Structure and function of the septum nasi and the underlying tension chord in crocodylians

Abstract

A long rostrum has distinct advantages for prey capture in an aquatic or semi-aquatic environment but at the same time poses severe problems concerning stability during biting. We here investigate the role of the septum nasi of brevirostrine crocodilians for load-absorption during mastication. Histologically, both the septum nasi and the septum interorbitale consist of hyaline cartilage and therefore mainly resist compression. However, we identified a strand of tissue extending longitudinally below the septum nasi that is characterized by a high content of collagenous and elastic fibers and could therefore resist tensile stresses. This strand of tissue is connected with the m. pterygoideus anterior. Two-dimensional finite element modeling shows that minimization of bending in the crocodilian skull can only be achieved if tensile stresses are counteracted by a strand of tissue. We propose that the newly identified strand of tissue acts as an active tension chord necessary for stabilizing the long rostrum of crocodilians during biting by transforming the high bending stress of the rostrum into moderate compressive stress.

Keywords: finite element analysis; histology; septum nasi; tension chord.

Figure 1

(A) Photograph of a near‐midline sagittal view of a Nile crocodile skull demonstrating the position of the septum nasi and the septum interorbitale. The m. pterygoideus is partly deflected to reveal the septum interorbitale. The white outline indicates the position of the detail shown in (B). Anterior is to the right. (B) Higher magnification photograph of the relative position of the septum nasi and the underlying tension chord in the crocodilian rostrum. (C) Dorsal view of the entire tension chord dissected from the skull of a semi‐adult Caiman crocodilus extending from the region of the prefrontal pillar to the region of the nostrils. Scale bar: 1 cm.

Figure 2

Histological analysis of sagittal sections of the septum nasi (A,C,D), septum interorbitale (E,F) in crocodilyans, and of tangential sections of meniscus of chicken (B) using different staining protocols. (A,E) AFG staining reveals chondrocytes in their territories embedded in a homogeneous hyaline matrix (green). (B) For comparison, AFG staining shows the typical fibrocartilage appearance of the chicken meniscus. (C) Toluidine Blue staining of proteoglycans in the matrix. (D,F) Safranin staining of proteoglycans. Arrowheads indicate chondrocytes, arrows point to chondrocyte territories. Scale bars: 100 μm.

Figure 3

Orientation of chondrocyte territories in the septum nasi (A,B) and the septum interorbitale (C,D). The vertical extent of the septum was normalized (%), and the orientation (°) of the territory (abscissa) was plotted vs. the distance of the territory from the ventral margin of the septum (ordinate). 0° and 180° indicate an anterior‐posterior orientation, 90° indicates a vertical orientation. (A,C) Data from sections through peripheral parts of the septum. (B,D) Data from the mediolateral center of the septum.

Figure 4

Histological analysis of the tissue strand extending below and parallel to the septum nasi in sagittal (A,B) and frontal sections (C–F). AFG staining (A,C,E) reveals collagen fibers (green) and elastic fibers (purple). In Orcein‐stained tissue (B,D,F) elastic fibers are selectively revealed (dark purple). They are densest in the dorsal and especially in the ventral margin of the tissue strand. Arrows point to elastic fibers (A,B) and their profiles (E,F). bv, blood vessel; V, naso‐palatine nerve, a branch of the maxillary ramus of the trigeminal nerve. Scale bars: 50 μm (A,B,E,F) and 100 μm (C,D), respectively.

Figure 5

Calculation of the center of the cross‐sectional area at three positions of the rostrum of a Caiman crocodilus based on CT images available at www.digimorph.org. (A) Left lateral view of the caiman skull, vertical lines indicate the positions of the cross‐sections (1: B,C, 2: D,E, 3: F,G). Scale bar: 1 cm. (B,D,F) CT images of cross‐sections through the Caiman rostrum, scale bar in (B) represents 1 cm for (B–G). (C,E,G) models of the corresponding CT images. The center of the cross‐sectional area is represented by crosses.

Figure 6

Two‐dimensional FE‐models for a holding bite at the anterior jaws. (A) Constraints, insertions and directions of the forces used in the FE models. (1) Constraint at the position of the quadrato‐articular joint, (2) constraint at the occipital condyle as an indicator for bending moments, (3) bite force, (4–8, 9 as reacting force) stepped forces of the tension chord with different points of insertion in the sagittal plane to eliminate buckling of the rostrum. The force of the tension chord is generated by m. pterygoideus anterior (10) spreading from the cartilago transiliens (c.t.) on both sides of the real skull. Likewise, m. pseudotemporalis (11), m. adductor mandibulae (12), m. intramandibularis (13), and m. pterygoideus posterior (14) are positioned on both sides of the real skull. (B,C) model M1 without tension chord. (D,E) model M2 with tension chord. Compressive stresses are shown in (B) and (D), tensile stresses in (C) and (E). Compressive stresses shown in (D) are homogenized in the rostrum and tensile stresses in (E) are eliminated. Therefore, bending is eliminated in the rostrum as well. Compressive and tensile stresses are color‐coded according to the inset.

Figure 7

Two‐dimensional FE‐models for crushing bites. (A,B) Model M3 for the middle position without tension chord, (C,D) Model M4 for the middle position with an implemented tension chord. Compressive stresses are homogenized, and bending is eliminated in M4 (C). Tensile stresses are eliminated in M4 (D). (E,F) Model M5 for the posterior position of a crushing bite without tension chord. The rostrum is already free of stresses, a tension chord is unnecessary. (A,C,E) Compressive stresses, (B,D,F) Tensile stresses. Other conventions as in Fig. 6.

Figure 8

Two‐dimensional FE‐model shows the stress distribution under superposition of all load cases: holding bite, crushing bite middle position, and crushing bite posterior position with implemented tension chord. This superposition corresponds to the functional loading of biological structures. (A,B) Model M6, compressive stresses are homogenized in the skull and bending is eliminated (A). Tensile stresses are zero (B).