Title: On the Origins of Fracture Toughness in Advanced Teleosts: How the Swordfish Sword's Bone Structure and Composition Allow for Slashing under Water to Kill or Stun Prey

Abstract

The osseous sword of a swordfish (Xiphias gladius) is specialized to incapacitate prey with stunning blows. Considering the sword's growth and maturation pattern, aging from the sword's base to the tip, while missing a mechanosensitive osteocytic network, an in-depth understanding of its mechanical properties and bone quality is lacking. Microstructural, compositional, and nanomechanical characteristics of the bone along the sword are investigated to reveal structural mechanisms accounting for its exceptional mechanical competence. The degree of mineralization, homogeneity, and particle size increase from the base toward the tip, reflecting aging along its length. Fracture experiments reveal that crack-growth toughness vastly decreases at the highly and homogeneously mineralized tip, suggesting the importance of aging effects. Initiation toughness, however, is unchanged suggesting that aging effects on this hierarchical level are counteracted by constant mineral/fibril interaction. In conclusion, the sword of the swordfish provides an excellent model reflecting base-to-tip-wise aging of bone, as indicated by increasing mineralization and decreasing crack-growth toughness toward the tip. The hierarchical, structural, and compositional changes along the sword reflect peculiar prerequisites needed for resisting high mechanical loads. Further studies on advanced teleosts bone tissue may help to unravel structure-function relationships of heavily loaded skeletons lacking mechanosensing cells.

Authors:

Schmidt, Felix N.  ^[1];

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• Search DOE PAGES for ORCID "0000-0001-6586-6794"

Zimmermann, Elizabeth A. ^[1]; Walsh, Flynn ^[2]; Plumeyer, Christine ^[1]; Schaible, Eric ^[3]; Fiedler, Imke A. K. ^[1]; Milovanovic, Petar ^[1]; Rößle, Manfred ^[4]; Amling, Michael ^[1]; Blanchet, Clément ^[4]; Gludovatz, Bernd ^[5]; Ritchie, Robert O.  ^[2];

• Search DOE PAGES for author "Ritchie, Robert O."
• Search DOE PAGES for ORCID "0000-0002-0501-6998"

Busse, Björn  ^[6]

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• Search DOE PAGES for ORCID "0000-0002-3099-8073"

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+ Show Author Affiliations

1. Department of Osteology and BiomechanicsUniversity Medical Center Hamburg‐Eppendorf Lottestrasse 55A 22529 Hamburg Germany
2. Materials Sciences DivisionLawrence Berkeley National LaboratoryDepartment of Materials Science and EngineeringUniversity of California Berkeley CA 94720 USA
3. Advanced Light SourceLawrence Berkeley National Laboratory Berkeley CA 94720 USA
4. European Molecular Biology LaboratoryHamburg Outstation Hamburg 22607 Germany
5. School of Mechanical and Manufacturing EngineeringUNSW Sydney NSW 2052 Australia
6. Department of Osteology and BiomechanicsUniversity Medical Center Hamburg‐Eppendorf Lottestrasse 55A 22529 Hamburg Germany, Forum Medical Technology Health Hamburg (FMTHH) Hamburg 22529 Germany

Publication Date:

Thu May 02 00:00:00 EDT 2019

Research Org.:

Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:

USDOE Office of Science (SC)

OSTI Identifier:

1510355

Alternate Identifier(s):

OSTI ID: 1510357; OSTI ID: 1572015

Grant/Contract Number:  

AC02‐05CH11231; AC02-05CH11231

Resource Type:

Published Article

Journal Name:

Advanced Science

Additional Journal Information:

Journal Name: Advanced Science Journal Volume: 6 Journal Issue: 12; Journal ID: ISSN 2198-3844

Publisher:

Wiley

Country of Publication:

Germany

Language:

English

Subject:

59 BASIC BIOLOGICAL SCIENCES; biomechanical performance; biomimetics; fracture mechanics; toughness