Predatory Magpies!

I saw something a little ghastly yesterday. On my way up to the office, there's a hill filled with trees and brush. On that hill, I heard a great deal of squawking and chirping. I walked up to the hill and saw two magpies chattering at each other. One of them was standing on top of a poor little woodpecker! The woodpecker was squeaking and often scared. I shoo'ed the magpies away. They didn't really fly away as much as hop off to the side. The woodpecker was in bad shape. One of its eyes was gone, and there was a lot of blood under one of its shoulders. I felt bad, because there was nothing I could do for the woodpecker. As soon as the magpies stepped away, however, it stopped squeaking and was breathing heavily.

I left everyone alone and let nature take its course. I was expecting a dead woodpecker when I came back, so I brought a plastic bag with which to carry the corpse (woodpecker skull!). Oddly, EVERYTHING WAS GONE four hours later. Nothing remained of the woodpecker except some primary feathers that had been torn from the hands. The woodpecker was almost as big as the magpies, so they couldn't have flown off with it, but a raven might have.

It's the first time I've seen predatory behavior in magpies. I wonder if they actively attacked the woodpecker, or the woodpecker was already injured?

A Jurassic bird from China helps clarify theropod digital homologies

A new article printed in Nature on Thursday (Xu, et al. 2009) describes a Jurassic bird, pushing back the origin of birds almost 80 million years, Protoavis notwithstanding. More importantly, the new animal demonstrates that avian digital homologies have existed for just as long, and that, therefore, theropod dinosaurs cannot have been the ancestors of birds. The digits of theropod dinosaurs—especially maniraptorans, who are most often cited as likely avian ancestors—display a pattern of lateral digit reduction (LDR). In the most basal theropods, all five digits were present, though digit V was reduced to a bony splint. Later in theropod evolution, digit IV was lost as well. In all known tetanurine theropods, the remaining digits are, unquestionably, digits I-III (thumb, index, and middle fingers). This pattern of digit loss is at odds with most other animals, especially mammals, who tend to reduce their digits based on bilateral digit reduction (BDR). Were this the case in theropods, we would expect to see tetanurine theropods with digits II-IV (digits I and V would be lost).

Paleontologists have been at a loss to explain how theropods with digits I-III evolved into birds, which retain digits II-IV (based on embryology studies). The Hox genes are usually blamed for the switch, but genetic correlates do not fossilize well. Paleontologists have further attempted to discredit the studies which demonstrate that birds develop digits II-IV, insisting that the microscopic limb and digit buds in bird embryos cannot be accurately seen, and thus, perhaps birds really do develop digits I-III. This author thinks they doth protest too much, and that it is far more parsimonious to believe that, in fact, the ancestors of birds must have gone through a period of BDR, while theropods, who exhibit LDR, are not suitable ancestors for birds.

The new fossil is unfortunately named Limusaurus by the authors (who wear their bias on their sleeves), who consider it a ceratosaur. Ceratosaursia is a primitive group of theropod dinosaurs including such familiar forms as Ceratosaurus and Carnotaurus. These are big, toothy predators with robust features and powerful jaws. Limusaurus, by contrast, is a very small bird with long legs built for fast running; extremely reduced, splint-like arms; a toothless mouth covered in a rhamphotheca (beak); a single, fused sternal plate; and a gastric mill implying herbivory. These are all features indicative of an avian classification for Limusaurus. What’s more, the presence of a large singular sternal plate suggests that Limusaurus’ ancestors were flighted. Given its suite of basal and advanced features, Limusaurus may, in fact, be a basal paleognathid, obviously more derived than the tinamous, but could be an extremely basal ratite. For these reasons, I believe a name change is in order. To reflect the true phylogenetic nature of the animal, I recommend that Limusaurus be changed to Limuornis.

The authors correctly note that Limuornis retains a stub of digit I in the form of a single rounded metacarpal. This is not surprising in basal bird, and it is even less surprising to see that digit IV is also extremely reduced, though not the same extent, in a flightless animal. Digits II and III, though small, are fully-formed and possess small, blunt claws. The entire arm is very short, reflecting the condition seen in modern ratites. In some ways, the arms are vestigal, but they were probably used in courtship or aggression displays. The long legs and small, raised hallux suggest that Limuornis was strongly cursorial and did not fly or use its arms for prey capture. In fact, prey capture was not probable anyway—a large gastric mill of stones suggests that Limuornis was an herbivorous animal or, at the very most, omnivorous as in modern ratites. As stated above, Limuornis’ finger formula is II-III-IV, like modern birds but unlike theropod dinosaurs. More interestingly, the particular phalangeal formula of Limuornis’ fingers are incompatible with theropod hands. Whereas the tetanurine theropod hand formula is 1-2-3-x-x (metacarpals not included), the formula of Limuornis is x-3-3-x. Even if theropods did have fingers II-III-IV, their phalangeal formula is unlike Limuornis, so hand morphology is again incompatible. A reduction in manual phalanges is not unexpected given Limuornis’ flightless condition.

Despite its many derived features, Limuornis retains a few strikingly basal characters, including the presence of a long tail and a triradiate pelvis. Though incomplete, the tail is probably as short or shorter than in Archaeopteryx. While it may seem strange that a basal bird would retain its tail, keep in mind that a variety of basal flying birds, including Archaeopteryx and Jeholornis have long tails, and almost all flightless Mesozoic birds, including dromaeosaurs and troodontids, also have long tails—in some cases longer than Archaeopteryx. A long tail is obviously primitive for Aves, and it may have been lost multiple times within the group, including here, in paleognathes. The triradiate pelvis is a bit more difficult to explain, but, like the long tail, is probably primitive for Aves. Modern ratites have a pelvis that is not unlike Cretaceous flightless birds, though the pubis is more backswept. If a long tail was lost multiple times among birds, can we not say the same for the triradiate pelvis? This structure is potentially primitive for paleognathes as well, and the pubis retrovated to make room for a larger gut as herbivory became more important to the ratite diet. This would explain the differences between ratite pelvic girdles and those of flighted birds—the quadraradiate pelvis is merely a case of parallelism. Notably, the back half of the iliac blade in Limuornis is surprisingly similar to the same structure in emus and ostriches.

Limuornis is an exciting discovery which suggests that crown-group birds originated sometime in the Triassic period or, at the latest, the Early Jurassic. Incompatible finger formula notwithstanding, it is clear that the theropod dinosaurs that lived during the Late Triassic and Early Jurassic are horrible candidates for avian ancestry. They are either too large and ungainly (Dilophosaurus, Herrerasaurus) or too unspecialized (Eoraptor). While it remains possible that birds and dinosaurs share an arboreal common ancestor, I believe that Limuornis demonstrates that birds evolved prior to theropod dinosaurs, and that the two must have evolved from highly disparate groups of tetrapods.

Crouching Daddies, Hidden Implications

By now, you're probably all aware of the new study published a few weeks ago in Science magazine about how male maniraptors brooded the eggs. It's old news, I know, but I'll lay out the basics for you anyway. Three dinosaurs have been found sitting atop nests: Citipati, Oviraptor, and Troodon. Everyone assumed they were females, but not so fast, kiddies! Now there's a way to tell. Remember way back when Horner and his colleagues sliced open a T.rex femur and found gold...I mean, medullary bone inside? Well, medullary bone has since been found in Allosaurus and Tenontosaurus. Finding medullary bone in dinosaurs isn't particularly surprising, as it's present in crocodilians and birds. For the uninformed, medullary bone is laid down in the long bones of archosaurs just before, during, and after a female becomes pregnant and provides the calcium needed to produce egg shells.

So if we assume that female archosaurs produce medullary tissue in their long bones in association with egg-laying (all signs point to "yes"), we can test those "nesting" theropod fossils to see if girls, but instead of lifting up their skirts, we're sawing their femurs in half. Anyway, it turns out that all three nesting dinosaurs, Citipati, Oviraptor, and Troodon, lack medullary bone, which means they're males. That means males brood the nest, a trait shared by modern paleognathine birds (ratites + tinamous), which most likely means that male brooding predates "modern" birds. Given the clutch sizes of the three dinosaurs, it also seems likely that, again like paleognathes, nests were filled by more than one female. So that's awesome--now we know a whole lot more about maniraptoran breeding behavior and physiology. We can probably assume that chicks were precocial and left the nest soon after hatching, although in some ratites, the chicks stay with the parent for several months to a year.

But wait--there's more! The authors of the paper perhaps did not realize that if maniraptors bred like paleognathine birds, there are implications for sexual dimorphism, too. In modern paleognathine birds, sexual dimorphism is limited to small size differences between the sexes. In the ostrich, plumage in males is more "flashy" than females. In general, however, paleognathine birds have fairly drab plumage. The cassowary is the most colorful ratite, but that's because its neck skin is bright blue! Bright plumage seems to be linked with mating dances and competition between males for females...however, with the flashy performances comes maternal brooding, biparental care and altricial young.

Another possibility is that the three nesting dinosaurs are males by coincidence, and that those species bred like raptorial birds. In raptors, both parents share brooding duties. The young are born extremely altricial but develop quickly. Like ratites, raptors don't show much sexual dimorphism aside from size differences. However, the clutch size of the fossil brooders argues against a modern raptor comparison. Raptors will often lay only two or three eggs in a single large nest. Paleognathine birds lay many more eggs, and oftentimes, multiple females will deposit their eggs in a shared nest, which the male then broods. So I think the paleognathine interpretation is the right one. Now, as for sexual dimorphism and coloration, I wonder if we could carry the ratite comparison over to non-avian maniraptors, too. Food for thought!

Zhongornis haoae

Zhongornis haoae is an itty-bitty, teeny-weeny juvenile bird from the Early Cretaceous of China. At just over 10 centimeters long, the little guy is positively tiny. The drawing above is a measured one: every piece of the body was drawn according to its length as described in the description. Zhongornis is unique for a number of reasons. First and foremost, its tail is transitional between the long bony tails of Archaeopteryx and Jeholornis and the short lil' pygostyles of the...Pygostylia. Zhongornis has 13 short 'n' stumpy caudal vertebrae which anchored a lengthy tail fan. Additionally, Zhongornis' third manual digit is made up of only three phalanxes, making Zhongornis unique among known birds, both living and extinct.

The skull is badly crushed, so whether the little bird had teeth or not is unknown. I decided to give it a short little beak instead--maybe its teeth grew in later. Gao, et al. (the describers) suggest that Zhongornis' reduced third finger is also in line with the transition from outgroup birds to modern forms, but that can't be true. If Zhongornis is intermediate between long-tailed birds and Pygostylia, one would expect to see confuciusornid birds with just three phalanxes in their third manual digit, but in fact they retain all four. So Zhongornis developed that particular mutation by itself. If anybody would like a copy of the paper, I have it in PDF form, so let me know and I'll send it your way.

Reference:

Gao, C., Chiappe, L. M., MEng, Q., O'Connor, J. K., Wang, X., Cheng, X. & Liu, J. (2008). A new basal lineage of Early Cretaceous birds from China and its implications on the evolution of the avian tail. Palaeontology 51(4): 775-791.

Zhongornis is coming...

I've got a life restoration brewing. Life-size, if you're lucky! Look for it in the coming days.

Yes, I know, non-avian maniraptors had uncinates, too.

There's a new paper out at the Royal Society, finally detailing one of the more ignored aspects of maniraptoran anatomy: the uncinate processes. Codd, et al. for perhaps the first time as far as I can remember, actually discusses the role and phylogenetic importance of these structures, which must have been quite widespread among the Maniraptora. The role of these rib protrusions has never been entirely clear, but Codd, et al. suspect that they have something to do with respiration. I had always learned that the uncinates strengthened the boxy structure of a bird's torso. While this is almost certainly one part of the equasion, it would seem that uncinates serve several purposes. Of minor importance is that, at least in Sphenodon punctatus (tuatara), the uncinates connect to the gastralia via external oblique muscles. Non-avian maniraptoran dinosaurs (and even some avian ones) seem to have had well-developed gastralia, so that function may have been retained.

But more importantly, in modern birds, the uncinates act as levers that, together with muscle action and sternal ribs, actually raise and lower the sternum during respiration. The "pump" action of the sternum has long been known as a major factor in avian breathing, but it's surprising to see the uncinates actually facilitating this movement. But that's not even the focus of the paper. Rather, Codd et al. merely strive to understand the phylogenetic consequences of uncinates in the Theropoda, and what that might mean for theropod activity levels.

The paper is actually disappointingly short, especially when you realize that it could've actually been shorter. It turns out that uncinate processes have a fuzzy preservation record. This should not surprise us, because they are attached to the ribs with cartilage, and the processes themselves were thin, strut-like bones. At any rate, they are only known with certainty in Oviraptor, Citipati, Khaan, Velociraptor, Deinonychus, and Microraptor. Thanks to phylogenetic bracketing, we can pretty safely conclude that the common ancestor, at least, of Oviraptor and Deinonychus also had uncinates. So that means we can expect to find more complete remains of, say, Nothronychus with uncinates, and troodontids, too.

In modern birds, the sternum's keel provides a key muscle attachement site for respiration, but Codd et al. suggest that, because non-avian maniraptors did not have keels, they may have retained their gastralia for essentially the same purpose. Short paper, but these are things that needed to be said!

Terrestrial Mesozoic Birds?

So the whole point of being a bird is to get up into the air, right? You're safe from predators up there, after all. You can raise your chicks, find food, and basically live it up without worrying about hungry terrestrial predators. The air and treetops represents a safe haven! So why wouldn't birds take advantage of it right away? As it turns out, they might not have. A new study in Current Biology by Christopher Glen & Michael Bennett suggests that, paradoxically, Mesozoic birds may have been primarily ground-lovers. The two authors came to this surprising conclusion by measuring the curvature of the claw of digit III in several Holocene and Mesozoic birds. They found that, in modern birds, claw curvature increases with degree of arboreality. Many birds, it turns out, forage on the ground. But many, many birds spend their days on the ground and in the trees. Among living species, a large spectrum is represented. Glen & Bennett created six categories to fit their birds into: "ground-based birds," "dedicated ground foragers," "predominantly ground foragers," "predominantly arboreal foragers," "dedicated arboreal foragers," and "vertical surface foragers."

For some idea of this spectrum, I'll list examples of birds which match the categories listed above: ostrich, chicken, pigeon, cuckoo, (no example given), woodpecker. Claw morphologies across modern groups seems to be indicative of degree of arboreal foraging--the more curved the claw, the more arboreal the bird.

Glen & Bennett measured the claws of several Mesozoic taxa, incuding Archaeopteryx, Microraptor, and Confuciusornis. Of all the Mesozoic birds sampled, only Sapeornis fell within the "predominant arboreal forager" category. All of the other ancient avians fell below that grouping, and were generally found to be either "dedicated ground foragers" or "predominant ground foragers." Not surprisingly, Caudipteryx fell within the "ground-based bird" category, while Pedopenna, Microraptor, Archaeopteryx, and Jeholornis were strong terrestrial in their habits.


The paper raises a number of questions. First, the very idea that birds "escaped" to the trees must be abandoned, if they did most of their business on the ground. One might be tempted to believe that, in China anyway, large predators did not exist to yet to threaten these largely terrestrial birds, but the recent discovery of dromaeosaur tracks in China indicates that a Deinonychus-sized predator existed alongside those smaller avian critters. Also, the motivation for the evolution of the reversed hallux must be questioned. While generally thought of as a means to perch, I think the idea that Archaeopteryx and its kin were spending a lot of time soilside downplays the importance of the hallux. Why did the reversed hallux evolve if trees were not the enormous draw we once thought they were?

These are important questions, and I'm happy to see that Glen & Bennett have brought them up. The trip from the ground to the trees may have been a lot more complicated than we awknowledge, but that's fine by me. It just means there's so much more to discover!

Hat-tips to Will and Brian, of course, for letting me know this story existed.

Glen, C. L. & Bennett, M. B. (2007). Foraging modes of Mesozoic birds and non-avian theropods. Current Biology 17(21): published online.

Li, R., Lockley, M. G., Makovicky, P. J., Matsukawa, M., Norell, M. A., Harris, J. D. & Liu, M. (2007). Behavioral and faunal implications of Early Cretaceous deinonychosaur trackways from China. Naturwissenschaften: published online.

Greg Paul Was Right...AGAIN!

I mean, Predatory Dinosaurs of the World was published in 1988, and back then, Greg Paul was illustrating his raptor dinosaurs with feathers. Extensive feathers. This is just another instance of the man knowing the Theropoda better than most professional paleontologists. Just for fun, here are some more Greg Paul theories put forth in Predatory Dinosaurs that were later proven absolutely freaking correct:
1) Spinosaurus and Baryonyx form a monophyletic clade.
2) Spinosaurus is not a big allosaur, and was not related to Acrocanthosaurus.
3) Archaeopteryx has a hyperextendable second toe.
4) Birds, dromaeosaurs, and troodontids form a monophyletic clade (now known as Paraves).
5) Carnotaurus is a big ceratosaur.
6) Ceratosaurus and Coelophysis shared a recent common ancestor.
7) Some higher theropods were arboreal.
8) Many theropods, including dromaeosaurs, troodontids, and higher tetanurines had feathers.

And, just to balance things out, here are a few things he was wrong about. In 1988.

1) Tyrannosaurs evolved from allosaurs (he still alludes to this in 2003's Dinosaurs of the Air)
2) Deinonychus and Velociraptor are cogeneric.
3) Therizinosaurs were incredibly derived, late-surviving prosauropods.

Pretty good balance in favor of "this guy is right a lot." Anyway, I bring this up because in today's issue of Science, Turner, Makovicky & Norell announced that Velociraptor mongolensis, which is actually one of the smallest core group dromaeosaurs, had feathers. They came to this conclusion after studying a single well-preserved ulnar bone, which retains feather quill knobs. In modern birds, quill knobs line the ulnar bones and serve to attach the large secondary feathers and greater secondary coverts to the ulna itself with the help of follicular ligaments. That is, the quills don't erupt from the bone, but the secondary feather follicles are very deep, ensuring their rigidity. This is actually nothing compared to primary feathers, which grow from the crest of the 2nd finger over the 3rd finger. The entire primary quill is covered by a thick web of skin. You can't pull a bird's primaries off without damaging the manual bones.

Anyway, that's not the point. The authors suppose that, given the amount of quill knobs preserved (6) and the spacing of individual knobs, Velociraptor probably had 14 secondary feathers. Archaeopteryx has around 12, and Microraptor may have had 18. This may seem like a large range in feather count, but feather growth is not set in stone like, say, number of cervical vertebrae (which isn't either, but...you see what I mean). Even within a single species of living bird, there is variation in the number of secondary feathers.

The authors close the short paper by noting that: "An examination of the living families of birds shows a significant correlation between the absence of ulnar papillae and the loss and/or reduction in volancy, even though some strong flyers lack papillae. This raises the possibility that ulnar papillar reduction or absence in large-bodied derived dromaeosaurids reflects loss of aerodynamic capabilities from the clade's ancestral members." What this basically means is that, in extent birds, the reduction and loss of quill knobs is often correlated with a reduced flight performance. The fact that Velociraptor still has quill knobs (and a lot of them) suggests that its immediate ancestors could fly to some degree, although Velociraptor itself was clearly flightless.
So, actually, that means Greg Paul is right about one more thing, from his more recent Dinosaurs of the Air: Deinonychosaurs are secondarily flightless. And thus, we may be able to replace the "Paraves" label with "Aves" and call it good. We can think of Velociraptor, Troodon, and all the little deinonychosaurs in between as the first flightless birds!

Birds--Fliers Not All

I probably should have blogged about this last year, but I honestly forgot about it until I was leafing through my papers and found Phil Senter's 2006 discussion about primitive birds and their flying abilities. Basically, Senter looks at the orientation of the scapula in relation to the ribcage in the fossil animals, kind of like in this story, and discovered that fossilization pretty well demonstrates real-life scapular orientation. In crown-group and enantiornithine fossils, the scapula sits atop the ribcage. This position, of course, lifts the glenoid up and out, so that the bird's arms "face" outward--thus allowing a flight stroke. However, fossils like Archaeopteryx, Jeholornis, and Confuciusornis have scapular blades that lie against the ribcage, angled upward, like the case in every other theropod dinosaur, including (sniff) the deinonychosaurs. The possibility of post-mortem skeletal movement is real, but it's interesting that in obviously avian fossils the scapulae are oriented in the modern manner consistently. Why would non-avian dinosaurs be more inclined to have loose scapulae?

This is fairly important, because all previous discussions of how Archaeopteryx are now moot (assuming that Senter is right). Instead, we're forced to confront the idea that Archaeopteryx, the first bird, could not actually fly. Rather, because it could not life its arms above the horizontal, it could not complete a recovery stroke and could not generate lift. Senter says that in the Ornithothoraces clade, which includes enantiornithines and neornithes, the scapula migrated up the ribcage to lay at the top of the ribs, on either side of the spinal column, allowing birds to complete a flight stroke.

Senter posits that Archaeopteryx, Confuciusornis, and Jeholornis were all gliders. And gliding does not equal flying. And yet all three of these "birds" were blessed with asymmetrical flight feathers. In a previous blog, I correlated asymmetrical feathers with flight, and flight with Aves. In this way, I was able to show that Microraptor is a bird, given its asymmetrical feathers which apparently equate flying ability. According to Phil Senter, this is not the case, and Aves may need to be rethought once again. If our definition of Aves includes the ability to achieve a recovery stroke, then a bunch of primitive forms have been kicked out. Apparently, asymmetrical feathers predated flight.

Of course, it asymmetrical feathers constitute the golden rule for defining Aves, than Archaeopteryx, Confuciusornis, Jeholornis, and the deinonychosaurs are still in the club.

P.S. I suppose the possibility exists that Archaeopteryx, Confuciusornis, Jeholornis, and deinonychosaurs constitute a sister group to the Ornithothoraces, whereupon the common ancestor of this largest group is defined as having asymmetrical feathers, but one branch (Archaeopteryx & Co.) were content to glide while the ornithothoraces developed powered flight. Exactly how close Archaeopteryx and Confusiusornis are is a matter of some debate.