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Muscle Function During Swimming and Running in Aquatic, Semi-Aquatic and Cursorial Birds

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Muscle Function During Swimming and Running in Aquatic, Semi-Aquatic and Cursorial Birds Muscle Function During Swimming and Running in Aquatic, Semi-Aquatic and Cursorial Birds A dissertation presented by Jennifer A. Carr To The Department of Biology In partial fulfillment of the requirements for the degree of Doctor of Philosophy in the field of Biology Northeastern University Boston, Massachusetts January 2008 ii Muscle Function During Swimming and Running in Aquatic, Semi-Aquatic and Cursorial Birds A dissertation presented by Jennifer A. Carr ABSTRACT OF DISSERTATION Submitted n partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biology in the Graduate School of Arts and Sciences of Northeastern University, January 2008 iii Abstract The function of large hindlimb muscles with long fascicles and complicated architecture has been studied in many organisms specialized for terrestrial locomotion. Studies of muscle function, energetics and blood flow have allowed a to more accurate determination of which muscles play an important roles during running. One muscle that has been hypothesized to play such a role in birds is the Iliotibialis Lateralis pars Post Acetabularis (ILPO). The ILPO is a large muscle in the hindlimb of cursorial birds, receives a large proportion of the blood flow during running at high speeds, and tends to be reduced or lost in birds that do not employ walking or running as their primary form of locomotion. One of the goals of this study was to comprehensively characterize the function of the ILPO, taking into account the ILPO’s long fascicles that vary in length, the muscle’s complex origin and insertion, and its anatomical variations seen across different bird orders. In order to characterize the ILPO’s function during running, length changes and electrical activity were measured along the posterior fascicle of the ILPO and between the anterior and posterior fascicle of the ILPO in the Helmeted Guinea Fowl (Numida meleagris). These results were compared to those predicted by a moment arm and kinematics model developed in the guinea fowl. To determine how the ILPO functions during other types of locomotion in species that are not specialized for cursorial locomotion, the function of the ILPO was measured during swimming and running in the Common Moorhen (Gallinula chloropus), a bird that employs both swimming and terrestrial forms of locomotion, and the Mallard (Anas platyrhynchus), a bird that – while capable of terrestrial locomotion – locomotes primarily via surface swimming. Finally, iv the function of another muscle was measured in the mallard that, based on blood flow and anatomical studies, appears to play an important role during swimming, the Flexor Cruris Lateralis (FCL). The FCL, like the ILPO, is a large muscle with a complex origin and insertion in cursorial locomotors. However unlike the ILPO this muscle does not appear to be reduced or absent in birds that locomote via swimming: instead it appears to have been significantly modified in birds that employ swimming as a primary form of locomotion. Our results demonstrate that, when active, the ILPO in the guinea fowl experiences similar amounts of length change and has the same average velocity during active lengthening and active shortening between fascicles. It is hypothesized that the varying moment arm at the hip as well as the tendinous aponeurosis play a role in maintaining a uniform amount of active strain among fascicles of different lengths. Along a fascicle, the strain in the ILPO was uniform in the different segments of the posterior ILPO during the active shortening part of the length change cycle and differential strain was found to occur between proximal, central and distal segments during active lengthening, passive lengthening and passive shortening. These proximal to distal differences may be caused by different amounts of length change when the ILPO is being passively shortened followed by compensatory length-tension effects during the period when the ILPO is being actively lengthened. In the common moorhen and mallard, the ILPO’s function during terrestrial locomotion appears to be relatively conserved and a similar strain pattern during cursorial locomotion is observed in all three species. Although the ILPO is active during swimming in both the mallard and the common moorhen, our results suggest that the v ILPO does not play a large functional role during swimming in either species. Our results show that although the ILPO is active in the common moorhen during swimming, it experiences less strain than it does during running. Our measurements of ILPO function in a swimming mallard show that there is a significant decrease in both strain and electrical activity. Finally, there is no significant effect of speed on emg activity of the ILPO during swimming in either the common moorhen or mallard, indicating that although the limb as a whole must produce more work to go faster, it is not producing the extra work needed using the ILPO in either species of swimming birds. Based on our results, the FCL of the mallard appears to function in both terrestrial locomotion and during swimming. During running, the FCL actively shortens during the stance phase, producing positive work which likely counteracts cocontracting knee extensors and driving knee flexion. During swimming the FCL is actively lengthened, and later isometric, for a large portion of the swim cycle. When the FCL is isometric it is possible that the FCL is holding the knee and hip in a flexed position and decreasing the amount of drag on the mallard by increasing the streamlined appearance of the body. This research demonstrates how muscles can function in different types of locomotion and in different species during the same type of locomotion. The variations observed within the ILPO and the FCL in terms of both structure and function demonstrates the importance of muscles functioning to produce positive work and demonstrates how muscles play an important role in stability during both swimming and running either by remaining isometric or by being lengthened while active. vi Acknowledgements I would like to begin by acknowledging my advisor Dr. Richard Marsh, without his support and knowledge these experiments would not have been possible, through his guidance I have become a better scientist and a better teacher. I would like to thank my committee members Gwilym Jones, Fred Davis, Rebeca Rosengaus and Thomas Roberts who have always been available for assistance, for moral support and encouragement. This dissertation would not have been possible without the support of my coworkers in the lab both past and present who assisted with surgeries, bird care and experiments including David Ellerby, Jonas Rubenson, Havalee Henry, Thomas Hoogendyk, Gwenn Catterfeld, Rosemary Truong, Amanda Flynn, Jade McPherson and Matthew Propert. I would like to thank my family and friends who have been there supporting me throughout my thesis project especially my mom who made me go back to school, Kris Severi, Jessica Gonyor and Nathan McDaniel. Finally I would like to thank the person who was an invaluable source of love and support my husband Francis (Igor) Carr, who helped me deal with both the joys and frustrations associated with this project and kept me focused on what was important in life. vii Table of Contents Table of Contents Abstract iii Acknowledgements vi Table of Contents vii List of Abbreviations xiii List of Figures xiv Chapter 1 Differential Strain in an Active Muscle During Locomotion I. Introduction 1 II. Materials and Methods A. Animals and Training 4 B. Muscle Architecture 4 C. Surgery 5 D. Recordings 6 E. Videography 6 F. Myofilament Length and Length-Tension Curve 7 G. Sarcomere Measurements 8 H. Length and Velocity Changes 9 I. Statistical Analysis 11 III. Results viii A. Length Changes 13 B. Velocity Changes 14 C. Electromyography 14 D. Predicted Sarcomere Operating Lengths 15 IV. Discussion A. Length Changes and Electrical Activity in the ILPO 16 B. Alternative Hypothesis for Differential Strain 17 C. Length Tension Effects 19 D. Summary 20 V. Literature Cited 22 Chapter 2 Compensatory Mechanisms in a Muscle with Varying Moment Arms I. Introduction 33 II. Materials and Methods A. Animals and Training 39 B. Moment Arm Measurements 39 C. Statistical Analysis 41 III. Results ix A. Length and Velocity Changes 43 B. Moment Arm Measurements 43 C. Calculated vs. Experimental Length Changes 44 IV. Discussion 46 VI. Literature Cited 51 Chapter 3 Iliotibialis Lateralis pars Post Acetabularis (ILPO) Function in Helmeted Guinea Fowl (Numida meleagris) I. Introduction 62 II. Materials and Methods A. Animals and Training 66 B. Sonomicrometry and Electromyography 66 C. Recordings 67 D. Videography 68 E. Sarcomere Measurements 69 F. Length and Velocity Changes 70 G. Blood Flow versus Emg Measurements 72 H. Statistical Analysis 73 III. Results x A: Muscle Length Change 74 B. Velocity Changes as a Function of Speed and Incline 75 C. Sarcomere Measurements 75 D. Electrical Activity 76 E. Blood Flow versus Emg Comparison 76 IV. Discussion A. Function of Active Lengthening in the ILPO 79 B. Function of the ILPO During Active Shortening 82 C. Length Tension Effects 82 D. Emg Analysis versus Blood Flow 84 E. Summary 84 V. Literature Cited 86 Chapter 4: Iliotibialis Lateralis pars Post Acetabularis (ILPO) Function During Swimming and Running in an Aquatic and Semi-Aquatic Bird Species I. Introduction 105 II. Materials and Methods A. Animals and Training 110 B. Surgery 111 xi C. Recordings 112 D. Videography 112 E. Sarcomere Measurements 113 F. Length Changes 115 G. Statistical Analysis 119 III. Results A. ILPO Length Changes During Running & Swimming 120 B. ILPO Electrical Activity During Running & Swimming 122 IV. Discussion A. ILPO Function During Running 125 B. Length and Electrical Activity Changes During Swimming 127 C. Conclusion 129 V. Literature Cited 131 Chapter 5: A Swimming Muscle with a Novel Function I. Introduction 146 II. Materials and Methods A.
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