New paper out today: Aureliano et al. (2023) on pneumaticity in the early dinosaur Macrocollum

March 28, 2023

Figure 1. Skeletal reconstruction of the unaysaurid sauropodomorph Macrocollum (CAPPA/UFSM 0001b) showing vertebral elements along the spine and putative reconstruction of the air sac systems involved. (a) Pneumatic posterior cervical vertebra and a cross-section CT slice in b. (c) a pneumatized anterior dorsal vertebra with cross-section CT slice in d, and detail of the pneumatic foramen in e. (f) Detail of the pneumatic foramen in a reconstructed 3D model of the element. (g) Anterior cervical element (apneumatic). (h) Posterior dorsal vertebra shows no traces of PSP. The sacral series (i), as well as the anterior (k) and mid-caudal (j) series are apneumatic. a, g, h, j, and k are in left lateral view. c, e and f are in right lateral view. i is in dorsal view. ABD, abdominal diverticula; CER, cervical diverticula; LUN, lung; pf, pneumatic foramen. The reconstruction was made by Rodrigo T. Müller. Scale bar of the skeletal reconstruction = 500 mm; a–j = 20 mm. (Aureliano et al. 2023)

New paper out today:

Tito Aureliano, Aline M. Ghilardi, Rodrigo T. Müller, Leonardo Kerber, Marcelo A. Fernandes, Fresia Ricardi-Branco, Mathew J. Wedel. 2023. The origin of an invasive air sac system in sauropodomorph dinosaurs. The Anatomical Record

This paper is basically the second part of a one-two punch with our paper on vertebral internal structure in early saurischians from last December (Aureliano et al. 2022). In that paper we found no evidence of invasive pneumaticity in the basal sauropodomorphs Buriolestes and Pampadromaeus, nor in the herrerasaurid Gnathovorax, although we did find some pretty interesting non-pneumatic anatomy inside the vertebrae. In this study we did find invasive pneumaticity in the basal sauropodomorph Macrocollum — but not in the way that I expected.

I’ve been noodling around about the origins of pneumaticity in saurischian dinosaurs for a while now. Early on, I expected that the origin of pneumaticity would be found in the lateral fossae in the centra of presacral vertebrae. I even drew a figure illustrating that hypothesis in my 2007 prosauropod pneumaticity paper:*

TEXT-FIG. 8. Diagram showing the evolution of fossae and pneumatic chambers in sauropodomorphs and their outgroups. Vertebrae are shown in left lateral view with lines marking the position of the cross-sections, and are not to scale. The omission of ‘prosauropods’ from the figure is deliberate; they have no relevant apomorphic characters and their vertebrae tend to resemble those of many non-dinosaurian archosaurs. Cross-sections are based on first-hand observation (Giraffa and Arizonasaurus), published sections (Barapasaurus, Camarasaurus and Saltasaurus) or CT scans (Apatosaurus and Haplocanthosaurus). Giraffa based on FMNH 34426. Arizonasaurus based on MSM 4590 and Nesbitt (2005, fig. 17). Barapasaurus based on Jain et al. (1979, pls 101–102). Apatosaurus based on CM 11339. Haplocanthosaurus based on CM 572. Camarasaurus based on Ostrom and McIntosh (1966, pl. 24). Saltasaurus modified from Powell (1992, fig. 16). (Wedel 2007)

*When I announced the publication of that paper to friends and colleagues, I quipped, “Were prosauropods pneumatic? The fossils don’t say. Somehow I stretched that out to 16 pages.” Mike later told me that because of that self-deprecating description, he’d never been able to take that paper very seriously.

Yates et al. (2012) blew up that clean hypothetical sequence. The best available evidence at the time showed that pneumaticity was actually pretty widespread in basal sauropodomorphs, but the most diagnostic pneumatic features were not on the centrum. Rather, they were the laminae and subdivided fossae just ventral to the diapophyses. 

Fig. 9. Middle posterior dorsal vertebra of Antetonitrus ingenipes (BP/1/4952); A, right lateral; B, posterior views; C, left posterior infradiapophyseal fossa; D, right posterior infradiapophyseal fossa in oblique posterolateral and slightly ventral views; E, Close up of invasive left posterior infradiapophyseal subfossa. Abbreviations: cpol, centropostzygapophyseal lamina; dp, diapophysis; hs, hyposphene; il, internal lamina; midf, middle infradiapophyseal fossa; nc, neural canal; ncas, neurocentral articuloar surface; ns, neural spine; pcdl, posterior centrodiapophyseal lamina; pidf, posterior infradiapophyseal fossa; podl, postzygadiapophyseal lamina; poz, postzygopophysis; pp, parapophysis; prz, prezygopophysis; sf, subfossa. Scale for A, B, C and D, 100 mm; for C, 20 mm. (Yates et al. 2012)

That finding would dovetail with my work with Jessie Atterholt on paramedullary diverticula in birds and other dinosaurs (finally published last year but gestating much longer; Atterholt and Wedel 2022) and with my work with Mike on the developmental sequence of spinal cord -> spinal arteries -> pneumatic diverticula (Taylor and Wedel 2021), culminating in this figure:

Figure 4. Fossae and foramina adjacent to the neural canal in ornithodiran archosaurs. Fossae are shown in dark grey, foramina in black. Neural canals are labelled “nc”. A: Pterosauria, represented by cervical vertebra 9 of Pteranodon sp. YPM 2767 in anterior view (traced from Bennett 2001: figure 42). B: Theropoda, represented by dorsal vertebra 14 of Allosaurus fragilis UUVP 6000 in anterior view (traced from Madsen 1976: plate 23). C: Basal Sauropodomorpha, represented by a posterior dorsal vertebrae of Aardonyx celestae BP/1/6566 in posterior view (traced from Yates et al. 2012: figure 7). D: Neosauropoda, represented by cervical vertebra 5 of Diplodocus carnegii CM 84 in posterior view (traced from Hatcher 1901: plate 6). (Taylor and Wedel 2021)

…and this passage (Taylor and Wedel 2021: p. 8):

It is also notable that paired pneumatic fossae or foramina occur lateral or dorsolateral to the neural canal in every archosaurian clade with postcranial pneumaticity (Figure 4). These fossae and foramina occur in taxa with and without lateral cavities in the centra, and with and without laminated neural arches, so they are probably the most consistent osteological correlates of pneumaticity across non-avian ornithodirans. The consistent appearance of vertebral pneumaticity in areas adjacent to the neural canal corroborates the hypothesis that segmental spinal arteries were crucial in “piloting” pneumatic diverticula as they developed.

But I never looped that back to prosauropods. For a long stretch — 10 years — I wasn’t working on prosauropods or the origin of pneumaticity, in part that was because I was working on other things, but more importantly, because I had no new data on prosauropods. Then Tito Aureliano invited me to collaborate, and here we are. 

What’s surprising to me about the pneumaticity in Macrocollum is that although some of the vertebrae have pneumatic fossae in their centra, the most consistent and most invasive pneumaticity is in the neural arches. Arguably I should have seen that coming, especially after the bit I just quoted about how pervasive is pneumaticity adjacent to the neural canal. But even after that, I thought of neural arch pneumaticity as a sort of sideshow or opening act, just warming things up before the real pneumatization took off in the centrum.

Figure 3. Micro-CT scan of the anterior (second) dorsal vertebra of the unaysaurid sauropodomorph Macrocollum (CAPPA/UFSM 0001b). (a) and (b) show cross-sections of the entire vertebra in anterior view at the approximate midpoint. (e) and (f) show midshaft slices in lateral view. (f) shows three fossae in the neural arch (cprf, cdf and cpof). c, centrum; cdf, centrodiapophyseal fossa; cdl, centrodiapophyseal lamina; ctr, chaotic trabeculae; cpof, centropostzygapophyseal fossa; cpol, centropostzygapophyseal lamina; cprf, centroprezygapophyseal fossa; d, diapophysis; dia, diagenetic artifact; nc, neural canal; ncf, neural canal foramen; pf, pneumatic foramen; po, postzygapophysis; pocdf, postzygapophysealcentrodiapophyseal fossa; pr, prezygapophysis; prcdf, prezygapophysealcentrodiapophyseal fossa; ptc, protocamera; s, neural spine. Scale bar = 10 mm.

Not so, says Macrocollum. Some of the centra have deeply incised lateral fossae, which can be strikingly asymmetrical, but lots of the vertebrae have foramina up under the diapophyses that communicate with pneumatic chambers inside the neural arch. Chambers, plural, in a complex arrangement. That’s a pretty amazing thing to find in such an early sauropodomorph.  And it’s especially exciting to me because it means that possibly I’ve been conceiving of the evolution of vertebral pneumaticity precisely backwards, for decades. I’d much rather be wrong in an interesting way than right in a boring way — especially if I get to be an author on the paper that surprises me.

Here’s my takeaway thought: loads of prosauropods and early theropods have fossae up under the diapophyses. Heck, externally, that’s about all you can see in Macrocollum. And as Yates et al. (2012) pointed out, those fossae are not often prepared completely. But CT reveals that in Macrocollum, those fossae house foramina that communicate with internal chambers. Maybe that form of pneumaticity is actually widespread, and we (= humans) don’t know because we haven’t scanned very many things yet. The horizon is open, and the story can only get richer and stranger from here. What a delightful thing to realize after doing this for 25 years.


8 Responses to “New paper out today: Aureliano et al. (2023) on pneumaticity in the early dinosaur Macrocollum

  1. Brad Lichtenstein Says:

    Agreed that this is an exciting opportunity for someone with lots of time with a CT scanner! And congrats on a paper!!

    Thinking back to your post a few years ago about pelican wing bones, and not meaning to be rude in the least: how is this different? Creating an air cavity in a long cylinder is conceptually about as simple as making macaroni, whereas there’s nothing simple about the developmental gymnastics needed to make the same bone growth mechanisms create the very complex 3D shapes that are vertebrae: wouldn’t the same process produce exactly these multi-chamber results, given the folding and merging also creates laminae and weird shaped outgrowth (as well as the main structural cylinder hidden somewhere in the mess)?

    But even if I’ve got that backwards, that the bone does its gymnastics aiming at its final form, THEN gets penetrated (invasively, as you say) – wouldn’t that be just as true in the pelican wing? And just like the mechanical strain preserves enough thickness in the pelican cylinder’s walls (and crosslinks the ends), wouldn’t the mechanical strains on the vertebra help define pneumatic exclusion zones? Simple shape yields simple pneumatic cavity, complex shape yields complex chambers.

    Sounds good, but…?

  2. Matt Wedel Says:

    Everything you say makes sense, I’ve just never heard it put that way, or thought of it in those terms myself. As far as I can tell, you’ve proposed a new hypothesis that is at the bleeding edge of pneumaticity research.

  3. Brad Lichtenstein Says:

    Well, if that’s actually plausible and not nooby noobness – then I have to apologize that I have neither the CT scanner nor an anatomy lab at my disposal, lol. But I do think the flow-through lung would have had to have been figured out by the length of the windpipe in a sauropod, tho I guess one could posit air exchange in the neck.

  4. llewelly Says:

    Brad, I don’t understand why the length of the sauropod wind-pipe would help figure out flow-through lungs. Is the sauropod wind pipe thought to be flow-through?

    If I am understanding this diagram correctly, the avian wind-pipe is two-way, *not* flow-through, and only the Paleopulmonic parabronchi are flow-through

    I had assumed the same was true of the sauropod wind-pipe. Am I wrong?

  5. Brad Lichtenstein Says:

    Besides mentioning that in the wrong post, I freely admit I know little of the subject. Just humans can’t take a 30 foot (10m) length of garden hose and breathe through it – we simply don’t have the lung capacity to evacuate that much volume. Yes, sauropods will have more lung capacity, but when one of these blog owners used the flow through system as a sauropod prerequisite to actually avoid the stale-air problem otherwise posed by long necks – I assumed they somehow juggled two tubes. I mean, I also assume giraffes don’t, but that’s one reason their necks are so short.

  6. llewelly Says:

    After some thought, I vauguely recall a long thread on this blog that was about the “dead air problem”, but I cannot find it, and the only thing I recall about it was thinking that the huge volume of sauropod lungs would dwarf the volume of the sauropod wind pipe, even without air sacs; I think bird-like lungs probably wouldn’t be necessary. Sperm whales have very long nasal passages that don’t take a direct route (the larger left nasal passage bends around the spermaceti organ, while the right passes under the spermaceti, connects to a distal sac, and then the sac connects to the left nasal passage), and yet they manage.

    For me, the human trying to breathe through a hose is a bad analogy, because if things are scaled up to sauropod size, lung volume will grow as the third power, while wind-pipe volume will be dominated by only the length, because the radius is relatively small. That means the ratio of lung volume to windpipe volume in a sauropod would be much better than for human trying to breath through a hose. The human trying to breathe through a hose is a bad analogy for the same reason a human-sized flea can’t leap tall buildings in a single bound, but this time the faster growth of volume works in the sauropod’s favor.

    The giraffe analogy is a little bit better, but it’s still much smaller than a sauropod, so it still doesn’t work.

    Bird-like lungs would help, because air would passing through the parabronchi while the sauropod was breathing out, but it seems unlikely they would be necessary.

  7. Matt Wedel Says:

    Belatedly chiming in here:

    As far as anyone knows, sauropods had a single trachea with bidirectional airflow. There are a few extant vertebrates that have a divided trachea (left and right halves separated by a midline septum), but they still inhale and exhale through both pipes at the same time. Nobody inhales through one pipe while exhaling through the other. So whatever problems come along with the large dead space imposed by a long trachea simply have to be overcome.

    Birds sometimes have stupidly long tracheae (see some phenomenal images in this post, and the volume of the air sacs, especially the big abdominal air sacs, simply overwhelms the tracheal dead space.

    The same was probably true of sauropods, in that we have loads of evidence for a complex air sac system. But it’s not super-clear that it was necessary. A sperm whale has a trachea about as long as that of Diplodocus and gets on fine with normal mammalian lungs (see our 2013 PeerJ paper for more on this). But we can’t rule out having air sacs facilitated the evolution of long looped or coiled tracheas in at least some sauropods, just like trumpeter swans or some birds of paradise today.

  8. llewelly Says:

    Thank you for replying, Matt, and especially for pointing out that you brought up sperm whales in your 2013 paper; I am sure that’s where I got the idea to bring them up from, though subconsciously, as I didn’t recall it at the time I wrote my comment. The specific quote wasn’t hard to find once you pointed me in the right direction.

    Here it is for completeness:

    “However, whales provide an example suggesting it is unlikely that the evolution of long necks in terrestrial mammals has been limited by tracheal dead space. In a male sperm whale (Physeter) with a total body length of 16 m, the length of the head is 5.6 m (Nishiwaki, Ohsumi & Maeda (1963), cited in Cranford (1999, table 1)). The largest sperm whales are up to 20 m in total body length (Gosho, Rice & Breiwick, 1984), which would give a head length of 7 m if these largest individuals scaled isometrically with the 16-m whales. ”

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