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Ocean chemistry and the evolution of multicellularity
Stockholm University, Faculty of Science, Department of Geological Sciences.
2012 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Oxygen has been assumed to be a vital trigger for the evolution of multicellular life forms on Earth, partly based on its power to promote substantial energy flux in cell respiration and partly as biosynthesis of compounds like collagen require oxygen. However, the co-evolution of large life and the Earth’s chemical environment is not well understood at present, and there is particular disagreement in the field about whether the Cambrian explosion of animal life forms was a chemical or biological event. Here, I discuss the evolution of multicellularity, divided in simple or complex forms, in light of the evolution of ocean water column chemistry in both the Proterozoic and the early Paleozoic. Even if the appearance of animals is confined to the Ediacaran, other fossil evidence of complex multicellularity can be argued to occur in the Paleo-, Meso- and Neoproterozic. These finds are, if anything, reason enough to keep searching for early experiments in complex multicellularity. In this search, we may have to expand our toolbox by looking at e.g. trace element aggregations and the isotopic composition of key elements. 

Research over the last couple of years have accentuated that much of the interval between the Ediacaran and the Devonian was dramatic with transitional ocean chemistry at the same time that large forms of animal life experienced dynamic radiation and ecological expansion. Results presented here describe some aspects of this time, including geochemistry from Chengjiang and a mechanism for preserving non-mineralized Cambrian animals that was partly dependent on specific ocean chemistry. Also, geochemical proxies using iron and molybdenum are used to infer a Paleozoic atmosphere with less than 50% of present levels of oxygen. The possibility that the subsequent rise is due to terrestrial plants and linked to the appearance of large predatory fish is discussed. Finally, the first mass extinction in the end-Ordovician is linked to low oxygen concentrations in the water column. It appears that more than oxygen was critical to allow the radiation of large life forms on Earth, but that chemistry and tectonic activity were intimately intertwined to biology, in a dance of permitting and being determined by certain aspects of ecology.

Abstract [sv]

Under lång tid har vi sett atmosfärens syrehalt som avgörande för att stora livsformer skulle börja utvecklas på jorden, delvis eftersom syre är ett energirikt bränsle men också för att det krävs vid sammansättningen av vissa ämnen som djur behöver, till exempel proteinet kollagen. Men, i själva verket, har vi inte lyckats reda ut detaljerna om hur utvecklingen av tidigt, stort liv och miljö satt samman, och om den kambriska explosionen framförallt var en biologisk eller kemiskt händelse. I den här avhandlingen diskuterar jag hur utvecklingen av flercellighet, då uppdelat i enkla och komplexa former, kan vara kopplad till hur havens kemi förändrats både i proterozoikum (2.5-0.5 miljarder år sedan) och paleozoikum (0.5-0 miljarder år sedan. Även om fossil från moderna djur dyker upp runt ediacaran och kambrium, så finns det långt äldre fossil som kan påvisa flercellighet. Dessa fossil ger, om inte annat, anledning att leta vidare efter fler spår av pre-kambrisk flercellighet och kanske kan vi utöka våra sökmetoder till att också tolka ansamlingar, eller isotopsammansättningar, av spårmetaller.

Den kambriska explosinen av djurliv (med startskott för 543 miljoner år sedan) är ett etablerat begrepp, men den senaste årens forskning har satt fokus på att en längre period, från ediacaran till devon, var en dynamisk tid med skiftande havskemi, nya djurarter och experimentella ekologiska nätverk. I den här avhandlingen presenteras några resultat som belyser just denna övergångstid, som geokemin i Chengjiang som beskriver hur havets kemi skiftar från syrefritt till sulfatfritt till syrerikt, och hur djur utan skal och ben kunde bli bevarade genom att flera unika förhållanden sammanföll. En annan studie visar hur molybden använts för att påvisa att atmosfärens syrehalt, under den här perioden, var högst hälften av vår moderna nivå. Vi hävdar att stigningen som skedde i devon, delvis tack vare växternas intåg på land, och att stigningen kan speglas i att fiskar först då hade råd att jaga och växa sig stora. Slutligen visar jag också på hur det första stora massutdöendet kan vara sammankopplat med syrefria hav, snarare än kyla och mer syre än djuren klarade av. Ett komplext samspel mellan flera kemiska ämnen, utöver syre, tektonisk aktivitet och biologi ser ut att höra samman med den dramatiska uvecklingen för stora livsformer på jorden.

Place, publisher, year, edition, pages
Stockholm: Department of Geological Sciences, Stockholm University , 2012. , 51 p.
Series
Meddelanden från Stockholms universitets institution för geologiska vetenskaper, 350
Keyword [en]
Geochemistry, biology, paleontology, evolution, multicellularity
National Category
Geochemistry
Research subject
Geochemistry
Identifiers
URN: urn:nbn:se:su:diva-75466ISBN: 978-91-7447-486-2 (print)OAI: oai:DiVA.org:su-75466DiVA: diva2:516750
Public defence
2012-06-11, William-Olssonsalen, Geovetenskapens hus, Svante Arrhenius väg 14, Stockholm, 13:00 (English)
Opponent
Supervisors
Available from: 2012-05-10 Created: 2012-04-19 Last updated: 2012-05-03Bibliographically approved
List of papers
1. Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago
Open this publication in new window or tab >>Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago
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2010 (English)In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 466, no 7302, 100-104 p.Article in journal (Refereed) Published
Abstract [en]

The evidence for macroscopic life during the Palaeoproterozoic era (2.5-1.6 Gyr ago) is controversial(1-5). Except for the nearly 2-Gyr-old coil-shaped fossil Grypania spiralis(6,7), which may have been eukaryotic, evidence for morphological and taxonomic bio-diversification of macroorganisms only occurs towards the beginning of the Mesoproterozoic era (1.6-1.0 Gyr)(8). Here we report the discovery of centimetre-sized structures from the 2.1-Gyr-old black shales of the Palaeoproterozoic Francevillian B Formation in Gabon, which we interpret as highly organized and spatially discrete populations of colonial organisms. The structures are up to 12 cm in size and have characteristic shapes, with a simple but distinct ground pattern of flexible sheets and, usually, a permeating radial fabric. Geochemical analyses suggest that the sediments were deposited under an oxygenated water column. Carbon and sulphur isotopic data indicate that the structures were distinct biogenic objects, fossilized by pyritization early in the formation of the rock. The growth patterns deduced from the fossil morphologies suggest that the organisms showed cell-to-cell signalling and coordinated responses, as is commonly associated with multicellular organization(9). The Gabon fossils, occurring after the 2.45-2.32-Gyr increase in atmospheric oxygen concentration(10), may be seen as ancient representatives of multicellular life, which expanded so rapidly 1.5 Gyr later, in the Cambrian explosion.

National Category
Geochemistry
Research subject
Geochemistry
Identifiers
urn:nbn:se:su:diva-48911 (URN)10.1038/nature09166 (DOI)000279343800042 ()
Note
21Available from: 2010-12-10 Created: 2010-12-10 Last updated: 2017-12-11Bibliographically approved
2. Burgess Shale-type biotas were not entirely burrowed away
Open this publication in new window or tab >>Burgess Shale-type biotas were not entirely burrowed away
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2012 (English)In: Geology, ISSN 0091-7613, E-ISSN 1943-2682, Vol. 40, no 3, 283-286 p.Article in journal (Refereed) Published
Abstract [en]

Burgess Shale–type biotas occur globally in the Cambrian record and offer unparalleled insight into the Cambrian explosion, the initial Phanerozoic radiation of the Metazoa. Deposits bearing exceptionally preserved soft-bodied fossils are unusually common in Cambrian strata; more than 40 are now known. The well-documented decline of soft-bodied preservation following the Middle Cambrian represents the closure of a taphonomic window that was only intermittently open in marine environments thereafter. The prevailing hypothesis for this secular shift in taphonomic conditions of outer shelf environments is that soft-bodied biotas were literally burrowed away from the fossil record by increasing infaunal activity in muddy substrate environments; this would have affected geochemical gradients and increased the efficiency of organic matter recycling in sediments. New and recently published data, however, suggest a more complex scenario. Ichnologic and microstratigraphic data from Burgess Shale–type deposits indicate that (1) bioturbation exerts a limiting effect on soft-bodied preservation; (2) the observed increase in the depth and extent of bioturbation following the Middle Cambrian would have restricted preservation of Burgess Shale?type biotas in a number of settings; but (3) increasing depth and extent of bioturbation would not have affected preservation in many other settings, including the most richly fossiliferous portions of the Chengjiang (China) deposit and the Greater Phyllopod Bed of the Burgess Shale (Canada). Therefore, increasing bioturbation cannot account for the apparent loss of this pathway from the fossil record, and requires that other circumstances, including, but not limited to, widespread benthic anoxia, facilitated widespread exceptional preservation in the Cambrian.

National Category
Geochemistry
Research subject
Geochemistry
Identifiers
urn:nbn:se:su:diva-75465 (URN)10.1130/G32555.1 (DOI)
Available from: 2012-04-19 Created: 2012-04-19 Last updated: 2017-12-07Bibliographically approved
3. The influence of sulfate concentration on soft-tissue decay and preservation
Open this publication in new window or tab >>The influence of sulfate concentration on soft-tissue decay and preservation
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2011 (English)In: Palaeontographica Canadiana No. 31: International Conference on the Cambrian Explosion - Proceedings / [ed] Paul A. Johnston & Kimberley J. Johnston, 2011, Vol. 31, 141-156 p.Conference paper, Published paper (Refereed)
Series
Palaeontographica Canadiana, ISSN 0821-7556 ; 31
National Category
Geochemistry
Research subject
Geochemistry
Identifiers
urn:nbn:se:su:diva-67664 (URN)978-1-897095-59-1 (ISBN)
Conference
The International Conference on the Cambrian Explosion - Charles Walcott and the Discovery of the Burgess Shale, Banff, Alberta, August 3-8, 2009
Available from: 2011-12-30 Created: 2011-12-30 Last updated: 2012-05-03Bibliographically approved
4. Mechanism for Burgess Shale-type preservation
Open this publication in new window or tab >>Mechanism for Burgess Shale-type preservation
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2012 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 109, no 14, 5180-5184 p.Article in journal (Refereed) Published
Abstract [en]

Exceptionally preserved fossil biotas of the Burgess Shale and a handful of other similar Cambrian deposits provide rare but critical insights into the early diversification of animals. The extraordinary preservation of labile tissues in these geographically widespread but temporally restricted soft-bodied fossil assemblages has remained enigmatic since Walcott’s initial discovery in 1909. Here, we demonstrate the mechanism of Burgess Shale-type preservation using sedimentologic and geochemical data from the Chengjiang, Burgess Shale, and five other principal Burgess Shale-type deposits. Sulfur isotope evidence from sedimentary pyrites reveals that the exquisite fossilization of organic remains as carbonaceous compressions resulted from early inhibition of microbial activity in the sediments by means of oxidant deprivation. Low sulfate concentrations in the global ocean and low-oxygen bottom water conditions at the sites of deposition resulted in reduced oxidant availability. Subsequently, rapid entombment of fossils in fine-grained sediments and early sealing of sediments by pervasive carbonate cements at bed tops restricted oxidant flux into the sediments. A permeability barrier, provided by bed-capping cements that were emplaced at the seafloor, is a feature that is shared among Burgess Shale-type deposits, and resulted from the unusually high alkalinity of Cambrian oceans. Thus, Burgess Shale-type preservation of soft-bodied fossil assemblages worldwide was promoted by unique aspects of early Paleozoic seawater chemistry that strongly impacted sediment diagenesis, providing a fundamentally unique record of the immediate aftermath of the “Cambrian explosion.”

Keyword
exceptional preservation, ocean chemistry, sedimentology
National Category
Geochemistry
Research subject
Geochemistry
Identifiers
urn:nbn:se:su:diva-75464 (URN)10.1073/pnas.1111784109 (DOI)000302294700022 ()
Available from: 2012-04-19 Created: 2012-04-19 Last updated: 2017-12-07Bibliographically approved
5. Devonian rise in atmospheric oxygen correlated to the radiations of terrestrial plants and large predatory fish
Open this publication in new window or tab >>Devonian rise in atmospheric oxygen correlated to the radiations of terrestrial plants and large predatory fish
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2010 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 107, no 42, 17911-17915 p.Article in journal (Refereed) Published
Abstract [en]

The evolution of Earth's biota is intimately linked to the oxygenation of the oceans and atmosphere. We use the isotopic composition and concentration of molybdenum (Mo) in sedimentary rocks to explore this relationship. Our results indicate two episodes of global ocean oxygenation. The first coincides with the emergence of the Ediacaran fauna, including large, motile bilaterian animals, ca. 550-560 million year ago (Ma), reinforcing previous geochemical indications that Earth surface oxygenation facilitated this radiation. The second, perhaps larger, oxygenation took place around 400 Ma, well after the initial rise of animals and, therefore, suggesting that early metazoans evolved in a relatively low oxygen environment. This later oxygenation correlates with the diversification of vascular plants, which likely contributed to increased oxygenation through the enhanced burial of organic carbon in sediments. It also correlates with a pronounced radiation of large predatory fish, animals with high oxygen demand. We thereby couple the redox history of the atmosphere and oceans to major events in animal evolution.

Keyword
Phanerozoic, molybdenum, black shale, ocean oxygenation, paleocean redox
National Category
Geochemistry
Research subject
Geochemistry
Identifiers
urn:nbn:se:su:diva-51687 (URN)10.1073/pnas.1011287107 (DOI)000283184800015 ()
Note
10Available from: 2011-01-12 Created: 2011-01-12 Last updated: 2017-12-11Bibliographically approved
6. Reply to Butterfield: The Devonian radiation of large predatory fish coincided with elevated athospheric oxygen levels
Open this publication in new window or tab >>Reply to Butterfield: The Devonian radiation of large predatory fish coincided with elevated athospheric oxygen levels
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2011 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 108, no 9, E29- p.Article in journal (Refereed) Published
Abstract [en]

We welcome this opportunity to clarify the conclusions and implications of our recent publication in PNAS. Butterfield (1) raises four issues regarding the oxygenation of the Paleozoic Earth's surface and its correlation to animal evolution. Our geochemical and paleontological data supported ocean oxygenation in the Silurian-Early Devonian (2), a critical transition in Earth history that influenced biogeochemical cycles and biological systems.

First, Butterfield suggests that evidence of charcoal in late Silurian rocks is incompatible with our claim that the earlier Paleozoic atmosphere had oxygen levels below 50% PAL (present-day atmospheric level). This counterargument rests on the assumption that the “fire window” of 62–166% PAL oxygen is well defined, but this is not the case (3).

National Category
Geochemistry
Research subject
Geochemistry
Identifiers
urn:nbn:se:su:diva-65878 (URN)10.1073/pnas.1018818108 (DOI)000287844400002 ()
Note
8Available from: 2011-12-15 Created: 2011-12-15 Last updated: 2017-12-08Bibliographically approved
7. Do large predatory fish track ocean oxygenation?
Open this publication in new window or tab >>Do large predatory fish track ocean oxygenation?
2011 (English)In: Communicative & Integrative Biology, ISSN 1942-0889, E-ISSN 1942-0889, Vol. 4, no 1, 92-94 p.Article in journal (Refereed) Published
Abstract [en]

The Devonian appearance of 1-10 meter long armored fish (placoderms) coincides with geochemical evidence recording a transition into fully oxygenated oceans.1 A comparison of extant fish shows that the large individuals are less tolerant to hypoxia than their smaller cousins. This leads us to hypothesize that Early Paleozoic O2 saturation levels were too low to support >1 meter size marine, predatory fish. According to a simple model, both oxygen uptake and oxygen demand scale positively with size, but the demand exceeds supply for the largest fish with an active, predatory life style. Therefore, the largest individuals may lead us to a lower limit on oceanic O2 concentrations. Our presented model suggests 2-10 meter long predators require >30-50% PAL while smaller fish would survive at <25% PAL. This is consistent with the hypothesis that low atmospheric oxygen pressure acted as an evolutionary barrier for fish to grow much above ~1 meter before the Devonian oxygenation.

National Category
Geochemistry
Research subject
Geochemistry
Identifiers
urn:nbn:se:su:diva-65872 (URN)10.4161/cib.4.1.14119 (DOI)
Available from: 2011-12-15 Created: 2011-12-15 Last updated: 2017-12-08Bibliographically approved
8. A sulfidic driver for the end-Ordovician mass extinction
Open this publication in new window or tab >>A sulfidic driver for the end-Ordovician mass extinction
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2012 (English)In: Earth and Planetary Science Letters, ISSN 0012-821X, E-ISSN 1385-013X, Vol. 331, 128-139 p.Article in journal (Refereed) Published
Abstract [en]

The end-Ordovician extinction consisted of two discrete pulses, both linked, in various ways, to glaciation at the South Pole. The first phase, starting just below the Normalograptus extraordinarius Zone, particularly affected nektonic and planktonic species, while the second pulse, associated with the Normalograptus persculptus Zone, was less selective. Glacially induced cooling and oxygenation are two of many suggested kill mechanisms for the end-Ordovician extinction, but a general consensus is lacking. We have used geochemical redox indicators, such as iron speciation, molybdenum concentrations, pyrite framboid size distribution and sulfur isotopes to analyze the geochemistry in three key Hirnantian sections. These indicators reveal that reducing conditions were occasionally present at all three sites before the first pulse of the end-Ordovician extinction, and that these conditions expanded towards the second pulse. Even though the N. extraordinarius Zone appears to have been a time of oxygenated deposition, pyrite is significantly enriched in 34S in our sections as well as in sections reported from South China. This suggests a widespread reduction in marine sulfate concentrations, which we attribute to an increase in pyrite burial during the early Hirnantian. The S-isotope excursion coincides with a major positive carbon isotope excursion indicating elevated rates of organic carbon burial as well. We argue that euxinic conditions prevailed and intensified in the early Hirnantian oceans, and that a concomitant global sea level lowering pushed the chemocline deeper than the depositional setting of our sites. In the N. persculptus Zone, an interval associated with a major sea level rise, our redox indicators suggests that euxinic conditions, and ferruginous in some places, encroached onto the continental shelves. In our model, the expansion of euxinic conditions during the N. extraordinarius Zone was generated by a reorganization of nutrient cycling during sea level fall, and we argue, overall, that these dynamics in ocean chemistry played an important role for the end-Ordovician mass extinction. During the first pulse of the extinction, euxinia and a steepened oxygen gradient in the water column caused habitat loss for deep-water benthic and nektonic organisms. During the second pulse, the transgression of anoxic water onto the continental shelves caused extinction in shallower habitats.

Keyword
mass extinction, Ordovician, geochemistry, sulfur
National Category
Geochemistry
Research subject
Geochemistry
Identifiers
urn:nbn:se:su:diva-75463 (URN)10.1016/j.epsl.2012.02.024 (DOI)000306030500012 ()
Available from: 2012-04-19 Created: 2012-04-19 Last updated: 2017-12-07Bibliographically approved

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