Connective tissue in squid mantle is arranged to accommodate strain gradients.

The hollow, cylindrical shape of many soft-bodied animals results in nonuniform circumferential strain across the muscular body wall as the body diameter changes. This could complicate reinforcement with connective tissue because fibers in one region of the body wall must accommodate greater strain than those in other regions. We investigated this issue in the mantle of the squid Doryteuthis pealeii. During escape jet locomotion, the decrease in diameter during the jet requires circumferential strain at the inner surface of the mantle wall to be 1.5 times greater than that at the outer surface of the mantle wall, with a continuous gradient of strain between the two surfaces. We predicted that, to accommodate the greater strain, the intramuscular collagen fibers near the inner surface would either be arranged in a different manner or would have different mechanical properties from fibers near the outer surface. We observed a different arrangement: when the mantle was contracted, fibers from near the inner surface of the mantle wall were significantly more folded than the fibers along the outer surface. When the mantle was fully expanded radially, all of the fibers straightened almost completely, with no significant difference in folding between the inner and outer fibers. The modification of the connective tissue network in the mantle in response to a nonuniform distribution of strain may not be limited to squid, but may be important in other soft-bodied invertebrates and in the walls of blood vessels. Hollow, cylindrical muscular organs and bodies are widespread in animals and are used for movement, locomotion, burrowing, and pumping, with support provided by a hydrostatic skeleton (1, 2). The muscular walls typically lack compressible gas-filled spaces (but see 3), and the tissues are thus essentially constant in volume so that the wall thickness changes when the diameter changes; the magnitude of the thickness change depends on the extent of both diameter change and any simultaneous length change. This change in wall thickness means that when these cylindrical muscular organs change diameter, the circumferential strain (strain is typically defined as the change in length divided by the original length) near the inner surface can be significantly greater than that near the outer surface (4, 5) (Fig. 1A). A nonuniform distribution of circumferential strain has implications for muscle function and also poses challenges for the connective tissue fibers that play critical roles in controlling deformation. Specifically, collagen fiber networks in one region of the body wall may need to accommodate significantly greater strain during locomotion and movement than in other regions. Given the stiffness and limited extensibility of collagen, how are the organization and material properties of collagen fiber networks altered to accommodate these differences in circumferential strain? We investigated aspects of this question in connective tissue fibers in the mantle of squid. The mantle of squid contains distinct networks of intramuscular collagen fibers. We focused on the fibers in a network termed Intramuscular Fiber System 3 (IM-3); the fibers run circumferentially around the mantle, parallel to the circular muscle fibers that provide power for jet propulsion and ventilation of the mantle cavity (6, 7) (Fig. 1B, C). These fibers appear crimped or wavy in a resting or contracted mantle and are thought to provide an upper limit to mantle expansion (8). They have also been implicated in elastic energy storage during certain patterns of respiration and especially during “hyper-inflation” (expansion of the Received 10 March 2014; accepted 23 June 2014. * To whom correspondence should be addressed. E-mail: jkurth@live. unc.edu Reference: Biol. Bull. 227: 1–6. (August 2014) © 2014 Marine Biological Laboratory