{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,16]],"date-time":"2026-10-16T19:56:24Z","timestamp":1792180584287,"version":"4.4.0"},"reference-count":61,"publisher":"Wiley","issue":"4","license":[{"start":{"date-parts":[[2021,12,20]],"date-time":"2021-12-20T00:00:00Z","timestamp":1639958400000},"content-version":"am","delay-in-days":365,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#am"},{"start":{"date-parts":[[2020,12,20]],"date-time":"2020-12-20T00:00:00Z","timestamp":1608422400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["IOS \u20101055080"],"award-info":[{"award-number":["IOS \u20101055080"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["IOS\u20100818973"],"award-info":[{"award-number":["IOS\u20100818973"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010663","name":"H2020 European Research Council","doi-asserted-by":"publisher","award":["695517"],"award-info":[{"award-number":["695517"]}],"id":[{"id":"10.13039\/100010663","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100003575","name":"American Association of Anatomists","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100003575","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100001461","name":"American Philosophical Society","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100001461","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100008294","name":"Louisiana State University","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100008294","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Journal of Anatomy"],"published-print":{"date-parts":[[2021,4]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>The avian lung is highly specialized and is both functionally and morphologically distinct from that of their closest extant relatives, the crocodilians. It is highly partitioned, with a unidirectionally ventilated and immobilized gas\u2010exchanging lung, and functionally decoupled, compliant, poorly vascularized ventilatory air\u2010sacs. To understand the evolutionary history of the archosaurian respiratory system, it is essential to determine which anatomical characteristics are shared between birds and crocodilians and the role these shared traits play in their respective respiratory biology. To begin to address this larger question, we examined the anatomy of the lung and bronchial tree of 10 American alligators (<jats:italic>Alligator mississippiensis<\/jats:italic>) and 11 ostriches (<jats:italic>Struthio camelus<\/jats:italic>) across an ontogenetic series using traditional and micro\u2010computed tomography (\u00b5CT), three\u2010dimensional (3D) digital models, and morphometry. Intraspecific variation and left to right asymmetry were present in certain aspects of the bronchial tree of both taxa but was particularly evident in the cardiac (medial) region of the lungs of alligators and the caudal aspect of the bronchial tree in both species. The cross\u2010sectional area of the primary bronchus at the level of the major secondary airways and cross\u2010sectional area of ostia scaled either isometrically or negatively allometrically in alligators and isometrically or positively allometrically in ostriches with respect to body mass. Of 15 lung metrics, five were significantly different between the alligator and ostrich, suggesting that these aspects of the lung are more interspecifically plastic in archosaurs. One metric, the distances between the carina and each of the major secondary airways, had minimal intraspecific or ontogenetic variation in both alligators and ostriches, and thus may be a conserved trait in both taxa. In contrast to previous descriptions, the 3D digital models and CT scan data demonstrate that the pulmonary diverticula pneumatize the axial skeleton of the ostrich directly from the gas\u2010exchanging pulmonary tissues instead of the air sacs. Global and specific comparisons between the bronchial topography of the alligator and ostrich reveal multiple possible homologies, suggesting that certain structural aspects of the bronchial tree are likely conserved across Archosauria, and may have been present in the ancestral archosaurian lung.<\/jats:p>","DOI":"10.1111\/joa.13358","type":"journal-article","created":{"date-parts":[[2020,12,21]],"date-time":"2020-12-21T02:41:46Z","timestamp":1608518506000},"page":"845-873","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":33,"title":["Anatomy, ontogeny, and evolution of the archosaurian respiratory system: A case study on <i>Alligator mississippiensis<\/i> and <i>Struthio camelus<\/i>"],"prefix":"10.1111","volume":"238","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8636-925X","authenticated-orcid":false,"given":"Emma R.","family":"Schachner","sequence":"first","affiliation":[{"name":"Department of Cell Biology &amp; Anatomy School of Medicine Louisiana State University Health Sciences Center New Orleans LA USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4446-3405","authenticated-orcid":false,"given":"Brandon P.","family":"Hedrick","sequence":"additional","affiliation":[{"name":"Department of Cell Biology &amp; Anatomy School of Medicine Louisiana State University Health Sciences Center New Orleans LA USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4081-1073","authenticated-orcid":false,"given":"Heather A.","family":"Richbourg","sequence":"additional","affiliation":[{"name":"Department of Orthopaedic Surgery University of California San Francisco San Francisco CA USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6767-7038","authenticated-orcid":false,"given":"John R.","family":"Hutchinson","sequence":"additional","affiliation":[{"name":"Department of Comparative Biomedical Sciences, Structure &amp; Motion Laboratory Royal Veterinary College University of London Hatfield UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4532-7755","authenticated-orcid":false,"given":"CG","family":"Farmer","sequence":"additional","affiliation":[{"name":"Department of Biology University of Utah Salt Lake City UT USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2020,12,20]]},"reference":[{"key":"e_1_2_8_2_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.1001853"},{"key":"e_1_2_8_3_1","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.1989.0094"},{"key":"e_1_2_8_4_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1140273"},{"key":"e_1_2_8_5_1","first-page":"317","article-title":"An anatomical study of the respiratory air sacs in ostriches","volume":"66","author":"Bezuidenhout A.J.","year":"1999","journal-title":"Onderstepoort Journal of Veterinary Research"},{"key":"e_1_2_8_6_1","doi-asserted-by":"publisher","DOI":"10.1016\/0034-5687(72)90078-3"},{"key":"e_1_2_8_7_1","doi-asserted-by":"publisher","DOI":"10.1016\/0034-5687(79)90021-5"},{"key":"e_1_2_8_8_1","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.152.1.93"},{"key":"e_1_2_8_9_1","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.145.1.227"},{"key":"e_1_2_8_10_1","first-page":"224","article-title":"Die Embryonalentwicklung der Lungen bei Krokodilen und Seesschildkr\u00f6ten","volume":"84","author":"Broman I.","year":"1939","journal-title":"Jahrbuch f\u00fcr Morphologie Mikroskopisch\u2010Anatomische"},{"key":"e_1_2_8_11_1","doi-asserted-by":"publisher","DOI":"10.1016\/0034-5687(88)90010-2"},{"key":"e_1_2_8_12_1","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2148-14-128"},{"key":"e_1_2_8_13_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1405088111"},{"key":"e_1_2_8_14_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00360-016-0983-3"},{"key":"e_1_2_8_15_1","doi-asserted-by":"publisher","DOI":"10.1002\/ar.24293"},{"key":"e_1_2_8_16_1","first-page":"239","article-title":"Gross and microscopic anatomy of the respiratory system of the turkey III. The air sacs","volume":"14","author":"Cover M.S.","year":"1953","journal-title":"American Journal of Veterinary Research"},{"key":"e_1_2_8_17_1","first-page":"1","article-title":"The lung air sac system of birds. A contribution to the functional anatomy of the respiratory apparatus","volume":"45","author":"Duncker H.R.","year":"1971","journal-title":"Ergebnisse der Anatomie und Entwicklungsgeschichte"},{"key":"e_1_2_8_18_1","doi-asserted-by":"publisher","DOI":"10.1016\/0034-5687(72)90016-3"},{"key":"e_1_2_8_19_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.resp.2006.04.014"},{"key":"e_1_2_8_20_1","doi-asserted-by":"publisher","DOI":"10.1086\/605335"},{"key":"e_1_2_8_21_1","doi-asserted-by":"publisher","DOI":"10.1152\/physiol.00056.2014"},{"key":"e_1_2_8_22_1","first-page":"1","article-title":"Similarity of crocodilian and avian lungs indicates unidirectional flow is ancestral for Archosaurs","author":"Farmer C.G.","year":"2015","journal-title":"Integrative and Comparative Biology"},{"key":"e_1_2_8_23_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.zool.2015.06.001"},{"key":"e_1_2_8_24_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1180219"},{"key":"e_1_2_8_25_1","doi-asserted-by":"publisher","DOI":"10.3382\/ps.0592642"},{"key":"e_1_2_8_26_1","doi-asserted-by":"publisher","DOI":"10.1186\/s12862-016-0761-6"},{"key":"e_1_2_8_27_1","first-page":"204","article-title":"Comparative clinical anatomy of ratites","volume":"22","author":"Fowler M.E.","year":"1991","journal-title":"Journal of Zoo and Wildlife Medicine"},{"key":"e_1_2_8_28_1","unstructured":"Gadow H.(1891)V\u00f6gel. In: Bronn's Klassen und Ordnungen. Tierreich 6."},{"key":"e_1_2_8_29_1","doi-asserted-by":"publisher","DOI":"10.1111\/joa.12449"},{"key":"e_1_2_8_30_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1004637"},{"key":"e_1_2_8_31_1","doi-asserted-by":"publisher","DOI":"10.1017\/S1431927618000399"},{"key":"e_1_2_8_32_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1096-3642.1882.tb02762.x"},{"key":"e_1_2_8_33_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jbiomech.2010.08.027"},{"key":"e_1_2_8_34_1","first-page":"96","volume-title":"International review of general and experimental zoology","author":"King A.S.","year":"1966"},{"key":"e_1_2_8_35_1","first-page":"110","volume-title":"Birds: Their Structure & Function","author":"King A.S.","year":"1975"},{"key":"e_1_2_8_36_1","unstructured":"Legendre P. &Oksanen M. J.(2018).Package \u2018lmodel2\u2019.https:\/\/CRAN.R\u2010project.org\/package=lmodel2"},{"key":"e_1_2_8_37_1","doi-asserted-by":"publisher","DOI":"10.1002\/aja.1000190306"},{"key":"e_1_2_8_38_1","doi-asserted-by":"publisher","DOI":"10.1002\/aja.1000200102"},{"key":"e_1_2_8_39_1","first-page":"307","volume-title":"Form and function in birds","author":"Maina J.N.","year":"1989"},{"key":"e_1_2_8_40_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-185X.2006.tb00218.x"},{"key":"e_1_2_8_41_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.resp.2006.05.005"},{"key":"e_1_2_8_42_1","doi-asserted-by":"publisher","DOI":"10.1111\/brv.12292"},{"key":"e_1_2_8_43_1","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.203.18.2865"},{"key":"e_1_2_8_44_1","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.204.13.2313"},{"key":"e_1_2_8_45_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.resp.2009.09.011"},{"key":"e_1_2_8_46_1","first-page":"221","volume-title":"Form and function in birds","author":"McLelland J.","year":"1989"},{"key":"e_1_2_8_47_1","first-page":"365","article-title":"The air\u2010sacs of the pigeon","volume":"50","author":"M\u00fcller B.","year":"1908","journal-title":"Smithsonian Miscellaneous Collections"},{"key":"e_1_2_8_48_1","doi-asserted-by":"publisher","DOI":"10.1002\/jmor.10190"},{"key":"e_1_2_8_49_1","doi-asserted-by":"publisher","DOI":"10.1038\/nature03716"},{"key":"e_1_2_8_50_1","doi-asserted-by":"publisher","DOI":"10.1656\/1528-7092-7.3.541"},{"key":"e_1_2_8_51_1","doi-asserted-by":"publisher","DOI":"10.1006\/dbio.2000.9880"},{"key":"e_1_2_8_52_1","doi-asserted-by":"publisher","DOI":"10.1002\/ar.22427"},{"key":"e_1_2_8_53_1","volume-title":"Recherches sur L'appareil Respiratoire des Oiseaux","author":"Sappey P.\u2010C.","year":"1847"},{"key":"e_1_2_8_54_1","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2017.2631"},{"key":"e_1_2_8_55_1","doi-asserted-by":"publisher","DOI":"10.1038\/nature12871"},{"key":"e_1_2_8_56_1","doi-asserted-by":"publisher","DOI":"10.7717\/peerj.60"},{"key":"e_1_2_8_57_1","doi-asserted-by":"publisher","DOI":"10.1111\/joa.12722"},{"key":"e_1_2_8_58_1","doi-asserted-by":"publisher","DOI":"10.1016\/0034-5687(72)90019-9"},{"key":"e_1_2_8_59_1","volume-title":"Biometry","author":"Sokal R. R.","year":"2012"},{"key":"e_1_2_8_60_1","doi-asserted-by":"publisher","DOI":"10.18637\/jss.v045.i03"},{"key":"e_1_2_8_61_1","doi-asserted-by":"publisher","DOI":"10.1016\/0034-5687(88)90131-4"},{"key":"e_1_2_8_62_1","first-page":"19","volume-title":"Functional morphology in vertebrate paleontology","author":"Witmer L.M.","year":"1995"}],"container-title":["Journal of Anatomy"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/joa.13358","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/joa.13358","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/am-pdf\/10.1111\/joa.13358","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/joa.13358","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,8,24]],"date-time":"2023-08-24T02:48:42Z","timestamp":1692845322000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/joa.13358"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,12,20]]},"references-count":61,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2021,4]]}},"alternative-id":["10.1111\/joa.13358"],"URL":"https:\/\/doi.org\/10.1111\/joa.13358","archive":["Portico"],"relation":{},"ISSN":["0021-8782","1469-7580"],"issn-type":[{"value":"0021-8782","type":"print"},{"value":"1469-7580","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,12,20]]},"assertion":[{"value":"2020-08-16","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2020-10-23","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2020-12-20","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}