The musculotendinous system of an anguilliform swimmer: Muscles, myosepta, dermis, and their interconnections in Anguilla rostrata

Abstract

Eel locomotion is considered typical of the anguilliform swimming mode of elongate fishes and has received substantial attention from various perspectives such as swimming kinematics, hydrodynamics, muscle physiology, and computational modeling. In contrast to the extensive knowledge of swimming mechanics, there is limited knowledge of the internal body morphology, including the body components that contribute to this function. In this study, we conduct a morphological analysis of the collagenous connective tissue system, i.e., the myosepta and skin, and of the red muscle fibers that sustain steady swimming, focusing on the interconnections between these systems, such as the muscle-tendon and myosepta-skin connections. Our aim is twofold: (1) to identify the morphological features that distinguish this anguilliform swimmer from subcarangiform and carangiform swimmers, and (2) to reveal possible pathways of muscular force transmission by the connective tissue in eels. To detect gradual morphological changes along the trunk we investigated anterior (0.4L), midbody (0.6L), and posterior body positions (0.75L) using microdissections, histology, and three-dimensional reconstructions. We find that eel myosepta have a mediolaterally oriented tendon in each the epaxial and hypaxial regions (epineural or epipleural tendon) and two longitudinally oriented tendons (myorhabdoid and lateral). The latter two are relatively short (4.5-5% of body length) and remain uniform along a rostrocaudal gradient. The skin and its connections were additionally analyzed using scanning electron microscopy (SEM). The stratum compactum of the dermis consists of approximately 30 layers of highly ordered collagen fibers of alternating caudodorsal and caudoventral direction, with fiber angles of 60.51 +/- 7.05 degrees (n = 30) and 57.58 +/- 6.92 degrees (n = 30), respectively. Myosepta insert into the collagenous dermis via fiber bundles that pass through the loose connective tissue of the stratum spongiosum of the dermis and either weave into the layers of the stratum compactum (weaving fiber bundles) or traverse the stratum compactum (transverse fiber bundles). These fiber bundles are evenly distributed along the insertion line of the myoseptum. Red muscles insert into lateral and myorhabdoid myoseptal tendons but not into the horizontal septum or dermis. Thus, red muscle forces might be distributed along these tendons but will only be delivered indirectly into the dermis and horizontal septum. The myosepta-dermis connections, however, appear to be too slack for efficient force transmission and collagenous connections between the myosepta and the horizontal septum are at obtuse angles, a morphology that appears inadequate for efficient force transmission. Though the main modes of undulatory locomotion (anguilliform, subcarangiform, and carangiform) have recently been shown to be very similar with respect to their midline kinematics, we are able to distinguish two morphological classes with respect to the shape and tendon architecture of myosepta. Eels are similar to subcarangiform swimmers (e.g., trout) but are substantially different from carangiform swimmers (e.g., mackerel). This information, in addition to data from kinematic and hydrodynamic studies of swimming, shows that features other than midline kinematics (e.g., wake patterns, muscle activation patterns, and morphology) might be better for describing the different swimming modes of fishes.