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Annual Review of Ecology, Evolution, and Systematics

Volume 46, 2015

The Ecological Physiology of Earth's Second Oxygen Revolution

Abstract

Living animals display a variety of morphological, physiological, and biochemical characters that enable them to live in low-oxygen environments. These features and the organisms that have evolved them are distributed in a regular pattern across dioxygen (O) gradients associated with modern oxygen minimum zones. This distribution provides a template for interpreting the stratigraphic covariance between inferred Ediacaran-Cambrian oxygenation and early animal diversification. Although Cambrian oxygen must have reached 10–20% of modern levels, sufficient to support the animal diversity recorded by fossils, it may not have been much higher than this. Today's levels may have been approached only later in the Paleozoic Era. Nonetheless, Ediacaran-Cambrian oxygenation may have pushed surface environments across the low, but critical, physiological thresholds required for large, active animals, especially carnivores. Continued focus on the quantification of the partial pressure of oxygen (O) in the Proterozoic will provide the definitive tests of oxygen-based coevolutionary hypotheses.

Keyword(s): animal evolution, Cambrian, Ediacaran, environmental change, paleontology
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2015-12-04
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Literature Cited

  1. Alexander RMN. 1971. Size and Shape London: Edward Arnold
  2. Algeo TJ, Rowe H. 2012. Paleoceanographic applications of trace-metal concentration data. Chem. Geol. 324–325:6–18 [Google Scholar]
  3. Barghoorn ES, Tyler SA. 1965. Microorganisms from the Gunflint Chert. Science 147:563–75 [Google Scholar]
  4. Bergman NM, Lenton TM, Watson AJ. 2004. COPSE: A new model of biogeochemical cycling over Phanerozoic time. Am. J. Sci. 304:397–437 [Google Scholar]
  5. Berry WBN, Wilde P. 1978. Progressive ventilation of the oceans—an explanation for the distribution of the lower Paleozoic black shales. Am. J. Sci. 278:257–75 [Google Scholar]
  6. Bograd SJ, Castro CG, Di Lorenzo E, Palacios DM, Bailey H. et al. 2008. Oxygen declines and the shoaling of the hypoxic boundary in the California Current. Geophys. Res. Lett. 35:L12607 [Google Scholar]
  7. Braeckman U, Vanaverbeke J, Vincx M, van Oevelen D, Soetaert K. 2013. Meiofauna metabolism in suboxic sediments: currently overestimated. PLOS ONE 8:e59289 [Google Scholar]
  8. Breur ER, Law GTW, Woulds C, Cowie GL, Shimmield GB. et al. 2009. Sedimentary oxygen consumption and microdistribution at sites across the Arabian Sea oxygen minimum zone (Pakistan margin). Deep-Sea Res. II 56:296–304 [Google Scholar]
  9. Budd GE, Jensen S. 2000. A critical reappraisal of the fossil record of the bilaterian phyla. Biol. Rev. 75:253–95 [Google Scholar]
  10. Burd BJ. 1988. Comparative gill characteristics of Munida quadrispina (Decapoda, Galatheidae) from different habitat oxygen conditions. Can. J. Zool. 66:2320–23 [Google Scholar]
  11. Butterfield NJ. 1997. Plankton ecology and the Proterozoic-Phanerozoic transition. Paleobiology 23:247–62 [Google Scholar]
  12. Butterfield NJ. 2007. Macroevolution and macroecology through deep time. Palaeontology 50:41–55 [Google Scholar]
  13. Butterfield NJ. 2009. Oxygen, animals and oceanic ventilation: an alternative view. Geobiology 7:1–7 [Google Scholar]
  14. Campbell IH, Squire RJ. 2010. The mountains that triggered the Late Neoproterozoic increase in oxygen: the second great oxidation event. Geochim. Cosmochim. Acta 74:4187–206 [Google Scholar]
  15. Canfield DE, Poulton SW, Knoll AH, Narbonne GM, Ross G. et al. 2008. Ferruginous conditions dominated later Neoproterozoic deep-water chemistry. Science 321:949–52 [Google Scholar]
  16. Canfield DE, Poulton SW, Narbonne GM. 2007. Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315:92–95 [Google Scholar]
  17. Canfield DE, Teske A. 1996. Late Proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies. Nature 382:127–32 [Google Scholar]
  18. Canfield DE, Thamdrup B. 2009. Towards a consistent classification scheme for geochemical environments, or, why we wish the term ‘suboxic’ would go away. Geobiology 7:385–92 [Google Scholar]
  19. Cawood PA, Hawkesworth CJ. 2014. Earth's middle age. Geology 42:503–6 [Google Scholar]
  20. Childress JJ. 1995. Are there physiological and biochemical adaptations of metabolism in deep-sea animals?. Trends Ecol. Evol. 10:130–36 [Google Scholar]
  21. Cloud PE. 1968. Atmospheric and hydrospheric evolution on primitive Earth. Science 160:729–36 [Google Scholar]
  22. Costa DP, Sinervo B. 2004. Field physiology: physiological insights from animals in nature. Annu. Rev. Physiol. 66:209–38 [Google Scholar]
  23. Crowe SA, Dossing LN, Beukes NJ, Bau M, Kruger SJ. et al. 2013. Atmospheric oxygenation three billion years ago. Nature 501:535–38 [Google Scholar]
  24. Dahl TW, Canfield DE, Rosing MT, Frei RE, Gordon GW. et al. 2011. Molybdenum evidence for expansive sulfidic water masses in ∼750 Ma oceans. Earth Planet. Sci. Lett. 311:264–74 [Google Scholar]
  25. Dahl TW, Hammarlund EU, Anbar AD, Bond DPG, Gill BC. et al. 2010. Devonian rise in atmospheric oxygen correlated to the radiation of terrestrial plants and large predatory fish. PNAS 107:17911–15 [Google Scholar]
  26. Danovaro R, Dell'Anno A, Pusceddu A, Gambi C, Heiner I, Kristensen RM. 2010. The first metazoa living in permanently anoxic conditions. BMC Biol. 8:30 [Google Scholar]
  27. Davis DW, Williams IS, Krogh TE. 2003. Historical development of zircon geochronology. Rev. Mineral. Geochem. 53:145–81 [Google Scholar]
  28. Derry LA, Kaufman AJ, Jacobsen SB. 1992. Sedimentary cycling and environmental change in the Late Proterozoic: evidence from stable and radiogenic isotopes. Geochim. Cosmochim. Acta 56:1317–29 [Google Scholar]
  29. Dzik J. 2007. The Verdun syndrome: simultaneous origin of protective armour and infaunal shelters at the Precambrian-Cambrian transition. Geol. Soc. Lond. Spec. Publ. 286:405–14 [Google Scholar]
  30. Emerson SR, Huested SS. 1991. Ocean anoxia and the concentrations of molybdenum and vanadium in seawater. Mar. Chem. 34:177–96 [Google Scholar]
  31. Erwin DH, Laflamme M, Tweedt SM, Sperling EA, Pisani D, Peterson KJ. 2011. The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334:1091–97 [Google Scholar]
  32. Farquhar J, Wing BA. 2003. Multiple sulfur isotopes and the evolution of the atmosphere. Earth Planet. Sci. Lett. 213:1–13 [Google Scholar]
  33. Fedonkin MA, Simonetta A, Ivantsov AY. 2007. New data on Kimberella, the Vendian mollusc-like organism (White Sea region, Russia): palaeoecological and evolutionary implications. Geol. Soc. Spec. Publ. 286:157–79 [Google Scholar]
  34. Fike DA, Grotzinger JP, Pratt LM, Summons RE. 2006. Oxidation of the Ediacaran ocean. Nature 444:744–47 [Google Scholar]
  35. Frei R, Gaucher C, Poulton SW, Canfield DE. 2009. Fluctuations in Precambrian atmospheric oxygenation recorded by chromium isotopes. Nature 461:250–53 [Google Scholar]
  36. Frei R, Gaucher C, Stolper D, Canfield DE. 2013. Fluctuations in late Neoproterozoic atmospheric oxidation: Cr isotope chemostratigraphy and iron speciation of the late Ediacaran lower Arroyo del Soldado Group (Uruguay). Gondwana Res. 23:797–811 [Google Scholar]
  37. Gaidos E, Knoll AH. 2012. Our evolving planet: from the dark ages to an evolutionary renaissance. Frontiers of Astrobiology C Impie, J Lunine, J Funes 132–53 Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  38. Gehling JG, Runnegar BN, Droser ML. 2014. Scratch traces of large Ediacara bilaterian animals. J. Paleontol. 88:284–98 [Google Scholar]
  39. Gill BC, Lyons TW, Saltzman MR. 2007. Parallel, high-resolution carbon and sulfur isotope records of the evolving Paleozoic marine sulfur reservoir. Palaeogeogr. Palaeoclimatol. Palaeoecol. 256:156–73 [Google Scholar]
  40. Gill BC, Lyons TW, Young SA, Kump LR, Knoll AH, Saltzman MR. 2011. Geochemical evidence for widespread euxinia in the later Cambrian ocean. Nature 469:80–83 [Google Scholar]
  41. Gilly WF, Beman JM, Litvin SY, Robison BH. 2013. Oceanographic and biological effects of shoaling of the oxygen minimum zone. Annu. Rev. Mar. Sci. 5:393–420 [Google Scholar]
  42. Gooday AJ, Levin LA, Aranda da Silva A, Bett BJ, Cowie GL. et al. 2009. Faunal responses to oxygen gradients on the Pakistan margin: a comparison of foraminiferans, macrofauna and megafauna. Deep-Sea Res. II 56:488–502 [Google Scholar]
  43. Grieshaber MK, Völkel S. 1998. Animal adaptations for tolerance and exploitation of poisonous sulfide. Annu. Rev. Physiol. 60:33–53 [Google Scholar]
  44. Halverson GP, Hoffman PF, Schrag DP, Maloof AC, Rice AHN. 2005. Toward a Neoproterozoic composite carbon-isotope record. Geol. Soc. Am. Bull. 117:1181–207 [Google Scholar]
  45. Halverson GP, Wade BP, Hurtgen MT, Barovich KM. 2010. Neoproterozoic chemostratigraphy. Precambrian Res. 182:337–50 [Google Scholar]
  46. Hansel CM, Learman DR. 2015. The geomicrobiology of manganese. Erlich's Geomicrobiology HL Ehrlich, DK Newman, A Kappler 347–420 Boca Raton, FL: CRC, 6th ed.. [Google Scholar]
  47. Hardison RC. 1996. A brief history of hemoglobins: plant, animal, protist, and bacteria. PNAS 93:5675–79 [Google Scholar]
  48. Harvey EN. 1911. Studies on the permeability of cells. J. Exp. Zool. 10:507–56 [Google Scholar]
  49. Helly JJ, Levin LA. 2004. Global distribution of naturally occurring marine hypoxia on continental margins. Deep-Sea Res. I 51:1159–68 [Google Scholar]
  50. Hoffmann FG, Opazo JC, Hoogewijs D, Hankeln T, Ebner B. et al. 2012. Evolution of the globin gene family in deuterostomes: lineage-specific patterns of diversification and attrition. Mol. Biol. Evol. 29:1735–45 [Google Scholar]
  51. Hofmann AF, Peltzer ET, Walz PM, Brewer PG. 2011. Hypoxia by degrees: establishing definitions for a changing ocean. Deep-Sea Res. I 58:1212–26 [Google Scholar]
  52. Holland HD. 1962. Model for the evolution of the Earth's atmosphere. Petrologic Studies: A Volume in Honor of A.F. Buddington AEJ Engel, HL James, BF Leonard 447–77 Boulder, CO: Geol. Soc. Am. [Google Scholar]
  53. Holland HD. 2006. The oxygenation of the atmosphere and oceans. Philos. Trans. R. Soc. B 361:903–15 [Google Scholar]
  54. Jacobs DK, Haney TA, Louie KD. 2004. Genes, diversity, and geologic processes on the Pacific coast. Annu. Rev. Earth Planet. Sci. 32:601–52 [Google Scholar]
  55. Jeffreys RM, Levin LA, Lamont PA, Woulds C, Whitcraft CR. et al. 2012. Living on the edge: single-species dominance at the Pakistan oxygen minimum zone boundary. Mar. Ecol. Progr. Ser. 470:79–99 [Google Scholar]
  56. Johnson JE, Gerpheide A, Lamb MP, Fischer WW. 2014. O2 constraints from Paleoproterozoic detrital pyrite and uraninite. Geol. Soc. Am. Bull. 126:813–30 [Google Scholar]
  57. Johnston DT, Poulton SW, Dehler CM, Porter S, Husson J. et al. 2010. An emerging picture of Neoproterozoic ocean chemistry: insights from the Chuar Group, Grand Canyon, USA. Earth Planet. Sci. Lett. 290:64–73 [Google Scholar]
  58. Joydas TV, Damodaran R. 2014. Infaunal macrobenthos of the oxygen minimum zone on the Indian western continental shelf. Mar. Ecol. 35:22–35 [Google Scholar]
  59. Kah LC, Bartley JK. 2011. Protracted oxygenation of the Proterozoic biosphere. Int. Geol. Rev. 53:1424–42 [Google Scholar]
  60. Knoll AH. 2013. Systems paleobiology. Geol. Soc. Am. Bull. 125:3–13 [Google Scholar]
  61. Knoll AH, Sperling EA. 2014. Oxygen and animal evolution. PNAS 111:3907–708 [Google Scholar]
  62. Laakso TA, Schrag DP. 2014. Regulation of atmospheric oxygen during the Proterozoic. Earth Planet. Sci. Lett. 388:81–91 [Google Scholar]
  63. Laflamme M, Xiao S, Kowalewski M. 2009. Osmotrophy in modular Ediacara organisms. PNAS 106:14438–43 [Google Scholar]
  64. Lamont PA, Gage JD. 2000. Morphological responses of macrobenthic polychaetes to low oxygen on the Oman continental slope, NW Arabian Sea. Deep-Sea Res. II 47:9–24 [Google Scholar]
  65. Leavitt WD, Halevy I, Bradley AS, Johnston DT. 2013. Influence of sulfate reduction rates on the Phanerozoic sulfur isotope record. PNAS 110:11244–49 [Google Scholar]
  66. Levin LA. 2003. Oxygen minimum zone benthos: adaptation and community response to hypoxia. Oceanogr. Mar. Biol. 41:1–45 [Google Scholar]
  67. Levin LA, Gage JD. 1998. Relationships between oxygen, organic matter and the diversity of bathyal macrofauna. Deep-Sea Res. II 45:129–63 [Google Scholar]
  68. Levin LA, Gutierrez D, Rathburn A, Neira C, Sellanes J. et al. 2002. Benthic processes on the Peru margin: a transect across the oxygen minimum zone during the 1997–98 El Niño. Progr. Oceanogr. 53:1–27 [Google Scholar]
  69. Love GD, Grosjean E, Stalvies C, Fike DA, Grotzinger JP. et al. 2009. Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457:718–21 [Google Scholar]
  70. Lyons TW, Reinhard CT, Planavsky NJ. 2014. The rise of oxygen in Earth's early ocean and atmosphere. Nature 506:307–15 [Google Scholar]
  71. Macdonald FA, Strauss JV, Sperling EA, Halverson GP, Narbonne GM. et al. 2013. The stratigraphic relationship between the Shuram carbon isotope excursion, the oxygenation of Neoproterozoic oceans, and the first appearance of the Ediacara biota and bilaterian trace fossils in northwestern Canada. Chem. Geol. 362:250–72 [Google Scholar]
  72. Maloof AC, Porter SM, Moore JL, Dudas FO, Bowring SA. et al. 2010. The earliest Cambrian record of animals and ocean geochemical change. Geol. Soc. Am. Bull. 122:1731–74 [Google Scholar]
  73. Mentel M, Roettge M, Leys S, Tielens AGM, Martin WF. 2014. Of early animals, anaerobic mitochondria, and a modern sponge. Bioessays 36:924–32 [Google Scholar]
  74. Metcalfe NB, Alonso-Alvarez C. 2010. Oxidative stress as a life history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Funct. Ecol. 24:984–96 [Google Scholar]
  75. Middelburg J, Levin L. 2009. Coastal hypoxia and sediment biogeochemistry. Biogeosci. Discuss. 6:3655–706 [Google Scholar]
  76. Mills B, Lenton TM, Watson AJ. 2014. Proterozoic oxygen rise linked to shifting balance between seafloor and terrestrial weathering. PNAS 111:4168–72 [Google Scholar]
  77. Mills DB, Canfield DE. 2014. Oxygen and animal evolution: Did a rise of atmospheric oxygen trigger the origin of animals?. Bioessays 36:1145–55 [Google Scholar]
  78. Mills DB, Ward LM, Jones C, Sweeten B, Forth M. et al. 2014. The oxygen requirements of sponges: modern analogues for the earliest animals. PNAS 111:9073–78 [Google Scholar]
  79. Moffitt SE, Moffitt RA, Sauthoff W, Davis CV, Hewett K, Hill TM. 2015. Paleoceanographic insights on recent Oxygen Minimum Zone expansion: lessons for modern oceanography. PLOS ONE 10:e0115246 [Google Scholar]
  80. Mullins HT, Thompson JB, McDougall K, Vercoutere TL. 1985. Oxygen-minimum zone edge effects: evidence from central California upwelling system. Geology 13:491–94 [Google Scholar]
  81. Narbonne GM, Gehling JG. 2003. Life after snowball: the oldest complex Ediacaran fossils. Geology 31:27–30 [Google Scholar]
  82. Nosenko T, Schreiber F, Adamska M, Adamski M, Eitel M. et al. 2013. Deep metazoan phylogeny: when different genes tell different stories. Mol. Phylogen. Evol. 67:223–33 [Google Scholar]
  83. Och LM, Shields-Zhou GA. 2012. The Neoproterozoic oxygenation event: environmental perturbations and biogeochemical cycling. Earth-Sci. Rev. 110:26–57 [Google Scholar]
  84. Palma M, Quiroga E, Gallardo VA, Arntz W, Gerdes D. et al. 2005. Macrobenthic animal assemblages of the continental margin off Chile (22° to 42°S). J. Mar. Biol. Ass. U.K. 85:233–45 [Google Scholar]
  85. Partin CA, Bekker A, Planavsky NJ, Scott CT, Gill BC. et al. 2013. Large-scale fluctuations in Precambrian atmospheric and oceanic oxygen levels from the record of U in shales. Earth Planet. Sci. Lett. 369–370:284–93 [Google Scholar]
  86. Paulmier A, Ruiz-Pino D, Garcon V. 2011. CO2 maximum in the oxygen minimum zone (OMZ). Biogeosciences 8:239–52 [Google Scholar]
  87. Pavlov AA, Kasting JF. 2002. Mass-independent fractionation of sulfur isotopes in Archean sediments: strong evidence for an anoxic Archean atmosphere. Astrobiology 2:27–41 [Google Scholar]
  88. Payne JL, Boyer AG, Brown JH, Finnegan S, Kowalewski M. et al. 2009. Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity. PNAS 106:24–27 [Google Scholar]
  89. Payne JL, McClain CR, Boyer AG, Brown JH, Finnegan S. et al. 2010. The evolutionary consequences of oxygenic photosynthesis: a body size perspective. Photosynth. Res. 107:37–57 [Google Scholar]
  90. Peterson KJ, McPeek MA, Evans DAD. 2005. Tempo and mode of early animal evolution: inferences from rocks, Hox, and molecular clocks. Paleobiology 31:Suppl. 536–55 [Google Scholar]
  91. Planavsky NJ, Reinhard CT, Wang X, Thompson D, McGoldrick P. et al. 2014. Low mid-Proterozoic atmospheric oxygen levels and the delayed rise of animals. Science 346:635–38 [Google Scholar]
  92. Raman AV, Damodaran R, Levin LA, Ganesh T, Rao YKV. et al. 2014. Macrobenthos relative to the oxygen minimum zone on the East Indian margin, Bay of Bengal. Mar. Ecol. 36:679–700 [Google Scholar]
  93. Reinhard CT, Planavsky NJ, Robbins LJ, Partin CA, Gill BC. et al. 2013. Proterozoic ocean redox and biogeochemical stasis. PNAS 110:5357–62 [Google Scholar]
  94. Revsbech NP, Larsen LH, Gundersen J, Dalsgaard T, Ulloa O, Thamdrup B. 2009. Determination of ultra-low oxygen concentrations in oxygen minimum zones by the STOX sensor. Limnol. Oceanogr. Methods 7:371–81 [Google Scholar]
  95. Rhoads DC, Morse JW. 1971. Evolutionary and ecologic significance of oxygen-deficient marine basins. Lethaia 4:413–28 [Google Scholar]
  96. Runnegar B. 1982. The Cambrian explosion: animals or fossils?. J. Geol. Assoc. Aust. 29:395–411 [Google Scholar]
  97. Runnegar B. 1991. Precambrian oxygen levels estimated from the biochemistry and physiology of early eukaryotes. Palaeogeogr. Palaeoclimatol. Palaeoecol. 97:97–111 [Google Scholar]
  98. Sahoo SK, Planavsky NJ, Kendall B, Wang X, Shi X. et al. 2012. Ocean oxygenation in the wake of the Marinoan glaciation. Nature 489:546–49 [Google Scholar]
  99. Sanders H. 1969. Benthic marine diversity and the stability-time hypothesis. Brookhaven Symp. Biol. 22:71–81 [Google Scholar]
  100. Schopf JW. 2006. Fossil evidence of Archaean life. Philos. Trans. R. Soc. B 361:869–85 [Google Scholar]
  101. Schrag DP, Higgins JA, Macdonald FA, Johnston DT. 2013. Authigenic carbonate and the history of the global carbon cycle. Science 339:540–43 [Google Scholar]
  102. Scott C, Lyons TW, Bekker A, Shen Y, Poulton SW. et al. 2008. Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452:456–59 [Google Scholar]
  103. Sim MS, Bosak T, Ono S. 2011. Large sulfur isotope fractionation does not require disproportionation. Science 333:74–77 [Google Scholar]
  104. Somero GN, Childress JJ, Anderson A. 1989. Transport, metabolism and detoxification of hydrogen sulfide in animals from sulfide-rich marine environments. Crit. Rev. Aquat. Sci. 1:591–614 [Google Scholar]
  105. Sperling EA. 2013. Tackling the 99%: Can we begin to understand the paleoecology of the small and soft-bodied animal majority?. Paleontol. Soc. Pap. 19:77–86 [Google Scholar]
  106. Sperling EA, Frieder CA, Raman AV, Girguis PR, Levin LA, Knoll AH. 2013a. Oxygen, ecology, and the Cambrian radiation of animals. PNAS 110:13446–51 [Google Scholar]
  107. Sperling EA, Halverson GP, Knoll AH, Macdonald FA, Johnston DT. 2013b. A basin redox transect at the dawn of animal life. Earth Planet. Sci. Lett. 371–372:143–55 [Google Scholar]
  108. Sperling EA, Wolock CJ, Morgan AS, Gill BC, Kunzmann M. et al. 2015. Statistical analysis of iron geochemical data suggests limited late Proterozoic oxygenation. Nature 523:451–54 [Google Scholar]
  109. Stanley SM. 1973. An ecological theory for the sudden origin of multicellular life in the late Precambrian. PNAS 70:1486–89 [Google Scholar]
  110. Stramma L, Johnson GC, Sprintall J, Mohrholz V. 2008. Expanding oxygen-minimum zones in the tropical oceans. Science 320:655–58 [Google Scholar]
  111. Tribovillard N, Algeo TJ, Lyons T, Riboulleau A. 2006. Trace metals as paleoredox and paleoproductivity proxies: an update. Chem. Geol. 232:12–32 [Google Scholar]
  112. Tyler SA, Barghoorn ES. 1954. Occurrence of structurally preserved plants in pre-Cambrian rocks of the Canadian Shield. Science 119:606–8 [Google Scholar]
  113. Tyson RV, Pearson TH. 1991. Modern and ancient continental-shelf anoxia: an overview. Geol. Soc. Lond. Spec. Publ. 58:1–24 [Google Scholar]
  114. Ulloa O, Canfield DE, DeLong EF, Letelier RM, Stewart FJ. 2012. Microbial oceanography of anoxic oxygen minimum zones. PNAS 109:15996–6003 [Google Scholar]
  115. Vaquer-Sunyer R, Duarte CM. 2010. Sulfide exposure accelerates hypoxia-driven mortality. Limnol. Oceanogr. 55:1075–82 [Google Scholar]
  116. Vinther J. 2015. The origins of molluscs. Palaeontology 58:19–34 [Google Scholar]
  117. Völkel S, Grieshaber MK. 1994. Oxygen-dependent sulfide detoxification in the lugworm Arenicola marina. Mar. Biol. 118:137–47 [Google Scholar]
  118. Waldbauer JR, Newman DK, Summons RE. 2011. Microaerobic steroid biosynthesis and the molecular fossil record of Archean life. PNAS 108:13409–14 [Google Scholar]
  119. Woulds C, Cowie GL, Levin LA, Andersson JH, Middelburg JJ. et al. 2007. Oxygen as a control on seafloor biological communities and their roles in sedimentary carbon cycling. Limnol. Oceanogr. 52:1698–709 [Google Scholar]
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The Ecological Physiology of Earth's Second Oxygen Revolution
Annual Review of Ecology, Evolution, and Systematics 46, 215 (2015); https://doi.org/10.1146/annurev-ecolsys-110512-135808
/content/journals/10.1146/annurev-ecolsys-110512-135808
/content/journals/10.1146/annurev-ecolsys-110512-135808
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