{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,12]],"date-time":"2026-09-12T00:23:03Z","timestamp":1789172583120,"version":"build-2803163510"},"reference-count":30,"publisher":"The Company of Biologists","issue":"17","license":[{"start":{"date-parts":[[2026,9,11]],"date-time":"2026-09-11T00:00:00Z","timestamp":1789084800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"crossref","award":["2018-04172"],"award-info":[{"award-number":["2018-04172"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"crossref","award":["1283784"],"award-info":[{"award-number":["1283784"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100008572","name":"University of Ottawa","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100008572","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,9,15]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>The gills are hypothesized to play a key role in early vertebrate evolution by replacing the skin as the primary site of gas exchange. In this scenario, water flow across the gills for suspension feeding was coopted for gas exchange in stem vertebrates, facilitating the evolution of larger, active fishes. This is supported by a stem-vertebrate origin for structures increasing gill capacity for gas exchange. However, these structures might have enhanced an already dominant capacity at ancestral deuterostome gills. To test this, we characterized gill function in the suspension-feeding hemichordate Protoglossus graveolens. We measured oxygen uptake and ammonia excretion in whole worms and worm halves with or without gills at 10\u00b0C and 20\u00b0C to stimulate gill recruitment. Gills did not enhance oxygen uptake or ammonia excretion, suggesting they are not a primary site of gas exchange. This provides critical functional support for the long-hypothesized vertebrate origin of gills as the primary gas exchange organ.<\/jats:p>","DOI":"10.1242\/jeb.253087","type":"journal-article","created":{"date-parts":[[2026,8,26]],"date-time":"2026-08-26T07:40:37Z","timestamp":1787730037000},"source":"Crossref","is-referenced-by-count":1,"title":["Gills are not the primary site of gas exchange in the suspension-feeding hemichordate\n                    <i>Protoglossus graveolens<\/i>"],"prefix":"10.1242","volume":"229","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8206-6836","authenticated-orcid":false,"given":"Michael A.","family":"Sackville","sequence":"first","affiliation":[{"name":"University of Ottawa 1 Department of Biology , , Ottawa, ON , , K1N 6N5","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christopher B.","family":"Cameron","sequence":"additional","affiliation":[{"name":"Universit\u00e9 de Montr\u00e9al 2 D\u00e9partement de Sciences Biologiques , , Montr\u00e9al, PQ , , H3C 3J7","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Colin J.","family":"Brauner","sequence":"additional","affiliation":[{"name":"University of British Columbia 3 Department of Zoology , , Vancouver, BC , , V6T 1Z4","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","published-online":{"date-parts":[[2026,9,11]]},"reference":[{"key":"2026091109313823800_JEB253087C1","volume-title":"The Biology of Hemichordata and Protochordata","author":"Barrington","year":"1965"},{"key":"2026091109313823800_JEB253087C2","first-page":"403","article-title":"Appendix: Physicochemical parameters for use in fish respiratory physiology","volume-title":"Fish Physiology","author":"Boutilier","year":"1984"},{"key":"2026091109313823800_JEB253087C3","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1016\/j.resp.2012.07.011","article-title":"Ontogeny and paleophysiology of the gill: New insights from larval and air-breathing fish","volume":"184","author":"Brauner","year":"2012","journal-title":"Respir. Physiol. Neurobiol."},{"key":"2026091109313823800_JEB253087C4","doi-asserted-by":"publisher","first-page":"196","DOI":"10.1139\/z04-190","article-title":"A phylogeny of the hemichordates based on morphological characters","volume":"83","author":"Cameron","year":"2005","journal-title":"Can. J. Zool."},{"key":"2026091109313823800_JEB253087C5","doi-asserted-by":"publisher","first-page":"4469","DOI":"10.1073\/pnas.97.9.4469","article-title":"Evolution of the chordate body plan: New insights from phylogenetic analyses of deuterostome phyla","volume":"97","author":"Cameron","year":"2000","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2026091109313823800_JEB253087C6","doi-asserted-by":"publisher","first-page":"268","DOI":"10.1126\/science.220.4594.268","article-title":"Neural crest and the origin of vertebrates: a new head","volume":"220","author":"Gans","year":"1983","journal-title":"Science"},{"key":"2026091109313823800_JEB253087C7","doi-asserted-by":"publisher","first-page":"729","DOI":"10.1016\/j.cub.2017.01.022","article-title":"The origin of vertebrate gills","volume":"27","author":"Gillis","year":"2017","journal-title":"Curr. Biol."},{"key":"2026091109313823800_JEB253087C8","doi-asserted-by":"publisher","first-page":"898","DOI":"10.1111\/j.1095-8312.2009.01332.x","article-title":"The gill slits and pre-oral ciliary organ of Protoglossus (Hemichordata: Enteropneusta) are filter-feeding structures","volume":"98","author":"Gonzalez","year":"2009","journal-title":"Biol. J. Linn. Soc."},{"key":"2026091109313823800_JEB253087C9","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1016\/j.diff.2014.02.001","article-title":"The lamprey: a jawless vertebrate model system for examining origin of the neural crest and other vertebrate traits","volume":"87","author":"Green","year":"2014","journal-title":"Differentiation"},{"key":"2026091109313823800_JEB253087C10","doi-asserted-by":"publisher","first-page":"474","DOI":"10.1038\/nature14436","article-title":"Evolution of vertebrates as viewed from the crest","volume":"520","author":"Green","year":"2015","journal-title":"Nature"},{"key":"2026091109313823800_JEB253087C11","doi-asserted-by":"publisher","first-page":"91","DOI":"10.2108\/zsj.27.91","article-title":"Regeneration in the hemichordate Ptychodera flava","volume":"27","author":"Humphreys","year":"2010","journal-title":"Zool. Sci."},{"key":"2026091109313823800_JEB253087C30","doi-asserted-by":"publisher","first-page":"2359","DOI":"10.1016\/j.cub.2023.04.048","article-title":"Cambrian stem-group ambulacrarians and the nature of the ancestral deuterostome","volume":"33","author":"Li","year":"2023","journal-title":"Curr. Biol."},{"key":"2026091109313823800_JEB253087C12","doi-asserted-by":"publisher","first-page":"171","DOI":"10.1016\/S0091-679X(04)74008-X","article-title":"Hemichordate embryos: procurement, culture, and basic methods","volume":"74","author":"Lowe","year":"2004","journal-title":"Methods. Cell. Biol."},{"key":"2026091109313823800_JEB253087C13","doi-asserted-by":"publisher","first-page":"456","DOI":"10.1038\/nature14434","article-title":"The deuterostome context of chordate origins","volume":"520","author":"Lowe","year":"2015","journal-title":"Nature"},{"key":"2026091109313823800_JEB253087C14","doi-asserted-by":"publisher","first-page":"821","DOI":"10.1016\/0300-9629(79)90009-4","article-title":"Vanadium in tunicates: oxygen-binding studies","volume":"62","author":"Macara","year":"1979","journal-title":"Comp. Biochem. Physiol. A Mol. Integ. Physiol."},{"key":"2026091109313823800_JEB253087C15","doi-asserted-by":"publisher","first-page":"41","DOI":"10.3354\/meps087041","article-title":"Response of Saccoglossus kowalevskii (phylum Hemichordata, class Enteropneusta) to changes in diet","volume":"87","author":"Miller","year":"1992","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"2026091109313823800_JEB253087C16","doi-asserted-by":"publisher","first-page":"916","DOI":"10.1242\/dev.091066","article-title":"Genetic lineage labeling in zebrafish uncovers novel neural crest contributions to the head, including gill pillar cells","volume":"140","author":"Mongera","year":"2013","journal-title":"Development"},{"key":"2026091109313823800_JEB253087C17","doi-asserted-by":"publisher","first-page":"419","DOI":"10.1038\/nature13414","article-title":"A primitive fish from the Cambrian of North America","volume":"512","author":"Morris","year":"2014","journal-title":"Nature"},{"key":"2026091109313823800_JEB253087C18","doi-asserted-by":"publisher","first-page":"316","DOI":"10.1111\/brv.12908","article-title":"Worms and gills, plates and spines: The evolutionary origins and incredible disparity of deuterostomes revealed by fossils, genes, and development","volume":"98","author":"Nanglu","year":"2023","journal-title":"Biol. Rev."},{"key":"2026091109313823800_JEB253087C19","doi-asserted-by":"publisher","first-page":"274","DOI":"10.1002\/jez.b.21063","article-title":"The new head hypothesis revisited","volume":"304","author":"Northcutt","year":"2005","journal-title":"J. Exp. Zool. B Mol. Dev. Evol."},{"key":"2026091109313823800_JEB253087C20","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1007\/BF00310102","article-title":"The ultrastructure of the blood vessels of Branchiostoma lanceolatum (Pallas) (Cephalochordata). I. Relations between blood vessels, epithelia, basal laminae and \u2018connective tissue","volume":"97","author":"Rahr","year":"1981","journal-title":"Zoomorph"},{"key":"2026091109313823800_JEB253087C21","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1007\/978-90-481-2767-2_10","article-title":"Regeneration in hemichordates and echinoderms","volume-title":"Stem Cells in Marine Organisms","author":"Rychel","year":"2009"},{"key":"2026091109313823800_JEB253087C22","doi-asserted-by":"publisher","first-page":"699","DOI":"10.1038\/s41586-022-05331-7","article-title":"Ion regulation at gills precedes gas exchange and the origin of vertebrates","volume":"610","author":"Sackville","year":"2022","journal-title":"Nature"},{"key":"2026091109313823800_JEB253087C23","doi-asserted-by":"publisher","first-page":"1856","DOI":"10.1242\/jeb.118851","article-title":"The effects of temperature on aerobic metabolism: towards a mechanistic understanding of the responses of ectotherms to a changing environment","volume":"218","author":"Schulte","year":"2015","journal-title":"J. Exp. Biol."},{"key":"2026091109313823800_JEB253087C24","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1038\/46965","article-title":"Lower Cambrian vertebrates from south China","volume":"402","author":"Shu","year":"1999","journal-title":"Nature"},{"key":"2026091109313823800_JEB253087C25","doi-asserted-by":"publisher","first-page":"459","DOI":"10.1038\/nature16150","article-title":"Hemichordate genomes and deuterostome origins","volume":"527","author":"Simakov","year":"2015","journal-title":"Nature"},{"key":"2026091109313823800_JEB253087C26","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1111\/jfb.12797","article-title":"Design and setup of intermittent-flow respirometry system for aquatic organisms","volume":"88","author":"Svendsen","year":"2016","journal-title":"J. Fish. Biol."},{"key":"2026091109313823800_JEB253087C27","doi-asserted-by":"publisher","first-page":"118","DOI":"10.2307\/1539342","article-title":"Regeneration of the enteropneust, Saccoglossus kowalevskii","volume":"120","author":"Tweedell","year":"1961","journal-title":"Biol. Bull."},{"key":"2026091109313823800_JEB253087C28","doi-asserted-by":"publisher","first-page":"399","DOI":"10.1016\/0043-1354(78)90107-0","article-title":"Ammonia determination based on indophenol formation with sodium salicylate","volume":"12","author":"Verdouw","year":"1978","journal-title":"Water. Res."},{"key":"2026091109313823800_JEB253087C29","doi-asserted-by":"publisher","first-page":"1865","DOI":"10.1098\/rspb.2002.2104","article-title":"New evidence on the anatomy and phylogeny of the earliest vertebrates","volume":"269","author":"Xian-guang","year":"2002","journal-title":"Proc. R. Soc. Lond. B Biol. Sci."}],"container-title":["Journal of Experimental Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.biologists.com\/jeb\/article-pdf\/doi\/10.1242\/jeb.253087\/3713606\/jeb253087.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/jeb\/article-pdf\/doi\/10.1242\/jeb.253087\/3717110\/jeb253087.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/jeb\/article-pdf\/doi\/10.1242\/jeb.253087\/3717110\/jeb253087.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,11]],"date-time":"2026-09-11T13:31:43Z","timestamp":1789133503000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/jeb\/article\/229\/17\/jeb253087\/372859\/Gills-are-not-the-primary-site-of-gas-exchange-in"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,11]]},"references-count":30,"journal-issue":{"issue":"17","published-print":{"date-parts":[[2026,9,15]]}},"URL":"https:\/\/doi.org\/10.1242\/jeb.253087","relation":{},"ISSN":["0022-0949","1477-9145"],"issn-type":[{"value":"0022-0949","type":"print"},{"value":"1477-9145","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,11]]},"article-number":"jeb253087"}}