeah, and they emit a yelping noise when grabbed (Halliday & Verrell 1986). Sirens have a fossil record extending back to the Upper Cretaceous, and while the extant species are all North American, fossil representatives have been described from Sudan, Germany, India and Bolivia. However, the identification of all of these fossils as sirenids has recently been challenged (Gardner 2003) [image below shows the Lesser siren S. intermedia].
Ok, gotta stop there. I have a horrible feeling this is all going to take longer than planned, but I next need to get through amphiumas, proteids, mole salamanders, salamandrids and plethodontids. Surely that can’t be difficult…
Refs – –
Brazil, M. 1997. Mission massive. BBC Wildlife 15 (4), 62-67.
Estes, R. 1981. Handbuch der Paläoherpetologie. Teil 2. Gymnophiona, Caudata. Gustav Fischer Verlag, Stuttgart.
Evans, S. E., Lally, C., Chure, D. C., Elder, A. & Maisano, J. A. 2005. A Late Jurassic salamander (Amphibia: Caudata) from the Morrison Formation of North America. Zoological Journal of the Linnean Society 143, 599-616.
– . & Milner, A. R. 1996. A metamorphosed salamander from the early Cretaceous of Las Hoyas, Spain. Philosophical Transactions of the Royal Society of London B 351, 627-646.
Gao, K. & Shubin, N. H. 2003. Earliest known crown-group salamanders. Nature 422, 424-428.
Gardner, J. D. 2003. Revision of Habrosaurus Gilmore (Caudata; Sirenidae) and relationships among sirenid salamanders. Palaeontology 46, 1089-1122.
Halliday, T. R. & Verrell, P. 1986. Salamanders and newts. In Halliday, T. & Adler, A. (eds) Animals of the World: Reptiles and Amphibians. The Leisure Circle (Wembley, UK), pp. 18-29.
Marjanovi?, D. & Laurin, M. 2007. Fossils, molecules, divergence times, and the origin of lissamphibians. Systematic Biology 56, 369-388.
Pryor, G. S., German, D. P. & Bjorndal, K. A. 2006. Gastrointestinal fermentation in greater sirens (Siren lacertina). Journal of Herpetology 40, 112-117.
Venczel, M. 1999. Land salamanders of the family Hynobiidae from the Neogene and Quaternary of Europe. Amphibia-Reptilia 20, 401-412.
Wang, U. & Evans, S. E. 2006. A new short-bodied salamander from the Upper Jurassic/Lower Cretaceous of China. Acta Palaeontologica Polonica 51, 127-130.
Wiens, J. J., Bonett, R. M. & Chippindale, P. T. 2005. Ontogeny discombobulates phylogeny: paedomorphosis and higher-level salamander relationships. Systematic Biology 54, 91-110.
Zhang, P., Chen, Y.-Q., Zhou, H., Liu, Y.-F., Wang, X.-L., Papenfuss, T. J., Wake, D. B. & Qu, L.-H. 2006. Phylogeny, evolution, and biogeography of Asiatic salamanders (Hynobiidae). Proceedings of the National Academy of Sciences 103, 7360-7365.