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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:
ORCiD logo [1];  [1];  [2];  [1];  [3];  [1];  [1];  [4];  [1];  [4];  [5]; ORCiD logo [6]; ORCiD logo [7]
  1. Univ. Medical Center Hamburg‐Eppendorf, Hamburg (Germany)
  2. Univ. of California Berkeley, CA (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. European Molecular Biology Lab., Hamburg (Germany)
  5. UNSW Sydney (Australia)
  6. Univ. of California, Berkeley, CA (United States)
  7. Univ. Medical Center Hamburg‐Eppendorf, Hamburg (Germany); Forum Medical Technology Health Hamburg (FMTHH), Hamburg (Germany)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (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 Volume: 6; Journal Issue: 12; Journal ID: ISSN 2198-3844
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biomechanical performance; biomimetics; fracture mechanics; toughness

Citation Formats

Schmidt, Felix N., Zimmermann, Elizabeth A., Walsh, Flynn, Plumeyer, Christine, Schaible, Eric, Fiedler, Imke A. K., Milovanovic, Petar, Rößle, Manfred, Amling, Michael, Blanchet, Clément, Gludovatz, Bernd, Ritchie, Robert O., and Busse, Björn. 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. United States: N. p., 2019. Web. doi:10.1002/advs.201900287.
Schmidt, Felix N., Zimmermann, Elizabeth A., Walsh, Flynn, Plumeyer, Christine, Schaible, Eric, Fiedler, Imke A. K., Milovanovic, Petar, Rößle, Manfred, Amling, Michael, Blanchet, Clément, Gludovatz, Bernd, Ritchie, Robert O., & Busse, Björn. 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. United States. doi:10.1002/advs.201900287.
Schmidt, Felix N., Zimmermann, Elizabeth A., Walsh, Flynn, Plumeyer, Christine, Schaible, Eric, Fiedler, Imke A. K., Milovanovic, Petar, Rößle, Manfred, Amling, Michael, Blanchet, Clément, Gludovatz, Bernd, Ritchie, Robert O., and Busse, Björn. Thu . "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". United States. doi:10.1002/advs.201900287.
@article{osti_1510355,
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},
author = {Schmidt, Felix N. and Zimmermann, Elizabeth A. and Walsh, Flynn and Plumeyer, Christine and Schaible, Eric and Fiedler, Imke A. K. and Milovanovic, Petar and Rößle, Manfred and Amling, Michael and Blanchet, Clément and Gludovatz, Bernd and Ritchie, Robert O. and Busse, Björn},
abstractNote = {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.},
doi = {10.1002/advs.201900287},
journal = {Advanced Science},
number = 12,
volume = 6,
place = {United States},
year = {2019},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
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DOI: 10.1002/advs.201900287

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Cited by: 1 work
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    Works referencing / citing this record:

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    journal, April 2015

    • Zimmermann, Elizabeth A.; Ritchie, Robert O.
    • Advanced Healthcare Materials, Vol. 4, Issue 9
    • DOI: 10.1002/adhm.201500070

    Modifications to Nano- and Microstructural Quality and the Effects on Mechanical Integrity in Paget's Disease of Bone: NANO/MICROSTRUCTURE EFFECTS ON MECHANICAL INTEGRITY IN PDB
    journal, January 2015

    • Zimmermann, Elizabeth A.; Köhne, Till; Bale, Hrishikesh A.
    • Journal of Bone and Mineral Research, Vol. 30, Issue 2
    • DOI: 10.1002/jbmr.2340

    The amazing osteocyte
    journal, January 2011

    • Bonewald, Lynda F.
    • Journal of Bone and Mineral Research, Vol. 26, Issue 2
    • DOI: 10.1002/jbmr.320

    Changes in the mineral density distribution in human bone with age: Image analysis using backscattered electrons in the SEM
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    • Liu, Yifei; Manjubala, Inderchand; Schell, Hanna
    • Journal of Bone and Mineral Research, Vol. 25, Issue 9
    • DOI: 10.1002/jbmr.84

    Osteonal and hemi-osteonal remodeling: The spatial and temporal framework for signal traffic in adult human bone
    journal, July 1994


    The Formation of Calcified Nanospherites during Micropetrosis Represents a Unique Mineralization Mechanism in Aged Human Bone
    journal, November 2016

    • Milovanovic, Petar; Zimmermann, Elizabeth A.; vom Scheidt, Annika
    • Small, Vol. 13, Issue 3
    • DOI: 10.1002/smll.201602215

    Mechanical properties of bone tissues with greatly differing functions
    journal, January 1979


    Nanostructure and mineral composition of trabecular bone in the lateral femoral neck: Implications for bone fragility in elderly women
    journal, September 2011


    Mixed-mode fracture of human cortical bone
    journal, October 2009


    The significance of crack-resistance curves to the mixed-mode fracture toughness of human cortical bone
    journal, July 2010


    Fracture resistance of human cortical bone across multiple length-scales at physiological strain rates
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    Bone mineralization density distribution in health and disease
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    Trends in trabecular architecture and bone mineral density distribution in 152 individuals aged 30–90years
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    journal, September 2006

    • Nalla, R. K.; Kruzic, J. J.; Kinney, J. H.
    • Materials Science and Engineering: C, Vol. 26, Issue 8
    • DOI: 10.1016/j.msec.2005.08.021

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    • DOI: 10.1021/nn401360u

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    Intrinsic mechanical behavior of femoral cortical bone in young, osteoporotic and bisphosphonate-treated individuals in low- and high energy fracture conditions
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    Eigenschaften des Osteozytennetzwerks in gesundem und erkranktem Knochen
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    Age-related changes in the plasticity and toughness of human cortical bone at multiple length scales
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    • Zimmermann, E. A.; Schaible, E.; Bale, H.
    • Proceedings of the National Academy of Sciences, Vol. 108, Issue 35
    • DOI: 10.1073/pnas.1107966108

    Remodeling in bone without osteocytes: Billfish challenge bone structure–function paradigms
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    • Atkins, Ayelet; Dean, Mason N.; Habegger, Maria Laura
    • Proceedings of the National Academy of Sciences, Vol. 111, Issue 45
    • DOI: 10.1073/pnas.1412372111

    A SAXS/WAXS/GISAXS Beamline with Multilayer Monochromator
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    • Domenici, P.; Wilson, A. D. M.; Kurvers, R. H. J. M.
    • Proceedings of the Royal Society B: Biological Sciences, Vol. 281, Issue 1784
    • DOI: 10.1098/rspb.2014.0444

    Vitamin D Deficiency Induces Early Signs of Aging in Human Bone, Increasing the Risk of Fracture
    journal, July 2013

    • Busse, Björn; Bale, Hrishikesh A.; Zimmermann, Elizabeth A.
    • Science Translational Medicine, Vol. 5, Issue 193
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    The Effect of Age on Fracture Risk: A Population-Based Cohort Study
    journal, January 2016


    Comparison of structural, architectural and mechanical aspects of cellular and acellular bone in two teleost fish
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    • Cohen, L.; Dean, M.; Shipov, A.
    • Journal of Experimental Biology, Vol. 215, Issue 11
    • DOI: 10.1242/jeb.064790

    Feeding in billfishes: inferring the role of the rostrum from a biomechanical standpoint
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    • Habegger, M. L.; Dean, M. N.; Dunlop, J. W. C.
    • Journal of Experimental Biology, Vol. 218, Issue 6
    • DOI: 10.1242/jeb.106146

    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
    text, January 2019

    • Schmidt, Felix N.; Zimmermann, Elizabeth A.; Walsh, Flynn
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    Age and growth of the swordfish (Xiphias gladius Linnaeus, 1758) in the southeastern Pacific off Chile (2001)
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