Mechanical properties of sea-urchin lantern muscles: a comparative investigation of intact muscle groups in Paracentrotus lividus (Lam.) and Stylocidaris affinis (Phil.) (Echinodermata, Echinoidea)

The jaw apparatus, or lantern, of sea-urchins contains five pairs of retractor and protractor muscles which are responsible for lantern displacement. Using intact retractor or protractor groups, the force-length relations of these muscles were compared in two taxonomically distant species, Paracentrotus lividus and Stylocidaris affinis. The total contractile forces generated by the muscles can be resolved into vertical and horizontal components. It was found that the vertical component of the retractors is maximal at a lantern position which is significantly lower (i.e. more protruded) in Paracentrotus than in Stylocidaris. Total forces generated by the retractors were in both species maximal at or above the lantern `resting positions'. In Paracentrotus alone, the total force-displacement curves tended to be bimodal. It is hypothesized that the retractors of Paracentrotus contain two populations of muscle fibres, one adapted for jaw opening and one for lantern retraction. No significant differences in the properties of the protractors of the two species could be identified. The lantern of Paracentrotus is more mobile than that of Stylocidaris and is able to exploit a wider range of food sources. This investigation has shown that the force-length relations of the lantern muscles match their differing working conditions. Accepted: 3 November 1997     

Mechanical analysis of the sea-urchin lantern: the overall system in Paracentrotus lividus

The dental apparatus or Aristotle's lantern of sea-urchins is a complex system of interacting skeletal ossicles, joints, muscles and ligaments arranged in a rigorous geometry and involved in a variety of activities. In this paper we study the movement of the whole lantern system modelled as a rigid body. The model lantern is constrained at its apex by the peristomial membrane and its movement is controlled by five pairs of antagonistic forces (retractor and protractor muscles). The other main forces applied to the lantern are the elastic reactions of both muscles and ligamental structures (compass depressors and peristomial membrane). The lantern is allowed to perform vertical movements and lateral inclinations but cannot rotate around its main axis. The equilibrium conditions of the system have been found by means of a numerical iterative procedure for solving non-linear equations. The results of the present analysis allow simulation of the overall mechanical activity of the lantern taking into account the experimental data regarding active and passive muscular forces and the tensile constraints due to ligaments.     

The lantern of Aristotle: organization of its coelom and origin of its muscles (Echinodermata,Echinoida)

Summary Comparative ultrastructural analyses of the muscles that work the lantern of Aristotle support the opinion that the muscles in question are myoepithelially organized or derivatives of myoepithelia. They are part of the epithelium of the peripharyngeal cavity (=lantern coelom). The coelom epithelium may become multiplelayered in certain regions and is composed of (1) a layer of muscle cells that vary in number and size, (2) nerve cells and their processes that are interspersed between the muscle layer and (3) monociliated adluminal cells that build a continuous cell lining and completely cover the muscle layer. According to their complexity, the lantern muscles exhibit consecutive stages of myoepithelial variations and may finally simulate subepithelial musculature. The results of this study support the hypothesis of a histological development of subepithelial musculature from simple myoepithelia, although both epithelial and mesenchymal musculature may occur in the Echinodermata. Detailed knowledge of the organization of the lantern's coelom space was a prerequisite for the present study. In contrast to previous examinations the lantern coelom is not a continuous space, but is subdivided into several cavities that are partially completely separated from each other. On the one hand, this subdivision is probably caused by the sophisticated arrangement of the lantern's ossicles and on the other by the septa that give rise to muscles that fulfill different functions. lanter's ossicles and on the other by the septa that give     

Congruence between muscle activity and kinematics in a convergently derived prey-processing behavior

Quantification of anatomical and physiological characteristicsof the function of a musculoskeletal system may yield a detailedunderstanding of how the organizational levels of morphology,biomechanics, kinematics, and muscle activity patterns (MAPs)influence behavioral diversity. Using separate analyses of theseorganizational levels in representative study taxa, we soughtpatterns of congruence in how organizational levels drive behavioralmodulation in a novel raking prey-processing behavior foundin teleosts belonging to two evolutionarily distinct lineages.Biomechanically divergent prey (elusive, robust goldfish andsedentary, malleable earthworms) were fed to knifefish, Chitalaornata (Osteoglossomorpha) and brook trout, Salvelinus fontinalis(Salmoniformes). Electromyography recorded MAPs from the hyoidprotractor, jaw adductor, sternohyoideus, epaxialis, and hypaxialismusculature, while sonomicrometry sampled deep basihyal kinesisand contractile length dynamics in the basihyal protractor andretractor muscles. Syntheses of our results with recent analysesof cranial morphology and raking kinematics showed that rakingin Salvelinus relies on an elongated cranial out lever, extensivecranial elevation and a curved cleithrobranchial ligament (CBL),and that both raking MAPs and kinematics remain entirely unmodulated—ahighly unusual trait, particularly among feeding generalists.Chitala had a shorter CBL and a raking power stroke involvingincreased retraction of the elongated pectoral girdle duringraking on goldfish. The raking MAP was also modulated in Chitala,involving an extensive overlap between muscle activity of thepreparatory and power stroke phases, driven by shifts in hypaxialtiming and recruitment of the hyoid protractor muscle. Sonomicrometryrevealed that the protractor hyoideus muscle stored energy fromretraction of the pectoral girdle for ca. 5–20 ms afteronset of the power stroke and then hyper-extended. This mechanismof elastic recoil in Chitala, which amplifies retraction ofthe basihyal during raking on goldfish without a significantincrease in recruitment of the hypaxialis, suggests a uniquemechanism of modulation based on performance-enhancing changesin the design and function of the musculoskeletal system.     

A spicule-reinforced contractile mesentery: organisation and mechanical behaviour of the exterior coelomic septum of Stylocidaris affinis (Echinodermata, Echinoida)

The exterior coelomic septum (ECS) is a mesentery-like structure that encloses the lantern of regular sea-urchins and connects it to the inner surface of the test. This paper describes the ultrastructure and microarchitecture of the ECS in Stylocidaris affinis (Cidaridae, Echinoida) and provides information on its contractile and passive mechanical properties. The ECS forms five interambulacral pouches each of which has adthecal (test-facing) and adambulacral (ambulacrum-facing) walls. The ECS wall comprises two coelothelia separated by a layer of connective tissue. The outer coelothelium is a single layer of monociliated cuboidal peritoneocytes and basally located axon-like processes. The inner coelothelium is a single layer of squamous peritoneocytes overlying axon-like processes and, in the adthecal regions only, parallel arrays of elongated myocytes orientated obliquely or horizontally. The intraseptal connective tissue consists mainly of collagen fibrils with sparsely distributed spherule cells and cells containing heterogeneous vesicles. In the adambulacral regions of the ECS hollow beaded microfibrils 20–23 nm in diameter form fibre-like aggregations. This layer also contains calcite spicules of variable size, shape, abundance and orientation. Isolated preparations of the ECS show concentration-dependent contractile responses to K⁺ ions and acetylcholine. The magnitude of the contractile force varies with the vertical position of the lantern (which determines the starting length of the ECS) in an unusual pattern. Cyclical loading-unloading tests indicate that, as the lantern is raised, the ECS shows low stiffness until the lantern reaches its normal resting position. It is concluded that the adthecal regions of the ECS help to set a limit to lantern retraction and that their contractility assists the protractor muscles in exerting a downward pull on the lantern. Accepted: 24 August 2000     

How do ants stick out their tongues?

The mouthparts are very important tools for almost any task performed by ants. In particular, the labiomaxillary complex is essential for food intake. In the present study we investigated the anatomical design of the labiomaxillary complex in various ant species, focusing on movement mechanisms. Six labial and six maxillary muscles with different functions control the several joints and ensure the proper performance of the labiomaxillary complex. According to our measurements of sarcomere lengths, muscle fiber lengths and diameters, and the relative muscle volumes, the labial and maxillary muscles feature rather slow than fast muscle characteristics and do not seem to be specialized for specific tasks. Since glossa protractor muscles are absent, the protraction of the glossa, the distal end of the labium, is a nonmuscular movement. By histological measurements of hemolymph volumes we could exclude a pressure-driven mechanism. Additional experiments showed that, upon relaxation of the glossa retractor muscles, the glossa protracts elastically. This elastic mechanism possibly sets an upper limit to licking frequency, thus influencing food intake rates and ultimately foraging behavior. In contrast to many other elastic mechanisms among arthropods, glossa protraction in ants is based on a mechanism where elasticity works as an actual antagonist to muscles. We compared the design of the labiomaxillary complex of ants with that of the honeybee and suggest an elastic mechanism for glossa protraction in honeybees as well.     

The interpyramidal muscle of Aristotle's lantern: its myoepithelial structure and its growth (Echinodermata,Echinoida)

Summary The interpyramidal muscles of the lantern of Diadema setosum have been studied as an example of such muscles in regular echinoids. The light- and electron microscopic study proves that the interpyramidal muscle is nothing but a continuous, highly folded myoepithelium. Although it is a powerful and specialized comminator muscle its histological organization (a pseudostratified myoepithelium) is rather simple when compared with other echinoderm myoepithelia. It consists of only two cell types: 1) a single layer of well-developed myocytes and 2) monociliated adluminal cells that totally cover the myocytes and touch the basal lamina by thin basal processes. The interpyramidal muscle grows by addition of new folds to its upper region. Consecutive stages of the myoepithelial differentiation are found in each of the young folds. The origin of the cells which are necessarily added to the growing epithelium is unknown. The growth rate of the muscle is in accordance with the enlargement of the lantern ossicles. The respective data are discussed in detail.     

Muscles advance the teeth in sand dollars and other sea urchins

We demonstrate the action of the dental promoter muscles in advancing the continuously growing teeth of sand dollars and sea urchins. Teeth wear at the occlusal end, while new calcite is added to the opposite end. Dental ligaments rigidly hold teeth during chewing, but soften and reform during advancement. The source of forces that advance the teeth was unknown until our discovery of the dental promoter muscles. The muscles, which underly the tooth, attach centrally to the stereom of the pyramid of the Aristotle''s lantern (jaw) and peripherally to a membrane that covers the distal end of the tooth. The muscles shorten along an axis nearly parallel to the long axis of the tooth. We stimulated contraction by addition of acetylcholine, with increasing concentrations of acetylcholine generating higher forces. Forces exerted by this muscle are appropriate for its size and are 1000 times lower than forces exerted by interpyramidal muscles that generate chewing forces. In sand dollars, a single muscle contraction of the dental promoter muscle can account for half the mean daily advancement of the teeth.     

Further pharmacological study on the cholinergic and glutaminergic properties of the radula muscles of a mollusc,Rapana thomasiana

1. In the radula protractor of the prosobranch mollusc Rapana thomasiana, both twitch contractions and acetylcholine contractions were markedly depressed or blocked by propantheline (10⁻⁵ M) and strychnine (10⁻⁵ M), but in the radula retractor, only acetylcholine contraction was markedly affected by the antagonists,2. Glutamate contractions of both of the muscles were little or slightly affected by the drugs.3. Twitch contraction of the protractor was slowly depressed when the muscle was immersed in concanavalin A (0.3 mg/ml), while that of the retractor was first potentiated and then slowly depressed in it.4. In both of the muscles, glutamate contractions were markedly enhanced by the lectin, but acetylcholine contractions were not affected.5. These results support the notion that the principal excitatory neurotransmitter in the protractor is acetylcholine, whereas that in the retractor is glutamate.     

The pelvic girdle and fin in certain Indian hill stream fishes

This paper deals with the functional morphology of the pelvic girdle and fins in various genera of hill stream cyprinid and sisorid fishes. The pelvic plate of Pseudecheneis shows the greatest modification; it is unusually large and reaches the coracoids of the pectoral arch in front.
The elaborate working of the pelvic muscles and their function in bringing about effective adhesion by the pelvic fins is described in detail. The formation of a new muscle, M. pars retractor ischii of the M. mesioventralis, is reported in Garra and Psilorhynchus (Cyprinidae) and in Glyptothorax and Pseudecheneis (Sisoridae). In Pseudecheneis , the complete separation of this muscle from the M. mesioventral, and modification of the M. protractor ischii, are discussed in relation to the crawling habit of the genus. The appearance of the M. arrector pel vicalis ventralis in Glyptothorax and Pseudecheneis among sisorids has been associated with the adhesive function of the outer ray.     

Ontogeny of the hyoid musculature in the African catfish, Clarias gariepinus (Burchell, 1822) (Siluroidei: Glariidae)

Three ontogenetic stages of the African catfish Clarias gariepinus have been used to describe and discuss the ontogeny of the hyoid musculature. During ontogeny, an asynchrony in the development of the muscles is observed: the intermandibularis and protractor hyoidei are the first to develop and which bear their insertions, followed by the hyohyoideus inferior and the sternohyoideus. The hyohyoideus abductor and adductor muscles are the last of the hyoid muscles to develop. In the juvenile stage (136.2 mm SL specimen), the intermandibularis is still present. The protractor hyoidei is well developed, as it may play an important role in the opening of the mouth, the elevation of the hyoid bars and, as a typical catfish feature, the displacement of the mandibular barbels. The protractor hyoidei arises as three pairs of muscle bundles (a pars ventralis, a pars lateralis and a pars dorsalis), of which the pars ventralis and the pars lateralis become fused to each other. This fusion gives rise to four different fields of superficial fibres for the manipulation of the mandibular barbels. The pars dorsalis, with its tendinous insertion, may be of more importance for mouth opening and/ or hyoid elevation. The hyohyoid muscle is well differentiated into an inferior, abductor and adductor muscles, acting on the hyoid bars, the branchiostegal rays and the opercular bone.     

Jaw movement kinematics and jaw muscle (EMG) activity during drinking in the pigeon (Columba livia)

Summary Movements of the maxilla and mandible were recorded during drinking in the head-fixed pigeon and correlated with electromyographic activity in representative jaw muscle groups. During drinking, each jaw exhibits opening and closing movements along both the dorso-ventral and rostro-caudal axes which may be linked with or independent of each other. All subjects showed small but systematic increases in cycle duration over the course of individual drinking bouts. Cyclic jaw movements during drinking were correlated with nearly synchronous activity in the protractor (levator) of the upper jaw and in several jaw closer muscles, as well as with alternating activity in tongue protractor and retractor muscles. No EMG activity was ever recorded in the lower jaw opener muscle, suggesting that lower jaw opening in this preparation is produced, indirectly, by the contraction of other muscles. The results clarify the contribution of the individual jaws to the generation of gape variations during drinking in this species.Abbreviations AMEM adductor mandibulae externus muscle - DM depressor mandibulae muscle - EMG electromyographic - GENIO geniohyoideus muscle - LB lower beak - LED light-emitting diode - PQP protractor quadrati et pterygoidei muscle - PVL pterygoideus ventralis muscle, pars lateralis - SeH/StH serpihyoideus or stylohyoideus muscle - UB upper beak     

Cephalic muscle development in the Australian lungfish,Neoceratodus forsteri

Lungfishes are the extant sister group of tetrapods. As such, they are important for the study of evolutionary processes involved in the water to land transition of vertebrates. The evolution of a true neck, that is, the complete separation of the pectoral girdle from the cranium, is one of the most intriguing morphological transitions known among vertebrates. Other salient changes involve new adaptations for terrestrial feeding, which involves both the cranium and its associated musculature. Historically, the cranium has been extensively investigated, but the development of the cranial muscles much less so. Here, we present a detailed study of cephalic muscle development in the Australian lungfish, Neoceratodus forsteri, which is considered to be the sister taxon to all other extant lungfishes. Neoceratodus shows several developmental patterns previously described in other taxa; the tendency of muscles to develop from anterior to posterior, from their region of origin toward insertion, and from lateral to ventral/medial (outside‐in), at least in the branchial arches. The m.protractor pectoralis appears to develop as an extension of the most posterior m.levatores arcuum branchialium, supporting the hypothesis that the m.cucullaris and its derivatives (protractor pectoralis, levatores arcuum branchialium) are branchial muscles. We present a new hypothesis regarding the homology of the ventral branchial arch muscles (subarcualis recti and obliqui, transversi ventrales) in lungfishes and amphibians. Moreover, the morphology and development of the cephalic muscles confirms that extant lungfishes are neotenic and have been strongly influenced via paedomorphosis during their evolutionary history.     

Cranial endothermy and a putative brain heater in the most basal tuna species, Allothunnus fallai

Field studies on the slender tuna Allothunnus fallai revealed cranial temperatures that were 4·8 ± 0·4° C (mean ± s . d .) above the ambient sea surface temperature. Dissections aimed at documenting the cranial heat source revealed a fused extraocular muscle complex positioned beneath the brain of this basal tuna species. The muscle complex is structurally distinct from that documented for any other fish species. In A. fallai , all four extraocular rectus muscle pairs (superior, inferior, medial and lateral rectus) are incorporated into one distinct tissue complex which is positioned between the orbits and in direct contact with the braincase. A combination of morphological, physiological and biochemical techniques were used to characterize the modified muscle tissue, and high-resolution magnetic resonance imaging was used to illustrate its association with the brain and optic nerves. The modified eye muscles lack organized contractile proteins and are perfused by an extensive vascular counter-current system that originates from the internal carotid artery. Vessel diameters, artery–vein configuration, and anatomic position between the systemic circulation and the warm eye muscles all suggest that this system is a heat exchanger. Collectively, these findings suggest that A. fallai has evolved extraocular muscles that may function to warm the brain and eye region. This is the first record of a cranial modification comprised of all four rectus muscles and the only documented occurrence of this mechanism for cranial endothermy among the tunas.     

Morphological convergence of pharyngeal jaw structure in durophagous perciform fish

This study investigated the ecomorphology of pharyngeal jaw structure and durophagy in three families of marine teleosts: the Sciaenidae, Haemulidae and Carangidae. Regressions of the bone and muscle mass of pharyngeal jaws were generated to elucidate the differences associated with eating hard-bodied and soft-bodied prey; within-family comparisons revealed significant differences in masses of bones and muscles involved with processing the former. Generally, the durophagous species − Trachinotus carolinus (Carangidae), Pogonias cromis (Sciaenidae) and Anisotremus surinamensis (Haemulidae) − had heavier and stronger pharyngeal toothplates and larger protractor pectoralis muscles, with masses of these musculoskeletal elements ranging from five times to nearly an order of magnitude larger than those of their soft-prey feeding relatives. Pogonias cromis and T. carolinus demonstrate convergence in the ontogeny and morphological modification of the pharyngeal toothplates and protractor pectoralis muscles that enhance crushing ability. In the Haemulidae, moderate size increases in a few pharyngeal jaw elements (and larger overall body size in A. surinamensis ) are sufficient for durophagy. Morphospace analysis of six species from the three families illustrates the strong functional association between the biomechanical properties of prey and the relative sizes of biting and transport mechanisms.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80 , 147−165.     

The Aristotle's lantern of the sea-urchin Stylocidaris affinis (Echinoida,Cidaridae): functional morphology of the musculo-skeletal system

Summary The Aristotle's lantern, or masticatory apparatus, of regular sea-urchins is a complex musculo-skeletal system which is thought to have contributed significantly to the evolutionary success of these animals. This paper gives an account of the antomical relationships and functional morphology of both skeletal and soft tissue components in the lantern and related structures of the sea-urchin Stylocidaris affinis (Cidaridae), and compares these features with their equivalent in the previously described lantern of the sea-urchin Paracentrotus lividus (Echinidae, Camarodonta). There are major differences in the skeletons of these lanterns which involve mostly the arrangement and morphology of elements participating in movement, i.e. joints and articular surfaces, and which highlight the generally heavier and less mobile nature of the lantern in the Cidaridae. There are remarkably few differences, however, in the microstructure of the skeletal stereom. Significant dissimilarities were found in the anatomical arrangement of muscles and ligamentous structures and in their macro- and microstructure. The implications of these morphological features for the functioning of the lantern of the Cidaridae are discussed in the context of an integrated model of lantern biomechanics.     

Diversity of mechanical responses and their possible underlying mechanisms in the proboscis muscles ofBusycon canaliculatum

Summary Mechanical responses of the radular protractor and retractor, the odontophore retractor and the radular sac muscles ofBusycon canaliculatum were compared. The radular protractor responded to both ACh and high K salines with similar slow, smooth contractures showing no evidence of fast twitch activity. The radular sac, odontophore retractor, and radular retractor muscles responded to low K salines with bursts of fast twitches at a mechanical threshold below that for responses in the radular protractor. With high K salines these three muscles showed inactivation of fast twitch activity and replacement by slow maintained tonic force. With rare exceptions, the ACh responses of all four muscles consisted of slow, maintained tonic contractures with no fast twitch activity, although individual muscles differed in their ACh sensitivity. A scheme is presented to explain the mechanical modus operandi of this complex organ by the co-operative actions of these four physiologically diverse muscles. It is proposed that fast twitch responses depend upon the activity of fast transient Ca channels showing strong voltage sensitivity and ready voltage inactivation. It is proposed that maintained tonic contractures in all the muscles depends upon the activity of slow long-lasting voltage-dependent Ca channels which only open with substantial membrane depolarization. It is suggested that K-induced and ACh-induced responses may activate a similar cellular Ca pool but by different membrane transduction routes.