The wonder that is the internally fertilizing salamander clade: caudates part II

In the previous article, we covered Mesozoic stem-caudates, the cryptobranchoids, and the sirens. The latter are almost certainly part of the most diverse salamander clade, Salamandroidea (also named Salamandriformes or Diadectosalamandroidei), aka the 'internally fertilizing salamanders', or IFS clade (Larson & Dimmick 1993). You can guess from the name what makes the IFS clade a big deal (more on that in a second). Yes, I know you've all been waiting for this - it's finally time to cover the amphiumas, mudpuppies, waterdogs and olms, the mole salamanders, the lungless salamanders. Aww, hell, let's just get it over and done with before you burst an internal organ with excitement...

At, as usual, a risk of insulting my readership's intelligence: you might be wondering what the deal is with this 'internally fertilizing' thing, particularly given that male salamanders don't have an intromittent organ with which they can do their internal fertilizing. Rather, they produce a special, elaborately shaped sperm package (the spermatophore). Superficially, spermatophores looks like pure white handbags or shoes (well, I think they do anyway: insert hilarious joke about females being unable to resist collection of handbag- or shoe-shaped objects). The male deposits the spermatophore on the substrate, and it's then picked up by the female's cloaca (some salamanders do all of this on land, others on the floor of a pond or stream. Some species are, err, well stocked and can produce multiple spermatophores in fairly rapid succession). In order to get the female's cloaca to make contact with the spermatophore, the male has to guide or place the female correctly, and salamanders have evolved all kinds of tricks to make sure this happens. Once a female has absorbed the spermatophore's sperm-filled cap, she retains the sperm in special cloacal pockets called spermathecae, and it might be stored here for months or even years (by the way, at least one salamandrid breaks all the rules, and engages in cloacal contact during sperm transfer. What is it with evolution and its blatant disregard for rules and consistency?) [image at top shows Spanish sharp-ribbed newts Pleurodeles waltl with Banded newt Ommatotriton vittatus below].

Super-weird amphiumas

In the previous article we looked at the bizarre sirens. Also long-bodied and super-weird are the amphiumas, or amphiumids. They're represented by just three extant species in one genus (Amphiuma): all are restricted to the south-eastern USA, and fossil genera show that the group has been present in North America since the Upper Cretaceous at least (Gardner 2003). Like sirens, amphiumas are eel-like, neotenic salamanders that lack eyelids, but unlike sirens they possess hindlimbs and don't have external gills. They have rather long skulls with unusually textured bone in the facial region and, unlike sirens, practise internal fertilization. The alternative name 'congo eel' (often misunderstood as 'conger eel' by laypeople: the real conger eels really are, of course, eels) is particularly dumb, given that they aren't eels and don't come from the Congo or anywhere near it. Amphiumas are reportedly of unpleasant temperament and are said to bite savagely. My mate Jon (yes, Jon Downes of the CFZ) once owned one which he discovered in a pet shop in Enfield, though sadly it died before reaching the epic length he hoped it might. He named it Cuddles.

Surprisingly perhaps, amphiumas have been found to be the sister-group to the plethodontids in some studies (Wiens et al. 2005), and both groups were allied in the newly named clade Xenosalamandroidei by Frost et al. (2006). Yay, another 'xeno' name [reference]. Incidentally, Edward Cope thought that amphiumas were ancestral to caecilians.

Mudpuppies, waterdogs and olms

Also aquatic and neotenic are the proteids: the mudpuppies, waterdogs and olms. Like amphiumas but unlike sirens and cryptobranchoids, proteids practise internal fertilization and are definitely parts of the IFS clade. They have bushy external gills, laterally compressed tails and lack maxillae (sirens also have reduced maxillae). Only two extant genera are recognised - Necturus from North America (the mudpuppies and waterdogs) and Proteus from Europe (the olms). Fossil taxa take the group back to the Palaeocene (Estes 1981). Proteid monophyly has been found to be questionable in some studies (Weisrock et al. 2005) but supportable in others (Trontelj & Goricki 2003, Wiens et al. 2005, Frost et al. 2006) [image below shows Mudpuppy N. maculosus. I have a toy one: see it here].

Olms used to be regarded as uniquely cave-dwelling, but we now know of a surface-dwelling form, the Black olm P. anguinus parkelj. For a more detailed look at olms, there's a ver 1 post here. Proteids have been variously shuffled about the salamander family tree, but some recent studies have found them to be the closest relatives of the sirens (Gao & Shubin 2001, Frost et al. 2006): Frost et al. used the name Perennibranchia Latreille, 1825 for the siren-proteid clade. If this position for sirens is correct, the fact that they practise external fertilization must mean that they've lost the derived conditions of internal fertilization and spermatophore production. They also lack spermathecae, and this absence must also be a reversal.

Axolotls and their friends and relatives

The 33 species of mole salamander, or ambystomatids, derive their name from their predominantly fossorial habits and are robust-bodied North American salamanders, some of which - like the Tiger salamander Ambystoma tigrinum - are large (reaching 40 cm) and brightly coloured. Particularly well known is the fact that some, like the Axolotl A. mexicanum, are neotenous and aquatic. While the Axolotl is abundant as a pet and laboratory animal, the wild population - endemic to Mexico's Lake Xochimilco - is in danger. Two mole salamander species are particularly odd in that they consist only of females.

Dicamptodon, the four species of Pacific giant salamander ('giant' = 30 cm), is included by some workers in Ambystomatidae, but has been regarded by others as worthy of its own 'family' (Dicamptodontidae). It has a particularly solid-boned skull and blade-like teeth and is said to be a voracious predator of smaller salamanders, rodents and small snakes [adjacent image shows D. tenebrosus... and mouse]. Surprisingly, it's a pretty good climber and has been seen clambering about in vegetation 2.4 m off the ground (Stebbins 1966). Fossil dicamptodontids go back to the Palaeocene (in fact Dicamptodon itself goes back this far), with a couple of taxa being European: Rocek (1994) said that these are dicamptodontids 'beyond any doubt' (p. 53), but in an in-press article on Miocene European urodeles, Márton Venczel notes that there is doubt about this for some of the taxa concerned. Incidentally, one of the European taxa is Bargmannia Herre, 1955, but by googling this name I've learnt that it's preoccupied by the siphonophore Bargmannia Totton, 1954 (ha - one year!).

Rhyacotritonidae, named only for the semi-aquatic torrent salamanders Rhyacotriton from the north-western US and previously grouped with Dicamptodon, might instead be closer to amphiumas and/or plethodontids. In contrast to most ambystomatids and dicamptodontids, torrent salamanders are small (total length 10 cm or less) and with poorly ossified skulls, wrists and ankles. They're animals of cold mountain streams and seepages, often found in splash zones or wet mossy places.

The lungless salamanders

Plethodontids - the mostly American lungless salamanders - are the most speciose (c. 380 species) and most diverse salamander group with aquatic, terrestrial, fossorial, cave-dwelling and even arboreal species. The smallest salamanders, those of the genus Thorius, belong to this group and may be adult at just 30 mm in total length (yes, including the tail... hence 'total' length). They lack lungs entirely, with all respiration occurring across the skin and membranes of the pharynx. Vertical grooves running the length of the body - the costal grooves - draw moisture up around the body, helping the skin remain moist. Phylogenetic studies show that plethodontids have done some freaky things in their evolution, with reversals and rampant convergence being well documented in some lineages: I previously covered some of this stuff here and here [adjacent pic shows Northern red salamander Pseudotriton ruber ruber. Despite its colour it's often said not to be poisonous and to mimic the toxic red eft stage of the salamandrid Notophthalmus viridescens. This might not be true though, as red salamanders do secrete toxins and are unpalatable to at least some potential predators (Brandon et al. 1979)].

Some plethodontids escape from predators by tucking in their limbs and rolling downhill, others have ballistic tongues or highly sensitive binocular vision. The Painted ensatina Ensatina eschscholtzi can actually squirt venom from the base of its tail directly at an attacker (it aims for the eyes). The venom jets can be over 2 m long, and in humans a direct hit is said to result in excrutiating pain and temporary blindness (Carwardine 1995). Plethodontids are not just really interesting, but have also proved really instructive in terms of what they've taught us about speciation, hybridisation, species concepts and how evolution works. Much of this research has been produced by University of California's David B. Wake and his colleagues and students: his lab's webpage (with many free pdfs) is here.

We saw previously that some salamanders (the sirens) appear to be facultative herbivores. Equally remarkable is the claim that some plethodontids are fungivores: if, that is, observations reported by Miller (1944) are correct. Miller wrote that the Santa Cruz black salamander Aneides flavipunctatus niger (recognised as a full species by some workers) ate the fruiting bodies of fungi, and it's been suggested that other Aneides species might do likewise. However, there is some scepticism about this, and other salamander workers haven't reported the same behaviour (to my knowledge) [adjacent image shows Speckled black salamander A. f. flavipunctatus adult and babies: I couldn't find any Santa Cruz black salamander freely available for use].

Plethodontids are not uniquely American, as the European cave salamanders also belong to this group. Furthermore, a really amazing recent discovery is that this group also exists in Asia: to date, only one Asian species belonging to the group is known - the Korean crevice salamander Karsenia koreana Min et al., 2005 (I blogged about it on ver 1 here) - but it's possible and perhaps likely that additional Asian species await discovery. The plethodontid fossil record isn't great, extending back to the Miocene in both North America and Europe.

Salamandrids: ribs as weapons, viviparity, sex aids

To many people, the most familiar of salamanders are the salamandrids: the mostly North American-Eurasian group that includes the newts and the familiar Fire salamander Salamandra salamandra and its relatives. There are about 75 living species. Some studies have found salamandrids to be close kin of mole salamanders (Larson & Dimmick 1993, Frost et al. 2006); others have allied them with plethodontids (Gao & Shubin 2001). Salamandrids are generally amphibious, terrestrial outside of the breeding season, and often with poisonous skin glands and brightly coloured undersides. Some species (most famously the North American Taricha newts) are among the most poisonous of amphibians, and some perform a special contorted display - called an unkenreflex - to show off the vivid reds, oranges or yellows they have on their bellies. Neoteny occurs in some populations of some species, and viviparity has been evolved within two lineages. There's a lot of really neat stuff to say about them (as you might guess from the subtitle above): I've written lots, but it made this article too long so I've decided to leave it for later. If you can't wait until then there's the article about newts here. The adjacent photo is of Frobie, my frozen French Fire salamander. Poor beast, he was a road casualty.

So there we have it. Congrats if you made it this far (say 'I did' in the comments so I know you did and that it was all worth it) - we can now say that we've gotten through both caecilians and caudates. As for anurans, well... there's still just enough time to get them finished before the deadline. This is going to be a stupidly hectic week, with at least three scheduled announcements set to appear here at Tet Zoo.

Finally, I am reliably informed that series 2 of Primeval started over the weekend. As per just about every episode last year, Will and I were out and about while it was on and missed it. During the making of the series (recall that I worked at Impossible Pictures during 2007), we joked about the possibility of somehow getting Tet Zoo featured in the background (on a PC or laptop screen of course). While on the subject of TV, you will all know of course that David Attenborough's series on amphibians and reptiles, Life in Cold Blood, starts screening later this month. I don't like the title but, whatever, I'm sure it will be excellent. And given that you're all now fired-up and excited about the amazing world of amphibians, you will all remember to tell your friends, relatives and colleagues that 2008 is...... Year of the Frog!!!

Refs - -

Brandon, R. A., Labanick, G. M. & Huheey, J. E. 1979. Relative palatability, defensive behavior, and mimetic relationships of Red salamanders (Pseudotriton ruber), Mud salamanders (Pseudotriton montanus), and Red efts (Notophthalmus viridescens). Herpetologica 35, 289-303.

Carwardine, M. 1995. The Guinness Book of Animal Records. Guinness Publishing, Enfield, Middlesex.

Estes, R. 1981. Handbuch der Paläoherpetologie. Teil 2. Gymnophiona, Caudata. Gustav Fischer Verlag, Stuttgart.

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.

Gardner, J. D. 2003. The fossil salamander Proamphiuma cretacea Estes (Caudata; Amphiumidae) and relationships within the Amphiumidae. Journal of Vertebrate Paleontology 23, 769-782.

Gao, K. & Shubin, N. H. 2001. Late Jurassic salamanders from northern China. Nature 410, 574-577.

Larson, A. & Dimmick, W. W. 1993. Phylogenetic relationships of the salamander families: an analysis of congruence among morphological and molecular characters. Herpetological Monographs 7, 77-93.

Miller, L. 1944. Notes on the eggs and larvae of Aneides lugubris. Copeia 1944, 224-230.

Rocek, Z. 1994. A review of the fossil Caudata of Europe. Abhandlungen und Berichte für Naturkunde 17, 51-56.

Stebbins, R. C. 1966. A Field Guide to Western Reptiles and Amphibians. Houghton Mifflin Company, Boston.

Trontelj, P. & Goricki, S. 2003. Monophyly of the family Proteidae (Amphibia: Caudata) tested by phylogenetic analysis of mitochondrial 12S rDNA sequences. Natura Croatica 12, 113-120.

Weisrock, D. W., Harmon, L. J. & Larson, A. 2005. Resolving deep phylogenetic relationships in salamanders: analyses of mitochondrial and nuclear genomic data. Systematic Biology 54, 758-777.

Wiens, J. J., Bonett, R. M. & Chippindale, P. T. 2005. Ontogeny discombobulates phylogeny: paedomorphosis and higher-level salamander relationships. Systematic Biology 54, 91-110.