A little while ago, news of a new paper by Devon Quick and John Ruben, both of Oregon State University, appeared on the newswires. It got its fair share of publicity.

Entitled 'Cardio-pulmonary anatomy in theropod dinosaurs: implications from extant archosaurs', the paper (Quick & Ruben 2009) purports to show that modern birds are fundamentally different from non-avian dinosaurs in terms of abdominal soft-tissue morphology, ergo birds cannot be modified dinosaurs. In slightly more detail, the paper asserts that a specialised 'femoral-thigh complex', combined with a synsacrum and ventrally separated pubic bones, provides crucial mechanical support for the abdominal wall in modern birds, and has thereby allowed the evolution of large abdominal air-sacs that function in respiration. In contrast, say the authors, theropod dinosaurs (non-avian theropods from hereon, thank you very much) lack these features and, worst of all, had a highly mobile femur that cannot have been incorporated into abdominal support - ergo, non-avian theropods cannot have had abdominal air-sacs that functioned like those of modern birds, ergo non-avian theropods were fundamentally different from modern birds. The implication from this - it's not mentioned in the paper but was of course bigged-up in the press interviews - is that birds cannot be dinosaurs! [adjacent Grey heron Ardea cinerea photo by Neil Phillips].

I said a while ago that I wasn't planning to cover this research, predominantly because I don't find it at all interesting nor worthy of review. After all, Ruben and colleagues seem to have made a career of publishing papers in which they assert that 'birds cannot be dinosaurs because of [insert supposed fatal flaw in the 'birds are dinosaurs' model]', and there's no indication that criticism of their conclusions will cause them to stop now. However, a brief discussion held over at Penguinology has changed my mind: we should try and set the record straight. Or, with great power comes great responsbility, or whatever. What makes this research particularly grating is that, like all the other papers by Ruben, Feduccia, Martin and colleagues, the 'birds are not dinosaurs' movement relies on two under-handed tricks that should be exposed.

Firstly, the papers never really demonstrate anything, but merely try to shoot holes in a given line of supporting evidence. So...

-- respiratory turbinates supposedly falsify dinosaur endothermy (Ruben et al. 1996), even though it's never been demonstrated that respiratory turbinates really are a requirement for any given physiological regime, and even though there are endotherms that lack respiratory turbinates

-- the innards of Sinosauropteryx and Scipionyx supposedly falsify avian-like air-sac systems in non-avian coelurosaurs and demonstrate a croc-like hepatic piston diaphragm (Ruben et al. 1997, 1999), even though a gigantic dose of personal interpretation is required to accept that this claim might be correct, even though crocodilians and dinosaurs are fundamentally different in pelvic anatomy, and even though some living birds have the key soft-tissue traits reported by Ruben et al. in Sinosauropteryx and Scipionyx yet still have an avian respiratory system [alleged diaphragm of Sinosauropteryx highlighted in adjacent image; unconvincing on all levels]

-- the weird leg proportions of birds supposedly falsify the classification of indisputably feathered Caudipteryx as non-avian (Jones et al. 2000), even though there is overlap between birds and non-birds in these data, and even though most of the data is screwy or suspect anyway (Christiansen & Bonde 2002, Dyke & Norell 2005)

... and so on.

Secondly, the papers either practise extremely selective citation, or fail to cite or mention stuff that contradicts what they say. One example: the size and shape of the sternal plates in non-avian coelurosaurs might have important implications for the respiratory physiology used by these animals (read on), yet Ruben and colleagues have repeatedly shown a schematic and incorrect diagram that shows the maniraptoran sternum to be a tiny little blob located along the ventral midline. In fact, the sternum was a gigantic plate (or two gigantic plates), similar to that of birds. In the new paper, Quick & Ruben (2009) figure a dinosaur skeletal reconstruction from 1916, which seems bizarre given that this is now substantially inaccurate in ways that are potentially important to the strength of their case (read on for more on this) [here's the actual reconstruction that Quick & Ruben (2009) use: that's right, Osborn's Tyrannosaurus from 1916, with three fingers and everything].

The hypothesis of 'paradoxical collapse'

As mentioned above, Quick & Ruben (2009) assert that non-avian theropods were fundamentally different in abdominal morphology from extant birds, and they hypothesise (note: hypothesise) that the sub-horizontal avian femur and its associated musculature might be required to prevent collapse of the lateral abdominal wall: most non-avian theropods evidently moved their femora a lot during normal locomotion, hence the femur could not have provided mechanical support to the abdominal walls and hence, say Quick & Ruben, could not have had abdominal air sacs that functioned like those of birds. As we'll see below, this doesn't mean - say the authors - that air-sacs were absent, just that they couldn't have been used like those of birds without paradoxical collapse being a problem. The main problem with this is that it's a hypothesis, or in other words a suggestion, and the authors do say this in the paper (p. 7 of the preprint). Does this hypothesis withstand observation?

The authors would like it to, but, no, it doesn't because the femur is not held sub-horizontally all the time in all birds. Many people know that the thigh moves extensively in running ostriches, and hence there's a lot of time in the running cycle when the thigh isn't providing this supposedly critical support to the abdominal wall. Worst still, ostriches are not unique: the thigh might be sub-horizontal in a standing bird, but the thigh moves up and down, in normal movement, in just about all birds [femoral movement in a guineafowl shown in adjacent image; from Gatesy (1990)]. Strangely, the authors acknowledge this (p. 10 of the preprint), yet still imply throughout the paper that the avian thigh somehow provides a sort of abdominal support that's different from what's seen in other theropods.

I really don't get it: why?? Where is this difference? Here we might find the reason for Quick & Ruben's use of the semi-erect tyrannosaur reconstruction from 1916: when posed like this, theropods have a large, unsupported space between the femur and the posterior end of the ribcage. Yet accurate, modern reconstructions (where the body is posed more horizontally, and the femur is slanted anteroventrally) reduce the size of this space. Quick & Ruben (2009) also note that the avian synsacrum might play a role in preventing paradoxical collapse, but this is not explained, nor it is clear how modern birds are fundamentally different from non-avians in this respect. They also argue that modern birds have much larger 'free pelvic cross-sectional area' than do non-avian theropods (that is, there's more space between the two halves of the neornithine pelvis than there is in the non-avian theropod pelvis): this is true, but, at best, all it means is that non-avian dinosaurs had less space for abdominal air-sacs. It not does demonstrate that they were absent. It all looks like an effort to make non-avian theropods and birds fundamentally different, whereas they actually aren't, and all of the features that seem distinct between the 'extremes' actually form part of a continuum.

In conclusion, paradoxical collapse is probably not a fatal problem for the function of large, avian-style respiratory air-sacs.

Abdominal air-sacs: a role in respiration, or not?

While Quick & Ruben (2009) argue that abdominal air-sacs cannot function in respiration without the 'femoral support' discussed above, they seem not to reject the existence of abdominal air-sacs... instead, they reject the possibility that the sacs were used in avian-style respiration, arguing instead that weight loss was their primary function. Ok, so they agree that abdominal air-sacs were present. Why do they reject, in non-avian dinosaurs, the role of abdominal air-sacs in respiration? Why? Answer: because, so they say, non-avian dinosaurs lack the sternal and costal anatomy required to ventilate air-sacs. Oh really? [image below shows the distribution of air-sacs in a neornithine bird, from Wedel (2003) but modified from Duncker (1971). Note the enormous sternum].

As is well known, birds use extensive dorsoventral movement of their often enormous sternum to ventilate their abdominal air-sacs, and hence their lungs. Quick & Ruben (2009) assert that sternal movement - of the sort used by birds - was not possible in non-avian dinosaurs; they say this because 'in nonavians, sternocostal articulations are flat wherein the distal sternal ribs abut the lateral edges of the sternum to form gliding, synovial joints or firmer, cartilaginous articulations and bird-like motion of the sternum is not permitted' (p. 6 of the preprint). The idea that birds rely on dorsoventral movement of their sterna, and that a huge sternum and associated mobile, ossified sternal ribs are a requirement for avian-style respiration, has been heavily promoted in other Ruben and colleagues papers (though Quick & Ruben (2009, pp. 9-10 of the preprint) do note that sternal length might not be important: read on) [ossified sternal ribs and complex sternocostal joints of a neornithine shown below, from Quick & Ruben (2009)].

Well, ignorance is bliss I suppose. There are two major problem areas here.

Contrary to these assertions (Ruben et al. 1997, 1998, Chinsamy & Hillenius 2004, Quick & Ruben 2009), data from living birds shows that neither a gigantic sternum, nor ossified sternal ribs, nor complex, rotating joints between the sternal edges and the sternal ribs, are requirements for avian-style ventilation of the abdominal air-sacs. To their credit, Quick & Ruben (2009) do note that some birds (including kiwis, emus and the extinct elephant birds and mihirungs) have very small sterna that don't extend as far posteriorly as the abdominal air-sacs: these sterna are actually smaller, compared to trunk length, than those of such non-avian saurischians as dromaeosaurs and diplodocoid and macronarian sauropods (Wedel 2007). However, it's not clear why ossified sternal ribs, or sternal ribs with a particular kind of articulation with the sternal plate, have been deemed so important by Ruben and colleagues: the thoracic ribs and their attendant cartilaginous ribs could do the job just as well, and indeed function perfectly well in the respiratory mechanics of most tetrapods.

The second major problem is that the (often large) sternal plates of some Cretaceous non-avian theropods are usually poorly preserved or distorted, and they're often not preserved at all. One might get the impression from Quick & Ruben's (2009) statement that we have many specimens to go on, but it would be more honest to admit that we really don't have as much information here as we might like. Furthermore, which specimens did Quick & Ruben (2009) have in mind when making the assertion quoted above? They don't say: they merely cite Hillenius & Ruben (2004) and, guess what, this paper doesn't even mention the subject of sternal ventilation or sternal rib morphology.

As it happens, there are in fact a couple of non-avian theropod specimens that are particularly informative here. In the Spanish ornithomimosaur Pelecanimimus, PÃ©rez-Moreno & Sanz (1999) described 'slightly ginglymous' joints between the costal processes on the sternum and the sternal ribs, while in the dromaeosaur Sinornithosaurus, Xu et al. (1999) stated that the sternal rib facets on the sternum 'imply the presence of hinged sternocostal joints in dromaeosaurids, which is not concordant with recent arguments about the ribcage-pectoral girdle complex and the respiratory pattern of theropods' (p. 263: they were referring to Ruben et al. (1997)). In the dromaeosaur sternal plate described by Godfrey & Currie (2004), the sternal articulations for the sternal ribs are 'smooth, roughly circular' (p. 147). Finally, the sternal rib processes in Bambiraptor haven't been described in detail, but they look like convex structures that would have permitted sternal rib rotation (Burnham et al. 2000, Burnham 2004) [the large sternal plates of Velociraptor shown in adjacent image, from Norell & Makovicky (1997). These sternal plates are 20% the length of the trunk: proportionally longer than those of kiwis (17%) and other neornithines with a fully functional set of abdominal air-sacs (Wedel 2007)].

These articulations (I'd be interested to know if others have been described in the literature: this seems to be about it) indicate mobile, synovial sternocostal joints, exactly what Quick & Ruben (2009) say are absent. So thorax morphology in at least some non-avian theropods does indicate that avian-style movement of large, avian-style sternal plates, sternal rib and sternal rib facet morphology was present. As discussed above, however, enormous sternal plates and 'special' sternocostal joints aren't required for avian-style air-sac ventilation in the first place, and saurischian dinosaurs (yes, sauropodomorphs as well as non-avian theropods) do possess the anatomical features required for an avian-style air-sac system.

Papers with a hidden agenda

In conclusion, the presence of abdominal air-sacs in non-avian dinosaurs seems agreed upon - and if you need to know more about the evidence for these structures then go on over to SV-POW! Evidence for the existence of sternocostal movement in coelurosaurian theropods looks good, despite what Quick & Ruben (2009) say. If we combine these bits of information, the logical conclusion is that non-avian theropods were using their sterna and sternal ribs to ventilate their abdominal air-sacs, and here is the avian condition, albeit in less 'extreme' form. The raison d'Ãªtre of Quick & Ruben's (2009) paper is to assert that sternocostal movement didn't happen (when it probably did), and to propose that the thigh was somehow integral to the prevention of 'paradoxical collapse' (when it doesn't seem at all clear why this should be so) [the adjacent picture seems to be accompanying quite a few of the discussions of Quick & Ruben (2009) seen online. I don't know where it came from].

A particularly sympathetic interpretation of their paper might be that enlarged, abdominal air-sacs didn't function in respiration until after the sub-horizontal femur was in place to prevent 'paradoxical collapse'. As outlined here, this is not in agreement with the evidence and can be rejected... but at least it sounds like a proper scientific hypothesis.

A less sympathetic interpretation might be that this is another poor attempt to try and shoot holes in what is actually a tremendously well supported phylogenetic model. What I really object to is the fact that Quick & Ruben (2009) seem to have written their paper with a hidden agenda in mind: in all of the press statements, they've been touting the idea that their paper helps falsify the dinosaurian ancestry of birds, with statements such as the following being thrown around: "It just seems pretty clear now that birds were evolving all along on their own and did not descend directly from the theropod dinosaurs, which lived many millions of years later" (this one was from Devon Quick). Yet this aspect of their approach is not discussed in the paper, nor stated explicitly. This is just downright dishonest. Look, if you have a problem with an idea - so much so that it inspires you to write a paper looking at one aspect of that subject, and so much so that you feel the need to discuss it at length with any journalist who displays interest in your research - at least have the decency and the balls to put your objections and reasoning into the technical literature. Papers are meant to report results, observations and hypotheses: they are not vehicles that allow you to preach your hidden agenda to the press.

The fact that Ruben has been saying things to the press like "Frankly, there's a lot of museum politics involved in this, a lot of careers committed to a particular point of view" doesn't encourage you to think that the authors have a realistic view of how and why we got where we are in the bird origins debate. Of course, creationists just love what Quick and Ruben have been saying.

Refs - -

Burnham, D. A. 2004. New information on Bambiraptor feinbergi (Theropoda: Dromaeosauridae) from the Late Cretaceous of Montana. In Currie, P. J., Koppelhus, E. B., Shugar, M. A. & Wright, J. L. (eds) Feathered Dragons. Studies on the Transition from Dinosaurs to Birds. Indiana University Press (Bloomington & Indianapolis), pp. 67-111.

- ., Derstler, K. L., Currie, P. J., Bakker, R. T., Zhou, Z. & Ostrom, J. H. 2000. Remarkable new birdlike dinosaur (Theropoda: Maniraptora) from the Upper Cretaceous of Montana. The University of Kansas, Paleontological Contributions 13, 1-14.

Chinsamy, A. & Hillenius, W. J. 2004. Physiology of nonavian dinosaurs. In Weishampel, D. B., Dodson, P. & OsmÃ³lska, H. (eds) The Dinosauria, Second Edition. University of California Press (Berkeley), pp. 643-659.

Christiansen, P. & Bonde, N. 2002. Limb proportions and avian terrestrial locomotion. Journal of Ornithology 143, 356-371.

Duncker, H. R. 1971. The lung air sac system of birds. Advances in Anatomy, Embryology, and Cell Biology 45, 1-171.

Dyke, G. J. & Norell, M. A. 2005. Caudipteryx as a non-avialan theropod rather than a flightless bird. Acta Palaeontologica Polonica 50, 101-116.

Gatesy, S. M. 1990. Caudofemoral musculature and the evolution of theropod locomotion. Paleobiology 16, 170-186.

Godfrey, S. J. & Currie, P. J. 2004. A theropod (Dromaeosauridae, Dinosauria) sternal plate from the Dinosaur Park Formation (Campanian, Upper Cretaceous) of Alberta, Canada. In Currie, P. J., Koppelhus, E. B., Shugar, M. A. & Wright, J. L. (eds) Feathered Dragons. Studies on the Transition from Dinosaurs to Birds. Indiana University Press (Bloomington & Indianapolis), pp. 144-149.

Hillenius, W. J. & Ruben, J. A. 2004. Getting warmer, getting colder: reconstructing crocodylomorph physiology. Physiological and Biochemical Zoology 77, 1068-1072.

Jones, T. D., Farlow, J. O., Ruben, J. A., Henderson, D. M. & Hillenius, W. J. 2000. Cursoriality in bipedal archosaurs. Nature 406, 716-718.

Norell, M. A. & Makovicky, P. J. 1997. Important features of the dromaeosaur skeleton: information from a new specimen. American Museum Novitates 3215, 1-28.

PÃ©rez-Moreno, B. P. & Sanz, J. L. 1999. Theropod breathing mechanism: the osteological evidence. In Renesto, S. (ed) Third International Symposium on Lithographic Limestones (Bergamo, Italy). Revista del Museo Civico di Scienze Naturali 'Enrico Caffi' (Bergamo), Supplement to no. 20, pp. 121-122.

Quick, D. E. & Ruben, J. A. 2009. Cardio-pulmonary anatomy in theropod dinosaurs: implications from extant archosaurs. Journal of Morphology doi: 10.1002/jmor.10752

Ruben, J., Dal Sasso, C., Geist, N. R., Hillenius, W. J., Jones, T. D. & Signore, M. 1999. Pulmonary function and metabolic physiology of theropod dinosaurs. Science 283, 514-516.

- ., Hillenius, W., Geist, N. R., Leitch, A., Jones, T. D., Currie, P. J., Horner, J. R. & Espe, G. 1996. The metabolic status of some Late Cretaceous dinosaurs. Science 273, 1204-1207.

- ., Jones, T. D., Geist, N. R. & Hillenius, W. J. 1997. Lung structure and ventilation in theropod dinosaurs and early birds. Science 278, 1267-1270.

- ., Jones, T. D., Geist, N. R. & Hillenius, W. J. 1998. Ventilation and gas exchange in theropod dinosaurs. Science 281, 47-48.

Wedel, M. J. 2003. Vertebral pneumaticity, air sacs, and the physiology of sauropod dinosaurs. Paleobiology 29, 243-255.

- . 2007. Postcranial pneumaticity in dinosaurs and the origin of the avian lung. Ph.D. dissertation, University of California, Berkeley.

Xu, X., Wang, X.-L. & Wu, X.-C. 1999. A dromaeosaurid dinosaur with a filamentous integument from the Yixian Formation of China. Nature 401, 262-266.