Dorsal vertebra of a rhea from the LACM ornithology collection. Note the pneumatic foramina in the lateral wall of the neural canal.

If you’ve been here for very long you know I have a bit of a neural canal fixation. Some of this is related to pneumaticity, some of it is related to my interest in the nervous systems of animals, and some of it is pure curiosity about an anatomical region that seems to receive very little attention in proportion to its weirdness – especially in birds.

Human thoracic vertebrae in midsagittal section showing vertebral venous plexus. Gray (1918, image 579), available from Bartleby.com.

The neural canals of mammals are pretty boring. The canal is occupied by the spinal cord and its supporting layers of meninges, and the rest of the volume is padded out by adipose tissue and blood vessels, notably an extra-dural venous plexus. Aaand that’s about it, as far as I know. (If there are weird things inside mammalian neural canals that I’ve missed, please let me know in the comments – I’m a collector.)

But not so in birds, which have a whole festival of weird stuff going on inside their neural canals. Let’s start with pneumaticity, just to get it out of the way. Many birds have supramedullary diverticula inside their neural canals, and these can leave osteological traces, such as pneumatic foramina, in the walls of the neural canal. That’s cool but it’s a pretty well-known system – see Muller (1908) on the pigeon, Cover (1953) on the turkey, and these previous posts – and I want to get on to other, even stranger things.

The lumbosacral spinal cord of a 3-week-old chick in dorsal view. The big egg-shaped mass in the middle is the glycogen body. Watterson (1949: plate 1).

The spinal cords of birds have several gross morphological specializations not seen in mammals, as do their meninges, and most of these apomorphic structures can also leave diagnostic traces on the inner walls of the neural canal. In fact, birds have so many weird things going on with their spinal cords – at least five different things in the lumbosacral region alone – that I spent a week back in January just sorting them out. To crystalize that body of knowledge while I had it all loaded in RAM, I made a little slideshow for myself, and I’ll use screenshots of those slides to illustrate the morphologies I want to discuss. We’ll cover the vanilla stuff in the next post, and the really weird stuff in subsequent posts.

Stay tuned!

References

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Illustration talk slide 51

Here’s a working version of that link.

Illustration talk slide 52

Illustration talk slide 53

Working link.

Illustration talk slide 54

Illustration talk slide 55

Illustration talk slide 56

Illustration talk slide 57

Working links:

The rest of this series.

Reference

  • Powell, Jaime E.  2003.  Revision of South American Titanosaurid dinosaurs: palaeobiological, palaeobiogeographical and phylogenetic aspects.  Records of the Queen Victoria Museum 111: 1-94.

This  is the fifth in a series of posts reviewing the Apatosaurus maquette from Sideshow Collectibles. Other posts in the series are:

There are really only a couple of interesting points to discuss for posture: the neck and the feet.

The neck posture is fine. Easy to say, but since I’m one of the “sauropods held their necks erect” guys, it might need some unpacking.

On one hand, animals really do use stereotyped postures, especially for the neck and head (Vidal et al. 1986, Graf et al. 1995, van der Leeuw et al. 2001). The leading hypothesis about why animals do this is that the number of joints and muscle slips involved in the craniocervical system permits an almost limitless array of possible postures, and that having a handful of stereotyped postures cuts down on the amount of neural processing required to keep everything going. That doesn’t mean that animals only use stereotyped postures, just that they do so most of the time, when there’s no need to deviate.

This might work something like the central pattern generators in your nervous system. When you’re walking down the sidewalk thinking about other things or talking with a friend, a lot of the control of your walk cycle is handled by your spinal cord, not your brain. Your brain is providing a direction and a speed, but the individual muscles are being controlled from the spinal cord. Key quote from the Wikipedia article: “As early as 1911, it was recognized, by the experiments of T. Graham Brown, that the basic pattern of stepping can be produced by the spinal cord without the need of descending commands from the cortex.”

But then you see a puddle or some dog doo and have to place your foot just so, and your brain takes over for a bit to coordinate that complex, ad hoc action. After the special circumstance is past, you go back to thinking about whatever and your spinal cord is back in charge of putting one foot in front of the other. This is the biological basis of the proverbial chicken running around with its head cut off: thanks to the spinal cord, the chicken can still run, but without a brain it doesn’t have anywhere to go (I have witnessed this, by the way–one of the numerous benefits to the future biologist of growing up on a farm).

Similarly, if the craniocervical system has a handful of regular postures–alert, feeding, drinking, locomoting, and so on–it lightens the load on the brain, which doesn’t have to figure out how to fire every muscle slip inserting on every cervical vertebra and on the skull to orient the head just so in three-dimensional space. That doesn’t mean that the brain doesn’t occasionally step in and do that, just like it takes over for the spinal cord when you place your feet carefully. But it doesn’t have to do it all the time.

van der Leeuw et al. (2001) took this a step further and showed that birds not only hold their heads and necks in stereotyped postures, they move between stereotyped postures in very predictable ways, and those movement patterns differ among clades (fig. 7 from that paper is above). There is a lot of stuff worth thinking about in that paper, and I highly recommend it, along with Vidal et al. (1986) and Graf et al. (1995), to anyone who is interested in how animals hold their heads and necks, and why.

So, on one hand, its wrong to argue that stereotyped postures are meaningless. But it’s also wrong to infer that animals only use stereotyped postures–a point we were careful to make in Taylor et al. (2009). And it’s especially wrong to infer that paleoartists only show animals doing familiar, usual things–I wrote the last post partly so I could make that point in this one.

For example, I think it would be a mistake to look at Brian Engh’s inflatable Sauroposeidon duo and infer that he accepts a raised alert neck posture for sauropods. He might or might not–the point is that the sauropods in the picture aren’t doing alert, they’re doing “I’m going to make myself maximally impressive so I can save myself the wear and tear of kicking this guy’s arse”. The only way the posture part of that painting can be inaccurate is if you think Sauroposeidon was physically incapable of raising its neck that high, even briefly (the inflatable throat sacs and vibrant colors obviously involve another level of speculation).

Similarly, the Sideshow Apatosaurus has its neck in the near-horizontal pose that is more or less standard for depictions of diplodocids (at least prior to 2009, and not without periodic dissenters). But it doesn’t come with a certificate that says that it is in an alert posture or that it couldn’t raise its neck higher–and even if it did, we would be free to ignore it. Would it have been cool to see a more erect-necked apatosaur? Sure, but that’s not a new idea, either, and there are other restorations out there that do that, and in putting this apatosaur in any one particular pose the artists were forced to exclude an almost limitless array of alternatives, and they had to do something. (Also, more practically, a more erect neck would have meant a larger box and heftier shipping charges.)

So the neck posture is fine. Cool, even, in that the slight ribbing along the neck created by the big cervical ribs (previously discussed here) gives you a sense of how the posture is achieved. Visible anatomy is fun to look at, which I suspect is one of the drivers behind shrink-wrapped dinosaur syndrome–even though it’s usually incorrect, and this maquette doesn’t suffer from it anyway.

Next item: the famous–or perhaps infamous–flipped-back forefoot. I have no idea who first introduced this in skeletal reconstructions and life restorations of sauropods, but it was certainly popularized by Greg Paul. It’s a pretty straightforward idea: elephants do this, why not sauropods?

Turns out there are good reasons to suspect that sauropods couldn’t do this–and also good reasons to think that they could. This already got some air-time in the comments thread on the previous review post, and I’m going to start here by just copying and pasting the relevant bits from that discussion, so you can see four sauropod paleobiologists politely disagreeing about it. I interspersed the images where they’re appropriate, not because there were any in the original thread.

Mike Taylor: the GSP-compliant strong flexion of the wrist always look wrong to me. Yes, I know elephants do this — see Muybridge’s sequence [above] — but as John H. keeps reminding us all, sauropods were not elephants, and one might think that in a clade optimsied for size above all else, wrist flexibility would not be retained without a very good reason.

Adam Yates: Yes I agree with Mike here, the Paulian, elephant-mimicking hyperflexion of the wrist is something that bugs me. Sauropod wrist elements are rather simple flat structures that show no special adaptation to achieve this degree of flexion. [Lourina sauropod right manus below, borrowed from here.]

Heinrich Mallison: Hm, I am not too sure what I think of wrist flexion. Sure it looks odd, but if you think it through the very reasons elephant have it is likely true in sauropods. And given the huge amount of cartilage mossing on the bones AND the missing (thus shape unknown) carpals I can well imagine that sauropods were capable of large excursions in the wrist.

 Mike: What are those reasons?

Heinrich: Mike, long humeri, very straight posture – try getting up from resting with weak flexion at the wrist. Or clearing an obstacle when walking. I can’t say too much, since this afternoon this has become a paper-to-be.

Mike: OK, Heinrich, but the Muybridge photos (and many others, including one on John H.’s homepage) show that elephants habitually flex the wrist in normal locomotion, not just when gwetting up from resting or when avoiding obstacles. Why?

The interesting thing here is that this is evidence of how flawed our (or maybe just my) intuition is: looking at an elephant skeleton, I don’t think I would ever have guessed that it would walk that way. (That said, the sauropod wrist skeleton does look much less flexible than that of the elephant.)

Matt: (why elephants flex their wrists) Possibly for simple energetics. If the limb is not to hit the ground during the swing phase, it has to be shortened relative to the stance limb. So it has to be bent. Bending the limb at the more proximal joints means lifting more weight against gravity. Flexing the wrist more might be a way to flex the elbow less.

(sauropod wrists look less flexible) Right, but from the texture of the ends of the bones we already suspect that sauropods had thicker articular cartilage caps than do mammals. And remember the Dread Olecranon of Kentrosaurus (i.e., Mallison 2010:fig. 3).

Mike: No doubt, but that doesn’t change the fact that elephant wrists have about half a dozen more discrete segments.

Matt: Most of which are very tightly bound together. The major flexion happens between the radius and ulna, on one hand, and the carpal block on the other, just as in humans. Elephants may have more mobile wrists than sauropods did–although that is far from demonstrated–but if so, it’s nothing to do with the number of bony elements. [Loxodonta skeleton below from Wikipedia, discovered here, arrow added by me.]

(Aside: check out the hump-backed profile of the Asian Elephas skeleton shown previously with the sway-backed profile of the African Loxodonta just above–even though the thoracic vertebrae have similar, gentle dorsal arches in both mounts. I remember learning about this from the wonderful How to Draw Animals, by Jack Hamm, when I was about 10. That book has loads of great mammal anatomy, and is happily still in print.)

And that’s as far as the discussion has gotten. The Dread Olecranon of Kentrosaurus is something Heinrich pointed out in the second of his excellent Plateosaurus papers (Mallison 2010: fig. 3).

Heinrich’s thoughts on articular cartilage in dinosaurs are well worth reading, so once again I’m going to quote extensively (Mallison 2010: p. 439):

Cartilaginous tissues are rarely preserved on fossils, so the thickness of cartilage caps in dinosaurs is unclear. Often, it is claimed that even large dinosaurs had only thin layers of articular cartilage, as seen in extant large mammals, because layers proportional to extant birds would have been too thick to be effectively supplied with nutrients from the synovial fluid. This argument is fallacious, because it assumes that a thick cartilage cap on a dinosaur long bone would have the same internal composition as the thin cap on a mammalian long bone. Mammals have a thin layer of hyaline cartilage only, but in birds the structure is more complex, with the hyaline cartilage underlain by thicker fibrous cartilage pervaded by numerous blood vessels (Graf et al. 1993: 114, fig. 2), so that nutrient transport is effected through blood vessels, not diffusion. This tissue can be scaled up to a thickness of several centimeters without problems.

An impressive example for the size of cartilaginous structures in dinosaurs is the olecranon process in the stegosaur Kentrosaurus aethiopicus Hennig, 1915. In the original description a left ulna (MB.R.4800.33, field number St 461) is figured (Hennig 1915: fig. 5) that shows a large proximal process. However, other ulnae of the same species lack this process, and are thus far less distinct from other dinosaurian ulnae (Fig. 3B, C). The process on MB.R.4800.33 and other parts of its surface have a surface texture that can also be found on other bones of the same individual, and may indicate some form of hyperostosis or another condition that leads to ossification of cartilaginous tissues. Fig. 3B–D compares MB.R.4800.33 and two other ulnae of K. aethiopicus from the IFGT skeletal mount. It is immediately obvious that the normally not fossilized cartilaginous process has a significant influence on the ability to hyperextend the elbow, because it forms a stop to extension. Similarly large cartilaginous structures may have been present on a plethora of bones in any number of dinosaur taxa, so that range of motion analyses like the one presented here are at best cautious approximations.

One of the crucial points to take away from all of this is that thick cartilage caps did not only expand or only limit the ranges of motions of different joints. The mistake is to think that soft tissues always do one or the other. The big olecranon in Kentrosaurus probably limited the ROM of the elbow, by banging into the humerus in extension. In contrast, thick articular cartilage at the wrist probably expanded the ROM and may have allowed the strong wrist flexion that some artists have restored for sauropods. I’m not arguing that it must have done so, just that I don’t think we can rule out the possibility that it may have. And so the flipped-back wrist in the Sideshow Apatosaurus does not bother me–but not everyone is convinced. Welcome to science!

I can’t finish without quoting a comment Mike left on Matt Bonnan’s blog a little over a year ago:

Ever since I saw Jensen’s (1987) paper about how mammals are so much better than dinosaurs because their limb-bones articulate properly, I’ve been fuming on and off about this — the notion that the clearly unfinished ends we see are what was operating in life. No.

This is a pretty fair summary of Jensen’s position. Of course, thanks to Heinrich, now we know why dinosaurs had such crap distal limb articulations: they weren’t mammals (part 1part 2part 3).

Finally, interest in articular cartilage is booming right now, as Mike blogged about here. In addition to the Dread Olecranon of Kentrosaurus, see the Dread Elbow Condyle-Thingy of Alligator from Casey Holliday’s 2001 SVP talk, and of course the culmination of that project in Holliday et al. (2010), and, for a more optimistic take on inferring the shapes of articular surfaces from bare bones, read Bonnan et al. (2010).

Next time: texture and color.

References

Necks lie, redux

September 1, 2011

In a recent post I showed photos of the trachea in a rhea, running not along the ventral surface of the neck but along the right side. I promised to show that this is not uncommon, that the trachea and esophagus of birds are usually free to slide around under the skin and are not constrained to like along the ventral midline of the neck, as they usually are in mammals. Here goes.

Here’s figure 5 from van der Leeuw et al. (2001): a lateral x-ray of a duck, reaching up just a bit with its head and neck, possibly to get a bite or just look around. Click through for the unlabeled version.

There’s a LOT of stuff going on in this image:

  • As promised, the trachea (blue lines) is taking a very different path to the head than the vertebrae and skeletal muscles.
  • As usual for tetrapods, the neck is extended at the base in the caudal half and flexed at the head in the cranial half.
  • The epaxial (dorsal) muscles at the base of the neck are not tied down to the vertebral column so they are free to bowstring across the U-bend at the base of the neck (black arrow)–this was the point of the figure in the original paper. Although the gross outline of the neck also deviates from the vertebral column on the ventral side near the head, this is caused by the trachea and gullet approaching the pharynx, not because the hypaxial muscles are bowstringed across the curve.
  • As the post title intimates, this neck lies: the cervical vertebrae are significantly more extended than one would expect based on the external appearance of the neck alone. The red line shows the angle of the most strongly retroverted vertebra, which I measure at 48.5 degrees from vertical (41.5 degrees above horizontal)–slightly closer to horizontal than to vertical! We have seen this before, in most mammals and in a couple of small birds (see this post); here we see it even in a reasonably large, long-necked bird.
  • Worse, the gross outline of the neck–what one can see from the outside–lines up with nothing on the inside: the trachea is less curved and the vertebral column is more curved.

Same points again, this time in a chicken in an alert posture (Vidal et al. 1986: fig. 7). Here the most strongly retroverted cervical is 36 degrees from vertical (54 degrees above horizontal).

What’s all this got to do with sauropods?

First, it shows that even in animals with long, slender necks, it’s not enough to show a photo or painting of an extant animal and make assertions about what the cervicals are doing (necks lie, again). It’s even less defensible to make the dual assertions that (a) the gross outline of the neck shows the path of the cervicals and (b) the cervicals are in ONP, all based on a photo or painting of a living animal. The first point can only be established by radiography, and the second by manipulation of the skeleton, either physically or digitally. It may seem like I’m tilting at windmills here, but we’ve seen these very assertions made in conference talks. As always, we’ll follow where the evidence leads, but not until we see some actual evidence.

Second,  I am increasingly haunted by the idea that we are all waaay too influenced, even (maybe especially) subconsciously, by big mammals when we think about sauropods and their necks. Big mammals–like, say, horses and giraffes–have:

  • only 7 cervical vertebrae;
  • lots of big muscles that attach to the thorax and the head and cross the cervical column without attaching to it much or at all;
  • presacral neural spines that max out, height-wise, over the shoulders, creating withers;
  • alert neck postures that are elevated (like all tetrapods) but often short of vertical, with the vertebrae often held more-or-less straight through the middle section of the neck (camels are an obvious exception here).

In contrast, birds have:

  • many cervical vertebrae, from a 12  or so up to 27 or 28;
  • almost no muscles that span from thorax to skull;
  • presacral neural spines that rise monotonically to the synsacrum (except–maybe–in Giraffatitan);
  • alert neck postures that are S-shaped, with the craniocervical joint over or just slightly in front of the cervicodorsal junction.

Which group sauropods had more in common with is left as an exercise for the reader.

References

  • van der Leeuw, A.H.J., Bout, R.G., and Zweers, G.A. 2001. Evolutionary morphology of the neck system in ratites, fowl, and waterfowl. Netherlands Journal of Zoology 51(2):243-262.
  • Vidal, P.P., Graf, W., and Berthoz, A. 1986. The orientation of the cervical vertebral column in unrestrained awake animals. Experimental Brain Research 61: 549­-559.