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. 2021 Jul 1;239(5):1096–1103. doi: 10.1111/joa.13489

Musculoskeletal anatomy and nomenclature of the mammalian epipubic bones

Gabby Guilhon 1,2,✉, Caryne Braga 3, Nick Milne 4, Rui Cerqueira 5
PMCID: PMC8546510  PMID: 34195985

Abstract

Despite the well‐established anatomy nomenclature for the marsupial skeleton, there are no names for the epipubic bone structures. Epipubic bones are paired bones articulating with the pubis and projecting cranially in the ventral body wall, present on the pelvic girdle of cynodonts, monotremes and marsupials. These bones were commonly thought to be related to pouch support in marsupials and more recently associated with locomotion. The parts of the epipubic bones have not been named and this has impeded proper morphological analysis. We analyzed the epipubic bones of 302 skeletons comprising American and Australian marsupials, as well as 27 monotreme skeletons, and dissected 10 marsupials for myological attachments analysis. We suggest the following nomenclature for the epipubic bone structures: crest for the cranial end, shaft for the body of the bone, lateral tubercle and the medial articular process. Some markings on the epipubic bone include the oblique line, pertaining to the attachment of external abdominal oblique muscle from the opposite side. The pyramidalis line is the suggested nomenclature for the pyramidalis muscle attachment and the inguinal ligament line for the inguinal ligament attachment. Regarding myology and attachments, based on dissections and review of the literature, the muscles pyramidalis, pectineus, external and internal abdominal oblique, transversus abdominis and rectus abdominis and the structures linea alba, linea semilunaris and the inguinal ligament are connected to the epipubic bone. As has been previously noted, anatomically, epipubic bones are so named due to their position (epi—above, pubic—pubis), and the same applies to structures such as the “epipubic process” or “epipubic cartilage” in amphibians and reptiles. While testing epipubic bone homology in vertebrates is beyond the scope of this work, we believe that using “epipubic bones” or epipubic cartilage/process as standardized terms for the structures found in the most cranial part of the superior ramus of the pubis would facilitate better anatomical communication. This should be valid for other similar terms, such as “epipubes” or “prepubis”, that might occur in the literature in relation to this same physiographic position, and it should also be named as epipubic. We believe that this nomenclature will help in future morphologic studies.

Keywords: anatomy, janitores marsupii, marsupial bone, marsupial morphology, ossa marsupialia

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1. INTRODUCTION

Epipubic bones are paired bones articulating with the pubis near the symphysis and projecting cranially in the body wall. These bones were first described in the Virginia opossum by Tyson (1698), who referred to them as ossa marsupialia or janitores marsupii due to their anatomical proximity to the marsupium (marsupial pouch). For a long time, the function of these bones was commonly associated with pouch support in marsupial females carrying their litter (Coues, 1872; Elftman, 1929; Tyson, 1698; White, 1989). However, epipubic bones are also present in pouchless species and marsupial males, as well as other taxonomic groups such as monotremes and cynodonts (Kielan‐Jaworowska, 1975; Kielan‐Jaworowska et al., 2004; Leche, 1891; Lillegraven, 1969) and some extinct basal eutherians (Novacek et al., 1997). More recently, epipubic bone function was also linked with sexual dimorphism (Cervantes & Oviedo‐Martínez, 2020; Guilhon et al., 2017) and locomotion (Guilhon et al., 2017; Reilly et al., 2009, 2010; Reilly & White, 2003; White, 1989). Apart from the discussion regarding their function, the epipubic bone anatomical structures and morphology remain understudied.

The general nomenclature of mammalian and especially human anatomy is well established (Kachlik et al., 2008; Thieme, 1998). Domestic animals have also been extensively studied and associated terminology is regularly updated in the Nomina Anatomica Veterinaria (Nomina Anatomica Veterinaria [NAV], 2017; Schaller, 2007). Detailed atlases on some wild species have been published (e.g., Smith & Schenk, 2000, 2001). The most recent and complete marsupial muscle descriptions and comparative studies pertain to forelimbs and hindlimbs, yet, abdominal and pelvic muscles, including the epipubic bones, are rarely fully described (e.g., Diogo et al., 2016; Stein, 1981; Warburton et al., 2015).

The muscle attachments of epipubic bones were first explored in Didelphis virginiana by Tyson (1698) and Coues (1872), and with more detail in Trichosurus vulpecula (Barbour, 1963). Other myology studies described or cited some of the epipubic bone muscles together with hindlimb musculature (Diogo et al., 2016; Elftman, 1929; Reilly et al., 2009, 2010; Reilly & White, 2003; Stein, 1981), leaving doubts regarding their attachments. These studies concur that the pyramidalis, rectus abdominis, external abdominal oblique, internal abdominal oblique and pectineus muscles are attached to epipubic bones. Most controversial in the literature is the pectineus muscle, about which there are divergent views: to wit, that it is attached to the epipubic bones (Coues, 1872; Reilly et al., 2010), directly to the pubis (Warburton et al., 2015), to both the pelvis and the epipubic bone (Barbour, 1963), or in the ischium and the epipubic bone (Stein, 1981).

Due to the lack of an established nomenclature for parts of the epipubic bone, it is difficult to interpret descriptions of the muscle attachments on the bone. Previous authors strove to describe its anatomical position as accurately as possible: for example, the outer border of the base of the marsupial bone (Coues, 1872, p. 128) or the deep surface, the cranial border and the cranial edge of the ventral surface of the transverse ramus of the marsupial bone (Barbour, 1963, p. 533). Although some such descriptions assume a simple clarity during dissections and direct observation, others are quite unclear—especially for non‐anatomists—and may easily be misinterpreted.

The establishment of a stable nomenclature is very important to the universal understanding of skeletal structure, rendering it easier to raise skeletal homologies hypotheses and summarize character definitions, morphometric landmarks and other morphological questions. Therefore, in aiming to define the epipubic bone structures, we seek not only to present our view on the muscle attachments to such bones but also to support future morphological descriptions and phylogenetic analysis.

2. MATERIAL AND METHODS

We examined the epipubic bone structures in 302 skeletons comprising 143 American marsupials, 132 Australian marsupials and 27 monotremes deposited in the following mammal collections: Museu Nacional da Universidade Federal do Rio de Janeiro (MN/UFRJ), Museu de Zoologia da Universidade de São Paulo (MZUSP), Centro de Coleções Taxonômicas da Universidade Federal de Minas Gerais (CCT/UFMG), Pontifícia Universidade Católica de Minas Gerais (PUC/MG), Museu de Zoologia da Universidade Federal de Viçosa (MZUFV), Laboratório de Biologia e Parasitologia de Mamíferos Silvestres e Reservatórios (LBCE/IOC), Smithsonian National Museum of Natural History (USNM), Museum of Comparative Zoology of Harvard University (MCZ), Australian Museum (AU), Queensland Museum (QM) and Western Australian Museum (WAM) (Table 1). Bones from small species were examined with a magnifying glass or a microscope.

TABLE 1.

Sample number of marsupials and monotremes skeletons analyzed, grouped by genus and also shape category. Based on Figure 1: category A (wide and robust), category B (slender and curved) and category C (thin and straight)

Group Genus Sample number Shape category
Marsupialia
Acrobates 3 B
Aepyprymnus 5 B
Antechinus 8 B
Bettongia 6 B
Caluromys 15 B
Caluromysiops 2 B
Chironectes 12 B
Dactylopsila 1 B
Dasyurus 9 B
Dendrolagus 8 B
Didelphis 30 B
Dromiciops 1 B
Echymipera 1 B
Glironia 1 B
Gracilinanus 1 B
Isoodon 13 C
Lasiorhinus 4 B
Lutreolina 9 B
Macrotis 1 B
Marmosa 16 B
Metachirus 15 B
Monodelphis 16 B
Myrmecobius 1 B
Perameles 10 C
Petaurus 9 B
Petrogale 7 B
Phascolarctos 9 B
Philander 19 B
Potorous 6 B
Pseudocheirus 5 B
Sarcophilus 8 B
Setonix 5 B
Trichosurus 10 B
Vombatus 3 B
Monotremata
Ornithorhynchus 12 A
Tachyglossus 13 B
Zaglossus 2 B
Total 302
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Dissections were done to report the muscle attachments and relations of the epipubic bone in seven marsupial species including three South American and four Australian species. Didelphis aurita (n = 2), Didelphis albiventris (n = 2) and Lutreolina crassicaudata (n = 2) were dissected at MN/UFRJ and CCT/UFMG laboratories in Rio de Janeiro and Minas Gerais, Brazil, and Phascolarctos cinereus (n = 1), Notamacropus irma (n = 1), Isoodon obesulus (n = 1) and Trichosurus vulpecula (n = 1) were dissected at Murdoch University (MU) and University of Western Australia (UWA) in Perth, Australia.

3. RESULTS

We found three different shapes of epipubic bones. The first one is wide, robust and triangular and was found only in the platypus Ornithorhynchus (Figure 1a). The second is slender, with a variable curvature in its body, but with a larger base. It was the most common shape found, including in all the Neotropical marsupials and nearly all Australian marsupials examined (Figure 1b, Table 1), plus the monotreme echidna Tachyglossus and Zaglossus. We observed a slight variation in shape in the numbat and the bettong (genera Myrmecobius and Bettongia), but in general, the major difference occurred in size, as per the tiny epipubic bones of the sugar glider Petaurus or very large epipubics in the koala Phascolarctos. The third shape is straight and substantially thinner than the others. This shape was found in peramelemorphians such as the bandicoots Perameles and Isoodon but not in the bilby Macrotis (Figure 1c, Table 1). Most of the genera analyzed were photographed for comparison of different shapes (Supplementary Material Figure S1–24).

FIGURE 1.

FIGURE 1

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Ventral view of the right epipubic bone and its different shapes. (a) Wide and robust from the platypus Ornithorhynchus, (b) slender and curved, being the most common shape in marsupials, from Didelphis and (c) thin and straight like a stick from the peramelid Isoodon

Based on standard anatomical nomenclature of other bone structures (e.g., humerus, femur), as seen in Schaller (2007), NAV (2017) and from our analysis of marsupial muscles and skeletons, we propose names for parts of the epipubic bone. The crest is the cranial end of the bone, and with the shaft, it forms the body of the bone. The lateral tubercle and the medial articular process, articulating with the craniomedial angle of the pubis near the symphysis, forms the base of the epipubic bone. The medial articular process is the only structure that is always articulated with the cranial edge of the body of the pubis, near the symphysis, forming the definitive connection of the epipubic bones and the pelvic girdle, while the lateral tubercle is the most lateral projection of the epipubic bone base. These structures are well marked in both ventral and dorsal views (Figure 2).

FIGURE 2.

FIGURE 2

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Nomenclature for epipubic bone structures from Didelphis aurita. (a) Ventral view of the right epipubic bone: crest, shaft, lateral tubercle, oblique line and the medial articular process. (b) Dorsal view of the right epipubic bone: pyramidalis line and inguinal ligament line

The muscles attaching to the epipubic bone include: (i) pyramidalis, a fan shaped muscle originating from the linea alba and attaching to the dorsal surface of the shaft from the crest to the medial articular process, in the pyramidalis line; (ii) rectus abdominis muscle, originating from the sternum and inserting on the dorsal aspect of the epipubic, deep to the pyramidalis muscle; (iii) pectineus muscle, originating from both ventral and dorsal sides of the lateral tubercle of the epipubic bone and inserting on the femoral shaft—this muscle was well developed in Nomacropus irma, and its origin reached the pectineal process; (iv) transversus abdominis muscle, from the false and floating ribs, thoracolumbar fascia, iliac crest and spine, inserting on the dorsal aspect of the cranial part of the shaft, and more cranially the dorsal wall of the rectus sheath; (v) internal abdominal oblique muscle, from the lumbar fascia and ilio‐gluteal fascia, near the transversus muscle origin and inserting on the lateral side of the crest, and more cranially the walls of the rectus sheath and (vi) external abdominal oblique muscle, originating from the lower ribs and inserting on the ventral aspect of the shaft near the crest. It is interesting to note that some fibres of this muscle continue to the base of the epipubic bone from the opposite side, crossing the linea alba and attaching to the oblique line. More cranially, the external abdominal oblique muscle forms the anterior wall of the rectus sheath. The linea alba stretches from the xiphoid process to the medial articular process, while the linea semilunaris forms the lateral edge of the rectus sheath and goes from the costal cartilages to the crest of the epipubic bone. The lines only attach to the pubis through the epipubic bone. Finally, in the caudal end of the pyramidalis line, there is a curvature towards the lateral tubercle in which the inguinal ligament dorsally attaches, so this structure was named as the inguinal ligament line. The inguinal ligament comes from the iliac crest and, along with the external oblique muscle and the epipubic bones, they compose the superficial inguinal ring (Figures 3 and 4). During the dissections, we observed that the epipubic bone moves back and forth in the sagittal plane when the pectineus muscle is pulled. The only exception found was in the peramelid Isoodon, where the origin of the pectineus muscle is restricted to the iliopectineal eminence.

FIGURE 3.

FIGURE 3

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Muscle attachments of epipubic bones from Didelphis aurita. (a) Ventral view of the right epipubic bone: linea alba and linea semilunaris, internal and external abdominal oblique and pectineus muscles. (b) Dorsal view, right epipubic bone: transversus abdominis, pyramidalis, rectus abdominis muscles and the inguinal ligament

FIGURE 4.

FIGURE 4

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Dissection of Notamacropus irma. Pyr, pyramidalis muscle; RA, rectus abdominis muscle; Ex Ob (op side), external abdominal oblique from opposite side; Pec, pectineus muscle; IL, inguinal ligament; Sp cr, spermatic cord with cremaster muscle; Ex Ob, external abdominal oblique muscle; In Ob, internal abdominal oblique muscle; TA, tranversus abdominis muscle; L sl, linea semilunaris. It is possible to observe the external inguinal ring formed by the external abdominal oblique and the inguinal ligament, and the internal inguinal ring formed by the internal abdominal oblique

During the analysis of the skeletons, epipubic bones could be found attached—or not—to the cranial side of the pubic body with dried connective tissue. They are usually not attached probably due to the cleaning and storage process of the skeletons. For those which were articulated, we observed that several media to large American specimens (1 kg or more), with well‐developed epipubic bones, had both medial articular process and lateral tubercle attached to the cranial edge of the pubis (attached to near the pubic symphysis and the superior ramus, respectively). However, most small marsupials we observed had only the medial articular process attached to the cranial edge of the body of the pubis near the symphysis, and the lateral tubercle was not connected to the pelvis. Furthermore, marsupials with the third thin shape (Figure 1c) had only the medial articular process attached near the pubic symphysis.

4. DISCUSSION

We assigned the name ‘crest’ to the cranial end of the epipubic bone because it does not articulate with any other bone and, in that regards, it is similar in shape to the iliac crest. The pyramidalis and internal abdominal oblique muscles attach to the crest, and the external abdominal oblique muscle attaches just deep to the internal abdominal oblique muscle attachment, as observed long ago by Coues (1872) in Didelphis virginiana.

The shaft is the main body and usually the longest part of the bone and is similar to the shaft of a rib or femur. In the dorsal view (the ‘back’ of the epipubic bone), there is a smooth, narrow depression along the entire length of the bone where the pyramidalis muscle attaches. Barbour (1963) described this pyramidalis attachment site as from the medial edge of the longitudinal ramus of the marsupial bone and from a longitudinal raphe on the surface of the rectus abdominis (Barbour, 1963, p. 553). Therefore, this structure was named the pyramidalis line, similar to the gluteal lines of the ilium where the gluteal muscle attaches. This line seems to follow the epipubic bone size and curvature, which is known to be a sexual dimorphic and also taxonomic feature in marsupials (Flores, 2009; White, 1989). Although it is expected that this feature will also be reflected in the attachment size of the pyramidalis muscle, Coues (1872) observed it to be similarly developed in both sexes. We were unable to test this due to the small sample size regarding males and females specimens.

We observed and noted the attachments of the rectus abdominis, pyramidalis (recognized as ‘rectus internus’ and ‘rectus externus’, respectively, by Coues, 1872), pectineus, abdominal oblique muscles (external and internal) and the inguinal ligament, but the cremaster muscle (males) and ilio marsupialis muscle (cremaster of females) were only considered attached to the epipubic bones by Coues (1872). In fact, the cremaster/ilio marsupialis muscles and the spermatic cord was found to pass through the superficial inguinal ring, without connecting to the epipubic bones. The superficial ring is delimitated by the inguinal ligament, part of the lateral edge of the epipubic bone and the external abdominal oblique opening (see Figure 4). This feature was clearly observed in all dissections.

The gracilis muscle was considered attached to the epipubic bones by Coues (1872) in Didelphis, by Sonntag (1922) in Pseudocheirus peregrinus and Phalanger orientalis and by Hopwood and Butterfield (1976) in Macropus giganteus. Despite that, in the present work, the attachment of the gracilis muscle was actually limited to the pubic symphysis, without any connection with the epipubic bones in Didelphis and Notamacropus irma. Unfortunately, however, we did not have access to any Pseudocheirus or Phalanger specimens to confirm the findings of Hopwood and Butterfield (1976). Our observations on the gracilis muscle are in accordance with the hindlimb myology descriptions of other marsupials (Diogo et al., 2016; Stein, 1981; Warburton et al., 2015).

In the present work, the pectineus muscle was found to be attached to the lateral tubercle of the epipubic bones of Didelphis, Lutreolina, Phascolarctos, Notamacropus and Trichosurus, but not in the peramelid Isoodon. In Trichosurus, this muscle was not considered attached to the epipubic bones by Barbour (1963), but it was indeed attached according to Reilly et al., (2010), who analyzed the function of the pectineus muscle in Trichosurus with electromyography. In relation to Isoodon, as for most peramelids, the epipubic bone has a different shape with no lateral tubercle (Figure 1c, Table 1 refers) and the pectineus muscle attaches directly to the iliopectineal eminence of the pubis (Warburton, 2015) which, in some specimens, is just caudal where the lateral tubercle would be positioned. This same situation might occur in the smaller species, such as Marmosa, in which the lateral tubercle is not articulated to the pubis as mentioned above, but this requires further investigation. While Diogo et al., (2016) made no personal mention of the pectineus muscle being attached to the epipubic bones, several other authors considered that it is indeed attached thus (Coues, 1872; Elftman, 1929; Reilly et al., 2009, 2010; Reilly & White, 2003; Stein, 1981). Elftman (1929) observed that although the pectineus muscle regularly originates from the epipubic bones, in Macropus, it originates from the pectineal process. During our dissections, which included a species of the wallaby (Notamacropus irma) we observed that the pectineus muscle is attached both to the pectineal process and the lateral tubercle. Another interesting feature was the back‐and‐forth movement of the epipubic bone in the sagittal plane observed by Tyson (1698), but he did not specify which muscle performs this movement. Our observations suggest that the forward movement is accomplished by pulling the pectineus muscle.

Considering that different bone sizes and shapes can determine the amount of muscle attached to them, as well as limb movements in marsupials (Argot, 2001, 2002, 2003), it is possible that the different shapes of epipubic bones are related to a specific feature or type of locomotion (Guilhon et al., 2017). The slender, curved shape (Figure 1b refers) seems to be the most common, being found in all American and most Australian marsupials and in the monotreme echidna, where some species have relatively large (e.g, Didelphis and Phascolactos) and others, very small epipubic bones (e.g., Marmosa and Petaurus). This could be the basal shape of epipubic bones, since it is also seen in basal eutherians (Ji et al., 2002) and Tritylodontidae cynodonts (Novacek et al., 1997).

As has been previously noted, anatomically, epipubic bones are so named due to their position (epi—above, pubic—pubis), and the same applies to structures such as the “epipubic process” or “epipubic cartilage” (Cannatela & Trueb, 1988; Carling et al., 2014; Gadel‐Rab et al., 2018, just to cite a few) in amphibians and reptiles. Although these structures share the same position, they are very different in size, shape (Wyneken, 2001) and organic composition (cartilaginous or ossified), raising questions about homology. They were considered to be homologous with epipubic bones by Huxley (1879) and several of his contemporaries, as he stated. Villiers (1925) described muscle attachments that might correspond to the mammalian pectineus and pyramidalis muscles, in the cartilaginous ‘epipubes’ of Xenopus frog, which could be considered another evidence for this homology. More recently, the epipubic process/cartilage are still being described in living species (Asadi et al., 2016; Couper et al., 1993), but we could not find recent descriptive studies on the myology of these structures and their attachments. Also, these structures are frequently missing in fossil specimens (Li et al., 2018), which makes it more difficult to reconstruct the ancestral character state and suggest direct homologies. However, Harris (2004) made an interesting point that “some structures occupy a common physiographic position in the body but are not evolutionarily homologous and probably not functional homologues” (Harris, 2004, p. 1244). He considered this ambiguity between reptiles and mammals an example of that, despite neither hypothesis having been properly tested. With respect to the functional homology, most muscle attachments of the present work were found in the epipubic bone and not the pubis, which suggests that the former may be derived from detached parts of the pubic bone, possibly including the pubic crest and pubic tubercle. Parsons (1903) speculated similarly based on relations of the epipubic bone and its myology. It is interesting to notice that similar muscle attachments were found in amphibian and reptilian epipubic processes (Huxley, 1879), which could be evidence of similar functionality of these structures in several vertebrates. Besides, the function of epipubic bones in marsupials might be related to reproduction but is also associated with both locomotion and breathing activities (Reilly et al., 2009), which could point to the function of the epipubic processes in other vertebrates. While testing epipubic bone homology in vertebrates is beyond the scope of this work, we believe that using epipubic bones or epipubic cartilage/process as standardized terms for the structures found in the most cranial part of the superior ramus of the pubis would facilitate better anatomical communication. This should be valid for other similar terms, such as “epipubes” or “prepubis”, that might occur in the literature in relation to this same physiographic position, and it should also be named as “epipubic”. Nevertheless, we agree that analysis aiming to confirm evolutionary homologies (Harris, 2004) is needed, especially in vertebrates outside the crown‐group Mammalia.

The examination undertaken in this study of a large and diverse sample of mammals from both Neotropical and Australian regions allowed for a better understanding of epipubic bone morphology and muscle attachments. We hope that this work might contribute to standardizing the nomenclature of epipubic bone structures in mammals and perhaps other vertebrates, facilitating future studies regarding anatomy, functional morphology and the establishment of new taxonomical characters.

AUTHOR CONTRIBUTIONS

GG developed the idea, analysis, dissections and main manuscript, CB and RC supervised the whole work, suggesting what to do at each time, and participated in the writing of the preliminary draft and the final version. NM helped with UWA dissections, analysis of dissections, fruitful discussions about comparative anatomy and manuscript writing.

Supporting information

Supplementary Material

Click here for additional data file. (11.3MB, docx)

ACKNOWLEDGEMENTS

This work is part of a master’s thesis presented by GG to the Universidade Federal do Rio de Janeiro, which was funded by CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior). R. Cerqueira received grants from CNPq, FAPERJ, PPBIO/CNPq and PROBIO/MCT/MMA/GEF. We would like to thank F. A. Silveira for the review and fruitful discussion, L. O. Drummond for photo editing and the curators and technicians who provided access to the collections: J. Gualda, I. P. Jesus, M. de Vivo, G. Lessa, C. G. Costa, S. Ingleby, H. Parnaby, H. Janetzki, K. Travouillon, V. Hayes, M. Omura, D. Lunde and specially J. A. Oliveira, F. A. Perini and N. M. Warburton which provided specimens for dissections. We also thank both anonymous referees for their careful revision. The authors have no conflicts of interest.

Guilhon, G. , Braga, C. , Milne, N. & Cerqueira, R. (2021) Musculoskeletal anatomy and nomenclature of the mammalian epipubic bones. Journal of Anatomy, 239, 1096–1103. 10.1111/joa.13489

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