Wednesday, January 27, 2016

Insulation Without Feathers - A New Hypothesis Addressing Thermoregulatory Strategies of Naked Skinned Dinosaurs

The startling and unprecedented cavalcade of evidence of definite non-scaly integumentary structures on dinosaurs stands as one of the most exciting developments in dinosaur research over the last several decades. Whether in the form quills, feathers, pynofibers or any of the variously described features put under the banner of "dino-fuzz" these features continue to bedazzle us, further blur the line between dinosaur and bird, and offer up important new vistas and possibilities as to what and how dinosaurs looked and behaved. A speculative movement towards "enfluffening" - that a more widespread and encompassing integumentary parade of dinosaurs of all sizes and stripes was likely - has come into vogue. At the acme of this development are speculative depictions of shaggy coated arctic ceratopsids, woolly sauropods, and furry ankylosaurs.

However even a cursory review of known feathered dinosaurs shows an astonishing bias towards theropods and especially smallish theropods (insert discussion on taphonomic bias). Among ornithischians we have evidence of quill structures on Psittacosaurus, "protofeathers" on the heterodontosaurud Tianyulong, and of course the startling, unexpected and weird mash-up of scales and novel assorted integumentary structures found on the basal ornithopod Kulinadromeus. Never the less this is a paltry selection compared to the abundance of evidence in theropods. Lack of evidence arguments can be applied to a failure to find structures in sauropodomorphs, iguantodontids, marginocephalians, and thyreophorans but these arguments - in my opinion - sound more and more like special pleading. It is more likely that these groups either never evolved such structures, minimally featured them, or secondarily lost them. Long and short of it is that I think that the signal we are getting from the fossil record is, in broad strokes, correct. Theropods were primarily the fuzzy, feathered dinosaurs and such structures were rare, reduced or absent in many of the more derived sauropods and ornithischians. However these structure may have been quite endemic and numerous in small and/or basal members of several ornithischian clans. 

Wherever the truth lies among who wore their hair long, shorn, or not at all among dinosaurs is still very contentious - chances are you might agree with some of what I said but probably not all of it. That is ok. This post is really not out to settle that debate. What this post is about is offering an alternative to "dino-fuzz" that accounts for the notable lineages of dinosaurs that so far lack good evidence for extensive insulatory pelages and that also lived in some pretty chilly environments. 

That some dinosaurs lived in what can only be described as cold climates has been known for some time now. While the Mesozoic was for the most part a hothouse climate with equitable climates penetrating much highter in latitude than modern ones, these areas still went through months of darkness as well as heavy cloud cover during immense precipitation events. To say that the Cretaceous north slope of Alaska was Minnesota cold is probably an overstatement but maybe as chilly as Seattle or even Tierra del Fuego might be more accurate. You would want to wear some layers in such environments. While presumably fuzzy theropods (and possibly some ornithischians) were important components of Mesozoic arctic faunas these environments also hosted dinosaurs that we have no evidence of integumentary structures. Examples include a titanosaur and the ankylosaur Antarctopelta  from Antarctica, Muttabarasaurus from polar Australia, and of course the abundant remains of ceratopsids, hadrosaurs, and ankylosaurs from the Cretaceous north slope of Alaska, among others. Integumentary insulatory structures are either wholly or almost completely unknown in these lineages. Most notable is the complete lack of structures found in hadrosaurs, despite the abundant, remarkable, and compelling skin preservation record for this group without even a stitch of integumentary structure found in their ranks. Now that is something to think about.

Despite the paltry or non-existent record of non-scaly integumentary structures in these groups we do have a pretty good record of skin impressions, scutes, osteoderms, and especially for hadrosaurs direct skin "mummifications" if you will. What I am going to suggest is a novel method of thermoregulation that these structures converge upon and that may in fact negate the need for an extensive outer insulating coat of feathers.

Before I get to the fun part just a little basic physics and assumptions that I am working from. First off I am working from the assumption that dinosaurs had a heightened level of internal thermal control - whether you want to call if "warm-bloodedness" or endothermy - they could generate internal heat on their own. However, ecotherms or "cold-blooded" physiologies are going to play a crucial part in this theory when it is all said and done... hint, hint. Next, just a little background on insulation and the physics of thermal flow. In modern day furred or feathered birds and mammals insulation works by trapping a layer of warmed air close to the body surface which retards the loss of heat from the body. Now it is more complicated than that of course with recent studies pointing to other uses of fur/feathers such as diffusing thermal radiation. But for simplicity's sake I am going to ride with the idea of trapping a layer of air being crucial to modern furry endotherms, people wearing clothes, and dinosaurs as well. That air plays such a crucial role in insulation is due to the fact that it does not conduct heat very well or more precisely temperature from a hot body to a cold surrounding or vice versa hot surroundings into a relatively cold body. This is why you can be fairly comfortable walking around with minimal clothing in 55 degree fahrenheit weather (13 celsius) but jump in water of that same temperature and you will be singing a different tune!! A liquid medium, or increased air flow, is going to whisk away heat from a body more quickly than a still layer of air - better yet for insulation would be a vacuum seal of air with minimal molecules. One way you can picture it is the less molecules bouncing around and "stealing" warmth from a body the better for insulation. That organisms that generate their own body heat find it evolutionarily advantageous to insulate themselves is fairly obvious. Not doing so would mean that extra calories are getting burnt to keep the house heated. Such large heating bills require an organism to eat that much more to stay at an optimal temperature. And endotherms, more so than ectotherms generally, want to keep their temperature in fairly narrow band that is optimized for their own enzymatic and physiologic pathways.

So how does a scaly, osteoderm studded, naked hided dinosaur trap a layer of warm air around itself to retard heat loss without an outer layer of insulation? 

The answer is simple and should be familiar to anyone who has installed insulation in a house. Dinosaurs did not trap a layer of warm air on the outside of the skin, but inside the skin.

In this scenario the outer layer of keratinized skin, osteoderms, plates, and other assorted scaly structures - largely dead, keratinized material anyway - act as the outer insulatory layer shielding the all important layer of warm air directly underneath them. Evidence of such thin ampullae, or hollowed out spaces visceral to the outer integumentary layer of dinosaurs, is very prevalent and I will go through them in a moment. What creates such hollow air spaces is simply shunting blood away from the exterior of the animal. Vasoconstriction is a simple and elegant mechanism known in all tetrapods that will withdraw blood away from extremities leaving behind, essentially a vacuum sealed outer layer of warm, insulating air with these structures. As I mentioned earlier a vacuum sealed air layer is the best type of insulatory layer (less molecules bouncing around stealing warmth).

Triceratops internal skin mould. credit Rapid City Journal
Above is the quite startling and unexpected internal skin mould of a Triceratops still unpublished in any sort of meaningful venue. But understand you are looking at the skin from the inside out. What you will notice is the large raised scales creating sort of a honeycomb effect. Also some of the scales have what has been described as a "nipple" like projection arising from them, best seen in the photo below of the external skin. To feed and grow such structures blood flow would be necessary, but in cold weather or especially hot weather blood flow would be shunted away from these outer extremities leaving the convex scales with their nipple like projections with a layer of warm insulating air underneath. The flipside is also a possibility. In extremely hot conditions blood flow to the extremities could be shut off insulating the cooler insides from the outside temperature extremes. When the animal wanted to cool off - in water, shade, or a prevailing wind - blood flow could be opened up engorging the outer scales and nipples, the large surface area allowing efficient conduction of heat away from the body.

External mould Triceratops skin. Rapid City Journal
The analogy to insulating a house is useful but let us also think about how a thermos works. A thin outer metallic layer separated by a thin layer of air, another layer of metal and the inside fluids. A thermos works to keep its fluids from heating up or cooling down, i.e. they work to keep cold stuff cold in hot outside temperatures and warms stuff warm in cold outside temperatures, All because of that thin layer of internal insulating vacuum sealed air.

But wait it gets better....

Remember that giant titanosaur osteoderm from Madagascar? Probably not, I had to do some internet sleuthing to rediscover it. But it is amazing.

The adult-sized osteoderm is the most massive integumentary skeletal element yet discovered, with an estimated volume of 9.63 liters. Uniquely, this specimen possesses an internal cavity equivalent to more than half its total volume. Large, hollow osteoderms may have functioned as mineral stores in fecund, rapidly growing titanosaurs inhabiting stressed environments.

I am not saying such structures did not serve as mineral stores but the possibility for thermoregulatory air space is a potential use too.

However the real pantheon of evidence for a subdermal insulating layer of air comes from the hadrosaurs, dinosaurs that for whatever reasons left us with a lot of skin evidence.

hadrosaur skin from museum quality fossil casts. inside and outside texture

Now take a good long look at this fossil cast chunk of hadrosaur skin. You will notice two general morphologies; in the upper section a nice bit of what has been described as hadrosaur "pavement" scales, non-overlapping convex polygonal; but trending down and to the left you see a distinctly different type of scale that has a raised outer rim and is concave. Go back and compare this morphology to the internal skin mold of the triceratops I discussed earlier. No, you are not looking at an internal mold of hadrosaur skin but in fact are looking at the layer of skin directly underneath the outermost layer of scales. Another way to put it is that the outer layer of skin has been stripped away through some taphonomic process in the lower quadrant leaving us with an image of what lies directly beneath the outermost layer of scale. What we see is that the interstitial space on the outer scale become an raised interstitial border on the visceral layer - in affect a mirror image - and what we have is a nice little hollowed out area immediately underneath the outermost layer of skin.

But don't take my word for it in describing what you are seeing in this unpublished chunk of hadrosaur skin taken from a fossil cast store. It is merely a good visual representation for what has already been described in the chapter on hadrosaur skin in the epic tome Hadrosaurs (2014, Indiana Univ Press): A Review of Hadrosaur Skin Impressions.

In describing Sternberg's famous mummified Lambeosaurus magnicristatus Evans & Reisz (2007) describe (pp 583):

"...The authors also noted and unusual relationship between raised polygonal scales and scales demarcated by raised insterstitial tissue, similar to what would be expected in a negative impression. In the area of the neck, the raised scales lie immediately external (superficial) to the grid of raised interstitial tissue. This suggests the preservation of both epidermal and deeper (dermal) tissues (cf. Manning et al., this volume). Regardless of their relationship, the size and morphology of the scales and deeper integument are consistent with one another. A similar relationship between raised scales and interstitial tissue is present also on an specimen of Edmontosaurus regalis (ROM 801) from an unknown region of the body (fig 34.2)." 

Catch all that? Evidence positive of a dermal pocket immediately beneath the outer dermis and which could potentially serve as a vacuum sealed layer of air when blood flow was shut off to the extremities.

Here is another good graphic of this system from the massive Baja lambeosaurine Magnapaulia.

Magnapaulia skin preservations. credit Prieto-Marques, Chiappe & Joshi. CC 2.5

Here is that same hollowed out morphology in the internal cast photos of Saurolophus skin (Bell, 2012).

credit Phil R. Bell. CC

And guess what, it get's better. Check out Dave Hone's website here where you can quite clearly see that Kulinadromeus exhibits the same morphology!!

I want now to take the liberty to name this integumentary feature.



The acronym spells out SIGIL or to maybe use it in sentence: "Does the integument show evidence of SIGIL?" or "Are there SIGI layers?"

As I alluded to earlier in this post I believe that modern ectothermic reptiles have a strong role to play in all of this. Given that dinosaurs are nestled between modern crocodilians and birds - scaly hided and feathered respectively - for those dinosaurs that most likely were scaly hided modern reptiles prove a useful proxy model for investigating thermoregulatory functions in these dinosaurs. Wouldn't it be useful if there were some studies addressing this very issue? 

Turns out there is and a just recently published paper by Witmer labs (Porter  & Witmer 2015) that looks at this question through the lens of an ancestral diapsid condition that is remarkably precise in it's ability to fine tune the flow of blood for thermoregulatory functions.

What the study shows is that the ability to move and shunt blood - especially with relation to the cranio-cephalic region - is highly refined in modern diapsids
 and likely ancestral to the whole group. In other words reptiles can bask longer in hot conditions without cooking their brains or eyeballs due to their ability to move around blood and cool it off at select spots. The take home message is that this system was likely ancestral to dinosaurs.

For our interests here there is no reason to preclude dinosaurs from having a similar system of blood control, especially with regards to active peripheral control of blood movement.

However the study is really a refinement of what has been known for a while. That reptiles are not passive recipients of their thermal environment but active harvesters and, to an extent, hoarders of thermal energy. What this boils down to is that once a reptile has achieved its optimal temperature it can  maintain this temperature - despite what the ambient temperature is - for a lot longer that would be possible if it just had an open door policy with its environment.

It is worthwhile now to mention one man who is most responsible for how we now view reptile thermal physiology more than any other, Raymond B. Cowles. 

From his seminal paper from all the way back in 1957 "Possible Origin of Dermal Temperature Regulation" on the assumption that temperature regulation via insulation and vasoconstriction/dilation originated with endothermy:

What underpinned much of Cowles' work was a strange notion that dinosaurs - which at the time were believed to be ectothermic - died during a hot flash at the end of the Mesozoic. Cowles investigation into desert reptiles overturned the prevailing notion that desert reptiles had insatiable tolerance and proclivity towards heat - so much so that strange tails of snakes crawling into campfires were commonplace. Instead, Cowles found that desert reptiles had no such special proclivity towards heat and would die if left exposed to high temperatures for prolonged periods. Going with this strand of thought Cowles speculated - with no supporting evidence - that a sudden hot flash at the end of the Mesozoic killed off the dinosaurs. This "serendipitous flash" of inspiration that guided much of Cowles research into reptiles has not been borne out with prevailing evidence in the decades since. Never the less his work on reptile physiology that dovetailed with this "serendipitous flash" and then revolutionized the field is a fascinating story documented by Scott J. Turner titled Raymond J. Cowles and the Biology of Temperature in Reptiles (1984). I highly recommend taking the time to read Turner's paper on Cowles and his research.

Some excerpts from Turner's paper (Pp 433):

And finally (Pp 434): 

So what of this slight aside into the story of the iconoclastic reptilian physiologist Raymond J. Cowler? While I doubt there is any validity in his "serendipitous flash" theory of dinosaur extinction I do think that his life's work - showcasing reptiles as "masters not slaves of their thermal environment" is instrumental and prescient in establishing the success - not the failure - of dinosaurs.

What I suggest was going on with a great many dinosaurs, especially those that evolved layers of SIGI and equivalent integumentary features as I have outlined on this post, is that they were double-dipping. That is dinosaurs were harvesting thermal resources as an ectotherm would when it suited them but also generating internal heat when conditions were not favorable in their environment. In essence a blending of the best of the two physiologies of an ectotherm and endotherm with neither of the "perceived" limitations of either. In other words dinosaurs could conserve energy that would otherwise go into heat production when they were harvesting thermal energy to warm themselves. To retard heat loss they would take advantage of the thermally insulating potential in their layers of SIGI. Alternatively they could avoid overheating by either withdrawing blood away from the peripheral tissue (utilizing their insulatory layer) or by shifting it peripherally for heat loss through convection via wind, water or other cooling mediums. When the environment shifted towards cool conditions - at night, during monsoons, high latitudes etc. etc - endothermic generating gear would kick in, again, with heat loss minimized via SIGIL(s). 

There is numerous implications inherent in this idea with respect to dinosaur growth rate, efficiency and size attained that should be immediately apparent. Additionally there is the obvious benefit in the ability to sequester a free and abundant resource - solar thermal energy - that was plentiful during the often times hot-house world of the Mesozoic.

Gee, this is all very neat and interesting you are probably thinking but wouldn't it be nice if we had at least one reptile that displayed this "double-dipping" of both physiologies at hand? Well, in what I can only describe as "serendipitous" what came out this last week but a paper describing just such a reptile that utilizes both classic reptilian ectothermy and what can only be described as a primitive seasonal "warm-bloodedness" in tegu lizards (Salvator merianae).

credit Tattersall et al, 2016 Creative Commons

Pretty darn cool. This study even suggests the impetus to evolve endothermy for reproductive success. I wonder if there could be any similarities in the subdermal anatomy of tegu skin and dinosaur skin... hmmm looks almost like a "skin envelope" where have you heard that term before (hint, hint dinosaur mummies).

Salvator genus tegu. credit Donar Reiskoffer CC3.0

Before I dig into several studies suggesting thermoregulatory functions in the dermal structures in  armored dinosaurs a brief word on the concept of "mesothermy" and nuance in dinosaur temperature range. A recent study (Grady, 2014) pointed to widescale mesothermy in dinosaurs (mesothermy implying temperatures generally lower than modern mammals and birds but higher than the environment). Furthermore a study looking at isotopes in eggshells as a proxy for dinosaur temperature surprisingly found oviraptors maintaining lower body temperatures than titanosaurs. I don't intend to do a full review of the literature on dinosaur temperature only suggest that a wide range was possible and probable. We should not insist on or expect a "one size fits all" approach to optimal dinosaur temperature.

In an extensive review of ankylosaur dermal armor Hayashi et al. (2010) found that dermal structures that differed in morphology had a remarkably consistent pattern of histology. Although some dermal structures, especially in later ankylosaurs showed increasing cortical strength and integrity (implying use in combat) other osteoderms seemed remarkably thin and underequipped for defensive purposes. "Pipe" like structures and extensive vascularization in all of the dermal armor implied a potential for thermoregulatory purposes which the authors compared to the use of osteoderms in crocodiles.

If, as the above study suggest, such highly vascularized structures had blood flow restricted via vasoconstriction the numerous ampullae "pipe" like structures and other hollowed out features would now serve as a buffering insulatory layer as I discussed with layers of SIGI. However the main function was of course to exchange heat with the environment.

Another study, this time looking at stegosaur plates, found the exact same pattern of extensive vascularization and large "pipe" like structures (Farlow, Hayashi, & Tattersall 2010).  Note that Tattersall is the same Tattersall from the work on Tegu lizards I discussed earlier, hmmm very interesting coincidence there.

From the abstract:

"In Stegosaurus the potential thermoregulatory role of the plates may have been greater than in other thyreophorans, by virtue of their extensive internal and external vascularity, their large size, thin cross sections above the plate base, dorsal position, and alternating arrangement."

Again, the authors make the connection between the stegosaur plates (which are actually modified osteoderms) and crocodile osteoderms. The study also shows experimental evidence that the osteoderms scutes on the back of crocodilians - in this case a Caiman latirsostris - are fundamentally important in the animals' thermal bank account.

As I mentioned earlier different dinosaurs may have varied in the relative amount of internal heat that they generated and external heat that they absorbed. It was likely not a one size fits all situation. Note also that uses for display and combat are not mutually exclusive with uses of thermoregulation.

I also noted this cryptic little sentence in the paper:

"Our observations on plate vascularity say nothing about whether heat exchange with the environment primarily involved heat gain or loss."

Hmmm, I wonder if Hayashi, Dodson & Tattersall know or suspect more than they are letting on. In either case they are being good, conservative scientists about it - not really speculating beyond the data. An approach I will not take.

Now finally onto the crocodile question. Both of the last two studies kept coming back to a comparison of the dermal structures in thyreophorans to crocodile osteoderms. This is a little weird because thyreophorans likely had some degree of endothermy while crocodiles do not. Wait a second, let me correct myself, modern crocodiles are cold blooded but several lines of evidence - a four chambered heart, avian style unidirectional breathing , erect gait - point to a history of endothermy in crocodylomorpha.

Actually what I think was going on was that "endothermic" crocodylomorphs of the past were actually  switch hitters like naked skinned dinosaurs. They could, if needed, generate heat internally but were more than happy to let their intricate osteoderm soak up rays like a built in solar panel. Later, when crocs became more specialized towards an ambush, semi-aquatic existence they abandoned the expensive physiology of endothermy and simply co-opted their solar panel osteoderms for a fully cold-blooded lifestyle.

What has muffled the issue of dinosaur physiology for naked skinned species is that from the extant phylogenetic bracket for dinosaurs - birds and crocodiles - the naked skinned crocodilians have possibly secondarily lost their capacity to generate heat. If endothermic crocodilians were still around we would have a much clearer analogy to the thermoregulatory strategy of many dinosaurs. However since the only extant endothermic archosaurs around are birds - their physiology and obligate insulatory feathers have dominated thought on how and what it means to achieve a heightened metabolism in dinosaurs.

Well then, I think that is a lot to digest. I have taken you through my thought process and how I arrived at this theory as best as I can. It doubtless needs refinement and additional testing. I might be totally right, partially right, or way off. But it is something to think about and offers some new perspective and thought on the issue of dinosaur integument, physiology and what it really means to be warm or cold blooded.

In conclusion,

Since the gradual and accumulating evidence for widespread endothermy or at least mesothermy in many dinosaurs it has become somewhat anathema to compare dinosaur thermal physiology to ectomthermic reptiles. While mounting evidence suggests the potential for widespread insulatory coats in many, if not all theropod lineages, such evidence is much thinner in many other dinosaur lineages and completely absent in several despite abundant casts and direct skin preservations. Research, thought, or even speculation has been lacking in terms of explaining how such naked skinned dinosaurs insulated themselves given wide distributions up into polar regions. Here is presented a novel hypothesis addressing insulation in such naked skinned species. An anatomical feature referred to as the subdermal interstital gridded insulatory layer(s) - or SIGIL - is outlined and referenced via several lines of evidence. Through vasoconstriction blood flow can be diminished to this layer creating an insulating, vacuum sealed layer of air visceral to the outer skin and which insulated dinosaurs from temperature extremes. Additionally, this layer could be vasodilated and engorged with blood to facilitate heat shedding or heat uptake into or from the environment respectively. This ability to control blood flow to the extremities is likely ancestral to all tetrapods and is a simple co-option of known capabilities in extant ectothermic reptiles. A novel ability to both absorb thermal energy from the environment and create internal heat is inferred for many dinosaurs via the efficient capacity for heat exchange and insulation through SIGIL. The extent of this dual functionality likely varied significantly across families and genera and offers potential insight into efficiently achieving gigantism and fast growth rates with minimal or non-existent parental provisioning of food and at rates much more efficient than other endotherms in terms of food intake. The intricate vascularized osteoderms of several types of dinosaurs are argued to represent the acme of this "dual functionality" and crocodylomorphs are inferred to have a congruent thermal function for their osteoderms as well as secondarily losing this "dual funtionality" in their evolutionary history that they once shared with their extinct archosaurian brethren.


Bell, Phil R. (2014) A Review of Hadrosaur Skin Impressions. Hadrosaurs Univ.  of Indiana Press editors David A. Eberth & David C. Evans

Bell PR (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. doi:10.1371/journal.pone.0031295

Cowles, Raymond B. (1957) Possible origin of dermal temperature regulation. Evolution Vol 12 No. 3

Grady, J. M.Enquist, B. J.Dettweiler-Robinson, E.Wright, N. A. & Smith, F. A. Evidence for mesothermy in dinosaursScience 34412681272 (2014)

Farlow James O, Hayashi Shoji, & Tattersall Glenn J (2010) Internal vascularity of the dermal plates of Stegosaurus (Ornithischia: Thyreophora) Swiss Geological Society

Prieto-Márquez A, Chiappe LM, Joshi SH (2012) The Lambeosaurine DinosaurMagnapaulia laticaudus from the Late Cretaceous of Baja California, Northwestern Mexico. PLoS ONE 7(6): e38207. doi:10.1371/journal.pone.0038207

Tattersall Glenn J., Leite Cleo AC, Sanders Colin E, Viviana Cadena, Andrade Denis V, Abe Augusto S, Milsom WIlliam K (2016) Seasonal reproductive endothermy in tegu lizards. Science Advances Jan 22 Vol. 2 No. 1

Turner, Scott J. (1984) Raymond J. Cowles and the Biology of Temperature in Reptiles. Journal of Herpetology Vol 18 No. 4.

Witton, Mark. Dinosaur Skin: Some Thoughts for Artists. December 24, 2015

"A Long habit of not thinking a thing wrong, gives it a superficial appearance of being right, and raises at first a formidable outcry in defense of custom". Thomas Paine

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Tuesday, January 5, 2016

The Disservice of Tyrannomania: Taking the Tyrant Lizards Down A Notch

This post, necessarily in my opinion, addresses both a social and scientific melange surrounding that guy and his cohorts - the tyrant lizards. I have been putting off talking about Tyrannosaurus rex and the tyrant lizards in this theropod themed kick I have been on lately because what really is new to say about them? I mean they are probably the most studied group of dinosaurs nay prehistoric critters of any type and we probably know more about not just the anatomy but foraging/biting behavior of these animals than many extant predators such as sperm whales or several giant deep sea teuthids.

To give a bit of a qualifier here I really do love and adore the tyrant lizards. I and probably several of you reading this post would likely not be here if it wasn't for them. I mean that head, the bite force, the whole package is just iconic. However I do think it necessary to take down these animals a peg or two relative to other theropods. Ok, ok maybe not take tyrannosaurids down a peg so much as elevate other theropods. I think that - both culturally and scientifically - tyrant lizards have become too much the yardstick for what it means to be a hyper-carnivorous theropod. It should always bear repeating: these animals are overgrown coelurosaurs largely independent in descent from the other large carnivorous theropods.

People love stories, are drawn to them, and understand the world through stories. When we look at the story of theropod evolution it should not go unnoticed that tyrannosaurids, and most pertinently Tyrannosaurus rex, appear at the end and culmination of the dinosaur saga respectively. I know that will be common knowledge to my readers but just breath that thought in for a second: Tyrannosaurus rex not only was for many years the largest recognized theropod but it was one of the last. The fact that it occurred in the American west only adds to the lore, mystique, and seemingly manifest destiny of this penultimate theropod to lord over all other theropods.

It is, when you really stop and think about it, quite amazing the coincidence of the largest, biggest, baddest, and last hyper-carnivorous theropod occurring at the death knell of the Cretaceous in the eternal frontier of the American west... quite a good story if you unpack it a bit. With these thoughts swimming around in your head it should come as no great stretch to imagine a popular narrative unfolding: Tyrannosaurids and Tyrannosaurus rex represent the apex, the gold standard of theropod evolution, all other theropods were lesser versions of this last and final model.

The take home message being that yeah Allosaurus was all right but it was merely a lesser, imperfect version of Tyrannosaurus rex. Mapusasaurus was cool, but still not a tyrannosaurid. Crylophosaurus, pretty neat but no T. rex. What this is all smacks of is some real neo-Lamarckian thinking. As if, for 140 million years give or take of theropod evolution, theropods finally get it right with the tyrannosaurid model after many botched, failed attempts.

Of course this way of thinking about evolution is inherently wrong. Organisms are not striving to become some ultimate model or have some type of end game in sight. Evolution is blind and groping and just hobbling together with the best fit jerry-rigged from existing parts at the time. Unfortunately I think we - including some paleontologists - lose sight of this picture and play a little bit of Monday morning quarterback with interpretations of past organisms. If failed, botched attempts are such a hallmark of the fossil record then where are they now in our present biota? What animals represent such evolutionary hiccups?

This is of course a cultural unpacking - that is not too great a controversy I am sure we can all find some truth in. But what I believe is that this narrative has spilled over into the scientific realm. What I speak of - the controversial bit I can not dispense with - is the notion that tyrannosaurids in general and Tyrannosaurus rex in particular were far and away more devestating, powerful, and all consuming than other hyper-carnivorous theropods.

Where I think this line of thinking gets the greatest cashet is the notion of bone consumption and dismemberment among tyrannosaurids - a topic of much interest for me. The general gist of tyrannosaurs being elevated over other theropods, by both lay and professionals, is most succinctly summarized as such: "only the great tyrant lizards - especially Tyrannosaurus rex - had jaws robust enough and teeth strong and stout enough to pulverize and consume bone". And the corollary: "Blade toothed theropods (i.e. everybody else besides tyrannosaurids) avoided bone assiduously and were especially careful eaters".

These statements have become a bit of a mantra among both fans of dinosaurs and most professionals. They all tow the party line - tyrannosaurids ate bone but other theropods did not. But the way I read it is different. For some reason theropods waited more than 140 million years to eat bone? Furthermore blade toothed theropods not only had to have been especially careful and dainty eaters to avoid chipping a tooth while biting into the internal bone of dinosaur prey, but had to be careful in biting into the skin of a wide variety of dinosaurs? The reason is that osteoderms - bone growing in and essentially embedded within the skin - is especially widespread among dinosaurs!! Nodosaurs, stegosaurs, ankylosaurs - essentially all thyreophora - had osteoderms. Among sauropods titanosaurids seem to have been especially bony skinned. And osteoderms were especially abundant among the various archosauromorphs that evolved with the first theropods. Blade toothed theropods lived with and evolved with osteoderm bearing animals for pretty much the duration of the Mesozoic. To take this notion seriously - that blade toothed theropods were so careful and selective in biting into their fellow prey species - is patently ludicrous in my opinion and just flies in the face of what it takes to have been at least a somewhat competent predator,  much less the most successful and persistent radiation of terrestrial vertebrae predators ever.

And besides these two arguments is the evidence of deliberate, unequivocal and sometimes alarming bone cutting, chewing, and consumption that can only be attributable to blade toothed theropods.

Tyrannosaurus rex gets all the headlines in terms of bone consumption but if you really investigate all the lines of evidence it falls short compared to blade toothed theropods in two pretty notable categories.

1) The largest and most bone riddled theropod coprolite does not - as often claimed - belong to the tyrant king but actually is the work of a particularly bone hungry Allosaurus way back in the late Jurassic. I talked about this little known tid-bit on my post on Allosaurus feeding mechanics here but it is worth a reprint:

A turd 1.52 meters long!! And 50% of it is of bone fragments - not whole bones but minced shards of bone. Exactly what would be expected to occur in the "bonesaw shimmy" method I postulated. It is worth reiterating that bone passes largely undigested through theropod guts and there is no evidence of gastroliths in Allosaurus. This bone chipping was being done in the mouth, not the work of a bone cruncher but a bone mincer.

T. rex (L) and Allosaurus (R) Two solutions to the same problem, A bone cruncher and a bone saw

So T. rex can not lay claim to the biggest and most bone riddled turd we know of.

2) The "tyrant lizard king" can not even lay claim to the biggest and deepest score marks on bone. The largest and deepest score marks on bone comes from an unknown early Cretaceous theropod that left traces on some giant sauropod caudal vertebrae in Korea:

These deep scores are not the work of T. rex nor are they likely the work of any classic late Cretaceous style "bone crunching" tyrannosaurid. Although a tyrannosauroid can not be ruled out here it is worth noting that early Cretaceous tyrannosauroids had a lot more in common with other blade toothed theropods than the latter bananna toothed killers.  I consider earlier tyrannosauroids as likely candidates for the "bonesaw shimmy". I also am starting to seriously consider that the young of giant tyrannosaurids as well as alioramids as likely candidates for neck driven vibrational feeding.

Alioramis. All the hallmarks of a true chainsaw mouth. credit SteveoC CC3.0
I think the question that we should be asking is not why did blade toothed theropods fail where tyrannosaurids succeeded in bone consumption because a thorough review of multiple lines of evidence suggests that blade toothed theropods evolved a parallel method of bone processing (i.e. chainsaw mouthed, neck driven "bonesaw shimmy" in my opinion) but what made tyrannosaurids so different from the vast majority of carnivorous theropods? That is the question in my mind although I don't really have a precise answer. Some have suggested ornithischian dominated habits stimulated a crushing/pulverizing bite. I am not certain as there were nodosaur and iguanodont dominated formations in the early-middle Cretaceous. Gregory S. Paul often spoke of an arms race between tyrannosaurids and their prey - perhaps part of this arms race involved the increasing dermal thickness of prey species? Additionally the pulverizing bite of tyrannosaurids may have allowed for more quicker and efficient killing than blade toothed theropods and therefore more time to consume prey before competitors and especially conspecifics showed up to challenge for a bite. Likely a combination of these and multiple factors...

Why have tyrannosaurids, and especially T. rex, received all the attention for bone consumption?

Well, in addition to the narrative I have played up so far, I think that there are several not entirely mutually independent reasons.

1) The pull of the recent. Tyrannosaurid bearing formations are younger, well sampled, well studied, and generally get a lot of attention. Western North America in particular. For many of the formations such as Dinosaur Provincial Park or Hell Creek there are so many good remains that meaningful statistical analyses can occur. I don't think you can do the same for let's say middle Jurassic Chinese stegosaurids or early Cretaceous Australian titanosaurids. We just have better representation of tyrannosaurid dominated formations and therefore "see" more evidence of bone utilization.

However, even from my armchair analysis of what I find peppered on the web I keep coming across published and more anecdotal references of bone chips in theropod coprolites or - especially in the Morrison formation - quite dramatic unpublished and published tooth marks on bones. I mean, check out this carvery done on a Camarasaurus ilium. Can you really chalk that up to "incidental contact"? From SV-POW credit Matt Weddel used w/permission.

theropod damage on a Camarasaurus ilium. credit Matt Weddel SV-POW

2) The hyena mindset. Bone crunching not bone slicing or mincing is how we are "prepared" to think about bone utilization since that is what the most famous bone consumers hyenas do. Since we have this mindset in place already we "expect" stout bananna toothed tyrannosaurids to access bone but blade toothed theropods not so much. But when direct and unequivocal evidence of bone utilization in non-tyranosaurid bearing formations is found it seems to be discounted, ignored, explained away, or even sometimes attributed to some unknown crocodile or as yet undiscovered lineage of tyrannosaurid in the late Jurassic or early Cretaceous. Not to, you know, the blade toothed theropods that actually lived there.

What is interesting when we think about the hyena analogy is that hyenas - which we can all agree are bone consumers - do not indiscriminately eat every scrap of bone available to them. In fact this study  on the extinct giant hyena Pachycrocuta makes the point explicit. Marrow rich long bones were highly sought after but other bones left relatively unscathed. Tyrannosaurids likewise did not eat every scrap of bone available to them - in fact there is much evidence of nipped and delicately stripped bones by tyrannosaurids despite their awesome jaws and bone crunching dentition. So just because you can eat bone doesn't mean you eat it all the time, eat other parts preferentially, or just ignore the bone. Some bones in dinosaur carcasses - especially highly pneumatic ones - were likely left alone. The more marrow rich bones in dinosaur carcasses - which no one really knows which ones they are although I suspect the ilium, caudal vertebrae, and some ends of long bones - may have been more heavily exploited.

Let us escape from the paradigm of bone crunching and think about sharks and shark attacks for a bit. Reading about shark attack accounts is both horrifying and terrific. What is amazing about them is that they are rife with accounts of sharks cutting through and sawing through human bone, literally dismembering humans while still alive. Happens all the time. These are sawing animals, not hyena like crunchers. We know from the work of Brinke et al (2015) that theropod teeth were mechanically stronger than other ziphodont predators and likely better rooted and reinforced than shark teeth. In my estimation there's nothing a shark could do that a similar sized blade toothed theropod couldn't do. Sharks shake their body left and right to allow their serrations to work their way through hard objects. Theropods shook their neck and/or body fore and aft to allow their serrations on the front and back end of their teeth (labial & lingual) to work their way through tough objects.

However, for whatever reasons these nuanced conditions that determine when to eat or not eat bone go out the window when we talk about blade toothed theropods. Despite the fact that for many dinosaurs - and especially sauropods - we have a sample size of n=1 so, unlike the abundant hadrosaurids and certatopsids in tyrannosaurid formations, it's sort of hard to make any meaningful claims on the frequency of bone exploitation in large sauropod dominated formations.  However it is also worth mentioning where are all the juvenile, teenage, and subadult sauropods in formations dominated by blade toothed theropods? Not all sauropods would have been whale sized behemoths. In any sauropod population numerically there would have been many more elk, water buffalo, rhino, and elephant sized sauropods than whale sized adults. Where are they all? These would have been sauropods too big to be swallowed whole (the baby killer specialist scenario as postulated by Dave Hone) but large enough to have easily been preserved in the fossil record. So where are they all? If blade toothed theropods were assiduously avoiding bones we should have them or at least their bones... Could it be that blade toothed theropods were in fact "disappearing" entire carcasses Joe Pesci style? ( a future post hint, hint) Let me flip the script here a bit and suggest that blade toothed theropods were eating more bones than tyrannosaurids - in fact they were eliminating entire size classes of sauropods from entering the fossil record. After all it is blade toothed theropods that hold the record for largest bone riddled poop and deepest bone score mark on bone - not the tyrant lizards.

heavily worn Carcharodontosaurus tooth. paleodirect
ditto. note wearing down of tip

"A long habit of not thinking a thing wrong, gives it a superficial appearance of being right, and raises at first a formidable outcry in defense of custom". Thomas Paine

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Tuesday, December 15, 2015

Theropod Table Manners: Did Concavenator Sport A Spiked Arm Gauntlet?

One theme that I keep addressing in this ongoing theropod series is that theropod table manners at large carcasses (i.e. who gets to eat what and when they get to eat it) is a subject of much natural interest but has received relatively little rigorous scientific attention. Instead much research focuses on how prey or landscape is partitioned but what about how large carcasses were partitioned? What I mean by this is that when we look at large carcasses - especially giant sauropods or even some of the bigger saurolophine hadrosaurs - this is a bonanza of resources that just begs to be exploited by the local theropod population. And I mean, the whole local theropod population...

There is a recurring sentiment that I keep coming across in theropod research - that overemphasizes niche partitioning to an extreme. "The young of such and such tyrannosaur species had different jaw mechanics and therefore ate different prey than the adults." Or the other corollary that "multiple coexisting large theropods had some almost benevolent driving force admonishing them to concentrate on different food stuffs to avoid too much competition etc. etc." And this is probably true to a certain extent I have to concede. However too often we assume that extreme partitioning has to occur. Modern examples beg to differ. For example lions and spotted hyenas are both social, live in the exact same habitats, and have significant dietary overlap.

When the shit hits the fan environmentally - when all the small prey has went into torpor, when all the fish have retreated with receding water or aestivated in the mud, when all the young dinos have migrated out of the neighborhood - that is when the true crucible of theropod competitive fires is stoked.  That cauldron I speak of is who gets to eat what, how much, and when at carcass gatherings. This really should come at no surprise when we look at how modern theropods i.e. birds partition carcasses especially in times of environmental stress. Let's forgo the vulture example because it is too obvious and instead pay some credence to the importance of large carcasses to many passerines, corvids, and raptors in areas of extreme winters.

What I want to attract your attention to is a sentence towards the end: "As snow depth increased, jays and great tits increased scavenging. We suggest that carrion use by scavengers is not random, but a complex process mediated by extrinsic factors and by behavioural adaptations of scavengers."

Most readers of this blog are in know well enough to be aware of carcass utilization by such birds but I think it bears a little reinforcement that such usage is often linked to environmental stress - in this case heavy snow. In the Mesozoic it could as well have been a devastating drought. In such circumstances partitioning for theropod dinosaurs as it is often invoked goes out the window and truly weird menageries of scavenging theropod guilds potentially gathered at carcasses. Yes I am even looking at theropods traditionally interpreted as herbivorous, insectivorous, and omnivorous such as ornithomimids, oviraptorids, alvarezaurids and therizinosaurids potentially joining the cue to exploit carcasses in such circumstances.

Chickadee scavenging elk carcass credit Jacob W. Frank

As interesting an aside as the thought of therizinosaurids moving in to scavenge among more traditional predatory theropods is, the take home message I am trying to convey is that such feeding bouts at  carcasses likely shaped theropod social and behavioral ecology. Furthermore it is also entirely possible that some theropods developed intimidation and defense mechanisms to gain leverage at such dinner parties.

Among mammalian carnivores we don't often think of them having defensive mechanisms at hand or combative/intimidation arsenals to dominate carcasses - aside from their teeth and claws - and growling/hissing. Social carnivores can dominate carcasses in relatively cohesive groups but, especially among solitary felids, retreat is the usual option - even when faced with throngs of scavenging birds. Several bears - armed with bulk, a thick skin, and a fat layer - are well provisioned for carcass monopolization and spotted hyenas with size, thick skin, muscular forequarters, strength, and group tactics also come to mind.

However among several extant diapsids better analogies exist that offer lessons in Mesozoic theropod table manners. Crocodiles and komodo dragons have dermal ossifications embedded in their skin which offer utility in rugged feeding encounters. It is also little appreciated that nile crocodiles will swarm en masse to drive off land based predators from carcasses. Which suggests some semblance of, dare we say it, "group social tactics"

Despite the attractiveness of looking towards big toothy lizards and crocs when it comes to how Mesozoic theropods monopolized carcasses we are literally spoiled with analogies among modern theropods that regularly feed on such foodstuffs: giant petrels and vultures. No need to look so far away phylogenetically when we have, you know, actual dinosaurs that do this stuff today. Furthermore not only are carcass feeding vultures and giant petrels better analogies phylogenetically, they are, let's be honest here,  a lot cooler to watch around carcasses than big crocs, monitor lizards, or mammalian mega-predators anyways!!

If there is one word I can use to describe these birds around carcasses it is theatrical. I really love this video of giant petrels gesticulating around a pinniped carcass. Not only does the video have a nice, grainy 1980's VHS gore movie quality to it the birds put on quite a dramatic show. The racket raises some questions - at least for me - about what these skirmishes really mean. There appears to be enough food there for all the birds yet the battles, both mock and actual, never let up. Are these confrontations really about setting up a pecking order when food is actually not so easy to come by? Another observation I want to draw attention to which I will return to later is the use of outstretched wings to maintain a "zone of influence" on the carcass that keeps other birds at bay.

Of course I would be remiss to not pay heed to one of the great Grande Guignol Theropoda performers of all time - the always on point lappet-faced vulture. Such presence. Such gravitas.

Note also in this portrait I am painting of intensely theatrical, gesticulating, and combative carcass skirmishing theropods, the last post I made on face biting theropods plays directly into this one. Grotesquely adorned, carnuncled, and gnarly faced/necked/forequarters would have all come into beautiful display and usage in such barbaric feeding bouts.

With these disturbing thoughts and images swimming inside your head let us revisit the paradoxical situation of the ulnar quill knobs in Convavenator. I refer to the situation as paradoxical because - although the trend of increasing "birdiness" in theropods is certainly a thing (or is it that increasing theropodness in birds is a better way to put it?) Concavenator was truly and squarely a carcharodontosaurid. These "land shark" megapredatorial theropods were not becoming birds nor were there antecedents on the way to or from flightedness. If anything they seem to be going in the opposite direction with smaller and smaller forelimbs and pretty much dedicated to hyper-carnivorous ways with out even the slightest hints of even an omnivore among the ranks. It is weird that quill knobs implying some sort of feather quill in these theropods appears, almost like evolution by proximity?

from Ortega 2010
There has been some skepticism which, as far as I know has been some critiques voiced online by Darren Naish and others (at least according to Wiki) that the irregular placement of these features argues against quill knobs and that they can be ulnar muscle scars. Addressing these contentions is an abstract presented at SVP2015 by Cuesta, Ortega, & Sanz that, well let me just cut and paste the abstract in their own words.

So their work seems to indicate that muscle scars don't best explain the features and that there is more diversity in these features placement in modern birds than generally assumed. Let us for arguments sake assume that their findings are valid and robust that as they put it "indicates the presence of skin appendages in Convavenator, preceding the wing feathers present in Maniraptora".

Note the careful language that they use calling them"skin appendages" instead of feathers and "preceding the wing feathers in Maniraptora".  I think that Cuesta et al. were very intelligent in making these semantic distinctions. What was most likely there - and what is most likely the most basal integument in dinosaurs - is literally a simple, shaft "quill" type feature.

The important word to keep in mind here is "quill" and here I want to revisit the observation I drew your attention to earlier of giant petrels establishing a "zone of influence" with outstretched wings at carcasses. If we imagine sharp and robust "quill" type appendages attached to these notably unusually placed "ulnar knobs" then it is not too hard to imagine their obvious utility at feeding bouts. Like the giant petrels earlier with wings outstretched these posteriolaterally projecting quills would help Concavenator "elbow in at the dinner table" among other theropods.

Concavenator "Mouth For War... Last Fix2" by Duane Nash
Of course such a general theropod gestalt has been portrayed before. Brett Booth has been drawing spiky projections coming off the arms of theropods for some time now. BTW what happened to that artist?

Such devices remind me of the ludicrous spiked arm gauntlets worn by some black metal artists. I do recall going to several punk/metal shows and how studded shoulder spikes and wrist spikes were a definite and dubious threat in the mosh pit and became banned at many venues for their danger!!

Here I wanted to depict three very different predatory theropods Concavenator and a mega-dromaesaurid and baronychine converging on a Pelecanimimus carcass. Normally there is some dietary partitioning between these predators but a drought has forced them into proximity and competition over carcasses. With it's spiked and uncouth countenance the Concavenator is able to monopolize the carcass.

Theropod Table Manners Gone Bad by Duane Nash

It's also worth noting that the outstretched wings of maniraptorine theropods could serve a similar function at carcass disputes - serving to both intimidate and establish a zone of influence at carcasses.



Referencia: Cuesta, E., Ortega, F., Sanz, J. Ulnar bumps of Concavenator: Quill Knobs or Muscular scar? Myological Reconstruction of the forelimb of Concavenator corcovatus (Lower Cretaceous, Las Hoyas, Spain). Abstracts of papers of the 75th Anuual Meeting of the Society of Vertebrate Paleontology: 111-112.

Naish, D. (2010). Concavenator: an incredible allosauroid with a weird sail (or hump)... and proto-feathers?. Tetrapod Zoology, September 9, 2010.

Ortega, F.; Escaso, F.; Sanz, J.L. (2010). "A bizarre, humped Carcharodontosauria (Theropoda) from the Lower Cretaceous of Spain" (PDF)Nature 467 (7312): 203–206. doi:10.1038/nature09181.PMID 20829793.

Selva, N.; Jedrzejewska, B.; Jedrzejewska W.;  Wajrak, A. Factors affecting carcass use by a guild of scavengers in European temperate woodland. Canadian Journal of Zoology December 2005 83(12): 1590-1601 pdf

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