Hierarchical Organization Modulates Transient Thermal Relaxation Dynamics in Chitinous Cuticles from Marine and Terrestrial Organisms

Abstract Chitinous cuticles are hierarchical biological composites in which the molecular organization spans multiple structural length scales. Although the relationships between chitin chemistry and mechanical performance have been extensively investigated, the structural factors governing transient thermal relaxation remain poorly understood. In particular, it remains unclear whether localized thermal dissipation in biological cuticles can be predicted from the molecular composition alone. Here, we investigate transient thermal relaxation in hydrothermal tubeworm cuticles, purified tubeworm chitin, and terrestrial beetle cuticles using time-resolved photothermal measurements correlated with Fourier-transform infrared spectroscopy, X-ray photoelectron spectroscopy, and structural analyses with wide-angle X-ray scattering. Despite exhibiting broadly similar chemical signatures, the investigated cuticles display markedly different thermal accumulation, heat dissipation kinetics, and relaxation behaviors under localized laser excitation. By comparing thermal responses of the chitinous samples from marine and terrestrial organisms and the native versus protein-renovelled samples, we found that transient thermal relaxation cannot be predicted from molecular composition alone but emerges from hierarchical organization across multiple structural levels.