Spring or string: does tendon elastic action influence wing muscle mechanics in bat flight?

Abstract

Tendon springs influence locomotor movements in many terrestrial animals, but their roles in locomotion through fluids as well as in small-bodied mammals are less clear. We measured muscle, tendon and joint mechanics in an elbow extensor of a small fruit bat during ascending flight. At the end of downstroke, the tendon was stretched by elbow flexion as the wing was folded. At the end of upstroke, elastic energy was recovered via tendon recoil and extended the elbow, contributing to unfurling the wing for downstroke. Compared with a hypothetical 'string-like' system lacking series elastic compliance, the tendon spring conferred a 22.5% decrease in muscle fascicle strain magnitude. Our findings demonstrate tendon elastic action in a small flying mammal and expand our understanding of the occurrence and action of series elastic actuator mechanisms in fluid-based locomotion.

Validation of XMALab software for marker-based XROMM

“…Indeed, many studies have used XrayProject and obtained precision better than 0.1 mm (e.g. Camp and Brainerd, 2015;Dawson et al, 2011;Gidmark et al, 2012;Konow et al, 2015). Despite this difference in user effort, the comparison is a good test for XMALab because it shows high precision and repeatability (see below) with XMALab, even for a tutorial dataset when users are novices and are not putting extra effort into data refinement.…”

“…The result is a precise and accurate XROMM animation of 3D bone meshes moving in 3D space (Brainerd et al, 2010;Gatesy et al, 2010). Over the past 8 years, researchers have used XROMM to study in vivo skeletal motion in numerous behaviors and species including: terrestrial locomotion of alligators , dogs (Wachs et al, 2016), rats (Bonnan et al, 2016) and birds (Kambic et al, 2014(Kambic et al, , 2015; arboreal locomotion of sloths (Nyakatura and Fischer, 2010); jumping in frogs (Astley and Roberts, 2012) and humans (Miranda et al, 2013); feeding in pigs (Menegaz et al, 2015), ducks (Dawson et al, 2011), geckos (Montuelle and Williams, 2015) and fish (Camp and Brainerd, 2015;Gidmark et al, 2012); flight in bats (Konow et al, 2015) and birds Heers et al, 2016;Heers and Dial, 2012); lung ventilation in iguanas ; and trackway formation in theropod dinosaurs (Falkingham and Gatesy, 2014). Methods include marker-based XROMM, in which radio-opaque markers are surgically implanted into skeletal elements (Brainerd et al, 2010;Tashman and Anderst, 2003), and markerless XROMM, which includes manual scientific rotoscoping and semi-automated bone model registration methods (Banks and Hodge, 1996;Miranda et al, 2011;You et al, 2001).…”

Dynamic Musculoskeletal Functional Morphology: Integrating diceCT and XROMM

“…However, controlled eccentric activity immediately prior to shortening, termed a stretch‐shortening cycle (SSC) or countermovement, increases shortening force (Abbott and Aubert, ; Cavagna et al, ; Cavagna and Citterio, ; Gregor et al, ; Finni et al, 2000). An abundance of evidence suggests that elastic energy storage in tendons and titin—a large, calcium‐dependent, spring‐like protein spanning half of the sarcomere—underlies the enhanced and increased metabolic efficiency of force production during SSCs and may actually protect the sarcomeres from damage during whole muscle stretch (Edman et al, ; Roberts et al, ; Biewener et al, ; Joumaa et al, ; Leonard et al, ,b; Nishikawa et al, ; Joumaa and Herzog, ; Azizi and Roberts, ; Holt et al, ; Konow et al, ; Monroy et al, ; Powers et al, ; Pace et al, ). Indeed, Herzog and colleagues () argue that titin should be considered a third myofilament alongside actin and myosin due to its substantial contributions to force production during active fiber lengthening.…”

“…Previous studies have integrated XROMM and kinetic or EMG measurements in a limited number of muscles to relate muscle behavior to skeletal outputs by implanting individual muscles with tantalum beads or by reconstructing their attachments on bone from osteological landmarks (Astley and Roberts, ; Gidmark et al, ; Camp et al, ; Konow et al, ). We demonstrate how diceCT can be incorporated into XROMM and EMG workflows to study over a dozen muscles, many of which are difficult to access surgically for FMM.…”

Inspiration for wing design: how forelimb specialization enables active flight in modern vertebrates

“…Length change is typically measured using sonomicrometry, piezoelectric crystals implanted into the muscle fascicle that signal ultrasonically to each other to determine separation [42], which is used to calculate strain (figure 3c). A newer technique tracks radiopaque markers using fluoroscopes [50]. Force is calculated from strain measured at the insertion points where the flight muscles connect to the humerus (figure 3c) [42].…”