A Nomenclature for Vertebral Fossae in Sauropods and Other Saurischian Dinosaurs

The axial skeleton of extinct saurischian dinosaurs (i.e., theropods, sauropodomorphs), like living birds, was pneumatized by epithelial outpocketings of the respiratory system. Pneumatic signatures in the vertebral column of fossil saurischians include complex branching chambers within the bone (internal pneumaticity) and large chambers visible externally that are bounded by neural arch laminae (external pneumaticity). Although general aspects of internal pneumaticity are synapomorphic for saurischian subgroups, the individual internal pneumatic spaces cannot be homologized across species or even along the vertebral column, due to their variability and absence of topographical landmarks. External pneumatic structures, in contrast, are defined by ready topological landmarks (vertebral laminae), but no consistent nomenclatural system exists. This deficiency has fostered confusion and limited their use as character data in phylogenetic analysis.We present a simple system for naming external neural arch fossae that parallels the one developed for the vertebral laminae that bound them. The nomenclatural system identifies fossae by pointing to reference landmarks (e.g., neural spine, centrum, costal articulations, zygapophyses). We standardize the naming process by creating tripartite names from “primary landmarks,” which form the zygodiapophyseal table, “secondary landmarks,” which orient with respect to that table, and “tertiary landmarks,” which further delineate a given fossa.The proposed nomenclatural system for lamina-bounded fossae adds clarity to descriptions of complex vertebrae and allows these structures to be sourced as character data for phylogenetic analyses. These anatomical terms denote potentially homologous pneumatic structures within Saurischia, but they could be applied to any vertebrate with vertebral laminae that enclose spaces, regardless of their developmental origin or phylogenetic distribution

Representative vertebrae of <i>Apatosaurus louisae</i>.

<p>Anterior (top), left lateral (middle), and posterior (bottom) views of anterior cervical (cv 6), posterior cervical (cv 11), anterior dorsal (dv 3), posterior dorsal (dv 8), and anterior caudal (ca 2) vertebrae representing a single individual (CM 3018) and are to scale. Important changes along the column include the loss of the sprf and spof in bifid-spined posterior cervical and anterior dorsal vertebrae, appearance of the prcprf in posterior cervical vertebrae, and the division of the cdf into the cdf and cpaf in mid- and posterior dorsal vertebrae. Images modified from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017114#pone.0017114-Gilmore1" target="_blank">[52]</a>:pls. 24–26). Abbreviations and color scheme as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017114#pone-0017114-g007" target="_blank">Figure 7</a>.</p

Representative vertebrae of <i>Rapetosaurus krausei</i>.

<p>Anterior (top), left lateral (middle), and posterior (bottom) views of anterior cervical (cv 3), posterior cervical (cv 11), anterior dorsal (dv 3), posterior dorsal (dv 7), and anterior caudal (ca 2) vertebrae. Specimens represent a single juvenile individual (FMNH PR 2209) and are to scale. Several important changes along the column are related to the anteroposteriorly shortened and reclined neural spines of the pectoral region, including the development of broad, flat sprfs, loss and re-emergence of the sdf/posdf. As in many other titanosaurs, there is a broad, subtly divided sdf that bears crenulated texture in the mid-cervical region and a dorsally restricted pacdf in the mid-dorsal region. Green/blue gradient in the lateral view of ca 2 indicates that the pocdf and posdf cannot be distinguished from one another. Images modified from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017114#pone.0017114-CurryRogers1" target="_blank">[22]</a>; photographs of dv 3 and dv 7 have been reversed. © Copyright 2009 The Society of Vertebrate Paleontology. Reprinted and distributed with permission of the Society of Vertebrate Paleontology. Abbreviations and color scheme as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017114#pone-0017114-g007" target="_blank">Figure 7</a>.</p

Variable development of the epipophyseal-prezygapophyseal lamina (eprl) and the divided spinodiapophyseal fossa (sdf) in cervical vertebrae.

<p>The eprl in its most basic form (<b>A</b>) connects the prezygapophysis directly with the epipophysis of the postzygapophysis, dividing the sdf into upper (sdf1) and lower (sdf2) subfossae. More commonly, the eprl is conjoined for at least a portion of its length with two or more laminae (<b>B</b>, <b>C</b>), although sdf1 and sdf2 are still readily identifiable. Blue (sprl, spol, prdl, podl) and yellow (eprl) bars represent single laminae; green bars represent conjoined laminae. Examples of conjoined eprl and the indentification of the fossae they bound are given using the holotypic cervical vertebrae of <i>Erketu ellisoni</i> (IGM 100/1803; <b>D</b>, <b>E</b>) and <i>Nigersaurus taqueti</i> (MNN-GAD 512; <b>F–H</b>) in left lateral view, with diagrammatic representation of laminae and landmarks bounding the sdf. Development of the eprl dividing the sdf is dependent on relative position of landmarks, particularly the separation of the summit of the neural spine (s) and the postzygapophysis (po), as well as the relative positions of the prezygapophysis (pr) and diapophysis (d). Even in taxa with a strongly developed eprl, such as <i>Nigersaurus</i>, the lamina is separate from either the sprl or the podl for only a short distance. Taxa with extremely elongate cervical vertebrae, such as <i>Erketu</i>, may have a slightly different arrangement of connectivity between the eprl, spino-zygapophyseal laminae, and zygapophyseal-diapophyseal laminae, although the presence of the eprl can still be traced. Seventh cervical vertebra of <i>Nigersaurus</i> reversed from right lateral. Not to scale.</p

Neural arch fossa morphospace.

<p>Comparative diagram illustrating relative complexity of neural arch fossae in four theropods and nine sauropodomorphs. light gray squares represent unique fossae above the zygodiapophyseal table; dark gray squares represent unique fossae below the table. Unique fossae are defined as midline fossae and either the right or left paramedian fossae. Midline fossae that are subsequently divided count as two unique fossae. Therefore, a vertebra with two midline fossae (the sprf and spof) and two paramedian fossae (the prsdf and the posdf) is represented by four light gray squares. If a similar vertebra has a divided sprf but is otherwise identical, it is represented by five light gray squares. Note the general increase in complexity above and below the table in Neosauropoda compared to basal eusauropods (e.g., <i>Shunosaurus</i>), basal sauropods (e.g., <i>Antetonitrus</i>), basal sauropodomorphs (e.g., <i>Panphagia</i>), and theropods, although reduced complexity does occur in <i>Dicraeosaurus</i> and <i>Isisaurus</i>. Tree topology is based on several recent phylogenies <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017114#pone.0017114-Wilson5" target="_blank">[34]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017114#pone.0017114-CurryRogers2" target="_blank">[46]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017114#pone.0017114-Yates1" target="_blank">[60]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017114#pone.0017114-Holtz1" target="_blank">[61]</a>.</p

Representative vertebrae of <i>Mamenchisaurus youngi</i>.

<p>Anterior (top), left lateral (middle), and posterior (bottom) views of anterior cervical (cv 9), posterior cervical (cv 17), anterior dorsal (dv 2), posterior dorsal (dv 8), and anterior caudal (ca 1) vertebrae. Specimens come from a single individual (holotype ZDM 0083) and are to scale. Posterior view of cv 9 and anterior views of cv 9, cv 17, and dv 8 not available; anterior view of dv 7 used for dv 8. Important changes along the column include the appearance of a pcpl and the division of the cdf into a pacdf and a cpaf. Images are modified from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017114#pone.0017114-Ouyang1" target="_blank">[33]</a>:figs. 15, 17, 20, 26, 30). Abbreviations and color scheme as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017114#pone-0017114-g007" target="_blank">Figure 7</a>.</p

Configuration of vertebral laminae and fossae associated with the parapophysis in presacral vertebrae.

<p>Left, a cervical or anterior dorsal vertebra, in which the parapophysis is positioned on the centrum. Two laminae extend ventrally from the diapophysis (acdl, pcdl), helping to bound three fossae (prcdf, cdf, pocdf). Center, a simple mid- or posterior dorsal vertebra in which the parapophysis has risen onto the neural arch and is connected to the diapophysis and anterior centrum via two complementary laminae (ppdl, acpl). The configuration of fossae and their nomenclature, however, remains the same: the three fossae are still bounded by the zygapophyses, diapophysis, and centrum. Right, a complex mid- or posterior dorsal vertebra in which the parapophysis has risen onto the neural arch and four, rather than two, laminae extend from it (ppdl, acpl, pcpl, prpl). The addition of two laminae bisects the fossae between the diapophysis and centrum (cdf) and between the diapophysis, centrum, and prezygapophysis (prcdf). Four fossae are created, two of which require special naming (noted by asterisks). The fossa between the parapophysis and centrum does not contact the zygodiapophyseal table and thus lacks a primary landmark; in this case the parapophysis is enlisted as a primary landmark (cpaf). The fossa between the diapophysis, parapophysis, and prezygapophysis is not bounded by a secondary landmark (i.e., neural spine or centrum), and the parapophysis is enlisted as a secondary landmark (prpadf).</p

Representative vertebrae of <i>Brachiosaurus brancai</i>.

<p>Anterior (top), left lateral (middle), and posterior (bottom) views of anterior cervical (cv 3), middle cervical (cv 5), anterior dorsal (?dv 5), posterior dorsal (?dv 12), and anterior caudal (ca 1) vertebrae. Specimens come from several skeletally mature individuals (MB.R. 2180, MB.R. 3824, MB.R. 3822, MB.R. no number, see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017114#pone.0017114-Janensch1" target="_blank">[45]</a>: pl. 2) and are to scale. Important changes along the column include the appearance of numerous irregular fossae in the sdf of cervical vertebrae and the absence of a cpaf in mid-dorsal vertebrae. Green/blue gradient in the lateral view of ca 1 indicates an undistinguishable pocdf + posdf. Photographs of ?dv 12 and ca 1 have been reversed. Abbreviations and color scheme as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017114#pone-0017114-g007" target="_blank">Figure 7</a>.</p

Vertebral fossae in the sauropod dinosaur <i>Rapetosaurus krausei</i>.

<p>Vertebral fossae in sauropods are hypothesized to be produced by pneumaticity, which is usually limited to the axial column, excluding the atlas, chevrons, and distal caudal vertebrae (bottom image). The middle photograph shows fossae in a cervical vertebra, which in the neural arch are bounded by vertebral laminae. The close-up photograph (top) shows the that bone texture within the fossa is often smooth, crenulated, and shiny, which is indicative of pneumatic bone. Silhouette reconstruction from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017114#pone.0017114-CurryRogers3" target="_blank">[49]</a>; cervical vertebra from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017114#pone.0017114-CurryRogers4" target="_blank">[59]</a>:fig. 10). Scale bar equals 1 m in silhouette; scale bars equal 3 cm in photographs. ©Copyright 2009 The Society of Vertebrate Paleontology. Reprinted and distributed with permission of the Society of Vertebrate Paleontology.</p