Vertebral laminae in – shock-horror – eel-like salamanders
July 15, 2010
SV-POW! is, as I’m sure you know, devoted to sauropod vertebrae. But occasionally we look at other stuff… and you might have noticed that, in recent months, we’ve been looking at, well, an awful lot of other stuff. I’m going to continue that theme here and talk about salamanders. Yeah: not sauropods, not sauropodomorphs, not saurischians, and not even dinosaurs or archosaurs. But salamanders. Don’t worry, all will become clear. This all started back in May 2010 when I blogged about amphiumas over at Tet Zoo. Amphiumas are very unusual, long-bodied aquatic salamanders.
A Three-toed amphiuma _Amphiuma tridactylum_. Photo by Brad Moon.
As it happens, amphiuma vertebrae are particularly interesting if you work on saurischians because (drum-roll)… they have laminae. The term lamina is not restricted to structures present only in pneumatic saurischians: I would argue that it should be used for any sheet-like bony process on a vertebra, and I hope everyone agrees with me. Laminae are not common outside of Saurischia, but are present here and there: they’re present in stem-archosaurs (like Erythrosuchus), various crurotarsan archosaurs (including aetosaurs), some neosuchian crocodilians, and silesaurids (Desojo et al. 2002, Parker 2003, Nesbitt 2005, Wedel 2007, Butler et al. 2009). Even weirder, they’re present in Aneides lugubris, the Arboreal salamander of California and Baja California (Wedel 2007). But that’s about it.
Why would a salamander ‘want’ vertebral laminae? The laminae of the Arboreal salamander are presumed to be related to the extensive accessory ossification present in the skeleton of this animal, itself a consequence of adaptation to a peculiar climbing lifestyle. In other words, it’s hypothesised that the function (if I may be so bold as to use that word…) of the salamander’s laminae is nothing like that of the archosaurs that have them.
And now we know that A. lugubris isn’t the only salamander with laminae: amphiumas have them too. They’re clearly figured in the amphiuma literature (Gardner 2003), but (so far as I know) no-one has previously drawn attention to them when discussing archosaur laminae.
A mid-dorsal vertebra of _Amphiuma_, from Gardner (2003).
Gardner (2003) figured schematic amphiuma dorsal vertebrae that were based on a combination of features present in two of the three living amphiuma species (namely, Amphiuma means and A. tridactylum). On the lateral sides of the centra are structures that – if seen in an archosaur – would almost certainly be identified as anterior and posterior centrodiapophyseal laminae (using, as always, the nomenclature proposed by Wilson (1999)) [see the digram above, from Gardner (2003)]. There are also structures on the dorsal surfaces of the postzygapophyses that look something like laminae: they extend from the posterolateral parts of the neural arch and run across the tops of the postzygapophyses, hence recalling spinopostzygapophyseal laminae. Actually, I’ve just realised that similar structures are also sometimes present in anurans (frogs and toads) where they’ve been called paraneural crests or paraneural processes. These structures do have a ‘known’ function: in amphiumas they’re associated with complex dorsalis trunci epaxial muscles. Unlike the spinopostzygapophyseal laminae of saurischians, the structures in the amphibians are low ridges that don’t contact the neural spines, so it could be argued that they aren’t so lamina-like after all.
But what about the structures on the sides of the centra? Why are laminae present in a group of long-bodied aquatic salamanders? Why are laminae present at all? This question has been asked a few times here on SV-POW! (here, for example), and there are two primary hypotheses. One is that the laminae keep the various air sacs separate from each other, perhaps because they persist while much of the bone around them is resorbed during ontogeny, while the other is that they somehow provide mechanical support and are aligned along lines of stress (for more on this subject see the piece on finite element analysis).
An assortment of _Amphiuma_ cervical, dorsal and caudal vertebrae, from Gardner (2003). The 'paraneural crests' (the lamina-like structures on the postzygapophyses) are visible in G and L, and the lateral central laminae are visible in some of the other vertebrae figured here.
The pneumaticity explanation can’t work for amphiumas (given that they’re apneumatic): does the ‘mechanical support’ one apply instead? We don’t know anything about stress distribution in amphiuma vertebrae – in fact, I don’t think we know anything about the mechanics of amphiumas at all – but it’s possible that the laminae might play this role, especially given that amphiumas have to bend, twist and push with their bodies while excavating burrows.
In conclusion, we just don’t really know what’s going on here. In fact, all we can really do at the moment is wave our arms around a bit and say “Hey, amphiumas have vertebral laminae, too”, and that’s pretty much all I’m doing here. It’s also possible that the structures I’m talking about in amphiumas are very different in detail from the vertebral laminae present in archosaurs: I’ve never even seen a single amphiuma skeletal element and am basing all of this on photos and diagrams in the literature. Nevertheless, it’s something definitely worth bringing attention to. As usual, we stand poised at the abyss, straining our eyes to see into the infinite darkness ahead.
References
Butler, R. J., Barrett, P. M. & Gower, D. J. 2009. Postcranial skeletal pneumaticity and air-sacs in the earliest pterosaurs. Biology Letters 5, 557-60.
Desojo, J. B., Arcucci, A. B. & Marsicano, C. A. 2002. Reassessment of Cuyosuchus huenei, a Middle–Late Triassic archosauriform from the Cuyo Basin, west-central Argentina. Bulletin of the New Mexico Museum of Natural History and Science 21, 143–148.
Gardner, J. D. 2003. The fossil salamander Proamphiuma cretacea Estes (Caudata; Amphiumidae) and relationships within the Amphiumidae. Journal of Vertebrate Paleontology 23, 769-782.
Nesbitt, S. J. 2005. Osteology of the Middle Triassic pseudosuchian archosaur Arizonasaurus babbitti. Historical Biology 17, 19–47.
Parker, W. G. 2003. Description of a new specimen of Desmatosuchus haplocerus from the Late Triassic of northern Arizona. Unpublished MS thesis, Northern Arizona University, Flagstaff, AZ, 312 pp.
Wedel, M. J. 2007. What pneumaticity tells us about ‘prosauropods’, and vice versa. Special Papers in Palaeontology 77, 207-222.
Wilson, J. A. 1999. A nomenclature for vertebral laminae in sauropods and other saurischian dinosaurs. Journal of Vertebrate Paleontology 19, 639-653.
Sauropod Vertebra Picture of the Week 
July 15, 2010 at 11:11 am
Time someone sent Darren a dead amphiuma to dissect. Anyone out there have one handy? Anyone?
What, no-one?
July 15, 2010 at 11:14 am
Some of my colleagues (not mentioning any names) once found themselves with a dead amphiuma. The corpse was then involved in a bizarre practical joke involving a public toilet. Very funny, but what a waste of a good corpse.
July 15, 2010 at 11:19 am
[…] This post was mentioned on Twitter by Chris Rowan, JP – Research Lab. JP – Research Lab said: Vertebral laminae in – shock-horror – eel-like salamanders: SV-POW! is, as I’m sure you know, devoted to sauropod … http://bit.ly/dmokrX […]
July 15, 2010 at 8:20 pm
I doubt the joke would have been less effective had the spine been excised first. Shame on somebody.
When you call some structure a lamina, shouldn’t that imply it (is thought to have) developed by progressive thinning?
July 16, 2010 at 8:40 pm
“Laminae are not common outside of Saurischia, but are present here and there: they’re present in stem-archosaurs (like Erythrosuchus), various crurotarsan archosaurs (including aetosaurs), some neosuchian crocodilians, and silesaurids (Desojo et al. 2002, Parker 2003, Nesbitt 2005, Wedel 2007, Butler et al. 2009). Even weirder, they’re present in Aneides lugubris, the Arboreal salamander of California and Baja California (Wedel 2007). But that’s about it.”
Add _Homo sapiens_ to that list too. We have laminae on our vertebral arches. In fact a common practice for viewing the spinal cord in human cadavers, is to chop off the vertebral arches at the level of these laminae. A process fittingly called: a laminectomy.
July 18, 2010 at 8:55 am
Add _Homo sapiens_ to that list too. We have laminae on our vertebral arches. In fact a common practice for viewing the spinal cord in human cadavers, is to chop off the vertebral arches at the level of these laminae. A process fittingly called: a laminectomy.
All true. But the “laminae” of human vertebrae are quite different from the laminae of sauropods, salamanders, and sundry others. In human anatomy, the neural arch is divided into the pedicles, which extend from the centrum up to the zygs and transverse processes, and the laminae, which extend from those structures to the spinous process. So if we’re using lamina in that sense, then every vertebrate whose spinal cord is enclosed by bone has “laminae”.
In paleontology, laminae are taken to mean sheets of bone that connect the various apophyses of the vertebrae. Human and other mammalian vertebrae are made of fairly thick bony rami, as opposed to the collections of intersecting flat plates that pass for vertebrae in many sauropods and other archosaurs.
When you call some structure a lamina, shouldn’t that imply it (is thought to have) developed by progressive thinning?
Great question. The short answer is, no, some of them might have grown outward by accretion, and some of them probably represent a combination of both modes of development. The long, detailed answer is in this paper. An intermediate answer would make a pretty good SV-POW! post, if I can ever find the time.
August 18, 2010 at 2:03 pm
Useless comment of the day:
just thinking of the similarities of this salamander, hagfish and slugs. Something weird about them… but I haven’t had my coffee yet.
September 9, 2010 at 5:54 am
Some day, somebody oughta have a hard look at snake and other squamate vertebrae to see how much of this ‘lamina’ terminology can be applied. The terms currently used are various and not always clearly defined (e.g. is a ‘zygosphene’ a median process as Owen seemed to imply when describing Palaeophis in 1850, or one of a pair of lateral ones – as in many lizards – that sometimes coalesce?), and structures that lack names (like odd little ridges here and there) tend to get little attention in comparisons and diagnoses.
September 21, 2010 at 6:27 am
For lack of a better place to ask about nonsauropod (sort of) pneumaticity, I’ll post this here: I read a new paper about pathological pneumatization of the atlas vertebra in humans. It mentioned that the pneumatization in this case didn’t seem to be causing damage, so it got me wondering, is it possible that the vertebral pneumaticity in saurischians started out as a tendency to ‘pathological’ pneumatization that turned out not to be harmful after all, then was selected for? Could the mechanisms have been similar — or is there enough known about the origin of pneumaticity to rule out this possibly half-baked idea?
(The paper is available online at http://archotol.ama-assn.org/cgi/content/full/136/7/731 by the way)
September 21, 2010 at 7:29 pm
Cool, thanks for the link to the paper. I hadn’t seen that one, but I have cited other similar papers in my published work. And I have often wondered the same thing.
To me, the most amazing thing about postcranial pneumaticity in birds and other archosaurs is that the diverticula get out of the coelom, or body cavity. There are all kinds of developmental anomalies that lead to connections from the coelom to other spaces in the body, and usually they don’t turn out too well. I suspect that the early phases of the evolution of diverticula and pneumaticity didn’t provide any selective benefit but also no deficit. I infer the “no benefit” side because the diverticula would have been replacing too little tissue (bone or fat) to make a difference at first, and the “no deficit” side because if there had been any deficit, in the absence of a compelling benefit, one would expect diverticula to have gotten weeded out of the population. In evolutionary terms we would say that the primordial diverticula were “invisible to selection”, and in clinical terms we would say that they were “asymptomatic”.
In humans accessory bones of the foot are pretty common, and something like 30 different types have been catalogued. There are a couple that, if present, can impinge on nearby joints or tendons and cause pain, but the vast majority of accessory bones of the foot are asymptomatic, and their major clinical relevance is that they sometimes trick radiologists into thinking that something is wrong when in fact everything is okay. So these things are just evolutionarily floating along, mostly invisible to selection. If at some point in the future it becomes selectively advantageous to have them, they’ll be there, and in the meantime there is no selective pressure to get rid of them. The earliest diverticula might have worked that way, with the obvious difference that they did have a big selective payoff eventually, whereas accessory foot bones probably won’t.
But it’s good food for thought. A hypothetical Triassic physician might find that the lungs of one of his basal ornithodiran patients had herniated out of the body cavity and produced pneumatocoels up against the vertebrae. He’d probably call that a pathology, albeit a benign one. Where you get morphological discontinuities in evolution, some individual critter has to be the first to manifest the new thing, and compared to the rest of the population or species, that individual is abnormal. But the same developmental processes that produced the first individual may produce others in the same population, and these may be the seeds of new species and ultimately new higher taxa. Developmental pathologies are variations, and variation is the raw material of evolution.
September 22, 2010 at 11:15 am
Cool.
It probably wouldn’t be the *exact* same process, as what’s mentioned in that paper doesn’t seem to be genetic, but just the fact of an (abnormal) pneumatized vertebra in a non-PSP taxon (humans) got me thinking about it.
Another nonsauropod pneumaticity question: somewhere on SV-POW! it’s been mentioned that osteoglossomorph fish have pneumatized vertebrae. This sounds interesting, where can I read more about it?
September 23, 2010 at 2:46 pm
I don’t know, it might be the same process. Things like this are usually epigenetically controlled timing issues. We know that some epigenetic controls can be passed on, but as far as I know, it isn’t clear how. At some point, I could see an epigenetic control that continued to be passed on, possibly as a result of some selective pressure, falling under genetic control, thus ensuring its continued existence. Course, I’m waving my arms hard enough to fly here, but still.