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Cited by 355Paleontology and Stratigraphy of FossilsEvolution and Paleontology StudiesOrigins and Evolution of Life

Oxygen requirements of the earliest animals

Open access
Mills, Daniel B., Ward, Lewis M., Jones, CarriAyne, Sweeten, Brittany, Forth, Michael, Treusch, Alexander H., Canfield, Donald E.·2014·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.1400547111PMC PMC3964089
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Abstract

A rise in the oxygen content of the atmosphere and oceans is one of the most popular explanations for the relatively late and abrupt appearance of animal life on Earth. In this scenario, Earth's surface environment failed to meet the high oxygen requirements of animals up until the middle to late Neoproterozoic Era (850-542 million years ago), when oxygen concentrations sufficiently rose to permit the existence of animal life for the first time. Although multiple lines of geochemical evidence support an oxygenation of the Ediacaran oceans (635-542 million years ago), roughly corresponding with the first appearance of metazoans in the fossil record, the oxygen requirements of basal animals remain unclear. Here we show that modern demosponges, serving as analogs for early animals, can survive under low-oxygen conditions of 0.5-4.0% present atmospheric levels. Because the last common ancestor of metazoans likely exhibited a physiology and morphology similar to that of a modern sponge, its oxygen demands may have been met well before the enhanced oxygenation of the Ediacaran Period. Therefore, the origin of animals may not have been triggered by a contemporaneous rise in the oxygen content of the atmosphere and oceans. Instead, other ecological and developmental processes are needed to adequately explain the origin and earliest evolution of animal life on Earth.

Integrity signals

Registry

Crossref · 10.1073/pnas.1400547111

Cites

54 of 54 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

3 of 31 cited sources checked · 1 supported · 0 flagged · accuracy not yet measured

  • Premisecitation

    Internal anoxia is a common feature of sponge physiology.

    “Internal anoxia, however, does appear to be a common feature of sponge physiology (34,35).”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites [34] 34. Hoffmann F, et al. (2005) An anaerobic world in sponges. Geomicrobiol J 22(1-2):1-10. source
    • cites [35] 35. Hoffmann F, et al. (2008) Oxygen dynamics and transport in the Mediterranean sponge Aplysina aerophoba. Mar Biol 153(6):1257-1264. source

      The Abstract and the Discussion section on oxygen dynamics report internal anoxia in non-pumping A. aerophoba, with tissue becoming anoxic within 15 minutes after pumping stops. They do not establish that internal anoxia is common across sponges; the Discussion also notes that prolonged non-pumping was not observed in an in situ study of A. aerophoba unless the sponge was disturbed. (LLM, conf=0.88)

      Experimental — accuracy not yet measured
  • Findingown data

    H. panicea respiration follows Michaelis-Menten kinetics with a Vmax of 2.42% air saturation/h·g dry weight (7.93 μM O2/h·g dry weight) and a Km of 4.86% air saturation (15.9 μM O2).

    “Overall, the patterns of oxygen uptake observed during the initial drawdown to anoxia followed Michaelis-Menten kinetics, with a V max of 2.42% air saturation/h•g dry weight , or 7.93 μM O 2 /h•g dry weight , and a K m of 4.86% of air saturation, or 15.9 μM O 2 , at the water salinity and temperature of our experiments (Fig. 3).”
    Quote in the paperSubstantial claim
  • Interpretationown data
    § Oxygen requirements of the earliest animals

    Modern demosponges, serving as analogs for early animals, can survive under low-oxygen conditions of 0.5-4.0% PAL.

    “Here we show that modern demosponges, serving as analogs for early animals, can survive under low-oxygen conditions of 0.5-4.0%present atmospheric levels.”
    Quote in the paperSubstantial claim
  • Premisecitation

    Sponges were observed on the Volcano 7 seamount in the eastern tropical Pacific, where oxygen concentrations ranged from 4.5 to 7.2 μM O2.

    “Sponges were also observed on the Volcano 7 seamount in the eastern tropical Pacific, where oxygen concentrations ranged from 4.5 to 7.2 μM O 2 (31) .”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [31] 31. Levin LA, Huggett CL, Wishner KF (1991) Control of deep-sea benthic community structure by oxygen and organic matter gradients in the eastern Pacific Ocean. J Mar Res 49(4):763-800. source
  • Interpretationreasoning
    § Oxygen requirements of the earliest animals

    The origin of animals may not have been triggered by a contemporaneous rise in the oxygen content of the atmosphere and oceans.

    “Therefore, the origin of animals may not have been triggered by a contemporaneous rise in the oxygen content of the atmosphere and oceans.”
    Quote in the paperSubstantial claim
  • May combine two claims. 15
  • Classified as probably not a substantial claim. 3

  • May combine two claims.

    Premisecitation

    Oxygen levels of 0.5-4% PAL may have been reached as early as the Great Oxidation Event 2.3-2.4 Ga and may have persisted through much of the intervening time, with some swings to lower levels around 1.8 Ga.

    “Indeed, oxygen levels this high may have been reached as early as the Great Oxidation Event some 2.3-2.4 billion years ago (43,45) and may have persisted at these levels through much of the intervening time (43,44), with some likely swings to lower levels, however, around 1.8 billion years ago (46).”
    Quote in the paperSubstantial claim1 of 4 sources checked
    • cites [43] 43. Kump LR (2008) The rise of atmospheric oxygen. Nature 451(7176):277-278. source
    • cites [45] 45. Bekker A, Holland HD (2012) Oxygen overshoot and recovery during the early Pale- oproterozoic. Earth Planet Sci Lett 317-318:295-304. source
    • cites [44] 44. Canfield DE (2014) Proterozoic Atmospheric Oxygen. Treatise on Geochemistry, eds Holland HD, Turekian KK (Elsevier, Oxford), 2nd Ed., pp 197-216. source
    • cites [46] 46. Canfield DE, et al. (2013) Oxygen dynamics in the aftermath of the Great Oxidation of Earth's atmosphere. Proc Natl Acad Sci USA 110(42):16736-16741. source

      The Significance section (page unavailable) places a rise in oxygen at the Great Oxidation Event about 2.3 billion years ago, followed by elevated levels for roughly 200 million years and then a collapse. The Results and Discussion section (page unavailable) describes later low-oxygen episodes, but the paper does not establish the cited 0.5–4% PAL range or its persistence through much of the intervening time. (LLM, conf=0.85)

      Experimental — accuracy not yet measured

  • May combine two claims.

    Premisecitation
    § Oxygen requirements of the earliest animals

    The earliest proposed signs of animals in the rock record, as well as molecular clock divergence estimates, predate the earliest evidence for deep ocean oxygenation, potentially by tens of millions of years.

    “Indeed, according to present evidence, the earliest proposed signs of animals in the rock record (9,10), as well as molecular clock divergence estimates (11,12), predate the earliest evidence for deep ocean oxygenation (1), potentially by tens of millions of years.”
    Quote in the paperSubstantial claim1 of 5 sources checked
    • cites [9] 9. Love GD, et al. (2009) Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457(7230):718-721. source
    • cites [10] 10. Maloof AC, et al. (2010) Possible animal-body fossils in pre-Marinoan limestones from South Australia. Nat Geosci 3(9):653-659. source
    • cites [11] 11. Peterson KJ, Butterfield NJ (2005) Origin of the Eumetazoa: Testing ecological pre- dictions of molecular clocks against the Proterozoic fossil record. Proc Natl Acad Sci USA 102(27):9547-9552. source
    • cites [12] 12. Erwin DH, et al. (2011) The Cambrian conundrum: Early divergence and later eco- logical success in the early history of animals. Science 334(6059):1091-1097. source
    • cites [1] 1. Sahoo SK, et al. (2012) Ocean oxygenation in the wake of the Marinoan glaciation. Nature 489(7417):546-549. source

  • May combine two claims.

    Findingown data

    The demosponge Halichondria panicea can tolerate and grow at low oxygen levels from 0.5% to 4% present atmospheric levels (PAL).

    “We show that although sensitive to oxygen, H. panicea can both tolerate and grow at low oxygen levels from 0.5% to 4% PAL.”
    • Also stated in: § Results and Discussion · plain
      “Overall, the sponges were able to both respire and feed to oxygen levels cycling between 0.5% and 4% PAL.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    H. panicea hosts a diversity of symbiotic microbes, including a significant population of ammonium-oxidizing Archaea and betaproteobacteria, as well as other aerobic organisms.

    “functional gene and 16S rRNA analyses reveal a significant population of ammonium-oxidizing Archaea and betaproteobacteria, as well as other aerobic organisms (Fig. S6 and Table S1).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The majority of oxygen uptake and Rhodomonas consumption observed during the experiments can be attributed to the sponges, with background rates likely attributed to free-living microbes.

    “Therefore, the majority of the oxygen uptake and Rhodomonas consumption observed during the experiments can be attributed to the sponges, with the background rates likely attributed to free-living microbes in our experimental system.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    H. panicea is sensitive to both anoxia and prolonged exposure to relatively stagnant seawater.

    “Our results suggest that H. panicea is sensitive to both anoxia and prolonged exposure to relatively stagnant seawater.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationown data

    The Km of H. panicea (4.86% air saturation) is less than half of 10% PAL, the estimated minimum atmospheric oxygen for deep ocean oxygenation around 580 Ma, and less than the level estimated to permit millimeter-width diffusion-limited animals.

    “This K m is less than half of the 10% PAL serving as the estimated minimum level of atmospheric oxygen thought to have permitted the oxygenation of the deep oceans around 580 Ma (2), as well as the level estimated to permit the existence of millimeter-width, diffusionlimited animals (15).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [2] 2. Canfield DE, Poulton SW, Narbonne GM (2007) Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315(5808):92-95. source
    • cites [15] 15. Catling DC, Glein CR, Zahnle KJ, McKay CP (2005) Why O2 is required by complex life on habitable planets and the concept of planetary "oxygenation time" Astrobiology 5(3):415-438. source

  • May combine two claims.

    Premisecitation

    Although atmospheric oxygen may have reached 10% PAL by 580 Ma, the geochemical record does not preclude oxygen levels of 0.5-4% PAL during the Cryogenian Period.

    “Although levels of atmospheric oxygen may have reached 10% PAL by 580 Ma, the geochemical record does not preclude oxygen levels of 0.5-4% PAL during the Cryogenian Period (43,44).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [43] 43. Kump LR (2008) The rise of atmospheric oxygen. Nature 451(7176):277-278. source
    • cites [44] 44. Canfield DE (2014) Proterozoic Atmospheric Oxygen. Treatise on Geochemistry, eds Holland HD, Turekian KK (Elsevier, Oxford), 2nd Ed., pp 197-216. source

  • Probably not a substantial claim: may not pass S4 (based).

    Premisereasoning
    § Oxygen requirements of the earliest animals

    Direct experimental evidence on minimum oxygen requirements can reasonably be obtained by studying modern animals that resemble the earliest metazoans.

    “Such evidence can reasonably be obtained by studying modern animals that resemble the earliest metazoans.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    Necrosis observed during experiment 1 was likely due to infrequent exchange of fresh seawater and not necessarily low oxygen levels.

    “Given the complete absence of necrosis in the sponges maintained at both low and high oxygen levels during this run, the necrosis observed during experiment 1 was likely due to the infrequent exchange of fresh seawater and not necessarily the low oxygen levels.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationown data

    Although 3-4% PAL oxygen may not compromise H. panicea's growth or maintenance of healthy tissue, anoxia still does.

    “This suggests that although 3-4% PAL oxygen may not compromise H. panicea's growth or maintenance of healthy tissue, anoxia still does.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationcitation
    § Oxygen requirements of the earliest animals

    The similarities between choanocytes and choanoflagellates were inherited from a common ancestor, and the choanocyte-based feeding mode retained by sponges is likely ancestral to all animals.

    “This suggests that the similarities between choanocytes and choanoflagellates were inherited from a common ancestor and that the choanocytebased feeding mode, as retained by sponges, is likely ancestral to all animals (29).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [29] 29. Nichols SA, Dayel MJ, King N (2009) Genomic, phylogenetic, and cell biological in- sights into metazoan origins. Animal Evolution: Genes, Genomes, Fossils and Trees, eds Telford MJ, Littlewood DTJ (Oxford University Press, Oxford), pp 24-32. source

  • Classified as probably not a substantial claim.

    Premisenone given
    § Oxygen requirements of the earliest animals

    To establish that low levels of atmospheric oxygen delayed the origin of animal life, it is necessary to know the minimum oxygen requirements of early animals.

    “Furthermore, to establish that low levels of atmospheric oxygen, in fact, delayed the origin of animal life on Earth, it is necessary to know the minimum oxygen requirements of early animals.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S2 (checkable).

    Premisereasoning
    § Oxygen requirements of the earliest animals

    Direct experimental evidence is required to more conclusively determine the minimum oxygen requirements of metazoans.

    “Therefore, to more conclusively determine the minimum oxygen requirements of metazoans, direct experimental evidence is required.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    LMA sponges have shorter and wider water canals, as well as larger choanoflagellate chambers, than high-microbial abundance (HMA) sponges.

    “LMA sponges are known to have shorter and wider water canals (38), as well as larger choanoflagellate chambers (39), than high-microbial abundance (HMA) sponges.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [38] 38. Vacelet J, Donadey C (1977) Electron-microscope study of association between some sponges and bacteria. J Exp Mar Biol Ecol 30(3):301-314. source
    • cites [39] 39. Boury-Esnault N, de Vos L, Donadey C, Vacelet J (1990) Ultrastructure of Choanosome and Sponge Classification (Smithsonian Institution Press, Washington, DC), pp 237-244.

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • May combine two claims.

    Interpretationreasoning

    Under this scenario, the origin of animal life was not a response to atmospheric oxygenation but part of the ecological reworking of marine biogeochemical cycles.

    “Under this scenario, the origin of animal life was not a response to atmospheric oxygenation but part of the ecological reworking of marine biogeochemical cycles.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Recent molecular clock estimates place the last common ancestor of all sponges at nearly 800 Ma, whereas putative sponge-like body fossils are found in rocks dated between 660 and 635 Ma in the Cryogenian Period.

    “Recent molecular clock estimates place the last common ancestor of all sponges at nearly 800 Ma (12), whereas putative sponge-like body fossils are found in rocks dated between 660 and 635 Ma (10) in the Cryogenian Period (850-635 Ma).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [12] 12. Erwin DH, et al. (2011) The Cambrian conundrum: Early divergence and later eco- logical success in the early history of animals. Science 334(6059):1091-1097. source
    • cites [10] 10. Maloof AC, et al. (2010) Possible animal-body fossils in pre-Marinoan limestones from South Australia. Nat Geosci 3(9):653-659. source

  • May combine two claims.

    Interpretationown data

    The last common ancestor of animals could have thrived in oxygen levels as low as 0.5% to 4% PAL, which were likely met on Earth well before animals evolved.

    “We provide experimental evidence suggesting that the last common ancestor of animals could have thrived in oxygen levels as low as 0.5% to 4% of present atmospheric levels, which were likely met on Earth well before animals evolved.”
    Quote in the paperSubstantial claim
18 of 18

  • The paper relies on this without support.

    The minimum oxygen requirements of modern sponges and their metabolic response to low oxygen had not been investigated prior to this study.

    “Despite these observations, however, the minimum oxygen requirements of modern sponges and their metabolic response to low oxygen have not, to our knowledge, been investigated.”
1 of 1

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Under most conditions, the estimated tolerance range for basal metazoan organisms is only safely exceeded throughout the year at pO2 on the order of ~5-10% PAL.

    “Indeed, under most conditions, the estimated tolerance range for basal metazoan organisms (12) is only safely exceeded throughout the year at p O2 on the order of ∼ 5 -10% PAL.”

    From Earth's oxygen cycle and the evolution of animal life (2016) · cites this paper as [12]

    The introduction reports theoretical estimates of 6–10% PAL for early animals, which partly supports the cited tolerance range. But the Significance section reports that a demosponge tolerated and grew at 0.5–4% PAL, and the paper does not establish that 5–10% PAL is needed to exceed basal metazoan tolerance throughout the year (pages unavailable in our copy). (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Experimental work with the modern demosponge Halichondria panacea suggests an empirical O2 threshold of ~0.5-4.0% PAL for basal metazoan life.

    “Experimental work with the modern demosponge Halichondria panacea suggests an empirical O2 threshold of ∼ 0.5 -4.0% of the present atmospheric level (PAL; corresponding to an equilibrium concentration of ∼ 1 -10 μ mol · kg -1 for air-saturated water at 25 °C and a salinity of 35 ‰ ) for basal metazoan life (12)”

    From Earth's oxygen cycle and the evolution of animal life (2016) · cites this paper as [12]

    The Significance and Results and Discussion sections report that the demosponge H. panicea tolerated, fed, and grew at 0.5–4% PAL. But Results and Discussion calls these the lowest levels the experiments could maintain and suggests some sponges could grow at still lower levels; it does not establish 0.5–4% PAL as a threshold for basal metazoan life. The citing sentence also misspells the species name as H. panacea. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

  • The isotope data and models suggest that there were ample amounts of O2 for animals in the surface ocean at the onset of the Cambrian.

    “Finally, in the greater context of what triggered the emergence of complex animal ecosystems on Earth, our isotope data and models suggest that there were ample amounts of O2 for animals in the surface ocean at the onset of the Cambrian (69).”

    From Atmosphere-ocean oxygen and productivity dynamics during early animal radiations (2019) · cites this paper as [69]

    The paper’s Significance section (page unavailable) says oxygen levels sufficient for sponge-like early animals were likely present well before animals evolved, and its introduction describes ocean oxygenation before the Cambrian. It does not establish oxygen amounts specifically in the surface ocean at the onset of the Cambrian or show that those amounts met the needs of animals generally, rather than the basal animals it studied. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

  • The early originating suspension-feeding sponges had low O2 requirements and may have helped consume the large dissolved organic carbon reservoir that acted as a major redox buffer in the Proterozoic ocean.

    “The early originating suspension-feeding sponges had low O2 requirements63, and may have helped consume the large dissolved organic carbon reservoir that acted as a major redox buffer in the Proterozoic ocean12.”

    From Rise to modern levels of ocean oxygenation coincided with the Cambrian radiation of animals (2015) · cites this paper as [63]

  • The BACE pre-dates the first appearance of Treptichnus pedum.

    “The BACE pre-dates the first appearance of Treptichnus pedum (31,32)”

    From Integrated records of environmental change and evolution challenge the Cambrian Explosion (2019) · cites this paper as [31]

    The section on sponge evolution and environmental oxygen levels discusses the timing of sponge fossils and ocean oxygenation, not the order of the BACE and the first appearance of Treptichnus pedum. Searches for both terms and for their proposed temporal relationship found no passage addressing the claim. (LLM, conf=0.77)

    Experimental — accuracy not yet measured

Cites

Flagged first, then by citations

Research works printed but not linked: 1

  1. N Boury-Esnault, L de Vos, C Donadey, J Vacelet Ultrastructure of Choanosome and Sponge Classification (Smithsonian Institution Press, Washington, DC), pp. 237–244 (1990).

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Related

Authors
Mills, D. B., Ward, L. M., Jones, C., Sweeten, B., Forth, M., Treusch, A. H., & Canfield, D. E.
Affiliations
  • University of Southern Denmark (DK)
  • California Institute of Technology (US)
  • University of British Columbia (CA)
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2014-02-18
Volume
111
Issue
11
Pages
4168-4172
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.1400547111
PMC
PMC3964089
OpenAlex
W2029322624
Semantic Scholar
ac41b42cf0cc457afe8379a4d86261edcc53d9e5
Cited by
355
References
53
Citations by year
2026: 15 · 2025: 29 · 2024: 24 · 2023: 24 · 2022: 39 · 2021: 40 · 2020: 29 · 2019: 29 · 2018: 33 · 2017: 23 · 2016: 27 · 2015: 32 · 2014: 11
FWCI
22.57
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • CaltechAUTHORS (California Institute of Technology) (submittedVersion)
  • University of Southern Denmark Research Portal (University of Southern Denmark) (submittedVersion)
Funders
  • Agouron Institute
  • National Research Foundation
  • Danmarks Grundforskningsfond (Grant DNRF 53, DNRF 53)
Topics
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Stratigraphy of Fossils
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
  • Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
Keywords
origin of animals, Ediacaran, oxygen requirement, demosponges, low oxygen tolerance, atmospheric oxygenation, Neoproterozoic, animal evolution
MeSH terms
Adaptation, Biological, Animals, Atmosphere, Base Sequence, Denmark, Biological Evolution, Kinetics, Molecular Sequence Data, Oxygen, Oxygen Consumption, Porifera, Polymorphism, Restriction Fragment Length, RNA, Ribosomal, 16S, Sequence Analysis, DNA, Microbiota

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