The evolution of ocean color

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1 The evolution of ocean color Victor Ariel Gallardo 1, 2, Carola Espinoza 1 1 Laboratorio de Bentos, Departamento de Oceanografía and Center for Biotechnology 2 Universidad de Concepción, Concepción, Chile ABSTRACT Analog examples of what primeval oceans might have looked in the Precambrian are probably extant in various regions and at various size scales in present day oceans albeit they have not been sufficiently recognized and/or studied. The Eastern Boundary Current Ecosystems (EBCEs), with their characteristic high productivity-inducing coastal upwelling events, their extensive and intensive anoxic/hypoxic water column and methane and sulfide-rich benthic environment, appear to represent such analogs. Moreover, recent studies have shown that they possess diverse anaerobic prokaryotic communities of mat-forming large multi-cellular filamentous bacteria similar to fossils found in Archean and Proterozoic rocks. Observations in the Bay of Concepcion, central Chile (~36 S), inserted in the second most productive EBCE of the world, suggests that given similar oceanographic dynamics, past oceans may have presented different predominant colorations after the first probable red color of the reduced iron-rich Archean ocean and prior to the present day blue color. In this coastal ecosystem a black coloration has been observed to form as the result of the floating to the surface layer of sulfide-blackened benthic detritus together with chunks of microbial mats, and a milky to turquoise coloration resulting from different concentrations of colloidal, nano-sized particles which may include elemental sulfur and/or microorganisms. If the present is the key to the past we posit that black color oceans could have existed during the Proterozoic Canfield sulfidic ocean followed by milky to turquoise colored oceans during later stages of the Proterozoic. Meso-scale examples of milky and turquoise portions of oceans, caused by elemental sulfur from oxidized hydrogen sulfide eruptions, have been described from off Namibia and there appear to also exist elsewhere. Examples of black oceans have apparently not been reported but the name of the Black Sea, the largest permanent anoxic basin on Earth, suggests that at some point in time it may have been black, at least locally and/or for short periods, prompting the name. We conclude suggesting that analogous to the present Blue Planet denomination, in the past our Earth could possibly have deserved the successive names of Red, Black and Milky-Turquoise Planet. Keywords: Ocean color, sea discoloration, Eastern Boundary Current Ecosystems, Proterozoic, Namibia. The Blue Planet 1. INTRODUCTION Fig. 1 MODIS Blue (Marble) Planet Earth true color composite (2002) 1 Ever since our planet was seen from space for the first time it became known as the Blue Planet due to the blue color of the oceans in present day Earth, covering a significant two thirds of its total surface area (Fig. 1). The blue color is an indication of the transparency of the ocean water in the large scale observation. But, could have oceans in the geological history of Earth had other predominant colors? Ocean conditions have strongly changed throughout time. 2 Just as from space Earth today looks predominantly blue and is believed by some to have been blue ever since the Archean, has it really been so? In this work, based on present day observations, we suggest that Earth oceans might have had other generalized colors. Thanks to Google Earth, it is a commonplace observation that oceans beyond the predominant blue of today exhibit localized and probably varyingly transient colors due to the various factors that affect the scattering of light, i.e., sediment plumes, phytoplankton and bacterial blooms, pollution, etc. 3 What we here address however are colors and causes that might have had the potential of giving a more persistent and distributed coloration to Earth in other periods of its geological history. For this purpose several analogs 1

2 of primeval oceans could be studied, 2 i.e., (1) natural: (i) the so-called Oxygen Minimum Zones (OMZs) overlying continental margins, including the major productive EBCEs such as the Benguela and the Humboldt ecosystems; (ii) the shelf areas of the Arabian Sea and the Sea of Bengal; (iii) the euxinic Baltic and Black Seas, and various major anoxic basins such as the Cariaco Basin, off Venezuela; (iv) fjords, mangrove swamps and productive estuaries; and (2) manimpacted: (i) the more or less extensive dead zones, such as the one off the Mississippi river; the Maracaibo Lake and the Gulf of Venezuela, in Venezuela, among many other situations, including the supposedly pollution-caused halo around Australia. 4 Of this list we will center our discussion mainly on observations performed in a small area of the Humboldt Eastern Boundary Current System but we will also use images from Google Earth. The red ocean To start let us consider the possibility of a red ocean, possibly suggesting a Red Planet. This condition could be related with the processes responsible for the rusting of the oceans resulting in the red Banded Iron Formations (BIFs), deposited intermittently from earlier than 3.5 to about 2 Ga ago. 2 How could this process have lent a red color to the oceans? The key may be in a recent finding of extremely small nanospheres of hematite ( nm in diameter) in BIFs from Australia. 5 This finding is considered a strong evidence for the occurrence, about 2.5 Ga ago, of colloidal ferric iron hydroxide particles in suspension in that primeval ocean resulting from the oxidation of Fe +2 by the incipient levels of oxygen photosynthetically produced by cyanobacteria and most probably also by other photosynthetic microorganisms. Although it is granted that presently these colloidal-size hematite nanospheres are features of limited known distribution, their widespread presence in the studied area strongly suggests that colloidal processes were important in the production of Precambrian BIFs, and as a consequence, in lending a red color to the oceans while formed in the pelagic realm. Thus, during the Archean, and given the history of recurrence of BIFs 2, in the Proterozoic, Earth could have looked, albeit sporadically, red from space. The black ocean In a similar way as ocean processes in the Archean could have tinted the oceans red what other long lasting colorations could have the oceans exhibited during later phases of the evolution of the ocean? And, are there today ecological analogs that could provide hints of how Earth could have looked under such different conditions as the rise in hydrogen sulfide and of dissolved oxygen in the ocean system? 2 The highly productive EBCEs, in general, contain hypoxic to anoxic water masses (Oxygen Minimum Zones OMZs) 6,7 that occasionally impinge on the sub-littoral and bathyal sea bottom creating unusual ecological oceanographic conditions in present day Earth, i.e., sediments and benthic boundary layers rich in hydrogen sulfide and methane, among other substances derived from the decomposition of organic matter, conditions probably somewhat similar to those in Proterozoic oceans. Besides, we have shown that these regions sustain rich and diverse mat-forming communities of giant non-photosynthetic sulfide-oxidizing filamentous multi-cellular 8, 9, 10 and unicellular spherical prokaryotes 11 some fully anaerobic and others chemolithoautotrophic microaerophilic organisms, similar morphologically to fossils found in Archean to Proterozoic rocks of different parts of the world 12, 13, 14. We thus posit that observations off central Chile, i.e., the Bay of Concepcion, ~36 S), a small scale portion of the Humboldt Eastern Boundary Current Ecosystem, could be tentatively considered likely analog of preterit Precambrian ocean conditions and their behavior suggesting also likely occurrences in the past. Most of our observations have been carried out during the recent years after the major El Niño , representing cold or normal ENSO conditions at this latitude (~36S). In spring-summer, at the peak of the highly productive seasonal cycle, a black or blackened discoloration in the most organically-loaded areas of the Bay of Concepcion has been observed due to surfacing of chunks of dark bottom detritus, including bacterial mat fragments, carried there by large bubbles of gasses resulting from the decomposition of bottom organic matter. The surrounding air is sulfide-smelling and bubbling is widespread (Fig. 2, a and b). While due to these emanations no casualties have been reported so far, the air conditions in warm summer days are quite unpleasant reminding a cesspool. It should be mentioned that besides the natural productivity of the bay waters, effluents from local fishery industries might contribute to the situation but these are considered minor compared to the naturally high 2

3 productivity of the bay. Research around this phenomenon and others described below are still minimal but we hope in this way to stimulate the scientific community to study them in the multidisciplinary manner that the problem requires. Fig. 2, a and b. Portions of sulfide-blackened detritus/bacterial mat matrix lifted from about 10 m depth by bubbles containing hydrogen sulfide and probably methane, as observed in the most organic matter-rich, anoxic of the Bay of Concepcion, central Chile. The background water is milky in color (see below). This phenomenon occurs during calm days of the austral summer months. Fotos: Jan. 4, Ever since the cyanobacteria 15,16, and probably too the recently discovered proteorhodopsin-bearing microbes, 17,18 started producing oxygen that rusted the oceans, the fall out of photosynthetic organic matter to the shallower seas would have eutrophicated the ocean bottom due to an increased burial of organic matter, 19 intensifying the anoxia. Sulfatereducing bacteria would have then produced hydrogen sulfide within an as yet inefficient anaerobiosis-driven ecosystem. This would be the so-called Canfield s sulfidic ocean 2. We posit thus that just as it happens in the Bay of Concepcion, the raise of black bottom matrices to the surface by bubbles of hydrogen sulfide and other decomposition gasses such as methane, could have also occurred in the Proterozoic with a generalized anoxic ocean bottoms, especially if the sea was not so deep as today, provoking, through similar mechanisms, the black coloring of large areas of the ocean, what we would rather call a cesspool ocean. The mechanism by which this phenomenon can happen has been dealt with and it has been termed an upward excursion to the sea surface of the chemocline allowing for massive eruptions of hydrogen sulfide. 20 Thus, massive releases of hydrogen sulfide would have been possible for more than a billion of years during the Proterozoic (and later) due to persistent oceanic anoxia under a low oxygen atmosphere and thus might have created black oceans, probably co-existing with the following situation, through the extensive distribution of black reduced bottom material. The milky to turquoise ocean Furthermore, in the same Bay of Concepción a milky to turquoise discoloration concurs with only a spatial separation from the previously discussed discoloration (Fig. 3). The photograph shows the discoloration of the Bay of Concepcion as seen from the North-East, spreading from the most organic matter-loaded and anoxic area at the head of the bay, just off the port of Talcahuano. The pattern of the color spreading clearly indicates that the source point of the discoloration is the SW corner of the bay. While the first record of this type of discoloration dates from 1956, a non-el Niño year, this series of discoloration phenomena started in 2001, i.e., three years after the last major El Niño of Previous to that our records are incomplete but an intense discoloration occurred in the years previous to El Niño and in the summer of From previous experience we are now convinced that the milky to turquoise ocean color occurs only during La Niña or normal cold phases of the ENSO cycle, with some lag time after the occurrence of the preceding EN event, probably to allow the system to become loaded with successive spring-summer-produced organic matter. The phenomenon appears to become more intense and long-lasting in the latter years however. While in early years the discoloration was observed for a few weeks at the end of the austral summer, in the latter two-three years it has started even in December and persisted almost continuously until the end of the summer. Although local studies are not yet conclusive as to what causes the milky to turquoise discoloration, preliminary chemical analyses indicate that elemental sulfur is present in the discolored water. It remains to be determined whether this elemental sulfur is the result of inorganic chemical reactions or it is biologically-mediated. A less extensive discoloration of the sea in the same Bay of 3

4 Concepción is observed in Fig 4 from Google Earth. The image was most surely obtained during our austral summer. Zooming of the Google Earth image allows resolving extremely fine detail, where black, milky and turquoise discolorations are discerned. Fig. 3. The photograph shows the inter-annually recurrent turquoise color of the Bay of Concepcion during the austral summer of Photo Didier Rousseau, Jan. 14, Fig. 4. Image of the Bay of Concepcion extracted from Google Earth (2008) where black, grey, milky and turquoise discolorations are discerned besides the dark green background. As mentioned above, similar discolorations attributed to colloidal granules of elemental sulfur resulting from the oxidation of hydrogen sulfide passing through oxygenated surface waters are reported from off Namibia (Fig. 5). 21,22 In the Black Sea it was found that the oxidation of hydrogen sulfide by oxygen resulted in thiosulfate and sulfate. Indirect evidence, however, suggested that the elemental sulfur found there was possibly produced by the oxidation of hydrogen sulfide by the abundant green phototrophic sulfur bacteria present in the chemocline. 23 It would be important to solve this issue, i.e., where and when is either inorganic or bacterially-mediated elemental sulfur being produced under anoxic or sub-oxic conditions, and whether the two processes can co-exist in the same location, and furthermore, how commonly they cause the milky to turquoise discolorations. An applied side to this knowledge has to do with the sardine and anchovy fisheries in the Chilean bay, since fishers see their catches diminished or vanished during the duration of this type of discolorations. Fig. 5. Satellite images for off Namibia showing a milky to turquoise discoloration: (a) March 18, (b) March 25, (c) March 29 and (d) April 3, According to the authors the milky turquoise coloration in the panels indicates high concentrations of suspended sulfur granules in the surface waters; redrawn from Weeks et al Whatever the cause of this type of the discoloration in the Bay of Concepcion, i.e., whether inorganicallyproduced colloidal elemental sulfur as suggested for that off Namibia or biologically mediated (or both), we here posit that their occurrence during long geologic periods in the late Proterozoic, during the so-called Canfield ocean, could have 4

5 lent a substantial and widespread milky to turquoise colorations to the ocean and thus originating perhaps black- milkyturquoise oceans. Through Google Earth it is nowadays possible to pin point a variety of local ocean discolorations that will stimulate research to unveil their specific causes and effects. Some of these discolorations may be caused by phenomena similar to those described from the Bay of Concepcion, others by phytoplankton blooms, pollution, etc. While there are several ocean color programs in the Internet mostly are focused on the subjects mentioned above and, except the Namibian situation, the possibility that some might correspond to colloidal elemental sulfur and their associated benthic processes is not considered. A related image extracted from Google Earth shows the Black Sea with a variety of colors ranging from black, dark blue, dark and light green, and mostly, turquoise (Fig. 6). The black coloration in the central south margin calls our attention because in the literature there is no plausible explanation as to the denomination Black Sea for this body of water. We suggest that it is possible that at some point in time a local black coloration like the one seen on this image off the central southwest coast of the Black Sea, might have prompted in forgone times the designation. Fig. 6. Image of the Black Sea extracted from Google Earth. There are many other examples of milky to turquoise discolorations both in Google Earth and other Internet sources which could help direct further enquiry. We present a few of these in Fig. 7. Fig. 7. Examples of pertinent sea discolorations: (1) NE corner of the Sea of Asov, (2) NE corner of the Caspian Sea; (3) SE corner of the Caspian Sea; (4) northern Tasmania, Australia, 4 (5) Bay of Bengal; (6) SE Isabella Island, Galapagos Archipelago, Ecuador; (7) Gulf of Martaban, Myanmar; (8) Van Diemen Gulf, Tasmania, Australia. Source: NASA images from Google Earth. Beyond the value of considering how Earth might have appeared differently colored in its past history, and of the underlying causes, our hope is that scientists will focus on discolored areas ( ground truth ), in particular, of those that might be reflecting the occurrence of microbial ecosystems, communities, species, and processes somewhat similar to those of ancient ocean environments. 5

6 ACKNOWLEDGEMENTS We express our deep gratitude to the Global Program Census of Marine Life for continuous support and encouragement and to the Chilean National Commission for Scientific and Technological Research (CONICYT/FONDECYT, Project ), for financing our research. We would also like to thank our students and members of the crew of our research vessel Kay Kay and Kay Kay II. REFERENCES 1. Stöckli, R., Vermote E., Saleous N., Simmon, R., Herring D. The Blue Marble Next Generation - A true color earth dataset including seasonal dynamics from MODIS, H. D. Holland, The oxygenation of the atmosphere and oceans, Philosophical Transactions R. Soc., 361, , R. Fearon, The coastal pollution halo. Paper prepared for the 2006 Australian State of the Environment Committee, Department of the Environment and Heritage, Camberra, 5. Ahn, J.H., P. R. Buseck, Hematite nanospheres of possible colloidal origin from a Precambrian Banded Iron Formation, Science, 250, , J.J. Helly, L.A. Levin, Global distribution of naturally occurring marine hypoxia on continental margins, Deep- Sea Research, I, 51, , L. A. Levin, Oxygen minimum zone benthos: adaptation and community response to hypoxia, Oceanography and Marine Biology: an Annual Review, 41, 1-45, V. A. Gallardo, Large benthic microbial communities in sulphide biota under Peru-Chile subsurface countercurrent, Nature (London), 268, , V. A. Gallardo, C. Espinoza, New communities of large filamentous sulfur bacteria in the eastern South Pacific, International Microbiology, 10, , V. A. Gallardo, C. Espinoza, Large multicellular filamentous bacteria under the oxygen minimum zone of the eastern South Pacific: a forgotten biosphere, in Instruments, Methods, and Missions for Astrobiology X, edited by Richard B. Hoover, Gilbert V. Levin, Alexei Y. Rozanov, Paul C. W. Davies, Proc. of SPIE 6694, 1H-11H, H. N. Schulz, Brinkhoff, T., Ferdelman, T. G., Hernández-Mariné, M., Teske, A., Jørgensen, B. B., Dense populations of a giant sulfur-bacterium in Namibian shelf sediments, Science, 284, , H. J. Hoffman, J. W. Schopf, Early Proterozoic microfossils. In: J. W. Schopf (ed.), Earth s earliest biosphere. Its origin and evolution. Princeton Press, NJ, USA, pp , J. W. Schopf, Atlas of representative Proterozoic microfossils. In: J. W. Schopf and C. Klein (eds.), The Proterozoic Biosphere. A multidisciplinary study. Cambridge University Press, Cambridge, MA, USA, pp , J.V. Bailey, S. B. Joye, K. M. Kalanetra, B. E. Flood, F. A. Corsetti. Evidence of giant sulphur bacteria in Neoproterozoic phosphorites, Nature, 445, , M. A. Arthur, Sageman, B. B., Marine black shales: depositional mechanisms and environments of ancient deposits, Ann. Rev. Earth Planet Sci., 22, J. Raymond, Segrè, D., The effect of oxygen on biochemical networks and the evolution of complex life, Science, 311, , D. B. Rusch, Halpern, A. L., Sutton, G., Heidelberg, K. B., Williamson, S. et al., The Sorcerer II Global Ocean sampling expedition: Northwest Atlantic through eastern tropical Pacific, PLoS Biol., 5, 3, e77, L. Gómez-Consarnau et al., Light stimulates growth of proteorhodopsin-containing marine Flavobacteria, Nature, 445, , D. E. Canfield, A new model for Proterozoic ocean chemistry, Nature, 396, , L. R. Kump, Pavlov, A., Arthur, M. A. Massive release of hydrogen sulphide to the surface cean and atmosphere during intervals of oceanic anoxia, Geology, 33, 5, ,

7 21. S. J. Weeks, Currie B., Bakun, Massive emissions of toxic gas in the Atlantic, Nature, 415, , S. J. Weeks, Currie B., Bakun, A., Peard, K. R. Hydrogen sulphide eruptions in the Atlantic Ocean off southern Africa: implications of a new view based on SeaWiFS satellite imagery, Deep-Sea Research, I 51, , B. B. Jørgensen, Fossing H., Wirsen, C. O., Jannasch, H. W., Sulfide oxidation in the anoxic Black Sea chemocline, Deep-Sea Research, 38, 2, S1083-S1103,

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