JOURNAL OF MORPHOLOGY 273:519-529 (2012) The Locomotory System of PearlfishCarapus acus: What Morphological Features are Characteristic for Highly Flexible Fishes? Cathrin Schwarz,1,2* Eric Parmentier,3 Stefan Wiehr,4 and Sven Gemballa2 1Steinmann-Institut für Geologie, Mineralogie und Paläontologie, Bereich Paläontologie, University of Bonn, Germany institute of Evolution and Ecology, Comparative Zoology, University of Tübingen, Germany 3Laboratoire de Morphologie Fonctionnelle et Evolutive, Institut de Chimie, Université de Liège, Belgium 4Department of Preclinical Imaging and Radiopharmacy, Laboratory for Preclinical Imaging and Imaging Technology of the Werner Siemens-Foundation, Eberhard Karls University of Tübingen, Germany ABSTRACT The body curvature displayed by fishes the other hand, some species like eels show differs remarkably between species. Some nonmuscular extreme body curvatures during routine turns features (e.g., number of vertebrae) are known to influence (review in: Domenici, 2003). One reason for this axial flexibility, but we have poor knowledge of the difference in body curvatures could be a simple influence of the musculotendinous system (myosepta and correlation between axial flexibility and number of muscles). Whereas this system has been described in stiff­ bodied fishes, we have little data on flexible fishes. In this vertebrae (Lindsey, 1978; Long and Nipper, 1996; study, we present new data on the musculotendinous sys­ Brainerd and Patek, 1998). However, exceptions to tem of a highly flexible fish and compare them to existing this simple correlation have been found in sharks data on rigid fishes. We use microdissections with polarized (Kajiura et al., 2003). Furthermore, Porter et al. light microscopy to study the three-dimensional anatomy of (2009) identified a set of 11 nonmuscular features myoseptal tendons, histology and immunohistology to study that correspond to the observed body curvatures the insertion of muscle fiber types into tendons, and p-CT during routing turns in five species of sharks. scans to study skeletal anatomy. Results are compared with Thus, the correlation between axial morphology published data from stiff-bodied fishes. We identify four im­ and axial flexibility seems to be more complex portant morphological differences between stiff-bodied than previously thought. fishes and Carapus acus: ( 1) Carapus bears short tendons in the horizontal septum, whereas rigid fishes have elon­ Besides nonmuscular features that influence body gated tendons. (2) Carapus bears short lateral tendons in flexibility, the musculotendinous system might be its myosepta, whereas stiff-bodied fishes bear elongated another complex that significantly influences axial tendons. Because of its short myoseptal tendons, Carapus flexibility. Although this idea has never been retains high axial flexibility. In contrast, elongated tendons explored, body curvature is not a result of nonmus­ restrict axial flexibility in rigid fishes but are able to cular body mechanics but is under active control of transmit anteriorly generated muscle forces through long the musculotendinous system of the body, i.e., tendons down to the tail. ( 3) Carapus bears distinct epineu- actively produced by trunk muscles. ral and epipleural tendons in its myosepta, whereas these In fishes, these muscles are organized in seg­ tendons are weak or absent in rigid fishes. As these tendons mented blocks of specific three-dimensional (3D) firmly connect vertebral axis and skin in Carapus, we consider them to constrain lateral displacement of the ver­ folding, the myomeres. Adjacent myomeres are tebral axis during extreme body flexures. (4) Ossifications separated by thin sheets of connective tissue, of myoseptal tendons are only present in C. acus and other the myosepta. Muscles and myosepta form the more flexible fishes but are absent in rigid fishes. The func­ musculotendinous system of the trunk. Within this tional reasons for this remain unexplained. J. Morphol. system, muscle fibers insert into myosepta, and 273(519-529, 2012. © 20U Wiley Periodicals, Inc. myosepta are connected to the fibrous dermis and KEY WORDS: myoseptal tendons; body flexibility; fish ^Correspondence to: Cathrin Schwarz, Steinmann-Institut für locomotion; Carapus acus Geologie, Mineralogie und Paläontologie, Bereich Paläontologie, University of Bonn, Nussallee 8, D-53115 Bonn, Germany. INTRODUCTION E-mail: [email protected] The body curvature displayed by fishes is Received 14 February 2011; Revised 31 August 2011; extremely diverse among species. On one hand, Accepted 27 September 2011 fast swimming open ocean predators like tunas or Published online 22 December 2011 in lamnid sharks are known for their relatively stiff Wiley Online Library (wileyonlinelibrary.com) bodies that display only slight body curvatures. On DOI: 10.1002/jmor. 11038 © 2011 WILEY PERIODICALS, INC. 520 C. SCHWARZ ET AL. the vertebral column (Gemballa and Röder, 2004; at the cloaca of the sea cucumber (Fig. 1A) and Danos et al., 2008). Some features of the musculo­ moving the thin tail forward alongside its own tendinous system of the trunk have been identified body at the level of the lateral line until his caudal to be highly conservative among gnathostome extremity is inside the holothurian (Fig. 1B-E). fishes. For example, the 3D-folding of myosepta is After this initial penetration, the carapid redresses similar in all investigated species. Furthermore, itself (Fig. 1F-H) and enters the holothurian with myosepta bear tendinous tracks of collagen fibers backward movements (Kloss and Pfeiffer, 2000; oriented in a specific way and referred to as myosep­ Parmentier and Vandewalle, 2003, 2005). tal tendons. As this condition occurs in many widely Obviously, during penetration the fish displays separated gnathostome taxa (from sharks to derived extreme body curvatures (e.g., Fig. 1B-E). Given teleostean groups), it represents the gnathostome the data from previous studies listed above, we pre­ groundplan condition (Gemballa et al., 2003a). dict that C. acus will bear short myosepta with Recent studies revealed some musculotendinous short lateral tendons and distinct ENT and EPT. features in rigid fishes (tunas, lamnid sharks) that We expect other features of the musculotendinous clearly differ from the groundplan condition (Donley system in C. acus, for example, connections of myo­ et al., 2004; Gemballa et al., 2006; Shadwick and septal tendons and red muscles and attachment of Gemballa, 2006). Most striking features in these myosepta to the vertebral column, being clearly dif­ species are elongated myoseptal tendons (lateral ferent from those in rigid fishes of the open ocean. tendons) that reach up to 20% of body length and Thus, we consider this study to be a step towards a might hamper body flexibility and the lack of characterization of the locomotor morphology of another set of tendons (epineural tendon [ENT] and extremely flexible fishes that will stay in contrast epipleural tendon [EPT]) that is usually present in to the well-described morphology of rigid fishes fishes. In contrast to rigid fishes, our knowledge of (e.g., Shadwick and Gemballa, 2006). the musculotendinous system of extremely elongate and flexible species is scarce. So far, only Anguilla MATERIALS AND METHODS rostrata has been investigated in sufficient detail Material Examined (Danos et al., 2008). Its system of myoseptal ten­ dons differs in several respects from that of more We studied two species of C. acus (pers. collection C. Schwarz). One specimen (159 mm total length [TL]) was used rigid fishes. Myomeres are numerous and the lat­ for clearing and staining, the other (137 mm TL) for pCT-scans eral tendons, being elongated in rigid fishes, are and sagittal sectioning. short. Moreover, the ENT and EPT that are absent The distribution of muscle fiber types in C. acus was recorded in rigid fishes are very pronounced. from cross serial sections of four specimens with a TL of 80- The aim of this study is to examine the musculo­ 150 mm from the collection of the Laboratoire de Morphologie Fonctionnelle et Evolutive of the University of Liège, Belgium. tendinous system of another highly flexible but For living observations of the axial flexibility and extreme non-eel species and to test whether the contrasting turns, we collected 21 living specimens of C. acus from the dissec­ morphology between rigid fishes and flexible fishes tion of 434 sea cucumbers (mainly Holothuria tubulosa), which holds true. For this purpose, we considered pearl- were collected in the Mediterranean Sea (Calvi, Corsica) in June 2008. Specimens were kept in tanks with fresh sea water at ambi­ fish, Carapus acus (family Carapidae, tribe Cara- ent water temperature. The penetrations into sea cucumbers pini) to be an excellent candidate. Species of the were filmed simultaneously from a lateral and dorsal position Carapini (Carapidae, Ophidiiformes) live in differ­ (Sony VX 1000 Standard digital camera; Panasonic HC5 High ent invertebrate hosts such as sea stars, sea definition digital camera at 25 frames per second). Video frames cucumbers, or bivalves (Markle and Olney, 1990; were exclusively used for qualitative analysis. Parmentier et al., 2000a). The adults of C. acus (Emery, 1880) are inquilinists, live inside the Myosepta and Horizontal Septum respiratory tree or body cavity of sea cucumbers We carried out microdissections on a cleared and stained and use them as a shelter (Trott, 1970; Shen and specimen of C. acus to analyze