1. Introduction
Hamadryas or mantled baboons (
Papio hamadryas) can be encountered as free-ranging animals in the horn of Africa and the Arabian Peninsula. There, these non-human primates are also kept as pets by nomads. They can, however, be admired worldwide in zoos and are housed in research facilities as human models [
1]. It is obvious that captive settings restrict their natural social and foraging behavior and physical needs to prevent stress and abnormal behaviors [
2]. Providing these animals with the appropriate diet, social structure, habitat, and medical care is, thus, essential. Regarding the latter, baboons living in captivity might require medical attention when injured. The larger majority of injuries occur in males and are inflicted by means of the canines [
3]. The bodily distribution of injuries in yellow baboons (
Papio cynocephalus) is characterized by a preponderance of injuries at the head, neck, shoulders, chest, and arms [
3]. The location of injuries in male hamadryas baboons differs from that of yellow baboons in that most injuries are inflicted on the hands and forearms [
4]. At these locations, fractures often occur in the phalanges of the fingers, but fractures of the long bones and the clavicles are also common [
5].
Without a doubt, proficiency in species-specific anatomy is fundamental when treating wounded animals. The interpretation of radiographs and the execution of operations illustrate this statement. Unfortunately, the anatomical knowledge of the mantled baboon is still debatable. For sure, there is a large body of publications that elaborate on a very specific aspect of the baboon’s anatomy. A quick literature search on the Internet demonstrates the scattered availability of knowledge. However, those publications fall short when systematic, comprehensive information on an anatomical system of the baboon is sought after. A reference work worthwhile mentioning is ‘An Atlas of Primate Gross Anatomy: Baboon, Chimpanzee and Man’ [
6]. Since the intention of this atlas is to clarify the anatomical relationships among the mentioned species, the anatomical descriptions of each species stay rather superfluous. This prompted the authors of the present study a few years ago to begin revisiting the anatomy of the mantled baboon. A first manuscript presenting an in-depth description of the osteology was published in this journal in 2023 [
7]. As is custom in anatomical atlases and handbooks, the study of the joints (arthrology) follows. Surprisingly, no chapter on the arthrology of the baboon is included in the above-cited atlas. A similar finding is found when browsing through the renowned source of data on primate anatomy published by Ankel-Simons [
8]. That work is further characterized by a comparative approach rather than providing species-specific details.
The present arthrological work focuses on the synovial joints of the appendicular skeleton and, more specifically, those of the thoracic limb (
articulationes membri thoracici) of the mantled baboon. It is the first part of three, with the arthrology of the pelvic limb and the axial skeleton forthcoming. In contrast to humans, the baboon’s thoracic limb (arm) plays an important role in locomotion [
9]. It should, consequently, withstand great forces, resulting in mechanical stresses on the bones, muscles, and joints. In addition, the primate hand is also used for precision handling [
10]. These conflicting functions require that the size, stability, and sturdiness of the hand should be balanced with minimal weight, flexibility, and agility [
11]. As such, knowledge of human anatomy and, in particular, biomechanics cannot be extrapolated to the mantled baboon. Nonetheless, veterinarians responsible for the medical care of baboons often rely on human anatomical works when wounds have to be tended or surgical interventions are required. The reason can be found in the fact that primates, including baboons and humans, share massive amounts of anatomical traits due to their close genetic relationship [
12].
To facilitate the use of this manuscript as a dissection guide and reference work for veterinarians who are responsible for the medical care of baboons, all the synovial joints that are present in the baboon’s thoracic limb (i.e., those present in the shoulder region, elbow region, and hand) are topographically approached. This means that not only the typical connective-tissue elements that form the joints but also the associated muscle tendons are depicted by means of labeled color photographs of dissections. The osseous structures to which these components attach are identified as well. Veterinary anatomical terminology is primarily used and derived from the
Nomina Anatomica Veterinaria (N.A.V.) [
13]. Nevertheless, it is complemented by human terminology listed in the
Terminologia Anatomica (T.A.) [
14]. This approach has its foundation in the fact that only domestic mammals are included in the N.A.V. Structures specific for primates are not listed there but might be found in the T.A. considering the great similarity between humans and other primates [
12].
The aim of the present work is to provide a thorough description of the gross anatomy of the thoracic limb joints of the mantled baboon, using contemporary anatomical terminology. The textual descriptions are supported by 25, often multipanel, color photographs, as a picture is worth a thousand words. Several points of view are presented from the superficial layer to the deepest, guiding the reader through the dissections. As such, the present work could be valuable as a dissection guide. It is not the intention of the work to provide a major comparative functional or evolutionary perspective. Though, the discussion will bring forward a few remarkable differences between the anatomy of the baboon, on the one hand, and humans and domestic mammals, on the other hand. This is to illustrate that the extrapolation of species-specific anatomical data should be performed with caution. Furthermore, providing functional and evolutionary insights also falls beyond the scope of the present work because too many structures are reviewed. This work could perhaps be a source of inspiration for further research on a particular matter. A potential research topic could be the radiographic examination of the baboon’s joints, as imaging exams are commonly used in the clinical routine for baboons. Such a complementary method for visualizing bone structures and joints could build further on the recently published manuscript on the osteology and the present manuscript on the arthrology of the mantled baboon.
4. Discussion
This manuscript presents the anatomy of the synovial joints of the thoracic limb of the hamadryas baboon. The various joints were dissected in three animals, taking color photographs during the subsequent steps. The observations were textually described aiming for the use of this work as an anatomical atlas or dissection guide. The rationale behind this approach can be found in the fact that veterinarians responsible for the medical care of baboons are confronted with the lack of comprehensive species-specific anatomical data. This should not be interpreted as if there are no data at all. Numerous studies have been published examining particular aspects of the joints of the baboon. These studies are often very in-depth and, therefore, fail to provide the general conformation of the joint under study. In addition, since baboons are wildlife species, their anatomy is not taught in the standard curriculum of veterinary medicine. The only comprehensive work on baboon anatomy is the atlas by Swindler and Wood [
6]. It shows many illustrations of various anatomical systems. Regrettably, the quantity of supporting text is restricted. In addition, only black-and-white line drawings that fail to recapitulate the anatomical details are included. As a result, doubtful identifications might appear during dissections or surgical interventions. However, all of this is irrelevant in this specific context, since the arthrology is not included in the Swindler and Wood atlas [
7]. The reason for this can only be guessed at. Own experience has learned that the study of this anatomical system is challenging, though. Veterinarians working with primates, thus, fall back on human anatomy atlases, a choice that is based on the great similarity between humans and other primates that has its origin in their close genetic relationships [
12]. Below, a number of striking differences between baboon and human anatomy are briefly reviewed. These potentially find their origins in the way the thoracic limb is used, i.e., focus on locomotion and stabilization in genus
Papio vs. focus on practical usage and fine motor dexterity in man. The aim of the enumeration is to underscore that the consultation of human anatomical works can be misinforming when other primate species, in case of the baboon, are under study. It should be clear that baboon-specific anatomical data can contribute to the welfare of baboons requiring medical attention.
The dissimilarities observed in the shoulder region are considered first, starting with the myology. The dorsoepitrochlearis muscle of the baboon arises from the ventral margin of the latissimus dorsi muscle and merges with the long head of the triceps brachii muscle. During evolution, it has fused with the latissimus dorsi muscle. It is, consequently, absent in most humans, although the muscle can be encountered as an anatomical variation [
18].
The baboon coracobrachialis muscle is composed of the deep and the middle coracobrachialis muscles. Among the domestic mammals, a similar division is also present in the horse, ruminants, and the rabbit [
16]. In these species, a proximal, deep part and a distal, superficial part are present. In contrast, it is a single muscle in the larger majority of humans [
19,
20].
The pectoralis musculature slightly differs in morphology and nomenclature between the baboon and man. The baboon pectoralis superficialis and profundus muscles are largely the analogues of the pectoralis major and minor muscles in humans, respectively. However, the sternocapsular part of the superficial pectoral muscle as seen in the baboon is more developed in humans. Only a very limited attachment to the clavicle is present in the baboon, whereas the medial third of the clavicle is the attachment site of the clavicular part (
pars clavicularis) in man [
20].
Moving on to the arthrology, it was observed that the transverse humeral ligament secures the tendon of the biceps brachii muscle in the intertubercular groove. In human anatomy, the true nature of this ligament is under debate. It could be regarded as a mere continuation of the tendon fibers of the subscapularis and pectoralis superficialis muscles [
21]. Although it is included in the T.A. [
14], human anatomy atlases including the highly esteemed Sobotta [
20,
22] do not mention the name. In contrast, it is a well-developed ligament in domestic mammals [
23]. However, the term
ligamentum transversum humeri has been replaced by the term
retinaculum transversum [
13].
As the clavicle is present in both baboons and humans, it is expected that similar ligaments securing the position of this bone can be encountered. In humans, the coracoclavicular ligament consists of the trapezoid ligament (
lig. trapezoideum) and the conoid ligament (
lig. conoideum) [
20]. The former attaches to the basis of the coracoid process whereas the latter has the transition of the scapular neck to the basis of the coronoid process as its attachment site. Such bipartite ligament was not observed in the dissected specimens. Only a single ligament resembling the human trapezoid ligament could be identified. A costoclavicular ligament was not observed in the dissected baboons. In contrast, such ligament supports the sternoclavicular joint in apes and humans in which it limits horizontal and vertical clavicle movement. Consequently, its absence allows for a greater mobility of the thoracic limb in the baboon [
24]. Since no or only a reduced clavicle is present in domestic mammals, neither of these ligaments can be observed in these quadrupedal species. In quadrupedal primates possessing a clavicle such as baboons, this bone allows for the upper limb to realize movements outside the sagittal plane, without hindering quadrupedal locomotion [
25]. The latter probably is the reason why the baboon has an intermediate position, in terms of the presence of clavicular ligaments, in between man and domestic mammals.
Furthermore, the coracoacromial ligament (lig. coracoacromiale) spans between the tip of the coracoid process and the tip of the acromion in man. It was not found in any of the dissected specimens. In contrast, the coracohumeral ligament extending between the coracoid process and the greater tubercle is present in both the baboon and man.
The elbow joint is subsequently considered, reflecting first on the myology. A few minor dissimilarities with man are communicated first. In contrast to humans, the baboon flexor carpi radialis muscle only consists of the humeral head and no ulnar head could be observed. This was also described earlier [
6]. Also, the anconeus muscle in man is very short. It spans from the lateral humeral condyle to the olecranon. The anconeus muscle in the baboon is well developed. It arises from the caudal side of the distal third of the humerus and attaches to the anconeal process. The muscle in the baboon that closely resembles the human anconeus muscle is the epitrochleoanconeus muscle. However, this muscle is located at the medial side of the elbow joint. The prevalence in a central European population is only 4% [
26].
The insertions of the biceps brachii and brachialis muscles deserve sufficient attention. According to the description of genus
Papio by Swindler and Wood [
6], the biceps brachii muscle inserts into the radial tuberosity. This is also the case in humans [
20,
27]. However, the distal tendons of the biceps brachii muscles in the dissected baboons inserted into the radial tuberosity and the interosseous membrane. This membrane seems a secondary attachment site for the biceps brachii muscle in the baboon. In humans, the distal tendon of the biceps brachii muscle presents an aponeurotic expansion toward the antebrachial fascia (
aponeurosis bicipitis brachii) [
20]. A comparable condition appears in domestic mammals, in which this so-called
lacertus fibrosus that is particularly well-developed in ungulates unites with the extensor carpi radialis muscle and not with the antebrachial fascia [
19]. This structure is, thus, located at the medial side of the human arm. In contrast, it lies at the lateral side of the thoracic limb is domestic mammals. Surprisingly, such structure was not identified in the baboon during the present study. Further examinations specifically targeting this matter could potentially provide more insight. It was observed that the inserting tendon of the baboon’s brachialis muscle attaches to the ulnar tuberosity, which is located distal to the medially oriented coronoid process of the ulna. This process serves as the distal site of attachment for the anterior part of the ulnar (medial) collateral ligament in humans. The posterior part not only attaches posterior to it but also somewhat more proximal. Both parts are, however, tied to each other [
20]. In the dissected baboons, the medial collateral ligament of the elbow joint consisted of a proximal part and a distal part, attaching proximal and distal to the ulnar tuberosity, respectively. In between both, the tendon of the brachialis muscle inserted into the ulnar tuberosity.
In a study assessing terminal elbow extension in the olive baboon, the role of the anterior oblique ulnar collateral ligament bundle was investigated [
28]. First, it is advised to use veterinary nomenclature, thus using the term cranial oblique medial collateral ligament. The authors also mention a middle part of the ulnar collateral ligament. This might suggest that a caudal part is additionally present. In humans and hamadryas baboons, an anterior/cranial and a posterior/caudal part are present [
20]. No caudal part is visible on the photographs shown by the authors. As a consequence, that middle part probably represents the caudal part. Further complicating this matter, it should be noticed that the T.A. only mentions the
ligamentum collaterale ulnare cubiti in humans without detailing the existence of an anterior and a posterior part [
14]. In contrast, the Sobotta does [
20]. Since the cranial part of the ulnar collateral ligament attaches more distally on the ulna, it shows an oblique course. As a result, it could be understood that the anterior ulnar collateral ligament and the oblique ulnar collateral ligament are synonyms. Thus, no posterior oblique ulnar collateral ligament exists. This point of discussion makes it clear that the use of standardized anatomical nomenclature is pivotal for the correct interpretation of studies.
Finally, some thoughts on the articulations of the hand are communicated. In both the baboon and man, the carpal articular surface of the radius rests on the scaphoid and lunate bones. A proper congruency is present between these bones. However, it was previously stated that baboons are the only taxon in which the dorsal lip of the scaphoid does not appear to fully engage with the bony lip of the dorsal radius, which is in contrast to what is observed in palmigrade-capable monkeys to which baboons belong [
29]. As a result of this incongruency, a semilunar meniscus sitting in the dorsolateral aspect of the radiocarpal joint is described in baboons [
30]. Unfortunately, no unambiguous images of such meniscus are available in literature. To be precise, only a black-and-white photograph of a scaphocentrale-triquetral ligament originating from the presumed ill-visible semilunar meniscus and attaching to the scaphoid, central and triquetrum bones can be found in literature. This ligament seems to correspond to the more proximal ligament of the dorsal ligamentous complex that is called the
ligg. intercarpea dorsalia in the present manuscript. A semilunar meniscus could not be isolated from that ligament in the present study. It is suggested that the meniscus is a mere reinforcement of the origin of the ligament on both the bony lip of the dorsal radius and the scaphoid bone. In contrast, the head of the ulna is not fitting the triquetrum bone in man. As a consequence, an articular disc provides the congruency [
20]. Such a disc was not encountered in the dissected specimens. The reason might be found in the elongated ulnar styloid process in the baboon, in comparison with the poorly developed human counterpart. In the baboon, the ulnar styloid process seems to connect well with the triquetrum bone, excluding the need for an articular disc. However, the male hamadryas baboon that was dissected in the present study had an additional carpal bone that was not found in the other two specimens. Since it was located between the styloid process of the ulna and the triquetrum bone, it resembled an articular disc at first sight. Nevertheless, it was a bony structure and was attached to the dorsal radioulnar ligament proximally and to the lateral collateral ligament distally. In addition, it sat more in front of the joint between the ulnar styloid process and the triquetrum bone. It is, therefore, plausible that the structure was an ossification of the ligaments in which it was embedded. Future studies on more baboon hands could perhaps render more insight into the potential presence of an articular disc in the articulation between the ulnar styloid process and the triquetrum and/or pisiform bone. No other variations were found between the three dissected specimens. The low number of specimens dissected could be regarded as a limitation of our study. More specimens should be dissected in future studies when potential anatomical variations are to be discovered.
The robust ligaments that are characteristic for terrestrial primates disperse the ground forces over the entire hand [
31]. In this regard, numerous studies have been published investigating the adaptation of the primate hand to the mode of locomotion. It should therefore not be surprising that manifold dissimilarities in the conformation of the baboon and human hand are present [
31]. Reviewing the literature on this topic stretches beyond the scope of the present study. As a veterinarian, gaining insight into the specific build of the human hand is, nonetheless, superfluous and distracting when being confronted with arm and hand injuries in the baboon. The aim of the present work was to provide the veterinarian responsible for the medical care of baboons with anatomical data on the arthrology of this species’ thoracic limb should medical interventions be imposed.