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      Mechanical analysis of avian feet: multiarticular muscles in grasping and perching

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          Abstract

          The grasping capability of birds' feet is a hallmark of their evolution, but the mechanics of avian foot function are not well understood. Two evolutionary trends that contribute to the mechanical complexity of the avian foot are the variation in the relative lengths of the phalanges and the subdivision and variation of the digital flexor musculature observed among taxa. We modelled the grasping behaviour of a simplified bird foot in response to the downward and upward forces imparted by carrying and perching tasks, respectively. Specifically, we compared the performance of various foot geometries performing these tasks when actuated by distally inserted flexors only, versus by both distally inserted and proximally inserted flexors. Our analysis demonstrates that most species possess relative phalanx lengths that are conducive to grasps actuated only by a single distally inserted tendon per digit. Furthermore, proximally inserted flexors are often required during perching, but the distally inserted flexors are sufficient when grasping and carrying objects. These results are reflected in differences in the relative development of proximally and distally inserted digital flexor musculature among ‘perching’ and ‘grasping’ taxa. Thus, our results shed light on the relative roles of variation in phalanx length and digit flexor muscle distribution in an integrative, mechanical context.

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          Most cited references18

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          Many-to-One Mapping of Form to Function: A General Principle in Organismal Design?

          We introduce the concept of many-to-one mapping of form to function and suggest that this emergent property of complex systems promotes the evolution of physiological diversity. Our work has focused on a 4-bar linkage found in labrid fish jaws that transmits muscular force and motion from the lower jaw to skeletal elements in the upper jaws. Many different 4-bar shapes produce the same amount of output rotation in the upper jaw per degree of lower jaw rotation, a mechanical property termed Maxillary KT. We illustrate three consequences of many-to-one mapping of 4-bar shape to Maxillary KT. First, many-to-one mapping can partially decouple morphological and mechanical diversity within clades. We found with simulations of 4-bars evolving on phylogenies of 500 taxa that morphological and mechanical diversity were only loosely correlated (R(2) = 0.25). Second, redundant mapping permits the simultaneous optimization of more than one mechanical property of the 4-bar. Labrid fishes have capitalized on this flexibility, as illustrated by several species that have Maxillary KT = 0.8 but have different values of a second property, Nasal KT. Finally, many-to-one mapping may increase the influence of historical factors in determining the evolution of morphology. Using a genetic model of 4-bar evolution we exerted convergent selection on three different starting 4-bar shapes and found that mechanical convergence only created morphological convergence in simulations where the starting forms were similar. Many-to-one mapping is widespread in physiological systems and operates at levels ranging from the redundant mapping of genotypes to phenotypes, up to the morphological basis of whole-organism performance. This phenomenon may be involved in the uneven distribution of functional diversity seen among animal lineages.
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            Skeletal muscle design to meet functional demands.

            Skeletal muscles are length- and velocity-sensitive force producers, constructed of a vast array of sarcomeres. Muscles come in a variety of sizes and shapes to accomplish a wide variety of tasks. How does muscle design match task performance? In this review, we outline muscle's basic properties and strategies that are used to produce movement. Several examples are provided, primarily for human muscles, in which skeletal muscle architecture and moment arms are tailored to a particular performance requirement. In addition, the concept that muscles may have a preferred sarcomere length operating range is also introduced. Taken together, the case is made that muscles can be fine-tuned to perform specific tasks that require actuators with a wide range of properties.
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              Muscle and tendon contributions to force, work, and elastic energy savings: a comparative perspective.

              Muscle-tendon architecture underlies muscle function. Whereas muscles generally contribute most to mechanical work, tendons provide the majority of elastic energy savings. Isometric or eccentric contractions enhance force and further reduce energy cost. However, elastic savings is probably constrained by the need to reduce compliance for accurate control of position.
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                Author and article information

                Journal
                R Soc Open Sci
                R Soc Open Sci
                RSOS
                royopensci
                Royal Society Open Science
                The Royal Society Publishing
                2054-5703
                February 2015
                25 February 2015
                25 February 2015
                : 2
                : 2
                : 140350
                Affiliations
                [1 ]Department of Mechanical Engineering and Materials Science, Yale University , New Haven, CT 06511, USA
                [2 ]Department of Ecology and Evolutionary Biology, Brown University , Providence, RI 02917, USA
                Author notes
                Author for correspondence: Spencer B. Backus e-mail: spencer.backus@ 123456yale.edu
                Article
                rsos140350
                10.1098/rsos.140350
                4448815
                26064598
                997b6f75-4fae-4262-9183-3d41b2b8ff54
                © 2015 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : 3 October 2014
                : 4 February 2015
                Categories
                1001
                1004
                164
                25
                Biology (Whole Organism)
                Custom metadata
                February, 2015

                birds,grasping,foot morphology,underactuated mechanisms,digit flexors

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