The Enfluffening

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,

Woolly woolly

A mess of speculation: An ankylosaur not unlike a club-tailed sauropeltine nodosaur wityh enormous spines on the club, the nasal openings elaborated into paired prorhisces not unlike the tapir’s snout, and of course fuz, fuzz, everywhere.

or sauropods,

Dream the Impossible Dream

A basal titanosauriform shows that even scaly sauropods can “shine.”

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.
Lingham-Soliar, T. 2011. The evolution of the feather: Sinornithosaurus, a colourful tail. Journal of Ornithology 152(3):567-577. [pre-press copy of the paper, dated 8 Nov 2010 here]
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.
Prum, R. O. 1999. Development and evolutionary origin of feathers. Journal of Experimental Zoology 285:291-306.
Prum, R. O. & Brush, A. H. 2002. The evolutionary origin and diversification of feathers. The Quarterly Review of Biology 77(3):261-295.
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.

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24 Responses to The Enfluffening

  1. Enter Foth showing that the preservation of feathers will typically make them look simpler structured than they were…… ;)

  2. saurian says:

    Excellent post – there does seem to be a few more voices of reasoning with this debate now. I am glad that this is happening since it did seem for a while that one could be considered a heretic for daring to suggest that dinosaurs were not “enfluffened” – and you have put it so much better than I could have done!

  3. I must say that I am not as enraged (exaggerating here) as some are about the enfluffing trend. It is partly (and is partly intended to be) a warning shot across the bow of the nay-sayers’ fleet. We’ve seen this with regards to habitat, locomotion, metabolism: there is always a crowd out that the implicitly turns the absence of evidence into evidence of absence, then cries foul when their logic is questioned. Sometimes, you need a crowbar to open their minds, and massive enfluffing is such a crowbar.

    So yes, some people overdo it, but the vast majority seems to know very well that much of what they are doing is in the 1% chance range. But hey, the “classic” view often is just as (im-)probable, so why not show all sides of the debate?

    My suggestion for palaeoartists is that if they work with digital stuff, and thus can produce variations of an artwork easily, they should always make several versions: a “likely” one, a “only positive evidence” one, and a “anything goes” one. Obviously, the “anything goes” one must be what I term 1-P (possible). The conservative, “only positive evidence” one should be 2-P (possible, plausible), and the “likely” one should be 3-P (possible, plausible, probable), if we have sufficient evidence.

    • It is my silly intention in the near future — i.e., in the bare-bones concepting stage — to illustrate an animal in progressive layers to show potential variation in structure and what leeway is given to various parts. Muscles, for example, would show the “skinny” rump, and the fatter, more crocodilian but also avian rump (it amazes me how I could have been so blind to this topic that you, Currie and Persons have discussed in the past, that birds and crocs have these amazing “butts” but we drew the thin form anyways, perhaps due to Paul’s influence); skin would be squamous, “fuzzy,’ or feathered, depending on taxon chosen for the tack, and so on. I would almost certainly be picking an oviraptorosaur, which gives ME a warning to reconstruct outside my comfort zone and pick something much more noticeable, and perhaps ambiguous on integument. A small carnosaur, perhaps, or ornithischian. Or, you know, a “prosauropod!”

  4. Mark Witton says:


    Just to point out that the skin impressions of other ceratopsids were not ‘pointed out’ to me, but actually were the focus of a lot of discussion in my article on the _possibility_ of fuzz in Pachyrhinosaurus. I agree that we need to be cautious with reconstructing integuments, but I also think we are over-reliant on the phylogenetic bracketing, and that other factors – palaeoclimate, lifestyle, etc. – should be considered in palaeoartistic works. My fuzzy pachyrhinosaur reconstruction endeavoured to incorporate these factors, as well as phylogenetic bracketing, as much as possible.

    • Sorry, I meant to imply that the discussion following your illustration included the structures being brought up. It would be erroneous of me to say that they were used to contradict your arguments in that post. As I commented in that thread, the idea has possibility, and we cannot directly counter it given its bounded reasoning — but similarly, the output of your argument is equivocal when using inference from other taxa. If we presume that the extensive impressions of squamous skin in hadrosaurs, including taxa that are almost certainly very closely related to those on the North Slope (“Edmontosaurus sp.”) are the rule and not a suggestion, we can cast extensive doubt on the viability of woolly ornithsichians “giants.” Even presuming the use of woolly mammals and their less woolly congeners, it may be useful to note that for woolly arctic and alpine animals, the same growth of hair can occur in animals in more temperate environments (for example, woolly Mammuthus primigenius at La Brea in southern California, while not as “temperate” as today, far warmer than the neararctic of its “normal” range). It seems more parsimonious then to argue that the presence of “woolly” “dinofuzz” on large neararctic ornithischians (or even small ones!), even for the purpose of insulation, is not as tenable as one without. Perhaps, instead, we can speculate on the possibility of non-“fuzzage” ornithischians to adapt to the cold before we coat them in wool. As I said in reply to your post on your blog, your idea is not without merit; I merely think that the speculation to be equivalent to other potentials we’ve not attempted to illustrate yet. Perhaps because it is too sexy to illustrate otherwise.

      • Mark Witton says:

        But, as we discussed previously, hadrosaur skin impressions are unusually common, and were therefore atypical, at least in terms of their resistance to decay, among dinosaur integuments. They may not, therefore, be great models for other dinosaurs. Or they could be. We don’t know, because our skin datasets are poor outside of hadrosaurs, even for non-hadrosaurian ornithopods. I do agree that fuzzy hadrosaurs are harder to rationalise, however.

        And yes, I agree that fuzz is only one means for insulating dinosaurs, and said so in my post. Fatty tissues was another. I stayed away from these, however, because of John Conway’s overweight Parasaurolophus.

        One last question: are M. primigenius known from La Brea? I don’t think they made it that far south. Other mammoths are known from there, certainly, but not the woolly kind, to my knowledge.

        • I wonder that the form of preservation tends to favor hadrosaurs for skin impressions over ceratopsians, implying a different ecological regime. Ceratopsian skin impressions seem much more fragmentary than hadrosaurs, while we get body mommies of hadrosaurs and ankylosaurs. Perhaps, rather, ceratopsians are more montane/upland, while the others favor lowland/flood plain domains as a matter of course, so even associations between the two result in different preservation regimes: in situ silt riverbanks and lakeshores preserve better than washed up mudstone carcasses, a case Horner makes several times when it comes to crappy versus excellent preservation in Hell Creek ceratopsians (intact skulls tend to be found in sandstone facies, but not mudstones).

          I may be confusing prmigenius with finds of possible mammoth hair of long form from the tars at Rancho La Brea. Will be double checking this. It may be sloth hair, but still seeming rather long. It looks like range extants do not follow the coast, though cross-overs between columbi (“sparse”) and prmigenius (“hairy”) appears to occur. I will get back on this point, and retract my earlier statement if need be. I should also make the statement, in my own defense, that extremely hairy animals exist in temperate environments, such as extant sloths, but that won’t defend me from being wrong about mammoths.

          • Mark Witton says:

            Hadrosaur skin impressions seem to be common because of their inherent structure, not because of a taphonomic effect. At least, this is the conclusion Davis (in press) has found:

            Click to access app20120077_acc.pdf

          • Yes, the “hadrosaur skin is more cohesive” argument, or “tougher.” Maryańska and Osmólska’s, and Davis’ arguments aside, a substantive survey of ceratopsian skin fragments has not, to date, occurred. It seems that investigating the less frequent impressions, along with taxa like sauropods, would be useful to this. It would also be interesting to focus on why, if hadrosaurs without dermal armor, can have denser, tougher, thicker skin than, say, ankylosaurs. I’m not sure something intrinsic to hadrosaur skin is responsible, though it is certainly interesting to investigate in greater depth!

  5. saurian says:

    Preservational bias (or the lack of it) is another issue that is often forgotten about. Feathers and fuzz are little more than carbonized imprints at the end of the day and it is amazing that they fossilise in sedimentary rocks in the first place. Having said that, some of the scale impressions we have are so perfect, so well preserved that it seems almost impossible, if indeed integument was present on a carcass, that there would be no trace remaining. I would quantify that, however, by suggesting that I would expect more feather/fuzz impressions to start turning up simply because more and more researchers will be looking for them now on taxa where they were not considered to be present in the first place.

  6. I’ve heard some comments that the Triceratops mummies have quills knobs after all, though.

    If not the result of preservation issues (which appearently are more severe than previously thought), then ornithischians are frankly one of the most metabolically bizarre animal clades that have ever existed, giving up insulatory integrument for scales.

  7. Balaeniceps says:

    Bitterly disappointed you paleontologists haven’t perpetuated this thread.

    If we take your argument at face value, we have to believe that its quite likely endothermy and fluffy integument evolved many times from stem pterosaurs to assorted ornithischians to coelurosaurs with lacuna in between.

    • Forgive me for being confused, but are you saying we SHOULD argue that multiple instances of “fluffy” integument occurred, and just just but also that with ti comes endothermy, not even that endothermy arises separately? The issue isn’t about multiple arising cases of “fuzz” but its loss. One of the mere persistent arguments out there is that at a particular size (perhaps rhino or so) integument ceases to be “fuzz” and is squamous; “fuzz” arises once in dinosaurs, and is lost in various lineages for which squamous integument is known. Alternately, “fuzz” arises multiple times but is lost in each lineage among dinosaurs. In either case, we can extent the origin of “fuzz” back to pterosaurs, but it is not necessary. In none of these cases is endothermy required to coincide with “fuzz:” histological sectioning of ornithischian and theropod long bones implies, rather, that they were endothermic, and this doesn’t tend to vary. Mark Witton has a great point, as has Fiorillo and the Richs before him — and notes this on his blog — that animals that crossed the Arctic or Antarctic Circles almost certainly must have been ectothermic, and this may have included ANY ornithischan or theropod, and by inference also sauropods.

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