Black Drum Fish Teeth: Built for Crushing Mollusk Shells

Zhifei Deng; Hyun-Chae Loh; Zian Jia; Cayla A Stifler; Admir Masic; Pupa U P A Gilbert; Ron Shahar; Ling Li

doi:10.1016/j.actbio.2021.10.023

Black Drum Fish Teeth: Built for Crushing Mollusk Shells

Acta Biomater. 2022 Jan 1:137:147-161. doi: 10.1016/j.actbio.2021.10.023. Epub 2021 Oct 19.

Authors

Zhifei Deng¹, Hyun-Chae Loh², Zian Jia¹, Cayla A Stifler³, Admir Masic², Pupa U P A Gilbert⁴, Ron Shahar⁵, Ling Li⁶

Affiliations

¹ Department of Mechanical Engineering, Virginia Polytechnic Institute of Technology and State University, Blacksburg, VA 24060, USA.
² Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
³ Department of Physics, University of Wisconsin-Madison, Madison, WI 53706, USA.
⁴ Department of Physics, University of Wisconsin-Madison, Madison, WI 53706, USA; Lawrence Berkeley National Laboratory, Chemical Sciences Division, Berkeley, CA 94720, USA.
⁵ Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, Israel.
⁶ Department of Mechanical Engineering, Virginia Polytechnic Institute of Technology and State University, Blacksburg, VA 24060, USA. Electronic address: lingl@vt.edu.

PMID: 34673226
DOI: 10.1016/j.actbio.2021.10.023

Abstract

With an exclusive diet of hard-shelled mollusks, the black drum fish (Pogonias cromis) exhibits one of the highest bite forces among extant animals. Here we present a systematic microstructural, chemical, crystallographic, and mechanical analysis of the black drum teeth to understand the structural basis for achieving the molluscivorous requirements. At the material level, the outermost enameloid shows higher modulus (E_r = 126.9 ± 16.3 GPa, H = 5.0 ± 1.4 GPa) than other reported fish teeth, which is attributed to the stiffening effect of Zn and F doping in apatite crystals and the preferential co-alignment of crystallographic c-axes and enameloid rods along the biting direction. The high fracture toughness (K_c = 1.12 MPa⋅m^1/2) of the outer enameloid also promotes local yielding instead of fracture during crushing contact with mollusk shells. At the individual-tooth scale, the molar-like teeth, high density of dentin tubules, enlarged pulp chamber, and specialized dentin-bone connection, all contribute to the functional requirements, including confinement of contact compressive stress in the stiff enameloid, enhanced energy absorption in the compliant dentin, and controlled failure of tooth-bone composite under excessive loads. These results show that the multi-scale structures of black drum teeth are adapted to feed on hard-shelled mollusks. STATEMENT OF SIGNIFICANCE: The black drum fish feeds on hard-shelled mollusks, which requires strong, tough, and wear-resistant teeth. This study presents a comprehensive multiscale material and mechanical analysis of the black drum teeth in achieving such remarkable biological function. At microscale, the fluoride- and zinc-doped apatite crystallites in the outer enameloid region are aligned perpendicular to the chewing surface, representing one of the stiffest biomineralized materials found in nature. In the inner enameloid region, the apatite crystals are arranged into intertwisted rods with crystallographic misorientation for increased crack resistance and toughness. At the macroscale, the molariform geometry, the two-layer design based on the outer enameloid and inner dentin, enlarged pulp chamber and the underlying strong bony toothplate work synergistically to contribute to the teeth's crushing resistance.

Keywords: Black drum teeth; Durophagous behavior; Fracture resistance; Microstructure.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Apatites
Bite Force
Fishes
Mollusca
Tooth*

Substances

Apatites