Sunday, June 04, 2006

Introducing the plethodontids

Some weeks ago I said in my olm post that I’d been thinking a lot about plethodontid salamanders, and was planning to post on them soon. Alas, a few things got in the way, not least of them being a little bit of phd research. So in the interest of keeping my promises I went back and dug out what I’d written on plethodontids. It’s actually quite a lot, and as has happened so many times, it now consists of too much text for one post. Expect several on plethodontids to appear in the future, therefore.

What are plethodontids? Often called lungless salamanders (for the obvious reason), they’re a predominantly American clade, consisting of over 280 species of terrestrial, aquatic, cave-dwelling and arboreal salamanders. They range in length from 40 to 325 mm: that upper limit is a pretty respectable size for a salamander, but they presumably can’t get much bigger than this for reasons of the surface area : volume ratio constraint discussed previously in connection with giant frogs. Conventionally allied with salamandrids, plethodontids may in fact be closest to amphiumas and rhyacotritonids. Uniquely among salamanders, many of them have evolved direct development: that is, the eggs hatch into miniature adults, and the larval phase has been skipped (read on for more on this).

They are also odd among salamanders in that some species can drop the tail as a predator-defence mechanism (properly called caudal autotomy), and in that some species have only four toes on the hindfeet. Some plethodontids curl up into a ball and roll downhill to escape predators (García-París & Deban 1995), a behaviour reported elsewhere in tetrapods among pangolins by the way (Tenaza 1975). While many species capture insects with a projectile tongue, Hydromantes supramontis (one of the European plethodontids) actually fires its tongue skeleton out of its mouth, with the tongue protruding for up to 80% of its body length during this act. It’s ‘the only vertebrate known to shoot part of the visceral skeleton completely out of its body as a projectile’ (Deban et al. 1997, p. 28).

North America has a high diversity of plethodontids, with 14 genera and c. 120 species. South America is home to about eight genera (some of which also occur in North America however) and c. 150 species. Note that, for reasons that will be discussed in another post, these figures are vague and hard to verify. One genus and one genus alone, Speleomantes, the cave salamanders, is present in Europe. Speleomantes Dubois, 1984 was previously included within Hydromantes Gistel, 1848, and whether the two should be considered distinct remains one of the most contested areas in plethodontid systematics (and a new name, Hydromantoides Lanza & Vanni, 1981, has been used by some authors for the American members of Hydromantes).

If Hydromantes and Speleomantes are the same genus, the distribution of this taxon is pretty odd: it occurs as relict populations in Italy, France and Sardinia, and then also in California. If these populations do belong to the same genus, then this is a pretty impressive example of so-called discontinuous distribution. The North American Hydromantes species are sometimes called web-toed salamanders.

When I was learning the herpetofauna of Europe as a teenager, Hydromantes (= Speleomantes) was always said to include just two species (H. italicus Dunn, 1923 and H. genei (Temminck & Schegel, 1838)). Recent studies have led to the resurrection or naming of a further five species (H. ambrosii Lanza, 1955, H. strinatii Aellen, 1958, H. imperialis Stefani, 1969, H. supramontis Lanza et al., 1986 and H. flavus Stefani, 1969), all of which can be distinguished morphologically (Griffiths 1995). Inhabitants of caves and rocky outcrops where there is running water, they’re pretty bizarre, with small sensory tentacles on the upper lip, an almost immobile lower jaw, an oval glandular swelling on the chin, partially webbed toes and a semi-prehensile tail. They’re good climbers and able to ascend even vertical surfaces, and H. imperialis ‘emits a strong smell’ apparently. We’ve already seen above the amazing projectile tongue some species possess.

Note that all of the European cave salamander species listed above, bar one, were named in the 20th century. New plethodontid species are routinely described from tropical America as well as from North America, including from well-studied ‘non-remote’ areas. Batrachoseps campi, described for the first time by Wake (1996), is from the San Gabriel Mountains: a location less than 50 km from downtown Los Angeles. A quick look at author dates for plethodontids reveals numerous recently named genera, among them Bradytriton Wake & Elias, 1983; Dendrotriton Wake & Elias, 1983; Nototriton Wake & Elias, 1983; Nyctanolis Wake & Elias, 1983; Ixalotriton Wake & Johnson, 1989; and Cryptotriton García-París & Wake, 2000. Some of these are long-known but have only recently been split from other genera, while others really are new discoveries. Incidentally, the ‘Wake’ listed there is David B. Wake, a leading expert on plethodontids at the University of California.

The presence in Europe of plethodontids is unusual enough (albeit well known), but the biggest surprise in plethodontid research has been the recent discovery of an Asian member of the group, the Korean crevice salamander Karsenia koreana Min et al., 2005 (the animal depicted in the photo above). First collected in 2003, Karsenia is a small, somewhat robust plethodontid that recalls Plethodon in overall appearance (Min et al. 2005). Its discovery indicates a long, and hitherto totally unknown, history of plethodontids in Asia, and the fact that only one Asian species is known suggests that rates of speciation were far lower among Asian plethodontids than they were among American ones. What next among the Asian herpetofauna – extant albanerpetontids?*

* For those who don’t know, that was a reference to the recent discovery of albanerpetontids from the Pliocene (Venczel & Gardner 2005).

All of this data on new species matches the species discovery rates recorded for other lissamphibian groups. A 13% increase in valid recognised lissamphibians occurred between 1985 and 1992, with a further 6% increase from 1992 to 1995. Glaw & Köhler (1998) correctly predicted that the extant number of valid lissamphibian species would exceed 5000 by the year 2000, and Hanken (1999) wondered ‘Why are there so many new amphibian species when amphibians are declining?’.

The phylogenetic arrangement of plethodontid clades is interesting. In the classic morphology-based phylogeny produced by Wake (1966), a basal desmognathine clade is sister to a far larger plethodontine clade that includes Hemidactyliini* (c. 25 species with aquatic larvae, including the genera Eurycea, Hemidactylium and so on), Bolitoglossini (c. 220 species lacking aquatic larvae, including the genera Bolitoglossa, Dendrotriton, Oedipina, Pseudoeurycea and so on) and Plethodontini (c. 55 species lacking aquatic larvae: the genera Aneides, Ensatina and Plethodon).

* This name was coined by Wake in 1966, and some have argued that it is a synonym of Mycetoglossini Bonaparte, 1850.

However, a recent molecular analysis (Mueller et al. 2004) rejected the monophyly of ALL of these groups with the exception of Desmognathinae (but rather than being the sister-taxon to Plethodontinae it was nested within this group, and within it the sister-taxon to a ‘Hydromantes’-Aneides clade). If this new phylogeny is valid (I should note by the way that Wake was on the authorship of Mueller et al., so it's not as if this study disagrees with his own research), it means that we have to re-assess the evolution of the different life history strategies seen in plethodontids. Wake argued that direct development had evolved twice in plethodontids (once within desmognathines and once again at the base of the bolitoglossin + plethodontin clade), and in both cases it had evolved from ancestors that possessed a larval stage.

But Mueller et al.’s (2004) cladogram favours more complex scenarios. They argued that at least four transitions from the possession of a biphasic life history to the presence of direct development had occurred. Furthermore, in at least one instance, the presence of a larval phase must have re-evolved from an ancestor with direct development: ‘a morphological transition rarely reported and previously considered unlikely’ (Mueller et al. 2004, p. 13823). That’s pretty incredible, but it’s perhaps not without precedent among lissamphibians as there are some indications that one group of marsupial tree-frogs may also have switched from direct development back to the possession of a tadpole stage.

This area was also considered by Chippindale et al. (2004): their phylogeny wasn’t as heterodox as that of Mueller et al. (2004), but they did agree on the recovery of desmognathines within Plethodontinae. Because desmognathines possess a larval stage, while the taxa around them in the new phylogeny are all direct-developing species, desmognathines simply must have re-evolved biphasic life history from direct development. So, as Chippindale et al. (2004) discussed, the reversal of direct development in plethodontine plethodontids shows yet again that complex features may be regained (they drew analogy with the re-evolution of wings in stick insects and of hindlimbs in snakes, though the evidence for the latter is still controversial).

Why re-evolve the larval stage however? Surely it’s good to stick with direct development once it’s evolved? Well, is it a coincidence that desmognathines occur in an area where plethodontid diversity is extremely high (with up to 11 direct-developing species occurring sympatrically), where non-desmognathine plethodontids dominate all ecosystems available to salamanders except for stream habitats, and in an area where direct-developing plethodontids are (get this) THE most important vertebrates in terms of biomass (Burton & Likens 1975)? Chippindale et al. (2004) therefore made a good case that desmognathines have re-evolved biphasic life history in order to exploit the ‘only’ available habitats, those represented by streams and streamsides, in regions densely packed with other plethodontid species. Desmognathines have clearly done well at this, sometimes occurring at densities of 6.9 individuals per square metre, and even evolving species that prey on direct-developing plethodontines.

That’ll do for starters. More on plethodontids some time in the near future. In fact, for the latest news on Tetrapod Zoology do go here.

The photo above depicts the Korean crevice salamander Karsenia koreana. It was taken by David Vieites and is widely available on the web.

Refs - -

Burton, T. M. & Likens, G. E. 1975. Salamander populations and biomass in the Hubbard Brook Experimental Forest, New Hampshire. Copeia 1975, 541-546.

Chippindale, P. T., Bonett, R. M., Baldwin, A. S. & Wiens, J. J. 2004. Phylogenetic evidence for a major reversal of life-history evolution in plethodontid salamanders. Evolution 58, 2809-2822.

Deban, S. M., Wake, D. B. & Roth, G. 1997. Salamander with a balistic tongue. Nature 389, 27-28.

García-París, M. & Deban, S. M. 1995. A novel antipredator mechanism in salamanders: rolling escape in Hydromantes platycephalus. Journal of Herpetology 29, 149-151.

Glaw, F. & Köhler, J. 1998. Amphibian species diversity exceeds that of mammals. Herpetology Review 29, 11-12.

Griffiths, R. A. 1996. Newts and Salamanders of Europe. T & A D Poyser, London.

Hanken, J. 1999. Why are there so many new amphibian species when amphibians are declining? Trends in Ecology & Evolution 14, 7-8.

Min, M. S., Yang, S. Y., Bonett, R. M., Vieites, D. R., Brandon, R. A. & Wake, D. B. 2005. Discovery of the first Asian plethodontid salamander. Nature 435, 87-90.

Tenaza, R. R. 1975. Pangolins rolling away from predation risks. Journal of Mammalogy 56, 257.

Venczel, M. & Gardner, J. D. 2005. The geologically youngest albanerpetontid amphibian, from the Lower Pliocene of Hungary. Palaeontology 48, 1273-1300.

Wake, D. B. 1966. Comparative osteology and evolution of the lungless salamanders, family Plethodontidae. Memoirs of the South California Academy of Sciences 4, 1-111.

- . 1996. A new species of Batrachoseps (Amphibia: Plethodontidae) from the San Gabriel Mountains, southern California. Contributions in Sciences of the Natural History Museum of Los Angeles County 463, 1-12.


Anonymous David Marjanović said...

What next among the Asian herpetofauna – extant albanerpetontids?

Please! Please! Please! :-)

Those reversals from direct development are funky indeed...

BTW, congratulations, Doc! I'm looking forward to reading your thesis while starting to work on my own.

10:12 PM  
Anonymous Anonymous said...

"[Some] curl up into a ball and roll downhill to escape predators
...‘the only vertebrate known to shoot part of the visceral skeleton completely out of its body as a projectile’... small sensory tentacles on the upper lip, an almost immobile lower jaw... and a semi-prehensile tail."

Holy crud. Who knew amphibians could be so /weird/?

Tongue bone? I knew about penis bones, but who ordered that?

An almost immobile lower jaw? How does it, um, eat?

Doug M.

9:20 AM  
Blogger Darren Naish said...

Thanks for comments. Response to Doug M: on lissamphibian weirdness, this isn't the half of it. Wait for future blogs. I don't want to give the game away.

'Tongue bones' are hyoids - they're actually in the floor of the mouth and all tetrapods have them (assorted throat and tongue muscles are attached to them).

Yup, the lower jaw is pretty much immobile (in Hydromantes/Speleomantes), but they get round this by having a mobile UPPER jaw! That is, the cranium rotates upwards relative to the jaw joint.

12:52 PM  
Anonymous David Marjanović said...

Doug, in humans, the (remaining ossified) hyoids have fused into a horseshoe-shaped bone that lies above the cartilage that forms the Adam's apple. So... imagine shooting out the whole apparatus from the tongue to the voice box.

And then there's the tongue retractor muscle that is anchored to the... pelvis.

4:52 PM  
Anonymous Anonymous said...

It's also worth noting that Hydromantes platycephalus was first described and named by Charles L. Camp, the famous University of California - Berkeley vertebrate paleontologist. Incidently, that publication and several others originated out of fieldwork he did as an undergrad at Cal.


1:39 AM  
Blogger Dorm said...

Interesting post-and nice to see the Korean Crevice Salamander which I was fortunate enough to discover some years ago(in 2001 actually). It's doing fine-seems to be common in many(if not all) localities found, which now number 23. God's best to all-Steve Karsen

11:03 PM  

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