Neoproterozoic oxygenation event

Short description: Neoproterozoic surge in atmospheric oxygen

For the first (Paleoproterozoic) surge in atmospheric oxygen, see Great Oxidation Event.

O2 build-up in the Earth's atmosphere. Red and green lines represent the range of the estimates while time is measured in billions of years ago (Ga).

* Stage 1 (3.85–2.45 Ga): Practically no O2 in the atmosphere. The oceans were also largely anoxic – with the possible exception of O2 in the shallow oceans.
* Stage 2 (2.45–1.85 Ga): O2 produced, rising to values of 0.02 and 0.04 atm, but absorbed in oceans and seabed rock. (Great Oxidation Event)
* Stage 3 (1.85–0.85 Ga): O2 starts to gas out of the oceans, but is absorbed by land surfaces. No significant change in oxygen level.
* Stages 4 and 5 (0.85 Ga – present): Other O2 reservoirs filled; gas accumulates in atmosphere.[1] Stage 4 is known as the neoproterozoic oxygenation event.

The Neoproterozoic Oxygenation Event (NOE), also called the Second Great Oxidation Event, was a geologic time interval between around 850 and 540 million years ago during the Neoproterozoic era, during which the oxygen concentration in Earth's atmosphere and oceans rose significantly.[2] Taking place after the end to the Boring Billion, a euxinic period of extremely low atmospheric oxygen spanning from the Statherian period of the Paleoproterozoic era to the Tonian period of the Neoproterozoic era, the NOE was the second major increase in atmospheric and oceanic oxygen concentration on Earth, though it was not as prominent as the Great Oxidation Event (GOE) of the Neoarchean-Paleoproterozoic boundary. Unlike the GOE, it is unclear whether the NOE was a synchronous, global event or a series of asynchronous, regional oxygenation intervals with unrelated causes.[3]

## Contents

* 1 Evidence for oxygenation
* 1.1 Carbon isotopes
* 1.2 Nitrogen isotopes
* 1.3 Sulfur isotopes
* 1.4 Strontium isotopes
* 1.5 Chromium isotopes
* 1.6 Molybdenum isotopes
* 1.7 Uranium isotopes
* 2 Causes
* 2.1 Increase in nitrogen fixation
* 2.2 Increase in day length
* 2.3 Organic carbon burial
* 2.4 Phosphorus removal
* 3 Consequences
* 3.1 Glaciation
* 3.2 Biological diversity
* 4 See also
* 5 References

## Evidence for oxygenation

### Carbon isotopes

Beginning around 850 Mya to around 720 Mya, a time interval roughly corresponding to the Late Tonian, between the end of the Boring Billion and the onset of the Cryogenian "Snowball Earth", marine deposits record a very significant positive carbon isotope excursion. These elevated δ13C values are believed to be linked to an evolutionary radiation of eukaryotic plankton and enhanced organic burial, which in turn indicate a spike in oxygen production during this interval.[4] Further positive carbon isotope excursions occurred during the Cryogenian.[5] Although several negative carbon isotope excursions, associated with warming events, are known from the Late Tonian all the way up to the Proterozoic-Phanerozoic boundary, the carbon isotope record nonetheless maintains a noticeable positive trend throughout the Neoproterozoic.[2]

### Nitrogen isotopes

δ15N data from 750 to 580 million year-old marine sediments hailing from four different Neoproterozoic basins show similar nitrogen isotope ratios to modern oceans, with a mode of +4% and a range from -4% to +11%. No significant change is observed across the Cryogenian-Ediacaran boundary, implying that oxygen was already ubiquitous in the global ocean as early as 750 Mya, during the Tonian period.[6]

### Sulfur isotopes

Seawater sulfate δ34S values, which saw a gradual increase over most of the Neoproterozoic punctuated by major drops during glaciations,[7] show a significant positive excursion during the Ediacaran, with a corresponding decrease in pyritic δ34S. High fractionation rates between sulfte and sulfide indicate an increase in the availability of sulfate in the water column, which in turn is indicative of increased reaction of pyrite with oxygen.[8] In addition, genetic evidence points to the occurrence of a radiation of non-photosynthetic sulfide-reducing bacteria during the Neoproterozoic. Through bacterial sulfur disproportionation, such bacteria further deplete marine sulfide of heavier sulfur isotopes.[9] Because such bacteria require significant amounts of oxygen to survive, an oxygenation event during the Neoproterozoic raising oxygen concentrations to over 5-18% of modern levels is believed to have been a necessary prerequisite for the diversification of these microorganisms.[10]

### Strontium isotopes

δ13C can reliably indicate changes in net primary productivity and oxygenation if the rates of weathering into the oceans and carbon dioxide outgassing remain constant or increase, since a decrease in either of these could cause a positive δ13C excursion through continued preferential biological consumption of carbon-12 by existing communities while the supply of available carbon decreased, without indicating an increase in primary productivity and oxygen production.[4] The ratio of strontium-87 to strontium-86 is used as a determinant of the relative contribution of continental weathering to the ocean's nutrient supply;[2] an increase in this ratio, as observed throughout the Neoproterozoic and into the Cambrian until reaching a peak at the end of the Cambrian, suggests a rise in continental weathering and bolsters evidence from carbon isotope ratios for high oxygenation in this interval of time.[11]

### Chromium isotopes

Surface oxidation of Cr(III) to Cr(VI) causes isotopic fractionation of chromium; Cr(VI), typically present in the environment as either chromate or dichromate, has elevated values of δ53Cr, or the ratio of chromium-53 to chromium-52, whereas bacterial reduction of Cr(VI) to Cr(III) is associated with negative chromium isotope excursions. Following the riverine transport of oxidised chromium into the ocean, the reaction reducing Cr(VI) back into Cr(III) and subsequently oxidising ferrous iron into ferric iron is highly efficient at sequestering Cr(VI), as is the precipitation of Cr(III) with ferric oxyhydroxide, meaning that chemically precipitated chromium isotope ratios in sediments abundant in ferric iron accurately reflect seawater chromium isotope ratios at the time of deposition. Because efficient oxidation of Cr(III) to Cr(VI) is only possible in the presence of the catalyst manganese dioxide, which is only stable and abundant at high oxygen fugacities, a positive excursion of δ53Cr indicates an increase in atmospheric oxygen concentrations. Banded iron formations (BIFs) deposited during the Neoproterozoic consistently display highly positive δ53Cr values, from 0.9% to 4.9%, demonstrating the era's oxygenation of the atmosphere.[12][4] Oxidative chromium cycling began approximately 0.8 Ga, indicating that oxygen level rise began well before the Cryogenian glaciations.[13] Chromium isotopes also show that during the Cryogenian interglacial interval, between the Sturtian and Marinoan glaciations, oxygenation of the ocean and atmosphere was slow and subdued; this interval marked a lull in the NOE.[14]

### Molybdenum isotopes

δ98Mo values were slightly higher during the Late Ediacaran than in the Cryogenian or the Early and Middle Ediacaran. This isotopic proxy indicates the level of oxygenation of the Late Ediacaran ocean was comparable to that of Mesozoic oceanic anoxic events.[15]

### Uranium isotopes

The very low values of δ238U, commonly used as an isotopic measurement of changes in seawater oxygenation, during much of the Neoproterozoic have been interpreted to reflect progressive oxygenation punctuated by temporary, transient expansions of anoxic and euxinic waters.[16] During the Early Ediacaran, the shift in uranium isotopes occurred in tandem with enrichment in light carbon isotopes.[17]

## Causes

### Increase in nitrogen fixation

During the Boring Billion, open ocean productivity was very low compared to the Neoproterozoic and Phanerozoic as a result of the absence of planktonic nitrogen-fixing bacteria. The evolution and radiation of nitrogen-fixing bacteria and non-nitrogen-fixing picocyanobacteria capable of occupying marine planktonic niches and consequent changes to the nitrogen cycle during the Cryogenian are believed to be a culprit behind the rapid oxygenation of and removal of carbon dioxide from the atmosphere, which also helps explain the development of extremely severe glaciations that characterised this period of the Neoproterozoic.[18]

### Increase in day length

The slowdown of the Earth's rotation and corresponding increase in day length has been suggested as a possible cause of the NOE on the basis of experimental findings that cyanobacterial productivity is higher during longer periods of uninterrupted daylight compared to shorter periods more frequently interrupted by darkness.[19]

### Organic carbon burial

The Neoproterozoic saw organic carbon burial occur in large lakes with anoxic bottom waters on a massive scale. As carbon was locked away in sedimentary rock, it was unable to be oxidised, permitting a buildup of atmospheric oxygen.[20]

### Phosphorus removal

The increasing diversity of eukaryotes has been proposed as a cause of increased deep ocean oxygenation by means of phosphorus removal from the deep ocean. The evolution of large multicellular organisms led to increased amounts of organic matters sinking to the seafloor (marine snow). This, combined with the evolution of benthic filter feeders (e.g. choanoflagellates and primitive poriferans such as Otavia), is believed to have shifted oxygen demand further down in the water column, which would result in a positive feedback loop wherein phosphorus was removed from the ocean, which reduced productivity and decreased oxygen demand, which in turn led to increasing oxygenation of deep ocean water. Increasingly well oxygenated oceans enabled further eukaryotic dispersal, which likely acted as a positive feedback loop that accelerated oxygenation.[21]

## Consequences

### Glaciation

Main article: Earth:Snowball Earth

The rapid increase in organic carbon sequestration as a result of the increased rates of global photosynthesis by both cyanobacteria and eukaryotic photoautotrophs (green and red algae), occurring in conjunction with an increase in silicate weathering of continental flood basalts resulting from the breakup of the supercontinent Rodinia,[22] is believed to have been a trigger of the Sturtian and Marinoan glaciations during the Cryogenian, the middle period of the Neoproterozoic.[18]

### Biological diversity

During the Tonian, very early multicellular organisms may have evolved and diversified in oxygen "oases" in the deep oceans, which acted as cradles in these early stages of eukaryote evolution.[23] However, the persistence of anoxia and euxinia over the late Tonian despite some increases in oxygen content meant eukaryotic diversity overall remained low.[24] Over the course of the Ediacaran period, the oceans gradually became better oxygenated,[25] with the time interval immediately after the Gaskiers Glaciation displaying evidence of significantly increasing marine oxygen content.[26] The rapid diversification of multicellular life during this geologic period has been attributed by some authors to an increase in oxygen content,[27] enabling the iconic oxygen-consuming multicellular eukaryotes of the Ediacaran biota to become ubiquitous and widespread.[28][29][30] Initially restricted to deeper, colder waters that possessed the most dissolved oxygen, metazoan life gradually expanded into warmer zones of the ocean as global oxygen levels rose.[31]

## See also

* Great Oxidation Event
* Avalon explosion
* Cambrian explosion
* Silurian-Devonian Terrestrial Revolution

## References

1. ↑ Holland, Heinrich D. (19 May 2006). "The oxygenation of the atmosphere and oceans". Philosophical Transactions of the Royal Society: Biological Sciences 361 (1470): 903–915. doi:10.1098/rstb.2006.1838. PMID 16754606.
2. ↑ 2.0 2.1 2.2 Och, Lawrence M.; Shields-Zhou, Graham A. (January 2012). "The Neoproterozoic oxygenation event: Environmental perturbations and biogeochemical cycling". Earth-Science Reviews 110 (1–4): 26–57. doi:10.1016/j.earscirev.2011.09.004. Bibcode: 2012ESRv..110...26O. https://www.sciencedirect.com/science/article/abs/pii/S0012825211001498. Retrieved 10 November 2022.
3. ↑ Stern, Robert J.; Mukherjee, Sumit K.; Miller, Nathan R.; Ali, Kamal; Johnson, Peter R. (December 2013). "~750 Ma banded iron formation from the Arabian-Nubian Shield—Implications for understanding neoproterozoic tectonics, volcanism, and climate change". Precambrian Research 239: 79–94. doi:10.1016/j.precamres.2013.07.015. Bibcode: 2013PreR..239...79S. https://www.sciencedirect.com/science/article/abs/pii/S030192681300226X. Retrieved 20 December 2022.
4. ↑ 4.0 4.1 4.2 Shields-Zhou, Graham A.; Och, Lawrence M. (March 2011). "The case for a Neoproterozoic Oxygenation Event: Geochemical evidence and biological consequences". GSA Today 21 (3): 4–11. doi:10.1130/GSATG102A.1. Bibcode: 2011GSAT...21c...4S. https://discovery.ucl.ac.uk/id/eprint/1354478/1/1354478_Shields-Zhou%20and%20Och_2011.pdf. Retrieved 10 November 2022.
5. ↑ Riding, Robert (17 November 2006). "Cyanobacterial calcification, carbon dioxide concentrating mechanisms, and Proterozoic–Cambrian changes in atmospheric composition". Geobiology 4 (4): 299–316. doi:10.1111/j.1472-4669.2006.00087.x. Bibcode: 2006Gbio....4..299R. https://onlinelibrary.wiley.com/doi/epdf/10.1111/j.1472-4669.2006.00087.x. Retrieved 10 November 2022.
6. ↑ Ader, Magali; Sansjofre, Pierre; Halverson, Galen P.; Busigny, Vincent; Trindade, Ricardo I. F.; Kunzmann, Marcus; Nogueira, Afonso C. R. (15 June 2014). "Ocean redox structure across the Late Neoproterozoic Oxygenation Event: A nitrogen isotope perspective". Earth and Planetary Science Letters 396: 1–13. doi:10.1016/j.epsl.2014.03.042. Bibcode: 2014E&PSL.396....1A. https://www.sciencedirect.com/science/article/abs/pii/S0012821X14001940. Retrieved 10 November 2022.
7. ↑ Hurtgen, Matthew T.; Arthur, Michael A.; Halverson, Galen P. (1 January 2005). "Neoproterozoic sulfur isotopes, the evolution of microbial sulfur species, and the burial efficiency of sulfide as sedimentary pyrite". Geology 33 (1): 41–44. doi:10.1130/G20923.1. Bibcode: 2005Geo....33...41H. https://pubs.geoscienceworld.org/gsa/geology/article-abstract/33/1/41/129257/Neoproterozoic-sulfur-isotopes-the-evolution-of?redirectedFrom=fulltext. Retrieved 10 November 2022.
8. ↑ Halverson, Galen P.; Hurtgen, Matthew T. (15 November 2007). "Ediacaran growth of the marine sulfate reservoir". Earth and Planetary Science Letters 263 (1–2): 32–44. doi:10.1016/j.epsl.2007.08.022. Bibcode: 2007E&PSL.263...32H. https://www.sciencedirect.com/science/article/abs/pii/S0012821X07005195. Retrieved 10 November 2022.
9. ↑ Fike, D. A.; Grotzinger, J. P.; Pratt, L. M.; Summons, R. E. (7 December 2006). "Oxidation of the Ediacaran Ocean". Nature 444 (7120): 744–747. doi:10.1038/nature05345. PMID 17151665. Bibcode: 2006Natur.444..744F. https://www.nature.com/articles/nature05345#citeas. Retrieved 10 November 2022.
10. ↑ Canfield, Donald Eugene; Teske, Andreas (11 July 1996). "Late Proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies". Nature 382 (6587): 127–132. doi:10.1038/382127a0. PMID 11536736. Bibcode: 1996Natur.382..127C. https://www.researchgate.net/publication/11809182. Retrieved 10 November 2022.
11. ↑ Kennedy, Martin J.; Droser, Mary L.; Mayer, Lawrence M.; Pevear, David; Mrofka, David (10 March 2006). "Late Precambrian Oxygenation; Inception of the Clay Mineral Factory". Science 311 (5766): 1446–1449. doi:10.1126/science.1118929. PMID 16456036. Bibcode: 2006Sci...311.1446K. https://www.researchgate.net/publication/7318278. Retrieved 10 November 2022.
12. ↑ Frei, Robert; Gaucher, Claudio; Poulton, Simon W.; Canfield, Donald Eugene (10 September 2009). "Fluctuations in Precambrian atmospheric oxygenation recorded by chromium isotopes". Nature 461 (7261): 250–253. doi:10.1038/nature08266. PMID 19741707. Bibcode: 2009Natur.461..250F. https://www.nature.com/articles/nature08266. Retrieved 10 November 2022.
13. ↑ Casado, Juan (17 October 2021). "A Review of the Neoproterozoic Global Glaciations and a Biotic Cause of Them". Earth Systems and Environment 5 (4): 811–824. doi:10.1007/s41748-021-00258-x. Bibcode: 2021ESE.....5..811C.
14. ↑ Xu, Lingang; Frank, Anja B.; Lehmann, Bernd; Zhu, Jianming; Mao, Jingwen; Ju, Yongze; Frei, Robert (21 October 2019). "Subtle Cr isotope signals track the variably anoxic Cryogenian interglacial period with voluminous manganese accumulation and decrease in biodiversity". Scientific Reports 9 (1): 15056. doi:10.1038/s41598-019-51495-0. PMID 31636318. Bibcode: 2019NatSR...915056X.
15. ↑ Tan, Zhaozhao; Wu, Jinxiang; Jia, Wanglu; Li, Jie; Kendall, Brian; Song, Jianzhong; Peng, Ping'an (20 April 2023). "Molybdenum isotope evidence from restricted-basin mudstones for an intermediate extent of oxygenation in the late Ediacaran ocean". Chemical Geology 623. doi:10.1016/j.chemgeo.2023.121410. ISSN 0009-2541. Bibcode: 2023ChGeo.623l1410T. https://www.sciencedirect.com/science/article/pii/S0009254123001109. Retrieved 28 September 2023.
16. ↑ Clarkson, Matthew O.; Sweere, Tim C.; Chiu, Chun Fung; Hennekam, Rick; Bowyer, Tim; Wood, Rachel A. (February 2023). "Environmental controls on very high δ238U values in reducing sediments: Implications for Neoproterozoic seawater records". Earth-Science Reviews 237. doi:10.1016/j.earscirev.2022.104306. https://www.sciencedirect.com/science/article/pii/S0012825222003907. Retrieved 17 June 2023.
17. ↑ Chen, Bo; Hu, Chunlin; Mills, Benjamin J. W.; He, Tianchen; Andersen, Morten B.; Chen, Xi; Liu, Pengju; Lu, Miao et al. (1 January 2022). "A short-lived oxidation event during the early Ediacaran and delayed oxygenation of the Proterozoic ocean". Earth and Planetary Science Letters 577. doi:10.1016/j.epsl.2021.117274. Bibcode: 2022E&PSL.57717274C. https://www.sciencedirect.com/science/article/abs/pii/S0012821X21005306. Retrieved 17 June 2023.
18. ↑ 18.0 18.1 Sánchez-Baracaldo, Patricia; Ridgwell, Andy; Raven, John A. (17 March 2014). "A Neoproterozoic Transition in the Marine Nitrogen Cycle". Current Biology 24 (6): 652–657. doi:10.1016/j.cub.2014.01.041. PMID 24583016. Bibcode: 2014CBio...24..652S.
19. ↑ Klatt, J. M.; Chennu, A.; Arbic, B. K.; Biddanda, B. A.; Dick, G. J. (2 August 2021). "Possible link between Earth's rotation rate and oxygenation". Nature Geoscience 14 (8): 564–570. doi:10.1038/s41561-021-00784-3. Bibcode: 2021NatGe..14..564K.
20. ↑ Spinks, Samuel C.; Parnell, John; Bowden, Stephen A.; Taylor, Ross A.D.; Maclean, Màiri E. (December 2014). "Enhanced organic carbon burial in large Proterozoic lakes: Implications for atmospheric oxygenation" (in en). Precambrian Research 255: 202–215. doi:10.1016/j.precamres.2014.09.026. https://linkinghub.elsevier.com/retrieve/pii/S0301926814003441. Retrieved 18 July 2024.
21. ↑ Lenton, Timothy M.; Boyle, Richard A.; Poulton, Simon W.; Shields-Zhou, Graham A.; Butterfield, Nicholas J. (9 March 2014). "Co-evolution of eukaryotes and ocean oxygenation in the Neoproterozoic era". Nature Geoscience 7 (4): 257–265. doi:10.1038/ngeo2108. Bibcode: 2014NatGe...7..257L. https://www.nature.com/articles/ngeo2108#citeas. Retrieved 10 November 2022.
22. ↑ Cox, Grant M.; Halverson, Galen P.; Stevenson, Ross K.; Vokaty, Michelle; Poirier, André; Kunzmann, Marcus; Li, Zheng-Xiang; Denyszyn, Steven W. et al. (15 July 2016). "Continental flood basalt weathering as a trigger for Neoproterozoic Snowball Earth". Earth and Planetary Science Letters 446: 89–99. doi:10.1016/j.epsl.2016.04.016. Bibcode: 2016E&PSL.446...89C.
23. ↑ Wang, Haiyang; Liu, Aoran; Li, Chao; Feng, Qinglai; Tang, Shida; Cheng, Meng; Algeo, Thomas J. (April 2021). "A benthic oxygen oasis in the early Neoproterozoic ocean". Precambrian Research 355: 1–11. doi:10.1016/j.precamres.2020.106085. Bibcode: 2021PreR..35506085W. https://www.sciencedirect.com/science/article/abs/pii/S0301926820306744. Retrieved 29 April 2023.
24. ↑ Stacey, Jack; Hood, Ashleigh v.S.; Wallace, Malcolm W. (October 2023). "Persistent late Tonian shallow marine anoxia and euxinia" (in en). Precambrian Research 397. doi:10.1016/j.precamres.2023.107207. https://linkinghub.elsevier.com/retrieve/pii/S0301926823002474. Retrieved 18 July 2024.
25. ↑ Álvaro, J. Javier; Shields-Zhou, Graham A.; Ahlberg, Per; Jensen, Sören; Palacios, Teodoro (23 May 2015). "Ediacaran–Cambrian phosphorites from the western margins of Gondwana and Baltica". Sedimentology 63 (2): 350–377. doi:10.1111/sed.12217. https://onlinelibrary.wiley.com/doi/10.1111/sed.12217. Retrieved 10 November 2022.
26. ↑ Macdonald, Francis A.; Strauss, Justin V.; Sperling, Erik A.; Halverson, Galen P.; Narbonne, Guy M.; Johnston, David T.; Kunzmann, Marcus; Schrag, Daniel P. et al. (20 December 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". Chemical Geology 362: 250–272. doi:10.1016/j.chemgeo.2013.05.032. Bibcode: 2013ChGeo.362..250M. https://www.sciencedirect.com/science/article/abs/pii/S0009254113002490. Retrieved 10 November 2022.
27. ↑ Fan, Haifeng; Zhu, Xiangkun; Wen, Hanjie; Yan, Bin; Li, Jin; Feng, Lianjun (1 September 2014). "Oxygenation of Ediacaran Ocean recorded by iron isotopes". Geochimica et Cosmochimica Acta 140: 80–94. doi:10.1016/j.gca.2014.05.029. Bibcode: 2014GeCoA.140...80F. https://www.sciencedirect.com/science/article/abs/pii/S0016703714003585. Retrieved 10 November 2022.
28. ↑ Canfield, Donald Eugene; Poulton, Simon W.; Narbonne, Guy M. (5 January 2007). "Late-Neoproterozoic Deep-Ocean Oxygenation and the Rise of Animal Life". Science 315 (5808): 92–95. doi:10.1126/science.1135013. PMID 17158290. Bibcode: 2007Sci...315...92C.
29. ↑ Evans, Scott D.; Diamond, Charles W.; Droser, Mary L.; Lyons, Timothy W. (13 July 2018). "Dynamic oxygen and coupled biological and ecological innovation during the second wave of the Ediacara Biota". Emerging Topics in Life Sciences 2 (2): 223–233. doi:10.1042/ETLS20170148. PMID 32412611. https://portlandpress.com/emergtoplifesci/article-abstract/2/2/223/77113/Dynamic-oxygen-and-coupled-biological-and. Retrieved 10 November 2022.
30. ↑ Pehr, Kelden; Love, Gordon D.; Kuznetsov, Anton; Podkovyrov, Victor; Junium, Christopher K.; Shumlyanskyy, Leonid; Sokur, Tetyana; Bekker, Andrey (4 May 2018). "Ediacara biota flourished in oligotrophic and bacterially dominated marine environments across Baltica". Nature Communications 9 (1): 1807. doi:10.1038/s41467-018-04195-8. PMID 29728614. Bibcode: 2018NatCo...9.1807P.
31. ↑ Boag, Thomas H.; Stockey, Richard G.; Elder, Leanne E.; Hull, Pincelli M.; Sperling, Erik A. (12 December 2018). "Oxygen, temperature and the deep-marine stenothermal cradle of Ediacaran evolution". Proceedings of the Royal Society B: Biological Sciences 285 (1893): 1–10. doi:10.1098/rspb.2018.1724. PMID 30963899.

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