Insect antennae: Coupling blood pressure with cuticle deformation to control movement
Insect antennae: Coupling blood pressure with cuticle deformation to control movement
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DOI：
10.1016/j.actbio.2022.05.044
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发表时间：
2022-07-01
影响因子：
9.7
通讯作者：
Kornev, Konstantin G.
中科院分区：
文献类型：
--
作者：
Donley, Griffin;Sun, Yueming;Kornev, Konstantin G.
昆虫触角是中空的、充满血液的纤维，形状复杂。两个基部的肌肉控制触角的运动，但其余部分（鞭毛）没有肌肉。昆虫可以可控地弯曲、扭转和横向操纵其触角。为了解释这种行为，我们对美洲大蠊（Periplaneta americana）、卡罗莱纳天蛾（Manduca sexta）和瓦妮莎·卡杜伊（Vanessa cardui）的触角的结构和拉伸特性进行了比较研究。这些触角表现出一系列可区分的拉伸特性，表现为脆性纤维或应变自适应纤维，在拉伸时会变硬。扫描电子显微镜和拉伸过程中触角断裂的高速成像揭示了血压和触角角质层变形之间的复杂耦合。固体力学的广义拉米理论被发展到包括充满血液的触角管的力驱动变形。我们通过使用不带可调参数的人造天线进行的实验验证了该理论。当昆虫的触角膨胀时，血压会升高；当触角受到外部拉伸负载时，血压会降低到环境压力以下。压力-角质层耦合可以通过触角腔中血量的变化来控制。在触角腔内没有充满血液的昆虫中，缺乏这种血压控制，并且触角仅通过肌肉激活做出反应。我们建议，我们发现的昆虫触角原理也适用于其他具有腿起源的附肢。我们的工作为基于纤维的多功能微流体提供了有前途的新应用，这些微流体可以传输流体并根据需要由相同的流体进行操纵。重要性声明昆虫触角是充满血液的分段纤维，两个基部有肌肉。长末端节段没有肌肉，但可以弯曲。为了解释这种行为，我们研究了蟑螂、天蛾和蝴蝶触角的结构-功能关系。天蛾的触角表现为脆性纤维，但蝴蝶和蟑螂的触角表现出应变适应性行为，就像拉伸时会变硬的纤维一样。拉伸过程中触角破裂的视频显微镜揭示了血压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。因为触角是腿衍生的附属物，所以我们建议我们发现的原理适用于腿衍生祖先的其他附属物。我们的工作为基于纤维的多功能微流体提供了新的应用，这些微流体可以传输流体并根据需要由流体操纵。 (c) 2022 Acta Materialia Inc. 由 Elsevier Ltd 出版。保留所有权利。
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 Lametheory 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 significanceInsect 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. (c) 2022 Acta Materialia Inc. Published by Elsevier Ltd. All rights reserved.