Okay, special dissection post, coming to you live from the Symposium  of Vertebrate Palaeontology and Comparative Anatomy in Lyme Regis, on the Jurassic coast of England, well past my bedtime. First, check out this comment from Neil and see the linked image of some neck muscles in the anhinga. Here’s a small version I’m swiping. There are a couple of short, single-segment muscles shown, but the big long ones in this image are longus colli ventralis (on the ‘front’ or ‘bottom’ of the neck) and longus colli dorsalis (on the ‘back’ or ‘top’).

Now, grok these photos of the same dorsal muscle. Or muscle group, if you prefer. Note that in all cases shown here and in the link–anhinga, rhea, and turkey–the muscle inserts on the anterior cervical vertebrae, and not on the skull.

In Rhea:

In Meleagris (turkey):

The rhea was dissected by Vanessa back at Western a couple of weeks ago, the turkey by me on Mike’s dining room table on Monday. Full story to follow…at some point.

In the meantime, go buy your own turkey and cut up its neck. It’s cheap and you’ll learn a ton.


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.


  • 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.

Wedel’s Theorem:

freezer full of interesting dead animals + great anatomy student who actually wants to get up on Saturday morning and dissect = happiness

The rhea has been the gift that keeps on giving. Saturday was my fourth session with some part of this bird, going back to 2006 (previous posts are here, here, and here). The first two sessions were just about reducing the bird to its component parts, and the last session was all about midline structures.

The goal for the neck is to dissect down to the vertebrae and document everything along the way–muscles, tendons, fascia, blood vessels, and especially diverticula. In the past I have been pessimistic about the chances of seeing diverticula without having them injected with latex or resin or something. But this bird is changing my mind, as we saw in a previous post and as you can see below.

The goal for Vanessa is to grok all of this anatomy, and hopefully make some publishable observations along the way. She has a chance to do something that I think is rather rare for a sauropod paleobiologist, which is to get a firm, dissection-based grounding in bird and croc anatomy before she first sets foot in a museum collection to play with sauropod bones.

That sounds awesome, and probably will be awesome, but before there can be any awesomeness, the fascia has to be picked off the neck. And by ‘picked’ I mean ‘actually cut away, millimeter by arduous millimeter’. It wasn’t that bad everywhere–the fascia over the long dorsal muscles came off very easily. But the lateral neck muscles were actually originating, in part, from the inner surface of the fascia. That’s not unheard of, it happens in the human forearm and leg all the time, but I’ve never seen it as consistently as in this rhea. So picking fascia took a loooong time–that’s what Vanessa is doing in the photo at top.

Once the fascia was off, Vanessa started parting out the long tendons of the hypaxial muscles in the left half of the neck. Meanwhile, I started stripping fascia from the right half. I had forgotten that the right half of the neck still had the trachea and esophagus adhered to the side. That probably sounds weird, given that our trachea and esophagus–and those of most mammals–run right down the middle of our necks and aren’t free to move around much. In birds, they’re more free-floating and can drift around between the skin and the vertebral muscles, sometimes even ending up dorsal to the  vertebral column–there’s a great x-ray of a duck in a  2001 paper that shows this, which I’ll have to blog sometime.

Anyway, when I cut the fascia to pull back the trachea and esophagus, I found that they were separated from the underlying tissues by a dense network of pneumatic diverticula winding through the fascia.

I had heard, anecdotally, of networks of diverticula described as looking like bubble wrap. I can now confirm that is true, for at least some networks. What was especially cool about these is that they were occupying space that would be filled with adipose or other loose connective tissue in a mammal, which illustrates the point that pneumatic epithelium seems to replace many kinds of connective tissue, not just bone–something Pat O’Connor has talked about, and which I also briefly discussed in this post.

I should mention that there was no connection between these diverticula and the trachea, as there is between the subcutaneous throat sac and the trachea in the emu (story and pictures here).

While I was geeking out on diverticula, Vanessa was methodically separating the long hypaxial muscles, which looked pretty cool all fanned out.

And that’s all we had time for on Saturday. But we’re cutting again soon, so more pictures should be along shortly.

I have a new paper out:

Wedel, M.J. 2012. A monument of inefficiency: the presumed course of the recurrent laryngeal nerve in sauropod dinosaurs. Acta Palaeontologica Polonica 57(2):251-256.

Update June 6, 2012: the final version was formally published yesterday, so the rest of this paragraph is of historical interest only. Like Yates et al. on prosauropod pneumaticity, it is “out” in the sense that the manuscript has been through peer review, has been accepted for publication, and is freely available online at Acta Palaeontologica Polonica. Technically it is “in press” and not published yet, but all that formal publication will change is to make a prettier version of the paper available. All of the content is available now, and the paper doesn’t include any of those pesky nomenclatural acts, and so, as with the prosauropod pneumaticity paper, I don’t see any reason to pretend it doesn’t exist. Think of the accepted manuscript as the caterpillar to the published version’s butterfly: different look, but same genome.

This one came about because last summer I read a review of Richard Dawkins’s book, The Greatest Show on Earth: The Evidence for Evolution. The review mentioned that the book includes a lengthy discussion of the recurrent laryngeal nerve (RLN) in the giraffe, which is a spectacularly dumb piece of engineering and therefore great evidence against intelligent design creationism. It wasn’t the first time I’d heard of the RLN, of course. It’s one of the touchstones of both human anatomy and evolutionary biology; anatomy because of its clinical importance in thyroid surgery, known for more than two millennia, and evolutionary biology because it is such a great example of a developmental constraint. (Dawkins’s coverage of all of this is great, BTW, and you should read the book.)

No, the reason the book review inspired me to write the paper was not because the RLN was new to me, but because it was overly familiar. It is a cool piece of anatomy, and its fame is justly deserved–but I am sick and tired of seeing the stinkin’ giraffe trotted out as the ultimate example of dumb design. My beloved sauropods were way dumber, and it’s time they got some credit.

But first, let’s talk about that nerve, and how it got to be there.

No necks for sex? How about no necks for anybody!

Embryos are weird. When you were just a month old (counting from fertilization), you had a set of pharyngeal arches that didn’t look radically different from those of a primitive fish. These started out quite small, tucked up underneath your comparatively immense brain, and each pharyngeal arch was served by a loop of artery called an aortic arch. What we call the arch of the aorta in an adult human is a remnant of just one of these embryonic aortic arches, and as you’ve no doubt noticed, it’s down in your chest, not tucked up next to your brain. When you were in the embryonic stages I’m talking about, you didn’t yet have a neck, so your brain, pharyngeal arches, aortic arches, and the upper parts of your digestive system were all smooshed together at your front end.

One thing you did have at that stage was a reasonably complete peripheral nervous system. The nerve cell bodies in and near your central nervous system sent out axons into the rest of your body, including your extremities. Many of these axons did not persist; they failed to find innervation targets and their parent neurons died. Imagine your embryonic central nervous system sending out a starburst of axons in all directions, and some of those axons finding targets and persisting, and others failing and dying back. So the architecture of your nervous system is the result of a process of selection in which only some cells were successful.

Crucially, this radiation and die-off of axons happened very early in development, when a lot of what would become your guts was still hanging under your proportionally immense brain like the gondola on a blimp. This brings us to the recurrent laryngeal nerve.

Going back the way we came

The fates of your embryonic pharyngeal arches are complex and I’m not going to do a comprehensive review here (go here for more information). Suffice it to say that the first three arches give rise to your jaws and hyoid apparatus, the fourth and sixth form your larynx (voicebox), and fifth is entirely resorbed during development. Update: I made a pharyngeal arch cheat sheet.

There are two major nerves to the larynx, each of which is bilaterally paired. The nerve of the fourth pharyngeal arch becomes the superior laryngeal nerve, and it passes cranial to the fourth aortic arch. The nerve of the sixth pharyngeal arch becomes the inferior or recurrent laryngeal nerve, and it passes caudal to the sixth aortic arch. At the time that they form, both of these nerves take essentially straight courses from the brainstem to their targets, because you’re still in the blimp-gondola stage.

If you were a shark, the story would be over. The more posterior pharyngeal arches would persist as arches instead of forming a larynx, each arch would hold on to its artery, and the nerves would all maintain their direct courses to their targets.

The normal fate of the aortic arches in humans. From http://education.yahoo.com/reference/gray/subjects/subject/135

But you’re not a shark, you’re a tetrapod. Which means that you have, among other things, a neck separating your head and your body. And the formation of your neck shoved your heart and its associated great vessels down into your chest, away from the pharyngeal arches. This was no problem for the superior laryngeal nerve, which passed in front of the fourth aortic arch and could therefore stay put. But the inferior laryngeal nerve passed behind the sixth aortic arch, so when the heart and the fourth and sixth aortic arches descended into the chest, the inferior laryngeal nerve went with them. Because it was still hooked up to the brainstem and the larynx, it had to grow in length to compensate.

As you sit reading this, your inferior laryngeal nerves run down your neck into your chest, loop around the vessels derived from the fourth and sixth aortic arches (the subclavian artery on the right, and the arch of the aorta and ductus arteriosus on the left) and run back up your neck to your larynx. Because they do this U-turn in your chest and go back the way they came, the inferior laryngeal nerves are said to ‘recur’ to the larynx and are therefore more commonly referred to as the recurrent laryngeal nerves (RLNs).

An enlightening diversion

The RLN is the poster child for “unintelligent design” because it is pretty dumb. Your RLNs travel a heck of a lot farther to reach your larynx than they ought to, if they’d been designed. Surely an intelligent designer would have them take the same direct course as the superior laryngeal nerve. But evolution didn’t have that option. Tetrapod embryos could not be built from the ground up but had to be modified from the existing “sharkitecture” of ancestral vertebrates. The rules of development could not be rewritten to accommodate a shorter RLN. Hence Dawkins’s love affair with the RLN, which gets 7 pages in The Greatest Show on Earth. He also appeared on the giraffe episode of Inside Nature’s Giants, in which the RLN was dug out of the neck and the continuity of its ridiculous path was demonstrated–probably the most smack-you-in-the-face evidence for evolution that has ever been shown on television (said the rabid fan of large-tetrapod dissections).

Incidentally, the existence and importance of the RLN has been known since classical times. The RLN innervates the muscles responsible for speech, and on either side it passes right behind the thyroid gland, which is subject to goiters and tumors and other grotesque maladies. So a careless thyroidectomy can damage one or both of the RLNs; if one gets snipped, the subject will be hoarse for the rest of his or her life; if both are cut, the subject will be rendered mute. The Roman physician Galen memorably demonstrated this by dissecting the neck of an immobilized but unanesthetized pig and isolating the RLNs (Kaplan et al. 2009). One moment the poor pig was squealing its head off–as any of us would be if someone dug out our RLNs without anesthesia–and the next moment Galen severed the RLNs and the animal abruptly fell silent, still in unbelievable pain but now without a mechanism to vocally express its discomfort.

Galen versus pig. Figure 2 from Kaplan et al. 2009.

The name of the nerve also goes back to Galen, who wrote:

I call these two nerves the recurrent nerves (or reversivi) and those that come upward and backward on account of a special characteristic of theirs which is not shared by any of the other nerves that descend from the brain.

Like at least some modern surgeons, Galen does not seem to have been overly burdened by humility:

All these wonderful things, which have now become common property, I was the first of all to discover, no anatomist before me ever saw one of these nerves, and so all of them before me missed the mark in their anatomical description of the larynx.

Both of those quotes are from Kaplan et al. (2009), which is a fascinating paper that traces the knowledge of the recurrent laryngeal nerve from classical times to the early 20th century. If you’d like a copy and can’t get hold of one any other way, let me know and I’ll hook you up.

Share and share alike

By now you can see where this is going: all tetrapods have larynges, all tetrapods have necks, and all tetrapods have recurrent laryngeal nerves. Including giraffes, much to the delight of Richard Dawkins. And also including sauropods, much to the delight of yours truly.

Now, I cannot show you the RLN in a living sauropod, nor can I imagine a scenario in which such a delicate structure would be recognizably preserved as a fossil. But as tetrapods, sauropods were bound to the same unbreakable rules of development as everything else. The inference that sauropods had really long, really dumb RLNs is as secure as the inference that they had brainstems, hearts, and larynges.

Wedel (2012) Fig. 1. Course of the left vagus nerve and left recurrent laryngeal nerve in a human, a giraffe, and Supersaurus. The right recurrent laryngeal nerve passes caudal to the right subclavian artery rather than the aorta and ductus arteriosus, but otherwise its course is identical to that of the left.

Giraffes have necks up to 2.4 meters long (Toon and Toon 2003), so the neurons that make up their RLNs approach 5 meters in the largest indiividuals. But the longest-necked sauropods had necks 14 meters long, or maybe even longer, so they must have had individual neurons at least 28 meters long. The larynx of even the largest sauropod was probably less than 1 meter away from the brainstem, so the “extra” length imposed on the RLN by its recurrent course was something like 27 meters in a large individual of Supersaurus. Take that, Giraffa.

Inadequate giraffe is inadequate.

One way or another

It is possible to have a nonrecurrent laryngeal nerve–on one side, anyway. If you haven’t had the opportunity to dissect many cadavers, it may come as a surprise to learn that muscles, nerves, and blood vessels are fairly variable. Every fall in Gross Anatomy at WesternU, we have about 40 cadavers, and out of those 40 people we usually have two or three with variant muscles, a handful with unusual branching patterns of nerves, and usually half a dozen or so with some wackiness in their major blood vessels. Variations of this sort are common enough that the better anatomy atlases illustrate not just one layout for, say, the branching of the femoral artery, but 6-10 of the most common patterns. Also, these variations are almost always asymptomatic, meaning that they never cause any problems and the people who have them usually never know (ask Mike about his lonely kidney sometime). You–yes, you, gentle reader!–could be a serious weirdo and have no idea.

Variations in the blood vessels seem to be particularly common, possibly because the vessels develop in situ with apparently very little in the way of genetic control. Most parts of the body are served by more than one artery and vein, so if the usual vessel isn’t there or takes an unusual course, it’s often no big deal, as long as the blood gets there somehow. To wit: occasionally a person does not have a right subclavian artery. This does not mean that their right shoulder and arm receive no blood and wither away; usually it means that one of the segmental arteries branching off the descending aorta–which normally serve the ribs and their associated muscles and other soft tissues–is expanded and elongated to compensate, and looks for all the world like a normal subclavian artery with an abnormal connection to the aorta. But if the major artery that serves the forelimb comes from the descending aorta, and the 4th aortic arch on the right is completely resorbed during development, then there is nothing left on the right side to drag the inferior laryngeal nerve down into the torso. A person with this setup will have an inferior laryngeal nerve on the right that looks intelligently designed, and the usual dumb RLN on the left.

Can people have a nonrecurrent laryngeal nerve on the left? Sure, if they’ve got situs inversus, in which the normal bilateral asymmetry of the internal organs is swapped left to right. Situs inversus is pretty darned rare in the general population, occurring in fewer than 1 in 10,000 people. It is much more prevalent in television shows and movies, where the hero or villain may survive a seemingly mortal wound and then explain that he was born with his heart on the right side. (Pro tip: the heart crosses the midline in folks of both persuasions, so just shoot through the sternum and you’ll be fine. Or, if you’re worried about penetration, remember Rule #2 and put one on either side.) Anyway, take everything I wrote in the preceding paragraph, mirror-image it left to right, and you’ve got a nonrecurrent laryngeal nerve on the left. But just like the normally-sided person who still has an RLN on the left, a person with situs inversus and no remnant 4th aortic arch on the left (double variation alert!) still has an RLN looping around the aorta and ductus arteriosus on the right.

Bottom line: replumb the vessels to your arms, swap your organs around willy-nilly, you just can’t beat the aorta. If you have an aorta, you’ve got at least one RLN; if you don’t have an aorta, you’re dead, and no longer relevant to this discussion.

Nonrecurrent laryngeal nerves–a developmental Hail Mary?

But wait–how do we know that the inferior laryngeal nerve in embryonic sauropods didn’t get rerouted to travel in front of the fourth and sixth aortic arches, so it could be spared the indignity of being dragged into the chest later on?

First of all, such a course would require that the inferior laryngeal nerve take an equally dumb recurrent course in the embryo. Or maybe it should be called a procurrent course. Instead of simply radiating out from the central nervous system to its targets in the sixth pharyngeal arch, the axons that make up the RLN would have to run well forward of their normal course, loop around the fourth and sixth aortic arches from the front, and then run back down to the sixth pharyngeal arch. There is simply no known developmental mechanism that could make this happen.

Even if we postulated some hypothetical incentive that would draw those axons into the forward U-turn, other axons that took a more direct course from the central nervous system would get to the sixth pharyngeal arch first. By the time the forwardly-recurring axons finished their intelligently-routed course and finally arrived at the sixth pharyngeal arch, all of the innervation targets would be taken, and those axons would die off.

Also, at what point in the evolution of long necks would this forwardly-looping course supposedly be called into existence? Ostriches and giraffes have RLNs that take the same recurrent course as those of humans, pigs, and all other tetrapods. The retention of the recurrent course in extant long-necked animals is further evidence that the developmental constraint cannot be broken.

Finally, the idea that a non-recurrent laryngeal nerve would need to evolve in a long-necked animal is based on the perception that long nerve pathways are somehow physiologically taxing or otherwise bad for the animals in which they occur. But almost every tetrapod that has ever lived has had much longer neurons than those in the RLN, and we all get on just fine with them.

In dire extremity

Probably you have seen enough pictures of neurons to know what one looks like: round or star-shaped cell body with lots of short branches (dendrites) and one very long one (the axon), like some cross between an uprooted tree–or better yet, a crinoid–and the Crystalline Entity. When I was growing up, I always imagined these things lined up nose to tail (or, rather, axon to dendrite) all down my spinal cord, arms, and legs, like boxcars in a train. But it ain’t the case. Textbook cartoons of neurons are massively simplified, with stumpy little axons and only a few to a few dozen terminals. In reality, each neuron in your brain is wired up to 7000 other neurons, on average, and you have about a hundred billion neurons in your brain. (Ironically, 100 billion neurons is too many for your 100 billion neurons to visualize, so as a literal proposition, the ancient admonition to “know thyself” is a non-starter.)

Back to the axons. Forget the stumpy little twigs you’ve seen in books and online. Except for the ganglia of your autonomic nervous system (a semi-autonomous neural network that runs your guts), all of the cell bodies of your neurons are located in your central nervous system or in the dorsal root ganglia immediately adjacent to your spinal cord. The nerves that branch out into your arms and legs, across your face and scalp, and into your larynx are not made of daisy chains of neurons. Rather, they are bundles of axons, very long axons that connect muscles, glands, and all kinds of sensory receptors back to the nerve cell bodies in and around your brain and spinal cord.

Indulge me for a second and wiggle your toes. The cell bodies of the motor neurons that caused the toe-wiggling muscles to fire are located in your spinal cord, at the top of your lower back. Those motor neurons got orders transmitted down your spinal cord from your brain, and the signals were carried to the muscles of your feet on axons that are more than half as long as you are tall.

Some of your sensory neurons are even longer. Lift your big toe and then set it down gently, just hard enough to be sure that it’s touching down on the floor or the sole of your shoe, but not hard enough to exert any pressure. When you first felt the pad of your toe touch down, that sensation was carried to your brain by a single neuron (or, rather, by several neurons in parallel) with receptor terminals in the skin of your toe, axon terminals in your brainstem, and a nerve cell body somewhere in the middle (adjacent to your sacrum and just a bit to one side of your butt crack, if you want the gory details). That’s right: you have individual sensory neurons that span the distance from your brainstem to your most distal extremity. And so does every other vertebrate, from hagfish to herons to hippos. Including, presumably, sauropods.

I had you set your toe down gently instead of pushing down hard because the neurons responsible for sensing pressure do not travel all the way from toe-tip to brainstem; they synapse with other neurons in the spinal cord and those signals have been through a two-neuron relay by the time they reach your brainstem. Ditto for sensing temperature. But the neurons responsible for sensing vibration and fine touch go all the way.

If you want to experience everything I’ve discussed in this post in a single action, put your fingertips on your voicebox and hum. You are controlling the hum with signals sent from your brain to your larynx through your recurrent laryngeal nerves, and sensing the vibration through individual neurons that run from your fingertips to your brainstem. Not bad, eh?

Wedel (2012) Fig. 2. The longest cells in the bodies of sauropods were sensory neurons that connected receptors in the skin of the extremities with interneurons in the brainstem, a pattern of neural architecture that is present in all extant vertebrates. The nerve cell bodies would have been located in the dorsal root ganglia adjacent to the spinal cord. The diagram of the neuron is based on Butler and Hodos (1996: fig. 2–1B).

Getting back to big animals: the largest giraffes may have 5-meter neurons in their RLNs, but some of the sensory neurons to their hindfeet must be more like 8 meters long. I don’t think anyone’s ever dissected one out, but blue whales must have sensory neurons to the tips of their flukes that are almost 30 meters (98 feet) long (subtract the length of the skull, but add the lateral distance from body midline to fluke-tip). And Supersaurus, Amphicoelias, and the like must have had neurons that were approximately as long as they were, minus only the distance from the snout-tip to the back of the skull. I could be wrong, and if I am I’d love to be set straight, but I think these must have been the longest cells in the history of life.

Oh, one more thing: up above I said that almost every tetrapod that has ever lived has had much longer neurons than those in the RLN. The exceptions would be animals for which the distance from brainstem to base of neck was longer than the distance from base of neck to tip of limb or tail, so that twice the length of the neck would be longer than the distance from base of skull to most distal extremity. In that case, the neurons that contribute to the RLN would be longer than those running from brainstem to tail-tip or toe-tip. Tanystropheus and some of the elasmosaurs probably qualified; who else?

Parting Thoughts

In this post I’ve tried to explain the courses that these amazingly long cells take in humans and other vertebrates. I haven’t dealt at all with the functional implications of long nerves, for which please see the paper. The upshot is that big extant animals get along just fine with their crazy-long nerves, and there’s no reason to assume that sauropods were any more troubled. So why write the paper, then? Well, it was fun, I learned a lot (dude: axoplasmic streaming!), and most importantly I got to steal a little thunder from those silly poseurs, the giraffes.

Department of Frivolous Nonsense: yes, I titled the paper after those TV ads for Chili’s hamburgers from a few years back. If you never saw them, the ads compared mass-produced, machine-stamped fast-food burgers with restaurant burgers painstakingly built by hand, and concluded with, “Chili’s Big-Mouth Burgers: monuments of inefficiency!”

Update: All of the following is out of date now that the paper has been formally published. Department of Good Karma: since the paper is at the “accepted manuscript” stage, I still have the chance to make (hopefully minor) changes when I get the proofs. As is always, always, always the case, I caught a few dumb errors only after the manuscript had been accepted. Here’s what I’ve got so far, please feel free to add to the list:

  • Page 1, abstract, line 3: pharyngeal, not pharyngial
  • Page 1, abstract, line 8: substitute ‘made up’ for ‘comprised’
  • Page 6, line 12: substitute ‘make up’ for ‘comprise’
  • Page 9, line 5: citation should be of Carpenter (2006:fig. 3), not fig. 2
  • Page 10, line 7: “giant axons of squid are”, not ‘ares’
  • Page 12, entry for Butler and Hodos should have year (1996)
  • Page 12, entry for Carpenter has ‘re-evaluation misspelled
  • Page 16, entry for Woodburne has ‘mammalian’ misspelled

(Notes to self: stop trying to use ‘comprise’, lay off the ‘s’ key when typing bibliography.)


Thanks to everyone who joined in the discussion last time on why sauropods had such long necks.  I’ve discussed this a little with Matt, and we are both amazed that so many different hypotheses have been advanced (even if some of them are tongue-in-cheek).  We’ll probably come back to all these ideas later.

But today, we want to draw your attention to a new contribution to this discussion — a paper in the Journal of Zoology, with the tell-it-like-it-is title “The long necks of sauropods did not evolve primarily through sexual selection”, written by the three of us SV-POW!er rangers together with our buddy Dave “Archosaur Musings” Hone (Taylor et al. 2011).

Taylor et al. (2011), fig. 1: Sauropod necks, showing relationships for a selection of species, and the range of necks lengths and morphologies that they encompass. Phylogeny based on that of Upchurch et al. (2004: fig. 13.18). Mamenchisaurus hochuanensis (neck 9.5 m long) modified from Young & Zhao (1972: fig. 4); Dicraeosaurus hansemanni (2.7 m) modified from Janensch (1936: plate XVI); Diplodocus carnegii (6.5 m) modified from Hatcher (1903: plate VI); Apatosaurus louisae (6 m) modified from Lovelace, Hartman & Wahl (2008: fig. 7); Camarasaurus supremus (5.25 m) modified from Osborn & Mook (1921: plate 84); Giraffatitan brancai (8.75 m) modified from Janensch (1950: plate VIII); giraffe (1.8 m) modified from Lydekker (1894:332). Alternating grey and white vertical bars mark 1 m increments.

This is one of those papers that has been literally years in the making, which is why it’s a rather belated response to the paper that we were responding to — Phil Senter’s (2006) argument that sexual selection was the primary driver of neck elongation in sauropods.

Senter supported his hypothesis by laying out six predictions which he argued should be true for sexually selected necks; then showing that, while the first two could not be assessed, the last four all supported sexual selection.  In our paper, we do three things.  First, we make the point that sexual selection and feeding advantage are not mutually exclusive.  Second, we revisit all six predictions and show that they do not in fact support sexual selection — in fact, most of them provide support for feeding advantage.  Finally, we show that no tetrapod clade comparable with Sauropoda has consistently selected for a single sexual signal.

My email records show that Darren, Matt and I were discussing this as early as 22 September 2006, just six weeks after Senter’s paper was published, and that we started working on a response only a couple of days later.  But as so often happens, it got crowded out by a hundred other things.  Then in November 2007 Dave Hone mentioned that he was independently thinking of writing a response, and we decided to join forces.  And then … we all went back to working on other things again, touching on the necks-for-sex issue every now and then.  It’s mostly due to Dave’s repeated prods that this project wasn’t allowed to wither away, and has now, finally, made it across the finish line.

Like the neck-posture paper (Taylor et al. 2009), this was a true collaboration — one of those where, for many parts of the text, none of us is sure which of us originally wrote it.  It went through the wringer many times before reaching its final form, and most of the text must have been rewritten two or three times along the way.  We hope all the shuffling and polishing has resulted in a paper that reads straightforwardly and even seems obvious.  “When something can be read without effort, great effort has gone into its writing” — Enrique Jardiel Poncela.  That’s the goal, anyway.

The paper itself is available at the link below, so take a look and see whether you find our argument convincing.  As always, comments are open!

Update (the next morning)

Co-author Dave Hone discusses this paper on his own blog.


When you last saw this rhea neck, I was squeezing a thin, unpleasant fluid out of its esophagus. Previous rhea dissection posts are here and here; you may also be interested in my ratite clearing house post.

We did that dissection back in 2006. Since then I finished my dissertation, got a tenure-track job, and moved twice. The rhea neck followed me, living in a succession of freezers until last spring.

Last spring I thawed it out, straightened it (it had been coiled up in a gallon ziploc), refroze it, and had it cut in half sagittally with a bandsaw. I did all of this for a project that is not yet ready to see the light of day, but there’s a ton of cool morphology here that I am at liberty to discuss, so let’s get on with it.

Throughout the post, click on the images for full resolution, unlabeled versions.

In the image above, you’ll notice that the saw cut was just slightly to the left of the midline, so that almost the entire spinal cord was left in the right half of the neck (the one toward the top of the image; the left half, below, is upside down, i.e. ventral is towards the top of the picture). The spinal cord is the prominent yell0w-white stripe running down the middle of the hemisectioned neck. It’s a useful landmark because it stands out so well. Dorsal to it are the neural arches, spines*, and zygapophyses of the vertebrae, and epaxial muscles; ventral to it are the vertebral centra and the hypaxial muscles.

* If you want to call them that–some of them are barely there!

Here’s the large supraspinous ligament (lig. elasticum interspinale), which is similar to the nuchal ligament of mammals but independently derived. Compare to the nuchal ligament of a horse (image borrowed from here):

Note how the actual profile of the neck is vastly different from what you’d suspect based on the skeleton alone. This is one of the reasons that necks lie. For more on the supraspinous ligament in rheas and its implications for sauropods, see Tsuihiji (2004) and Schwarz et al. (2007).

Birds also have very large interspinous ligaments (lig. elasticum interlaminare), each of which connects the neural spines of two adjacent vertebrae. In the above photo, the blunt probe is passing under (= lateral to) the unpaired, midline interspinous ligament. Rheas are unusual among birds in having such a large supraspinous ligament, and you can see that this interspinous ligament is almost as big. If you tear down the neck of a chicken or turkey, you will find huge interspinous ligaments, and the supraspinous ligament will be tiny if you can identify it at all.

Here’s something I don’t think we’ve ever shown before here on SV-POW!: a photograph of an actual pneumatic diverticulum. That’s the dark hole in the middle of the photo. You can see that we’re in the left half of the neck, lateral to the spinal cord, almost to the postzygapophysis, the articular surface of which is more lateral still (“below” or “deep to” the surface you see exposed in this cut). Usually at each intervertebral joint there is a connection between the lateral pneumatic diverticula that run up the side of the cervical column and pass through the cervical rib loops and the supramedullary diverticula that lie dorsal to the spinal cord inside the neural canal. That connecting diverticulum is the one exposed here.

NB: diverticulum is singular, diverticula is plural. There are no diverticulae or, heaven forbid, diverticuli, although these terms sometimes crop up in the technical literature, erroneously. (I hesitate to point this out, not because it’s not important, but because I’ll be lucky if I didn’t screw up a Latin term elsewhere in the post!)

Here are pneumatic diverticula in a transverse CT section of an ostrich neck (Wedel 2007b: fig. 6; compare to Wedel 2003: fig. 2, another slice from the same neck). In this view, bone is white, muscles and other soft tissues are gray, and air spaces are black. A, lateral diverticula running alongside the vertebral centra. B, air spaces inside the bone. C, supramedullary airways above the spinal cord. This section is close to the posterior end of a vertebra; the flat-bottomed wing-like processes sticking out to either side are the anterior portions of the postzygapophyses. If the slice was a few mm more posterior, we would see the prezygapophyses of the preceding vertebra in contact with them. Also, the vertical bars of bone connecting the centrum to the postzygs would pinch out, and we’d see the diverticula connecting the lateral (A) and supramedullary (C) airways–that’s the diverticulum revealed in the photo two images up.

Here’s another cool section showing a diverticulum and some muscles. Note the short interspinous muscles, which connect the neural spines of adjacent vertebrae. The probe indicates another open diverticulum, and the very tip of the probe is under one of the very thin layers of epithelium that line the diverticula. You can see that this diverticulum lies on the dorsal surface of the vertebra, posterior to the prezygapophysis and anterior to the neural spine. This supravertebral diverticulum is near and dear to my heart, because I have published an image of its traces before.

Lots going on in this photo (remember that you can click for an unlabeled version). This is a middle cervical vertebra of an emu, in anterodorsal view, with anterior towards the bottom of the picture. Bonus geek points if you recognized it as the basis for Text-fig. 9 in Wedel (2007a). I published this photo in that paper because it so nicely illustrates how variable the skeletal traces of pneumaticity can be, even from left to right in a single bone. On the right side of the photo (left side of the vertebra), the bone resorption adjacent to the supravertebral diverticulum produced a pneuamtic fossa, but one without distinct bony margins or a pneumatic foramen. On the other side, the fossa contains a pneumatic foramen which communicates with the internal air spaces, but the fossa is otherwise identical. Fossae like the one on the right are a real pain in the fossil record, because they might be pneumatic, but then again they might not be; such shallow, indistinct fossae can house other soft tissues, including cartilage and fat. This is what I was talking about when I wrote (Wedel 2009: p. 624):

If progressively more basal taxa are examined in the quest to find the origin of PSP [postcranial skeletal pneumaticity], the problem is not that evidence of PSP disappears entirely. It is that the shallow, unbounded fossae of basal dinosaurs are no longer diagnostic for pneumaticity.

For more on that problem, see Wedel (2007a) and the post, “X-Men Origins: Pneumaticity”.

The other labelled bits in the above photo are all muscle attachment points, and you may find Wedel and Sanders (2002), especially Fig. 2, a useful reference for the rest of the post. The dorsal tubercles, or epipophyses, are rugosities dorsal to the postzygapophyses that anchor most of the long, multi-segment epaxial muscles, which in birds are the M. longus colli dorsalis, which originates on the anterior faces of the neural spines, and M. ascendens cervicalis, which originates on the cervical rib loops. The crista transvers0-obliqua is a low, bony crest connecting each dorsal tubercle to the neural spine; it corresponds to the spino-postzygapophyseal lamina (SPOL) of sauropods (see Tutorial 4: Laminae!), and anchors the Mm. intercristales, a group of short muscles that span the cristae of adjacent vertebrae, like the Mm. interspinales only more lateral.

The carotid tubercles serve as points of origin for the M. longus colli ventralis, one of the largest and longest of the multi-segment hypaxial muscles; they have no obvious homolog or analog in sauropods. The lack of this feature might indicate that the hypaxial muscles were less of a big deal in sauropods, for whom lifting the neck was presumably a bigger problem than lowering it. Alternatively, the M. longus colli ventralis of sauropods might have attached to the medial sides of the parapophyses and the capitula of the cervical ribs, which tended to be larger and more ventrally-directed than in basal sauropodomorphs and theropods.

The unlabeled red arrows mark the lateral tubercles and crests of the cervical rib loop, to which we will return momentarily.

Here you can see a big bundle of long epaxial muscles, including both the M. longus colli dorsalis and M. ascendens cervicalis, inserting on the left dorsal tubercle of the vertebra on the right.  Note that the cut here is quite a bit lateral of the midline, and actually goes through the lateral wall of the neural canal in the vertebra on the right (that vert is the fifth back from the front of the section of neck featured in this post, which is incomplete). That is why you see the big, multi-segment muscles here, and not the shorter, single-segment muscles, which lie closer to the midline.

Here are some more muscle attachment points in a bird vertebra (a turkey this time, courtesy of Mike). The lateral crests and tubercles (tubecula ansae and cristae laterales, if you’re keeping track of the Latin) are the same bony features indicated by the red arrows in the photo of the emu vertebra up above. They anchor both the long M. ascendens cervicalis, which inserts on the dorsal tubercles of more anterior vertebrae, and the short Mm. intertransversarii, which span the cervical rib loops of adjacent vertebrae. Sauropods usually have at least small rugosities on their diapophyses and the tubercula of their cervical ribs (which articulate with the diapophyses) that probably anchored homologous muscles.

Here’s a dorsal tubercle above the postzyg on the neural arch of a juvenile Apatosaurus (cervical 6 of CM 555, shown in right lateral view). Notice that the spinopostzygapophyseal lamina (SPOL) and postzygodiapophyseal lamina (PODL) actually converge on the dorsal tubercle rather than on the postzyg. This is pretty common, and makes good mechanical sense.

Dorsal tubercles again, this time on the world’s most wonderful fossil, cervical 8 of the HM SII specimen of Giraffatitan brancai, in the collections of the Humbolt museum in Berlin. While you’re here, check out the pneumato-riffic sculpting on the lateral faces of the neural arch and spine, and the very rugose texture on the tip of the neural spine, SPOLs, and dorsal tubercles. In fact, compare the numerous pocket-like external fossae on this vertebra with the internal air cells exposed in the cross-sectioned rhea neck. I have argued here before that sauropod cervical vertebrae are pretty similar to those of birds; the main differences are that the cervical rib loops are proportionally much smaller in sauropods, and sauropod vertebrae mostly wore their pneumaticity on the outside.

Farther anteriorly in the neck–the three vertebrae pictured here are the third, fourth, and fifth (from right to left) in this partial neck–and somewhat closer to the midline. Now you can see some short epaxial muscles, probably Mm. intercristales and Mm. interspinales (the two groups grade into each other and are often not distinct), spanning adjacent vertebrae. As in several previous photos, the supravertebral diverticulum is visible, as well as the communicating diverticulum that connects the lateral diverticula to the supramedullary airways. I forgot to label them, but ventral to the centra you can see long, light-colored streaks running through the hypaxial muscles. These are the tendons of the M. longus colli ventralis, and in some of the previous photos you can see them running all the way to their origination points on the carotid tubercles. These extend posteriorly from the short cervical ribs of birds, and are homologous with the long cervical ribs of sauropods.

That’s all I have for this time. If you’d like to see all of this stuff for yourself, turkey necks are cheap and big enough to be easy to work with. Geese are good, too. You can see all the same bits in a chicken or a duck, it’s just harder because everything is smaller (if you’re a real glutton for punishment, try a Cornish game hen).

When I first started working on sauropods, their cervical vertebrae made no sense to me. They were just piles of seemingly random osteology. The first time I dissected a bird neck was an epiphany; ever since then, it is hard for me to look at sauropod vertebrae and not see them clad in the diverticula and muscles that shaped their morphology. Go have fun.


Many thanks to Mark Evans of the New Walk Museum, Leicester, for this photograph of yet another camel skeleton, this one from the MNHN in Paris, France:


Head and neck of Bactrian camel (Camelus bactrianus) in right lateral view. Photograph by Mark Evans.


This is especially interesting because it’s our first Bactrian camel — the Cambridge Camel and the Oxford camel are both dromedaries.  I’d wondered whether one species might have a better articulating cervical skeleton than the other, but it seems there is little or nothing to choose between them.

Also of note in this photo is the juvenile camel giraffe in the background, which has thoughtfully been mounted with its nuchal ligament in place.  It’s interesting to see how this ligament has branches that insert separately on the neural spines of all seven cervical vertebrae.  Note, too, that the intervertebral cartilage seems to have been left in place.  This would be good to see in the flesh …  sigh … another reason to revisit Paris, the most hostile city in the world.

Getting back to the adult dromedary in the foreground, here’s a zoom into the joint between the second and third cervicals, with the background smoothed out between them so that you can more easily see the gape between the centra:


Articulated cervical vertebrae 2 and 3 of Bactrian camel (Camelus bactrianus) in right lateral view. Photograph by Mark Evans.


And remember that, once more, the posture adopted for the skeletal mount is much less strongly flexed than the habitual posture in life.  And other postures also adopted in life are more extreme still:


Male dromedary camels (Camelus dromedarius) in rut, with extended necks. Photograph by Gordon Grigg.


This photograph, kindly provided by Gordon Grigg of the University of Queensland, shows typical rutting behaviour of dromedary camels, which he observed closely for his recent paper on the role of strategic hypothermia in reproductive success (Grigg et al. 2009).  The more distant of the two camels is in a truly ridiculous pose.  And it’s ever siller when we bear in mind that necks lie: knowing what we do about the trajectory of the cervical vertebral column within the fleshy neck of tetrapods, it seems likely that the cervical skeletons of these animals were posed something like this:

If you compare these postures with the one that I photoshopped in the Cambridge Camel post, you’ll see that these are more extreme.  I ought to ‘shop the Cambridge camel vertebrae into this pose some time and see just how dumb it looks.

But of course, this may not be as extreme as camel neck poses get.  A few times in recent articles and comments, we’ve alluded to the camel-neck illustration from Kent Stevens’s 2005 talk to the German Research Group on Sauropod Biology at the Sauriermuseum in Aathal, Switzerland.  For those who don’t want to download the complete set of slides, here is that illustration:

We don’t know the provenance of this picture — or, given the low resolution — even whether it’s a photograph or a drawing.  But if it’s real, it’s … stunning.

Anyone know where it’s from?  [Update: see Jerry Harris’s comment below.]


  • Grigg, Gordon, Lyn Beard, Birgit Dörges, Jürgen Heucke, Jocelyn Coventry, Alex Coppock and Simon Blomberg.  2009.  Strategic (adaptive) hypothermia in bull dromedary camels during rut; could it increase reproductive success?  Biology Letters 5:853-856, first published online 15 July 2009.  doi: 10.1098/rsbl.2009.0450