Morphology of powerful suction organs from blepharicerid larvae living in raging torrents

Abstract Background Suction organs provide powerful yet dynamic attachments for many aquatic animals, including octopus, squid, remora, and clingfish. While the functional morphology of suction organs from some cephalopods and fishes has been investigated in detail, there are only few studies on suc...

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Main Authors: Victor Kang, Richard Johnston, Thomas van de Kamp, Tomáš Faragó, Walter Federle
Format: Article
Language:English
Published: BMC 2019-12-01
Series:BMC Zoology
Subjects:
Online Access:https://doi.org/10.1186/s40850-019-0049-6
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author Victor Kang
Richard Johnston
Thomas van de Kamp
Tomáš Faragó
Walter Federle
author_facet Victor Kang
Richard Johnston
Thomas van de Kamp
Tomáš Faragó
Walter Federle
author_sort Victor Kang
collection DOAJ
description Abstract Background Suction organs provide powerful yet dynamic attachments for many aquatic animals, including octopus, squid, remora, and clingfish. While the functional morphology of suction organs from some cephalopods and fishes has been investigated in detail, there are only few studies on such attachment devices in insects. Here we characterise the morphology and ultrastructure of the suction attachment organs of net-winged midge larvae (genus Liponeura; Diptera: Blephariceridae) – aquatic insects that live on rocks in rapid alpine waterways where flow speeds can reach 3 m s− 1 – using scanning electron microscopy, confocal laser scanning microscopy, and X-ray computed micro-tomography (micro-CT). Furthermore, we study the function of these organs in vivo using interference reflection microscopy. Results We identified structural adaptations important for the function of the suction attachment organs in L. cinerascens and L. cordata. First, a dense array of spine-like microtrichia covering each suction disc comes into contact with the substrate upon attachment, analogous to hairy structures on suction organs from octopus, clingfish, and remora fish. These spine-like microtrichia may contribute to the seal and provide increased shear force resistance in high-drag environments. Second, specialised rim microtrichia at the suction disc periphery were found to form a continuous ring in close contact and may serve as a seal on a variety of surfaces. Third, a V-shaped cut on the suction disc (“V-notch“) is actively opened via two cuticular apodemes inserting on its flanks. The apodemes are attached to dedicated V-notch opening muscles, thereby providing a unique detachment mechanism. The complex cuticular design of the suction organs, along with specialised muscles that attach to them, allows blepharicerid larvae to generate powerful attachments which can withstand strong hydrodynamic forces and quickly detach for locomotion. Conclusion The suction organs from Liponeura are underwater attachment devices specialised for resisting extremely fast flows. Structural adaptations from these suction organs could translate into future bioinspired attachment systems that perform well on a wide range of surfaces.
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spelling doaj.art-c4f6156d0c904c80a21a642136a5c8152022-12-21T23:30:03ZengBMCBMC Zoology2056-31322019-12-014111410.1186/s40850-019-0049-6Morphology of powerful suction organs from blepharicerid larvae living in raging torrentsVictor Kang0Richard Johnston1Thomas van de Kamp2Tomáš Faragó3Walter Federle4Department of Zoology, University of CambridgeMaterials Research Centre, College of Engineering, Swansea UniversityLaboratory for Applications of Synchrotron Radiation (LAS), Karlsruhe Institute of Technology (KIT)Institute for Photon Science and Synchrotron Radiation (IPS), Karlsruhe Institute of Technology (KIT)Department of Zoology, University of CambridgeAbstract Background Suction organs provide powerful yet dynamic attachments for many aquatic animals, including octopus, squid, remora, and clingfish. While the functional morphology of suction organs from some cephalopods and fishes has been investigated in detail, there are only few studies on such attachment devices in insects. Here we characterise the morphology and ultrastructure of the suction attachment organs of net-winged midge larvae (genus Liponeura; Diptera: Blephariceridae) – aquatic insects that live on rocks in rapid alpine waterways where flow speeds can reach 3 m s− 1 – using scanning electron microscopy, confocal laser scanning microscopy, and X-ray computed micro-tomography (micro-CT). Furthermore, we study the function of these organs in vivo using interference reflection microscopy. Results We identified structural adaptations important for the function of the suction attachment organs in L. cinerascens and L. cordata. First, a dense array of spine-like microtrichia covering each suction disc comes into contact with the substrate upon attachment, analogous to hairy structures on suction organs from octopus, clingfish, and remora fish. These spine-like microtrichia may contribute to the seal and provide increased shear force resistance in high-drag environments. Second, specialised rim microtrichia at the suction disc periphery were found to form a continuous ring in close contact and may serve as a seal on a variety of surfaces. Third, a V-shaped cut on the suction disc (“V-notch“) is actively opened via two cuticular apodemes inserting on its flanks. The apodemes are attached to dedicated V-notch opening muscles, thereby providing a unique detachment mechanism. The complex cuticular design of the suction organs, along with specialised muscles that attach to them, allows blepharicerid larvae to generate powerful attachments which can withstand strong hydrodynamic forces and quickly detach for locomotion. Conclusion The suction organs from Liponeura are underwater attachment devices specialised for resisting extremely fast flows. Structural adaptations from these suction organs could translate into future bioinspired attachment systems that perform well on a wide range of surfaces.https://doi.org/10.1186/s40850-019-0049-6Aquatic invertebratesAdhesionUnderwaterMorphologyMicrostructuresSealing
spellingShingle Victor Kang
Richard Johnston
Thomas van de Kamp
Tomáš Faragó
Walter Federle
Morphology of powerful suction organs from blepharicerid larvae living in raging torrents
BMC Zoology
Aquatic invertebrates
Adhesion
Underwater
Morphology
Microstructures
Sealing
title Morphology of powerful suction organs from blepharicerid larvae living in raging torrents
title_full Morphology of powerful suction organs from blepharicerid larvae living in raging torrents
title_fullStr Morphology of powerful suction organs from blepharicerid larvae living in raging torrents
title_full_unstemmed Morphology of powerful suction organs from blepharicerid larvae living in raging torrents
title_short Morphology of powerful suction organs from blepharicerid larvae living in raging torrents
title_sort morphology of powerful suction organs from blepharicerid larvae living in raging torrents
topic Aquatic invertebrates
Adhesion
Underwater
Morphology
Microstructures
Sealing
url https://doi.org/10.1186/s40850-019-0049-6
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