Developmental changes in bone mechanics from Florida manatees (Trichechus manatus latirostris), obligate swimming mammals

Abstract

Mammals living in aquatic environments load their axial skeletons differently from their terrestrial counterparts. The structure and mechanical behavior of trabecular bone can be especially indicative of varying habitual forces. Here, we investigated vertebral trabecular bone mechanical properties (yield strength, stiffness and toughness) throughout development in Florida manatees (Trichechus manatus latirostris), obligate undulatory swimmers. Thoracic, lumbar and caudal vertebrae were dissected from manatees (N=20) during necropsies. We extracted 6 mm 3 samples from vertebral bodies and tested them in compression in three orientations (rostrocaudal, dorsoventral and mediolateral) at 2 mm min −1. We determined variation in mechanical properties between sexes, and among developmental stages, vertebral regions and testing orientations. We also investigated the relationships between vertebral process lengths and properties of dorsoventrally and mediolaterally tested bone. Rostrocaudally tested bone was the strongest, stiffest and toughest, suggesting that this is the principal direction of stress. Our results showed that bone from female subadults was stronger and stiffer than that of their male counterparts; based on these data, we hypothesize that hormonal shifts at sexual maturity may partially drive these differences. In calves, bone from the posterior region was stronger and tougher than that from the anterior region. We hypothesize that as animals grow rapidly throughout early development, bone in the posterior region would be the most ossified to support the rostrocaudal force propagation associated with undulatory swimming.

Metabolic trade-offs in tropical and subtropical marine mammals: unique maintenance and locomotion costs in West Indian manatees and Hawaiian monk seals

“…This diet, consumed in a continuous grazing mode of feeding, is sufficient for meeting the manatee's energetic demands that are extraordinarily low, even relative to the carnivorous monk seal. Although the increased bone density of sirenian species ( Domning and de Buffrenil, 1991 ; Ingle and Porter, 2020 ) may partially account for the relative decrease in mass-specific RMR compared with other marine mammals ( Rea and Costa, 1992 ), the effect is minimal compared with the combined effects of diet and environmental temperature ( Costa and Maresh, 2017 ). Interestingly, the extinct Steller's sea cow also maintained an herbivorous diet but resided in the frigid waters of the Bering Sea.…”

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

“…Once vertebral segments were dissected from the column, they were stored on ice during transport to the laboratory (Florida Atlantic University), where they were wrapped gauze soaked in mammalian Ringer's solution and frozen. Detailed protocols for vertebrae storage and cleaning are previously outline (Ingle & Porter, 2020). Additionally, spinous processes, transverse processes, and chevron bones were removed with a band saw before transportation to Friday Harbor Laboratories (University of Washington).…”

“…Detailed protocols for vertebrae storage and cleaning are previously outline (Ingle & Porter, 2020). Additionally, spinous processes, transverse processes, and chevron bones were removed with a band saw before transportation to Friday Harbor Laboratories (University of Washington).…”

“…Extensive research has been conducted on the microarchitecture of bone from terrestrial mammalian vertebrae, which supports the body's axis against gravitational loads (Arlot et al, 2008;Borah et al, 2000;Follet et al, 2011;Mittra et al, 2005;Teo et al, 2006;Ulrich et al, 1997). However, less in known about the long-term (i.e., multi-year, lifelong, or evolutionary) structural adaptations of vertebral bone in non-weight-bearing conditions (Arfat et al, 2014;Dumont et al, 2013;Ingle & Porter, 2020; in review; Rolvien et al, 2017;Swartz & Middleton, 2008). As mammals that are obligate to aquatic life, where gravitational loads are countered by buoyant forces, cetaceans (dolphins, whales, and porpoises) represent an ideal model to investigate bone structure in non-weight-bearing environments, with potential differences among locomotion modes and behavioral ecology (Berta, 2015;Buchholtz, 2001).…”

“…Additionally, trabecular mechanical behavior, which is dependent on bone volume and architecture, has been previously shown to vary throughout development and among vertebral morphologies, swimming modes, and diving behaviors in fully aquatic mammalian species (Borah et al, 2000;Ingle and Porter, in review;Kabel et al, 1999;Mittra et al, 2005;Ryan et al, 2010;Ulrich et al, 1997). A study by Ingle & Porter (2020) found that vertebral trabecular mechanical properties varied throughout development in Florida manatees (Trichechus manatus latirostris). In T. manatus latirostris calves, who experience rapid body growth during the first 2 of years of life, only bone from the posterior region was as strong and tough as in older animals to support undulatory force propagation toward the tail during swimming.…”