Comparative morphology of changeable skin papillae in octopus and cuttlefish

Abstract

A major component of cephalopod adaptive camouflage behavior has rarely been studied: their ability to change the three-dimensionality of their skin by morphing their malleable dermal papillae. Recent work has established that simple, conical papillae in cuttlefish (Sepia officinalis) function as muscular hydrostats; that is, the muscles that extend a papilla also provide its structural support. We used brightfield and scanning electron microscopy to investigate and compare the functional morphology of nine types of papillae of different shapes, sizes and complexity in six species: S. officinalis small dorsal papillae, Octopus vulgaris small dorsal and ventral eye papillae, Macrotritopus defilippi dorsal eye papillae, Abdopus aculeatus major mantle papillae, O. bimaculoides arm, minor mantle, and dorsal eye papillae, and S. apama face ridge papillae. Most papillae have two sets of muscles responsible for extension: circular dermal erector muscles arranged in a concentric pattern to lift the papilla away from the body surface and horizontal dermal erector muscles to pull the papilla's perimeter toward its core and determine shape. A third set of muscles, retractors, appears to be responsible for pulling a papilla's apex down toward the body surface while stretching out its base. Connective tissue infiltrated with mucopolysaccharides assists with structural support. S. apama face ridge papillae are different: the contraction of erector muscles perpendicular to the ridge causes overlying tissues to buckle. In this case, mucopolysaccharide-rich connective tissue provides structural support. These six species possess changeable papillae that are diverse in size and shape, yet with one exception they share somewhat similar functional morphologies. Future research on papilla morphology, biomechanics and neural control in the many unexamined species of octopus and cuttlefish may uncover new principles of actuation in soft, flexible tissue.

Adaptive optoelectronic camouflage systems with designs inspired by cephalopod skins

“…In all cases, compatibility with large-area electronics holds promise for scalable manufacturing. Ability to reproduce physical texture, as in many cephalopods (34), remains as an interesting and challenging topic for research.…”

Mimicking Human and Biological Skins for Multifunctional Skin Electronics

“…In addition to human skin, the unique structures and functionalities of natural creatures have provided us a great inspiration for new types of e‐skin systems . Multidimensional architectures found in mammals and insects enable various functionalities, such as visual expression of stimuli, reversible dry/wet adhesion, and environment adaptation, which provide a great motivation for recent user‐interactive and skin‐attachable e‐skin applications. Furthermore, biomimetic micro/nanostructures such as whisker, porous, crack, interlocking, and hierarchical structures offer a diverse geometrical advantage with easy deformability, large surface area, and stress‐direction‐sensitive variation of structural deformation, suggesting advanced e‐skins with high tactile‐sensing capability and multifunctionality.…”

Do squids breathe through their skin?

“…Because squid lack cutaneous blood vessels, they lack this ability to draw oxygen deeper into the body. Also, as noted above, Octopus skin is likely more metabolically active than squid skin owing to the higher density of chromatophores (Messenger, 2001) and muscular papillae (Allen et al, 2014).…”

“…One plausible explanation is that octopus skin requires vascularization because it is more metabolically active than squid skin. Octopus skin contains both muscular papillae that can alter the skin's threedimensional texture (Allen et al, 2014) and one to two orders of magnitude more chromatophores than squid skin (Messenger, 2001). Such active muscular structures in the skin may require greater O 2 supply than can be supplied by diffusion from the skin surface.…”