How scaling approaches can reveal fundamental principles in physiology and biomechanics

Among terrestrial mammals, the largest, the 3 tonne African elephant, is one-million times heavier than the smallest, the 3 g pygmy shrew. Body mass is the most obvious and arguably the most fundamental characteristic of an animal, impacting many important attributes of its life history and biology. Although evolution may guide animals to different sizes, shapes, energetic profiles or ecological niches, it is the laws of physics that limit biological processes and, in turn, affect how animals interact with their environment. Consideration of scaling helps us to understand why elephants are not merely scaled-up shrews, but rather have modified body proportions, posture and locomotor style to mitigate the consequences of their large size. Scaling offers a quantitative lens into how biological features vary compared with predictions based on physical laws. In this Review, we provide an introduction to scaling and its historical context, focusing on two fields that are strongly represented in experimental biology: physiology and biomechanics. We show how scaling has been used to explore metabolic energy use with changes in body size. We discuss the musculoskeletal and biomechanical adaptations that animals use to mitigate the consequences of size, and provide insights into the scaling of mechanical and energetic demands of animal locomotion. For each field, we discuss empirical measurements, fundamental scaling theories and the importance of considering phylogenetic relationships when performing scaling analyses. Finally, we provide forward-looking perspectives focused on improving our understanding of the diversity of form and function in relation to size.