Structure and growth pattern of pseudoteeth in Pelagornis mauretanicus (Aves, Odontopterygiformes, Pelagornithidae)

Abstract

The extinct Odontopterygiformes are the sole birds known to possess strong and sharp bony pseudoteeth, the shape and location of which are closely mimetic of real teeth. The structure of the pseudoteeth is investigated here in a late Pliocene/early Pleistocene species, Pelagornis mauretanicus, using X-ray microtomography and thin sections. The results are interpreted with regard to the pseudotooth mode of growth, and have implications concerning aspects of Pelagornis ecology. The larger pseudoteeth are hollow and approximately cone-shaped, and the smaller ones are rostro-caudally constricted. The walls of pseudoteeth are composed of bone tissue of the fibro-lamellar type, which is intensively remodeled by Haversian substitution. The jaw bones display the same structure as the pseudoteeth, but their vascular canals are oriented parallel to the long axis of the bones, whereas they are perpendicular to this direction in the pseudoteeth. There is no hiatus or evidence of a fusion between the pseudoteeth and the jaw bones. Two possible models for pseudotooth growth are derived from the histological data. The most plausible model is that pseudotooth growth began after the completion of jaw bone growth, as a simple local protraction of periosteal osteogenic activity. Pseudotooth development thus occurred relatively late during ontogeny. The highly vascularized structure and the relative abundance of parallel-fibered bone tissue in the pseudoteeth suggest poor mechanical capabilities. The pseudoteeth were most likely covered and protected by the hardened, keratinized rhamphotheca in the adult during life. The late development of the pseudoteeth would involve a similarly late and/or partial hardening of the rhamphotheca, as displayed by extant Anseriformes, Apterygiformes and some Charadriiformes. This would add support to the hypothesis of a close phylogenetic relationship between Odontopterygiformes and Anseriformes. The late maturation of the Pelagornis feeding apparatus, and hence the delayed capability for efficient prey catching, suggests that Pelagornis was altricial.

Figure 1. Pelagornis mauretanicus skull in right lateral view, showing the morphology and spatial organization of pseudoteeth.

The line drawing of skull is a reconstruction using the general shape in species of Pelagornis. The fossils used in this study are shown magnified in the inserts, with indication of the ranking of the pseudoteeth, based on their relative size, shape and position. Given the fragmentary nature of our specimens, their precise location within or among jaw bones is not known, and their locations shown here are one example among other possibilities. It is however precisely shown to which part of a sequence the specimens belong, and their orientation (latero-medial and caudo-rostral), with the help of more complete series in . hk, hook; irh, intra-ramal hinge; nar, outer narial opening; nvs, neurovascular sulcus; rg, rostral groove; trf, transverse furrow; tt, tomial “teeth” (from [3], [6], [7], [9], [17]). PT, pseudotooth. 1 to 4 indicate the rank of a pseudotooth. Main frame scale bar = 2 cm. Scale bar in inserts = 2 mm.

Figure 2. Microanatomical features of Pelagornis pseudoteeth as seen in computed tomographic reconstructions.

(A) Specimen AaO-PT-B in caudo-medial view (and oblique from a slightly occlusal view), showing the morphology of second and fourth rank pseudoteeth (PT2, PT4) and the fragment of the jaw bone from which they developed. Note the density of vascular pits on the largest tooth, and the laterally shifted implantation of the rank 4 pseudotooth. (B) Specimen AaO-PT-C in lateral view, showing the well-marked caudo-lateral ridge (arrows) on the first rank pseudotooth. (C) Specimen AaO-PT-A in lateral view, showing the rank 3 and the two rank 4 pseudoteeth (one of them with more of the apex missing than the other). There is a small amount of sedimentary matrix still attached to parts of this specimen. (D) Virtual parasagittal section in AaO-PT-B showing the hollow inside of the pseudoteeth, and the large vascular pit perforating the basal plate (vertical arrow). The insert is an enlargement of the main view showing branching and anastomoses (arrow) in the vascular network. (E) Virtual parasagittal slice in specimen AaO-PT-B showing the hollow core of a large pseudotooth and the abundant vascular canals that run inside the basal plate, and from this plate occlusally to the pseudotooth walls. Note also the absence of any discontinuity between the pseudotooth and the jaw bone, with enlargement in the insert. The rank 4 pseudotooth of this specimen is visible tangentially on this slice because rank 4 pseudoteeth are positioned more laterally than the axis of larger pseudoteeth. (F) Virtual transverse slice in the rank 2 pseudotooth of specimen AaO-PT-B. (G) Virtual transverse slice in the rank 3 pseudotooth of specimen AaO-PT-A. Note in F and G the hollow core of the pseudotooth, the abundance of vascular canals in both the pseudotooth walls and the basal plate, and the difference in the orientation of the canals in the pseudotooth (vertical, dorso-ventral, i.e., basal-apical orientation) and in the basal plate (sagittal, rostro-caudal orientation). Scale bars = 2 mm.

Figure 3. Virtual reconstruction of the vascular network in specimen AaO-PT-B showing ranks 2 and 4 pseudoteeth.

A few of the widest and of the thinnest canals do not appear here due to the used parameters of extraction of the vascular canals network, but this does not modify the general view. (A) Caudo-medial detail view. (B) Transverse section in the rank 2 pseudotooth. (C) Parasagittal section in more oblique, partly occlusal and medial view. The dense network of canals extends continuously from the basal plate occlusally to the walls of the pseudoteeth. The canals of the basal plate are clearly sagittal (arrow in B) as the other canals of the jaw bone. Some of them are clearly inflected occlusally to colonize the walls of the pseudotooth. Scale bars = 2 mm.

Figure 4. General architecture of different pseudoteeth, as seen on transverse thin sections.

(A) Pseudotooth of rank 4 in specimen AaO-PT-A. (B) Pseudotooth of rank 3 of specimen AaO-PT-A. (C) Pseudotooth of rank 1 in specimen AaO-PT-C. Wall thickness is proportionally thinner, and hence total pseudotooth compactness lower, in larger pseudoteeth. Scale bar = 2 mm.

Figure 5. Location and orientation of the sections shown in Figure 6.

Thin sections (A–C, E–G) and one virtual slice (D) were made in the rank 1 pseudotooth of specimen AaO-PT-C. The letters are those used in Figure 6. Scale bar = 2 mm.

Figure 6. Histological features of the rank 1 pseudotooth of specimen AaO-PT-C.

(A) Horizontal thin section in the apical region. Main frame: polarized transmitted light; insert: ordinary transmitted light. Remnants of primary bone tissue (asterisk) are scarce, whereas longitudinal primary and secondary (O₂) osteons are abundant and appear monorefringent. Reversion lines (rl) are clearly visible around the secondary osteons. (B) Transverse thin section in the walls of the pseudotooth. Polarized transmitted light. The osteons are brightly birefringent, which reflects the longitudinal orientation of their collagen fibers. (C) Transverse thin section in the pseudoteeth walls. Ordinary transmitted light. Osteocyte lacunae have a spindle-like morphology in the parallel-fibered bone forming the osteons. There is an artefactual wrenching at the lower right of the image. (D) Virtual horizontal slice (microtomographic) showing differences in the mineralization rate of the osteons. (E) Transverse thin section in ordinary transmitted light. Howship's lacunae (arrows) on the deep side of the wall. (F) Aspect of the basal plate viewed in a transverse thin section. Polarized (centre of the section) and ordinary (lateral parts) transmitted light. Osteons (mostly secondary) are oriented sagittally. Some superficial resorption occurred locally (arrow), whereas the deep face of the basal plate was partly reconstructed by endosteal deposits (asterisk) after resorption. (G) Longitudinal thin section. Polarized transmitted light. The osteon orientation creates a sharp distinction between the basal plate (bp) and the walls of the pseudotooth (wpt). Scale bars = 200 µm.

Figure 7. Schematic reconstruction of the first hypothesis for pseudotooth growth.

The basal plate is totally part of the jaw bone, and pseudotooth growth occurs after completion of jaw bone growth. Two growth stages are represented: (1) early stage, before pseudotooth growth; (2) late stage, when the pseudotooth is growing. There would be no acceleration, but a simple protraction of bone accretion to form the pseudotooth. In stage 2 the light grey areas are the ancient, now resorbed, states of the bone at stage 1. Green arrows show the directions of bone accretion and red arrows the directions of bone resorption; both are longer when the phenomenon is of greater amplitude. The crosses within the jaw bone indicate that the orientation of primary vascular canals at growth stage 1 is unknown. In the pseudotooth (growth stage 2), the elongated oval segments, blue with white centre, represent the basal-apical (occlusal) orientation of primary and secondary osteons. In transverse section, they are cut along their elongation axis. The small blue circles with white centres in the jaw bone (basal plate included) represent the rostro-caudal orientation of secondary osteons at growth stage 2. In transverse section, they are cut orthogonally to their elongation axis. Green dashed lines show areas of secondary (reconstructive) endosteal bone deposits.

Figure 8. Schematic reconstruction of the second hypothesis for pseudotooth growth.

The basal plate is part of the pseudotooth, and the latter grows simultaneously with the jaw bone. In an early growth stage (1), the pseudotooth and the jaw bone are actively growing, but sub-periosteal accretion is faster on the pseudotooth, which results in its differentiation from the subjacent jaw bone. At this stage, the pseudotooth is a solid cone with primary osteons sub-parallel to the main growth direction. When local growth is ending (2), a resorption field inside the pseudotooth creates a broad cavity, and provokes the differentiation of the basal plate. At this stage, the vascular canals within the basal plate still have their original orientation. In a late growth stage (3), extensive remodeling in the jaw bone and in the basal plate creates longitudinally oriented secondary osteons. Same symbols and color code as for Figure 7.