Tracking energy expenditure in insect flight: from the contractile proteins to the animal's wake

昆虫是地球上最多样、最成功、最重要的经济目之一，而飞行是它们成功的关键。飞行是最耗费能量的运动方式之一，昆虫的生态、行为和生理方面几乎没有不受其能量需求影响的。在所有的运动模式中，肌肉将化学能(最终来自食物)转化为机械功，最终转移到环境中产生运动。理想情况下，为了实现对该系统的全面了解，我们需要能够追踪从收缩蛋白到传递到动物觉醒的动量的所有组织层次之间的能量转移，并将其与动物的运动表现、形态和生态联系起来。对于任何一种运动模式来说，这还没有实现。然而，通过将利兹大学在肌肉生理学和运动能量学方面的研究专长与牛津大学的流体力学相结合，可以在昆虫飞行中实现这一目标。这项拟议研究的总体目标是使用一种综合的、多学科的方法来确定在昆虫飞行中，通过肌肉将能量从生化势能转移到周围空气中。这将通过以下量化来跟踪能量的传递来实现。首先，我们将通过测量在风洞中系留飞行时的氧气消耗和二氧化碳产生的速率来确定整个生物体的代谢率。其次，我们将通过测量肌肉收缩过程中的总热来测量肌肉的代谢率--这是飞行肌肉产生的机械功和由于收缩效率低下而释放的热量的总和。肌肉产生的机械功将通过模拟飞行过程中肌肉长度的变化和活动模式来确定。同时，我们将使用热电堆测量收缩过程中和收缩后释放的热量，并确定交叉桥的效率、线粒体通过氧化磷酸化重新合成ATP的效率以及由于肌肉激活成本而产生的效率低下。最后，我们将确定翅膀将飞行肌肉产生的功转化为空中有用能量的效率。这将使用一种名为粒子图像测速(PIV)的技术来完成，该技术可以量化机翼周围和尾流中的空气速度。通过选择具有同步或异步飞行肌肉的昆虫，具有不同生态环境的密切相关物种，表现出生态和形态进化趋同的无关物种，以及不同体型的几何相似物种，我们将找出一系列大小、行会和分类群体运动效率差异的主要原因。我们将能够从基本过程的角度来解释整体运动效率的差异：交叉桥的效率，线粒体重新合成ATP的效率，翅膀的空气动力学效率，以及肌肉弹性中储存能量的能力的差异。总而言之，我们的结果将提供对这一多样化和生态重要群体的能源支出的前所未有的了解。

Insects are amongst the most diverse, successful and economically important orders on earth and flight is key to their success. Flight is one of the most energetically expensive modes of locomotion and there are few aspects of an insect's ecology, behaviour and physiology that are not affected by its energetic demands. During all modes of locomotion, muscles convert chemical energy (ultimately derived from food) into mechanical work that is ultimately transferred to the environment to produce movement. Ideally, to achieve a full understanding of the system, we need to be able to trace the transfer of energy between all levels of organisation from the contractile proteins to the momentum transferred to the animal's wake and relate this to the animal's locomotor performance, morphology and ecology. This has not yet been achieved for any mode of locomotion. However, by combining research expertise in muscle physiology and locomotor energetics at Leeds and fluid dynamics at Oxford it is achievable in insect flight. The overall aim of this proposed research is to use an integrative, multidisciplinary approach to determine, in insect flight, the transfer of energy from biochemical potential energy, through the muscles, to the surrounding air. This will be achieved by tracking the transduction of energy by quantifying the following. First, we will determine the whole organism metabolic rate by measuring the rates of oxygen consumption and carbon dioxide production during tethered flight in a wind tunnel. Second, we will measure the muscle's metabolic rate by measuring the total enthalpy during contraction - this is the sum of the mechanical work generated by the flight muscles and the heat that is liberated due to the inefficiencies of the contraction. The mechanical work generated by the muscles will be determined by simulating the muscle length change and activity pattern during flight. At the same time, we will use a thermopile to measure the heat liberated both during and after the contraction and determine the efficiency of the crossbridges, the efficiency with which the mitochondria re-synthesise ATP by oxidative phosphorylation and the inefficiencies arising due to the costs of muscle activation. Finally we will determine the efficiency of the wings in transferring the work generated by the flight muscles into useful energy in the air. This will be done using a technique called Particle Image Velocimetry (PIV) that allows the velocities of air flowing around the wings and in the wake to be quantified. By selecting insects with either synchronous or asynchronous flight muscles, closely related species with different ecologies, unrelated species demonstrating convergent ecological and morphological evolution and geometrically similar species across a range of body sizes, we will identify the main cause or causes of differences in locomotor efficiency across a range of sizes, guilds and taxonomic groups. We will be able to explain differences in overall efficiency of locomotion in terms of the underlying processes: the efficiency of the crossbridges, the efficiency of the mitochondria in re-synthesising ATP, the aerodynamic efficiency of the wings and differences in the ability to store energy in muscle elasticity. Together, our results will provide an unprecedented understanding of energy expenditure in this diverse and ecologically important group.