Proteins dynamically exhibit fluctuating conformations, primarily driven by variations in their main chain dihedral angles phi (ϕ) and psi (ψ). In general, these conformational ensembles are such that the overall three-dimensional structure of proteins remains invariant. The conservation of three-dimensional structure thus imposes limits on variations in individual residues’ ϕ and ψ, and moreover, compensatory mechanisms exist when one of these dihedral angles undergoes a significant change. This study attempts to quantify conformational variability in protein structures by analysing dihedral angle fluctuations across diverse protein families using Shannon entropy. We assessed 26 protein families, whose structures have been determined by X-ray crystallography, NMR spectroscopy, and for one structure on which molecular dynamics simulations have been carried out. Additionally, we included a family of protein structures predicted using AlphaFold and compared the results with those of experimentally determined structures. Our findings reveal consistent Shannon entropy values across most protein families with slight variability, suggesting a natural limit to dihedral angle fluctuations that balance structural integrity and flexibility. Significant local correlations in dihedral angle adjustments reveal sophisticated compensatory mechanisms essential for maintaining overall structural integrity. These insights enhance our understanding of the delicate balance between protein stability and flexibility and have significant implications for protein engineering, drug design, and the broader study of protein dynamics.