Tanystropheus spp., 1852

Rytel, Adam, Surmik, Dawid, Szczygielski, Tomasz, Spiekman, Stephan N. F., Kamp, Thomas van de, Zuber, Marcus & Scheyer, Torsten M., 2024, Unique internal anatomy of vertebrae as a key factor for neck elongation in Triassic archosauromorphs, Zoological Journal of the Linnean Society 202 (3), pp. 1-21 : 6-11

Bone histology and internal structure of vertebrae of Tanystropheus spp.

Anatomy of the middle cervicals

Within all of the studied vertebrae, a large cavity could be identified, surrounded by relatively thick cortex composed of alternating layers of well-organized parallel-fibred to lamellar bone ( Figs 5–8 ). In the anterior and posterior terminal portions of the cervicals, discs of secondary cancellous bone of endosteal origin formed the articular regions of the centrum ( Fig. 5B–D ). Above them, the openings of the neural canal were present. In some of the middle cervicals the neural canal floor extended only slightly from the openings towards the middle of the vertebra, forming a shelf that partially separated the internal cavity from the neural canal ( Figs 5B–E , 6C, F ), although in some other of these vertebrae the neural canal transitioned smoothly into the internal cavity (compare Fig. 6B to Fig. 5B ; Fig. 7B ). In the transverse cross section, the inner surface of the bone wall of the internal cavity was generally parallel to the circumferential outline of the vertebra ( Fig. 8A–E ). In most of the studied specimens, the dorsal part of the internal cavity seemed to preserve a semicircular shape in the transverse cross section, whereas tissue layout of its ventrolateral portion was usually much less uniform, with an irregular resorption front cutting through multiple annuli ( Fig. 8A, C, E ). This was especially evident in larger specimens, whereas in the smallest cervical, the regions of resorption were much less developed, and the outline of the internal cavity in the transverse cross section was more regularly oval ( Fig. 8B ). The neural spine extended over two deep fossae, located on both of its anteroposteriorly terminal portions. They were triangular in longitudinal cross section and ventrally delimited by thin bone trabeculae, that also constituted the roof of the neural canal. The posterior cavity was larger, forming the ‘postzygapophyseal trough’ ( Rieppel 2001). Contrary to what was observed for ‘ P ’. antiquus , in none of the studied sections of the Tanystropheus spp. middle cervicals did the internal cavity contain bony trabeculae extending internally from the surface of the bone wall. Some semi-symmetrical, slanted trabeculae of endosteal origin were present only incidentally in the anteroposteriorly terminal sections of the vertebrae (see Broili 1915: plate 3, fig. 4c). The roof of the neural canal was generally straight and parallel to the longitudinal axis of the vertebra. The ventral delimitation of the neural canal was seemingly absent for most of its length within a vertebra. Intriguingly, in one of the transverse polished sections from the anterior part of U-MO BT 738.00 ( Fig. 8F ), minute bony projections appeared symmetrically on each lateral side of the internal cavity. The colour of the limestone infill of the vertebra changed drastically at the same horizontal level, at which these projections were situated. Similar characteristics could be noted for the transverse thin section of ZPAL V. 36/166 ( Fig. 8E ), in which corresponding projections composed of periosteal bone were also present in the dorsolateral regions of the internal cavity. Between them, there was a sharp transition in sediment fraction, with the more coarse-grained infill occupying the ventral-more space. Presence of this feature possibly shows the differences in taphonomical microenvironments of the ventral and dorsal portions of the internal cavity, which may have been caused by the original existence of a no longer preserved barrier between them. Near the anteroposterior midpoint of the middle cervicals, two symmetrically placed foramina were located on the ventral side of the centrum. They entered the internal cavity as straight canals ( Fig. 8B, E ), perforating the dense cortex.

While in ‘ P ’. antiquus the neural spine was easily identifiable, it was much less recognizable in the middle cervicals of Tanystropheus spp. It was impossible to demarcate the border between the neural arch and the vertebral centrum—they were completely fused, with no preserved remnants of the suture between them, even in the smallest specimens, and little to no trabeculae within the neural arch. Continuous layers of dense parallel-fibred tissue sheathed the internal cavity. In the middle section of the larger middle cervicals of Tanystropheus spp. the outermost of these zones formed complete rings, whereas the ones located innermost were discontinued only due to resorption of the region ventral into the internal cavity, as well as the presence of the neural spine ( Fig. 8A, C , Fig. 9B ). In some of the studied transverse thin sections, including the smallest specimens, the spinous process was developed only as a thin, vertically oriented plate. It was located directly above the internal cavity and emerged from the parallel-fibred tissue of the bone walls in the dorsalmost portion of the vertebra, projecting slightly from the smooth outline of the transverse cross section. In the smallest specimen from Miedary, ZPAL V. 36/181, the neural spine was never overlain by parallel-fibred bone ( Fig. 8B ). In all of the larger specimens from Miedary, the anteroposteriorly middle part of the spinous process was obscured by thick layers of tissue that formed the walls of the internal cavity. Compared to what was noted for ‘ P ’. antiquus , the dorsolateral regions of the Tanystropheus spp. cervicals were thickened (see Fig. 9 ). The neural spine was, thus, not relatively reduced in the latter, but rather embedded within the walls of the tubularly structured vertebra. As a result, the neural canal was located close to the middle of the height of the vertebra, as in ‘ P ’. antiquus . However, in Tanystropheus spp. there was more tissue dorsolaterally (see Fig. 9 ), due to the neural spine being hypertrophied along the middle section of its anteroposterior length.

Anatomy of the posterior cervicals

In Tanystropheus sp. from Miedary, the external morphology of the cervicals changed near the posterior subregion of the neck. The 10th and 11th vertebrae were still elongate, but, contrary to the middle cervicals, exhibited a well exposed, relatively tall and continuous neural spine ( Fig. 6 ). The two last cervicals were relatively much shorter ( Fig. 6B, C ), and more similar in proportions to the dorsals ( Rieppel et al. 2010, Rytel et al. 2024). This transition was paired with the modifications in the internal structure of these elements. The relative volume occupied by the trabeculae within the centra increased caudally, especially along the neck-torso transition. In the middle cervicals the centrum was nearly devoid of trabecular bone, but this changed within the more posterior vertebrae, with the last two cervicals and the dorsals exhibiting sparse trabeculae occupying the space between the articular discs. The 10th and 11th vertebrae were generally similar in their anatomy to the middle cervicals, with their internal cavities being surrounded by a dense cortex, forming a tube-like structure ( Fig. 6I ). However, in the succeeding vertebrae the internal cavity was greatly reduced and exhibited much thicker walls, composed of two regions: a relatively thin cortex and porous, cancellous bone encompassed by it. Especially in the middle portion of the centrum of the last two cervicals, there were several large chambers, similar to those present in the anteroposteriorly terminal portions of the more anteriorly located vertebrae ( Fig. 8D ). Some of them connected to the neural canal through its floor ( Fig. 6E, F, H, I ). The transverse cross sections of the posteriormost cervicals were less oval than in the preceding vertebrae, with the centrum being much more ventrally expanded, forming a distinct keel ( Fig. 6J, K ). The diameter of the neural canal was relatively constant along the length of each of the two last vertebrae. In the longitudinal cross section, it had a sagging appearance, with its middle portion being located more ventrally. In the transverse cross section, it was oval, with its dorsolateral regions being roughly semicircular and symmetrical in outline ( Fig. 6J, K ). A similar shape could be noted in the anteroposteriorly terminal sections of the rest of the postaxial cervicals, in which the neural canal floor was still present (e.g. Fig. 8D ), and also in the dorsal vertebrae ( Fig. 6L ). In each of the two posteriormost neck vertebrae of Tanystropheus sp. from Miedary, up to two small subcentral foramina could be traced, with some specimens exhibiting only one subcentral foramen or none at all. In the studied posteriormost cervical ZPAL V. 36/110, a straight, non-branching canal connected the one present foramen with the neural canal ( Fig. 10 ).

The dorsal vertebrae were generally similar to the posteriormost cervicals in their internal anatomy. They differed in a complete lack of subcentral foramina. Moreover, the neural canal of the dorsals extended anteroposteriorly straight, with its roof and floor remaining on a relatively constant horizontal level ( Fig. 6H ). Its transverse cross section was similar in shape to the posteriormost cervicals, but more regular. Congruently to what could be observed in the 12th and 13th cervical vertebrae, the internal portion of the centrum was composed of sparsely distributed trabeculae containing a large number of cavities, some of which opened to the neural canal through its floor.

Vertebral histology

The histological characteristics of the studied vertebrae of Tanystropheus spp. were congruent with the results of the study performed by Jaquier and Scheyer (2017 and the supplemental data provided therein). New data presented herein expand our knowledge on the anteroposterior and ontogenetic variation of their structure. The walls of the internal cavity were built of primary compact lamellar to parallel-fibred matrix of periosteal origin. Some intervals with decreased vascularization could be traced within these bone walls—they formed ellipsoidal annuli that alternated with more vascularized zones in parallel to the circumference of the vertebra (see Jaquier and Scheyer 2017). Closer to the terminal portions of the anteroposterior length of the cervicals, the tissue composition changed, with the internal cavity being dorsolaterally lined with secondary endosteal lamellar bone ( Fig. 8H ) and the ventrolateral portions of the bone centrum not exhibiting the regular annuli, but rather being nearly completely composed of endosteal lamellar bone scattered with secondary osteons and erosion cavities of varying size, forming a net of sparse trabeculae ( Figs 5B–D , 8D, G ). The core of the neural spine in larger specimens was highly remodelled with longitudinally oriented secondary osteons. Simple primary vascular canals extended radially in the middle part of the vertebrae, but became more longitudinally oriented, larger, and less organized in the anteroposteriorly terminal portions. The number of vascular canals was also smaller in the more compact sections of the cortex within a single cross section.

Figures

Figure 5.Middle cervicals of Tanystropheus sp.from Miedary: A, B, D—ZPAL V.36/101; C, E, F—ZPAL V. 36/102; A is a surface model in left lateral view.B, C, longitudinal CT cross sections of an anterior (B) and a posterior portion (C) of the vertebra. D, E, F, transverse CT cross sections. Sectioning planes and walls of the neural canal and internal cavity have been outlined with white dashed lines, with the lines signifing the sectioning planes being thicker than the internal cavity outline. Anatomical abbreviations: ic—internal cavity; nc—neural canal; ns— neural spine; poz—postzygapophysis; prz—prezygapophysis.

Figure 6. Vertebrae of Tanystropheus sp. from Miedary:A, E, I—ZPAL V.36/106, 11th cervical; B, F, J—ZPAL V.36/108, 12th cervical; C, G, K—ZPAL V.36/110, 13th (last) cervical; D—ZPAL V.36/1036, dorsal; H, L—ZPAL V. 36/112, dorsal. A–D, surface models in left lateral view. E–H, longitudinal CT cross sections. I–L, transverse CT cross sections.White dashed lines mark the sectioning planes (yellow) and walls of the neural canal and internal cavity (white). Anatomical abbreviations:ic—internal cavity; nc—neural canal; ns—neural spine; poz— postzygapophysis; prz—prezygapophysis. Scale bars equal 2 cm for A–H, and 1 cm for the other panels.

Figure 7. Internal cavity volume in the cervical vertebrae of ‘P’.antiquus MGUWr 3895s (A) and Tanystropheus sp. from Miedary ZPAL V. 36/181 (B). Anatomical abbreviation:ic—internal cavity. Images obtained using ‘xray’ shader in MeshLab v.2020.12 (Cignoni et al.2008).

Figure 8. Transverse cross sections through the cervicals of Tanystropheus ‘conspicuus’ (F) and Tanystropheus sp. from Miedary (all other panels). A, ZPAL V. 36/150, middle cervical, middle portion; (B) ZPAL V. 36/181, middle cervical, middle portion; (C) ZPAL V. 36/193, middle cervical, middle portion; (D) ZPAL V. 36/1099, 10th cervical, posterior portion; (E) ZPAL V.36/166, 10th cervical, middle portion; (F) UMO BT 738.00, 11th cervical, anterior portion; (G) ZPAL V.36/1099, 10th cervical, posterior portion, close-up on the right ventrolateral portion of the vertebra with bundles of longitudinally oriented secondary osteons; (H) ZPAL V. 36/156, middle cervical, middle section, close-up on the base of neural spine with the endosteal bone lining.A, C, D, E, G, H, thin sections viewed in polarized light. B, µCT image.F, polished section.Anatomical abbreviations: elb—endosteal lamellar bone; ic—internal cavity; nc—neural canal; ns—neural spine; scf—subcentral foramen; so—secondary osteons; tb—trabecular bone.Scale bar equals 2 mm for B, G, H, and 5 mm for the other panels.

Figure 9. Interpretative drawings of the internal anatomy of a cervical vertebra of ‘P’.antiquus (A) and a middle cervical of an adult individual of Tanystropheus spp.(B) shown in the transverse cross section near the midpoint of their anteroposterior length.

Figure 10. Longitudinal cross section of ZPAL V.36/110, 13th (last) cervical vertebra of Tanystropheus sp.from Miedary, showing the course of the arterial canal (locations of its end sections are indicated with arrows). The anterior end of the vertebra points towards the left. Anatomical abbreviations: nc—neural canal; ns—neural spine.