Hypermineralized Whale Rostrum as the Exemplar for Bone Mineral

Abstract

Although bone is a nanocomposite of mineral and collagen, mineral has been the more elusive component of study. A standard for bone mineral is clearly needed. We hypothesized that the most natural, least-processed bone mineral could be retrieved from the most highly mineralized bone. We therefore studied the rostrum of the toothed whale Mesoplodon densirostris, which has the densest recognized bone. Essential to establishment of a standard for bone mineral is the documentation that the proposed tissue is bone-like in all properties except for its remarkably high concentration of mineral. Transmitted-light microscopy of unstained sections of rostral material shows normal bone morphology in osteon geometry, lacunae concentration, and vasculature development. Stained sections reveal extremely low density of thin collagen fibers in most of the bone, but enrichment of thicker collagen fibers around vascular holes and in a minority of osteons. Field-emission scanning electron microscopy shows the rostrum mostly consists of dense mineral prisms. Most rostral areas have the same chemical–structural features, i.e., Raman spectroscopically dominated by strong bands at ∼962 Δcm^–1 and weak bands at ∼2940 Δcm^–1. Spectral features indicate that the rostrum is composed mainly of the calcium phosphate mineral apatite and has only about 4 wt.% organic content. The degree of carbonate substitution (∼8.5 wt.% carbonate) in the apatite is in the upper range found in most types of bone. We conclude that, despite its enamel-like extraordinarily high degree of mineralization, the rostrum is in all other features bone-like. Its mineral component is the long-sought uncontaminated, unaltered exemplar of bone mineral.

• bone mineral
• rostrum
• apatite
• histology
• scanning electron microscopy
• Raman spectroscopy

ACKNOWLEDGMENTS

The work is partially funded by NIH grant 1R21AR055184-01A2. The histological sectioning and staining were carried out by Crystal Idleburg in Washington University Musculoskeletal Research Center, Award Number P30AR057235 from the National Institute of Arthritis, Musculoskeletal, and Skin Diseases. We thank Prof. Keith Rogers for providing the KR rostrum sample and Dr. Vivian de Buffrénil and Dr. Olivier Lambert for the MNHN rostrum samples. We appreciate the help of Dr. James Mead and Charles Potter in obtaining cores of the USNM rostrum and for information on the biology and habits of Mesoplodon densirostris. We also appreciate discussions with Dr. Brigitte Wopenka and Dr. Stavros Thomopoulos on biomin-eralization and bioapatite. We thank the support staff at the Nano Research Facility at Washington University in St. Louis for assistance with FE-SEM analyses.