I imagine that by now, everyone who reads this blog is familiar with Mark Witton’s painting of a giant azhdarchid pterosaur alongside a big giraffe. Here it is, for those who haven’t seen it:

Arambourgiania vs giraffe vs the Disacknowledgement redux Witton ver 2 low res

(This is the fifth and most recent version that Mark has created, taken from 9 things you may not know about giant azhdarchid pterosaurs.)

It’s one of those images that really kicks you in the brain the first time you see it. The idea that an animal the size of a giraffe could fly under its own power seems ludicrous — yet that’s what the evidence tells us.

But wait — what do we mean by “an animal the size of a giraffe”? Yes, the pterosaur in this image is the same height as the giraffe, but how does its weight compare?

Mark says “The giraffe is a big bull Masai individual, standing a healthy 5.6 m tall, close to the maximum known Masai giraffe height.” He doesn’t give a mass, but Wikipedia, citing Owen-Smith (1988), says “Fully grown giraffes stand 5–6 m (16–20 ft) tall, with males taller than females. The average weight is 1,192 kg (2,628 lb) for an adult male and 828 kg (1,825 lb) for an adult female with maximum weights of 1,930 kg (4,250 lb) and 1,180 kg (2,600 lb) having been recorded for males and females, respectively.” So it seems reasonable to use a mass intermediate between those of an average and maximum-sized male, (1192+1930)/2 = 1561 kg.

So much for the giraffe. What does the azhdarchid weigh? The literature is studded with figures that vary wildly, from the 544 kg that Henderson (2010) found for Quetzalcoatlus, right down to the widely cited 70 kg that Chatterjee and Templin (2004) found for the same individual — and even the astonishing 50 kg that seems to be favoured by Unwin (2005:192). In the middle is the 259 kg of Witton (2008).

It occurred to me that I could visualise these mass estimates by shrinking the giraffe in Mark’s image down to the various proposed masses, and seeing how credible it looks to imagine these reduced-sized giraffes weighting the same as the azhdarchid. The maths is simple. For each proposed azhdarchid mass, we figure out what it is as a proportion of the giraffe’s 1561 kg; then the cube root of that mass proportion gives us the linear proportion.

  • 544 kg = 0.389 giraffe masses = 0.704 giraffe lengths
  • 259 kg = 0.166 giraffe masses = 0.549 giraffe lengths
  • 70 kg =0.0448 giraffe masses = 0.355 giraffe lengths

Let’s see how that looks.

Arambourgiania vs giraffe vs the Disacknowledgement redux Witton ver 2 low res

On the left, we have Mark’s artwork, with the giraffe massing 1561 kg. On the right, we have three smaller (isometrically scaled) giraffes of masses corresponding to giant azhdarchid mass estimates in the literature. If Don Henderson (2010) is right, then the pterosaur weighs the same as the 544 kg giraffe, which to me looks pretty feasible if it’s very pneumatic. If Witton (2008) is right, then it weighs the same as the 259 kg giraffe, which I find hard to swallow. And if Chatterjee and Templin (2004) are right, then the giant pterosaur weighs the same as the teeny tiny 70 kg giraffe, which I find frankly ludicrous. (For that matter, 70 kg is in the same size-class as Georgia, the human scale-bar: the idea that she and the pterosaur weigh the same is just silly.)

What is the value of such eyeball comparisons? I’m not sure, beyond a basic reality check. Running this exercise has certainly made me sceptical about even the 250 kg mass range which now seems to be fairly widely accepted among pterosaur workers. Remember, if that mass is correct then the pterosaur and the 259 kg giraffe in the picture above weight the same. Can you buy that?

Or can we find extant analogues? Are there birds and mammals with the same mass that are in the same size relation as these images show?

References

  • Chatterjee, Sankar, and R. J. Templin. 2004. Posture, locomotion, and paleoecology of pterosaurs. Geological Society of America, Special Paper 376. 68 pages.
  • Henderson, Donald M. 2010. Pterosaur body mass estimates from three-dimensional mathematical slicing. Journal of Vertebrate Paleontology 30(3):768-785.
  • Witton, Mark P. 2008. A new approach to determining pterosaur body mass and its implications for pterosaur flight. Zitteliana 28:143-159.

Having given pterosaurs all the glory in two earlier posts, it’s time to move yet further away from the sauropods we know and love, and look at epipophyses outside of Ornithodira.

Here, for example, is the basal archosauriform Vancleavea. (Thanks to Mickey Mortimer, whose a comment on an earlier post put us onto this, and various other candidate epipohysis-bearers which we’ll see below.)

Here is a pair of Vancleavea cervical vertebrae:

Nesbitt et al. (2009: fig. 11A). Vertebrae of Vancleavea campi. Two articulated cervical vertebrae (PEFO 33978) in left lateral view.

Nesbitt et al. (2009: fig. 11A). Vertebrae of Vancleavea campi. Two articulated cervical vertebrae (PEFO 33978) in left lateral view.

No ambiguity here: the epipophysis is even labelled.

But we can find epipophyses even outside Archosauriformes. Here, for example, is the the rhynchosaur Mesosuchus:

Dilkes (1998: fig. 7A). Mesosuchus browni. Holotype SAM 5882. Partial skull and jaws and cervical vertebrae in left lateral view.

Dilkes (1998: fig. 7A). Mesosuchus browni. Holotype SAM 5882. Partial skull and jaws and cervical vertebrae in left lateral view.

Check out the rightmost vertebra (C7), clicking through for the full resolution if necessary. There is a definite eminence above the postzyg, separated from it by a distinct groove. Unless the drawing is wildly misleading, that is a definite epipophysis, right there.

But even more basal archosauromorphs have epipophyses. Check out Teraterpeton, described by Hans-Dieter Sues in 2003:

Sues (2003: figure 7). Teraterpeton hrynewichorum, NSM 999GF041 (holotype), cervical and anterior dorsal vertebrae and ribs, associated with right scapula (sc), ?clavicles (cl?), ?interclavicale (ic?), and incomplete right humerus (h), in right lateral view. Scale bar = 1 cm. a.p., accessory process above postzygapophysis; ax, axis; c3, c4, cervical vertebra 3 and 4, respectively; t, displaced tooth.

Sues (2003: figure 7). Teraterpeton hrynewichorum, NSM 999GF041 (holotype), cervical and anterior dorsal vertebrae and ribs, associated with right scapula (sc), ?clavicles (cl?), ?interclavicale (ic?), and incomplete right humerus (h), in right lateral view. Scale bar = 1 cm. a.p., accessory process above postzygapophysis; ax, axis; c3, c4, cervical vertebra 3 and 4, respectively; t, displaced tooth.

This is another one where the epipophysis is labelled (though not recognised as such — it’s just designated an “accessory process”).

Can we go yet more basal? Yes we can! Here are cervicals 2 and 3 of the trilophosaur Trilophosaurus (in an image that I rearranged and rescaled from the published original for clarity):

Spielmann et al. (2008: figure 30, rearranged). Cervical vertebrae 2-3 (i.e. axis and C3) of Trilophosaurus buettneri TMM 31025-140. Top row: right lateral. Second row: dorsal, with anterior to the left. Third row, left to right: anterior, left lateral, posterior. Bottom row: ventral, with anterior to the left.

Spielmann et al. (2008: figure 30, rearranged). Cervical vertebrae 2-3 (i.e. axis and C3) of Trilophosaurus buettneri TMM 31025-140. Top row: right lateral. Second row: dorsal, with anterior to the left. Third row, left to right: anterior, left lateral, posterior. Bottom row: ventral, with anterior to the left.

The parts of this image to focus on (and you can click through for a much better resolution) are the postzyg at top right of the left-lateral view, which has a distinct groove separating the zygapophyseal facet below from the epipohysis above; and the posterior view, which also shows clear separation on both sides between these two structures.

While we’re playing with trilophosaurs here’s here’s another one (probably), Spinosuchus:

Spielmann et al. (2009: figure 3N). Spinosuchus caseanus holotype UMMP 7507, 5th cervical vertebra in left lateral view.

Spielmann et al. (2009: figure 3N). Spinosuchus caseanus holotype UMMP 7507, 5th cervical vertebra in left lateral view.

Again, the groove separating postzygapophyseal facet from epipophysis (at top right in the image) is clear.

But there’s more! Even the protorosaurs, pretty much the most basal of all archosauromorphs, have convincing epipophyses. Here are two that I found in Dave Peters’ post from two years ago, which I only discovered recently. [Here I must insert the obligatory disclaimer: while Dave Peters is a fine artist and has put together a really useful website, his ideas about pterosaur origins are, to put it mildly, extremely heterodox, and nothing that he says about phylogeny on that site should be taken as gospel. See Darren’s write-up on Tet Zoo for more details.]

Dave shows some probable, but not super-convincing epipophyses in the protorosaur Macrocnemus (shaded purple here) …

Cervicals 1-6 of the protorosaur Macrocnemus, modified from an uncredited image on Dave Peters' site. Postzygapophyses in yellow, epipophyses in purple.

Cervicals 1-6 of the protorosaur Macrocnemus, modified from an uncredited image on Dave Peters’ site. Postzygapophyses in yellow, epipophyses in purple.

… and some much more convincing epipophyses in the better known and more spectacular protorosaur Tanystropheus:

Unspecified single cervical of Tanystropheus, from Dave Peters' site. Postzygapophysis in yellow, epipohysis in purple.

Unspecified single cervical of Tanystropheus, from Dave Peters’ site. Postzygapophysis in yellow, epipohysis in purple.

Frustratingly, Dave doesn’t attribute these images, so I don’t know where they’re originally from (unless they’re his own artwork). Can anyone enlighten me? There’s a nice illustration in figure 57 of Nosotti’s (2007) epic Tanystropheus monograph that is at least highly suggestive of epipophyses:

Nosotti (2007:figure 57). Reconstruction of an anterior cervical vertebra (A) and of a mid-cervical vertebra (B) in small-sized specimens of Tanystropheus longobardicus. Left lateral view. Not to scale. Watercolor: Massimo Demma. Abbreviation pzp = postzygapophyseal process.

Nosotti (2007:figure 57). Reconstruction of an anterior cervical vertebra (A) and of a mid-cervical vertebra (B) in small-sized specimens of Tanystropheus longobardicus. Left lateral view. Not to scale. Watercolor: Massimo Demma. Abbreviation pzp = postzygapophyseal process.

But it’s not as good as the one Peters used, as that one shows a distinct notch between postzyg and epipophysis, so I’d like to track that down if I can.

With this, I believe I am done on cataloguing and illustrating epipophyses, unless something dramatic turns up. (For example, this commenter thinks that nothosaurs have epipophyses, but I’ve not been able to verify that.) Here’s what we’ve found — noting that we’ve illustrated epipophyses on every taxon on this tree except Crocodylia:

tree

So it seems that epipophyses may well be primitive at least for Archosauromorpha — which implies that they were secondarily lost somewhere on the line to modern crocs.

With this lengthy multi-part digression complete, hopefully, we’ll get back to sauropods next time!

References

  • Dilkes, David W. 1998. The Early Triassic rhynchosaur Mesosuchus browni and the interrelationships of basal archosauromorph reptiles. Philosophical Transactions of the Royal Society of London B 353:501-541.
  • Kellner, Alexander W. A., and Yukimitsu Tomida. 2000. Description of a new species of Anhangueridae (Pterodactyloidea) with comments on the pterosaur fauna from the Santana Formation (Aptian-Albian), Northeastern Brazil. National Science Museum monographs, Tokyo, 17. 135 pages.
  • Nesbitt, Sterling J., Michelle R. Stocker, Bryan J. Small and Alex Downs. 2009. The osteology and relationships of Vancleavea campi (Reptilia: Archosauriformes). Zoological Journal of the Linnean Society 157:814-­864.
  • Nosotti, Stefania. 2007. Tanystropheus longobardicus (Reptilia, Protorosauria): re-interpretations of the anatomy based on new specimens from the Middle Triassic of Besano (Lombardy, Northern Italy). Memorie della Societa Italiana di Scienze Naturali e del Museo Civico di Storia Naturale di Milano 35(III). 88pp.
  • Spielmann, Justin A., Spencer G. Lucas, Larry F. Rinehart and Andrew B. Heckert. 2008. The Late Triassic Archosauromorph Trilophosaurus. New Mexico Museum of Natural History and Science Bulletin 43.
  • Justin A. Spielmann, Spencer G. Lucas, Andrew B. Heckert, Larry F. Rinehart and H. Robin Richards III. 2009. Redescription of Spinosuchus caseanus (Archosauromorpha: Trilophosauridae) from the Upper Triassic of North America. Palaeodiversity 2:283-313.
  • Sues, Hans-Dieter. 2003. An unusual new archosauromorph reptile from the Upper Triassic Wolfville Formation of Nova Scotia. Canadian Journal of Earth Science 40:635-649.

It’s well known that there is good fossil material of the giant azhdarchid pterosaur Quetzalcoatlus out there, but that for various complicated reasons it’s yet to be published. But as part of our ongoing quest for pterosaur epipophyses, I have obtained these photos of a pretty well preserved single cervical, probably C3, which is either Quetzalcoatlus or something pretty darned close.

TMP 1992.83.7, Quetzalcoatlus sp., cervical 3. Top, dorsal view; bottom, ventral view. Scale bar = 10 cm.

TMP 1992.83.7, Cf. Quetzalcoatlus, cervical 3. Top, dorsal view; bottom, ventral view. Anterior is to the left. Scale bar = 10 cm. Click through for high resolution.

My thanks go, in chronological order, to Rob Knell of QMC for taking the photos; to Don Brinkman for permission to share them publicly; and to Mike Habib (the USC one, not the Elsevier one) for passing them on to me. (The composition is my own work, which anyone is free to reuse so far as I’m concerned.)

Here’s what Mike Habib says about the specimen:

… well preserved TMP azhdarchid cervical vertebra. It is likely a CIII vert, and appears to be from an animal very similar to the small morph of Quetzalcoatlus in overall morphology. The associated humerus is just about an exact match. This cervical, however, does not quite match the proportions of any of the Q. sp. cervical verts, though that’s not a surprise given that the animals come from different horizons. There is a much larger, but poorly preserved cervical vert at the TMP as well (a Q. northropi sized animal, give or take).

Here are Mike’s measurements:

  • maximum length: 142.2 mm
  • minimum mediolateral breadth: 39.3 mm
  • minimum dorsoventral breadth: 27.4 mm
  • midshaft mediolateral breadth 40.0 mm
  • midshaft dorsoventral breadth 27.0 mm
  • mediolateral breadth across prezygapophyses: 65.6 mm
  • mediolateral breadth across postzygapophyses: 68.5 mm
  • dorsoventral breadth at postzygapophyses: 35.8 mm

(I mean those are the measurements that Mike provided for the vertebra, not the measurements of Mike himself. He’s much bigger than that.)

So does this specimen have epipophyses? Frustratingly, there don’t seem to be lateral or posterior-view photos, so it’s very hard to tell from these dorsal and ventral ones. Happily, the same specimen was illustrated and briefly described by Godfrey and Currie (2005:294-299), along with several other less well-preserved cervicals — so we do have drawings of these other views:

Godfrey and Currie (2005:figure 16.1). Azhdarchid cervical vertebra (TMP 92.83.7) in (A) dorsal, (B) left lateral, (C) ventral, (D) anterior, (E) posterior, and (F) posterodorsal views. Abbreviations: hyp, hypapophysis; nc, neural canal; pn, pneumatopore; prz, prezygapophysis.

Godfrey and Currie (2005:figure 16.1). Azhdarchid cervical vertebra (TMP 92.83.7) in (A) dorsal, (B) left lateral, (C) ventral, (D) anterior, (E) posterior, and (F) posterodorsal views. Abbreviations: hyp, hypapophysis; nc, neural canal; pn, pneumatopore; prz, prezygapophysis.

(The specimen number given here is slightly different from that given for the photos, but matches the label in the ventral-view photo. I assume that the leading “93” part of the specimen number is a year, and that it’s sometimes but not always given in four digits.)

The text of the description does not mention epipophyses, and skips very lightly over the whole postzygapophyseal area. But figures 16.1B (lateral) and 16.1E (posterior) both seem to show distinct bulbous eminences well above the postzygapophyseal facets. I think these have to be epipophyses. So Mark Witton’s caution not to write off azhdarchid epipophyses on the strength of their apparent absence in Phosphatodraco proves well-founded.

What is the moral here?

The more we look for epipophyses, the more we find them.

Which will be strangely familiar to anyone who remembers our experience with caudal pneumaticity in sauropods, which was: the more we looked for it, the more we found it.

If we have an SV-POW! motto (other than “sauropods are awesome”, of course), it’s “Measure your damned dinosaur!“. But if we had a third motto, it would be like unto it: look at your damned dinosaur. Or pterosaur, as the case may be. The odds are, you’ll see things you weren’t expecting.

Many thanks for the various people who chipped in, both in comments on the last post and in this thread on twitter, where I asked a bunch of pterosaur experts for their thoughts on epipophyses in pterosaurs. I now know more than I previously knew about epipophyses outside of Sauropoda — and especially outside Dinosauria. I’ll try to credit everyone who contributed.

Occasional SV-POW!sketeer Darren Naish claims that according to the literature, ornithischians lack epipophyses — something that we’ve seen is untrue. I never got references out of him, though. Can anyone point me to the guilty literature?

Darren also gave me the rather cryptic instruction “Look at Anhanguera monographs. Sorry, can’t check myself.” Like something from a spy novel. Checking out Kellner and Tomida (2000), I found their illustration of the Anhanguera atlas/axis complex, in figure 14B, suggestive:

KellnerTomida2000-fig14

It took me a while to figure this out, but I think this is showing the first three cervicals, not two: the atlas is tiny, and is smushed onto the front of the axis; C3 is shown, but only in outline, and is ignored in the caption.

As labelled, the postzygapophyseal facet of the axis is tiny — and there’s a definite protuberance above it, which can only be an epipophysis. But we’d need photos to be confident. The good news is that there is a photo in the paper — part A of the same figure. But the bad news is that here’s how it looks in my scan:

KellnerTomida2000-fig14a

Not so helpful. If anyone has a good scan — or better still an original photo — I’d like to see it.

Darren also commented “Most big pterosaurs lack epipophyses. Ornithocheirids may be the exception”, but there his hints dried up. Mark Witton cautioned me: “Not sure for azhdarchids. Well preserved verts have reduced features, but not entirely absent as badly preserved verts suggest.” So perhaps the Phosphatodrado vertebrae in the last post are not so compelling as they seem.

Liz Martin suggested “off the top of my head you could check Wellnhofer papers. 1991 and 1985 I think show verts.” But I couldn’t find any vertebrae in the only Wellnhofer (1985) that I have; and there are at least three Wellnhofer publications from 1991, which I’ve not checked yet. Any more guidance, anyone?

So how widespread are epipohyses? Brusatte et al. (2010:73) gave “Epipophyses on the cervical vertebrae” as a synapomorphy diagnosing Dinosauria:

2.4.1.4. Epipophyses on the cervical vertebrae. Epipophyses are projections of bone, likely for muscle and ligament attachment, which protrude from the dorsal surfaces of the postzygapophyses of the cervical vertebrae. All basal dinosaurs possess epipophyses (Langer and Benton, 2006), although the size, shape, length, and projection angle of these processes vary considerably (e.g., compare Coelophysis (Colbert, 1989) with the more derived theropod Majungasaurus (O’Connor, 2007)). Basal ornithischians (e.g., Heterodontosaurus) only have epipophyses on the anterior cervical vertebrae, whereas saurischians have epipophyses in nearly all cervical vertebrae (Langer and Benton, 2006). Epipophyses are not present in the closest relatives of dinosaurs (e.g., Marasuchus, Silesaurus), but are present in some crurotarsans (e.g., Lotosaurus and Revueltosaurus).

It’s surprising that they’d mention dinosaurs and croc-line archosaurs, but overlook pterosaurs, which are phylogenetically bracketed by that group. But there’s lots of useful detail to follow up in the citations, which I’ll be doing soon.

So: moving down the tree from Sauropoda, we see epipophyses:

  • often but not always in sauropods
  • rarely in basal sauropodomorphs
  • often, maybe always, in theropods
  • intermittently but not infrequently in ornithischians
  • in at least some basal dinosauriforms
  • in some groups of pterosaurs but not others
  • in at least some croc-line archosaurs — but not, for example, in alligators.

Does anyone know of epipophyses outside Archosauria?

We seem now to be stumbling towards a conclusion of sorts, which is that epipophyses seem to be rather phylogenetically labile, coming and going within numerous lineages. As with so many vertebral features, they also vary with serial position, which complicates matters; and, I dare guess, with ontogeny.

I’ve not been able to locate any publications that are specifically about epipophyses (just lots that mention them in passing). Does anyone know of such a thing?

References

Matt’s last post contained a nice overview of the occurrence of epipophyses in sauropodomorphs: that is, bony insertion points for epaxial ligaments and muscles above the postzygapophyseal facets. What we’ve not mentioned so far is that these structures are not limited to sauropods. Back when we were preparing one of the earlier drafts of the paper that eventually became Why sauropods had long necks; and why giraffes have short necks (Taylor and Wedel 2013a), I explored their occurrence in related groups. But that section never got written up for the manuscript, and now seems as good a time as any to fix that.

Theropods (including birds)

Most obviously, epipophyses occur in theropods, the sister group of sauropodomorphs.

Taylor and Wedel (2013a: figure 11). Archosaur cervical vertebrae in posterior view, Showing muscle attachment points in phylogenetic context. Blue arrows indicate epaxial muscles attaching to neural spines, red arrows indicate epaxial muscles attaching to epipophyses, and green arrows indicate hypaxial muscles attaching to cervical ribs. While hypaxial musculature anchors consistently on the cervical ribs, the principle epaxial muscle migrate from the neural spine in crocodilians to the epipophyses in non-avial theropods and modern birds, with either or both sets of muscles being significant in sauropods. 1, fifth cervical vertebra of Alligator mississippiensis, MCZ 81457, traced from 3D scans by Leon Claessens, courtesy of MCZ. Epipophyses are absent. 2, eighth cervical vertebra of Giraffatitan brancai paralectotype HMN SII, traced from Janensch (1950, figures 43 and 46). 3, eleventh cervical vertebra of Camarasaurus supremus, reconstruction within AMNH 5761/X, “cervical series I”, modified from Osborn and Mook (1921, plate LXVII). 4, fifth cervical vertebra of the abelisaurid theropod Majungasaurus crenatissimus,UA 8678, traced from O’Connor (2007, figures 8 and 20). 5, seventh cervical vertebra of a turkey, Meleagris gallopavo, traced from photographs by MPT.

Taylor and Wedel (2013a: figure 11). Archosaur cervical vertebrae in posterior view, Showing muscle attachment points in phylogenetic context. Blue arrows indicate epaxial muscles attaching to neural spines, red arrows indicate epaxial muscles attaching to epipophyses, and green arrows indicate hypaxial muscles attaching to cervical ribs. While hypaxial musculature anchors consistently on the cervical ribs, the principle epaxial muscle migrate from the neural spine in crocodilians to the epipophyses in non-avial theropods and modern birds, with either or both sets of muscles being significant in sauropods. 1, fifth cervical vertebra of Alligator mississippiensis, MCZ 81457, traced from 3D scans by Leon Claessens, courtesy of MCZ. Epipophyses are absent. 2, eighth cervical vertebra of Giraffatitan brancai paralectotype HMN SII, traced from Janensch (1950, figures 43 and 46). 3, eleventh cervical vertebra of Camarasaurus supremus, reconstruction within AMNH 5761/X, “cervical series I”, modified from Osborn and Mook (1921, plate LXVII). 4, fifth cervical vertebra of the abelisaurid theropod Majungasaurus crenatissimus,UA 8678, traced from O’Connor (2007, figures 8 and 20). 5, seventh cervical vertebra of a turkey, Meleagris gallopavo, traced from photographs by MPT.

In this figure from the 2013 paper, the rightmost images show cervical vertebrae of Majungasaurus (an abelisaurid theropod) and a turkey, both in posterior view. The red arrows indicate epaxial musculature pulling on the epipophyses. They are particularly prominent in Majungasaurus, rising almost a full centrum’s height above the postzygapophyseal facets.

The epipophyses are very prominent in the anterior cervicals of Tyrannosaurus, but much less so in its posterior cervicals — presumably because its flesh-tearing moves involved pulling upwards more strongly on the anterior part of the neck. Here’s a photo of the AMNH mount, from our post T. rex‘s neck is pathetic:

amnh-tyrannosaurus-is-pathetic

You can see something similar in the neck of Allosaurus, and the trend generally seems to be widespread among theropods.

Ornithischians

Note the very prominent epipophyses protruding above the postzygs in the anterior cervicals of this Heterodontosaurus in the AMNH public gallery:

Cast of AMNH 28471, Heterodontosaurus tucki, collected from the Early Jurassic Voisana, Herschel district, South Africa. Anterior to the left.

Cast of AMNH 28471, Heterodontosaurus tucki, collected from the Early Jurassic Voisana, Herschel district, South Africa. Neck in left lateral view.

Here’s the hadrosaur Corythosaurus:

AMNH 5338, Corythosaurus casuarius, from the Campanian of the Red Deer River, Alberta, Canada. Collected by Barnum Brown and P. C. Kaisen, 1914. Cervicals 1-4 in right lateral view.

AMNH 5338, Corythosaurus casuarius, from the Campanian of the Red Deer River, Alberta, Canada. Collected by Barnum Brown and P. C. Kaisen, 1914. Cervicals 1-4 in right lateral view.

The prominent vertebra is C2: note that is has both a modest blade-like neural spine and prominent epipophyses — but that already by C3 the epipophyses are gone. Here is that C2 postzyg/epipophyses complex is close-up, clearly showing anteroposteriorly directed striations on the epipophysis, presumably representing the orientation of the attaching ligaments and muscles:

As previous image: close-up of posterior part of C2.

As previous image: close-up of posterior part of C2.

Here’s a close-up of the neck of the boring ornithopod Tenontosaurus, also in the AMNH gallery. (I’m not sure of the specimen number — if anyone can clarify, please leave a comment).

AMNH ?3554, Tenontosaurus tilletti, cervcials 2-4 in right lateral view.

AMNH ?3554, Tenontosaurus tilletti, cervicals 2-4 in right lateral view.

The interesting thing here is that it its axis (C2) seems to lack epipophyses (unlike C3), and to have a tall blade-like neural spine, as seen in mammals. We don’t really see C2 spines this big in other dinosaurs — compare with the much more modest spine in Corythosaurus, above. The texture of this part of the Tenontosaurus specimen looks suspicious, and I wonder whether that neural spine is a fabrication, created back in the day by AMNH staff who were so used to mammals that they “knew” what a C2 should look like? Anyway, the epipophysis above the postzyg of C3 is very distinct and definitely real bone.

Pterosaurs

Things get much more difficult with pterosaurs, because their cervicals are so fragile and easily crushed (like the rest of their skeleton, to be fair). While it’s easy to find nice, well-preserved ornithischian necks on display, you don’t ever really see anything similar for pterosaurs.

As a result, we have to rely on specimen photographs from collections, or more often on interpretive drawings. Even high-resolution photos, such as the one in Frey and Tischlinger (2012: fig 2) tend not to show the kind of detail we need. Usually, the only usable information comes from drawings made by people who have worked on the specimens.

Here, for example, is Rhamphorhynchus, well known as the most difficult pterosaur to spell, in figure 7 from Bonde and Christiansen’s (2003) paper on its axial pneumaticity:

BondeChristiansen2003-axial-pneumaticity-of-rhamphorhynchus-fig7It’s not the main point of the illustration, but you can make out clear epipophyses extending posteriorly past the postzygapophyseal facets in at least C3 and C5 — in C4, the relevant area is obscured by a rib. (Note that the vertebrae are upside down in this illustration, so you need to be looking towards the bottom of the picture.)

I’m pretty sure I’ve seen a better illustration of Rhamphorhynchus epipophyses, but as I get older my memory for Rhamphorhynchus epipophyses is no longer what it used to be and I can’t remember where. Can anyone help?

But also of interest is the azhdarchid pterosaur Phosphatodraco, here illustrated by Pereda Suberbiola et al. (2003):

Pereda Suberbiola et al. (2003: fig. 3). Phosphatodraco mauritanicus gen. et sp. nov, OCP DEK/GE 111, Late Cretaceous (Maastrichtian), Morocco: (a) cervical five in two fragments, ventral and left lateral views; (b) cervical six in ventrolateral view; (c) cervical seven in ventral view; (d) cervical eight in left lateral view; (e) cervical nine in posterior view; (f) cervical six in anterior view. c, centrum; co, condyle; ct, cotyle; hyp, hypapophysis; nc, neural canal; ns, neural spine; poe, postexapophysis; poz, postzygapophysis; prz, prezygapophysis; su, sulcus; tp, transverse process.

Pereda Suberbiola et al. (2003: fig. 3). Phosphatodraco mauritanicus gen. et sp. nov, OCP DEK/GE 111, Late Cretaceous (Maastrichtian), Morocco: (a) cervical five in two fragments, ventral and left lateral views; (b) cervical six in ventrolateral view; (c) cervical seven in ventral view; (d) cervical eight in left lateral view; (e) cervical nine in posterior view; (f) cervical six in anterior view. c, centrum; co, condyle; ct, cotyle; hyp, hypapophysis; nc, neural canal; ns, neural spine; poe, postexapophysis; poz, postzygapophysis; prz, prezygapophysis; su, sulcus; tp, transverse process.

The cervicals of Phosphatodraco seem to have no epipophyses. So they were not ubiquitous in pterosaurs.

What does it all mean? This post has become a bit of a monster already so I’ll save the conclusion for another time. Stay tuned for more hot epipophyseal action!

References

  • Bonde, Niels and Per Christiansen. 2003. The detailed anatomy of Rhamphorhynchus: axial pneumaticity and its implications. pp 217-232 in: E. Buffetaut and J-M Mazin (eds), Evolution and Palaeobiology of Pterosaurs. Geological Society, London, Special Publications 217. doi:10.1144/GSL.SP.2003.217.01.13
  • Frey Eberhard and Helmut Tischlinger. 2012. The Late Jurassic Pterosaur Rhamphorhynchus, a Frequent Victim of the Ganoid Fish Aspidorhynchus? PLoS ONE 7(3):e31945. doi:10.1371/journal.pone.0031945
  • Janensch, Werner. 1950. Die Wirbelsaule von Brachiosaurus brancai. Palaeontographica, Supplement 7 3:27-93.
  • O’Connor Patrick M. 2007. The postcranial axial skeleton of Majungasaurus crenatissimus (Theropoda: Abelisauridae) from the Late Cretaceous of Madagascar. pp 127-162 in: S. D. Sampson., D. W. Krause (eds), Majungasaurus crenatissimus (Theropoda: Abelisauridae) from the Late Cretaceous of Madagascar. Society of Vertebrate Paleontology Memoir 8.
  • Osborn, Henry F., and Charles C. Mook. 1921. Camarasaurus, Amphicoelias and other sauropods of Cope. Memoirs of the American Museum of Natural History, New Series 3:247-387.
  • Pereda Suberbiola, Xabier, Nathalie Bardet, Stéphane Jouve, Mohamed Iarochène, Baadi Bouya and Mbarek Amaghzaz. 2003. A new azhdarchid pterosaur from the Late Cretaceous phosphates of Morocco. pp 79-90 in: E. Buffetaut and J-M Mazin (eds), Evolution and Palaeobiology of Pterosaurs. Geological Society, London, Special Publications 217. doi:10.1144/GSL.SP.2003.217.01.08
  • Taylor, Michael P., and Mathew J. Wedel. 2013. Why sauropods had long necks; and why giraffes have short necks. PeerJ 1:e36 doi:10.7717/peerj.36

This came out two months ago, and I should have blogged about it then, but as usual I am behind. I’m blogging about it now because it deals with a question that has been on my mind for about 10 years now. If you want to skip my blatherations and get on to the good stuff, here’s the paper (Martin and Palmer 2014).

An Unsolved Problem

Back in 2004 I realized that if one had CTs or other cross-sections of a pneumatic bone, it was possible to quantify how much of the cross-sectional space was bone, and how much was air, a ratio I called the Air Space Proportion (ASP). That was the subject of my 2004 SVP talk, and a big part–arguably the most important part–of my chapter in The Sauropods in 2005. Of course the same calculation works for marrow-filled bones as well, where you would refer to it as an MSP rather than an ASP. If you can quantify the areas of bone, air, and marrow, you can figure out how dense the element was. One-stop shopping for all the relevant (simple) math is in this post.

(From Wedel 2005)

(From Wedel 2005)

Sometimes in science you end up with data that you don’t know what to do with, and that was my situation in 2004. Since I had CTs and other cross-sectional images of sauropod vertebrae, I could calculate ASPs for them, but I didn’t know what those results meant, because I didn’t have anything to compare them to. But I knew where to get I could get comparative data: from limb bone cross-sections. John Currey and R. McNeill Alexander had published a paper in 1985 titled, “The thickness of the walls of tubular bones”. I knew about that paper because I’d become something of an R. McNeill Alexander junkie after reading his book, Dynamics of Dinosaurs and Other Extinct Giants (Alexander 1989). And I knew that it had data on the cross-sectional properties of the limb bones in a host of animals, including crocs, birds, mammals, and–prophetically–pterosaurs.

If you know the inner and outer radii of a tubular bone, it is trivial to convert that to an ASP. So I could take the data from Currey and Alexander (1985) and calculate ASPs for the pneumatic bird and pterosaur bones in their study. Cubo and Casinos (2000) had a much larger sample of bird limb bones, and those got fed into my 2005 paper as well.

I was alert to the possibility that a mid-shaft cross-section might not be representative of the whole bone, and I hedged a bit in describing the bird ASPs (Wedel 2005: p. 212):

For the avian long bones described above, data were only presented for a single cross sec- tion located at midshaft. Therefore, the ASP values I am about to discuss may not be representative of the entire bones, but they probably approximate the volumes (total and air) of the diaphyses. For tubular bones, ASP may be determined by squaring K (if r is the inner diameter and R the outer, then K is r/R, ASP is πr^2/πR^2 or simply r^2/R^2, and ASP = K^2). For the K of pneumatic bones, Currey and Alexander (1985) report lower and upper bounds of 0.69 and 0.86, and I calculate a mean of 0.80 from the data presented in their table 1. Using a larger sample size, Cubo and Casinos (2000) found a slightly lower mean K of 0.77. The equivalent values of ASP are 0.48 and 0.74, with a mean of 0.64, or 0.59 for the mean of Cubo and Casinos (2000). This means that, on average, the diaphysis of a pneumatic avian long bone is 59%–64% air, by volume.

Now, even though I hedged and talked about diaphyses (shafts of long bones) rather than whole bones, I honestly expected that the ASP of any given slice would not change much along the length of a bone. Long bones tend to be tubular near the middle, with a thick bony cortex surrounding the marrow or air space, and honeycombed near the ends, with much thinner cortices and lots of bony septa or trabeculae (for marrow-filled bones, this is called spongy or trabecular bone, and for air-filled bones it is best referred to as camellate pneumatic bone). I figured that the decrease in cortical bone thickness near the ends of the bone would be offset by the increase in internal bony septa, and that the bone-to-air ratio through the whole element would be under some kind of holistic control that would keep it about even between the middle of the bone and the ends.

It is fair to ask why I didn’t just go check. The answer is that research is to some extent a zero-sum game, in that every project you take on means another that gets left waiting in the wings or abandoned completely. I was mainly interested in what ASP had to say about sauropods, not birds, and I had other fish to fry.

So that’s me from 2004-2012: aware that mid-shaft cross-sections of bird and pterosaur long bones might not be representative of whole elements, but not sufficiently motivated to go check. Then at SVPCA in Oxford that fall, Liz Martin rocked my world.

journal.pone.0097159.g001

Figure 1. CT scan images from two different regions of pterosaur first wing phalanx. A and B show the unmodified CT scans from A) the distal end of UP WP1 and B) the mid-shaft of UP WP1, while C and D show the modified and corrected images used in the calculation. Air space proportion (ASP) is calculated by determining the cross-sectional area of the internal, air filled cavity (the black centre of D) and dividing that by the total cross-sectional area, including the white cortical tissue and the black cavity. In areas with trabeculae, like C, the calculation of the air space includes the air found in individual trabeculae around the edges. Scale = 10 mm. doi:10.1371/journal.pone.0097159.g001 (From Martin and Palmer 2014)

A Paper in the Can

At SVPCA 2012, Liz Martin gave a talk titled, “A novel approach to estimating pterosaur bone mass using CT scans”, the result of her MS research with Colin Palmer at the University of Bristol. In that talk–the paper for which has been submitted to JVP–Liz and Colin were interested in using CT scans of pterosaur bones to quantify the volume of bone, in order to refine pterosaur mass estimates. I was fully on board, since estimating the masses of extinct animals is a minor obsession of mine. But what really caught my attention is that Liz and Colin had full stacks of slices spanning the length of each element–and therefore everything they needed to see how or if ASPs of pterosaur wing bones changed along their lengths.

At the next available break I dashed up to Liz, opened up my notebook, and started scribbling and gesticulating and in general carrying on like a crazy person. It’s a wonder she didn’t flee in terror. The substance of my raving was that (1) there was this outstanding problem in the nascent field of ASP research, and (2) she had everything she needed to address it, all that was required was a little math using the data she already had (I say this as if running the analyses and writing the paper were trivial tasks–they weren’t). Fortunately Liz and Colin were sufficiently interested to pursue it. Their paper on ASPs of pterosaur wing bones was submitted to PLOS ONE this February, and published on May 9 (while their earlier paper continues to grind its way through JVP).

And I’m blogging about it because the results were not what I expected.

Pterosaur wing bone ASPs - Martin and Palmer 2014

Figure 2. Plot of air space proportion over the length in six pterosaur wing bones. These plots show a polynomial line fit for each bone to show the general shape distribution. Exact measurements can be seen in Table S1. (From Martin and Palmer 2014).

Here’s the graph that tells the tale. Each line traces the ASP per slice along the length of a single pterosaur wing bone. A few things jump out:

  • Almost all of the lines drop near the left end. This is expected–if you’re cutting slices of a bone and measuring the not-bone space inside, then as you approach the end of the bone, you’re cutting through progressively more bone and less space. A few of the lines also drop near the right. I’m puzzled by that–if my explanation is correct, the ASP should plunge about equally at both ends. And the humerus USNM 11925 doesn’t follow the same pattern as the rest. As Martin and Palmer write, “It is unknown if this is a general feature of humeri, or this single taxon and more investigation is needed.”
  • Almost all of the bones have MUCH lower ASPs at mid-shaft than near the ends, on the order of 10% or more. So mid-shaft cross-sections of pterosaur wing bones tend to significantly underestimate how pneumatic they were. It would be interesting to know if the same holds true for bird long bones, or for the vertebrae of pterosaurs, birds, and sauropods. As Martin and Palmer point out, more work is needed.
  • The variation in ASP along the length of a single bone is in some cases greater than the variation between elements and individuals. That’s pretty cool. On the happy side, it means that getting into the nitty-gritty of ASP is not just stamp-collecting; you really need to know what is going on along the length of a bone before you can say anything intelligent about ASP or the density of the element. On the less happy side, that’s going to be a righteous pain in the butt for sauropod workers, because vertebrae are tough to get good scans of, assuming they will fit through a CT scanner at all (most don’t).
  • Finally, pterosaurs turn out to be even more pneumatic than you would think from looking at the already-freakishly-thin-walled shafts of their long bones. That’s pretty awesome, and it dovetails nicely with the emerging picture that pneumaticity in ornithodirans was more prevalent and more interesting than even I had suspected–it’s in prosauropods (Yates et al. 2012) and brachiosaur tails (Wedel and Taylor 2013) and rebbachisaur hips (Fanti et al. 2013) and saltasaur shoulders (Cerda et al. 2012) and, er, a couple of places that I can’t mention just yet. So life is good.

A few last odds and ends:

You can read more of this story at Liz Martin’s blog, scattered over several recent posts.

If you have CTs of bones and you want to follow in the footsteps of Martin and Palmer, you can do a lot of the work, and maybe all of it, in BoneJ, a free plug-in for ImageJ, which is also free.

A final note: this is Liz Martin’s first published paper, so congratulations are in order. Well done, Liz!

Almost Immediate Update: As soon as I posted this, I sent the link to Liz to see if I’d missed anything important. She writes, “It may be worth mentioning that it’s a question that I am actively following up on in my PhD, and looking into it with birds too hopefully. And it is indeed all possible using ImageJ, as that’s how I did the whole thing!”

References