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Uyeno, T.A. and Kier, W.M. (2015) JOURNAL OF MORPHOLOGY 276:403–414 (2015) The Structure and Function of a Muscle Articulation-Type Jaw Joint of a Polychaete Worm Theodore A. Uyeno* and William M. Kier Department of Biology, University of North Carolina at Chapel Hill, CB #3280, Coker Hall, Chapel Hill, North Carolina 27599 3280 ABSTRACT The arrangement of the musculature and nections between rigid links that allow motion. the fibers of the extracellular matrix (ECM) in the flexible This flexibility, however, causes these joints to jaw joint of the sandworm Alitta virens (Annelida, Poly- buckle when loaded in compression, which may chaeta) was studied using dissection and histology. The explain why they are less common than sliding jaws are capable of a wide range of motions principally joints (Alexander, 1983). Examples include flexible related to defense and feeding. The left and right jaws are embedded in and moved by a compact pharyngeal joints between chiton valves (Wainwright et al. bulb of muscle and ECM that also forms the mouth and 1982) and the flexible cuticle between stiff subsec- esophagus. Eight pharyngeal bulbs were removed and dis- tions of locust tarsi (Alexander, 1983). sected to document gross anatomical features or pre- The muscular joint between octopus beaks rep- served and embedded in plastic for sectioning in multiple resents a type of flexible joint that resists compres- planes. The sections were stained with toluidine blue and sion while supporting complex and diverse basic fuchsin to differentiate muscle and ECM. The sec- movements. Because muscle serves a crucial role tions were then digitized and used to develop a three- in support and movement, it has been termed dimensional computer illustration. We hypothesize that a “muscle articulation.” This type of joint relies on the muscle and fibers in the ECM are arranged as a mus- a muscular hydrostatic mechanism in which a cular hydrostat to support the movement of the jaws. Four specimens were recorded using a digital video cam- tightly packed three-dimensional (3D) array of era and a tank with an angled mirror to record lateral muscle fibers functions both as the effector of and ventral views of jaw movements during locomotion movement and as the support for movement. Com- and biting associated with burrow guarding and feeding. plex deformations and movements can be created Frame by frame kinematic analysis of this video showed and the stiffness of the entire structure is under that the jaws move symmetrically in a roughly horizontal active control (Kier and Smith, 1985; Smith and plane. Although the angle between the jaws increases and Kier, 1989). Although the structure and function then decreases after maximum gape has been reached, of this joint type has been investigated the beaks the jaws also translate relative to each other such that of octopus (Uyeno and Kier, 2005, 2007) and in the axis of rotation is not fixed. Together, these functional extensible hook bearing proboscides of interstitial morphological and behavioral data identify the jaw mech- anism as a flexible joint known as a muscle articulation. flatworms (Uyeno and Kier, 2010), the taxonomic As muscle articulations have been previously described distribution and general principles of form and only in the beaks of cephalopods and flatworms, this function have yet to be thoroughly explored. Here, study implies that this type of joint is more common and important than previously recognized. J. Morphol. 276:403–414, 2015. VC 2014 Wiley Periodicals, Inc. Additional Supporting Information may be found in the online version of this article. KEY WORDS: muscle articulation; joint mechanics; jaws; Annelida; polychaeta; Alitta virens; sandworm; Contract grant sponsor: American Microscopical Society Summer king ragworm fellowship; Sigma Xi Grant-in-aid-of-research; Contract grant spon- sor: UNC-CH Department of Biology H.V. Wilson Summer scholar- ship (T.A.U); Contract grant sponsor: National Science Foundation; INTRODUCTION Contract grant number: IBN-9728707; Contract grant sponsor: Animal Joints DARPA (W.M.K.); Contract grant number: N66001-03-R-8043. Joints allow relative motion between adjacent *Correspondence to: Theodore A. Uyeno, Department of Biology, rigid skeletal elements or “links.” In the biological Valdosta State University, 1500 N. Patterson St. Valdosta, GA joint categorization scheme developed by Wain- 31698. E-mail: [email protected] wright et al. (1982) and Alexander (1983), there are two broad structural categories. Sliding joints, Received 21 March 2014; Revised 21 October 2014; common in arthropods and vertebrates, transfer Accepted 18 November 2014. loads directly between abutting links; the shapes Published online 15 December 2014 in of the contacts govern possible movements (Wain- Wiley Online Library (wileyonlinelibrary.com). wright et al., 1982). Flexible joints are pliable con- DOI 10.1002/jmor.20349 VC 2014 WILEY PERIODICALS, INC. 404 T.A. UYENO AND W.M. KIER Fig. 1. Alitta virens, A) A three-quarter dorso-frontal view of the first body segment (chaetiger) and head (peristomium and prostomium) with the pharyngeal bulb (blue) and jaws (gold) ever- ted. B) A ventral (left) and medial (right) view of a 3D reconstruction of the right jaw of A. virens showing its parts (see text). we present an analysis of the movement, morphol- ecological niches. The Nereididae show a range of ogy, and biomechanics of the Nereididae jaw joint feeding modes including omnivory (Goerke, 1971), to elucidate the general principles of support and herbivory (Copeland and Wieman, 1924), detritivory, movement in this dynamic joint type. and carnivory (Goerke, 1971; Fauchald and Jumars, 1979). They also absorb dissolved organic matter The Jaws and Pharynx of Phyllodocida (Stephens, 1968). Alitta virens juveniles are likely Polychaetes detritus feeders and the adults have diverse carniv- orous or omnivorous diets, consuming vegetal or A biomechanically useful classification system of animal detritus, diatoms, crustaceans, gastropods, polychaete feeding strategies proposed by Dales foraminiferans, nematodes, hydrozoans, and poly- (1962) shows a striking diversity. This diversity chaetes (Caron et al. 2004). may be due to foregut adaptability (Fauchald and Jumars, 1979; Markert et al., 2007) resulting in a remarkable range of pharyngeal morphology Jaw Movements in Alitta virens (Rouse and Fauchald, 1997). The pharynx is com- Alitta virens uses pharyngeal bulb eversions and monly in an axial position and muscularization of quick, forceful jaw movements in feeding, defense, the pharyngeal wall to form a fortified pharyngeal and burrowing. Despite the variation in diet and bulb is also common (Dales, 1962). This axial mus- feeding modes in the Nereididae, the morphology cular bulb is perhaps the most prominent in the (Pilato, 1968a) and jaw movements during feeding Phyllodocida (Rouse and Fauchald, 1997) in which (Turnbull, 1876; Gross, 1921; Copeland and Wie- it supports two large jaw elements embedded in man, 1924) are similar. During biting, the probos- muscle that may function as a muscle articulation. cis is rapidly turned inside out so that the The focus of this study is on one of the species in pharyngeal bulb is anteromost (Fig. 1A) with the this group, the King Ragworm or clamworm, Alitta jaws in a half-opened gape. The jaws are opened virens (Sars 1835) sensu Pettibone (1963 as Nereis and closed to cut algal blades or large prey. virens), Nereididae. These large, common, widely Smaller pieces of food are then grasped with the distributed (Wilson and Ruff, 1988; Olive, 1993) jaws and the bulb is retracted. marine worms are of considerable ecologic and Alitta virens also uses its jaws for defense. A. commercial importance (Brown, 1993, Goerke, virens is extremely thigmotactic (Copeland and 1971; Commito, 1982). They are speciose (Fauchald, Wieman, 1924) and spends most of its time within 1977; Bakken and Wilson, 2005) and inhabit a vari- its burrow (Turnbull, 1876) where it preferentially ety of habitats (Pettibone, 1963; Wilson, 2000) and feeds from the entrance (Fauchald and Jumars, Journal of Morphology THE RAGWORM JAW MUSCLE ARTICULATION 405 1979; Wilson and Ruff, 1988) and vigorously defends as the esophagus. The musculature of the bulb is the burrow against predators and conspecifics complex with muscle fibers of many orientations. (Turnbull, 1876; Gross, 1921; Evans, 1973; Miron Pilato (1968a) grouped muscles into those that et al., 1992a, 1992b; Lewis et al, 2003). The defen- originate on the jaws and those that do not. The sive pharyngeal bulb movements are similar to prey jaw muscles include thirteen pairs of jaw protrac- capture and food manipulation: rapid extension of tors and retractors, jaw base adductors and abduc- the bulb followed by a forceful closing of the jaws as tors, jaw fang adductors, and jaw elevator and the proboscis retracts. A single bite can cut an adult depressor muscles. The names reflect as yet conspecific in two (Turnbull, 1876). untested hypotheses of function. Muscles not attached to the jaws include eight orientations of muscle fibers dispersed throughout the bulb Jaw Morphology named for their arrangement rather than their Jansonius and Craig (1971) established the ter- actions: the superficial circular, transverse and minology used here to describe Nereididae jaw longitudinal fibers, radial fibers, dorsoventral structures (Fig. 1B). The two sharp, nonarticu- transverse fibers, and posterolateral fibers. lated, hook-shaped jaws resemble open-ended In this study, we analyze the morphology and cones with curved anterior tips referred to as kinematics of the pharyngeal bulb of A. virens to fangs. A series of teeth, or denticles, are found develop hypotheses of the functional role of the along the hardened inner margin formed at the muscle and a fibrous sheath of extracellular matrix sharp edge of the inner face (Birkedal et al., (ECM). One difficulty in assessing muscular func- 2005). The opening at the base of the cone is tion in a structure with many fiber orientations is referred to as the myocoele opening and leads to an in understanding how the contraction of one orien- innerspaceknownasanantrumormyocoele.The tation affects others.
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