Muscle system organization in the echinoderms: II. Microscopic anatomy and functional significance of the muscle‐ligament‐skeleton system in the arm of the comatulids (Antedon mediterranea)

Abstract

Comatulids are able to perform quick and complex movements of the arms which are used to swim, creep, walk, and also form a rigid, feeding-filtration fan. To perform such versatile movements, the arms of these animals are equipped with a classical endoskeletal system, with joints, muscles, ligaments, and a hydroskeleton of three different coelomic channels. Light microscopic study of the detailed anatomical organization of the arm clarifies both the complex relations between the parts involved in the movements and their functional responsibilities. In particular, (1) the ventral muscle bundles show a heterogeneous structure that consists of different and variously arranged populations of fibers, which allows the different flexing movements of the arms (i.e., flexion and maintaining the flexed state); (2) the ligaments (both dorsal and interarticular) consist only of collagen fibrils and, therefore, have a passive function in binding the skeletal pieces together: their possible active engagement in the extending movements of the arms is thus excluded; (3) owing to the absence of other suitable antagonists to the flexor muscles, the only efficient antagonist system seems to be the coelomic cavities, which are well separated from each other and are also provided with muscular valves. They thus function as typical hydraulic systems, which allows the arm to perform both simple extensions and very complex combined movements and to maintain some rigid straight or twisted positions.

The Role of Ligaments in Arm Extension in Feather Stars (Echinodermata: Crinoidea)

“…Instead, both these workers conclusively demonstrated that the aboral and not the oral nerve mediates swimming behavior. The wounds made by Carpenter and Marshall were relatively small and thus do not conclusively refute the idea of Candia Carnivali and Saita (1985) that hydrostatic pressure extends the feather star arm. According to these last authors, the coelomic canals become constricted by intrinsic muscles at intervals along the length of the arm and hydrostatic pressure then builds up in the lumen of each canal segment, alternating with the constrictions; as already mentioned, this pressure results from contractions of intrinsic muscles in the canal walls and extrinsic muscles in the surrounding tissues.…”

“…The coelomic spaces in the arm are the water canal, the genital canal, the subtentacular canal and the aboral canal (the detailed, three-dimensional topography of these coeloms is illustrated in Grimmer and Holland 1979). The subtentacular and aboral canals are the coeloms that are most important for the hydraulic extension mechanism proposed by Candia Carnivali and Saita (1985). After our gouging operation on the proximal half of each arm LM and SEM showed that we had removed the soft tissues oral to the dashed line in Fig.…”

“…According to these last authors, the coelomic canals become constricted by intrinsic muscles at intervals along the length of the arm and hydrostatic pressure then builds up in the lumen of each canal segment, alternating with the constrictions; as already mentioned, this pressure results from contractions of intrinsic muscles in the canal walls and extrinsic muscles in the surrounding tissues. If one assumes for a moment that Candia Carnivali and Saita (1985) are correct about the series of constrictions along the coelomic canals, the gouging away of a short stretch of a given canal would not release the hydrostatic pressure in any part of the canal beyond the nearest constriction proximal and distal to the wounded zone. Therefore, we destroyed the coelomic canals along the entire proximal half of all ten arms of Florometru serrutissirnu.…”

“…Although it has long been accepted that this arm extension results entirely from the elasticity of ligaments (CuCnot 1948, Hyman 1955, Breimer 1978, this view has recently been challenged. The alternative view, proposed by Candia Carnivali and Saita (1985), is that the ligaments of the feather star arm perform no more than "a passive function in binding the skeletal pieces together: their possible active engagement in the extending movement of the arms is thus excluded." In addition, Candia Carnivali and Saita (1985) concluded that the motive force for arm extension is supplied not by elastic ligaments, but by hydraulic pressure in the coelomic cavities of the arm; this pressure results from contraction of intrinsic muscles in the canal walls and extrinsic muscles in the surrounding tissues.…”

“…The alternative view, proposed by Candia Carnivali and Saita (1985), is that the ligaments of the feather star arm perform no more than "a passive function in binding the skeletal pieces together: their possible active engagement in the extending movement of the arms is thus excluded." In addition, Candia Carnivali and Saita (1985) concluded that the motive force for arm extension is supplied not by elastic ligaments, but by hydraulic pressure in the coelomic cavities of the arm; this pressure results from contraction of intrinsic muscles in the canal walls and extrinsic muscles in the surrounding tissues. Because these conclusions about the dynamics of swimming were based entirely on static histological data, we have investigated the same problem experimentally.…”