Oxygen as a Driver of Early Arthropod Micro-Benthos Evolution

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 PO(2) 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 PO(2) 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 O(2). Interrogation of the Cambrian record of bivalve arthropod micro-benthos suggests a strong control on ecosystem evolution exerted by changing seawater O(2) levels. The PO(2) 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 O(2). 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 PO(2) 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 O(2). 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

Ediacaran skeletal Metazoans: affinities, ecology and the role of oxygenation

The evolution of the Metazoa is among the greatest success stories in Earth history. From modest origins, probably in the Cryogenian (~720 - 635 Ma), metazoans had acquired hard parts, and a vast range of life strategies and body plans by the middle Cambrian (around 520 Ma). This leaves a long delay between the origin of the Metazoa and their rise to ecological dominance. A popular explanatory hypothesis for this delay is that atmospheric oxygen levels, low in the Proterozoic (< 0.001 % PAL), began to rise towards modern levels towards the end of the Neoproterozoic. Among the earliest known putative metazoans are Namacalathus, Namapoikia and Cloudina, calcified marine invertebrates abundant in the latest Ediacaran (~ 548-541 Ma) Nama Group, Namibia. Although they were pioneers of metazoan biomineralisation, little is known of their affinities or palaeocology. The Nama Group, a well-characterised, relatively undeformed mixed carbonate and siliciclastic succession, provides a rare opportunity to investigate the palaeoecology of these important organisms in their environmental context. New geochemical data from the Nama Group confirm the heterogeneity of Ediacaran redox conditions. These contextualise in situ fossil assemblages which reveal diverse ecological strategies among the calcified metazoans of the Nama Group, and offer constraints on their affinities. Based on its large size (< 1 m), modular body plan and internal structure of interlinked tubules, Namapoikia was a long-lived specialist and possible Poriferan. I show that Namapoikia colonised both lithified and living microbial substrates in oxic, mid-ramp reef crypts. By contrast, size and occurrence data show that Namacalathus was an environmental generalist, forming large, thick aggregations in persistently oxic, mid-ramp reef environments but opportunistically exploiting the transiently oxic, inner ramp setting. Bilaterally symmetrical, asexual budding and a microlamellar skeletal ultrastructure suggest that Namacalathus may have been an early lophophorate, and had flexible growth depending on environmental setting, showing a cup diameter of 2 – 35 mm, and size distributions varying with substrate type, redox and water depth. In oxic mid-ramp reefs, Cloudina constructed large (> 20 m) reefs showing mutual attachment and consistent orientation in life position, making it the earliest known reef-building metazoan and suggesting that it was a passive suspension feeder. I further present food webs based on fossil assemblages from Ediacaran to Cambrian Stage 4 carbonate successions and evaluate their usefulness in tracking metazoan trophic diversification in the early Cambrian. Ediacaran redox conditions were a major control on the ecologies of the earliest metazoans. A requirement for oxygen made persistently oxic conditions a prerequisite for complex and long-lived ecologies, while highly flexible life strategies were used to exploit changeable environments. Ediacaran metazoans represent a phylogenetic and ecological foreshadowing of the complexity of the Phanerozoic, but it was not until much later that the Metazoa would attain their evolutionary potential

Life Cycle and Morphology of a Cambrian Stem-Lineage Loriciferan

Cycloneuralians form a rich and diverse element within Cambrian assemblages of exceptionally preserved fossils. Most resemble priapulid worms whereas other Cycloneuralia (Nematoda, Nematomorpha, Kinorhyncha, Loricifera), well known at the present day, have little or no fossil record. First reports of Sirilorica Peel, 2010 from the lower Cambrian Sirius Passet fauna of North Greenland described a tubular lorica covering the abdomen and part of a well developed introvert with a circlet of 6 grasping denticles near the lorica. The introvert is now known to terminate in a narrow mouth tube, while a conical anal field is also developed. Broad muscular bands between the plates in the lorica indicate that it was capable of movement by rhythmic expansion and contraction of the lorica. Sirilorica is regarded as a macrobenthic member of the stem-lineage of the miniaturised, interstitial, present day Loricifera. Like loriciferans, Sirilorica is now known to have grown by moulting. Evidence of the life cycle of Sirilorica is described, including a large post-larval stage and probably an initial larva similar to that of the middle Cambrian fossil Orstenoloricus shergoldii