Macrobiomineralogy: Insights and Enigmas in Giant Whale Bones and Perspectives for Bioinspired Materials Science

The giant bones of whales (Cetacea) are the largest extant biomineral-based constructs known. The fact that such mammalian bones can grow up to 7 m long raises questions about differences and similarities to other smaller bones. Size and exposure to environmental stress are good reasons to suppose that an unexplored level of hierarchical organization may be present that is not needed in smaller bones. The existence of such a macroscopic naturally grown structure with poorly described mechanisms for biomineralization is an example of the many yet unexplored phenomena in living organisms. In this article, we describe key observations in macrobiomineralization and suggest that the large scale of biomineralization taking place in selected whale bones implies they may teach us fundamental principles of the chemistry, biology, and biomaterials science governing bone formation, from atomistic to the macrolevel. They are also associated with a very lipid rich environment on those bones. This has implications for bone development and damage sensing that has not yet been fully addressed. We propose that whale bone construction poses extreme requirements for inorganic material storage, mediated by biomacromolecules. Unlike extinct large mammals, cetaceans still live deep in large terrestrial water bodies following eons of adaptation. The nanocomposites from which the bones are made, comprising biomacromolecules and apatite nanocrystals, must therefore be well adapted to create the macroporous hierarchically structured architectures of the bones, with mechanical properties that match the loads imposed in vivo. This massive skeleton directly contributes to the survival of these largest mammals in the aquatic environments of Earth, with structural refinements being the result of 60 million years of evolution. We also believe that the concepts presented in this article highlight the beneficial uses of multidisciplinary and multiscale approaches to study the structural peculiarities of both organic and inorganic phases as well as mechanisms of biomineralization in highly specialized and evolutionarily conserved hard tissues.