Microstructural insights into the functional morphology and formation logic of spherulitic–fibrous prismatic architecture in the shell–like eggcase of the argonaut octopods

Argonautid octopods (genus Argonauta) possess a unique shell-like biomineralized eggcase, which was suggested to be produced by the first dorsal arms rather than by the mantle tissue, as in typical molluscan shells. In this study, we conducted scanning electron microscopy to investigate the microstructures of both undamaged and post-repair eggcases. Our analysis revealed that a normal eggcase comprises five layers: an outermost organic membrane, an outer spherulitic-fibrous prismatic layer, a middle organic layer, an inner spherulitic-fibrous prismatic layer, and an innermost organic membrane. Both prismatic layers exhibit bidirectional growth from the middle organic layer, a unique feature not observed in typical molluscan shells but, intriguingly, resembles the microstructures of cuttlefish cuttlebones, stony coral calcareous skeletons, and avian eggshells, indicating possible convergence. We propose that the observed eggcase microstructure is formed in four stages: nucleation on the organic scaffold, bidirectional crystal growth from the organic mid-layer, crystal growth perpendicular to the eggcase surface, and organic membrane encapsulation. We also identified two possible repair mechanisms: reattachment of broken fragments and regeneration via new secretions. Our findings thus question the assumed role of the first dorsal arms in calcification. The eggcase also represents the formation of a complex extended phenotype through convergence.