Nanomechanical properties of modern and fossil bone

Abstract

Relatively little is known about how diagenetic processes affect the mechanical properties of mineralized tissues such as vertebrate bones. Diagenesis can involve the alteration of bone's organic phase, mineral phase, and structural organization, all of which contribute to bone's nanomechanical properties. Nanoindentation allows submicrometer investigation of alterations in bone properties that occur during diagenesis. In this preliminary study, the nanomechanical properties (modulus and hardness) of recent and fossil bone were compared through the use of depth-sensing nanoindentation. Additionally, X-ray diffraction and density measurements were used to investigate changes in the mineral phase. Nanoindentation revealed that the basic mechanical anisotropy of modern bone can be preserved in fossil bones going back at least to the early Eocene (∼ 50 Ma), as the elastic modulus ( i.e., stiffness) values measured perpendicular to the long axis of each bone sample were consistently lower than longitudinal values (as is the case for modern bones). While a general increase in mechanical properties was observed with the geological age of the samples, a relatively small increase was seen in fossil bone samples older than the Miocene, suggesting that mineral infilling is limited by spatial saturation, as the modulus approached that of fully dense minerals such as quartz or apatite. Further, evidence for modification of the mineral phase was demonstrated by an increase in crystallinity and density with the geological age of the bone. Both increased crystallinity and density correlated with increased modulus values, suggesting that the size and perfection of the bioapatite crystals contribute to the mechanical properties of the bones. Rather unexpectedly, the early Oligocene-aged bones demonstrated reduced modulus and hardness values compared to the Miocene and Eocene samples, which we hypothesize to be related to the diagenetic environment. Specifically, the fossil-bearing strata at the Oligocene-aged locality contain volcanic ash which is known to dissolve bone mineral — a plausible cause for the decreased mechanical properties of the Oligocene bones. Our study demonstrates that nanoindentation, a relatively nondestructive tool, is useful in investigating tissue-level diagenesis in bone that cannot be seen with the naked eye, and can provide insight into the functional significance of mineralized tissues even after diagenesis has occurred.