by

This year has seen the discovery of two big deal dinosaur specimens. At least they are a big deal in regards to dinosaur integument and, possibly, metabolism.

First off from a few months ago we had the announcement the theropod Yutyrannus hauli, the “beautiful feathered tyrant.”

Xu, X., Kebai, W., Ke, Z., Qingyu, M., Lida, X., Sullivan, C., Dongyu, H., Shuqing, C., Shuo, W. 2012. A Gigantic Feathered Dinosaur from the Lower Cretaceous of China. Nature. Vol.484:92-95

This was not just a single fossil, but a collection of three fossils (one might be tempted to call it a family group, but that would only be speculation). As with all other dinosaur fossils that have been found to have filamentous integument, these guys come from Liaoning, China. They are suspected to have come from the Jehol Group in the Yixian formation. I say suspected because the complete three specimen set was a purchase from a fossil dealer, an all too common occurrence for Chinese fossils. As such the provenance information is unknown. A lot of Chinese fossil dealers don’t like to give away the location of their find due to the potential loss of other profitable specimens. This current trend in China is a good example of what happens when capitalism comes into play with fossil collecting (something that the U.S. has been mostly, but not entirely, able to avoid). So it is currently uncertain whether these fossils are from the Yixian. However given that all the others guys are too it is probably a good bet. Given the sketchy nature in which many Yixian fossils are collected, coupled with the possibly large consequences of the find, one should naturally be skeptical of the fossil. Had it been one individual on multiple slabs I would question its validity as a real thing. However since Y.huali is known from three individuals, and the filaments seem to follow a consistent pattern around the body (compare that to the helter-skelter nature of Tianyulong‘s preservation), forgery seems unlikely. These guys are probably the real deal. This has some potentially far reaching consequences to interpretations of Late Cretaceous coelurosaurs and the Jehol Biota itself (more on this in a bit).

The second announcement came just a few weeks ago. This was the discovery of a potentially new, miniscule theropod from Bavaria Germany.

Rauhut, O.W.M., Foth, C., Tischlinger, H., Norell, M.A. 2012. Exceptionally Preserved Juvenile Megalosauroid Theropod Dinosaur with Filamentous Integument from the Late Jurassic of Germany. PNAS Early Edition:1203238109v1-201203238.

The specimen is exceptionally well preserved. So well preserved in fact that it actually looks like a plastic toy. While this degree of preservation warrants importance all its own, the main interest behind this new guy—dubbed: Sciurumimus albersdoerferi (Albersdörfer’s squirrel mimic)—is the apparent presence of filamentous integument on the body coupled with its apparent placement among much more basal theropods. This discovery has far reaching consequences for theropod integument interpretations. Note: As with Y.hauli, Sciurumimus albersdoerferi was also purchased from a private collector. I don’t suspect forgery here either as this was in Germany, where fossil dealing is neither a big problem nor a lucrative business. The exceptional detail on the specimen would also require a substantial amount of theropod knowledge to pull off. Anyone having that amount of knowledge is more likely to be a real paleontologist than a get rich quick forger.

The filamentous brouhaha

As I mentioned above, the big appeal of both specimens was the presence (or apparent presence) of filamentous integument. I am purposely avoiding the use of both “feathers” and “protofeathers” in this post as both of these are loaded terms. They assume that these structures had something, if anything, to do with the formation of real feathers. This has been a current trend that I have seen both online and in the literature. It is a trend that I think has skewed many interpretations of features found on or near fossil specimens (e.g., see Ortega et al. 2010) . The fact is that we don’t know for certain that what we are seeing has anything to do with feathers. Both of Y.hauli and S.albersdoerferi preserve what Prum (1999) referred to as stage I feathers, or basically long shafts with no branches. This most basic hypothetical precursor is not all that descriptive. Basically any long filament falls under stage I feather territory, including mammalian, insect, and arachnid hairs. Even the dorsal spikes on many iguanian and gekkotan lizards have the potential to fall under this category, especially when all one has to look at is a 2D smashed fossil.

That theropods were on the line that lead to birds does suggest that these filaments had some role in the evolution of feathers, but even that train of thought may be misleading. Sawyer et al. (2003) were the first to point out that not every filament on a bird is a feather. In particular, Sawyer looked at the filaments that compose the “beard” of turkeys (Meleagris gallapovo). Despite being filamentous, hollow, and containing feather beta-keratins, these structures were not feathers, or even feather offshoots. They were outgrowths of the epidermis that were more akin to fingernails than to feathers. One of the take-home messages of the Sawyer et al. paper was to be very cautious about any stage-I feather, as true identification of these feathers requires a level of detail that is currently missing in the fossils.

Yutyrannus huali: 1.4 tonnes and fluffy

The presence of extensive filamentous integument on the body of the Y.huali specimens has some potentially large consequences for interpretations of large theropod body coverings. As discussed previously, since the discovery of filamentous coverings in maniraptoran coelurosaurs back in 98, there has been a slow, but steady push from many in the paleo community to add fuzz to dinosaurs whenever possible. All this despite a preponderance of evidence for most dinosaurs having scales. A common argument put forth to handle this apparent paradox has been that large size would be a deterrent to feather formation since larger animals would have surface area/volume ratios that would naturally result in heat retention anyway. Under this scenario larger dinosaurs would be scaly so as to promote heat loss, while the smaller guys could sport filaments.

The discovery of Yutyrannus hauli changes all of this. At an estimated 1.4 tonnes in size (based on ZCDM V5000, the largest specimen), this animal falls in the size range of medium to large size theropods like Allosaurus fragilis. At that size the heat retained in the body by simply being big would be enough to warrant a switch to heat-loss “promoting” scales. However the fossils tell a completely different story. Even at 1.4 tonnes, a large filament covered theropod shows no signs of feather loss. As the authors mentioned:

Although feather preservation is patchy in these specimens…the distribution of the preserved filamentous feathers in the three specimens of Y. huali implies that this taxon had an extensively feathered integument in life.

There may be another reason why Y.hauli was sporting filaments. We’ll cover that in a bit, but first…

Sciurumimus albersdoerferi: baby megalosauroid with a fluffy tail?

Despite the better preservation and farther reaching connotations of the discovery of S.albersdoerferi, it seems to have made a much smaller splash in the paleo community than expected. The biggest reason behind this is probably due to the way in which it was originally announced. Rauhut et al. originally “leaked” images online of S.albersdoerferi some nine months ago before the description came out. At the time it was also rumoured that the phylogenetic placement was going to be more basal than other filamentous theropods.

So what of these filaments? Looking at the slab that contains the specimen one would be hard pressed to see anything integumentary at all. In visible light there are very little signs of integument on the specimen. The filament discovery came from UV analysis of the slab. Many fossils will fluoresce under UV light. By mixing and matching UV wavelengths it is possible to make certain features “pop out.” Rauhut et al. accomplished this for S.albersdoerferiby using the refined techniques of their co-author Helmut Tischlinger. Tischlinger’s work has appeared in multiple paleo papers over the past few years. His talent for UV is unmatched and has allowed researchers to view structures that would otherwise be obscured by the matrix that housed them. That said, just because something appears under UV does not necessarily mean it is real (note how the specimen also shows a few vertical black stripes under UV. This was likely the glue used to hold the specimen together).

This brings us to the observations Rauhut et al. made on the S.albersdoerferi specimen. The authors used a variety of lighting techniques to get the structures they wanted to highlight, to pop out. In some cases one can tell that there are two different things in place. For instance the bones of S.albersdoerferi fluoresce a nice greenish colour under the UV lighting scheme. Along the tibia, vertebrae, ilium, ischium, and part of the scapula, one can see different colours popping out from the underlying bone. The trouble is determining exactly what those colours represent. The authors argued that the yellow-coloured blobs seen along the base of the tail, were indicative of skin, while similar yellow blobs on the tibia represented muscle. Perhaps there is some feature of soft tissue that would make it fluoresce this particular colour. However, when looking at the alleged filaments, they fluoresced a more greenish-blue colour. If these filaments were epidermal in nature then I don’t see why they would fluoresce a different colour from the rest of the skin. No other fossil examined under UV seems to show this type of distinction; at least none that I have read about. It seems more likely that the skin Rauhut et al. refer to is more muscle tissue on the base of the tail. This would appear to make sense as it basically looks just like the hypothesized muscle tissue by the tibia. The same could be argued for the apparent filaments above the scapular region (which fluoresce the same yellow colour as the muscle, collagen and “skin”). In that case they could be torn muscle fibres, or collagen fibres. As for the filaments themselves, it is strange that they appear to jut straight out from the bone, with no room for muscle or other soft tissue in between. Once again, if one looks at other dinosaur specimens that are known to preserve filamentous integument (e.g., Sinosauropteryx prima, Caudipteryx zoui, Microraptor gui), there tends to be a halo a few millimeters-centimeters from the bones, indicating where the body wall ended and the epidermal covering began. The only times that the epidermis runs close to the bone are towards the tip of the tail, or at the ends of the limbs, where soft tissue thickness is usually minimal. We don’t see this in S.albersdoerferi. Instead the filaments seem to come right off the bone. Perhaps this S.albersdoerferi specimen had dried out prior to burial, though given the environment it was in this would seem unlikely.

Another possibility could be that these apparent filaments are actually preparation artifacts. If so that would make the discovery and description of Sciurumimus albersdoerferi very similar to the recent rediscription of Juravenator starki by Chiappe & Gohlich (2010). The biggest difference is that the alleged filaments for J.starki were much finer and could only be seen under UV using high magnification. In both cases neither specimen preserves unambiguous filaments. As it stands I would be hesitant to use either of these guys as examples of filamentous integument in theropods.

Yutyrannus the tyrannosaur?

As the title of the paper hinted at, Yutyrannus huali popped up as a tyrannosauroid on the dinosaur family tree. This places Y.huali in that nebulous region of Coelurosauria reserved for animals that seem to be closer to Tyrannosaurus rex and Daspletosaurus torosus than to other coelurosaurs. This position is somewhat problematic given what is currently known about dinosaur integument distribution. While Y.huali and the other putative tyrannosauroid Dilong paradoxus both present evidence of a filamentous covering on the body, the later evolved tyrannosaurids T.rex, Tarbosaurus bataar, Albertosaurus sarcophagus and D.torosus all preserve scaly integument.

This suggests one of three things are occurring.

1) Filamentous integument evolved somewhere around the base of Coelurosauria and was later lost at or near the base of Tyrannosauridae

2) Dilong and Yutyrannus are not actually tyrannosauroids

3) Tyrannosaurids are not actually tyrannosauroids

The first scenario is certainly possible. Evolutionary Development (Evo-Devo) tests have shown that making feathers from scales is “easier” than going the other way around (Dhouailly 2009), which would suggest that something about tyrannosaurid lifestyle selected for scaly integument over filaments or bare skin.

The second scenario seems a bit more likely (at least to me). The placement of Yutyrannus hauli in tyrannosauroidea has already been greeted with some initial skepticism. Part of the skepticism lay in the matrix choices the authors used for their placement of Yutyrannus (Choniere et al. 2010). This matrix was missing a lot of data and produced phylogenies that had weak statistical support, as evidenced by Bremer support values of 1 and 2 for many of the major branching points, including Maniraptora. Bremer support values act almost like statistics. They let researchers know how many extra steps it takes in a phylogeny for a relationship to change. The higher the number of steps, the more stable that relationship is (given the characters and taxa used). Typically a Bremer support value of 3 is considered okay, while 5 and up are considered highly supported. The tree used also contained substantial polytomies for groups like Tyrannosauroidea, Carcharodontosauria, and Tetanurae. As a test for the relationship of Alvarezsauroids among Maniraptors the tree did the job, but it was probably not the best choice for establishing tyrannosauroid relationships (especially given that it had weak support for tyrannosauroids in general). So there was that. There was also some question of affinity based on a certain aspect of the skull (a pneumatic midline headcrest). Crests such as this appear similar to carcharodontosaurs like Concavenator corcovatus. The authors noted this in the paper, but also pointed out that a similar crest is also seen in the tyrannosauroid Guanlong wucaii. Nonetheless it was enough to make some researchers consider Y.huali as a potential carcharodontosaur. If true then this would push the origin of filamentous integument closer to the base of tetanurae, a more inclusive group that contains theropods like Allosaurus fragilis. This would make for an even more messy phylogeny, as known skin impressions for Allosaurus show that scales were typical for this animal. Instead of one loss of filaments there would now be two or more losses. While not out of the realm of possibility, this is not a very parsimonious option (of course this is nothing compared to what Sciurumimus suggested, but we’ll get to that).

There is also the chance that Y.huali and D.paradoxus were closer to maniraptors than to tyrannosauroids? This scenario has some merit to it. As mentioned above, the tree choice for fitting Yutyrannus was already suspect, but even if one moves to better phylogenies that are more focused on tyrannosaur relationships (such as Brusatte et al 2010) one still finds weak support for the members of tyrannosauroidea, in particular Dilong, Guanlong and a handful of other guys. Coupled that with at least two relatively recent phylogenies that have moved Dilong closer to Maniraptora (Turner et al. 2007, Lee & Worthy 2011) and it would seem that membership of Tyrannosauroidea is a nebulous one with the potential for one or multiple taxa getting drawn into this portion of the tree based on vague/homoplasious (i.e., convergent) characters.

The third option could happen, but in a roundabout way. Should higher resolution analyses of Tyrannosauroidea wind up popping a lot of its current members into different clades, Tyrannosauridae could be left nested within a clade that is within an (essentially empty) clade, making the name Tyrannosauroidea useless. However given its stem-based definition (Brusatte et al. 2010), the potential usefulness of Tyrannosauroidea suggests it won’t be leaving anytime soon.

This is an area that only future finds and better phylogenetic analyses will help resolve.

Sciurumimus the megalosaur?

Continuing on the theme of questionable phylogenetic affinities, we have the placement of S.albersdoerferi as a basal megalosaurid. If this is correct, and the alleged filaments prove to be real, that would bring filamentous integument down almost to the base of Theropoda, creating a nasty mess for the evolution and loss of filaments in dinosaurs; far worse than if Yutyrannus hauli were a carcharodontosaur. Of course “if” is the operative word here.

While Yutyrannus hauli’s placement was greeted with some skepticism, Sciurumimus albersdoerferi‘s placement as a basal megalosaur has seen substantial more skepticism. There is good reason for this, as S.albersdoerferi is known from a single (albeit well preserved) juvenile specimen. When it comes to juveniles, ontogeny discombobulates phylogeny. Young individuals tend to show plesiomorphic traits that wind up placing them further down a phylogenetic tree than they would otherwise be. This makes dealing with juvenile animals in phylogenies very difficult. Typically the only time one would incorporate juveniles would be if one had a good growth series to work with. That way one could incorporate character changes that were known to happen during ontogeny. There is no such growth series for S.alberdoerferi. To authors’ credit, they do address this a bit in the supplementary material, stating that they coded all characters that they considered to be ontogenetically variable, as “?” in the matrices.

Speaking of matrices, Rauhut et al. used three of them to test the phylogenetic placement of S.alberdoerferi. The first was from Smith et al. 2008, the second from Choniere et al. 2010, and the last from Benson et al. 2010. I mentioned the problem with Choniere et al. 2010 above, but Smith et al. 2008 suffered from a similar lack of coding completion. Benson et al. 2010 was better, but it did not look at Coelurosaurian relationships. Rauhut et al. used this last paper for their official analysis of S.alberdoerferi after “confirming” its placement as a basal megalosauroid in the previous analyses. The trouble with using matrices that have such large amounts of missing data, is that it can be very easy to move taxa around a tree with just one or two characters. The nebulous nature of S.albersdoerferi is made evident in the supplementary information of the paper as the authors repeatedly mention that this taxon’s placement had exceedingly low statistical support (bootstrap values below 50%. For reference a bootstrap value of 80% is considered minimal for good support). I find it strange that Rauhut et al. argued that because they were able to have Sciurumimus albersdoerferi place around megalosauroids in three separate analyses, it should count as strong support for its placement lower in tetanuran phylogeny. That all three analyses showed weak statistical support for most nodes suggests that these matrices are not that robust. Further let’s not forget that a bootstrap analysis takes that phylogeny, mixes things up and runs it again. That S.albersdoerferi and other theropods in these matrices were in the positions Rauhut found them in less than 50% of the time suggests that they either probably don’t belong there, or that the matrices used are too inadequate to resolve these relationships. Andrea Cau over at the Theropoda blog input S.albersdoerferi in his “megamatrix” for theropods and did not have any trouble getting this little guy to nest comfortably in Coelurosauria (though I’m not sure with how much support). While this is not a published analysis, I would not be surprised to see future papers finding S.albersdoerferi to be a coelurosaur in the near future.

The feather-scale dichotomy

The location of preserved integument on the three specimens of Y.hauli provides insight into filament locations in dinosaurs. As previously mentioned, we have extensive data on preserved integument in most representative dinosaur species. Among species with preserved integument the vast majority exhibit scales. It is really only in coelurosaurs (and even then it is typically maniraptors) that we see the move towards filaments instead. Among this large dataset are the theropods Allosaurus (Pinegar et al 2003), Carnotaurus (Czerkas & Czerkas 1997), Gorgosaurus, Daspletosaurus, Albertosaurus, Tarbosaurus (Currie et al. 2003) and Tyrannosaurus. The last one, T.rex, comes from the the Black Hills Institute and their “Wyrex” specimen. More info (including skin picture) can be found here. Given such a large assortment of data showing the presence of scales, why is there such a push to put filaments if not full-on feathers on T.rex and other scaly dinosaurs?

One likely reason has to do with the scale impressions themselves. All of these scale impressions have come from isolated patches on the body, typically near the pelvis or in the thoracic region. These isolated pockets have lead some folks to question how extensive this scaly covering was. That is to say, some have argued that just because scales are seen on one portion of the body (e.g., the belly), that doesn’t mean that it was representative of the entire body, as scales could have been present on patches of the body that showed feather loss due to large size. This very argument has been made by both Xu et al. for Y.hauli and Rauhut et al. for S.albersdoerferi. The problem I have with this argument—much like the arguments from ontogeny—is that it routinely assumes that scales and naked skin are the same thing. Nothing could be further from the truth. Scales are a unique form of integument akin to hair and feathers, nails, and claws. Evo-Devo studies suggest that feathers evolved from scales by “hijacking” the scale developmental pathway early in the process (Somes 1990, Sawyer & Knapp 2003, Sawyer et al. 2005, Dhouailly 2009). Further, their relationship to feathers is such that the two integumentary types appear to be mutually exclusive. Integument forms through a series of cascading events, with integument in extant archosaurs occurring in a series of waves starting with the main body (trunk, tail, proximal limbs), then the neck, head and terminal limbs (Widelitz et al. 2000, Alibardi & Thompson 2001). Given this knowledge one may able to reasonably infer extent of integument based on where a skin impression was found. If it was found on the foot, or tarsometatarsal region one should be able to infer that integument was present along the foot and ankle, leaving the rest of the body as an unknown. Should the skin impression be found on the tail, pelvis, or thoracic region though, one should be able to reasonably infer that it was representative of the integument found across the body up to the head, ankle, and wrist regions. Evo-Devo data on scale and feather formation in birds (Sawyer and Knapp 2003, Dhouailly 2009) suggests that feathers covered the entire body when they first appeared. This prediction has so far been borne out by early feathered dinosaurs like Microraptor gui (Xu et al. 2003) and Anchiornis huxleyi (Hu et al. 2009) as well as the “first bird*:” Archaeopteryx lithographica (Christiansen & Bonde 2004).

This all-or-none principle and antagonistic relationship of feathers and scales has been doubted in the paleo literature, with some authors arguing that Evo-Devo studies actually support a hodge-podge scale-feather relationship (Chiappe & Gohlich 2010, Rauhut et al. 2012). However, the references that are often cited for this do not actually support this view. Some such as Chang et al 2009, Widelitz et al. (2000, 2003) and Dhouailly et al. (1980) point to evidence of latent feather forming ability in avian scales. This ability was discovered through manipulation of scale epidermis by incorporating different compounds (e.g., B-Catenin, Retinoic Acid) during development. Results of these studies have shown that feathers can be induced from scale epidermis at certain times during development. However just because a feather was developing does not indicate that scales and feathers made good bedfellows. Quite the opposite in fact. As Dhouailly (1980) states:

It is clear, however, in view of the existence of domestic breeds of fowl with feathered feet (genetic ptilopody), that RA [Retinoic Acid] somehow interferes with scale morphogenesis and thereby reveals a latent ability of avian foot integument to produce feathers. Apparently the formation of scales requires additional and possibly inhibitory region-specific information on top of the trivial and ‘ubiquitous feather message’ (Dhouailly,1978). Retinoic acid,by weakening the scale message, would leave the feather message free to be expressed.

To put it another way: scale formation in birds requires active feather suppression.

Some rather recent work on avian scale histology and development has uncovered yet another twist in the feather-scale dynamic. In general, avian scales are composed of three morphological types:

Scuta – Large overlapping scales that cover the dorsal side of the tarsometatarsus and the foot digits Scutella – Somewhat smaller overlapping scales that cover the ventral side of the tarsometatarsus Reticula – Small non-overlapping scales that form on the underside of the foot

Whereas scuta and scutella contain the standard scale histological makeup (largely β-keratin with an α-keratin hinge), the reticula have been found to be composed of only α-keratin. Developmentally, reticula neither form from dermal condensations (a requirement for most other epidermal appendages) nor from a placode (as avian feathers and scales form from). These data suggest that reticula are not true scales. So if reticula are not scales then what are they?

Feathers. Yep, feathers.

From Dhouailly 2009:

…reticula are not true cutaneous appendages, and appear to be feathers arrested in the initiation step of their morphogenesis: formation of a slight bump, without a placode. …reticulate scales, which cover the plantar surface of all living birds, cannot be the remnants of the ancestral granulated beta-keratinized skin of first sauropsids, and correspond to a secondary, almost complete, inhibition of feather formation.

Bringing this all together it would seem that the most parsimonious integumentary covering for a dinosaur with known skin impressions, like T.rex, would still be scales. The discovery of Yutyrannus huali further supports this view as filamentous impressions are found along the pelvis and tail region; areas that were previously argued to be scaly in large theropods when based on skin impressions.

So once again it would seem that the concept of the dinosaur with a feathered mohawk gets relegated to the fiction bin.

* I put first bird in quotes to reflect the recent fuss over the relationship of Archaeopteryx to extant birds.

“Wooly” theropods of the “chilly” Mesozoic

One of the appealing aspects of a Xu et al. article is that the authors tend to cover their bases as best they can while trying to avoid speculating beyond the data. This article is no different. The authors entertain alternate reasons behind the presence/function of the filaments. One of those aspects has receive a bit more attention than it probably should have.

From the article:

Alternatively, if scales were indeed the dominant integumentary structures in most Late Cretaceous tyrannosauroids, the presence of long feathers in the gigantic Y. huali could represent an adaptation to an unusually cold environment.

As one can see from the image at the beginning of this post, this aspect of the paper has been blown a bit out of proportion. There is some indirect evidence to indicate that the Yixian was a time of unusual (for the Mesozoic) cold temperatures (Amiot et al. 2011). However—and this is the part the news organizations and blogs don’t mention—those temperatures aren’t all that cold. Amiot et al. determined that the mean annual air temperature for the environment of the Jehol Biota was around 10°C (50°F). For perspective that is the same mean annual temperature of present day Ohio. These are hardly arctic conditions that we are talking about here (in fact Ohio gets bloody hot in the late Spring and Summer).

So it seems a bit weird that in what was likely a balmy to slightly cold environment (during part of the year) a 1.4 tonne theropod would be sporting a “wooly coat.” Also, while the preserved filaments were fairly long and shaggy (15-20cm [~6-8 inches]) that is well within the range of modern emu (Dromaius novaehollandiae) which lives in hotter environments than those predicted for the Jehol Biota. They are also a far cry from the actual wooly coats of mammoths and wooly rhinos (up to 0.91 meters [3 ft] long in the former). This brings us to another important thing to consider. Is the trend we see in mammals (thicker coats in winter, wooly coats for arctic animals) a physiological response to temperature, or a mammalian physiological response to temperature?

Put another way: is there such a thing as a wooly bird? Surprisingly a survey of the literature seems to indicate that birds don’t really change their feather thickness with latitude, or climate. While all birds molt, molting frequency and timing are taxon specific, with only some species having winter molts. It is generally thought that birds that molt prior to winter do so in preparation for the cold. Thus their “winter coat” is thicker than their summer coat. However there is very little analytical data to back this up. Irving et al. (1955) looked at a variety of birds from various latitudes and found no real difference in contour feather thickness.

Perhaps this is to be expected though. Unlike mammals, bird feathers grow on specialized regions of the body (tracts). These tracts limit the locations for new feathers to form. Feather tracts appear to make it difficult for a bird to put on more feathers at any one time of the year. This apparent limit to feather placement is borne out by the only observation I could find for a “winter coat” in birds.

The willow ptarmigan and Northern grouses do seem to put on thicker coats of feathers in the winter. They bypass the feather tract problem by making unique feathery structures referred to as “afterfeathers.”

After feathers are a secondary structure produced from the main axis, or rachis of the contour feather, having a plumulaceous barb and barbule structure greatly enhancing insulation…. The afterfeathers of ptarmigan in winter are three-fourths as long as the feathers from which they are derived, adding considerably to the thickness of the body plumage. – Marchand 1996

So it would appear that Yutyrannus hauli was unlikely to have been a “wooly theropod.” It was probably just a filament-covered coelurosaur that just so happened to get big.

Filaments and metabolism

Despite being the hardest and least likely thing to ever find evidence for, dinosaur metabolism continues to feature prominently in dinosaur studies. Finds such as this, that involve potentially insulative coverings, probably draw the most attention to the ultimate question of what “metabolic camp” dinosaurs were in. This is due in most part to the oft held assumption that insulation only benefits animals that produced heat internally. After all insulation by itself does not confer warmth but simply retards the flow of heat to or from a body (this is the reason why a thermos works in the summer and in the winter). If an ectothermic animal were to have insulation, so the argument goes, it would be unable to effectively raise its body temperature in the sun. There is surprisingly little empirical backing for this logic, most of it stems from mathematical models that predict heat flow in stationary (typically geometric) objects. There are extremely few physiological tests out there. This may help explain why one of the most popular physiological tests of insulation is that of Raymond Cowles (1958) and his study on dermal temperature regulation in amphibians and reptiles.

Part of Cowles’ paper made reference to a class project that Cowles had performed (or rather, had one of his students [Richard Grossman] perform) in which two heliothermic lizards—a desert iguana (Dipsosaurus dorsalis) and a chuckwalla (Sauromalus obesus)—were wrapped in a mink coat. Yep, you heard right, lizards wearing mink. The animals were then warmed up for 18 and 12 minutes respectively. Afterwards the animals were chilled to 15°C (59°F) before being reheated for 69 minutes and then chilled again. The results Cowles’ student obtained were a noticeable lag in heating and cooling. These heliothermic lizards were taking longer to warm up, but they were also taking longer to cool down. From this Cowles concluded that insulation would be a detriment to an ectothermic animal.

…animals might tend to profit from insulation by their retention of heat when once warmed,but this advantage would in turn be cancelled by the retardation in warming rates. For diurnal heliothermic animals there might be some extension of activity during the latter part of each day ,but a delayed or late start each morning would incur a penalty. For nocturnal animals there would seem to be similar cancellations of advantages and disadvantages, the disadvantages being aggravated by evaporative cooling if the insulated covering had absorbed either dew or rain. – Cowles 1958

And so the party line has stuck. However looking at Cowles’ original paper there are some noticeable flaws in the experiment that could greatly change the outcome. For starters, this experiment was performed by a student for a class project. This is not mean to knock Mr. Grossman’s work, but the fact that it was a class experiment meant that Cowles never bothered to write up the materials and methods for the experiment. Cowles only ever mentions that the animals were encased in “a crude ‘wrap-around’ of mink!” No mention is given to how tightly wrapped the lizard were, how extensive the covering was, or even how thick the mink covering was. All of these would be essential to an accurate assessment of the effect of insulation on an ectothermic animal. Cowles does not go into detail about the heating and cooling experiment either; only giving the reader two figures which mention a heating source, but not what that source was, or how extensive it was (are we talking about a spotlight?, a heat rock?, some form of heat tape?, multiple spotlights?, etc.). We are also not told how long the animals were allowed to acclimate, or what conditions they were allowed to thermoregulate in (thus letting us know how stressed the lizards may have been). All of these factors could greatly affect the outcome of the experiment. That none of this was really followed through makes this experiment really more of an anecdote more than anything else (indeed it isn’t even the main thrust of the paper).

Methodological problems aside, Cowles’ assumption that insulative coverings are inert objects is also untrue. Anyone who has seen a scared cat, watched a dog dry off, or has had goosebumps knows that filamentous integument can be manipulated muscularly. This makes filamentous integument a dynamic addition to the body, allowing for increased, or decreased insulation at a moments notice. This swapping of insulative abilities has been demonstrated in the wild with roadrunners (Geococcyx californianus) and turkey vultures (Cathartes aura), both species which are known to employ ectothermic “sunning” postures to warm up in the morning (Ohmart & Lasiewski 1971, Clark & Ohmart 1985, Ruben & Jones 2000).

Then there is the other side of the coin, bradymetabolic animals that do have insulation. Moths, bees, caterpillars, tarantulas and leatherback sea turtles (Dermochelys coriacea) to name but a few. In some animals like the moths and leatherback, insulation serves to retain metabolically produced heat (but via muscular action rather than visceral as seen in mammals and birds), in other animals like the thousands of hairy spider and caterpillar species, the integument seems to act as a sense organ, or a deterrent to predators. Then there is the crazy “yeti crab” (Kiwa hirsuta) which uses its integument for…something we have yet to identify.

The importance of integument to bradymetabolic thermoregulators was also demonstrated by Seebacher (2003). The author used a mathematical model based on thermoregulating saltwater (Crocodylus porosus) and freshwater (C.johnstoni) crocodiles to estimate the average daily body temperatures of 701 dinosaurs operating under the assumption that they were bradymetabolic, ectothermic animals that thermoregulated. Under this model Seebacher found that body temperature fluctuations were greatest only in small (<100kg [220lbs]) dinosaurs living at mid-high latitudes. Yet, by simply incorporating insulation into animals like Sinosauropteryx prima (estimated body mass of 3.8kg [8.4 lbs]), body temperatures practically stabilized (variations of ≤3.1°C [~6°F]) while core body temperature increased (from 23.8°C [75°F] without insulation to 32.4°C [90°F] with insulation). Seebacher’s model was fairly conservative and incorporated some aspects from modern times (e.g., daily temperature flux) that may not have been true back in different epochs of the Mesozoic. Yet with these caveats in mind, his model was able to show the effectiveness of insulation for even a bradymetabolic animal.

So with all this in mind, what does the presence of extensive filaments on Y.hauli tell us? It tells us that the animal had a layer of insulation around it that would have aided in maintaining core body temperature. How that temperature was obtained and maintained remains unknown. A key thing to remember is that given the location and currently estimated paleoclimate, an insulative covering would have been advantageous regardless of thermophysiology.

~Jura

References

Alibardi, L., Thompson, M. 2001. Fine Structure of the Developing Epidermis in the Embryo of the American Alligator (Alligator mississippiensis, Crocodilia, Reptilia). J.Anat. Vol.198:265-282

Amiot, R., Wang, X., Zhou, Z., Wang, X., Buffetaut, E., Lecuyer, C., Ding, Z., Fluteau, F., Hibino, T., Kusuhashi, N., Mo, J., Suteethorn, V., Wang, Y., Xu, X., Zhang, F. 2011. Oxygen Isotopes of East Asian Dinosaurs Reveal Exceptionally cold Early Cretaceous Climates. PNAS. Vol.108(13):5179-5183

Benson, R.B.J., Carrano, M.T., Brusatte, S.L. 2010. A New Clade of Archaic Large-Bodied Predatory Dinosaurs (Theropoda: Allosauroidea) That Survived to the Latest Mesozoic. Naturwissenschaften Vol.97:71–78

Brusatte, S.L., Norell, M.A., Carr, T.D., Erickson, G.M., Hutchinson, J.R., Balanoff, A.M., Bever, G.S., Choiniere, J.N., Makovicky, P.J., Xu, X. 2010. Tyrannosaur Paleobiology: New Research on Ancient Exemplar Organisms. Science. Vol.329:1481-1485

Chang, C., Wu, P., Baker, R.E., Maini, P.K., Alibardi, L., Chuong, C-M. 2009. Reptile Scale Paradigm: Evo-Devo, Pattern Formation and Regeneration. Int.J.Dev.Biol. Vol.53:813-826

Chiappe, L.M., Gohlich, U.B. 2010. Anatomy of Juravenator starki (Theropoda: Coelurosauria) from the Late Jurassic of Germany. N.Jb.Geol.Palaont.Abh. Vol.258(3):257-296

Choiniere, J. N. Xu, X, Clark, J.M., Forster, C.A., Yu G., Fenglu H. 2010. A Basal Alvarezsauroid Theropod from the Early Late Jurassic of Xinjiang, China. Science. Vol.327:571-574

Christiansen, P., Bonde, N. 2004. Body Plumage in Archaeopteryx: A Review and New Evidence from the Berlin Specimen. C.R.Pale. Vol.3:99-118

Clark, R.G., Ohmart, R.D. 1985. Spread-Winged Posture of Turkey Vultures: Single or Multiple Function? Condor. Vol.87:350-355

Cowles, R.B. 1958. Possible Origin of Dermal Temperature Regulation. Evolution Vol.12(3):347-357

Currie, P.J., Badamgarav, D., Koppelhus, E.B. 2003. The First Late Cretaceous Footprints from the Nemegt Locality in the Gobi of Mongolia. Ichnos. Vol.10:1-12

Czerkas, S. A., Czerkas, S.J.. 1997. The Integument and Life Restoration of Carnotaurus. in Wolberg, D.L., Rosenberg, G.D. (eds.), Dinofest International, Proceedings of the Symposium at Arizona State University, pp. 155–158. Philadelphia Academy of Natural Sciences, Philadelphia.

Dhouailly, D. 2009. A New Scenario for the Evolutionary Origin of Hair, Feather, and Avian Scales. J.Anat. Vol.214:587-606

Dhouailly, D., Hardy, M., Sengel, P. 1980. Formation of Feathers on Chick Foot Scales: A Stage-Dependent Morphogenetic Response to Retinoic Acid. J.Embryol.Exp.Morph. Vol. 58:63-78

Hu, D., Hou, L., Zhang, L., Xu, X. 2009. A Pre-Archaeopteryx Troodontid Theropod from China with Long Feathers on the Metatarsus. Nature. Vol.461:640-643

Irving, L., Krog, H., Monson, M. 1955. The Metabolism of Some Alaskan Animals in Winter and Summer. Phys.Zool. Vol.28(3):173-185

Lee, M. S. Y., Worthy, T.H.. 2011. Likelihood Reinstates Archaeopteryx as a Primitive Bird. Biology Letters doi: 10.1098/rsbl.2011.0884

Marchand, P.J. 1996. Life in the Cold. 3rd edition. University Press of New England. p.234

Ohmart, R.D., Lasiewski, R.C. 1971. Roadrunners: Energy Conservation by Hypothermia and Absorption of Sunlight. Science. Vol.172:67-69.

Ortega, F., Escasco, F., Sanz, J.L. 2010. A bizarre, Humped Carcharodontosauria (Theropoda) from the Lower Cretaceous of Spain. Nature. Vol. 467:203-206

Pinegar, R.T., Loewen, M.A., Cloward, K.C., Hunter, R.J., Weege, C.J. 2003. A Juvenile Allosaur with Preserved Integument from the Basal Morrison Formation of Central Wyoming. JVP. vol.23(3):87A-88A

Prum, R.O. 1999. Development and Evolutionary Origin of Feathers. J.Exp.Zool.(Mol.Dev.Evol) Vol.285:291-306

Rauhut, O.W.M., Foth, C., Tischlinger, H., Norell, M.A. 2012. Exceptionally Preserved Juvenile Megalosauroid Theropod Dinosaur with Filamentous Integument from the Late Jurassic of Germany. PNAS Early Edition:1203238109v1-201203238.

Ruben, J.A., Jones, T.D. 2000. Selective Factors Associated with the Origin of Fur and Feathers. Amer.Zool. Vol.40:585-596

Sawyer, R.H., Knapp, L.W. 2003. Avian Skin Development and the Evolutionary Origin of Feathers. J.Exp.Zool.(Mol.Dev.Evol) Vol.298B:57-72

Sawyer, R.H., Rogers, L., Washington, L., Glenn, T.C., Knapp, L.W. 2005. Evolutionary Origin of the Feather Epidermis. Dev.Dyn. Vol.232:256-267

Sawyer, R.H., Washington, L.D., Salvatore, B.A., Glenn, T.C., Knapp, L.W. 2003. Origin of Archosaurian Integumentary Appendages: The Bristles of the Wild Turkey Beard Express Feather-Type B Keratins. J.Exp.Zool.(Mol.Dev.Evol) Vol.297B:27-34

Seebacher, F. 2003. Dinosaur Body Temperatures: The Occurrence of Endothermy and Ectothermy. Paleobiology. Vol.29(1):105-122

Smith, N.D., Makovicky, P.J., Agnolin, F.L., Ezcurra, M.D., Pais, D.F., Salisbury, S.W. 2008. A Megaraptor-Like Theropod (Dinosauria: Tetanurae) in Australia: Support for Faunal Exchange Across Eastern and Western Gondwana in the Mid-Cretaceous. Proc.Biol.Sci Vol.275:2085–2093

Somes, R. G. 1990. Mutations and Major Variants of Plumage and Skin in Chickens. in “Poultry Breeding and Genetics” Crawford, D.R. (ed). Elsevier, New York

Turner, A.H., Pol, D., Clarke, J.A., Erickson, G.M., Norell, M.A. 2007. A Basal Dromaeosaurid and Size Evolution Preceding Avian Flight. Science. Vol.317:1378-1381

Widelitz, R.B., Jiang, T-X., Lu, J., Chuong, C-M. 2000. B-Catenin in Epithelial Morphogenesis: Conversion of Part of Avian Foot Scales into Feather Buds with a Mutated B-Catenin. Devl.Biol. Vol.210:98-114

Widelitz, R.B., Jiang, T.X., Yu, M., Shen, T., Shen, J-Y, Wu, P., Yu, Z., Chuong, C-M. 2003. Molecular Biology of Feather Morphogenesis: A Testable Model for Evo-Devo Research. J.Exp.Zool.(Mol.Dev.Evol). Vol.298B:109-122

Xu, X., Kebai, W., Ke, Z., Qingyu, M., Lida, X., Sullivan, C., Dongyu, H., Shuqing, C., Shuo, W. 2012. A Gigantic Feathered Dinosaur from the Lower Cretaceous of China. Nature. Vol.484:92-95

Xu, X., Zhou, Z, Wang, X., Kuang, X., Zhang, F., Du, X. 2003. Four-Winged Dinosaurs from China. Nature Vol.421:335-340

by