NEW NOMENCLATURE AND THE SYNONYMY OF CRANIAL MUSCULATURE IN TURTLES

Nomenclatural Traditions

In the literature, a large confusion about the terminology of muscular structures in vertebrates exists (Starck 1982). One reason is the anatomical, ontogenetic, and phylogenetic plasticity of muscular structures. If a muscle is separated into two prominent muscle heads – often performing particular functions – authors tend to name the parts of a single muscle as new "musculi" or "muscle portions". In older literature, authors introduced muscle names of mammals that they assumed to be "comparable" (homologous) to those of non-mammalian groups (e.g., Bojanus 1819-21; Cuvier 1935; Kesteven 1942-45; Starck 1982). In some cases, tables of synonyms are adopted from authors without checking the particular information that was previously presented by other authors cited within. In this study, I compared published tables of synonyms (e.g., Ogushi 1913b; Schumacher 1953-54, 1972, 1973; Poglayen-Neuwall 1953a) and re-checked all cited references by comparing the original anatomical descriptions in detail. All cranium-associated muscular structures that were ever described for turtle species are listed, including their related synonyms, proposed functions, and innervation patterns (Appendix 1). The criteria used to correlate synonyms in this study are based on the origin, insertion, spatial orientation, tendinuous framework, and innervation pattern of respective muscular structures. Homologies were also considered based on the pattern of muscle development known thus far (Edgeworth 1935; Rieppel 1990; Tvaroková 2006; personal observation). For the definition (Appendix 1) and discussion of particular structures of turtles see below.

Definition of Nomenclature

The origin and insertion sites (Figure 1.1) of a muscular structure are any kind of hard or soft tissue material – except another muscular structure. Within the highly differentiated cranium, extended definitions of muscular structures – basically following proposals of fish anatomists Winterbottom (1974) with extensions by Hertwig (2005, 2008) and Werneburg (2007, 2009b) – are necessary as depicted in Figure 1 and described as follows.

In many cases, the definition of origin and insertion is very clear: the posterior, the dorsal, or the less mobile structures (punctum stabile) provide the origin sites, while anterior or ventral structures or structures with a higher degree of mobility (punctum mobile) provide the insertion site (Starck 1982). There are more complicated examples, however, such as muscles of the tongue or the mouth floor. Concerning those, I define the following hierarchy of consideration for muscles only stretching between cranial structures: When defining an origin or insertion site, one should first consider the criterion of mobility to decide between both alternatives. If one cannot decide based on the mobility, one should consider the anterior-posterior axis next. If it is still not possible to decide between origin and insertion, one should consider the dorsoventral axis, with next option being the mediolateral axis. In that case, the origin would be medial, and the insertion would be lateral. One can summarise that hierarchy of consideration and define the related value of functional and spatial orientation as follows: mobility > anterior-posterior axis > dorsoventral axis > mediolateral axis. One example: A muscle spans between the symphysis of the dentaries and the dorsal integument of the tongue (m. genioglossus, No. 63). Although the lower jaw is situated more anteriorly and more ventrally, one has to consider the lower jaw to be the origin because it has less mobility when compared to the tongue.

In the nasal and the internal eye region, ring-shaped radiar muscular structures occur (No. 5-7, 11). I define the central attachment to be the origin and the outer attachment to be the insertion.

A muscle (Figure 1.1) is defined as having an own origin, course, and insertion site. It can be partly separated into muscle heads or muscle portions. Scanlon (1982) for example described one particular muscular structure (m. coracohyoideus Pars principalis, No. 58). During its course the muscle spatially splits into two muscle bellies, shortly after origin and shortly before insertion site those bellies are indistinguishably fused, hence the whole structure should be considered as a muscle sensu stricto (s. s.) (muscle layer, see below and Figure 1.5).

Muscles display different shapes. A parallel fibred muscle can have two direct (A in Figure 1.6) or one tendinuous attachment (B in Figure 1.6). A muscle with fan-shaped fibres generally attaches via a tendon (C in Figure 1.6). If the muscle has tendinuous attachments in the origin as well as in the insertion site it becomes spindle shaped (D in Figure 1.6). In a bipinnated muscle, the fibres have direct attachments on the one hand and bilaterally attach to an internal tendon on the other hand (E in Figure 1.6). If fibres attach to such a tendon only on one side, a pinnated muscle is formed (Figure 1.6).

Muscle heads (Figure 1.2) – often confusingly described as singular muscles or muscle portions in the literature – are here defined as regional partitions of a muscle or a muscle portion. Muscle heads (singular: caput, plural: capitis) have either an own origin or an own insertion site. In their course, they fuse with other muscle heads into one inseparable muscle belly. Because of dependence to a particular muscle – or muscle portion – muscle heads are only considered in a descriptive way and in principle they do not gain a separated number (as a muscular unit) in Appendix 1 and Figure 6, Figure 7, Figure 8, Figure 9, Figure 10, Figure 11, Figure 12, Figure 13, Figure 14, Figure 15, and Figure 16.

Muscle portions (singular: pars, plural: partes) (Figure 1.3) are partitions of a muscle, in which separate origins, courses, and insertions are recognisable. The muscle portions are muscle fibre bundles that are still connected to each other by shared or intercrossing fibres, or at least by a common tendon. One example is the nomenclature of "m. pseudotemporalis" and "m. intramandibularis" (Figure 2, Figure 3, Figure 4, Schumacher 1953-54) that I define as two portions of m. adductor mandibulae internus. Both portions are only connected to each other by a tendon ("Zwischensehne" of Poglayen-Neuwall 1953a). Parts of the "pseudotemporalis" portions are still connected to the remaining parts of m. adductor mandibulae internus (Figure 16) and consequently "pseudotemporalis" and "intramandibularis" have to be defined as portions of adductor mandibulae internus (No. 23-25). Bipinnated muscles may have two muscle portions as shown as E in Figure 1.6, characterised by a separated origin or insertion. In contrast, if this attachment of the whole muscle would be inseparable and the fibre courses would still be bipinnate, the whole structure would be called a muscle s. s. with an internal tendon (G in Figure 1.6). In the literature, some cases exist where the identity of a "muscle bundle" is not entirely clear, due to lack of descriptions or insufficient depiction concerning the homologisation propositions here presented. One case is the "Nebenbündelchen" ("little bundle nearby") of König (1934-35), who described internal eye musculature. For now, I incorporated such unclear structures as a muscle head to the related donor muscle or muscle portion; however, the identity of the "Nebenbündelchen" needs to be re-checked by specific studies of this region.

A muscle section (Figure 1.4) is defined as a completely separated muscle s. s. that clearly originates from another muscle in phylogeny. However – due to difficulties of prejudiced homologisations and developmental hierarchy – the term "section" is only used for discussion, but is not to name a particular muscle structure.

Finally, as an additional term one has to define the muscle layer. These are muscle fibres within one of the above defined muscular structures having a separated course and orientation. When compared to the surrounding or underlying muscle fibres, they never fully correspond to any origin or insertion site of a muscle, a muscle portion, or a muscle head (Figure 1.5).

In several cases, such as in trionychids (Ogushi 1913b; Lakjer 1926), little muscles (sections) or muscle portions obviously are separations of a donor muscle that one can see in related species as a consistent structure. If the bigger donor muscle retains its identifying (Appendix 1) general origin, course, insertion, and innervation, I only introduced a new term and number for the little muscle, but kept the nomenclature of the donor muscle as compared to the similar muscle of other species. Hence, by strict definition the synonyms (Appendix 1) do not necessarily represent homologous structures in the species as a whole structure, but instead only insertion/origin/innervation are comparable. An example is a set of species with an m. adductor mandibulae internus Pars pseudotemporalis (No. 23), which originates from the processus descendens of the parietal and inserts to the medial side of the lower jaw. Some of those species have an additional Pars pseudotemporalis superficialis (No. 24) – showing a different origin/insertion pattern – that most likely separated from Pars pseudotemporalis in evolution. The Pars pseudotemporalis (No. 23) does not show a major anatomical difference in those species, hence it should keep its name by the definition of Appendix 1. Following Sondhi (1958), I put an additional, informative term, "principalis", in brackets after the donor muscle name to differentiate it clearly, when a superficialis portion (No. 24) also exists. It would thus be Pars pseudotemporalis (principialis) (No. 23), while preserving its indicating number. Muscular units as described in Appendix 1 should be considered as homologous at first glance (primary homology). If a small muscular structure turns out to be autapomorphically present in one group of species (secondary homology), one should consider the phylogenetic origin of that structure from a donor muscle/portion.

The terms anterior and posterior correspond to a defined region of a particular element, whereas rostral and caudal are used to indicate a spatial orientation of one element or a part of it when compared to others. Dorsal, ventral, lateral, and medial are used for both cases. Terms ending with -ad (e.g., mediad) indicate a direction. In combined terms, antero-/rostro- and postero-/caudo- form the first part, hierarchically followed by dorso- and ventro-. The terms –lateral/d and –medial/d always form the second part. Only two terms can be combined. As commonly found in recent literature, such constructions as "anterodorsomedial at element A" should be re-described as 'anterodorsally on the medial face of element A'.

Ordering

Following the approach of Bojanus (1819-21), Hoffmann (1890), and Ogushi (1913b), I created a numeration system for cranium-associated muscular structures. I introduce the term muscular units – which are, by definition, non-partitioned (non-portioned) muscles (s. s.) parri passu muscle portions (s. s.). Each muscular unit gains one number: listed and illustrated in Figure 6, Figure 7, Figure 8, Figure 9, Figure 10, Figure 11, Figure 12, Figure 13, Figure 14, Figure 15, and Appendix 1. There are several examples in which muscular units can occur as a muscle portion or as a separated muscle in different species. The assumption behind the statement of primary homology is based on spatial orientation (origin, course, insertion) and innervation pattern. The decision whether a muscular unit is named as a real muscle or as a muscle portion (Pars) in Appendix 1 is based on the most common behaviour of that muscular unit known in turtles. If a "regularly" occurring muscle portion "irregularly" occurs as a separated muscle in a particular species, it may gain a slightly modified name (musculus vs. Pars) (e.g., pterygoideus or pyramidalis muscular structures in Emydura subglobosa) – however, it should be discussed in regard to the numbers as defined in Figure 6, Figure 7, Figure 8, Figure 9, Figure 10, Figure 11, Figure 12, Figure 13, Figure 14, Figure 15, and Appendix 1. Muscular units should be seen as numbered spatial, homologisable structures. In contrast, using only muscle names would lead to confusions and prepossessions in homology assumptions. Using the presented numbering system of muscular units, clear homologisation tables will be possible for comparing turtle data with those of other reptiles and other vertebrates. If muscles A and B are inferred to have fused in phylogeny, they may be discussed as a new muscle No. C (= A/B). The same is imaginable in ontogeny: if a muscle Anlage is known to separate into muscle D and E in development, it may be called Anlage No. D/E.

The muscular units presented in this study (Appendix 1, Figure 6, Figure 7, Figure 8, Figure 9, Figure 10, Figure 11, Figure 12, Figure 13, Figure 14, Figure 15) are grouped and ordered first according to their innervation (cranial nerves: n. III-XII, spinal nerves: n. S1, etc.) and separation pattern (muscle portions of a muscle) and – within those groups – in a regional and alphabetical order.

Neck muscles are often innervated by several spinal nerves at the same time, depending on the anterior-posterior extend, and the detailed anatomy of the muscle, hence a clear order of neck muscles – as done for the cranial nerves innervated muscles – was not possible. Gasc (1981) discussed the problem with allocating neck muscles of turtles to the epaxial and hypaxial system due to unclear ontogenetic and phylogenetic identities and innervation patterns. In the highly differentiated neck muscles, embryological rearrangements and integrations of several myotomes were also conceivable. After reviewing all available descriptions of cranium-associated neck musculature in turtles, I was able to assign each muscular unit to epaxial (dorsal branches of spinal nerves, nn. Sd) or hypaxial (ventral branches of spinal nerves, nn. Sv) musculature; within both groups muscular units are ordered in an alphabetical order. In some cases, the controversial identity of particular structures is discussed in this paper.

Abbreviation Guide

Due to space restrictions, abbreviations are often necessary in journal figures. However, abbreviations are defined differently in the literature, mainly intuitively, and are based on the anatomical focus of the respective author – introducing difficulties when broadening the anatomical structures analysed (Rieppel 2007; Jones et al. 2009). I present a new and traceable abbreviation system that is primarily designed using the first three letters in the respective word parts (e.g., cil for "ciliaris"). If word parts contain less than three letters (e.g., "exoccipital") or begin with the same three letters (e.g., "sup..."), particular abbreviations are used – formed by the first letter of the word and the first letter(s) of the following syllable(s) (compare to "coronoid" or "corpus"; Appendix 7) – finally forming three letters (eoc for "exoccipital"). A few exceptions are of course unavoidable; however, this approach could be easily used to define abbreviations of additional anatomical elements.

The abbreviations of muscular units (Appendix 1) also follow the abbreviation guide (Appendix 7). Therein normal letters are used for the muscle (s. s.), and capital letters are used to indicate muscle portions of that muscle, e.g., the Pars medialis of an m. adductor mandibulae externus is abbreviated as m. addmaneteMED (No. 17). For easier reading, the muscle numbers as defined in Appendix 1 are added to the abbreviations. Muscle heads (s. s.) do not gain an anatomical term; however, they may gain an additional additive description in the text and can be labelled as regular letters added to the number of the muscular unit to which it belongs (e.g., caput "a" of muscular unit No. 40 = No. 40a).

Spatial structures expanding over several singular elements are labelled without abbreviation in the figures of this study (e.g., otic chamber, proc. trochlearis pterygoidei, or fascia); however, selected synonyms and suggestions for their abbreviation can be found in Appendix 5. Tendons – tendinuous attachments of muscular units with a +/- round cross section – do not gain a separate name and are handled in a descriptive way. The names of cartilages (car.), of strong connective tissue spanning between bones (ligaments, lig.), as well as flat tendinuous attachments of muscular units (aponeuroses, apo.), are abbreviated like bones and nerves (Appendix 7) or muscles (Appendix 1).