Dynamic Mechanical Properties of Body-Wall Dermis in Various Mechanical States and Their Implications for the Behavior of Sea Cucumbers

Abstract

The dermis of the sea cucumber body wall is a typical catch connective tissue that rapidly changes its mechanical properties in response to various stimuli. Dynamic mechanical properties were measured in stiff, standard, and soft states of the sea cucumber Actinopyga mauritiana. Sinusoidal deformations were applied, either at a constant frequency of 0.1 Hz with varying maximum strain of 2%-20% or at a fixed maximum strain of 1.8% with varying frequency of 0.0005-50 Hz. The dermis showed viscoelasticity with both strain and strain-rate dependence. The dermis in the standard state showed a J-shaped stress-strain curve with a stiffness of 1 MPa and a dissipation ratio of 60%; the curve of the stiff dermis was linear with high stiffness (3 MPa) and a low dissipation ratio (30%). Soft dermis showed a J-shaped curve with low stiffness (0.3 MPa) and a high dissipation ratio (80%). The strain-induced softening was observed in the soft state. Stiff samples had a higher storage modulus and a lower tangent delta than soft ones, implying a larger contribution of the elastic component in the stiff state. A simple molecular model was proposed that accounted for the mechanical behavior of the dermis. The model suggested that stiffening stimulation increased inter-molecular bonds, whereas softening stimulation affected intra-molecular bonds. The adaptive significance of each mechanical state in the behavior of sea cucumbers is discussed.

Interfibrillar stiffening of echinoderm mutable collagenous tissue demonstrated at the nanoscale

“…Samples were rinsed in ASW after sectioning. After the sections were prepared, and before mechanical testing, all samples were allowed to relax in ASW for 1 h. Following this, specimens were incubated in ASW (control), KASW (stiff; high [K + ]), or CaF-ASW (soft) for 1.5 h. Compositions of these three solutions (ASW, KASW, and CaF-ASW) followed the protocol described previously by Motokawa and Tsuchi (14). As expected, this procedure resulted in relative elevation and reduction of stiffness for KASW-treated and CaF-ASW-treated dermis, consistent with other studies of chemically treated MCT (30).…”

“…A notable exception is the mutable collagenous tissue (MCT) of echinoderms (e.g., starfish, sea urchins, sea cucumbers), which undergoes rapid changes in stiffness under the control of the nervous system via ATP-independent mechanisms (10)(11)(12). MCT is ubiquitous in echinoderms (12), for example, in the dermis (skin) of sea cucumbers (13,14), in the compass depressor ligament (CDL) of sea urchins (15)(16)(17), and in the arms of feather stars (18). The presence of MCT enables functionally diverse behaviors; for example in starfish, MCT enables body wall stiffening during feeding on prey and it also enables irreversible body wall softening before arm autotomy as a defense against predation (12).…”

“…The initial identification of connective tissue of echinoderms as having mechanically unusual properties-illustrated by its denotation as "catch" connective tissue-was through the observed stiffening and softening response of such tissues to sea water of different ionic compositions, as well as neurotransmitters (e.g., acetylcholine) (14) and drugs (e.g., cocaine) (21). Such chemical means to induce mutability in MCT remain a convenient and reproducible method to induce mechanically altered states (15,22,23).…”

“…Such chemical means to induce mutability in MCT remain a convenient and reproducible method to induce mechanically altered states (15,22,23). Specifically, previous studies demonstrated that alteration of extracellular Ca 2+ and K + levels modulates the stiffness of living tissues in sea urchin spine ligaments (14,(24)(25)(26)(27)(28), holothurian dermis (13,22,29,30), and starfish (30). Increased K + concentration increases the stiffness of these particular examples of MCT, whereas decreased Ca 2+ concentration lowers stiffness, compared with artificial sea water (ASW) as a reference solution.…”

Unfolding/Refolding Study on Collagen from Sea Cucumber Based on 2D Fourier Transform Infrared Spectroscopy

“…The dermis of the body wall is a typical connective tissue with mutable mechanical properties that rapidly changes in response to various stimuli [2]. Although the body walls of uncooked sea cucumbers are very hard to masticate, they become as tender as jelly after cooking [3].…”