Abstract
Although vertebral bone microarchitecture has been studied in various tetrapods, limited quantitative data are available on the structural and compositional changes of vertebrae in marine mammals. Whales exhibit exceptional swimming and diving behaviour, and they may not be immune to diving-associated bone pathologies. Lumbar vertebral bodies were analysed in three toothed whale species: the sperm whale (Physeter macrocephalus), orca (Orcinus orca) and harbour porpoise (Phocoena phocoena). The bone volume fraction (BV/TV) did not scale with body size, although the trabeculae were thicker, fewer in number and further apart in larger whale species than in the other two species. These parameters had a negative allometric scaling relationship with body length. In sperm whales and orcas, the analyses revealed a central ossification zone (“bone-within-bone”) with an increased BV/TV and trabecular thickness. Furthermore, a large number of empty osteocyte lacunae was observed in the sperm whales. Quantitative backscattered electron imaging showed that the lacunae were significantly smaller and less densely packed. Our results indicate that whales have a unique vertebral bone morphology with an inside-out appearance and that deep diving may result in a small number of viable osteocytes because of diving depth-related osteocyte death.
Highlights
Animals living in marine environments require a skeleton that is optimised for swimming and diving in conditions of changed gravity, density and dysbarism
Age was determined via annual growth layer group (GLG) analyses of the teeth of sperm whales, and the results revealed that the three sperm whales in this study were 12, 13 and 15 years of age and had body lengths of 10.5, 10.95 and 11.4 metres, respectively
All three whale species showed a mammalian-like morphology of the lumbar vertebral bodies, with transverse and spinous processes based on computed tomography (CT) and high-resolution quantitative computed tomography (HR-pQCT) imaging (Fig. 1a, for size and weight see Table 1)
Summary
Animals living in marine environments require a skeleton that is optimised for swimming and diving in conditions of changed gravity, density and dysbarism. This adaptation may not always be successfully implemented. Mechanosensitive bone cells called osteocytes are entrapped and represent the most abundant cell type in the skeleton. The vertebral bodies of three toothed whale species (odontocete cetaceans) were comparatively studied to gain deeper insights into mammalian bone biology in marine environments. The cause of the sperm whale stranding event around the North Sea remains unclear; weather changes may be the most likely factor that misdirected whales into shallow waters. An orca (Orcinus orca) and several harbour porpoises (Phocoena phocoena) were found stranded on the coast of the North Sea
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