Introduction

Crab-eating raccoon (Procyon cancrivorus) is a species belonging to the family Procyonidae, suborder Caniformia, and order Carnivora (Nyakatura and Bininda-Emonds 2012; Hassanin et al. 2021). It is only geographically distributed in the American continent from Mexico to Argentina and Uruguay (Reid et al. 2016). The family Procyonidae phylogenetically diverged from the superfamily Musteloidea with other families (Mustelidae, Mephitidae, and Ailuridae) around 37.4–33.0 million years ago (Hassanin et al. 2021). Within the family Procyonidae are the extant genera Procyon (raccoons), Nasua and Nasuella (coatis), Bassaricyon (olingos), Bassariscus (ringtails), and Potos (kinkajous), where the latter was the first to diverge in the Oligocene while the others diverged posteriorly in the Miocene (Hassanin et al. 2021). Among them, the genus Procyon is anatomically characterized by having long thoracic limbs with manus adapted to a semidigitigrade support (McClearn 1992), and high tactile sensitivity (Vélez-García et al. 2023b). These limbs are mainly used for cursorial locomotion (terrestrial quadrupedalism), but also to swim, manipulate food, and climb trees when is vitally necessary, such as escape from predators (Nowak 2005; Whiteside 2009; Santos et al. 2015). This species, in addition to feeding vegetables, also eats aquatic vertebrates, thus it has adapted to swim and catch these animals underwater (Pellanda et al. 2010; Ceron et al. 2020). To these functions in this species, the antebrachial muscles perform several movements, such as rotation, flexion, and extension of the manus and digits (Perdomo-Cárdenas et al. 2021; Vélez-García et al. 2022a, b; Tarquini et al. 2023). However, the proximal thoracic limb muscles must act to move and fix the shoulder and elbow joints, giving support in the thoracic limb to allow more precise movements of the manus (Ercoli et al. 2015; Vélez-García et al. 2023a).

The intrinsic muscles of the scapular, shoulder, and brachial regions have been mostly studied in several caniforms to review interspecific gross anatomical differences (Fisher et al. 2009; Ercoli et al. 2015; Pereira et al. 2016; Souza-Junior et al. 2018; Vélez et al. 2018; Vélez-García et al. 2018b, 2023a; Smith et al. 2020; Tarquini et al. 2023). Specifically on P. cancrivorus, there are only four anatomical studies where the shoulder and brachial muscles are involved (Windle 1888; Pereira et al. 2010; Santos et al. 2010b; Tarquini et al. 2023). Among them, the more recent study performed a detailed anatomical description of Nasua nasua, where only the differences with P. cancrivorus were included (Tarquini et al. 2023). There are several differences among these studies regarding some muscles. Among them, the m. triceps brachii has been reported with three (Windle 1888), four (Pereira et al. 2010; Santos et al. 2010b), and five heads (Tarquini et al. 2023). The m. biceps brachii was reported to insert onto the radial and ulnar tuberosities (Pereira 2010; Santos et al. 2010b), and only onto the radial tuberosity (Windle 1888; Tarquini et al. 2023). The m. brachialis was also reported with insertions onto radial and ulnar tuberosities (Santos et al. 2010b), only onto radial tuberosity (Pereira et al. 2010) or proximomedial aspect of the ulnar shaft (Tarquini et al. 2023). These insertions to both muscles could be intraspecific anatomical variations in P. cancrivorus, since the brachialis and biceps brachii muscles in most species of the infraorder Arctoidea only insert onto the ulna and radius, respectively (Windle and Parsons 1897; Davis 1964; Böhmer et al. 2020; Vélez-García et al. 2023a). The other insertion onto the ulna by the m. biceps brachii is normally only present in species of the family Canidae (Windle and Parsons 1897; Pereira et al. 2016; Souza-Junior et al. 2018; Vélez et al. 2018; Böhmer et al. 2020; Hermanson 2020). Therefore, one of the characteristics to review in the present study is the anatomical arrangement of the biceps brachii and brachialis muscles in P. cancrivorus.

Caudal to the m. tensor fasciae antebrachii was found an accessory belly with origin from the m. cutaneus trunci, which the authors concluded that said muscle is not a part of the m. tensor fasciae antebrachii (Tarquini et al. 2023). However, these authors did not take into account the innervation, which should be included together with the topology to infer the evolutionary muscle derivation (Diogo and Abdala 2010), such as has been performed in other muscular groups in carnivorans (Diogo et al. 2012; Vélez-García and Miglino 2023; Vélez‐García et al. 2023c). For this belly to be considered part of the cutaneous trunci muscle, it would have been innervated by the lateral thoracic nerve. Specifically, in the procyonid P. flavus, the cranial belly to the m. tensor fasciae antebrachii was considered part of this muscle since it is innervated by the radial nerve (Vélez-García et al. 2023a). Therefore, one of the hypotheses of the present study is that the accessory belly is part of the m. tensor fasciae antebrachii, and not of the m. cutaneus trunci in P. cancrivorus.

Another muscle that is not taken into account in several studies is the m. anconeus medialis (m. anconeus epitrochlearis) (Windle 1888; Pereira et al. 2010; Santos et al. 2010b). In a recent study, this muscle was considered as a head of the m. triceps brachii (Tarquini et al. 2023). This may have occurred because the name of this muscle is not present at the Nomina Anatomica Veterinaria (International Committee on Veterinary Gross Anatomical Nomenclature 2017), and its evolutionary derivation was not considered as proposed in vertebrates (Diogo et al. 2018). In a former study and a recent study performed through a literature review and direct gross dissections in non-ursid arctoids was established that the m. anconeus medialis is the most constant muscle in these species and is innervated by the ulnar nerve (Windle and Parsons 1897; Vélez-García et al. 2023a). In the domestic cat (Felis catus), there is one author who agrees with the name m. anconeus medialis because it is independent of the m. triceps brachii and is located medially collateral to the m. anconeus, which thus is named m. anconeus lateralis (Barone 2020b). Thereby, in the procyonid P. flavus, the m. anconeus medialis was not considered as a head of the m. triceps brachii since its origin and insertion were independent, and it was innervated by the ulnar nerve (Vélez-García et al. 2023a). This agrees with the evolutionary derivation of the m. anconeus medialis with the m. flexor carpi ulnaris, such as has been found in vertebrates from amphibians (Diogo and Abdala 2010; Diogo et al. 2018). Therefore, another hypothesis is that the m. anconeus medialis in P. cancrivorus is not a head of the m. triceps brachii, and conserves the evolutionary origin of most mammals.

The present study aimed to review the topology and anatomical variants of the intrinsic scapular, shoulder, and brachial muscles in P. cancrivorus compared with those reported in previous studies (Windle 1888; Pereira et al. 2010; Santos et al. 2010b; Tarquini et al. 2023). The arterial supply to these muscles is also described to complement the study. Besides, to discuss the evolutionary derivation, the innervation reported previously was retaken in more detail (Vélez-García et al. 2023b). All these characteristics will contribute to the knowledge of evolutionary adaptations, muscle reconstructions in fossils, and veterinary procedures (Tarquini et al. 2019; Dunn et al. 2022; Vélez‐García et al. 2022b).

Materials and methods

Six cadavers of P. cancrivorus fixed in 10% formaldehyde (two females and four males) were used. Two specimens that had been run over on roads of the Goiás State (Brazil) were collected to the Wild Animals Comparative Anatomy Laboratory of the Universidade Federal de Catalão with the environmental license number 37072-2 (SISBIO). Two specimens were collected from roads of Caldas Department (Colombia) and donated firstly to the Universidad de Caldas by the CORPOCALDAS (environmental authority of Caldas Department, Colombia), and after from this entity, the cadavers were transported to the Universidad del Tolima. Two specimens had died of natural causes in the wildlife care center of CORTOLIMA (environmental authority of Tolima Department, Colombia) and donated to the Universidad del Tolima. These four specimens remain at the Veterinary Anatomy Laboratory of the Universidad del Tolima. Five specimens were previously dissected for the brachial plexus study (Vélez-García et al. 2023b); however, the characteristics of the intrinsic shoulder and brachial muscles were not reported in that study. In Vélez-García et al. (2023b), one specimen had been identified as an adult due to its size, however, the long bones of its thoracic limbs had physis after removing the muscles (PcS5—Table 1). Thus, in the present study, it was considered a sub-adult animal similar to the sixth specimen, and each specimen was identified in order of dissection (Table 1).

Table 1 Identification of Procyon cancrivorus specimens and thoracic limbs dissected
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Gross anatomical dissections from superficial to deep of the intrinsic scapular, shoulder, and brachial muscles of all specimens were performed. The terminology was mainly based on the Nomina Anatomica Veterinaria (International Committee on Veterinary Gross Anatomical Nomenclature 2017), and other muscle terms were used, such as m. anconeus lateralis, m. anconeus medialis (Barone 2020b), pars caudalis and pars cranialis of the m. tensor fasciae antebrachii (Vélez-García et al. 2023a). The muscle architecture was defined based on its shape and the fiber direction in longitudinal sections performed at the muscle belly. The thoracic limb bones of a juvenile male specimen identified with the number 009613 from the Zoology Museum of the University of Sao Paulo were used to perform the muscle maps. The arterial supply was only studied in three specimens (PcS1, PcS5, and PcS6), which had vascular repletion with natural latex tinctured with red vinyl. Photographs of the dissections were taken with a Canon T5i camera associated with a macro lens of 60 mm, and an EOS 6D camera associated with a macro lens of 100 mm. This research was approved by the bioethics committees of the Universidad del Tolima (agreement number 2.3-059), Universidade de São Paulo (CEUAx agreement number 3928240820), and Universidade Federal de Catalão (CEUA-UFCAT agreement number 01/22).

Results

Lateral scapular and shoulder muscles

M. deltoideus

The m. deltoideus has two parts, pars acromialis and pars scapularis (Fig. 1). The pars acromialis is unipennate, originates via tendinous and fleshy fibers from the ventral margin of the hamatus process of the acromion. The origin is tendinous superficially and fleshy deep- and caudally. Distally its fleshy fibers join to the pars scapularis tendon and also insert directly onto the deltoid tuberosity. It also receives muscle fibers cranially from the m. cleidobrachialis. The pars scapularis is triangular and fusiform, originates via an aponeurosis from the lateral and medial aspects of the fascia over the m. infraspinatus and the distal half of the scapular spine. It originates via fleshy fibers from the caudal aspect of the suprahamatus process (Fig. 2). It forms a wide tendon, which is also formed by a few tendinous fibers of the pars acromialis, and it receives fleshy fibers from this latter to insert onto the distal half of the lateral aspect to the crest of greater tubercle and deltoid tuberosity (Fig. 3). In one specimen unilaterally (PcS1-RTL), the pars scapularis also originates from the middle third of the caudal margin of the scapula via a common aponeurosis with the m. teres minor (Fig. 4). Both parts are innervated by the axillary nerve and supplied by the caudal circumflex humeral artery. The pars scapularis is also supplied by the subscapular artery (Fig. 1).

Fig. 1
figure 1

Lateral views of the intrinsic shoulder and brachial muscles in Procyon cancrivorus. Superficial (a) and deep views (b) of left thoracic limbs. B, m. brachialis; BcN, Brachiocephalic nerve; CdCHA, caudal circumflex humeral artery (a. circumflexa humeri caudalis); ClB, m. cleidobrachialis; Da, m. deltoideus pars acromialis; Ds, m. deltoideus pars scapularis; IS, m. infraspinatus; LD, m. latissimus dorsi; SbA, subscapularis artery (a. subscapularis); SS, m. supraspinatus; SS’, cranial accessory belly of SS; SS’’, caudal accessory belly of SS; TB, m. triceps brachii; TBLa, caput laterale; TBLo, caput longum; TFACd, m. tensor fasciae antebrachii pars caudalis; TMaj, m. teres major; TMin, m. teres minor. White bars: 10 mm

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Fig. 2
figure 2

Muscle maps in a left scapula of Procyon cancrivorus. Lateral (a), caudal (b), medial (c) and cranial (d) views. BB, m. biceps brachii; CB, m. coracobrachialis; Da, m. deltoideus pars acromialis; Ds, m. deltoideus pars scapularis; IS, m. infraspinatus; LD, m. latissimus dorsi; Sb, m. subscapularis; Sb + SS, intermuscular septum of Sb and SS; Sb + TMaj, intermuscular septum of Sb and TMaj; SS, m. supraspinatus; TBLo, m. triceps brachii caput longum; TMaj, m. teres major; TMaj’, Origin of TMaj over IS; TMin, m. teres minor. White bars: 10 mm

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Fig. 3
figure 3

Muscle maps in a left humerus of Procyon cancrivorus. Cranial (a), lateral (b), medial (c), caudal (d), proximal (e), and distal (f) views. AL, M. anconeus lateralis; AM, m. anconeus medialis; B, m. brachialis; CB, m. coracobrachialis; D, m. deltoideus; IS, m. infraspinatus; ISB, infraspinous bursa; Sb, m. subscapularis; SS, m. supraspinatus; TB, m. triceps brachii; TBa, caput accessorium; TBLa, caput laterale; TBm, caput mediale; THR, Transverse humeral retinaculum; TMaj + LD, common insertion of the teres major and latissimus dorsi muscles; TMin, m. teres minor. White bars: 10 mm

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Fig. 4
figure 4

Deep views of the intrinsic shoulder and brachial muscles in Procyon cancrivorus. a Lateral view of a right scapular region after to retract the supraspinatus and infraspinatus muscles; b deep lateral view of the brachial region after to retract the caput laterale of the m. triceps brachii; c medial view of a right m. biceps brachii with two heads. AL, m. anconeus lateralis; AM, m. anconeus medialis; Ax, axillaris nerve; B, m. brachialis; BB, m. biceps brachii; BBa, accessory head of BB; CdCHA, caudal circumflex humeral artery; ClB, m. cleidobrachialis; Da, m. deltoideus pars acromialis; DBA, deep brachial artery (a. profunda brachii); Ds, m. deltoideus pars scapularis; Ds + TMin, common origin tendon of both muscles; IS, m. infraspinatus; R, radial nerve; RCA, radial collateral artery (a. collateralis radialis); Sb, m. subscapularis; SbAp, perforating branch of the subscapular artery; SS, m. supraspinatus; SSc, suprascapular nerve; TB, m. triceps brachii; TBa, caput accessorium; TBLa, caput laterale; TBLo, caput longum; TBm, caput mediale; TMaj, m. teres major; TMin, m. teres minor. White bars: 10 mm

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M. supraspinatus

The m. supraspinatus is bipennate, originates via fleshy fibers from the supraspinous fossa, cranial aspect of the scapular spine (Figs. 1, 2), and intermuscular septum with the m. subscapularis (Supplementary Fig. 1). It also originates dorsally from the scapular cartilage in the juvenile specimens. It inserts onto the proximal extreme of the greater tubercle of the humerus via a strong tendon (Figs. 2, 3, 4a), which begins its development internally at the two proximal thirds of the belly, and is only free of muscle fibers close to its insertion. In two cases bilaterally (PcS5 and PcS6), it also inserted caudally via fleshy fibers. In one case (PcS5-LTL), an accessory belly originated from the distal margin of the acromion, and inserted via fleshy fibers caudally to the supraspinatus tendon. In that same limb (PcS5-LTL), an accessory belly was formed cranially, which was separated from the main belly for the pass of the brachiocephalic nerve to the shoulder skin (Fig. 1b). The muscle is innervated by the suprascapular nerve (Fig. 4), and in one case was also innervated by the brachiocephalic nerve (PcS5-LTL). The lateral and medial branches of the suprascapular artery supply the muscle.

M. infraspinatus

The m. infraspinatus is pyramidal and bipennate, originates in a fleshy manner from the infraspinous fossa, the caudal aspect of the scapular spine, the medial aspect of the suprahamatus process, and the aponeurosis of origin of the m. teres minor (Figs. 1, 2). It also originates dorsally from the scapular cartilage in the juvenile specimens. It inserts via a tendon onto the caudolateral aspect of the greater tubercle (facies m. infraspinatus), and there is a synovial bursa deep to the infraspinatus tendon (Bursa subtendinea m. infraspinati) (Figs. 1, 3). It is innervated by the suprascapular nerve, and is supplied by the subscapular, caudal circumflex humeral, and circumflex scapular arteries (Figs. 1, 4a; Supplementary Fig. 2).

M. teres minor

The m. teres minor is fusiform, originates via an aponeurosis from the ventral third of the scapular caudal margin (Fig. 2), and inserts onto the teres minor tuberosity, distally to the insertion of the supraspinatus tendon (Figs. 1, 3). It originated from the ventral half of the scapular caudal margin in PcS6, and the two ventral thirds in PcS5. In one specimen unilaterally (PcS1-RTL), it originated via a common aponeurosis with the m. deltoideus pars scapularis (Fig. 4a). It is innervated by the axillary nerve, and supplied mainly by the caudal circumflex humeral artery and a branch of the subscapular artery. This latter branch passed between the two parts of the origin tendon of m. triceps brachii caput longum, which also supplied to the m. subscapularis (Figs. 1, 4b).

Medial scapular and shoulder muscles

M. teres major

The m. teres major is unipennate, originates from the lateral and caudal surfaces of the caudal angle of the scapula, the adjacent fascia over the m. infraspinatus close to the caudal angle, the dorsal third of the caudal margin of the scapula, and the dorsal half of the intermuscular septum with the m. subscapularis (Figs. 2, 5, and Supplementary Fig. 1). It joins to the m. latissimus dorsi at the proximal extreme of the brachium, and both muscles form a common tendon to insert onto teres intertubercular groove at the level of crests of greater and lesser tubercles, cranial to the origin tendon of the caput mediale of m. triceps brachii (Figs. 3, 5). It is innervated by the axillary nerve, and supplied by the thoracodorsal, subscapular, caudal circumflex humeral, and cranial circumflex humeral arteries (Fig. 6 and Supplementary Fig. 2).

Fig. 5
figure 5

Medial photographic views of the intrinsic shoulder and brachial muscles of the right thoracic limb of a Procyon cancrivorus. a m. tensor fasciae antebrachii pars cranialis was displaced caudally; b m. tensor fasciae antebrachii pars cranialis and pars caudalis were displaced caudally, and the m. biceps brachii cranially; c TFACr, TFACd, LD, CB, and Sb were removed. AM, m. anconeus medialis; B, m. brachialis; BB, m. biceps brachii; CB, m. coracobrachialis; LD, m. latissimus dorsi; Sb, m. subscapularis; SS, m. supraspinatus; TB, m. triceps brachii; TBa, caput accessorium; TBLa, caput laterale; TBLo, caput longum; TBm, caput mediale; TFACr, m. tensor fasciae antebrachii pars cranialis; TFACd, m. tensor fasciae antebrachii pars caudalis; TMaj, m. teres major; TMaj + LDTi, insertion common area of both muscles; TMaj + LDT, common insertion tendon of both muscles. White bars: 10 mm

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Fig. 6
figure 6

Medial photographic views of the arterial and nerve supply to the intrinsic shoulder and brachial muscles in a right thoracic limb of Procyon cancrivorus. a TFACr and TFACd were displaced caudally, and the BB cranially; b the arteries were removed. AA, axillary artery (a. axilaris); AM, m. anconeus medialis; Ax, axillary nerve (n. axillaris); B, m. brachialis; Bc, brachiocephalic nerve; BB, m. biceps brachii; BA, brachial artery (a. brachialis); CB, m. coracobrachialis; LD, m. latissimus dorsi; Mc, musculocutaneous nerve (n. musculocutaneus); Mc’, branch to CB; Mc’’, proximal muscular branch (ramus muscularis proximalis); Mc’’’, distal muscular branch (ramus muscularis proximalis); R, Radial nerve (n. radialis); R’, branches to the TFA and TBLo; Sb, m. subscapularis; SbA, subscapular artery; SBA, superficial brachial artery (a. brachialis superficialis); Sbn, subscapular nerves (nn. subscapularis); SCA, superficial cervical artery (a. cervicalis superficialis); SS, m. supraspinatus; SSn, suprascapular nerve (n. suprascapularis); TB, m. triceps brachii; TBa, caput accessorium; TBLa, caput laterale; TBLo, caput longum; TBm, caput mediale; TCA, transverse cubital artery (a. transversa cubiti); TD, thoracodorsal nerve (n. thoracodorsalis); TFACr, m. tensor fasciae antebrachii pars cranialis; TFACd, m. tensor fasciae antebrachii pars caudalis; LTA, lateral thoracic artery (a. thoracica lateralis); TMaj, m. teres major; U, ulnar nerve (n. ulnaris); UCA, ulnar collateral artery (a. collateralis ulnaris). Black wide arrows: deep brachial artery (a. profunda brachii); White arrows, thoracodorsal artery (a. thoracodorsalis); *, bicipital arteries; **branch to TBm. White bars: 10 mm

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M. subscapularis

The m. subscapularis is multipennate with seven bipennate bellies that originate from the subscapular fossa, the cranial margin of the scapula, the middle third of the caudal margin of scapula (between the origins of the teres major and triceps brachiii caput longum muscles) (Figs. 2, 5), and the dorsal thirds of the intermuscular septa with the supraspinatus and teres major muscles (Supplementary Fig. 1). The origin from the cranial margin of the scapula at the level of the scapular incisure is fibrous equal to the caudal margin. The muscle presented six bellies in one case (PcS5-RTL). It inserts via a thick tendon onto the lesser tubercle of the humerus. In three cases (PcS5-RTL and PcS6-both limbs), it was also inserted onto the joint capsule and via fleshy fibers onto the caudal extreme of lesser tubercle. It is innervated by the subscapular and axillary nerves, and supplied by the subscapular, suprascapular, and deep cervical arteries (Figs. 5, 6; Supplementary Fig. 2). This latter artery supplied it after passing through the m. serratus ventralis cervicis. In one case (PcS6-LTL), it was also supplied by a branch originating directly from the axillary artery.

M. coracobrachialis

The m. coracobrachialis is a bipennate muscle with a reverse arrangement, which originates from the coracoid process via a tendon that passes medial to the subscapular tendon (Figs. 2, 5). Its origin tendon is protected by a synovial sheath that is adhered to the tendon of the m. subscapular. The m. coracobrachialis inserts via fleshy and tendinous fibers onto the caudal surface of the crest of lesser tubercle, just medial to the origin of the caput accessorium of m. triceps brachii (Figs. 3, 5, 6). In two cases (PcS5-RTL and PcS6-LTL), it also inserted via fleshy fibers onto the caput accessorium of m. triceps brachii. It is innervated by the musculocutaneous nerve, and supplied by the cranial circumflex humeral artery. In one specimen (PcS6), it was supplied by the caudal circumflex humeral artery in the left limb, and by a branch directly from the common circumflex humeral artery in the right limb (Supplementary Fig. 2).

Cranial group of the brachium

M. biceps brachii

The m. biceps brachii is bipennate and originates from the supraglenoid tubercle via a tendon (Fig. 2), which passes deeply to the shoulder joint capsule and intertubercular groove, protected by the transverse humeral retinaculum. The muscle inserts via a flat tendon onto the caudolateral surface of the radial tuberosity (Figs. 5, 6, 7). The tendon is protected by a synovial bursa in the medial surface of the radial tuberosity. The muscle belly distal and medially develops the lacertus fibrosus, which inserts onto the antebrachial fascia over the m. pronator teres. The muscle is innervated by the proximal muscular branch of the musculocutaneous nerve, and in three cases it was also innervated by another branch distally of the musculocutaneous nerve (PcS1 both limbs and PcS6-LTL). In PcS1 bilaterally, the muscle had an accessory head (humeral head) that originated from the intertubercular groove, proximal to the insertion of the common tendon of the teres major and latissimus dorsi muscles (Fig. 4c). That belly was innervated by the second branch of the musculocutaneous nerve after passing through the main belly. In PcS5 unilaterally (RTL), the belly was shorter and distally divided into two gross fibrous fascicles, where one extended to the radial tuberosity and the other one joined to the m. brachialis. The more lateral fleshy fibers of the belly were directed toward the lateral fascicle. The medial antebrachial cutaneous nerve and the transverse cubital artery passed to the antebrachium between both fibrous fascicles (Supplementary Fig. 3). The m. biceps brachii is supplied proximally by the cranial circumflex humeral artery, at the medium by two bicipital arteries (both originate directly from the brachial artery), and distally by the transverse cubital and superficial brachial arteries (Fig. 6). In one case (PcS5-RTL), the muscle was not supplied by the latter two arteries because the belly did not reach the distal third of the brachium. In one case (PcS1), one of the bicipital arteries originates from a distal deep brachial artery (Supplementary Fig. 4b). In one case (PcS6-LTL), the muscle was also supplied by other two branches of the brachial artery. One of them also supplied the caput mediale of m. triceps brachii, and the other one the m. tensor fascia antebrachii pars cranialis.

Fig. 7
figure 7

Muscle maps in left radius and ulna of Procyon cancrivorus. lateral (a), medial (b), and proximal (c) views. AL, M. anconeus lateralis; AM, m. anconeus medialis; B, m. brachialis; BB, m. biceps brachii; BTCr, bursa tricipitalis cranialis; BTCd, bursa tricipitalis caudalis; TBa, caput accessorium; TBamLa, common insertion of TBa, TBLa and TBm; TBLa, caput laterale; TBLaLo, common insertion of TBLa and TBLo; TBLo, caput longum; TBLm, caput mediale; TFA, m. tensor fasciae antebrachii; TFA + TBLo, common insertion of TFA and TBLo. White bars: 10 mm

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M. brachialis

The m. brachialis is bipennate, originates mainly via fleshy fibers and also some superficial tendinous fibers from a wide region of the humerus, reaching the caudal and lateral surfaces of the humerus. Its origin area comprises the lateral aspect of the humeral neck, the caudal aspect of the deltoid tuberosity, the lateral aspect of the humeral crest (adjacent to the insertion of the cleidobrachialis tendon), and the three proximal thirds of the medial aspect of the lateral supracondylar crest (Figs. 3, 8). Its belly is adhered by a strong fascia cranially to the elbow joint capsule. It inserts via a flat tendon onto the distal surface to the medial coronoid process of the ulna (Figs. 5, 7). It is innervated by the distal muscular branch of the musculocutaneous nerve, and supplied by the radial collateral and transverse cubital arteries (Fig. 6 and Supplementary Fig. 2). In two cases (PcS2-RTL and PcS5-LTL), it was also innervated by the radial nerve (Supplementary Fig. 2).

Fig. 8
figure 8

Deep photographic views of the brachial muscles of the right thoracic limb of a Procyon cancrivorus. a Lateral view where the caput laterale was disposed caudally; b caudal view after to have disposed laterally the TBLa and TBLo; c proximal view of the tricipital bursas; d caudal view after remove all triceps brachii heads. AL, m. anconeus lateralis; AM, m. anconeus medialis; B, m. brachialis; BB, m. biceps brachii; BTCd, bursa tricipitalis caudalis; BTCr, bursa tricipitalis cranialis; Sb; m. subscapularis; TB, m. triceps brachii; TBa, caput accessorium; TBLa, caput laterale; TBLo, caput longum; TBm, caput mediale. White bars: 10 mm

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Caudal group of the brachium

M. triceps brachii

The m. triceps brachii is multipennate with four heads, such as caput longum, caput laterale, caput mediale and caput accessorium. The caput longum originates via a strong flat tendon from the medial aspect of the ventral third of caudal scapular margin, and a stronger tendon from the infraglenoid tubercle (Figs. 2, 5c). Both tendons internally have fleshy fibers that also originate directly from the scapula. A branch of the subscapular artery passes between both tendons to supply the teres minor and subscapularis muscles (Fig. 4b). The caput longum is supplied by the caudal humeral circumflex, deep brachial, collateral radial, and subscapular arteries (Figs. 4, 6; Supplementary Fig. 2).

The caput laterale originates via an aponeurosis from the brachial fascia, tricipital line and lateral half of the humeral neck. Fleshy fibers were also observed originating from the humeral neck in four specimens bilaterally (PcS1, PcS2, PcS5 and PcS6). Its aponeurosis of origin was proximally fused to the aponeurosis of the m. brachialis bilaterally in two cases (PcS5 and PcS6). The caput laterale sends oblique fleshy fibers to the longum and accessorium heads at the middle of the brachium, and to the caput mediale at the distal third. It is supplied by the radial collateral and caudal humeral circumflex arteries (Fig. 6; Supplementary Fig. 2). It also was supplied by the deep brachial artery in one specimen unilaterally (PcS1-RTL) (Fig. 4b).

The caput accessorium originates mainly via fleshy fibers, extending from the medial half of the humeral neck to a short distance of the humeral shaft where begins the origin of the caput mediale (Figs. 3, 5). Tendinous fibers are observed medially in its origin. It is supplied by the caudal humeral circumflex, deep brachial, and radial collateral arteries. The laterale and accessorium heads were fused in one limb (PcS5-LTL), and there only was a short proximal space for the pass of the radial collateral artery (Supplementary Fig. 2b and 2c). In PcS6, proximal fleshy fibers also originated from the shoulder joint capsule.

The caput mediale originates via an aponeurosis from the proximal quarter of the medial aspect of humeral shaft and sends fibers to the caput accessorium at the distal third of the brachium (Figs. 3, 5, 8). It is supplied by the deep brachial and ulnar collateral arteries (Fig. 6), and a branch directly from the brachial artery. In one limb (PcS6-LTL), this latter branch originated from a common artery to the m. biceps brachii, and distally, it was also supplied by the nutrient humeral artery.

The laterale, accessorium and mediale heads insert through a tendon onto the cranial aspect of the olecranon tuberosity. The laterale and longum heads insert onto the caudal aspect of the olecranon tuberosity. The tendon of the caput laterale also inserts onto the lateral margin of the olecranon, parallel to the insertion of the m. anconeus lateralis. The caput mediale also inserts via fleshy fibers at the medial aspect of the olecranon tuberosity, just proximal to the insertion of the m. anconeus medialis. There are two tricipital synovial bursas between the tendons and the olecranon tuberosity. One is located caudally between the common tendon of the longum and laterale heads, and the common tendon of the laterale, mediale and accessorium heads. Another one is located cranially between the common tendon of the laterale, mediale and accessorium heads, and the m. anconeus lateralis (Figs. 7, 8). All heads are innervated by the radial nerve (Fig. 6).

M. tensor fasciae antebrachii

The m. tensor fasciae antebrachii is divided into two flattened bellies, cranial and caudal parts (pars cranialis and pars caudalis). The cranial part is totally located at the medial aspect of the brachium, parallel and cranial to the caudal part. It originates from a common tendon of several extrinsic thoracic limb muscles (medial belly of the m. latissimus dorsi, caudal part of the m. pectoralis profundus, and cutaneus trunci muscles) via fleshy fibers mainly and its cranial extreme via an aponeurosis. The caudal part is located at the caudal and medial aspects of the caput longum of m. triceps brachii, being always observed from the lateral view of the dissections of the brachium. It originates via fleshy fibers from the main belly of the m. latissimus dorsi, and in some cases via fibrous fibers from the m. teres major (PcS3-RTL, PcS4-RTL, PcS5, PcS6) (Fig. 9). In PcS6, it was extended more cranially and was partially covered by the cranial part in both limbs (Fig. 9c, d). Both parts only join at the distal brachium in a common wide aponeurosis that fuses with the caudal and medial aspect of the triceps brachii caput longum tendon (Fig. 9c, d). It also inserts independently onto the medial margin of the olecranon and antebrachial fascia (Figs. 5, 9). The cranial part was absented in two limbs (PcS2-LTL, and PcS3-RTL) and had a vestigial shape in one limb (PcS3-LTL, Supplementary Fig. 3). Both parts are innervated by the radial nerve (Fig. 6). The caudal part is supplied by the deep brachial and ulnar collateral arteries, and the cranial part by branches of the latter and directly from the brachial artery.

Fig. 9
figure 9

Superficial photographic views of the tensor fasciae antebrachii muscle in Procyon cancrivorus. a Medial view of a left brachium; b caudal view; c medial view of a right brachium. BB, m. biceps brachii; CT, m. cutaneus trunci; LD, m. latissimus dorsi; PS, mm. pectorales superficiales; PPCd, m. pectoralis profundus pars caudalis; TB, m. triceps brachii; TBLa, caput laterale; TBLo, caput longum; TFACr, m. tensor fasciae antebrachii pars cranialis; TFACd, m. tensor fasciae antebrachii pars caudalis; TMaj, m. teres major. White bars: 10 mm

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M. anconeus lateralis (M. anconeus)

The m. anconeus lateralis is pyramidal and originates via fleshy fibers from the distal third of the humeral shaft, caudal aspect of the lateral supracondylar crest, lateral epicondyle of the humerus, and proximal surface to the supracondylar foramen (Figs. 3, 8). It inserts via fleshy and tendinous fibers onto the lateral surface of the olecranon and caudolateral margin of the olecranon (Figs. 7, 8). The muscle deeply fused to the joint capsule of the elbow. It is innervated by the radial nerve, and supplied by the collateral ulnar and collateral radial arteries.

M. anconeus medialis

The m. anconeus medialis is triangular, originates via fleshy fibers from the proximomedial margin of the supracondylar foramen, and via tendinous fibers from the medial epicondyle of the humerus (Fig. 3). It inserts onto the medial surface of the olecranon, proximally via tendinous fibers, and distal- and deeply via fleshy fibers (Figs. 7, 8). It is innervated by the ulnar nerve (Supplementary Fig. 4) and supplied by the collateral ulnar artery (Fig. 6).

Discussion

Comparative anatomy of the intrinsic scapular and shoulder muscles in procyonids

The m. deltoideus of P. cancrivorus had a similar arrangement to that described formerly in the same species (Santos et al. 2010b; Tarquini et al. 2023), and other procyonids, such as Procyon lotor (Allen 1882; Feeney 1999), Nasua nasua (Mackintosh 1875; Santos et al. 2010a; Böhmer et al. 2020; Tarquini et al. 2023), Nasua narica (Mackintosh 1875), Bassaricyon alleni (Beddard 1900), and P. flavus (Beswick-Perrin 1871; Windle and Parsons 1897; Böhmer et al. 2020). However, the pars scapularis always originated from the fascia of the m. infraspinatus, in contrast with the findings of Tarquini et al. (2023) who only found that origin in N. nasua. On the other side, the variant origin of the pars scapularis from a common aponeurosis with the m. teres minor was not reported in any procyonid.

The extended origin cranially to the cranial margin of scapula of the supraspinatus and subscapularis muscles forming an intermuscular septum had been described similarly in the same species (Santos et al. 2010b) and N. nasua (Santos et al. 2010a). The origin between both muscles was not reported in other studies in the same species (Windle 1888; Tarquini et al. 2023), and neither in P. lotor (Allen 1882; Windle and Parsons 1897) and P. flavus (Beswick-Perrin 1871; Windle and Parsons 1897; Böhmer et al. 2020; Vélez-García et al. 2023a). In one specimen of N. nasua, a strong fascia was between both muscles, and in another specimen both muscles shared fibers (Tarquini et al. 2023). The variant presence of two bellies in the m. supraspinatus also was reported in P. cancrivorus (Tarquini et al. 2023), but in that case, the accessory belly was superficial but not located cranially, such as occurred in one P. cancrivorus specimen of the present study and one P. lotor (Allen 1882). The insertion onto the transverse humeral retinaculum was found in none, while Tarquini et al. (2023) found it in their three specimens.

The m. teres minor was completely independent to the m. infraspinatus in P. cancrivorus, such as was formerly described in the same species (Windle 1888; Pereira et al. 2010; Santos et al. 2010b; Tarquini et al. 2023) and other procyonids (Davis 1949; Böhmer et al. 2020; Tarquini et al. 2023; Vélez-García et al. 2023a). In some specimens of P. lotor and P. flavus, this muscle may be fused to the m. infraspinatus (Beswick-Perrin 1871; Allen 1882; Julitz 1909). The origin of the m. teres minor from the infraglenoid tubercle as was reported in P. cancrivorus and N. nasua (Santos et al. 2010a, b) was not found because the tubercle was occupied by the origin tendon of the m. triceps brachii caput longum as recently reported (Tarquini et al. 2023). The origin of the m. infraspinatus from the aponeurosis of origin of the m. teres minor has only been described in P. flavus (Vélez-García et al. 2023a).

Based on the most authors, the m. subscapularis does not have important differences among procyonid species (Beswick-Perrin 1871; Mackintosh 1875; Windle and Parsons 1897; Julitz 1909; Santos et al. 2010a, b; Böhmer et al. 2020). However, it is divided into two portions in Bassariscus (Davis 1949), P. lotor (Davis 1949), N. narica (Davis 1949), and N. nasua (Tarquini et al. 2023). Besides, this muscle does not only originate from the subscapular fossa but from the cranial and caudal margins of the scapula in P. cancrivorus (Tarquini et al. 2023; present study) and N. nasua (Tarquini et al. 2023).

The origin of the m. teres major from the fascia over the m. infraspinatus and intermuscular septum with the m. subscapularis contrasts with other studies that did not find a connection with these muscles in the same species (Santos et al. 2010b; Tarquini et al. 2023). While in P. lotor (Allen 1882; Davis 1949), B. astutus, N. narica (Davis 1949) and N. nasua (Tarquini et al. 2023), the origin is very similar to that found in our P. cancrivorus specimens. The origin from the m. infraspinatus is not found in P. flavus (Windle and Parsons 1897; Julitz 1909; Vélez-García et al. 2023a), and in some specimens of N. nasua (Santos et al. 2010a). Other authors did not report none origin to this muscle in P. cancrivorus (Windle 1888) and Nasua (Mackintosh 1875). On the other side, the insertion onto the humerus was not found to be separated from the m. latissimus dorsi as was previously reported in one P. cancrivorus specimen and represented in the muscle maps by other authors (Tarquini et al. 2023).

The m. coracobrachialis of P. cancrivorus presented a small shape, such as was reported formerly in the same species (Windle 1888; Tarquini et al. 2023), and other procyonids (Mackintosh 1875; Allen 1882; Beddard 1900; Santos et al. 2010a; Tarquini et al. 2023). Potos flavus has another m. coracobrachialis named m. coracobrachialis longus (Beswick-Perrin 1871; Windle and Parsons 1897; Julitz 1909; Vélez-García et al. 2023a), which is absent in P. cancrivorus and other procyonids. However, it can also be absent in some P. flavus specimens (Vélez-García et al. 2023a).

Comparative anatomy of the brachial muscles in procyonids

The m. biceps brachii had one head in most specimens of P. cancrivorus, being similar to that formerly described (Mackintosh 1875; Windle 1888; Pereira et al. 2010; Santos et al. 2010a, b; Tarquini et al. 2023). The other insertion onto the ulnar tuberosity described by some authors (Pereira et al. 2010; Santos et al. 2010a, b) was not found by us and other studies (Windle 1888; Tarquini et al. 2023). In P. flavus, the presence of a well-developed second head (caput breve) originating from the coracoid process of the scapula is a typical condition (Beswick-Perrin 1871; Windle and Parsons 1897; Julitz 1909; Böhmer et al. 2020; Vélez-García et al. 2023a). In P. lotor, that same head may be present in a feeble shape as anatomical variant (Windle and Parsons 1897). However, that head (caput breve) is not the same accessory head found in one P. cancrivorus specimen, since it originated from the humerus. Similarly, a small humeral head was found in one case of P. flavus (Vélez-García et al. 2023a).

The m. brachialis originated from the caudolateral surface of the humerus including the medial aspect of the lateral supracondylar crest in P. cancrivorus, which is similar to that reported previously (Tarquini et al. 2023). In contrast, other studies reported the origin only from the proximal part of the humerus in the same species (Pereira et al. 2010; Santos et al. 2010b) and N. nasua (Santos et al. 2010a; Böhmer et al. 2020). The origin from the whole lateral surface of the humerus was described in N. nasua (Mackintosh 1875; Tarquini et al. 2023), N. narica (Mackintosh 1875), P. lotor (Allen 1882), and P. flavus (Julitz 1909; Vélez-García et al. 2023a). However, the origin has been described from the proximal half of the humerus in the latter species (Beswick-Perrin 1871). The insertion only onto the ulna agrees with that described by most authors in procyonids (Beswick-Perrin 1871; Mackintosh 1875; Allen 1882; Windle 1888; Beddard 1900; Julitz 1909; Böhmer et al. 2020; Tarquini et al. 2023), while the insertion onto the radius described by some authors in P. cancrivorus and N. nasua was not found (Pereira et al. 2010; Santos et al. 2010a, b).

The four heads of the m. triceps brachii in P. cancrivorus were found as was previously reported by other authors (Pereira et al. 2010; Santos et al. 2010b), and similar to B. alleni (Beddard 1900), P. lotor (Allen 1882; Feeney 1999), N. nasua (Santos et al. 2010a), and P. flavus (Julitz 1909; Vélez-García et al. 2023a). Several studies did not describe the caput accessorium of the m. triceps brachii or a homologous portion in procyonids (Beswick-Perrin 1871; Mackintosh 1875; Windle 1888; Böhmer et al. 2020). Former studies only reported three heads in P. cancrivorus (Windle 1888), N. nasua (Mackintosh 1875), and P. flavus (Beswick-Perrin 1871). A more recent study named four heads in N. nasua and P. flavus (Böhmer et al. 2020), although the caput mediale accessorium is actually the m. anconeus medialis (Vélez-García et al. 2023a). In another more recent study was described that the muscle has five heads in P. cancrivorus and N. nasua (Tarquini et al. 2023), although, the caput mediale accessorium is actually the m. anconeus medialis. Procyon lotor and P. flavus may have five heads due to the presence of a second caput laterale (Windle and Parsons 1897; Vélez-García et al. 2023a). Nasua narica may have four heads due to the presence of a second caput longum from the edge of the glenoid cavity (Mackintosh 1875), which could be similar to that found in P. cancrivorus where the caput longum had two origins. In our study, several differences were found concerning to that described to the m. triceps brachii by Tarquini et al. (2023). Among them, we found: two tricipital bursas; the caput laterale originated also via an aponeurosis and sent fleshy fibers to all other heads; the caput laterale fused to the caput accessorium as anatomical variant; and the caput longum tendon was found divided.

The formation of two parts (cranial and caudal parts) in the m. tensor fasciae antebrachii in P. cancrivorus has only been described in P. lotor (Feeney 1999), P. flavus (Vélez-García et al. 2023a) and B. alleni (Beddard 1900). The origin from the m. teres major was only found in N. narica (Mackintosh 1875) and P. flavus (Vélez-García et al. 2023a). The insertion onto the olecranon and antebrachial fascia was reported in P. flavus (Beswick-Perrin 1871; Julitz 1909; Vélez-García et al. 2023a) and one study in P. cancrivorus (Pereira et al. 2010). While the unique insertion onto the olecranon was described in most procyonids (Mackintosh 1875; Allen 1882; Santos et al. 2010a; Böhmer et al. 2020; Tarquini et al. 2023). The tendinous fusion with the caput longum tendon of m. triceps brachii was not reported in any other study.

The m. anconeus medialis in P. cancrivorus had a similar arrangement to that described in a homologous part (with another term or portion of the m. triceps brachii) in the same species ("caput mediale accessorium" Tarquini et al. 2023), N. nasua ("m. triceps brachii caput mediale" Böhmer et al. 2020; Mackintosh 1875), P. lotor ("m. anconeus epitrochlearis" Allen 1882; Windle and Parsons 1897), and P. flavus (Beswick-Perrin 1871; Windle and Parsons 1897; Vélez-García et al. 2023a). We found origin also from the medial epicondyle of the humerus in all P. cancrivorus specimens similar to that found in the same species (Tarquini et al. 2023) and P. flavus (Vélez-García et al. 2023a). In contrast, it differs from that reported in N. nasua where the origin only was from the supracondylar foramen (Tarquini et al. 2023). This muscle or a homologous portion was not described by other authors (Windle 1888; Pereira et al. 2010; Santos et al. 2010b), however, in one of those studies, it was pointed as accessory head of the m. triceps brachii in the Fig. 3 (Santos et al. 2010b). This corroborates that the muscle several times is missed by the authors, which may be because it is not present at the NAV (International Committee on Veterinary Gross Anatomical Nomenclature 2017). In the case of N. narica, both anconei muscles are reported united to the biceps (Mackintosh 1875). However, this union could be a mistake of the author and could have referred to the m. triceps brachii since the anatomical relationship is closer with this muscle than the m. biceps brachii.

The origin of the m. anconeus lateralis (m. anconeus) extended proximally reaching part of the humeral shaft in our specimens of P. cancrivorus, which differed from other studies where the muscle only originates from the lateral supracondylar crest (Mackintosh 1875; Pereira et al. 2010; Santos et al. 2010b; Böhmer et al. 2020; Tarquini et al. 2023). Procyon lotor (Allen 1882) and P. flavus (Vélez-García et al. 2023a) are the only two procyonid species where the muscle reaches the humeral shaft, even being more proximally extended than P. cancrivorus. The muscle was not reported in a former study of P. cancrivorus (Windle 1888). In some specimens of P. flavus, the m. anconeus lateralis may be fused to the caput mediale of the m. triceps brachii (Beswick-Perrin 1871; Julitz 1909).

Anatomical variants of P. cancrivorus present in other carnivorans

Some anatomical variants found in P. cancrivorus may be present in other species within the order Carnivora. The presence of two bellies in the m. supraspinatus has been reported in the canid Cerdocyon thous (Vélez-García et al. 2018b), the felid Panthera leo (Barone 1967), and the viverrid Civettictis civetta (Macalister 1873b). While in the mustelid Galictis cuja, it has three bellies (Ercoli et al. 2015). The origin of the m. infraspinatus from the aponeurosis of the m. teres minor has been described in the ailurid Ailurus fulgens (Fisher et al. 2009).

The m. tensor fasciae antebrachii has only been reported with more than one part in a few species. In some arctoid species, it has been reported with two similar portions to those of P. cancrivorus, such as the mephitids Mephitis mephitis and Spilogale gracilis (Hall 1926), mustelids Eira barbara (Macalister 1873), Martes martes (Yousefi et al. 2018), Pekania penanti (Feeney 1999), and the ursid Ailuropoda melanoleuca (Davis 1964). However, in those mephitids and mustelids, the caudal part originates from the caudal angle of the scapula (Macalister 1873; Hall 1926; Yousefi et al. 2018). In Martes caurina, three parts were reported, two parts originate from the m. latissimus dorsi (“m. epitrochlearis” according to Hall 1926) and another one from the caudal angle of the scapula ("caput anguli of triceps brachii" according to Hall 1926). In the ursid Ursus americanus, it was also reported with three portions and inserted onto the medial epicondyle and olecranon (Shepherd 1883). The insertion onto the triceps brachii tendon by the m. tensor fasciae antebrachii has been reported in the canid Canis lupus familiaris (Hermanson 2020), the mustelid M. martes (Yousefi et al. 2018) and the felid Leopardus pardalis (Julik et al. 2012). The origin from the m. teres major by the m. tensor fascia antebrachii has been reported in U. americanus (Shepherd 1883), M. martes (Yousefi et al. 2018) and the felid Puma concolor (Concha et al. 2004).

From our knowledge, two anatomical variants found in P. cancrivorus have not been reported in other carnivorans, such as the common origin aponeurosis of the teres minor and deltoideus pars scapularis muscles; the two variations of the m. biceps brachii; and the fusion of the laterale and accessorium heads of the m. triceps brachii.

Comparative functional and evolutionary analysis of the intrinsic shoulder and brachial muscles in Procyon cancrivorus based on the topology and innervation

The functional analysis has been excellently developed in the study of Tarquini et al. (2023) since they compared the muscle volume among muscular groups and other species. However, below, we include other functional and evolutionary inferences that were not analyzed in P. cancrivorus (Fig. 10 and Table 2).

Fig. 10
figure 10

Left lateral view of a Procyon cancrivorus specimen with the thoracic limb bones interposed to represent the attachments and functions of the intrinsic shoulder and brachial muscles. Blue, m. triceps brachii muscle; Fluorescent green, m. teres minor; Dark green, m. anconeus lateralis; Green, m. teres major; Gray dashed line, m. anconeus medialis; Orange, m. deltoideus; Orange dashed line, m. subscapularis; Pink, m. tensor fasciae antebrachii; Red, m. supraspinatus; Sky blue, m. coracobrachialis; Yellow, m. infraspinatus; white, m. biceps brachii; purple, m. brachialis. The dashed lines also represent that the muscle is medial to the anatomical structure. The green and blue curve arrows indicate the flexor and extensor surfaces in the shoulder and elbow regions, respectively. The bones do not correspond to the specimen of the photo and are located in a tentative anatomical position. They were only interposed to schematize the attachments and functions of the muscles

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Table 2 Anatomical characteristics of the intrinsic shoulder and brachial muscles in Procyon cancrivorus
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The m. deltoideus in procyonids is mainly divided into two parts, however, based on the topology of the m. cleidobrachialis and the distribution of the axillary nerve (Enciso-García and Vélez-García 2022; Vélez-García et al. 2023b), this latter muscle corresponds to the third part of the m. deltoideus, named pars clavicularis (Vélez-García and Miglino 2023). Evolutionarily, it was a part joined to the pars acromialis from the reptiles to the last common ancestor of mammals ("deltoideus acromialis et clavicularis" Diogo et al. 2016). In carnivorans, both parts should have been separated due to the involution of the clavicle and its functional antagonism. This is because the acromialis and scapularis parts act together to flex and abduct the shoulder, and the pars clavicularis act to extend the shoulder together the m. cleidocephalicus (Diogo et al. 2012; Hermanson 2020; Vélez-García and Miglino 2023; Vélez‐García et al. 2023c). The origin in common of the deltoideus pars scapularis and teres minor muscles in one limb of P. cancrivorus could be associated with the evolutionary derivation of the m. teres minor from the m. deltoideus in tetrapods (Diogo et al. 2018, 2019). Formerly, the m. teres minor was considered to be derived from the m. infraspinatus because several former authors had found it fused to it in several mammals (Diogo and Abdala 2010). For example, among carnivorans, this fusion had been reported in P. flavus (Beswick-Perrin 1871; Windle and Parsons 1897; Julitz 1909), Aonyx sp. (Macalister 1870), Enhydra lutris (Howard 1973), Mephitis mephitis (Hall 1926), and Ursus americanus (Shepherd 1883). However, recent studies proposed its evolutionary derivation from the m. deltoideus based on its presence in monotremes and innervation by the axillary nerve (Gambaryan et al. 2015; Diogo et al. 2018). This could also be supported within carnivorans because recently in a study in Lontra longicaudis, the m. infraspinatus was being innervated by the axillary nerve when the m. teres minor was fused to it (Ramírez Arango et al. 2024). Besides, an embryological study in humans confirmed that the m. teres minor is derived from the m. deltoideus at the seventh gestational week (Diogo et al. 2019). Therefore, the presentation of a common origin of the deltoideus pars scapularis and teres minor muscles occurred in a P. cancrivorus specimen is a phylogenetic trade associated with the muscular derivation of the shoulder flexor muscles in mammals (Figs. 11, 12).

Fig. 11
figure 11

Hypotheses regarding the evolution and homologies of the supraspinatus, infraspinatus, deltoideus, teres minor, brachialis, coracobrachialis, and biceps brachii muscles in procyonids based on the literature review and the results of the present study. *Based on Diogo et al. (2018), **Based on Gambaryan et al. (2015), ***Based on Richards et al. (2023), ***Based on Vélez-García et al. (2023a, b, c). The black arrows indicate the hypotheses of the muscle evolutionary derivation based on Diogo et al. (2018). The grey dash arrows indicate alternate hypotheses based on Diogo et al. (2018). The red arrows indicate the hypotheses based on the present study. LCA, Last common ancestor; mars, Marsupialia; plac, Placentalia

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Fig. 12
figure 12

Some of the major features of the intrinsic shoulder and brachial muscles from the order Carnivora to family Procyonidae based on literature review and the present study. The phylogenetic tree was based on Nyakatura et al. (2012)

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The shoulder joint is extended and stabilized by the supraspinatus and subscapularis muscles (Hermanson 2020). Besides, the presence of an intermuscular septum between the supraspinatus and subscapularis muscles in P. cancrivorus could be related to greater strength to extend and stabilize the shoulder since the bands of both muscles are disposed cranially to the scapula, such as was found in cursorial species as canids (Feeney 1999; Vélez-García et al. 2018b; Hermanson 2020). Even this arrangement supports the results of Tarquini et al. (2023) who found similar mean mass values in the intrinsic shoulder muscles between P. cancrivorus and C. lupus familiaris. Other muscles that support the extension and stabilization of the shoulder are the infraspinatus and biceps brachii muscles since their tendons cross lateral- and cranially the shoulder joint capsule, respectively. The stabilization is mainly performed when the limb is supporting the substrate (Hermanson 2020).

The teres major, teres minor, subscapularis, and triceps brachii caput longum muscles are shoulder flexors (Hermanson 2020). We can infer that they are powered by the m. tensor fasciae antebrachii pars caudalis due to its caudal arrangement together with the m. triceps brachii caput longum in P. cancrivorus. The same muscle support should occur in other carnivorans where the m. tensor fasciae antebrachii has a caudal arrangement, such as other procyonids (Beswick-Perrin 1871; Julitz 1909; Böhmer et al. 2020; Vélez-García et al. 2023a), mephitids (Hall 1926), most mustelids (Macalister 1873; Hall 1926; Cohen and Hart 1968; Howard 1973; Leach 1977; Ercoli et al. 2015; Böhmer et al. 2018, 2020; Yousefi et al. 2018; Ramírez Arango et al. 2024), ursids (Shepherd 1883; Davis 1964), and some felids (Concha et al. 2004; Vargas et al. 2017). Rotational movements of the humerus are essential in P. cancrivorus because these movements would allow better handling abilities to manipulate the food or when individuals are searching for food in dark areas. Therefore, the teres major and infraspinatus muscles should act as medial and lateral rotators of the humerus, respectively (Hermanson 2020).

The m. coracobrachialis is an adductor and extensor of the shoulder (Hermanson et al. 2020). The presence of only one m. coracobrachialis (m. coracobrachialis brevis) in P. cancrivorus agrees with the other phylogenetically close procyonids, while differs from P. flavus which conserves two coracobrachialis muscles (m. coracobrachialis brevis and m. coracobrachialis longus) (Vélez-García et al. 2023a). The presence of two coracobrachialis muscles is a character present in a few species of the suborders Caniformia and Feliformia (Tarquini et al. 2023). Among non-procyonid caniforms, both coracobrachialis muscles are present in mustelids of the genera Martes, Pekania and Eira (Macalister 1873; Mackintosh 1875; Leach 1977; Yousefi et al. 2018), the ailurid Ailurus fulgens (Carlsson 1925; Fisher et al. 2009), and ursids (Shepherd 1883; Kelley 1888; Windle and Parsons 1897; Davis 1964; Annie et al. 2019). Among feliforms, they are present in the euplerid Cryptoprocta ferox (Carlsson 1925; Böhmer et al. 2020), viverrids of the genus Genetta (Taylor 1974), and occasionally in Felis catus (Barone 2020b). The presence of two coracobrachialis muscles is phylogenetically related to the amphibians (Diogo et al. 2018), and that arrangement persists in reptiles, monotremes, some marsupials, and some eutherians (Gambaryan et al. 2015; Diogo et al. 2018; Richards et al. 2023). In mammal species from the phylogenetic line in which the family Carnivora diverged, such as some ruminants (cetartiodactyla) and perissodactyls (Nyakatura and Bininda-Emonds 2012), both coracobrachialis muscles may be present (Budras et al. 2009; Budras and Habel 2011; Barone 2020b). Posteriorly, as the species diverged, the m. coracobrachialis longus disappeared in the most carnivorans, or even it disappeared together the m. coracobrachialis brevis, such as occurred in mephitids (Hall 1926) and mustelids of the subfamily Lutrinae (Haughton 1864; Windle and Parsons 1897; Cohen and Hart 1968; Howard 1973; Ramírez Arango et al. 2024) (Fig. 12). Therefore, both coracobrachialis brevis and coracobrachialis longus muscles could potentially be present in the last common ancestor of carnivorans, remaining in a few extant species (Fig. 12).

The elbow flexion is mainly performed by the biceps brachii and brachialis muscles, besides during flexion, they are supported by the brachioradialis and extensor carpi radialis muscles (Hermanson 2020; Vélez-García et al. 2022a, b). On the other hand, the adhesion of the m. brachialis to the elbow joint capsule should retract cranially the capsule when the elbow is flexing. We infer that due to when we detached the muscle and flexed the specimen elbow, the radial head and medial coronoid process of the ulna pinched the capsule. From our knowledge, the anatomical variants as the union between the brachialis and biceps brachii muscles, and the presence of a humeral head have not been reported in other carnivorans different to P. flavus. In some mammals distant phylogenetically to carnivorans, the former is normally present in some xenarthrans (Taylor 1978; Torres Suárez et al. 2024), and the latter has also been described as an anatomical variant in some primates (Monroy‐Cendales et al. 2020). Therefore, both variants could be related to another evolutionary hypothesis where the m. biceps brachii was also derived together with the m. brachialis from the m. humeroantebrachialis of amphibians (Diogo et al. 2018). The presence of a second head in the m. biceps brachii should potentiate the elbow flexion intraspecifically in P. cancrivorus due to an origin more distal since it originated from the humerus. In other carnivorans with caput breve, the elbow flexion should increase the flexion velocity of the elbow since it has a more proximal origin (scapula), such as occurs in P. flavus (Böhmer et al. 2020; Vélez-García et al. 2023a), A. fulgens (Fisher et al. 2009), and some ursids (Shepherd 1883; Kelley 1888; Davis 1964). The presence of a vestigial caput breve of m. biceps brachii in a P. lotor specimen (Windle and Parsons 1897) could support the hypothesis that the common ancestor of procyonids potentially had it and conserved it from the common ancestor of arctoids (Ercoli et al. 2015). The caput breve could have disappeared within the family Procyonidae when the non-Potos genera diverged from the genus Potos (Figs. 11, 12). Previously, the presence of several bicipital arteries had been associated with a higher activity of the m. biceps brachii in P. flavus (Vélez-García et al. 2023a). However, after reviewing the arterial supply to the m. biceps brachii in P. cancrivorus, the presence of several bicipital arteries from the brachial artery could be a characteristic within procyonids, which differs from C. thous (Vélez et al. 2018), C. lupus familiaris (Hermanson et al. 2020), A. melanoleuca (Davis 1964) and F. catus (International Committee on Veterinary Gross Anatomical Nomenclature 2017; Barone 2021). In C. lupus familiaris, two bicipital arteries may only be formed occasionally, one originates from the brachial artery and the other from the superficial brachial artery (Hermanson et al. 2020; Barone 2021). This latter origin is the unique present in F. catus (International Committee on Veterinary Gross Anatomical Nomenclature 2017; Barone 2021). On the other hand, the cranial and caudal circumflex humeral arteries originated from a common trunk in P. cancrivorus, which is not reported in any of the mentioned species.

The elbow extension in P. cancrivorus is powered by a m. triceps brachii with four heads, two anconeal muscles, and the two parts of the m. tensor fasciae antebrachii. Tarquini et al. (2023) for P. cancrivorus reported the cranial part of the m. tensor fascia antebrachii as a “caudal belly” to this, which originated from the m. cutaneous trunci and was also considered as part of this latter. However, these authors did not take into account the innervation and the direction of the muscle fibers to this belly, which should be reviewed to infer muscle derivation in vertebrates (Diogo and Abdala 2010). Therefore, based on the radial nerve distribution where the branch to the caudal part branched also to the cranial part, and the direction of the fibers is parallel, said belly is actually a part of the m. tensor fasciae antebrachii (Fig. 6). Furthermore, the insertion aponeurosis is also fused to the tendon of the m. triceps brachii caput longum (Fig. 7), which is not reported in other studies of the same species and other procyonids. Thus, the synapomorphy of several origins in arctoids for the m. tensor fasciae antebrachii is also retained in P. cancrivorus. Previous studies in caniforms have determined that canids only conserve the cranial part of the m. tensor fasciae antebrachii while arctoids the caudal part (Feeney 1999; Vélez-García et al. 2023a). In contrast, based on the origin of the m. tensor fasciae antebrachii only from the m. latissimus dorsi in canids (Feeney 1999; Pereira et al. 2016; Souza-Junior et al. 2018; Vélez et al. 2018; Böhmer et al. 2020; Smith et al. 2020), actually the part more conserved in caniforms is the caudal part while the presentation of the cranial part is variable in arctoids. What happens is that the m. tensor fasciae antebrachii is so developed in arctoids that it extends caudally to the caput longum of the triceps brachii, and is observed in the lateral views of the figures of several studies (Hall 1926; Davis 1964; Fisher et al. 2009; Moore et al. 2013; Ercoli et al. 2015; Böhmer et al. 2020; Tarquini et al. 2023; Vélez-García et al. 2023a; Ramírez Arango et al. 2024). Besides, based on its topology and innervation, we could infer that this muscle is derived from the caput longum of the m. triceps brachii in carnivorans, which agrees with the evolutionary derivation from the last common ancestor of mammals (Diogo et al. 2018). The presence of a caput accessorium in the m. triceps brachii has been found in monotremes, and it has been inferred that it is a division of the caput mediale caused by the pass of the radial nerve (Gambaryan et al. 2015), which also occurs in carnivorans. On the other hand, the fusion presented by the laterale and accessorium heads in one P. cancrivorus specimen, and the distribution of the radial nerve to these heads, allow us to suggest that the caput accessorium could also be evolutionarily derived from the caput laterale in procyonids (Fig. 13).

Fig. 13
figure 13

Hypotheses regarding the evolution and homologies of the subscapularis, teres major, triceps brachii, tensor fasciae antebrachii, and anconeus medialis (epitrochleoanconeus) muscles in procyonids based on the literature review and the results of the present study. *Based on Diogo et al. (2018), **Based on Gambaryan et al. (2015), ***Based on Richards et al. (2023), *** Based on Vélez-García et al. (2023a, b, c). The black arrows indicate the hypotheses of the muscle evolutionary derivation based on Diogo et al. (2018). The grey dash arrows indicate alternate hypotheses based on Diogo et al. (2018). The blue arrow indicate hypothesis based on Gambaryan et al. (2015). The red arrows indicate the hypotheses based on the present study. LCA, Last common ancestor; mars, Marsupialia; plac, Placentalia

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Based on the former dissections performed by Windle and Parsons (1897) in several carnivorans, the m. anconeus medialis is the most constant and is supplied by the ulnar nerve. This has been corroborated more recently in procyonids (Enciso-García and Vélez-García 2022; Vélez-García et al. 2023b), the mustelid L. longicaudis (Ramírez Arango et al. 2024), and felids (Barone 2020a; Barreto‐Mejía et al. 2022). In contrast, this muscle normally is not present in canids (Pereira et al. 2016; Souza-Junior et al. 2018; Vélez et al. 2018; Hermanson 2020; Smith et al. 2020) and ursids (Shepherd 1883; Davis 1964). If it is present in those species, it has a vestigial shape (Kelley 1888; Vélez-García et al. 2018a; Böhmer et al. 2020) or is fused to the caput mediale of the m. triceps brachii as was reported in the ursid Ailuropoda melanoleuca (Davis 1964). Therefore, the m. anconeus medialis lost functionality in the families Canidae and Ursidae. Several myological studies have named this muscle as another head of the m. triceps brachii in species of the order Carnivora, such as those studies performed in caniforms (Shepherd 1883; Leach 1977; Fisher et al. 2009; Ercoli et al. 2015; Böhmer et al. 2020; Tarquini et al. 2023) and feliforms (Julik et al. 2012; Viranta et al. 2016; Böhmer et al. 2020; Smith et al. 2021; Dunn et al. 2022). However, due to its topology and innervation by the ulnar nerve, the m. anconeus medialis in the order Carnivora retains its evolutionary derivation together the m. flexor carpi ulnaris in the caudolateral muscular complex of the antebrachium (Figs. 12, 13). This is due to the muscle is present in chordates from the amphibians, and it is not derivate from the m. triceps brachii (Diogo and Abdala 2010; Diogo et al. 2018; Molnar and Diogo 2021). In carnivorans, the presence of the m. anconeus medialis is not only a phylogenetical relationship but it could be correlated functionally with the presence of supracondylar foramen because this structure could have generated the need of medial muscular support at the elbow. Thus, the m. anconeus medialis should also act as a medial stabilizer of the elbow joint.

The elbow extensor muscles are supplied by the caudal circumflex, deep brachial, collateral radial, and collateral ulnar arteries in P. cancrivorus, similar to that described in P. flavus (Vélez-García et al. 2023a), A. melanoleuca (Davis 1964), C. thous (Vélez et al. 2018), C. lupus familiaris (Hermanson et al. 2020; Barone 2021) and F. catus (Barone 2021). The caudal circumflex humeral artery is considered the main arterial supply to the heads of the m. triceps brachii, from which is formed the collateral radial artery (Hermanson et al. 2020; Barone 2021). However, the origin and distribution of this later artery vary among carnivorans. It originates medially to the m. teres major from the caudal circumflex humeral artery and is directed distolaterally between the caput mediale and caput accessorium of the m. triceps brachii in C. lupus familiaris (Hermanson et al. 2020). It originates laterally to the m. teres major and is directed distally between the caput accessorium and caput laterale of the m. triceps brachii in P. flavus (Vélez-García et al. 2023a) and P. cancrivorus (Fig. 4 and Supplementary Fig. 3). Both distributions can occur in C. thous, however, it originates from the cranial circumflex humeral artery in the former distribution (Vélez et al. 2018). In F. catus, it presents commonly the latter distribution, and in some cases may originate directly from the axillary artery (Barone 2021). Two deep brachial arteries were formed unilaterally in one specimen of P. cancrivorus (PcS1-RTL), which may occur occasionally in C. lupus familiaris (Hermanson et al. 2020; Barone 2021). On the other hand, the deep brachial artery originated from the thoracodorsal artery bilaterally in one P. cancrivorus specimen (PcS6), which was not described in any of the species previously mentioned. Therefore, the arterial supply in carnivorans varies intra- and interspecifically, and requires more studies with a higher sample of specimens and species to find vascular phylogenetic relationships.

In conclusion, the most intrinsic shoulder and brachial muscles of P. cancrivorus potentially conserve the evolutionary derivation of the last common ancestor of mammals based on the topology, innervation, and anatomical variants. However, the division of the m. tensor fasciae antebrachii into two parts is a characteristic that appears within the infraorder Arctoidea and remains in most cases in P. cancrivorus.