Anatomy and Histology of the Fibrocartilago humerocapsularis in Some Species of European Wild Birds

Authors

  • Marco Canova,

    Corresponding author
    1. Department of Veterinary Medical Science, University of Bologna – Via Tolara di Sopra 50, Italy
    2. University Museum System, University of Bologna – Via Zamboni 33, Bologna, Italy
    • Correspondence to: Marco Canova; Department of Veterinary Medical Science, University of Bologna - Via Tolara di Sopra 50, 40046, Ozzano dell'Emilia (BO) Italy. Fax: +3951-2097953. E-mail: marco.canova4@unibo.it

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  • Cristiano Bombardi,

    1. Department of Veterinary Medical Science, University of Bologna – Via Tolara di Sopra 50, Italy
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  • Nadia De Sordi,

    1. Department of Veterinary Medical Science, University of Bologna – Via Tolara di Sopra 50, Italy
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  • Paolo Clavenzani,

    1. Department of Veterinary Medical Science, University of Bologna – Via Tolara di Sopra 50, Italy
    2. University Museum System, University of Bologna – Via Zamboni 33, Bologna, Italy
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  • Annamaria Grandis

    1. Department of Veterinary Medical Science, University of Bologna – Via Tolara di Sopra 50, Italy
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ABSTRACT

The occurrence and structure of the fibrocartilago humerocapsularis (FHC) in the shoulders of 72 subjects of various species of wild birds were evaluated by gross dissection and histological examination with the purpose of increasing the body of knowledge regarding this structure and verifying the functional hypotheses submitted in the past in other species. The results showed that the FHC has a conical shape with a narrow cavity on the inside. The structure is heterogeneous in the various species and consists of different tissues, such as hyaline cartilage, fibrous cartilage, and bone. From the data obtained in this study, there does not appear to be any correlation between ossification and the weight of the prey lifted, wing shape, and aging. This study also provided interesting preliminary data regarding the ossification of the FHC. In fact, in the Hooded Crow (Corvus cornix), the ossification seemed to be correlated with the mechanical stimulation of flying. Additional studies are necessary to confirm this hypothesis. Anat Rec, 297:1189–1194, 2014. © 2014 Wiley Periodicals, Inc.

Abbreviations used
FHC

fibrocartilago humerocapsularis

HSB

humeroscapular bone

INTRODUCTION

The fibrocartilago humerocapsularis (FHC), also known as the “humeroscapular bone” (HSB), is a structure present in the shoulder of some species of birds (Baumel et al., 1993). If present, it is developed in the dorsal part of the articular capsule of the shoulder joint, and lies on the deep surface of the pars major deltoid muscle (Hudson and Lanzillotti, 1955; George and Berger, 1966; Meyers, 1992; Smith and Smith, 1992; Baumel et al., 1993; Vanden Berge and Storer, 1995).

The FHC is roughly triangular in shape with the long axis oriented at a right angle to the long axis of the wing. The base of the FHC is covered with cartilage and forms the articular surface of the structure that is in contact with the humerus. It lies on the deep surface of the pars major of the deltoid muscle adjacent to the humeral articular face of the scapula. The tendon of the m. supracoracoideus runs immediately cranial to the cranial margin of the “humeroscapular bone”. The structure is intimately associated with both the pars major of the deltoid muscle and the shoulder joint capsule. Two well-developed ligaments attach the FHC to the humerus. The more cranial of these ligaments attaches the cranial edge of the FHC over the convex surface of the humeral head and terminates at the proximal edge of the pectoral crest of the humerus. The caudal ligament attaches the caudal aspect of the FHC to the ventral tubercle of the humerus, near the pneumatic foramen and just distal to the attachment of the coracobrachialis muscle to the humerus (Smith and Smith, 1992).

In the past, few authors have investigated the FHC in different birds with the aim of identifying which species possess it, trying to correlate the presence of the FHC with a specific function. In particular, Smith and Smith (1992) showed some Raptors with a bony FHC and others without it; the latter group included species which possessed a fibrocartilaginous FHC. The same authors, suggesting a possible role of the sesamoid bone, hypothesized that the determining factors related to the development of an osseous structure could be correlated to the magnitude of friction or wear imparted to the deltoid muscle during its passage over the humeral head. They also hypothesized a correlation between the presence of a bony FHC and the weight of the prey lifted or the wing shape. Despite the attempts of authors to study this structure in the largest number of animals possible, many species have yet to be examined.

Therefore, the goal of this study was to determine the presence, shape and histological characteristics of the FHC in European species of birds in order to provide useful data for a functional interpretation of this structure.

MATERIALS AND METHODS

Seventy-two specimens from deceased subjects were obtained from Italy in 2010 provided by the Museum of the ex-National Institute for Wildlife (ex-INFS) of the Institute for Environmental Protection and Research (ISPRA), and by the Italian League for Bird Protection (LIPU) Rehabilitation Center of Bologna. The subjects were stored at −20°C and thawed at room temperature before use. Animals of different ages, sex, functional characteristics, biometrical and morphological aspects as well as different flying abilities and wing aspect ratios were chosen. The species and number of subjects are summarized in Table 1.

Table 1. The presence and structure of the fibrocartilago humerocapsularis with correlated wing type in 13 species of wild birds
Species examinedNumber of subjectPresenceHistological aspectaWing typeb
  1. a

    FC, fibrocartilage; HC, hyaline cartilage; B, bone.

  2. b

    Cramp et al. (2004).

  3. c

    With the only exception of one subject of Athene noctua, of Corvus cornix, and of Nycticorax nycticorax, all the animals were full-grown.

Accipiter nisus11 (5 ♂; 6 ♀)+FCShort and rounded
Athene noctuac9 (5 ♂; 4 ♀)+FC (Ad)Rather short and broad, tip rounded
FC (Juv)
Buteo buteo5 (3 ♂; 2 ♀)+Broad and rounded
Corvus cornixc3 (2 ♂; 1 ♀)+B (Ad)Rather short, broad at base, tip bluntly pointed
HC (Juv)
Dendrocopos major3 (2 ♂; 1 ♀)+BRather short, broad at base, tip rounded
Falco tinnunculus9 (4 ♂; 5 ♀)+FCLong and pointed
Falco vespertinus4 (2 ♂; 2 ♀)+BLong and pointed
Pernis apivorus1 (♂)+Long and relatively narrow
Apus apus10 (5 ♂; 5 ♀) Long and narrow, tapering gradually to sharp tip
Ardea cinerea3 (2 ♂; 1 ♀) Long and broad
Columba livia10 (4 ♂; 6 ♀) Rather long, pointed; relatively broad at base
Nycticorax nycticoraxc1 (♂) Broad and rounded
Puffinus yelkouan3 (1 ♂; 2 ♀) Long and narrow

Each subject was bilaterally dissected at the level of the shoulder, performing a progressive exposition of tissue until the joint was reached (Fig. 1). The dorsal approach was preferred. Dissection of the skin in the shoulder joint region made visualization of the deltoideus pars propatagialis muscle and the pars major possible, showing different development in the various species. The muscle was then excised, leading to direct visualization of the FHC. Using a scalpel, the ligaments and the joint capsule were cut off and the FHC was sampled in two different ways.

Figure 1.

A stepwise dissection of the shoulder joint region of a Hooded Crow was performed starting from the skin up to the level of the Fibrocartilago humerocapsularis (FHC). (a) The skin was dissected and detached from the muscular plane; (b) the deltoideus pars propatagialis muscle (asterisk) was isolated; (c) the deltoideus pars major muscle (triangle) was incised longitudinally; (d) the pars major was reflected cranially exposing the FHC (arrow); (e) higher magnification of the FHC (arrow).

The first sample was fixed, demineralized, dehydrated, paraffin-embedded, and serially cut at 12.5 µm. A group of 8–10 sections was alternatively stained with Hematoxylin-Eosin and Masson's trichrome stains.

The second sample was subjected to enzymatic maceration to obtain a clean bone. The specimens were then placed on graph paper and photographed perpendicularly using a digital camera. They were subsequently measured as to their maximum extensions on horizontal and vertical axes using Adobe Photoshop CS4 Extended® (Adobe System Incorporated) (Fig. 2).

Figure 2.

Fibrocartilago humerocapsularis of the Common Buzzard (a–c) and the Great Spotted Woodpecker (d). Three different views are shown: lateral view (a), dorsal view (b), and ventral view (c). In the latter, the articular surface is visible. (d) Shows the projection of the greatest height of the structure on the vertical axis. Square: 1 mm2; Bar 2 mm.

All the photographs used in this study were taken using a digital camera and were processed with Adobe Photoshop CS4 Extended® (Adobe System Incorporated).

RESULTS

Gross dissection showed a different conformation of the structures. The results of the presence or absence of the FHC in the various species are summarized in Table 1. Although having the general shape of a truncated cone, the FHC can be shaped differently in terms of dimension and silhouette, showing a slender profile, as in the case of the Hooded Crow (Corvus cornix) and the Great Spotted Woodpecker (Dendrocopus major), rather than round, as in specimens of the Common Buzzard (Buteo buteo). In the Sparrow Hawk (Accipiter nisus), the FHC has a general shape comparable to a truncated cone. Histological examination provided a heterogeneous pattern; at the level of the base and periphery of the FHC, it was possible to see some cartilage lacunae mixed with collagenous fibers disposed parallel or radially to the surface whereas the tissue surrounding the cavity was composed of bone. Regarding different patterns related to age, there seemed to be no relevant differences between the subjects at 1 year of age and older animals. Gross dissection of the Little Owl (Athene noctua) showed that, in this species, the FHC was present (even in the nestling) and had a much rounder shape as compared to the Sparrow Hawk (Accipiter nisus). Histological examination showed that the base was quite developed and the major cavity was situated near the apex (Fig. 3a). The cartilaginous cells, single or arranged in small groups, appeared to be surrounded by a capsule which was deep blue when stained with Masson's trichrome stain. In spite of the typical blue color of the fibrous cartilage which had been stained with Masson's trichrome stain, it was possible to see profuse bundles of irregularly disposed fibres embedded in an abundant red-stained amorphous ground substance (Fig. 4b). In the Common Buzzard (Buteo buteo), the FHC appeared round in shape (Fig. 2a–c). Unfortunately, in this species, it was not possible to evaluate the samples for histological examination due to their deterioration during the staining procedures. In the Hooded Crow (Corvus cornix), the FHC appeared thinner vertically than that seen in the Sparrow Hawk (Accipiter nisus), with a concave aspect laterally. Macroscopically, it was possible to see a central red zone. It corresponded to the narrow cavity extending from the base (just above the articular surface) to the apex of the structure. The histological examination carried out on two adult subjects of this species suggested an FHC composed of bone rich in an amorphous ground substance (Fig. 3d). The examination of a juvenile subject of this species, unable to fly freely, provided an interesting tissue pattern. It was characterized by a large population of chondrocytes located in broad lacunae, some of which constituted characteristic isogen groups, suggesting tissue composed of hyaline cartilage (Figs. 4c and 3c). The Great Spotted Woodpecker (Dendrocopos major) had an FHC with an atypical shape. The measurements showed that it was thinner at the level of the apex of the body, with a very large base as compared to the others. The body also presented a non-linear course vertically. These features gave it the general shape of a reversed and oblique T. In spite of the oblique course of the FHC in this species, we measured it, projecting the largest height of the structure onto the vertical axis (Fig. 2d). In this way, it was possible to compare these data with the measurements obtained from the species. Histological examination showed an FHC composed of bone rich in an amorphous ground substance, except for the articular surface which was made up of fibrocartilage (Fig. 3b). In the Common Kestrel (Falco tinnunculus) we found only one large narrow cavity ventrodorsally located at the center of the FHC which, in this species, was composed of fibrocartilage (Figs. 3e and 4a). The composition of the FHC did not differ substantially in relationship to the age of the subject. In the Red-footed Falcon (Falco vespertinus), the FHC was slightly thinner as compared to the Sparrow Hawk (Accipiter nisus). Histological examination revealed an FHC composed of bone rich in an amorphous ground substance (Figs. 3f and 4d). Unfortunately, during the histological examination, the FHC of the only Honey Buzzard (Pernis apivorus) found for this study deteriorated and it could not be examined further. The data regarding the size of the structure (if present) are summarized in Table 2. Finally, the FHC was not found in: the Grey Heron, Pigeon, Hooded Crow, Black-crowned Night Heron, Mediterranean Shearwater and the Common Swift.

Figure 3.

Histological examination showing that, in the Little Owl (a) the Fibrocartilago humerocapsularis is composed of fibrocartilage with the narrow cavity located near the apex whereas. In the Great Spotted Woodpecker (b), it is mainly composed of bone except at the base. Note the different histological aspects of the FHC composed of hyaline cartilage (c) in a juvenile, or bone (d) in a 1-year-old subject. The Common Kestrel shows a fibrocartilaginous structure (e) while the Red-footed Falcon possesses a bony FHC (f). Masson's trichrome stain. Bar: 0.5 mm.

Figure 4.

The Fibrocartilago humerocapsularis can have various compositions: fibrocartilage (a, the Common Kestrel), fibrocartilage embedded in an abundant red-stained amorphous ground substance (arrows) (b, the Little Owl), hyaline cartilage (c, the Hooded Crow), and bone (d, the Red-footed Falcon). In (b) and (c), the arrowheads indicate isogen groups of the cartilage. Masson's trichrome stain. Bar: 100 μm.

Table 2. Measurements carried out on the axis of the Fibrocartilago humerocapsularis in the species where it has been found
Species examinedVertical (mm)Horizontal (mm)
  1. a

    The vertical axis of the Dendrocopos major was obtained by projection because it was not perpendicular to the horizontal one.

Accipiter nisus2.5 ± 0.162.3 ± 0.16
Athene noctua2.3 ± 0.152.5 ± 0.16
Buteo buteo3.7 ± 0.203.7 ± 0.21
Corvus cornix4.8 ± 0.224.0 ± 0.20
Dendrocopos major3.4 ± 0.19a3.6 ± 0.19
Falco tinnunculus3.6 ± 0.202.7 ± 0.17
Falco vespertinus2.9 ± 0.172.3 ± 0.15
Pernis apivorus4.43.8

DISCUSSION

The present study proved the presence of the FHC in species (Table 1) which had not previously been described by other authors (George and Berger, 1966; Meyers, 1992; Smith and Smith, 1992; Baumel et al., 1993; Vanden Berge and Storer, 1995).

The FHC appeared, generally, as a truncated cone, showing different sizes and silhouettes throughout the species, with widths and heights ranging from 3.2 to 4.0 mm and 3.2 to 4.8 mm, respectively (Table 2).

Regarding the histological appearance, the FHC was heterogeneous in the various species and consisted of different tissues, such as hyaline cartilage, fibrous cartilage and bone, sometimes coexisting in the same structure (Figs. 4a–d). Interestingly, in some species which possessed fibrous (Accipiter nisus, Athene noctua) or bony (Corvus cornix, Dendrocopos major and Falco vespertinus) FHC, the amorphous ground substance was plentiful. Since the matrix allowed the tissue to maintain good hydration, from a functional point of view, it would allow the FHC to better resist the mechanical stress which occurs during the flight.

Smith and Smith (1992) argued that this structure was composed of bone in some species. On the basis of their results, they classified the birds into two groups: those which possessed an osseous structure (HSB) and those which did not possess it or had it composed of fibrocartilage (FHC). Baumel et al. (1993), and Vanden Berge and Storer (1995), however, considered the terms FHC and HSB as synonymous, describing this structure as a fibrocartilaginous or osseous mass developed within the ligaments of the shoulder joint. In our opinion, the animals should be distinguished, first of all, on the basis of the presence or absence of this structure and, secondarily, on the histological aspect. However, the presence of a fibrocartilaginous mass should not be interpreted merely as an absent structure.

Smith and Smith (1992) tried to find some functional interpretation regarding the presence/absence and histological appearance of the FHC. They proposed a correlation between a bony FHC and the wing shape. These authors argued that animals with long and tapered wings did not possess a FHC or had one composed of fibrous cartilage while subjects with short and rounded wings had an osseous FHC. Conversely, on the basis of our data and the literature (Cramp et al., 2004), species with similar wing shapes showed differences regarding the occurrence of the structure. For example, in the Honey Buzzard (Pernis apivorus), the FHC was present while, in the Mediterranean Shearwater (Puffinus yelkouan), it was not. Since there is no uniformity between ornithological (Cramp et al., 2004) and morphological (King and McLelland, 1984) data regarding the classification of the wing shape in the various species, it would be more appropriate to try to find a possible correlation between the presence of an FHC and the wing shape on the basis of the measurements and mathematical calculations on aerodynamic size, such as aspect ratio or wing load.

In addition, we found different histological aspects in the same genus; in fact, the Common Kestrel (Falco tinnunculus) showed a fibrocartilaginous structure (Fig. 3e) while the Red-footed Falcon (Falco vespertinus) possessed a bony FHC (Fig. 3f). It is well known that these two species possess similar mass and morphology but have different dietary habits (Brichetti et al., 1992). In fact, the Common Kestrel eats heavier prey (mainly small mammals and small birds) while the Red-footed Falcon eats mainly insects. This evidence seems to be in contrast with Smith and Smith's (1992) thesis concerning a possible correlation between the ossification of the FHC and the weight of the prey lifted during flapping flight.

Interestingly, we also observed that, in a juvenile Hooded Crow (Corvus cornix) not yet able to fly well, the FHC was composed of hyaline cartilage with evidence of bone formation in the structure (Fig. 3c). This result was in contrast to the composition of the FHC in adults (Fig. 3d) of the same species in which it is completely composed of bone. This evidence should not be interpreted as a process related to aging but, perhaps, as an adaptive feature in biomechanics and kinematics of locomotion. Various species of birds show a mechanism of ossification of the tendons, and some theories have been advanced in order to find an explanation for intratendinous ossification in birds (Smith and Smith, 1992; Vanden Berge and Storer, 1995). According to Smith and Smith (1992), the ossification of the FHC could be related to the magnitude of friction imparted on the shoulder by the bellies of the periarticular muscles. In fact, on the basis of our preliminary data, we could hypothesize that the FHC was going to ossify in response to the mechanical stimulation when attempting to fly. Additional studies should be carried out to find a possible correlation, especially comparing young birds not yet able to fly with adults of the same species.

Additionally, further considerations should be carried out on the nomenclature of this structure. In fact, many terms have been used to identify the FHC. Baumel et al. (1993) named it fibrocartilago humerocapsularis or fibrocartilago humeroscapularis, while Smith and Smith (1992) called it humeroscapular bone (also the Nomina Anatomica Avium reports this term as synonym). Since the FHC is developed in the shoulder joint capsule over which the deltoid muscle pass, we agree with the Smith and Smith (1992) suggestion of a possible role of this structure as sesamoid. According to this, we believe that a new plausible term for the FHC could be “sesamoid of pars major of the deltoid muscle” (Os sesamoideum in parte majore m. deltoidei).

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