Department of Biological Sciences, Clemson University, 118 Long Hall Clemson, SC 29634, USA.
Department of Biological Sciences, New Jersey Institute of Technology, Newark, NJ 07102, USA.
Integr Comp Biol. 2023 Sep 15;63(3):705-713. doi: 10.1093/icb/icad039.
The limb bones of vertebrates have a critical role in supporting the weight of the body and transmitting forces that power locomotion. The loads that limb bones experience can vary in association with a range of factors, including locomotor environment or developmental stage. Limbed vertebrates that are habitually found in environments with low locomotor loads (e.g., water) might be predicted to also exhibit limb bones with less elevated mechanical properties, such as yield stiffness and yield stress. Frogs provide a distinctive case, in which these ideas can be tested as they experience changes in both locomotor style and habitat as they develop. However, while many frog taxa shift from aquatic to terrestrial habitats as they metamorphose, some lineages, such as pipids, maintain an aquatic lifestyle even after metamorphosis, providing a comparative framework for the effects of habitat shifts on developing limbs in vertebrates. This study compares the material composition and mechanical properties of the femur between frog species that are aquatic specialists (Xenopus laevis) vs generalists that spend considerable time both on land and in water (Lithobates catesbeianus) as they transition from metamorphic tadpoles to fully grown adults. MicroCT scanning was used to determine changes in bone density related to developmental stage and hindlimb use during swimming. Microindentation was then used to collect hardness values from the cortical bone of each femur, which was used to evaluate bone material properties. We found that aquatic frogs had less overall bone mineral density (BMD) than terrestrial frogs and that BMD was more elevated in the cortical region of the diaphysis than trabeculae and distal and proximal epiphyses. Despite its less elevated BMD, bone mechanical properties were not significantly different in aquatic specialist X. laevis than in more terrestrial L. catesbeianus. Our results suggest that the limb bones of aquatic frogs may experience compensatory effects through development to offset their lower BMD. Furthermore, changes in bone density and material properties across development may help to explain some of the differences in locomotor performance found between aquatic and terrestrial metamorphic frogs, providing insight into how environmental factors might correlate with bone ossification.
脊椎动物的肢骨在支撑身体重量和传递运动力量方面起着至关重要的作用。肢骨所承受的负荷会因一系列因素而变化，包括运动环境或发育阶段。那些经常生活在低负荷运动环境（例如水）中的有肢脊椎动物，其肢骨的机械性能可能也较低，例如屈服刚度和屈服应力。青蛙提供了一个独特的案例，可以在它们发育过程中研究运动方式和栖息地变化对它们的影响。然而，尽管许多青蛙类群在变态过程中从水生栖息地转变为陆生栖息地，但有些谱系，如 pipids，即使在变态后仍保持水生生活方式，为研究脊椎动物发育中肢骨的栖息地变化对其的影响提供了比较框架。本研究比较了在从变态蝌蚪发育为完全成熟个体的过程中，作为水生专家的青蛙物种（非洲爪蟾）和作为水陆两栖专家的青蛙物种（牛蛙）的股骨的材料组成和力学性能。微计算机断层扫描用于确定与发育阶段和游泳时后肢使用相关的骨密度变化。然后，使用微压痕法从每个股骨的皮质骨中收集硬度值，用于评估骨材料性能。我们发现，水生青蛙的整体骨矿物质密度（BMD）低于陆生青蛙，皮质骨的 BMD 高于骨小梁和远侧和近侧骨骺。尽管 BMD 较低，但水生专家非洲爪蟾的骨力学性能与更陆生的牛蛙没有显著差异。我们的研究结果表明，水生青蛙的肢骨可能通过发育产生代偿效应，以弥补其较低的 BMD。此外，发育过程中骨密度和材料性能的变化可能有助于解释水生和陆生变态青蛙在运动性能上的一些差异，为了解环境因素如何与骨骨化相关提供了线索。
