As we dig deeper into the past and our investigative techniques broaden and our perspectives with it, biological aspects of ancient life become more and more interesting. Of the most visual of these is the presence of non-scaly integument in dinosaurs. We’ve known of feathered theropod dinosaurs for a while, but not so long ago an ornithischian was discovered with unusual, atypical integument, a psittacosaur from China with long “quills” extending from the base of the tail (Mayr et al., 2002). This was followed by another ornithischian with “quills” (Zheng et al., 2009), but this one was covered in fine, filamentous structures. Theropod dinosaurs have already been recovered with this filamentous structure, especially Sinosauropteryx prima (Chen et al., 1998) which has been affectionately called “dinofuzz.” Subsequently, the stuff has shown up on more theropod dinosaurs, some more primitive seeming than Sinosauropteryx. Even more curious is the presence of similar structures in ornithischians, and their relation to the “fuzzage” of pterosaurs — being affectionately termed “pterofuzz” [n1].
Several scientists have gone out to try to classify these structures:
1. Prum (1999) classified the structures of avian feathers by their development, and along with Alan Brush in 2002 developed a scheme by which theropod integument evolved in keeping with feather ontogeny. I discussed this in more detail here and here.
2. Xu et al. (2009) threw fuel on the fire of chaos by qualifying variation of preserved integumental structures in dinosaurs by classifying structures by their form, rather than an ontogenetic scheme.
3. Lingham-Soliar (for example, 2011) argued that the structure and nature of these structures was entirely mistaken, taking up the “BAND”wagon and arguing as many others had (detailed here) that the integument either could not represent feather-related structures, or if they did they were indicative of avian affinites — and that the animals could not be dinosaurs, as if they were mutually exclusive. Foth (2012) also disagreed, but for different reasons, implying that some aspects of these schemes were potentially mistaken due to preservation biases: The filaments, rather than representing natural structures by themselves, were the remnants of more complete structures, filamentous bundles or the raches of slender, slight feathers, based on taphonomic studies of extant bird specimens. Indeed, Currie & Chen (2001) provided support that the “filaments” in Sinosauropteryx prima were not merely single strands, but bundles of such, basally branching, or even that they might have been arranged in vanes along the thicker, central structure.
But perhaps more interesting than their form or identity is their presence: These structures are present in a wide range of archosaurs, from pterosaurs to dinosaurs. In their distribution, however, there are gaps. No known saruopodomorphan fossil has them, while some sauropods are known to possess scaly skin, have embedded dermal ossicles in the skin or, in the case of some (e.g., Agustinia ligabuei, Spinophorosaurus nigerensis) there are enlarged dersmal spikes. Some ornithischians have peculiar integument, but they are fairly peculiar: Tianyulong confuciusi, a heterodontosaurid, and an unnamed, possibly unique specimen attributed to Psittacosaurus sp., both with quills but the former with “fuzz.” Other ornithischians have dermal ossicles, dermal armor in the form of spikes or plates or such, such as Ankylosauria and Stegosauria, or with evidence that the body was generally covered in “normal” scales (Ceratopsidae). This leaves one to surmise that “dinofuzz” may be present for all Dinosauria, at least basally, but was lost subsequently in multiple lineages, and many of these are fairly large-bodied or utterly gigantic. With recent work highlighting the effect of mammalian hair distribution relative to body mass and surface area, and how even large elephants have hair (as do hippos and rhinos) despite their mass (Myhrvold, Stone & Bou-Zeid, 2012), we realize we’ve merely scratched the surface when it comes to inferring integument for most of dinosaur: It’s not so cut and dry.
Enter Mark Witton, whom in conjunction with the All Yesterdays project of friends John Conway, Memo Koseman and Darren Naish has speculated on the integument of ceratopsids. In one thoughtful piece, Witton suggested that the cold climate of the North Slope of Alaska, in which the ceratopsian Pachyrhinosaurus lakustai has been found, along with hadrosaurs and tyrannosaurs, would have been conducive to promoting dinosaurian “fuzzy” integument. They would be woolly rhinosaurs, would be epic … but unlikely. We have direct evidence, as had been pointed out to Witton, that ceratopsian skin from Dinosaur Park in Alberta showed squamous skin. The same is true of hadrosaurs, which while also present on the North Slope, have representatives of different taxa (the lambeosaurines Lambeosaurus magnicristatus and lambei, Parasaurolophus walkeri and Corythosaurus casuarius, the saurolophines Brachylophosaurus canadensis, Saurolophus angustirhinus and osborni, the edmontosaurine Edmontosaurus annectens, the “kritosaur” Gryposaurus notabilis) that show skin impressions (following Bell, 2012).
Thus is becomes questionable that these taxa would have been “fuzzy.” In a conversation with Brian Switek, I through out the term “enfluffen” [n2] when it came to the trend towards illustrating taxa otherwise perceived to be “naked” (i.e., scaly) as covered or partially covered in “dinofuzz.” Brian took off with that term, and I kinda like it myself, but there was a warning in that: There is now a trend toward illustrating any and all taxa that might conceivably be “fuzzy” as though they were, and one can wag a finger at Witmer’s “Extant Phylogenetic Bracket” — as some have done — as though to support their argument. In some cases, I detect an adverse reaction to use of the EPB, one which seems to suggest that the users are misunderstanding it. To clarify:
The EPB involves degrees of inference. A first level inference is one in which NO speculation is required to determine the presence or absence of a structure, and in this the lack of that tissue in the fossil is meaningless; Witmer (1995) directly used the inference of eyeballs in tyrannosaurs, and on this it is hard to disagree. A second level inference is one in which a structure appears in a related animal, but can be determined not to exist in other, more distantly related animals, but is unknown in the given animal; in this, the presence or absence of certain types of integument are good examples, and Witmer uses the presence of feathers in Ichthyornis as an example (the EPB is equivocal: birds have ’em, crocs lack ’em). Finally, a third level inference is one in which speculation of the presence of a structure follows further speculation on the relationship of structures; and Witmer uses the issue of “cheeks” in ornithischians as an example, and one in which I’ve expounded upon quite extensively here.
Integument reconstruction for dinosaurs involves the second level inference, but with direct preservation of some integument types within Dinosauria, we can reduce the degree of speculation towards birds-like dinosaurs having feathers (direct preservation) or the absence of “fuzz” in hadrosaurs (direct preservation). We can, in fact, make more specific inferences by “bracketing” those taxa for which integument of a form is known. And for dinosaurs, several ornithischian clades are known to have scaly integument at their terminal ends, in which the largest species are known, while non-scaly integument is known for the basal elements of some of these clades, which are represented almost exclusively by small species. This might be telling. The largest theropod known for which integument can be determined would be Tyrannosaurus or Tarbosaurus, clades for which specimens of possible species have been attributed showing scaly skin, but of uncertain position on the body; smaller than that, though, is Yutyrannus huali (Xu et al., 2012) which seems to display “fuzzage” over parts of the body, much like its smaller relative Dilong paradoxus. With small compsognathids having skin impressions (Chen et al., 1998), it is quite likely that all of Coelurosauria was at least “fuzzy” and bore stage I feathers (per Prum & Brush, 2002), if not bearing stage II or even III feathers. If these structures are homologous with those of pterosaurs and basal ornithsichians for which they are known, then it is possible many clades of dinosaur were so integumented. And if that is the case, it is possible, regardless of the skin impressions and integumental structures like ossicles present, that we’d have “fuzzy” ankylosaurs,
even stegosaurs and, as Witton’s illustration portends, ceratopsians. Why, the sky’s the limit.
This is a warning rattle. The enfluffening is both an elaboration of what we know, and a caution for not getting carried away. Moreover, it is about being careful in your speculation to proscribe it as such. I point to the studies and technical works involving this stuff, and hope at least that the artists follow through and look more carefully through the lens of speculation (used, as Witmer, Conway et al., and others do, without pejorative).
[n1] The terms “dinofuzz,” “pterofuzz,” and even “fuzzage” — itself derived from “plumage” and “pelage,” terms used for avian feathers and mammalian hair, respectively — are informal, and no scientists have attempted to formalize these terms. “Pterofuzz” was formally named by Kellner as “pycnofibres,” but their nature as potential bird-like stage I “feathers” is a matter of debate.
[n2] A minor aside: Brian has used the term on his own, though as “enfluffle.” I do not think the difference here is significant to correct anyone, merely that it departs from my original use, and is adequate to explain the term. If you Google the first term, or the second, you should get the same kinds of discussion, so that’s fine. The term “enfluffen” exists outside of this discussion, however, where it merely means “to fluff up,” as in pillows, baking, padding a coversation, etc. I’m enfluffing this note, for example.
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.
Chen P.-j., Dong Z.-m. & Zhen S.-n. 1998. An exceptionally well-preserved theropod dinosaur from the Yixian Formation of China. Nature 391:147-152.
Currie, P. J. and Chen P.-j. 2001. Anatomy of Sinosauropteryx prima from Liaoning, northeastern China. Canadian Journal of Earth Sciences — Revue canadienne des sciences de la Terre 38(4):1705-1727.
Foth, C. 2012. On the identification of feather structures in stem-line representatives of birds: Evidence from fossils and actuopalaeontology. Paläontologische Zeitschrift 86:91-102.
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Mayr, G., Peters, D. S., Plodowski, G. & Vogel, O. 2002. Bristle-like integumentary structures at the tail of the horned dinosaur Psittacosaurus. Naturwissenschaften 89(8):361–365.
Myhrvold, C. L., Stone, H. A. & Bou-Zeid, E. 2012. What is the use of elephant hair? PLoS ONE 7(10):e47018.
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Witmer, L. M. 1995. The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. pp.19–33 in Thomasen, J. J. (ed.) Functional Morphology in Vertebrate Paleontology. Cambridge University Press, New York City.
Xu X., Wang K.-b., Zhang K., Ma Q.-y., Xing L.-d., Sullivan, C., Hu D.-y., Cheng S.-c. & Wang S. 2012. A gigantic feathered dinosaur from the Lower Cretaceous of China. Nature 484:92–95.
Xu X., Zheng, Z.-t. & You H.-l. 2009. A new feather type in a nonavian theropod and the early evolution of feathers. Proceedings of the National Academy of Sciences of the United States of America, Philadelphia 106(3):832-834.
Zheng X.-t., You H/-l., Xu X. & Dong Z.-m. 2009. An Early Cretaceous heterodontosaurid dinosaur with filamentous integumentary structures. Nature 458:333–336.