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Monday, 12 September 2016

A salute to the Erythrosuchidae

Two Garjainia madiba decide who gets the table scraps. The reconstructions here are modified from the life reconstruction I provided for Gower et al. (2014).
I find erythrosuchids, large, big-headed Triassic archosauriforms, very charismatic fossil animals. If nothing else, it's hard not to admire their no-nonsense approach to carnivory. Take a fairly standard reptilian bauplan, weld an oversize theropod dinosaur face to the front, then point it at the things you want to die: simple. They're the Mesozoic equivalent of mounting a howitzer on a golf cart and calling it a tank. We might question the rudimentary nature of the design, but we can't argue with the results.

Alas, erythrosuchids don't get as much love from palaeoartists or outreach projects as they deserve. Their marriage of a proportionally huge, sharp-toothed skull with a crocodile- or lizard-like body is unlike anything around today and it's difficult not to wonder how they functioned as living animals. Closer inspection of their anatomy reveals more sophistication than we might assume from the few illustrations of these animals available online or in books, and it seems that their role in Mesozoic ecosystems and reptile evolution was an important one. These were a successful, abundant group of predators with an evolutionary run spanning the Early and Middle Triassic (12 million years in total) and a near cosmopolitan distribution. Moreover, they remain important species for understanding the early evolution of archosaur-line reptiles. They really do have a lot going for them, but they just haven't quite caught public imagination.

A few years ago I was commissioned to reconstruct the small(ish), early erythrosuchid Garjania madiba for David Gower and his colleagues for their 2014 descriptive paper (below). The brief was for a straight illustration of the animal rather than a restored scene, and I promised the team I would put this reconstruction in a landscape one day. Two years later, I've finally got around to it: the results are above. Posting this painting seems like as good an excuse as any to lavish some much needed attention on these most encephalised of reptiles, so let's get stuck in.

G. madiba reconstruction from Gower et al. (2014). Note prominent bosses on the face, a characteristic feature of this species.

What, exactly, is a erythrosuchid?

You can find erythrosuchids in Triassic rocks on every continent except North America and Antarctica and, although relatively complete specimens are not common, many species are represented by large inventories of bones. Despite this relative glut of material, the classification of erythrosuchids - from the fine anatomical characteristics of the group, to their position in the reptilian tree and the number of species contained in the clade - has been the subject of long-standing, ongoing discussions among palaeontologists. Older erythrosuchid literature is confused by a multitude of different classifications which entwine erythrosuchids with other large-headed, carnivorous archosauriforms such as raisuchians and proterosuchids. Researchers have long realised the problems with these schemes, but unpicking the relationships of these groups and other early archosaur-line reptiles has been tricky. With the arrival of extremely detailed and well sampled cladistic analyses of archosauromorphs (e.g. Nesbitt 2011; Ezcurra 2016) we might be moving towards greater consensus on the systematics of these animals, however. In modern schemes, erythrosuchids are recovered as non-archosaur archosauriforms close(ish) to the base of Archosauria. More specifically, they are the sister clade to the the Eucrocopoda, the large clade that contains the likes of Euparkeria and proterochampsids, as well as the true archosaurs (Ezcurra 2016).
Erythrosuchus africanus skull, restored by Gower (2003). Note the extremely robust construction of the bones and expanded areas for neck muscle attachment.
Several erythrosuchid species are well known: Erythrosuchus africanus from the Middle Triassic of South Africa, Garjainia prima from the Early Triassic of Russia, and Shansisuchus shansisuchus (that's not a typo) from the Middle Triassic of China. These species are represented by associated remains as well as large numbers of fragmentary referred specimens, and allow for a relatively complete insight into their overall form. The largest taxa, like Erythrosuchus, are big animals with head-tail lengths approaching 5 m - the length of a good-sized car - and even small taxa like Garjainia are over 2 m long. The most arresting aspect of eyrthrosuchid anatomy is, of course, their skulls (above). Superficially theropod-like, these long, deep and robust structures are sub-rectangular in lateral view, but taper markedly towards the snout in dorsal or ventral aspect. These animals are yet another reminder that restoring fossil animals needs more than a lateral view of a skeleton: those massive skulls are considerably narrower than we might expect. Their teeth are thecodont, large, serrated and recurved. A characteristic of the group is the complicated shape of the upper jaw, where the jaw tip is vertically displaced from a ventrally bowing maxillary region (Parrish 1992), creating something of a 'notch' towards the front of the jaw. Beneath this, the mandible has a slightly dorsoventrally expanded tip, as well as a swollen posterior region. At least the skull of Erythrosuchus is essentially akinetic, although minor movements of some bones may have been possible (Gower 2003). Although erythrosuchid skulls are fairly conservative in morphology, some species were not above frivolous accessorising: prominent bosses above and below the eye are known from Garjainia madiba (Gower et al. 2014 - see reconstructions, above), and Pickford (1995) reports a long, low boss on the snout of an undescribed Karoo Basin specimen.

Although erythrosuchid skulls were almost certainly pneumatised in some areas, the largest opening in the skull is not, as we might expect in such large headed animals, anything to do with a pneumatic cavity. Rather, it's the lower temporal fenestra, an opening typically associated with allowing bulges of the jaw adductor muscles. This, as well as the presence of a small sagittal crest between the superior temporal openings (which overly the same muscle block) and the depth of the posterior mandible likely betrays the presence of massive adductor muscles in temporal region of the skull. Eryhtrosuchid skull bones certainly look sufficiently robust to withstand powerful biting, the bones forming the temporal fenestra, jaw and orbital margins being extremely massive and thick and tightly interlocking with complex sutures between each bone. Interestingly, Shansisuchus has the same partly invaded orbit shape that Henderson (2003) linked with reinforcement against heavy bite forces in theropod dinosaurs: perhaps similar buttressing was taking place in these Triassic reptiles

The dorsal extent of the occipital face in Eryhtrosuchus africanus, posterior view. The rounded flanges at the top poke above the rest of the skull, and perhaps indicate expanded neck muscles in this and other species. From Gower (2003).
The posterior surface of the skull is interesting. Rather than the relatively flat surface we see in most animals, the posterior erythrosuchid skull is recessed so that several aspects of the skull - the jaws and lateral extents of the occipital surface - extend further back than the vertebral/skull joint. The area which anchored the neck musculature extended across this recessed surface, even exceeding the dorsal margins somewhat by means of a pair of semiscircular flanges projecting above the rest of the skull (visible in at least Erythrosuchus and Garjainia - see above). Assuming a typically reptilian muscle plan, these indicate that muscles anchoring above the skull-neck articulation were larger than usual, as might be expected for animals with ginormous heads. Similar dorsal expansion of the occipital region is seen in tyrannosaurids, and is also thought to reflect large cervical musculature (Paul 1988). It thus seems the vertebrae and posterior skull of erythrosuchids were deeply buried in neck tissues, befitting animals with a giant head to support and utilise in predatory acts. But I wonder if all this support and strength compromised the mobility of the skull-neck joint somewhat. Moving the neck articulation forward to sit within the boundaries of the skull likely shortened the length of the skull flexor muscles, as well as buried the joint in masses of potentially restrictive muscle and bone. Motion of the head may have been limited at the front of the neck, then, but unfortunately for erythrosuchid prey, the size of the shoulder skeleton and stoutly built humeri suggest this was accounted for with powerful muscles at the base of the neck, as well as forelimbs able to shove the forequarters around at speed. Dashing left or right against a charging erythrosuchid was unlikely to save you from a nasty, gigantic and powerful bite.

Behind the skull we see a fairly typical Triassic archosauriform body (below). The neck is short, and especially so in some of the larger species, and the majority of the vertebrae are adorned with tall neural spines: these almost certainly provided anchorage for axial musculature related to supporting the head and back. The pectoral elements, which are also employed somewhat in neck musculature, are also robust. Their tails are moderately long, with deep chevrons in the anterior region likely related to hindlimb musculature. Behind these, the tail becomes rather slender. Gower (2001) proposed that Erythrosuchus vertebrae possessed pits and depressions possibly related to the development of post-cranial pneumaticity, the first found outside of pterosaurs and dinosaurs. This would be a significant find, telling us something of erythrosuchid lung structure as well as the early evolution of postcranial pneumaticity in archosaur-line reptiles. However, both O'Connor (2006) and Butler et al. (2012) argued against this interpretation, noting that the features in question were not associated with internal cavities, thus failing to meet criteria for structures of pneumatic origin. An important caveat to this, however, was raised by Butler et al. (2012): the phenomenon of pneumatic tissues invading vertebrae and other postcranial bones almost certainly did not evolve in one swoop. Its earliest stages may have simply been pneumatic tissues 'pushing' against external bone walls, forming pits and cavities, rather than invading them entirely. If so, the sort of thing Gower (2001) found in Erythrosuchus might be what we'd expect of early stage, postcranial pneumaticity. So while we have to concede that these structures do not meet our current definition of a postcranial pneumatic structure, perhaps we also need to learn more about the early evolution of postcranial pneumaticity before this hypothesis can be ruled out entirely.

Mounted Garjainia prima skeleton as mounted at the Paleontological Institute, Moscow. Certain aspects of this skeleton are reconstructed or sculpted, so take some details with a pinch of salt. From Ivakhnenko and Kurochkin (2008).
The limbs of erythrosuchids are not, to my knowledge, completely known from any species but their major limb bones are powerfully built and surprisingly lengthy: you could never call them 'long-limbed', but they are not the stumpy-legged animals we often see them reconstructed as. Their hands and feet are poorly known. Rare examples of erythrosuchid ankles are thought to indicate an mesotarsal condition (Gower 1996), and their pelves show signs of advanced features that we see developed further in true archosaurs. These features led to our G. madiba reconstruction having semi-erect hindlimbs, while the forelimbs remained sprawling. The typical pose of erythrosuchids remains to be determined from further study of their limb bones.

A point of contention among researchers is whether or not erythrosuchids had osteoderms. Two examples of such structures have been found in association with a specimen of Erythrosuchus, but they show no consistency in their morphology (Gower 2003). Moreover, the extensive inventory of Erythrosuchus and other erythrosuchids have yet to show additional evidence of dermal bones (Ezcurra et al. 2013). The safe bet, for the time being at least, is to assume these reptiles did not have osteoderms, and that those previously referred to the group were a fluke association from another animal.

The life and times of Triassic big-heads

We have much to learn about many aspects of erythrosuchid palaeobiology: details of their dietary preferences, locomotor mechanics and likely habitats remain only provisionally researched. Much of what we've learned about their lifestyles comes from 'bigger picture' assessments of Triassic diversity and faunal turnover, so we can only paint a broad-brush picture of their ecology at this time. That's not to say we have no specific palaeobiological insights into these animals, however. For instance, there is consistent histological evidence that erythrosuchids grew quickly, perhaps at rates comparable to pterosaurs and dinosaurs, until they reached reproductive maturity (de Ricqlès et al. 2008; Botha-Brink and Smith 2011; Ezcurra et al. 2013). Given that this trait is not limited to erythrosuchids among Early and Middle Triassic reptiles, this is one reason it's thought that archosaur-line reptiles may not be ancestrally ectothermic. Whatever the cause, rapid growth may have played some role in the success of erythrosuchids and other reptiles as ecosystems were rebuilt in the early Mesozoic (Sookias et al. 2012).

Erythrosuchid ecology remains only lightly investigated, but they have been considered arch terrestrial predators by some (Sennikov 1996 - see below). Interestingly, their size puts them among the largest terrestrial animals known from their respective faunas (Sookias et al. 2012). This is unusual: in post-Middle Triassic ecosystems we generally find herbivores are the largest animals in terrestrial ecosystems, so what's going on here? It's thought that physiological distinctions between large Early-Middle Triassic reptiles and the synapsid herbivores they coexisted with may explain the size difference (briefly summarised, archosauriform growth rates and respiratory anatomy may have permitted larger overall body size than therapsids - see Sookias et al. 2012), but how did this translate into ecological balance? Energy is lost as it is transferred between species in food webs, so how did populations of relatively 'giant' top-tier erythrosuchids sustain themselves on consistently smaller prey? Perhaps they were simply comparatively rare, or very energy-efficient, or maybe they supplemented their diet with non-terrestrial food items - did they also take food from aquatic realms, perhaps?

An Early Triassic terrestrial food web, reconstructed for the Yarenga Formation by Sennikov (1996). In this scheme, most things ended up in the bellies of erythrosuchids or rausuchians.
Speaking of aquatic habitats, the concept of erythrosuchids as strictly terrestrial predators is not the only interpretation of their habits. Indeed, for much of the 20th century erythrosuchid proportions were considered evidence of aquatic or semi-aquatic habits: their huge heads and robust limbs were thought to permit only cumbersome, laboured movement on land (see Ezcurra et al. 2013 for a brief review). The words offered by Reig (1970) paint an excellent summary of these older interpretations: "We doubt that bulky and clumsy animals like Erythrosuchus and Shansisuchus should be considered very active animals... It is more likely that they were inhabitants of swamp marshes, able to prey upon big, slow herbivorous vertebrates, inhabiting the same environments, which could be caught by a relatively slow and heavily built predator" (p. 261). Potentially further evidence of semi-aquatic lifestyles are the relatively thick limb bone walls common to all erythrosuchids, these being comparable in thickness to those of modern alligators (Botha-Brink and Smith 2011; Gower et al. 2014).

In recent years, however, erythrosuchids seem to have been perceived as more terrestrial animals (Sennikov 1996; Botha-Brink and Smith 2011; Ezcurra et al. 2013). Their thick bone walls are explained as being a consequence of their large size rather than aquatic habits (Botha-Brink and Smith 2011) and the deficit of obvious aquatic adaptations in their skeletons has been noted by several authors (Botha-Brink and Smith 2011; Ezcurra et al. 2013; Gower et al. 2014).

Aquatic, semi-aquatic or fully terrestrial? This guy's meant to have taken a dip in the water, but was it intentional or accident? We may not have the data to say exactly what erythrosuchids did for a living yet.
All this said, I must admit to desiring more work in this area. The habits of strange Triassic animals are difficult to fathom in many instances, and we're yet to see particularly comprehensive assessments of the most basic elements of erythrosuchid functional anatomy, let alone application of modern techniques like isotope analysis, stress modelling of jaws and so on to this problem. My gut feeling - and thus in no means a basis for a hypothesis - is open to both interpretations of erythrosuchid habits, and I wouldn't be surprised if terrestrial and aquatic prey were on their radars. I'm suspicious about the weight of the head being a problem for terrestrial locomotion. A decade of looking at terrestrially-competent, large-headed pterodactyloid pterosaurs and recent monkeying about with mass fractions of giant-necked Tanystropheus suggest our intuitive grasp of front-heaviness might be poorly calibrated. Animal heads and necks are often much lighter than we think in contrast to torso and limb masses, and we should remind ourselves that erythrosuchid skulls are actually quite narrow, presumably well-pneumatised structures. This is the sort of thing that can be relatively easily investigated using digital models, and we might hope this approach is applied to erythrosuchids in future. But if that supports a terrestrial habit, the notched upper jaw and swollen mandibular tip of erythrosuchids argues contrarily: similar jaw tips are seen in fish-eating animals like modern crocodylians and pike conger eels, as well extinct presumed fishers such as spinosaurids and some pterosaurs. Might this not imply that small swimming animals were sometimes eaten by erythrosuchids, too? Lest we forget, animals do not necessarily need to be dedicated swimmers to be able to eat aquatic prey. There's a lot of scope for further work and investigation here, and it would be great to see some dedicated functional assessments and ecological investigations of erythrosuchids in future.

I love it when a bauplan comes together

Perhaps one of the most interesting things mentioned recently about erythrosuchids is how little their postcrania differs from those of other archosauriforms, despite their substantial cranial modifications (Ezcurra 2016). This is something we see again and again in Triassic reptiles: relatively conservative bodies with highly localised outlandish anatomy, and is true even for the weirdest Triassic creatures. For example, Tanystropheus isn't that strange aside from its incredible neck, and (what we know of) the body of Sharovipteryx is not that atypical in spite of its leg-wings. I wonder if Triassic animals get the short shrift in popular circles because they're viewed as boring 'also rans' taxa which evolved strange, untenable anatomies but without moving too far from a typically 'reptilian' visage.

But perhaps what we're seeing with these animals is far more interesting than it first appears: a display of the intrinsic adaptability of the archosauromorph bauplan, and how applicable it was to many lifestyles with only localised modification. We can be particularly impressed with erythrosuchids because of their rapid evolution so early in the Triassic: they very quickly and successfully jumped into the niche of large, hypercarnivorous apex-predator after the end-Permian extinction event, and then held that niche worldwide for 12 million years. The fact they did so without much additional modification to the postcrania is evidence that their success was not a fluke, and that the basal archosaur-line body plan was a strong one. Perhaps instead of looking at erythrosuchids and other Triassic archosauromorphs as those strange, but ultimately dull animals that struck it lucky before the more successful ones took over, we might view them as some of the earliest evidence that the archosaur-line bauplan had real potential, and a sign of what was to come.

Big blog posts about big headed reptiles need big support - thank goodness for Patreon

The paintings and words featured here are sponsored by a group of tetrapods with more modestly proportioned skulls, my Patreon backers. Supporting my blog from $1 a month helps me produce researched and detailed articles with paintings to accompany them, and in return you get access to bonus blog content: additional commentary, in-progress sneak-previews of paintings, high-resolution artwork, and even free prints. For this post, we'll be looking at the history of the painting up top, documenting its long 2-year journey from illustration to, er, a more detailed illustration. I'll also share the bizarre, sausage piglet monster version of Garjainia that you were never meant to see. Sign up to Patreon to get access to this and the rest of my exclusive content!

References

  • Botha-Brink, J., & Smith, R. M. (2011). Osteohistology of the Triassic archosauromorphs Prolacerta, Proterosuchus, Euparkeria, and Erythrosuchus from the Karoo Basin of South Africa. Journal of Vertebrate Paleontology, 31(6), 1238-1254.
  • Butler, R. J., Barrett, P. M., & Gower, D. J. (2012). Reassessment of the evidence for postcranial skeletal pneumaticity in Triassic archosaurs, and the early evolution of the avian respiratory system. PloS one, 7(3), e34094.
  • de Ricqlès, A., Padian, K., Knoll, F., & Horner, J. R. (2008). On the origin of high growth rates in archosaurs and their ancient relatives: Complementary histological studies on Triassic archosauriforms and the problem of a “phylogenetic signal” in bone histology. In Annales de paleontologie (Vol. 2, No. 94, pp. 57-76).
  • Ezcurra, M. D., Butler, R. J., & Gower, D. J. (2013). ‘Proterosuchia’: the origin and early history of Archosauriformes. Geological Society, London, Special Publications, 379(1), 9-33.
  • Ezcurra, M. D. (2016). The phylogenetic relationships of basal archosauromorphs, with an emphasis on the systematics of proterosuchian archosauriforms. PeerJ, 4, e1778.
  • Gower, D. J. (1996). The tarsus of erythrosuchid archosaurs, and implications for early diapsid phylogeny. Zoological Journal of the Linnean Society, 116(4), 347-375.
  • Gower, D. J. (2001). Possible postcranial pneumaticity in the last common ancestor of birds and crocodilians: evidence from Erythrosuchus and other Mesozoic archosaurs. Naturwissenschaften, 88(3), 119-122.
  • Gower, D. J. 2003, Osteology of the early archosaurian reptile Erythrosuchus africanus, Broom. Annals of the South African Museum, 110(1), 1 - 84.
  • Gower, D. J., Hancox, P. J., Botha-Brink, J., Sennikov, A. G., & Butler, R. J. (2014). A new species of Garjainia Ochev, 1958 (Diapsida: Archosauriformes: Erythrosuchidae) from the Early Triassic of South Africa. PloS one, 9(11), e111154.
  • Henderson, D. M. (2003). The eyes have it: the sizes, shapes, and orientations of theropod orbits as indicators of skull strength and bite force. Journal of Vertebrate Paleontology, 22(4), 766-778.
  • Ivakhnenko, M. F. & Kurochkin, E. N. (eds.) 2008. Fossil Vertebrates of Russia and adjacent countries. Fossil reptiles and birds. Part 1: A. Reference book for paleontologists, biologists and geologists. GEOS, 2008, 348 pp.
  • Nesbitt, S. J. (2011). The Early Evolution of Archosaurs: Relationships and the Origin of Major Clades. Bulletin of the American Museum of Natural History, 1-292.
  • O'Connor, P. M. (2006). Postcranial pneumaticity: An evaluation of soft‐tissue influences on the postcranial skeleton and the reconstruction of pulmonary anatomy in archosaurs. Journal of Morphology, 267(10), 1199-1226.
  • Parrish, J. M. (1992). Phylogeny of the Erythrosuchidae (Reptilia: Archosauriformes). Journal of Vertebrate Paleontology, 12(1), 93-102.
  • Paul, G. S. (1988). Predatory dinosaurs of the world: a complete illustrated guide. Simon & Schuster.
  • Pickford, M. (1995). Karoo Supergroup palaeontology of Namibia and brief description of a thecodont from Omingonde. Palaeontologia Africana, 32, 51-66
  • Sennikov, A. G. (1996). Evolution of the Permian and Triassic tetrapod communities of Eastern Europe. Palaeogeography, Palaeoclimatology, Palaeoecology, 120(3), 331-351.
  • Reig, O. A. (1970). The Proterosuchia and the early evolution of the archosaurs; an essay about the origin of a major taxon. Bulletin of the Museum of Comparative Zoology, 139(5), 229-292.

Wednesday, 31 August 2016

New paper: at last, a small pterosaur species from the latest Cretaceous

As the Cretaceous fossil record enters its final two stages - the Campanian and Maastrichtian - several unusual things seem to happen in the world of flying reptiles. Firstly, we see the end result of a steady drop off in pterosaur diversity leaving only azhdarchids - those often long-necked, long faced animals that we cover here with some regularity - with a strong, widespread fossil record. It's known that nyctosaurids and (thanks to recent discoveries) perhaps pteranodontids survived until the very end of the Mesozoic in at least two locations, but azhdarchids are globally distributed and dominate the pterosaur fossil record at this time. The overwhelming precedence of azhdarchids in the Late Cretaceous is an anomaly: at no other point in the pterosaur fossil record does one clade feature so prominently.

Secondly, Campanian and Maastrichtian pterosaurs are, without exception, pretty big animals. Many species from this time are renowned for their gigantic size: it's these stages which give us the famous 10 m wingspan, 250 kg colossi like Quetzalcoatlus, Arambourgiania and Hatzegopteryx, as well as a number of other giant azhdarchids which are too poorly known for generic titles. Coinciding with the evolution of the giants is a loss of small pterosaur taxa - those animals less than 2.5 m across the wings which are present, more-or-less, throughout the rest of pterosaur history. This shift in body size is sometimes interpreted as pterosaurs demonstrating 'Cope's Rule', the somewhat controversial proposal that species evolve towards large body size over time (Hone and Benton 2007; Benson et al. 2014). It's argued by some that competition from birds may be the driver behind this trend, as early avians fought small flying reptiles for ecological space and ultimately forced pterosaurs into larger sizes (e.g. Benson et al. 2014). Note that this concept is not without its detractors, including myself - I won't go into my reasons now but I plan to outline them here eventually.

Whether you agree with the bird-pterosaur competitive displacement hypothesis or not, we can't disagree that the end of the Cretaceous is almost entirely devoid of small pterosaur remains. Only a handful of specimens record small pterosaurs in the Campanian and Maastrichtian, and they're all tricky to work with. Aside from being highly fragmentary, some are controversially identified (such as Piksi barbarulna, an alleged small pterosaur from the Two Medicine Formation - see Agnolin and Varricho 2012 for the pro-pterosaur case) and others represent probable juvenile individuals (Godfrey and Currie 2005). Whatever it signifies, the lack of diminutive pterosaur specimens from the close of the Mesozoic is a real phenomenon of our fossil record, and any new specimen of a small, latest Cretaceous flying reptile has to be something to get excited about.

Enter: a new small, latest Cretaceous pterosaur specimen to get excited about

Title slide of my SVPCA 2016 talk, discussing the findings of Martin-Silverstone et al. 2016, out today. If you don't get the reference, you clearly get out too much, have too many friends and aren't watching enough crap TV.
It's this point where a new paper, published today by Liz Martin-Silverstone, myself, Victoria Arbour and Phil Currie comes in. Our new work, which you can check out without restriction at the open access journal Royal Society Open Science, presents a new small pterosaur fossil from the Campanian Northumberland Formation of British Columbia. The specimen number - RBCM.EH.2009.019.0001 - is pretty unwieldy, so I've been calling it the 'Hornby azhdarchoid' or the 'Hornby pterosaur' after it's discovery on Hornby Island, just off the coast of Vancouver. As you can see  below, the Hornby specimen is not pretty. Following our presentation of the fossil at SVPCA 2016, pterosaur guru David Unwin suggested we might have the ugliest pterosaur fossil on record (or at least tied the game). But while not well preserved, we do at least have several bones to play with: most of a humerus, three fused vertebrae (from the notarium, a set of fused shoulder vertebral elements), a few loose dorsal vertebrae and some other odds and ends that defy identification. This makes it the first set of associated bones of a small latest Cretaceous pterosaur, which is at least a step in the right direction for their paltry fossil record. For reasons discussed in the paper (concerning taphonomy, element size and likely identifications) we assume these remains represent one individual.

RBCM.EH.2009.019.0001, a fragmentary azhdarchoid pterosaur from the Campanian Northumberland Formation, British Columbia. It's, er, not the prettiest pterosaur specimen you'll ever see. Combination of figures from Martin-Silverstone et al. 2016.
I don't want to rehash the full gory details of our study here - please read the paper for the technical aspects - but instead want to outline our main points. The first thing to clear is that we've been careful to rule out an avian ID for the specimen. The Northumberland Formation contains several bird fossils and the quality of the specimen means that many obvious pterosaur features are missing. The Royal British Columbia Museum was kind enough to ship the specimen all the way from Vancouver, Canada to Southampton, UK just so Liz and I make a thorough assessment on this issue. Happily, we found the specimen to be very pterosaur like in every aspect (even as fragments, pterosaur bones are quite distinctive) as well as differing from Mesozoic birds in several ways. It particularly contrasts in having a notarium, which seem absent from Mesozoic birds (note that we compared the notarium element compared carefully with Mesozoic bird synsacra to be sure of our identification), as well as having a pterosaur-like, rather than avian, proximal humerus morphology. But we're not bird workers so, to be extra sure, we showed the material to fossil bird experts in Canada and the UK (including people who've identified and published on the Northumberland Formation avians). No-one we spoke to suggested an avian ID and, moreover, we are aware that other people with expertise in both birds and pterosaurs (including our paper editor) have seen the material and prefer a pterosaur ID. Based on our research and the testimonials of others, we're as confident as we can be that the Hornby fragments represent a pterosaur, not a bird.

We've identified the Hornby specimen as an azhdarchoid, and noted several features indicative of, but not conclusive to, an azhdarchid ID. We suspect the specimen is an azhdarchid because of its provenance and its basic anatomical characteristics, but the specimen does not contain the right bits to confirm an azhdarchid identity. Nonetheless, narrowing the specimen down to Azhdarchoidea allows us to estimate its body proportions and confirm that the specimen was indeed a small animal when it died. We estimated its wingspan using two methods factoring both the humerus and vertebrae, and each pointed to a wingspan between 1.4 and 1.6 m. That puts our pterosaur at a comparable size to a good sized-seagull and, while these are respectably-sized modern birds, this is small for a latest Cretaceous pterosaur. Rather than poking giraffes in the face, our little chap would only just be beyond predation risk from an average housecat (below). The only contemporary pterosaur competing with the Hornby azhdarchoid for size is Piksi, a poorly known possible pterosaur from the western US. Our new study lists a number of reasons why the pterosaurian characterisation of Piksi is problematic however: in short, its morphology is all wrong for a flying reptile and we suspect a non-pterosaurian ID is more likely. The Hornby specimen is thus a contender for the smallest latest Cretaceous pterosaur currently known.

A 1.5 m wingspan azhdarchoid next to one (SI) MrTiddlesmetre. From Martin-Silverstone et al. (2016).
This million dollar question, of course, is whether the specimen is a small juvenile or a small adult. The former would be neat, but the latter is potentially significant. The findings of recent, detailed histological examinations of pterosaur fossils are permitting increasingly good understanding of their growth regimes (e.g. de Ricqles et al. 2000; Prondvai et al. 2012), so we made a section of the humerus to understand how old the Hornby animal was when it died. Our section showed a mix of bone textures, some indicating that the specimen was still growing, but other features (secondary osteons, an endosteal lamella, lines of arrested growth and a large structure forming on the internal bone surface) are indicative of relative maturity (de Ricqles et al. 2000; Prondvai et al. 2012). We found the endosteal lamella (a band of bone deposited around the internal bone cavity) of particular interest, as this seems to signify the end of internal bone expansion in azhdarchoids, and is thus a hallmark of near-mature animals (note that this is not true for all pterosaurs - see Prondvai et al. 2012). The fused dorsal vertebrae are a further marker of maturity, as pterosaurs do not develop these features until they're at least subadults. The exact timing of notarium formation seems to differ from taxon to taxon (e.g. Bennett 1993; Kellner 2015), but their development does not seem to start until these animals were near to full size, if not at full size already. Putting these and a few other observations together suggests that the Hornby pterosaur was a latest-stage juvenile or subadult: in other words, it looks like a genuinely small pterosaur, not just a juvenile one. We don't know how much larger it might have got before it reached full size, but its ontogenetic characteristics and what we know of pterosaur growth regimes suggests it was close to maximum size at time of death. Given its estimated 1.5 m wingspan, it had a good chance of remaining smaller than the next smallest, 2.5 m wingspan pterosaur currently known the Campanian or Maastrichtian (McGowen et al. 2002).

What's inside the RBCM.EH.2009.019.0001 humerus? A mix of things, but among them are features indicative of late-stage juvenility/subadulthood. Please see the paper for details of this figure. From Martin-Silverstone et al. 2016.

A small pterosaur amongst the pigeons

There's obviously a limit to what a single fragmentary specimen can tell you about the evolution of a group, but what the Hornby specimen means for pterosaur evolution is interesting and - if we've interpreted it correctly - potentially significant. Most obviously, it suggests that small pterosaurs may have been present in the Campanian stage of the Late Cretaceous after all, at least in one part of the world. Regular readers will be aware that there's growing evidence for Late Cretaceous pterosaur faunas being less uniform than previously realised (e.g. Vremir et al. 2013, 2015), and our new specimen plugs into this picture nicely: it increasingly seems that the end Cretaceous wasn't just a stage for large-to-giant long-necked azhdarchids. What's more, while the specimen only provides one data point against the idea that birds ousted small pterosaurs, the presence of at least two types of bird in the Northumberland Formation seems to indicate small pterosaurs and birds coexisted in at least this palaeoenvironment. We might see this as a continuation of the coexistence pterosaurs and birds demonstrate in Jurassic and Early Cretaceous localities: maybe pterosaurs and birds got along OK after all.

...except when pterosaurs stole their eggs. Our PR art for the new paper, where a group of Hornby azhdarchoids perform guerrilla raids on shore-living Campanian bird nests. Take THAT, birds.
To my mind, one of the most significant things we do in the paper is discuss the 'face value' interpretations of Late Cretaceous pterosaur diversity: should we really be interpreting the lack of small pterosaur fossils as a genuine feature of their history when their fossil record is so patchy? We point out that some types of small pterosaurs - juveniles - had to exist in the Late Cretaceous, and yet their fossils are almost entirely unknown. We argue that this indicates a preservation bias against small bodied pterosaurs of any kind in the Campanian and Maastrichtian. Until we amass a good number of small juvenile pterosaur bones from this time without any small adults we cannot distinguish preservational interference from genuine biological signals. Perhaps the shift of pterosaurs from marine to non-marine habits through the Cretaceous (Butler et al. 2013) accounts for this lack of data. It's well known that terrestrial settings are less conducive to preserving relatively delicate fossils and small examples of even robust terrestrial animals like dinosaurs rarely fossilise in these deposits. We have to wonder what chance small pterosaur skeletons - which were strong in life, but fragile and weak once exposed to decay - have of making it into the fossil record in these settings. The fact the Hornby specimen is in such a sorry state perhaps reflects the rough time small pterosaur fossils experience under 'typical' fossilisation regimes, rather than the far gentler handling of animal remains evident at fossil Lagerstätten.

With all this said, the most important message of the paper has to be this: we need more data on small pterosaurs in the latest Cretaceous. The specimens we have are scrappy, hard to work with and offer limited scope for analysis. Thus, any small Late Cretaceous pterosaur material is significant, and whether they're lying unnoticed in museum collections or pulled straight out of the field, they are noteworthy specimens which need to be put on record. Curators and researchers, please keep your eyes peeled!

And that, in a nutshell, is our new paper: be sure to check it out if you want more details. You can also read Liz's take on the study over at The Conversation and other experts have been chiming in at news sites covering the story. With a bit of luck, this is not the only news you'll be hearing about Late Cretaceous pterosaurs from these quarters this year - more on these projects as they move along. All that's left to do is to thank Liz and Victoria for inviting me to collaborate with them on the new specimen - I learned a huge amount trying to get my head around this challenging material and its histology, and had a blast working with them.

This blogpost, paper and artwork are sponsored by Patreon

Regular readers will know that this blog and its art are sponsored by a suite of awesome Patrons, but this post is proof that this support goes further than mere internet tomfoolery and contributes to papers and outreach, too. Supporting my blog from $1 a month not only helps keep this blog ticking over, but helps me contribute thoughts, words and illustrations to scientific research. In return you get access to bonus blog content: additional commentary, in-progress sneak-previews of paintings, high-resolution artwork, and even free prints. For this post, we'll be talking about the PR art I've done for this research: how was the azhdarchoid reconstructed from that pile of rubble specimen? What's the story with the landscape image and why is there an ammonite in it? How many iterations did we go through to get that composition? Head over to Patreon to get access to this and the rest of my exclusive content!

References

  • Agnolin, F. L., & Varricchio, D. (2012). Systematic reinterpretation of Piksi barbarulna Varricchio, 2002 from the Two Medicine Formation (Upper Cretaceous) of Western USA (Montana) as a pterosaur rather than a bird. Geodiversitas, 34(4), 883-894.
  • Bennett, S. C. (1993). The ontogeny of Pteranodon and other pterosaurs. Paleobiology, 19(01), 92-106.
  • Benson, R. B., Frigot, R. A., Goswami, A., Andres, B., & Butler, R. J. (2014). Competition and constraint drove Cope's rule in the evolution of giant flying reptiles. Nature communications, 5, 3567.
  • Butler, R. J., Benson, R. B., & Barrett, P. M. (2013). Pterosaur diversity: untangling the influence of sampling biases, Lagerstätten, and genuine biodiversity signals. Palaeogeography, Palaeoclimatology, Palaeoecology, 372, 78-87.
  • Godfrey, S. J., & Currie, P. J. (2005). Pterosaurs. Dinosaur Provincial Park: A Spectacular Ancient Ecosystem Revealed, 292-311.
  • Hone, D. W. E., & Benton, M. J. (2007). Cope's Rule in the Pterosauria, and differing perceptions of Cope's Rule at different taxonomic levels. Journal of Evolutionary Biology, 20(3), 1164-1170.
  • Kellner, A. W. (2015). Comments on Triassic pterosaurs with discussion about ontogeny and description of new taxa. Anais da Academia Brasileira de Ciências, 87(2), 669-689.
  • Martin-Silverstone, E., Witton, M. P., Arbour, V. M, & Currie, P. J. (2016). A small azhdarchoid pterosaur from the latest Cretaceous, the age of flying giants. Royal Society Open Access, 3, 160333.
  • McGowen, M. R., Padian, K., De Sosa, M. A., & Harmon, R. J. (2002). Description of Montanazhdarcho minor, an azhdarchid pterosaur from the Two Medicine Formation (Campanian) of Montana. PaleoBios, 22(1), 1-9.
  • Prondvai, E., Stein, K., Ősi, A., & Sander, M. P. (2012). Life history of Rhamphorhynchus inferred from bone histology and the diversity of pterosaurian growth strategies. PLoS One, 7(2), e31392.
  • Vremir, M., Kellner, A. W., Naish, D., & Dyke, G. J. (2013). A new azhdarchid pterosaur from the Late Cretaceous of the Transylvanian Basin, Romania: implications for azhdarchid diversity and distribution. PLoS One, 8(1), e54268.
  • Vremir, M., Witton, M., Naish, D., Dyke, G., Brusatte, S. L., Norell, M., & Totoianu, R. (2015). A Medium-Sized Robust-Necked Azhdarchid Pterosaur (Pterodactyloidea: Azhdarchidae) from the Maastrichtian of Pui (Haţ eg Basin, Transylvania, Romania). American Museum Novitates, (3827), 1-16.

Friday, 12 August 2016

Trunk or no trunk, small or giant ears, long or short neck... what did the giant rhinocerotoid Paraceratherium really look like?

Giant, Oligocene rhinocerotoids Paraceratherium transouralicum engage in some early morning flirting. Because, in rhino speak, playing hard to get involves shoulder barges and head-butts.
Depictions of the giant indricotherines, relatives of modern rhinoceros that lived across mid- and eastern Asia during the Oligocene, have varied over time. We've known about these animals - which are part of a longer-lived (Eocene-Miocene) indricotherine lineage that includes a number of smaller, almost okapi-or horse-like species - for over 100 years and they have become regular fixtures in museums, books and those rare documentaries which offer glimpses into ancient life outside of the Mesozoic. Any yet, when we think of our favourite indricothere paintings - including those by our most celebrated mammalian palaeoartists such as Knight, Burian, Anton, and Buell - they often differ markedly in their depiction of these 15-20 tonne animals. Most notably, their neck proportions, overall robustness, the development of a proboscis or trunk, and - most recently - the size of the ears are all inconsistent. Why are these animals so differently depicted, and should we rule out some of the anatomies we've seen in palaeoart in the last century? Having faced these questions recently when asked to restore this animal myself (above), I thought I'd share some of what I learned in my research here.

The obligatory note on nomenclature

It almost seems tradition that any article or paper on indricotherines requires an aside on their confused taxonomy. As has been the case for decades now, the taxonomy and systematic nomenclature of these giant rhinocerotoids are a matter of ongoing discussion. It is widely appreciated that several giant indricotherine species from roughly contemporaneous Oligocene Asian sediments can be identified, but how many species they represent, and how they are related to each other, is not clear. At least seven generic titles and many more species names have been given to the largest of these animals over the years (Indricotherium and Baluchitherium are perhaps the most famous generic labels), but some authors (e.g. Lucas and Sobus 1989, Prothero 2013) tidy all or most of these taxa into three species of the oldest established genus, Paraceratherium. Arguments persist, however, that at least one other, perhaps slightly smaller genus existed, Dzungariotherium (Qiu and Wang 2007). Geologically older indricotherine genera such as the Eocene Urtinotherium are also wrapped into these discussions as remains attributed to the Oligocene genera are sometimes argued as having greater affinity to these older taxa (Prothero 2013).

This confusion is sometimes framed as a 'lumper/splitter' philosophical distinction, but it does not help that the fossil record of these giant rhinocerotoids is far from exemplar: giant indricotherine specimens can be fragmentary, of starkly contrasting size with one another, and many suffer from distortion. The fact that 20th century indricotherine science developed with Asian and American teams working largely in isolation, with limited access to certain specimens and literature, has also contributed to the confused history of this group. Those interested in the history of indricothere taxonomy should check out Prothero (2013) for an overview. For now, it will serve us to simply state that the best known, biggest and most famous of these animals currently resides as the taxonomic address of Paraceratherium transouralicum. This is the species most of us think of as 'the' giant indriotherine as well as the taxon that has carried both the Indricotherium and Baluchitherium label at one time or another. It's also the focus of most artwork of giant rhinoceratoids, and thus forms our primary interest here.

Giant rhino, bulky giraffe or giant workhorse?

One reason we see such variation in indricotherine appearance is that researchers have produced vastly different interpretations of its anatomy in the last 100 years. But unlike, say, dinosaurs, where older reconstructions have been (for the most part) abandoned in favour of newer, more accurate interpretations, educators and researchers continue to publish skeletal reconstructions published in the 20s and 30s despite our improved knowledge of indricotherine anatomy, documented criticisms of these older works, and the availability of more modern, theoretically better-informed reconstructions.

Many readers may be aware that the first reconstruction of Paraceratherium, published by Osborn (1923a), showed a form not too far off a giant rhinoceros - a heavyset, short-necked animal with a deep torso and short legs. Osborn published a revised version almost immediately after his first effort, which had a much longer neck and longer legs thanks to data provided by additional fossil material (Osborn 1923b). A shorter-necked version was then produced by Granger and Gregory (1935, 1936), who scaled the remains of numerous, differently-sized individuals from a range of collections to create their robust, gigantic take on indricotherine anatomy. Although this reconstruction has been quite influential, Fortelius and Kappelman (1993) have been critical of the scaling methods used by Granger and Gregory, calling their interpretation 'a highly speculative creation indeed'.

Paraceratherium has been variably reconstructed over the years, with particular disagreement over how long the neck was compared to the body. So far as I can tell, a consensus on the life appearance of these animals has yet to be reached.
A third contrasting reconstruction was published a few decades later by Gromova (1959), based on a composite mounted skeleton in the Paleontological Institute, Russian Academy of Sciences. This reconstruction, executed by N. Yanshinova, was accompanied by several wonderful muscle and skin reconstructions which palaeoart fans will not want to miss. Both the mount and reconstruction show a gracile, giraffe-like form with a remarkably long neck and, in being based on a relatively complete set of giant indricotherine remains, some have argued it is a superior take on indricotherine anatomy than those produced by Osborn, or Granger and Gregory (Fortelius and Kappelman 1993). The most striking aspect of this reconstruction is its very long neck. We have to stress that this is extrapolated from a few incomplete cervicals associated with postcranial material, and its exact length remains uncertain - a complete set of neck bones remains elusive for Paraceratherium. This is another reconstruction which has been quite influential (helped, no doubt, by its apparent basis for the BBC's Walking with Beasts 'Indricotherium') but, again, it has not escaped criticism. Paul (1997) suggested that multiple aspects of this mount and reconstruction were erroneous, including the length of the neck, the size of the pelvis and depth of the ribcage, the length of the feet, and the ratio of the humerus and femur, as well as the fully erect posture of the limbs.

And so we turn to another indricotherine skeletal reconstruction, produced by Paul (1997). This restoration incorporated data from the same specimens used in the efforts above and came out somewhat 'averaged' between the more heavyset restorations of the early 20th century and the gracile interpretation of the 1950s. It looks, in overall form, more like a giant workhorse than it does a giant rhino or bulky giraffe. Paul (1997) provides some discussion of the reconstruction process - this is worth a read if you're interested in the life appearance of Paraceratherium and its relatives. Paul's interpretation has, to my knowledge, escaped criticism to date and, to the contrary, Larramendi (2016) described this reconstruction as 'accurate', although did not elaborate on why it should be considered superior to older efforts.

The million dollar question here is obvious: which one of these different takes on Paraceratherium is 'right'? To be honest, I'm not sure. The situation is compounded by the fact that a lot of indricotherine literature is obscure, that the specimens fragmentary and that many of them await description. I was hoping that Donald Prothero's recent (2013) book Rhinoceros Giants, which is solely dedicated to Paraceratherium, would provide some insight on this matter, but it's not a great help here - it provides no real evaluation on the different reconstructions and does not even mention Paul's 1997 effort. My work above is primarily based on Paul's (1997) skeletal but this is largely because of principle rather than real insight. Paul's work is the most modern and, of course, he's made a career out of reliably reconstructing extinct animals. The brief endorsement from Larramendi (2016) helps here too, of course, but a longer discussion of the relative merits and detriments of each interpretation would be useful. Opinions from others with more insight into this matter are welcome in the comments below.

A tapir-like proboscis... on a rhino?

Turning our attention to the face, did Paraceratherium and its relatives have relatively short-lipped faces like those of rhinos, or long, mobile proboscides like their more distant relatives, the tapirs? Despite mammal lips and nasal tissues being highly fleshly and thus only rarely entering the fossil record, this is a surprisingly easy question to answer. Whether rhino, tapir or anything else, a suite of osteological characters seem to correlate well with the presence of proboscides. Briefly summarised, these are: narrow snouts; retraction of the nasal openings towards the orbits; the presence of large muscle scars, bony knobs and other muscle attachment markers around the nasal opening (particularly in the dorsal region); retraction of the nasal bone (the 'roof' of of the nasal opening); deepening of the premaxillary bone (the bone making the jaw tip); anterior migration of the orbit; a large intraorbital canal (a foramen situated in the cheek region, just in front of the eye - it houses the nerves and blood vessels for our anterior face muscles); and strengthening of the posterior skull regions related to supporting the weight of the head on the neck (Wall 1980). Note that the criteria for elephant-like trunks are similar, but slightly different.

Paraceratherium transouralicum (formerly Baluchitherium grangeri) skull in dorsal, lateral and ventral views. Note features around the skull anterior linked to proboscis development (see text). From Osborn (1923b).
Paraceratherium skulls (above) meet these criteria well and, all else being equal, we have to say that yes, it looks likely that these giant rhinoceratoids had short proboscides in life, presumably to assist browsing from trees and bushes (Prothero 2013). The view that they had more typically rhinoceros-like faces is hard to defend in light of these cranial features: mammal skulls just don't have those retracted nasal openings, associated deep muscle scarring etc. unless they were doing something unusual and sophisticated with their upper lip and nasal tissues. The reality of giant indricotherines with dangly noses may seem hard to swallow for those of us used to shorter lipped versions, but given the relationships between rhinos and tapirs, the fact that some other fossil rhinocerotoids probably had proboscides as well (e.g. Wall 1980), and the independent development of long, flexible noses in numerous mammal lineages, we can't really see this as unusual. Moreover, we need to remember that modern rhinos are derived animals in their own right and separated from the indricotherine lineage by tens of millions of years. They aren't necessarily always going to be the best models for the life appearance of their fossil ancestors.

And big, elephant-like ears, right?

Finally, let's tackle the component that everyone now mentions about indricotheres since seeing the Carl Buell's cover art for Donald Prothero's Rhinoceros Giants:

Indiana University Press.
Yikes, elephant ears? For those of us familiar with the history of indricotheres in art, where their ears are restored as typically rhinoceros-like, this is a shocking, double-take image. Within the book, Prothero justifies the restoration:

"...indricotheres were larger in body mass than any living elephant and almost certainly had problems regulating their body heat at such large size. Elephants must do all they can to increase the surface area of their bodies to release as much excess heat as possible, which is why they have huge fan-like ears full of blood vessels that are essentially giant radiators. Given the huge size of indricotheres, it seems likely that they too should have had elephant-like ears, or at least very large ears of some shape, much larger than they are usually drawn."
Prothero, 2013, p. 90.

The text continues to suggest that this appearance is not without anatomical support, the prominence of the mastoid and paroccipital processes (projections of bone situated behind the ear opening, adjacent to the posterior surface of the skull) being similar to the condition in certain elephants and mastodonts, and therefore indicative of large, flappy ears (Prothero 2013).

I have mixed feelings about this reconstruction. I like it for two reasons. The first is that it's nice to see indricotheres being distanced from their depiction as giant, long-necked rhinoceroses - again, it's not unreasonable to think they may have looked quite different in to modern rhinocerotids in many aspects. I also like these ears for being an All Yesterdays-style speculation on soft-tissue adaptations in extinct species. If we can use this as an excuse to give fat stores to desert sauropods or fuzzy hides to Arctic ceratopsids, then we can give large ears to giant rhinoceratoids.

On the other hand, I'm not convinced that they're as likely as Rhinoceros Giants suggests. It's clear from our modern fauna that ear size does not correlate with body mass in terrestrial mammals. By this logic many rhinos and giraffes should have proportionally large ears too, which they evidently do not. We also have to consider that even larger animals than indricotheres, dinosaurs, almost certainly got by without giant ears to help lose heat. And yes, while dinosaurs may have used different metabolic strategies to mammals, one inescapable consequence of giant size is a constant high body temperature. At least some investigations into the proportions of large dinosaurs suggest that development of their features - such as sauropod necks - were not driven by thermoregulatory pressures (Henderson 2013).

We should also consider the unusual nature of elephant thermoregulation: they are not typical mammals when it comes to controlling body heat. For one, they're atypically compact compared to other large mammals because they have extremely short necks, giant, round heads, and big, rotund torsos. This is a suboptimal bauplan for thermoregulation because it minimises surface area with respect to volume, and thus reduces the available area for elephants to dump excess heat. Moreover, unlike most mammals, they lack sweat glands (Wright and Luck 1984), do not pant, and they live in climates which are so warm that for much of the day they cannot shed heat through simple convection, big ears or not (Weissenböck et al. 2012). Elephants can, of course, regulate their temperature, but they need to employ different strategies to the rest of us mammals. These include maintaining moist skin with mud bathing and trunk spraying (Wright and Luck 1984), maintaining a sparse set of body hair to aid thermal escape (Myhrvold et al. 2012), using heterothermy (Weissenböck et al. 2012), the development of 'thermal windows' in their skin (Weissenböck et al. 2010), having loose and highly wrinkled skin to boost surface area and - of course - fanning their blood-vessel rich ears to help lose heat, when ambient temperatures are low enough for this to make a difference.

Silhouettes of the largest land mammals of all time, Paraceratherium transouralicum and Palaeoloxodon namadicus. Note the relatively gracile build of Paraceratherium - all the better for improving surface area:volume ratio, and thus superior for radiating heat. The numbers at the base of the image refer to estimated shoulder heights and tonnage. From Larramendi (2016).
These facts suggest elephants should not be used as direct thermoregulatory models for a giant rhinoceratoid. Modern rhinos other perissodactyls are much more typical in their thermoregulatory approaches: they have sweat glands and use panting behaviours (Hiley 1977) as well as some special tactics, such as enhanced vascularisation in the skin folds of certain rhino species (Endo et al. 2009). We have to assume that indricotherines at least had these entry level perissodactyl adaptations and, if so, they would have an advantage over elephants in hot climates. Indricotherines also benefit from being more complicated in form than elephants. They have longer limbs and necks, as well as a proportionally smaller head, and this enhances their surface area:volume ratio. Again, makes them better adapted to cope with heat as they have a shape better suited to radiating excess body heat. And of course, there's no reason to assume this could not have been augmented with wrinkled or folded skin or sparse hair. The picture emerging from these points is that big ears are only one strategy that big animals may use to keep cool, and maybe one that will only arise in specific circumstances. The idea that indricotherines would have big ears just because of their size is far from certain.

Basic muscle layout and trajectories (arrowed lines) of a modern horse. Note their superficial attachment and position high on the head - the ear canal itself is about halfway down the back of the skull. The 's' is the scutiform cartilage, which hangs out in front of the ear over the jaw muscles. From Goldfinger (2004).
But isn't all this moot because of Prothero's (2013) observations about the mastoid and paroccipital processeses being expanded, and thus giving big ears something to hang off? I'm suspicious about the significance of this observation. So far as I can determine, neither the mastoid or paroccipital have anything to do with anchoring ear tissues in modern perissodactyls (or perhaps any mammal). This might be because in most mammals - primates being one obvious exception - the ear pinnae are vertically displaced from the ear canal and attach to the head via a series of muscles and cartilages at the top of the skull (above). Only select few of the ear muscles reach the skull directly and these anchor, with very small attachments, to the skull midline, dorsoposterior margin and zygomatic arch. The rest have no osteological connection at all, anchoring instead to cartilage, membranes overlying facial musculature, or even the side of saliva glands. The paraoccipital and mastoid processes do have important roles in the muscular system but these are to do with neck, jaw and tongue muscles, not ears. Thus, unless indrictotheres were doing something different to modern mammals, those particularly big processes behind their ear openings were probably more to do with supporting and moving the head than they were holding big ears, and may have little significance to the big-eared indricotherine hypothesis.

So...

Putting all this together, it seems that there might be less need for uncertainty about indricothere appearance than our various artworks suggest. We should be saying 'yes' to some sort of proboscis, and 'probably not' to big ears (or, at least, 'there's no reason for them'). The elephant (or, giant rhino, if you prefer) in the room is the proportion issue, and it would be good to see folks who really know rhinocerotoid anatomy pore over those various reconstructions to ascertain which (if any) are the best representation of indricotherine form.

Next time: either the Next Big (but also kinda small) Thing in pterosaur research, or another trip to the Triassic.

Big rhinos need big support - thank goodness for Patreon

The paintings and words featured here are sponsored by another group of (metaphorically) giant mammals, my Patreon backers. Supporting my blog from $1 a month helps me produce researched and detailed articles with paintings to accompany them, and in return you get access to bonus blog content: additional commentary, in-progress sneak-previews of paintings, high-resolution artwork, and even free prints. For this post, we'll be taking a further look at the anatomy of the Paracertherium in my painting, above. Why do they have little manes and stripy faces? Are those child rhinos at the back a bit fuzzy? And why do the main animals look like they're fighting? Head over, and sign up to Patreon to get access to this and the rest of my exclusive content!

References

  • Endo, H., Kobayashi, H., Koyabu, D., Hayashida, A., Jogahara, T., Taru, H., Oishi, M., Itou, T., Koie, H. & Sakai, T. (2009). The morphological basis of the armor-like folded skin of the greater Indian rhinoceros as a thermoregulator. Mammal Study, 34(4), 195-200.
  • Fortelius, M., Kappelman, J., 1993. The largest land mammal ever imagined. Zoological Journal of the Linnean Society, 108, 85-101.
  • Goldfinger, E. (2004). Animal Anatomy for Artists: The Elements of Form. Oxford University Press.
  • Granger, W., & Gregory, W. K. (1935). A revised restoration of the skeleton of Baluchitherium, gigantic fossil rhinoceros of Central Asia. American Museum of Natural History, 787, 1-3.
  • Granger, W., & Gregory, W. K. (1936). Further notes on the gigantic extinct rhinoceros, Baluchitherium, from the Oligocene of Mongolia. American Museum of Natural History, 72, 1-73.
  • Gromova, V. (1959). Giant rhinoceroses. Trudy Paleontologiskei Institut Akademie Nauk, 71, 1-164.
  • Henderson, D. M. (2013). Sauropod necks: are they really for heat loss?. PloS one, 8(10), e77108.
  • Hiley, P. G. (1977). The thermoregulatory response of the rhinoceros (Diceros bicornis and Ceratotherium simum) and the zebra (Equus burchelli) to diurnal temperature change. African Journal of Ecology, 15, 337-337.
  • Larramendi, A. (2016). Shoulder height, body mass and shape of proboscideans. Acta Palaeontologica Polonica, 61, 537-574
  • Lucas, S. G., & Sobus, J. C. (1989). The systematics of indricotheres. In: Prothero, D. R., and R. M. Schoch (eds.) The Evolution of Perissodactyls. Oxford University Press, New York, 358-378.
  • Myhrvold, C. L., Stone, H. A., & Bou-Zeid, E. (2012). What is the use of elephant hair?. PloS one, 7(10), e47018.
  • Osborn, H. F. (1923). The extinct giant rhinoceros Baluchitherium of Western and Central Asia. Natural History, 23, 208–228.
  • Osborn, H. F., & Berkey, C. P. (1923b). Baluchitherium grangeri, a giant hornless rhinoceros from Mongolia. American Museum of Natural History, 78, 1-15.
  • Qiu, Z. X., Wang, B. Y., 2007. Paracerathere fossils of China. Palaeontologia Sinica, C29, 1-396
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  • Weissenböck, N. M., Weiss, C. M., Schwammer, H. M., & Kratochvil, H. (2010). Thermal windows on the body surface of African elephants (Loxodonta africana) studied by infrared thermography. Journal of Thermal Biology, 35, 182-188.
  • Weissenböck, N. M., Arnold, W., & Ruf, T. (2012). Taking the heat: thermoregulation in Asian elephants under different climatic conditions. Journal of Comparative Physiology B, 182(2), 311-319.
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Monday, 25 July 2016

The 'Pteranodon complex' and dismantling our understanding of the most famous flying reptile

Pteranodon longiceps, Pteranodon sp. or something else entirely? In recent years one of our most famous and abundant pterosaurs has been carved up into multiple species, but is this overzealous taxonomic splitting, or is there more to it than that?
Writing about pterosaurs can be difficult because so much of their classification is disputed. The number of pterosaur species, their assignment to different groups, appropriate clade nomenclature and the arrangement of branches in the pterosaur tree are all contested, sometimes to polarising extents.
A bastion of taxonomic stability in all this is Pteranodon, everyone's favourite giant, toothless Late Cretceous ornithocheiroid (or pteranodontoid) from interior regions of the United States. Known since the late 1860s, Pteranodon is one of the most substantially sampled of all pterosaurs and we now have well over 1100 specimens in museums around the world. This record stems from a relatively limited geographical area and is constrained stratigraphically to the Smoky Hill Chalk Member of the Niobrara Formation, with a smattering of fossils from the overlying Pierre Shale Group.

A series of papers documenting Pteranodon anatomy, variation and stratigraphy, all penned by pterosaur expert S. Christopher Bennett during the 1980s-2000s, have made this pterosaur one of the best understood of all flying reptiles (perhaps the most important entries in this series are Bennett 1992, 1993, 1994, 2001a, 2001b). These publications are the result of examining several hundred Pteranodon specimens and are among the most significant and comprehensive contributions to pterosaur literature in modern times. I recommend them to any students of vertebrate palaeontology: even if you don't agree with their conclusions, they're great examples of clear writing, of hypotheses being established and tested, and of large amounts of data being presented clearly and logically.

Skeletal restorations of P. longiceps male (the larger animal) and female morphs, based on Bennett (1992). Illustration from Witton (2013).
For pterosaur workers, one of the most important outcomes of Bennett's work was a robust taxonomy for Pteranodon. This genus was once a polyspecific monster composed of 13 species, but Bennett (1994) whittled it down to two, stratigraphically segregated forms: the geologically older Pteranodon sternbergi and its direct descendent, Pteranodon longiceps (Bennett 1994). Measurements and observations of hundreds of Pteranodon fossils and detailed analysis of its growth regime suggested that most variation seen in Pteranodon samples resulted from sexual dimorphism (above), where (presumed) males are identical to females except for being 50% larger, bearing bigger headcrests and narrower pelves (Bennett 1992). We can recognise osteologically mature Pteranodon by details of skeletal fusion, bone texture and histological structure (Bennett 1993), thus allowing us to determine that the small, 'female' individuals were not just juveniles but, in fact, relatively small adults. Although sexual dimorphism had been proposed for pterosaurs previously, few studies went to such detail in making their case and Bennett's 1992 work stands as one of the better cases made for sexual dimorphism in a fossil reptile. This complex consideration of Pteranodon diversity can be viewed as a milestone in our modernisation of pterosaur research, it being a clear sign that pterosaur studies were maturing to the level attained by dinosaur or mammal vertebrate palaeontology in the 1980s and 1990s. This work has been uncontested for over a decade and subsequent studies have since found evidence for similar morphological trends in other pterosaur species. Hurrah, hooray and huzzah for Pteranodon, then, the pterosaur worker's faithful friend and our securest mast in a taxonomic storm.

But then things got a complex

Given the established status of Pteranodon taxonomy it came as something of surprise when, in 2010, a counterargument to Bennett's interpretation of Pteranodon was published. Another big name in modern pterosaur research, Alexander Kellner, proposed that Bennett's Pteranodon was in fact a 'complex' of at least four species (perhaps five) in three genera (Kellner 2010). Kellner's alternative scheme suggested that the giant, swollen-crested sternbergi was different enough from longiceps to warrant a separate genus, and resurrected the 'subgenus' Geosternbergia for this purpose (giving us the rather daft name Geosternbergia sternbergi). A second Geosternbergia species was proposed for a partial skull referred to P. longiceps by Bennett (1994), which Kellner named G. maiseyi. Another skull, this one with a broken crest but the best preserved rostrum of any giant Pteranodon specimen, was said to represent a third pteranodontid genus, the deep-snouted Dawndraco kanzai. Finally, although not naming a new taxon, Kellner (2010) singled out another P. longiceps specimen as being distinct from this species, arguing that this long-crested specimen has a crest which is too upright to be referred to longiceps: he referred this simply to Pteranodon sp. for now. You can see these skulls, and how they contrast with Bennett's older scheme, below.
Differing interpretations of some important Pteranodon skulls. Blue text and panelling reflects the Bennett (1994) interpretation of Pteranodon skull taxonomy, green text shows where Kellner (2010) differs. Skull images borrowed from Bennett (1994).
This might not seem like a big deal - after all, famous fossil species are carved up all the time - but this has implications beyond just having to learn a few new binomials. The presence of multiple genera in our 'Pteranodon' sample makes it difficult to classify the majority of Smoky Hill pterosaur material, and thus our thousand-strong Pteranodon catalogue mostly becomes Pteranodontidae incertae sedis, with a few named skulls. With that, the statistical support for our hypotheses of Pteranodon variation, growth and sexual dimorphism require reevaluation, because we've lost our grip on what animals those hundreds of measurements actually pertain to. For pterosaur workers, this is something to pay attention to: one of our 'cornerstone' taxa might not be the dependable, go-to reference pterosaur that we thought it was, and its palaeobiology may not be as well understood as previously considered.

I've been asked about the 'Pteranodon complex' several times and thought it was time to share my thoughts here. I normally avoid talking about detailed taxonomy because I'm aware how dry it can be, but the Pteranodon controversy is pretty interesting. There are lot of strands of data to consider, some philosophising about palaeontology itself, and - if nothing else - the reality about the fossils behind Pteranodon might be of interest. This is only a summary of course - if you're interested, you really need to check out the papers cited below for the full details.


How understanding hundreds of Pteranodon specimens hinges on a handful of important ones

The holotype skull of Pteranodon longiceps, the only Pteranodon specimen which can be objectively referred to the genus. This skull is from a small (presumed female) morph. From Eaton 1910.
Since at least Eaton (1910) it's been recognised that the majority of Pteranodon specimens are not diagnostic to specific level. Most Pteranodon fossils are bits of limb or scraps of bodies that can be identified as Pteranodon (or pteranodontid, if you prefer) but not much further. To know what species we're looking at we need the back of a skull, and ideally, a big one with a good amount of crest. One of the key points to stem from both Bennett's (1994) taxonomic review and Kellner's (2010) paper is that Pteranodon species are best differentiated by the orientation and shape of their headcrests. Bennett (1994) considered this in a fairly simple way: sternbergi has an upright and distally swollen crest, while longiceps has a more posteriorly directed, distally tapering one. These distinctions can be seen in smaller skulls, but are most obvious in the bigger ones. sternbergi and longiceps might also be distinguished by the orientation of the posterior skull margin (sternbergi being more upright than longiceps) and slenderness of the mandible (sternbergi being a touch shallower) but the crest shape and angle is the best way to tell these taxa apart.

Bennett's characterisation may seem quite broad, maybe even simplistic, but there's a reason for that: no two Pteranodon crest specimens are entirely alike and none of our better, larger skull specimens are complete (below). We have some excellent and complete smaller skulls (above), and several incomplete large specimens, but any visage you see of a long skulled, long-crested Pteranodon fossil is an interpretation of fragmentary specimens. Bennett's (1994) taxonomy reflects this, using relatively broad characters to separate the species because the material ultimately offers limited scope for detailed comparison or augmentation with other characters. The fact that the crests differ somewhat within Bennett's species is explained by their likely role in visual communication rather than biomechanics (Bennett 1992; Tomkins et al. 2010): such structures are often far more variable in appearance, and sensitive to factors like ontogeny, than strictly 'functional' anatomies.
Line drawings of important Pteranodon/pteranodontid skulls from Witton (2013). A, skull still referred to P. longiceps; B, isolated crest and part of the braincase region referred to either longiceps (Bennett 1994) or Pteranodon sp. (Kellner 2010); C, holotype of longiceps; D, holotype of Pteranodon (or Geosternbergia) sternbergi. Note the twisted posterior skull face in B and how little of the skull remains in D.
Kellner (2010) argues that Bennett's interpretation accommodates too much morphological variation however, picking out several skull characters as sufficiently distinctive to warrant erecting new genera and species. The diagnoses for these new taxa are much more specific than those offered by Bennett, pertaining not only to crest shape and angle, but also size and shapes of skull bones, skull openings and rostrum morphology. Partly because these criteria are quite specific, these novel pteranodontids are currently represented by single specimens. And it's here that I think we hit a bump with the 'Pteranodon complex' hypothesis. The diagnoses are quite specific, and we have good reason to think a lot of the variation apparent in Pteranodon fossils is not taxonomic in origin. For instance, taphonomic damage and the significant crushing that affects all Pteranodon bones (most Pteranodon bones are reduced to thicknesses of mere millimetres) means no two Pteranodon skulls are identical, and many diagnostic characters suggested by Kellner (2010) - specifically those pertaining to bone lengths, fenestra sizes and so on - have yet to be demonstrated through illustrative or quantified means. We've yet to see the measurements, data tables or an illustrated series of Pteranodon skulls which show these features are atypical against a range of specimens, and thus suitable to base new taxa on.

It's not just taphonomic and diagenetic effects which are of concern: there are palaeobiological trends to consider, too. For example, Kellner (2010) uses the breadth of the crest base as a diagnostic feature for both Dawndraco and G. maiseyi, noting that the former has a crest base located largely behind the eye socket, while the latter is expanded to erupt well in front of the orbital region. But Bennett (1994) gives reason to think that crest base size is linked to growth and size, not taxonomy. As can be seen above, there's a steady correlation between crest base size and skull size: larger skulls have much thicker crest bases extending far in front of the orbit than smaller skulls (Bennett 1994, 2001a). Although Kellner (2010) mentions that Dawndraco is a relatively mature specimen, and thus maybe unlikely to change its crest size, there's no discussion of the fact that the Dawndraco skull is quite a bit smaller than some other 'large' Pteranodon skulls (below). The fact this small skull has a smaller crest is, of course, consistent with Bennett's crest scaling hypothesis. Similarly, the wide-crested maiseyi skull meets Bennett's predictions that it should - as a big individual - also have a relatively large crest base.

Dawndraco (red) is a bit of a wimp compared to the largest Pteranodon skulls. Black is the sternbergi holotype, blue is the maiseyi holotype. Note how the crest bases of the black and blue skulls are much broader than that of Dawndraco. Illustrations adapted from Bennett (1994).
Some parts of the 'Pteranodon complex' hypothesis also face issues with specimen comparability. Some allegedly diagnostic features are based on very poorly understood aspects of Pteranodon anatomy, such as the relatively deep jaw of the Dawndraco skull. According to Kellner (2010) this rostrum is diagnostically deep and peculiarly shaped: this is certainly true when compared to complete smaller Pteranodon skulls, but no large Pteranodon has well-preserved jaws and we can't compare like-with-like. The best we can do is look at fragmentary remains, all of which suggest large Pteranodon also had deep, subparallel-sided jaws (below; Bennett 1994, 2001a). However, because none of these are associated with posterior skull remains, we can't gauge their depth in any context. This being the case, the fact that Dawndraco has the deepest rostrum known from a pteranodontid is of questionable significance: similar morphologies clearly existed in other Pteranodon, we just can tell if they're identical to Dawndraco or not. Similar issues occur when trying to fathom the significance of cranial crest shape and orientation for some unusually crested specimens. Many of these crests are only partly preserved, or not associated with substantial skull remains. As noted above, we have reason to think the context of the wider skull anatomy is important for interpreting crest anatomy, and this is reason for caution when it comes to erecting new pteranodontid taxa based on these specimens. Clearly, the issue here is that we have a huge amount of data for Pteranodon, but only a tiny part of it is taxonomically relevant, and only a fraction of that portion can be compared to a meaningful degree across a good number of specimens. Big sample sizes are meant to make things clearer in science, but for Pteranodon they seem to make things more complicated!

The Dawndraco skull compared to fragmentary Pteranodon sp. jaw tips. Note how the subparallel dorsal and ventral margins and (predicted) Dawndracro overbite are present in other Pteranodon fossils. Note that some small Pteranodon have overbites too. Drawings after Bennett (1994).

Pteranodon stratigraphy and the significance (or not) of geological boundaries

Both Bennett's and Kellner's taxonomies consider Pteranodon distribution through the Niobrara Formation and neighbouring rock units, but there are fundamental differences in how they treat this data. Bennett's (1994) approach sees morphology trump stratigraphy in that the ranges of his species are dictated wholly by specimen anatomy. This is essentially the approach typically taken by biostratigraphers, where it is considered (and relied upon) that species distribution is not linked to our designation of rock units. In this scheme, it doesn't matter where the specimen occurs, but what it looks like that matters. The fact that all the 'sternbergi morphs' occur at the base of the Smoky Hill Chalk Member, and all the 'longiceps morphs' occur at the top (and somewhat beyond - see below) is the basis for Bennett's (1994) idea that our Pteranodon sample is a single, evolving population which entered the fossil record as sternbergi, and left as longiceps. The fact that these species do not overlap can be viewed as helping the verify the Pteranodon chronospecies hypothesis.

Kellner (2010) takes a different approach to stratigraphy, where provenance is a factor in the likelihood of a specimen being assigned distinct taxonomic status. A good chunk of Kellner (2010) is devoted to discussing the role of stratigraphy in taxonomy, it being argued that Pteranodon skulls found several levels away from each other were not contemporaries and thus cannot be reliably assessed for intraspecific variation. When this happens, taxonomic significance takes over as the most likely (or perhaps default) interpretation of morphological differences.

Kellner (2010) makes specific mention of the fact that neither the Dawndraco or maiseyi skulls are from the same horizons as other Pteranodon type material (below). Particular attention is drawn to maiseyi, which comes from the Sharon Springs Formation: a unit two formations above the Niobrara Formation and its glut of Pteranodon material. Of this, Kellner states: "One could argue that the morphological differences of Geosternbergia maiseyi might be due to ontogeny, individual variation or even sexual dimorphism, but there is a considerable time gap between these [pteranodontid] species that never co-existed." (Kellner 2010, p. 1078). The implication here is that there is a stratigraphic limit to when similar-looking animals might be considered conspecific, and that morphological similarity is eventually overruled by provenance.

Pteranodons in time - click to embiggen and see full details. Grey lines show distribution of key Pteranodon
specimens, black lines show those associated with skull illustrations. Skull diagrams from Bennett (1994), data from Bennett (1994); Hargrave (2007) and Kellner (2010). These discussions touch on almost philosophical elements of palaeontological science, and I expect readers will differ as to which approach they think is most useful. Personally, I don't agree with the use of stratigraphy in taxonomic considerations. It's generally accepted that paleontology uses a morphology-based species concept (morphospecies) and, if that's the case, we have to stick by it. This means letting morphology dictate the ranges of fossil species and not deciding a priori that a span of time/extent of rock exceeds an acceptable 'species range'. For abundant, well-documented groups we may be able to bolster such concepts with a sense of their speciation frequency but, with rare fossils like pterosaurs, we know next to nothing about their evolutionary rates. And as unusual as it may seem for a pterosaur to span several formations, there are taxa that seem to do this (Anhanguera, Istiodactylus, Quetzalcoatlus, Rhamphorhynchus are well known examples). Moreover, plenty of other groups pay little attention to the stratigraphic boundaries that we set. Indeed, the whole science of biostratigraphy is is more or less founded on this fact: we can date the rock record using fossils because so many species do transcend stratigraphic boundaries. Stating that a fossil cannot be conspecific with another just because it occurs in younger or older rocks seems presumptuous and at odds with trying to understand evolutionary history.

More specific concerns with the 'Pteranodon complex' approach to stratigraphy is that its perceived issue with Pteranodon ranges are not mirrored by those who work on other Niobrara Formation vertebrates. From fish to marine reptiles, it's widely thought that many Niobrara species persisted through big chunks of the three million year period recorded by the Smoky Hill Chalk Member and Pierre Shale Group (e.g. Everhart 2005; Carpenter 2008). If large swathes of the Smoky Hill Chalk fauna can survive over long periods of time, why can't Pteranodon species? It is noteworthy here that Hargrave (2007) identified new, potentially diagnostic Pteranodon longiceps bones from the Pierre Shale. If so, this bolsters older suggestions that longiceps occurs above the Niobrara Chalk (Kellner (2010) was unconvinced of their referral to longiceps, however). We might also note that the 'Pteranodon complex' taxa accord less with stratigraphy than alternatives, in that Geosternbergia disappears during the interval represented by the upper Smoky Hill Chalk and Gammon Ferruginous Formation, only to reappear in Sharon Springs beds. This is despite there being a higher number of skulls the upper Smoky Hill than any other Pteranodon bearing interval (Bennett 1994). This isn't an insurmountably complex distribution of course, but in terms of parsimony, Bennett's (1994) scheme must be seen as simpler and more congruent with stratigraphic data.

'Pteranodon complex', or Pteranodon simple?

Tying this all together, I hope it's clear that the 'Pteranodon complex' is quite a complicated issue, and one that will take some work to resolve one way or the other. I've had to skim over many of the details here, so be sure to read the papers cited herein if you'd like to read the full story. Many are available online.

It would perhaps be remiss to outline all this without giving my own take on this shake up of Pteranodon taxonomy. In my 2013 book I said I preferred Bennett's (1994) scheme and followed it accordingly and, revisiting this debate several years later has not changed my mind. I stress that I'm not 'against' the idea of more Pteranodon species, just that - in my opinion - the evidence points to Pteranodon containing longiceps and sternbergi, and that these species are each others closest relatives and might as well stay congeneric in Pteranodon. For reasons outlined above I find the stratigraphic arguments about separating these taxa unconvincing, and I don't think the morphological arguments are developed enough yet to overturn those for synonymy.

Concerning the specific taxa, the Dawndraco skull seems to be about right for a small 'male morph' P. sternbergi, and probably mostly seems atypical because of it's relatively completeness. Most large Pteranodon probably have those big rostra (you'll note that all my paintings of large Pteranodon, like that above and here, have this feature). What I've seen of its postcrania is extremely Pteranodon-like too, right down to its peculiar, highly characteristic tail (see Kellner 2010, p. 1074). I can appreciate why some folks might consider the maiseyi specimen a different taxon because of its seemingly unusual crest. However, the fact the leading crest edge is relatively complete but does not swell forwards means it is not particularly sternbergi-like, despite Kellner's (2010) suggestion that the maiseyi specimen is more closely related to sternbergi than anything else (Kellner 2010). Indeed, as preserved, the maiseyi crest meets the criteria of longiceps provided by Bennett (1994) as well as his predictions that it should have a huge crest base because of its large overall skull size. Moreover, the posterior and dorsal crest margins are broken: there is greater potential for the complete maiseyi crest to be more longiceps-like (longer, posteriorly directed) than sternbergi-like (tall, expanded forwards).

As for the large longiceps crest referred to Pteranodon sp., the specimen is not only (and obviously) very incomplete but the crest base is badly deformed, and I find it difficult to orientate the specimen against other skulls to determine the crest angle. There are suggestions that the crest base is too tall over the orbit to be longiceps (Kellner 2010) but, again, this region seems to change a lot with size and this specimen seems to have belonged to a big skull (judging by the orbit proportions): this needs to be considered carefully. The crest shape itself is generally longiceps-like, of course, and I suspect this specimen is just a big, mature version of this species.

So cheer up matey, you might not be a 'sp.' after all.
Of course, all this is subject to change should new ideas and data on Pteranodon be published in future. I should close by saying that the 'Pteranodon complex hypothesis' will soon become the 'Pteranodon complex debate': several authors are working on technical follow ups to Kellner's (2010) paper and describing relevant specimens that have bearing on this topic. This matter, then, is far from closed, and it's going to be interesting to see how it pans out. Now that we have a 'primer' article, if and when new papers are published, perhaps we'll cover them here.

This blog post on the 'Pteranodon complex' was made less complex because of support from Patreon

The paintings and words featured here are sponsored by a most excellent group of people, my Patreon backers. Supporting my blog from $1 a month helps me produce researched and detailed articles with paintings to accompany them, and in return you get access to bonus blog content: additional commentary, in-progress sneak-previews of paintings, high-resolution artwork, and even free prints. For this post, we'll be taking a look at one of the most interesting, and barely ever mentioned parts of Pteranodon anatomy. If you want to know what it is, head over to Patreon to get access!

References

  • Bennett, S. C. (1992). Sexual dimorphism of Pteranodon and other pterosaurs, with comments on cranial crests. Journal of Vertebrate Paleontology, 12(4), 422-434.
  • Bennett, S. C. (1993). The ontogeny of Pteranodon and other pterosaurs. Paleobiology, 19, 92-106.
  • Bennett, C. S. (1994). Taxonomy and systematics of the late Cretaceous pterosaur Pteranodon (Pterosauria, Pterodactyloidea). Occasional papers of the Natural History Museum. 169, 1-70
  • Bennett, S. C. (2001a). The osteology and functional morphology of the Late Cretaceous pterosaur Pteranodon Part I. General description of osteology. Palaeontographica Abteilung A, 1-112.
  • Bennett, S. C. (2001b). The Osteology and Functional Morphology of the Late Cretaceous Pterosaur Pteranodon Part II. Size and Functional Morphology. Palaeontographica Abteilung A, 113-153.
  • Carpenter, K. (2008). Vertebrate biostratigraphy of the Smoky Hill Chalk (Niobrara Formation) and the Sharon Springs Member (Pierre Shale). In High-Resolution Approaches in Stratigraphic Paleontology (pp. 421-437). Springer Netherlands.
  • Eaton, G. F. (1910). Osteology of Pteranodon. Connecticut Academy of Arts and Sciences, Memoirs.
  • Everhart, M. J. (2005). Oceans of Kansas. Indiana University Press.
  • Hargrave, J. E. (2007). Pteranodon (Reptilia: Pterosauria): stratigraphic distribution and taphonomy in the lower Pierre Shale Group (Campanian), western South Dakota and eastern Wyoming. Geological Society of America Special Papers, 427, 215-225.
  • Kellner, A. W. (2010). Comments on the Pteranodontidae (Pterosauria, Pterodactyloidea) with the description of two new species. Anais da Academia Brasileira de Ciências, 82(4), 1063-1084.
  • Tomkins, J. L., LeBas, N. R., Witton, M. P., Martill, D. M., & Humphries, S. (2010). Positive allometry and the prehistory of sexual selection. The American Naturalist, 176(2), 141-148.
  • Witton, M. P. (2013). Pterosaurs: natural history, evolution, anatomy. Princeton University Press.