Osteological and Soft-Tissue Evidence for Pneumatization in the Cervical Column of the Ostrich (Struthio camelus) and Observations on the Vertebral Columns of Non-Volant, Semi-Volant and Semi-Aquatic Birds

© 2015 Apostolaki et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [4.0], which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. The attached file is the published version of the article

Distribution of pneumatic elements of caudal column per taxon.

<p>Presence (+) and absence (-) of pneumatic characters found on the caudal vertebrae from specimens of the 11 taxa studied. The penguin with the pneumatised vertebrae is <i>Pygoscelis papua</i> (NHMUK unregistered). For more details see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0143834#pone.0143834.s014" target="_blank">S1 Table</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0143834#pone.0143834.s016" target="_blank">S3</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0143834#pone.0143834.s026" target="_blank">S13</a> Tables. Abbreviations: PF, pneumatic foramina; F, fossae; L, laminae; Sept., septated; N/A, non-available.</p

Dorsal view of ostrich (<i>Struthio camelus</i>) cervical column.

<p><b>(A)</b> Posterolateral view of CV4 (BRS MG Ag1174.2), revealing the <i>foramen pneumaticum</i> ventral to the <i>lamina arcocostalis</i>, the <i>foramen pneumaticum</i> ventral to the processus transversus, and the <i>foramen transversarium</i>; note the vertebral foramen located posterior to the <i>processus spinosus</i>; <b>(B)</b> Ventral view of CV3 (BRSMG Ag1174.1) from which the <i>foramen vertebrale laterale</i>, the <i>crista ventralis</i> that runs along the <i>corpus</i>, and the pneumatic foramina on the anterior-most margin of the vertebral foramen can be viewed; <b>(C)</b> Left anteroventral view of a cervical vertebra (CV10: BRSMG Ag1174.8) exposing the pneumatic foramen on the inner wall of the vertebral foramen and the multiple pneumatic foramina within the costotransverse ring; <b>(D)</b> Left ventrolateral view of CV5 (BRSMG Ag1174.3) showing the centrodiapophyseal lamina, the <i>lamina arcocostalis</i> just above the pneumatic foramen on the arcocostal surface's posterior-most margin, and a pneumatic foramen on both the <i>corpus</i> along the line of the neurocentral suture and on the posterolateral surface of the cotyle; <b>(E)</b> Ventral view of CV11 (BRSMG Ag1174.9) exposing the centroparapophyseal laminae, two pneumatic foramina on the ventral side of the left <i>processus costarius</i> and one on the right side of the cotyle; <b>(F)</b> Ventral view of CV9 (BRSMG Ag1174.9) showing pneumatic foramina on both hypapophyses and both centroparapophyseal laminae. The scale bar corresponds to the main cervical column. The main cervical column photograph was taken by Simon Powell. Abbreviations: cv <i>crista ventralis</i>; cdpl centrodiapophyseal lamina; cpal centroparapophyseal lamina; pac <i>processus articularis cranialis</i>; paa <i>processus articularis caudalis</i>; fp <i>foramen pneumaticum</i>; ft <i>foramen transversarium</i>; fvl <i>foramen vertebrale laterale</i>; la <i>lamina arcocostalis</i>; pc <i>processus costarius</i>; ps <i>processus spinosus</i>.</p

Distribution of pneumatic elements of thoracic column per taxon.

<p>Presence (+) and absence (-) of pneumatic characters found on the thoracic vertebrae from specimens of the 11 taxa studied. The penguin with the pneumatised vertebrae is <i>Pygoscelis papua</i> (NHMUK unregistered). For more details see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0143834#pone.0143834.s014" target="_blank">S1 Table</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0143834#pone.0143834.s016" target="_blank">S3</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0143834#pone.0143834.s026" target="_blank">S13</a> Tables. Abbreviations: PF, pneumatic foramina; F, fossae; L, laminae; Sept., septated.</p

Distribution of pneumatic elements on the cervical column per taxon.

<p>Presence (+) and absence (-) of pneumatic characters found on the cervical vertebrae from specimens of the 11 taxa studied. The penguin with the pneumatised vertebrae is <i>Pygoscelis papua</i> (NHMUK unregistered). For more details see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0143834#pone.0143834.s014" target="_blank">S1 Table</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0143834#pone.0143834.s016" target="_blank">S3</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0143834#pone.0143834.s026" target="_blank">S13</a> Tables. Abbreviations: PF, pneumatic foramina; F, fossae; L, laminae; Sept., septated.</p

Right lateral view of the ostrich neck with flesh depictions.

<p><b>(A)</b> Anterolateral view of the anterior part of the neck revealing the free end of the cervical artery; <b>(B)</b> Same for (a) but with the artery extended revealing its associated semi-transparent diverticular membrane that attaches within the muscle layers; <b>(C)</b> Partially dissected ostrich neck with some of the exterior muscle layers stretched out showing the intertwined air sac membranes; <b>(D)</b> Image exposing the interior surface of the cut-open cervical artery located on the ventral side of the cervical column; <b>(E)</b> Lateral view of a cervical vertebra exposing the air sac lateral vertebral diverticulum and its transparent extensions invading the <i>foramen pneumaticum</i> positioned dorsally to the lateral vertebral diverticulum; <b>(F)</b> Posterior view of a cervical vertebra showing a cluster of 3–4 pneumatic foramina within the foramen vertebrale inner ventral wall. Abbreviations: paa <i>processus articularis caudalis</i>; fs <i>fossa spinalis</i>; fp <i>foramen pneumaticum</i>; LVDv lateral vertebral diverticulum. The scale bar corresponds to the main cervical column.</p

Schematic representation of air sac complex with its associated muscles.

<p>Right lateral view of a <i>Struthio camelus</i> (ostrich) mid-cervical vertebra, showing a local fraction of the air sac diverticular complex and the muscle groups (red) associated with it and the vertebra. The black lines represent the various borders of the diverticular membrane extensions; the purple shows the air sac's lateral vertebral diverticulum along the corpus; the light blue depicts the membranes that extend from the diverticulum, anchoring on the <i>corpus</i> and invading the brown <i>foramen pneumaticum</i>. Abbreviations: fp <i>foramen pneumaticum</i>; MOS <i>M</i>. <i>obliquospinalis</i>; MOT <i>M</i>. <i>obliquotransversalis</i>; MIS <i>M</i>. <i>interspinalis</i>; MLCV <i>M</i>. <i>longus colli ventralis</i>; MIT <i>M</i>. <i>intertransversalis</i>.</p

Dorsal view of the dissected ostrich neck with dissection captions.

<p><b>(A)</b> Anterolateral view of a cervical vertebra revealing a <i>foramen pneumaticum</i> on the <i>corpus</i> and the purple air sac's lateral vertebral diverticulum (LVDv) that extends along the <i>corpus</i> and attaches on the posterior margin of the <i>facies terminalis caudalis</i>. Note the obliquotransverse muscle (<i>M</i>. <i>obliquotransversalis</i>) anterodorsally to the foramen as well as the transparent air sac diverticular extensions that attach on the foramen's margin and invade it; <b>(B)</b> Another close-up from another cervical vertebra showing a pneumatic foramen directly above the air sac diverticulum (LVDv) and below the air sac membrane attachment; <b>(C)</b> Part of the ostrich neck before the removal of the exterior muscles. Note the transparent air sac membrane that folds beneath the muscle complex. The membrane system is a continuous network that engulfs the bone and is covered by the muscular system; <b>(D)</b> Right posterolateral view of the last cervical vertebra revealing the air sac membrane network anchoring laterally to the muscular system and medially to the <i>corpus</i>. Scale bar corresponds to the main cervical column. Abbreviations: c <i>corpus</i>; fp <i>foramen pneumaticum</i>; faa <i>facies articularis caudalis</i>; LVDv lateral vertebral diverticulum.</p

General status of each avian taxon studied.

<p>Tabulation of bird taxa with their orders, indicating locality, state of preservational condition of the specimen (St.pr.con.), number of specimens, pneumaticity status, Pneumaticity Index (PI%), ontogenetic stage, and registered specimen number (Reg.sp.no.). Abbreviations: D, diver; FL, flyer; FLS, flightless; ND, non-diver; P, pneumatic; SP, semi-pneumatic.</p

Triple schematic of ostrich vertebra-air sac-flesh tissue system.

<p><b>(A)</b> Depiction of a semi-transparent layer of the actual close-up of the air sac diverticulum system with its surrounding tissue placed on top of the cervical vertebra; <b>(B)</b> Magnified air sac diverticulum and its membranous extensions. The <b>black</b> lines indicate the various folds and borders of the air sac diverticulum and its membranes as they expand on the bone; <b>(C)</b> Only the bony tissue with the schematic representation of the air sac diverticulum/membrane system without the surrounding flesh tissue. Same colour codes apply as described in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0143834#pone.0143834.g002" target="_blank">Fig 2</a>. Please note that the air sac is not inflated and thus intraspecific variation is highly probable.</p