Diadema setosum sea urchins. Photo credit: Tatsuo Motokawa.

Diadema setosum sea urchins. Photo credit: Tatsuo Motokawa.

Most connective tissue is fairly inert, providing padding or holding cells and tissue in place. But when soft starfish want to prise apart a mollusc or a sea urchin wants to hold its spines rigid, they stiffen a unique form of connective tissue, known as catch connective tissue, to hold themselves firm. ‘The merit of this tissue is economy’, says Tatsuo Motokawa from the Tokyo Institute of Technology, explaining that the tissue can maintain a posture over lengthy periods with very little energy cost, unlike muscle, which requires a constant supply of energy. Motokawa adds that there was plenty of indirect evidence that changes in the material properties of this exotic tissue were controlled by nerves, but there was no definitive proof. So, as he approached retirement, Motokawa set his focus on finally proving that the well-documented dramatic material changes that catch connective tissue undergo to either hold structures rigid or soften are controlled by nerves (p. 703).

Unfortunately, doing neurophysiology on echinoderms is very difficult: ‘Action potentials are seldom observed in echinoderm nerves’, Motokawa explains, adding that electrical signals caused by stimuli only travel small distances in echinoderm tissue, making it hard to decide whether an electric current was propagated through the nerves or simply spread through the tissue to directly stimulate a target. However, he knew that sea urchins (Diadema setosum) wave their spines when a shadow passes over – in a bid to avoid being nibbled by a fish – and that the movement is controlled by the radial nerve. He also reasoned that the catch connective tissue encasing the spine joint must soften in synch with activation of the muscles that move the spines. Motokawa realised that if he could show that shadows caused the catch connective tissue to soften in conjunction with spine waving, then: he says, ‘We could provide the definitive evidence for coordination…[that] is mediated by nerves’.

Carefully dissecting sections of the delicate sea urchin shell – complete with spines and intact nerve – and then slowly wiggling one spine (at 0.1 Hz) to measure the catch connective tissue stiffness, Yoshiro Fuchigami began testing the effects on the spine joint of a gentle nudge and plunging the urchin shell into darkness (to simulate a passing shadow). Tapping the spine, Fuchigami found that it became immobile and upright while the connective tissue stiffened 1.5 times within 10 s of the impact. However, when he tapped the adjacent spine, the catch connective tissue in the joint of the spine that he was studying softened, in a bid to lay flat to protect the region of shell that had just been touched (known as the ‘convergence response’). And when Fuchigami turned the light off, the spine began waving as the muscles activated while the stiffness of the connective tissue halved. However, when Fuchigami cut the nerve to the spine before turning the lights out, the spine no longer waved and the connective tissue remained stiff. Finally, Fuchigami electrically stimulated the base of the spine and the connective tissue softened again, exactly as it had done when he simulated the effect of a passing shadow.

‘The present results clearly showed coordination between the catch apparatus and spine muscles through nerves’, says Motokawa, who is pleased to have finally confirmed that catch connective tissue is under neural control, and is optimistic that the next generation of smart materials could benefit from the lessons that sea urchins can teach us.

Coordination between catch connective tissue and muscles through nerves in the spine joint of the sea urchin Diadema setosum
J. Exp. Biol.