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. 2011;6(12):e28183.
doi: 10.1371/journal.pone.0028183. Epub 2011 Dec 2.

Oxygen as a driver of early arthropod micro-benthos evolution

Mark Williams  1 , Jean Vannier, Laure Corbari, Jean-Charles Massabuau
Affiliations

Oxygen as a driver of early arthropod micro-benthos evolution

Mark Williams et al. PLoS One. 2011.

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 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.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Respiration in water-breathers from simple gaseous diffusion (1) to ventilatory and circulatory convection (5).
PwO2, PeO2, PcellO2, Pw′O2, PaO2, PvO2 correspond to the partial pressure of oxygen in water, in the extracellular medium, at cell level, within external chamber (e.g. branchial chamber), in arterial hemolymph, and in venous hemolymph. Today, the PO2 in the blood and tissues of water-breathing animals (see for a review), is remarkably low, ranging between 1 and 3 kPa and is largely independent of ambient PO2. PcellO2 results from the equilibrium between O2 supply and O2 consumption (90% by mitochondria). PwO2>Pw′O2>PaO2>PeO2>PcellO2.
Figure 2
Figure 2. External respiratory features of Cambrian arthropods.
A, B, Waptia fieldensis Walcott from the middle Cambrian Burgess Shale, British Columbia, Canada, USNM 138231 with trunk appendages bearing gill-like feature, dorsal view and close-up. C, Naraoia longicaudata Zhang and Hou from the early Cambrian Maotianshan Shale, Yunnan Province, China, NIGPAS 115315, biramous appendage with numerous gill-like filaments attached to exopodial branch. Scale bars: 1 cm in A and 1 mm in B and C.
Figure 3
Figure 3. Chronostratigraphy for the Cambrian.
Correlation of regional stratigraphies (modified from [58]) provides the key to understanding the bradoriid and phosphatocopid ranges reconstructed for Figure 4.
Figure 4
Figure 4. Temporal distribution of Cambrian arthropods conventionally assigned to the Bradoriida and Phosphatocopida.
Bradoriid ranges are compiled from , , , and references therein, representing a global dataset. Thick lines indicate definite ranges, whilst thin lines represent a questionable or imprecisely defined range. Only data from and are used to reconstruct the ranges of Bradoriida from China. The phosphatocopid data are from China , , Britain , Scandinavia and north Germany , , , , , , , , : phosphatocopids are also known from the Antarctic , North America , Australia and Kazakhstan . The Borregård Member of Bornholm (equivalent to the Exsulans Limestone) was originally identified as the oldest horizon in Scandinavia with the phosphatocopids Hesslandona, Vestrogothia, Bidimorpha and Falites . The Borregård Member is equivalent to the P. gibbus Biozone of uppermost Stage 5 , . However, later the same author [82, p. 887] referred the material of to the ‘Andrarum Limestone Breccia’, a horizon equivalent to the P. forchhammeri Biozone. Accordingly, we take the lower ranges of these phosphatocopids as Guzhangian. Our range for Waldoria includes material referred to Falidoria in . We plot genera as a proxy for species diversity. This is reasonable given that most bradoriid genera contain only between 1 and 3 species. Exceptions to this include Cambria, Liangshanella, Anabarochilina, Indiana and Hipponicharion. For phosphatocopids, a multitude of species are referred to Dabashanella, but most of these are synonyms of D. hemicyclica . Later Cambrian phosphatocopids including Falites, Cyclotron, Hesslandona, Vestrogothia and Bidimorpha all contain more than 3 species , emphasising the diversity of Guzhangian and Pabian phosphatocopid assemblages. Also shown are the major Carbon Isotope Excursions (CIEs) after , and oxygen levels reconstructed from . For the latter, the red line represents the oxygen reconstruction (with error shown in pink envelope) of and the blue line [with error envelope] is the Berner reconstruction quoted therein. In the text and figures we use the terms ‘early’, ‘middle’ and ‘late’ Cambrian informally to denote Cambrian Series 1 and 2 combined, Series 3, and Series 4 respectively. Note that some authors would tentatively include Epactridion, Dielymella, Liangshanella, Flemingopsis, Alutella, Oepikaluta and Gladioscutum in the Phosphatocopida. For morphological reasons outlined in we include these taxa within the Bradoriida. Abbreviations for CIEs are: BAsal Cambrian Carbon isotope Excursion (BACE); ZHUjiaqing Carbon isotope Excursion (ZHUCE); SHIyantou Carbon isotope Excursion (SHICE); Cambrian Arthropod Radiation isotope Excursion (CARE); MIngxinsi Carbon Isotope Excursion (MICE); Archaeocyathid Extinction Carbon isotope Excursion (AECE); Redlichiid-Olenellid Extinction Carbon isotope Excursion (ROECE); Drumian Carbon isotope Excursion (DICE); StePtoean Carbon Isotope Excursion (SPICE); Top of Cambrian Excursion (TOCE).
Figure 5
Figure 5. Respiration and circulation in Recent myodocopid ostracods.
Simplified transverse section through anterior body and carapace: hemolymph route indicated by the red arrows. Hemolymph sinuses in pink (see Figure 6). Gaseous diffusion through the inner lamella of the carapace (see [51]) indicated by yellow arrows. The soft body, with or without gills or gas-exchange area, is bathing in the domiciliary cavity ventilated by the beating activity of two ventilatory plates.
Figure 6
Figure 6. General morphology of Recent ostracods exemplified by myodocopids.
A, B, Vargula hilgendorfii (Müller), left lateral view of live female carrying embryos in her domiciliar cavity (carapace translucent) and lateral view of left valve in transmitted light showing the gas-exchange area, an integumental hemolymph network (yellow arrows indicate hemolymph circulation). C, Azygocypridina sp. from New Caledonia, France. Scanning electron micrograph showing appendages, left valve removed, including the ventilatory plates (courtesy of Vincent Perrier). D, E, transverse section through the carapace of Vargula hilgendorfii showing hemolymph sinuses, stained microtome serial section and scanning electron micrograph, respectively (see [51], [76]). Scale bars: 1 mm in A–C, and 20 µm in D and E. ef, epipodial fan for ventilation; hs, hemolymph sinus; il, inner lamella; ol, outer lamella.
Figure 7
Figure 7. Recent ostracods with gills.
Leuroleberis surugaensis Hiruta from Japan. A–C, scanning electron micrographs showing book gills in the branchial cavities, left lateral and posterior views. D, gill in transmitted light showing internal hemolymph sinuses. E, F, stained microtome serial sections, showing 8 pairs of gills on both sides of the soft body and detailed features through individual gills (e.g. hemolymph sinuses). Scale bars: 1 mm in A and B, 500 µm in D and E, 200 µm in C, and 50 µm in F. bg, book gill (integumental lamina attached to thoracic wall); ef, epipodial fan for ventilation; hs, hemolymph sinus in book gills.
Figure 8
Figure 8. General morphology of phosphatocopid arthropods.
A, Hesslandona angustata from the late Cambrian of western Hunan, China, ventral view of complete specimen with phosphatised appendages (see [77]). B, Klausmuelleria salopiensis Siveter, Waloszek & Williams from the Protolenus-Strenuella Limestone, early Cambrian (Series 2), Shropshire England, reconstruction of appendages in ventral view (courtesy of Dieter Waloszek, Ulm). Reconstruction is based on a specimen 0.34 mm long . C, Vestrogothia spinata Müller, from the late Cambrian “Orsten” of Sweden, three-dimensional model, lateral and frontal views (courtesy of Joachim Haug). Scale bar: 100 µm.
Figure 9
Figure 9. General morphology of bradoriid arthropods.
A, B, Kunmingella douvillei (Mansuy) from the early Cambrian Maotianshan Shale, Yunnan Province, China, dorsal views of two specimens showing bivalved open carapace in “butterfly” position and posterior appendages, Chen Jun-Yuan's personal collections, Chengjiang and RCCBYU 10258, respectively (B, courtesy of Derek Siveter). C, Anabarochilina sp., middle Cambrian from Kazakhstan, PIN N4343/55, partly exfoliated right valve. D, Anabarochilina primordialis (Linnarsson), middle Cambrian from Västergötland, Sweden, SGU 8662, partly exfoliated right valve. E, Tsunyiella gridinae Melnikova from the early Cambrian (Atdabanian) of North Central Kazakhstan, PIN N4343/12, left valve, internal mould. F, Cambria melnikovi Ivanova from the early Cambrian (Atdabanian) of the eastern part of Siberia, Russia, PIN N2175/1, largely exfoliated left valve. Small white arrows indicate supposed integumental hemolymph networks (see [51]). All scale bars: 1 mm. For repositories of figured specimens see , .
Figure 10
Figure 10. Early ostracods from the Cambrian and Ordovician.
A, Kimsella luciae Salas, Vannier & Williams, lateral view of right valve. Tremadocian, lower part of the Parcha Formation, Abra de Sococha Section, Province of Salta, Argentina, CORD-MP 11186. B, Altajanella costulata Melnikova, lateral view of right valve. Late Cambrian, Tandoshka Formation, Gorny Altay, PIN N4346/1. C, Vojbokalina magnifica Melnikova, left lateral view of carapace. Middle Cambrian, Leningrad Region, Russia, PIN N4341/6. D, Nanopsis coquina Salas, Vannier & Williams, lateral view of left valve. Tremadocian, Upper Member of the Coquena Formation, Quebrada Chalala Section, Cordillera Oriental, Argentina, CORD-MP 11179. Scale bars are: 100 µm. For repositories of figured specimens see .
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