Neuroanatomy of flying reptiles and implications for flight, posture and behaviour

Abstract

Comparison of birds and pterosaurs, the two archosaurian flyers, sheds light on adaptation to an aerial lifestyle. The neurological basis of control holds particular interest in that flight demands on sensory integration, equilibrium, and muscular coordination are acute1,2,3,4,5,6,7,8. Here we compare the brain and vestibular apparatus in two pterosaurs based on high-resolution computed tomographic (CT) scans from which we constructed digital endocasts. Although general neural organization resembles birds, pterosaurs had smaller brains relative to body mass than do birds. This difference probably has more to do with phylogeny than flight, in that birds evolved from nonavian theropods that had already established trends for greater encephalization5,9. Orientation of the osseous labyrinth relative to the long axis of the skull was different in these two pterosaur species, suggesting very different head postures and reflecting differing behaviours. Their enlarged semicircular canals reflect a highly refined organ of equilibrium, which is concordant with pterosaurs being visually based, aerial predators. Their enormous cerebellar floccular lobes may suggest neural integration of extensive sensory information from the wing, further enhancing eye- and neck-based reflex mechanisms for stabilizing gaze.

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Figure 1: Relationships and skulls of pterosaur taxa.
Figure 2: Endocasts and labyrinths of pterosaurs compared to brains of extant archosaurs.
Figure 3: Relative brain size in pterosaurs compared to birds and other reptiles.
Figure 4: Skull and head postures of pterosaurs.

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Acknowledgements

D. S. Berman (Carnegie Museum of Natural History) and J. Maisey (American Museum of Natural History) agreed to the loan and preparation of the pterosaur specimens. M. Atanassov assisted with body mass estimates and other morphometrics. Z. Zheng acid-prepared the fossils. M. Colbert, J. Humphries, R. Ketcham, and J. Maisano assisted with the CT scanning, data processing, and web delivery. Figures were drafted by R. Ridgely (Figs 2 and 3a, c) and K. McQuilkin (Fig. 3b, d, e and Fig. 4). We thank G. R. Hurlburt and D. S. Wharton for sharing data in their doctoral dissertations. We thank G. R. Hurlburt, P. M. O'Connor, E. Weber, and D. S. Wharton for fruitful discussion of pterosaurs and neuroscience, and R. J. Templin for providing aerodynamic expertise. The manuscript benefited from comments provided by D. M. Unwin & S. C. Bennett. Funding was provided by NSF grants to L.M.W. and T.R. and by Texas Tech University to S.C.

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Correspondence to Lawrence M. Witmer.

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Supplementary information

Supplementary Movie: Anhan_waxspin.mov: QuickTime movie of reconstructed skull spinning axially around a longitudinal axis (MOV 1872 kb)

Supplementary Movie: Anhan_whorspin.mov: QuickTime movie of reconstructed skull spinning horizontally around a vertical axis (MOV 1782 kb)

Supplementary Movie: Anhan_wsagspin.mov: QuickTime movie of reconstructed skull spinning sagittally around a transverse axis (MOV 1770 kb)

Supplementary Movie: Anhan_transv_slices.mov: QuickTime movie of serial transverse CT slices (MOV 2061 kb)

Supplementary Movie: Anhan_horiz_slices.mov: QuickTime movie of serial horizontal CT slices (MOV 1875 kb)

Supplementary Movie: Anhan_sag_slices.mov: QuickTime movie of serial sagittal CT slices (MOV 1756 kb)

Supplementary Movie: Anhan_RollSpinEndocast.mov: QuickTime movie of reconstructed endocast spinning horizontally around a vertical axis (MOV 561 kb)

Supplementary Movie: Anhan_YawSpinEndocast.mov: QuickTime movie of reconstructed endocast spinning axially around a longitudinal axis (MOV 722 kb)

Supplementary Movie: Rhamph_RollSpinHeadSkel.mov: QuickTime movie of reconstructed skull spinning axially around a longitudinal axis (MOV 1290 kb)

Supplementary Movie: Rhamph_YawSpinHeadSkel.mov: QuickTime movie of reconstructed skull spinning horizontally around a vertical axis (MOV 719 kb)

Supplementary Movie: Rhamph_PitchSpinHeadSkel.mov: QuickTime movie of reconstructed skull spinning sagittally around a transverse axis (MOV 1006 kb)

Supplementary Movie: Rhamph_transv_slices.mov: QuickTime movie of serial transverse CT slices (MOV 3625 kb)

Supplementary Movie: Rhamph_hor_slices.mov: QuickTime movie of serial horizontal CT slices (MOV 1198 kb)

Supplementary Movie: Rhamph_sag_slices.mov: QuickTime movie of serial sagittal CT slices (MOV 1215 kb)

Supplementary Movie: Rhamph_YawSpinEndocast.mov: QuickTime movie of reconstructed endocast spinning horizontally around a vertical axis (MOV 661 kb)

Supplementary Movie: Rhamph_RollSpinEndocast.mov: QuickTime movie of reconstructed endocast spinning axially around a longitudinal axis (MOV 929 kb)

Supplementary Movie legends (DOC 23 kb)

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Witmer, L., Chatterjee, S., Franzosa, J. et al. Neuroanatomy of flying reptiles and implications for flight, posture and behaviour. Nature 425, 950–953 (2003). https://doi.org/10.1038/nature02048

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