A couple of times now, I’ve pitched in an abstract for a Masters project looking at neck cartilage, hoping someone at Bristol will work on it with me co-supervising, but so far no-one’s bitten. Here’s how I’ve been describing it:

Understanding posture and motion in the necks of sauropods: the crucial role of cartilage in intervertebral joints

The sauropod dinosaurs were an order of magnitude bigger than any other terrestrial animal. Much sauropod research has concentrated on their long necks, which were crucial to their success (e.g. Sander et al. 2010). One approach to understanding neck function tries to determine neutral posture and range of motion by modelling the cervical vertebrae as a mechanical system (e.g. Stevens and Parrish 1999).

The raw material of such studies is fossilised vertebrae, but these are problematic for several reasons. The invariable incompleteness and distortion of sauropod neck fossils causes fundamental difficulties; but even given perfect fossils, the lack of preserved cartilage means that the bones are not shaped or sized as they were in life.

Ignoring cartilage has dramatic consequences for neutral posture, range of motion and even length of necks: pilot studies (Cobley 2011, Taylor 2011) found that intact bird necks are 8–12% longer than articulated sequences of their dry bones, and that figure is as high as 24% for a juvenile giraffe neck. A turkey neck postzygapophysis was 26% longer when cartilage was included than after being stripped down to naked bone.

We do not yet know how much articular cartilage sauropods had in their necks, nor even what kind of intervertebral joints they had: crocodilians have fibrocartilaginous discs like those of mammals, while birds have synovial joints, so the extant phylogenetic bracket is uninformative.

The project will involve dissection and measurement of bird and crocodilian necks, documenting the extent and shape of articular cartilage, identifying osteological correlates of fibrocartilaginous and synovial joints, and applying this data to sauropods to determine the nature of their neck joints and length of their necks, to reconstruct the lost cartilage, and to determine its effect on neutral pose and range of motion.

Following completion, we anticipate publication of the project.

References

Cobley, Matthew J. 2011. The flexibility and musculature of the ostrich neck: implications for the feeding ecology and reconstruction of the Sauropoda (Dinosauria: Saurischia). MSc Thesis, Department of Earth Sciences, University of Bristol. vi+64 pages.

Sander, P. Martin, Andreas Christian, Marcus Clauss, Regina Fechner, Carole T. Gee, Eva-Maria Griebeler, Hanns-Christian Gunga, Jürgen Hummel, Heinrich Mallison, Steven F. Perry, Holger Preuschoft, Oliver W. M. Rauhut, Kristian Remes, Thomas Tütken, Oliver Wings and Ulrich Witzel. 2010. Biology of the sauropod dinosaurs: the evolution of gigantism. Biological Reviews 86:117–155. doi:10.1111/j.1469-185X.2010.00137.x

Stevens, Kent A., and J. Michael Parrish. 1999. Neck Posture and Feeding Habits of Two Jurassic Sauropod Dinosaurs. Science 284:798–800. doi:10.1126/science.284.5415.798

Taylor, Michael P., and Mathew J. Wedel. 2011. Sauropod necks: how much do we really know?. p. 20 in Richard Forrest (ed.), Abstracts of Presentations, 59th Annual Symposium of Vertebrae Palaeontology and Comparative Anatomy, Lyme Regis, Dorset, UK, September 12th–17th 2011. 37 pp. http://www.miketaylor.org.uk/dino/pubs/svpca2011/TaylorWedel2011-what-do-we-really-know.ppt

(Obviously some part of this have since been covered by my and Matt’s first cartilage paper, but plenty has not.)

I now think there are two reasons no-one’s taken up this project: first, because I wrote it as very focussed only on the question of what type of joint was present, whereas there are plenty of related issues to be investigated along the way; and second, because I wrote it as a quest to discover a specific treasure (an osteological correlate), with the implication that if there’s no treasure to be found then the project will have been a failure.

But I do think there is still plenty of important work to be done in this area, and that there’s lots of important information to be got out of comparative dissection of extant critters.

If anyone out there fancies working in this area, I’d be delighted. I’d also be happy to offer whatever advice and help I could.

Update (18 October 2014)

Somehow I’d forgotten, when I wrote this post, that I’d previously written a more detailed post about the discs-in-sauropod-necks problem. If you’re interested in the problem, you should read that.

Last time, we looked at how including intervertebral cartilage changes the neutral pose of a neck — or, more specifically, of the sequence of cervical vertebrae. The key finding (which is inexplicably missing from the actual paper, Taylor and Wedel 2013c) is that adding cartilage of thickness x between vertebrae whose zygapophyses are height y above the mid-height of the centra elevates the joint’s neutral posture by x/y radians.

Figure 14. Geometry of opisthocoelous intervertebral joints. Hypothetical models of the geometry of an opisthocoelous intervertebral joint compared with the actual morphology of the C5/C6 joint in Sauroposeidon OMNH 53062. A. Model in which the condyle and cotyle are concentric and the radial thickness of the intervertebral cartilage is constant. B. Model in which the condyle and cotyle have the same geometry, but the condyle is displaced posteriorly so the anteropos- terior thickness of the intervertebral cartilage is constant. C. the C5/C6 joint in Sauroposeidon in right lateral view, traced from the x-ray scout image (see Figure 12); dorsal is to the left. Except for one area in the ventral half of the cotyle, the anteroposterior separation between the C5 cotyle and C6 condyle is remarkably uniform. All of the arrows in part C are 52 mm long.

Figure 14. Geometry of opisthocoelous intervertebral joints. Hypothetical models of the geometry of an opisthocoelous intervertebral joint compared with the actual morphology of the C5/C6 joint in Sauroposeidon OMNH 53062. A. Model in which the condyle and cotyle are concentric and the radial thickness of the intervertebral cartilage is constant. B. Model in which the condyle and cotyle have the same geometry, but the condyle is displaced posteriorly so the anteroposterior thickness of the intervertebral cartilage is constant. C. the C5/C6 joint in Sauroposeidon in right lateral view, traced from the x-ray scout image (see Figure 12); dorsal is to the left. Except for one area in the ventral half of the cotyle, the anteroposterior separation between the C5 cotyle and C6 condyle is remarkably uniform. All of the arrows in part C are 52 mm long.

But how thick was the intervertebral cartilage in sauropods?

At the moment, no-one really knows. As Kent Stevens (2013) points out in his contribution to the PLOS ONE sauropod gigantism collection:

Determining the ONP of a sauropod’s cervical vertebral column given only its bones requires is necessarily speculative since the cartilage, and thus the intervertebral spacing, is unknown.

Part of the our goal in our own PLOS collection paper (Taylor and Wedel 2013c) was to take some very tentative first steps towards estimating the cartilage thickness. To do this, we used two approaches. First, we looked at CT scans of articulated vertebrae; and second, we measured the cartilage thickness in a selection of extant animals and thought about what we could extrapolate.

Since the CT scans were Matt’s domain, I’m going to pass over those for now, in the hope that he’ll blog about that part of the paper. Here, I want to look at the extant-animal survey.

Figure 18. Cartilage in the neck of a rhea. Joint between cervicals 11 (left) and 10 (right) of a rhea, sagittally bisected. Left half of neck in medial view. The thin layers of cartilage lining the C11 condyle and C10 cotyle are clearly visible.

Figure 18. Cartilage in the neck of a rhea. Joint between cervicals 11 (left) and 10 (right) of a rhea, sagittally bisected. Left half of neck in medial view. The thin layers of cartilage lining the C11 condyle and C10 cotyle are clearly visible.

The first thing to say is that our survey is inadequate in many ways. We worked with the specimens we could get hold of, in the state we had them. This means that:

  • we have a very arbitrary selection of different animals,
  • they are at different ontogenetic stages, and
  • their cartilage thickness was measured by a variety of methods.

Our goal was not at all to reach anything like a definitive answer, but just to get the question properly asked, and so hopefully to catalyse much a more detailed survey.

With that proviso out of the way, here are our main results (from Table 4 of the paper, though here I have removed the sauropod CT-scan rows since we’ll be writing about those separately).

Taxon Thickness Reference Notes
Turkey 4.56% This study Difference in measurements of intact neck and articulated sequence of cleaned, degreased and dried vertebrae.
Ostrich 6.30% Cobley et al. (2013) Difference in measurements of individual vertebrae with and without cartilage.
Rhea 2.59% This study Measurement of in situ cartilage in bisected neck.
Alligator 14.90% This study Measurement of in situ cartilage from photograph of cross section.
Horse 6.90% This study Measurement of in situ cartilage from photograph of cross section.
Camel 13.00% This study Crude measurement from condyle margin to cotyle lip of lateral-view X-ray. This is an interim measurement, which we hope to improve on when we obtain better images.
Dog 17.00% This study Measurement of intervertebral gaps in lateral-view X-ray, uncorrected for likely concavity of cotyles.
Giraffe 24.00% This study Difference in measurement of intact neck and closely articulated sequence of cleaned vertebrae. Young juvenile specimen.
Muraenosaurus 14.00% Evans (1993) Measurement of in situ cartilage in fossils.
Cryptoclidus 20.00% Evans (1993) Measurement of in situ cartilage in fossils.

We’ve expressed the measurements as a ratio between cartilage thickness and the length of the bone itself — that is, cartilage/bone. Another way to think of this is that the percentage is a correction factor which you need to add onto bone length to get whole-segment length. Note that this is not the same ratio as the proportion of total segment length that consists of cartilage: that would be (cartilage thickness + bone length) / bone length.

(We also tossed in some measurements of plesiosaur neck cartilage that Mark Evans made way back when. Get that thing properly published, Mark!)

Even this small survey throws up some interesting points.

First, there is a huge range of proportional cartilage thicknesses: almost an order of magnitude from the 2.59% of the Rhea up to the 24% of the juvenile giraffe — or, even if you discard that because of its ontogenetic stage, up to 17% for the dog. And note that the 17% for the dog is probably an under-estimate, since we were working from an X-ray that doesn’t show the concavity of the vertebral cotyles.

Figure 22. Dog neck in X-ray. Neck of a dog (dachsund), in X-ray, with the seven cervical vertebrae indicated. This photo has been used with permission from the Cuyahoga Falls Veterinary Clinic.

Figure 22. Dog neck in X-ray. Neck of a dog (dachsund), in X-ray, with the seven cervical vertebrae indicated. This photo has been used with permission from the Cuyahoga Falls Veterinary Clinic.

(Two reviewers expressed scepticism that this is the usual condition for dogs, but this X-ray is consistent with those of other dogs illustrated in the veterinary literature.)

The second thing to note is that the cartilage measurements for birds (average 4.5%) are are much lower than those of crocodilians (14.9%) or mammals (15.2%). What does this mean? Among these groups, sauropods are most closely related to birds; but birds and crocs form the extant phylogenetic bracket, so we can’t tell from phylogeny alone whether to expect them to more closely approach the avian or crocodilian condition. Furthermore, in being opisthocoelous (condyle in front, cotyle at the back) sauropod cervicals most closely resemble those of mammals in gross structure — and they have the thickest cartilage of all.

The third thing to note is that there is considerable variation within groups. Although the cartilage is proportionally thin for all three birds, it’s more than twice as thick in the ostrich as in the rhea (although some of this could be due to the different measurement methods used for these two birds). More interestingly, among mammals the cartilage is twice as thick in camels as in horses. In the horse, the condyles are deeply inserted into the cotyles of the preceding vertebrae; but in camels, they don’t reach even the lip of the cotyle. This should worry us, as horse and camel cervicals are grossly similar, and no osteological correlates have been identified that would allow us to determine from the bones alone how very different the cartilage is between these two mammals. So it seems possible that there were similarly dramatic differences in the neck-cartilage thickness of different sauropods.

Note: I said that no osteological correlates have been identified. That doesn’t mean they don’t exist. One thing I would love to see is a serious attempt to analyse cartilage thickness across a broad range of mammals, and to examine the corresponding dry bones to see whether in fact there are correlates that could be informative in this respect. One lesson that Matt and I have learned over and over again is that there’s often plenty of data in places that are out in the open, but where no-one’s thought to look.

Next time: more on searching for osteological correlates of cartilage. Then, measurements of sauropod-neck cartilage from CT scans, and likely implications for cartilage thickness in life.

References

Back when we were at Cambridge for the 2010 SVPCA, we saw taxidermied and skeletonised hoatzins, and were struck that the cervical skeleton was so very much longer than the neck as it appears in life — because necks lie. At Oxford last week for the 2012 SVPCA, we saw a similar pair of hoatzin mounts (one adult, one juvenile) that clarified the situation:

And here is juvenile in side-view:

As you can see, it’s folding its neck way down out of the way, so that externally it appears much shorter. (And comparing with the Cambridge specimen, you can see that the neck skeleton is proportionally much longer than this in adult.)

Why does it do this? I have no idea.

But I do know it’s not unique to hoatzins. Another nice illustration of how misleading birds’ necks are when viewed in a live animal is this parrot (probably Amazona ochrocephala) in the Natuurhistorisch Museum of Rotterdam (from this Love in the Time of Chasmosaurs post):

One thing that’s not clear to me is how much of the neck the bird can extend in life. If the parrot wants to uncoil all that spare cervical skeleton to reach upwards or forwards, can it? Will the soft tissue envelope allow it? My guess is not, otherwise you’d surely see them doing it. But then … why is all that neck in there at all?

Back in early Februrary, Darren and I got an email out of the blue from biomechanics wizard and all all-round good guy John Hutchinson, saying that he’d obtained the neck of a baby giraffe — two weeks old at the time of death — and that if we wanted it, it was ours.

Of course, the timing wasn’t great for me — Brontomerus day was coming up fast, and the final publicity arrangements were buzzing around like crazy, so it wasn’t possible to go and fetch the neck right then.  But John had an even better proposition: that he could keep the neck frozen, and we could come to the Royal Veterinary College and dissect it on site.  As soon as I’d established with Darren that I’d get to be the one to keep the bones when the dissection was done, we enthusiastically agreed, and booked a date with John.  [The photo here shows a baby giraffe, not the one that we had — note that the neck is proportionally much shorter than in an adult.]

And so it was that on Wednesday 9th March, I drove up from Ruardean to Potter’s Bar and picked up Darren and pterosaur-jockey John Conway from the railway station.  From there, we found our way to the RVC campus easily enough, with only the statutory minimum number of times getting lost (once).

The bad news was that the neck had already been skinned before it made its way to the RVC.  We don’t know why, by whom, or when, and more importantly we don’t know how much of the other soft tissue was removed in the process — for example, the trachea and oesophagus were gone — along with, we assume, the recurrent laryngeal nerve that Matt had asked us to look out for — and we wonder whether our nuchal ligament was complete.  (That is the long ligament that runs along the top of the neck and helps to prevent it from sagging.)

But anyway, here is our baby, in left lateral view, as it came out of its plastic sack, measuring a healthy 51 cm in length.

Like so many specimens, at this point it really looks like an undifferentiated blob of gloop.  There are a couple of things to look for, though.

On the left of the picture, you’ll see that the terminal 10% or so is well separated from the rest, ahead of of portion of exposed bone.  That bone is the anterior margin of the axis (i.e. the second cervical vertebra).  The atlas (first cervical) is still encased in soft tissue at this point, but could be moved around fairly freely, including twisting.

On the right, and you’ll probably need to click through to see this, is a strange metal pin, stuck right into the back of C7.  This was firmly embedded and we never figured out what it was, or what it was doing there.  As you’ll see in the photos below, I’ve allowed it to stay in place, even in the final prepared vertebrae.  If anyone knows what it is, do tell!

I took a bunch of photos and measurements before we ploughed in, but I am ashamed to say that I failed to get many, many of the images and numbers that I should have.  Even allowing for the fact that the specimen was not intact when we got it, we and particularly I fumbled the ball badly.  So much so that I will shortly publish a tutorial on How To Dissect A Neck which will be based primarily on what we failed to do.

I suppose it’s true that we only ever learn from mistakes.  The trick is to learn from other people’s, rather than going through the frustrating and expensive process of making your own.  Oh well.  Next time, for sure.

Here we have John (left) and Darren (right) hard at work teasing away the long epaxial muscles from their fascia.

It was only after that process was complete that we thought to do one of the things we should have done up front — test the range of motion.  We put the necks into poses of maximal extension, flexion and lateral deflection.  Contrary to what I would have expected, the last of these was significantly more impressive than the other two, and is shown here.  You can easily make out the separate extents of vertebrae 2, 3, 4 and 5, and from those see where 1, 6 and 7 are.

(Those are the long epaxial muscles in the background.)

We continued removing muscle and fascia until we had the vertebrae as close to naked as we could manage without risking damage to them, while retaining the integrity of the intervetebral joints — both intercentral and zygapophyseal articulations.  One of the big surprises to us was how very flexible and fragile the latter were compared with the former.  The membrane that contains the zygapophyseal joint is very thin and would contribute almost no mechanical strength of its own.  By contrast, the adjacent centra were bonded very firmly together by extremely tough tissue.  There was no trace of a separate cartilage disc between any pair of centra, just this very dense but flexible material which had to be slowly cut away with scalpels before the vertebrae could be be separated.

The exception to this was the atlas-axis joint, which surprised all three of us in how completely different it was to all the others.  There was no connective tissue at all between the front of the axis and the back of the atlas — the two bones (or rather their cartilaginous surfaces) were free to move against each other without let or hindrance, as shown here (right anterolateral view with anterior towards the bottom of the picture):

And yet the axis was very firmly attached to the axis: although we couldn’t see any attachment, it wouldn’t come away — not even when a great deal of force was applied.  The connection turned out to be between the ventral face of the odontoid process and the dorsal surface of the ventral portion of the atlas.  (If you’re not familiar with anterior cervicals, this should become clearer later on when I show you the individual bones.)  Suffice it for now to say that the atlas is basically ring-shaped, and that the odontoid process is a chunk of the axis that sticks out the front of that bone and sits within the O of the atlas.

Before we separated the vertebrae, though, we prepared the nuchal ligament out from its surrounding muscle.  Here it is, with John and Darren holding its posterior portion up above the vertebrae: you can see that it’s in the form of a sheet rather than, as often envisaged, a cylinder.  (It does extend further anteriorly than shown here, but its much less extensive over C2 than it is more posteriorly.)

We did the best we could at detaching this ligament intact so that we could measure how compliant it is.  It was difficult to remove without damaging, and much more irregular in shape than we’d expected, so that the anteriormost portion had almost no strength and broke as soon as we exerted any force on it.

We were initially able to remove a portion that measured 45 cm at rest (from a total neck length of 51 cm, remember), but once the thin anterior end had broken off, we were left with 32 cm.  We were able, by application of a significant force courtesy of Darren, to extend this to 42 cm but no further.  That’s a strain of (42-32)/32 = 0.3125, which is a lot less than I’d been expecting.  Alexander (1989:64-65) wrote (in the passage that was my first ever encounter with nuchal ligaments):

I am going to suggest that these necks [i.e. those of sauropods] were supported in the same way as the necks of horses, cattle, and their relatives.  These animals have a thick ligament called the ligamentum nuchae running along the backs of their necks (figure 5.5).  Unlike most other ligaments it consists mainly of the protein elastin, which has properties very like rubber.  It can be stretched to double its initial length without breaking […]  In experiments with deer carcasses, my colleagues and I found that the ligament was 1.4 times its slack length when the head was raised to the position of figure 5.5 [i.e. a typical alert posture], and almost twice its slack length when it was lowered to the position of figure 5.5b [grazing posture].  Notice that the ligament was stretched even when the head was high: I doubt whether a deer can get into a position that allows the ligament to shorten to the point of going slack.  If you cut the ligament in a dissection the cut ends spring apart, as if you had cut a stretched rubber band.

So the least stretched life position of the ligament, according to Alexander, is significantly more extended than the most stretching we could achieve.  What does this mean?  I see four possibilities:

  • Alexander was talking a pile of poo.  I don’t believe this for a moment, and mention it only for completeness.
  • I am talking a pile of poo.  I can see why you’d think so, but I know it ain’t so (and Darren and John can verify it).
  • The composition of the nuchal ligament changes through ontogeny, becoming more elastic as the animal gets older: we had a baby, and Alexander had adults.  I don’t think this is very likely either — I can’t see any reason why juveniles would need less elastic ligaments than adults.
  • The composition of the giraffe nuchal ligament is different from that of the deer.

Since I already eliminated the first three options, it won’t come as a great surprise to find that I favour the last one.  And this has some interesting implications if it’s true.  (Darn, darn, we should have saved a chunk of the ligament and found a way to get it analysed for composition.)  If that nuchal ligament of giraffes is largely collagen rather than elastin, then it suggests the possibility of something similar for sauropods, and that would be interesting because the tensile strength of collagen is much greater than that of elastin.

Does anyone know if anyone’s done any work on this?

Well, anyway.

I drew the long straw, and got to bring the remains of the neck home to prepare out as bones.  I simmered gently, then removed the cooked flesh, and was astonished to find how much there was, removed from vertebrae that we thought we’d cleaned pretty well at dissection time:

The disappointing part of this is that such large parts of the vertebrae turned out to be cartilage (partially ossified, I guess) and so came away during the simmering: huge chunks at the front and back of each centrum, like a full centimeter at each end, and all of the zygapophyseal articular surfaces.  I wish I could have kept them intact … and of course a different preparation method probably would have done.  More stupid still, I neglected to get photos of the individual vertebrae before simmering, which would at least have enabled me to show you before-and-after comparisons.  Sorry.

Anyway, having peeled off the soft-tissue including cartilage, I re-simmered, re-picked, then bathed in dilute hydrogen peroxide for two days, and dried out the vertebrae in the sun.  This is the result — C1-C7 in order, in left lateral view:

Note that the odontoid process of the axis is a separate bone from the rest of the axis — you can see it on the left, between atlas and axis.  There was a big chunk of sculpted cartilage joining it to the rest of the atlas, and that’s all gone now, so I am not sure how I am going to join it up — maybe layer on layer of PVA representing the cartilage?

Oh, and notice that the metal pin is still in C7.

In the picture about, I have laid the vertebrae out in such a way that the total neck length (front of C1 to C7) is 51 cm, the same as it was in life.  Notice how this leaves huge gaps between the central: for example, as here between C5 and C6:

Needless to say, anyone trying to reconstruct the living animal from the bones alone — from fossils, say — would get a hopelessly wrong neck if they didn’t take the missing cartilage into effect.  As we’ve noted before, the same is true of sauropod necks.

But just how informative is a juvenile neck?  No doubt, the cartilaginous portions of these vertebrae were proportionally much larger than they would be in an adult, so we do need to be careful about casually extrapolating the huge gaps between ossified centra in the images above into our interpretation of sauropods.  For sure, I now need to go through this process with the neck of an adult giraffe — and if anyone happens to acquire one, I would love the opportunity to dissect it, please contact me if this comes up!

But maybe it’s not quite so misleading as it looks — for two reasons.  First, nearly all the sauropod specimens we have are from subadults, as shown by lack of fusion between scapula and coracoid in, for example, the Giraffatitan paralectotype HMN SII.  So it may be that their vertebrae were also not fully ossified.  And second, sauropods are more closely related to birds than to mammals, and in my limited experience bird necks seem to have a larger cartilaginous component than those of mammals.

Well.  Draw your own conclusions.  But keep ’em qualitative for now.

Next time, I’ll be presenting a tutorial on how to dissect a neck.  But it will be based on what we should have done rather than what we actually did.

Isn’t it funny how often an idea seems to pop up all over the place at about the same time?  The classic example is the independent and more or less simultaneous invention of calculus by both Isaac Newton and Wilhelm Leibniz, but similar kinds of things seem to happen quite often.

And there’s something similar going on right now.  After a century of everyone ignoring the role of cartilage in dinosaur anatomy, suddenly everyone’s up and running all at once:

  • Here at SV-POW!, Matt, Darren and I have been running the series on camel necks (which by the way isn’t over yet — stay tuned!)  In that series we have repeatedly made the point that “it is useless to try to reach conclusions about neck posture based on osteology alone. We need to understand the soft-tissue systems — especially the articular cartilage — as well”.
  • Meanwhile, over on his blog Jurassic Journeys, Matt Bonnan has been writing about “long bones and the space between“, emphasising how we can’t really understand sauropod locomotion when we don’t know the true sizes and shapes that the long-bones had in life.
  • Independently of that, Heinrich Mallison, on the Palaeontologia Electronica blog, wrote about the importance of cartilage in his Plateosaurus digital modelling projects.  I highly recommend reading this very relevant article if only for its section headings, which sum up the state of play perfectly: Ask your doctor for advice // Palaeontology is an interdisciplinary science — we just tend to forget // Have you ever read the Journal of International Orthopaedics? // How do these go together? Where’s the manual? HELP!
  • The next thing we know, Casey Holliday and his colleagues wrote about the same issue — not merely blogging, but producing a long-awaited peer-reviewed article in PLoS ONE, “Cartilaginous Epiphyses in Extant Archosaurs and Their Implications for Reconstructing Limb Function in Dinosaurs“.  Casey and his group have gone much further than the rest of us: rather than just whining about the problem of cartilage, they’ve taken steps to solve it — see below for details.
  • Finally, it turns out that Dave Hone has had a blog entry on this subject in the works at Archosaur Musings for a year or more.

It’s a pretty amazing confluence of thought, and the Holliday et al. paper really couldn’t have come at a better time.  It gives us, for the first time, qualitative estimates of the thickness of articular cartilage in limb-bones.  They dissected birds and alligators, measured their limb bones before and after the removal of their cartilage caps, compared the measurements, and determined what they called cartilage correction factors (CCFs) that quantify the increase in limb length when cartilage is included.  They also examined the osteological correlates of extensive articular cartilage, and drew conclusions about the likely form and function of these structures in sauropods (and, yes, I suppose, other dinosaurs as well).

This all ties in nicely with a long-running background project of mine, first presented at Progressive Palaeontology in 2005, and then again at the German sauropod-fest in 2008.  While Holliday et al. were investigating the thickness of articular cartilage, I was thinking in a very naive way about its area as part of a study tentatively entitled Upper limits on the mass of land animals estimated through the articular area of limb-bone cartilage.  The slides for the talk are available, and contain a Godzilla joke that will be hauntingly familiar to anyone who saw my talk on neck elongation at SVPCA this year.

Poorly executed slide from my 2005 Progressive Palaeontology talk. Despite the clumsy graphics, the point should be clear: that the area of articular cartilage available to withstand static and locomotory forces depends hugely on how extensive the cartilage caps are, and on their shape.

I ought to be clear that my work on this was very preliminary and that I am, as usual, years behind where I wanted to be in terms of getting this written up rigorously.  In fact the talk ended with a slide in which I pointed that I was pretty confident that “my figures are correct within a factor of 756”.  And I stand by that :-)

My point is just this: suddenly there’s a visible swell of palaeontologists all saying the same thing: that we can’t expect to understand how the skeletons of extinct animals worked by looking only at their bones, which is a bit of a shame when their bones are usually all we have.  The Holliday et al. paper (2010) is a very welcome first step towards wrasslin’ with this problem as it deserves.

Oh, and it’s open access — go read it!

References

I Cannot Brain Today, I Have the Dumb

Man, I hate making mistakes. The only thing worse than making mistakes is making them in public, and the only thing worse than that is finding them in published papers when it’s too late to do anything about them. About the only consolation left–if you’re lucky–is getting to be the one to rat yourself out (we have to do this a lot). So here goes.

fig4-head-and-neck-angles 480

Neck angle FAIL

In our figure 4 (from Taylor et al. 2009) we showed the skulls of three sauropodomorphs, Massospondylus, Camarasaurus, and Diplodocus, posed with horizontal semicircular canals (HSCCs) level, angled 30 degrees above horizontal, and angled 20 degrees below horizontal, as it is written (by Duijm 1951). We also showed the angle of the occipital condyle when the HSCCs are level; if the craniocervical joint was in osteologically neutral pose (ONP), that line would indicate the angle of the anterior cervicals.

Trouble is, we put the neck lines for Diplodocus and Camarasaurus in the wrong places.

As any idiot can see from Sereno et al. (2008: fig 1), the brain, brainstem, and occipital condyle form a line that runs from roughly the upper part of the orbit (in lateral see-through view) out the back of the head. Now if you look at our fig. 4 you’ll see that the ONP lines for Camarasaurus and Diplodocus are much too inclined, so that if the brain was in line with the anterior neck–which it should be, in ONP–it would be sticking out the back of the head.

If that doesn’t make sense, just look at the above illustration, imagine the brain and spinal cord in a straight line parallel to the black neck line but also dorsal to it, and you’ll see that the brain would be outside the skull. Those incorrect neck lines don’t represent impossible postures, but they don’t represent ONP, either.

Sauropodomorph head figure redone 480

Taxonomic variation WIN!

Here’s a corrected up version of the figure to show what I mean. The black lines are still the ONP neck lines, and now I’ve put in shadowy necks at +30 and -20 to go with the shadowy heads. The 50 degree spans marked out by the shadowy necks are the ranges within which the neck could articulate in ONP with skulls stuck in the 50-degree “Duijm window”.

Caution: it is very easy to misread the shadowy necks as showing a range of movement within an individual; in fact, the neck lines are ‘anchored’ to the skulls in ONP as the skulls rotate through the 50 degrees allowed by the HSCCs. They are not individual movement but the possible range of taxonomic variation in HSCC orientation according to Duijm (1951).

Worth noting here is the likelihood that Massospondylus had a more elevated neck than any of the neosauropods studied so far–certainly a finding at odds with the traditional depictions of basal sauropodomorphs. (It is just a likelihood, though, since the top, neck-wise, of Massospondylus‘s Duijm window overlaps with the windows of the other taxa a bit.)

Nigersaurus, buddy, why so down?

Nigersaurus, buddy, why so down?

In this version I’ve gone one step farther and included Nigersaurus (modified from Sereno et al. (2008: fig 1). Nigersaurus differs from Diplodocus in the angle of the face from the HSCCs and occipital condyle, not in the angle between the HSCCs and the occipital condyle, which is remarkably similar in Camarasaurus, Diplodocus, and Nigersaurus. This suggests that Nigersaurus held its head differently than other sauropods, but not necessarily its neck.

Keep in mind, though, that the difference in facial angle between Diplodocus and Nigersaurus is less than 50 degrees, and that some of the head postures in the respective Duijm windows of the two taxa are identical. So we can’t say for certain that Nigersaurus held its head differently than Diplodocus; it is possible that they held their heads at the same angle and that Nigersaurus just carried its HSCCs at a different angle. If that were the case, the neck of Nigersaurus would have been more inclined than that of Diplodocus. I’m not arguing that that’s likely–it seems perfectly plausible that the two taxa might have held their necks similarly and their heads differently, as suggested above–I’m just pointing out the very wide range of possibilities allowed by the data. To reiterate one of the points of the paper, HSCCs aren’t useless for determining habitual head posture, they just can’t narrow things down very far on their own.

Also note that some of the neck postures allowed by the Duijm window have the anterior cervicals running down, below horizontal, not up. And many of the allowed neck postures for the neosauropods are close to horizontal. So, we were wrong and HSCCs + occipital condyles show that most sauropods held their necks close to level and not strongly elevated after all, right?

Onward and Upward, or Down in Flames?

Not so fast. Remember that all of the neck lines in the above figures show the angle of the anterior neck if the neck was in ONP with the skull. But Vidal et al. (1986) found that the skull is habitually flexed on the neck, even in lizards, and we have since verified this for salamanders, turtles, and more. And sometimes the flexion is dramatic.

Our figure 1 (from Taylor et al. 2009) shows the cranium, cervicals, and first few dorsals from a hare in ONP and in the posture shown by Vidal et al. (1986: fig. 4b). The difference between the anteriorly-directed ONP pose and the backward-leaning Vidal-compliant pose is striking. I measured the angle between the cervical column and the maxillary toothrow to be ~110 degrees in the ONP pose and ~70 degrees in the Vidal-compliant pose (try it yourself with Paint or Photoshop, or download some free image manipulation software). That means the head is flexed on the neck by 40 degrees! That is a big angle. If sauropods did the same, you could take the neck lines shown above and crank them down by 40 degrees (remember that the heads are “fixed” into the 50-degree Duijm windows allowed by the HSCCs), which would make Mike’s elevated Diplodocus look not just achievable, but perhaps even conservative.

Where does all that leave us? In sauropods for which HSCC orientation is known, putting the HSCCs level the anterior neck is still inclined, and even with the HSCCs angled 20 degrees down the ONP neck would only be slightly below horizontal, and if the head was Vidal-compliant (strongly flexed on the neck), the neck would have to be above horizontal. So heads still tell us about necks, and in particular they tell us that the necks angled up. Our neck lines for Camarasaurus and Diplodocus are not correct for ONP, but probably represent attainable postures. My first head ‘n necks post has the angles too exaggeraged for ONP, too, but again all of those poses are not just possible but likely if the head was flexed on the neck.

Miscellanea

We owe mad props to Brian Engh, a.k.a. The Historian, who burst on the paleo-rap scene with a rap video about crocodilian predation and almost certainly the first ever kung-fu rap video to name-check titanosaurs. Brian stumbled across Mike’s extra goodies page for the new paper about week before the paper was due out, and kindly suppressed the information until after D-Day. You can and should download his entire album, Earth Beasts Awaken (open access, yo), and kick it old school.

Congratulations to Francisco “Paco” Gasco, who just got funding for a PhD to do a complete morphological and paleobiological workup on the giant Spanish sauropod Turiasaurus. You’ll be hearing more about Paco in the not-too-distant future, we promise.

Finally, here’s that video of an elephant grabbing an ostrich by the neck that you ordered.

ostrichvselephant

The End of the Beginning?

This brings us to the end of ten solid days of new posts, which is a new record for us and one not likely to be broken for a long time, if ever. We never planned to do all this; in the beginning we each were going to contribute one post and that would have been that. But we kept finding things that we felt needed to be discussed.

As all of us have been saying in every available medium, this is not the end of anything. The sauropod neck posture debate is not over; in a few years we may look back and see that in 2009 we were still stumbling to the real starting line. We don’t think this stuff is unimportant or unknowable, and we’re going to keep working on it, and we hope lots of others do as well.

We’ll see you out there.

Ridem dino 480

Up, boy, up! Heyaaah!!

References