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Macro-to-nanoscale investigation of wall-plate joints in the acorn barnacle Semibalanus balanoides: correlative imaging, biological form and function, and bioinspiration

Ed Pope Orcid Logo, R. L. Mitchell, M. Coleman, P. Davies, L. North, E. C. Pope, C. Pleydell-Pearce, W. Harris, R. Johnston, Mark Coleman Orcid Logo, Richard Johnston Orcid Logo, Cameron Pleydell-Pearce, Ria Mitchell Orcid Logo

Journal of The Royal Society Interface, Volume: 16, Issue: 157, Start page: 20190218

Swansea University Authors: Ed Pope Orcid Logo, Mark Coleman Orcid Logo, Richard Johnston Orcid Logo, Cameron Pleydell-Pearce, Ria Mitchell Orcid Logo

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DOI (Published version): 10.1098/rsif.2019.0218

Abstract

Correlative imaging combines information from multiple modalities (physical–chemical–mechanical properties) at various length scales (centimetre to nanometre) to understand the complex biological materials across dimensions (2D–3D). Here, we have used numerous coupled systems: X-ray microscopy (XRM)...

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Published in: Journal of The Royal Society Interface
ISSN: 1742-5689 1742-5662
Published: 2019
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Here, we have used numerous coupled systems: X-ray microscopy (XRM), scanning electron microscopy (SEM), electron backscatter diffraction (EBSD), optical light microscopy (LM) and focused ion beam (FIB-SEM) microscopy to ascertain the microstructural and crystallographic properties of the wall-plate joints in the barnacle Semibalanus balanoides. The exoskeleton is composed of six interlocking wall plates, and the interlocks between neighbouring plates (alae) allow barnacles to expand and grow while remaining sealed and structurally strong. Our results indicate that the ala contain functionally graded orientations and microstructures in their crystallography, which has implications for naturally functioning microstructures, potential natural strengthening and preferred oriented biomineralization. Elongated grains at the outer edge of the ala are oriented perpendicularly to the contact surface, and the c-axis rotates with the radius of the ala. Additionally, we identify for the first time three-dimensional nanoscale ala pore networks revealing that the pores are only visible at the tip of the ala and that pore thickening occurs on the inside (soft bodied) edge of the plates. The pore networks appear to have the same orientation as the oriented crystallography, and we deduce that the pore networks are probably organic channels and pockets, which are involved with the biomineralization process. Understanding these multiscale features contributes towards an understanding of the structural architecture in barnacles, but also their consideration for bioinspiration of human-made materials. 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spelling 2019-09-06T10:02:21.7924509 v2 51051 2019-07-10 Macro-to-nanoscale investigation of wall-plate joints in the acorn barnacle Semibalanus balanoides: correlative imaging, biological form and function, and bioinspiration cc94aaa2d177220c8df0b3b3edae1370 0000-0001-5781-5575 Ed Pope Ed Pope true false 73c5735de19c8a70acb41ab788081b67 0000-0002-4628-1077 Mark Coleman Mark Coleman true false 23282e7acce87dd926b8a62ae410a393 0000-0003-1977-6418 Richard Johnston Richard Johnston true false 564c480cb2abe761533a139c7dbaaca1 Cameron Pleydell-Pearce Cameron Pleydell-Pearce true false fcfffafbafb0036c483338f839df45e5 0000-0002-6328-3998 Ria Mitchell Ria Mitchell true false 2019-07-10 SBI Correlative imaging combines information from multiple modalities (physical–chemical–mechanical properties) at various length scales (centimetre to nanometre) to understand the complex biological materials across dimensions (2D–3D). Here, we have used numerous coupled systems: X-ray microscopy (XRM), scanning electron microscopy (SEM), electron backscatter diffraction (EBSD), optical light microscopy (LM) and focused ion beam (FIB-SEM) microscopy to ascertain the microstructural and crystallographic properties of the wall-plate joints in the barnacle Semibalanus balanoides. The exoskeleton is composed of six interlocking wall plates, and the interlocks between neighbouring plates (alae) allow barnacles to expand and grow while remaining sealed and structurally strong. Our results indicate that the ala contain functionally graded orientations and microstructures in their crystallography, which has implications for naturally functioning microstructures, potential natural strengthening and preferred oriented biomineralization. Elongated grains at the outer edge of the ala are oriented perpendicularly to the contact surface, and the c-axis rotates with the radius of the ala. Additionally, we identify for the first time three-dimensional nanoscale ala pore networks revealing that the pores are only visible at the tip of the ala and that pore thickening occurs on the inside (soft bodied) edge of the plates. The pore networks appear to have the same orientation as the oriented crystallography, and we deduce that the pore networks are probably organic channels and pockets, which are involved with the biomineralization process. Understanding these multiscale features contributes towards an understanding of the structural architecture in barnacles, but also their consideration for bioinspiration of human-made materials. The work demonstrates that correlative methods spanning different length scales, dimensions and modes enable the extension of the structure–property relationships in materials to form and function of organisms. Journal Article Journal of The Royal Society Interface 16 157 20190218 1742-5689 1742-5662 31 8 2019 2019-08-31 10.1098/rsif.2019.0218 COLLEGE NANME Biosciences COLLEGE CODE SBI Swansea University UKRI, EP/M028267/1 2019-09-06T10:02:21.7924509 2019-07-10T14:55:38.6047544 Faculty of Science and Engineering School of Engineering and Applied Sciences - Uncategorised Ed Pope 0000-0001-5781-5575 1 R. L. Mitchell 2 M. Coleman 3 P. Davies 4 L. North 5 E. C. Pope 6 C. Pleydell-Pearce 7 W. Harris 8 R. Johnston 9 Mark Coleman 0000-0002-4628-1077 10 Richard Johnston 0000-0003-1977-6418 11 Cameron Pleydell-Pearce 12 Ria Mitchell 0000-0002-6328-3998 13 0051051-15082019124359.pdf 51051.pdf 2019-08-15T12:43:59.3400000 Output 2645678 application/pdf Version of Record true 2019-08-14T00:00:00.0000000 Released under the terms of a Creative Commons Attribution License (CC-BY). true eng
title Macro-to-nanoscale investigation of wall-plate joints in the acorn barnacle Semibalanus balanoides: correlative imaging, biological form and function, and bioinspiration
spellingShingle Macro-to-nanoscale investigation of wall-plate joints in the acorn barnacle Semibalanus balanoides: correlative imaging, biological form and function, and bioinspiration
Ed Pope
Mark Coleman
Richard Johnston
Cameron Pleydell-Pearce
Ria Mitchell
title_short Macro-to-nanoscale investigation of wall-plate joints in the acorn barnacle Semibalanus balanoides: correlative imaging, biological form and function, and bioinspiration
title_full Macro-to-nanoscale investigation of wall-plate joints in the acorn barnacle Semibalanus balanoides: correlative imaging, biological form and function, and bioinspiration
title_fullStr Macro-to-nanoscale investigation of wall-plate joints in the acorn barnacle Semibalanus balanoides: correlative imaging, biological form and function, and bioinspiration
title_full_unstemmed Macro-to-nanoscale investigation of wall-plate joints in the acorn barnacle Semibalanus balanoides: correlative imaging, biological form and function, and bioinspiration
title_sort Macro-to-nanoscale investigation of wall-plate joints in the acorn barnacle Semibalanus balanoides: correlative imaging, biological form and function, and bioinspiration
author_id_str_mv cc94aaa2d177220c8df0b3b3edae1370
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author_id_fullname_str_mv cc94aaa2d177220c8df0b3b3edae1370_***_Ed Pope
73c5735de19c8a70acb41ab788081b67_***_Mark Coleman
23282e7acce87dd926b8a62ae410a393_***_Richard Johnston
564c480cb2abe761533a139c7dbaaca1_***_Cameron Pleydell-Pearce
fcfffafbafb0036c483338f839df45e5_***_Ria Mitchell
author Ed Pope
Mark Coleman
Richard Johnston
Cameron Pleydell-Pearce
Ria Mitchell
author2 Ed Pope
R. L. Mitchell
M. Coleman
P. Davies
L. North
E. C. Pope
C. Pleydell-Pearce
W. Harris
R. Johnston
Mark Coleman
Richard Johnston
Cameron Pleydell-Pearce
Ria Mitchell
format Journal article
container_title Journal of The Royal Society Interface
container_volume 16
container_issue 157
container_start_page 20190218
publishDate 2019
institution Swansea University
issn 1742-5689
1742-5662
doi_str_mv 10.1098/rsif.2019.0218
college_str Faculty of Science and Engineering
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hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Engineering and Applied Sciences - Uncategorised{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Engineering and Applied Sciences - Uncategorised
document_store_str 1
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description Correlative imaging combines information from multiple modalities (physical–chemical–mechanical properties) at various length scales (centimetre to nanometre) to understand the complex biological materials across dimensions (2D–3D). Here, we have used numerous coupled systems: X-ray microscopy (XRM), scanning electron microscopy (SEM), electron backscatter diffraction (EBSD), optical light microscopy (LM) and focused ion beam (FIB-SEM) microscopy to ascertain the microstructural and crystallographic properties of the wall-plate joints in the barnacle Semibalanus balanoides. The exoskeleton is composed of six interlocking wall plates, and the interlocks between neighbouring plates (alae) allow barnacles to expand and grow while remaining sealed and structurally strong. Our results indicate that the ala contain functionally graded orientations and microstructures in their crystallography, which has implications for naturally functioning microstructures, potential natural strengthening and preferred oriented biomineralization. Elongated grains at the outer edge of the ala are oriented perpendicularly to the contact surface, and the c-axis rotates with the radius of the ala. Additionally, we identify for the first time three-dimensional nanoscale ala pore networks revealing that the pores are only visible at the tip of the ala and that pore thickening occurs on the inside (soft bodied) edge of the plates. The pore networks appear to have the same orientation as the oriented crystallography, and we deduce that the pore networks are probably organic channels and pockets, which are involved with the biomineralization process. Understanding these multiscale features contributes towards an understanding of the structural architecture in barnacles, but also their consideration for bioinspiration of human-made materials. The work demonstrates that correlative methods spanning different length scales, dimensions and modes enable the extension of the structure–property relationships in materials to form and function of organisms.
published_date 2019-08-31T04:02:48Z
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