You're Doing It Wrong : Dino Foot Scales

Above: Our subject matter.

It's often said by those who support a strict phylogenetics-based system of naming life that it's only by restricting well-known names from neontology (the study of modern organisms) to crown groups can we avoid making unjustified assumptions about members of stem-groups.

These kinds of unjustified assumptions have been rampant in the history of studying stem-birds. Archaeopteryx has traditionally been depicted, incorrectly, with a reversed hallux, and occasionally even with beak-like structures, simply because it's a "bird", and those are features all birds have. Except Archaeopteryx is not a true "bird", it's a stem-bird, more closely related to birds than to any other living animal group, but not a member of the group that includes all modern birds. It's fair to assume that an extinct member of the duck lineage, like Vegavis, had a bill, but that's not necessarily so for, say, Patagopteryx, despite the fact that it is usually referred to as a "bird".

Modern bird feet, by Philip Henry Gosse, 1849, public domain. Note overlapping scutes on
the top surfaces, and pebbly, polygonal reticulae on the bottom surfaces.

Most paleoartists have absorbed these kinds of warnings, and do a good job of avoiding obvious errors based on typology, the assumption that all species in a certain "type" share "key characteristics." But there are some typological memes in the bird lineage that are more pernicious, possibly because their actual evolution is something most artists don't think about very much.

Take, for example, the bird-like scutes that are almost universally illustrated covering the tarsus (upper foot/lower hind limb) of dinosaurs. Is there any evidence that these were actually present in any given group of non-theropod stem birds? Well... no. Not that I'm aware of (if you know differently, please comment!).

Sinosauropteryx prima with tarsal scutes.
Image by Matt Martyniuk,  licensed.

I'm not sure when this meme began, and if it's related to the Dinosaur Renaissance when the link between birds and dinosaurs was re-established. Looking at some Charles Knight paintings, such as his famous "Leaping Lealaps", it appears that the feet of his theropods were scaled based on modern lizards (more on the differences between lizard scales and other types of "scales" below). Bakker's influential early restoration of Deinonychus does not include any obvious scutes on the feet or tarsus. Mark Hallet, on the other hand, did include what look like oblong bird-like scutes on his theropods. At any rate, it's hard to deny that "bird feet" are typical of almost all modern reconstructions of dinosaurs, including my own, and are not limited to theropods. Bird-feet are often restored on ornithischians and even pterosaurs.

Of course, like many paleo-memes that developed during the 1980s, the main idea seems to be using this as a flourish to make otherwise scaly dinosaurs seem more bird-like. And thanks to skin impressions, we know that many dinosaurs had scales, right?



The problem here is that people tend to lump any scale or scute-like dermal structure that's not a hair or a feather into the category of "scale", despite long-documented and rather drastic differences in their structure and development.

Tarsal scutes

Tarsal scutes of a seriama. Photo by Matt Edmonds, licensed.

Let's survey the body covering of modern birds. Birds actually have three basic types of integument: feathers (of course, though they come in a variety of forms which themselves develop differently), reticula, and scuta.

Scuta are the broad, flat, semi-overlapping "scales" on the top of the tarsus and the toes. The development of these structures is controversial, but as many of you may know, they might in fact be derived from feathers themselves, and not related to the true scales found in lizards and snakes at all (Dhouailly, 2009). Rather famously, the scuta of bird feet can easily be converted partially to feathers in experiments (the tips become feathery, while the anterior portions stay scute-like) and in natural mutations, as in some chickens.

Skin impressions from the foot of Saurolophus osborni, showing
only reticulae. From Bell 2012, licensed (CC BY).

More interestingly, in mutations where the scuta become feathers, they specifically become remiges (wing feathers) or remix-like feathers. It appears not to be possible to induce the reverse (feathers on the body to become scuta). Researchers like Dhouailly (2009) have suggested that these scuta might be homologous with the hind-wings feathers of basal paravians like Microraptor, and that the ancestral condition prior to the evolution of scutes from foot remiges as a fully- or nearly-fully feathered foot. The only non-feather skin impressions from non-avialan maniraptorans that I know of come from the "Dave" specimen of Sinornithosaurus. This preserves reticula (see below) on the plantar surface of the digits, but not scuta. It's very possible the rest of the foot was covered in feathers, with reticular "pads" for walking (think the foot pads of dogs). Skin impressions from hadrosaurids like Saurolophus demonstrate that bird-like tarsal scutes were absent, and that the entire surface of the metatarsus and digits was covered in reticulae (see photo above).

(The bird-foot meme is so ingrained that I found some blogs reporting that these specimens actually had tarsal scutes, even speculating on their purpose, despite the paper clearly contradicting the idea!)

Reticula, or "Tuberculate scales"

Feet of a Little Egret. Photo by J.M. Garg, licensed.

Reticula, often referred to as "tuberculate scales", are the bumpy structures on the plantar side of the foot. These are also, famously, the type of "scales" found in just about all non-feathered stem-bird skin impressions. And here's the kicker--these have very little to do with the "scales" of squamates or even crocodiles.

In modern birds, the reticula, unlike feathers or scutes, do not form from placodes. Unlike lizard scales, scuta, and feathers, they're made not of beta-keratin, but alpha-keratin (the same as mammalian hair and amphibian 'warts'). The reticulae do start with an overlying beta-keratin layer that is shed during development. While they don't form from placodes, they appear to be similar to the pre-placode stage of feather formation. Reticula apparently never morph into scales in nature (I suppose ptarmigans start with naked skin on their feet?), this can be induced in the lab. Dhouailly suggests that, given the weight of the developmental evidence, reticula appear to be feathers which are arrested in a very early stage of development.

You read that right--tuberculate "scales" are probably modified feathers! So, those fossilized hadrosaurid mummies covered in "scales"? It's possible or even likely that they had feathered ancestors, and evolved in such a way to stop the development of feathers early on, instead yielding a fine, pebbly skin covering derived from old feather genes.

Dhouailly, in her phylogeny of amniote skin coverings, supposes that both feathers and crocodilian scutes evolved from a hypothetical, primitive, amphibian-like granulated skin covering consisting of alpha-leratin, which also have rise to mammalian hair. Tuberculate scales and bird scuta are suggested to both be derived from feathers secondarily, with reticula only being superficially similar to the ancestral, 'warty' condition. Dhouailly shows non-theropod dinosaurs in her diagram to have croc-like scutes, but most reported skin impressions from dinosaurs actually show reticula instead. The exception may be the large osteoderm scutes of thyreophorans and the reported larger scute-like scales and croc-like belly scales of Triceratops, though given the variety in bird "scales", these could easily be feather derivatives as well. In all cases of dinosaurs with osteoderms, they seem to be interspersed among tuberculate scales the same way the scutes of bird feet are, rather than being arranged in neat rows bordered by bare skin as in crocs.

Dino Feet
So, back to the main premise here: what does this mean for artists? The fact that tarsal scutes appear to be derived from feathers, and from pennaceous feathers in particular, suggest they are probably restricted to at most Tetanurae, given the current phylogenetic bracketing. However, numerous maniraptoran fossils preserve fully-feathered hind limbs, including toes but probably excluding foot pads, which were covered in reticulae (e.g. Sinornithosaurus). The most basal stem-birds with evidence of tarsal scutes are Yanornis (Zheng et al. 2013) and Concavenator, with some fluffy-footed forms in between, suggesting that once developed, the genetic 'switch' between feathered and scutted feet may have been highly variable, as it is in modern birds.

In feathered species, the feathers on the bottom of the foot seem to have been developmentally changed to reticula for better traction/less damage to feathers. In some large species, fossorial species, semi-aquatic species, etc., the reticula probably spread to other parts of the body. The general feather-derived skin covering also could have produced the various other kinds of skin covering, like psittacosaur "quills" (Dhouailly, 2009).

In the end, while the paleo-art meme of scuty tarsals in non-theropod stem-birds was invented to make the link between dinosaurs and birds more obvious, it turns out that it may actually be too bird-like for many of them. Hopefully, another unjustified assumption about the stem-group made by copying a trait from the crown can go the way of the ornithischian.

As for the evolution of scales and feathers and the different kinds and patterns of skin coverings in stem-birds, at the very least it should be clear that a simple dichotomy of scales vs. feathers is about as far from reality as you can get. Feathers could become "scales", scale-like scutes could become feathers, and novel structures of all kinds can appear, derived from any of them (like the beards of turkeys, which are derived from alpha-keratin and are not true feathers, but some kind of derivative like tuberculate scales [Sawyer & Knapp, 2003]). Each different lineage of stem-birds may have been doing very different things with the very adaptable basic feather or feather-like structures made possible by their crazy dermal genes.

UPDATE: As I figured I might, I overlooked a major data point here--Concavenator (thanks to Tom Parker in the comments for pointing this out!). Concavenator is an interesting case that shows these type of things are not always cut and dry, since it does preserve scutes on the tarsals and toes, and scutes on some other parts of the body including the underside of the tail.* So, if Dhouailly 2009, Zheng et al. 2013, etc. are correct about the development and evolution of tarsal scutes from feathered feet, where does this leave Concavenator? A few possibilities: one, the developmental data is wrong, and tarsal scutes are precursors to pennaceous feathers rather than the other way around. Two, the tarsal scutes of Concavenator are not homologous with those of birds. Three, Concavenator evolved from ancestors with feathers or feathered feet. I find the third option to be the most likely right now. Notoriously, Concavenator was described with structures resembling quill knobs on the arm, which in eumaniraptorans anchor the sort of pennaceous feathers developmental data suggests are the precursors of tarsal scutes. While the identification of these knobs has been challenged, the fact that tarsal scutes exist in this species may be further support for the idea that Concavenator did indeed have remixes (or that its ancestors did).

* I originally wrote "reticulate scales on the rest of the body", but this is not correct--scutes, not reticulae, are preserved in impressions other than the pes.

Coming real soon, much more on a particularly cool branch of stem-birds, in the form of the amazing new book by Mark Witton...

References

Bell, P. R. (2012). Standardized terminology and potential taxonomic utility for hadrosaurid skin impressions: a case study for Saurolophus from Canada and Mongolia. PloS one, 7(2), e31295.

Dhouailly, D. (2009). A new scenario for the evolutionary origin of hair, feather, and avian scales. Journal of anatomy, 214(4), 587-606.

El-Sayyad, H. I., Fouda, Y. A., Khalifa, S. A., AL-Gebaly, A. S., & El-Sayyad, O. K. (2013). Studies on epidermal appendages of chick embryos. Int. J. Curr. Microbiol. App. Sci, 2(5), 315-327.

Sawyer, R. H., & Knapp, L. W. (2003). Avian skin development and the evolutionary origin of feathers. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 298(1), 57-72.

Zheng, X., Zhou, Z., Wang, X., Zhang, F., Zhang, X., Wang, Y., ... & Xu, X. (2013). Hind wings in basal birds and the evolution of leg feathers. Science,339(6125), 1309-1312.