A new Devonian euthycarcinoid reveals the use of different respiratory strategies during the marine-to-terrestrial transition in the myriapod lineage.

Pierre Gueriau,Roy A Wogelius,James C Lamsdell,Victoria M Egerton,Julien Denayer,Uwe Bergmann,Phillip L Manning,Loïc Bertrand

doi:10.1098/rsos.201037

Abstract

Myriapods were, together with arachnids, the earliest animals to occupy terrestrial ecosystems, by at least the Silurian. The origin of myriapods and their land colonization have long remained puzzling until euthycarcinoids, an extinct group of aquatic arthropods considered amphibious, were shown to be stem-group myriapods, extending the lineage to the Cambrian and evidencing a marine-to-terrestrial transition. Although possible respiratory structures comparable to the air-breathing tracheal system of myriapods are visible in several euthycarcinoids, little is known about the mechanism by which they respired. Here, we describe a new euthycarcinoid from Upper Devonian alluvio-lagoonal deposits of Belgium. Synchrotron-based elemental X-ray analyses were used to extract all available information from the only known specimen. Sulfur X-ray fluorescence (XRF) mapping and spectroscopy unveil sulfate evaporation stains, spread over the entire slab, suggestive of a very shallow-water to the terrestrial environment prior to burial consistent with an amphibious lifestyle. Trace metal XRF mapping reveals a pair of ventral spherical cavities or chambers on the second post-abdominal segment that do not compare to any known feature in aquatic arthropods, but might well play a part in air-breathing. Our data provide additional support for amphibious lifestyle in euthycarcinoids and show that different respiratory strategies were used during the marine-to-terrestrial transition in the myriapod lineage.

Highlights

The establishment of complex terrestrial ecosystems is a critical event in the history of life, which imposed multiple constraints upon the water-to-land transition of aquatic organisms, such as osmoregulation, respiration and reproduction in air, as well as locomotion without the help of buoyancy, and exposure to ultraviolet radiation (e.g. [1] and references therein)
Ericixerxes potii gen. et sp. nov. is only the second Devonian euthycarcinoid known with H. rhyniensis from the Early Devonian Rhynie and Windyfield cherts
The peculiarity of E. potii gen. et sp. nov. is the pair of quite large, ventral spherical cavities or chambers on the second post-abdominal segment revealed by the distribution of As

Summary

Introduction

The establishment of complex terrestrial ecosystems (terrestrialization) is a critical event in the history of life, which imposed multiple constraints upon the water-to-land transition of aquatic organisms, such as osmoregulation (water balance to avoid dehydration), respiration and reproduction in air, as well as locomotion without the help of buoyancy, and exposure to ultraviolet radiation (e.g. [1] and references therein). Air-breathing is more challenging, as the gill-modified appendages of aquatic arthropods are not rigid and are highly vulnerable to dehydration. Pulmonate arachnids (e.g. scorpions, whip scorpions and spiders) and (semi-)terrestrial crabs have internalized and/or adapted their gills, respectively, into book lungs found inside open ventral abdominal air-filled cavities ([1,3] and references therein), and through gill stiffening and gill chamber enlargement and/or smooth to highly convoluted lining Terrestrial isopods (including woodlice) use their gills, formed by part of their abdominal legs (endopods), for respiration; some groups modify exopods into invaginations to form lung-like structures ([1,3] and references therein). Myriapods (e.g. centipedes and millipedes), apulmonate arachnids (e.g. harvestmen, mites, ticks and pseudoscorpions) and terrestrial hexapods (bristletails, silverfish and insects) except for some springtails (which exchange gases by diffusion across the cuticle, a capability linked to their small size), independently evolved an entirely new respiratory system, the tracheal system, which consists of small pores (the spiracles) opening on an extensive and elaborate system of air-tubes (the tracheae)

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Conclusion