Inner ear anatomy is a proxy for deducing auditory capability and behaviour in reptiles and birds

Inferences of hearing capabilities and audition-related behaviours in extinct reptiles and birds have previously been based on comparing cochlear duct dimensions with those of living species. However, the relationship between inner-ear bony anatomy and hearing ability or vocalization has never been tested rigorously in extant or fossil taxa. Here, micro-computed tomographic analysis is used to investigate whether simple endosseous cochlear duct (ECD) measurements can be fitted to models of hearing sensitivity, vocalization, sociality and environmental preference in 59 extant reptile and bird species, selected based on their vocalization ability. Length, rostrocaudal/mediolateral width and volume measurements were taken from ECD virtual endocasts and scaled to basicranial length. Multiple regression of these data with measures of hearing sensitivity, vocal complexity, sociality and environmental preference recovered positive correlations between ECD length and hearing range/mean frequency, vocal complexity, the behavioural traits of pair bonding and living in large aggregations, and a negative correlation between ECD length/rostrocaudal width and aquatic environments. No other dimensions correlated with these variables. Our results suggest that ECD length can be used to predict mean hearing frequency and range in fossil taxa, and that this measure may also predict vocal complexity and large group sociality given comprehensive datasets.

[1]  Avian-like attributes of a virtual brain model of the oviraptorid theropod Conchoraptor gracilis , 2007, Naturwissenschaften.

[2]  E. Kalisińska.  Anseriform Brain and Its Parts versus Taxonomic and Ecological Categories , 2005, Brain, Behavior and Evolution.

[3]  E. Wever,et al.  The reptile ear : its structure and function. , 1978 .

[4]  S. M. Dunn,et al.  National Research Council of Canada , 1998 .

[5]  S. Walsh,et al.  Avian brain evolution: new data from Palaeogene birds (Lower Eocene) from England , 2009 .

[6]  L. T. Evans.  The development of the cochlea in the gecko, with special reference to the cochlea‐lagena ratio and its bearing on vocality and social behavior , 1936 .

[7]  J. W. Lang,et al.  Social Signals and Behaviors of Adult Alligators and Crocodiles , 1977 .

[8]  D. Blumstein,et al.  Does Sociality Drive The Evolution Of Communicative Complexity? A Comparative Test With Ground‐Dwelling Sciurid Alarm Calls , 1997, The American Naturalist.

[9]  Geoffrey A. Manley,et al.  Audiogram, body mass, and basilar papilla length: correlations in birds and predictions for extinct archosaurs , 2005, Naturwissenschaften.

[10]  P. D. Manley,et al.  Peripheral Hearing Mechanisms in Reptiles and Birds , 1990, Zoophysiology.

[11]  M. John,et al.  Structure of the brain cavity and inner ear of the centrosaurine ceratopsid dinosaur Pachyrhinosaurus based on CT scanning and 3 D visualization , 2008 .

[12]  Paul C. Sereno,et al.  Structural Extremes in a Cretaceous Dinosaur , 2007, PloS one.

[13]  J. Endler.  Signals, Signal Conditions, and the Direction of Evolution , 1992, The American Naturalist.

[14]  D. R. Wylie,et al.  Relative Wulst volume is correlated with orbit orientation and binocular visual field in birds , 2008, Journal of Comparative Physiology A.

[15]  A. Feng,et al.  Old world frog and bird vocalizations contain prominent ultrasonic harmonics. , 2004, The Journal of the Acoustical Society of America.

[16]  B. Kempenaers,et al.  Avian olfactory receptor gene repertoires: evidence for a well-developed sense of smell in birds? , 2008, Proceedings of the Royal Society B: Biological Sciences.

[17]  L. Witmer,et al.  Using CT to Peer into the Past: 3D Visualization of the Brain and Ear Regions of Birds, Crocodiles, and Nonavian Dinosaurs , 2008 .

[18]  M. Konishi.  Comparative neurophysiological studies of hearing and vocalizations in songbirds , 1970, Zeitschrift für vergleichende Physiologie.

[19]  L. Witmer,et al.  CRANIOFACIAL ANATOMY OF MAJUNGASAURUS CRENATISSIMUS (THEROPODA: ABELISAURIDAE) FROM THE LATE CRETACEOUS OF MADAGASCAR , 2007 .

[20]  T. Rowe,et al.  The avian nature of the brain and inner ear of Archaeopteryx , 2004, Nature.

[21]  S. Rogers,et al.  Exploring Dinosaur Neuropaleobiology Computed Tomography Scanning and Analysis of an Allosaurus fragilis Endocast , 1998, Neuron.

[22]  Sankar Chatterjee,et al.  Neuroanatomy of flying reptiles and implications for flight, posture and behaviour , 2003, Nature.

[23]  Charles H. Brown,et al.  Hearing and communication in blue monkeys (Cercopithecus mitis) , 1984, Animal Behaviour.

[24]  D. Weishampel.  Acoustic analyses of potential vocalization in lambeosaurine dinosaurs (Reptilia: Ornithischia) , 1981, Paleobiology.

[25]  J. L. Gittleman,et al.  Carnivore olfactory bulb size allometry phylogeny and ecology , 1991 .

[26]  G. Manley.  A REVIEW OF SOME CURRENT CONCEPTS OF THE FUNCTIONAL EVOLUTION OF THE EAR IN TERRESTRIAL VERTEBRATES , 1972, Evolution; international journal of organic evolution.

[27]  A H Clarke,et al.  On the vestibular labyrinth of Brachiosaurus brancai. , 2005, Journal of vestibular research : equilibrium & orientation.

[28]  P. Galton,et al.  Braincase of Enaliornis, an Early Cretaceous bird from England , 1991 .

[29]  David K. Smith,et al.  The endocranium of the theropod dinosaur Ceratosaurus studied with computed tomography , 2005 .

[30]  P. Currie,et al.  A New Horned Dinosaur from an Upper Cretaceous Bone Bed in Alberta , 2008 .

[31]  Kevin Padian,et al.  The origin and early evolution of birds , 1998 .