Alternative splicing, muscle calcium sensitivity, and the modulation of dragonfly flight performance.
ABSTRACT: Calcium sensitivity of myosin cross-bridge activation in striated muscles commonly varies during ontogeny and in response to alterations in muscle usage, but the consequences for whole-organism physiology are not well known. Here we show that the relative abundances of alternatively spliced transcripts of the calcium regulatory protein troponin T (TnT) vary widely in flight muscle of Libellula pulchella dragonflies, and that the mixture of TnT splice variants explains significant portions of the variation in muscle calcium sensitivity, wing-beat frequency, and an index of aerodynamic power output during free flight. Two size-distinguishable morphs differ in their maturational pattern of TnT splicing, yet they show the same relationship between TnT transcript mixture and calcium sensitivity and between calcium sensitivity and aerodynamic power output. This consistency of effect in different developmental and physiological contexts strengthens the hypothesis that TnT isoform variation modulates muscle calcium sensitivity and whole-organism locomotor performance. Modulating muscle power output appears to provide the ecologically important ability to operate at different points along a tradeoff between performance and energetic cost.
Project description:Vertical lifting performance in 67 hummingbird species was studied across a 4000 m elevational gradient. We used the technique of asymptotic load-lifting to elicit maximum sustained muscle power output during loaded hovering flight. Our analysis incorporated direct measurements of maximum sustained load and simultaneous wingbeat kinematics, together with aerodynamic estimates of mass-specific mechanical power output, all within a robust phylogenetic framework for the Trochilidae. We evaluated key statistical factors relevant to estimating slopes for allometric relationships by performing analyses with and without phylogenetic information, and incorporating species-specific measurement error. We further examined allometric relationships at different elevations because this gradient represents a natural experiment for studying physical challenges to animal flight mechanics. Maximum lifting capacity (i.e. vertical force production) declined with elevation, but was either isometric or negatively allometric with respect to both body and muscle mass, depending on elevational occurrence of the corresponding taxa. Maximum relative muscle power output exhibited a negative allometry with respect to muscle mass, supporting theoretical predictions from muscle mechanics.
Project description:Aerodynamic theory has long been used to predict the power required for animal flight, but widely used models contain many simplifications. It has been difficult to ascertain how closely biological reality matches model predictions, largely because of the technical challenges of accurately measuring the power expended when an animal flies. We designed a study to measure flight speed-dependent aerodynamic power directly from the kinetic energy contained in the wake of bats flying in a wind tunnel. We compared these measurements with two theoretical predictions that have been used for several decades in diverse fields of vertebrate biology and to metabolic measurements from a previous study using the same individuals. A high-accuracy displaced laser sheet stereo particle image velocimetry experimental design measured the wake velocities in the Trefftz plane behind four bats flying over a range of speeds (3-7 m s(-1)). We computed the aerodynamic power contained in the wake using a novel interpolation method and compared these results with the power predicted by Pennycuick's and Rayner's models. The measured aerodynamic power falls between the two theoretical predictions, demonstrating that the models effectively predict the appropriate range of flight power, but the models do not accurately predict minimum power or maximum range speeds. Mechanical efficiency--the ratio of aerodynamic power output to metabolic power input--varied from 5.9% to 9.8% for the same individuals, changing with flight speed.
Project description:Diurnal and seasonal increases in body mass and seasonal reductions in wing area may compromise a bird's ability to escape, as less of the power available from the flight muscles can be used to accelerate and elevate the animal's centre of mass. Here, we investigated the effects of intra-specific variation in wing morphology on escape take-off performance in blue tits (Cyanistes caeruleus). Flights were recorded using synchronised high-speed video cameras and take-off performance was quantified as the sum of the rates of change of the kinetic and potential energies of the centre of mass. Individuals with a lower wing loading, WL (WL=body weight/wing area) had higher escape take-off performance, consistent with the increase in lift production expected from relatively larger wings. Unexpectedly, it was found that the total power available from the flight muscles (estimated using an aerodynamic analysis) was inversely related to WL. This could simply be because birds with a higher WL have relatively smaller flight muscles. Alternatively or additionally, variation in the aerodynamic load on the wing resulting from differences in wing morphology will affect the mechanical performance of the flight muscles via effects on the muscle's length trajectory. Consistent with this hypothesis is the observation that wing beat frequency and relative downstroke duration increase with decreasing WL; both are factors that are expected to increase muscle power output. Understanding how wing morphology influences take-off performance gives insight into the potential risks associated with feather loss and seasonal and diurnal fluctuations in body mass.
Project description:The aerodynamic mechanisms of bat flight have been studied using a numerical approach. Kinematic data acquired using a high resolution motion capture system was employed to simulate the unsteady air flow around a bat's wings. A flapping bat wing contains many degrees of freedom, which make 3D motion tracking challenging. In order to overcome this challenge, an optical motion capture system of 21 cameras was used to reduce wing self-occlusion. Over the course of a meter-long flight, 108 discrete marker points on the bat's wings (Pratt's roundleaf bat, Hipposideros pratti) were tracked. The time evolution of the surface of each wing was computationally reconstructed in 3D space. The resulting kinematic model was interfaced with an unsteady incompressible flow solver using the immersed boundary method (IBM) and large eddy simulation (LES). Verification and validation of the flow simulation were conducted to establish accuracy. The aerodynamic forces calculated from the simulation compared well to the forces theoretically needed to sustain the observed flight trajectory. The transient flow field generated by the simulation allowed for the direct calculation of lift, drag, and power output of the bat during flight. The mean lift coefficient was found to be 3.21, and the flap cycle averaged aerodynamic power output was 1.05 W. Throughout the flap cycle, the planform area of the wings varied up to 46% between the largest and smallest values. During the upstroke, wing rotation was found to mitigate negative lift thereby improving overall flight efficiency. The high resolution motion capture and flow simulation framework presented here has the potential to facilitate the understanding of complex bat flight aerodynamics for both straight and maneuvering flight modes.
Project description:Insect- and bird-size drones-micro air vehicles (MAV) that can perform autonomous flight in natural and man-made environments are now an active and well-integrated research area. MAVs normally operate at a low speed in a Reynolds number regime of 10(4)-10(5) or lower, in which most flying animals of insects, birds and bats fly, and encounter unconventional challenges in generating sufficient aerodynamic forces to stay airborne and in controlling flight autonomy to achieve complex manoeuvres. Flying insects that power and control flight by flapping wings are capable of sophisticated aerodynamic force production and precise, agile manoeuvring, through an integrated system consisting of wings to generate aerodynamic force, muscles to move the wings and a control system to modulate power output from the muscles. In this article, we give a selective review on the state of the art of biomechanics in bioinspired flight systems in terms of flapping and flexible wing aerodynamics, flight dynamics and stability, passive and active mechanisms in stabilization and control, as well as flapping flight in unsteady environments. We further highlight recent advances in biomimetics of flapping-wing MAVs with a specific focus on insect-inspired wing design and fabrication, as well as sensing systems.This article is part of the themed issue 'Moving in a moving medium: new perspectives on flight'.
Project description:Competing hypotheses about evolutionary origins of flight are the 'fundamental wing-stroke' and 'directed aerial descent' hypotheses. Support for the fundamental wing-stroke hypothesis is that extant birds use flapping of their wings to climb even before they are able to fly; there are no reported examples of incrementally increasing use of wing movements in gliding transitioning to flapping. An open question is whether locomotor styles must evolve initially for efficiency or if they might instead arrive due to efficacy. The proximal muscles of the avian wing output work and power for flight, and new research is exploring functions of the distal muscles in relation to dynamic changes in wing shape. It will be useful to test the relative contributions of the muscles of the forearm compared with inertial and aerodynamic loading of the wing upon dynamic morphing. Body size has dramatic effects upon flight performance. New research has revealed that mass-specific muscle power declines with increasing body mass among species. This explains the constraints associated with being large. Hummingbirds are the only species that can sustain hovering. Their ability to generate force, work and power appears to be limited by time for activation and deactivation within their wingbeats of high frequency. Most small birds use flap-bounding flight, and this flight style may offer an energetic advantage over continuous flapping during fast flight or during flight into a headwind. The use of flap-bounding during slow flight remains enigmatic. Flap-bounding birds do not appear to be constrained to use their primary flight muscles in a fixed manner. To improve understanding of the functional significance of flap-bounding, the energetic costs and the relative use of alternative styles by a given species in nature merit study.This article is part of the themed issue 'Moving in a moving medium: new perspectives on flight'.
Project description:How aerodynamic power required for animal flight varies with flight speed determines optimal speeds during foraging and migratory flight. Despite its relevance, aerodynamic power provides an elusive quantity to measure directly in animal flight. Here, we determine the aerodynamic power from wake velocity fields, measured using tomographical particle image velocimetry, of pied flycatchers flying freely in a wind tunnel. We find a shallow U-shaped power curve, which is flatter than expected by theory. Based on how the birds vary body angle with speed, we speculate that the shallow curve results from increased body drag coefficient and body frontal area at lower flight speeds. Including modulation of body drag in the model results in a more reasonable fit with data than the traditional model. From the wake structure, we also find a single starting vortex generated from the two wings during the downstroke across flight speeds (1-9 m s-1). This is accomplished by the arm wings interacting at the beginning of the downstroke, generating a unified starting vortex above the body of the bird. We interpret this as a mechanism resulting in a rather uniform downwash and low induced power, which can help explain the higher aerodynamic performance in birds compared with bats.
Project description:A major goal of flight research has been to establish the relationship between the mechanical power requirements of flight and flight speed. This relationship is central to our understanding of the ecology and evolution of bird flight behaviour. Current approaches to determining flight power have relied on a variety of indirect measurements and led to a controversy over the shape of the power-speed relationship and a lack of quantitative agreement between the different techniques. We have used a new approach to determine flight power at a range of speeds based on the performance of the pectoralis muscles. As such, our measurements provide a unique dataset for comparison with other methods. Here we show that in budgerigars (Melopsittacus undulatus) and zebra finches (Taenopygia guttata) power is modulated with flight speed, resulting in U-shaped power-speed relationship. Our measured muscle powers agreed well with a range of powers predicted using an aerodynamic model. Assessing the accuracy of mechanical power calculated using such models is essential as they are the basis for determining flight efficiency when compared to measurements of flight metabolic rate and for predicting minimum power and maximum range speeds, key determinants of optimal flight behaviour in the field.
Project description: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.
Project description:Hummingbirds are known to defend food resources such as nectar sources from encroachment by competitors (including conspecifics). These competitive intraspecific interactions provide an opportunity to quantify the biomechanics of hummingbird flight performance during ecologically relevant natural behavior. We recorded the three-dimensional flight trajectories of Ruby-throated Hummingbirds defending, being chased from and freely departing from a feeder. These trajectories allowed us to compare natural flight performance to earlier laboratory measurements of maximum flight speed, aerodynamic force generation and power estimates. During field observation, hummingbirds rarely approached the maximal flight speeds previously reported from wind tunnel tests and never did so during level flight. However, the accelerations and rates of change in kinetic and potential energy we recorded indicate that these hummingbirds likely operated near the maximum of their flight force and metabolic power capabilities during these competitive interactions. Furthermore, although birds departing from the feeder while chased did so faster than freely-departing birds, these speed gains were accomplished by modulating kinetic and potential energy gains (or losses) rather than increasing overall power output, essentially trading altitude for speed during their evasive maneuver. Finally, the trajectories of defending birds were directed toward the position of the encroaching bird rather than the feeder.