The Mechanics of Terrestrial Locomotion and the Function and Evolutionary History Of
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The Mechanics of Terrestrial Locomotion and the Function and Evolutionary History of Head-bobbing in Birds A dissertation presented to the faculty of the College of Arts and Sciences of Ohio University In partial fulfillment of the requirements for the degree Doctor of Philosophy Jennifer Ann Hancock August 2010 © 2010 Jennifer Ann Hancock. All Rights Reserved. 2 This dissertation titled The Mechanics of Terrestrial Locomotion and the Function and Evolutionary History of Head-bobbing in Birds by JENNIFER ANN HANCOCK has been approved for the Department of Biological Sciences and the College of Arts and Sciences by ___________________________________________ Audrone R. Biknevicius Associate Professor of Biomedical Sciences ___________________________________________ Benjamin M. Ogles Dean, College of Arts and Sciences 3 ABSTRACT Hancock, Jennifer Ann, Ph.D., August 2010, Biological Sciences The Mechanics of Terrestrial Locomotion and the Function and Evolutionary History of Head-bobbing in Birds (194 pp.) Director of Dissertation: Audrone R. Biknevicius Head-bobbing is the fore-aft movement of the head exhibited by some birds during terrestrial locomotion. It is primarily considered to be a response to enhance vision. This has led some researchers to hypothesize that head-bobbing should be found in birds that are visual foragers and may be correlated with the morphology of the retina. In contrast, other researchers suggest that head-bobbing is mechanically linked to the locomotor system and that its visual functions are secondarily adapted. This dissertation explored the mechanics of terrestrial locomotion and head- bobbing of birds in both the lab and field. In the lab, the kinetics and kinematics of terrestrial locomotion in the Elegant Crested Tinamous (Eudromia elegans) were analyzed using high-speed videography and ground reaction forces. In the field, the kinematics of the terrestrial locomotion of charadriiform birds were analyzed using high- speed videography. These biodynamic studies found that birds have two distinct locomotor transitions. The first transition occurs as they move from vaulting mechanics to bouncing mechanics, and the second transition occurs when they incorporate an aerial phase during running. Thus, many birds use grounded running during intermediate speeds. Also, this study found in general that head and neck movements are coordinated with limb 4 movements during terrestrial locomotion in charadriiform birds, but were not coordinated in the Elegant-crested Tinamou. Thus, the coordination is neither perfect nor obligatory. Additionally, the evolutionary histories of retinal morphology, head-bobbing and foraging type in birds were investigated through a comprehensive review of avian literature. The data were compiled and mapped onto a composite avian phylogeny. Then, the correlation of characters was analyzed using pairwise comparisons. This study found that a nasal unifoveate retina with a band-shaped area centralis, non-head-bobbing and visual foraging appear to be the ancestral character states for birds. Additionally, there were no significant correlations between head movement, retinal pattern or foraging mode. Although some general trends were observed, most were within clades and, thus, a result of the independent evolutionary history of head movement, retinal pattern or foraging mode. Approved: _____________________________________________________________ Audrone R. Biknevicius Associate Professor of Biomedical Sciences 5 ACKNOWLEDGMENTS I would like to thank my advisor, Audrone R. Biknevicius, for all of her guidance, support and revisions. I also thank my dissertation committee members, Donald B. Miles, Patrick M. O’Connor, Nancy J. Stevens and Nancy E. Tatarek, for the comments and support. I also thank Kay Earls for her assistance in data collection and LabVIEW programming; Josh Hill, Emily Bevis, Ozan Sauer, Kristin Stover and Jessica Freimark who also assisted in data collection and analysis; and the Ohio University Evolutionary Morphology Group, especially Steve Reilly, Eric McElroy and Andy Lammers (now at Cleveland State University) for discussions and support. Financial support was provided by National Science Foundation (IBN 0080158 to S. M. Reilly and A.R.B.), Sigma Xi, Joseph Grinnell Student Research Award and the Ohio University College of Medicine Direct Grant. 6 TABLE OF CONTENTS Page Abstract............................................................................................................................... 3 Acknowledgments............................................................................................................... 5 List of Tables ...................................................................................................................... 7 List of Figures..................................................................................................................... 8 Chapter 1: Introduction..................................................................................................... 11 Chapter 2: Whole-body mechanics and kinematics of terrestrial locomotion in the Elegant-crested Tinamou (Eudromia elegans) ................................................................. 19 Chapter 3: The effect of head-bobbing on terrestrial locomotion of birds: A case study of the Elegant-crested Tinamou (Eudromia elegans) ........................................................... 41 Chapter 4: The mechanics of locomotion and head-bobbing in charadriiform birds ....... 67 Chapter 5: The evolution of retinal morphology in birds ................................................. 91 Chapter 6: head-bobbing, retinal morphology and foraging in birds............................. 121 Chapter 7: Conclusions and Future Directions ............................................................... 171 References....................................................................................................................... 179 7 LIST OF TABLES Page Table 2-1: Center of mass mechanics and footfall parameters in Tinamous .................36 Table 3-1: Relative durations between locomotor events and head-bobbing events in Tinamous.........................................................................................................................58 Table 4-1: Numbers of individuals and strides, presence or absence of head-bobbing and foraging ecology in charadriiform species .....................................................................80 Table 4-2: Results for the least squares regressions of log 10 stance and stride duration versus log 10 speed ...........................................................................................................81 Table 5-1: The retinal patterns in birds.........................................................................107 Table 6-1: The retinal patterns, head movements and foraging types in birds.............143 8 LIST OF FIGURES Page Figure 1-1: Diagram of a head-bob..................................................................................16 Figure 1-2: The refraction of light by the fovea ..............................................................17 Figure 1-3: The different retinal configurations of the fundus oculi of birds..................18 Figure 2-1: External mechanical energy profiles for representative Tinamous trials......37 Figure 2-2: Graphs of phase shift, duty factor and energy recovery in Tinamous ..........38 Figure 2-3: Video images of a tinamou utilizing grounded running locomotion ............39 Figure 2-4: Graphs of peak vertical force, relative stride length and stride frequency in Tinamous ..................................................................................................40 Figure 3-1: Sagittal movements of the head relative to stance phases of the feet in a walking pigeon..............................................................................................59 Figure 3-2: The hypothesized effect of footfalls and head-bobbing on the pitching of the torso.........................................................................................................60 Figure 3-3: Graphs of relative hold phase, relative duration from liftoff to the beginning of hold phase and relative duration of touchdown to the beginning of thrust phase in Tinamous.........................................................61 Figure 3-4: Ground reaction forces and torso pitch in four representative trials of Tinamous.......................................................................................................62 Figure 3-5: Stance duration of hold versus thrust steps in Tinamous..............................63 Figure 3-6: Relative times of peak vertical force and fore-aft transition in hold versus thrust steps in Tinamous ....................................................................64 Figure 3-7: Phase shift and mechanical energy recovery for hold versus thrust steps in Tinamous. .................................................................................................65 Figure 3-8: A diagram of COM movement during pitching of the torso.........................66 Figure 4-1: A phylogeny of Charadriiformes indicating head-bobbing and non-head- bobbing species ............................................................................................82 Figure 4-2: Relative hold phase as a function of speed ...................................................83 9 Figure 4-3: The relative duration from liftoff to the beginning of hold phase