Microarchitecture of cetacean vertebral trabecular bone among swimming modes and diving behaviors

Abstract

Cetaceans (dolphins, whales, and porpoises) are fully aquatic mammals that are supported by water's buoyancy and swim through axial body bending. Swimming is partially mediated by variations in vertebral morphology that creates trade-offs in body flexibility and rigidity between axial regions that either enhance or reduce displacement between adjacent vertebrae. Swimming behavior is linked to foraging ecology, where deep-diving cetaceans glide a greater proportion of the time compared to their shallow-diving counterparts. In this study, we categorized 10 species of cetaceans (Families Delphinidae and Kogiidae) into functional groups determined by swimming patterns (rigid vs. flexible torso) and diving behavior (shallow vs. deep). Here, we quantify vertebral trabecular microarchitecture (a) among functional groups (rigid-torso shallow diver (RS), rigid-torso deep diver (RD), and flexible-torso deep diver (FD)), and (b) among vertebral column regions (posterior thoracic, lumbar, caudal peduncle, and fluke insertion). We microCT scanned vertebral bodies, from which 1-5 volumes of interest were selected to quantify bone volume fraction (BV/TV), specific bone surface (BS/BV), trabecular thickness (TbTh), trabecular number (TbN), trabecular separation (TbSp), and degree of anisotropy (DA). We found that BV/TV was greatest in the rigid-torso shallow-diving functional group, smallest in flexible-torso deep-diving species, and intermediate in the rigid-torso deep-diving group. DA was significantly greater in rigid-torso caudal oscillators than in their flexible-torso counterparts. We found no variation among vertebral regions for any microarchitectural variables. Despite having osteoporotic skeletons, cetacean vertebrae had greater BV/TV, TbTh, and DA than previously documented in terrestrial mammalian bone. Cetacean species are an ideal model to investigate the long-term adaptations, over an animal's lifetime and over evolutionary time, of trabecular bone in non-weight–bearing conditions.