A Turonian Pterosaur Turnover?

The early Cretaceous had a great diversity of pterosaurs. All four major groups of pterodactyloid – Archaeopterodactyloidea, Dsungaripteridae, Pteranodontoidea, and Azhdarchoidea – are present, and very diverse (Barrett et al., 2008). Even a few anurognathids were still present until at least the Aptian. By the end of the Cretaceous, this diversity had been reduced to only two clades: Pteranodontia and Azhdarchidae. What happened?

I looked through the lit and did a census of Cretaceous pterosaur taxa to get a sense of how diversity changed over time. I adopted a few arbitrary criteria for selecting what made the list, so things didn’t get too out of hand: the remains have to be diagnostic to one of the arbitrary taxonomic categories I chose; the remains have to be differentiable from other taxa in the same formation (for example, Santanadactylus was not counted as it cannot be satisfactorily distinguished from other contemporary anhanguerians like Anhanguera and Maaradactylus due to lack of overlap); the remains have to be dated narrower than Early/Late Cretaceous. Classifications follow my phylogenetic analysis (so e.g. Argentinadraco and Montanazhdarcho are considered azhdarchids), as well as those of Longrich et al. (2018) and Pêgas et al. (2019). I used this data to generate diversity curves for each stage of the Cretaceous.

pterosaurs absolute

The absolute diversity curves spike in the Aptian-Albian before crashing in the Cenomanian to the Turonian, then gradually increase to the end of the Maastrichtian. I would not read anything into this. The Aptian-Albian was when several major pterosaur lagerstatten were deposited, so the peak in diversity is certainly an artifact of preservational bias.

pterosaurs scaled

Scaling the diversity curves to show relative diversity of each taxonomic category tells a different story, however. Throughout the Early Cretaceous, the majority of pterosaur diversity is toothed pterosaurs, such as ctenochasmatoids, dsungaripterids, and lanceodontians. Toothless pterosaurs appear at the very beginning of the Cretaceous, and slowly increase in diversity up to the Cenomanian. Then, between the Cenomanian and the Coniacian, toothed pterosaurs (as well as non-azhdarchid azhdarchoids) disappear entirely. Nyctosaurids and pteranodontids appear in the Turonian-Coniacian. Meanwhile, azhdarchids steadily increase in diversity from their first appearance in the Aptian-Albian up to the end of the Cretaceous.

This turnover may be even sharper than it looks. No toothed pterosaurs in the dataset are dated strictly to the Turonian, only more broadly to the Cenomanian-Turonian (from the Chalk and Winton Formations). It’s possible, therefore, that these lineages went extinct either before or very shortly after the Cenomanian-Turonian boundary (Pentland et al., 2019). If this were the case, then the only pterosaur lineages that would make it to the Turonian are Azhdarchidae, Pteranodontia, and whatever Cretornis is. Why did so many pterosaurs go extinct at or shortly after the Cenomanian-Turonian boundary?

The Cenomanian-Turonian boundary is associated with an anoxic event. Preceded by changes in oceanic ecosystems through the Cenomanian, it ended up as the second worst extinction of the Cretaceous (Fischer et al., 2016). It heavily affected aquatic fauna, but had little to no impact on terrestrial animals (Eaton et al., 1997). Although the greatest effect seems to have been on small things, it’s likely that the extinctions at the base of the marine food chain had a ripple effect, impacting marine reptiles as well. The last ichthyosaurs disappear at the boundary (Bardet, 1992). Pliosaurs hung on for a little while after, but disappeared before the Coniacian (Albright et al., 2007). They may have been a dead clade walking: pliosaurs survived the event but could not recover, and the impact the event had led to their eventual extinction. The extinction of ichthyosaurs and pliosaurs left the seas open for mosasaurs to become apex predators; in fact it’s possible that competition from mosasaurs contributed to the final extinction of pliosaurs (Schumacher, 2011). I’ll also note that spinosaurids, who had been becoming steadily more aquatic over time (Ibrahim et al., 2020), also seem to disappear at the end of the Cenomanian.

I think a similar thing may have happened with pterosaurs. The toothed pterosaur groups that went extinct around the Cenomanian-Turonian boundary likely fed on aquatic prey such as fish and crustaceans: Anhangueria, Lonchodectidae, Mimodactylidae, and Targaryendraconia. Although they lived on the wing, they would have occupied a comparable tier on the food chain to ichthyosaurs, pliosaurs, and Spinosaurus. So these pterosaurs may have been impacted by the aquatic dieoffs in a similar way, and went extinct either at the beginning of the Turonian or not long afterward. Pteranodontids and nyctosaurids quickly replaced them, taking over fishing niches from the Turonian onward.

The disappearance of non-azhdarchid azhdarchoids is a more interesting question. They’re unlikely to have had as aquatic diets as the toothed pterosaurs of the time. Could the Cenomanian-Turonian event have had a greater effect on terrestrial fauna than we recognize, did these pterosaurs have greater aquatic components of their diet than we currently think, or is it just coincidence?  The dating of the Goio-Ere Formation is of crucial importance here; it’s been dated anywhere between the Aptian and the Campanian, and since it contains Caiuajara and Keresdrakon it could potentially be the youngest definite record of non-azhdarchid azhdarchoids. For the purposes of the dataset I adopted an Aptian-Albian date after Batezelli (2015). Whether more ambiguous taxa like Argentinadraco and Montanazhdarcho are azhdarchids or non-azhdarchid azhdarchoids is also highly important here.

Of course, there are still many questions that remain unanswered. The youngest chaoyangopterid is Microtuban, which unlike every other chaoyangopterid was found in marine sediments. Might it have fed on marine food, and thus been directly impacted by the event? The sudden appearance of pteranodontians in the Turonian-Coniacian produces a ghost lineage going all the way back to the beginning of the Cretaceous, and we have no idea what “branch-pteranodonts” were like or how they survived the event. Ctenochasmatoids also fed aquatically, but there are no confirmed Cenomanian specimens to my knowledge. Did they go extinct before the Cenomanian-Turonian boundary, or have we not found them yet? And given the nature of pterosaur preservation, how much of this apparent pattern is affected by preservational bias is unknown.

Before you mention Piksi: if that thing even is a pterosaur, I consider it not diagnostic enough to any of the taxonomic categories, so it was not included. Same for Navajodactylus.

References
Albright, L.B.; Gillette, D.D.; Titus, A.L. (2007). “Plesiosaurs from the Upper Cretaceous (Cenomanian-Turonian) tropic shale of southern Utah, part 1: new records of the pliosaur Brachauchenius lucasi“. Journal of Vertebrate Paleontology 27(1): 31-40.
Bardet, N. (1992). “Stratigraphic evidence for the extinction of the ichthyosaurs”. Terra Nova 4(6): 649-56.
Barrett, P.M.; Butler, R.J.; Edwards, N.P.; Milner, A.R. (2008). “Pterosaur distribution in time and space: an atlas”. Zitteliana B28: 61-107.
Batezelli, A. (2015). “Continental systems tracts of the Brazilian Cretaceous Bauru Basin and their relationship with the tectonic and climatic evolution of South America”. Basin Research 29(51): 1-25.
Eaton, J.G.; Kirkland, J.I.; Hutchison, J.H.; Denton, R.; O’Neill, R.C.; Parrish, J.M. (1997). “Nonmarine extinction across the Cenomanian-Turonian boundary, southwestern Utah, with a comparison to the Cretaceous-Tertiary extinction event”. GSA Bulletin 109(5): 560-7.
Fischer, V.; Bardet, N.; Benson, R.B.J.; Arkhangelsky, M.S.; Friedman, S. (2016). “Extinction of fish-shaped marine reptiles associated with reduced evolutionary rates and global environmental variability”. Nature Communications 7: 10825.
Ibrahim, N.; Maganuco, S.; Dal Sasso, C.; Fabbri, M.; Auditore, M.; Bindellini, G.; Martill, D.M.; Zouhri, S.; Mattearelli, D.A.; Unwin, D.M.; Wiemann, J.; Bonadonna, D.; Amane, A.; Jakubczak, J.; Joger, U.; Lauder, G.V.; Pierce, S.E. (2020). “Tail-propelled aquatic locomotion in a theropod dinosaur”. Nature 581: 67-70.
Longrich, N.R.; Martill, D.M.; Andres, B. (2018). “Late Maastrichtian pterosaurs from North Africa and mass extinction of Pterosauria at the Cretaceous-Paleogene boundary”. PLoS Biology 16(3): e2001663.
Pêgas, R.V.; Holgado, B.; Leal, M.E.C. (2019). “On Targaryendraco wiedenrothi gen. nov. (Pterodactyloidea, Pteranodontoidea, Lanceodontia) and recognition of a new cosmopolitan lineage of Cretaceous toothed pterodactyloids”. Historical Biology 1-15.
Pentland, A.H.; Poropat, S.F.; Tischler, T.R.; Sloan, T.; Elliott, R.A.; Elliott, H.A.; Elliott, J.A.; Elliott, D.A. (2019). “Ferrodraco lentoni gen. et sp. nov., a new ornithocheirid pterosaur from the Winton Formation (Cenomanian-lower Turonian) of Queensland, Australia”. Scientific Reports 9: 13454.
Schumacher, B.A. (2011). “A ‘woolgari-zone mosasaur’ (Squamata; Mosasauridae) from the Carlile Shale (Lower Middle Turonian) of central Kansas and the stratigraphic overlap of early mosasaurs and pliosaurid plesiosaurs”. Transactions of the Kansas Academy of Science 114(1-2):1-14.

The evolution of stem-bird vocalization

I wrote this essay for a course on evolution last year. I’ve made a few edits and reproduced it here.

Most tetrapods capable of vocalization, such as mammals, utilize vocal cords located within the larynx for this purpose (Senter, 2008). Birds, however, utilize an organ located at the base of the trachea: the syrinx. Unlike the larynx, which produces sound through the vibration of vocal folds, the syrinx produces sound by vibrating the walls of the trachea. The syrinx is capable of more complex vocalization than the larynx, including being able to function asymmetrically and produce two sounds at once (Naish, 2009, Clarke et al., 2016). Only found in modern birds, the syrinx is an unusual example of a novel organ in that it has completely functionally replaced the larynx as the primary vocal organ (Kingsley et al., 2018). The syrinx presumably evolved somewhere on the stem-bird lineage, which contains non-avian dinosaurs and pterosaurs. Understanding the origin of the avian syrinx can therefore have implications regarding the potential vocalization of stem-birds.

https://academy.allaboutbirds.org/wp-content/uploads/ARTICLE-SONG-1440X8002.png
Anatomy of the avian syrinx. Courtesy of All About Birds.

As birds use the syrinx for vocal communication, did stem-birds ever use laryngeal vocal cords? Senter (2008) suggested that, due to lack of fossil evidence of the syrinx or laryngeal vocal cords, stem-birds were likely mute. Modern tetrapods that lack both, such as New World vultures and many squamates, are limited to simple hissing and drumming sounds (Senter, 2008; pers. obs.). However, the potential presence of laryngeal vocal cords ancestrally in Ornithodira (the clade containing birds, non-avian dinosaurs, and pterosaurs) was not considered. The larynx leaves no osteological trace, making the presence or absence of vocal cords impossible to discern in the fossil record. Laryngeal vocal cords are present in the two extant outgroup taxa to the Aves total group, crocodylians and turtles, and laryngeal vocal cords have evolved many times independently in modern tetrapods (Senter, 2008; Chen and Weins, 2020). The presence of laryngeal involvement in vocalization has also been recorded in modern birds, albeit not through vibration of vocal folds (Naish, 2009). More modern hypotheses on syrinx evolution (e.g. Riede et al., 2019) assume the ancestral presence of vocal cords before the syrinx. If laryngeal vocal cords are an efficient enough sound production mechanism to evolve at least six times independently in tetrapods, it is not implausible that they may have also evolved in stem-birds.

hadroskulls
The internal nasal passageways of Corythosaurus, Lambeosaurus, and Parasaurolophus (Weishampel, 1981)

The resonating chambers of lambeosaurine hadrosaurs may have implications regarding the presence of a vocal organ. These dinosaurs have prominent bony head crests, through which the nasal passages arc and loop through. It is likely that these nasal passages were used in sound production (Weishampel, 1981). The dinosaur most famous for this is probably Parasaurolophus, and the potential sound produced by the crest of P. tubicen has been reconstructed using a computer simulation, resonating virtual air waves through the nasal passages to produce a deep trumpeting sound (Diegert and Williamson, 1998). Among other tetrapods, ruminant ungulates perhaps bear the most functionally similar structures. Rutting male saiga (Saiga tatarica) inflate their nasal passages to produce a loud nasal roar, amplifying sound made by the larynx (Frey et al., 2007). The extinct bovid Rusingoyrx atopocranion had expanded bony nasal passages looping through a cranial dome, convergently evolved with those of lambeosaurines. The nasal passages of Rusingoryx were likely used similarly to those of saiga, amplifying sound made by the larynx (O’Brien et al., 2016). By analogy with these ungulates, it is possible that the nasal passages of lambeosaurines also have evolved to amplify and resonate sound produced by a vocal organ. Thus, these nasal passages may serve as indirect evidence for the presence of a vocal organ in non-avian dinosaurs.

https://www.researchgate.net/profile/Ilya_Volodin/publication/5875434/figure/fig7/AS:267932441772047@1440891480654/Nose-extension-in-an-adult-male-saiga-during-the-rut-according-to-video-clip-single.png
Extension of the nose in a roaring male saiga (Frey et al., 2007). The crests of hadrosaurs (and if I may speculate, the expanded nasal regions of several other ornithischian dinosaurs) may have provided a similar function.

If non-avian dinosaurs and pterosaurs had vocal organs, what did they sound like? This is impossible to answer, as vocal organs never completely fossilize, but we can make a few inferences. By comparing the shape of the inner ear with those of birds and crocodilians, Gleich et al. (2005) inferred that many non-avian dinosaurs likely had a similarly well-developed sense of hearing. Although a few clades of ornithischian dinosaur may have secondarily lost external ear openings (Nassif et al., 2018), this does not necessarily preclude vocal ability, as certain living lepidosaurs that lack external ears produce sound anyways (Senter, 2008). Larger Mesozoic dinosaurs were more attuned to low-frequency sounds (e.g. Evans et al., 2009; Brusatte et al., 2016). Living large-bodied archosaurs, such as crocodylians and ratites, commonly utilize closed-mouth vocalization, in which sound is directed into an inflating resonating cavity, producing a lower-frequency sound than if the mouth was open. Examples include alligator bellows, ostrich booms, and owl hoots. These closed-mouth vocalizations may have also been prevalent in large stem-birds (Riede et al., 2016). This being said, open-mouth vocalizations were likely not absent in stem-birds; crocodylians and birds that frequently use closed-mouth vocalization also utilize open-mouth vocalization in different contexts (pers. obs.). Closed-mouth vocalizations are usually implemented in territorial or courtship displays (Riede et al., 2016), and are also present in a few mammal species, e.g. the nasal roar of the saiga and the inflatable throat sac of the siamang Symphalangus syndactylus (pers. obs.). However, most mammals adopt a different solution to produce loud, low-frequency sound; they evolve modifications of the vocal cords and vocal tract to produce deep “roaring” vocalizations (Frey and Gebler, 2010). It has been commonly reported in popular news media that non-avian dinosaurs did not roar (e.g. Orf, 2016). While it is unlikely that non-avian dinosaurs roared using the same mechanism as mammals, they may have produced functionally similar sounds regardless.

The exact timing of syrinx origin remains mysterious. Until recently it was thought that the syrinx could not fossilize, due to the lack of fossilized syrinxes older than the Pleistocene epoch. However, a good portion of the syrinx is biomineralized, similar to bone or shell, and this incorporation of hard minerals into tissue can increase fossilization potential. The mineralized portion of the syrinx has been identified in three genera of fossil anseriform birds: the Eocene Presbyornis, the Maastrichtian Vegavis (Clarke et al., 2016), and the Paleocene Conflicto (Tambussi et al., 2019). The fossilization potential of the syrinx raises the question of why no stem-birds have been found with fossilized syrinxes, even those close to crown-Aves. This may be due to the preservational bias in the fossil record, or it could indicate that the full syrinx was a late-arising feature in bird evolution (Clarke et al., 2017). In living birds, the syrinx remains unmineralized until after three months post-hatching, but can still produce sound before mineralization (Hogg, 1982). This raises the possibility that a sound-producing syrinx may have first appeared as an unmineralized structure, and thus would be difficult to fossilize.

https://www.researchgate.net/profile/Federico_Agnolin/publication/309091824/figure/fig2/AS:416868201451521@1476400532990/Comparison-of-the-Cretaceous-Vegavis-and-Eocene-Presbyornis-syrinxes-to-extant-avian.png
Morphology of the syrinx in several birds, including Vegavis and Presbyornis (Clarke et al., 2016)

A proxy for timing of syrinx evolution has been proposed in the ornithodiran skeleton. The syrinx is entirely surrounded by the clavicular air sac, one component of the ornithodiran air sac system (Wedel, 2009). Embryological observations indicate that the clavicular air sac forms relatively late in ontogeny, as an outgrowth of the lungs and two other air sacs (Locy and Larsell, 1916). This suggests that the clavicular air sac is a later development than the rest of the ornithodiran air sac system (Senter, 2008). The presence of an air sac can be inferred osteologically, as air sacs often invade the surrounding bone, leaving pits or depressions. This phenomenon is called skeletal pneumaticity. The clavicular air sac pneumatizes the humerus, furcula, sternum, and pectoral girdle (Wedel, 2009). Pneumatization by the clavicular air sac is present in Ornithothoraces, a clade including modern birds, but not in avialans basal to this clade (Senter, 2008). However, pneumatization consistent with the clavicular air sac is also present in pterosaurs, the theropod genera Aerosteon and Buitreraptor (Wedel, 2009) and the sauropod clade Saltasaurini (Cerda et al., 2012). This suggests that either the clavicular air sac evolved multiple times, or the clavicular air sac may have been present deeper in the bird stem lineage than Ornithothoraces.

Embryology demonstrates that the ornithodiran air sac system develops before pneumatization of bones (Locy and Larsell, 1916), and two clades of modern birds, loons and penguins, lack postcranial pneumaticity entirely but still bear a full air sac system. Postcranial pneumaticity is entirely absent in ornithischians and non-dinosaurian dinosauromorphs, and it is unlikely the entire air sac system evolved multiple times. Therefore, the air sac system may have evolved once, at the base of Ornithodira, and only grew to pneumatize the surrounding bones in certain taxa (Wedel, 2009).  The same could also apply to the clavicular air sac; it may have evolved before the origin of Ornithothoraces, extending the potential origin of the syrinx even earlier. However, it cannot be ruled out that the clavicular air sac indeed evolved multiple times; after all, it does appear to be a later development than the rest of the air sac system, and two of the clades that bear it, pterosaurs and Ornithothoraces, may have needed it for flight.  As well, vocalization with the syrinx is possible without the clavicular air sac necessarily being involved (e.g. Brackenbury, 1980), but it is unclear whether this reflects a possible ancestral condition or is a novel occurrence in some bird species. Ultimately, the exact timing of syrinx evolution remains unclear, and more data is needed to pinpoint its exact origin.

The evolutionary reason for the appearance of the syrinx is also a question worth looking into. Riede et al. (2019) carried out models and experiments to test efficiency of the syrinx relative to laryngeal vocal cords. Their results found that a sound source at the base of the neck is more acoustically efficient than one at the top of the throat, supporting the idea that the syrinx is a more efficient vocal organ than the larynx. One reason for this is that, with a sound source at the base of the throat, the vocal tract can be longer, producing a more resonant sound. Therefore, the syrinx may have evolved initially as a complement to the larynx, in response to selective pressure for efficient vocalization. The syrinx is most efficient relative to the larynx if the tracheal length is between 50 and 100 cm (Riede et al., 2019). The lineage of theropods that led to birds underwent sustained miniaturization over time (Lee et al., 2014), so the syrinx may have begun to take over the larynx’s duties at a certain body size due to its increased efficiency. The larynx may have then simply become obsolete as a vocal organ, and use of vocal cords was lost before the avian MRCA.

Summarizing all these pieces of evidence, we may speculate a tentative picture of vocal evolution in stem-birds. Ancestrally, stem-birds may have produced sound using laryngeal vocal cords, perhaps sharing an evolutionary origin with those present in crocodylians. Larger-bodied stem-birds may have produced closed-mouth booming or bellowing sounds, while some clades, notably lambeosaurine hadrosaurs, expanded on this setup to produce more complex sound. Selective pressure for efficient vocalization in theropods may have led to the evolution of a new organ, the syrinx, as a complement at the base of the throat. As the bird lineage continued to shrink in body size, the syrinx took over as the primary vocal organ, leaving birds with a truly unique method of vocalization.

References

Brackenbury, J. (1980). “Control of sound production in the syrinx of the fowl Gallus gallus“. Journal of Experimental Biology 85: 239-51.
Brusatte, S.L.; Averianov, A.; Sues, H.-D.; Muir, A.; Butler, I.B. (2016). “New tyrannosaur from the mid-Cretaceous of Uzbekistan clarifies evolution of giant body sizes and advances senses in tyrant dinosaurs”. Proceedings of the National Academy of Sciences 113(13): 3447-52.
Cerda, I.A.; Salgado, L.; Powell, J.E. (2012). “Extreme postcranial pneumaticity in sauropod dinosaurs from South America”. Palaontologische Zeitschrift 86(4): 441-9.
Chen, Z.; Wiens, J.J. (2020). “The origins of acoustic communication in vertebrates”. Nature Communications 11: 369.
Clarke, J.A.; Chatterjee, S.; Li, Z.; Riede, T.; Agnolin, F.; Goller, F.; Isasi, M.P.; Martinioni, D.R.; Mussel, F.J.; Novas, F.E. (2016). “Fossil evidence of the avian vocal organ from the Mesozoic”. Nature 538: 502-5.
Clarke, J.A.; Li, Z.; Riede, T.; Goller, F. (2017). “Insight into the volution of the Avian Vocal Organ, or Syrinx, from Enhanced-Contrast X-ray Computed Tomography and Fossil Data”. The FASEB Journal 31(1 supp.), abstract number 247.3.
Diegert, C.F.; Williamson, T.E. (1998). “A digital acoustic model of the lambeosaurine hadrosaur Parasaurolophus tubicen“. Journal of Vertebrate Paleontology 18(sup003): 38A.
Evans, D.C.; Ridgely, R.; Witmer, L.M. (2009). “Endocranial Anatomy of Lambeosaurine Hadrosaurids (Dinosauria: Ornithischia): A Sensorineural Perspective on Cranial Crest Function”. The Anatomical Record 292(9): 1315-37.
Frey, R.; Volodin, I.; Volodina, E. (2007). “A nose that roars: anatomical specializations and behavioural fetures of rutting male saiga”. Journal of Anatomy 211(6): 717-36.
Frey, R.; Gelber, A. (2010). “Mechanisms and evolution of roaring-like vocalization in mammals”. Handbook of Behavioral Neuroscience 19: 439-50.
Gleich, O.; Dooling, R.J.; Manley, G.A. (2005). “Audiogram, body mass, and basilar papilla length: correlations in birds and predictions for extinct archosaurs”. Naturwissenschaften 92(12): 595-8.
Hogg, D.A. (1982). “Ossification of the laryngeal, tracheal, and syringeal cartilages in the domestic fowl”. Journal of Anatomy 134(1): 57-71.
Kingsley, E.P.; Eliason, C.M.; Riede, T.; Li, Z.; Hiscock, T.W.; Farnsworth, M.; Thomson, S.L.; Goller, F.; Tabin, C.J.; Clarke, J.A. (2018). “Identity and novelty in the avian syrinx”. Proceedings of the National Academy of Sciences 115(41): 10209-17.
Lee, M.S.Y.; Cau, A.; Naish, D.; Dyke, G.J. (2014). “Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds”. Science 345(6916): 562-6.
Locy, W.A.; Larsell, O. (1916). “The embryology of the bird’s lung, based on observations of the domesticated fowl, part II”. American Journal of Anatomy 20: 1-44.
Naish, D. (2009). “Ridiculous super-elongate, coiled windpipes allow some birds to function like trombones – or is it violins?” Tetrapod Zoology. https://scienceblogs.com/tetrapodzoology/2009/04/29/elongate-avian-trachea
Nassif, J.P.; Witmer, L.M.; Ridgely, R.C. (2018). “Preliminary osteological evidence for secondary loss of a tympanic membrane in multiple clades of ornithischian dinosaurs”. 78th Annual Meeting of the Society of Vertebrate Paleontology, Albuquerque.
O’Brien, H.D.; Faith, J.T.; Jenkins, K.E.; Peppe, D.J.; Plummer, T.W.; Jacobs, Z.L.; Li, B.; Joannes-Bayou, R.; Price, G.; Feng, Y.; Tryon, C.A. (2016). “Unexpected Convergent Evolution of Nasal Domes between Pleistocene Bovids and Cretaceous Hadrosaur Dinosaurs”. Current Biology 26(4): 503-8.
Orf, D. (2016). “Dinosaurs Probably Didn’t Roar, But Some Definitely Quacked”. Popular Mechanics. https://www.popularmechanics.com/science/animals/a23362/dinosaurs-probably-didnt-roar-but-quacking-isnt-out-of-the-question/
Riede, T.; Eliason, C.M.; Miller, E.H.; Goller, F.; Clarke, J.A. (2016). “Coos, booms, and hoots: The evolution of closed-mouth vocal behavior in birds”. Evolution 70(8): 1734-46.
Riede, T.; Thomson, S.L.; Titze, I.R.; Goller, F. (2019). “The evolution of the syrinx: an acoustic theory”. PLoS Biology 17(2): e2006507.
Senter, P. (2008) “Voices of the past: a review of Paleozoic and Mesozoic animal sounds”. Historical Biology 20(4): 255-87.
Tambussi, C.P.; Degrange, F.J.; De Mendoza, R.S.; Sferco, E.; Santillan, S. (2019). “A stem anseriform from the early Palaeocene of Antarctica provides new key evidence in the early evolution of waterfowl”. Zoological Journal of the Linnean Society 186(3): 673-700.
Wedel, M.J. (2008). “Evidence for Bird-Like Air Sacs in Saurischian Dinosaurs”. Journal of Experimental Zoology 311A: 1-18.
Weishampel, D.B. (1981). “Acoustic Analyses of Potential Vocalization in Lambeosaurine Dinosaurs (Reptilia: Ornithischia)”. Paleobiology 7(2): 252-61.

On the paratype of Santanadactylus brasiliensis

Santanadactylus brasiliensis is one of the many Romualdo Formation pterosaurs, named by P.H. de Buisonje (1980). The holotype is University of Amsterdam M 4894, an associated humerus and scapulocoracoid. The humerus looks pretty standard for Anhangueria, and it likely belongs to this clade (in fact I would not be surprised if it is within Anhanguera sensu lato, but that’s a problem for another day).

de Buisonje referred another specimen, University of Amsterdam M 4895, as the paratype. This specimen consists of two flattened, elongate cervical vertebrae. Although not associated with the holotype, they were found in the same chalk nodules. Since the original publication, the assignment of these cervicals to the same taxon as the holotype has been questioned (e.g. Bennett 1989, Kellner 1995, Leal et al. 2018), with the latter two publications considering the specimen an azhdarchoid.

To test the affinities of the paratype (hereafter the Amsterdam specimen), I coded it into my azhdarchoid phylogenetic analysis. I also added the holotype of Santanadactylus brasilensis, although the fragmentary nature of the specimen and the dataset’s non-focus on anhanguerians makes it difficult to place.

amsterdam
The results. Cretornis insisted on being the sister taxon to Eopteranodon for reasons I don’t quite understand.

The Amsterdam specimen ended up as the outgroup to the Chaoyangopteridae + Azhdarchidae clade (I refuse to call it Neopterodactyloidea). Could this represent an azhdarchoid outside any of the four major groups? The specimen shows an interesting mix of features present in both tapejarids (e.g. lateral pneumatic foraminae) and chaoyangopterids (e.g. sunken neural arch, low neural spine). It may be a transitional form between the plesiomorphic state and the derived “elongate” form epitomized in azhdarchids.

Of course, it is not implausible that the Amsterdam specimen is an aberrant member of another clade. Forcing it into Chaoyangopteridae takes 3.999 to 7.208 extra steps (depending on wheteher Cretornis or Microtuban are included), where it ends up as the outgroup to everything else. It only takes 2.206 extra steps to force it into Tapejaridae, although it ends up within Sinopterus, which I’m confident is artifactual due to there being no clear synapomorphies. So although other alternatives are not far off, a position outside the chaoyangopterid-azhdarchid clade seems to be the best-supported preliminarily.

Overall, the pterosaur fauna of the Crato and Romualdo Formations are fairly similar, with thalassodromids, tapejarines, and anhanguerians present in both. Definite chaoyangopterids are only present in the Crato Formation (represented by Lacusovagus and the cervical series UFC 721), while the Amsterdam specimen hails from the overlying Romualdo. If the Amsterdam specimen is indeed its own lineage, this implies the presence of a ghost lineage – a fifth major azhdarchoid lineage – since it postdates the chaoyangopterid-azhdarchid split. But more material and study is needed before we can say anything definite.

While we’re on the topic of Santanadactylus, historically it has been a mess. Many other remains have been referred to Santanadactylus, but in light of Romualdo’s pterosaur diversity, little of it has any right to be so. S. spixii, based on a partial wing, is generally agreed to not be related to Santanadactylus now (my analysis tentatively recovers it as a dsungaripterid, but support is not high, and I haven’t been able to access the full description so the codings are incomplete). Although other material has been referred to Santanadactylus brasiliensis, due to lack of association, overlap, or diagnosability, the taxon should be restricted to the holotype (Kellner and Tomida 2000), and the relationships between it, S. pricei, and the other Romualdo anhanguerians is still murky. But that’s another issue for another day.

Kudos to Dean Schnabel for bringing this specimen to my attention.

References

Bennett, S.C. (1989). “A pteranodontid pterosaur from the Early Cretaceous of Peru, with comments on the relationships of Cretaceous pterosaurs”. Journal of Paleontology 63: 669-77.
de Buisonje, P.H. (1980). “Santanadactylus brasilensis nov. gen., nov. sp., a long-necked, large pterosaurier from the Aptian of Brasil”. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen B 83(2): 145-72.
Kellner, A.W.A. (1995). “The relationships of the Tapejaridae (Pterodactyloidea) with comments on pterosaur phylogeny”. In: Sun, A.; Wang, Y. (eds). Sixth Symposium on Mesozoic Terrestrial Ecosystems and Biota, Short Papers. China Ocean Press, Beijing: 73-7.
Kellner, A.W.A.; Tomida, Y. (2000). “Description of a new species of Anhangueridae (Pterodactylidea) with comments on the pterosaur fauna from the Santana Formation (Aptian-Albian), northeastern BRazil”. National Science Museum Monographs 17.
Leal, M.E.C.; Pegas, R.V.; Bonde, N.; Kellner, A.W.A. (2018). “Cervical vertebrae of an enigmatic pterosaur from the Crato Formation (Lower Cretaceous, Araripe Basin, NE Brazil). From Hone, D.W.E.; Witton, M.P.; Martill, D.M. (eds). New Perspectives on Pterosaur Palaeobiology. Geological Society, London, Special Publications, 455: 195-208.

 

The paleocolor list

I apologize for the lack of updates. As you may or may not know, I presented my azhdarchoid phylogeny at the 1st Palaeontological Virtual Conference, and I’ve been trying to get something done with it elsewhere (fingers crossed!)

And now for something completely different: paleocolor! For only a tiny fraction of fossil taxa do scientists and paleoartists have any indication of color, be it through preserved melanosomes, preserved patterns, genetic inference, or even cave art. This can certainly be useful in reconstructing the past and understanding the evolution of color. However, information on paleocolor can be pretty scattered; Albertonykus’ In Living Color (Maybe) and megabass22’s Colouration in Mesozoic creatures are good starting points, but there isn’t one big handy list of paleocolor available.

So I made one.

This list summarizes every indication of prehistoric color I’m aware of, with relevant citations. I’m nowhere near a competent enough visual artist to attempt visualizing each of these (note to self: add images in the future, that might be useful). As well, some lines of evidence (e.g. cave art) may not close the case when it comes to color for certain taxa. Nonetheless, I hope this list can be useful. Please let me know if there’s anything that I missed!

The “molecular paleontology” list

And might as well publicize this list too while I’m at it.

Preserved biomolecules in extinct taxa, such as DNA and proteins, are quite a fascinating topic. They allow scientists to place extinct taxa in molecular phylogenies, understand evolution of certain genes, and quantify prehistoric population dynamics. As well, hypothetically, sequences derived from ancient nuclear DNA can be implemented in the process of de-extinction. Unfortunately, there doesn’t seem to be a handy list of taxa with recovered ancient DNA yet. GenBank has a list of extinct taxa in its database, but of course not every reported sequence is accounted for here.

So a few months ago I made another list. It’s a hopefully semi-comprehensive compilation of all reports of “old” DNA, proteins, etc. “Old” being from extinct taxa and/or older than 4,600 years. The list also includes failed attempts at biomolecule extraction, discredited reports, and even hoaxes. Please let me know of anything I missed!

Fuzzy anurognathids!

anurognathids
Distribution of preserved pycnofibres in NJU-57003 (left) and CAGS-Z070 (right). From Yang et al. 2019

As you probably know, a recent paper reports complex branched filaments in two anurognathid specimens (Yang et al. 2019). While this hasn’t been the first time branched pycnofibres have been reported (Czerkas and Ji 2002, Cincotta et al. 2016), this is the most credible case yet. Since then I’ve seen a lot of discussion regarding this. Some of it has been kinda confusing. And some of the reports I’ve seen (particularly “pterosaurs have feathers now”) are potentially misleading. So let’s clear things up.

What is a feather?

A lot of the discussion and confusion I’ve seen regards whether pterosaurs have feathers now. I think a lot of this is because there hasn’t been a consistent definition of what a feather is – and therefore, whether the pycnofibres in these anurognathids qualify. Some have said that they do, because these pycnofibres branch. Some say they do, because they’re homologous to modern bird feathers. Some say they don’t, because true, complex feathers are only found in coelurosaurs. So what gives? I think a lot of it goes down to people not agreeing on what a feather is.

In this post, I’ll use the following definitions

  • Feather: filamentous integument homologous with those in modern birds, of any complexity
  • Pycnofibre: the filamentous integument of pterosaurs
  • Monofilament: filamentous integument that does not branch
  • Branching feather: well, a feather that branches
  • Protofeather: a feather without a rhachis. This is admittedly an arbitrary definition, but it is done to distinguish earlier feather types from those found in modern birds
  • Advanced feather: a feather with a rhachis. Again arbitrary.

Fuzz in Anurognathids

Previously, the only confirmed pycnofibre morphology in anurognathids was monofilamentous (present in Jeholopterus). These two specimens show a wide variety of pycnofibres. There are four types of pycnofibre: a monofilament, similar to those previously described in pterosaurs; a filament that branches distally, similar to the “paintbrush-like” feathers of scansoriopterygids; a monofilament with small projections about halfway through, similar to the sensory bristles of some modern birds; and filaments that share a base, similar to the “stage 2” feathers of coelurosaurs. The bristle-like pycnofibres are present around the mouth, presumably acting like nightjar rictal bristles (furthering the analogy between these two clades), while the “stage 2” pycnofibres cover the wings (yep – there are anurognathids even fuzzier than Jeholopterus!). They do not have filaments that look just like those in modern birds – the pycnofibres do not have distinct rhachises, no barbules, and all pycnofibres appear to have been still flexible. But the pycnofibres do resemble protofeathers of dinosaurs – to paraphrase Steve Brusatte, if you saw them on a dinosaur, you would call them feathers.

anurognathid filament types
The filaments seen in CAGS-Z070: monofilaments (1), paintbrush-like pycnofibres (2), bristle-like pycnofibres (3), and Stage 2-like pycnofibres (4). From D’Alba 2019.

Are pycnofibres feathers?

Are pycnofibres homologous to feathers in dinosaurs? Did the ancestor of dinosaurs and pterosaurs have filamentous integument? Are pycnofibres feathers sensu this post? These are all the same question phrased in different ways. So far there have been three major ancestral state reconstructions regarding filamentous integument in ornithodirans. Barrett et al. (2015) concluded that the ancestor of ornithodirans, and filamentous integument evolved independently in pterosaurs, ornithischians, and theropods. However, they assume a priori that pycnofibres are not homologous to dinosaur feathers, and coded pterosaurs as “scaly” – which is a risky assumption. Indeed, when the ASR was ran with pycnofibres coded as homologous to dinosaur feathers, ancestrally feathered ornithodirans becomes the most likely possibility. Holtz (2018) also tested this, and found a similar conclusion – coding pycnofibres as homologous to dinosaur feathers makes ancestrally feathered ornithodirans likely, and coding pycnofibres as not homologous makes ancestrally feathered ornithodirans less likely. Clearly, the probability of ancestrally filamentous ornithodirans (and dinosaurs, for that matter) rests heavily on pycnofibres.

Yang et al. argue that pycnofibres are homologous to feathers, and code them so, finding ancestrally feathered ornithodirans most likely. Structurally and functionally, the two types of integument are pretty much identical. There are also no basal ornithodirans that preserve scales (which would indicate they evolved separately) – but then again, there are almost no basal ornithodirans with preserved integument at all. It should be noted that the most basal major ornithischian group – Heterodontosauridae – and potentially one of the most basal major pterosaur groups – Anurognathidae – both are fuzzy. There’s some stuff in the works that could indirectly indicate one way or the other in saurischians, but as it currently stands there just isn’t any well-preserved archosaur integument from before the early Jurassic.

That being said, if these filaments are not homologous, there are multiple instances of filament gain and filament loss within ornithodirans. If they are homologous, then there are still multiple instances of filament loss, but only one instance of gain. Multiple filament losses happen either way – we can be pretty confident the mechanism to do that existed, and happened multiple times regardless. It is the multiple filaments gains that lack direct evidence, so it becomes the less parsimonious option. And per Occam’s razor, the simplest hypothesis should be taken as the null.

TL:DR; if you say “feathers” are “all bird-line fluff”, then pycnofibres are probably feathers. They look like branched protofeathers, but don’t resemble the feathers of modern birds.

Are the branched pycnofibres the same thing as branched dinosaur feathers?

Yang et al. also conclude that the branching pycnofibres are homologous to the branching feathers of dinosaurs, and that branching feathers were also present at the base of Ornithodira. As mentioned earlier, these anurognathids are not the first report of branching pycnofibres. Pterorhynchus was reported to have pycnofibres that resemble ostrich feathers, rhachis and all (Czerkas and Ji 2002). The only copy I can find doesn’t have figures, and rumor has it the specimen is incredibly difficult to access (Adam Fitch, pers. comm.), so this claim cannot be independently verified. The lead author was also a BANDit (a proponent that birds did not evolve from dinosaurs), and the paper implies that pterosaurs and birds share an ancestor not shared by dinosaurs, so I would take this claim with a grain of salt. An undescribed tapejarid (which looks a lot like Tupandactylus) shows a mix of monofilaments and a type of branching pycnofibre (Cincotta et al. 2016). The latter resembles Stage 3 feathers, but from what I can see no distinct rhachis is visible (I like to call this state “stage 2.5”). The new anurognathids are currently the most credible instance of branching pycnofibres, though.

The branched pycnofibres in anurognathids are remarkably structurally similar to branched feathers in coelurosaurs, indeed, but I would caution that this may be a premature observation. If this were the case, you would expect to also see these filaments in ornithischians – but this isn’t the case. Tianyulong only shows monofilaments. Kulindadromeus has complex feathers, but they look nothing like those in anurognathids and coelurosaurs. Kulindadromeus has a feather type that appears to be hairlike filaments extending from a base plate, as well as a unique type of bundled ribbon-like filament. I’m not sure if it’s the best of ideas to code them identically to the branching filaments in anurognathids and coelurosaurs – I classify them separately in my feather type infographic for this reason. On the other hand, though, given the paucity of integument preserved in basal ornithodirans, it’s still entirely possible that branched filaments were present back then and just not preserved in Tianyulong for whatever reason. Who knows. Only further finds will be able to clear this up (or, as is almost always the case in paleontology, muddy things further).

filament comparison
Comparison between branched filaments seen in aurognathids (left), Kulindadromeus (center), and coelurosaurs (right)

This would not be the first time that something happened almost identically in numerous independent groups of ornithodirans. Toothless beaks evolved a minimum of 7 times in Ornithodira – and likely many more – each time with the anterior beak losing teeth first and moving posteriorly. As well, reticulate scales appeared on the majority of the body multiple times in dinosaurs independently. Presumably, the same genetic mechanism was present somewhere at the base of Ornithodira, and was expressed multiple times in each of these taxa. It wouldn’t be far out of the question that something similar happened with the filaments in pterosaurs and coelurosaurs.

As well, the identity of the “type 4” filaments has been questioned. They only appear on where the wing membranes should be, but aren’t preserved. David Unwin and Chris Bennett have both expressed skepticism that these structures are filaments, with the former suggesting that they could be degraded actinofibrils. A bit of uropatagium is preserved in one of the anurognathids and shows actinofibrils distinct from the branching filaments, but Unwin’s observation would be a striking coincidence. Only further studies will be able to tell us what the true nature of these structures are.

TL:DR; I don’t think the branching fuzz in pterosaurs and coelurosaurs are the same thing, but until further evidence comes up, it’s still in the air.

In Summary

Yang et al. 2019 is an important paper for multiple reasons. It’s the first report of branching pycnofibres in peer-reviewed literature, it adds further evidence to support the presence of feathers at the base of Ornithodira, it shows that some pterosaurs had pycnofibres covering the entire wings (probably), and it’s the first paper to determine the color of anurognathids (at least one was reddish!). It’s an exciting publication, and I look forward to any future studies on pterosaur fuzz.

As an aside, in life, these anurognathids would have probably been very cute.

red_baron_by_hyrotrioskjan_dcumbwa-pre
Red Baron” by Joschua Knüppe

References

Barrett, P.A.; Evans, D.C.; Campione, N.E. (2015). “Evolution of dinosaur epidemeral structures”. Biology Letters 11(6).
Cincotta, A.; Godefroit, P.; Yans, J. (2016). “Study of preserved tissues in a tapejarid pterosaur”. XIV Annual Meeting of the European Association of Vertebrate Palaeontologists, Haarlem.
Czerkas, S.A.; Ji, Q. (2002). “A new rhamphorhynchoid with a headcrest and complex integumentary structures.” In: Czerkas, S.J. (ed.). Feathered Dinosaurs and the Origin of Flight. The Dinosaur Museum: Blanding, 15-41.
D’Alba, L. (2019). “Pterosaur plumage”. Nature Ecology & Evolution 3: 12-3.
Godefroit, P.; Sinitsa, S.M.; Dhouailly, D.; Bolotsky, Y.L.; Sizov, A.V.; McNamara, M.E.; Benton, M.J.; Spagna, P. (2014). “A Jurassic ornithischian dinosaur from Siberia with both feathers and scales”. Science 345(6195): 451-5.
Holtz, T.R. (2018). “‘Integumentary Status: It’s Complicated’: Phylogenetic, Sedimentary, and Biological Impediments to Resolving the Ancestral Integument of Mesozoic Dinosauria”. 78th Annual Meeting of the Society of Vertbrate Paleontology, Albuquerque.
Yang, Z.; Jiang, B.; McNamara, M.E.; Kearns, S.L.; Pittman, M.; Kaye, T.G.; Orr, P.J.; Xu, X.; Benton, M.J. (2019). “Pterosaur integumentary structures with complex feather-like branching”. Nature Ecology & Evolution 3: 24-30.

The Romanian Azhdarchid Mandible: The Missing Piece?

Vremir et al. recently published a paper on a new partial mandible of a large (+8 m wingspan) Azhdarchoid pterosaur from Romania. This specimen was collected in 1984 and is… not particularly well-preserved, but it is informative enough to give us an idea of its relations. The authors tentatively proposed a position as a primitive Azhdarchid, due to a combination of characters present in both Azhdarchids and Tapejarids.

LPB R.2347, the giant Hateg mandible being discussed here. From Vremir et al. 2018.

This new specimen (hereafter the Hateg mandible) is a lot like Bakonydraco. The mandible gently downturns anteriorly and has a deep, wide keel, unlike the thin crests of Tapejarids or the narrow keels of Tupuxuara or other Azhdarchids. The posterior symphysis has raised margins and a noticeable sulcus, and what may be a sulcus on the ventral surface. It even has medullary-type bone in the mandible too!

https://upload.wikimedia.org/wikipedia/commons/a/aa/Bakonydraco.jpg
The holotype mandible of Bakonydraco galaczi. It also has all those traits. From Osi et al. 2005.

The Hateg mandible doesn’t overlap with any of the Hatzegopteryx material, and Vremir et al. take the conservative stance of not referring this bone to the taxon. I still suspect there’s a link between the two anyways. How? The bone interior. Vremir et al. note they both have comparable internal bone, with relatively thick bone walls (up to 4-5 mm) and a spongy internal texture. Relatively thick bone walls are also seen in fossils of Hatzegopteryx, including the referred cervical EME 315. It could be argued this is an artifact of size, but the vertebra of the giant Arambourgiania has thinner bone walls (2.6 mm) and different internal structure (Naish and Witton 2017). The interior bone texture, likewise, is only known in other giant Romanian Azhdarchids – namely, EME 315 and the type material of Hatzegopteryx. Barring further material, it seems the Hateg mandible has as much right to be Hatzegopteryx as the cervical does.

I updated the Azhdarchoid matrix, adding the Hateg mandible and updating the codings of Bakonydraco. Earlier, the codings had followed the precedent of Andres et al. 2014, and thus recovered Bakonydraco as a Tapejarid. In light of the Hateg mandible, however, I felt it prudent to recode this specimen, with a different interpretation of multiple characters (e.g. de-coding the ventral keel as homologous with Tapejarid crests). I should note that the Bakonydraco OTU as is includes the (clearly Azhdarchid) rostrum fragment referred to it by Osi et al. 2011. The unassociated Azhdarchid cervicals described by Osi et al. 2005 seem to come in two different morphotypes (which may or may not relate to position in the neck), so I didn’t add them to the OTU. In any case, in light of the most probably Azhdarchid nature of the Hateg mandible, it seems Bakonydraco might just be a very weird Azhdarchid after all – there is no other evidence for a non-Azhdarchid in Santonian Hungary.

I ran the analysis two times, one with the Hateg mandible and Hatzegopteryx constrained and one without, to little difference. Hatzegopteryx is part of a clade of “short-necked” Azhdarchids that also includes the short-necked Pui Azhdarchid and the Canadian TMP 92.83. The Hateg mandible is part of this clade even without constraints due to sharing bone wall thickness and internal bone texture with Hatzegopteryx, and it drags Bakonydraco into the clade as well. This could be a more reasonable result than it might appear at first – there are Azhdarchid cervicals from the Csehbanya Formation that resemble other members of this clade (MTM Gyn/450; Osi et al. 2005). Perhaps this morphotype belongs to Bakonydraco. It is perhaps also noteworthy that both Hatzegopteryx and Bakonydraco have very wide skulls at the jaw joint.

Short necked clade.png
Results of the analysis. Several OTUs outside the short-necked clade are not shown here so as to not give too much away.

tl:dr; the new Romanian mandible can probably be tentatively assumed to be Hatzegopteryx. Bakonydraco might be an Azhdarchid after all, and the two might be related.

Hatzegopteryx skull.png
Reconstruction of the skull of Hatzegopteryx. Scale bars 25 cm; top scaled to LPB R.2357, bottom scaled to the holotype occiput.

And to address the elephant in the room: I’m not sure if this mandible fragment was part of the giant Romanian Azhdarchid material being hyped up as “Dracula”, which is allegedly different from and bigger than Hatzegopteryx thambema. Until more material is published I would take this with a grain of salt.

References
Naish, D.; Witton, M.P. (2017). “Neck biomechanics indicate that giant Transylvanian azhdarchid pterosaurs were short-necked arch predators”. PeerJ 5: e2908.
Osi, A.; Weishampel, D.B.; Jianu, C.M. (2005). “First evidence of azhdarchid pterosaurs from the Late Cretaceous of Hungary”. Acta Palaoentoloigca Polonica 50(4): 777-787.
Osi, A.; Buffetaut, E.; Prondvai, E. (2011). “New pterosaurian remains from the Late Cretaceous (Santonian) of Hungary (Iharkut, Csehbayna Formation)”. Cretaceous Research 32(4): 456-463.
Vremir, M.; Dyke, G.; Csiki-Sava, Z.; Grigorescu, D.; Buffetaut, E. (2018). “Partial mandible of a giant pterosaur from the uppermost Cretaceous (Maastrichtian) of the Haţeg Basin, Romania”. Lethaia

Lonchodectid Lifestyle Logic

Ah, Lonchodectids. One of the most obscure and little-known pterosaur clades. The clade could include Lonchodectes, Lonchodraco , “Palaeornis” cliftii, Prejanopterus, Serradraco, Unwindia, Yixianopterus, the unnamed specimen BEXHM 2015.18, and an unpublished specimen nicknamed “Chang-e”. Most of these, except Yixianopterus and allegedly Chang-e, are known from pretty fragmentary remains; and of those two, the latter is unpublished and the former is only preliminarily described and I can’t find it. Unfortunately, my main source of information on it is going to be a photograph on *shudder* Pterosaur Heresies Update: Thanks to Jorge Bar for getting me a copy!

The phylogenetic position of Lonchodectidae is also somewhat murky. They’d been previously proposed as Ctenochasmatoids (Unwin 2003), Azhdarchoids (Unwin et al. 2008), miscellaneous Lophocratians (Witton 2013), and Pteranodontians (Andres et al. 2014). For the record, I’ve preliminarily found them in the same grade as Istiodactylidae, but that isn’t the main topic of this post. No, here I’ll discuss their lifestyle. Despite the mystery of this group, a preliminary proposed lifestyle has been proposed – long-necked terrestrial generalists (Unwin et al. 2008, Witton 2013). But does this hold up?

https://upload.wikimedia.org/wikipedia/commons/d/da/Serradraco_sagittirostris_Kellner_and_Rodriguez_2013.jpg
The only known specimen of Serradraco sagittirostris, showing a typical Lonchodectid dentition. From Rodrigues & Kellner 2013.

The first step would be looking at Lonchodectid teeth. Lonchodectid teeth are distinctive – they’re well-spaced, “raised” from the jawline, short, laterally compressed, and recurved. It’s hard to tell what they were doing with them. They come across to me as potentially being the teeth of piscivores or carnivores, which would be a fairly standard Ornithocheiromorph diet. They remind me of the teeth of the gharial. The snout tip of Lonchodraco giganteus at least almost seems like a subtle version of the “fish grab” anterior snouts of many Anhanguerians, and the anteriorly-confined teeth of Unwindia may (or may not) have been something similar.

https://upload.wikimedia.org/wikipedia/commons/b/b1/Gavialis_gangeticus%2C_ZOO_Praha_045.jpg
The gharial, Gavialis gangeticus. Its dentition resembles those of Lonchodectids in being small, evenly spaced, and recurved, set in a long, narrow snout. Original by Matěj Baťha on Wikimedia Commons.

The only Lonchodectid postcranial remains are the skeletons of Yixianopterus and Chang-e, the fragmentary postcrania of Lonchodraco and BEXHM 2015.18, the single humerus that is “Palaeornis” cliftii, and postcrania referred to Lonchodectes. BEXHM 2015.18 and the postcrania of Lonchodraco are really fragmentary and relatively uninformative as to lifestyle (Bowerbank 1846, Rigal et al. 2018).

The referred Lonchodectes postcrania catches my eye most. The most interesting and perhaps most phylogenetically informative specimen is a humerus, CAMSM B54081, figured by Unwin 2003. Cervical vertebrae and other limb elements have also been referred to it, most of which have apparently not been figured (but see Unwin 2001, Witton 2013 for exceptions). This referral apparently began in the 19th century, and was followed by Unwin 2001, Unwin 2003, and Witton et al. 2009 without comment.

Now I have to ask, on what grounds should these be referred to Lonchodectes in particular? Every species ever referred to it (excepting L. (now Lonchodraco) giganteus, which has really fragmentary postcrania and no humerus) is based on a fragment of rostrum or mandible (Rodrigues and Kellner 2013). Lonchodectes compressirostris – the only one remaining – isn’t even known from a snout tip like so many other Ornithocheiromorphs! There’s no real reason why any of the postcrania should belong to Lonchodectes in particular, especially knowing the Chalk Formation (L. compressirostris’ locality, and from what I can tell a completely different formation from the postcrania) and Cambridge Greensand are multitaxic. From what I can see, the postcranial remains referred to Lonchodectes are very similar to those of Azhdarchoids. And Azhdarchoids are certainly known from early Cretaceous England. Indeed, in 2012 CAMSM B54081 was re-referred to Ornithostoma and interpreted as belonging to an Azhdarchoid (Averianov 2012) [I have my doubts about this referral too, but that’s going off-topic].

https://bdj.pensoft.net/showimg.php?filename=oo_22082.jpg
This is everything that can reasonably be said to belong to Lonchodectes. From Rodrigues and Kellner 2013

And with this, it’s probable “Palaeornis” cliftii is not a Lonchodectid either. The only fossil – a humerus – looks very much like those of Azhdarchoids too. It doesn’t have a solid phylogenetic position in my Azhdarchoid analysis, but appears to be a non-Azhdarchid Azhdarchoid. As does CAMSM B54081, which I coded in on its own.

Perhaps the most fabled Lonchodectid is “Chang-e”. It was presented at SVPCA 2008, and sounded like a goldmine of Lonchodectid information. A well-preserved skeleton, with “copious phylogenetic data” with long hindlimbs and a relatively short wing finger that placed Lonchodectids as either the sister taxon to or within Azhdarchoidea (Unwin et al. 2008). How exciting! Unfortunately, it seems to be a composite, and the manuscript is apparently dead now. Bummer if this is true.

Yixianopterus.PNG
JZMP-V-12, the holotype and only known specimen of Yixianopterus jingangshanensis. From Lu et al. 2006

What about Yixianopterus? Apart from the skull (which was apparently forged before the fossil was acquired by the JZMP), it’s one of the (if not the) most complete Lonchodectid fossils thus far, and the anterior jaws look pretty similar to those of Unwindia. If Yixianopterus is a Lonchodectid, it offers perhaps the best information about Lonchodectid postcrania thus far. The limb proportions are interesting. They don’t match up with those of Azhdarchoids. The short metacarpal IV relative to ulna, size of the wing finger in general, and wing phalanges 2/1 ratio remind me more of those of Istiodactylids or Anhanguerids. Both are thought to have been long-distance fliers in primarily terrestrial and marine settings respectively (Witton 2013). Perhaps Yixianopterus had similar flight habits.

And then there’s Prejanopterus. It’s hard to tell what’s up with it. It’s small and has a long, really narrow, slightly upturned snout, with more teeth than Lonchodectids typically seem to have – if it is a Lonchodectid at all. It’s hard to know what it was doing, but it was probably doing something relatively “unorthodox”. I don’t want to say fishing because that feels like a cop-out, but that might be a reasonable preliminary guess.

What image forms out of this? Perhaps Lonchodectids were aerial piscivores like Anhanguerids – their gharial-like jaws hint at a potential fishing lifestyle, and their limb proportions match up with a life mostly on the wing. Of course, given the general quality of Lonchodectid remains, more fossils are probably needed before anything concrete could be said.

References
Andres, B.; Clark, J.; Xu, X. (2014). “The Earliest Pterodactyloid and the Origin of the Group”. Current Biology 24: 1011-6.
Averianov, A.O. (2012). “Ornithostoma sedgwicki – valid taxon of azhdarchoid pterosaurs”. Proceedings of the Zoological Institute RAS, 316(1): 40-49.
Bowerbank, J.S. (1846). “On a new species of pterodactyl found in the Upper Chalk of Kent (Pterodactylus giganteus)”. Quarterly Journal of the Geological Society of London, 2: 7-9.
Lu, J.; Ji, S.; Yuan, C.; Gao, Y.; Sun, Z.; Ji, Q. (2006). “New pterodactyloid pterosaur from the Lower Cretaceous of Western Liaoning”. In: Lu, J.; Kobayashi, Y.; Huang, D.; Lee, Y. (eds). Papers from the 2005 Heyuan International Dinosaur Symposium. Geological Publishing House: 195-203.
Rigal, S.; Martill, D.M.; Sweetman, S.C. (2018). “A new pterosaur specimen from the Upper Tunbridge Wells Sand Formation (Cretaceous, Valanginian) of southern England and a review of Lonchodectes sagittirostris (Owen 1874).” In: Hone, D.W.E.; Witton, M.P.; Martill, D.M. (eds). New Perspectives on Pterosaur Palaeobiology. Geological Society of London Special Publications, 455.
Unwin, D.M. (2001). “An overview of the pterosaur assemblage from the Cambridge Greensand (Cretaceous) of Eastern England”. Mitt. Mus. Nat.kd. Berl., Geowiss. 4: 189-221.
Unwin, D.M. (2003). “On the phylogeny and evolutionary history of pterosaurs”. In: Buffetaut, E.; Mazin, J-M. (eds). Evolution and Palaeobiology of Pterosaurs. Geological Society of London Special Publications, 217: 139-190.
Rodrigues, T.; Kellner, A.W.A. (2013). “Taxonomic review of the Ornithocheirus complex (Pterosauria) from the Cretaceous of England”. Zookeys, 308: 1-112.
Unwin, D.M.; Wang, X.; Meng, X. (2008). “How the Moon Goddess, Chang-e, helped us to understand pterosaur evolutionary history” SVPCA 2008.
Witton, M.P.; Martill, D.M.; Green, M. (2009). “On pterodactyloid diversity in the British Wealden (Lower Cretaceous) and a reappraisal of “Palaeornis” cliftii Mantell, 1844″. Cretaceous Research, 30: 676-686.
Witton, M.P. (2013). Pterosaurs: Natural History, Evolution, Anatomy. Princeton University Press.

Update: Kudos to Renato Filipe Vidal Santos for giving this a read-through and catching a few things.

On Caupedactylus and Tupuxuara deliradamus

In 1988, Alexander Kellner and Diogenes de Almedeia Campos described a new species of pterosaur, Tupuxuara longicristatus, known from an anterior section of skull, mostly the front part of the nasoantorbital fenestra. Six years later, it was joined by T. leonardii, which is also fragmentary but distinguishable by a less extensive palatal ridge. Later, a much more complete specimen, IMCF 1052, was referred to T. leonardii on the basis of the palatal ridge extent.

In 2009, Mark Witton described and named T. deliradamus, and assigned two specimens. The holotype is a posterior section of skull. The referred specimen, KPMNH DL 84, is more complete, and shares these traits.

In 2013, Kellner named another species of pterosaur, Caupedactylus ybaka. This differs from Tupuxuara in, among other things, the downturn of the rostrum, palatal morphology… the posterior border of the NAOF and the inclination of the quadrate. Also that year, Hebert Bruno Campos and Jaime Headden presented a poster that, among other things, argued the mandible of the referred T. deliradamus specimen probably didn’t belong to it, but pointed out additional diagnostic characters from this specimen’s palate.

tupuxuara
Clockwise from top left: T. longicristatus, holotype of T. leonardii, IMCF 1052, C. ybaka, referred specimen of T. deliradamus, holotype of T. deliradamus. After Witton 2009, Kellner 2013, and Campos and Headden 2013. Not to scale.

T. longicristatus and T. leonardii can (probably) be distinguished from each other (depending on whether the extent of the palatal ridge is diagnostic – see Martill and Naish 2006, but see also Vremir et al. 2015), and Caupedactylus can easily be distinguished from both, but what about T. deliradamus? The diagnosis of T. deliradamus after Witton 2009 is as follows – the additional diagnostic characters provided by Campos and Headden 2013 are only visible in the referred specimen and are not considered right here.

  1. The angle of the quadrate relative to the occlusal margin is 150 degrees
  2. Lacrimal forms an angle of 120 degrees relative to the dorsal border of the nasoantorbital fenestra
  3. Posterior border of the NAOF is straight
  4. Orbit lies below half the height of the NAOF

Caupedactylus ybaka has all of these features. So it seems tempting to sweep that taxon into deliradamus. But the referred specimen of deliradamus – which also falls into this species’ diagnosis – is probably a different species than C. ybaka. The Kanagawa specimen has a distinctive palate, which differs from C. ybaka in the (probable) lack of a postpalatal fenestra and the presence of more developed vomers (Campos and Headden 2013). This, combined with the relative shortness and texture of the crest and other minor skull details, likely distinguish it from C. ybaka at the species level.

This means the holotype of deliradamus is indistinguishable from two species. As well, the holotype of deliradamus doesn’t preserve the anterior snout, whereas T. longicristatus and T. leonardii are only known from the anterior snout. So there’s a chance, even if small, that it could also be either of those. So that’s two to four different species that the deliradamus holotype is indistinguishable from. This would make Tupuxuara deliradamus a nomen dubium.

What, then, is the referred specimen? It differs considerably from IMCF 1052. It differs from C. ybaka. There’s very little overlap with the type of T. longicristatus, but they are pretty similar where they do overlap – for one, the angle of the NAOF is near-identical. The biggest difference is that the crest in T. longicristatus is deeper relative to the maxillary ramus despite the specimen being smaller. It’s uncertain whether this is of systematic significance or if it’s due to individual variation or sexual dimorphism – although the lack of perceptible dimorphism in Caiuajara (Manzig et al. 2014) does go against the latter. The anterior extent of the palatal ridge cannot be ascertained in KPMNH DL 84. It’s fair to assume KPMNH DL 84 is probably its own species of Thalassodromid.

Another specimen may also fall into this fray. In 2015, Ross Elgin figured and described an unnumbered “Tupuxuara-like Azhdarchoid” in the SMNK collections. It’s got great postcrania, but only the posterior skull is preserved. It also has a wide quadrate angle, an angled posterior NAOF border, and a low orbit. Unlike Caupedactylus ybaka and the Kanagawa specimen, though, it has a greater quadrate angle (161 degrees) and a really long, spear-like mandible. Might it be a third species in this mire?

elgin specimen.png
The Karlsruhe Tupuxuara-like azhdarchoid. From Elgin 2015.

In the data matrix of Azhdarchoid pterosaurs I’m building, all putative specimens of Tupuxuara are coded separately. Where they overlap, the codings for the holotype of T. deliradamus are identical to those of both the referred specimen and Caupedactylus. When I run the analysis, Caupedactylus ybaka and the two specimens of deliradamus form a polytomy, with the Karlsruhe specimen as the outgroup to that. Interesting.

caupedactylus tree section.png
The state of things. A couple postcrania-only specimens (incl. the Crato “Azhdarchid” SMNK PAL 2342, which is a Thalassodromid) were excluded due to instability

Should we call all these specimens Caupedactylus? For now I will. Though there is an element of subjectivity to generic assignment, keeping the “T. deliradamus” specimens in Tupuxuara would make the genus polyphyletic with respect to Caupedactylus and Thalassodromeus.

tl:dr; T. deliradamus likely nomen dubium, maybe we should be calling it Caupedactylus.

References
Campos, H.B.N.; Headden, J.A. (2013). “A review of Tupuxuara deliradamus (Pterosauria, Azhdarchoidea, Thalassodromidae) from the Early Cretaceous Romualdo Formation of Brazil”. International Symposium on Pterosaurs – Rio Ptero 2013.
Elgin, R.A. (2015). “Paleobiology, Morphology and Flight Characteristics of Pterodactyloid Pterosaurs”. Dissertation, University of Heidelberg.
Kellner, A.W.A. (2013). “A new unusual tapejarid (Pterosauria, Pterodactyloidea) from the Early Cretaceous Romualdo Formation, Araripe Basin, Brazil”. Earth and Environmental Science Transactions of the Royal Society of Edinburgh 103(3-4): 409-421.
Manzig, P.C.; Kellner, A.W.A.; Weinschutz, L.C.; Fragoso, C.E.; Vega, C.S.; Guimaraes, G.B.; Godoy, L.C.; Liccardo, A.; Ricetti, J.H.Z.; de Moura, Camila C. (2014). “Discovery of a Rare Pterosaur Bone Bed in a Cretaceous Desert with Insights on Ontogeny and Behavior of Flying Reptiles”. PLoS ONE 9(8): e100005.
Martill, D.M.; Naish, D. (2006). “Cranial Crests Development in the Azhdarchoid Pterosaur Tupuxuara, With Review of the Genus and Tapejarid Monophyly”. Palaeontology 49(4): 925-941.
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 (Hateg Basin, Transylvania, Romania)”. American Museum Novitates 3827.
Witton, M.P. (2009). “A new species of Tupuxuara (Thalassodromidae, Azhdarchoidea) from the Lower Cretaceous Santana Formation of Brazil, with a note on the nomenclature of Thalassodromidae”. Cretaceous Research 30(5): 1293-1300.

Pterosaurs of the Kem Kem Beds

The Kem Kem Beds lie on the border of Morocco and Algeria. This formation produces fossils that date to the Cenomanian, which reveal a coastal deltaic wetland environment. It’s most famous for the various large theropod dinosaurs such as Carcharodontosaurus and Spinosaurus (leading to the infamous Stromer’s Riddle – why are there so many large predatory dinosaurs in the same time and place?)

All of the pterosaur fossils from Kem Kem seem to hail from the Aoufous Formation (~95 Ma) and all come in the form of isolated bones, but given this quality of preservation a surprisingly high pterosaur diversity is known. At least five distinct taxa can be distinguished, indicating a probably Azhdarchoid-dominated assemblage. Chiarenza and Cau 2016 proposed that the high diversity of the Beds is exaggerated by ambiguous stratigraphy, and that the theropods, and by extension other fauna, hail from different units that were laid down at different times. Hence, they weren’t all contemporaneous. The same could apply for other fauna, including pterosaurs. But even if this weren’t the case (and they were all contemporaneous), Stromer’s Riddle likely wouldn’t apply to the pterosaurs – the diversity in jaw shapes in the recovered pterosaurs imply they all probably exploited different niches.

Anhanguerians

Only one toothed pterosaur, Siroccopteryx, is currently named from the Kem Kem formation. There are a lot of isolated teeth, however, and they fall into four distinct morphotypes (Wellnhofer and Buffetaut 1999). It’s unknown whether this might hint at higher diversity or if they could have all come from different positions in one pterosaur’s mouth.

Siroccopteryx moroccensis

siroccopteryx_coloborhynchus_by_hyrotrioskjan-d8ag6l3
Life restoration of Ernst Stromer, with Siroccopteryx for scale. By Joschua Knüppe, used with permission.

The first pterosaur named from Kem Kem, Siroccopteryx is an Ornithocheirid closely related to Coloborhynchus. In fact I’d say it was a species of Coloborhynchus if Coloborhynchus didn’t live 40 million years earlier. The only known remains are, like many old world Anhanguerians, a snout tip, which is basically only useful at telling us what it’s related to. It was fairly medium-sized and like most Anhanguerians probably piscivorous. A handy diet for a coastal environment.

Azhdarchids

Azhdarchids are more well-represented from Kem Kem. Not only are there two named species based on skull material, there are at least two morphs of cervical vertebrae (whether the differences are taxonomic or due to position in the neck are unclear) and an isolated humerus that could pertain to either. Interestingly, the two Azhdarchid species here might be related…

Alanqa saharica

j8cubnl7rl2waactoofg_alanqa
Life restoration of Alanqa. By Joschua Knüppe, used with permission.

Alanqa was named in 2010 based on a mandible that was at first interpreted as a possible Pteranodontid snout. More mandible and rostrum chunks were referred to it. The jaws are notable for being very long straight, even when compared to other Azhdarchids. What’s also notable is that near the back of the mandible was a pair of ridges on the occlusal face. A piece of palate was later found with similar ridges, and it’s likely this portion was positioned so the ridges met when the jaws closed (Martill & Ibrahim 2015).

It’s uncertain what these ridges were used for – Martill & Ibrahim suggested crushing hard-shelled prey, attachment for turkey-like snoods, attachment for “cheeks”, or simple display features. I personally am inclined towards the first or last options; there’s no evidence for any cheek-like structures in pterosaurs, and being at least partially in the inside of the mouth a soft-tissue attachment would be awkward. The ridges could indicate Alanqa was at least partially durophagous, crushing hard-shelled aquatic invertebrates. This would make it similar ecologically to modern openbill storks or oystercatchers.

Xericeps curvirostris

Xericeps-skull4.png
Reconstruction of the skull of Xericeps. Scale bar = 10 cm.

Xericeps was named by Martill and colleagues in 2017 off another mandible with paired ridges. Unlike Alanqa, the mandible is rounder in cross-section and gently curves upward. It’s been likened to the jabiru by Joschua Knüppe (I see a pattern here in comparing Azhdarchids to storks…). Ridges like these combined with a pointed/upturned anterior snout may have been an attempt at being a “toothless heterodont”, being able to process different foods (e.g. small vertebrates vs. shelled invertebrates) in different areas of the mouth (Headden, pers. comm.). The different shape of the jaws relative to Alanqa imply niche partitioning between these two pterosaurs.

What’s interesting is that both the Kem Kem Azhdarchids have almost identical paired parallel ridges near the back of the mandible (and in Alanqa, maybe the palate too). These mandibular ridges differ from the independently-evolved horizontal ridge in Bakonydraco and “Huaxiapterus benxiensis” and the single anterior ridge in Thalassodromeus. My analysis currently has Alanqa and Xericeps form a clade that may include Argentinadraco, which also has similar mandibular ridges.

Rodrigues et al. 2011 describe another fragment of rostrum, CMN 50859, which was broadly referred to Dsungaripteroidea (=Ornithocheiroidea) indet. based on the lack of diagnostic features. I think it might be Xericeps. Both have a convex ventral margin and a roughly oval cross-section.

xlebw0k3syczpwsqmwwt_xericeps_joschua-knuppe
Life restoration of Xericeps. By Joschua Knüppe, used with permission.

Other Pterosaurs

Kem Kem “Pteranodontid”

Another mandible fragment, MN 7054-V, was described by Kellner et al. 2007 and proposed to be a Pteranodontid. Very little anatomical information can be gleaned from this fossil, but a few things can be determined: it lacks teeth, is roughly triangular in cross-section, gently curves upward and doesn’t have any foraminae. The lack of foraminae probably excludes it from Azhdarchidae (Ibrahim et al. 2010), and the gentle upturn and lack of prominent tomia probably exclude it from Tapejaridae or Thalassodromidae. This leaves two possible clades – Pteranodontidae and Chaoyangopteridae. Around this time, unambiguous Pteranodontians are unknown in the fossil record, but Chaoyangopterids may be if Microtuban turns out to be one. The fossil is significantly less elongate than Pteranodontian mandibles but closer to (though still shorter than) that of Shenzhoupterus in length, and proportionally wider than Pteranodon mandibles seem to be, more closely resembling Lacusovagus in this respect. So take this with a grain of salt, but I think it might hint at a slightly short-snouted Kem Kem Chaoyangopterid.

kem kem chaoyangopterid
Very hypothetical reconstruction of MN 7054-V as a Chaoyangopterid. Scale bar = 5 cm.

 

Kem Kem Tapejarid

Kem Kem tapejarid
The beak chunk of the Tapejarid, in dorsal/ventral (a) and lateral (b) views. From Wellnhofer and Buffetaut 1999. Scale bar= 5 cm.

Finally, there’s this last little beak chunk, BSP 1997 I 67. It’s hard to tell whether it’s a mandible or a rostrum, but in any case this specimen shows the beginning of a deep crest. Contra Averianov 2014, it probably isn’t Alanqa; no Azhdarchid has a similar crest or similarly narrow jaws, and this fragment lacks the paired foraminae at the front of the jaw seen in Alanqa and several other Azhdarchids (they’re apparent even in tiny specimens referred to Azhdarcho, so they probably didn’t appear with age). Whatever it is, it seems to fit most among Tapejarids (possibly a basal one due to the relatively gentle curvature). This specimen implies a fairly large Tapejarid, similar in size to Tupandactylus. Assuming it was other Tapejarids, it was probably omnivorous/predominantly herbivorous, rounding out the ecological diversity in Kem Kem pterosaurs.

References
Averianov, A. (2014). “Review of taxonomy, geographic distribution, and paleoenvironments of Azhdarchidae (Pterosauria)”. ZooKeys 432: 1-107.
Chiarenza, A.A.; Cau, A. (2016). “A large abelisaurid (Dinosauria, Theropoda) from Morocco and comments on the Cenomanian theropods from North Africa“. PeerJ 4: e1754.
Ibrahim, N.; Unwin, D.M.; Martill, D.M.; Baidder, L.; Zouhri, S. (2010). “A New Pterosaur (Pterodactyloidea: Azhdarchidae) from the Upper Cretaceous of Morocco”. PLoS ONE 5(5): e10875.
Kellner, A.W.A.; Mello, A.M.S.; Ford, T. (2007). “A survey of pterosaurs from Africa with the description of a new specimen from Morocco”. In: Paleontologia: Cenários de Vida pp. 257-267.
Martill, D.M.; Ibrahim, N. (2015). “An unusual modification of the jaws in cf. Alanqa, a mid-Cretaceous azhdarchoid pterosaur from the Kem Kem beds of Morocco”. Cretaceous Research 53: 59-67.
Martill, D.M.; Unwin, D.M.; Ibrahim, N.; Longrich, N. (2017). “A new edentulous pterosaur from the Cretaceous Kem Kem beds of south eastern Morocco”. Cretaceous Research, in press.
Rodrigues, T.; Kellner, A.W.A.; Mader, B.J.; Russell, D.A. (2011). “New Pterosaur Specimens from the Kem Kem Beds (Upper Cretaceous, Cenomanian) of Morocco”. Rivista Italiana di Paleontologia e Stratigrafia 117(1): 149-160.
Wellnhofer, P.; Buffetaut, E. (1999). “Pterosaur remains from the Cretaceous of Morocco”. Paläontologische Zeitschrift 73 :133-142.