SSStttooonnnyyy BBBrrrooooookkk UUUnnniiivvveeerrrsssiiitttyyy The official electronic file of this thesis or dissertation is maintained by the University Libraries on behalf of The Graduate School at Stony Brook University. ©©© AAAllllll RRRiiiggghhhtttsss RRReeessseeerrrvvveeeddd bbbyyy AAAuuuttthhhooorrr... The Semicircular Canals of Birds and Non-Avian Theropod Dinosaurs A Dissertation Presented by Justin Scott Sipla to The Graduate School in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in Anatomical Sciences Stony Brook University August 2007 Stony Brook University The Graduate School Justin Scott Sipla We, the dissertation committee for the above candidate for the Doctor of Philosophy degree, hereby recommend acceptance of this dissertation. Catherine A Forster, Ph.D. – Dissertation Advisor Associate Professor Department of Anatomical Sciences William L. Jungers, Ph.D. – Chairperson of Defense Professor Department of Anatomical Sciences Jack T. Stern, Ph.D. – Dissertation Advisor Professor Department of Anatomical Sciences James M. Clark, Ph.D. – Outside Member Professor Department of Biological Sciences George Washington University This dissertation is accepted by the Graduate School Lawrence Martin Dean of the Graduate School ii Abstract of the Dissertation The Semicircular Canals of Birds and Non-Avian Theropod Dinosaurs by Justin Scott Sipla Doctor of Philosophy in Anatomical Sciences Stony Brook University August 2007 The invasion of aerial habits by primitive birds involved massive reorganization of neurological and sensory systems, many of which are coordinated in the brain by vestibular cues from the semicircular canals. These organs sense angular accelerations experienced by the head and body with every movement. Canal signals are combined with visual and somatosensory inputs and are used to generate a wide-range of reflexive behaviors necessary for stabilizing gaze, maintaining posture, and coordinating body movements. This dissertation focuses on understanding the relationship between locomotor behavior and vestibular function in birds and non-avian theropod dinosaurs, both from a comparative and functional perspective. Widespread use of noninvasive computed tomography (CT) has opened great possibilities for visualizing canal structures, which are often preserved in fossil specimens. The otic capsules of 178 species of extant birds and iii 15 species of non-avian theropods were CT scanned and the vestibular structures reconstructed and measured from digitally prepared volumes. The morphology of the semicircular canals in non-avian theropods and many flightless birds is shown to reflect their status as bipedal cursors, while the pattern seen in volant avians is found to correlate strongly with different flying behaviors. Independent measures of aerobatic maneuverability, such as wing loading, also correlate with canal morphology, demonstrating that, at least in flying birds, larger and thus more sensitive canals are possessed by agile species flying at slower speeds. Freed in air from the need for intermittent contact with a surface substrate, birds can employ a wider repertoire of body movements during locomotion, including forms of rotation that would be improbable on land. In the absence of somatosensory cues from postural interactions with the ground, it is argued that these movements place increased demands on the vestibular system of avian fliers. Investigation into the size and shape of avian semicircular canals permits evaluation of the mode of flight employed by primitive avialans, like Archaeopteryx , shedding light on some of the broader neurophysiological adaptations to flight behavior that characterize bird evolution. iv In preparing this dissertation, my wife Kathryn was a constant support, as in all things. She endured my labors with patience, confidence, and love. This work is dedicated to her. Table of Contents List of Figures............................................................................................................ viii List of Tables............................................................................................................. ix Acknowledgements.................................................................................................... x Introduction................................................................................................................ 1 Chapter 1: Anatomy and function of the vestibular system....................................... 4 1.1. Historical perspective.............................................................................. 4 1.2. Evolution and anatomy of vestibular end organs....................................7 1.2.1. Anatomical organization of the gnathostome labyrinth……............... 9 1.2.2. The otolith organs................................................................................ 11 1.2.3. The semicircular canals........................................................................13 1.2.4. Other vestibular sensors....................................................................... 17 1.3. Transduction of mechanical energy into neural signals.......................... 18 1.3.1. Hair cell types...................................................................................... 21 1.3.2. Afferent signaling and efferent control................................................ 23 1.4. Functional morphology of the semicircular ducts.................................. 25 1.4.1. Basic fluid mechanics.......................................................................... 26 1.4.2. Significance of physical parameters.................................................... 30 1.4.3. Attunement of the canals to the frequency spectra of movements….. 40 1.5. Central processing of vestibular input and canal-mitigated reflexes...... 45 1.5.1. Central processing................................................................................ 46 1.5.2. The vestibuloocular reflex (VOR) and optokinetic reflex (OKR)....... 49 1.5.3. The vestibulospinal reflex (VSR) and vestibulocollic reflex (VCR)... 51 Chapter 2: The biology of flight and vestibular control........................................... 55 2.1. The origin of birds and evolution of avian flight.................................... 57 2.1.1. Birds are theropod dinosaurs............................................................... 59 2.1.2. Extant bird diversity............................................................................. 67 2.1.3. Evolution of the flight stroke............................................................... 70 2.2. The aerodynamics of flapping flight....................................................... 74 2.2.1. Introduction to basic principles............................................................ 75 2.2.2. Patterns of thrust generation in cruising flight..................................... 77 2.2.3. Maneuvering during flight................................................................... 82 2.2.4. Stability and head control during flight............................................... 89 2.2.5. How well could Archaeopteryx fly?.................................................... 92 Chapter 3: Research design........................................................................................ 94 3.1. Goals and predictions.............................................................................. 94 3.1.1. Hypotheses........................................................................................... 99 3.2. Materials and methods............................................................................ 103 3.2.1. Specimens............................................................................................ 103 3.2.2. CT scanning and image processing...................................................... 104 vi 3.2.3. Measurements...................................................................................... 106 3.2.4. Statistical analyses............................................................................... 111 3.2.5. Bonferonni correction.......................................................................... 117 3.2.6. Phylogenetic constraints and “adjusted-N”......................................... 117 Chapter 4: The semicircular canals of birds and relationship to flight...................... 120 4.1. Morphology of the semicircular canals of birds and their ancestors...... 120 4.1.1. The canals of birds............................................................................... 121 4.1.2. The canals of non-avian theropods...................................................... 127 4.2. Canal size variation in birds and non-avian theropod dinosaurs............ 130 4.2.1. Phylogenetic constraints and “adjusted N”.......................................... 132 4.2.2. Allometry of bird and theropod canals................................................ 134 4.2.3. Differential expansion of the canals.................................................... 139 4.2.4. Relationship between semicircular canal size and morphological correlates of flight behavior............................................................... 144 4.3. Discussion............................................................................................... 158 4.3.1. Interspecific variation in canal size...................................................... 161 4.3.2. Canal size and flight behavior.............................................................. 172