Oxygen as a Driver of Early Arthropod Micro-Benthos Evolution Mark Williams1*, Jean Vannier2, Laure Corbari3, Jean-Charles Massabuau4 1 Department of Geology, University of Leicester, Leicester, United Kingdom, 2 UMR 5276 CNRS, Laboratoire de Ge´ologie de Lyon: Terre, Plane`tes, Environnement, Universite´ Lyon 1, Villeurbanne, France, 3 UMR 7138 CNRS, Syste´matique, Adaptation, Evolution, Muse´um National d’Histoire Naturelle, Paris, France, 4 UMR 5805-EPOC CNRS, Universite´ Bordeaux 1, Arcachon, France Abstract Background: We examine the physiological and lifestyle adaptations which facilitated the emergence of ostracods as the numerically dominant Phanerozoic bivalve arthropod micro-benthos. Methodology/Principal Findings: The PO2 of modern normoxic seawater is 21 kPa (air-equilibrated water), a level that would cause cellular damage if found in the tissues of ostracods and much other marine fauna. The PO2 of most aquatic breathers at the cellular level is much lower, between 1 and 3 kPa. Ostracods avoid oxygen toxicity by migrating to waters which are hypoxic, or by developing metabolisms which generate high consumption of O2. Interrogation of the Cambrian record of bivalve arthropod micro-benthos suggests a strong control on ecosystem evolution exerted by changing seawater O2 levels. The PO2 of air-equilibrated Cambrian-seawater is predicted to have varied between 10 and 30 kPa. Three groups of marine shelf-dwelling bivalve arthropods adopted different responses to Cambrian seawater O2. Bradoriida evolved cardiovascular systems that favoured colonization of oxygenated marine waters. Their biodiversity declined during intervals associated with black shale deposition and marine shelf anoxia and their diversity may also have been curtailed by elevated late Cambrian (Furongian) oxygen-levels that increased the PO2 gradient between seawater and bradoriid tissues. Phosphatocopida responded to Cambrian anoxia differently, reaching their peak during widespread seabed dysoxia of the SPICE event. They lacked a cardiovascular system and appear to have been adapted to seawater hypoxia. As latest Cambrian marine shelf waters became well oxygenated, phosphatocopids went extinct. Changing seawater oxygen-levels and the demise of much of the seabed bradoriid micro-benthos favoured a third group of arthropod micro-benthos, the ostracods. These animals adopted lifestyles that made them tolerant of changes in seawater O2. Ostracods became the numerically dominant arthropod micro-benthos of the Phanerozoic. Conclusions/Significance: Our work has implications from an evolutionary context for understanding how oxygen-level in marine ecosystems drives behaviour. Citation: Williams M, Vannier J, Corbari L, Massabuau J-C (2011) Oxygen as a Driver of Early Arthropod Micro-Benthos Evolution. PLoS ONE 6(12): e28183. doi:10.1371/journal.pone.0028183 Editor: Anna Stepanova, Paleontological Institute of Russian Academy of Science, United States of America Received July 20, 2011; Accepted November 2, 2011; Published December 2, 2011 Copyright: 2011 Williams et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This study was supported by Agence Nationale de la Recherche [ANR] grant ORECO-BLAN06-3-136294 ‘RALI’ The Rise of Animal Life [http://www. agence-nationale-recherche.fr/Intl]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: mri@le.ac.uk Introduction Molecular, geochemical and fossil evidence suggests that the first animals (eumetazoans) appeared during the late Precambrian [1] when atmospheric PO2 was between 8 and 15 kPa [2] com- pared to the modern 21 kPa, and the oceans were therefore less oxygenated than present. Recent geochemical studies indicate that atmospheric oxygen-levels increased during the late Precambrian, to reach high levels by the late Cambrian, perhaps as high as 30 kPa for several million years during the Furongian [3]. Whereas the earliest animals must have developed physiologies that allowed them to respire in benthic or pelagic environments where oxygen was less abundant, those that developed in the later Cambrian had to cope with similar or higher than present oxygen levels. Today, the PO2 in the blood and tissues of water-breathing aquatic animals (e.g. crustaceans, fish and molluscs; see [4,5]), is remarkably low, ranging between 1 and 3 kPa and is largely independent of ambient PO2 ([4]; Figure 1). In mammalian tissues, the most frequently measured PO2 is also between 1 and 3 kPa [6]. Massabuau [4,7] proposed that this widespread cellular oxygena- tion status using low oxygen level was a ‘memory’ of conditions that prevailed in the early stages of animal evolution when ambient oxygen levels were lower. The postulate is that maintaining cellular oxygenation at a very low level independent of the changes in ambient oxygenation that occurred throughout the Phanerozoic seems to have been a vital constraint to most aquatic animals, and is important in all animals for avoiding oxygen toxicity that would damage cell membranes and cellular machinery. Gaseous diffusion through the integument was probably sufficient for the smallest organisms relying on O2-metabolism to transport oxygen to their tissues, providing there was a sufficient gradient between the external medium and the tissues (PO2 in sea water .PO2 in tissues). This simple respiratory mode that requires no specialized organs may also have been used by larger sheet-like Ediacaran organisms PLoS ONE | www.plosone.org 1 December 2011 | Volume 6 | Issue 12 | e28183