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Jointed Setae – Their Role in Locomotion and Gait Transitions In Journal of Experimental Marine Biology and Ecology, L 228 (1998) 273±290 Jointed setae ± their role in locomotion and gait transitions in polychaete worms Rachel Ann Merz* , Deirdre Renee Edwards Department of Biology, Swarthmore College, Swarthmore, PA 19081, USA Received 15 August 1997; received in revised form 3 February 1998; accepted 7 February 1998 Abstract Many families of polychaete worms have jointed setae in which the joint is external to the body and is not directly controlled by muscles or nerves. We assessed the role of these specialized structures in the hesionid polychaete, Ophiodromus pugettensis, by examining speed, step length, stride distance, stride frequency and gait transitions in worms with and without setal joints. Individual worms were videotaped while they moved over sandy surfaces at a range of speeds. The worms were then anaesthetized and all their compound setae were trimmed either distally or proximally to the setal joints. After two days of recovery the worms were videotaped a second time while they again moved over sandy surfaces at a range of speeds. From the video tapes we analyzed their locomotory performance before and after setal ablation. Animals in which the setae were shortened but in which the joint was left intact showed no consistent change in speed, step length, stride distance, stride frequency or gait transitions. Animals in which the joint had been removed both changed gaits at slower speeds (walking to undulatory walking and undulatory walking to swimming) and showed a signi®cant decrease in maximum swimming speeds and stride distance. A subset of data containing only cases where the worms were moving at the same speed in the same gait before and after setal ablation was analyzed. In these instances, after the removal of the joint, the worms had signi®cantly smaller stride distances and compensated for this by increasing stride frequency. In O. pugettensis, the undulatory walking gait is analogous to the trot±gallop transition in quadrupedal mammals because the animal switches from moving the appendages on a relatively rigid body to using a combination of body ¯exion and appendage movement to achieve propulsion, however, unlike quadrupedal mammals this transition takes place over a wide range of speeds and at different sites on the body as speed increases. These experiments indicate that jointed setae may be important both in allowing a worm to better control setal contact and traction with the substrate as well as in altering the effectiveness of its swimming stroke. 1998 Elsevier Science B.V. All rights reserved. Keywords: Annelids; Polychaete worms; Ophiodromus pugettensis; Setae; Locomotion; Gaits *Corresponding author. Tel.: 1 1 610 3288051; fax: 1 1 610 3288663; e-mail: [email protected] 0022-0981/98/$ ± see front matter 1998 Elsevier Science B.V. All rights reserved. PII: S0022-0981(98)00034-3 274 R.A. Merz, D.R. Edwards / J. Exp. Mar. Biol. Ecol. 228 (1998) 273 ±290 1. Introduction Polychaete annelids typically have dorsal and ventral arrays of chitinous setae associated with the parapodia of most segments (Fig. 1). Although these familiar structures are used extensively for identi®cation by taxonomists, there is relatively little known about the way they function on living worms (although, see Mettam, 1971, 1984; Roy, 1974; Knight-Jones and Fordy, 1979; Knight-Jones, 1981; Woodin and Merz, 1987). One major variety of these structures, known as jointed or compound setae, are found in 28 polychaete families (Fauchald, 1977; Fauchald and Rouse, 1997). Com- pound setae are associated with mobile or discreetly mobile worms but never with sedentary polychaetes (as de®ned by Fauchald and Jumars, 1979). Each compound seta is the product of a single cheatoblast and associated follicular cells and extends out of the body from the setal sac within a parapodium (Bobin, 1947; Bauchot-Boutin and Bobin, 1954; Schroeder, 1967, 1984; O'Clair and Cloney, 1974; (Fig. 1)). In compound setae, the joint has a socket in which the distal blade of the seta is typically anchored by both a ligament and a hinge (Gustus and Cloney, 1973) (Fig. 2). A functioning joint, therefore, is external to the body and is neither directly controlled Fig. 1. SEM of a midbody parapodium of O. pugettensis, viewed from a ventral anterior position. The notopodium is relatively reduced. Compound setae can be identi®ed throughout the neuropodium, scale bar is 200 mm. R.A. Merz, D.R. Edwards / J. Exp. Mar. Biol. Ecol. 228 (1998) 273 ±290 275 Fig. 2. SEM of morphological details of the compound setae of O. pugettensis. (a): Tip of the distal blade, scale bar 5 1 mm. (b): Ventral view of two unbent setal joints, scale bar 5 10 mm. (c): Lateral view of two setal joints with their distal blades displaced slightly to the side, scale bar 5 2 mm. (d): View of the socket of the setal shaft, the base of the distal blade and the ligamentous attachment, scale bar 5 2 mm. by muscles nor innervated by nerves (Gustus and Cloney, 1973). The way in which compound setae bend at the joint is controlled by the shape of the cup and the attachment of the ligament (Gustus and Cloney, 1973; Schroeder, 1984; Merz and Woodin, 1987) (Fig. 2). We are aware of no report in the literature of the direct observation or test of the function of these setae (Schroeder, 1984). Gustus and Cloney (1973) suggest that based on morphology they expect the blade to move relative to the shaft, although it has no intrinsic power. When the seta is thrust against a substrate the 276 R.A. Merz, D.R. Edwards / J. Exp. Mar. Biol. Ecol. 228 (1998) 273 ±290 joint would allow ¯exibility, albeit con®ned to some degree by the hinge and ligament. This ¯exibility would presumably confer increased friction and reduce slippage. To understand if and how these structures function in polychaete locomotion, we compared the locomotory performance of worms with unaltered setae to the same animals' performances after the compound setae had been trimmed either distally or proximally to the joint (the distal treatment is essentially a control for the process of trimming and the effect of shortening setae; the proximal treatment examines the role of the joint per se). If the joint is crucial in locomotion, then we expected a diminution in performance when it is removed. Merely shortening the setae could also have a negative effect on locomotion; if that is true, then animals with setae that are ablated distal to the joint should have a diminished performance. For our test animal we chose the hesionid polychaete, Ophiodromus pugettensis (5 Podarke pugettensis) which lives from British Columbia to the Gulf of California. It is an active, mobile worm that is found in a variety of habitats including muddy bays, rocky shores, among fouling organisms on ¯oats and pilings and in the subtidal to the continental shelf (Morris et al., 1980; Kozloff, 1983). It can be free living with a diet of small invertebrates (Shaffer, 1979; also see Oug, 1980) or can live as a facultative commensal with a number of different partners (e.g., within the ambulacral grooves of star®sh (mainly Pateria) (Hickok and Davenport, 1957; Lande and Reish, 1968), on the holothurian Protankyra bidentata (Okuda, 1936), with the terebellid polychaete Eupolymnia heterobranchia (Shaffer, 1979), or on hermit crabs together with a nereid polychaete (Berkeley and Berkeley, 1948)). O. pugettensis was selected for this project because (1) it readily displays a variety of locomotory gaits, (2) it naturally lives and moves on a variety of substrates, (3) it has a morphology and size that make it amenable to experimental alteration and (4) it readily adapts to life in the laboratory (often occurring as an accidental resident in sea-water tables). 2. Materials and methods 2.1. Collection and housing of animals Worms were collected by hand during low tide from the mud ¯ats of Garrison Bay, San Juan Island, Washington. They were found crawling on a variety of substrates including the surface of the mud, under and on cockle and clam shells, in mats of algae, and on an old sock. After collection the worms were transferred to sea-water tables at the Friday Harbor Laboratories where they were housed with Enteromorpha and Ulva collected at the same site and presumably inhabited by the copepods and other small invertebrates that are reported to make up the diet of O. pugettensis (Shaffer, 1979). Even though O. pugettensis is often found in the sea-water tables at the laboratories and appears to live well under those circumstances, for these experiments we used only animals that we had collected from the ®eld within the previous ten day period. R.A. Merz, D.R. Edwards / J. Exp. Mar. Biol. Ecol. 228 (1998) 273 ±290 277 2.2. Videotaping techniques We used only active worms whose setae, parapodia and body wall appeared to be undamaged. The worms were relatively similar in size (mean length 21.0 mm, S.D.61.6 mm, n 5 15). Each worm was ®lmed both before and after setal trimming (see below) in a 7.2 3 7.2 cm plastic container in which there was a layer of ®ne grain white sand covered with about 1 cm of sea-water. We used a Sony DXC-107 CCD color video camera attached to a Pentax macrolens mounted above the ®eld of view which was illuminated with a GenRad GR 1546 stroboscope held 7.5 cm above the substrate, ¯ashing at 60 ¯ashes/second. The images were taped at 30 frames/second (this rate was con®rmed during data collection). Each taping sequence began by video recording a millimeter scale placed on the sand surface.
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