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      In Vivo Time-Resolved Microtomography Reveals the Mechanics of the Blowfly Flight Motor

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Time-resolved X-ray microtomography permits a real-time view of the blowfly in flight at a previously unprecedented level of detail, revealing how the tiny steering muscles work.

          Abstract

          Dipteran flies are amongst the smallest and most agile of flying animals. Their wings are driven indirectly by large power muscles, which cause cyclical deformations of the thorax that are amplified through the intricate wing hinge. Asymmetric flight manoeuvres are controlled by 13 pairs of steering muscles acting directly on the wing articulations. Collectively the steering muscles account for <3% of total flight muscle mass, raising the question of how they can modulate the vastly greater output of the power muscles during manoeuvres. Here we present the results of a synchrotron-based study performing micrometre-resolution, time-resolved microtomography on the 145 Hz wingbeat of blowflies. These data represent the first four-dimensional visualizations of an organism's internal movements on sub-millisecond and micrometre scales. This technique allows us to visualize and measure the three-dimensional movements of five of the largest steering muscles, and to place these in the context of the deforming thoracic mechanism that the muscles actuate. Our visualizations show that the steering muscles operate through a diverse range of nonlinear mechanisms, revealing several unexpected features that could not have been identified using any other technique. The tendons of some steering muscles buckle on every wingbeat to accommodate high amplitude movements of the wing hinge. Other steering muscles absorb kinetic energy from an oscillating control linkage, which rotates at low wingbeat amplitude but translates at high wingbeat amplitude. Kinetic energy is distributed differently in these two modes of oscillation, which may play a role in asymmetric power management during flight control. Structural flexibility is known to be important to the aerodynamic efficiency of insect wings, and to the function of their indirect power muscles. We show that it is integral also to the operation of the steering muscles, and so to the functional flexibility of the insect flight motor.

          Author Summary

          A blowfly's wingbeat is 50 times shorter than a blink of a human eye, and is controlled by numerous tiny steering muscles—some of which are as thin as a human hair. To visualize the movements of these muscles and the deformations of the surrounding exoskeleton, we developed a technique to allow us to look inside the insects during tethered flight. We used a particle accelerator to record high-speed X-ray images of the flying blowflies, which we used to reconstruct three-dimensional tomograms of their flight motor at ten different stages of the wingbeat. We measured the asymmetric movements of the steering muscles associated with turning flight, together with the accompanying movements of the wing hinge—arguably the most complex joint in nature. The steering muscles represent <3% of total flight muscle mass, so a key question has been how they can modulate the output of the much larger power muscles. We show that by shifting the flight motor between different modes of oscillation, the fly is able to divert mechanical energy into a steering muscle that is specialized to absorb mechanical energy. In general, we find that deformations of the muscles and thorax are key to understanding this remarkable mechanism.

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          Most cited references 25

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          Wing rotation and the aerodynamic basis of insect flight.

          The enhanced aerodynamic performance of insects results from an interaction of three distinct yet interactive mechanisms: delayed stall, rotational circulation, and wake capture. Delayed stall functions during the translational portions of the stroke, when the wings sweep through the air with a large angle of attack. In contrast, rotational circulation and wake capture generate aerodynamic forces during stroke reversals, when the wings rapidly rotate and change direction. In addition to contributing to the lift required to keep an insect aloft, these two rotational mechanisms provide a potent means by which the animal can modulate the direction and magnitude of flight forces during steering maneuvers. A comprehensive theory incorporating both translational and rotational mechanisms may explain the diverse patterns of wing motion displayed by different species of insects.
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            How animals move: an integrative view.

            Recent advances in integrative studies of locomotion have revealed several general principles. Energy storage and exchange mechanisms discovered in walking and running bipeds apply to multilegged locomotion and even to flying and swimming. Nonpropulsive lateral forces can be sizable, but they may benefit stability, maneuverability, or other criteria that become apparent in natural environments. Locomotor control systems combine rapid mechanical preflexes with multimodal sensory feedback and feedforward commands. Muscles have a surprising variety of functions in locomotion, serving as motors, brakes, springs, and struts. Integrative approaches reveal not only how each component within a locomotor system operates but how they function as a collective whole.
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              Muscular force in running turkeys: the economy of minimizing work.

              During running, muscles and tendons must absorb and release mechanical work to maintain the cyclic movements of the body and limbs, while also providing enough force to support the weight of the body. Direct measurements of force and fiber length in the lateral gastrocnemius muscle of running turkeys revealed that the stretch and recoil of tendon and muscle springs supply mechanical work while active muscle fibers produce high forces. During level running, the active muscle shortens little and performs little work but provides the force necessary to support body weight economically. Running economy is improved by muscles that act as active struts rather than working machines.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                March 2014
                25 March 2014
                : 12
                : 3
                Affiliations
                [1 ]Department of Zoology, University of Oxford, Oxford, United Kingdom
                [2 ]Department of Bioengineering, Imperial College London, London, United Kingdom
                [3 ]Swiss Light Source, Paul Scherrer Institute, Villigen, Switzerland
                [4 ]Department of Comparative Biomedical Sciences, The Royal Veterinary College, London, United Kingdom
                [5 ]Institute for Biomedical Engineering, ETH Zurich and University of Zurich, Switzerland
                Lund University, Sweden
                Author notes

                The authors have declared that no competing interests exist.

                The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: DAS RM MS SMW HGK GKT. Performed the experiments: SMW DAS RM MW TM MD HGK GKT. Analyzed the data: SMW DAS RM GKT. Contributed reagents/materials/analysis tools: DAS MS RM HGK SMW GKT. Wrote the paper: SMW GKT.

                Article
                PBIOLOGY-D-13-04259
                10.1371/journal.pbio.1001823
                3965381

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Pages: 12
                Funding
                The research leading to these results has received funding from the European Community's Seventh Framework Programme (FP7/2007-2013) under grant agreement no. 226716, and from the European Research Council under the European Community's Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement no. 204513 to GKT. The instrumentation was supported through PSI FOKO grants (proposals #20100810 and #20110908) to HGK. SMW is supported by a Royal Society University Research Fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Anatomy
                Nervous System
                Motor System
                Musculoskeletal System
                Biomechanics
                Biological Locomotion
                Flight Mechanics (Biology)
                Bone and Joint Mechanics
                Biophysics
                Biotechnology
                Bioengineering
                Bionics
                Biomaterials
                Neuroscience
                Systems Biology
                Zoology
                Animal Physiology
                Entomology
                Engineering and Technology
                Physical Sciences
                Materials Science
                Physics
                Electromagnetic Radiation
                X-Radiation

                Life sciences

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