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

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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

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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].

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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.

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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

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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.

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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

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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.


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I did. We had mudpuppies around when I was growing up, in East Tennessee. Or at least something we called mudpuppies - they weren't aquatic, or at least not solely aquatic; they'd walk around on the ground near the creeks. Quite large and brown.

Olm is my favorite. Spectacular European animal, but overlooked and so hard to see in captivity (any in zoos?). Why?

How a *** Olm can starve for nine years? Why nobody is interested - looks like incredible study topic for molecular biologists!

And do fire salamander embryos cannibalise in ureto? Or only sharks do it?

I did. There are no extant native urodeles (nor caudates) in the continent I inhabit, but a rumour of an Eocene fossil (no Google hits, likely a mistake or it would have been published by now), so apart from the odd pet axolotl (OK, reportedly they've gone feral too) and a few species in zoos (including an Andrias!) I haven't seen much of them. But in 1993 I was on a palaeo field trip to the Alps out of the Institut fuer Palaeontologie in Bonn, and when visiting a Triassic bituminous limestone outcrop on the Swiss-Italian border in a rather exciting thunderstorm I came across a large Fire salamander on the forest path. Some things stick in the memory.

By John Scanlon, FCD (not verified) on 14 Jan 2008 #permalink

I did and it was a wonderful ride.

I did, 'cause these are some of my favorites.
I kept an amphiuma for many years (and gave it to somebody who may well still have it). That thing was dumb as a post but reacted spectacularly when pinky mice were dropped in the tank. Scared the shit out of many an undergraduate.
I was fortunate to see Proteus years ago in the Postojna cave in Slovenia (then still Yugoslavia), where the barely-English-speaking tour guide called them "human fish." Oh so weird and oh so cool.
OK. Ensatina squirting venom for 2m from the base of the tail???? I don't believe this. For one thing, I can't find a reference to this anywhere (sorry, the Guiness Book of Records is not a good enough source for me), for another, I have personally collected dozens of Ensatina in California, including some of the most colorful varieties, and have never been squirted. Further, this would be an interesting enough behavior that you'd think Robert Stebbins, who probably collected more Ensatina than everybody else in the world combined, would have mentioned it somewhere. He didn't. So I'm calling bullshit. I was happy to be proven wrong about siren herbivory but I'd put money on this one.
Salamanders are cool enough without making shit up.

By Sven DiMilo (not verified) on 14 Jan 2008 #permalink

I did.

By Peter Lund (not verified) on 14 Jan 2008 #permalink

I did too.

We have neotenic tiger salamanders here in New Mexico, as well as "normal" ones. People use them for catfish bait. But will someone tell me how they get into metal, above- the- ground cattle watering tanks??

Sven: I somehow don't think that Mark Carwardine (I don't know if you know who he is, but he's a pretty respected naturalist) made up the stuff about venom-squirting in Ensatina, though I am troubled that his book is the only publication I've seen that mentions this behaviour (and I also checked stuff by Stebbins, Wake and others). I'll ask him.

I did. Another great set of articles to follow on the anuran and caecilian series. Thanks!

I did.

I have to say it seems a bit harsh to accuse Darren of 'making shit up'! Not kindest words for the keeper of the worlds' best blog.

By Emma Mlikovski (not verified) on 14 Jan 2008 #permalink

Amphiumas are reportedly of unpleasant temperament and are said to bite savagely...

Indeed. The only scar I bear from an animal bite was inflicted by a small amphiuma some thirty years ago. It wasn't due to an unpleasant disposition, though, just over-excitement at feeding time.

I didn't accuse Dr. Naish of making shit up. He cited his source. Now as soon as we can find out the source's source, we can start figuring out who made it up. Or, more charitably, is confused.
Of course, I could be wrong...again...

By Sven DiMilo (not verified) on 14 Jan 2008 #permalink

I found some kind of statement that the European "dicamptodontids" are all just caudates incertae sedis, which is why we didn't include them in our paper, but I don't remember where that was. Venczel working on the problem is good news.

There is a vertebra from the Maastrichtian of Spain which is said to be either a plethodontid or a salamandrid. The only published illustration is hardly accessible, though.

It should be mentioned that the European cave salamanders (Speleomantes or Hydromantes (Speleomantes)) are limited to Sardinia and parts of the south slope of Italy. Elsewhere they haven't been seen since the Pliocene or early Pleistocene.

By David Marjanović (not verified) on 14 Jan 2008 #permalink

I did. And I'm just about to click on several of the enticing links you've provided.

I did. And just to make everyone jealous, I have had the great fortune of spending time every summer, for several years running, at a world hotspot for plethodontid species diversity.

One thing I've found rather interesting over the years is that with all of the crazy mating systems, neoteny, defense adaptations, and feeding styles in salamanders...not one (to my knowledge) has lost the tail. I mean, with all of the exceptions in biology we would expect at least one group of caudates to reject the title. Go figure.



By Mike Habib (not verified) on 14 Jan 2008 #permalink

Darren, you may enjoy the frog articles in the Atlanta Journal-Constitution: here and here.

Look for a gallery of frog photos at the link under the photo of the Blue Poison Dart Frog at the second link.

Very interesting post as usual. Salamanders, newts and their relatives are in general very underrepresented in popular literature, although they evolved some of the most remarkable abilities and oddities among tetrapods (those wheel-driving salamanders are just weird...).
And they show sometimes very strange behavior. Amphiuma tridactylum is reported to use its stumpy hind limbs to maneuvrate big pieces of food into the mouth. I have also seen fire salamanders doing very strange things, for example using the foot of one of the hind limbs to hold a big worm which was already trapped with its other end in the mouth to rip it apart. And sometimes they climb in vegetation. And sometimes they burrow in the ground. And they like it to shit while bathing.
BTW, if you need ever any further photos of Salamandra salamandra (salamandra), I have plenty of them, including full skin shedding and skin eating sequences.

Salamanders are fascinating. I've had the pleasure of owning a rather large...and also kind of dumb...tiger salamander for about a year now. He looks like a Muppet Show reject. I still can't figure out his cycle though...he'll disappear for weeks into the substrate, then wake up and want to be fed every day for a couple of weeks...then disappears again. Neither the average temp or light cycle seems to have changed. And yeah, I can attest to the biting...while I can't say that I noticed any teeth, once he clamps on it's pretty much just a waiting game...your arm in the tank, him dangling there until he gets bored and lets go.

I did. Thanks!

if Diplodactylus geckos can squirt from their tails, then so can ensatinas

What kind of logic is that?
Actually, now that you've reminded me of the gecko behavior (I knew it sounded familiar), I suspect it is at the root of the mix-up.

By Sven DiMilo (not verified) on 15 Jan 2008 #permalink

while I can't say that I noticed any teeth

Oh, they are there. Among amphibians, only toads in the strict sense are toothless.

By David Marjanovi? (not verified) on 15 Jan 2008 #permalink

OF COURSE I did! You have a way of proving that there are NO boring tetrapod clades.
Are you sure about:
the Tiger salamander Ambystoma tigrinum - are large (reaching 40 cm)
I thought I remembered reading that 20 cm (= 8 inches) was more like it.

By Allen Hazen (not verified) on 15 Jan 2008 #permalink

I did, and it was great!

From the "Caudates: Part I" thread:

Believe it or don't, there is a hypothesis positing the evolution of mammals (from mole-like ancestral forms) from amphisbaenians. I have yet to track down the reference...

Posted by: Darren Naish | January 14, 2008 8:59 AM

That is freaky fascinating, and if you run across the reference I'd like to know more.

By Stevo Darkly (not verified) on 15 Jan 2008 #permalink

>> What kind of logic is that?

Sorry, I wrote a misleading sentence. :(
What I meant was, given the weirdness of the system in geckos, reports of a less weird one in salamanders wouldn't be so far-fetched. Is that better?

I did, amazing amphibians.

Is there any adult amphibian which strongly resembles a typical larval tadpole? A young tadpole is a limbless amphibian with dorso-ventral flattening of the front but side to side flattening of the rear, are there any amphibians permanently like this? Do any salamanders go through a tadpole stage? Something seems to be missing, frogs can either have or not have a tadpole stage, is it the same for salamanders? Could early amphibian tadpoles have neonatally developed from mangrove mudskipper-like ancestors?

ps. I do like the strike-thru idea, but I don't know how to do it.

I did. Great writing, Darren. I agree with the poster above that a book should be considered. The lovely Banded Newt photo, alone, made my day.

I grew up in southeast Texas, near the Gulf, and I'm certain I've seen an Amphiuma tridactylum or two when I was wading around in bayous and ponds. Now I live in the Hill Country region of the same state, and we seem to be blessed with a plethora of Eurycea species: Blanco Blind Salamander, Barton Springs Salamander, Comal Blind Salamander, Cascade Caverns Salamander, etc. Though some sources state that all of the above are subspecies of the Texas Salamander, Eurycea neotenes. I'm not a taxonomist, but the species/populations in question are pretty isolated in their limestone caves and natural pools. It might just be that every Hill Country community or resort area wants its own salamander species. Anyway, I'll see if I can get some photos when the weather warms up a bit (shouldn't be long...not that it ever gets that cold here).

I did. Doesn't everyone? When I was wee lad some 50 years ago, tiger salamanders were so abundant that the roads between Bass and Rice lake were slippery in the early spring from the squashed bodies. Now, they are absent from the area. Drained vernal ponds and agricultural chemicals, I suspect.

By BlindSquirrel (not verified) on 17 Jan 2008 #permalink

Is there any adult amphibian which strongly resembles a typical larval tadpole?

Nope. (And "larval tadpole" is a repetition.)

Do any salamanders go through a tadpole stage?

Not really. The distinctive features of tadpoles are unique to frogs.

Something seems to be missing, frogs can either have or not have a tadpole stage, is it the same for salamanders?

Salamanders can have a larval stage or not, like frogs. The larva just never looks like a tadpole.

Could early amphibian tadpoles have neonatally developed from mangrove mudskipper-like ancestors?

No, why? Tetrapoda is a clade. This means it has one ancestor.

ps. I do like the strike-thru idea, but I don't know how to do it.

On ScienceBlogs with this font, you can't do it in the comments. No idea why. On Pharyngula, you write <strike> and </strike> around the text you want to strike through. Or wait... no, I think it's <s> on Pharyngula... I'll need to try it out again.

By David Marjanović (not verified) on 18 Jan 2008 #permalink

Hi, I have a salamander as a pet. I have had him for about a year as lng as I feed him and keep his tank clean he's perfectly happy. I think he makes a great pet for an older person. I'm Not older but still I like him.

(In case anyone wonders, it really is <s> in Pharyngula, <strike> outside of ScienceBlogs, and nothing works in the rest of ScienceBlogs.)

By David Marjanović (not verified) on 30 Nov 2008 #permalink

We just found a black salamander trying to enter my house. Number 1, is it toxic, number 2, I live in kelso, wa... WAY north of it's territory, what do I do with it now :) Randomly found your site. Thanks.

Astonishing stuff. Did anyone else think of Scrabble when they heard about olms? I know I did. ;-)

By John Wyatt (not verified) on 17 Nov 2010 #permalink