Neck biomechanics indicate that giant Transylvanian azhdarchid pterosaurs were short-necked arch predators - PubMed (original) (raw)
Neck biomechanics indicate that giant Transylvanian azhdarchid pterosaurs were short-necked arch predators
Darren Naish et al. PeerJ. 2017.
Abstract
Azhdarchid pterosaurs include the largest animals to ever take to the skies with some species exceeding 10 metres in wingspan and 220 kg in mass. Associated skeletons show that azhdarchids were long-necked, long-jawed predators that combined a wing planform suited for soaring with limb adaptations indicative of quadrupedal terrestrial foraging. The postcranial proportions of the group have been regarded as uniform overall, irrespective of their overall size, notwithstanding suggestions that minor variation may have been present. Here, we discuss a recently discovered giant azhdarchid neck vertebra referable to Hatzegopteryx from the Maastrichtian Sebeş Formation of the Transylvanian Basin, Romania, which shows how some azhdarchids departed markedly from conventional views on their proportions. This vertebra, which we consider a cervical VII, is 240 mm long as preserved and almost as wide. Among azhdarchid cervicals, it is remarkable for the thickness of its cortex (4-6 mm along its ventral wall) and robust proportions. By comparing its dimensions to other giant azhdarchid cervicals and to the more completely known necks of smaller taxa, we argue that Hatzegopteryx had a proportionally short, stocky neck highly resistant to torsion and compression. This specimen is one of several hinting at greater disparity within Azhdarchidae than previously considered, but is the first to demonstrate such proportional differences within giant taxa. On the assumption that other aspects of Hatzegopteryx functional anatomy were similar to those of other azhdarchids, and with reference to the absence of large terrestrial predators in the Maastrichtian of Transylvania, we suggest that this pterosaur played a dominant predatory role among the unusual palaeofauna of ancient Haţeg.
Keywords: Azhdarchids; Biomechanics; Cretaceous; Maastrichtian; Pterosaurs.
Conflict of interest statement
The authors declare there are no competing interests.
Figures
Figure 1. Giant azhdarchid cervical vertebra referred to Hatzegopteryx sp. (A–D) line drawings of EME 315 in anterior (A) right lateral (B) ventral (C) and dorsal (D) views; (E) proportions of EME 315 compared to other azhdarchid cervicals: note atypical combination of length/width ratio (l:w) and length compared to other azhdarchid cervicals, and especially against the only other known giant cervical, Arambourgiania (UJA RF1).
Light shading indicates damage; dark shading indicates filler. Abbreviations: co, cotyle; hy, hypapophysis; nc, neural canal; nsa; neural spine (anterior region); nsp, neural spine (posterior region); pnf, pneumatic foramen; prz, prezygapophysis; poz, postzygapophysis; vprzt, ventral prezygapophyseal tubercle (fused cervical rib). Scale bar is 100 mm.
Figure 2. Characteristics of azhdarchid vertebrae across their cervical series, demonstrated by several azhdarchid taxa.
(A) Azhdarcho lancicollis cervical III (ZIN PH 131/44), left lateral aspect; (B–C) Quetzalcoatlus sp. cervical III (TMM 41544.16) in dorsal (B) and left lateral (C) aspect; (D) A. lancicollis cervical IV (ZIN PH 144/44), left lateral aspect; (E) Q. sp. cervical V (TMM 41455.15), left lateral aspect; (F) Arambourgiania philadelphiae cervical V (UJA VF1), dorsal aspect; (G–H) A. lancicollis cervical VI (ZIN PH 147/44) in left lateral (G) and posterior (H) aspect (note especially large neural spine); (I) A. lancicollis cervical VII (ZIN PH 138/44), dorsal aspect; (J) Phosphatodraco cervical VII (OCP DEK/GE 111), left lateral aspect; (K) A. lancicollis cervical VIII (ZIN PH 137/44), dorsal aspect. Abbreviations as for Fig. 2, also with con; condyle; ex, exapophysis; ns, neural spine. (A, D, G–H) and (K) after Averianov (2010); (F) after Frey & Martill (1996); (J) after Suberbiola et al. (2003).
Figure 3. Relationships between azhdarchid cervical vertebrae to cervical III–VII length.
Figure 4. Metrics and cross sections used in estimates of bending strength analysis.
(A) EME 315 in dorsal view showing line of modelled section (dotted line) and projected 300 mm length; (B) UJA VF1 in dorsal view showing line of section and projected 770 mm length (Frey & Martill, 1996); (C) cross section and dimensions of EME 315; (D) cross section of UJA VF1. Note difference in shape and bone wall thicknesses in (C) and (D).
Figure 5. Measured and estimated azhdarchid pterosaur neck lengths against approximate wingspans.
Figure 6. Speculative skeletal reconstructions of Hatzegopteryx sp. and Arambourgiania philadelphiae (estimated wingspans ≥10 m—Frey & Martill, 1996; Buffetaut, Grigorescu & Csiki, 2003) to show discrepancy in neck length alongside a ‘typical’ azhdarchid body plan.
(A) Hatzegopteryx skeleton in lateral aspect; (B) dorsal view of EME 315 and FGGUB R1083 jaw elements, proportionate to actual size, suggesting Hatzegopteryx bore a wide, as well as relatively short, neck construction (soft-tissue outline in black). Jaw width after Buffetaut, Grigorescu & Csiki (2003); (C) reconstructed Arambourgiania philadelphiae cervicals III–VII in lateral aspect; (D) 4.6 m wingspan Q. sp. skeleton in lateral aspect; (E) Q. sp. cervical vertebrae III–V and skull in dorsal view; Note how the neck length of Hatzegopteryx is similar to this much smaller pterosaur. H. thambema holotype (FGGUB R1083) and undescribed referred elements are shown in (A); known elements of A. philadelphiae (UJA JF1) indicated in white shading in (C). Scale bar represents 1 m.
Figure 7. Azhdarchid craniocervical skeleton compared to those of some other tetrapods.
(A) Tanystropheus cf. longobardicus; (B) reconstruction of Zhejiangopterus linhaiensis cervical skeleton, vertebral morphology adapted from Averianov (2010); (C) Giraffa camelopardalis; (D) Camelus dromedarius; (E) Odocoileus virginianus. Note that the mid-series vertebrae of all taxa—even those with highly complex, strongly-muscled neck skeletons—have reduced features compared to those at the posterior and anterior: the fact that azhdarchid mid-series cervicals have reduced features does not necessarily reflect underdeveloped cervical soft-tissues. (A) reconstructed from fossils illustrated by Rieppel et al. (2010); (B) reconstructed from Cai & Wei (1993) and Averianov (2010); (C–E) after Goldfinger (2004). Images not to scale.
Figure 8. Azhdarchid disparity in cranial and limb anatomy.
(A) ZIN PH 112/44, rostral fragment of Azhdarcho lancicollis showing concave dorsal skull margin (after Averianov, 2010); (B) anterior skull and mandible of TMM 42489-2, unnamed azhdarchid from the Javelina Formation, USA; (C) restored skull of Quetzalcoatlus sp. (based on Kellner & Langston Jr, 1996); (D) skull of Zhejiangopterus linhaiensis (based on Cai & Wei, 1993); (E) MOR 69I, Montanazhdarcho minor holotype pectoral girdle and left forelimb (note stunted metacarpal IV); (F) M1323 postcrania of Z. linhaiensis. Abbreviations: car, carpals; cer, cervical vertebrae; cor, coracoid; fem, femur; hum, humerus; mcIV, metacarpal IV; pt, pteroid; rad, radius; tib, tibia; ul, ulna; wpI, wing phalanx I. Scale bars represent 100 mm, except for A (10 mm).
Figure 9. Diversity in predicted life appearance and ecologies for giant azhdarchid pterosaurs.
(A) two giant, long-necked azhdarchids—the Maastrichtian species _Arambourgiania philadelphiae_—argue over a small theropod; (B) the similarly sized but more powerful Maastrichtian, Transylvanian giant azhdarchid pterosaur Hatzegopteryx sp. preys on the rhabdodontid iguanodontian Zalmoxes. Because large predatory theropods are unknown on Late Cretaceous Haţeg Island, giant azhdarchids may have played a key role as terrestrial predators in this community.
Similar articles
- A new azhdarchid pterosaur from the Late Cretaceous of the Transylvanian Basin, Romania: implications for azhdarchid diversity and distribution.
Vremir M, Kellner AW, Naish D, Dyke GJ. Vremir M, et al. PLoS One. 2013;8(1):e54268. doi: 10.1371/journal.pone.0054268. Epub 2013 Jan 30. PLoS One. 2013. PMID: 23382886 Free PMC article. - A reappraisal of azhdarchid pterosaur functional morphology and paleoecology.
Witton MP, Naish D. Witton MP, et al. PLoS One. 2008 May 28;3(5):e2271. doi: 10.1371/journal.pone.0002271. PLoS One. 2008. PMID: 18509539 Free PMC article. - Review of taxonomy, geographic distribution, and paleoenvironments of Azhdarchidae (Pterosauria).
Averianov A. Averianov A. Zookeys. 2014 Aug 11;(432):1-107. doi: 10.3897/zookeys.432.7913. eCollection 2014. Zookeys. 2014. PMID: 25152671 Free PMC article. - Understanding selection for long necks in different taxa.
Wilkinson DM, Ruxton GD. Wilkinson DM, et al. Biol Rev Camb Philos Soc. 2012 Aug;87(3):616-30. doi: 10.1111/j.1469-185X.2011.00212.x. Epub 2011 Dec 16. Biol Rev Camb Philos Soc. 2012. PMID: 22171805 Review. - How the pterosaur got its wings.
Tokita M. Tokita M. Biol Rev Camb Philos Soc. 2015 Nov;90(4):1163-78. doi: 10.1111/brv.12150. Epub 2014 Oct 31. Biol Rev Camb Philos Soc. 2015. PMID: 25361444 Review.
Cited by
- Helically arranged cross struts in azhdarchid pterosaur cervical vertebrae and their biomechanical implications.
Williams CJ, Pani M, Bucchi A, Smith RE, Kao A, Keeble W, Ibrahim N, Martill DM. Williams CJ, et al. iScience. 2021 Apr 14;24(4):102338. doi: 10.1016/j.isci.2021.102338. eCollection 2021 Apr 23. iScience. 2021. PMID: 33997669 Free PMC article. - A new specimen of Sinopterus dongi (Pterosauria, Tapejaridae) from the Jiufotang Formation (Early Cretaceous, China).
Shen C, Pêgas RV, Gao C, Kundrát M, Zhang L, Wei X, Zhou X. Shen C, et al. PeerJ. 2021 Oct 29;9:e12360. doi: 10.7717/peerj.12360. eCollection 2021. PeerJ. 2021. PMID: 34760376 Free PMC article. - Late Maastrichtian pterosaurs from North Africa and mass extinction of Pterosauria at the Cretaceous-Paleogene boundary.
Longrich NR, Martill DM, Andres B. Longrich NR, et al. PLoS Biol. 2018 Mar 13;16(3):e2001663. doi: 10.1371/journal.pbio.2001663. eCollection 2018 Mar. PLoS Biol. 2018. PMID: 29534059 Free PMC article. - Powered flight in hatchling pterosaurs: evidence from wing form and bone strength.
Naish D, Witton MP, Martin-Silverstone E. Naish D, et al. Sci Rep. 2021 Jul 22;11(1):13130. doi: 10.1038/s41598-021-92499-z. Sci Rep. 2021. PMID: 34294737 Free PMC article. - 150 million years of sustained increase in pterosaur flight efficiency.
Venditti C, Baker J, Benton MJ, Meade A, Humphries S. Venditti C, et al. Nature. 2020 Nov;587(7832):83-86. doi: 10.1038/s41586-020-2858-8. Epub 2020 Oct 28. Nature. 2020. PMID: 33116315
References
- Andres B, Ji Q. A new pterosaur from the Liaoning Province of China, the phylogeny of the Pterodactyloidea, and convergence in their cervical vertebrae. Palaeontology. 2008;51:453–469. doi: 10.1111/j.1475-4983.2008.00761.x. - DOI
- Andres B, Myers TS. Lone star pterosaurs. Earth and Environmental Science Transactions of the Royal Society of Edinburgh. 2013;103:383–398.
- Averianov AO. The osteology of Azhdarcho lancicollis (Nessov, 1984) (Pterosauria, Azhdarchidae) from the late Cretaceous of Uzbekistan. Proceedings of the Zoological Institute RAS. 2010;314:264–317.
- Averianov AO. Reconstruction of the neck of Azhdarcho lancicollis and lifestyle of azhdarchids (Pterosauria, Azhdarchidae) Paleontological Journal. 2013;47:203–209. doi: 10.1134/S0031030113020020. - DOI
- Bennett SC. The osteology and functional morphology of the Late Cretaceous pterosaur Pteranodon Part I. General description of osteology. Palaeontographica Abteilung A. 2001;260:1–112.
Grants and funding
The authors received no funding for this work.
LinkOut - more resources
Full Text Sources
Other Literature Sources