The Aerosteon saga, Part 1: Introduction and background

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Pneumatic dorsal vertebrae of Aerosteon (Sereno et al. 2008:fig 7)

Big news this week: Sereno et al. (2008) described a new theropod, aptly named Aerosteon (literally, "air bone"), with pneumaticity out the wazoo: all through the vertebral column, even into the distal tail; in the cervical and dorsal ribs; in the gastralia; in the furcula; and in the ilium. This is huge news, and it's free to the world at PLoS ONE. Pneumatic vertebrae and ribs are the norm in theropods and most sauropods (hence our interest here), but the axial elements of Aerosteon are extremely pneumatic. A pneumatic furcula was reported in the dromaeosaur Buitreraptor (Makovicky et al. 2005), but Aerosteon appears to be a basal tetanuran so it pushes furcular pneumaticity a good distance down the tree. Most exciting are the pneumatic ilium and gastralia. Ilial pneumaticity has been suspected in some sauropods and non-avian theropods but the evidence has been lacking until now; either the ilial chambers could not be traced to pneumatic foramina, or the suspected pneumatic foramina could not be shown to lead to internal cavities. Pneumatic gastralia are really wacky–according to the paper, it is the first discovery of pneumatized postcranial dermal bone, and I certainly don't know of any other examples.

Why is this important? In extant birds, the furcula is only pneumatized by diverticula of the interclavicular air sac, and the ilia are only pneumatized by the abdominal air sacs, so the presence of big pneumatic foramina leading to big internal chambers in both the furcula and ilia of Aerosteon is evidence not just for bird-like air sacs, but specifically air sacs from both the cranial and caudal groups within the thorax that are responsible for the flow-through lung ventilation of birds. It's pretty dynamite stuff.

Right?

Right?

We-ell . . . There is no question that the fossil material is pretty stunning and shows all the morphological features that Sereno et al. claim (and even some that they don't–stay tuned for Part 2). But there are parts of the paper that I disagree with, and to understand why, I have to tell you a little about recent research on pneumaticity in sauropods and theropods. In this post and the next I'll be discussing papers by Pat O'Connor and Leon Claessens, as well as my own; all of these are freely available at the links just provided. So, please, if you have a beef with anything I say below, go read all the relevant literature for yourself, weigh the evidence, and make up your own mind.

First, a brief sketch of what we've been up to. Except for the occasional weirdo (surveyed on the third page here), the only extant tetrapods with postcranial pneumaticity are birds. In birds, postcranial pneumaticity is the skeletal footprint of the lung/air sac system. So if we find postcranial pneumaticity in dinosaurs–say, sauropods, or Aerosteon–we can use the 'rules' from birds to make inferences about the morphology of the respiratory system. We can't tell which way the air was blowing in the lungs, but we can tell the minimum extent of the pneumatic diverticula, and we can make some inferences about lung structure. All of the logic of this is really nicely and concisely laid out in O'Connor and Claessens (2005), which is only three pages of text, so if you want to know more, just go read it.

The hypothesis that sauropods and theropods had air sacs like that of birds has been opposed in a couple of ways: pneumaticity doesn't tell us anything, and vertebral pneumaticity only indicates cervical air sacs. Neither of these counterarguments has gotten much traction, probably because they're so easily falsified. Let's have a look.

Historical Misconception #1: Pneumaticity Is Completely Uninformative

"Without integrating functional data into the study, the most that can be inferred from post-cranial pneumaticity in extinct animals is that, as pointed out by Owen (1856), the pneumatized bones received parts of the lung in the living animal… Because pneumaticity has no known functional role in ventilation or thermoregulation or metabolic rates, its usefulness as a hard-part correlate for lung structure and metabolism is, unfortunately, questionable." (Farmer 2006, pp. 91-92)

Farmer does not distinguish here between inferences based on the presence of postcranial pneumaticity and inferences based on the distribution of postcranial pneumaticity. If all we know about a bone is that it is pneumatic, then she is correct in stating that the most we can conclude is that it was connected to the respiratory system in some way. (The thermoregulatory function of pneumaticity discussed by Seeley [1870] has been demonstrated for cranial pneumaticity [Warncke and Stork 1977] but not for postcranial pneumaticity [Witmer 1997, O'Connor 2006]). But the inference of cervical and abdominal air sacs in non-avian dinosaurs does not depend simply on the existence of postcranial pneumaticity. Rather, these inferences are based on patterns of postcranial pneumaticity that are diagnostic for specific air sacs.

Verdict: Fail.

Historical Misconception #2: Vertebral Pneumaticity Only Comes From Cervical Air Sacs

"Pneumatization of the vertebrae and ribs is invariably accomplished by diverticuli [sic] of the cervical air sacs (McLelland 1989a), which are located outside the trunk and contribute little, if anything, to the respiratory air flow (Scheid and Piiper 1989). Presence of pneumatized vertebrae in non-avian dinosaurs therefore only speaks of the possible presence of such nonrespiratory diverticuli [sic], and cannot be regarded as indicative of an extensive, avian-style abdominal air-sac system." (Ruben et al. 2003, p. 153)

This remarkable statement is repeated pretty much verbatim by Chinsamy and Hillenius (2004) and Hillenius and Ruben (2004). What's remarkable about it is that is so thoroughly inaccurate. People have known for more than 100 years that the posterior parts of the vertebral column of birds are pneumatized by diverticula of the abdominal air sacs, and said as much in many papers–for example, Muller (1908), Cover (1953), King (1966, 1975), Duncker (1971), Hogg (1984a, b), and Bezuidenhout et al. (1999). Still, if McLelland said that the vertebrae and ribs are "invariably" pneumatized by diverticula of the cervical air sacs, it's not their bad, right?

Okay, first, McLelland (1989) is a review paper and presents no new data (this will become really important later on, when we get back to Aerosteon). Second, here's what McLelland actually said:

"What can be stated with certainty is that in birds generally the cervical air sac aerates the cervical and thoracic vertebrae (Fig. 5. 22) and the vertebral ribs; the clavicular air sac aerates the sternum, sternal ribs, pectoral girdle and humerus (Fig. 5. 23); and the abdominal air sac aerates the synsacrum, pelvis and femur." (pp. 271-272)

By listing the synsacrum and pelvis separately, McLelland clearly meant that the synsacral vertebrae are pneumatized by the abdominal air sac, and this is confirmed by the sources he cited elsewhere: Hogg (1984a, b).

So Ruben et al. (2003)–and those who recycled that text–were relying not on any of their own research, or any primary research at all, but on a single review paper that actually says exactly the opposite of what they claim it does, based on other primary research papers (those by Hogg) that themselves say the same (opposite) thing.

Verdict: EPIC FAIL.

The Brave New Post-2005 World

He said, she said, yadda yadda. There are lots of inaccuracies in the literature, and it's not like birds are extrasolar planets. If we want to know what is going on inside them, we can just look. That's what O'Connor and Claessens (2005) did, by injecting and dissecting 200+ birds representing 19 avian orders. Know what they found? The cervical diverticula do not EVER go farther down the vertebral column than the middle of the thorax. NEVER EVER. So if you find pneumatic vertebrae in the posterior dorsals, sacrum, or tail, it's pretty likely that they were pneumatized by diverticula of the abdominal air sacs.

I say "pretty likely" because it's always possible that dinosaurian diverticula worked differently, and that the air that got into the posterior part of the vertebral column actually came from the cervical air sacs, or the lungs directly, or from arse gills, or possibly magic rocks. We can imagine lots of ways for air to get into the back half of the vertebral column, but the only one that we've ever seen work in a tetrapod* is diverticula of the abdominal air sacs. Dinosaurs may have worked differently, and had wacky cervical diverticula or arse gills or whatever. But those are not the obvious choices, and we don't have any evidence for them; all the available evidence points to abdominal air sacs.

*Some osteoglossomorph fishes pneumatize the vertebral column from the swimbladder–strange but true!

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So, great. The old confusion has been swept away by a blood-dimmed tide of bird carcasses and good science. Pneumatization of the posterior vertebral column implies abdominal air sacs. The combination of pneumaticity in the neck, trunk, sacrum, and even tail of many theropods and sauropods shows that both cervical and abdominal air sacs were present (as in Apatosaurus, above), which means air sacs both anterior and posterior to the lungs, which means that most (maybe all) saurischians had at least some of the gear they would need for flow-through breathing like that of birds (O'Connor and Claessens 2005, O'Connor 2006, Wedel 2007).

And yea, verily, anatomical accuracy and scientific clarity reigned throughout the land . . .

. . . until now.

TO BE CONTINUED.

References

• Bezuidenhout, A.J., H.B. Groenewald, and J.T. Soley. 1999. An anatomical study of the respiratory air sacs in ostriches. Onderstepoort Journal of Veterinary Research 66:317-325.
• Chinsamy, A., and Hillenius, W.J. 2004. Physiology of nonavian dinosaurs; pp. 643-659 in Weishampel, D.B., Dodson, P., and Osmolska, H. 2004. The Dinosauria, Second Edition. University of California Press, Berkeley.
• Cover, M.S. 1953. Gross and microscopic anatomy of the respiratory system of the turkey. III. The air sacs. American Journal of Veterinary Research 14:239-245.
• Duncker, H.R. 1971. The lung air sac system of birds. Advances in Anatomy, Embryology, and Cell Biology 45(6),1-171.
• Farmer, C.G. 2006. On the origin of avian air sacs. Respiratory Physiology and Neurobiology 154:89-106.
• Hillenius, W.J., and Ruben, J.A. 2004. The evolution of endothermy in terrestrial vertebrates: Who? When? Why? Physiological and Biochemical Zoology 77:1019-1042.
• Hogg, D.A. 1984a. The distribution of pneumatisation in the skeleton of the adult domestic fowl. Journal of Anatomy 138:617-629.
• Hogg, D.A. 1984b. The development of pneumatisation in the postcranial skeleton of the domestic fowl. Journal of Anatomy 139:105-113.
• King, A.S. 1966. Structural and functional aspects of the avian lungs and air sacs. International Review of General and Experimental Zoology 2:171-267.
• King, A.S. 1975. Aves respiratory system; pp. 1883-1918 in Getty, R. (ed.), Sisson and Grossman's anatomy of the domestic animals, 5th edition, volume 2. W.B. Saunders, Philadelphia.
• Makovicky, P.J., Apesteguía, S., and Agnolín, F.L. 2005. The earliest dromaeosaurid theropod from South America. Nature 437:1007-1011.
• McLelland, J. 1989. Anatomy of the lungs and air sacs; pp. 221-279 in King, A.S., and McLelland, J. (eds.), Form and Function in Birds, Volume 4. Academic Press, London.
• Müller, B. 1908. The air-sacs of the pigeon. Smithsonian Miscellaneous Collections 50:365-420.
• O'Connor, P.M. 2006. Postcranial pneumaticity: an evaluation of soft-tissue influences on the postcranial skeleton and the reconstruction of pulmonary anatomy in archosaurs. Journal of Morphology 267:1199-1226.
• O'Connor, P.M., and Claessens, L.P.A.M. 2005. Basic avian pulmonary design and flow-through ventilation in non-avian theropod dinosaurs. Nature 436:253-256.
• Ruben, J. A., Jones, T. D. and Geist, N. R. 2003. Respiratory and reproductive paleophysiology of dinosaurs and early birds. Physiological and Biochemical Zoology 76:141-164.
• Seeley, H.G. 1870. On Ornithopsis, a gigantic animal of the pterodactyle kind from the Wealden. Annals and Magazine of Natural History, Series 4, 5: 279-283.
• Sereno, P.C., Martinez, R.N., Wilson, J.A., Varricchio, D.J., Alcober, O.A., Larsson, H.C.E. 2008. Evidence for avian intrathoracic air sacs in a new predatory dinosaur from Argentina. PLoS ONE 3(9): e3303. doi:10.1371/journal.pone.0003303
• Warncke, G., and Stork, H.G. 1977. Biostatische und thermoregulatorische Funktion der Sandwich-Strukturen in der Schädeldecke der Vögel. Zoologische Anzeiger 199:251-257.
• Wedel, M.J. 2007. What pneumaticity tells us about 'prosauropods', and vice versa. Special Papers in Palaeontology 77:207-222.
• Witmer, L.M. 1997. The evolution of the antorbital cavity of archosaurs: a study in soft-tissue reconstruction in the fossil record with an analysis of the function of pneumaticity. Society of Vertebrate Paleontology Memoir 3:1-73.