Scientific Anachronism and why Biostratigraphy Matters

Image: Stegosaurus confronts Tyrannosaurus, from Walt Disney's Fantasia. Such anachronistic views of paleontology could never form the basis of peer-reviewed literature, could they?

A new study (Carbone, Turvey &Bielby, 2011) suggests T. rex could not have been a pure scavenger.

Yeah, I know. This is already the universally accepted position of modern paleontologists. Of course T. rex scavenged if it could, but there is ample reason to think (and ample fossil support backing this up) that it hunted as well. Even the originator of the scavenging thoery, Jack Horner, has basically admitted that he only came up with it as a way to get young people to think critically about their own preconceptions (obviously, he has never met any young paleontology fans. I'd have given up that strategy after I witnessed my first T. rex vs. Spinosaurus debate).

However, as Denver Fowler pointed out on the DML today, drawing an obvious conclusion is the least of the paper's problems.

I recently participated in at least two paleoart discussion threads in which really awesome artists showed off some mind-blowingly fantastic paintings depicting the Jehol biota. I know first hand that both artists are completely on the ball and know their stuff. But both made common errors in the often neglected field of biostratigraphy.

In one, a Sinornithosaurus watches as two Microraptor glide down from the trees. These are two similar animals from around the same time and place. However, there is no evidence that they ever met. All known fossils of Microraptor come from the Jiufotang formation, dated to 120 million years ago, plus or minus 700k years. The youngest Sinornithosaurus fossils are from the upper Yixian formation, dated to around 122 million years ago. The timespan and environment are grossly similar, but 2 million years is still a long time in a world where most dinosaur species, if not genera, don't span more than a couple million years (and the ones that do are probably egregiously over-lumped, like Iguanodon).

Another painting portrayed a Yixian formation scene with Yixian ornithopods and Yixian insects being fed on by Jeholopterus, a pterosaur which lived in the Daohugou biota, in beds dating to at least 150 million years ago, a full 25 million years before the Yixian faunas existed. The error here was probably based on a confused history of dating the formations (old sources placed the Yixian in the late Jurassic), and many sources, both professional and popular, which tended to conflate the various Chinese feather-preserving formations into one amorphous pseudo-fauna.

Artistic depictions throwing together prehistoric animals from disparate times are obviously nothing new. Walt Disney Pictures has done this at least twice, first and most famously in Fantasia (Stegosaurus meets T. rex meets Pteranodon), and later and more flagrantly in Dinosaur (I can't think of any two animals in that movie that were actually contemporaries, and many didn't even live together on the same continent).

This is somewhat excusable when it's done for the sake of art (as long as that art isn't passed off as being scientifically rigorous). But this kind of disregard for, or generalization of, biostratigraphy can creep into science and completely foul up your results.

In Carbone et al. 2011, the authors attempt to calculate the amount of potential carcasses that would have been available to scavenging Tyrannosaurus rex in its environment to make their case. Their lists of T. rex contemporaries are reproduced in part below:

Species and body masses of carnivorous non-avian theropod dinosaurs of Late Cretaceous North America
Dromaeosaurus albertensis
Richardoestesia gilmorei
Richardoestesia isosceles
Saurornitholestes
Velociraptor sp.
Troodon formosus
Chirostenotes elegans
Chirostenotes pergracilis
Nanotyrannus lancensis
Albertosaurus sarcophagus
Tyrannosaurus rex

Species and body masses of herbivorous dinosaurs of Late Cretaceous North America
Parksosaurus warreni
Prenocephale edmontonensis
Ornithomimus velox
Struthiomimus sp.
Thescelosaurus garbanii
Thescelosaurus neglectus
Leptoceratops gracilis
Montanoceratops sp.
Pachycephalosaurus wyomingensis
Edmontosaurus annectens
Edmontosaurus regalis
Edmontosaurus saskatchewanensis
Lambeosaurus sp.
Parasaurolophus walkeri
Edmontonia rugosidens
Ankylosaurus magniventris
Triceratops horridus
Alamosaurus sanjuanensi

The authors state, "our species list is treated as representing a consistent sympatric faunal unit across this region for the purposes of analysis." But they absolutely don't represent that.

If you have even a little bit of a handle on Late Cretaceous biostratigraphy, or the paleoecology of T. rex, you may notice a few problems with these lists. Namely, the fact that they are complete messes, incorporating erroneous or outdated taxonomic assignments or over-generalizations of the geologic column.

This kind of data crunching would require taxa to be broken down on an environment-by-environment basis. That is, in order to be meaningful, all included taxa have to be demonstrated to be contemporaries. Most of the taxa in those lists were not, or can't be said to have been with any confidence.

To be fair, some of the mistakes are due to very new research, some of which has only appeared in abstracts or mentioned briefly in papers. For example, while Edmontosaurus regalis is widely reported from the late Maastrichtian Hell Creek and Lance formations, this is mainly by default, skeletons that are not identifiable to the species level. Ongoing stratigraphic and taxonomic work by Nicolas Campione has shown that E. regalis was actually not a contemporary of E. annectens, and specimens assignable to that species are only known from lower strata. The validity of E. saskatchewanensis, which is from the same stratographic level as T. rex, is pretty dubious. E. annectens is its likely synonym.

Parasaurolophus is known exclusively from the Campanian-age Dinosaur Park Formation, over five million years before the earliest known T. rex fossils. Same goes for Lambeosaurus. While the former was tentatively identified in the Hell Creek by Sullivan & Williamson (1999), this was based on very fragmentary remains that almost certainly belong to Edmontosaurus instead. Montanaceratops is from the St. Mary River Formation, dated to the early Maastrictian and also pre-dating T. rex.

Some cases are even more nuanced. Alamosaurus did coexist with T. rex, but not with many of the other listed species. Current indications are that the southern part of North America during the late Maastrichtian supported a different fauna from the north, comprised many of species which are related to, but distinct from, their northern counterparts. Alamosaurs, for example, did not coexist with Triceratops, but Ojoceratops (assuming they're distinct). It didn't coexist with Torosaurus latus (which the authors apparently lump with Triceratops), but with "Torosaurus" utahensis. Indications are that these beds are a bit earlier than the late Maastrichtian as well, so while Alamosaurus lived alongside Edmontosaurus, it was E. regalis rather than E. annectens.

The carnivores don't fare much better. Most are tooth taxa, like Troodon (another Dinosaur Park critter from the Campanian). While "Troodon" teeth are known from the same beds as T. rex, they're almost certainly not Troodon formosus. The same goes for Dromaeosaurus. However, these are taxonomic issues, not biostratigraphic ones, and don't really affect species count--whatever we name them, there were at least one troodontid and at least two dromaeosaurids present (though the authors erroneously list both Velociraptor and Saurornitholestes, based on the same specimens, first referred to the former and then the later, both incorreclty). Not so for the inexplicable inclusion of Albertosaurus. I can figure out where these other misplaced species came from, but I don't know of any albertosaur remains having been reported from Lancian-age deposits. Anybody? Either way, it's almost certainly an error (as is making Nanotyrannus a distinct taxon, but that's another story).

So you can see why failing to understand which dinosaurs lived together, specifically, can have major implications for actual science. This kind of paper also illustrates why it's a bad idea to keep non-diagnostic genera around as nomina dubia and not sink them into their better known, probably-synonymous counterparts or simply designate neotypes from the good material. These authors avoided pitfalls like including Thescelosaurus infernalis (=T. sp.), Manospondylus gigas (=Tyrannosaurus rex), Aublysodon molnari (=Tyrannosaurus rex), Thespesius occidentalis (=Edmontosaurus annectens), Trachodon mirabilis (=Edmontosaurus annectens), or Agathaumas sylvestris (=Triceratops horridus), but those taxa aren't doing science any favors by cluttering the playing field.

Here's my preliminary attempt to clean up their faunal lists, based on a Lancian-age, northern ecosystem: (updated thanks to additional information provided by Mickey Mortimer in the comments. note that I'm following the authors in not including avialans)
Dromaeosaurinae sp.
Zapsalis abradens
Richardoestesia gilmorei
Richardoestesia isosceles
Troodontidae indet. spp. (multiple species)

Pectinodon bakkeri

Paronychodon sp.

Avimimidae sp.
Chirostenotes elegans

Chirostenotes? sp.
Tyrannosaurus rex (=Manospondylus gigas)
Struthiomimus sedens

Ornithomimus velox

Ornithomimidae sp. (="Orcomimus")

Dromeiceiomimus sp.

Alvarezsauridae sp.

Therizinosauridae sp.
Thescelosaurus garbanii
Thescelosaurus neglectus
Leptoceratops gracilis
Pachycephalosaurus wyomingensis
Edmontosaurus annectens (=Thespesius occidentalis)
Edmontonia schlessmani (=Denversaurus schlessmani)
Ankylosaurus magniventris
Torosaurus latus?
Triceratops horridus (=Agathaumas sylvestrus?)


References:
* Campione, N.E. (2009). "Cranial variation in Edmontosaurus (Hadrosauridae) from the Late Cretaceous of North America." North American Paleontological Convention (NAPC 2009): Abstracts, p. 95a.

Brilliant New Anchiornis, the Bone Wars, and More

A few quick news items while I finish up a post exploring the extent and structure of beaks in theropods...

"Dinosaur Wars" on PBS's American Experience
I haven't had a chance to check out this new PBS special on the Bone Wars (darn you, unreliable internet connection!) but the whole thing can be seen here.

"Dinomorphosis" on National Geographic's Naked Science
Airing next week, this special explores current knowledge of feathered dinosaurs. You can see the trailer here (not bad, aside from the rampant bunny hands and baffling statement that all feathered dinosaurs were carnivorous), and a related article from the magazine with photo gallery.

Be sure to check out the image of an undescribed Anchiornis specimen in the photo gallery. The preservation is utterly phenomenal, and even the previously-described color pattern is visible to the naked eye.

Also exciting is a new paper on sexual dimorphism and reproduction in the pterosaur Darwinopterus. Check out the great article summarizing the findings at New Scientist, and this skimpier Discovery article highlighting an awesome new restoration of male and female specimens by Mark Witton.

Theropods That Fit the Bill

[Image: Skull of a gull compared to a living specimen. The apparent differences in the extent of the beak are caused by the presence of different kinds of rhamphotheca.]

One aspect of Mesozoic birds and other theropods that doesn't get discussed much are their bills. Beaks or beak-like structures (generally, rhamphotheca) have a wide but extremely spotty distribution among Mesozoic theropods, and numerous theropod groups seem to have evolved them independently of one another.

Perhaps the most basal known theropod that likely bore a beak (assuming we can safely exclude the skull material attributed to the infamous "first bird" Protoavis) is Limusaurus inextricabilis from the Oxfordian, about 160 million years ago. Though it belonged to the otherwise toothy clade Ceratosauria, Limusaurus was completely toothless. To be precise, most theropods have teeth in the three major sections of their jaws: the premaxilla at the front of the skull, the maxilla behind it, and the dentary, or lower jaw. Ornithischian dinosaurs had an additional bone, the predentary, at the tip of the lower jaw that was always toothless, indicating that almost all ornithischians probably bore a beak, at least on the lower jaw (and ceratopsians added an additional, pre-premaxilla: the rostral). Limusaurus lacked teeth in the premaxilla, maxilla, and dentary, so it was completely toothless and, therefore, it is assumed to have been beaked.

[Image: Skull reconstruction of Limusaurus, posted by Dave Hone at his Archosaur Musings blog.]

As far as I know, Limusaurus is the only non-coelurosaurian theropod that bore a beak. Generally, this fits well with the idea that non-coelurosaurian theropods were hypercarnivorous flesh eaters with little variation in their diets. However, as a number of recent papers by Lindsay Zanno and colleagues has shown, coelurosaurs started playing around with omnivory and herbivory, and as a consequence, many lineages cast off some or all the sharp teeth that characterized their ancestors.

[Image: Skull reconstruction of Pelecanimimus by Ville Sinkkonen]

The first coelurosaur lineage to start shedding their teeth permanently were the ornithomimosaurs. This group is well-known for their toothlessness, and evidence from specimens with preserved keratin sheaths on the jaws (Norell et al, 2001) show definitively that they bore keratinous beaks on both the upper and lower jaws, at least in advanced species. As expected, the most primitive ornithomimosaurs still retained teeth. Pelecanimimus polydon, as its name implies, had teeth in the premaxilla, maxilla and dentary. The next most advanced ornithomimosaur, Harpymimus, is the first example among theropods of the "half beak." While its upper jaw was toothless and likely beaked, it retained teeth in the lower jaw. I'll come back to the implications of these "half beaks" further down. The most basal ornithomimosaur wich lacked teeth completely seems to be Garudimimus, though the status of Beishanlong is unknown.

After the ornithomimosaurs, beaks are found in therizinosaurs. Again, early forms like Falcarius had a full compliment of teeth, but in laker ones like Beipiaosaurus, the teeth became restricted to the middle of the jaws, leaving room for a beak in the front, similar to ornithischians. Next, oviraptorosaurs seem to have developed beaks fairly early in their evolution. While Incisivosaurus had teeth in both jaws (though restricted to the tips), Caudipteryx had only a few teeth in the premaxilla, another example of a "half beak" where a toothless lower jaw is matched with a toothy upper jaw. While the several possible intermediate forms lack skulls, both caenagnathids and oviraptorids proper had fully toothless jaws, so presumably they were fully beaked by the time they diverged.

Next up were the deinonychosaurs, and while some seem to have dabbled in omnivory, they were mainly carnivorous, and none seem to have developed beaks. Greg Paul is infamous for restoring them with cornified tissue or "proto beaks" at the tips of their jaws adjacent to teeth, but there isn't much evidence to support this idea as far as I know. However, many deinonychosaurs which preserve feathers show a (usually small) portion near the tip of the snout that is unfeathered. This featherless snout tip is also seen in some toothed, presumably beakless enantiornithines. It's possible this could be evidence of "rhamphotheca" in its loosest sense--the very lightly cornifies, flexible bill skin found toward the back of the beaks in some modern birds, where the horn-like, kerationous portion thins out into normal skin. More on these flexi-bills down the page.

[Image: My own simplified cladogram of Aviremigia showing some notable occurrences of beaked and half-beaked and beak-free birds. Excuse the quality in close-up, some of these were yoinked from works in progress.]

Around the base of Avialae, the occurrence of half-beaks seems to explode. Almost all known basal, non-pygostylian avialans lack teeth in the upper jaw (e.g. Jeholornis, Yandangornis) or lower jaw (omnivoropterygids) and, possibly, both (Jixiangornis preserves no teeth and may have been full-beaked, but the skull is badly crushed, and crushing has been known to obscure the tiny teeth that should be present in other basal avialan specimens). This trend appears to culminate with the confuciusornithids, which are not only toothless but have sharply pointed jaws that, in some very rare specimens, preserve the actual keratin of the beak. These impressions show that even in these fully beaked birds, the rhamphotheca was thin and delicate and probably not as heavily mineralized as in modern birds.

The next bit is rather odd given the trends seen at the base of avialae. In most basal ornithothoraces (the group that includes enantiornithines and ornithuromorphs), the jaws are fully toothed, with no evidence for beaks. It's tempting to think that this could unite the enantiornithines with the toothy, beakless deinonychosaurs and Archaeopteryx in a "Sauriurae" to the exclusion of the beaked birds. However, given the numerous times beaks have evolved independently in vertebrates, it's not unthinkable that each of the half-beak examples above arose independently of one another (or, that some reversal occurred at the base of ornithothoraces to return birds to a state of fully-toothed maws). Either way, while many enantiornithines preserve jaw material, only a few exhibit the kind of toothlessness at the front of the jaws that could imply a beak. These include the half-beaked Alethoalaornis (with a toothless dentary but toothed premaxilla), the fully-beaked Gobipteryx, and the half-beaked Boluochia. Boluochia had teeth in the dentary but none in the upper jaw and, in fat, had a strongly hooked premaxilla similar to the hooked beaks of modern raptors. Enantiornithine relationships are too unresolved to be able to tell if these beaked birds all form a natural group, or if beaks evolved multiple times among enantiornithes, but given their diversity it's a safe bet that many different lineages came up with their own particular feeding solutions.

[Image: The compound rhamphotheca of an albatross is visible as distinct sutures, and is also found in some non-avian birds. Image from the RSPB.]

As expected based on the enantiornithine record, most primitive ornithuromorphs (the fan-tailed birds, including Aves) either lakced beaks or exhibited a half-beaked configuration. While Hongshanornis was originally reported to have a beak, Jingmai O'Connor and colleagues later showed that it had tooth sockets preserved in the upper and possibly lower jaws (same goes for the related Longicrusavis). The earliest fully-beaked ornithuromorph is also one of the most primitive, however: Archaeorhynchus lacked teeth and had a flattened, Spoonbill-like beak. The songlingornithids (such as Yixianornis), and the later hesperornithines and Ichthyornis all had a therizinosaur-like configuration, with toothless premaxilla (and even predentary-like bones in the hesperornithines) with toothy maxilla and dentaries. Evidence from bone texture shows that likely had keratinous beaks at the tips of their jaws, and either feathery toothed jaws or pliable, skin-like rhamphotheca further back. Since both major lineages of avians lack teeth, it's likely their common ancestor was also fully beaked, so teeth must have been lost for good in the bird lineage shortly after Ichthyornis diverged. Interestingly, studies of ichthyornithines and hesperornithine bone structure shows that they likely had "compound rhamphotheca", and this may have been the ancestral condition for modern birds (Heironymous & Witmer, 2010). While the quintessential bird beak is made up of a single keratin sheet covering the jaw, in species with compound beaks, the keratin is arranged in discrete plates on the jaws. This can best be seen in some modern seabirds like the Albatross.

Unfortunately, in interesting taxa like Hollanda, Gansus, and Patagopteryx, the condition is unknown. However, we can use parsimony and phylogenetic bracketing to try and come to a reasonable guess. Most studies find these three to be ornithuromorphs more primitive than the hesperornithines and Ichthyornis. Given the condition in Ichthyornis, it's most likely that Archaeorhynchus evolved its toothless beak independently of more advanced birds, most of which have toothed upper and lower jaws with beaked tips in the grade between Archaeorhynchus and Aves. While the three intermediate birds may well have lost some or all of their teeth independently again, it's probably more parsimonious to assume that like hesperornithids, hongshanornithids and songlingornithids, they were either fully toothed or had beaks restricted to the tips of the jaws.

[Image: Cassowary chick by Michael Thirnbeck, from Flickr. Note the horny beak only covers the tip of the bill, leaving the nostril surrounded by more skin-like tissue. Thanks to meidamon over at DinoForum for finding this and other pictures illustrating beak anatomy.]

So, to rephrase an old fallacy, what use is half a beak? Many Mesozoic coelurosaurs had teeth only on the upper or lower jaw, and most researchers have assumed that edentulous = beaked (see for example Zanno et al., 2009). But "beaks" are more complex than simple sheathes of keratin covering toothless parts of the jaw. As anatomist Larry Witmer has explained (in print as well as on the DML), rhamphotheca can consist of everything from solid, hard keratin (which, obviously, is a bit antithetical to tooth growth and replacement) to softer, pliable, barely mineralized tissue. For example, it's a general rule of thumb that the keratin rhamphotheca never completely encloses the external nares, meaning the nostrils of a bird are never encased in keratin. This is most obvious in species that have a cere, a prominent fleshy part of the posterior rhamphotheca found in pigeons, parrots and hawks, among other birds. But in many other birds (especially aquatic forms like ducks and gulls), the nostrils do appear to erupt from mid-bill. What's going on?

[Image: Duck skull by ~Oryx gazella~, from Flickr. Note that only the tip is fully keratinized.]

Basically, the "beak" of a duck (and many other birds) is only really solid towards the tip. The broad bill of a duck is, laterally, fairly soft, and made of rhamphotheca that is only lightly mineralized. Essentially, it's mostly toughened skin (this is why ducks and other anseriforms are particularly prone to bill injuries). In the kiwi, the nostrils don't just erupt from the "beak", they occur at the very tip. Again, the bill of a kiwi is not highly keratinized, but rather made up of soft, pliable integument full of sensory organs (Martin et al., 2007).

So, our mysterious half-beaked birds may have had some cere-like tissue covering the upper portion of the toothed bill, while the lower portion contained more keratinized rhamphotheca. Perhaps the upper jaw had a small keratinized tip wedged between the front teeth, as seen in toothed pterosaurs like Rhamphorhynchus and Pterodactylus. Or maybe the half-beaks of some of these birds contained little to no keratin at all. As the kiwi shows, it's not always necessary for all food-aquisition behaviors to have a beak or teeth.

Hopefully, this rough guide can also serve as a reference for artists, many of whom are a bit over-eager to add a beak to anything that is called a "bird." While a wide range of rhamphotheca like structures may have been present on Mesozoic birds, it wasn't necessarily present on all of them, and many probably looked a bit strange compared to the simple, smooth yellow bills of modern birds.

References
* Heironymous, L. and Witmer, L.M. (2010). "Homology and Evolution of Avian Compound Rhamphothecae." The Auk, 127(3): 590-604. doi: 10.1525/auk.2010.09122
doi: 10.1525/auk.2010.09122
* Martin, G.R., Wilson, K.-J., Wild, J.M., Parsons, S., Kubke, M.F., et al. (2007). "Kiwi Forego Vision in the Guidance of Their Nocturnal Activities." PLoS ONE, 2(2): e198. doi: 10.1371/journal.pone.0000198
* Zanno, L.E., Gillette, D.D., Albright, L.B., and Titus, A.L. (2009). "A new North American therizinosaurid and the role of herbivory in 'predatory' dinosaur evolution." Proceedings of the Royal Society B, 276(1672): 3505–3511. doi: 10.1098/rspb.2009.1029.