Department of Materials Science and Engineering, Clemson University, Clemson, SC 29634, USA.
Department of Evolutionary Biology, University of Vienna, Vienna A-1030, Austria.
Acta Biomater. 2022 Jul 15;147:102-119. doi: 10.1016/j.actbio.2022.05.044. Epub 2022 May 29.
Insect antennae are hollow, blood-filled fibers with complex shape. Muscles in the two basal segments control antennal movement, but the rest (flagellum) is muscle-free. The insect can controllably flex, twist, and maneuver its antennae laterally. To explain this behavior, we performed a comparative study of structural and tensile properties of the antennae of Periplaneta americana (American cockroach), Manduca sexta (Carolina hawkmoth), and Vanessa cardui (painted lady butterfly). These antennae demonstrate a range of distinguishable tensile properties, responding either as brittle or strain-adaptive fibers that stiffen when stretched. Scanning electron microscopy and high-speed imaging of antennal breakup during stretching revealed complex coupling of blood pressure and cuticle deformation in antennae. A generalized Lamé theory of solid mechanics was developed to include the force-driven deformation of blood-filled antennal tubes. We validated the theory against experiments with artificial antennae with no adjustable parameters. Blood pressure increased when the insect inflated its antennae or decreased below ambient pressure when an external tensile load was applied to the antenna. The pressure-cuticle coupling can be controlled through changes of the blood volume in the antennal lumen. In insects that do not fill the antennal lumen with blood, this blood pressure control is lacking, and the antennae react only by muscular activation. We suggest that the principles we have discovered for insect antennae apply to other appendages that share a leg-derived ancestry. Our work offers promising new applications for multifunctional fiber-based microfluidics that could transport fluids and be manipulated by the same fluid on demand. STATEMENT OF SIGNIFICANCE: Insect antennae are blood-filled, segmented fibers with muscles in the two basal segments. The long terminal segment is muscle-free but can be flexed. To explain this behavior, we examined structure-function relationships of antennae of cockroaches, hawkmoths, and butterflies. Hawkmoth antennae behaved as brittle fibers, but butterfly and cockroach antennae showed strain-adaptive behavior like fibers that stiffen when stretched. Videomicroscopy of antennal breakup during stretching revealed complex coupling of blood pressure and cuticle deformation. Our solid mechanics model explains this behavior. Because antennae are leg-derived appendages, we suggest that the principles we found apply to other appendages of leg-derived ancestry. Our work offers new applications for multifunctional fiber-based microfluidics that could transport fluids and be manipulated by the fluid on demand.
昆虫触角是中空的、充满血液的纤维，形状复杂。两个基部节段的肌肉控制触角的运动，但其余部分（鞭节）没有肌肉。昆虫可以控制地弯曲、扭曲和横向操纵其触角。为了解释这种行为，我们对美洲大蠊（美洲大蠊）、卡罗来纳角蝉（卡罗来纳角蝉）和 Vanessa cardui（彩绘女士蝴蝶）的触角的结构和拉伸性能进行了比较研究。这些触角表现出一系列可区分的拉伸性能，要么表现为脆性纤维，要么表现为应变适应性纤维，在拉伸时会变硬。在拉伸过程中对触角断裂的扫描电子显微镜和高速成像显示了血液压力和角质层变形在触角中的复杂耦合。我们开发了一个广义的固体力学拉梅理论，将充满血液的触角管的力驱动变形包括在内。我们使用没有可调参数的人工触角对该理论进行了实验验证。当昆虫充气其触角时，血压会升高，或者当外部拉伸载荷施加到触角上时，血压会降低到环境压力以下。通过改变触角管腔中的血液体积，可以控制血压-角质层耦合。在没有用血液充满触角管腔的昆虫中，这种血压控制是缺乏的，触角只能通过肌肉激活来反应。我们建议，我们为昆虫触角发现的原理适用于具有共同腿部起源的其他附属物。我们的工作为基于多功能纤维的微流控提供了有前景的新应用，该微流控可以按需输送流体并通过相同的流体进行操纵。
昆虫触角是充满血液的、分段的纤维，在两个基部节段中有肌肉。长的末端节段没有肌肉，但可以弯曲。为了解释这种行为，我们检查了蟑螂、天蛾和蝴蝶的触角的结构-功能关系。天蛾触角表现为脆性纤维，但蝴蝶和蟑螂触角表现出应变适应性行为，类似于拉伸时变硬的纤维。拉伸过程中触角断裂的视频显微镜显示了血液压力和角质层变形的复杂耦合。我们的固体力学模型解释了这种行为。由于触角是腿部衍生的附属物，我们认为我们发现的原理适用于腿部衍生的其他附属物。我们的工作为基于多功能纤维的微流控提供了新的应用，该微流控可以按需输送流体并通过流体进行操纵。
