Can we predict the horn shapes of fossil animals? A thought experiment starring Triceratops

Triceratops horridus with some crazy long and curving brow horns. Just speculation, right? Surprisingly, maybe not...

For palaeoartists, animals with flamboyant headgear are among the most rewarding to render, but it's not only the bony aspects of their cranial ornaments that we have to pay attention too. Animal headgear is covered with various amounts of soft-tissue that, in extreme cases, can dramatically augment the shape of the underlying bony features. The headgear of living species has a spectrum of soft-tissue coverings from nothing at all (mature deer antlers), to relatively thin dermal tissues (giraffe ossicones), through to hard keratin sheaths that can add significant depth and length to a horn or crest (most other animal horns). This excellent breakdown of a bighorn sheep face by Aaron Drake of Colorado State University (uploaded by Simpleware Software Solutions) gives a pretty good idea of how much tissue extreme keratin sheaths can add to the underlying skull.

Not all horns are augmented to the extent seen in bighorn sheep, but even modestly proportioned keratin sheaths can add a lot of bulk, length and characteristic geometry to horn tissues. Thus, anyone hoping to accurately predict the appearance of ancient horned animals should want to predict the shape of their horn sheaths along with understanding the skull geometry. This isn't easy because, though incredibly tough and resistant, keratin sheaths are still prone to decay and rarely fossilise.

Researching horn growth for an upcoming book project has made me wonder if horn sheath shape might be more predictable than we've traditionally thought, however. Horn sheath growth mechanics are relatively simple, closely related to bone shape, and constrained by the properties of heavily keratinised tissues. They're also fairly universal across across tetrapods - the same processes that make a goat horn will make the enormous keratin sheath of a skimmer jaw, for instance. These properties might allow insights into sheath shape in fossil species even when the sheath is not preserved. So what aspects of horn sheath growth might allow this, and how could we transfer them to fossil animals?

Growing horn sheaths in living animals

Keratin sheaths are dead tissue with their only living components being the cells that synthesise the keratin at the horn core/sheath interface (e.g. at the inner surface of the horn soft-tissues, see diagram, below). Because no living tissue reaches the outer horn surface, they cannot grow by adding tissue to the tip. Rather, they grow by internal accumulation of keratin layers, each new deposit displacing the older sheath from the bony core. This creates a stack of keratin cones, with new cones growing at the base and causing the horn tissues to lengthen. Continuous internal deposition and displacement of old material is what creates the soft-tissue horn extension, as each new keratin layer shoves the older material a little further from the bony tip. This makes the tip of a keratin horn the oldest part of the sheath, and in many bovids the tips are many years old. Conversely, the youngest part of the horn tissues are located at the base. As we discussed in a recent post about the horns of Arsinoitherium, this growth mechanism binds the internal horn tissues in the overlying sheaths, limiting their ability to change size or shape. Changes in size or curvature can only be achieved by displacing the older horn layers, but complicating the horn shape - say, by branching the tip - is impossible unless the sheath is shed, pronghorn-style. The sheath itself can't be modified after deposition either, on account of no living tissue reaching it. Thus, old sheaths permanently maintain the size and geometry they were created with.

Stylised bovid horn growth, heavily modified from Goss (2012).

This growth mechanic presents three important points relevant to predicting the shape of fossil horn sheaths. The first is that sheath tissues are synthesised directly over the horn core, effectively making the internal sheath margin a cast of the bone at the time it grew. The second is that the shape of new keratin layers are constrained by the keratin sheaths that preceded them. They can't deviate too radically from the overlying horn shape and the horn core of the emerging layer should mostly nestle into margins of the older one. The third is that horn extensions are not simply exaggerations of their contemporary horn core, but a keratinous record of the horn history. Geometry exhibited by the earliest growth stages is maintained in the extending sheath regardless of later changes to the horn core morphology, and only periodic shedding or heavy abrasion are likely to alter this.

This being the case, could ontogenetic changes in horn cores provide insight into the sheath shape of fossil animals? If bone shape translates to keratin sheath shape, and sheath shape dictates the horn extension profile, then a growth series of bony horn anatomy may allow us to reconstruct horn keratin accumulations that are otherwise lost to decay. Horn core profiles give us a 'cast' of the inner sheath margin for that growth stage, and we can fit these into the margin of the preceding sheath layer (which, of course, can be deduced by the shape of a ontogenetically preceding horn core). Building a stack of nestled horn core profiles creates something akin the bovid horn diagram above and tells us something of how keratin layers were accumulated for that horn shape. The very tip of the horn sheath is lost to time because we cannot predict external appearance from horn core casts (they only represent the internal structure) but if the youngest animal in a growth series is suitably juvenile, we probably aren't missing much.

As proof of concept, I've taken the horncore outlines from the schematic bovid horn above and attempted to recreate the horn shape. Stacking them was achieved by simply eyeballing the margins, trying to fit the horn core outlines together as tightly as possible without their margins overlapping. Here's how it turned out...


I don't think that's too bad. It's not perfect, but it gives a pretty good idea what's going on with the actual horn. This method is very simple, but - as outlined earlier - keratin horns are simple, so we might not need a particularly complex method to predict their shape. But you're not here to talk about ram horns: what happens when we apply this idea to a fossil animal with a well-known growth series, and how do the results compare to our conventional means of reconstructing horn sheaths in fossil taxa?

Step forward, Triceratops

Triceratops growth series from Horner and Goodwin (2006). Both species of Triceratops are included here, but the generalities of this growth sequence are thought to apply to both. Say, that brow horn curvature looks pretty changeable - what would that mean for horn sheath shape?

The super-famous horned dinosaur Triceratops is a great animal to explore this idea with. It's known from dozens of specimens representing a range of ontogenetic stages, from small juveniles to giant adults (above, Horner and Goodwin 2006 - and no, the adults in question here are not Torosaurus). Like the horns of other ceratopsids, Triceratops brow horns have well-developed epidermal correlates for keratinous sheaths (oblique foramina and anastomosing neurovascular channels - Horner and Marshall 2002; Hieronymus et al. 2009) and these textures are present in the smallest known skulls, indicating that most or all their life was spent with sheathed brow horns (Goodwin et al. 2006). Confirmation of a horn sheath comes from poorly-preserved soft-tissues found on some Triceratops horns (Farke 2004; Happ 2010).

Triceratops skulls underwent pretty major changes as they grew, including complete reorientation and allometric scaling of the brow horns. In juveniles these curve backwards, but in big adults they arc forwards (Horner and Goodwin 2006). Typically, artists have assumed that the keratin sheaths covering these horns changed shape with them. Even pros, such as Greg Paul (2016), who have stressed that the keratin sheath should extend the horn shape, render the sheaths as more-or-less reflecting the underlying horn core of a given growth stage, without any hangovers from a previous iteration of horn shape. Whether intentional or not, the implication here is that the horn sheath was dynamic - capable of changing as the animal grew.

....just like this. Note how the brow horns of this Triceratops group are clearly changing shape as the animals increase in size, but that the keratin sheaths don't reflect any earlier horn history. Hmm. Say, do you know this image is on the front of my 2018 calendar?

The model outlined above conflicts with this traditional take, however. If we assume that the horn extension was composed of a series of retained keratin sheaths, and using Horner and Goodwin's (2006) ontogenetic sequence as a basis, the resultant horn shape is pretty surprising. Stacking horn cores in the juveniles sees those recurved shapes pushed off the horn core to extend and extenuate the curve strongly, to the point where the horn tip even points posteriorly at one stage (below). As the horn base tips forward on the approach to adulthood, these arcing tips rotate with them, creating a long, elaborate set of horns which curved twice: once at the tip, and again, but inversely, at the base. If the Triceratops in this model retained the full history of their horn sheaths into adulthood, the result would be pretty fantastic: very long horns where the tips pointed 90° away from the point of the horn core. Yowsers - that's quite different from our traditional 'just make it pointier' approach.

Stacking Triceratops horn cores, mimicking how living animal keratin sheaths grow, suggest the keratinous extension of the brow horns was strongly curved even in adult animals. As in the mock bovid horn above, the horn cores were stacked simply by trying to make them fit as neatly as possible.

Which is more likely: twirly horn sheaths or the more conventional, 'dynamic' sheaths? Where morphing horn sheaths immediately lose points is their requirement for the inert keratin horn tissues to react to each horn core shape, as well as for the horn sheath history to continuously disappear. Modern horn sheaths just don't grow like this: their extensions only exist because the old keratin tissues hang around, and we have to ask how the extending sheaths are created in our 'dynamic' sheath model. There are perhaps two ways we could attain morphing sheaths: the first is through continuous eradication of old sheath material, allowing new keratin to grow over the horn core without being obscured by previous sheath layers. This might have been achieved by Triceratops shedding and regrowing sheath extensions, or by abrading outer sheath tissues away. The second is that the horns weren't covered in one sheath but several interlocking plates, like the beaks of some birds, which might allow for jimmying and reconfiguration of the horn tissues through growth without adding lots of material to the end.

Let's consider shedding first. It's possible that at least some layers of Triceratops horns were shed because exfoliation is common on keratin sheaths in living species. For instance, puffins shed the outer layer of their beaks annually, and bovids exfoliate outer layers of their horns once or twice in their lifetimes (O'Gara and Matson 1975; Goss 2012). The fact that only a superficial layer of tissue is lost prevents the sheath being significantly altered however: exfoliation alone would probably not give us particularly 'dynamic' horn sheaths.

Constant reshaping of horn tissues might be plausible if Triceratops could regularly shed and regrow the horn sheath, as performed by pronghorns. Unfortunately, these mammals show us that detecting this growth mechanic in fossil species is challenging, however. Despite their unusual habit of regrowing an entirely new sheath each year, pronghorn horn cores have similar textures to those of animals with permanent sheathing (Janis et al. 1998). There are some differences, but they're subtle. O'Gara (1990) reported that pronghorn horn cores have annually variable properties, alternating between a spongy, relatively rounded horn core when the sheath is growing, and a smooth-textured, sharper horn core at peak sheath hardness (O'Gara 1990). It's pretty well established that dinosaur skeletons grade from spongy, rounded bones to smoother, sharpened bones as they aged, so perhaps variation in texture and shape of Triceratops horns that broke this pattern could indicate horn shedding - provided these differences could be distinguished from ontogenetic or intraspecific factors. I'm not aware of any evidence of this kind, despite the frequency in which Triceratops skull bone texture is commented, but I also don't know that anyone has specifically looked for this variation yet.

Lovely, lovely epidermal correlates on the skull of Triceratops prorsus illustrated in Hatcher (1907). Note that there's no divide between the correlates on the brow horn and surrounding skull - might we expect some sort of dividing sulcus if the horn sheath was routinely cast? From Wikimedia, uploaded by Biodiversity Heritage Library, CC BY 2.0.

A more illuminating insight may be that the correlates for Triceratops horn keratin are continuous with the epidermal correlates of the face (above). Horner and Marshall (2002) noted that the horn correlates for keratin sheathing extend over virtually the entire face - including the back of the frill (this is why so many Triceratops reconstructions have smooth 'face shields' nowadays). However, what's not seen on Triceratops horns is a boundary dividing the face sheath and a hypothetical temporary horn sheath, as might be expected where two keratinous sheaths meet (I'm assuming that the entire face shield wasn't shed annually either (palaeoartists: exfoliating/shedding Triceratops face - go!) - that's not a discussion I want to get into here).

A last, more arm-wavy point against horn shedding is that it is not at all common among living animals, possibly not even being present in some close pronghorn relatives (Janis et al. 1998). If Triceratops did shed its horns, it would be part of a club with very few members. This isn't a particularly scientific argument, but we have to concede that permanent horn sheaths are - by some way - far more common than ephemeral ones, and probably the 'default' condition for horned animals. Maybe we should assume permanence until there's good reason to think otherwise?

Could wear and abrasion create our morphing, dynamic horn sheaths in Triceratops? It's certainly true that keratin horns can be worn down, sometimes considerably. Bighorn sheep, for instance, can wear away years of horn growth in a behaviour known as 'brooming', but the results do not look like our palaeoart - in other words, they don't look like these sheep stuck their horns in a pencil sharpener. Nor do they echo the shape of the underlying skeleton. Instead, the ends are blunt, frayed and fractured (below). Any Triceratops that removed horn keratin through abrasion would presumably adopt a similarly 'sawn-off' appearance, and lack neat, pointed tips.

The broomed horns of a bighorn sheep (Ovis canadensis) - notice that they're heavily and deliberately worn at the tips, but they aren't shaped into fine points. From Wikimedia, uploaded by Lake Mead NRA Public Affairs, CC BY-SA 2.0.

Might a compound horn sheath be a route to horn sheath dynamism for Triceratops? Some readers may recall that we discussed compound keratin sheath covers last month and that they typically have deep grooves between abutting sheets. We don't see grooves of this nature on Triceratops skulls despite the very obvious rugosity profile created by the epidermal tissues, so I think we have to reject this hypothesis outright. The coverage of Triceratops horn core epidermal rugosities are pretty near identical to what we see on the horns of animals like cattle or goats, and I think we have to assume they indicate a similar, all-encompassing sheath morphology.

If Triceratops horns couldn't be renewed or take advantage of a more complex sheath arrangement, the likelihood of dynamic Triceratops horn sheaths is probably low. But does this idea of continuous sheath growth and twirly horns fare better under scrutiny? It seems to pass some basic tests, at least. The Triceratops brow horn outlines fit together pretty well with only a little displacement of the preceding horn layer, which is just what in see in modern horn growth, and the fact that their horn profiles don't change suddenly is consistent with them being perpetually constrained by layers of hard tissue. The predicted Triceratops sheath profile it is unexpected, but not beyond anything we see in living animals. And it scores points generally for being a simple model that is grounded in a well-understood aspect of living animal biology, in not needing to explain the loss of sheath tissue, and for factoring data we know is relevant to horn growth in living animals. I'm not saying this model is correct, but I am thinking that explains and fits our available data better than the dynamic sheath concept.

Of course, there are still lots of caveats. Remember that the model here is rough, being based on a generic Triceratops dataset and not the growth regime of a single species. The growth series outlined by Horner and Goodwin (2006) is a good general illustration of Triceratops growth, but results might vary if we restricted the data to a single species. My illustrations do not assume any exfoliation or tip abrasion, and we still don't have any idea what the external sheath morphology - including the presence of absence of ridges, spirals and bosses - might have been like. My attempt to stack the horn core profiles has also assumed minimal sheath thickness. If the sheath was thicker, the arcs of the horn could be stretched out over longer distances. So if you're buying this concept, remember that the horn shape proposed is only a general one - it's more in keeping with our understanding of sheath grow in modern animals, but it's still quite sketchy.

So...

Perhaps the take-home message here is not, however, that Triceratops might have had loopy horns, but that there might be more to consider about fossil horn sheaths than we've assumed. Our discussion of dynamic horn sheaths does not just apply to Triceratops: artists take this approach with most horns and spikes in palaeoart, and it's clearly at odds with how most animals grow keratin sheaths today. But maybe this isn't just a topic for artists to ponder. There's potentially scope for a real study here and, seeing as fossil horn shape has a lot of functional significance, predicting sheath morphology would be a useful aid to predicting ancient behaviour. This needn't be restricted to horned dinosaurs, or even just horns, either: keratin sheaths on plates, spikes and so on grow in a similar way, and there's not reason this technique couldn't be used on other body parts, if validated. Moving this from food-for-thought-blog post to genuine science would require testing on modern species, perhaps through reconstructing living animal horns, to see how well it holds up. Recreating a schematic, 2D goat horn sheath using this method is fine, but real-world tests - especially using 3D horn casts, not just 2D drawings - might be more challenging. In the meantime, I'm curious to know what others think of all this - the comment field is open below...

"Hello, I'm Triceratops. I'll be your odd-looking concluding dinosaur reconstruction for this evening."

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References

• Farke, A. A. (2004). Horn use in Triceratops (Dinosauria: Ceratopsidae): testing behavioral hypotheses using scale models. Palaeontologia Electronica, 7(1), 1-10.
• Goodwin, M. B., Clemens, W. A., Horner, J. R., & Padian, K. (2006). The smallest known Triceratops skull: new observations on ceratopsid cranial anatomy and ontogeny. Journal of Vertebrate Paleontology, 26(1), 103-112.
• Goss, R. J. (2012). Deer antlers: regeneration, function and evolution. Academic Press.
• Happ, J. W. (2010). New evidence regarding the structure and function of the horns in Triceratops (Dinosauris: Ceratopsidae). In: Ryan, M. H., Chinnery-Allgeier, B. J. & Eberth, D. A. (Eds.) New Perspectives on Horned Dinosaurs: The Royal Tyrrell Museum Ceratopsian Symposium. Indiana University Press. pp. 271-281.
• Hieronymus, T. L., Witmer, L. M., Tanke, D. H., & Currie, P. J. (2009). The facial integument of centrosaurine ceratopsids: morphological and histological correlates of novel skin structures. The Anatomical Record, 292(9), 1370-1396.
• Horner, J. R., & Goodwin, M. B. (2006). Major cranial changes during Triceratops ontogeny. Proceedings of the Royal Society of London B: Biological Sciences, 273(1602), 2757-2761.
• Horner, J. R., & Marshall. C. (2002). Keratinous covered dinosaur skulls. Journal of Vertebrate Paleontology 22(3, Supplement):67A.
• Janis, C. M., Manning, E., & Ahearn, M. E. (1998). Antilocapridae. In: Janis, C. M., Scott, K. M., & Jacobs, L. L. (Eds.). Evolution of tertiary mammals of North America: Volume 1, terrestrial carnivores, ungulates, and ungulate like mammals (Vol. 1). Cambridge University Press
• O’Gara, B. W. (1990). The pronghorn (Antilocapra americana). In: Bubenik, G.A. & Bubenik, A. B. (Eds). Horns, pronghorns, and antlers: evolution, morphology, physiology, and social significance, Springer-Verlag. pp 231-264.
• O'Gara, B. W., & Matson, G. (1975). Growth and casting of horns by pronghorns and exfoliation of horns by bovids. Journal of Mammalogy, 56(4), 829-846.
• Paul, G. S. (2016). The Princeton field guide to dinosaurs. Princeton University Press.

The appearance and lifestyle of Thalassodromeus sethi, supercrested pterosaur

Thalassodromeus sethi, a juvenile Mirischia asymmetrica, and half a spinosaurid hang out in Cretaceous Brazil. The spinosaurid wants to go home.

One of my favourite pterosaurs is the Brazilian thalassodromid Thalassodromeus sethi: a large (4-5 m wingspan) Cretaceous azhdarchoid known only from a broken skull and cranial fragments of disputed affinity (Kellner and Campos 2002; Veldmeijer et al. 2005; Martill and Naish 2006). Characterised by an especially large bony cranial crest, toothless jaws and a robust skull construction, Thalassodromeus gained fame (and it's name, which translates to 'sea runner') from a presumed habit of skim-feeding. Long-time readers or pterosaur aficionados will know that multiple studies have suggested pterosaurian skim-feeding was unlikely on anatomical grounds (we discussed this most recently here and here) and was especially improbable for large species on account of the huge energy demands of ploughing large, blunt jaws through water (e.g. Humphries et al. 2007). A lack of skim-feeding habits does not make Thalassodromeus any less interesting however: it's a large, charismatic animal with a heavy dose of pterosaur weirdness, so there's still plenty to like. I recently had reason to overhaul the Thalassodromeus painting from my 2013 book (above) and took the opportunity to revisit my understanding of this animal's anatomy. The process had me fall for Thalassodromeus' cresty charms all over again, and I've taken this as impetus to share the love here.

The continuing puzzle of the Thalassodromeus skull

Thalassodromeus sethi skull elements as figured in Witton (2013). Note how the holotype skull is a giant jigsaw with well- and ill-fitting elements. The little (drawn) jaw to the left is no longer referred to Thalassodromeus, but is now the holotype of the dsungaripterid Banguela oberlii. This photo composite was created using photographs provided by the excellent Andre Veldmeijer and Erno Endenburg. 

The holotype skull of Thalassodromeus is pretty well preserved as pterosaur fossils go, but isn't quite as exceptional as it first appears (above). Though three dimensionally preserved and uncrushed, it's suffered damage in several areas and is broken into multiple pieces, some of which are ill-fitting with the rest of the skull or are missing entirely. It's a jigsaw puzzle which is complete enough to get the general picture of the skull shape, but some large areas remain open to interpretation. Pterosaur literature records that different bits of this specimen were once scattered across American research institutions and we have to hope that some of the last missing elements are still in a drawer somewhere, waiting to be reunited with the rest of the skull.

That the shape of the Thalassodromeus skull is somewhat ambiguous is evident by our history of T. sethi skull reconstructions (below). The first reconstruction - published in Kellner and Campos (2002) - is a little odd in that it shows a downturned, irregular upper jaw with a straight mandible. It also features 'classic' structures that we've come to know and love in this species: that badass 'V'-shaped chunk missing out of the back of the crest, a boss-like structure on the upper jaw, and a partly hooked mandibular tip. This reconstruction has always looked a little odd to me because I'm not sure how the animal is meant to close its mouth. A second reconstruction, which I presented in my 2013 book, was similar to the first except for showing both jaws as straight, without a downturned upper jaw. My logic was that Thalassodromeus should look something like the better known thalassodromid Tupuxuara, which has entirely straight jaws. Later, Headden and Campos (2015) presented a third interpretation, where the mandible was bent down at the base of the mandibular symphysis. Jaime Headden's (as far as I know unpublished) skull reconstruction hints at further differences from previous reconstructions, including a lack of that cool 'V' notch in the back of the crest.

Select T. sethi skull reconstructions, with my latest take at the bottom right. All three agree on some aspects of basic morphology, but there's not quite enough data to eliminate some possibilities of jaw and crest shape. Note that the 2017 skull outline is pretty conservative - the crest may have been longer and taller.

Which of these, if any, is correct? We await a comprehensive description of the skull to fully augment our understanding of T. sethi anatomy but, based on published information, it's likely that some of our earlier interpretations were erroneous. The gnarly crest shape drawn by Kellner and Campos (2002) probably takes damaged margins and missing elements too literally - this includes that awesome-looking V-shaped notch at the end, which is likely just another chunk of missing crest (this is certainly reported by colleagues who've examined the skull first hand). There's also no obvious reason why the mandible should be restored with an upturned tip. This interpretation was at least partly fuelled by an upturned jaw tip once referred to Thalassodromeus (Veldmeijer et al. 2005), but this specimen has since been considered a new genus of dsunagripterid pterosaur (Headden and Campos 2015).

It's also looking possible that - as indicated by Headden and Campos (2015) - both sets of Thalassodromeus jaws were downturned. It's difficult to be confident about any jaw reconstruction in this animal because these regions are not well represented in the holotype skull, but preserved elements of the upper and lower jaw margins imply a subtle downturn at the base of the rostrum and mandibular symphysis (and no, this isn't an effect of distortion or damage). Either Thalassodromeus had some sort of wibbly jaw shape or else it had a downturned jaw similar to azhdarchoids such as Tapejaridae* and Caupedactylus**. Whether this is convergence or further evidence of a close relationship between thalassodromids and tapejarids depends on your take on azhdarchoid interrelationships - this is still an area of disagreement that would benefit from dedicated investigation.

*of which thalassodromids - or thalassodromines - may, or may not be, a subdivision of. Ah, pterosaur phylogeny...

**I'm as confident as I can be that Caupedactylus is synonymous with my own "Tupuxuara" deliradamus. I should really write this up one day...

But hey, evidence for facial tissues and life appearance!

Thalassodromeus has some interesting features which allow us to reconstruct some aspects of its facial anatomy in detail, even in lieu of soft-tissue preservation. The crest of Thalassodromeus is marked by very conspicuous neurovascular grooves which were linked to a thermoregulatory function by Kellner and Campos (2002). They look pretty near identical to the sorts of branching grooves you find under bird beaks however (below), and my suspicion is that they're not a specialisation for controlling body temperature but simply a correlate for a keratinous sheath (Hieronymus et al. 2009). Similar grooves are seen on crestless parts of pterosaur jaws (the holotype of Serradraco sagittirostris has some especially obvious ones, for instance - see Rigal et al. 2017) as well as under the keratinous horns and beaks of animals everywhere. We don't need to imagine a unique function for these grooves just because they're on a big pterosaur crest, they're a standard variant of tetrapod skull anatomy.

Branching neurovascular networks on the Thalassodromeus crest - this is the region above the eye and posterior end of the nasoantorbital fenestra. Note the conspicuous groove crossing across the photo - this is the boundary between the premaxilla and underlying skull bones. From Kellner and Campos (2002).

Keratinous sheaths can have sharp margins which leave signature textures on the underlying skull. Bony steps or 'lips' can mark the transition to another tissue type, or a groove may form where one sheath plate abuts another. Both are evident in bird species which have beaks composed of multiple plates instead of a single keratinous covering (below), and we can look for similar features in fossil skulls to make predictions about life appearance. In Thalassodromeus we see a deep groove running along the boundary between the large premaxillary bone (the bone which makes up the jaw tip and top region of the entire crest) and the frontoparietal region (the base of the crest from the eye region backwards). Correlates for keratinous sheaths occur on both sides of this groove, so there's a chance that the crest covering was a compound structure composed of two abutting sheaths rather than one continuous one. If so, we might have been able to see this join on the live animal, just as we see the joins on the beaks of certain birds.

Gannet (Morus bassanus) skull with keratinous sheaths removed. Note the branching neurovascular impressions and deep grooves that mark the position of keratinous sheaths - we would predict a compound beak from these textures if we only knew gannets from fossils.

Can we test this idea? We could chop up our super-rare Thalassodromeus specimens to see if  histological data matches the surface texture interpretation (it's not only bone surface texture which records epidermal types - see Hieronymus et al. 2009) but I'll wager that most folks don't want the Thalassodromeus holotype carved up any more than it already is. Happily, there are other lines of data that might help us out. The first is the presence of the crest groove itself. Pterosaur skulls are normally devoid of sutures between bones because, in adults, they fuse so solidly that all trace of the original bone outlines is obliterated. Thus, the presence of a conspicuous groove in a mature Thalassodromeus specimen indicates that something unusual was happening, and influence from facial tissues is a well-known phenomenon that could explain this feature.

Schematic take on thalassodromid crest growth, from Martill and Naish (2006). The crest doesn't begin fully formed in juveniles, with the premaxillae (dark shading) having to overgrow the rest of the skull. Fun fact: my first ever PR palaeoart, now 11 years old, was to publicise this study.

A second line of support stems from studies into thalassodromid crest growth (Martill and Naish 2006). The "upper" (or premaxillary) component of the thalassodromid crest does not cover the skull in juveniles: rather, it has to overgrow the skull as the animal ages (above and below). Keratin sheaths are difficult to modify once formed because they're thick and inert (Goss 2012), so it's likely that parts of the premaxillary sheaths formed in juveniles migrated with the bone over the skull, meeting their counterparts at the skull posterior in later life. If the sheaths couldn't join once they met because they couldn't be modified or resorbed, they probably continued to grow as a compound cover, explaining the retention of an obvious groove between the two crest-forming bones. I find this idea pretty neat. Features like grooves on beaks or crests are nuances of animal appearance that are mostly lost to time but are important to characterising the appearance of living species. The idea that Thalassodromeus (and probably thalassodromids) had this feature makes them that little bit more real. Painting the images for this post certainly felt a little more like painting an animal than illustrating a hypothesis, just because of this detail.

Thalassodromid crest growth and compound keratinous sheathing, modelled by T. sethi. Note how the juvenile has an obvious 'two part' crest composition, and that the front/upper part (the premaxilla) sits on top of the posterior (frontoparietal) elements. With enough time, they form the monster-sized crest we know from big thalassodromid specimens. See Martill and Naish (2006) for more details.

Skull mechanics and lifestyle

It would be remiss to write about Thalassodromeus without mentioning its robust skull construction. The skull is proportionally wide, has especially deep jaws, a partly sealed orbit region, and the mandibular symphysis has a robust 'teardrop' cross section instead some flimsy crest. Its robustness is especially obvious when compared to the skull of the otherwise similar Tupuxuara (below), which has more typically open and airy pterosaurian cranial architecture. Thalassodromeus thus has a skull which looks like it could take a little more punishment than that of an average pterosaur, and this correlates nicely with observations that the regions for jaw adductor muscles are expanded on both the skull and lower jaw (Witton 2013; Pêgas and Kellner 2015). It's unsurprising that foraging hypotheses for Thalassodromeus have favoured forceful feeding habits such as skim-feeding (Kellner and Campos 2002) or being a predator of small-to-medium animals in terrestrial settings (Witton 2013).

Tupuxuara leonardii skull and mandible - looking pretty slender compared to the star of this post.

The possibility of downturned jaws in Thalassodromeus becomes especially interesting in light of its robust skull. Long, curving bones are a biomechanical paradox because they're weaker in compressive loading than a straight equivalent. This is, in part, because applying loads directly to both ends of a curved bone induces bending stresses even though the bone is not being bent in a traditional fashion. This is why big, slow animals tend to have straighter limb bones than smaller ones: they benefit from the increased strength of straight shafts, and they load their limbs in compression virtually all the time. From this perspective, the curved jaw of Thalassodromeus might seem like a disadvantage, being weaker under compression than that of a straight jawed animal. If striking violently at prey head on, the straight jawed species might be less likely to go home with a broken jaw.

However, curved bones are superior to straight bones at handling unpredictable, dynamic stresses. Curvature introduces predictability to stress distribution throughout a bone shaft, so they behave more reliably under a variety of loading regimes, be it compression, bending or twisting. A bone which responds to stress in the same way no matter how you deform it is easier to manage behaviourally, and to optimise mechanically, than a straight bone, and loss of raw strength created by bone curvature can be compensated for by modifying cross sections, shaft diameters and internal reinforcement (Bertram and Biewner 1988). These attributes have not been ignored by evolution and, in fact, most animal limb bones are curved to some degree to take advantage of these effects (Bertram and Biewner 1988). The superior compressive performance of a straight bone may not be as advantageous as the reliability and potential all-round stress resistance of a curved variant so, in simple terms, if you're planning some crazy stunts with your long bones, you want curved bone shafts, not straight ones.

A curved jaw thus complements the strong skull and jaw muscles of Thalassodromeus. If Thalassodromeus used foraging mechanics which were forceful or violent - such as catching big or powerful prey types, or using its beak to batter or tear at other animals - a curved beak may have served it well. This jaw shape - assuming we've interpreted it correctly, remember - could be further evidence of foraging habits at the more explosive and exciting end of the pterosaur ecological spectrum. Exactly what Thalassodromeus did for a living remains unknown, but it's hard not to compare these cranial features with other ideas of robust, terrestrial azhdarchoid predators - maybe this 'large pterosaur predator' niche has a longer roster than we've traditionally thought.

Hypothesis B: spinosaurids were allergic to curved jaws. Hey, it could happen.

Thalassodromids and their azhdarchoid kin are exceptionally interesting animals and we could probably talk about them all day, but we'll have to stop there. Coming soon: pterosaurs from the other end of the pterodactyloid spectrum, or a return to the world of extinct mammals. Probably.

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References

• Bertram, J. E., & Biewener, A. A. (1988). Bone curvature: sacrificing strength for load predictability?. Journal of Theoretical Biology, 131(1), 75-92.
• Headden, J. A., & Campos, H. B. (2015). An unusual edentulous pterosaur from the Early Cretaceous Romualdo Formation of Brazil. Historical Biology, 27(7), 815-826.
• Hieronymus, T. L., Witmer, L. M., Tanke, D. H., & Currie, P. J. (2009). The facial integument of centrosaurine ceratopsids: morphological and histological correlates of novel skin structures. The Anatomical Record, 292(9), 1370-1396.
• Humphries, S., Bonser, R. H., Witton, M. P., & Martill, D. M. (2007). Did pterosaurs feed by skimming? Physical modelling and anatomical evaluation of an unusual feeding method. PLoS Biology, 5(8), e204.
• Goss, R. J. (2012). Deer antlers: regeneration, function and evolution. Academic Press. 
• Kellner, A. W., & de Almeida Campos, D. (2002). The function of the cranial crest and jaws of a unique pterosaur from the Early Cretaceous of Brazil. Science, 297(5580), 389-392.
• Martill, D. M., & Naish, D. (2006). Cranial crest development in the azhdarchoid pterosaur Tupuxuara, with a review of the genus and tapejarid monophyly. Palaeontology, 49(4), 925-941.
• Pêgas, R. V., & Kellner, A. W. (2015). Preliminary mandibular myological reconstruction of Thalassodromeus sethi (Pterodactyloidea: Tapejaridae). Flugsaurier 2015 Portsmouth, abstracts, 47-48.
• Rigal, S., Martill, D. M., & Sweetman, S. C. (2017). A new pterosaur specimen from the Upper Tunbridge Wells Sand Formation (Cretaceous, Valanginian) of southern England and a review of Lonchodectes sagittirostris (Owen 1874). Geological Society, London, Special Publications, 455, SP455-5.
• Veldmeijer, A. J., Signore, M., & Meijer, H. J. (2005). Description of two pterosaur (Pterodactyloidea) mandibles from the lower Cretaceous Santana Formation, Brazil. Deinsea, 11(1), 67-86.
• Witton, M. P. (2013). Pterosaurs: natural history, evolution, anatomy. Princeton University Press.

The horns of Arsinoitherium: covered in skin or augmented with keratin sheaths?

1.5 Arsinoitherium zitteli trotting about Eocene Egypt, looking a bit like they could be advertising farm products. But what's with those more elaborate than usual horns?

The horns of the giant, Egyptian, Oligocene afrotherian Arsinoitherium zitteli are probably a key factor in its status as one of the better known fossil mammals. Though perhaps not quite as popular as mammoths or sabre-toothed cats, this 3 m long, four-horned species has enough osteological charisma to warrant display in many museums as well as starring roles in books and films (including, cinema fans, narrowly missing out on an appearance in the 1933 King Kong). And unlike a fossil rhinocerotid (to which it is not at all related), Arsinoitherium doesn't need us to imagine the shape of its ornament in life: two enormous horns project over the end of the snout and another pair of smaller, sub-vertical horns grew above the eyes.

Recently, I painted a portrait of Arsinoitherium for an upcoming book project and, based on my understanding of epidermal osteological correlates, I threw a keratinous sheath over the entire horn set (below). This is not a typical reconstruction - Arsinoitherium has been reconstructed with 'regular' mammalian skin (perhaps better termed 'villose skin' - Hieronymus et al. 2009) on its horns for decades but, as we all know, popularity and longevity don't always equal 'credibility' when it comes to fossil animal reconstructions.

Arsinoitherium zitteli, sporting antelope-like horn sheaths.

Shortly after this image was shared online, Darren Naish, he of Tetrapod Zoology (and the upcoming TetZooCon meeting, which you should definitely attend if you're in the UK and reading this article), had a question: had I checked horns without keratinous sheaths, like deer antlers or giraffe ossicones? It turns out that these are the more typical artistic analogues for Arsinoitherium horns, and their reconstruction without a keratinous sheath reflects this interpretation. It wasn't a question I could easily answer because I'd zeroed in on a keratinous sheath quickly in my research for the image and, in a major palaeoart faux pas, hadn't given due consideration to other options. Simultaneously, neither of us could argue for any model of Arsinoitherium horn coverage confidently because no-one has looked into this in any detail. There are some ideas in the literature, but they are fleeting and conflicting (keratin sheaths - Anonymous 1903; Andrews 1906; Osborn 1907; or skin, Prothero and Schoch 2002; Rose 2006).

It's difficult to turn away a good palaeobiological mystery, and because I like to make sure my work is as credible as it can be, I followed this question up with more research. I reasoned that the structure, development and surface texture of the three major types of mammalian headgear - horns, ossicones and antlers - could be compared to Arsinoitherium horns to see which, if any, is the best match and indicator of life appearance. Looking into this has been very informative and might be of interest to fellow palaeoartists as well as those interested in cool fossil animals, so I thought I'd share my thoughts and process here. We'll start by looking at Arsinoitherium horns themselves, then move through modern potential analogues, and finally compare them at the end to see which model seems most apt.

Arsinoitherium horns: growth, structure and surface texture

PV M 8463, the most famous of all Arsinoitherium skulls, as illustrated in Andrews (1906). Note the dotted lines across the horns - they mark the end of the preserved skull and the start of reconstructed elements.

As noted above, Arsinoitherium has two pairs of horns: a larger anterior set, which grows out of the nasal bones and over the snout, and a smaller, second pair formed from the frontal bones, above the eyes. Both sets are highly conspicuous and dominate the skull, the weight of the anterior pair presumably accounting for the development of a bony bar between the nostrils in mature animals (Andrews 1906; Court 1992). Note that the Arsinoitherium horns we're used to seeing in museums are partly reconstructed and thus of limited use as reference material. Most exhibited skulls are based on NHMUK specimen PV M 8463 (above), a 'moderately sized' adult specimen (Osborn 1907) in which neither horn is complete (Anonymous 1903; Andrews 1906). This skull was among the earliest Arsinoitherium skulls collected from Egypt but was restored rapidly once it arrived back in London. A 1903 report describes how the skull was:

"...brought home by Dr. Andrews from Egypt, and after cleaning, strengthening, and the restoration of parts deficient on the left side by modelling from the right side, is now exhibited in the central hall of the Natural History Museum in Cromwell Road."

Anonymous, 1903, p. 530

The fact that some parts of the skull were in less than stellar shape is evident from this photo of PV M 8463 (from the NHM's data portal): note the variation in colour and texture, reflecting places of reconstruction against real bone. Thus, while the familiar Arsinoitherium museum skull is a useful reference for morphology, illustrations and descriptions in technical literature will be more informative for reconstructing their integument. I've based my assessment mostly on Charles Andrews (1906) monograph, as well as that of Court (1992).

Structure. Both horn pairs of Arsinoitherium are relatively simple in gross shape and maintain the same basic morphology throughout their lives (below), though the horns of mature animals are wider, taller and more pointed than those of juveniles. The figures presented in Andrews (1906) show an increase in anterior horn base length from 41.6% in the smallest specimen to over 56% in the largest. Both horn sets are hollow, with vast internal cavities being supported by sheets of trabecular bone. In some places the exterior bone walls are surprisingly thin, only 5-10 mm (Andrews 1906).

Arsinoitherium zitteli skull ontogeny. I wonder if the horns of the largest skull should be reconstructed as longer and taller, given their arcs in the completely known skulls and gentler tapering of other nasal horn specimens (e.g. Sanders et al. 2004). Skull drawn from Andrews (1906), skull measurements by me.

Surface texture. The base of the horns are marked by deep, broad and branching neurovascular channels running from the facial region onto the horns themselves. The horn shafts are rugose on account of many deep pits, grooves and branching channels aligned along their long axes (Andrews 1906; Sanders et al. 2004). The horn tips of young animals have an especially spongy texture at the tip, presumably reflecting growth of the horn core (Andrews 1906). These textures are not typical of the rest of the skull, which are of a more typical, smooth mammalian variety even in regions where skin was probably in close proximity to the bone (e.g. the zygomatic arch, over the braincase). This is an important distinction, implying that a different epidermal configuration - different skin types, in other words - was present on the horns compared to the rest of the skull.

Having learned something of the Arsinoitherium condition, let's take a look at how modern horns, antlers and ossicones compare...

Analogue 1. Bovid-style horns (keratinous sheaths over a bone core)

Bovid horns typify a widely used approach to cranial ornamentation and weaponry across Tetrapoda. They are perhaps the simplest approach to producing a sturdy cranial projection, being little more than a bony horn core covered in a hard keratinous sheath and are permanent feature in almost animals that bear them. The one exception is the pronghorn, which sheds its horn sheath annually (it also isn't a bovid). Biology, eh: can't we have one rule without an exception?

Bovid (bighorn sheep, Ovis canadensis) horn anatomy. From Drake et al. 2016.

Structure. Bovid-style horns are composed of a hollow bony core lined with trabeculae that strengthens an otherwise thin-walled structure (Drake et al. 2016). The bone portion only occupies the basal portion of the horn, anchoring ever-growing bands of keratin that grow from the bone-keratin interface, not at the horn tip (below). This means that the tip of the horn sheath is the oldest part of the structure and that the base of the sheath is the youngest. Because keratin sheaths are inert, dead and tough tissue, they cannot be remodelled once they are formed. This dictates that the growing bony core has to forever comply with the shape of the horn sheath and cannot change shape much over time. Size changes can be accommodated as wider and longer sheath layers can cover expanding horn cores, but it is not possible to form a more complex shape - say a branch or spur - at the tip of the horn. And before anyone mentions pronghorns: their horn branches are entirely soft-tissue: the bony core retains a simple shape.

Schematic bovid horn growth, adapted from an illustration in Goss (2012).

Surface texture. Deep, oblique foramina and branching neurovascular canals characterise the surface texture of bovid horn cores. This rugosity profile is most pronounced in younger animals, but is maintained to a lesser extent in adults - in many bovids, the horns never stop growing, they just slow down a great deal. This texture is not unique to horns but accompanies many structures with keratinous sheathing, including claws and beaks (e.g. Heironymus et al. 2009). A sharp lip and particularly deep rugosity can mark the transition from horn to facial skin.

Analogue 2. Giraffe ossicones (skin over ossified dermis)

Giraffes have awesome skulls with two - and often more - ossicones that are covered in the same skin as the rest of their faces (Davis 2011). Their approach to cranial ornamentation is restricted to the giraffe clade and their fossil relatives, but might be an apt model for aberrant extinct forms and is worth reviewing here. Clive Spinage (1968) provides an excellent overview of ossicone structure and development: the following is taken from his work.

Structure. Ossicones are low humps or columnar protuberances, continuous with the surrounding skull anatomy but formed from dermal ossifications, not outgrowths of skull bones. They eventually fuse with the skull in adult life but, unlike the underlying skull bones, ossicones are solid and very dense - they are described as being 'ivory-like' in compactness and hardness by Spinage (1968). Mature specimens show increasingly complex shapes including development of swollen tips on the frontoparietal 'horns', as well as hornlets and bosses across the major 'forehead' ossicone. Having an adaptable, living integument is essential to this process, as the ossicone covering needs to change shape to reflect the changing size and complexity of the underlying bone.

Giraffe skulls are full of sinuses, but they do not extend to their ossicones, which are extremely dense. From Spinage (1968).

Surface texture. Generally smooth with oblique foramina in juveniles and young adults, but increasingly gnarly in mature animals (more so in males). The continued ossification of dermal tissues produces a conspicuous pitting and 'flaky' rugosity profile that overgrows the surrounding skull bones and obscures the textures from earlier growth stages. In mature males, this rugosity can overgrow the entire upper surface of the skull and enhance the height and ornamentation of the ossicones considerably.

Young adult male giraffe skull by Wikimedia user Nikkimaria, CC BY-SA 3.0. Note the flaky, irregular textures of the ossicones and their complex shape: they are much more intricate and developed than those of less mature animals. There's room for more irregularity and texture on this skull, too: the skulls of old males look like they have cathedral spires growing from their faces.

Analogue 3. Deer antlers (bony projections atop cranial pedicles)

The familiarity of deer antlers allows us to forget what remarkable and unusual structures they are. Present almost universally in male deer (and in female reindeer), these elaborate, sometimes enormous structures are cast and regrown each year using a regenerative process that is the source of much anatomical and medical interest - no other mammal can regenerate such a complex appendage in this way, and the speed of the regeneration process is remarkable. Antlers are so unusual that they are only partly useful to our discussion here: we are primarily interested in antlers when they are covered in their velvet (specialised antler skin), as this is most comparable to the likely Arsinoitherium condition. Antler skin itself is interesting as, although it is continuous with the skin of the underlying pedicle, it lacks sweat glands and arrector pili (the tiny muscles that pull hair up or give us goosebumps) (Li and Suttie 2000). The antler pedicle (the permanent bony base) in contrast, is covered in the same type of skin as elsewhere on the body (Li and Suttie 2000).

A happy-looking moose (Alces alces) with his fuzzy antlers. Note the visible blood vessels on the underside of each palm. Photo by AlbertHerring, in public domain.

Structure. Both antlers and pedicles are solid, and antlers can - by virtue of growing at their tips - become more complex as they grow, developing from single spurs into networks of brows, tines and palms. As with giraffes, antler skin needs to be living and adaptable to facilitate this: a covering of inert keratin would preclude this form of growth.

More Alces antlers, this time without velvet. Note the long, branching channels. By Wikimedia user Nkansahrexford, CC-BY-4.0.

Surface texture. Antlers have variably developed rugosities consisting of conspicuous, long and branching channels impressed into smooth bone or around prominences and tubercles. These grooves are the impressions of blood and nervous networks that facilitated rapid antler growth. These textures are easily discerned even from a distance, and thus contrast with the texture of the pedicles, which are smoother and lined with relatively shallow, narrow and long impressions of vascular networks. It is unusual for hairy skin to leave such a significant osteological scar on underlying bone: typically, this form of epidermis leaves little to no remnant on skull bones (Hieronymus et al. 2009).

Arsinoitherium vs the analogues

Having looked at three major types of cranial projection in living animals, which - if any - is the best match the condition in Arsinoitherium? Giraffe ossicones are incomparable to Arsinoitherium horns in several aspects, perhaps the most significant being their increasing complexity and development of flaking bone textures in later life. Furthermore, the development of giraffe ossicones from bony growths in dermal tissues suggests a fundamentally different relationship between skull and dermis than of Arsinoitherium, where the bony horn component represents elongated skull bones. There's enough differences here to question whether giraffe ossicones are a good model for the life appearance of Arsinoitherium horns.

In being formed of polished, deeply vascularised bone, deer antlers are closer approximations of Arsinoitherium horns. However, there is so much weirdness associated with deer antler formation and tissues that they almost remove themselves from meaningful comparison to permanent skull horn cores. The fact that antler velvet, as hairy skin, is (to my knowledge) unique in leaving deep vascular channel impressions is a major issue here, implying that either antler bone is unusually susceptible to neurovascular imprinting (do they grow so fast that they grow around their blood vessels?) or that velvet is better at altering bone textures than other skin types. Both scenarios point to antlers having some endemic oddness about them, which complicates their use as a model for life appearance of non-antlered species.

All is not lost with the cervid data, however: antler pedicles are comparable to Arsinoitherium horns in being permanent outgrowths of bone, and they also have neurovascular impressions. However, these shallow grooves compare poorly to the deeper channels and pitting of Arsinoitherium horns. Indeed, there is little about antler pedicle texture to distinguish them from the surrounding skull bones, whereas the opposite is true for Arsinoitherium.

Our comparisons improve with the bovid horn condition, which seems to chime with the Arsinoitherium skull in many regards. Both are hollow outgrowths of skull bones supported by internal trabeculae; both have bone textures characterised by deep, bifurcating neurovascular channels as well as conspicuous longitudinal grooves and oblique foramina; and both maintain the same basic shape throughout growth - excepting some basic changes in base width and horn length. Further similarities include the development of particularly deep rugosties at the base of the horn cores, which is evident in at least large Arsinoitherium skulls (Andrews 1906). This interpretation is consistent with one of the longer (but still rather short, if we're honest) interpretations of the blood vessel impressions in Arsinoitherium:

"These channels evidently lodged blood-vessels which served for the conveyance of blood to or from the covering of the horn, and judging from the marked way in which both these vessels and those on the anterior face of the horns impress the bone, it seems probable that the covering was hard and of much, the same nature as that clothing the horn-cores of the cavicorn ruminants."

C. Andrews (1906), p. 7

So...

Of the three models looked at here, it seems the basic structure and textural package of bovid-like horns best matches what we see in Arsinoitherium. Moreover, unlike the antler or ossicone models, there's no obvious mismatches with this configuration: pretty much everything we would correlate to a bovid-like horn anatomy seems present on or in the Arsinoitherium skull. The idea that a keratinous sheath might have existed in Arsinoitherium might seem odd, but it is not that outlandish given the apparent ease through which keratinous sheaths evolve. This is, after all, the tissue which has covered just about every claw, hoof, nail, horn, cranial dome and beak that has ever existed, whereas ossicones and antlers seem like specialised, clade-restricted approaches to cranial projections. The functionality of hollow Arsinoitherium horns is further reason to suspect a horn sheath. Studies of bovid horns suggest hollow cores and keratin sheaths compliment each other biomechanically, optimising the horns for for impact dissipation (Drake et al. 2016 and references therein). Stripped of a keratinous sheath, we find that hollow horn cores are great at transmitting energy but are brittle and prone to buckling and fracturing under heavy loading. It's only with a tough, fracture resistant keratin sheath that these structures can avoid breaking under heavy use so, if Arsinoitherium employed its horns for anything vaguely physically demanding, they probably needed a keratinous sheath.

It's possible, of course, that these structures were just for show, but they do look like they had a function beyond display. It occurs to me as I write this that this scene recalls the painting from Ghostbusters II. I guess we'll call this guy 'Vigo'. 

Putting all this together, I feel the case for a keratinous sheath over the Arsinoitherium horn sets is reasonable, at least so far as it can be made with publicly available data. Aspects of morphology, growth, surface texture and - perhaps - functionality seem fully consistent with a bovid-like horn configuration, whereas other potential models are less comparable. From an artistic perspective, this is exciting: horn sheaths can be extremely elaborate structures and exaggerate the size of the horn core considerably, so Arsinoitherium might have been far more extravagant in life than we have previously imagined. I've tried to hint at this with my reconstructions - remember, this animal wasn't just a funny-faced rhinoceros!

But - before we go crazy with this - do remember that the core of this analysis - the interpretation of Arsinoitherium headgear - is entirely literature based. I've not seen original specimens nor even modern, high-res imagery of an unreconstructed skull (this wasn't for lack of trying - the literature on these animals needs updating). Thus, while I've tried to be as thorough as I can with my observations, and as cautious as I can with my interpretations, I might be ignorant of some important detail. Take everything here with an appropriate pinch of salt, and please chime in below if you can provide superior insight. There's clearly scope for a more detailed study on this topic and, given how unique the horns of Arsinoitherium are, there might be some interesting functional findings to emerge from further investigation.

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This blog is sponsored through Patreon, the site where you can help online content creators make a living. If you enjoy my content, please consider donating $1 a month to help fund my work. $1 might seem a meaningless amount, but if every reader pitched that amount I could work on these articles and their artwork full time. In return, you'll get access to my exclusive Patreon content: regular updates on research papers, books and paintings, including numerous advance previews of two palaeoart-heavy books (one of which is the first ever comprehensive guide to palaeoart processes). Plus, you get free stuff - prints, high quality images for printing, books, competitions - as my way of thanking you for your support. As always, huge thanks to everyone who already sponsors my work!

References

• Andrews, C. W. (1906). A descriptive catalogue of the Tertiary Vertebrata of the Fayum. Publ. Brit. Mus. Nat. Hist. Land. XXXVII.
• Anonymous. (1903). A New Egyptian Mammal (Arsinoitherium) from the Fayûm. (1903). Geological Magazine, 10(12), 529-532.
• Court, N. (1992). The skull of Arsinoitherium (Mammalia, Embrithopoda) and the higher order interrelationships of ungulates. Palaeovertebrata, 22(1), 1-43.
• Davis, E. B., Brakora, K. A., & Lee, A. H. (2011). Evolution of ruminant headgear: a review. Proceedings of the Royal Society of London B: Biological Sciences, 278(1720), 2857-2865.
• Drake, A., Donahue, T. L. H., Stansloski, M., Fox, K., Wheatley, B. B., & Donahue, S. W. (2016). Horn and horn core trabecular bone of bighorn sheep rams absorbs impact energy and reduces brain cavity accelerations during high impact ramming of the skull. Acta biomaterialia, 44, 41-50.
• Goss, R. J. (2012). Deer antlers: regeneration, function and evolution. Academic Press.
• Hieronymus, T. L., Witmer, L. M., Tanke, D. H., & Currie, P. J. (2009). The facial integument of centrosaurine ceratopsids: morphological and histological correlates of novel skin structures. The Anatomical Record, 292(9), 1370-1396.
• Li, C., & Suttie, J. M. (2000). Histological studies of pedicle skin formation and its transformation to antler velvet in red deer (Cervus elaphus). The Anatomical Record, 260(1), 62-71.
• Osborn, H. F. (1907). Hunting the Ancestral Elephant in the Fayûm Desert: Discoveries of the Recent African Expeditions of the American Museum of Natural History. Century Company.
• Prothero, D. R., & Schoch, R. M. (2002). Horns, tusks, and flippers: the evolution of hoofed mammals. JHU press.
• Rose, K. D. (2006). The beginning of the age of mammals. JHU Press.
• Sanders, W. J., Kappelman, J., & Rasmussen, D. T. (2004). New large-bodied mammals from the late Oligocene site of Chilga, Ethiopia. Acta Palaeontologica Polonica, 49(3), 365-392.
• Spinage, C. A. (1968). Horns and other bony structures of the skull of the giraffe, and their functional significance. African Journal of Ecology, 6(1), 53-61.

The convention of shrink-wrapping: thoughts for artists

Europasaurus holgeri - twice. These portraits are of the same animal using the same specimen and the same view, but one is restored with extreme shrink-wrapping (above) and the other has a more generous amount of facial tissue (below). But which one is more plausible, and can we even tell from fossil bones alone?

You can't move around palaeoart circles on the internet nowadays without someone being criticised for 'shrink-wrapping' their reconstruction. This refers to the convention of restoring extinct animals with minimised soft-tissues, allowing details of muscle layouts and major skeletal contours to be seen in allegedly healthy living animals. At its most extreme, this includes clearly visible ribs and vertebrae, tissues sunk into skull openings, ultra-prominent limb girdles and skinny, sinewy legs. We owe the term 'shrink-wrapping to sauropod expert and SV:POW author Mathew Wedel who, in a 2010 article, compared the contour-hugging soft-tissues of these restorations to items wrapped in tight plastic for transport.

Shrink-wrapping is a well known convention among those interested in palaeoart but is a relatively modern invention. Palaeoartists restored ancient animals with relatively bulky soft-tissues until the end of the 20th century to an extent where visible deep-tissue anatomy is genuinely exceptional in pre-modern palaeoart (a well known exception are ichthyosaur sclerotic rings, reflecting erroneous interpretation of these structures among early palaeontologists - see Buckland 1836). Shrink-wrapping became popular as conservative reconstruction approaches became dominant in the 1970s and went on to become a standard palaeoart convention soon after. Many, perhaps most, of the restorations produced by late 20th century artists employed shrink-wrapping and it remains conspicuous in artwork produced today. It has even spawned related traditions, such as tightly cropping fur and feathers to ensure animal shapes remain obvious, and has influenced approaches to restoring colour and skin texture, these elements being used to outline the topography of underlying bones. Famous shrink-wrappers include artists like Gregory S. Paul and Mark Hallett, who tend to be on the less dramatic side of the tradition, showing slight contours of the skull features alongside lean, though well-muscled, bodies and limbs. More extreme shrink-wrappers, like Ely Kish and William Stout, have works where shrink-wrapping is taken to a wholly unrealistic level. Gaping vacuities exist between neck vertebrae; rib cages and limb girdles bulge from the torsos; limbs are extremely thin and faces are lipless and gaunt. It’s difficult not to look at some of these works and not think of starving animals or even decaying remains: they do not look like healthy, virile beings.

William Stout's Quetzalcoatlus, posted at Love in the Time of Chasmosaurs, has to be the most shrink-wrapped being ever rendered in paleoart. If it had any less tissue we'd be looking at moulds of the internal organs.

We might assign three reasons for the popularity of shrink-wrapping. The first is that its development coincided with a reinvention of dinosaurs as bird-like, active and powerful animals rather than oversized, under-muscled cold-blooded creatures. The athletic appearance of shrink-wrapped dinosaurs chimed with this renaissance and contrasted newer art from the plodding, perhaps over-voluminous animals of previous generations. Shrink-wrapping is not a dinosaur-exclusive tradition of course, but the popularity of these reptiles means that palaeoart conventions applied to dinosaurs are inevitably followed in artworks of other species. Secondly, images of prehistoric animals as heroically-built, powerful beings are preferred by many merchandisers and palaeoart fans, these interpretations most closely matching the erroneous but popular portrayal of prehistory as a savage struggle for survival, where only the most powerful animals survived. Thirdly, shrink-wrapping allows palaeoartists to ‘show our work’, demonstrating that the anatomy underlying the skin of a restored animal matches the osteological information provided by fossils.

How shrink-wrapping became unfashionable

Nowadays, shrink-wrapping is losing popularity among some parties as scientists and artists note a simple, but obvious problem: modern animals are generally not shrink-wrapped in the way we draw their extinct relatives. The most famous counter-shrink-wrapping arguments are in All Yesterdays (Conway et al. 2012) but something of an anti-shrink-wrapping movement was underway from the mid-2000s onward. Some now argue that, while champions of the rigorous reconstruction movement were right to draw attention to the true shapes of fossil animals and to emphasise their form in art, they might have gone too far in thinning out skin, muscle, fats and other tissues. Few animals have deeply sunken tissues over skull fenestra or distinctions in skin colour and texture correlating with skeletal anatomy, and no animals witnessed outside of veterinary clinics have detailed limb bone outlines projecting through their skin. Even reptiles - meant to be the living poster boys of shrink-wrapping - have a suite of elaborate, contour-altering soft-tissues. They include voluminous fat deposits; large amounts of wrinkly, saggy skin; eyes which bulge prominently from their sockets; deep lip tissues which fully sheath their teeth; jaw muscles which completely fill and swell from their skull housing; thick or pointed scales and, in some species, even expansive, mostly cartilaginous noses.

Matt Wedel's touching plea to end shrink-wrapping, from 2011. The struggle is still real: if you have spare paint, pixels clay or graphite, please donate generously.

Nowadays, many view skeletal elements as providing an important palaeoartistic foundation for soft-tissue shape, but concede that overlying tissues must have smoothed-over skeletal contours to produce 'softer' body forms. Indeed, there's something of an collective interest in knowing how deep extra-skeletal tissues can get. The answer, it seems, is 'very'. The necks of many birds and mammals are often flexed at much higher angles than we would assume based on their external appearance because their overlying tissues are so thick that the entire neck skeleton posture is hidden (Taylor et al. 2009). The muscles and bones of major anatomical elements – such as necks and proximal limb segments – can also be obscured under skin, fat and integument. Contour-altering structures like horns, spikes, spines, combs, humps, armour, fins, and webbing are often composed of soft-tissue, and the large, savage-looking teeth of mammals and lizards can be completely obscured by facial tissues. We need only look at x-rays of living animal species to see their often-startling lack of correlation between external appearance and internal anatomy.

Even seals get in on this action, as evidenced from this Irish Seal Sancutary x-ray. Their site appears to be down at time of writing, but SV:POW! has this image hosted there for the time being. 

It's from this general train of thought that a  push for more bulk, fuzz and fat in palaeoart has been born, and this general philosophy is lining up well with fossil data. We have direct evidence that the bodies of ichthyosaurus (Stenopterygius) and mosasaurs (Prognathodon) bore tall fins and paddle extensions that vastly exceeded the limits of their skeletal margins (McGowan and Motani 2003; Lindgren et al. 2013). Preserved body outlines of ichthyosaurs and plesiosaurs show deep tissues which created smooth, streamlined torsos that are much bulkier than the underlying skeleton (Frey et al. 2017). Fossils of early horned dinosaurs (Psittacosaurus), Tanystropheus and ‘mummified’ hadrosaurs (multiple taxa) show extensive muscle volume that bury their skeletons as well as elaborate structures – soft-tissue filaments, combs and skin membranes – that defy ‘shrink-wrapping’ conventions (e.g. Mayr et al. 2002; Renesto 2005; Bell 2014). The feather outlines on innumerable fossil theropods show that they were just as densely feathered as modern avians, and the fuzzy ‘halos’ of fossil mammals and pterosaurs suggest they too were also adorned with deep layers of filaments. Several pterosaur fossils (Pterodactylus, Pterorhynchus) also preserve unexpectedly broad neck tissue outlines which contrast against their thin, tubular neck vertebrae, as well as elaborations of crest tissues that create body outlines more voluminous than those predicted from musculoskeletal restorations (e.g. Frey and Martill 1998; Czerkas and Ji 2002). The 'shrink-wrapping hypothesis' is being falsified with regularity.

Select fossilised body outlines of exinct taxa: no shrink-wrapping here. A, plesiosaur Mauriciosaurus fernandezi, B, ichythyosaur Stenopterygius quadriscissus; C, dromaeosaur Sinornithosaurus millenii. A, after Frey et al. 2017; B after McGowan and Motani 2003.

Anti-anti-shrink-wrapping

But while cries of 'bulkier, deeper, fuzzier!' are generally well-placed in palaeoart discussions, we should be careful not to overshoot the mark. Amid the cry for deeper tissues, we might be overlooking the fact that some living creatures are somewhat shrink-wrapped - at least in some regions. In fact, virtually animals have areas where their extra-skeletal tissues are shallow and skeletal contours are visible. Common areas of thin tissue include the ends of limbs and tails; the midline of the sternal region; and some areas of the face, such as the frontal and nasal regions; the ‘cheek region’ (over the jugal in birds and reptiles, and the zygomatic arch in mammals), and the lower margins of the bottom jaw. Our own anatomy is no exception to these trends, as is borne out by the extremely well-studied tissue depths of human faces (e.g. Stephan and Simpson 2008) or the simple act of looking in a mirror. The osteoderms of sauropsids are another example of close interaction between skin and bone: as with modern armoured reptiles, extinct scaly sauropsids with extensive osteoderm arrangements probably looked pretty darn like their fossil remains - in other words, kinda shrink-wrapped.

There is no tissue, only Zuul.

In reality, there is a spectrum of tissue depth in living species and some are more 'shrink-wrapped' than others. While no healthy living animal attains the most extreme levels of shrink-wrappery portrayed in palaeoartworks, certain lizards, fish, and crocodylians have anatomies which are more shrink-wrapped than average, possessing large areas of relatively thin, skull-hugging tissues which recall shrink-wrapped art. These thin tissues are highly characteristic of these species and are something something palaeoartists would want to capture if restoring these animals from fossils. We would miss this, however, if we assume that all animals have their tissue volume settings cranked up to maximum.

These observations mean we have to be careful with applying a general philosophy to shrink-wrapping rather than scientific investigation. Tissue depth is evidently not a matter of palaeoartistic style or fashion, but a biological variable we should be aiming to predict and infer. If we're aiming to approach this topic like scientists, we should look to see what fossils and comparative anatomy can tell us about tissue depth to make informed, specific predictions about extinct animal appearance and avoiding a one-size-fits-all 'anti-shrink-wrap' philosophy. So, is there anything in the fossil record that elucidates how deeply buried animal skeletons were under muscle, skin and so on?

Looking for clues of 'shrink-wrapped' tissues

Frustratingly, one of the first lines of evidence we have to jettison are those body outline fossils. As great as they are, they can be of limited use for determining subtle variation in tissue thickness as their shapes are readily altered by taphonomy, preservation styles and even our own preparation work. Regions of thin tissue depth will be were especially sensitive to destructive processes and are easily obliterated by imperfect preservation or human error, so their chances of preservation are minimal. Phylogenetic bracketing is also of limited utility because the vastly different cranial architecture of extant and extinct animals makes such investigations almost meaningless. Non-avian dinosaurs, for instance, have skulls which are neither truly croc-like or bird-like, and it's probably not sensible to assume their extant relatives provide reliable insights into their facial tissues.

Predicting regions of thin tissue is thus largely left to comparative anatomy - predicting minimised tissue volumes using fossil bones and the living structural analogues. Among extant species, we see shrink-wrapping largely applying to animal faces, so if we investigate the skulls of ‘soft-faced’ animals like mammals, monitor lizards, snakes, and certain birds, and compare them to species with shrink-wrapped faces, like turtles, crocodylians, chameleons and well-ossified fish, we might find characteristics that correlate with facial tissue depth. These will then give us some criteria to assess tissue depth in fossil species. I've had a go at this, and suggest that osteological attributes related to facial tissue depth include:

How might we predict shrink-wrapping in fossil animals without good soft-tissue remains? It's challenging, but these attributes might give a general idea. From top to bottom: Burchell's zebra (Equus quagga burchellii); water monitor (Varanus salvator); Alligator mississipiensis and Arrau turtle (Podocnemis expansa).

Openness of skull architecture. The skull openings of softer-faced animals - including the temporal muscle openings, orbits and nares – tend to be large. At their most extreme these openings are not fully bordered by bone (e.g. many mammal orbits and nares, the lower temporal fenestrae of lizards). Larger skull openings necessitate a larger fraction of face structure be composed of soft-tissue, such as muscle, organs, and cartilage, and this overwhelms the contours of the bony skeleton to make a 'soft-faced' species. The nasal cartilages of monitors and mammals, as well as bulging mammalian jaw muscles, are examples of this. Conversely, shrink-wrapped species have smaller cranial openings, which impose physical limitations on how much soft-tissue can form the shape of the face. Muscles and organs might protrude from these somewhat, but their impact on facial structure is less than that of species with large skull openings, and more of the face shape reflects bony contours

Rugosity. Soft-faced animals tend to have smooth bone textures with limited or no areas of rugosity, whereas the skulls of shrink-wrapped species have large areas of rugose textures, often corresponding to specific epidermal features (e.g. scales or keratinous sheaths - see below and Hieronymus et al. 2009). This factor largely seems to reflect the proximity of epidermal tissue, which can leave characteristic textures in species with tightly-bound skin. Soft-faced species generally lack this rugosity because muscles, fat and voluminous integuments (fur and feathers) don’t leave broad osteological features (Hieronymus et al. 2009), or simply because their skin is displaced far enough from the bone that it doesn't alter its surface. We might also note that the skull contours of soft-faced species are generally more rounded than those of shrink-wrapped species, which can be crisp and sharp. Rugosity is a particularly useful criterion because it can show the presence of tight skin tissues with some precision. If one part of a skull is rugose, and another isn’t, there’s a good chance that the smoother region had a different tissue configuration which could - among other things - reflect a deeper or 'softer' facial covering.

Fossil skulls - like those of the centrosaurine Centrosaurus apertus - are covered with features that allow us to predict aspects of their facial skin. Often - as is the case here - they suggest fairly low-volume structures, like scales and horn sheaths, which generally don't deviate too much from the underlying bone (yes, I know there are exceptions, but we're looking for major trends here). Centrosaurus skull redrawn from this Wikipedia photo, data on facial tissue correlates from Hieronymus et al. (2009).

Pits, grooves and foramina. Shrink-wrapped species tend to have large numbers of perforations in their skulls, while soft-faced species show the opposite (Morhardt 2009). This is particularly evident around their jaws and presumably reflects the greater capacity for soft-faced animals to carry nutrients and sensory information through their soft-tissues, whereas shrink-wrapped animals are forced to run nervous and vascular networks through their face skeletons.

Correlates for epidermal projections. Elaborate skin projections – such as soft-tissue horns or crests - leave characteristic osteological signatures (Hieronymus et al. 2009). Given that these projections can alter animal faces quite substantially from the underlying skull shape, the presence of these is a clear indication that the species was not shrink-wrapped. We would expect a lack of correlates for epidermal projections in shrink-wrapped species.

As is often the case with zoological topics there are exceptions to these observations that preclude using any one of these criteria in isolation to determine tissue depth (e.g. smooth bone textures can underlie thin naked skin, so are not always a hallmark of deep tissues). However, applied collectively, they might give a general insight into how shrink-wrapped or 'soft-faced' an extinct animal was. I'm encouraged to see that these proposed osteological features of soft- and shrink-wrapped faces covaried in the past as much as they do for modern species. This doesn't mean these criteria are 'correct' as goes their relationship to tissue depth, but at least shows there's variation in their skull architecture that we can recognise as equivalent to that of modern species, and it isn't unreasonable to think the variance might reflect the same anatomical factors.

If we apply these criteria to some fossil taxa, what predictions might we make? The roomy, smooth-boned and foramina-lite skulls of cynodont-grade synapsids and fossil mammals match predictions for ‘softer-faced’ species, and this might be true of some fossil reptiles – like sauropod dinosaurs - too (this is not a new conclusion: both Matt Wedel and Darren Naish have been saying similar things about sauropods for years). If right, the 'soft-faced' sauropod that greeted you at the start of this post might be more likely that the shink-wrapped toilet-headed version we're so familiar with. At the other end of the spectrum, the highly textured, pitted bones and solidly-built skulls of ankylosaurs and anamniotes meet our criteria for shrink-wrapping very well, and they likely had facial anatomy tightly conforming to their skull shapes.

Applying the criteria outlined above might help us roughly sort predict 'shrinkwrapped', 'soft-faced' or intermediary conditions in extinct taxa. The placements of the animals here are only rough, but give an indication of their relation to the tissue-depth criteria outlined above. Fingers crossed that some of these will be corroborated or refuted with soft-tissue discoveries in future.

Careful examination of fossil skulls allows us to also predict partial or regionalised shrink-wrapping in species where some aspects of their facial anatomy conformed to the underlying bone, and others did not. An example of this configuration is demonstrated in some living lizards, like gila monsters, which have skull textures strongly indicating minimal tissue depth over much of their skull but smooth, foramina-lite jaw margins. In life, these animals have shrink-wrapped dorsal skull regions and snouts, but vast, fleshy lips, which is what we might predict based on their skull anatomy.

Partial facial shrink-wrapping seems apt for many fossil species. Gorgonopsians, for instance, might not have soft faces like living mammals as their snouts and foreheads are quite rugose and their nasal openings are small (e.g. Kammerer 2016). These features might indicate the presence of tighter skin over the snout. However, they have few jaw foramina and relatively open regions for jaw musculature, so they might have been fleshier around their jaw margins and at the back of head (below). Tyrant dinosaurs have skulls with relatively small openings compared to some of their theropod relatives, rugose snout textures, several hornlets (Carr et al. 2017), as well as a slightly elevated foramina count (Morhardt 2009). This cranial anatomy is consistent with tighter tissue depth in several areas, if someway short of a fully lipless, crocodylian-like degree of shrink-wrapping. Many pterosaurs show pitting and vascular canals embedded into their jaw margins, and some species have indications of tight sheathing on their crests and jaws, but the presence of striated bony crests – correlates for epidermal projections – as well as large skull openings and smooth bone textures in other parts of the skull, indicate that their faces might not have been entirely skeletal.

Was gorgonopsian Inostrancevia shrink-wrapped or soft-faced? According to the criteria of this post, maybe a little from column A, a little from column B. 

Time and testing will tell whether these criteria are a genuinely useful means to predict facial anatomy. I hope - as with other aspects of extinct animal appearance - that genuine research into this issue will be carried out one day. Criteria to predict tissue-depth are a desirable tool for any palaeoartist as it's simply more honest and scientific: if we're serious about this reconstructing extinct animals gig, predictive methods and sound hypotheses are infinitely better than sticking to our personal hunches, guesses or erring on what looks coolest. Regardless of whether we can predict tissue depth or not, the take home here is that we should not approach our artwork having already decided how thin or fat the tissue volumes of our subjects will be. There is probably not a single ‘universal truth’ that can be said about restoring tissue depth for all animals, whether we err toward thicker or thinner: the right tissue depth is the most defensible and best rationalised on for each subject and its constituent body parts.

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References

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