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Air Breathing in an Exceptionally Preserved 340-Million-Year-Old Sea Scorpion

2020; Elsevier BV; Volume: 30; Issue: 21 Linguagem: Inglês

10.1016/j.cub.2020.08.034

1879-0445

James C. Lamsdell, Victoria E. McCoy, Opal Perron-Feller, Melanie J. Hopkins,

Marine Invertebrate Physiology and Ecology

Arachnids are the second most successful terrestrial animal group after insects [1Purvis A. Hector A. Getting the measure of biodiversity.Nature. 2000; 405: 212-219Crossref PubMed Scopus (738) Google Scholar] and were one of the first arthropod clades to successfully invade land [2Dunlop J.A. Tetlie O.E. Prendini L. Reinterpretation of the Silurian scorpion Proscorpius osborni (Whitfield): integrating data from Palaeozoic and Recent scorpions.Palaeontology. 2008; 51: 303-320Crossref Scopus (40) Google Scholar]. Fossil evidence for this transition is limited, with the majority of arachnid clades first appearing in the terrestrial fossil record. Furthermore, molecular clock dating has suggested a Cambrian-Ordovician terrestrialization event for arachnids [3Lozano-Fernandez J. Tanner A.R. Puttick M.N. Vinther J. Edgecombe G.D. Pisani D. A Cambrian–Ordovician terrestrialization of arachnids.Front. Genet. 2020; 11: 182Crossref PubMed Scopus (8) Google Scholar], some 60 Ma before their first fossils in the Silurian, although these estimates assume that arachnids evolved from a fully aquatic ancestor. Eurypterids, the sister clade to terrestrial arachnids [4Garwood R.J. Dunlop J. Three-dimensional reconstruction and the phylogeny of extinct chelicerate orders.PeerJ. 2014; 2: e641Crossref PubMed Scopus (64) Google Scholar, 5Lamsdell J.C. Briggs D.E.G. Liu H.P. Witzke B.J. McKay R.M. A new Ordovician arthropod from the Winneshiek Lagerstätte of Iowa (USA) reveals the ground plan of eurypterids and chasmataspidids.Naturwissenschaften. 2015; 102: 63Crossref PubMed Scopus (25) Google Scholar, 6Aria C. Caron J.-B. A middle Cambrian arthropod with chelicerae and proto-book gills.Nature. 2019; 573: 586-589Crossref PubMed Scopus (13) Google Scholar], are known to have undergone major macroecological shifts in transitioning from marine to freshwater environments during the Devonian [7Lamsdell J.C. Braddy S.J. Cope’s Rule and Romer’s theory: patterns of diversity and gigantism in eurypterids and Palaeozoic vertebrates.Biol. Lett. 2010; 6: 265-269Crossref PubMed Scopus (54) Google Scholar, 8Lamsdell J.C. Selden P.A. From success to persistence: identifying an evolutionary regime shift in the diverse Paleozoic aquatic arthropod group Eurypterida, driven by the Devonian biotic crisis.Evolution. 2017; 71: 95-110Crossref PubMed Scopus (26) Google Scholar]. Discoveries of apparently subaerial eurypterid trackways [9Whyte M.A. Palaeoecology: a gigantic fossil arthropod trackway.Nature. 2005; 438: 576Crossref PubMed Scopus (20) Google Scholar, 10Draganits E. Braddy S.J. Briggs D.E.G. A Gondwanan coastal arthropod ichnofauna from the Muth Formation (Lower Devonian, Northern India): paleoenvironment and tracemaker behavior.Palaios. 2001; 16: 126-147Crossref Scopus (64) Google Scholar] have led to the suggestion that eurypterids were even able to venture on land and possibly breathe air [11Selden P.A. Eurypterid respiration.Philos. Trans. R. Soc. Lond. B. 1985; 309: 219-226Crossref Google Scholar]. However, modern horseshoe crabs undertake amphibious excursions onto land to reproduce [12Botton M.L. Tankersley R.A. Loveland R.E. Developmental ecology of the American horseshoe crab Limulus polyphemus.Curr. Zool. 2010; 56: 550-562Crossref Scopus (35) Google Scholar], rendering trace fossil evidence alone inconclusive. Here, we present details of the respiratory organs of Adelophthalmus pyrrhae sp. nov. from the Carboniferous of Montagne Noire, France [13Manning P.L. Dunlop J.A. The respiratory organs of eurypterids.Palaeontology. 1995; 38: 287-297Google Scholar], revealed through micro computed tomography (μ-CT) imaging. Pillar-like trabeculae on the dorsal surface of each gill lamella indicate eurypterids were capable of subaerial breathing, suggesting that book gills are the direct precursors to book lungs while vascular ancillary respiratory structures known as Kiemenplatten represent novel air-breathing structures. The discovery of air-breathing structures in eurypterids indicates that characters permitting terrestrialization accrued in the arachnid stem lineage and suggests the Cambrian-Ordovician ancestor of arachnids would also have been semi-terrestrial.