{"title":"The contractile efficiency of the mantle muscle of European common cuttlefish (Sepia officinalis) during cyclical contractions.","authors":"Nicholas W Gladman, Graham N Askew","doi":"10.1242/jeb.249297","DOIUrl":null,"url":null,"abstract":"<p><p>Escape jet propulsion swimming in cuttlefish (Sepia officinalis) is powered by the circular muscles surrounding the mantle cavity. This mode of locomotion is energetically costly compared with undulatory swimming. The energetic cost of swimming is determined by the mechanical power requirements and the efficiency with which chemical energy is transferred into useful mechanical work. One step in this energy transduction process is the transfer of energy from ATP hydrolysis into mechanical work by the muscles. Here, we determined the efficiency of this step, termed the contractile efficiency. Muscle preparations from the circular muscles of the mantle cavity were subjected to sinusoidal length changes at different cycle frequencies, and stimulated with a phase and duration that maximised initial net work. Changes in ATP, arginine phosphate and octopine content between control and exercised muscles were determined and used to calculate the energy released from ATP hydrolysis (Emet). The maximum contractile efficiency (the ratio of net work to Emet) was 0.37, occurring at the same cycle frequency at which mechanical power was maximal and that was used during jet propulsion swimming, suggesting that cuttlefish muscle is adapted to generate muscular power efficiently. The overall efficiency of cuttlefish jet propulsion swimming was estimated to be 0.17, which is broadly comparable to that measured during animal flight and human-powered pedalled locomotion, indicating the high energetic costs of jet propulsion swimming are not due to inefficient locomotion per se; instead, they result from the relatively high mechanical power requirements.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":null,"pages":null},"PeriodicalIF":2.8000,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Experimental Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1242/jeb.249297","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/11/8 0:00:00","PubModel":"Epub","JCR":"Q2","JCRName":"BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Escape jet propulsion swimming in cuttlefish (Sepia officinalis) is powered by the circular muscles surrounding the mantle cavity. This mode of locomotion is energetically costly compared with undulatory swimming. The energetic cost of swimming is determined by the mechanical power requirements and the efficiency with which chemical energy is transferred into useful mechanical work. One step in this energy transduction process is the transfer of energy from ATP hydrolysis into mechanical work by the muscles. Here, we determined the efficiency of this step, termed the contractile efficiency. Muscle preparations from the circular muscles of the mantle cavity were subjected to sinusoidal length changes at different cycle frequencies, and stimulated with a phase and duration that maximised initial net work. Changes in ATP, arginine phosphate and octopine content between control and exercised muscles were determined and used to calculate the energy released from ATP hydrolysis (Emet). The maximum contractile efficiency (the ratio of net work to Emet) was 0.37, occurring at the same cycle frequency at which mechanical power was maximal and that was used during jet propulsion swimming, suggesting that cuttlefish muscle is adapted to generate muscular power efficiently. The overall efficiency of cuttlefish jet propulsion swimming was estimated to be 0.17, which is broadly comparable to that measured during animal flight and human-powered pedalled locomotion, indicating the high energetic costs of jet propulsion swimming are not due to inefficient locomotion per se; instead, they result from the relatively high mechanical power requirements.
墨鱼(Sepia officinalis)的逃逸喷射推进游动是由套腔周围的环形肌肉提供动力的。这种运动方式的能量消耗比波状游泳者高。游泳的能量成本取决于所需的机械动力以及化学能转化为有用机械功的效率。能量转换过程中的一个步骤是肌肉将 ATP 水解产生的能量转移为机械功。在此,我们测定了这一步骤的效率,即收缩效率。对来自套腔圆肌的肌肉制备物进行不同周期频率的正弦长度变化,并以最大化初始净功的相位和持续时间进行刺激。测定对照组肌肉和运动组肌肉之间的 ATP、精氨酸磷酸和章鱼碱含量的变化,并以此计算 ATP 水解释放的能量(Emet)。最大收缩效率(净功与 Emet 之比)为 0.37,发生在机械动力达到最大值的相同周期频率,也是喷气推进游泳时使用的频率,这表明墨鱼肌肉适应于高效产生肌肉动力。墨鱼喷气推进游泳的总体效率估计为0.17,与动物飞行和人类脚踏运动时测得的效率大致相当,这表明喷气推进游泳的高能耗成本不是因为运动本身效率低下,而是因为需要相对较高的机械动力。
期刊介绍:
Journal of Experimental Biology is the leading primary research journal in comparative physiology and publishes papers on the form and function of living organisms at all levels of biological organisation, from the molecular and subcellular to the integrated whole animal.