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Variable Tensility of the Ligaments in the Stalk of Sea-Lily

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Variable Tensility of the Ligaments in the Stalk of Sea-Lily FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: © 1994 Elsevier B.V. This manuscript is an author version with the final publication available by http://www.sciencedirect.com/science/journal/03009629 and may be cited as: Wilkie, I. C., Emson, R. H., & Young, C. M. (1994). Variable tensility of the ligaments in the stalk of sea‐lily. Comparative Biochemistry and Physiology Part A: Physiology, 109(3), 633‐641. doi:10.1016/0300‐9629(94)90203‐8 Camp. Biod~em. Plqxiol. Vol. 109A. No. 3, pp. 633-64 I, 1994 Pergamon Copyright I$; 1994 Elsevier Science Ltd Printed in Great Britain. All rights reserved 03~-9629~94 $7.00 t 0.00 0~%2~%~1~9 Variable tensility of the ligaments in the stalk of a sea-lily I. C. Wilkie,* R. H. Emson”f and C. M. Young1 *Department of Biological Sciences, Gfasgow Caledonian University, 70 Cowcaddens Road, Glasgow G4 OBA, U.K.; tDivision of Life Sciences, King’s College, Campden Hill Road, London W8 7AH, U.K.; and $Harbor Branch Oceanographjc Institution, Box 196, Fort Pierce, FL 33450, U.S.A. The stalk of isocrinid sea-lilies consists largely of skeletal plates linked by collagenous ligaments. Although lacking contractile tissue, it can bend in response to external stimuli. The stalk of Cctnocrinusaster& was tested mechanically to determine whether the mechanical properties of its ligaments are under physiological control. In bending tests, ligaments at the mobile symplexal junctions showed a limited “slackening” response to high K+ concentrations which was blocked reversibly by the anaesthetic propylene phenoxetol. In bending tests and uniaxial loading tests, ligaments at the normally rigid synostosal junctions ruptured in response to high K+, con~~ing that these junctions are specialized for autotomy. It is concluded that the ligaments are mutable collagenous structures whose presence explains the mechanical versatility of the isocrinid stalk. Key words: Autotomy; Collagen; Crinoidea; Echinodermata; Mutable collagenous tissue; Sea-lily; Stalk ligaments; Variable tensility. Comp. Biochem. Physiol. lOgA, 633-641, 1994. In~od~ction The sea-lily stalk consists of a series of the virtually stalkless Cyrtocrinida; see disc-shaped ossicles connected by collage- Grimmer and Holland, 1990) has estab- nous ligaments. It functions primarily as lished that the stalk lacks any form of a strut which holds the main body of the musculature (Grimmer et al., 1984, 1985; animal with its crown of suspension-feeding Holland et al., 1991), it has been conjec- arms above the substratum. However, ob- tured that its flexibility can be altered servation of animals in situ has shown that through changes in the mechanical proper- the stalk can also bend to permit changes ties of the stalk ligaments (Donovan, 1989; in the orientation of the crown (Messing, Baumiller et al., 1991). 1985; Fujita et al., 1987; Baumiller et al., Collagenous tissues showing such vari- 1991). Since an ultrastructural examination able tensility, i.e. mutable collagenous of representatives of the three extant orders tissues (MCTs), are ubiquitous in the of truly stalked sea-lilies (i.e. excluding echinoderms and serve two main functions. Firstly, through reversible changes in tensile stiffness, they provide an energy-sparing Correspondence to: 1. C. Wilkie, Department of Bio- logical Sciences, Glasgow Caledonian University, means of fixing posture. Secondly, through 70 Cowcaddens Road, Glasgow G4 OBA, U.K. irreversible disintegration, they permit Received 3 March 1994; accepted 10 June 1994. autotomy of appendages or parts of the 633 634 I. C. Wilkie et al. body (Wilkie and Emson, 1988; Candia Materials and Methods Carnevali and Wilkie, 1992). With regard to the crinoids, it has been We collected specimens of the isocrinid demonstrated experimentally that the vari- sea-lily Cenocrinus asterius (L.) by suction able stiffness of the finger-like cirri in un- hose at a depth of around 600 m during two stalked comatulids depends on the presence dives in the Johnson-Sea-Link I submers- of MCTs (Wilkie, 1983). However, despite ible at Egg Island and Chub Cay, Common- work on the mechanical properties of the wealth of the Bahamas in May 1993. The sea-lily stalk (Baumiller and LaBarbera, animals were kept in a darkened, aerated 1993), there has been no direct confirmation aquarium at 10°C on board RV Seward that the tensility of its ligaments is under Johnson and used immediately or up to 4 physiological control. This is an important days after capture. omission, since the sea-lilies are the only The stalk ossicles of isocrinid sea-lilies survivors of a wide diversity of stalked are differentiated into nodals that carry the echinoderms which inhabited the seas of the jointed cirri and internodals that lack cirri Palaeozoic era (Paul and Smith, 1984). (Fig. 1). The flexibility of the stalk depends Although these animals were heavily cal- on the presence of mobile joints, or sym- cified, it has been inferred from their skel- plexies, between most of the ossicles, the etal morphology and microstructure that only exception being the junction between their skeletal elements were connected by each nodal and the internodal distal to it muscles only rarely, even in the jointed which is a rigid joint, or synostosis. feeding appendages (equivalent to the arms During the course of mechanical tests, of modern crinoids) (reviewed by Wilkie short lengths of stalk were subjected to and Emson, 1988; see Ausich and Bau- loads of up to 130 g applied through the miller, 1993). In view of their success during lever of an isotonic displacement transducer the Palaeozoic, it is highly unlikely that these animals were entirely unresponsive to external events such as predator attack or changes in bottom current speed and direc- tion. We have therefore speculated that the collagenous ligaments binding their skeletal elements consisted of MCT, and that the reversible “softening” of these ligaments permitted the posture and orientation of both the stalk and feeding appendages to be adjusted passively by gravity and/or water movements (Wilkie and Emson, 1988). The stalk of modern sea-lilies thus serves as an important model for the non- muscularized appendages of Palaeozoic echinoderms. In this paper, we provide data from experiments on the stalk of a sea-lily which indicate that the mechan- ical properties of its ligaments are variable Fig. 1. Diagrammatic representation of a short length and under physiological control. We have of the stalk of an isocrinid sea-lily. The stippled also demonstrated functional differen- ossicles are nodals (no), from each of which emerge tiation between different stalk ligaments: the cirri (ci). Nodals are separated by a series of internodal ossicles (in). The articulations between those at movable articulations show only most of the ossicles are mobile symplexies (symp). reversible changes in stiffness; those at im- However, that between each nodal and the internodal movable articulations show only irrevers- distal to it is a rigid synostosis (syno). The stalk ible disintegration and are involved in stalk ligaments are shown as vertical lines and comprise the autotomy. symplexal ligaments (sml), synostosal ligaments (snl) and peripheral through-going ligaments (ptl); these A preliminary report of some of these last are continuous from the internodal on the distal findings has already been published (Wilkie side of a nodal to the next nodal and therefore do not et al., 1993). cross a synostosis. Sea-lily stalk ligaments 635 lever ternodals on either side were clamped verti- cally and subjected to simple uniaxial tension in the form of a constant load ______.___P_3---------- (Fig. 2~). All experiments were conducted at room 0 temperature (20°C) with the preparations held in air but kept moist by being flooded frequently with seawater or other media. t Results Internodal preparations When a constant load was first applied, (b) cirrus (c) internodal preparations showed an immedi- Fig. 2. Mechanical testing method. Lengths of stalk ate deflection which stabilized within a few were held rigidly at one end in a clamp and the other seconds. Without subsequent treatment, end was attached via a heart clip and silver chain to the preparations did not bend any further. the lever of an isotonic displacement transducer. However, if they were flooded with a Internodal preparations (a) consisted of a series of internodal ossicles and included only symplexal artic- medium containing an elevated potassium ulations (symp). They were clamped horizontally and ion concentration (either seawater mixed showed an upwards deflection (d) when initially with 0.56M KC1 to give a K+ concen- loaded. Nodal preparations included a synostosal tration of 100 mM, or 0.56 M KC1 alone), articulation (syno) and were clamped either horizon- which would be expected to depolarize tally (b) or vertically (c). neural elements, most of them (73%; II = 15) exhibited a further deflection and (Fig. 2a). Two different preparations were then stabilized again, even under high loads used. (Fig. 3). The deflection began 25-106 set (1) Internodal preparations consisted of after the start of treatment (mean + SD: a series of seven to nine internodals and 49.7 +_31.5; II = 11). No internodal prep- included only symplexal articulations. They aration ruptured in response to K+, even were orientated horizontally and clamped at after prolonged exposure (for 16 min) to one end. The other end was attached via a 0.56 M KCl. Elevated K+ concentrations heart-clip and silver chain to the transducer had no effect on preparations which had lever. Application of a load to the other side been immersed for 30 min or more in a of the lever tended to deflect the preparation 0.1% seawater solution of the anaesthetic upwards (equivalent to the lateral flexion of propylene phenoxetol, although responsive- a stalk in its natural vertical attitude) ness was restored after washing in normal (Fig.
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