Know When To Fold 'Em

Above: Maximum wrist folding for the theropods studied by Sullivan et al. 2010. Not to scale.

(Cross-posted from Art Evolved)

To continue talking about aspects of maniraptoran anatomy that can be a bit vaguely defined in the minds of paleoartists, I'm going to write a bit on the issue of wrist folding. As most of you will know, a major characteristic of maniraptorans is the semi-lunate carpal, the half-moon shaped bone in the wrist that allows the blade of the hand (metacarpal 3) to fold backward toward the forearm (ulna). While this is common knowledge among paleo buffs and artists, what seems to be less understood is exactly how tightly the hand (and in aviremigians, the wing) could actually fold up. I myself have never been too clear on the issue, and there don't seem to be many papers addressing this. But in the last few years, a few papers have come along that can help shed light on the subject. The first was Senter 2006, which studied the full range of motion in the forelimbs of two dromaeosaurs, Deinonychus and Bambiraptor. The second was Sullivan et al. 2010, which examined the range of motion in the wrist of several species representing each major group of non-avialan maniraptorans.

Both papers, however, present geometric data that can come across as a bit inaccessible for your average artist, so I'm going to try to break down their conclusions for those of us who are more visual thinkers. The Sullivan paper, in particular, discusses the degree to which the wrist could fold, but doesn't necessarily provide diagrams or even final angle between the metacarpals and ulna for each species that could be used as a simple reference. I've done my best to translate their findings into the image at the top of this post, using modified skeletal diagrams by Scott Hartman and Jaime Headden.

Above: Anatomy of a maximally folded wing of the Wild Turkey Meleagris gallopavo, modified from Sullivan et al. 2010

The degree of wrist folding is controlled by two wrist bones. The cuneiform, on the inside where the wrist meets the bottom of the distal ulna, provides an inner limit. The cuneiform blocks the hand from actually touching the ulna. The radiale, on the outside of the fold, forms the surface which the wrist cannot fold beyond. This is basically a little process anchored to the tip of the radius where the top part of the hand articulates. The hand can obviously not fold beyond the angle of the radiale, or the animal would dislocate its wrist. Therefore, the angle the articular surface of the radiale forms with the ulna is used as the key factor in determining maximum wrist folding by Sullivan et al. Again, see my interpretation at the top for how their results likely translate into life position.

The results show that in almost all maniraptorans, the wrist could not be folded to the same degree as modern birds (for comparison, see the photo of the turkey wing above, which is at its own maximum folding point). Note that in actual, functional angle of folding in the turkey is 57 degrees between MCII (where the feathers attach) and the ulna. To see how this translates into a live animal, here's a photo of wild turkeys nicely showing the way the feathers fold (photo by D. Gordon E. Robertson, from Wikipedia, licensed):

The wrist is located about where the coverts form the point of a triangle, following the line formed by the border of the the brown secondary (ulna) feathers and white banded primary (metacarpus) feathers. Note that with the wrist folded at a 57 degree interior angle, the feathers (especially the secondaries, which help cover the primaries when folded) are basically stacked one on top of the other with little to no fanning out at the tips. This is because the feathers also have some ability to move at their bases, and can themselves fold relative to their anchor bones through muscle and ligament action.

Looking at the aviremigians in the diagram up top, it is apparent that their wrists could not fold tightly enough to fold the wing feathers to the same degree as a modern turkey. Small deinonychosaurs like Sinovenator and Bambiraptor could achieve close to a 100 degree angle (see image of Bambiraptor wing folding above, from Senter 2006), but larger ones like Deinonychus seem to have lost some of that folding ability, presumably for increased use of the forelimbs in predation. Indeed, if Deinonychus retained long remiges, they would hardly have been able to fold at all, and would have been permanently fanned out (not that this would have gotten in the way of grabbing prey, as Senter pointed out). This lack of ability to tightly fold the wrists may have posed a significant problem for those species with very long remiges, like Microraptor gui. Dave Hone, who was a co-author of the Sullivan paper, discussed alternative ways they could have kept their remiges free of the ground at his blog last year.

In pygostylians, the degree of wrist folding began to approach that found in modern birds. Eoconfuciusornis, for example, could fold its wing to about the same degree as a turkey. Where it gets weird is in the oviraptorosaurs. As I mentioned in my post on the Ashdown maniraptoran, oviraptorosaurs (at least the small basal ones like Caudipteryx) seem to have been capable of folding their wings far beyond what is possible for even many modern birds. It's unclear why this is so, especially as the remiges of Caudipteryx, while clearly for display, are not exactly very long compared to the body. Certainly its wings were much smaller than those of paravians, which would have presumably had more need to fold them up. I've seen this mentioned as possible evidence in support of the hypothesis that oviraptorosaurs are in fact avialans, and that the extreme folding of the wrist was inherited from flying ancestors, though I can't think of where. Sullivan et al. do note that more than folding up the remiges to keep them safe from wear and tear, wing folding is an important part of the avian flight stroke, and it makes sense that it would have become more developed in flying forms.

Anyway, we've only got a handful of specimens that have been specifically studied in regards to the degree of wrist folding, and there may well be exceptions in each maniraptoran group, where certain lineages independently evolved a greater or lesser degree of wrist folding from their ancestors as seems to have happened in therizinosaurs, where the derived Alxasaurus can fold its wrist more than the basal Falcarius, and deinonychosaurs, where the relatively derived Deinonychus can fold its wrist less than the more basal Bambiraptor. So this guide shouldn't be considered as a set of hard and fast rules, but rather a starting point for artists who want to make their restorations as plausible as possible.

Finally, a few days ago I posted a teaser for this post challenging people to determine what aspect of the above Deinonychus illustration was incorrect. By now it should be clear that the wrist is folded too far back. Appropriately enough, the first one to nail it was the artist, Nobu Tamura, himself! Commenter A.G. came close, speculating that it was due to the orientation of the glenoid, but that has more to do with the range of motion of the upper arm and how far it could extend into a bird-like flapping position, rather than the way the wing folds up. Good job guys!

References

* Senter, P. (2006). "Comparison of Forelimb Function Between Deinonychus And Bambiraptor (Theropoda: Dromaeosauridae)". Journal of Vertebrate Paleontology, 26(4): 897–906.
* Sullivan, C., Hone, D.W.E., Xu, X. and Zhang, F. (2010). "The asymmetry of the carpal joint and the evolution of wing folding in maniraptoran theropod dinosaurs." Proceedings of the Royal Society B, 277(1690): 2027–2033.

The Ashdown Maniraptoran

As you may have heard by now, Darren Naish and Steve Sweetman have described an incredibly small, yet apparently adult, cervical vertebra of a maniraptoran dinosaur from the Wadhurst Clay Formation. My first reaction upon seeing pictures of this nice little water-polished bone was "that is effing adorable," followed by "I need to restore this despite the fact that we can have no clue what it looked like." So I did, and the result is shown above (and on my deviantArt page). Let me emphasize again: this is a *highly speculative* restoration of the so-called Ashdown maniraptoran. Darren did a great job of discussing the new paper at TetZoo, so I won't go into details here.

While it is entirely speculative, based as it is on a single bone, it is possible to make some educated guesses about life appearance. Naish and Sweetman note several characteristics of the vertebra that are similar to oviraptorosaurs. However, it is from the early Valenginian age, about 140 million years ago. This is nearly 20 million years earlier than the oldest known definitive oviraptorosaurs, Caudipteryx and Protarchaeopterx. So, I essentially restored this as a very small protarchaeopterygid-grade animal, hence the short tail and tightly-folding wing feathers (oviraptorids could fold their wings more tightly than even many early birds).

There is also some influence from scansoripterygids, given its small size (and as a slight nod to GSP's interpretation of Epidexipteryx hui as a basal oviraptorosaur). Naish and Sweetman point out that the large neural canal of the vertebra is a characteristic of Avialae, but that it may also be a more general size-related character. The scansor influence is found mainly in the shape of the skull and the large procumbant teeth, but those these are the characteristics which are shared by early oviraptorosaurs anyway, and so allow extra wiggle room should it turn out to be closer to avialans. I made the legs quite long compared to the ratio seen in its larger possible relatives, and made the foot fairly large (to better emphasize the diminutive size). The longer legs would, I reckon, help escape hungry mammals, lizards, and whatever else was preying on tiny maniraptors.

Finally, the coloration is fairly drab and cryptic (inspired by small modern birds that spend time hiding in undergrowth) and I chose yellow hues to indicate a bit of an omnivorous diet.

So, while it's impossible to accurately depict an animal based on a single bone which we have trouble even assigning to any specific clade, using some knowledge of basal maniraptoran lineages (it is almost certainly a fairly basal member of whichever clade it belongs to, given its early age), we can make some pretty reasonable (I hope!) guesses.

References:
* Naish, D., and Sweetman, S.C. (2011). "A tiny maniraptoran dinosaur in the Lower Cretaceous Hastings Group: evidence from a new vertebrate-bearing locality in south-east England." Cretaceous Research, 32: 464-471.

Giants & Other Early Reptiles Online

When your average modern dino fan hears the name "David Peters", they probably think of lepidosaurian pterosaurs, archosaurian mammals, invisible babies and the most extreme examples of paleontological pareidolia since Chonosuke Okamura. But to the surprise of some commenters , Peters was, for a while, a somewhat prolific and outstanding paleoartist. I have long credited his two early 'gallery' style books with being one of my main early influences. These books more than anything except maybe Phil Tippet's Prehistoric Beast fostered my interest in paleontology as a kid and kept it going, giving me ample figures to copy... I mean... giving me plenty of references to use in my first attempts at palaeontography. Looking back through them I reckon those influences are still very much with me. Each page even functions as a scale chart, which must not have made too much of an impression on my developing mind.

For those also looking to be inspired by some 'old school' but still fairly accurate (especially in Gallery which features a Deinonychus so bird-like it blew my 12 year old mind) or at least interesting renditions of prehistoric animals, I recently discovered both of these gallery-style books are available as free PDFs from Peters' art site (often overlooked in favor of his more, um, eccentric science and phylogeny site).

Tyrannosaur Tooth Count

Making the rounds right now in the media is a story about a newly described, well-preserved baby Tarbosaurus bataar that helps shed some light on the way tyrannosaurs grow, as well as touches on lingering controversies. Plenty of other blogs have already covered this, so here's a link to the backstory from Brian Switek at Dinosaur Tracking.

Interestingly, the baby Tarb has 15 teeth in the lower jaw, the same number as adult T. bataar. There has been controversy over whether or not tyrannosaurs reduced their number of teeth as they grew, particularly when it comes to the controversial taxon Nanotyrannus lancensis. Nano is known from two specimens (one is nicknamed "Jane") that, depending who you talk to, might really be simply juvenile specimens of the contemporary Tyrannosaurus rex. The differences cited to separate the two boil down to differences in the braincase (certain braincase changes were demonstrated in the new juvenile Tarbosaurus as well), and the number of teeth. Adult T. rex are usually said to have only about 12 teeth in the dentary, while specimens of N. lancensis have a whopping 17. The new juvenile Tarb suggests that in at least some tyrannosaurs, the tooth count is not drastically reduced during growth from juvenile to adult. However, as the authors caution, this same pattern may not necessarily hold true for other tyrannosaurs, even very close relatives.

And, the same pattern does not hold true for the very closely related T. rex. Also making the blog rounds these last few days has been this video of Jack Horner's talk at TEDx in Vancouver (thanks to David Orr at Love in the Time of Chasmosaurs for posting the video link!).



Here Horner gives the basics of his theory that dinosaurs are oversplit, not in the subjective taxonomic sense, but in the more objective biological sense that specimens that could be shown to belong to one species actually represent juveniles of other species. You've all heard the details before, but towards the end he shows a slide (reproduced above) that is pretty damning to the crowd who support the validity of N. lancensis. In fact, adult specimens of T. rex show a very wide ranging tooth count, and it even appears to correspond with relative size (and presumably growth stage. If anything, the number of teeth seen in N. lancensis specimens are only one or two teeth outside the range of variation for T. rex proper, a minor variant that can almost certainly be attributed to ontogeny, and not some cryptic species of giant tyrannosaur lurking in the Lancian faunas that has so far only been identified by two juvenile specimens, while the very common T. rex is known from no juveniles at all.

Anybody know the tooth count for the "Tinker" specimen, currently held in a private collection?

Confuciusornis: Bird-o-Dactyl

There's been a lot of debate about Confuciusornis lately. Could it fly? If so, how? And how well? It probably wasn't doing anything like a modern bird does. Studies of its feather strength suggest it couldn't do more than glide (or could it?). But studies of its forelimb and shoulder girdle show it couldn't lift its arm much above the horizontal plane, making flapping pretty much impossible. Unless that huge, fenestrated deltopectoral crest gave it a rather unique flight stroke that only minimally involved the humerus.

Or, maybe this was a small theropod with enormous, high-aspect ratio wings larger than those of any other early bird, with asymmetrical feathers, puny feet and short legs ill suited for running and a small, barely reversed hallux ill suited for climbing, which couldn't flap and could barely glide with its thin feather shafts, yet is consistently found preserved as enormous flocks at the bottom of deep lake deposits. In which case the giant wings would be for display, obviously, to hopefully impress a predator so much that they decline to eat the poor bird which has no means of escape or defense other than to flee into the depths of the water like a 1960s brontosaur, only to remember that it also can't swim. No wonder they're extinct! Anyway... I hope much, much more study (and some wind tunnel tests) will eventually help untangle this mystery. For now, I was struck by something a little more frivolous. Working on a lateral view of Confuciusornis sanctus, checking and re-checking papers to make sure proportions are right, it started to look unmistakably like the profile of a... rhamphorhynchid pterosaur? Between this, and basal paravians with expanded, diamond-shaped vanes on the tips of their tails, in terms of general body plan there are some curious similarities (convergences?) between the first gliding/flying birds and primitive, long-tailed, high-aspect ratio-winged pterosaurs. My PhyloPic style silhouette version above.

Restoring _Hesperornis_

Wow, lots of great responses to Monday's challenge! Some of you came very close to the particular aspect of the anatomy I was thinking of, though nobody got the specifics. However, many of you brought up additional issues with the reconstruction so I'll address some of those observations below before I get to the real answer.

1. Trish brought up the Coot-like lobed feet. While not the major fix I had in mind, this is also something I had already changed in the new version. The toes of Hesperornis are extremely similar to Grebes in terms of their anatomy, so while no soft tissue impressions of the toes exist for this group, it is almost certain that the toes were lobed rather than webbed (as in Loons and many other diving birds). I had initially based my illustration on this model, which restores the toe lobes divided into somewhat Coot-like segments. However, given the similarity to Grebes, it's probably a safer bet to go with a Grebe-like foot, with non-segmented, asymmetrical lobes (that is, like the flight feathers of birds, the 'vane' of each lobe would be small on the outside edge of the toe but broad on the inside edge). As this was still a work in progress when I began the revisions, I didn't yet add to the podotheca (foot skin covering) with its distinct scutes, but skin impressions from Parahesperornis show that they were present and, again, fairly Grebe-like in appearance.

Above: The feet of Hesperornis probably looked very similar to those of this Grebe.

2. Nobu Tamura pointed out that I bungled my interpretation of the leg integument. Good catch! In my own defense the text of Williston 1896 (which described skin and feather impressions in a specimen now referred to Parahesperornis) isn't exactly clear on the issue and the figure doesn't help much. Williston wrote: "I count twenty-six [metatarsal scutes] on the slab, and to the back part of the bone, while impressions of the feathers will be seen on the opposite side. These feathers were evidently long, reaching nearly to the phalangeal articulation". I remembered this as saying that the feathers essentially cover the tarsometatarsus and that the scutes were present close to the phalanges, but re-reading it sounds more like the MTs were only partially covered in long feathers (on the proximal part of the bone?) while the scutes were present across the distal part. The feathers were long enough to reach the toes, forming some very odd 'bellbottoms' around the scaly part of the metatarsus. I've tried to make this more clear in the new version.

3. Several people suggested that the wings are too prominent/visible, and honestly I'm not sure about this one. I don't know of any research on forelimb musculature that could suggest whether they were external or internal to the body wall, or whether or not they'd be useful in steering or something. I suppose we artists have license to go either way on this one right now, but as you can see I've de-emphasized them in the new version. The old one began to strike me as too Penguin-like, suggesting (even subconsciously) a role in propulsion that was probably not there in life.

4. Marco Tedesco wondered if the orange feathers on the head were incorrect. I have previously blogged about the likelihood of certain feather colors based on diet and structure. However, I don't think Hesperornis would have had much trouble sinking its teeth into some carotenoids to deepen the chestnut hue possible through melanin alone into a richer orange. We know that many cephalopods (including, apparently, some ammonites with preserved pigment) contain deep red carotenoid pigmentation, as do many fish, both of which may have been parts of hesperornithine diet. And in fact, these are colors found in modern Penguins. While on the subject of color, I chose to give Hesperornis a distinct, Penguin-like counter-shaded pattern. It seems to me that counter-shading gets apparently stronger in several independent lineages of diving birds, with more specialized diving forms (Penguins, Loons, Auks) wearing similar black/white colors (at least among breeding males) while less specialized forms (ducks, etc.) are counter-shaded with more subtle earth tones. Hesperornithines are probably the most specialized diving birds of all time (Zinoviev 2010) so it made sense to me to give them generally Penguin or Auk-like coloration.

Ok, now on to the "real" answer. Several people got this pretty close. It does indeed involve the hindlimb anatomy, including the position of the femur, the degree of sprawl in the legs and, ultimately, the life posture and ability to move around on land.

Several online sources have stated that Hesperornis was unable to walk, and must have instead slid around on its belly when on land. As I hinted in the last post, the Web site for the BBC show Sea Monsters (and possibly the show itself which I haven't seen) flat out states that they couldn't walk. But as we all know, TV documentaries are not exactly reliable sources. I tried and (initially) failed to find any support for this in the literature, aside from Marsh's own speculation in his famous Odontornithes monograph: "It may be fairly questioned whether it could even be said to walk on land, although some movement on shore was of course a necessity."

Two pieces of information can be combined to give the answer, the second of which also strongly impacts any life restoration, on land or swimming/diving. First, while the feet of hesperornithines are extremely Grebe-like, the rest of the hind limb anatomy is very similar to that of Loons (Reynaud 2005). Like Loons, hesperornithines had very long tibiotarsi, very short femora, and a high-angle hip socket with a very limited range of motion. Essentially, this means that the upper legs of Hesperornis were locked into a sprawl, which would have made standing upright very awkward. Loons rarely walk upright, and in fact I can't find any images online of such behavior. Loons also will push themselves along on their bellies, "flopping and dragging" as one site describes it (image above from birdinginformation.com)

Now, while the femur was basically immobile, it still had a role in contributing propulsive forces, as demonstrated by the arrangement of muscle attachments, which allowed it to conduct strong backward force through the leg. This is quite a feat because, (finally the answer to the challenge!) as in Loons, the entire, laterally projecting femur, the knee joint, and most, if not all of the tibiotarsus, was likely encased inside the body wall! Yes, according to some recent research (Zinoviev 2010), "the tibiotarsus...was held close to the body and was probably enclosed in the thickly feathered skin of the body wall". So images like mine, and the one below by Nobu Tamura (from Wikimedia Commons, CC licensed) showing free legs are wrong.

Like Loons (image of Common Loon above by Matthew Studebaker, from his photo blog), the feet stick out laterally from the very rear end of the animal near the tail, and it is the feet, rather than the leg as a whole, that provide most of the thrust and control (though, again, even the internalized leg musculature contributes to this).

So, congrats you those who noticed something wonky with the hind limbs! In all, hesperornithines were essentially super-Loons with Grebe feet, though their unique specializations for diving exceeded nearly all modern divers, making them possibly the most truly aquatic dinosaurs that have ever lived.

One last thing: quilong suspected something off with the posture of the neck. As he points out, highly specialized diving birds tend to have advanced ligament systems to keep the neck positioned during dives, and it tends to be streamlined into the body, often in a tight s-curve. This is correct, and my image is a bit misleading as it's meant to depict a hesperorn swimming at the surface with its neck at full extension to reach above the water, like an Anhinga (or indeed, a swimming Loon, which tend to swim almost completely submerged except the top of the back, the head, and the neck). While diving, the long neck would almost certainly be held in a position closer to the body so as not to be subject to forces that would bend it every which way. Whether or not hesperorns did have advanced ligament systems in the neck to help with this, I don't know, but given their extremely derived morphology it wouldn't surprise me.


References:
* Johnsgard, P. (1987). "Diving Birds of North America: 2 Comparative Distributions and Structural Adaptation. " Papers in the Biological Sciences.

* Reynaud, F.N. (2005). "Functional morphology of the hindlimbs of Hesperornis regalis: A comparison with modern diving birds." Geological Society of America, 37(7): 133A.

* Zinoviev, A. (2010). "Notes on the hindlimb myology and syndesmology of the Mesozoic toothed bird Hesperornis regalis (Aves: Hesperornithiformes)." Journal of Systematic Paleontology, 9(1): 65-84.

I'm Doing It Wrong: More on _Hesperornis_

Following the last post on beak anatomy in toothed birds like Hesperornis regalis, I have been coming across some confusion online about another aspect of this ancient diving bird's anatomy. This factoid shows up in a lot of sources (including the official web site for a certain CGI-based TV show) but never, it seems, with a solid reference. I have been trying to dig into this issue myself and am finding out some interesting new info on the anatomy of this bird, to the point that one of my in-progress drawings had to be halted and revised. More on this in an upcoming post, but for now, see if you can figure out what's wrong with this picture: