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New perspectives on palaeobiology

DAVID W. E. HONE1*, MARK P. WITTON2 & DAVID M. MARTILL2 1Queen Mary University of , Mile End Road, London E14NS, UK 2School of Earth and Environmental Sciences, University of Portsmouth, Burnaby Road, Portsmouth PO1 3QL, UK *Correspondence: [email protected]

Abstract: were the first vertebrates to evolve powered flight and occupied the skies of the Mesozoic for 160 million years. They occurred on every continent, evolved their incredible pro- portions and anatomy into well over 100 species, and included the largest flying of all time among their ranks. Pterosaurs are undergoing a long-running scientific renaissance that has seen elevated interest from a new generation of palaeontologists, contributions from scientists working all over the world and major advances in our understanding of their palaeobiology. They have espe- cially benefited from the application of new investigative techniques applied to historical speci- mens and the discovery of new material, including detailed insights into their fragile skeletons and their soft tissue anatomy. Many aspects of pterosaur science remain controversial, mainly due to the investigative challenges presented by their fragmentary, fragile and notoriously patchy record. With perseverance, these controversies are being resolved and our understand- ing of flying is increasing. This volume brings together a diverse set of papers on numerous aspects of the biology of these fascinating reptiles, including discussions of pterosaur ecology, flight, ontogeny, bony and soft tissue anatomy, distribution and evolution, as well as revisions of their and relationships.

Gold Open Access: This article is published under the terms of the CC-BY 3.0 license.

... altogether the structure of these extinct members twenty-first century already has two (Unwin 2005; of the reptilian class is such as to rank them amongst Witton 2013). Public interest is demonstrated by the most extraordinary of all creatures yet discovered large exhibitions dedicated to these animals in in the ruins of the ancient earth. Owen (1854) London, Japan and the USA, as well as plans to con- Pterosaurs have one of the longest research histories struct a pterosaur museum in the Xinjiang Autono- of any extinct vertebrate group and have been mous Region of China. Dedicated, multi-million studied by some of the most notable names in verte- pound television documentaries and increasingly brate palaeontology, including Georges Cuvier, prevalent roles in popular media are further evi- William Buckland, , O.C. Marsh dence of pterosaurs occupying a more prominent and Harry Govier Seeley (Wellnhofer 2008). It is position in the public’s consciousness. widely known that pterosaurs were recognized as Pterosaur researchers have typically attributed flying animals as early as 1801 (Cuvier 1801) thanks this interest to the ever-increasing number of ptero- to material described by Collini (1784). However, saur fossils being discovered, many occurring in earlier letters between researchers showed that Brazilian and Chinese Lagersta¨tten. It is certainly pterosaurs were already in the minds of the scientists hard to overstate the impact and scientific excitement of the late 1700s (e.g. Hermann, see Taquet & associated with these sites, especially considering Padian 2004) and recent works suggest other speci- their discovery within a few decades of each other. mens were at least discovered, if not described, In rapid succession they led to the discovery of sev- before 1784 (O´´si et al. 2010). eral major clades, numerous new species, novel Aside from a notable hiatus in the mid-twentieth details of skeletal and soft tissue anatomy, exquisitely century, research into flying reptiles has advanced preserved three-dimensional specimens and the first more or less continuously since their discovery. fossils of pterosaur eggs. Collectively, this produced However, the last four decades have seen a great a wealth of new information and helped resolve many expansion in interest in pterosaurs from researchers, longstanding questions about pterosaur biology, as palaeoartists and laymen (Fig. 1). As evidence of well as prompting many new ones (Hone 2012). this, the entire twentieth century saw the publication The elevated discovery rates of new pterosaur of only three major overviews of pterosaur science specimens may have catalysed much of our renewed (Seeley 1901; Wellnhofer 1978, 1991) while the interest in this group, but it is continued study

From:Hone, D. W. E., Witton,M.P.&Martill, D. M. (eds) New Perspectives on Pterosaur Palaeobiology. Geological Society, London, Special Publications, 455, https://doi.org/10.1144/SP455.18 # 2017 The Author(s). Published by The Geological Society of London. Publishing disclaimer: www.geolsoc.org.uk/pub_ethics Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

D. W. E. HONE ET AL.

Fig. 1. Illustrations of the British pterosaur macronyx showing scientific developments through pterosaur research over two centuries. (a) Detail of a 1829 watercolour by Reverend G.E. Howman depicting D. macronyx as a monstrous ‘flying dragon found at Lyme Regis supposed to be noctivagous’ (Martill 2014). (b) An ungainly, bat-like reconstruction in the monograph of Owen (1870). (c) Harry Seeley’s progressive interpretation of D. macronyx as an erect-limbed quadruped from his 1901 book; note that an alternative interpretation of D. macronyx as a biped also appears in Seeley (1901); (d) The restoration of D. macronyx as a highly active, bird-like digitigrade biped by Padian (1983) – a controversial interpretation that nevertheless symbolises the reinvention of pterosaurs in the late twentieth century. (e) Modern interpretation of D. macronyx adult and speculative juveniles from the cover of this volume, reflecting contemporary interpretations of pterosaur soft tissues, muscle development and ecology. The flying juveniles reflect the long-awaited twenty-first century discovery of pterosaur embryos and their unexpected flight-ready anatomy. Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

INTRODUCTION TO PTEROSAUR PALAEOBIOLOGY and the insights provided by applying new palaeon- of specimens, to light, while others touch on ongo- tological methods to them that is sustaining, if ing uncertainties, controversies and issues within not increasing, their academic and popular appeal. pterosaur palaeobiology. Modern interest in pterosaurs has proved to be a Although the pterosaur record has improved self-perpetuating discipline within modern palaeon- considerably in recent years, enormous gaps in tology rather than a scientific ‘fad’. our knowledge still remain. Thus the reports of several new pterosaur specimens in this volume are International pterosaur symposia welcome additions to the literature. They include unpublished material of the giant, Late Recent pterosaur studies have been presented not Jordanian azhdarchid Arambourgiania philadel- only in books and research papers, but also in phiae, perhaps even lost elements of the holo- a series of pterosaur-themed volumes based on type, which are discussed by Martill & Moser the now regular international meetings of pterosaur (2017). Remains of another large, researchers. The meetings as they occur today pterodactyloid are reported by Bennett (2017). evolved from a workshop of pterosaur researchers This specimen, although fragmentary, is significant at the 55th Annual Meeting of the Society of for representing a rare American Turonian ptero- Vertebrate Paleontology, held in Pittsburgh, Penn- saur and allows a more complete understanding of sylvania, USA in 1995 and have now expanded to pterosaur evolution around the Western Interior a regular series with worldwide participation. Seaway. Rigal et al. (2017) describe new ptero- A second Society of Vertebrate Paleontology dactyloid specimens from the British Wealden symposium was held in New York in 1996 (Kellner Group, a Lower Cretaceous unit of historical impor- et al. 2013) and was followed by a gathering in Tou- tance to pterosaur workers, but frustratingly limited louse, France in the year 2000, the first meeting to with regard to new pterosaur material. Their work result in an associated published collection of ptero- has a bearing on the status and content of the con- saur papers (Buffetaut & Mazin 2003). Next was a troversial clade Lonchodectidae and includes the small meeting in Bergamo, Italy (Paganoni 2003) erection of a new genus. McLain & Bakker and then Munich, Germany in 2007. The Munich (2017) describe pterosaur material from the Late meeting was the first to be called Flugsaurier, now Jurassic Morrison Formation, which helps to eluci- a recurrent name for pterosaur symposia, and also date the taxonomic content of this poorly under- produced an associated paper volume (Hone & stood pterosaur fauna. Leal et al. (2017) describe Buffetaut 2008). Since then, pterosaur researchers new cervical material from Brazil providing further have convened at Flugsaurier 2010 (Beijing, China, suggestive evidence of chaoyangopterid ptero- resulting in a volume edited by Lu¨ et al. 2012) and saurs outside of Chinese deposits. Lu¨ et al. (2017) Rio Ptero 2013 (Rio de Janeiro, Brazil, resulting in briefly describe a new anurognathid specimen a volume edited by Kellner et al. 2015). The most from the Early Cretaceous of Liaoning, which may recent event, Flugsaurier 2015, held in Portsmouth, have a pedal grasping adaptation unlike any other UK, resulted in the current volume. pterosaur. Based on past successes and the promise of at Pterosaur researchers also remain challenged by least one more pterosaur meeting (scheduled for the poor documentation of existing discoveries. 2018 in Los Angeles, California, USA) it is clear Such a topic is addressed by Hone et al. (2017) that these congregations are a continued success. for the widely known, but poorly understood, The seven meetings have seen more than 200 pub- Early Cretaceous Chinese pterosaur Noripterus lished abstracts and collectively gathered hundreds complicidens. This species is represented by excel- of researchers from six continents. The benefits of lent material, but poor curation and relatively modern digital communications have doubtlessly scant attention from pterosaur workers means that enhanced modern palaeontological science, but our concept of Noripterus requires re-evaluation. they have not superseded the value of bringing A contentious aspect of pterosaur research is together individuals to meet, exchange ideas and their systematics. Several competing interpreta- examine specimens. tions of their phylogenetic relationships have been published in the last two decades (e.g. Unwin Proceedings of Flugsaurier 2015 2003; Kellner 2003; Andres et al. 2014) and much work remains to resolve related nomenclatural, As is now traditional for pterosaur meetings, a series taxonomic and phylogenetic disagreements. In of papers pertaining to content delivered in posters this volume, Vidovic & Martill (2017) present a and talks at Flugsaurier 2015 are presented in fourth distinct pterosaur phylogeny and challenge this volume, alongside a number of other pterosaur- recent taxonomic interpretations of the Solnhofen focused studies. The topics of these papers are pterodactyloids Pterodactylus antiquus, P. kochi broad, with many bringing new specimens, or details and Germanodactylus rhamphastinus. Evidently, Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

D. W. E. HONE ET AL. controversies over pterosaur systematics are set to References run for some time yet. Novel insights into pterosaur palaeobiology are Andres, B., Clark,J.&Xu, X. 2014. The earliest ptero- reported in several papers. Bennett & Penkalski dactyloid and the origin of the group. Current Biology, (2017) discuss unusual, banded growth patterns in 24, 1011–1016. the rostrum of the large Late Cretaceous, North Bennett, S.C. 2017. A large pterodactyloid pterosaur from the Late Cretaceous Ferron Sandstone of Utah. American Pteranodon. It is sobering for researchers Hone Witton Martill to consider that Pteranodon – undoubtedly one of In: , D.W.E., , M.P. & , D.M. (eds) New Perspectives on Pterosaur Palaeobiology. the best studied and documented pterosaurs – is Geological Society, London, Special Publications, still the source of new and unexpected information 455. First published online April 13, 2017, https:// on pterosaur anatomy. Codorniu´ et al. (2017) pro- doi.org/10.1144/SP455.11 vide a full description of an embryonic specimen Bennett, S.C. & Penkalski, P. 2017. Waves of bone of the Cretaceous filter-feeding pterosaur Ptero- deposition on the rostrum of the pterosaur Pteranodon. daustro guinazui, providing one of the most com- In: Hone, D.W.E., Witton, M.P. & Martill, D.M. prehensive insights into pre-hatchling pterosaur (eds) New Perspectives on Pterosaur Palaeobiology. anatomy to date. Geological Society, London, Special Publications, Welcome attempts to reconstruct functional 455. First published online February 22, 2017, https://doi.org/10.1144/SP455.2 anatomy are also provided. Frigot (2017) performs Buffetaut,E.&Mazin, J-.M. (eds) 2003. Evolution and one of the first detailed assessments of pterodacty- Palaeobiology of Pterosaurs. Geological Society, Lon- loid upper hindlimb myology using the exquisitely don, Special Publications, 217, https://doi.org/10. preserved holotype pelvis of the Cretaceous 1144/GSL.SP.2003.217.01.22 Wealden azhdarchoid Vectidraco daisymorrisae. Collini, C.A. 1784. Sur quelques Zoolithes du Cabinet Henderson (2017) presents one of the first quanti- d’Histoire naturelle de S.A.S.E. Palatine & de Bavie`re, fied assessments of pterosaur bite force and skull a` Mannheim. Acta Academiae Theodoro-Palatinae, 5, 58–103. mechanics using digital skull models, while Palmer Codorniu´ Chiappe Rivarola (2017) reports the physical modelling of pterosaur , L., ,L.& , D. 2017. Neo- nate morphology and development in pterosaurs: evi- wing membrane properties, providing valuable dence from a Ctenochasmatid embryo from the Early insights into wing anatomy and function. Cretaceous of Argentina. In: Hone, D.W.E., Witton, This volume also provides discussions attempt- M.P. & Martill, D.M. (eds) New Perspectives on ing to further understand pterosaur faunas and ecol- Pterosaur Palaeobiology. Geological Society, London, ogy. One means of understanding the role of flying Special Publications, 455. First published online reptiles in Mesozoic food webs is via fossils that August 22, 2017, https://doi.org/10.1144/SP455.17 preserve the gut contents, feeding traces or other Cuvier, G. 1801. Extrait d’un ouvrage sur les espe`ces de evidence of ancient trophic interactions. These are quadrupe`des don’t on a les ossemens dans l’inte´rieur reviewed by Witton (2017), revealing pterosaurs de la terre. Journal de Physique, Chimie, et d’Histoire Naturelle de l’Institut National, 52, 253–267. to be both consumers and consumed in Mesozoic Dalla Vecchia, F.M. 2017. A wing metacarpal from Italy ecosystems. O’Sullivan (2017) comments on the and its implications for latest Cretaceous pterosaur pterosaur assemblage of the Oxford Clay Formation diversity. In: Hone, D.W.E., Witton, M.P. & Mar- from the UK and examines the status of the till, D.M. (eds) New Perspectives on Pterosaur neglected taxon ‘Rhamphorhynchus jessoni’. Dalla Palaeobiology. Geological Society, London, Special Vecchia (2017) describes a wing metacarpal from Publications, 455. First published online February 17, the Late Cretaceous of Italy and discusses its impli- 2017, https://doi.org/10.1144/SP455.1 Frigot cations for the changing picture of pterosaur diver- , R.A. 2017. Pelvic musculature of Vectidraco dai- sity at the end of the Mesozoic. Unwin & Martill symorrisae and consequences for pterosaur locomo- tion. In: Hone, D.W.E., Witton, M.P. & Martill, (2017) revise the identity of a Jurassic specimen D.M. (eds) New Perspectives on Pterosaur Palaeobiol- from Thailand, which has been identified as azh- ogy. Geological Society, London, Special Publications, darchoid, but might be better considered to 455. First published online February 28, 2017, https:// be rhamphorhynchid. doi.org/10.1144/SP455.7 The unfamiliar nature of pterosaurs and their Henderson, D.M. 2017. Using three-dimensional, digital sparse fossil record render them a challenging models of pterosaur skulls for the investigation of their group to understand. However, as demonstrated relative bite forces and feeding styles. In: Hone, Witton Martill here, perseverance in the study of these flying D.W.E., , M.P. & , D.M. (eds) New reptiles rewards researchers with new insights and Perspectives on Pterosaur Palaeobiology. Geological Society, London, Special Publications, 455. First pub- ideas about their evolution and palaeobiology. lished online February 22, 2017, https://doi.org/10. This volume represents only the latest thinking in 1144/SP455.9 a long history of pterosaur research: we look for- Hone, D.W.E. 2012. Pterosaur research: recent advances ward to the scientific discussion and increased and a future revolution. Acta Geologica Sinica, 86, understanding that these papers will inspire. 1366–1376. Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

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Hone, D.W.E. & Buffetaut, E. 2008. Flugsaurier – Palaeobiology. Geological Society, London, Special Pterosaur papers in honour of Peter Wellnhofer. Publications, 455. First published online August 4, Zitteliana B, 28. 2017, https://doi.org/10.1144/SP455.14 Hone, D.W.E., Jiang,S.&Xu, X. 2017. A taxonomic O’Sullivan, M. 2017. The pterosaur assemblage of revision of Noripterus complicidens and Asian mem- the Oxford Clay Formation (Jurassic, Callovian– bers of the Dsungaripteridae. In: Hone, D.W.E., Wit- Oxfordian) from the UK. In: Hone, D.W.E., Witton, ton, M.P. & Martill, D.M. (eds) New Perspectives M.P. & Martill, D.M. (eds) New Perspectives on Pterosaur Palaeobiology. Geological Society, Lon- on Pterosaur Palaeobiology. Geological Society, Lon- don, Special Publications, 455. First published online don, Special Publications, 455. First published online February 22, 2017, https://doi.org/10.1144/SP455.8 March 16, 2017, https://doi.org/10.1144/SP455.10 Kellner, A.W.A. 2003. Pterosaur phylogeny and com- O´´si, A., Prondvai & Ge´czy, B. 2010. The history of Late ments on the evolutionary history of the group. In: Jurassic pterosaurs housed in Hungarian collections Buffetaut,E.&Mazin, J.-M. (eds) Evolution and and the revision of the holotype of Pterodactylus Palaeobiology of Pterosaurs. Geological Society, Lon- micronyx Meyer 1856 (a ‘Pester Exemplar’). In: don, Special Publications, 217, 105–137. Moody, R.T.J., Buffetaut, E., Naish,D.&Mar- Kellner, A.W.A., Saya˜o, H.M. & Costa, F.R. 2013. till, D.M. (eds) and Other Extinct Sauri- Welcome to Rio Ptero 2013 – International Sympo- ans: A Historical Perspective. Geological Society, sium on Pterosaurs. In: Saya˜o, J.M., Costa, F.R., London, Special Publications, 343 , 277–286, https:// Bantim, R.A.M. & Kellner, A.W.A. (eds) Short doi.org/10.1144/SP343.17 Communications/International Symposium on Ptero- Owen, R. 1854. Geology and Inhabitants of the Ancient saurs, Rio Ptero 2013. Universidade Federal do Rio World. Bradbury & Evans, London [reprinted Euston de Janeiro, Museu Nacional, Se´rie Livros, 50,9. Grove Press, London, 2013]. Kellner, A.W.A., Rodrigues,T.&Saya˜o, H.M. 2015. Owen, R. 1870. Monograph on the Fossil Reptilia of the Proceedings of the Rio International Symposium on Liassic Formations. I. Part III. Plesiosaurus, Dimor- Pterosaurs. Historical Biology, 27. phodon, and Ichthyosaurus. Palaeontographical Soci- Leal , M.E.C., Beˆgas, R.V., Bonde,N.&Kellner, ety, London. A.W.A. 2017. Cervical vertebrae of an enigmatic Padian, K. 1983. Osteology and functional morphology pterosaur from the Crato Formation (Lower Creta- of Dimorphodon macronyx (Buckland) (Pterosauria: ceous, Araripe Basin, NE Brazil). In: Hone, D.W.E., Rhamphorhynchoidea) based on new material in the Witton, M.P. & Martill, D.M. (eds) New Perspec- Yale Peabody Museum. Postilla, 189, 1–44. tives on Pterosaur Palaeobiology. Geological Society, Paganoni, A. 2003. after 30 years: history London, Special Publications, 455. First published of the finding and perspectives. Revista del Museo Civico online September 25, 2017, https://doi.org/10.1144/ di Scienze Naturale “Enrico Caffi” Bergamo, 22, 47–51. SP455.15 Palmer, C. 2017. Inferring the properties of the pterosaur Lu¨ , J., Unwin, D.M., Ji,S.&Ji, Q. 2012. Acta Geologica wing membrane. In: Hone, D.W.E., Witton, M.P. & Sinica, 86. Martill, D.M. (eds) New Perspectives on Pterosaur Lu¨ , J., Meng, Q., Wang, B., Liu, D., Shen,C.&Zhang, Palaeobiology. Geological Society, London, Special Y. 2017. Short note on a new anurognathid pterosaur Publications, 455. First published online February 17, with evidence of perching behaviour from Jianchang 2017, https://doi.org/10.1144/SP455.4 of Liaoning Province, China. In: Hone, D.W.E., Rigal, S., Martill, D.M. & Sweetman, S.C. 2017. A Witton, M.P. & Martill, D.M. (eds) New Perspec- new pterosaur specimen from the Upper Tunbridge tives on Pterosaur Palaeobiology. Geological Society, Wells Sand Formation (Cretaceous, Valanginian) London, Special Publications, 455. First published of southern England and a review of Lonchodectes online September 25, 2017, https://doi.org/10.1144/ sagittirostris (Owen 1874). In: Hone, D.W.E., Wit- SP455.16 ton, M.P. & Martill, D.M. (eds) New Perspectives Martill, D.M. 2014. Dimorphodon and the Reverend on Pterosaur Palaeobiology. Geological Society, George Howman’s noctivagous flying dragon: the ear- London, Special Publications, 455. First published liest restoration of a pterosaur in its natural habitat. online February 22, 2017, https://doi.org/10.1144/ Proceedings of the Geologists’ Association, 125, SP455.5 120–130. Seeley,H.G.1901.Dragons of the Air. Meuthuen, London. Martill, D.M. & Moser, M. 2017. Topotype specimens Taquet,P.& Padian, K. 2004. The earliest known resto- probably attributable to the giant azhdarchid pterosaur ration of a pterosaur and the philosophical origins of Arambourgiania philadelphiae (Arambourg 1959). Cuvier’s Ossemens Fossiles. Comptes Rendus Palevol, In : Hone, D.W.E., Witton, M.P. & Martill, D.M. 3, 157–175. (eds) New Perspectives on Pterosaur Palaeobiology. Unwin, D.M. 2003. On the phylogeny and oeigin of ptero- Geological Society, London, Special Publications, saurs. In: Buffetaut,E.&Mazin, J.-M. (eds) Evolu- 455. First published online February 22, 2017, tion and Palaeobiology of Pterosaurs. Geological https://doi.org/10.1144/SP455.6 Society, London, Special Publications, 217, 139–190. McLain, M.A. & Bakker, R.T. 2017. Pterosaur material Unwin, D.M. 2005. The Pterosaurs from Deep Time.Pi from the uppermost Jurassic of the uppermost Press, New York. Morrison Formation, Breakfast Bench Facies, Como Unwin, D.M. & Martill, D.M. 2017. Systematic reas- Bluff, Wyoming, including a pterosaur with pneuma- sessment of the first Jurassic pterosaur from Thailand. tized femora. In: Hone, D.W.E., Witton, M.P. & In: Hone, D.W.E., Witton, M.P. & Martill, D.M. Martill, D.M. (eds) New Perspectives on Pterosaur (eds) New Perspectives on Pterosaur Palaeobiology. Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

D. W. E. HONE ET AL.

Geological Society, London, Special Publications, Wellnhofer, P. 1991. The Illustrated Encyclopedia of 455. First published online August 14, 2017, https:// Pterosaurs. Salamander Books, London. doi.org/10.1144/SP455.13 Wellnhofer, P. 2008. A short history of pterosaur Vidovic, S.U. & Martill, D.M. 2017. The taxonomy and research. Zitteliana, 28, 7–19. phylogeny of Diopecephalus kochi (Wagner, 1837) Witton,M.P.2013.Pterosaurs:NaturalHistory,Evolution, and ‘Germanodactylus rhamphastinus’ (Wagner, Anatomy. Princeton University Press, Princeton, NJ. 1851). In: Hone, D.W.E., Witton, M.P. & Martill, Witton, M.P. 2017. Pterosaurs in Mesozoic food webs: D.M. (eds) New Perspectives on Pterosaur Palaeobiol- a review of fossil evidence. In: Hone,D.W.E., ogy. Geological Society, London, Special Publications, Witton,M.P.&Martill, D.M. (eds) New Perspec- 455. First published online June 27, 2017, https://doi. tives on Pterosaur Palaeobiology. Geological Soci- org/10.1144/SP455.12 ety, London, Special Publications, 455.First Wellnhofer,P.1978.Pterosauria, Part 19. In: Handbuch published online February 22, 2017, https://doi. der Pala¨oherpetologie, Gustav Fischer Verlag, Stuttgart. org/10.1144/SP455.3