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Research Article
Mechanical behavior of shark vertebral centra at biologically relevant strains
Danielle I. Ingle, Lisa J. Natanson, Marianne E. Porter
Journal of Experimental Biology 2018 221: jeb188318 doi: 10.1242/jeb.188318 Published 12 December 2018
Danielle I. Ingle
Department of Biological Sciences, Florida Atlantic University, Boca Raton, FL 33431, USA
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  • For correspondence: dingle2014@fau.edu
Lisa J. Natanson
Apex Predators Program, National Marine Fisheries Service, Narragansett, RI 02882, USA
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Marianne E. Porter
Department of Biological Sciences, Florida Atlantic University, Boca Raton, FL 33431, USA
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  • Fig. 1.
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    Fig. 1.

    Anatomy of shark vertebral centra. (A) Frontal view of a centrum details mineralized concentric rings that extend out toward the centrum edge. The neural arch extends dorsally in the shark, and the hemal arch, which is present in the caudal region only, extends ventrally. (B) Sagittal view of a cross-sectioned centrum detailing the double cone structure with apices pointing towards the center. The intermedialia (red) and corpus calcarea (blue) make up the mineralized double cone structure. (C) Centra were subjected to quasi-static compression tests. From centra X-rays (sagittal view), the area of double cone [blue (intermedialia) plus red (corpus calcarea)] was quantified in addition to the angles formed at the double cone apices (yellow). A and B are drawings by D.N.I.

  • Fig. 2.
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    Fig. 2.

    Sampling locations for six study species. Vertebrae were sampled from four locations in six shark species: (1) the pectoral fin insertion, (2) the first dorsal fin origin, (3) the second dorsal fin origin and (4) the pre-caudal pit. For this study, three vertebrae were sampled from each region per shark. For statistical analyses, mechanical properties from regions 1 and 2 were pooled as the anterior region and properties from regions 3 and 4 were combined as the posterior body region.

  • Fig. 3.
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    Fig. 3.

    Stress–strain curve of cartilaginous centra tested in compression. The centra were aligned with the pectoral fin insertion in the small (74.5 cm total length, TL; blue line) and large (226 cm TL; green line) dusky shark. The small shark centrum (blue line) demonstrates yield behavior and transitions into permanent deformation. The large shark centrum (green line) reached the 1000 N system threshold of the Instron E1000 within the linear portion of the curve (denoted by the red circle). The gray shading denotes the area under the curve (toughness) and stiffness (stress/strain) is indicated at 4% centrum length deformation for the small dusky shark. Additional stress–strain curves of shark centra in compression are provided in Fig. S1.

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    Fig. 4.

    Variation in centra mineralization among regions, animal sizes and species. Dusky, common thresher and shortfin mako representatives of the three shark families sampled: Carcharinidae, Alopidae and Lamnidae, respectively. YOY (young of the year), immature and mature denote the three animal developmental classifications. Anterior (A) and posterior (P) labels refer to centra aligned with the pectoral fin insertion and the second dorsal fin origin, respectively.

  • Fig. 5.
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    Fig. 5.

    Centra mechanical properties among shark ontogenetic groups. (A) Centra toughness was greatest in YOY animals, mature shark centra were the least tough and immature centra stiffness was intermediate (P<0.001). (B) Stiffest centra were also from YOY sharks, while the least stiff centra were from mature sharks and immature centra fell between the two ontogenetic groupings (P<0.001). Bars are means of ontogenetic groupings for shark species; error bars denote ±s.e.m. Letters above bars denote differences among anterior and posterior regions of each species.

  • Fig. 6.
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    Fig. 6.

    Centra mechanical properties from anterior (pectoral fin insertion and first dorsal fin origin: dark shade) and posterior (second dorsal fin and precaudal pit: light shade) body regions among species. (A) Overall, centra from the posterior body were tougher than those from the anterior body (P<0.001). Species in which posteriorly located centra were tougher than those in the anterior body were the dusky, mako and white shark. (B) Similarly, overall centra stiffness was greatest in the posterior body (P<0.001). Centra from the posterior vertebral column were significantly stiffer than those in the anterior region in the dusky and mako sharks. Bars are means of the two regions for each species; error bars denote ±s.e.m. Asterisks denote species with the significantly greatest means. Letters above bars denote differences among anterior and posterior regions of each species.

  • Fig. 7.
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    Fig. 7.

    Centra mechanical properties among three strain groups. (A) Toughness at 10% strain was significantly greater than that at 1% and 0.1% strain among all samples (P<0.001). (B) Stiffness was also the greatest at 10% strain (P<0.001). Graph values are means for each strain rate; error bars represent ±s.e.m. Asterisks above bar graphs denote the statistically greatest mean.

  • Fig. 8.
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    Fig. 8.

    Regression of toughness by stiffness of all centra. Doubling stiffness resulted in a nearly twofold increase in toughness (R2=0.82502, P<0.001).

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    Fig. 9.

    Regressions of mechanical properties by the angles formed at the double cone apex. (A) Centra toughness demonstrated an inverse relationship with double cone apex angle (R2=0.1749, P=0.0111). (B) Stiffness also decreased with increasing apex angle (R2=0.1825, P=0.0094).

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Keywords

  • Mineralized cartilage
  • Stiffness
  • Toughness
  • Double cone
  • Elasmobranch

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Research Article
Mechanical behavior of shark vertebral centra at biologically relevant strains
Danielle I. Ingle, Lisa J. Natanson, Marianne E. Porter
Journal of Experimental Biology 2018 221: jeb188318 doi: 10.1242/jeb.188318 Published 12 December 2018
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Research Article
Mechanical behavior of shark vertebral centra at biologically relevant strains
Danielle I. Ingle, Lisa J. Natanson, Marianne E. Porter
Journal of Experimental Biology 2018 221: jeb188318 doi: 10.1242/jeb.188318 Published 12 December 2018

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