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. 2018 Oct 31;234(1):120–131. doi: 10.1111/joa.12899

Morphometric, anatomic and radiographic study of the scapula in the white‐footed tamarin (Saguinus leucopus): report of scapular cartilage and one variation in cranial (superior) transverse scapular ligament

Juan Fernando Vélez‐García 1,2,✉, María José Monroy‐Cendales 2, Fabian Enrique Castañeda‐Herrera 1,3
PMCID: PMC6284428  PMID: 30378101

Abstract

The white‐footed tamarin (Saguinus leucopus) is an endangered endemic primate of Colombia, mainly due to the deforestation of its habitat and illegal trade, which generates a high incidence of these animals in wildlife care centres. Musculoskeletal system disorders in S. leucopus are one of the most common diseases and therefore the aim of this study was to contribute to the morphologic studies with a morphometric, anatomic and radiographic description of the scapula in this species to provide a basis for medical interventions, surgical approaches, radiologic diagnoses and comparative functions of this bone. Gross dissections of each scapular region were made in eight specimens without a diagnosis of osteomuscular disease. These specimens died from natural cases in the wildlife care centres of the Corporación Autónoma Regional de Caldas (CORPORCALDAS); after necropsy their carcasses were fixed with 10% formaldehyde, 5% mineral oil and 1% phenic acid in these centres over the course of at least 1 week. X‐rays of the scapula were taken in the small animal clinic of the Universidad del Tolima, and morphometric data of the scapulae were obtained with a digital calliper. The scapula of the white‐footed tamarin was a flat triangular bone with a deep scapular notch in its cranial margin, where there was a cranial transverse scapular ligament that was absent in two specimens. The coracoid process was highly developed, medially covering the humeral joint. The dorsal margin was covered by the scapular cartilage, which was highly developed in the caudal angle. In the dorsal fourth of the caudal margin, there was a surface from which the m. teres major originated. The lateral surface had a scapular spine with a long hamatus process of the acromion until the lateral part of the humeral joint. The infraspinatus fossa was wider than the supraspinous fossa. On the costal surface, the subscapular fossa was formed by three subscapular lines and one subscapular ridge, the latter helping to form the surface for the m. teres major. In the two radiographic views, caudocranial to the scapula and dorsoventral to the thorax, the scapular spine, acromion, coracoid process, scapular incisura, supraglenoid tubercle, caudal margin, subscapular ridge, and the joints with the clavicle and the humerus could be observed. The scapula of the white‐footed tamarin presented bony reliefs that share characteristics with other primates but also with domestic mammals due to its quadrupedal locomotion, which allowed us to correlate its morphologic adaptation with its quadrupedal arboreal displacement.

Keywords: primate, radiology, scapula, superior transverse scapular ligament, suprascapular incisura, thoracic limb

Introduction

The white‐footed tamarin (Saguinus leucopus) is an endemic primate of Colombia which is in the Endangered (EN) category according to the Red List of the IUCN (International Union for Conservation of Nature and Natural Resources) due to several causes such as its capture for the illegal trade as a pet, deforestation, and reduction of its habitat due to agricultural activities and construction (Morales‐Jiménez et al. 2008; Defler, 2010). Illegal traffic is constant in this species, which increases the probability of finding them in wildlife centres and zoos, where they may have been traumatized by the processes of capture, commercialization, transport and group fights (Fox et al. 2008); therefore, the musculoskeletal system is one of the most affected in this species (Varela et al. 2010) and it is of great importance to provide specific anatomic knowledge to perform adequate clinical and surgical treatment.

The body of the primates has been adapted to different forms of locomotion, from bipedal species such as the human, brachiators such as gibbons, and quadrupedal species as in the majority of primates; the latter form of locomotion requires the support of all four limbs for terrestrial and arboreal displacement, as is the case of Saguinus leucopus (Ankel‐Simons, 2007; Defler, 2010). The primate shoulder plays an important role in quadrupedal movement between trees; thus, these primates have muscles that provide adequate strength to move the levers formed by bones and joints, as well as restricting movement to avoid falling when the animal is supported by their limbs (Kardong, 2012; Vélez‐García et al. 2013). Among the bones that articulate in the shoulder, the scapula plays a fundamental role, as it articulates synovially with the humerus and the clavicle in primates, which gives greater mobility to this articulation when compared with mammals without a clavicle (Ankel‐Simons, 2007; Dyce et al. 2010; Preuschoft et al. 2010). For these movements, the scapula serves as the origin and insertion of muscles that generate movements of this bone, as well as the shoulder and complementarily the elbow (Dyce et al. 2010; Hermanson, 2013; Vélez‐García et al. 2013; Standring, 2016).

The scapula is a flat triangular bone located in the posterolateral part of the pectoral regions in humans (dorsolateral in domestic mammals), formed by three angles and three margins. In the upper (human) or cranial (quadruped) margin, there is a scapula notch (Incisura scapulae) through which the suprascapular nerve passes (Standring, 2016; Dyce et al. 2010). In humans, there are two ligaments in relation to the scapular incisura, one superior transverse scapular ligament (STSL) between the upper margin and coracoid process (Standring et al. 2016) and, in some cases, the anterior coracoscapular ligament (Avery et al. 2002; Bayramoğlu et al. 2003). The suprascapular nerve passes between the scapular incisura and the STSL; the different shapes of this ligament and the notch have been studied extensively because some of these shapes predispose to nerve entrapment (Bayramoğlu et al. 2003; Polguj et al. 2011, 2012a,b,c, 2014, 2016; Büyükmumcu et al. 2013; Kannan et al. 2014; Agrawal et al. 2015). In domestic mammals, this nerve passes between the supraspinatus and subscapular muscles (Budras et al. 2007, 2011, 2012; Evans & De Lahunta, 2013), a situation that normally does not occur in humans, and there is no ligament in relation with the scapular incisura. In the present investigation, we therefore performed a comparison between the scapula of S. leucopus (a quadrupedal primate) and other species, such as humans (a bipedal primate), domestic mammals and other primates. This investigation also contributes to the macroscopic and radiographic anatomic knowledge of the scapula in S. leucopus, to provide bases that serve for medical interventions, surgical approaches and radiologic diagnoses of this bone.

Material and methods

Eight cadavers of S. leucopus, four females and four males with no diagnosis of osteomuscular disease and without alterations in their thoracic limbs, were studied. Only adult animals were included, as corroborated by radiography. All specimens involved in this study weighed between 300 and 460 g, and died from natural causes between 2012 and 2013 in the wildlife care centres of Corporación Autónoma Regional de Caldas (CORPOCALDAS), the environmental authority of Caldas in Colombia; all animals were recovered from animal trafficking. No animal was sacrificed for the purposes of this study, which it was approved by the bioethics committee of the Universidad del Tolima. After a necropsy performed in the wildlife care centres, the specimens were fixed via subcutaneous and intramuscular routes with a solution of 10% formaldehyde, 5% mineral oil and 1% phenic acid. Subsequently, they were conserved by submersion in the same solution but without mineral oil for at least a week.

Gross dissections were made in the anatomy veterinary laboratory of the Universidad del Tolima, where both thoracic limbs were dissected from superficial to deep, focusing on the scapular (Regio scapularis) and humeral joint (Regio articulationis humeri) regions, in which the attachments (origins and insertions) of the muscles and ligaments into scapula were reviewed, as well as the synovial articulations with humerus and clavicle. Finally, all the soft tissues of the scapula were removed and it was posteriorly immersed in 10% hypochlorite until it was bleached. Photographs were taken during the process of dissection and maceration, and the anatomic characteristics were described according to the terminology of the Nomina Anatomica Veterinaria (International Committee on Veterinary Gross Anatomical Nomenclature, 2017) because it was a quadrupedal animal, and the Terminologia Anatomica (Federative International Committee on Anatomical Terminology, 1998) for a proposed comparison with the humans.

Radiographic study

Previous to gross dissections, radiographs were taken of both scapular regions of the specimens. The X‐ray machine (Ecoray 15‐25) of the small animal clinic was used at a source‐to‐image distance of 100 cm at 40 kVp and 80 mAs. The specimens were positioned in lateral decubitus and after the humeral joint was extended to obtain a caudocranial radiographic view of the scapula. Afterwards, they were positioned in ventral decubitus to obtain a dorsoventral radiographic view of the cranial part of the thorax where the two scapulas were observed. The images were obtained employed a computed radiography (CR) unit (AGFA CR 30‐X joined to a NX image processor software, AGFA Mortsel, Belgium).

Morphometric data

The following morphometric measurements of the scapulae (eight left and eight right) were obtained by an investigator with a digital calliper (Mitutoyo absolute 6‐inch) (Figs 1, 2, 3, 4):

Figure 1.

Figure 1

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Morphometric measurements of the scapula in Saquinus leucopus: 1 – scapular width with cartilage, 2 – scapular width without cartilage, 3 – maximal width with cartilage of scapula, 4 – maximal width without cartilage, 5 – width of supraspinous fossa, 6 – width of infraspinous fossa, 7 – projection length of scapular spine, 8 – scapular length, 9 – length of acromion.

Figure 2.

Figure 2

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Morphometric measurements of the scapular incisura and coracoid process. 10 – Maximal length of coracoid process, 11 – width of coracoid process, 12 – cranial transverse diameter of scapular incisura, 13 – maximal depth of scapular incisura.

Figure 3.

Figure 3

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Morphometric measurements of the glenoid cavity. 14 – Maximal width of glenoid cavity, 15 – minimal width of glenoid cavity: cranial diameter of cavity glenoid near to supraglenoid tubercle, 16 – length of glenoid cavity: distance between the maximal cranial and caudal point of glenoid cavity, 17 – width from coracoid process until acromion: distance between acromion and coracoid process.

Figure 4.

Figure 4

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Morphometric measurements of the surface for the origin of the m. teres major and scapular cartilage. 18 – Surface for the origin of the m. teres major: (a) caudal length, (b) cranial length, (c) dorsal width, (d) ventral width; 19 – scapular cartilage to level caudal angle: (a) dorsal margin, (b) caudal margin, (c) ventral margin.

  1. Scapular width with cartilage: distance between the cranial and cartilaginous caudal angle.

  2. Scapular width without cartilage: distance between the cranial and bony caudal angle.

  3. Maximal width with cartilage of scapula: distance between the maximum projection of cranial margin and cartilaginous caudal angle.

  4. Maximal width without cartilage: distance between the maximum projection of cranial margin and bony caudal angle.

  5. Width of supraspinous fossa: distance between the maximum projection of cranial margin and spine.

  6. Width of infraspinous fossa: distance between the base of the spine and the craniodorsal point of the surface for the m. teres major.

  7. Projection length of scapular spine: distance between the base of the spine and the cranioventral limit of the acromion.

  8. Scapular length: distance between the base of the spine and the centre of the glenoid cavity.

  9. Length of acromion: distance between the craniodorsal limit of the hamatus process and the caudoventral limit of the acromion.

  10. Maximal length of coracoid process: distance between the base and ventral limit of the coracoid process.

  11. Width of coracoid process: distance between the cranial and caudal margins of the coracoid process.

  12. Cranial transverse diameter of scapular incisura: maximal distance between ventral limit of the cranial margin and the base of the coracoid process.

  13. Maximal depth of scapular incisura: distance between the cranial transverse diameter and the maximal caudal limit of the scapular incisura.

  14. Maximal width of glenoid cavity: caudal diameter of cavity glenoid

  15. Minimal width of glenoid cavity: cranial diameter of cavity glenoid near to supraglenoid tubercle.

  16. Length of glenoid cavity: distance between the maximal cranial and caudal point of glenoid cavity.

  17. Width from coracoid process to acromion: distance between acromion and coracoid process.

  18. Surface for the origin of the m. teres major:

    • Caudal length: distance between caudodorsal and caudoventral limits of the surface for the m. teres major.

    • Cranial length: distance between craniodorsal and cranioventral limits of the surface for the m. teres major.

    • Dorsal width: distance between craniodorsal and caudodorsal limits of the surface for the m. teres major.

    • Ventral width: distance between cranioventral and caudoventral limit of the surface for the m. teres major.

  19. Scapular cartilage to level of the caudal angle

    1. Dorsal margin

    2. Caudal margin

    3. Ventral margin

Statistical analysis

The morphometric data were tabulated and analysed by descriptive statistics. The mean, standard deviation, median, range, minimum value and maximum value were obtained. The statistical differences between male and female measurements were evaluated using the Mann–Whitney U‐test at α = 0.05 with the software xlstat (Copyright © 2017 Addinsoft) (Tables 1 and 2).

Table 1.

Descriptive statistics of morphometric data of scapulae in Saquinus leucopus

Parameters Mean ± SD Median Range Minimum Maximum
1. Scapular width with cartilage 23.154 ± 0.882 23.205 2.98 21.72 24.7
2. Scapular width without cartilage 21.302 ± 1.102 21.425 4.15 19.35 23.5
3. Maximal width with cartilage of scapula 25.262 ± 0.957 25.505 3.71 23.15 26.86
4. Maximal width without cartilage 23.573 ± 1.996 23.27 9.09 20.08 29.17
5. Width of supraspinous fossa 7.378 ± 0.66 7.325 2.16 6.13 8.29
6. Width of infraspinous fossa 12.513 ± 1.122 12.53 4.03 9.94 13.97
7. Projection length of scapular spine 29.548 ± 1.958 29.75 8.18 24.77 32.95
8. Scapular length 25.966 ± 1.507 26.13 5.78 23.16 28.94
9. Length of acromion 55.84 ± 0.792 5.55 2.78 3.95 6.73
10. Maximal length of coracoid process 7.2888 ± 0.622 7.425 2.79 5.19 7.98
11. Width of coracoid process 2.61 ± 0.254 2.605 1.13 2.2 3.33
12. Cranial transverse diameter of scapular incisura 7.487 ± 1.333 7.335 3.76 5.84 9.6
13. Maximal depth of scapular incisura 2.668 ± 0.348 2.595 1.36 2.02 3.38
14. Maximal width of glenoid cavity 4.238 ± 0.145 4.215 0.6 3.97 4.57
15. Minimal width of glenoid cavity 2.418 ± 0.332 2.455 1.34 1.99 3.33
16. Length of glenoid cavity 6.404 ± 0.344 6.425 1.39 5.51 6.9
17.Width from coracoid process until acromion 11.587 ± 0.707 11.6 2.77 9.99 12.76
18. Surface of the origin for the m. teres major
a. Caudal length: 7.36 ± 1.407 7.675 5 4.41 9.41
b. Cranial length 12.101 ± 2.126 12.44 8.18 7.81 15.99
c. Dorsal width 3.711 ± 0.457 3.735 1.45 3.03 4.48
d. Ventral width 3.22 ± 0.549 3.22 2.18 2.3 4.48
19. Scapular cartilage to level caudal angle
a. Dorsal margin 7.178 ± 0.689 7.185 2.67 6 8.67
b. Caudal margin 3.949 ± 0.402 3.835 1.53 3.4 4.93
c. Ventral margin 6.573 ± 0.748 6.635 3.12 4.47 7.59
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SD, standard deviation.

Table 2.

Median, ranges and P‐value of the Mann–Whitney U‐test to morphometric data of scapulae in males and females of Saquinus leucopus

Parameters (mm) Males Females P‐value U‐test
Median Range Median Range
1. Scapular width with cartilage 23.310 2.980 22.950 2.580 0.937 NS
2. Scapular width without cartilage 21.450 3.810 21.170 2.880 0.000 c
3. Maximal width with cartilage of scapula 25.555 2.610 25.265 2.870 0.382 NS
4. Maximal width without cartilage 24.000 5.520 22.820 7.790 0.382 NS
5. Width of supraspinous fossa 7.920 1.860 7.260 2.110 0.382 NS
6. Width of infraspinous fossa 12.210 4.030 12.350 3.120 0.442 NS
7. Projection length of scapular spine 30.750 3.570 28.515 5.760 0.003 b
8. Scapular length 26.860 2.860 24.745 3.350 0.000 c
9. Length of acromion 5.420 1.750 5.680 2.780 0.959 NS
10. Maximal length of coracoid process 7.600 1.120 7.315 2.480 0.234 NS
11. Width of coracoid process 2.680 0.880 2.515 0.700 0.195 NS
12. Cranial transverse diameter of scapular incisura 6.950 3.690 7.675 3.820 0.878 NS
13. Maximal depth of scapula incisura: 2.590 0.930 2.650 0.980 0.381 NS
14. Maximal width of glenoid cavity 4.215 0.510 4.215 0.480 0.855 NS
15. Minimal width of glenoid cavity 2.515 1.170 2.155 0.640 0.070 NS
16. Length of glenoid cavity 6.580 0.960 6.375 1.390 0.342 NS
17. Width from coracoid process until acromion 11.960 1.910 11.460 1.910 0.105 NS
18. Surface of the origin for the m. teres major:
a. Caudal length 8.095 4.910 7.030 3.970 0.279 NS
b. Cranial length 13.325 4.110 10.080 5.680 0.003 b
c. Dorsal length 4.020 1.000 3.345 1.150 0.023 a
d. Ventral length 3.555 1.510 2.945 1.040 0.005 b
19. Scapular cartilage to level caudal angle.
a. Dorsal margin 7.070 1.770 7.325 2.150 0.281 NS
b. Caudal margin 3.785 0.640 3.915 1.530 0.341 NS
c. Ventral margin 6.590 3.120 6.715 1.380 0.442 NS
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NS, not significant.

a

P < 0.05.

b

P < 0.01.

c

P < 0.001.

Limitations of the study

  1. Only eight cadavers could be used, as S. leucopus is a species in danger of extinction. Although we received more cadavers, these were excluded due to alterations in their scapular regions or because they still had physeal lines and were included in other research; therefore, we could only use a descriptive statistic.

  2. X‐rays were taken in necropsied cadavers preserved in formaldehyde.

  3. The cranial transverse scapular ligament was not measured in these were damaged in most of the cases at the time of detachment from the origin of the supraspinatus and subscapular muscles.

Results

Anatomic description of the scapula

The scapula of the white‐footed tamarin was an elongated triangular flat bone positioned in the cranial part of the thorax obliquely from dorsocaudal to cranioventral. The cranial margin (Margo cranialis) was convex in its two dorsal thirds but developed a pronounced concaved scapular incisura in its ventral third (Incisura scapulae) that ended distally in the coracoid process (Processus coracoideus) (Fig. 5). A cranial transverse scapular ligament was found in both limbs of six specimens (Fig. 5b). This ligament ran from the cranial margin to the base of the coracoid process, which together with the scapular incisura formed a space for the passage of the suprascapular nerve and also served as an intermuscular septum between the supraspinatus and subscapularis muscles. The dorsal margin (Margo dorsalis) was semi‐straight and covered in its entire length by the scapular cartilage (Cartilago scapulae) (Fig. 5b). This cartilage was further developed at the level of the caudal angle (Angulus caudalis) extending up to about of the seventh rib, serving medially for the insertion of the rhomboid and serratus ventralis muscles and laterally as the origin of the m. teres major. The m. serratus ventralis was inserted along the medial side of the dorsal margin.

Figure 5.

Figure 5

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Left scapula of Saguinus leucopus. (a) Lateral view, (b) lateral view with incomplete corrosion, (c) ventral view, (d) medial view, (e) caudal view. 1 – cranial angle, 2 – dorsal margin, 3 – caudal angle, 4 – scapular cartilage, 5 – surface for the origin of the m. teres major, 6 – cranial margin, 7 – scapular incisura, 8 – cranial transverse scapular ligament, 9 – coracoid process, 10 – scapular spine, 11 – acromion, 11′ – hamatus process, 12 – supraglenoid tubercle, 13 – glenoid cavity, 14 – supraspinous fossa, 15 – infraspinatus fossa, 16 – caudal margin, 17 – subscapular fossa, 18 – subscapular lines, 19 – subscapular ridge, 20 – infraglenoid tubercle, 21 – scapular neck. Scale bar: 10 mm.

The caudal margin (Margo caudalis) was straight and projected more caudally at the level of its dorsal third, forming a surface together with the caudal angle where the m. teres major originated; m. teres minor originated in its middle third and the long head of m. triceps brachii in its distal third. The cranial angle (Angulus cranialis) was rounded and the caudal angle (Angulus caudalis) was acute and finished at the scapular cartilage. The ventral angle (Angulus ventralis) consisted of a piriform glenoid cavity (Cavitas glenoidalis) articulating with the humeral head (Fig. 5c), which was fixed to the latter by lateral and medial glenohumeral ligaments. In the cranial part to the glenoid cavity, the supraglenoid tubercle (Tuberculum supraglenoidale) was found providing the origin of the long head of the m. biceps brachii. Just proximal to this, a highly developed coracoid process was found that extended distally and covering the humeral joint medially. In the proximal part of this process, the clavicle was fixed through a coracoclavicular ligament; two coracobrachialis muscles and the short head of the m. biceps brachii originated from its distal part. In the caudal and dorsal part to the glenoid cavity, a small infraglenoid tubercle (Tuberculum infraglenoidale) was observed that was the origin of the long head of the m. triceps brachii (Fig. 5c).

On the lateral surface (Facies lateralis) of the scapula, a highly developed spine (Spina scapulae) was found from dorsal margin to scapular neck where the m. trapezoid inserted and the scapular part of the m. deltoid originated. This spine increases its shape progressively from dorsal to ventral, where it formed an acromion (Acromion) in the presence of a long hamatus process (Processus hamatus) extending to the lateral part of the humeral joint and forming a little arc that ran medially, articulating with the clavicle forming the acromioclavicular joint. The m. omotransversarius was inserted in the acromion, where the acromial part of the m. deltoid originated. Two fossas were formed cranial and caudal to the scapular spine, the supraspinous fossa (Fossa supraspinata), and infraspinous fossa (Fossa infraspinata), respectively; the first is smaller and has an irregular shape, whereas the second was larger and triangular in shape (Fig. 5a,b).

On the costal surface (Facies costalis), the subscapular fossa (Fossa subscapularis) was slightly concave, presenting three subscapular lines and one ridge near the caudal margin where the m. subscapular originated. This ridge was formed from the caudal angle to the caudomedial part of the scapular neck, together with the caudal margin, helping to develop the surface for the origin of the m. teres major at the level of the caudal angle (Fig. 5d,e). The scapular neck (Collum scapulae) was located between the scapular incisura and the infraglenoid tubercle; this was related laterally with the suprascapular nerve (Fig. 5a,d).

Radiographic description of the scapula

In the caudocranial radiographic view, the subscapular ridge and the scapular spine were identified as two highly radiopaque lines that cross to form an ‘X’. The caudal margin was radiopaque but only highly radiopaque when its dorsal third superimposed the subscapular ridge. The acromion was observed as a triangle with radiopaque edges in the distal third of the scapular spine. The glenoid cavity was delimited as a concave radiolucent line which articulated with the humeral head lying between the coracoid process and the acromion. The supraglenoid tubercle was observed as a rounded eminence. The coracoid process was a short line, highly radiopaque, positioned between the clavicle and humeral head. The hamatus process surrounded the humeral neck; the acromioclavicular joint was observed superimposed on the proximal metaphysis of the humerus where there is a radiolucent line. The scapular incisura, the cranial margin, the supraspinous fossa and the infraspinatus fossa were observed as slightly more radiopaque zones than the rest of the surrounding tissues; the dorsal margin and cranial angle were not identifiable (Fig. 6a).

Figure 6.

Figure 6

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Radiographic views of the scapula in Saguinus leucopus. Cd, caudal; Cr, cranial. (a) Ventrodorsal radiographic view; (b) caudocranial radiographic view of the right scapula: 1 – supraspinous fossa, 2 – scapular spine, 3 – infraspinatus fossa, 4 – caudal margin, 5 – scapular incisura, 6 – subscapular ridge, 7 – coracoid process, 8 – acromion, 9 – hamatus process, 10 – supraglenoid tubercle, 11 – glenoid cavity, 12 – cranial margin, 13 – clavicle, 14 – acromioclavicular joint, 15 – subscapular fossa, 16 – humerus.

On the dorsoventral view of the cranial part of the thorax, the caudal margin and the scapular spine could be identified as two lines with high radiopacity. The scapular spine had a greater increase in thickness and radiopacity at the level of the acromion, whereas the cranial margin and the scapular incisura were identified presenting a low radiopacity similar to that observed in the supraspinous and infraspinatus fossas. The coracoid process was observed as an oval, highly radiopaque area between the clavicle and the humeral head. The supraglenoid tubercles situated between the latter and coracoid process had a lower radiopacity. The dorsal margin and the cranial angle were not identifiable (Fig. 6b).

Morphometric study of the scapula

Statistical differences (α = 0.05) between males and females were found in the measurements obtained for the scapular width without cartilage (P = 0.000), projection length of scapular spine (P = 0.003), length of the scapula (P = 0.000), cranial length of the surface for the origin of the m. teres major (P = 0.003), dorsal width for the origin of the m. teres major (P = 0.023), and ventral width for the origin of the m. teres major (P = 0.005). For the other measurements taken, no statistical differences were found between the scapulae of males and females.

Discussion

Comparative anatomic terminology for the scapula

The scapula of S. leucopus has characteristics that are shared between domestic mammals and humans. In humans, the scapula is located in the posterior side of the thorax due to a clavicle that is relatively longer compared with S. leucopus and the anteroposterior compression of the thorax (Ankel‐Simons, 2007; Moore et al. 2010; Standring, 2016). Therefore, the lateral surface of the scapula of S. leucopus in humans is called a posterior surface (Facies posterior) and, on the other hand, due to the bipedal position of the human, its angles are denominated as superior, inferior and lateral, which correspond to the cranial, caudal and ventral angles, respectively, and their margins are designated as superior, inferior and medial (FICAT, 1998), corresponding to the cranial, caudal and dorsal margins, respectively, of S. leucopus and domestic mammals (ICVAGN, 2017; Dyce et al. 2010). Formerly, different anatomic terms have been used, e.g. the dorsal margin was called the vertebral margin due to its proximity to the vertebrae (Howell, 1937; Osman‐Hill, 1959; Stevens et al. 1977; Evans & De Lahunta, 2013) and the caudal margin was called the axillary margin due to it axillary orientation (Osman‐Hill, 1959; Brand, 2008). However, these terms are obsolete, and therefore, our descriptions of the scapula in the S. leucopus conserve the terms for quadrupedal mammals of the Nomina Anatomica Veterinaria (ICVGAN, 2017), which contains the appropriate directional terms for this species. In humans, the Incisura scapulae is denominated as the suprascapular notch [Federative International Committee on Anatomical Terminology (FICAT), 1998], and in domestic mammals as the scapular notch (Dyce et al. 2010; Evans & De Lahunta, 2013, 2017). Scapular incisura is a name closest to Latin; thus, we adopted this name for the scapula in S. leucopus.

Comparative functional anatomy of the scapula

The scapula in primates is located in a more dorsal side to allow greater shoulder mobility compared with other quadruped mammals (Chan, 2007). Laterolateral compression of the thorax in the genus Saguinus as in S. leucopus places the scapula in a more lateral position (Ankel‐Simons, 2007), similar in some ways to that of domestic mammals (Dyce et al. 2010); however, due to the presence of a functional clavicle, the ventral angle of the scapula is located farther lateral to the ribs; therefore, the glenoid cavity is more craniolateral and adapted to the caudal direction of the humeral head (Duque‐Parra & Vélez‐García, 2014), which should allow greater movements of the shoulder and elbow to be able to perform their different arboreal activities (Larson, 1993, 1995), such as improved climbing abilities (Ankel‐Simons, 2007).

The costal surface in domestic mammals has a wide serrata surface (Facies serrata) for the insertion of the ventral serratus muscles, which differs from S. leucopus and humans, where the insertion of this muscle is along the medial side of the dorsal margin of the scapula (Standring, 2016). On the other hand, there is a scapular cartilage on the dorsal margin of the scapula of domestic mammals, which is more developed in ungulates and is present as a narrow band in carnivores (Liebich et al. 2005; Evans & De Lahunta, 2013), where the latter species is similar to S. leucopus; however, in this species it is more developed in the caudal angle but also serves for the insertion of the rhomboideus muscle similar to carnivores (Liebich et al. 2005; Hermanson, 2013). The insertion of the rhomboideus muscles in different non‐human primates is described on to the dorsal margin and not on to scapular cartilage (Diogo & Wood, 2012); therefore, it could be that the majority of the species do not have the scapular cartilage, being similar to humans (Standring, 2016). However, in this species, the dorsal margin and the caudal angle present an ossification centre that ends ossifying after puberty (Standring, 2016), leading us to suggest that by evolution the scapular cartilage in humans and other primates may have developed as a bony part of the scapula and does not remain cartilaginous as in S. leucopus and domestic mammals. In ungulates, however, it is calcified with advancing of age (Liebich et al. 2005). In another quadruped primate, Lemur catta, adequate surfaces for insertion of the extrinsic muscles have been found that permit them to ‘support the body weight and absorb the shock of the footfall at the end of a quadrupedal leap’ (Makungu et al. 2015) This corroborates our findings in S. leucopus for a quadrupedal locomotion in trees by jumping, as reported by Defler (2010). The presence of the scapular cartilage increases the area of insertion of m. rhomboideus (Dyce et al. 2010), which is an extrinsic muscle and together with the cartilage should act as a shock absorber (Liebich et al. 2005).

In Callimico goeldii, it is reported that the caudal margin is virtually double, due to the formation of two lips, one lateral that extends directly from the dorsal margin, and one medial that is formed from the caudal angle (Osman‐Hill, 1959), similar to S. leucopus. However, the medial lip was observed as a ridge from which the subscapularis muscle originates; therefore, the lateral lip was the real caudal margin because that is where the long head of m. triceps brachii and the m. teres minor originate. In Pithecia sp., the caudal angle of the scapula expands to form a margin for the origin of the m. teres major (Fleagle & Meldrum, 1988), being similar to the surface for this muscle in S. leucopus, in other non‐human primates (Mivart, 1867) and clearly reported in L. catta (Makungu et al. 2015) and cercopithecids (Dunham et al. 2015). Although this surface is not found in the terminology of the scapula of humans (FICAT, 1998) or domestic mammals [International Committee on Veterinary Gross Anatomical Nomenclature (ICVGAN), 2017], it can be seen in the figures of the scapula of humans (Standring, 2016), the domestic dog (Hermanson, 2013) and other non‐human primates (Youlatus, 2000). This supports the importance represented by m. teres major in retracting the humerus in order to provide a larger area for its origin and thus greater strength while climbing trunks of the trees (Fleagle & Meldrum, 1988; Dunham et al. 2015). This surface has been found in other mammals such as armadillos and anteaters (Myrmecophaga, Tamandua). In the former species, m. teres major is highly developed for digging (Miles, 1941; Taylor, 1978; Monteiro & Abe, 1999) and the latter species for climbing, defence posture and knocking down ant hills (Taylor, 1978). On the basis of this, we can suggest that the development of this surface plus the scapular cartilage in S. leucopus provides a large enough area to contribute to the strength of the m. teres major for climbing and detaching the bark of the trees for eating latex (Defler, 2010).

At the level of the scapular spine of S. leucopus, the deltoid tubercle (Tuberculus deltoideus) found in humans (FICAT, 1998)] and a tuberosity of the scapular spine (Tuber spinae scapulae) of horses and pigs (ICVGAN, 2017; Liebich et al. 2005; Dyce et al. 2010) were not observed. In S. leucopus, an acromion similar to that in humans was found, which turned medially to articulate with the clavicle forming the clavicular articular facet (Standring, 2016). This medial projection was called a hamatus process according to the Nomina Anatomica Veterinaria (ICVGAN, 2017), being similar to that found in L. catta (Makungu et al. 2015); however, the suprahamatus process (Processus suprahamatus) of the cat is absent (ICVGAN, 2017; Dyce et al. 2010). The longer hamatus process in S. leucopus provides a major area for the origin of the acromial part of the m. deltoideus, which corroborates the increasing role of this muscle in primates (Brand, 2008), as it should act as a lateral rotator of the humerus, abductor and flexor of the humeral joint similar to humans (Standring, 2016); however, because S. leucopus is a pronograde species, the action of this muscle should be less compared with orthograde species such as humans, where the acromion overlies the humeral head (Brand, 2008), and different from domestic dog, where it only abducts and flexes the shoulder because its acromion is smaller (Hermanson, 2013).

The presence of lines in the subscapular fossa in S. leucopus is different to Saimiri sciureus, where two or three crests are reported for the origin of the m. subscapularis (Blanco et al. 2015); however, in S. leucopus, the development of only one ridge to subscapularis muscle was evident. The development of these lines and one ridge could have occurred in S. leucopus to increase the area of origin for the m. subscapularis and allow it to stabilize the humeral joint medially. This increase has been associated with generating an increase in the area of origin of the m. infraspinatus (Brand, 2008); therefore, it could explain the larger infraspinous fossa in S. leucopus.

As other primates, the coracoid process in S. leucopus is highly developed (Stevens et al. 1977; Casteleyn et al. 2012; Makungu et al. 2015; Standring, 2016) because it was necessary to permit an adequate adduction of the shoulder joint by the coracobrachialis muscle, which should provide the strength necessary for vertical suspension in the trunks of the trees (Defler, 2010), domestic mammals, in contrast, have a small coracoid process (Dyce et al. 2010).

The cranial transverse scapular ligament of S. leucopus is not found in domestic mammals (Liebich et al. 2005; Dyce et al. 2010; ICVGAN, 2017); however, it may also be absent in S. leucopus. In humans, this ligament is permanent and is called the superior transverse scapular ligament (Lig. transversum scapulae superius) because there is an inferior ligament (Lig. transversum scapulae inferius) between the acromion and the margin lateral to the glenoid cavity; however, its presence is an anatomic variant (FICAT, 1998; Moore et al. 2010; Standring, 2016) and it was absent in S. leucopus. In humans, the ossification of the superior transverse scapular ligament has been reported as an anatomic variant, forming a foramen through which the suprascapular nerve passes (Bayramoğlu et al. 2003; Büyükmumcu et al. 2013; Kannan et al. 2014; Polguj et al. 2014; Agrawal et al. 2015; Standring, 2016), a situation that can normally occur in primates of the genus Ateles (Mivart, 1867; Youlatus, 2000; Ackermann, 2003), Lagothrix (Mivart, 1867; Ankel‐Simons, 2007) and in Callimico goeldii (Osman‐Hill, 1959). Therefore, this ossification in humans could be for phylogenetic reasons, but it did not occur in our study in S. leucopus. In humans, this ligament can be found mainly in two shapes, in a band‐shaped or a fan‐shaped (Polguj et al. 2014), where the latter was the only form of this ligament in S. leucopus. Other shapes have been found in humans, e.g. bifid (Polguj et al. 2012a) and trifid (Polguj et al. 2012b), and on some occasions another ligament called the anterior coracoscapular ligament may be present (Avery et al. 2002; Bayramoğlu et al. 2003). It has even been hypothesized that when this ligament is ossified together with the superior transverse scapular ligament, it develops a double foramen (Polguj et al. 2012c), but none of these shapes was found in S. leucopus.

The cranial margin of the scapula in S. leucopus presented a common shape for all specimens, being very similar to that of domestic mammals (Dyce et al. 2010) and different to the upper margin of the scapula in humans, where it is commonly straight and oblique towards inferolateral. The scapular incisura in humans can have several shapes: ‘V’‐shaped (Iqbal & Iqbal, 2011; Agrawal et al. 2015), ‘U’‐shaped (Iqbal & Iqbal, 2011; Agrawal et al. 2015), inverted ‘V’‐shaped (Iqbal & Iqbal, 2011; Agrawal et al. 2015), without a notch (Iqbal & Iqbal, 2011; Mahato & Suman, 2013; Rekha, 2013; Agrawal et al. 2015; Pawar & Pawar, 2015), with a discrete notch (Polguj et al. 2011; Agrawal et al. 2015) and ‘J’‐shaped (Iqbal et al. 2010; Chhabra et al. 2016), the latter shape being similar to the scapular incisura of S. leucopus but differing in the convexity of the cranial margin, which in S. leucopus gives it a greater cranial projection and, therefore, wider supraspinous and subscapular fossae. This gives a wider origin for the m. supraspinatus and m. subscapularis, confirming a greater activity of these two muscles in quadrupedal tree locomotion, whereas in humans, these muscles normally have no relationship, even when the nerve goes through the scapular incisura, except when the m. subscapular is hypertrophied – which is another cause of nerve entrapment in humans (Bayramoğlu et al. 2003).

Although the presentation of this ligament increased the area of the supraspinous fossa, it is not always necessary, AS in some specimens it may be absent. The smaller shape of the supraspinous fossa compared with the infraspinatus fossa is similar to that in other primates (Brand, 2008; Young, 2008; Dunham et al. 2015; Makungu et al. 2015).

Primate species of the genus Ateles have comparatively greater differences in scapular morphology with respect to other genera due to their suspensory locomotion, in which the bone reliefs are more marked, e.g. an acromion that more projected laterally and a glenoid cavity more ovate and located more cranially, allowing these species a wide movement of the humeral joint compared with other quadruped primates such as Saguinus oedipus (Ackermann, 2003) and S. leucopus. A functional study of the shoulder in different primates reported that the scapula of quadruped primates is longer compared with that of primates with suspensory activities (Preuschoft et al. 2010), being similar to S. leucopus, which has a long and narrow scapula similar to domestic mammals and different from humans, in whom it is relatively wider and shorter (Ankel‐Simons, 2007). These differences are mainly due to the fact that this bone is modified according to the functional needs of each form of locomotion (Larson, 1993; Monteiro & Abe, 1999; Pearson & Lieberman, 2004; Martí et al. 2013) and it is therefore one of the bones that have undergone more morphologic adaptations during evolution (Brand, 2008).

Comparative radiologic anatomy of the scapula

For radiologic assessment of the scapula in small animals, it is recommended that views of the mediolateral and craniocaudal incidences be taken, to evaluate the scapula and humeral joint (Spaulding & Voges, 2015); however, the shoulder biomechanical characteristics of S. leucopus permit a great capacity for abduction of their thoracic limbs; therefore, the dorsoventral incidence of the cranial part of the thorax would show a complete lateromedial view of both scapulas. This view also allows a bilateral evaluation of the clavicle, humeral joint and acromioclavicular joint in a single image, similar to that recommended in humans, due to the possibility of comparing findings between the two limbs (Valencia et al. 2015). In L. catta in the mediolateral and caudocranial radiographic views of the shoulder joint, similar characteristics to S. leucopus were observed; however, in L. catta, the scapular incisura was not very deep and the subscapular ridge was not present (Makungu et al. 2015).

Comparative morphometric study of the scapula

Several studies in humans have evidenced scapular lengths greater in males than in females (Di Vella et al. 1994; Dabbs, 2010; Machado et al. 2011; Oliveira‐Costa et al. 2016), similar to this study in S. leucopus. The differences found in the sizes of the bones in males and females are attributed in humans to the distribution of the work according to sex in ancient humans, when men had to perform greater physical efforts, which required a greater dietary protein requirement, and they therefore developed larger muscles and bones (Charisi et al. 2011; Oliveira‐Costa et al. 2016). Scapular growth depends almost entirely on the development of their associated muscles (Hrdlička, 1942). The males of S. leucopus spend a greater amount of time in social type activities, exploration, recognition and locomotion compared with the females (Monsalve et al. 2007); this could explain a larger scapula in males because these activities could lead to a higher consumption of insects (more protein), which is associated with a greater effort in the movements of the thoracic limbs, generating more growth of the scapula.

Conclusions

  1. The scapula of the S. leucopus has anatomic characteristics adapted to quadrupedal locomotion in the trees. It shares characteristics with other primates such as bone reliefs, position and elongation, but it was differentiated in terms of the presence of the scapular cartilage which is similar to that of carnivores and the variable presentation of the cranial transverse scapular ligament, which are structures that must be taken into account in clinical and surgical scapula procedures in this species and allow us correlate its morphologic adaptation for its quadrupedal arboreal displacement.

  2. Its bony reliefs could be identified dorsoventral of the thorax and caudocranial of the scapula in radiographic views, except the dorsal margin and cranial angle.

  3. According to the Mann–Whitney U‐test, the present study evidenced statistically significant sexual dimorphism for some measurements obtained in the scapulae of S. leucopus.

Author contributions

Juan Fernando Vélez‐García: Conception and design of the study, morphometric and anatomic descriptive data acquisition and interpretation, drafted the article and approved the final version of the article. María José Monroy‐Cendales: Conception and design of the study, data acquisition and interpretation, and drafted the article. Fabian Enrique Castañeda‐Herrera: Conception and design of the study, data acquisition and interpretation, and drafted the article.

Acknowledgements

Thanks to Universidad del Tolima, Universidad de Caldas and CORPOCALDAS for financially supporting this research and Dr Diego Fernando Echeverry Bonilla, who advised us to take X‐rays and the vet Monica Franco, who fixed the cadavers in the CRFSOC (Centro de Rehabilitación de Fauna Silvestre del Oriente de Caldas).

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