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

Arachnids are the second most successful terrestrial animal group after insects [1] and were one of the first arthropod clades to successfully invade land [2]. 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 [3], 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 [4-6], are known to have undergone major macroecological shifts in transitioning from marine to freshwater environments during the Devonian [7, 8]. Discoveries of apparently subaerial eurypterid trackways [9, 10] have led to the suggestion that eurypterids were even able to venture on land and possibly breathe air [11]. However, modern horseshoe crabs undertake amphibious excursions onto land to reproduce [12], 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 [13], 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.