Int. Assoc. Sedimentol. Spec. Publ. (2011) 43, 315–392 Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines

JOHN K. WARREN International Master Program in Petroleum Geoscience, Department of Geology, Faculty of Science, Chulalongkorn University, Bangkok, 10330, Thailand. Formerly: Shell Professor in Carbonate Studies, Oil and Gas Research Centre, Sultan Qaboos University, Muscat, Oman (E-mail: [email protected])

ABSTRACT

Organic matter in modern saline systems tends to accumulate in bottom sediments beneath a density-stratified mass of saline water where layered hydrologies are subject to oscillations in salinity and brine level. Organic matter is not produced at a constant rate in such systems; rather, it is generated in pulses by a halotolerant community in response to relatively short times of less stressful conditions (brackish to mesohaline) that occur in the upper part of the layered hydrology. Accumulations of organic matter can occur in any layered brine lake or epeiric seaway when an upper less-saline water mass forms on top of nutrient-rich brines, or in wet mudflats wherever waters freshen in and above the uppermost few millimetres of a microbial mat. A flourishing community of halotolerant algae, bacteria and archaeal photosynthesizers drives the resulting biomass bloom. Brine freshening is a time of “feast” characterized by very high levels of organic productivity. In a stratified brine column (oligotrophic and meromictic) the typical producers are planktonic algal or cyanobacterial communities inhabiting the upper mesohaline portion of the stratified water mass. In mesohaline holomictic waters, where light penetrates to the water bottom, the organic-producing layer is typically the upper algal and bacterial portion of a benthic laminated microbialite characterized by elevated numbers of cyanobacteria. Short pulses of extremely high productivity in the upper freshened part of a stratified brine column create a high volume of organic detritus settling through the column and/or the enhanced construction of benthic microbial mats in regions where freshened waters reach the hypersaline base of the column. With the end of the freshening event, ongoing intensely arid conditions mean that salinity, temperature and osmotic stress increase rapidly in the previously freshened water mass. This leads to a time of mass die- off of the once flourishing mesohaline community (“famine”). First, these increasingly salty waters no longer support haloxene forms. Then, halotolerant life dies back, and finally by the halite precipitation stage, only a few halophilic archaea and bacteria remain in the brine column (typically acting as heterotrophs and fermenters). Repeated pulses of organic matter, created during a feasting event followed by a famine event, create laminated organic-enriched sediment on an anoxic bottom. There are three, possibly four, major mesohaline density-stratified settings where organic-rich laminites (petroleum source rocks) accumulated in ancient “famine or feast” saline settings: (1) basin-centre lows in marine-fed evaporitic drawdown basins, associated with basinwide evaporites; (2) mesohaline intra-shelf lows on epeiric plat- forms, associated with platform evaporites; (3) saline-bottomed lows in under-filled perennial saline lacustrine basins; (4) closed seafloor depressions in halokinetic deep- water marine slope and rise terrains. An inherently restrictive hydrology means that the same mesohaline settings show a propensity to evolve into regions characterized by the accumulation of widespread evaporite salts. If this happens soon after deposition of a layer of organic-rich sediment there is an increased likelihood of evaporite plugging in the source-rock layer, this in-turn decreases expulsion efficiency and downgrades the laminite bed’s ability to act as a prolific source rock. Keywords: Oil and gas, source rocks, halobiota, hypersaline, salinity

Ó 2011 International Association of Sedimentologists and published for them by Blackwell Publishing Ltd 317 318 J. K. Warren

INTRODUCTION

Back in 1988, Evans & Kirkland made the observa- tion that some 50% of the world’s oil may have been sourced in evaporitic carbonates. Heresy or not, the notion that much of the oil sealed by evaporite salts may also have also been sourced Oil-generating kerogen Gas-generating kerogen (sapropelic) (humic) in sediments deposited in earlier less saline, but A (Type I and II) (Type III) still related, evaporitic (mesohaline) conditions, is 20 Bacterial Bacterial worthy of consideration. The association between CH 4 CH4 saline waters, the accumulation of organic-rich Diagenesis Sapropelic Humic 50 (Eogenesis) sediments and the evolution of the resulting source source evaporitic carbonates into source rocks has been Ro<0.5% CO 2 CO2 noted by many, including: Woolnough (1937), C2H6+ Sloss (1953), Moody (1959), Dembicki et al. 100 (1976), Oehler et al. (1979), Malek-Aslani (1980), Catagenesis 0.5%

H2S Busson (1988), Evans & Kirkland (1988), Edgell H2S (1991), Hite & Anders (1991), Beydoun (1993), Metagenesis Benali et al. (1995), Billo (1996), Carroll (1998) and 200 2.0%

Table 1. Salinity-based classification of concentrated seawater and thalassic (seawater-like brines). Water density and dominant mineral precipitates are indicated (adapted from Warren, 2006)

Brine Stage Mineral precipitate Salinity Degree of Water loss Density (‰) evaporation (%) (g cm 3)

Brackish None <35 <1 0 1.000–1.040 Normal marine Alkaline earth carbonates 35 1 0 1.040 seawater (aragonite, Mg-calcite) Hypersaline Mesohaline Alkaline earth carbonates 35–140 1–4 0–75 1.040–1.100 or vitahaline (aragonite, Mg-calcite, dolomite) Penesaline CaSO4 (gypsum/anhydrite) 140–250 4–7 75-85 1.100–1.126 CaSO4 halite 250–350 7–11 85–90 1.126–1.214 Supersaline Halite (NaCl) >350 >11 >90 >1.214 Bittern salts (K-Mg) Extreme >60 99 >1.290

(icehouse climate mode). Bitterns at other times in All aerobic photosynthesizing organisms con- the Phanerozoic (greenhouse climate mode) tend tain the pigments chlorophyll-a and phycobilin to lack the MgSO4 minerals and have a propensity and use water as their electron source in reactions to form Mg-calcites in the mesohaline phase. that generate oxygen. Chlorophyll-a is a green Use of the term hypersaline in modern continen- pigment that absorbs red and blue-violet light, tal (non-marine) waters is much less well defined hence the typical green colour of photosynthesi- and is variably applied to waters with total dis- zers (Fig. 2A, B). It is made up of molecules that solved salt contents (TDS) that are more saline contain a porphyrin ‘head’ and a phytol ‘tail’ than 3 to 5‰. Nonmarine or continental waters (Fig. 2A). The polar (water-soluble) head is made can have ionic proportions considerably different up of a tetrapyrrole ring and a magnesium ion to seawater (athalassic), and so a broader range complexed to the nitrogen atoms of the ring, its of minerals can precipitate at all stages of brine phytol tail typically extends into the lipid layer of concentration. the thylakoid membrane. Phycobilisomes (phyco- cyanin, phycoerythrin) are proteins that absorb light of more energetic wavelengths than chloro- METABOLISM IN PRODUCERS phyll and are widespread pigments in the cyano- AND CONSUMERS bacteria and red algae (Fig. 2B). Their presence allows some members of the halotolerant com- Cyanobacteria and algae are the dominant pri- munity to photosynthesize into deeper brine and mary producers in most mesohaline waters, along sediment depths, where light with longer wave- with lower and varying inputs from the higher lengths is less transmitted and therefore less avail- plants and photosynthesizing bacteria. Algae and able directly to chlorophyllic photosynthesizers cyanobacteria typically make up the bulk of the (blue-green spectrum). Phycobilisome molecules planktonic biomass in the upper layer of a strati- are linear tetrapyrroles and are structurally related fied mesohaline brine column and construct the to chlorophyll-a, but lack the phytol side chain upper parts of microbial mats in oxygenated set- and the magnesium ion. In chlorophyll-rich tings where light penetrates to the water bottom. oxygen-evolving reaction centres in a cell (chlor- Cyanobacteria are prokaryotal (cell lacks a oplasts) the phycobilisomes help transmit photic nucleus) bacteria and, like eukaryotic (cell with energy and in cyanobacteria they are located in nucleus) algae and higher plants, are photoauto- chloroplasts in an extensive, intracellular system trophic and require oxygen to photosynthesize. of flattened, membranous sacs, called thylakoids, The typical aerobic photosynthetic reaction for all the outer surfaces of which are studded with three groups is: regular arrays of phycobilisome granules. Cyano-

CO2 þ 2H2O ¼ CH2O þ H2O þ O2 ð1Þ bacteria are the only prokaryotes that contain chlorophyll-a in their chloroplast and so show That is, carbon dioxide and water react in the strong affinity with the algae and the green presence of chlorophyll and sunlight to form car- plants. In the pre-genomic era of microbial studies bohydrate plus water plus oxygen. this meant they were typically classified as 320 J. K. Warren

Chlorophylls (oxic photosynthesis) Absorption spectra of photosynthetic pigments

Chlorophyll α Chlorophyll Phycoerythrin CH CH CH3 Phycocyanin 2 3 (universal in plants, O algae & cyanobacteria) H3C N N CO CH Mg 2 3 Chlorophyll α H N N H H C=CH CH CH CO CH CH=C(CH CH CH ) CH 2 2 3 2 2 2 2 2 3 3 Bacteriochlorophyll CH CH3 3 H CH3

Porphyrin head Phytyl tail Absorption

β-Caroten CH2CH3 CH3 Chlorophyll β O O (mostly in land plants) H C NN CO2CH3 Mg H N N H 250 300350 400 450 500 550 600 650 700 750 800 H C=CH 2 CH2CH3CO2CH2CH=C(CH2CH2CH2)3CH3 Ultra Violet Blue Green Yellow RedRed Infrared violet CH CH CH3 A 3 H 3 B Wavelength (nm)

Bacteriochlorophylls (anoxic photosynthesis) O O OH OH OH O

R NN R1 R1 1 NN NN NNR = Et, n-Pr, N N R = Et, n-Pr, Mg R1 = Et, n-Pr, 1 1 Mg Mg isobutyl Mg isobutyl, meopentyl Mg isobutyl N N N N N N R = Me, Et N N R2 = Me, Et N N R2 = Me, Et 2 R R2 R2 2

O O O O O OMe O O BChl a (purple sulphur bacteria) O OMe O O BChl b (purple sulphur bacteria) O O O phytyl, geranylgeranyl O O famesyl BChl c (green sulphur bacteria, phytyl O famesyl O famesyl chloroflexi = filament. green) BChl d (green sulphur bacteria) C BChl a BChl b BChl c BChl d BChl e BChl e (green sulphur bacteria)

Fig. 2. Structures and features of the main photosynthetic pigments. (A) Chlorophyll-a and -b showing porphyrin head and phytyl tail. Pink box shows difference in structure that defines the two forms. (B) Absorption spectra of the chlorophylls, b-carotene and phycobilisomes (phycoerythrin in dominant in blue-coloured cyanobacteria and phycocyanin in red- coloured cyanobacteria. (C) Bacteriochlorophyll structures.

“blue-green algae.” However, in terms of their donor, whereas the purple and green nonsulphur genomic signature and the fact that the cell lacks bacteria use electrons from hydrogen or organic a nucleus, they are better classified as prokaryotic substrates (Table 2). As in aerobic photosynthesis, bacteria. the resulting electrons (derived from the “light In contrast to the cyanobacteria, all other photo- reaction” of photosynthesis) are stored in glucose synthetic bacteria in saline waters are anaerobes and then used for CO2 fixation (aka the “dark and utilize a single type of photosynthetic reaction reaction” of photosynthesis). centre with a different pigment (bacteriochloro- The following simplified equation typifies phyll). When compared to chlorophyll and phy- anoxic photosynthesis of purple sulphur bacteria: cobilin, bacteriochlorophyll can absorb light with longer, less energy-rich wavelengths that extends CO2 þ 2H2S ¼ CH2O þ H2O þ 2S ð2Þ into the infrared spectrum. Such light-requiring bacteria (e.g. purple bacteria) live in anoxic con- That is, carbon dioxide and hydrogen sulphide ditions and their ability to utilize the infrared react with bacteriochlorophyll and sunlight to spectrum means they can thrive deeper in a sedi- form a carbohydrate (such as glucose) as well as ment or water column than aerobic photosynthe- water and sulphur. The light-absorbing pigments sizers (Figs 2B and 13). The green sulphur bacteria of the purple and green bacteria consist of bac- (Chlorobiaceae) and purple sulphur bacteria terial chlorophylls and carotenoids. Phycobilins, (Chromatiaceae) use elemental sulphur, sulphide, characteristic of the cyanobacteria, are not found thiosulphate, or hydrogen gas as the electron in these bacteria. All photoautotrophs (including Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 321

Table 2. Summary of Prokaryotes focusing on archaea and halophilic bacteria

Phylum or Informal group Metabolic lifestyles (selected halophilic family species)

Prokaryotes Halo-adapted Cyanobacteria Cyanobacteria Aerobic photoautotroph with chlorophyll-a bacteria plus phycobilicins, split water and generate oxygen (Arthrospira platensis, Dactylococcopsis sauna, Aphanothece halophytica, Microcoleus chthonoplastes) Proteobacteria Purple sulphur Anaerobic obligate photoautotroph – use bacteria H2S or sulphur as electron donor (Halorhodospira halophila may be a significant primary producer in some settings, e.g. at a halocline; Chromatium glycolicum, Ectothiorhodospira marismortui) Purple non-sulphur Anaerobic photoautotroph (tolerate low bacteria oxygen levels) – use hydrogen, but not from water, as the electron donor (e.g. Rhodospirillum sp.) Chlorobiaceae Green sulphur Anaerobic obligate photoautotroph – use bacteria H2S or sulphur as electron donor (Chlorobium limicola) Flexibacteria Green non-sulphur Anaerobic (thermophilic) photoautotroph – bacteria use hydrogen, but not from water, as the electron donor (Chloroflexus aurautiacus) Spirochetes Spirochetes Free-living obligate anaerobe (Spirochete halophila oxidizes Fe and Mn). Chemolithotrophic, some species can be symbiotic or parasitic Bacteriacea Flavobacteria Anaerobic organotrophs and chemoautotrophs, some species can be parasitic (Flavobacterium gondwanese and F. salegens are psychrotolerant halophiles isolated from Antarctic Lakes) (Salinibacter ruber is phylogenetically affiliated with this group) Archaea Euryarchaeota Halophile Aerobic photoautotroph, chemoautotroph (family Halobacteriales, includes: Halobacterium sp.; Haloarcula sp.; Halobaculum sp.; Halococcus sp.; Haloferax sp.; Natroncoccus sp.) Methanogen Anaerobic chemoautotroph (Methanocalculus sp., Methanohalophilus sp., Methanococcus sp.) Crenarchaeota Thermophile Anaerobic chemoautotroph (sulpho-archaea) (Crenarchaeota-domain clone sequences documented in hypersaline sediments including Shark Bay stromatolites, anthropogenic salterns and sediments of Lake Qinghai, China) Acidophile Aerobic- anaerobic chemoautotroph (as above), organotroph Nanoarchaeota Symbiont on Hosted on hot vent Archaea in Iceland. Its Ignoccus cell is only 400 nm long Korarchaeota New group of Only described from RNA samples (if it is a extreme real phylum then it is the closest to life’s thermophile universal ancestor of the earliest Archaean 3.7 Ga)

See Fig. 3 for additional information. 322 J. K. Warren higher plants, cyanobacteria and bacteria) contain Archaea are mostly extremophiles, that is they carotenoid pigments, which are red-orange and thrive in extreme conditions including: extremely yellow in colour as they absorb the blue-violet and saline (halophile), extremely hot (thermophile), blue-green wavelengths missed by chlorophyll extremely dry (xerophile), extremely acid (acido- (Fig. 2B). The green sulphur bacteria are probably phile), extremely alkaline (alkaliphile), and extre- the most energetically efficient of all phototrophic mely cold (psychrophile) environments. Some organisms and can live in environments with long- extremophiles are capable of surviving the multi- term light intensities that are less than 0.01% of plicity of extreme conditions that characterize typical daylight. Many purple and green sulphur arid environments and are known as polyextremo- bacteria store elemental sulphur as a reserve mate- philes (Kates et al., 1993). rial that, like glucose, can be further oxidized, in Archaea and bacteria that require extreme sali- this case to SO4, and so act as a photosynthetic nities to metabolize are called halophiles, those electron donor. that can tolerate salinities in excess of 25% are Modern chemoautotroph communities in saline termed hyperhalophiles, and almost all docu- microbial communities generally form a metabo- mented modern hyperhalophiles are archaea. lizing layer beneath the photosynthesizers (in One of the more impressive halophilic archaea is both mats and stratified brine columns) and on top Halobacterium lacusprofundi; it is both a halo- of the methanogens; some species in the chemo- phile and a psychrophile, it thrives in bottom waters autotrophic layer are lithotrophs. Lithotrophic of the supersaline (350‰) and cold (<0–11.7 C) sulphur oxidizers active in saline environments Deep Lake, Antarctica (Franzmann et al., 1988). include a number of species of both bacteria (e.g. The lake is too saline to freeze over, is thermally Thiobacillus) and archaea (e.g. Sulfolobus sp.). stratified and lies in an endoheic depression in the Thiobacillus is widespread in marine and hypersa- Vestfold Hills with a water surface that is some line microbialites and oxidizes thiosulphate and 50 m below sea level. elemental sulphur to sulphate. Other lithotrophic Throughout this paper, it will be discussed in bacteria use substances such as nitrate and reduce detail why microbes (archaea and bacteria) in sal- it to nitrite and include at least two species ine waters are halophilic, but it is notable that (Nitrobacter akalicus and Nitrosomas halophila) many halophiles are also thermophiles. World- that flourish in the freshened water stages in the wide, aerobic halophilic archaea of the order Kenyan soda lakes (Sorokin & Kuenen, 2005). Halobacteriales tend to have high growth optima Sulfolobus sp. tend to be hydrothermal vent dwell- at warm temperatures, typically between 35 and ers that prefer settings characterised by hot, saline 50 C and sometimes even higher (Oren, 2006). and acidic waters (see later). This may be an adaptation to the elevated temp- Sulfolobus is a species within the archaeal eratures that characterize stratified heliothermic domain (formerly known as the archaebacterial waters in salt lakes worldwide. Likewise, within domain), which constitutes the “third domain of the anaerobic halophilic bacteria of the order life” (see Glossary). While members of the archaea Haloanaerobiales there are several moderately ther- resemble bacteria in morphology and genomic mophilic representatives. Halothermothrix orenii, organization, they resemble eukarya in their the first truly thermophilic halophile discovered, method of genomic replication. The archaeal was isolated from Chott El Guettar, a warm saline domain is further subdivided into two kingdoms: lake in Tunisia. It grows optimally at 60 C and up the Crenarchaeota, of which all members pres- to 68 C at salt concentrations as high as 200‰ ently isolated are extreme thermophiles, and the (Cayol et al., 1994). The halophilic Acetohalobium Euryarchaeota, a diverse group, that includes the arabaticum strain Z7492 has a temperature opti- halophilic order Halobacteriaceae, certain thermo- mum of 55 C, can grow at salinities between 100‰ philes and all members of the methanogen group and 250‰ with an optimum around 150–180‰ (Table 2). All archaea are characterized by: (1) the and, like the halophilic archaea, has adapted to presence of characteristic tRNAs and ribosomal high salinities via the uptake of intracellular KCl RNAs; (2) the absence of peptidoglycan cell walls; (Zahran, 1997). (3) the presence of ether-linked lipids built from Even more extreme in its environmental prefer- branched-chain subunits; and (4) their occurrence ences is the archaea Sulfolobus tokodaii; it is a hot in unusual habitats (that seem extreme from an spring dweller and intracellularly transforms anthropocentric worldview). H2S to elemental sulphur. It flourishes at Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 323 temperatures in excess of 90 C and can live in acceptor. In aerobic respiration it is oxygen and the saline environments where pH hovers around 1. breakdown product is CO2, in anaerobic respira- Many such sulphur-dependant archaea are anae- tion it may be sulphate or nitrate and the break- robic chemoautotrophs that live in the vicinity of down product is H2S or nitrite. hydrothermal/volcanogenic vents in saline lacus- Halotolerant bacteria isolated from mesohaline trine rifts, or in marine hydrothermal brine springs, settings tend to be anoxygenic photosynthesizers or in the basal waters of density-stratified brine such as Chromatium salexigens, Thiocapsa halo- lakes and seaways. They also inhabit deep seafloor phila, and Rhodospirillum salinarum, with opti- brine pools on top of dissolving salt allochthons mal growth in these species between 60 and 110‰ and they can survive and possibly metabolize (Fig. 3; Caumette, 1993). In contrast to the cyano- hundreds of metres below the surface in bathy- bacteria, which are oxygenic phototrophs, these phreatic halite beds and sulphate caprocks (Grant anoxic phototrophs use H2S, organic compounds et al., 1998). Like these archaea, some chemoauto- or sulphur compounds as electron donors to pro- trophic bacteria can survive in extreme conditions, duce various oxidized sulphur metabolites, the even living in saline subterranean settings, as final product being sulphate. These anoxygenic evidenced by the recovery of viable halophilic halotolerant to halophilic photobacteria create chemolithotrophic bacteria (Haloanaerobium sp.) dense biogenic laminae in a variety of anoxic, from highly saline oil fields brines in Oklahoma generally poorly lit environments. Phototrophic where pore-water salinities are 150–200‰ sulphur-oxidizing bacteria in many salt lakes grow (Bhupathiraju et al., 1999). in narrow niches defined by interfaces that are Many halotolerant and halophilic bacteria and lit and also contain sulphide. In microbial mats archaea are heterotrophs feeding on the remains of they grow below the cyanobacterial and the photo- other organisms that had flourished in the same trophic bacterial layers, while in stratified brine water mass at lower salinities. Heterotrophic meta- columns they inhabit waters of the halocline. bolism shows variation in the terminal electron Intense blooms of purple or green sulphur bacteria

NaCl (‰) 50 100 150 200 250 300 Marine to slightly Chromatium buderi halophilic Chloroherpeton thalassium (15 to 60‰) Ectothiorhodospira mobilis Rhodobacter sulfidophilus Pelodictyon phaeum Rhodopseudomonas marina Ectothiorhodospira vacuolata Prosthecochloris phaeoasteroidea Thiorhodovibria winogradskyi Chlorobium chlorovibrioides Chromatium purpuratum Rhodobacter adriaticus Prosthecochloris aestuarii Chromatium vinosum HPC #Desulfobacter halotolerans

Moderately Rhodospirillum mediosalinum halophilic Rhodospirillum salexigens (30 to 150‰) Ectothiorhodospira marismortui Thiocapsa halophila Chromatium salexigens

Halophilic Ectothiorrhodospira abdelmalekii (sensu stricto) Rhodospirillum halophila (90 to 240‰) #Desulfovibrio halophilus #Desulfohalobium retbaense

Extremely Ectothiorhodospira halochloris halophilic Halorhodospira halophila (180 to 300‰) Salinibacter ruber

Fig. 3. Salinity tolerances of phototrophic halophilic bacteria, sulphate-reducers (#) and Salinibacter ruber. Star on bar indicates the salinity for optimal growth (after Ollivier et al., 1994; Caumette, 1993; Imhoff, 1988; Ventosa, 2006). 324 J. K. Warren can form brightly coloured water masses or sedi- sulphide-containing sediments form on the bottom ment layers. Most of the H2S they metabolize of modern coastal salinas and salt works well into is biogenic rising from below and generated by the penesaline salinity range (Oren, 2001). microbial sulphate reduction, except around brine Amongst the bacteria, most salt-tolerant halophilic springs and hydrothermal vents where there can sulphate-reducer thus far found is Desulfohalo- be high levels of abiogenic H2S (Knauth, 1998). The bium retbaense; it is a lactate oxidizer and was biodiversity of bacterial photosynthesizers fall off isolated from Lake Retba in Senegal. In the labora- as higher salinities are reached (Pedros-Ali o, 2005). tory it remained viable at NaCl concentrations of Purple and green bacteria growth is only possi- up to 240‰, with a growth optima of 100‰ (Olli- ble in settings where the chemical gradient of vier et al., 1994). Two other sulphate-reducing sulphide is stabilized against vertical mixing. In halophilic isolates are Desulfovibrio halophilus layered microbial mats this occurs at the interface and Desulfovibrio oxyclinae, which can tolerate between the oxygenated layer created by the photo- periods of NaCl concentration of up to 225‰ (Fig. 3; synthesizing cyanobacteria and the underlying Caumette, 1993; Krekeler et al., 1997). Another anoxic layer created by the sulphate reducers. In isolate, similar to Desulfovibrio halophilus has stratified brine columns, chemical gradients are been identified in brine pool samples collected in stabilized by density and temperature differences the allochthon-associated deep-water brine lakes between the cooler less saline surface waters and on the floor of the Red Sea where it grows in the warmer more saline bottom layers and so they salinities up to 240‰, but only slowly. tend to inhabit the halocline. Examples of sulphur- In sulphate reduction, the oxidation of acetate oxidizing bacteria in hypersaline settings include and CO2 yields more energy per cell compared to Atium volutans from Solar Lake, Beggiatoa alba the precursor oxidation of lactate. Recently the first from Guerrero Negro, and B. leptiformis from halophilic acetate-oxidizing sulphate-reducing Solar Lake (DasSarma & Arora, 2001). A unicellular bacterium was isolated: Desulfobacter halotoler- halophilic, chemoautotrophic sulphur-oxidizing ans (or Desulfohalobium utahense). It was col- bacterium, Thiobacillus halophilus, has also been lected from the hypersaline bottom sediments of described in a hypersaline Western Australia lake the North Arm of Great Salt Lake, Utah, and was where it grows in waters with salinities of up to found to have a rather restricted salinity tolerance, 240‰ (Wood & Kelly, 1991). it grows optimally at 10–20‰ NaCl, does not grow All modern halophilic sulphur-oxidizing bac- above 130‰ and is unable to survive above 240‰ teria are filamentous, CO2-fixers, typically motile NaCl (Fig. 3; Brandt & Ingvorsen, 1997; Jakobsen and utilize sulphide as an electron donor for their et al., 2006). Even so, it possesses the highest photosynthesis. Purple sulphur bacteria seem to NaCl-tolerance reported for any member of the flourish across a broad range of continental brine genus Desulfobacter. In terms of metabolic path- salinities. For example Ectothiorhodospira halo- ways in the various salt-tolerant or halophilic philic species dominate in the microbial sediments sulphate reducers, it seems species that oxidize of alkaline soda lakes in Egypt and Central Africa, lactate, such as Desulfovibrio halophilus, can tol- while the moderate halophile Ectothiorhodospira erate higher salinities of up to 250‰ than those marismortui is a strict anaerobe found in the species capable of oxidizing acetate, such as Desul- waters of hypersaline waters (170‰) of sulphur fobacter halotolerans, which do best in salinities of springs in the Dead Sea, where spring waters had a less than 100–120‰ (Figs 3 and 4). In contrast to the pH around 5.2 and a temperature of 40 C (Fig. 3). sulphate-reducers, it seems no viable sulphur-oxi- Isolates of this species grew poorly at a pH or dizing communities can survive at similar extreme 5.5 but thrived in the neutral pH range between salinities compared to the lactate oxidizers (Fig. 4). 7 and 8 (Oren et al., 1989). Another extremely Living below or among the sulphate-reducer halophilic sulphate-oxidizer Ectothiorhodospira communities in both microbial mats and stratified halochloris was isolated from Wadi Natrun in brine columns are the fermenters and the metha- 1977, in the laboratory it showed optimal growth nogens. One group of halophilic bacteria espe- in salinities in the range 140–270‰, a pH-range cially well adapted to the fermentative lifestyle between 8.1 and 9.1 and temperatures between is the Haloanaerobiales (Oren, 1992). Fermenters 47Cand50C (Fig. 3). live in anaerobic saline conditions when there is Dissimilatory sulphate reduction can occur up no electron acceptor, and different sugars and in to quite high salt concentrations and black, some cases amino acids are fermented to products Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 325

Salinity (‰) 0 100 200 300 Methanogenesis from acetate ? Autotrophic nitrite oxidation ? Autotrophic ammonia oxidation

Aerobic methane oxidation

Methanogenesis from H2 and CO2 Dissimilatory sulphate reduction – acetate oxidizers

Chemolithotrophic oxidation of sulphur compounds

Dissimilatory sulphate reduction – lactate oxidizers

Acetate formation from H2 and CO2 Fermentation

Methanogenesis from methylated amines

Denitrification

Aerobic respiration

Oxygenic photosynthesis

Anoxygenic photosynthesis

Fig. 4. Approximate upper salinity limits of selected microbial metabolic pathways (after Oren, 2001 and references therein). Values presented are based on laboratory studies of pure cultures (solid brown bars) and on activity measurements of natural communities in hypersaline environments (graded-colour extensions to bars). such as acetate, ethanol, butyrate, hydrogen, and the preservation of hydrogen-prone organic end- carbon dioxide. Fermentation breaks down an products (proto-kerogens). organic compound, such as a sugar or an amino Methanogens are archaea that create methane acid, into smaller organic molecules that then gas as they remove excess hydrogen and fermenta- accept the electrons released during the break- tion products produced by other forms of anaero- down of the energy source. When glucose is broken bic respiration. The methane then rises through down to lactic acid, each molecule of glucose the sediment or brine column to be utilized by the yields only two molecules of ATP, and consider- sulphate-reducers. Today some two-thirds to three able quantities of glucose must be degraded to quarters of the biogenic methane passed into provide sufficient energy for microbial growth. the atmosphere worldwide is the work of a few Fermentation means only a relatively small out- dozen species of methanogenic archaea most of put of energy per glucose molecule consumed as which live in relatively low salinity environments. any organic molecule is only partially oxidized. The remainder of the world’s methane comes from Fermentation tends to be the sole metabolic higher plants (Keppler et al., 2006; Houweling mechanism in the well-adapted halotolerant and et al., 2006). All methanogenic archaea are obligate halophilic species of the Haloanaerobiales that anaerobes thriving in three habitats: (a) bodies of inhabit the lowers parts of a microbial mat or brine anoxic fresh to hypersaline surface and subsurface column. It can be an emergency metabolic system water (e.g. the bottom brines of Solar Lake; (b) the in other microbes that find themselves in this vicinity of thermal brine springs; and (c) the diges- same environment. The presence of biomarkers tive tracts of ruminants). of fermentative microbes in saline and hypersaline The main methanogenic processes in freshwater Phanerozoic sediments or oils indicates deposi- environments and in the guts of ruminants are the tional conditions that were anoxic and highly reduction of CO2 with hydrogen and the aceticlastic stressed with respect to higher life forms. Such split mechanism where organic matter is split by brine- and pore-water conditions tend to facilitate oxido-reduction into methane and carbon dioxide, 326 J. K. Warren but neither of these reactions has been shown to Earth-bound primordial life first evolved as meth- occur at high salt concentrations (Oren, 2006 and anogens in hypersaline waters (Dundas, 1998; references therein). It seems that oxidation of organ- Knauth, 1998). ic matter is incomplete in settings with high levels Fermenters live in anaerobic saline conditions of NaCl when compared with that in other ecosys- using a metabolic pathway where there is no elec- tems (temperate lacustrine and marine ecosystems) tron acceptor, where different sugars, and in some where acetate, H2 þ CO2 are efficiently metabo- cases amino acids, are fermented to products such lized to produce CH4, or are oxidized by sul- as acetate, ethanol, butyrate, hydrogen and carbon phate-reducing bacteria whenever sulphate is dioxide (Hite & Anders, 1991). When evaporite available. At salinities higher than 150‰, the salts precipitate, these liquid organics are often mineralization of organic compounds is limited encased as brine inclusions in halite and other salt by poor rates, or the complete absence, of microbial crystals and so are not picked up in standard TOC sulphate reduction of acetate and the inherently determinations. Their relative contribution to any slow rates of methanogenesis utilizing H2 (Fig. 4). source rock potential is poorly understood in sub- The highest salt concentration at which such surface evaporitic systems where cross-flowing þ methanogenesis (from H2 CO2) occurs in nature basinal brines are dissolving buried halite beds. is in the 88‰ bottom waters of Mono Lake, Cali- They may be locally significant contributors volu- fornia (Fig. 4: Oremland & King, 1989). The result- metrically to the hydrocarbons moving in carrier ing accumulation of hydrogen and volatile fatty beds in contact with dissolving evaporites. acids (VFA) in saline sediment beneath brine col- The last groupings to be considered in this dis- umns more saline than this, implies that catabolism cussion of the various metabolic pathways active via interspecies hydrogen transfer hardly occurs at in hypersaline settings are the haloviruses and all in more hypersaline environments (Ollivier bacteriophages that must infect the haloarchaea et al., 1994). Hence sediment from the floor of the and bacteria. Compared to the literature-base for m Great Salt Lake contains up to 200 M dissolved H2. the halophilic archaea and bacteria little is known Similar results were obtained from Dead Sea sedi- and most published studies to date deal with the ments stimulated to reduce sulphate with H2 and haloviruses infecting the haloarchaea (Ventosa formate, although the same sediments did not 2006; Dyall-Smith et al., 2005). Nonetheless, given respond with acetate, propionate, or lactate treat- that in the natural world virus populations are ments. Energetic constraints may explain the greater than those of their prokaryotic hosts and apparent lack of truly halophilic methanogens cap- that each host species is susceptible to infection þ able of growing on H2 CO2 or on acetate, as these by several different viruses, it may be deduced methanogens use the energetically more expensive that a great diversity of such viruses must exist option of synthesizing organic osmotic solutes (see in hypersaline environments. later, “low salt in” discussion). Electron microscopy of hypersaline waters Methanogenesis occurs at much higher salt con- shows that they maintain high levels of virus-like centrations but only via a less productive meta- particles (about 10 times higher than the cell popu- bolic pathway that utilizes methylated amines, lation), with recognizable morphotypes including methanol, and dimethylsulphide substrates (Fig. 4; head–tail and lemon-shaped particles (Ventosa, Oren, 2001, 2006). The most salt-tolerant metha- 2006 and references therein). Guixa-Boixereu nogens known are Methanohalobium evestigatum et al. (1996) determined the abundance of viruses and M. portucalensis, which grow in up to in two different salterns in Spain and observed that 250–260‰ NaCl. Additional moderately halophi- the number of viruses increased in parallel to that lic methanogens have been isolated, growing opti- of prokaryotes, from 107 mL 1 in the lowest sali- mally at 40–120‰ salt (e.g. Methanohalophilus nity ponds to 109 mL 1 in the most concentrated mahii,M.halophilus,M.portocalensis,M.zhilinae). ponds (crystallizers), thus maintaining a propor- Modern halophilic methanogens can form rich tion of 10 virions per prokaryotic cell throughout microbial communities in the density-stratified the salinity gradient. A lemon-shaped virus was waters of deep-seafloor brine lakes, including found infecting square archaea; its abundance suprasalt allochthon areas on the deep Mediter- increased along the salinity gradient together with ranean seafloor where some anoxic bottom brines the abundance of the square archaea. Following have evolved to the bittern stage (MgCl2 saturation; a Dunaliella sp. bloom in freshened surface waters van der Wielen et al., 2005). It may well be that of the Dead Sea, Oren et al. (1997) observed the Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 327 presence of large numbers of virus-like particles in species grow and die (cycles of “famine or feast”). water (up to 107 virus-like particles mL 1), with a They can leave behind substantial volumes of oil- variety of morphologies, from spindle-shaped to prone organic residues in the bottom sediments, polyhedral and tailed phages. Details of the halo- especially in laminated mesohaline carbonates, biotal bloom in the Dead Sea will be discussed which on burial can evolve into prolific source later. It may be concluded that viruses and bacter- rocks. Even in modern saline environments, where iophages are abundant in the archaea and bacteria evaporite depositional settings are not as diverse or that inhabit hypersaline waters, but the various widespread as those of much of the past, conditions metabolic pathways operating within this infest- are such that mesohaline carbonates can preserve ing community have yet to be fully established and high levels of total organic carbon (TOC; Fig. 5). await further study. In summary, halophilic bacteria as a group are Salinity ranges of the modern halobiota capable of using several metabolic styles and so are more biochemically divergent than the halophilic Progressive brine concentration leads to sequential archaea. Some purple bacteria and gram-positive blooms of a macro and microbial biota adapted to bacteria are chemoautotrophic halophiles, while different ranges of salinity in both marine and halophilic cyanobacteria are oxygenic photoauto- continental settings (Fig. 6A and B). As a modern trophs. Under suitably stressed conditions many surface brine is concentrated from 60‰ to around halophilic bacteria become heterotrophic, utilizing 200‰, dense eukaryotic algal and cyanobacterial either anaerobic or aerobic respiration pathways. populations appear, grazed by ostracods, brine By evolving oxygen respiration some 2.5 billion shrimp and brine fly larvae. Halotolerant protozoa years ago, the cyanobacteria came to flourish and can be found feeding in this salinity range, as can ultimately displace the archaea. Ancient cyano- yeasts and other fungi (Gunde-Cimerman et al., bacteria lived in symbiosis with early eukaryotes; 2005). Halotolerant microbial mats cover the bot- by the Mesoproterozoic this had allowed eukaryo- tom of many hypersaline ponds and shallow lakes tic photosynthesis to develop and ultimately led in this salinity range. In anoxic waters in this salin- to the evolution of the higher plants and animals. ity range there are a variety of sulphur-oxidizing, Once oxygen was plentiful in the atmosphere sulphate-reducing, homoacetogenic, methanogenic (2.2 Ga), it was difficult for anaerobes (includ- and heterotrophic bacteria and archaea, especially ing photosynthesizing archaea and bacteria) to near the base of stratified brine columns or in the flourish in most surface waters. Some retreated lower parts of mesohaline microbial mats. to anaerobic environments, some acquired aerobic From about 240‰ to more than 320‰, red- bacteria as endosymbionts, and some continued orange haloarchaea (halophilic and hyperhalophi- to thrive in aerobic/dysaerobic conditions lic archaea) and halobacteria (e.g. Salinibacter that typify the hypersaline bottom waters of most ruber) come to dominate, mostly living on the density-stratified brine bodies. products of decomposing organic matter left over from an earlier lower salinity time (Pedros-Ali o, 2005). At the elevated salinities where these halo- BIOADAPTATIONS TO INCREASING philes and hyperhalophiles flourish, only a few SALINITY eukaryotes such as brine shrimp (Artemia and Parartemia sp.) can survive to graze on the remain- In 1957, in his classic book on evaporites, Lotze ing species of cyanobacteria and algae, especially made the statement: “Nicht das Leben, sondern der Dunaliella sp. – a unicellular green alga (Fig. 6A). Tod beherrscht die Salzbildungsstatten”€ (Not life, Above 300‰ no aerobic photosynthesis occurs, or but death rules the locales of salt deposition). at least is not known to occur based on the absence Saline environments were considered biotal of chlorophyll-a in the brines. As ever more ele- deserts, largely devoid of biological activity and vated salinities are attained, most other microbial hence were considered to be sedimentary systems activity first slows and then ceases. with little source rock potential. The following A variety of obligate and facultative halophytic discussion shows that this is not the case. Rather, plants can survive in the moderate-to-high salin- saline environments and water bodies are sites of ity soils that surround saline pans and lakes, e.g. periodic but intense organic activity where numer- Atriplex halimus, Mesembryanthemum crystalli- ous highly specialized algal, bacterial and archaeal num and Salicornia sp. Only a few species of 328 J. K. Warren

Solar Lake, Gulf of Aqaba (coastal salina) Laguna Guerro Negro, Baja California (coastal salina) Coorong ephemeral lakes, Australia (coastal salina) Lake Haywood, Australia (coastal salina) Kleberg Point lagoon, Baffin Bay (coastal salina) Coast Lake, Ross Is. Antarctica (cryogenic coastal salina) Harbour Is. Texas (restricted coastal lagoon) Laguna Lejia, Antofagasta, Chile (restricted coastal lagoon)

Perital or seepage Perital Abu Dhabi mats (saline mudflat) Abijan lagoon, Ivory Coast (restricted coastal lagoon) MARINE

Black Sea (silled sea) Red Sea (silled sea) Bahamian ooids (Caribbean marine platform) Gulf of Bacabano (Caribbean marine platform) Offshore Peru below upwelling (deep marine -15°S) Open marine Coriaco Trench (deep marine)

Lake Tanganyika (rift valley lake) Lake Kivu (rift valley lake) Lake Natron ("moat" facies in rift valley lake) Lake Nakuru (rift valley lake) Lake Rukwa (rift valley lake) Lake Urmia, Iran (continental collision lake)

Continental Lake Van, Turkey (continental collision lake)

NON- MARINE Dead Sea (continental transform lake) Salt Flat Playa, west Texas (continental dry mudflat) 0 5 10 15 20 25 30 35 Total organic carbon (% dry weight)

Fig. 5. Total organic carbon (TOC, dry wt%) in modern saline settings. Compiled from sources listed in Warren (1986, 2006). animal can tolerate hypersaline conditions compacta and Reticypris herbsti, copepods such as (Fig. 6A and B; DasSarma & Arora, 2001). The Nitocra lacustris and Robertsonia salsa, and brine highest salinity at which viable vertebrates have shrimps such as Artemia salina, Parartemia ziet- been observed is around 60‰. For example, the zianis and other related species. Brine shrimp sur- white-lipped or alkaline tilapid fish (Oreochromis vive a wide range of salinities from 25 to 240‰ with alcalica) flourishes in the mesohaline waters of the their optimal range around 60–100‰; they are African rift lakes. This setting includes thermal well adapted to the fluctuating oxygen and salinity spring waters at 36–40 C along the moat-like edges levels that characterize many mesohaline ecosys- of Lake Natron and Lake Magadi, where waters tems. Geddes 1975a–1975c argued that increased can have a pH as high as 10.5–11 and salinities in osmotic stress, not oxygen level, is the dominant excess of 65–70‰. limit on the upper salinity tolerance of Australian Large numbers of invertebrates can survive in brine shrimp (Parartemia zietzianis), and this is low to moderately mesohaline environments. probably also true for Artemia sp. (Geddes, 1981). Examples include salt-tolerant rotifers (aka wheel Halotolerant ostracods and brine shrimp feed on animalcules) such as Brachionus angularis and plankton living in the upper water mass of density- Keratella quadrata, and tubellarian worms (flat- stratified brine columns and ingest benthic mats worms) such as Macrostomum sp. Insects from where this less-saline water mass intersects the hypersaline environments include halotolerant lake margin or when bottom-water salinities are brine flies, such as Ephydra hians and E. gracillis, suitably lowered (de Deckker, 1981; De Deckker & which feed and lay their eggs in microbial mats Geddes, 1980). They produce pelleted carbonate and organic scum about the strandlines of modern detritus, which is a common component of saline lakes. Likewise, brine fly larva are adapted to many modern and ancient evaporitic laminites saline conditions, Ephydrella marshalli larvae col- (Warren, 2006). lected from commercial salt work lagoons on Port Diatoms (halotolerant bacillariophytal yellow- Phillip Bay, Victoria, have survived several days green algae with siliceous tests) are common plank- immersed in hypersaline sodium chloride media tonic forms in mesohaline and penesaline waters. at an osmotic concentration of 5848 mOsm L 1 They flourish at times of bloom in freshened salt- (175‰ NaCl; Marshall et al., 1995). lake waters or in zones of perennial seepage and Halotolerant crustaceans include ostracods such dissolution ponds (posas) about the edges of some as Cypridis torosa, Paracyprideinae sp., Diacypris salars. Their siliceous tests become a major detrital Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 329

Evaporation 1 1/2 1/4 1/7 1/11 ratio (Vi/Vo) Carbonate Transition Gypsum Halite domain domain domain 36-70‰ 70-140‰ 140-220‰ 220-300‰ >300‰

diatoms cyanobacteria green algae phototropic sulphur bacteria Artemia salina Parartemia zietziania Dunaliella A Halophilic archaea & eubacteria

Microalgae, cyanobacteria eubacteria & protozoa

Brine shrimp & brine fly larvae Fish & Red halophilic Biomass mangroves eubacteria & archaea Seagrass & seaweeds 35 100 150 200 250 B Salinity (‰)

EUBACTERIA ARCHAEA ces oup

teria ia teria my to elii

i ni

ia bacter

oteobac Planc van Cya oteobac bacterFlavobacterium gr sma

Pr bacter - exi -Pr

g Fl

nobacteria b les

teo oup -Proteo Chlamydia o Methanobacterium a ermopla

h

us jannaschi us

-Pr T d

ss thanococcus ospirillum gr Chlorob e Halobacteria ium M Methan Sp irochet es Met chaeoglobus

hanother rmococcus Ar Methanoco Met bus hanopyr mus The lfolo cus Clostridium Su llus us ococ Baci odictum oteus Heliobacterium Pyr DesulfurThermopr a ive bacteri Thermophilum -posit High-HC gram m obiu Thermomicr Thermus rmotoga The Halophilic members Aquifex

C EUKARYA

Fig. 6. Salinity tolerances of key biota. (A) Typical salinity ranges of the halotolerant biota where Vi is the volume of inflow to the basin and Vo is the volume of outflow (includes evaporation and reflux; after Barbe et al., 1990). (B) Typical salinity ranges and biomass proportions of the biota in modern marine saltwork ponds. (C) Phylogenetic tree of the bacteria and the archaea, based on 16S rRNA sequencing comparisons. Thick red lines indicate branches containing representatives able to grow at or near optimal rates at NaCl concentrations exceeding 15% (after Ventosa et al., 1998). component in some lacustrine stromatolites et al., 2000). The most halotolerant diatom taxa (Winsborough et al., 1994). Some halotolerant in the saltern ponds of Guerrero Negro, Baja varieties of diatoms live in mesohaline lake brines California Sur, Mexico, are Amphora subacutius- with salinities around 120‰, while the upper cula,Nitzschiafusiformis(bothAmphorataxa),and limit for diatom growth is around 180‰ (Clavero Entomoneis sp.; all grow well in salinities ranging 330 J. K. Warren from 5 to 150‰, Three strains of the diatom Pleur- found at a salinity exceeding 260‰ growing on osigma strigosum are unable to grow in salinities of submerged wood panels in the Great Salt Lake. less than 50‰ and so are true halophilic alga. Halophilic fungi (e.g. Polypaecilum pisce and In most moderately hypersaline (mesohaline to Basipetospora halophila) have also been isolated penesaline; 60–200‰) settings halotolerant cyano- as a cause of spoilage in salted fish and bacon, bacteria and green algae, rather than diatoms, are but their distribution in hypersaline waters is not the dominant primary organic producers and green well known. algal densities can be more than 105 mL 1. These Above 200–240‰ most photosynthetic algae and planktonic blooms can support many birds; one of halotolerant cyanobacteria cease to function and the most spectacular examples is the pink flamingo the halophilic archaea and bacteria come to population of African rift lakes. Mesohaline algae dominate, mostly as decomposers (Fig. 6A and B; are mostly obligately aerobic, photosynthetic, uni- Pedros-Ali o, 2005). The transition into a more cellular microorganisms with some species produ- archaeal-rich biota means that while eukaryotic cing large quantities of orange-coloured b-carotene metabolic pathways and biochemistry dominates pigment. Planktonic blooms in saline lakes can mesohaline waters, prokaryotic and archaeal meta- colour saline waters pink or red, especially at the bolisms come to dominate at higher salinities higher end of this salinity range. Green algae of the (see later biomarker discussion). genus Dunaliella (e.g. Dunaliella salina, D. parva, “Halobacteria” flourishing in supersaline waters and D. viridis) are ubiquitous in modern Northern belong to the archaeal family Halobacteriaceae. Hemisphere brine lakes, such as Great Salt Lake All known extremely halophilic archaea stain and the Dead Sea, and are the main source of food gram negative, do not form resting stages or spores, for brine shrimp and larvae of brine flies (DasSarma and reproduce by binary fission (Oren, 2006). & Arora, 2001). Most species of green algae are They are highly specialized micro-organisms, moderate halophiles, with only a few extremely most of which will not grow at total salt concen- halophilic species (e.g. Dunaliella salina and trations below 2.5–3 M (145–175‰ NaCl) and are Asteromonas gracilis) that survive in marginward destroyed by lower salinities (see cellular adap- refugia, even when the upper and low water layers tations). At present with the archaeal family in the Dead Sea are NaCl-saturated (see later). Halobacteriacea there are 14 known genera and Protozoa occur in most mesohaline waters, they 35 validly described species. Six of these genera are chemoheterotrophic protists that lack a cell are monotypic: Halobacterium; Halobaculum; wall and typically ingest algae and bacteria (Hauer Natrosomonas; Natrosobacterium; Halogeometri- & Rogerson, 2005). Identified species include cum; Haloterrigena. The other genera (Table 3; the moderate halophile Fabrea salina from a west Oren, 2006) are: Natrialba (2 species); Natrono- Australian salt lake and the extreme halophile coccus (2 species); Natrinema (2 species); Natror- Porodon utahensis from the Great Salt Lake. The ubrum (2 species); Halococcus (3 species); number of known protozoan species identified in Haloferax (4 species); Halorubrum (7 species), hypersaline waters (at salinities ranging from 90‰ Haloarcula (7 species). Halococcus sp. are strict to 220‰) has grown from <50 in the 1970s to more aerobes, their name reflects their coccoid cell than 200 today, and include a range of amoebae, shapes and they form pairs, tetrads, sarcinae or ciliates and flagellated protozoa. Fungi, mostly irregular clusters. Cells produce several orange yeasts, are another heterotrophic component of a or red carotenoid and retinal pigments needed to modern saline salt lake biomass (DasSarma & better cope with high levels of ultraviolet light Arora, 2001; Gunde-Cimerman et al., 2005). They that characterize supersaline brine settings. are chemoheterotrophic eukaryotes, some of which Haloferax prefers high-Mg waters and is a major are well adapted to tolerate markedly hypersaline constituent in the halophilic biota of the Dead environments. They grow best in aerobic con- Sea. The various Halococcoid species, along with ditions on carbohydrate substrates at moderate Haloferax and Haloarcula, flourish worldwide in temperatures and in acidic to neutral pH brines. hypersaline lakes, coastal salinas and brine lakes Debaromyces hansenii is a halotolerant yeast that, on the deep sea floor. when isolated from seawater, can grow aerobically Most interesting, but most problematic, are the in salinities up to 250‰ and is capable of assim- square-shaped archaea growing in many halite- ilating hydrocarbons. Another saprophytic hypho- precipitatingbrines.In1980,A.E.Walsbydescribed mycete (fungi), Cladosporium glycolicum, was the abundant presence of “square bacteria” in Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 331

Table 3. Constituent groups of the archaeal family Halobacteriaceae (after Oren, 2006)

Family Genus Species

Halobacteriaceae HalobacteriumT Halobacterium salinarumT Halobaculum Halobaculum gomorrenseT Halorubrum Halorubrum saccharovorumT H. sodomense H. lacusprofundi H. coriense H. distributum H. vacuolatum H. trapanicum Haloarcula Haloarcula vallismortisT H. marismortui H. hispanica H. japonica H. argentinensis H. mukohataei H. quadrata Natronomonas Natronomonas pharaonisT Halococcus Halococcus morrhuaeT H. saccharolyticus H. salifodinae Natrialba Natrialba asiaticaT N. magadii Natronobacterium Natronobacterium gregoryiT Halogeometricum Halogeometricum borinquenseT Natronococcus Natronococcus occultusT N. amylolyticus Haloferax Haloferax volcaniiT H.x gibbonsii H. denitrificans H. mediterranei Natrinema Natrinema pellirubrumT N. pallidum Haloterrigena Haloterrigena turkmenicaT Natronorubrum Natronorubrum bangenseT N. tibetense

T ¼ type genus of the family or type species of the genus. a small, halite-saturated brine pool, in the Sinai cells observed by Walsby were micro-organisms Peninsula (Walsby, 1980). These micro-organisms with a typical prokaryote structure. were collected from the surface of the pool, had Direct observations of brines of salterns and a large number of gas vesicles, and presented other hypersaline environments showed that these unique cell morphologies never observed pre- square cells were very abundant in such habitats, viously in the microbial world. The cells are especially in the most concentrated ponds with squares and very thin, with sizes from 1.5 to salinities higher than 3–4 M NaCl (at halite satura- 11 mm and a thickness of about 0.2 mm. Division tion, 175–233‰ NaCl), and they have been planes were observed, with an arrangement indi- reported to occur in many geographical locations cating that division occurred in two planes alter- in both the Northern and Southern Hemispheres nating at right angles, so that each square grows to (Oren, 1999a). For more than 20 years these were a rectangle which then divides into two equal considered uncultivable, until the work of Burns squares, producing sheets divided like postage et al. (2004) and Bolhuis et al. (2004), who inde- stamps (Walsby, 1980). In addition, different gas pendently cultivated what Bolhius and coworkers vesicles were observed, from spindle-shaped to informally named “Haloquadratum walsbyi”. The cylindrical with conical ends and, in many cases, isolation of the square archaea by two independent they were concentrated at the cell periphery. research groups introduced a new methodology Ultrastructure studies confirmed that the square that now permits the isolation of new fresh isolates 332 J. K. Warren of square archaea from various areas. Future work Until the late 1990s, when Salinibacter ruber will establish whether they are represented by a was first isolated and cultured from samples in single or several novel haloarchaeal species cap- anthropogenic salterns, the microbial popula- able of living amongst halite crystals. Work to date tion of halite-saturated waters was thought to be suggests that it is a new genus of the Halobacter- made up of a few species of archaea, including iaceae, rather than a species within the existing the distinctive archaeal phenotype with its square genera of the order. The question arises as to cell, which because of its unique four-sided mor- whether the square cellular shapes of this archaeal phology is widely known as the SHOW phylotype group, and the cubic outline of pores and inclu- (Square Haloarchaea Of Walsby; Bolhuis, 2005; sions in and amongst the halite meshwork it inha- Dyall-Smith et al., 2005). bits, are more than fortuitous. Two haloarchaeal It now seems that Salinibacter ruber is ubiqui- groups live only in high-pH high salinity waters of tous (some 5–25% of the biomass) in halite- soda lakes such as Wadi Natrun and Lake Magadi; saturated waters worldwide, and is typically com- these are Natronobacterium and Natronococcus. mingled with the SHOW phylotype (Anton et al., They grow only in hypersaline waters with high 2005). Most workers now agree that S. ruber and pH (8.5–11.0) and very low levels of Mg (<0.024 g the square haloarchaea are the dominant microbial L 1), and so are known as alkaliphiles. They have species at these elevated halite-saturated salinities not been found in marine-fed salterns or less alka- (Ventosa, 2006). Once isolated in pure culture, it line continental systems. However, the precise was evident that the similarity of S. ruber to many definition of genome systematics in halophiles haloarchaea could have hampered the isolation living in soda lakes is still in a state of flux (Grant of the bacterium. Both types of prokaryotes are et al., 1999). extremely similar at the phenotypic level: both are Haloarchaeal species growing at salt concen- extreme halophiles, aerobes, and heterotrophs trations above 150–200‰ characterize not only and pigmented by carotenoids. S. ruber, like many the Halobacteriaceae but also moderately halo- haloarchaea, accumulates high concentrations of philic methanogenic archaea, such as species of K þ to counterbalance the osmotic pressure of the Methanohalophilus and Methanococcus (Table 2; medium, has a high proportion of acidic amino Pfluger€ et al., 2005). The existence of methano- acids in its proteins, as well as enzymes functional genic archaea in hypersaline environments is at high salt concentrations and even has a high related to the presence of noncompetitive organic proportion of G þ C in its genome (65–70% for substrates such as methylamines, which origi- S. ruber, in the range of 59–70% for haloarchaea; nated mainly from the breakdown of osmoregula- Anton et al., 2005.). All these similarities, together tor amines, rather than the presence of carbon with the fact that S. ruber and “Haloquadratum dioxide, acetate and hydrogen (Fig. 4). The extre- walsbyi” dominate the biota in halite-saturated mely halophilic methanogen, Methanohalobium waters whenever prokaryotic density is high, pose evestigatum, with a NaCl optimum of 260‰,is interesting questions as to the evolutionary pro- also a thermophile with a temperature optimum cess. For example, what environmental conditions of 50 C. Halophilic methanogens are common in the Precambrian led to such a high degree of contributors to the biota of methane hydrates asso- metabolic similarity between two groups that now ciated with saline seeps and deep-sea brine pools occur in very genetically separate domains of life? above salt allochthons in the Gulf of Mexico It also shows that S. ruber is a bacterium that is as (Lanoil et al., 2001). Interestingly, unlike the Halo- halophilic and as salt dependant as any member of bactericaea, these various methanogenic species the Halobacteriaceae. seem to adapt to the increased salinity by a build Other than Salinibacter ruber, two groups of up of osmolytes in the cell, and so are not obligate halophilic bacteria are well represented in salinity halophiles. ranges in excess of 150‰; the fermentative bacteria As well as halophilic archaea, there are halo- belonging to the family Haloanaerobiaceae and philicbacteriaflourishinginwaterswithsali- the phototrophic sulphur-oxidizing bacteria of the nities in excess of 240‰. One of the most inter- family Ectothiorodhospiraceae (Figs 3 and 6C). esting is Salinibacter ruber; which can constitute Both groups are mostly made up of moderate between 5 and 25% of the prokaryotic community halophiles. Phototrophic halophilic bacteria are in a number of halite-saturated settings world- further divisible into purple and green bacteria wide (Anton et al., 2005; Bardavid et al., 2007). according to their respective bacteriochlorophylls Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 333 and carotenoids (Fig. 2C). For example, the shal- because they are more readily cultivated. Several low parts of soda lakes in the Wadi Natrun more recent studies carried out in actual hypersa- may be intensively red coloured due to the devel- line environments and not the culture dish have opment of Halorhodospira halophila (purple allowed some general conclusions to be drawn sulphur bacteria), while green non-sulphur bacter- (Ventosa, 2006): (a) square haloarchaea are very ia dominate the photosynthesizing layer of the abundant, but they have not been isolated (culti- hypersaline microbial mats in brines of similar vated) until recently; (b) many environmental salinity in Guerrero Negro, Baja Mexico (see “red clones within the haloarchaeal group are also waters and brines” in Glossary). Small brine pud- obtained from natural hypersaline settings that are dles in many hypersaline locations may show not phylogenetically closely related to previously separate development of green- and red-coloured described cultivated species of archaea and bacter- species of Halorhodospira, while top layers of the ia. In other words, the search to define the number sediments of Wadi Natrun lakes (Egypt) show of halophilic species and their relative contri- separate layers of the green-coloured and the bution to the biomass made up haloadaptive red-coloured Halorhodospira species (Imhoff microbes has only just begun. et al., 1979). Halorhodospira abdelmalekii, Halor- hodospira halochloris, and in particular Halorho- Cellular biochemical adaptations to hypersalinity dospira halophila are among the most halophilic phototrophic bacteria known (Imhoff, 1988). Iso- Halotolerant and halophilic species have devel- lates of Halorhodospira halophila from soda lakes oped special biochemical mechanisms to cope in the Wadi Natrun have salt optima of 250‰ with life’s fatal propensity to desiccate in mesoha- total salts and can survive in halite-saturated line and hypersaline waters, namely; motility, solutions (Fig. 3). slime, osmolytes and halo-adapted cellular mem- Oren (2001) has shown that in general in saline branes and proteins. Many of the halotolerant ecosystems the bioenergetic constraints of vari- cyanobacteria (still called “blue-green algae” by ous metabolic pathways at the cellular level define many geologists) form a significant component the upper salinity limit at which the different of photosynthesizing microbial mats in modern dissimilatory processes can occur (Fig. 4). Dissim- sabkhas and shallow brine lakes subject to both ilatory sulphate reduction of a lactate substrate periodic desiccation and hypersalinity. Such provides relatively little energy, and so the need microbial mats show a worldwide recurrence to spend a substantial part of the cell’s available of a few cosmopolitan cyanobacterial species: energy for the production of organic osmotic sol- Microcoleus chthonoplastes; Lyngbya sp.; Ento- utes probably sets the relative low upper limit to physalis sp.; and Synecococcus sp. All of these the salt concentration at which sulphate-reducing mat-forming taxa are embedded in matrices of bacteria can grow (Oren, 2001). extracellular polymeric mucous (slime), which Our understanding of which microbial species hold large amounts of water to protect the photo- dominate the halobiota at elevated salinities is synthesizing cell from osmotic stress and act as not yet fully developed. As Ventosa (2006) empha- a buffer against extreme temperatures and ultra- sized, numerous ecological studies have demon- violet rays (Gerdes et al., 2000a, 2000b). strate that haloarchaea may reach high cell densi- Aside from a greater likelihood of subaerial ties (>107 cells mL 1) in such hypersaline waters. desiccation, one of the effects of increasing salinity Traditional microbial studies based on cultivation is to increase osmotic pressure on all cellular life of viable cells from samples collected in such floating in a brine column. It may well be that the waters suggested that the predominant species dominant biomass control in subaqueous hyper- found in most neutrophilic hypersaline environ- saline and supersaline environments is not low- ments were related to the genera Halobacterium, ered oxygen levels but increased osmotic pressure. Halorubrum, Haloferax and Haloarcula. However, At a concentration of 300‰, a sodium chloride more recent molecular ecological studies based on brine exerts an osmotic pressure on a cell of more cultivation-independent methods indicate that, in than 100 atmospheres (Bass-Becking, 1928; Reed most natural hypersaline environments, members et al., 1984). Cells of haloxene species that typi- of these now well-documented halophilic genera cally inhabit marine or brackish waters quickly constitute no more than a small proportion of the desiccate in such brines, leading to rapid death microbial biomass. They are seen more often (e.g. Geddes, 1975b). 334 J. K. Warren

Accidental exposure of pelagic and bottom- algae can better cope with the high osmotic pres- living metazoans to osmotic stress and anoxia sure of its high salinity surrounds. Glycerol is an associated with hypersaline bottom waters has osmotically active substance (osmolyte) that takes contributed to many ancient lagerstatte associa- up space in the cellular fluids. It lowers the relative tions (fossil “death communities”), along with the water content of the cell and so raises the internal inherent excellent preservation of fine details of osmotic pressure. Cytoplasmic concentrations of the entrained largely undecomposed fossil forms. glycerol in Dunaliella parva can reach 7 mol L 1 For example, there are the numerous “death- and can constitute over 50% of the dry weight of dance” trackways in the Cretaceous Solnhofen cells growing in salinities 280‰. Glycerol is also micritic plattenkalk of Bavaria. The tracks lead used as an osmolyte by other halotolerant and to the fossil remains of intimately preserved mar- halophilic algae, as well as yeasts, fungi and brine ine crustaceans that once wandered into the high shrimp. Halotolerant and halophilic prokaryotes osmotic pressures associated with hypersaline can use a variety of other sugars, sugar alcohols, and anoxic bottom-waters of the lagoon that now amino acids and compounds derived from them preserves their remains (Viohl, 1996). Likewise, (such as glycine, betaine and ecotoine) as osmo- the feathers and skeleton of the bird-like dinosaur lytes, leading to characteristic biomarker assem- Archeopteryx were well preserved by the same blages in ancient saline sediments. anoxic hypersaline bottom waters. In contrast to an osmolyte solution, halophilic Communities of haloxene chemosynthetic mus- archaea have two main defence mechanisms to sels, which inhabit nutrient-rich deep dark bot- cope with the extreme osmotic gradients induced toms about the edges of modern anoxic brine lakes by hypersaline to supersaline waters. One is a modi- atop dissolving salt allochthons, can suffer mass fication of the plasma (cell) membrane; the other is extermination and immaculate preservation when an adaptation the protein structure itself. Unlike sediment slumps occur and these mollusc bios- most cell membranes, the plasma membrane of tromes are carried into lethal anoxic H2S-rich halophilic archaea is dominated by rhodopsins and hypersaline waters of the brine lake on the deep the cell membrane does not actively exclude salts, seafloor (MacDonald, 1992). Rich fossil-fish layers so the overall internal salt concentration in halo- characterize subaqueous lacustrine laminated archaeal cytoplasm is high. This adaptive mech- sediments of the Laney Shale Member of Eocene anism is sometimes called the “salt-in” strategy. Green River Formation. Almost all the fish in the However, the cell membrane is selective, it tends to lagerstatte are freshwater species, and this death exclude sodium, while actively pumping potas- assemblage indicates the presence of inimical sium into the cell against a thousand-fold concen- bottom waters tied to a salinity-stratified water tration gradient. The total ionic strength remains column. This stratified column formed during the the same on both sides of the plasma membrane, freshened highwater stage of the lake when dis- but the ratios of specific ions differ inside and solution of the underlying sodic evaporites of the outside the cell wall. Potassium is the dominant Wilkins Peak Member released brines that created cation within the cell, many cell functions require a condition of perennial anoxia in the deeper parts potassium, but would be disrupted by high levels of lake water column (Boyer, 1982). A similar brine of sodium. Cells of halophilic archaea can con- column stratification probably favoured the pre- tain up to 4 mol L 1 of potassium chloride, which servation of organic matter in the muddy lacus- is eight times its concentration in seawater. Anae- trine/lagoonal sediments that overlie the Mesozoic robic bacteria of the order Haloanaerobiales use Purbeck evaporites that crop out along the Dorset a similar “high potassium in the cell” strategy, as coast (Schnyder et al., 2009). does Salinibacter ruber (Oren, 1999b). Microbes that flourish in hypersaline waters have Halobacterium halobium is a well-studied adapted at the cellular level to survive the increased example of a well-adapted halophilic archaea; its osmotic stress that accompanies increased salinity. cell carries a combination of orange-red carotenoid At the intracellular molecular level, Dunaliella pigments, mostly b-carotene (C-40), and bacterior- parva, a halotolerant unicellular green alga that uberins (C-50). It is an aerobe-facultative anaerobe. flourishes in mesohaline waters worldwide (opti- When oxygen levels fall, but light penetrates the mum 120‰, survival 20–340‰), distributes gly- brine, photophosphorylation takes place in the cerol throughout its cytoplasm. This increases the absence of chlorophylls and redox carriers, so total solute concentration in the cell and so the waters and sediments where it flourishes can take Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 335 on a blue or purple tint. Bacteriorhodopsin’s proteins have evolved so as to maintain a high neg- characteristic purple colour has led to many ative charge on the protein surface. This attracts haloarchaea in their photo-active stage being water molecules and envelops the protein in a described historically (pre-genomic) as purple protective shroud of bound water. bacteria, not archaea. The main cellular metabo- Consider the halophilic archaea Haloarcula lism of Halobacterium halobium is heterotrophic marismortui, which flourishes during times of in brines with higher oxygen levels, and it freshened surface waters in the Dead Sea. Proteins flourishes in such conditions in Great Salt Lake, of its metabolic enzyme (malate dehydrogenase) Solar Lake and Lake Magadi. and its electron transfer protein (ferredoxin) are Cells in the heterotrophic mode are mostly wrapped in coats of acidic amino acid sidechains coloured by carotenoids, and waters where it is so that both proteins carry a negative charge in thriving appear red. This normal respiratory meta- neutral media. A predominance of charged amino bolic chain depends on b and c cytochromes as acids on the surfaces of cellular enzymes and well as cytochrome oxidase to create ATP. This is ribosomes better stabilizes the hydration shell of not a particularly unusual metabolic pathway for the various cytoplasm molecules, even when the most life forms, except that in this case the cell extracellular brines are well into the halite satura- itself is halophilic. As a result, in brines with tion field. This high-density surface charge binds relatively high levels of oxygen, these highly water molecules to the protein surface much more salt-adapted halophilic cells respire and produce effectively than any mesophile protein. Hence, ATP using their red membrane (carotenoids). Haloarcula proteins do not dehydrate or unfold Under anaerobic conditions they can survive but (denature) even when exposed to extremely high produce lesser volumes of ATP, either by fermen- salinities. However, the high levels of shielding tation of arginine or by anaerobic respiration with cations are lost by diffusion in low salinity envir- fumarate as an electron receptor. It means that they onments and an excess of negatively charged can still live, although at lower metabolic rates, ions then destabilizes the molecular structure in well-lit dysaerobic to anoxic hypersaline con- by ionic repulsion and so intracellular proteins ditions as they utilize their purple membrane tend to lyse or disintegrate. This means any spe- patches to pump protons and so maintain their cies using a “salt-in” cytoplasm strategy has an cellular metabolism (Oesterhelt & Marwan, 1993; innate restriction to highly saline environments Kates et al., 1993). (obligate halophiles) and does not cope well with Some halophilic archaeal strains, including rapidly oscillating schizohaline waters. Ironi- Halobacterium, contain another rhodopsin pig- cally, intracellular acids that unfold normal pro- ment in their purple membrane called halorhodop- teins in non-halophiles counteract this tendency sin. This acts as a Cl-pump, once again suitable for in the halophiles. generating energy in highly saline conditions. It In summary, bioadaptations at the cellular level is usually present in the cell membrane in much to highly saline conditions can be divided into two smaller amounts than bacteriorhodopsin, but con- groups of responses (Oren, 2001): tains the same retinal pigment. It too absorbs light, which it converts to an ion gradient. However, (a) The “high-salt-in” option instead of pumping protons out, like bacteriorho- Accumulation of salts in the cytoplasm dopsin, it pumps chloride ions inwards, which are maintained at concentrations equal to or helps maintain osmotic balance in highly saline higher than those of the outside medium. conditions. Since chloride ions have a negative Generally KCl is used as the main intracellular charge, moving chloride inwards is equivalent in salt. Aerobic halophilic archaea (family terms of energy to moving a proton outwards. Thus Halobacteriaceae) utilize this strategy, as do halorhodopsin generates a chloride ion gradient, fermenting bacteria, eubacterial acetogenic which also supplies energy to the cell. anaerobes (Haloanaerobium, Halobacteroides, Membrane adaptation shifts the osmotic balance Sporohalobacter, Acetohalobium), the extre- problem from the cellular to the molecular level. mely halophilic Salinibacter ruber and some Ions within the cell’s cytoplasm still compete with sulphate-reducers. Energetically, this strategy proteins and other biomolecules for that universal is relatively inexpensive, but requires far- solvent, water. In order to cope with high osmotic reaching adaptations of the intracellular enzy- stress at the molecular level, halophilic archaeal matic machinery to the presence of high salt 336 J. K. Warren

concentrations. Cells utilizing this strategy limited by the availability of inorganic nutrients show limited adaptability to changing salt con- and not by lack of light energy (Oren, 2001). Accord- centrations (obligate halophiles) and do best ingly, both oxygenic (Dunaliella,cyanobacteria) in environments where long-term salinities and anoxygenic phototrophs (Halorhodospira, remain elevated. That is, they do best in the Thiohalocapsa, Halochromatium) produce organic perennial hypersaline portions of salt lakes solutes for osmotic stabilization. They may be found such as the upper water mass of the Dead Sea up to very high salt concentrations and in several and do not do as well in parts of the deposi- cases survive well into the halite-saturation field. tional setting characterised by rapid and fre- However, in the case of chemolithotrophs and anae- quent bouts of schizohalinity. robic heterotrophs, the amount of energy generated (b) The “low-salt-in” option in the course of their dissimilatory metabolism is Exclusion of salts from the cytoplasm and the often insufficient to supply the demands of cell accumulation of organic osmotic “compatible” growth, osmotic adaptation, and life maintenance. solutes (osmolytes) may be employed to pro- Long-term growth and survival in hypersaline vide osmotic balance. This strategy is used by environments is not possible in such species. The halophilic and halotolerant eukaryotal micro- “high-salt-in” strategy is preferable for strongly organisms, by most salt-requiring and salt energy-limited organisms (haloarchaea) as it is tolerant bacteria, and also by halophilic metha- energetically much less costly than the production nogenic archaea. This strategy is energetically of organic osmotic solutes. Oren (2001) documen- expensive; the energetic cost depends on the ted an excellent correlation between the amount type of organic solute synthesized. No major of energy generated in the course of the different modification of the intracellular machinery is dissimilatory processes and the salinity-related needed compared to non-halophiles, and in occurrences of various metabolic styles (Fig. 4). most cases cells can rapidly adapt to changes Clearly the resulting biomarkers from the various in salinity. As such, they do better than the metabolic pathways will likewise preserve sali- “salt-in” biota in conditions of rapid and fre- nity-related indicator markers in the rock record. quent schizohalinity. Biomarkers and microbial responses As Oren (2001) clearly illustrated, organisms to salinity changes living in increasingly high salinity environments have to devote increasing large proportions of their The salinity-controlled transition between a halo- bioenergetic budgets to osmoregulation, either to tolerant and halophilic biota can been seen in their synthesize organic solutes or to activate and main- organic residues and subsequent biomarkers pre- tain ionic pumps. This creates a natural salinity- served in evaporitic source rocks. Biomarkers related control over various metabolic pathways can be thought of as molecular or chemical fossils and their energy efficiencies and hence to biomar- whose basic carbon skeleton is derived from once- ker distributions in the resulting sediments. The living organisms and are found in modern sedi- following metabolic adaptations and groups func- ments, as well as in petroleum and rock extracts. tion best at high salinities (Fig. 4): They can provide information about species diver- sity, depositional environment, thermal maturity, (1) Processes that use light as energy source and migration pathways and hydrocarbon alteration are generally not energy-limited; (Peters et al., 2005a, b). (2) Heterotrophs (bacteria as well as archaea) that Commonly accepted environmental generaliza- perform aerobic respiration, denitrification, tions based on biomarkers include the notion that and other dissimilatory processes that yield variation in the ratio between the isoprenoids large amounts of ATP; pristane and phytane indicates oxidizing versus (3) All types of metabolism performed by organ- reducing conditions (pristane and phytane are isms that use the “high-salt-in” strategy, even if both breakdown products of chlorophyll). In an the efficiency and amount of ATP obtained in oxidizing environment the cleavage of the phytol their dissimilatory metabolism is low. side chain of chlorophyll is followed by decarbox- ylation to produce phytane. In a reducing envi- Thus, the growth of phototrophic microorgan- ronment the sidechain cleavage of chlorophyll is isms in hypersaline surface waters is generally followed by its reduction to ultimately produce Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 337 pristane. Low pristane/phytane ratios in marine levels of phytane chains than bacteria and can and terrestrial settings are thought to indicate dominate the halobiota at higher salinities. reducing conditions, while higher values (>1) Phytane can also come from bacteriochlorophyll-a indicate oxidizing conditions (Table 4). Philp & and tocopherols, which can also be locally Lewis (1987) have shown that the chemistry of commonplace (Peters et al., 2005a, b; Koopmans chlorophyll breakdown is much more complicated et al., 1999). in many natural systems, and that variations in Likewise, differences in the distribution of the ratio may also indicate varying inputs from n-alkanes are thought to indicate depositional archaeal membranes, which contain much higher differences in the source contributors. Waxes in

Table 4. Depositional significance of selected biomarkers (see text for detail)

Setting Biomarker/indicator Detail

Hypersaline Gammacerane High relative to C31 hopanes in oils derived from sources deposited under hypersaline depositional conditions. High values indicate stratified water column during source deposition (Sinninghe Damste et al., 1995). Pristane/phytane Very low values (<0.5) in oils derived from source rocks deposited under hypersaline conditions, indicates contribution of phytane from halophilic bacteria/archaea (ten Haven et al., 1987, 1988). Acyclic isoprenoids Acyclic isoprenoid hydrocarbons are the predominant components in the organic matter extracted from sedimentary cores and oils of various hypersaline settings (Wang, 1998). Low diasteranes Oils from the hypersaline sources typically have very low amounts of diasteranes, which commonly suggests a source rock that has low content of catalytic clays, consistent with carbonate or evaporite source rocks (Mello & Maxwell, 1991; Peters & Moldowan, 1993). The amount of diasteranes in oils also decreases in highly reducing noncarbonate environments with increasing salinity (Philp & Lewis, 1987). Other biomarkers Even-over-odd dominance in the n-alkanes, presence of b-carotene and c-carotene, dominance of the C27 steranes. Organic sulphur There is a high abundance of organic sulphur compounds (thiolanes, compounds thianes, thiophenes and benzo-thiophenes) in many anoxic hypersaline settings (Wang, 1998). The distributions of the C-20 isoprenoid thiophenes in combination with those of the methylated 2-methyl-2-(4,8,12-trimethyltridecyl) chromans can be used to discriminate non-hypersaline from hypersaline paleoenvironments (Sinninghe Damste et al., 1989) 13 Carbon isotopes Heavy C values (20 to 30‰) are consistent with typical saline lake environments and reflect depletion of CO2 by photosynthetic organisms (Peters et al., 1996). Anoxic C35 homohopanes High relative to total hopanes in oils derived from source rocks deposited under anoxic conditions (Peters & Moldowan, 1993). Abundance of C35 homohopanes in oils (relative to C31–C34 homopanes) is correlated with source rock hydrogen index (Dahl et al., 1994). Pristane/phytane >1.0 can indicate anoxic conditions, but the ratio is affected by many other factors. Isorenieratane & Presence in oil indicates anoxic photic zone during source rock derivatives deposition, these compounds are biomarkers for green sulphur bacteria (Summons & Powell, 1987). V/(V þ Ni) Porphyrins High ¼ reducing conditions (Lewan, 1984). 28,30-bisnorhopane High in certain reducing environments (Schoell et al., 1992; Moldowan et al., 1994). Lacustrine Botryococcane Presence ¼ lacustrine source. Absence ¼ meaningless (e.g. Moldowan et al., 1985). b-Carotane Presence ¼ lacustrine source. Absence ¼ meaningless (Jiang & Fowler, 1986). Sterane/Hopanes Low in oils derived from lacustrine source rocks. (Moldowan et al., 1985) > C26/C25 tricyclic terpanes 1 in many lacustrine-shale-sourced oils (Zumberge, 1987) Tetracyclic polyprenoids High in oils from freshwater lacustrine sources (Holba et al., 2000). 338 J. K. Warren higher plants have significant concentrations of the non-marine highly saline environments (Peters & long chain C22–36 alkanes with a pronounced odd/ Moldowan, 1993). even distribution (Fig. 1A). Such organics tend to be For archaea, the cell membrane itself, due to its relatively rare in evaporitic source rocks, unless inherent high thermal stability, is a very good surface waters were periodically freshened by run- candidate for a biomarker. Archaeal cytoplasmic off from the land. Much of the terrestrial organic membranes do not contain the same lipids that material entering an evaporitic depression has been prokaryotes and eukaryotes do. Instead, their oxidized and biodegraded before it makes it to the membranes are formed from isoprene chains final site of deposition on the brine pool floor. In (ether lipids) made up from C5 isoprenoid units contrast, a high algal input is thought to be char- (as for the side chains of ubiquinone) rather than acterized by n-alkanes in the C16–18 region. C2 units (ester lipids) in the normal fatty acids of Waples et al. (1974), along with ten Haven the non-archaea (Fig. 7A). Moreover, the isopre- et al. (1986), noted that Tertiary sediments depos- noid chains are typically attached to glycerol by ited in saline evaporitic lagoons possess high con- ether linkages instead of esters. Thus the cell wall centrations of regular C25 isoprenoids (Table 4). of archaea is constructed of lipids, mainly of The activities of Chlorobiaceae, an anaerobic green glycerol, connected to phytanyl chains 20 carbons sulphur bacteria, thought to flourish in mesohaline in length by ether bonds to form phytanylic to hypersaline seaways, leads to the preservation diether. Typically these are organized in bilayers. of a series of 1-alkyl-2,3,6-trimethyl benzenes, In the case of archaea living in extreme con- thought to be derived from the breakdown of ditions, two glycerol molecules can be connected aromatic carotenoids in sulphate- and sulphide- to a double chain of phytanol to create a tetra- rich brines (Summons & Powell, 1987). ten Haven ether structure of forty carbons (Fig. 7B). Iso- et al. (1988) went on to propose a number of prene derivatives indicative of ancient archaea biomarker indicators of hypersalinity, including have been found in Mesozoic, Palaeozoic, and short-sidechain steranes and 5a(H), 14b(H), 17b(H) Precambrian sediments (Hahn & Haug, 1986). pregnanes and homopregnanes, as well as high Interestingly, their chemical traces have even gammacerane indices (gammacerane/C30 hopane). been found in sediments from the Isua district Gammacerane is a pentacyclic C30 triterpane of West Greenland, the oldest known sediments thought to be a diagenetic alteration product of on Earth, some 3.8 billion years old. tetrahymenol, a natural product produced by bac- Lipids entrained as organic residues in modern tiverous ciliates, such as Tetrahymena (Table 4). evaporitic carbonate and gypsum from modern At its simplest, much of the utility of biomarkers saline pans (mesohaline and lower penesaline in saline environments comes from salinity-related waters), are mostly derived from cyanobacteria and differences in contribution to organic matter of heterotrophic bacteria. Their n-alkane distributions the general categories of primary producers (auto- show a high predominance of n-docosane. Thus, trophs), namely prokaryotes (cyanobacteria and in the evaporitic carbonate domain (mesohaline bacteria) and eukaryotes (higher plants, algae) and waters), the presence of the C20 highly-branched the archaea. Most triterpanes are associated with isoprenoid olephines, tetrahymanol and large prokaryotic sources, whereas eukaryotic organisms amounts of phytol constitute precursors to most produce steranes. Thus, the triterpane/sterane lipids found in buried evaporitic sediments. In ratio can be a rough measure of the prokaryote/ contrast, the main lipid contributors in organics eukaryote contribution to the organic material. As accumulating in halites and bittern beds can be the salinity increases, the less salinity-tolerant eukar- extremely halophilic archaea and their organic yotic organisms (mostly sterane-producing green signatures are enriched in the isoprenoids, espe- algae) give way to more halotolerant bacteria and cially phytane (Barbe et al., 1990; Wang, 1998). cyanobacteria (tricyclic and hopane producers) However, both archaea and halophilic bacteria with a corresponding increase in the triterpane/ can flourish in upper penesaline and supersaline sterane ratio. Thus high alkalinity/salinity settings waters at salinities higher than 200–250‰, so the are characterized by tricyclics (C20–C24; m/z 191), biomarker signatures are not mutually exclusive b -carotene (C40H56 compound; m/z 125), gamma- (Caumette, 1993; Ollivier et al., 1994). Any high- cerane (C30 triterpane; m/z 191), all with prokar- salinity biota also includes the metabolic products yote sources. Hence, high levels of gammacerane of fermentators, homoacetogens, sulphate-reducers and b-carotene are typically associated with and methanogens. Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 339

A Headgroup Hydrophobic core Headgroup

O Diacyl glycerol Ester bond O P O CH2 + O H2C OH H3N Diacyl glycerol C O CH O 2 HC O C O O C O CH HC OH O H C O C 2 O CH O P O CH Bacterial lipid Ester bond 2 2 O

O

H C O P OCH Biphytanyl glycerol Ether bond 2 2 H C O 2 O C OH CO CH2 HC

HC OC CH OH O CH 2 C 2 H2C OH O Ether bond O CH2 Biphytanyl glycerol OH

Archaeal lipid HO OH

B 1.0 C

Lacustrine Cretaceous Normal marine Bucomazi Formation 0.8 environment 10 Angola

8 0.6 i nc re as 6 ing sa lin 0.4 ity 4 Pristane/Phytane

Mesohaline 10 x Gammacerane environment + Hopane Gammacerane 0.2 2 Hypersaline Jurassic Malm environment eastern Bavaria 0.0 0.0 0.2 0.4 0.6 0.8 1.0 1.8 2.0 2.2 2.4 MTTC ratio Pristane/Phytane

Fig. 7. Biomarkers: lipid structures and some rock characteristics. (A) Lipids from archaea and bacteria. Upper portion shows how phosphatidylanolamine forms a bi-layer lipid in bacterial cells. The acyl chain is usually, but not always straight. Some bacterial lipids have a methyl branch of a cyclohexal group at the end of the acyl chain, other lipids have one or more unsaturated bonds and the connection of glycerol to the acyl chain is via an ester linkage. The lower part shows how lipids are monolayers in archaea and the phytanyl chain contains isoprenoid-like branches. An ether linkage connects the phytanyl chain. Archaeal membranes also contain bilayer-forming diether lipids. (B) Relationship between pristane/phytane and the methyltrimethyltridecylchhroman (MTTC) ratio in Jurassic Malm carbonates of eastern Bavaria (after Schwark et al., 1998). The MTTC ratio is defined as 5,7,8-trimethylchroman/total MTTCs. (C) Variations in pristane/phytane ratio and the gammacerane index for oils from lacustrine source rocks in Angola (inset shows gammacerane structure). Independent biomarker evidence suggests a marine source for the point that lies off the shaded trend (after Peters et al., 2005a).

A predominance of degraded green algal and evaporite succession implies a subaqueous euha- cyanobacterial biomarkers in mesohaline settings line to mesohaline (30–40‰) transition into a is indicated by biomarkers preserved in organi- hypersaline marine-fed drawdown basin. These cally immature, evaporitic mesohaline laminates biomarkers are thought to have been derived from at the base of the Permian Zechstein evaporite green/purple sulphur bacteria (decomposers) succession in NW Europe (Bechtel & Puttmann, within organic-rich laminites and suggest that the 1997; Pancost et al., 2002). There the degree of bottom waters were saturated with H2S at the time methylation of 2-methyl-2-trimethyl-tridecylchro- of deposition. Maximum water depths were prob- mans (MTTCs) and the abundance of maleimides ably less than 100 metres (it was a stratified meso- and bacteriochlorophylls in the organic-rich haline drawdown basin at the onset of Zechstein Kupferschiefer shales at the base of the Zechstein salinity; Warren, 2006). Decomposers probably 340 J. K. Warren lived near the brine boundary between the photic associated reduced oxygen-levels in bottom waters. zone and the anoxic (euxinic) bottom water at Independent biomarker evidence suggests a mar- typical water depths of 10–30 metres below the ine source for the point that plots off the shaded water surface, as in modern marine-fed density- salinity trend in this figure. stratified systems, much like in Lake Mahoney Although the levels of entrained organics are today (Overmann et al., 1996). Primary production very low, similar covariant trends in pristane/ in the upper water column was dominated by phytane and gammacerane occur in C21–25 isopre- 13 photosynthetic cyanobacteria or green algae, while noids, along with relatively heavy d C signatures, sulphate reduction in the sediment was tied to in biomarkers extracted from the Miocene halites the availability of abundant sulphate and organic of the halokinetic Sedom Formation in Israel. They detritus from the overlying water column. indicate a predominance of halophilic archaea Methanogenesis was also active in or at the when the salt was deposited in a CO2 limited base of the water column during Kupferschiefer system (Grice et al., 1998; Schouten et al., 2001). deposition. This is reflected in the light carbon- Light and sulphide in modern hypersaline envir- isotopic composition of organic matter that had onments typically occur in opposing gradients, originated via recycling of CO2 generated by so the growth of halotolerant and halophilic photo- methane-oxidizing bacteria in the water column trophic sulphur bacteria is confined to narrow (Bechtel & Puttmann, 1997). Saccate pollen is the zones of overlap in stratified brine or water col- only morphologically preserved body fossil in umns. In Precambrian sediments bacterial life organic matter within the laminated Kupferschiefer forms were much more widespread in any water sediment, all other traces of cellular morphologies mass as the column was mostly anoxic. For exam- are gone. Euxinic (anoxic) conditions were con- ple, in Neoproterozoic and early Cambrian hyper- firmed by Pancost et al. (2002) over a much larger saline settings such as the Ara Salt Basin of area of Kupferschiefer deposition than studied Oman there were no higher life forms present in by Bechtel and Puttmann (1997). They concluded the depositional setting, and so this possibly nor- that almost all of the Kupferschiefer seaway was mal-marine setting, and the subsequent encase- subject to periods of photic zone stagnation and ment in salt, led to preservation of a unique set stratification during the early mesohaline history of bacterial biomarkers in blocks of salt-encased of the Zechstein Sea. marine platform source rocks (Terken et al., 2001; By themselves, high pristane/phytane ratios, Schoenherr et al., 2007). high amounts of gammacerane, and high MTTC The presence of mesohaline and marine carbo- ratios are not totally reliable indicators of hyper- nate muds, rather than aluminosilicate clays, in salinity. More reliable determinations can be made the matrix of many buried organic-rich evaporitic when two or more of these biomarkers are cross- source rocks can change maturity and migration plotted and the resulting output shows a consis- parameters compared with shale source rocks with tent trend. Figure 7B plots pristane/phytane ratio non-carbonate matrices. For example, mesohaline against the MTTC ratio in the Jurassic Malm Zeta carbonate source rocks are susceptible to early laminites of eastern Bavaria in SW Germany generation of bitumens and volatiles compared (Schwark et al., 1998). The plot shows a covariant with terrigenous shales (ten Haven et al., 1986; decrease in the two measures, which is interpreted di Primio & Horsfield, 1996). The proportion of as indicating a trend from normal marine to meso- bitumens (extractables) in the organics of carbo- haline deposition. nate source rock is high compared with that of A similar covariant trend can be seen in saline shales, as most mesohaline carbonates are largely lacustrine source rocks when the pristane/phytane isolated from high levels of terrigenous influx ratio is crossplotted against the gammacerane and the associated load of “spent” or oxidized index in Mesozoic source rocks from offshore West terrestrial organic matter (Warren, 1986). For Africa (Peters et al., 2005a). Figure 7C plots varia- the same reason, much of the early asphaltic tions in pristane/phytane (a redox and archaeal (hydrogen-prone) product in a mesohaline carbo- indicator) and gammacerane index for oils from nate laminite begins to migrate early in the burial a set of lacustrine source rocks. Increasing salinity history, driven in-part by recrystallization of the in the depositional setting explains the covari- carbonate matrix, whereas similar materials are ant trend in the plot, whereby higher salinity held to greater burial depths in the lattice of alu- was accompanied by density stratification and minosilicate clays (Warren, 1986; Cordell, 1992). Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 341

Espitalie et al., (1980) showed that carbonate salinity waters tend to float on top of higher salinity source rocks are likely to provide larger volumes waters. Depositional hydrologies in all modern of hydrocarbons for pooling compared with analo- and ancient evaporite systems are accordingly gous terrigenous shales for the same levels of TOC. layered and, as will be demonstrated below, the Geochemical analyses show that heavy oils from stability, temperature and salinity range of this carbonate source rocks can form at marginally layering largely controls whether and where organ- mature stages and at lower temperatures than ic matter accumulates in an evaporitic depression. required for oil generation from terrigenous shales Almost all primary organic matter in an evapori- (Jones, 1984). tic source rock was first photosynthesized in Lastly, some widely-used biomarker-derived surface brines outcropping at the top of the active maturity indicators formulated in marine sedi- phreatic zone or its capillary fringe. An active ments, are not as reliable in relatively young sal- phreatic flow regime encompasses the zones of ine-lacustrine basins or in hypersaline oils with seepage outflow, brine/seaway ponding, brine high sulphur contents, such as those sourced from reflux and meteoric flow. The brine surface of a hypersaline Oligocene laminites in the northern perennial brine lake or seaway is the outcropping Qaidam Basin, China or the Miocene mesohaline expression of the regional water table, and in carbonates of the Mediterranean (Hanson et al., marine-drawdown basins is by definition lower 2001; di Primio & Horsfield, 1996). The discre- than sea level. In the surrounds, where the regional pancy between mature indications coming from water table comes near the landsurface, the top of a vitrinite in these very young evaporitic source capillary fringe may be the outcrop expression of rocks and the immature indications derived from the same regional water table and so is the depo- various sterane isomerization ratios or other stan- sitional area where sabkhas dominate (Warren, dard source rock evaluation techniques, are in part 2006). Solar evaporation concentrates waters in explained by a lack of time for various sterane both ponded and vadose settings to form matrices equilibria to develop and by the complicating of bottom-nucleated and sabkha salts, respectively. effects of high sulphur levels on reaction kinetics Depressions with surface and near-surface brines in in systems with high levels of early asphaltenes. arid settings indicate groundwater discharge zones Some of these hypersaline heavy oils in China and their long-term outcropping creates discharge come from hydrogen-rich type-I lacustrine sources playas and ancient evaporite seaways. that may be as little as 3 million years old in the Where areas of strong topographic relief define Qaidam Basin. the margin of a modern evaporite basin, both unconfined and confined meteoric waters typi- cally discharge into the edges of a brine-saturated LAYERED BRINES AND ORGANIC depression, as in modern continental rift valleys of SIGNATURE the East African rift, or in a transtensional basin- and-range setting of the American southwest, or So far the biological factors and metabolic path- in the Dead Sea of the Middle East. Farther out, ways that control the type and volume of organic beneath the more central and topographically matter accumulating in saline settings have been lowest parts of the evaporite depression, density- discussed, without much consideration of the phy- induced brine reflux, and not meteoric throughput, sical conditions or hydrologies that control the is the dominant process driving shallow-subsur- condition or position of the brine and pore fluids face brine flow. The saline water mass driving this in which the organics accumulated. The presence reflux may be an ephemeral or perennial holomic- or absence of organics in an evaporite basin is tic surface water. Which hydrological style of sur- predicated on suitable hydrologies to manufacture face water dominates in an evaporite basin the requisite factors to create anoxia. Penecontem- (ephemeral versus perennial) is in part related to poraneously, the hydrological conditions of early the steepness of the surrounding topography and burial control whether organics are to be preserved the presence or absence of a hydrological conduit in its evaporitic matrix until any protokerogen is for water outflow (Warren, 2006). sufficiently buried to evolve into a source rock. In a large evaporite drawdown basin, such as in Brine density increases with increasing salinity, the Mediterranean in the Late Miocene, the basin so influxes of less dense brines into an evaporitic typically had no surface connection to the ocean, depression create a layered system where lower and the level of the discharge zone and the water 342 J. K. Warren surface of the perennial brine discharge lake was at (1) a perennial seaway or a brine lake that at times is times thousands of metres below sea level. Gravity- density stratified; and (2) an evaporitic mudflat induced seepage and associated evaporation of (sabkha) with a surface defined by the top of the surface waters cycled huge volumes of marine/ capillary fringe and its most saline water lying at or meteoric waters through the depression’s sur- just below the sediment surface. A common inter- rounds and into the drawdown depression. Reflux mediary stage is an evaporitic mudflat occasionally beneath a stratified perennial meromictic water covered by thin sluggish brine sheets (salt pan). mass is at its maximum when the brine column The hydrology of an evaporitic mudflat and its is holomictic (Warren, 2006). landward surrounds is controlled by the position of the water table in the sediments (Fig. 8A). Pores below the water table are filled by brine and make Hydrologies in saline basins up the phreatic or saturated zone where the water- Hydrological settings that allow most evaporitic volume saturation is total (equal to 1 or 100%). The carbonates and associated organics to accumulate phreatic zone is the region where gravity-driven can be divided into two end member situations: groundwaters seep down the potentiometric slope

Ground surface Evapotranspiration Soil moisture drives moisture changes zone

Potential for Vadose Unsaturated Moisture deflation zone zone distribution Matrix with air and varying water/brine in pores Stokes Surface (sabkha surface) Capillary fringe Water table 0 Saturation 100% Phreatic Saturated (Phreatic surface) zone zone

Hydrological Zones Matrix with water/brine A filled pores

NON-STRATIFIED Salinity Temperature

hypersaline Holomictic Depth bottom nucleates Brine reflux

STRATIFIED Salinity Temperature fresher halocline thermocline

hypersaline Depth pelagic cumulates Meromictic or Oligomictic Heliothermal B

Fig. 8. Hydrological classification in saline settings. (A) Hydrological zonation in an evaporitic mudflat (sabkha) and its landward surrounds. (B) Water mass zonation in a perennial brine lake or seaway (after Warren, 2006). Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 343 toward discharge zones (forced-convection) and sediments below the water table (sabkha-driven dense free-convecting brines sink into underlying brine reflux). As long as brine can be supplied from strata. Above the water table is the vadose zone, an updip source, closed cellular flow beneath the where pores are filled by a combination of soil air wet sabkha flat is the result. In a capillary zone- and varying levels of water and brine and water- bound system that is also subsiding, such wet volume saturation is less than one. sabkha hydrologies can retain continual hypersa- line brine saturation with associated dysaerobia or anoxia, and so sequences of hydrogen-prone Vadose hydrologies microbial organic matter can accumulate as mats The vadose zone in dry mudflats contains an and so be preserved into the burial environment. uppermost interval where the water content and Given enough time, waters in a brine plume the oxygen/CO2 content of the pore waters can vary beneath a wet sabkha or a periodically holomictic considerably and is known as the soil moisture brine lake will reach the bottom of the basin fill or zone. Light rains on a dry mudflat typically pene- be dispersed back into the regional cross flow on trate the soil moisture zone but are not sufficient in top of any aquiclude it intersects on its way down volume to saturate the pore space of the whole (Wood et al., 2002; Warren, 2006). In either case, vadose zone, and so are returned to the atmosphere the refluxed waters start to spread laterally and via evapotranspiration without ever replenishing back out toward the basin fringes, so mixing with the water table (Wood et al., 2002). Fluctuating fresher forced-convection waters beneath the lake, evapotranspiration levels in this zone vary widely playa or seaway margin. Ultimately this brine between storms, driven in part by the metabolic returns to the playa surface, usually in a diluted activities of the soil biota, by mean moisture con- form as a component of water-edge spring or seep tents, and by varying O2 and CO2 levels. Pedogenic waters. This convective flow is an effective way of carbonates and more soluble salts are precipitated moving salt load through large volumes of the basin as surface crusts and near-surface cements as a sediments beneath an accumulating salt bed, and result of these fluctuations. yet still maintain anoxic pore waters beneath a wet Ongoing and periodic oxidation of this vadose sabkha or salt lake (see discussion of brine curtains hydrology means any hydrogen-rich microbial in Warren 2006). Ongoing recycling of anoxic brine material tends to be decomposed/oxidized prior beneath a salt lake or seaway in-turn aids in the to burial. Dry mudflats in saline depressions are preservation of organic material. Thus, organics not areas with any potential for long-term preser- deposited in a perennial wet sabkha or saline vation of elevated amounts of hydrogen-prone mudflats with a long-term reflux curtain have the organics. With the next heavy rain the less soluble potential to be preserved as hydrogen-prone organ- carbonate precipitates remain, while the more ics until the sediment passes into the zone of soluble salts tend to be flushed through a now- catagenesis. saturated vadose profile to enter the water table. Even so, outcropping capillary-fringe areas There they continue to flow as dissolved phreatic where brine-saturated microbial mats reside about salts into the discharge depression where evapora- the edge of a saline water body, can be subject to tive concentration once again reprecipitates them episodes of water table lowering or to flushing by as wet sabkha and brine pool salts. fresh oxygenated meteoric waters. Then the micro- The lower part of the vadose zone beneath a dry bial organic matter may be intermittently stripped mudflat is made up of the capillary fringe. In parts of its hydrogen by aerobic decomposers that will of an evaporitic mudflat (sabkha) depression that flourish on top of and within the mats during times are actively accumulating displacive salts, the top of exposure or pore-water freshening. of capillary fringe is at or above the land surface (Fig. 8A). This allows the concentration of pore Perennial phreatic hydrologies brines to the attain hypersaline levels needed to precipitate the nodular and displacive salts that Permanent brine lakes and ancient epeiric seaways typify wet sabkhas and saline mudflats. Unlike the with variably holomictic water columns driving dry parts of a playa or mudflat, the inherently wet stable long-term reflux curtains or plumes, are capillary surface facilitates long-term evaporative much more likely than wet sabkhas to preserve concentration of the near-surface pore brines and hydrogen-rich organics into the zone of catagenetic the ongoing crossflow of dense brine into burial. Surface water-masses within perennial 344 J. K. Warren brine lakes or seaways routinely fluctuate between supplied to any water body via exchange with the stratified and nonstratified conditions, while the atmosphere and as a byproduct of photosynthesis bottom waters typically have a greater propensity of the biota living in the waters. In well-oxygenated to maintain long-term anoxia (Warren, 2006). An water columns most of the organics produced by upper fresher (less dense) water layer sits on top primary production the upper water mass are of a more saline (denser) lower water mass in a destroyed by microbial respiration and the conver- stratified system in a perennially brine-filled sion of organic matter back to CO2. Much of the depression (Fig. 8B). The narrow zone of transition improved preservation potential associated with in the brine column between the two waters is “higher than marine” bottom salinities in layered called a halocline or pycnocline. Often a stratified mesohaline to hypersaline settings reflects the saline lacustrine/seaway system is also thermally effect on biotal diversity of increasingly low levels stratified and heliothermic, with warmer waters of dissolved oxygen and CO2 in the bottom and constituting the lower water mass. The zone of pore waters on biotal diversity. transition separating the upper and lower water Oxygen levels in natural brines tend to decrease masses is the called the thermocline, or the che- with increasing salinity, independent of biological mocline, or the halocline, or the pycnocline. Ther- respiration. If not enhanced by the activities of mal stratification of brine masses with a cool top bottom-living photosynthesizers, natural bottom and a hot base is opposite to that found seasonally brines will be dysaerobic to anaerobic by the time in many temperate freshwater lakes and so is some- salinities reach halite saturation (Fig. 9; Kinsman, times called reverse thermal stratification, but 1973; Warren 1986). Dissolved CO2 shows a similar heliothermal is a more appropriate term. depletion; dissolved CO2 levels in marine-fed Heliothermy is a result of the contrast in specific modern salt pans decrease to around 50% of the heat response between less saline and more saline original value when the brine concentrations waters. Specific heat of a brine decreases as the increase from 1.5 to 4 times that of seawater (Lazar salinity increases (Kaufmann, 1960). Specific heat & Erez, 1992). CO2 concentration in brine is also is the amount of heat needed to raise one gram of a pH dependent; at a pH of 9 (reached by concentrat- substance by 1 C. For a given amount of heat input, ing seawater to around 70‰) the CO2 content is a unit volume of hypersaline water will show a near zero (Moberg et al., 1932). Those algae and greater increase in temperature than a less saline water. The resulting greater increase in tempera- ture in a lower hypersaline water mass, compared -1 to an upper less-saline water for the same degree Oxygen (mg L ) 0 246 of insolation, makes brine lakes and seaways 0 B heliothermic; independent of any salinity (osmo- B tic) or oxygen stresses, heliothermy can induce B pronounced heat stress in any benthic halobiota. B B B Modern heliothermal lakes occur in appropriately B 100 stratified saline water bodies on all continents and B B B B B B include numerous saline lakes on the steppes of Russia, Siberia and Canada, Solar Lake in the B B B Middle East (Fig. 11B), numerous coastal salinas B B 200 B B B in Australia, Lake Meggarine in Algeria, Hot Lake B B in Washington State and Red Pond in Arizona Salinity (‰) B B (Hammer, 1986). One of the more unusual exam- B B B B B B ples is Lake Vanda in Antarctica, which has a B B maximum water temperature of 25 C below the 300 chemocline (at a depth of 64 m in the water col- umn), yet the water surface remains ice-covered. Dissolved gas levels and temperature changes associated with periodically heliothermal bottom 400 waters create extreme levels of environmental Fig. 9. Oxygen levels in present-day surface brines under stress in bottom communities attempting to cope increasing salinity. Oxygen content of modern seawater is with hypersalinity. For example, oxygen is 5.4 mg L 1 (after Warren, 1986). Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 345 cyanobacteria, which are dependant on dissolved ocean. Gypsiferous carbonate muds with organic CO2 for photosynthesis, will suffer or die at higher contents of 1–5% accumulate on its microbially- salinities. bound floor beneath its small shallow perennial brine pool (0.6 km2 and less than 2–3 m deep). In the permanently inundated centre of the lake, Stability of brine stratification and anoxia where waters are 1–2 m deep even in late summer, in modern stratified brine lakes laminated benthic microbial mat communities Brine stratification occurs today in all perennial flourish and are dominated by photosynthesizing saline lakes, including many coastal salinas in cyanobacteria (mostly Cyanothece sp.). Filamen- Australia, rift valley lakes of the African Rift Valley tous Microcoleus sp., along with coccoids, and the Dead Sea, Israel and most are meromictic dominate the laminated to pustular mats in the and oligomictic (Warren, 2006). Lake Hayward, a seasonally-desiccated strand zone. Sediments in coastal salina in Western Australia, typifies such the lake centre accumulate under a limnology that stratified brine system. It is a sub-sea-level water- is density-stratified and heliothermal for much of filled marine seepage depression with bottom the year (Rosen et al., 1995). Meteoric winter brines possessing ionic proportions similar to that inflow creates a well-defined long-term mixolim- of seawater (thalassic). The seawater seeps into nion (Fig. 10A) where an upper, less dense and the basin as groundwater and there is no hydro- cooler water mass has salinities ranging from 50 to graphic (at-surface) connection to the nearby 210‰. It exists from late autumn to early summer

Mixolimnion HCO3 Temperature mixolimnion (upper water mass) Salinity Temp Dissolved O H S Monolimnion HCO Temperature monolimnion (lower water mass) Year 2 2 3 (‰) (ºC) (%sat.) (mg L-1) 60 Site1 300 0 1985 162 - 187 30.0 - 35.0 200 - 330 0 50 1986 176 - 210 22.0 - 39.5 41 - 250 0 1987 178 - 184 33.0 - 34.6 140 - 250 0 Temperature (ºC) ) Holomictic Holomictic -3 250 30 Nov 1988 222 42.4 0 35.4 40 50

(gm 1989 180 -234 24.5 - 43.0 0 - 46 0 -1.7

3 23 Sep 1993 160 28 378 0 200

HCO 30 Site 2 30 Nov 1988 216 43.2 0 23.8 150 100 20 1989 180 - 192 24 -36 50 -137 0 - trace

100 10 Purple sulphur bacterial BMC re-establishes 150 bloom in anoxic bottom oxygenation on bottom 1600 1400 Irradiance (µmol m Supersaturated 0.2 depth (cm) Water 1200 200 0 1000 Saturated 800 -0.2 600

250 -2

-0.4 s

400 -1 ) -0.6 200 Holomictic Holomictic 300 0 -0.8 Mixolimnion (upper water mass) Sep-1988 Dec-1988 Mar-1989 Jun-1989 Sep-1989 Dec-1989 Monolimnion (lower water mass) Undersaturated

Gypsum saturation index (Log IAP/KT) index Gypsum saturation 1/10/90 1/01/91 1/04/91 1/07/91 1/10/91 1/01/92 1/04/92 1/07/92 1/10/92 Secchi depth Irradiance at water surface A Date (D,M,Y) B Total depth Irradiance at sediment surface

Fig. 10. Brine stratification in Lake Hayward waters, West Australia. (A) Seasonal hydrogeochemical evolution. Uppermost plot shows temperature regime in upper (mixolimnion) and lower (monolimnion) water masses and bicarbonate content. As the lake mixes, the thermal and density stratification disappears. Immediately prior to mixing the bicarbonate concentration decreases, suggesting precipitation of calcium carbonate (aragonite; after Rosen et al., 1995). Lower plot shows saturation state of waters with respect to gypsum. The monimolimnion was saturated with respect to gypsum for summer 1991–1992 and was near saturation at the start of summer 1992–1993. The mixolimnion is only saturated when the lake water is homogeneous (after Rosen et al., 1996). (B) Effect of gypsum precipitation on benthic microbial communities and associated oxygenation in Lake Hayward, West Australia (compiled from data in Burke & Knott, 1997). 346 J. K. Warren

(May to February) as it floats on top of a lower long-term stratification that defined the winter denser and warmer water mass (monolimnion) months, brine layering in the transition to stratifi- with salinities in the range 150 to 210‰. cation was not stable as the upper and lower water Stratification disappears for a few months each bodies remixed a number of times extending over year from mid-summer to mid-to-late-autumn. periods of days before stable stratification set in During summer the waters of the upper water mass by mid-winter (Fig. 10A, May–June 1992; M. Rosen evaporate and concentrate as their bicarbonate pers. comm., 2006). content steadily increases. From the onset of stra- Lake Hayward bottom sediments also illustrate tification in late autumn, across mid-winter and on an aspect of pelagic evaporite precipitation that into to early summer the temperature trends of the is probably true for many ancient “deep water” two water masses are parallel (Fig. 10A). They form density-stratified saline settings. Namely, that a heliothermic system where the lower water mass while precipitation of pelagic evaporitic sediment is some 15–20 C hotter than the upper water mass. is seasonal, and it occurs in the surface water mass By mid-summer (e.g. January 1992) lower water even as the lake waters are density stratified, bot- mass began to cool, while the temperature of the tom salts can only accumulate when the whole upper water mass continued to rise. Once the brine column is saturated and unstratified (holo- temperatures (and densities) of the two water mictic). This is so even if the chemistry of the lower masses equalize, they mix as the lake overturns water mass is at gypsum or halite saturation almost (holomixis) and waters of the lower water mass all year round. Only pelagic sediments (including (the monolimnion) came into contact with the carbonates and organic residues) and terrigenous atmosphere once more. detritus (including eolian dust) make it to the While the water masses are stratified, the che- bottom when a saline lake is perennially stratified, mocline and the thermocline are sharply defined as was the case in the Dead Sea for the 400 years across a 10 cm interface with a salinity contrast that prior to 1979 (Warren, 2006). may be as much as 135–140‰ and a temperature Intensity of light penetration to the subaqueous difference of up to 19 C. The time of mixing is bottom of an evaporite-accumulating depression immediately preceded by a sharp fall in the level of is a significant control on how much photosyn- bicarbonate in the mixolimnion, suggesting that thetic oxygen can be generated by the bottom- from late summer to autumn the precipitation of living microbial community. In Lake Hayward a pelagic calcium carbonate (mostly aragonite) then healthy mat of photosynthesizing halotolerant gypsum occurs in the upper water mass (Fig. 10A, cyanobacteria drastically alters the levels of anox- upper plot; Rosen et al., 1995). For example, the ia in shallow bottom brines. Photosynthesis, via upper water mass in Lake Hayward was super- its benthic microbial mat community, is normally saturated with respect to gypsum and anhydrite sufficient to maintain supersaturation of the Lake from October 1991 to February 1992 (Fig. 10A, Hayward bottom waters with dissolved oxygen, lower plot; Rosen et al., 1996). When the lake even during periods of brine column stratification mixed from March 1992 until early May 1992, the (Fig. 10B). entire water body was at gypsum saturation, but Burke & Knott (1997) found that after an slightly undersaturated with respect to anhydrite. unusually dry year in 1987, the salinity of Lake A ‘whiting’ (a cloudy white appearance to the Hayward increased to 260‰ as gypsum precipi- water body) was observed in the lake in March, just tated throughout the lake waters. Brine turbidity at the time of first mixing of the lake waters. generated by the markedly increased pelagic crys- Analysis by scanning electron microscopy of the tallization of gypsum in the surface waters in that collected filtrate indicated that the “whiting” was year was sufficient to obscure the benthos comple- composed of gypsum and silica from diatom tests. tely, despite the shallowness of the lake. As a result At that time, there was a thin (10–20 mm) crust the amount of oxygenic photosynthesis and aero- of gypsum accumulating on the lake bottom. After bic decomposition was greatly reduced in the the “whiting”, when the water was unstratified benthic mats and they degraded. During brine (holomictic), both the monimolimnion and mixo- stratification in the following winter (1988), limnion were near saturation with respect to gyp- bottom waters became anoxic and sulphurous. sum. After mixing, with the next influx of meteoric During the next few years, after each subsequent waters building across the lake water surface, sali- brine column overturn, healthy microbial mats nity stratification re-established itself. Prior to the were re-established across the lake floor and they Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 347 were able to again supersaturate the bottom waters a well-documented heliothermal hydrology. It is with oxygen year round, as was seen in 1992, located on the Sinai coast of the Gulf of Aqaba which was the time of the Rosen et al. (1995, (Cytryn et al., 2000) and is separated from the 1996) study. ocean by a narrow permeable sand barrier. The Development of a healthy mat community in the barrier allows seawater to seep into the sub-sea- Lake Hayward salina prevents periodic bottom level hydrographically-isolated lake depression anoxia. Nearby lakes, that do not contain a healthy and so replace waters lost to evaporation. See- microbial benthos, tend to anoxia during stratifica- page-derived seawater can then pond on top of the tion. Comparisons between Lake Hayward and lake floor, along with lesser volumes of waters nearby lakes clearly show that healthy microbial supplied by occasional winter rains (Fig. 11A). mats function as a strong homeostatic mechanism Brine depth in the lake centre fluctuates between in the lake hydrology. Shallow meromictic but 4 and 6 m, driven by seasonal changes in the perennial salt lakes, with long-term stability of intensities of evaporation and the related levels photosynthetically elevated oxygen levels in the of seawater seepage and brine reflux. bottom, tend to have lower levels of preserved TOC Thick cyanobacterial mats carpet much of the due to the higher efficiencies of halotolerant aero- Solar Lake sediment surface and contain a highly bic decomposers acting on the benthic organic diverse microbial community of cyanobacteria matter. This can be seen when comparing TOC and haloarchaea. Unlike the microbial laminites levels in the microbial laminites of Lake Hayward of Lake Haywood, a structureless organic-rich gyp- and Solar Lake (Fig. 5). siferous mush constitutes the sediment across the Solar Lake in the Middle East is another small m-deep bottom of the anoxic lake centre (Fig. 11A; meromictic hypersaline lake (coastal salina) with see Warren, 2006 for geological detail). Fluctuating

I. Holomictic Stage (Sept. 1997) Temp (°C) Salinity (%) Oxygen (µM) Methane (µM) W Core 1 Core 2 Core 3 Core 4 25 35 55 5 10 15 20 0 100200 300 012 Gulf of 0 4 Elat 1 2 3 -4 Height (m) Brine reflux 4 5 0 25 50 75 100 125 150 175 0 1000 2000 Distance (m) Sulphide (µM) II. Early Stratification Stage (Dec. 1997) 25 35 55 5 10 15 20 0 100200 300 04 0 Core 1 Core 2 Core 3 Core 4 1 Hard Recycled 0 gypsum microbial 2 crust mats 20 3 Depth (m) 40 4 5 60 0 1000 2000 Conglomerate and loose gravels 80 Depth (cm) Laminated microbial mats III. Late Stratification Stage (June 1997) 100 25 35 55 5 10 15 20 0 100200 300 01020 Interlaminated gypsum and aragonite 0 120 Carbonate (aragonitic) mud 1

140 Lithoclastic sediment 2 3

4 A B 5 0 1000 2000

Fig. 11. Solar Lake, Sinai Peninsula, Middle East. (A) East–west topographic and lithological cross section based on cored sediments showing peripheral algal facies and a more central organic-rich gypsum zone (after Aharon et al., 1977). (B) Effects of the seasonal development of heliothermic and oxic stratification in the water column of Solar Lake (after Cytryn et al., 2000). 348 J. K. Warren planktonic microbial activity mirrors seasonal intense oxygenic photosynthetic activity at the changes in brine column layering by exporting brine surface and in underlying shallow salina varying volumes of oxygen, sulphide, and methane waters. Deeper in the brine column, and well into the brine column as this mush accumulates below the chemocline, a sharp rise in sulphide (Fig. 11B). concentration occurs reaching a maximum value High evaporation and aridity in the summer of 2150 mM at the water-sediment interface (Cytryn months raises Solar Lake salinity to 200‰. At that et al., 2000). Methane concentration increases time the brine column is completely mixed (holo- linearly below the brine surface and reaches a mictic) and the entire water column is oxygenated maximum value of 17 mM adjacent to the lake (Fig. 11B, September, 1997). Temperature and sali- bottom, implying methane, like the bacterially nity in the holomictic state vary little throughout derived H2S, is escaping from the sediments. the water column and sulphide and methane con- Increased evaporation rates in the mid- to later centrations are very low. By autumn, the water summer further increase the salinity of the surface column becomes stratified as a newly introduced layer and ultimately disrupt the stratification and seawater brine (50‰) layer overlies the residual, so lead into summer holomixis (as seen in the highly saline bottom water (180–200‰). A well- September 1997 profile). Unlike Lake Hayward, defined density gradient (halocline or pycnocline) conditions beneath the perennial lake floor of Solar separates an upper oxygenated cooler (16 C) brine Lake are anoxic for longer periods, oxygenic spe- mass (epilimnion) from the lower hotter (45–55 C) cies, including cyanobacteria, tend not thrive in anoxic sulphide-rich brine mass (hypolimnion; bottom waters for long periods, especially in the Fig. 11b, December 1997). A high sulphide con- deep central parts of the lake, where levels of centration develops in the anoxic waters below preserved organics tend to be higher (5–20% ver- the halocline and comes from the activities of sus 1–5% TOC in Lake Hayward; Fig. 5). sulphate-reducing bacteria both in the water col- Substantial density differences between the umn and in the underlying degrading cyanobac- upper and lower masses in most density-stratified terial mats. Crossing the halocline into the lower systems means diffusive mixing across any halo- brine there is a rapid downward increase in sul- cline is insignificant. When a hypersaline water phide concentration, which reaches a maximum mass is density stratified there is no mechanism to value of 1240 mM near the sediment-brine contact drive changes in saturation state and so there is no (Cytryn et al., 2000). At the same time a peak in widespread bottom nucleation of salts. Sedimen- methane concentration develops directly below tation on the floor of the lower water layer (espe- the halocline, where a maximum value of 6.5 mM cially if it is below the euphotic zone) is mostly by was measured in the December 1997 profile and a pelagic rain of organics and evaporite crystallites was in-part a reflection of the decomposer activ- formed in the upper water mass at the halocline via ities of the methanogenic haloarchaea. brine mixing. There may also be local changes in As winter passes into spring gradual heating, brine chemistry and the associated mineral preci- along with an increase in the salinity of the upper pitation driven by local influxes of spring and seep water mass, degrades the halocline (Fig. 11B). Thus waters. In contrast, when the upper and lower the June 1997 data portray a transitional state water masses equilibrate and homogenize, bottom between late stratification and the beginning of nucleation of salts is possible even at the base of holomixis. Salinity and temperature gradients deep brine columns, as is occurring with the pre- across the halocline are more gradual and deeper cipitation of coarsely crystalline halite at the base in the water column than those observed in the of the 350 m holomictic brine column in the Dead December 1997 profile. The deepening halocline of Sea today (Warren, 2006). In some perennial saline June 1997, when the chemocline was located lakes in more temperate climates the holomictic 3.25 m below the water surface, allowed oxygen stage is seasonal and so the sediment layers are to penetrate much deeper into the brine column, varves (e.g. Lake Hayward, Solar Lake, Lake Van, and so extend farther out across the subaqueous Lake Urmia), in others, holomictic mixing of sur- lake bottom than it had in the earlier stages of face with bottom water masses occurs across a stratification. Oxygen concentration in the upper longer time frame (e.g. the 400 year stability of the water mass in June 1997 reached a maximum value lower water layer in the Dead Sea driving episodes of 300 mM at a depth of 1 m below the water surface. of laminite versus coarse crystalline halite beds These supersaturated values of oxygen imply on the deep lake floor). Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 349

Whenever a homogenized brine mass restrati- hydrological cycle, with denser more saline waters fies, the lack of ongoing concentration in the lower supporting an ephemeral mass of less dense inflow water mass means the rate of brine reflux through water. The lower, denser part of the water mass bottom sediments beneath the sediment brine tends to be more stable and its physical conditions interface slows and ultimately stops. Hypersaline change less. In contrast, the conditions in the pore brines remain but in a stagnant condition as floating less-dense layer are much more variable there is no ongoing mechanism to resupply brines and its physical chemistry tends to oscillate. This denser than existing pore waters in the column upper layer periodically freshens to where it sup- substrate. High pore water salinities, a propensity ports a widespread planktonic bloom (feast). Then, for anoxia, anoxic pore brines and elevated bottom as ongoing evaporation concentrates the upper temperatures, all tend to exclude aerobic burrow- layer, conditions become increasingly less suitable ing and grazing animals from evaporite bottom for life (famine) and a mass die-off occurs, first of sediments beneath a stratified brine column. This the haloxene species, then the halotolerants, then minimizes the effects of oxygenic biota that would the halophiles. otherwise oxidize and destroy mesohaline micro- The die-back creates a pulse of organic matter bial debris, as in sediments deposited in less saline that can swamp the abilities of the decomposers in settings. the water column to strip it of its hydrogen, and so Although the daily temperature/stratification it can reach the sediment interface with its long- records of Lake Hayward and Solar Lake are prob- chain alkanes still intact. Even in conditions where ably the best documented examples of the long- light penetrates to the bottom of the brine column term hydrological cycling of a naturally stratified and the bottom waters immediately above the sedi- brine pool, they both have a number of limitations ment surface are oxygenated, the halotolerant pri- when attempting to use them as direct analogues mary producers can be sufficiently productive and for the hydrology of ancient stratified brine sea- the underlying anoxic decomposers sufficiently ways. Unfortunately, neither lake can act as a inefficient that substantial volumes of hydrogen- same scale hydrological analogue for ancient eva- rich microbial mater can be retained into burial. porite seaways, intraplatform depressions or even Some modern examples of hydrologically induced some of the larger ancient evaporitic lakes. They community layering in modern evaporitic settings suffer from the scaling limitations that enfeeble will now be considered. all modern marine-associated evaporite analogues (Warren, 2006). Although hydrographically Halotolerant plankton and water isolated and marine-seepage fed, neither lake is column layering situated in a hydrological setting where enough time or aerially extensive drawdown stability has The significance of periodic freshening on biomass transpired to allow substantial thicknesses of in stratified waters in creating conditions of mesohaline carbonates, halite or gypsum to accu- “famine or feast” for halotolerant and halophilic mulate. Their small aerial extents (0.6 km2) and species is clearly seen in the present productivity their centripetal meteoric inflow hydrologies (dri- cycle of the Dead Sea (Fig. 12; Oren 2005; Oren & ven by winter rains, a marked seasonal lowering of Gurevich, 1995; Oren et al., 1995). The main com- evaporation intensity, and a high-relief hinterland ponent of the halobiota in the Dead Sea waters is immediately adjacent to the water body) means a unicellular green alga, Dunaliella parva being they cannot be directly compared to ancient meso- the sole primary producer in the lake. Several haline epeiric brine seaways where inherently types of halophilic archaea of the family Halobac- low-relief topographies meant strandlines moved teriaceae then metabolize the glycerol and other up to hundreds of kilometres in a wet-dry cycle, organic compounds produced by the alga. As in and where unfractionated meteoric runoff from all ecosystems, producers and consumers in the the hinterland was much less significant in the brine-stratified water columns are codependent. freshening process. Halophilic archaea (Halobacterium and Halo- coccus) survive into much higher salinities than Dunaliella parva as they decompose the glycerol- Biological responses to layered hydrologies rich remains. Brines in modern evaporitic depressions are typi- Three distinct periods of organic productivity cally layered in terms of the annual or longer-term were seen in thirteen years of quantitative studies 350 J. K. Warren

Meromictic Holomictic A 405 700 ) 600 -2 Water level 410 Stability 500 (kj m y

400 415 300

200 420 100 Height (m below sea level) Height (m below Water column stabilit Water 425 0 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 Ye a r

Month (1992) Mar. Apr. May June July Aug. Sep. Oct. B 0 Specific Gravity (25 °C) 2.5 1.21 1.22 1.23 2 15 0.05 4 Bacteria (mL-1 x 107) 0.05 0 12341 6 0.5 1.5 8 0.025 Dunaliella cells (mL-1) 1 10 0 500 1000 1500 2000 0.1 0 12 Bacteria 14 2 Dunaliella cells (mL-1 x 103) Specific gravity 16 4 0 Depth (m) 3.5 6 2 3.0 2.5 2.0 4 8 1.5 6 1.0 0.5 Depth (m) 0.25 10 8 Dunaliella 10 12 12 14 14 22 September 1992 Bacteria (mL-1 x 107) 16

Fig. 12. Biodynamics in the Dead Sea, Middle East. (A) Long-term changes in quasi-salinity and temperature in the deep water body (below 100 m) of the Dead Sea in a meromictic to holomictic period (after Gertman & Hecht, 2002; with additional data from http://isramar.ocean.org.il/DeadSea, last accessed 29 September 2004). (B) Changes in the vertical distribution of Dunaliella and halobacteria during the rain flood-induced density stratification of the Dead Sea in 1992 (after Oren, 1993). Note the vertical distribution of Dunaliella and halobacteria relative to the halocline on 22 September 1992. See Warren (2006) for full discussion of long-term sedimentary dynamics of the Dead Sea and Lake Lisan depressions. of Dead Sea microbiology starting in 1980 (Oren, an associated rise in lake level of 1.5 m. This bloom 1993). Unlike more temperate lakes, organic had disappeared at the end of 1982, following blooms in the Dead Sea are not an annual event. complete mixing of the water column and the Mass developments of Dunaliella (up to 8800 cells associated salinity increase in the upper water mL 1) and red halophilic archaea (2 107 cells mass (holomixis). mL 1) were observed in 1980, following a dilution During the period 1983–1991 the Dead Sea was of the saline upper water layers by rain floods and holomictic, and no Dunaliella cells were observed. Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 351

Viable halophilic and halotolerant archaea were light penetrated to the bottom of the brine column present during this period, but in very low num- and a newly established freshened water layer inter- bers. Then heavy rain floods during the winter of sected the lake floor. The resulting algal blossoming 1991–1992 raised the lake level by 2 m and caused was instigated by resting cells that had survived new salinity stratification as the upper five metres near the sediment surface around the lake margin or of the water column was diluted to 70% of the in species refugia around freshwater springs. normal surface salinity (Fig. 12A). The meromictic The decline of the lake-wide bloom of halophilic phase lasted until 1996 when the current holomic- archaea in the Dead Sea appears to be related to tic conditions with seasonal stratification were viral infection (Oren et al., 1997). For example, in established, clearly illustrating the oligotrophic October 1994, there were between 0.9 and 7.3 107 hydrology of the Dead Sea brine column. Duna- virus-like particles per mL of brine during declen- liella reappeared in the upper less saline water sion of halophilic archaea in the upper 20 m of layer (up to 3 104 cells mL 1 at the beginning the Dead Sea water column and virus-like particles of May 1992, rapidly declining to less than outnumbered archaea by a factor of 0.9–9.5 (aver- 40 cells mL 1 at the end of July), while the bloom aging 4.4). By 1995 all water samples contained of the archaea (3 107 cells mL 1) continued and low numbers of both archaea and virus-like parti- imparted a reddish colour to the Dead Sea brines cles; 1.9–2.6 106 and 0.8–4.6 107 mL 1 respec- (Fig. 12B). The reddish hue of the surface waters at tively in April 1995. Viral numbers declined even this time was due to elevated levels of the carote- further so that by November 1995–January 1996 all noid pigment bacterioruberin, which absorbs light samples contained less than 104 particles mL 1. at wavelengths between 420–550 nm. Oren et al. (1997) further suggested that viruses Archaeal numbers in the Dead Sea decreased play a major role in the decline of halophilic only a little after the July 1992 decline of the archaeal communities in many other hypersaline Dunaliella bloom, and most of the haloarchaeal settings at salinities where protozoa and fungi are community was still present at the end of 1993. absent. However, the amount of carotenoid pigment per cell decreased 2–3-fold between June 1992 and Community layering in mesohaline microbialites August 1993 (Fig. 12B; Oren & Gurevich, 1995). No new algal and archaeal blooms developed after Laminated organic-rich sediments that typify the winter floods of 1992–1993, in spite of the fact many evaporitic microbial carbonates (possible that salinity values in the surface layer were suffi- petroleum source rocks) and described by sedi- ciently low to support a new algal bloom. A rem- mentologists using the general, and perhaps dated, nant of the 1992 Dunaliella bloom maintained terms algal mats and cryptalgal-laminites, are in itself at the lower end of the pycnocline (halocline) effect microbial “high rises,” as are many living at depths between 7 and 13 m (September stromatolites. They, and their entrained biomar- 1992–August 1993). Its photosynthetic activity kers, indicate the activities of an ecologically was small, and very little stimulation of archaeal layered microbial community that can thrive in growth and activity was associated with this algal both subaerial and subaqueous settings. Like community (Fig. 12B). This pattern suggests that microbial layering in the Dead Sea brine column, the photosynthetic activity of the algae may have layering in a microbial mat is divisible into an been limited by a lack of nutrients in the upper upper aerobic community and a lower layer of brine column. anaerobic decomposers (Fig. 13). As a microbial Colouration of the Dead Sea waters from the mat accretes, its organic constituents are buried. initial algal bloom allowed Oren & Ben Yosef The biochemical make-up of the initial halobiota, (1997) to use Landsat images, collected in May which flourished in the hypersaline conditions 1991 and in April and June 1992, to plot the (typically oxygenic) at or above the mat surface, development of the Dunaliella parva bloom. In is altered by the metabolic activities of various contrast, the carotenoids of the subsequent archaea decomposers flourishing below. bloom did not produce a recognizable signal in the In order to investigate early or syndepositional Landsat images. The April 1992 image obtained at changes in the dominant organic constituents and the time of the onset of the algal bloom, prior to its the main diagenetic processes influencing organic lake-wide spread, suggested it originated in the character, Grimalt et al. (1992) studied organic shallow areas near the shore of the lake, where profiles in cross sections through two different 352 J. K. Warren

CO O2 S-gases O CO CH Sediment surface Day Night Water or Ma 2 2 2 4 Mat 0 O surfacet Aphanothece surface 2 layer (brown) O2 B Cyanobacteria Oxygenated

Gypsum G fluctuates CH O O 2 2 3 crystal layer 2 2 Y O Aerobic light Visible Phormidium O heterotrophs layer (green) R Chemolithotrophic Dysae- robic 6 4 Purple bacteria sulphur bacteria Photosynthesisers Infrared radiation Infrared layer Phototrophic Depth (mm)

Depth (mm) sulphur bacteria 9 So SO4 6 H2S H2S Fermenters FeS HS- Decomposers Sulphate CO Black foetid reducers 2 Biomarkers

12 sediment with Anoxic 8 Oxygen cycle Organic H S/FeS Carbon cycle Methanogens CO 2 Representative acids, H2 4

Sulphur cycle Burial ABCmicrosensor measurements

Fig. 13. Layering and metabolism in microbial mats. (A) Typical microbial community in an evaporitic laminite in a modern coastal salina with salinity in the range 130 to 200‰ (after Caumette, 1993). (B) Inter-relationships between microbes and the oxygen, carbon and sulphur cycles in the uppermost 5–10 mm of a microbial mat. The oxic-anoxic transition shifts lower in the mat in the daytime and higher in the mat at night (when photosynthesis has stopped). (C) Biogeochemical cycles operating within the mat versus depth. subaqueous cyanobacterial mats in a modern photosynthesizers that fix sugars by utilizing coastal salina. Changes in lipid composition were the infrared portion of the light spectrum as they compared with the vertical distributions of the convert H2StoSO4. Infrared radiation penetrates various microbial populations. Vertical distribu- deeper into microbial sediment than the visible tions in the lipid patterns were defined using light used by the cyanobacteria (Fig. 13B). Utilizing enrichment cultures from typical species of cya- the redox gradient these purple sulphur-oxidizing nobacteria, diatoms, purple bacteria, sulphate- bacteria synthesize organic matter and create the reducers and methanogens obtained from the characteristic purple-orange layer seen below layered mats. Cyanobacteria Phormidium valder- the green layer in an aggrading microbial mat. The ianum and Microcoleus chthonoplastes were the sulphur-oxidizing bacteria can only metabolize in dominant primary producers in the sampled mats, a suitable redox gradient, and they need to locate they occurred almost as monocultures in the upper themselves exactly within this gradient, so they are 6 mm of the mats (Fig. 13A). Worldwide, these and typically the most motile forms in a microbial mat. other cosmopolitan filamentous cyanobacterial The redox gradient lies deeper in the mat commu- photosynthesizers are the most obvious organisms nity during the day due to oxygen production by in most mesohaline algal mats. Their chlorophyll the cyanobacteria, but it rises and can even reach creates a green layer with a sticky or slimy surface the mat surface in the dark of night (Fig. 13B). and defines the upper few millimetres of the mat Below the phototrophic sulphur-oxidizing bac- community. As layers of mucilaginous sheaths teria are the sulphate reducers, the fermenters and aggrade via periodic growth spurts, it creates the methanogens (Fig. 13C). In saline settings they biolamination. are relatively inefficient decomposers and tend to Below the photosynthesizing cyanobacteria is be active at salinities that are less than 150‰ (Figs 3 a layer of aerobic heterotrophs (bacteria and and 4; Ollivier et al., 1994). During the day the archaea), which in the presence of oxygen break sulphate-reducers metabolize organics deep in the down organics produced by the cyanobacteria microbial mat via anaerobic respiration, utilizing a (mostly abandoned algal sheaths and slime). How- variety of chemical constituents including manga- ever, because oxygen is only produced by photo- nese, nitrate, sulphate and even CO2. At night they synthesis, these organisms can only perform this rise somewhat with redox gradient and at times of process during daylight. The next layer below is prolonged bottom-brine anoxia and brine-column dominated by chemolithotrophic sulphur-oxidiz- turbidity can even reach the mat surface or enter ing bacteria. These are life forms that use the redox the lower parts of a density-stratified brine column. energy contained in the biochemical gradient They are very important decomposers in most between reduced sulphur compounds produced mesohaline microbial mats and give the lower by sulphate reducers (below) and oxygen produced parts of a mat its characteristic “rotten egg” smell. by the cyanobacteria (above). They are anaerobic They generally consume up to one third of the Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 353 organic carbon present in a typical mesohaline

40 e microbial mat and are most efficient at salinities s a Organic signatures

e ‰ r that are less than 120–140 . c modern and ancient

n i China

y

t Fermenters and reducers do not completely i

n

i 30 l break down the organics but create alcohols, lac- a S tates and other organic compounds (Ollivier et al., 18 Dongpu Basin 1994). The other group of anaerobic decomposers 20 deep in the mat is the methanogens. They are Jianghan, Basin Taian

archaea and utilize simple compounds created Phytane/nC by the fermenters (CO and hydrogen, along with 10 Dongpu (Eocene) 2 Jianghan (Eocene) organic components such as methanol, acetic acid, Taian (Cretaceous) formic acid and methylamines) to produce Lenghu (Jurassic) 0 Yangtze (Permian-Triassic) methane. This metabolic pathway produces little Ejinur salt lake (modern) biochemical energy and is usually the “last resort” community that makes up the lowermost living 0 5 10 15 layer in the microbial high-rise community that Pristane/nC17 inhabits a microbial mat or a stratified brine Fig. 14. Crossplot of pristane/nC17 versus phytane/nC18 column. ratios for various saline/hypersaline settings in China (after Stratification of the microbiota in response to, Wang, 1998). and in biofeedback with, oxygen levels has impor- tant implications in terms of the biomarkers found weight range, the C16 and C18 components are in preserved saline sediments (and source rocks). prominent, with the former dominant. For higher Grimalt et al. (1992) found that although the upper- homologues (greater than or equal to C20), docosa- most layers of saline microbial mats are dominated noic (C22) and tetracosanoic (C24) acids dominate by cyanobacteria, they typically leave no more the n-alkanoic acid homologues for the Jianghan than minor traces in the solvent-extractable lipids and Ejinur samples, respectively. Alkanoic acids (biomarkers) in the buried sediment. Rather, the with an isoprenoid skeleton are more abundant predominant fatty acid distributions in the lower in Jianghan samples, including C20,C21,C24,C25 parts of mesohaline mat sediments parallel the and C30 homologues, with a C25 component compositions observed in the enrichment cultures (3,7,11,15,19-pentamethyleicosanoic acid) most of sulphur-oxidizing bacteria, and appear to be pronounced in the lower part of the Qianjiang mixed with acids characteristic of heterotrophic Fm. The carbon skeletons of these isoprenoid acids bacteria, including purple bacteria and sulphate- are attributed to archaeal decomposers. Iso and reducers. In other words, the retained organic sig- anteiso branched carboxylic acids are prevalent natures, even as the mat lamina were accumulating in both the Lake Ejinur samples and the upper a few millimetres above, were those of the decom- portion of the Qiangiang Formation. (Wang, 1998). posers, not the primary producers (Fig. 13C). This They derive from bacteria, probably sulphate- implies that many biomarkers used to typify organ- reducing bacteria, and their abundances clearly ic production in modern and ancient hypersaline show again the importance of bacterial decompo- sediments typically do not come from organics of sers, along with haloarchaea as contributors to the the primary producers but from the products of the biochemical signature of organic matter in both decomposer community. modern and ancient saline lake sediments. The The overprinting effects of the decomposers in presence of hopanoid acids and a 3-carboxy ster- microbial laminites are clearly seen when mole- oidal acid in both further attest to contributions cular characteristics of recent hypersaline sedi- from bacterial and eukaryotic sources, respec- ment from the Ejinur salt lake (northern China) are tively. The occurrence of particular carboxylic compared to Tertiary (Eocene) core samples from acids in the Jianghan samples illustrate these com- the Qianjiang Formation (hypersaline lacustrine) pounds, indicators of halotolerant and halophilic of the Jianghan Basin, central eastern China decomposers, can survive as biomarkers in source (Fig. 14; Wang et al., 1998). N-alkanoic acids in rocks deposited in hypersaline settings. sediments from both areas (Ejinur and Jianghan) Defining where ancient halotolerant and halo- show a pronounced even-over-odd predominance philic decomposers lived (“in brine column” or “in and a bimodal distribution. In the lower molecular mat”) is not possible from an analysis of sediment 354 J. K. Warren biomarkers. It requires sedimentological interpre- Salinity controls on organic productivity: the tation of the rock matrix, which typically is a flamingo connection laminite. As discussed in Warren (1986), any When biodiversity is low and salinity is high, a assumption of “lamination indicating deeper proliferation of well-adapted mesohaline species brines” is fraught with difficulty, as ancient eva- can generate organic productivity levels in surface poritic laminites and biolaminites were subaqu- waters that are much higher than those observed in eous sediments with near-identical mm-scale most non-evaporitic settings. These saline systems textures accumulating beneath stratified and are indicative of general principles seen in stressed unstratified perennial brines columns at depths ecosystems, namely, as the harshness or abiotic ranging from less than one metre to hundreds of stress in a system increases, the biotic stress metres. Determination of water depth requires decreases on a few well-adapted species (as there sedimentary analysis of evaporitic sediments that are fewer predators and grazers). The total biodi- are intercalated with the laminites. versity (number of species) decreases, while at the same time the biomass (total mass of organisms in ORGANIC ENRICHMENT the system) initially increases (e.g. Garcia & Niell, 1993). Ultimately, as salinity rises further, biomass At the broader scale of petroleum source rock declines as conditions become unsuitable for any creation, the amount of organic matter preserved life. One of the most visually impressive indica- in evaporitic sediment, which becomes a potential tions of periodic very high levels of organic pro- source rock, is a function of three factors that can be ductivity in a modern salinity-stressed water body expressed in the equation (Bohacs et al., 2000): resides in the “flamingo connection”, a connection between flamingos, mesohaline planktonic blooms Organic Enrichment ¼ðP-DeÞ=ðDiÞð3Þ and saline lakes, well documented in Lake Nakuru where P is production, De is destruction (oxidation by Vareschi (1982) and first noted in the geological and biodegradation and Di is dilution (detrital literature by Kirkland & Evans (1981). influx and matrix precipitation). Maximum Flamingos are filter feeders thriving on the dense enrichment occurs when production is maximized cyanobacterial blooms in the shallows of saline and destruction and dilution are minimized. lakes around the world. For example, two species Production at mesohaline salinities is mostly via of flamingo intermittently occur in huge numbers photosynthetic fixation of CO2. It includes auto- in the various East African rift lakes. These are the chthonous organic matter, formed at or near the site greater and the lesser flamingo (Phoenicoptus of accumulation and derived from algae, bacteria ruber roseus and P. minor); the lesser flamingo is and aquatic plants, as well as allochthonous organ- the bird with the spectacular pink-red colouration. ic matter carried in during floods (Bohacs et al., These bright pink birds feed and breed in rift lakes 2000). Katz (1990) showed that varying levels of where cyanobacterial blooms can be so dense that solar input and water chemistry/stratification exert a secchi disc disappears within a few centimetres the largest effects on overall primary production in of the lake’s water surface (Warren, 1986). Lake mesohaline settings. Initial destruction of organic Natron is a major breeding ground for flamingos in matter is mostly a function of the efficiency of the East Africa and is the only regular breeding site for various scavengers and grazers, which is typically the lesser flamingo in Africa (Simmons, 1995). In a function of the availability of oxygen (Demaison fact, Lake Natron has the highest concentration of & Moore, 1980). In higher salinity settings the breeding flamingos of any lake in East Africa. Both scavenger/decomposer population is dominated the greater and the lesser flamingo are found there, by bacteria and archaea, while the density of the with the lesser flamingo outnumbering the greater metazoan grazers is largely inhibited by the same by a hundred to one. Lesser flamingos bred at Lake higher salinities. Dilution by an influx of mineral Natron in 9 out of 14 years from 1954 to 1967. While precipitates to possible areas of organic enrich- Lake Natron (a trona lake) is an essential breeding ment can limit levels of organic enrichment by site, it is not a focal feeding site for flamingos. Major decreasing the proportion of organic matter rela- feeding sites in the rift valley are Lakes Nakuru and tive to inorganic matrix. The source of dilution can Bogoria in Kenya, which are somewhat less saline be detrital siliciclastics or precipitates of gypsum than Lake Natron and so have a greater abundance and halite. of mesohaline plankton. Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 355

The main phytoplankton component in Lake “flamingo connection”). This is the same pigment Nakuru waters is the cyanobacterium, Arthrospira that turns waters red in Lake Natron and Lake platensis (previously known as Spirulina platen- Magadi, but in this case it comes mostly from the sis), it forms the main food component of the lesser halophilic archaea. Lesser flamingos, with their flamingo. In Nakuru it is also consumed by one narrower spacings of beak filters, survive solely species of tilapid fish and one species of copepod on Arthrospira and so have a more intense pink and a crustacean. Rotifers, waterboatmen, and colour than greater flamingos, a species that sits midge larvae also flourish in the waters of Lake higher in the lake food chain and get its feather Nakuru. The mouth-breeding tilapid fish Sarother- colour second-hand from the lake zooplankton. odon alcalicum grahami was introduced to the As well as possessing very high levels of phy- lake in the 1950s to control the mosquito problem coerythrin in its cytoplasm, Spirulina is also unu- and they have flourished ever since, at times dis- sual among the cyanobacteria in its unusually high placing the flamingos as the primary consumers of protein content. In Lake Chad and in some saline planktonic algae. Their introduction also increased lakes in Mexico it accumulates as a lake edge scum the number of fish-eating birds residing in the lake that is harvested by the local people and used to (Vareschi, 1978). make nutritious biscuits. In the 16th century it was In a good year more than a million flamingos mentioned in the diary of one of Cortez’s soldiers consume more than 200 tons of plankton per day who described how the Aztecs sold hard flat cakes from Lake Nakuru, a shallow saline soda lake with made from the dried remains of Arthrospira. The apH10.5 and a typical annual salinity range of Aztec word for it was Tecuitlatl, which translates 10–120‰. The lake measures some 6.5 km by literally as “excrement of stones.” The lack of 10 km, with waters up to 4.5 m deep in the lower cellulose in the A. platensis cell wall means it is parts of the lake during a “lake-full” period. Lake a source of plant protein readily absorbed by the levels are subject to change, both annually and on human gut, making it a potentially harvestable a longer time scale, with permanent eutrophic food source in water bodies in regions of deserti- waters developed in the lake centre during fication and it has become a popular alternative times of higher water (Fig. 15A and B; Vareschi, protein source in the developed world. 1978–1982). In 1972, Lake Nakuru waters held a surface The feeding style of the birds is to wade through biomass of 270 g m 3 and an average biomass of the shallows, with heads upside down and beaks 194 g m 3 but, as in most hypersaline ecosystems, waving side to side across the water surface. Fla- Nakuru’s organic production rate varies drastically mingo beaks have evolved to skim plankton from from year to year as water conditions fluctuate saline to brackish surface waters and are equipped (Fig. 15C; Vareschi, 1978). Arthrospira platensis with a filter-feeding system unlike any other bird was in a long-lasting bloom in 1971–1973, and on Earth and more akin to feeding apparatus of the accounted for 80–100% of the large phytoplankton krill-ingesting Great Whales. Flamingos siphon biomass in those years. In 1974, however, it almost the lake water through the beak filters to trap disappeared from the lake and was replaced by A. platensis and other plankton by swinging their coccoid cyanobacteria such as Anabaenopsis sp., upside-down heads from side to side and using Chroococcus sp. and by diatoms, all species that their fat tongues to swish water through their dealt better with elevated salinities. This change in beaks. They can filter as many as 20 beak-fulls of biota was tied to a serious reduction in biomass, plankton-rich water in a second. Spacings of the which in 1974 was down to 71 g m 3 in surface filters in the beak of the greater flamingo are wider waters, and averaged 137 g m 3 in the total water than those in the beaks of the lesser flamingo. mass. As a result, the flamingo population in the Greater flamingos feed mostly on zooplankton, lake declined from 1 million to several thousands while lesser flamingos feed almost solely on Spir- (Vareschi, 1978). ulina, thus in any saline lake where the two species The lower salinity limit for Arthrospira platensis co-exist they do not compete for the same food growth is 5‰ and in terms of water conductivity source. it does best in the range 10–50 mS cm 1. The driv- Arthrospira platensis provides high levels of ing mechanism for the change in biomass in Lake the red pigment phycoerythrin to the food chain Nakuru in the mid-1970s was not clearly docu- and it accumulates in flamingo feathers to give the mented. It was thought to be related to increased birds their world famous colouration (hence the salinity and lowering of lake levels, along with 356 J. K. Warren

4

Mean annual rainfall = 750 mm (peaks in Nov-Dec & April-May 3 Mean annual evaporation = 1800 mm Lake elevation 1759 m.s.l Mean water depth 2.5 m, maximum 4.5 m

2 Lake level (m) level Lake 1 no data 0 no data 1951 1931 1961 1971 1932 1952 1962 1972 1950 1930 1954 1960 1970 1974 1994 1964 1957 1967 1977 1997 1953 1933 1966 1956 1963 1993 1973 1976 1996 1958 1959 1968 1969 1978 1999 1979 1998 1955 1965 1995 1975 A Ye a r 1980-1992 1934-1949

b 1 km Conductivity 250 Algal biomass Arthrospira (%) 35

200

ry wt) ry 30

Njiro d

a Cormorant -3 150 25 (mS 20°C)

Point 100% y ss (g m (g ss

100 20 ma

50% bio

50 Conductivit 15

Lomudioc 4.4 Algal 10% 0 10 1972 1973 19741975 1976 1978 C Year Temperature (°C) 20 21 21 21 21 23 21 23 25 21 23 25 21 23 21 4.4 0

4.3

Baboon Cliff 1 Depth (m) 2 3 3.9 1.1 0 1 0900-10 B 100-1300 1500-1800 2200-0200 1800-2200 1300-1500 D 0200-0600 0600-0900 Makarlia Water depths in metres Nderit Average Air 16.1 15.5 19.2 22.1 24.3 22.0 17.4 Temp (°C) 14.3

O 20 200 2 Conductivity 120 5 Flamingo numbers Depth 100 ) 4 -1

) 15 150 ) -1 4 80 3 10 100 60 2 Depth (m) Oxygen (mg L

40 Flamingos (x10

5 Conductivity (mS cm 50 1 20

0 0 0 0 E 1993 1994 1995 1996 1997 1998 1999 2000 2001 Ye a r Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 357

the growth and bottom shading by planktonic to fall, salinities and rates of salinity change return algal species that were better adapted to higher to higher levels, then water conditions once again salinity. These better adapted were present in les- become appropriate for A. platensis. Environmen- ser volumes and with lower per cell protein cells tal stress on the flamingos also comes with drier (Fig. 15C; Vareschi, 1978). periods that elevate lake salinities into the upper During the mid- to late 1970s and in the 1980s end of A. platensis tolerance. Ongoing drought Lake Nakuru returned from a relatively saline dry ultimately leads to lake desiccation and the com- phase to more typical annual schizohaline oscilla- plete loss of the food supply in the lake. tions in water level and salinity (Fig. 15A). Sea- One of the reasons why Lake Nakuru is so sonally, in the 1980s, the A. platensis and flamingo suitable for cyanobacterial growth at times of populations returned to impressive numbers. A. platensis bloom, is the maintenance of suitable From the 1990s more reliable long-term data on temperatures and associated oxygenation in the physical lake condition and flamingo numbers upper water mass. The lake develops a remarkable have being compiled (Fig. 15E). In 1995 and daily thermocline in the upper 1.5 m of the column 1998 feeding flamingo populations in Lake Nakuru that dissipates each day via wind mixing in the were once again at very low levels and the remain- late afternoon, and so recycles nutrients back to ing population was stressed (Fig. 15E). In 1998, the oxygenated surface waters to facilitate the unlike 1974, the stress was related to freshening ongoing plankton bloom of the next diurnal cycle driving a decrease in A. platensis biomass, not (Fig. 15D). increased salinity and desiccation. This freshening Some environmentalists have argued in the pop- of the lake waters favoured a cyanobacterial assem- ular press that lower numbers of flamingos in Lake blage that also produced toxins (see Cyanobacterial Nakuru, such as occurred in 1995 when more than toxins in Glossary). In the preceding bountiful 50,000 birds died, are an indicator of: uncontrolled year (1996), the A. platensis-dominated biomass forest clearance; an uncontrolled increase in sew- had bloomed at times when salinities were favour- erage encouraging eutrophication; an increase in able, and died back at times of elevated salinities heavy metals from increasing industrial pollutants and lake desiccation, as in 1974. By 2000, the in the lake; and general stress on the bird popula- somewhat lower salinity cycles had once again tion from tourists and the drastic increase in local increased, making surface waters suitable for human population centered on the town of Nakuru another widespread A. platensis bloom and the (now the third largest in Kenya). Numbers of peo- associated return of high numbers of feeding ple in the town, which is the main city in the rift flamingos. valley, have grown by an average of 10% every It seems that breeding flamingos come to Lake decade for the past 30 years. Nakuru to feed in large numbers when there is Like many environmental doomsday arguments, water in the lake with appropriate salinity and the above are more based on opinionated predic- nutrient levels to facilitate an A. platensis bloom. tion than on scientific fact. Rise and fall of lake In some years when heavy rains occur, lake levels levels, drastic changes in salinity, a periodically rise significantly and the lake waters, although stressed biota, and a lack of predictability in water perennial, stay in the lower salinity tolerance range characteristics are endemic to saline ecosystems for A. platensis, as in the El Nino~ period between (cycles of “famine or feast”). Oscillations in one October 1997 and April 1998. Once lake levels start or more of these factors are not necessarily

3 Fig. 15. Physical and chemical characteristics, algal biomass and flamingo numbers of Lake Nakuru, Kenya. (A) Lake levels from 1930 to 1999. Data are not sufficiently detailed to record times of complete lake drying or drought, and there are also substantial times when no data were collected/published (1934–1949 and 1978–1992). (B) Lake bathymetry (December 1979) and strand-zone changes. Solid isopleths are actual shorelines at different lake levels over a 20-year period; from margin to centre these are: December 1979; January 1969; January 1967; and January 1961. Dashed isopleths are based on soundings taken in December, 1971. Two sewage plants are located at a and b. (C) Trends of algal biomass and conductivity of lake water during 1972–1978. The percent contribution of Arthrospira platensis (formerly Spirulina platensis) to the total algal biomass is also shown. (D) Mean water temperature profiles at different times of day from 1972–1973. (A–D) after Vareschi (1982). (E) Monitored water depths, conductivities, oxygen levels and flamingo numbers at Lake Nakuru for the period 1993 to mid- 2001. Water depth and flamingo data only available from 1994 to mid-2000 (data are digitized and replotted to a common time scale from a number of figures and pdf reports downloaded from http://www.worldlakes.org on 2 February 2004). 358 J. K. Warren anthropogenically induced. For example, the terms of their seasonal planktonic biomass (Grant amounts of most heavy metals (Cd, Cr, Cu, Hg, et al., 1999) and also places them among the Ni, Pb, Zn) in the lake sediments were found to world’s most productive ecosystems (Melack & be in the typical range of metals in natural lakes Kilham, 1974). As demonstrated above, the less worldwide (Svengren, 2002). The exception was saline soda lakes are dominated by periodic cadmium, which is elevated in the lake sediment blooms of cyanobacteria, especially Arthrospira and could perhaps be assigned to anthropogenic platensis, while the hypersaline lakes, such as pollution. All other metals are present at low Magadi, can on occasion support blooms of both levels, especially if one considers that Lake Nakuru cyanobacteria and alkaphilic phototrophic bacter- lies within a labile catchment where bedrock is ia belonging to the genera Ectothiorhodospira and an active volcanogenic-magmatic terrane. At the Halorhodospira (Jones et al., 1998). present time, sufficient base a scientific data are not The halotolerant and halophilic biota living yet available in Lake Nakuru, and so scientifically in the layered water columns of these soda lakes accurate determinations cannot be made of the constitute small-scale “famine or feast” ecosys- relative effects of humanity verses natural baseline tems, which at times of “feast” are far more pro- environmental stresses on bird numbers in this ductive than zones of marine upwelling (Fig. 16A). schizohaline ecosystem. A general observation of short periods of enhanced Nearby lakes Magadi and Natron have extensive organic productivity between somewhat less and trona platforms covered with brine sheets that are somewhat more saline episodes in schizohaline characterized by short periods of high productivity lake waters worldwide, reflects the general ecolo- and times of bright red waters. In this higher sali- gical principle that increased environmental stress nity ecosystem, the dominant producers of the favours the survival of a few well-adapted haloto- brine colour are haloalkaliphilic bacteria and lerant species, to the detriment of others better archaea. Archaeal species belonging to the genera suited to life in a less saline environment (see inset Natronococcus, Natronobacterium, Natrialba, in Fig. 16A). Ultimately, abiogenic stresses asso- Halorubrum, Natronorubrum and Natronomonas, ciated with more elevated salinity means all life, all occur in the lakes. Lake centre brines when this including the halophiles, ceases to function. biota flourishes are at trona/halite saturation, with The same general principle that schizohaline apH12. Stratified moat waters around the trona ecosystems encourage dominance by a few better- platform edge are at times almost as chemically adapted species can be clearly seen in the decrease extreme, and the moat bottom sediments are made in invertebrate species (grazers and predators) with up of aragonite/dolomite/detrital laminites that increasing salinity in the carbonate lakes of the can preserve elevated levels of organics (6–8%). Coorong of Southern Australia, where only brine As well as algae and cyanobacteria, Lake Magadi shrimp remain alive in waters with salinities in and Natron moat waters also harbour a varied excess of 200‰ (Fig. 16B). It reflects a general trend anaerobic bacterial community including cellulo- of decreasing faunal biomass with increasing sali- lytic, proteolytic, saccharolytic, and homoaceto- nity (Fig. 16C). A decreased level of biomass in a genic bacteria (Shiba & Horikoshi, 1988; Zhilina & mesohaline system does not necessarily mean less Zavarzin, 1994; Zhilina et al., 1996). When the source rock potential in the resulting sediments. homoacetogen Natroniella acetigena was isolated Preservation levels of organic matter and suitability from Lake Magadi its pH growth optimum was of the protokerogen (type I to type III) depends on found to be 9.8–10.0, and it continued to grow in what biotal contributors constitute the biomass waters with pH up to 10.7, making it an exemplary preserved in the sediment. alkaphile (Zhilina et al., 1996). Examples of “famine or feast” productivity have Regionally, salinities in the East Africa rift-val- so far focused on continental salt lakes. Similar ley lakes range from around 5‰ total salts (w/v) in enhancements of primary productivity can occur the more northerly lakes (Bogoria, Nakuru, Elmen- in modern coastal salinas during episodes of per- teita, and Sonachi) to trona and halite saturation iodic freshening as blooms of haloxene and halo- (>200‰) in lakes to the south (Lakes Magadi and tolerant microbes (oxygenic photosynthesizers) Natron). Yet across this salinity range, a combina- take place across formerly exposed mats. For exam- tion of high ambient temperature, high light inten- ple, a study of biolaminites collected from a mod- sity and a continuous resupply of CO2, makes these ern salina (Storr’s Lake in the Bahamas) showed soda lakes amongst the highest in the world in that a reduction in brine salinity from 90 to 45‰ Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 359

Upwelling zone (Peru near 15°S) 3000

Dry Valley Lake (Antarctica) 3600 Biomass

Soap Lake (USA) 7000 Drakesbad Hot Spring (USA) 2919 Great Salt Lake (USA) 6147 140 Devils Lake (USA) Marine upwelling Borax Lake (USA) 525 Abundance Biodiversity Waldsea Lake (Canada) 345 Little Manitou Lake (Canada) 2620 Humbolt Lake (Canada) 7968 Environmental stress (salinity, temperature, exposure) Shark Bay (Australia) 480 Spencer Gulf (Australia) 3100 Werowrap Lake (Australia) 7683 Red Rock Lake (Australia) 7531 Pink Lake (Australia) 184 Corongamite Lake (Australia) 4425

Lake Nakuru (Kenya) 12000 Kilotes Lake (Ethiopia) 4133 Aranguidi Lake (Ethiopia) 19000 Mariut Lake (Ethiopia) 9611 Solar Lake (Sinai) 12000 0 2000 4000 6000 8000 10000 12000 14000 16000 18000 20000 A Carbon (mg m-2 day-1)

70 14 Macroscopic benthic fauna in saline lakes 60 12 Metazoan species

in Coorong saline lakes ) 50 10 -2 40 8 Aragonite saturation Gypsum 6 30 saturation Seawater 4 20 Wet weight (g m weight Wet Number of species 2 10

0 0 0 50 100 150 200 250 300 0 20 40 60 80 100 120 140 160 180 C B Salinity (‰) Salinity (‰)

Fig. 16. Productivity and biodiversity in saline ecosystems. (A) Organic productivity in various saline ecosystems. Typical marine upwelling zone (offshore Peru) is 2000–3000 mg C m 2 day 1 (yellow line), open-marine waters average 20 mg C m 2 day 1 and coastal waters 40–50 mg C m 2 day 1. Preservation is more important than production rate in terms of source potential. Compiled from sources listed in Warren (1986, 2006). (B) The effect of increasing salinity on metazoan species diversity in the saline lakes of the Coorong region, South Australia (after de Decker & Geddes, 1980). (C) Standing crop (g m 2) of the macroscopic benthic fauna in selected athalassic (non-marine) saline lakes of the world (after Hammer, 1986).

significantly enhanced CO2 and N2 fixation rates, In other words, abiotic stress, induced by hyper- but additions of inorganic nutrients and dissolved saline conditions in the Bahamian lagoons, created organic carbons did not show any significantly lower productivity in the saline-tolerant microbial enhanced rates compared with the salinity con- mats, even when nutrient levels were high. Once trols (Pinckney et al., 1995). That is, dissolved the osmotic stress on the biota was relieved by a organic carbon/dissolved organic nitrogen uptake lowering of salinity, mats underwent enhanced was not influenced over the entire range of sali- primary production and nitrogen fixation as halox- nities (45–90‰) seen in this study of mesohaline ene producers could once again photosynthesize. mat growth. Changing nutrient levels were far less significant 360 J. K. Warren than changing salinity levels as controls on mat of eutrophication in man-made saltfields, Javor productivity in this stressed setting. Salinity- (2000) found that in shallow gypsum and pre- induced stress in these halotolerant microbial mats gypsum ponds there was an interesting inverse outweighs typical limiting factors regulating pri- relationship between the level of nutrients mary production in phototrophic communities at (nitrates and phosphates) in the brine column and the lower salinities that typify marine and brackish the development of microbial mats on the water waters. covered pan floor. In a high-nutrient brine system (eutrophic or “well-nourished pan”) the algae and bacteria flourished as planktonic forms and Organic production in saline waters the biomass buildup in the upper parts of the When surface water salinities are suitable, evapor- brine column tended to shade the sediment sur- ite basins have some of the highest measured rates face. There was little or no development of an of organic productivity in the world (Fig. 16A; oxygenated microbial mat and bottom waters were Warren, 1986). Times of elevated primary produc- dysaerobic to anoxic. In a low nutrient system tion (“feast”) in density-stratified hypersaline (oligotrophic or “poorly-nourished pan”) there brine lakes and evaporitic seaways appear to be was little or no planktonic development of algae controlled by two factors: (1) the ephemeral pre- or bacteria and microbial mats tended to flourish sence of a less saline surface water; and (2) a supply on the perennial pond floor. Benthic mats formed of nutrients (nitrate/ammonia and phosphate) from salinities of 50‰ to gypsum saturation in from the lower hypersaline water mass. The biota the poorly-nourished pans. In pans at even lower contributing the organics that ultimately reach the salinities the benthic mats were destroyed by the bottom sediments to form organic-rich laminae feeding activities of invertebrates and fish. (and so control their future biomarker signature) Preservation of microbial mats into early burial are largely dependent on the timing of photosyn- in hypersaline systems depends, in large part, on thetic activity. Perennial saline lakes subject to an the efficiency of nutrient recycling by the bacterial annual freshening of surface waters will deposit and archaeal decomposers that making up the varved carbonates (e.g. Lake Tanganyika with up to underside of the living part of a mat. Even if nitro- 7–11% TOC in deep bottom laminites; Cohen, gen and phosphorus levels are low in the overlying 1989), while other saline lakes and seaways with brine, there may be sufficient recycling of nutrients less predictable stratification may form similar within the mat community to allow the benthic mat carbonate laminites, but the organic layering may to continue to grow. Javor (1989) found that once not be annual, and the resulting organic biomar- a gypsum crust becomes well established over the kers contain elevated levels of isoprenoids due to floor of a crystallizer pond, there was little recy- the greater contribution from the haloarchaea. cling of nutrients from beneath the crust to the Microbial mats in some shallower saline lakes uppermost photosynthesizers, and from this point may be subject to short periods of photosynthetic downstream in the crystallizer pans, nitrate and oxygenation and even subaerial exposure, yet still phosphate nutrients were concentrated by eva- preserve elevated levels of hydrogen-prone organ- poration and recycled into the biomass living in ics (Warren, 1986). the brine column. In oligotrophic gypsum ponds Once brine moves into the gypsum precipitation the gypsum crust is stable and the bottom waters are field and beyond, the amount of organics accumu- oxygenated. In eutrophic gypsum ponds at the lating on the bottom is diluted by inherently rapid same salinities, the bottom waters become anoxic rates of crystal precipitation and accumulation, and sulphate-reducing bacteria flourish. In these especially if the bottom brine is photosynthetically systems, gypsum dissolves and a black slimy organ- oxygenated by its microbial community. Hypertro- ic-rich carbonate/detrital mud (a potential source phication, in combination with shading by pelagic rock in ancient counterparts) covers the bottom and crystallites, can overwhelm the delivery of oxygen contains no more than a few embayed and dis- to the bottom, as in Solar Lake and in Lake Hay- solved gypsum remnants. If portions of this slimy ward in the late 1980s. Evaporitic systems subject bottom become suspended and are flushed into to longer-term eutrophication can facilitate high the next stage of crystallizer they create a problem levels of pelagic organic delivery to bottom sedi- in the final salt product known as “black spot”. ments, even beneath shallow penesaline waters The difference in organic levels between oligo- (Horsfield et al., 1994; Warren 1986). In a study trophic systems such as Lake Hayward and Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 361 perennial eutrophic systems like Solar Lake prob- 5 Winter Autumn Micritic ably explains why the latter retains much higher Summer carbonate Spring 4 Mineral detritus, levels of hydrogen-prone organic material in its Winter Autumn pyrite, algae, preserved bottom sediments (Fig. 5). Javor’s work Summer 50 µm layers of Spring amorphous OM also demonstrated that as higher salinity brines 3 tend to concentrate nutrients, they will supply 2

these nutrients at times or at interfaces where (wt %) TOC supersaline waters in a natural schizohaline sys- 1 tem are subject to periodic freshening or mixing. Proximity of organic-rich mesohaline laminites 0 to bedded evaporites in ancient successions has 020406080100 led some geologists to postulate that bedded salts Sedimentation rate (cm kyr-1) are potentially also organic-rich sediments, with Fig. 17. Sedimentation rate versus percent of total organic the same level of source potential as mesohaline carbon (TOC) in laminite marls from the Oligocene evapor- carbonates. This is not borne out by TOC analysis ites of the Mulhouse Basin, France. Inset shows the scale of evaporitic salts; total organic matter levels in and mineral/organic distribution in the laminae (varve ancient CaSO and NaCl lithologies tend to be couplets) of the sampled intervals (after Hofmann 4 et al., 1993b). normal or depleted (Katz et al., 1987), although levels of dissolved organic matter and volatile fatty acids may be high in the entrained brine inclusions were able to plot the relationship between sedi- (Hite & Anders, 1991). The typically low organic mentation rate and TOC content in the marls matter levels in bedded gypsum and halite may (Fig. 17). Marls deposited during times of low reflect the higher depositional rates of evaporitic sedimentation tend to be organic-rich, while marls salts when compared with evaporitic carbonates deposited with higher sedimentation rates tend (dilution effect). Only in settings where bottom to contain lower amounts of organics. They extra- waters are anoxic in the gypsum stage can the polated that the even lower levels of organics in build up of H2S from sulphate reduction become the more saline salt beds (anhydrite and halite) high enough to remove CaSO4 minerals and so indicate greater dilution because of the inherently allow preservation of elevated levels of partially higher sedimentation rates of halite and gypsum degraded organics (as in Solar Lake today). compared to mesohaline carbonate. That organic enrichment mostly occurs in the mesohaline carbonate stage in an evaporite basin is Salinity-induced environmental stress (“famine clearly seen in organic contents of the evaporitic or feast”) facilitates organic preservation marls and salts of the Oligocene Mulhouse Basin (Fig. 17; Hofmann et al., 1993a, b). This deposit is Organic matter in modern saline systems tend to one of a few ancient evaporites where organic accumulate in bottom sediments beneath density- chemistry has been studied in a logical and stratified saline water and sediment columns in detailed fashion. Organic matter occurs mostly evaporitic settings where layered hydrologies are in finely laminated carbonate marls (varves), subject to oscillations in salinity and brine level. which can contain up to 7% TOC, anhydrite beds Organic matter is not produced at a constant rate in contain 0.08–0.78% TOC, halite beds 0.01–0.25% such systems, rather, it is produced as pulses by a TOC and the potash beds <0.1% TOC. The marls halotolerant community in response to relatively are characterized by thin, continuous bedding short times when less stressful conditions occur in parallel laminae that are not disturbed by any the upper part of the layered hydrology (Fig. 18A). bioturbation. They are interpreted as seasonal This happens when an upper less-saline water varves with the clay and carbonate forming alter- mass forms on top of nutrient-rich brines or within nate layers in the couplet (Fig. 17, inset). In spring wet mudflats when waters in and on top of the and summer the increased temperature in surface uppermost few millimetres of any microbial mat waters favoured precipitation of micritic carbo- freshen. The resulting bloom (a time of “feasting”) nate, in autumn and winter the phytoplankton by halotolerant algae and cyanobacteria is a time died back and rainfall/runoff transported silici- characterized by very high levels of organic clastic debris into the basin. On the basis that the productivity. In mesohaline waters where light laminar couplets are varves, Hofmann et al. (1993a) penetrates to the bottom, the organic-producing 362 J. K. Warren

Exponential Decline and expansion death Lag FEAST Stationary FAMINE Biotic stress Sigmoidal Abiotic stress growth Environmental harshness

Number of viable Number of viable cells halotolerant Biomass Onset of freshening Time

Lag: metabolising, but slow growth (immature) Expansion : numbers rise logarithmically (expansion) Abundance Biodiversity Stationary : growth decreases (nutrient limited or buildup of environmental toxins, salinity) Decline : harsh environmental conditions (high salinity, Environmental stress lack of nutrients or temperature exceeds tolerance) (salinity, temperature, exposure) A

Permanent Complexly tiered Long-term Haloxenes, Perennial Halophiles, High Low normal marine haloid specialists, high species stable moderate & lacustrine Perennial fewer trophic and diversity and biotic biodiversity communities interaction (osmolytes and (high biomass) stable community webs, ( lower biomass) anion adaption) Increasing biotic effects on preservation of organic remains of Mass die-back haloid community

Short-lived Habitiat Tolerance of Halotolerants, specialists permanence adverse Blooms of halophiles, lowest

Habitiat stability (very high conditions holotolerants biodiversity, most productivity (lowest active (moderate to Schizohaline hostile to life potential Source rock & biomass) Schizohaline biomass) low biodiversity) “FEAST” “FAMINE” “FAMINE” Temporary “FEAST” Low High Environmental adversity Stress on biota increases increases due to osmotic stress, anoxia, B temperature, salinity

Fig. 18. Life in saline systems. (A) General ecological principles in stressed saline ecosystems. Sigmoidal growth curve of life moving into a newly created niche (as created by a freshening event setting up a layered brine). As environmental harshness increases due to abiogenic stress factors (such as increasing salinity, osmotic stress and temperature) the level of biogenic stress (predation or grazing decreases, allowing a few well-adapted species to flourish, leading to a decrease in biodiversity and a short-term increase in biomass. (B) Schematic summary of the inter-relationships between habitat stability, environmental stress or adversity, biodegradation, anoxia and source rock potential in an evaporite basin, showing why schizohaline environmentally stressed mesohaline systems tend to favour the accumulation of organic matter in bottom sediments. layer is generally the upper algal and bacterial Short pulses of extremely high organic produc- portion of benthic laminated microbialites (typi- tivity during times of freshened mesohaline sur- cally characterized by elevated numbers of cyano- face waters in-turn create a high volume of organic bacteria). In stratified brine columns, the typical detritus settling through the water column and/or producers are the planktonic algal or cyanobacter- construction of benthic microbial mats. Then, with ial community inhabiting the upper water mass. the end of the freshening event, the ongoing inten- Halotolerant autotrophic microbial communities, sely arid climate that characterizes evaporitic living off the remains of this plankton, float mid- depressions means that salinities, temperatures water at the halocline of the density-stratified and osmotic stresses increase rapidly in the pre- brine columns. Similar aerobic decomposers can viously freshened water mass. This leads to a also constitute bottom-layer communities in zones time of mass die-off, in the once flourishing meso- of oxygenated oligotrophic waters. haline community (“famine;” Fig. 18B). First, these Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 363 increasingly salty waters can no longer support community takes up and recycles carbon very haloxene forms. Then halotolerant life dies back efficiently through the system and the potential and finally, by the halite precipitation stage, only for large volumes of carbon passing into the burial a few halophilic archaea and bacteria remain in realm is low and hence source potential is also low the brine column (typically acting as heterotrophs (a good example in the marine realm is a tropical and fermenters). Repeated pulses of organic coralgal reef). matter created during a freshening event in a stra- In contrast, a schizohaline system is one defined tified brine column thus create laminated bottom by high habitat instability, its lack of habitat per- sediment. manence encourages opportunistic lifestyles Hydrogen-rich algal and eubacterial debris is (cycles of “famine or feast”). Opportunist species best preserved within sediments where pore expand rapidly into any suitable niche space, but waters are anoxic and remain so until the resulting then just as quickly die back or encyst as conditions kerogen is sufficiently buried for it to generate become adverse. Such systems are characterised by liquid and gaseous hydrocarbons (Demaison & high biomass pulses and low species diversity, Moore, 1980). Thus the preservation of organics leading to pulses of organics accumulating in with long-chain hydrocarbons intact is most likely the evaporitic depression, with the remains likely in settings characterized by long-term anoxia to be buried and “pickled” beneath anoxic bottom (less efficient decomposers). This tends to occur brines and pore waters, giving such systems a beneath stratified eutrophic saline brine columns higher source rock potential (Fig. 18B). with a permanent anoxic mesohaline bottom water Some hypersaline settings are intermediates in mass and a transiently freshened upper water that their waters are constantly hypersaline, stress- mass. Preservation is also possible in benthic mats ful to most life, but suitable to a few well-adapted in shallow oligotrophic systems with permanently species. These regions are usually populated by hypersaline pore waters, but the propensity for a few very specialized species (e.g. “high-salt-in” periodic bottom oxygenation means preservation halophiles) that can survive and flourish in con- potential of oil-prone mats is less likely in this ditions where most life dies. They photosynthesize setting, as is also the case in mats of the strandzone. and metabolize successfully in these hypersaline Increasing rates of mineral precipitation at conditions (often for example living near halo- higher salinities means levels of hydrogen-prone clines), but do so at rates that are much slower organics are highest in sediments deposited in than the growth rates attained by halotolerant schizohaline waters that remain in the mesohaline “opportunists” at times of “feast.” The long-term field. Once ambient salinities pass into the penesa- cycling of organic materials means bottom sedi- line and supersaline, the proportion of organics in ment layers tend to have lower levels of entrained the sediment becomes insignificant as it is rapidly organics preserved compared to the schizohaline- diluted by large volumes of gypsum and halite mesohaline. (or trona and glauberite in some continental pene- To take an understanding of community and saline/supersaline waters). controls from the modern into ancient saline sys- Feast and famine cycles are a biotal response to tems, it is necessary to account for changes in both environmental salinity conditions that at first are scale and diversity when comparing the style and eminently suitable and then increasingly adverse setting of “famine or feast” in modern saline set- to life. It reflects the typical biological response to tings to those of the past. Put simply, there are no rapid niche creation and expansion as the fresh- modern same-scale analogues for ancient marine- ened water layer sets up in the evaporitic depres- fed evaporite depressions, and so there are no sion, and is known as the sigmoidal growth modern same-scale marine-fed evaporitic source response (Fig. 18A). Freshening of surface waters rocks (Warren 2006, 2010). creates a vacant ecological niche into which micro- bial life rapidly expands, flourishes and then once more dies back as drying or brine concentration ANCIENT EVAPORITIC SOURCE ROCKS shrinks suitable niche space. Long-term stability in any ecosystem leads to The common theme to deposition of all prolific domination by “specialist” species that are well source rocks, both evaporitic and non-evaporitic, adapted, diverse and efficient in terms of energy is that they require anoxic conditions to accumu- flow-nutrient utilization (Fig. 18B). This biodiverse late and preserve their organics (Demaison & 364 J. K. Warren

Moore, 1980). This in-turn requires some way of Most ancient marine-fed evaporite deposits are restricting the influx of oxygenated waters and is one or two orders of magnitude larger than today’s usually accomplished by thermal or density stra- marine-fed hypersaline systems and accumulated tification of a water body, in a setting where plank- in huge marine-seepage fed sub-sea-level tectonic tonic-producers flourish periodically in the upper depressions with no surface connection to the water mass. This is why so many ancient evaporitic ocean (Fig. 19). Well-documented source rock- settings are also places where organics tend to entraining ancient basinwide evaporite deposits accumulate. By definition, evaporites require include the Jurassic Hith, Permian Zechstein and restricted inflow conditions to accumulate, they Miocene Messinian evaporites, but none have a are also typically areas of density-stratified waters same-scale modern counterpart. Likewise, no with long-term elevated salinities in the lower widespread marine-fed platform evaporites have denser water mass. Levels of dissolved gases are accumulated since the Eocene. The Mediterranean negligible to non-existent in the lower brine body, Messinian salts (5.5 Ma) are the youngest known as it does not easily exchange with the atmosphere, basinwide evaporite. Well-documented marine- so encouraging long-term bottom anoxia. fed platform evaporites include the evaporite- This does not mean that all of the world’s anoxia- capped cycles of the Jurassic Arab Formation in associated source rocks were deposited in evapori- Saudi Arabia and the United Arab Emirates, the tic settings, only that the restricted conditions Permian Khuff Formation in the same region, and that favour the accumulation of evaporites are in the evaporite-capped Permian backreef strata of their early stages similar to conditions that favour Guadalupian age in West Texas and New Mexico. the accumulation of organics. In arid climates any Although platform and basinwide evaporites minor changes in inflow conditions can easily may have no Quaternary counterpart in terms of force a transition from one into the other. Hence scale or thickness, they can be interpreted the common association of source rocks with the using process models that are combinations of the freshened, typically early phases of the onset of hydrologies of Quaternary sabkhas, saline pans evaporitic sedimentation in many modern and and salinas. Accumulations of thick evaporite ancient lacustrine settings (Table 5). In the marine accumulations (continental or marine) and asso- realm, the same need for tectonic or eustatic restric- ciated mesohaline stages require a stable long-term tion to create basins suitable for source rock accu- brine curtain (100 kyr–1 Myr) to accumulate mulations (intrashelf, circular or linear sags) also to substantial thicknesses and lateral extents explains why, if further restriction and isolation (Warren, 2003, 2006). The hydrological position from surface connections to the oceans ensue, of the active top of an aggrading brine curtain, with the same regions are easily covered by a sequence respect to the evaporite depositional surface, in of salts (Fig. 19). both platform and basinwide settings, defines the dominant textural signature of the resulting salt sequence (saline-pan, evaporitic mudflat/sabkha, Tectonic and eustatic styles in ancient saltern, deeper slope and basin). evaporitic basins High amplitude, high-frequency 4th-order sea- Almost all of the information that has been gath- level oscillations of the current “icehouse” climate ered and analyzed so far in this paper comes from do not allow the set up of stable brine curtains organic accumulations in saline Quaternary lacus- behind laterally-continuous seepage shoals in pre- trine and marine-margin settings. Likewise, all sent-day carbonate platforms, and so there are no the largest and thickest examples of Quaternary Neogene examples of platform evaporites with sabkhas, saline pans and salinas are continental stable intrashelf depressions. Platform evaporites deposits (Warren, 2006). Quaternary saline sys- require greenhouse eustacy to form. Nor are there tems only define same-scale analogs for ancient suitable sub-sea-level rift-induced intracratonic continental lacustrine deposition and are not sags or soft-collision belts in arid marine-fed same-scale analogues for ancient marine-fed epei- settings where conditions are suitable for the crea- ric and basin-centre salt basins, or their entrained tion of basinwide marine drawdown deposits source rocks (Fig. 19; Warren 2006, 2010). Yet (Warren, 2006). compared to lacustrine sediments, these ancient The need for sub-sea-level tectonically-induced marine-associated deposits entrain and seal far basins explains why times of worldwide conti- greater volumes of evaporitic source rocks (Table 5). nent-continent collision followed by continental Table 5. Characteristics and settings of evaporitic source rocks. Basin styles: 1 = basin centre; 2 = intrashelf; 3 = lacustrine. See Warren (2006) for further detail on the significance of different basin styles

Formation/Group Basin Style Characteristics and depositional setting Reference locality and age

Messinian carbonates 1a Organic-rich laminated mudstones deposited in pre-evaporitic Benali et al., 1995 brines layered in feast” or “famine of cycles to responses mesohaline rocks: source Evaporitic Lorca Basin, Spain Basinwide evaporite mesohaline marginal basins with density- and salinity-stratified Russell et al., 1997 Upper Miocene marginal basin brine columns. The basin underwent sporadic phases of Rouchy et al., 1998 circulatory restriction with marked production and preservation of organic matter, culminating in evaporative sedimentation (latest Miocene). As the water in this basin evolved toward evaporative conditions, a number of organic- rich depositional phases (>25 wt% TOC) occurred. During the early parts of these phases, the upper water was nutrient rich and comparatively normal marine, and the bottom water was anoxic and more saline. This was followed by rising salinities in the surface waters, holomixis and short phases of evaporite formation. Gessoso-Solfifera 1a Biomarker compositions from immature organic sulphur-rich Damste et al., 1995 Formation, Sicily Basinwide evaporite marl samples from 10 of the 14 evaporite cycles in an Italian Keely et al., 1995 Upper Miocene marginal basin Messinian evaporitic basin (Vena del Gesso) indicate large Lugli et al., 2007 (Messinian) variations in the composition of species in the water column (e.g. dinoflagellates, diatoms and other algae, cyanobacteria, methanogens, green sulphur bacteria and bacterivorous ciliates) and in contributions from the continent (i.e. land plants) within each marl bed and between marl beds. The marl beds were deposited within a stratified lagoon where anoxic conditions extended into the photic zone for much of the time. Organic-rich marls, 3 Inclusion studies show evaporitic environment of deposition Kholief & Barakat, 1986 Rudeis, Kareem and Rift basin continental to (reducing conditions and high salinities), favoured oil- Rouchy et al., 1995 Belayim Fms. Gulf of transitional marine generating kerogen. Carbonate minerals and inclusions trapped Barakat et al., 1997 Suez Miocene in gypsum indicate possible mixing of marine water with a brine Alsharhan, 2003 of restricted occurrence at the time source rocks were deposited. Bresse and Valence salt 3 Organic matter is mostly immature and occurs in intercalated non- Curial et al., 1990 basins, France Rift basin continental to halite beds. Type-III kerogen is tied to terrigenous deposition. Paleogene transitional marine Type-I kerogen is abundant in mesohaline evaporitic laminites of Valence basin. Type-II is more abundant in Bresse Basin. Organics accumulated beneath a perennially stratified brine column of up to tens of metres. Syndepositional dissolution of halite may have aided the accumulation of significant amounts of oil-prone organic matter in non-soluble brecciated residues. (continued ) 365 Table 5. (Continued ) 366 Formation/Group Basin Style Characteristics and depositional setting Reference locality and age .K Warren K. J. Salt IV Formation, 3 Biomarker assemblages are dominated by acyclic isoprenoids, Damste et al., 1993 Mulhouse Salt Basin, Rift basin continental to especially phytane (0.13 < Pr/Ph < 0.52), n -alkanes with Hofmann et al., 1993a, b Europe Lower transitional marine specific distribution patterns, and steranes. Large differences in Hollander et al., 1993 Oligocene distribution indicate changes in paleoenvironment. The largest Keely et al., 1993 changes are in desmethyl- and methylsterane distributions and are probably linked to occasional reconnection of the stratified evaporite basin to the sea, leading to a dinoflagellate bloom in the upper waters of a density-stratified brine column. Eocene Qianjiang and 3 Anoxic evaporitic lacustrine source rocks generated most of the Jiang & Fowler, 1986 Lower Eocene- Foreland flexure basins, crude oils. High salinity and low Eh enhanced preservation of Huang & Shao, 1993 Paleocene Xingouzhui mountain-front fault oil-prone organic matter and facilitated incorporation of Peters et al., 1996 Formations of depressions sulphur. Anoxia and the unusual presence of abundant sulphate Ritts et al., 1999 Jiangling-Dangyang as gypsum resulted in microbial reduction of sulphate to sulfide Hanson et al., 2001 area, Jianghan Basin, and incorporation of this sulphur into the kerogen. Biomarkers Northwest China in Qianjiang Formation show that some source rocks (Sha 13 Eocene-Paleocene well -1322 m) was deposited under more saline, lower Eh conditions than others) Ling 80 well - 1808 m). Sha 13 sample is more organic-rich (6.62 vs 1.27 wt% TOC), has a higher hydrogen index (794 vs 501 mg HC g 1 TOC) and faster reaction kinetics. Kerogen from the Sha 13 sample is Type I. Green River Formation, 3 Laminated organic mudstones and oil shales deposited in deeper Ruble et al., 1994 Wyoming and Utah Foreland flexure basin anoxic bottom waters of a perennial saline and density-stratified Katz, 1995 Eocene from Laramide alkaline lake. Gilsonite and tabbyite bitumens are associated orogeny with Parachute Creek Member, deposited during a major expansion and freshening of ancient Lake Uinta. Compound specific isotopic analyses of b-carotene and phytane 13 (d C=32.6 to 32.1‰) from these bitumens reflect input from primary photosynthetic producers such as cyanobacteria. 13 Sterane d C values (34.5 to 29.2‰) reflect contributions 13 from lacustrine algae, while extremely depleted d C values for methylhopanes (58.1 to 61.5‰) suggest input from 13 methanotrophic bacteria/archaea. Variations in the d C values of the ab-hopanes (51.4 to 37.7‰) imply additional input from other bacterial sources. The wurtzilite bitumen generated from the saline facies of the Green River Formation was deposited during a later regression of Lake Uinta. Compound 13 specific isotopic analyses of phytane (d C=30.1‰) and 13 steranes (d C=29.6 to 26.7‰) from this bitumen indicate continued input from primary producers and eukaryotes. The 13 higher relative concentrations of gammacerane (d C=26.9‰) indicate increasing input from aerobic species. Slight 13 enrichment in d C in the wurtzilite extract (and several biomarkers) suggests sulphate-reducing bacteria outcompeted methanogens, thereby, eliminating the influence of methanotrophs in this later saline stage of deposition. Kongdian Formation 3 Natural gas contains the highest proportions of H2S (40–92%) Chen et al., 1996 (Ek) and Es4 member Continental half-graben among the sour gases encountered in China. The sedimentary Zhang et al., 2005 of the Shahejie Palaeogene rift with sequence consists of halite, anhydrite, carbonate, sandstone and Formation Neogene subsidence shale interbeds deposited in the evaporative brackish water Zhaolanzhuang field, lacustrine- salt lake setting. In the deepest part of the Jinxian sag,

Jizhong depression, the total thickness of evaporites is more than 1000 m, of which brines layered in feast” or “famine of cycles to responses mesohaline rocks: source Evaporitic Bohai Bay Basin, halite accounts for over 40%. Various organic-rich mudstones China intercalated with the evaporites are currently within the Eocene–Oligocene conventional hydrocarbon window (with a depth of 2500–3500 m), and likely the source for the oil and sour gas in the Zhaolanzhuang field. The temperatures of the gas reservoirs range from 75 to 100 C, too low for significant thermochemical sulphate reduction. The co-occurrence of abundant elemental sulphur with the sour gas and the d34 S values of the various sulphur-containing compounds indicate that the H2S gases were most likely derived from much deeper source kitchens where significant thermochemical sulphate reduction has occurred. Bucomazi Formation, 3 The Lower Congo hydrocarbon habitat is dominated by the Burwood et al., 1995, Cabinda, offshore Rift basin continental to Pre-Salt Bucomazi petroleum system. These lacustrine, often 1992 Angola transitional marine super-rich, laminated evaporitic sediments reveal considerable Burwood & Mycke, 1996 Cretaceous organofacies variations between their early lacustrine basin fill Schoellkopf & Patterson, and later sheet drape development with three major 2000 depositional regimes reflecting salinity and water depth control. 13 C depleted basal sediments, showing strong gammacerane/ 4-methyl sterane signatures, were segregated as seen by a major isotopic excursion. This event represents the transition from an early saline playa lake to a deeper water salinity-stratified mesohaline lake supporting a high level of bottom anoxia. For the intermediate sediments, sterane and tricyclic diterpane abundances, plus sterane/hopane ratios, had marine connotations and can be interpreted as the result of intermittent marine incursions. Foreshadowing irreversible oceanic ingression, a resurgence of gammacerane abundance in the uppermost sediments typified littoral-shallow marine depositional conditions. Lagoa Feia Formation, 3 Rift-stage lacustrine sediments are the source rock of all petroleum Trindade et al., 1995 Campos Basin, Brazil Rift basin continental to so far discovered in the Campos Basin, the most prolific oil Mello & Maxwell, 1991 Lower Cretaceous transitional marine province in Brazil. These organic-rich shales were deposited in anoxic brackish to saline lakes. Petroleum migration pathways involve direct contact between source and reservoir rocks within the rift sequence. Later migration to the marine sequence reservoirs is related to windows in the halokinetic salt layer connected to growth faults and unconformities. (continued ) 367 Table 5. (Continued ) 368

Formation/Group Basin Style Characteristics and depositional setting Reference locality and age .K Warren K. J. Muribeca and Maceio 3 Most hydrocarbon accumulations discovered in the Sergipe Mello et al., 1988 Formations, Sergipe Rift basin continental to subbasin are sourced by the protomarine Aptian marls and Basin, Brazil transitional marine calcareous shales of the Muribeca and Maceio formations both Lower Cretaceous below and above the Aptian salt (Ibura Member). These source rocks average about 6% TOC and are composed mainly of hydrogen-rich type II kerogen. Kimmeridgian Shale, 1b Seawater flowed southwards from Boreal Ocean into Tethyan Cooper et al., 1995 North Sea Sediment-starved deep Ocean but evaporation in the shallow waters of the archipelago Miller, 1990 Upper Jurassic marine basin centre of islands and shoals created waters of increased salinity and in generated by ongoing some cases local strong brines and evaporites, which sank and Permian-Mesozoic flowed as saline bottom currents (from 34–42‰) into deeper rifting and surrounded water. Areas of ponded deeper mesohaline water were by Purbeck evaporite- commonplace in the more rapidly subsiding grabens, separated carbonate platform by sills, denser waters accumulated until they were able to spill over the sills. In this way more saline waters migrated along the seabottom depressions, their paths being determined by local tectonic features, but mostly in a north to south direction. A stable water stratification ensued, the halocline being at about 50 m water depth and periods of widespread increased salinity are marked by “hot” shales. Purbeckian lacustrine 3 Within these beds, which immediately overlie the Purbeck Schnyder et al., 2009 beds, Dorset coast UK, Continental lagoons and evaporites, a large OM accumulation is recorded, with total Lower Cretaceous, lakes in sea-margin organic carbon (TOC) of up to 8.5 wt%. High hydrogen index position at edge of (HI) values (up to 956 mgHC g 1 TOC) point to a Type I OM, carbonate platform generally considered as derived from algal-bacterial biomass. This contrasts with the OM present in the underlying and overlying intervals, displaying in general lower TOC and HI values, and consisting of degraded algal-bacterial material with higher proportions of terrestrial OM. This organic-rich accumulation can be interpreted as a period of enhanced primary productivity within coastal lagoonal/lacustrine settings at times of low sea level and has strong affinities to modern Coorong Lakes in Australia. Shelf margin laminites, 2 Organic-rich laminated mudstones and wackstones deposited in Ayres et al., 1982 Arabian Gulf from NW Density-stratified pre-salt intrashelf, mesohaline basins on a gently downwarped Palacas, 1984 Iraq through the intrashelf basins epeiric platform. Intrashelf basins that retain organics all have a Evans & Kirkland, 1988 Arabian Gulf to central surrounded by density and salinity stratified water column with mesohaline Droste, 1990 Oman (e.g. Diyab, evaporitic platform. bottom carbonates. These basins source more than 90% of the Beydoun, 1993 Tuwaiq and Hanifa Some lows are possibly hydrocarbons in the Middle East. They are argillaceous Carrigan et al., 1995 Formations) tied to salt withdrawal dolomitic limestones that feed the most prolific petroleum Whittle & Alsharhan, Upper Jurassic system in the world and underlie the world’s richest reservoir: 1996 the Arab D in the Arab Formation. One of the most prolific source Ibrahim et al., 2002 units is the Hanifa Fm. in the Arabian Basin of Saudi Arabia. In the deeper parts of the intrashelf Arabian Basin (waters 30 m deep) the Hanifa is composed of laminite muds and marls, while in the surrounding shelf it is dominated by grainstones and packstones. Within the Hanifa laminites there are discrete but minor primary laminae of anhydrite (originally gypsum), as well as early diagenetic anhydrite nodules, both indicators of occasional hypersalinity. There are also laminae of fibrous

calcite, which some authors have interpreted as another brines layered in feast” or “famine of cycles to responses mesohaline rocks: source Evaporitic indicator of hypersalinity. The Hanifa is a widespread and prolific source, it can entrain more than 30 metres of laminites; total organic carbon exceeds 1%, with some sections having more than 5%. The kerogen is predominantly hydrogen rich, the generated oils have a high sulphur content, a Pr/Py < 1, and a predominance of even-numbered normal alkanes. Smackover trend of 2 Oil and gas in this trend are generated from algal-rich light-brown Oehler, 1984 Mississippi, Alabama Shallow restricted- to black laminated lime mudstones (argillaceous content <6%) Sassen, 1990 and Florida, circulation salinity of the Lower Smackover Formation. Deposition occurred in Mancini et al., 2003 northeastern Gulf of stratified intrashelf intraplatform depressions surrounded by a broad carbonate Mexico basin on a broad platform. Bottom waters were stratified with slightly saline Upper Jurassic carbonate platform waters supplied from the broad platform surrounds and the shoaling carbonate system was sealed by the sulfate evaporites of the Buckner Anhydrite. Todilto Formation 3 The Limestone Member of the Todilto Fm. is a widespread Vincelette & Chittum, Todilto Basin, USA Foreland flexural basin carbonate laminite up to 3 m thick, overlain in the subsurface by 1981 Middle Jurassic (lacustrine?) up to 30 m of CaSO4 known as the Gypsum Member, although it Evans & Kirkland, 1988 is mostly anhydrite. The Limestone Member is the source rock for 6 known hydrocarbon accumulations in the sands of the underlying Entrada Fm, while it and the overlying CaSO4 are the seal. The quantity of TOC is low (1%) for such a thin source rock and it has some unusual characteristics compared to most evaporitic source rocks. Laminite couplets are 0.15 mm thick yet are laterally continuous for up to 3.7 km and form widespread cohesive “sheets”, which invariably contain remnants of vascular plants. The Todilto is probably lacustrine with a marine seep hydrology, similar in hydrology to the coastal salinas of southern Australia. The organics reflect the growth of a healthy conifer cover in its surrounds and its waters were density-stratified lacustrine, probably fed via a marine seepage inflow and periodic seasonal runoff. This maintained a density- stratified brine column, first at carbonate saturation during deposition of the Limestone Member, then at gypsum saturation during the deposition of the Gypsum Member. Organic mudstones 3 Total organic carbon (TOC) values range from 1.23 to 7.41 wt% of Kagya, 1996 intercalated with Rift basin continental to kerogen Type II/III. The evaporite (hypersaline) influence is evaporites, Mandawa transitional marine indicated by the presence of C-24-tetracyclic terpanes, Basin, Tanzania gammacerane and C-35- homohopanes. The relative abundance

Triassic of tricyclic terpanes (C-19-C-28 +) with respect to pentacyclic 369 terpanes (C-27-C-35,) seems to change with depth, whereby (continued ) Table 5. (Continued ) 370 Formation/Group Basin Style Characteristics and depositional setting Reference locality and age .K Warren K. J. the tricyclic/hopanes ratio apparently increases with depth. The mixed organic input from marine and terrestrial precursors are indicated by mixed abundances of C-27-, C-28-, C-29- steranes. Sub salt-allochthon oil 3 The oil seeps are either associated with upper Horton Group Fowler et al., 1993 seeps, Windsor Group, Rift basin continental to (Ainslie Formation) or basal Windsor Group (Macumber Nova Scotia, Canada transitional marine Formation) sediments. The biomarker distributions of the Carboniferous samples are similar to Stoney Creek oils and their lacustrine carbonate source rock (Albert Shale) of the Moncton Sub-basin, New Brunswick, as are oils from seeps in the Pugwash Salt mine. Black shales in the 1a Organic-rich black shales (informally known as the Cane Creek, Evans & Kirkland, 1988 Paradox Member of the Foreland flexural basin Chimney Rock, Gothic shales) form a carbonate laminite basal Hite et al., 1984 Hermosa Formation, sequence to a number of salting-upward evaporite cycles in the Paradox Basin, USA Paradox Member. Mineralogically the shales are between Carboniferous 30–50% calcite or dolomite with clays and quartz sand forming (Pennsylvanian) the remainder of the matrix. TOC values of 5% of hydrogen- prone organics in the black shales are usual, with values of 10% not uncommon and the highest values more than 20%. The organics are mixtures of halotolerant debris and marine-style organics formed when surface waters were at marine salinities, as well as occasional terrestrial organics washed into the basin from the surrounding hinterland. Oil Shales, Junggar 3 Junggar Basin is one of the largest oil-producing basins in China, its Carroll, 1998 Basin, NW China Controversial, with Upper Permian oil shales are among the thickest and richest Carroll et al., 1992 Upper Permian tectonic lacustrine source rocks in the world. Together the Jingjingzigou, Tang et al., 1997 interpretations Lucaogou, and Hongyanchi Formations of the southern Junggar ranging from foreland Basin comprise over 1000 m of organic-rich lacustrine facies. flexure to regional They record an evolution from relatively shallow, evaporative transtensional basin lakes to freshwater lakes with fluvial systems. Jingjingzigou Formation was deposited in a perennial saline lake characterized by low TOC and HI, and biomarker features (such as abundant b-carotane) consistent with a specialized saline or hypersaline biota. Biomarker distributions in Jingjingzigou Formation extracts most closely resemble oils from the giant Karamay oilfield. Overlying Lucaogou Formation represents one of the richest and thickest lacustrine source rock intervals in the world, yet it contradicts conventional lacustrine source rock models in at least two important aspects. First, deposition occurred at middle palaeolatitudes (39–43N) rather than in the tropics. Second, limited nutrient supply in a drainage basin dominated by intermediate volcanic rocks appears to have caused low to moderate primary productivities. Stable salinity stratification and low inorganic sedimentation rates in a deep lake nonetheless resulted in deposits with up to 20% TOC and HI near 800. Overlying Hongyanchi Formation has 1–5% TOC but low HI, and was deposited in freshwater oxic to sub-oxic lakes. Ravnefjeld Formation, 3 The Ravnefjeld Formation is subdivided into five units that can be Christiansen et al., 1993 East Greenland Upper Rift basin continental to traced throughout the Upper Permian depositional basin. Two Permian transitional marine of the units are laminated and organic rich, and were deposited under anoxic conditions. They are considered good to excellent brines layered in feast” or “famine of cycles to responses mesohaline rocks: source Evaporitic source rocks for liquid hydrocarbons with initial average TOC (total organic carbon) values between 4 and 5% and HI (hydrogen index) between 300 and 400. The cumulative source rock thickness is between 15 and 20 m. The source rocks are separated and enclosed by three units of bioturbated siltstone with a TOC of less than 0.5% and an HI of less than 100. These siltstones were deposited under relatively oxic conditions. The organic geochemistry of the source rocks is typical for marine source rocks with some features normally associated with carbonate/evaporite rift environments [low Pr/Ph (pristane/phytane), low CPI (carbon preference index), distribution of tricyclic and pentacyclic terpanes]. The establishment of anoxic conditions and subsequent source rock deposition was controlled by eustatic sea level changes. Phosphoria Formation, 1b Correlations between biomarker indicators of anoxia and salinity Dahl et al., 1993 Little Sheep Creek, Foreland flexure basin suggest that anoxia was in part the result of a chemocline Montana separating normal marine waters above from more saline bottom Permian waters. Anoxia and salinity in the bottom waters increased with time making conditions in the basin progressively more hostile to benthic organisms. Kupferschiefer 1a Thin, widespread organic-rich laminated mudstone deposited in Bechtel & Puttmann, Formation, Rift basin, restricted shallow mesohaline marginal sea-lakes with waters which were 1997 NW Europe marine <100m deep and mostly 10–30 m deep. Surface exchange with Permian Zechstein ocean was restricted by palaeohighs. Anhydritic lacustrine 3 The UKCS well 9/16-3 drilled on the western flank of the Beryl Duncan & Buxton, 1995 beds, East Shetland Rift basin, restricted Embayment indicates local development of hypersaline Platform, North Sea marine environments equivalent to the Achanarras/Sandwick fish bed. Middle Devonian Shows close affinity with contemporaneous Middle Devonian source rocks of the Inner Moray Firth and crude oil in Beatrice oil field. Muskeg Formation and 1a Laminated organic-rich bituminous mudstones deposited in Clark & Philp, 1989 Lower Keg River Rift basin, restricted pre-evaporitic density stratified water columns. Vertical Stasiuk, 1994; Chen et Member, Alberta, marine migration from the Muskeg formation to the Muskeg Reservoirs al., 2005 Canada may have occurred through local fracturing of anhydrites driven Devonian by the dissolution of Black Creek Halite. Laminated evaporitic 1a Biomarker characteristics indicate a carbonate/evaporite source Gardner & Bray, 1984 A-1 mudstones, Rift basin, restricted rock deposited under hypersaline conditions in a strongly Obermajer et al., 1998,

Michigan Basin marine reducing environment. The source rocks occur in the basin 2000 371 Silurian centre in organic-rich laminites of the inter-reef A-1 Salina (continued ) 372 Table 5. (Continued )

Formation/Group Basin Style Characteristics and depositional setting Reference Warren K. J. locality and age

Formation, a mesohaline carbonate deposited beneath a density stratified brine column.

Chandler Formation, 1a Thin bituminous pre-evaporitic carbonate mudstone deposited Bradshaw, 1988 Amadeus Basin, Foreland flexure, subaqueously in a restricted basin immediately prior to the Australia Lower Restricted marine deposition of the thick halites of the Chandler Formation. Cambrian Hormuz Series, Arabian 1 Almost all the Persian Gulf and large areas of southern Iran and Amthor, 2000 Gulf and counterparts Foreland flexure, northeastern Arabia are underlain by a thick sequence of Edgell, 1991 in Oman, India and restricted marine sediments, known as the Hormuz Series, or the Huqf Group in Grantham et al., 1988 Pakistan Oman. It is made up of interbedded salt, anhydrite, dolomite, Peters et al., 1995 Neoproterozoic to Early shale and sandstone. It is not only the cause of many salt-dome- Terken & Frewin, 2000 Cambrian related oil and gas fields but is also considered to have been a Schoenherr et al., 2007, major source rock for hydrocarbons in Ordovician, Devonian, 2009 Carboniferous, Permian and perhaps younger reservoirs. These oils have characteristic biomarkers and highly depleted carbon isotopes signatures indicative of their prokaryotic precursor. Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 373

Hot Spot / Thermal Doming continental hydrology, supra-sea-level setting means marine seepage not possible). Wilson Cycle early Stage B Continental lacustrine source rocks (Quaternary with ancientcounterparts) Stage A Stable craton Elevation (km) Stage G Volcano: mafic if from hot spot. Felsic if from Peneplained 3 Horst Graben tinent prox melting of continental crust mountains -con imi Stage B -to ty nt bas e age ins p Early rifting sea tin p os Normal faults n ee si 0 o l s ble level C e ev -l Stage F a e Continent-Continent -s -3 b Collision u Felsic batholiths from fractional s

d

e melting of lower continental crust t

a WILSON

l

o

s I CYCLE Stage E Foundering of Rift Valley transition to restricted marine (stepped marine invasion Closing Remnant

via seepage spillover). Wilson Cycle later Stage B or early C. Ocean basin Stage C C

o

Marine source rocks in rift to incipient marine evaporite stage n Full Ocean basin

t

i

n

e

Aulocogen and intracratonic sag n

t s

f

a

r

a

(no Quaternary counterparts) p a

r Stage D t Elevation (km) Axial rift Continental Terrace Subduction Zone 3 subsealevel seepage basin Alluvial fan & Ocean begins to close (hinge zone) C lake deposits Sea Level sealevel 0 Brine level A -5

Continent-Continent Collision (periods of marine seepage coincident Increasingly restricted hydrographic entrance to a closing seaway. The restriction is with hydrographic isolation). Wilson Cycle Stages later E & F due to fault block rotation and transform offset in late Stage B to early C or foreland bulge of stages E & F. Basinwide evaporites will follow with complete hydrographic Continental lacustrine source rocks & evaporites Collision and/or sag belt evaporites isolation and onset of long-term sub-sea-level seepage. (Quaternary with ancient counterparts) (no Quaternary counterparts) Hinterland Volcanic front thrusts Suture zone Backarc Foreland basin (marginal) (sub-sea-level) Periplatform depression basin l (potential source rock site greenschist sea level Evaporitic Epeiric seaway with increasing restriction mudflat enta of shelf waters) sabkha amphibolite salina Intrabasinal way Ancient continental margin depression mudfla (stratified, sea sediment wedge (thrust- anoxic t granulit e faulted & folded) Periconcontin Ancient axial graben Open Organic-rich laminites in bottom depressions 500 km marine of a stratified mesohaline marine-fed basin B 500 m

Fig. 19. Tectonic settings of ancient evaporate source rocks. (A) Ancient evaporite source rocks and regions with Quaternary counterparts (in part after Warren, 2006). (B) Styles of intrashelf and platform depressions where anoxic mesohaline bottom brines tended to accumulate in an ancient evaporitic platform. (C) Characteristics of the Wilson Cycle.

rifting (“zip then split”) tectonics encourage the in the lower parts of the basin floor in waters accumulation of substantial volumes of salts and ranging from hundreds of metres deep to organic-rich evaporitic sediments in sub-sea-level ephemeral. tectonic depressions (Fig. 19). In the past 800 Myr there have been two such tectonic cycles defined Ancient mesohaline source rocks by supercontinent accretion and disaggregation (i.e. the accretion and disaggregation of Phanero- Worldwide, studies of ancient evaporitic basins zoic Pangea and Neoproterozoic Rodinia). Marine- have shown that organic-rich mesohaline sedi- fed evaporitic source rocks tend to form at times ments accumulate in ephemeral surface brines, when the tectonic depression is undergoing hydro- saltern sediments, or basin and slope settings in graphic isolation from the open ocean. The basin both marine and continental regimes (Evans & still has a surface (hydrographic) connection to Kirkland, 1981; Oehler, 1984; Warren, 1986; Bus- the ocean, but inflow is restricted and the basin son, 1988; Kirkland & Evans, 1988; Rouchy 1988). is typically surrounded by widespread salty The most prolific accumulations of organics in platforms with sheets of salterns and evaporitic ancient evaporitic sediments tend to have been mudflats (Fig. 19). When the surface connection deposited as laminated micritic carbonates that to the open ocean is completely cut-off, the accumulated beneath density-stratified moder- basin becomes a marine-fed sub-sea-level seepage ately-saline (mesohaline) anoxic water columns depression and widespread thick salts precipitate of varying brine depth. There are three, possibly 374 J. K. Warren

Pre-drawdown sea level ≈10s-100s m Brine surface 1a Messinian style Drawdown Basinwide evaporites

Marine-hypersaline across a restricted, in part evaporitic, arid platform Setting 1 Open sea B sea level ri Basinwide setting 1b n e Deep basinwide ≈ marine sediments 10s-100s m Kimmeridge style Stratified marineStratified

Restricted shallow epeiric seaway, at times evaporitic sea level 2a ≈10 m

Intraplatform Hanifa-Arab style Intraplatform depressions

Shelf edge algal bloom Setting 2

2b Phosphoria style ≈10s-100s m Upwelling Epeiric lows platform

Platf. edge Platf. (Nutrient-rich)

Lake water surface ≈ Setting 3 10s-100s m Green River style (Quaternary analogues) Saline lacustrine

sea level Gulf of Mexico style ≈10s-100s m Prograding delta/platform Setting 4 salt allochthon (Quaternary analogues) Halokinetic lows

Fig. 20. Dominant depositional styles for evaporitic source rocks (dark green). All the water bodies show evidence of salinity- related density stratification (indicated by dashed line); this is also reflected in an associated heliothermic stratification (after Warren, 2006). four, major mesohaline density-stratified settings (b) shelf-edge depressions with layered meso- where organic-rich laminites (source rocks) accu- haline brines. mulate in saline settings that are also associated (3) Saline-bottomed lows in perennial underfilled with, or evolve into, evaporite deposits (Fig. 20; saline lacustrine basins. Table 5). These are: (4) Closed seafloor depressions in halokinetic deep-water marine slope and rise terrains. (1) Basin-centre lows in marine-fed evaporitic drawdown basins: Basin Setting 1 (a) evaporite-plugged mesohaline basin centre; (b) evaporite platform rim surrounding There are two depositional styles for basin-centre restricted and stratified slightly-mesohaline or basinwide mesohaline source rocks: (a) basin- carbonate basin centre. centre drawdown laminites intercalated and (2) Mesohaline intrashelf lows on top of epeiric often sealed by basinwide salts; (b) basin-centre evaporitic platforms; laminites where the basin margin is a shallow, (a) intraplatform depressions with layered restricted, at times evaporitic platform that sur- mesohaline brines; rounds a slightly mesohaline deep-water starved- Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 375 basin centre. Bottom waters in this deeper part of 400 million barrels of oil and about 1 TCF of gas in the basin were never drawndown or concentrated the Paradox Basin in fields such as Ismay and to salinities where basinwide salts precipitated. Aneth (Peterson & Hite, 1969). Matrices in Setting 1b basin-centre laminites range The problem of evaporite plugging plagues many from limestones through marls to siliciclastics basinal source rocks where the basin centre (Fig. 20). evolved to accumulate basinwide evaporates, and is one of the main reasons for the dearth of large Basin Setting (1a) In this setting the basin is onshore oilfields beneath bedded salt or within largely isolated from a surface marine connection intrasalt carbonates in the Zechstein Basin of and high levels of organics accumulate as “black NW Europe. Organic-rich source intervals such shales” (typically carbonate laminites), which are as the Stinkdolomit, Stink-kalk, and Stinkscheifer intercalated with, and overlain by, basinwide eva- are widespread, but the associated oil accumula- porite salts (typically gypsum/halite). These lami- tions are never more than localized and are small nites accumulate on the bottom of mesohaline scale. This setting also created the salt-encased density-stratified pools in topographically closed self-sourced low-permeability reservoirs in the parts of the basin floor during the early stages Cambrian Ara Group platform carbonate stringers of isolation and drawdown. Inactive, typically and basin centre silicilytes of the South Oman subaerial, shelf margin reefs and pinnacles typi- Salt Basin (Al-Siyabi, 2005; Amthor et al., 2005; cally lay updip or encircled the basin-centre lows Schoenherr et al., 2007, 2009). Very rich organic (Warren, 2006). Subsequent encasement of these source beds can characterize Setting 1a sediments, platform buildups and other potential reservoirs but the intercalated seals prevent most of the vola- by “fill and spill” evaporites means these basins tiles from ever escaping into a reservoir. Some- easily become highly focused hydrocarbon flow times, as in the silicilytes of Oman, the source beds systems. Hydrocarbons accumulate in the reefs can become self-reservoiring. In later burial diag- or shelf margin shoals beneath basinwide evapor- enesis the trapped hydrocarbons can play an ite seals. Such systems typify the marine-fed Silur- important role as a reductant and metal fixer as ian reef/salina salt association in the Michigan ongoing burial dissolution of salt interbeds focuses Basin, USA (Gardner & Bray, 1984), the Devonian long-term contact with basinal waters carrying Rainbow Reef reservoirs of the Black Creek/Musk- Cu, Pb and Zn (Warren, 2000). eg Basin of Alberta (Clark & Philp, 1989), and the Messinian marls of the Lorca Basin, Spain (Russell Basin Setting 1b Basin-centre mesohaline accu- et al., 1997). mulations in this setting are much more efficient Expulsion efficiencies suffer from encasement petroleum producers than Setting 1a as they lack and widespread salt plugging of the potential intercalated beds of basinwide gypsum or halite, source rocks in many evaporite-rich Setting 1a which otherwise create salt-plugged and salt- basins. This style of deposit tends to retain vola- cemented source intervals. Setting 1b source rocks tiles in the source beds until the whole system develop where dense mesohaline bottom-waters becomes overmature. For example, in the Gibson pond on the bottom of a deep density-stratified Dome No. 1 well in the Paradox Basin, almost all restricted-marine basins. Slightly elevated bottom- of the black shales in the Upper Carboniferous brine salinities are maintained by a series of dense Paradox Member are mature enough to have gen- brine underflows, fed from nearby shoalwater eva- erated oil (Hite et al., 1984), but the hydrocarbons poritic platforms (Fig. 20). Such basins are typified have been largely retained in this mature source by a deep-water “marine” centre and the presence rock, reflecting the highly efficient sealing effect of widespread evaporitic and shoal water carbo- of the intercalated evaporite beds and salt plugs nate sediments in the surrounding platforms and (mostly halite). Only where the black shales are shelves. Setting 1b basins are best thought of as intercalated with porous carbonates have the stunted or underdeveloped basinwide evaporite hydrocarbons escaped. The source potential of systems. Development of the basinwide evaporite these shales is very high; the “Gothic shale” mem- hydrology was suspended prior to the basin ber is capable of generating almost 5000 barrels per centre drawdown reaching the state of sea-surface acre. But that potential is never more than partially (hydrographic) isolation, which is needed for realized. Paradox “shales” are responsible for widespread salt precipitation across the basin cen- an accumulative production of a little more than tre. Nonetheless, evaporitic conditions dominated 376 J. K. Warren in isolated platform depressions about the basin generating local briny anoxic bottoms on the dee- margin. Typical examples of this style of associa- per parts of the basin floor (Clark et al., 1999). tion are the Upper Jurassic Kimmeridge shales of the North Sea (Miller, 1990; Cooper et al., 1995), Basin Setting 2 the organic-rich laminites of the Cherry Canyon Formation in the Permian Delaware Basin of West Upper Jurassic source rocks of the Middle East are Texas (Jones, 1984), and possibly the Jurassic well-studied examples of the epeiric shelf or mar- Lower Smackover Formation in the Proto-Gulf of ine evaporitic platform settings and typify Setting Mexico (Sassen, 1990). 2a source rocks, which are deposited within local In Setting 1b, the deep-water basin centre somewhat deeper, density-stratified mesohaline remains “sediment starved” and density-stratified, intrashelf lows (Figs 19, 20 and 21; Table 5; Ayres with the upper less-saline part of the water column et al., 1982; Evans & Kirkland, 1988; Droste, 1990; typified by normal marine water, maintained Warren, 2006). In the Tethyan of the Middle East through surface connections to the open ocean. this style of source rock feeds a petroleum system The little sediment matrix that does accumulate that is probably the most efficient in the world. in the basin centre settles into an anoxic thermally/ It evolved from Upper Jurassic source rock accu- density stratified bottom, so that the sediment mulators (typically with TOC’s 1%, occasionally matrix of the source laminites is dominated by a up to 13%) into evaporitic mudflats sealing the planktonic or nektonic biota and a more or less mostly bioclastic carbonate reservoirs of the Arab constant elevated organic content. Carbonate Formation cycles, into the regional Hith Anhydrite banks or reefs in the surrounding platform grade seal, which was deposited on a saltern-covered landward through lagoonal and evaporitic plat- platform. form facies into terrestrial siliciclastics. At times The laminite source rocks in the various intra- of slightly lowered sea-level these epeiric plat- shelf depressions were deposited at times of wide- forms can go evaporitic and so deposit widespread spread epeiric carbonate deposition and stagnant platform salts (Warren, 2006). Such basins show a oceanic circulation. It was a time when a warm centrifugal salinity gradient where the highest shallow greenhouse sea covered much of the Ara- salinity areas are the shallow evaporite platforms, bian platform and was precipitating carbonates which supply dense saline waters that trickle and and evaporites over much of its extent. Denser seep basinward to pond in seafloor lows at the warmer waters, generated by evaporation of these anoxic base of a density-stratified water column. epeiric waters, along with waters supplied by the With Setting 1b, the formation of evaporites and surrounding evaporitic mudflats, were concen- saline waters about the basin edge is not typically trated to where they were somewhat more saline followed by the deposition of basin-centre evapor- than normal seawater. These dense brines then ites. At the time the deep-water organic laminites trickled and seeped over the shallow seafloor are accumulating, the deep basin-centre waters lie into the lower parts of restricted intrashelf basins at the bottom of the thick density-stratified water to create density-stratified bottom waters that column in a semi-enclosed seaway, and bottom were not more than tens of metres deep and no brines may be no more than 3–5‰ more saline than more than 10–30‰ more saline than seawater the normal marine waters. For example, at the time (Ayres et al., 1982). Ongoing mixing and dilution the Upper Jurassic Purbeck evaporites were accu- of the bottom-hugging brines during their passage mulating on the platforms of northern Europe, the to the lows meant that the basal waters on the anoxic bottom waters in the marine basin centre intrashelf lows, although saline, rarely attained where the Kimmeridge Clay was accumulating had gypsum saturation (mostly mesohaline anoxic salinities around 42‰, temperatures 30C and brines). The overlying column was typically at densities 1.027. The overlying near-normal near-normal marine salinities. Salt withdrawal marine waters had salinities of 34–39‰, surface and dissolution of salt diapirs and allochthons, temperatures of 26C in the south and as low as 6C sourced in the Precambrian Hormuz salt, perhaps farther north in the region of the Boreal Ocean helped create the intrashelf depressions and may inflow, and densities around 1.0267 (Miller, 1990). also have played a role in generating a portion of As the Kimmeridge Clay source rocks accumu- the bottom brines. lated, halokinesis and salt solution of Zechstein One of the most prolific intrashelf source rocks mother salt probably also played a role in in the Middle East is the Upper Jurassic Hanifa Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 377

W E Basin centre Basin margin GR (API) GR (API) 0 100 0 100 Jubaila Jubaila 6200 ft 5450 ft Hanifa

Peak source rock development waiq u T 5 m 10 ft Organic-rich lime mud/wackestones Hanifa Formation Hanifa Bioturbated lime mud to peloidal packstones

Anhydrite (some with gypsum ghosts) 6300 ft

Peak source Dolomite of NE basin margin rock development Grainstones of Tuwaiq Formation Tuwaiq Hardground

SW Arabian Basin NE Qatar Arabian Gulf Hanifa intraplatform Margin basin centre Margin

100 km

30 m

Fig. 21. Correlation and lithofacies of the Upper Jurassic Hanifa Formation, Saudi Arabia. This Setting 2 intraplatform basin source rock was deposited beneath relatively shallow and anoxic mesohaline bottom waters in a slight depression on the shelf and was surrounded by epeiric evaporitic sedimentation, as indicated by the presence of anhydrite in the Hanifa Formation (after Droste, 1990). Peaks in the organic content of these carbonate mudstones are indicated by peaks in the gamma curve. Cross section redrafted from Carrigan et al. (1995).

Formation deposited in the intrashelf Arabian mesohaline layered bottom waters are composed Basin of Saudi Arabia (Fig. 21; Droste, 1990; Car- of organic-rich laminite muds and marls, while rigan et al., 1995). It sources most of the hydro- sediments of the surrounding Arabian shelf are carbons reservoired in the Arab cycles of Saudi dominated by grainstones and packstones. As the Arabia and is regionally sealed by the Hith Anhy- various intrashelf depressions filled with lami- drite. The organic-rich portions of the Hanifa nites they shallowed to where the stratification and its equivalents elsewhere in the Middle East was lost and the sediment became an open- were deposited in the “deeper” parts of a number marine packstone-wackestone equivalent to sedi- of Jurassic intrashelf basins (waters 30 m deep). ments deposited over the rest of the Arabian Sediments accumulating beneath the slightly Platform. 378 J. K. Warren

Successive platform isolation, via buildups of The likelihood of numerous water level changes a transgressive platform rim and a slight fall in during the life of a saline lake especially affects sea level, then drove deposition of anhydritic salt- laminites deposited in shoal-water moats and mar- ern or mudflat caps of the various Arab cycles gin mudflats and so can lower their preservation (Cycles A–D; Warren, 2006). Within the Hanifa potential (Bohacs et al., 2000). Most oil-prone laminites, there are discrete laminae and thin beds Setting 3 lacustrine source rocks were deposited of primary anhydrite, as well as early diagenetic at the bottom of perennial salinity-stratified hydro- anhydrite nodules, both indicators of periodic logies, with water column depths measured in hypersalinity even as the laminites were accumu- metres to tens of metres, not as subaerially exposed lating. Likewise, the evaporitic cap to each of the algal mudflats. Examples include the Wilkins Peak source cycles in the Hanifa Formation in the Member of the Eocene Green River Formation, Arabian Basin preserves aligned gypsum ghosts USA, the Lower Cretaceous Lagoa Feia Formation indicating a subaqueous gypsum precursor. Simi- of the Alagoas portion of the Campos Basin in lar, but volumetrically less prolific, intrashelf Brazil, and the Permian Jingjingzigou Formation source rocks characterize the Lower Smackover in the Junggar Basin, China (Table 5). Formation (Upper Jurassic) of the northeastern Desiccation needed to form an underfilled lacus- Gulf of Mexico (Oehler, 1984; Sassen, 1990) and trine succession typically means that saline lacus- the Cretaceous Sunniland Formation of Florida trine phases have lesser aerial extents compared (Palacas et al., 1984). to units deposited at times of fresher water in the A variation on this density-stratified mesohaline lake depression. This does not necessarily mean platform-depression style of source rock accumu- the evaporitic lacustrine source rocks are less pro- lation is the phosphate and organic-rich Setting 2b lific than their freshwater counterparts. Within the source rocks sediment of the Phosphoria Forma- Green River Formation there are two associations tion in the USA (Stephens & Carroll, 1999). This (fresh and saline) of lacustrine organic laminites unit sources much of the oil in Wyoming and was exemplified by the Luman Tongue and the Laney deposited in somewhat-saline shelf-edge depres- Member (Fig. 22; Horsfield et al., 1994). The Luman sions of the Phosphoria Sea adjacent to an area of Tongue consists of organic matter-rich mudstones marine upwelling. The nutrient-rich waters facili- deposited as profundal sediments at a time when tated algal blooms near and above the shelf edge, lake waters were relatively fresh (Fig. 22A). Prox- while bottom-hugging brines, seeping seaward imal organic matter-poor sediments, as well as from the evaporitic hinterland, ponded in stagnant coals and thin sandstones, were deposited on the shelf-edge depressions. Overlap of the two systems lake plain. The highest levels of TOC in the Luman created local anoxic bottom-waters in the shelf- Tongue occur in lake-margin deposits, which con- edge depressions that preserved the organics fed by tain a mixture of alginite and vitrinite, but they the detritus of the overlying algal blooms (Fig. 20). have a low hydrogen index and a low petroleum generation potential (Fig. 22B, C). In fact, the pet- roleum generation potential of these freshwater Basin Setting 3 deposits is no more than moderate. These source rocks accumulated in sediment- In contrast, the organic percentages of the carbo- starved or underfilled saline lakes in arid climates. nate laminites of the evaporitic Laney Shale are The laminites typically accumulated in the early much higher (6–22%) and these are hydrogen continental stage of infill in an opening rift, prior to prone (Fig. 22B, C). The most organic-rich samples its opening into a marine-fed marginal evaporite were deposited in the lowest parts of the lake and basin (Figs 19 and 20), or in the restricted lacus- are composed mostly of alginite with relatively trine stage of a foreland flexure in a collision belt. minor contributions from higher plants. The much Modern underfilled saline rift lakes have some of higher petroleum potential of the Laney Shale the highest rates of organic productivity known reflects the marked density stratification of Lake and can accumulate high levels of organics within Gosiute waters at the time the Laney was accumu- carbonate laminites. Some of these lacustrine lami- lating. At that time bottom anoxia was stabilized nites accumulate beneath deep density-stratified by the perennial highly saline bottom waters water columns, while others accumulate as “moat (Boyer, 1982; Fischer & Roberts, 1991). The dis- facies” or microbial mudflats around lake margins solution of underlying evaporites to create density- (Fig. 20; Table 5). stratified lacustine waters also characterized the Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 379

Green River Rock Springs Washakie Basin Uplift Basin Lake West East chemistry Upper fresh Eocene saline

Laney Member evaporitic 2500 m Wilkins Peak Member saline Middle Eocene fresh

Luman Tongue A 250 km

1000 200 C I ) -1

800 100 S2 rock (mg g S2 rock

TOC) 0 -1 600 II 0 10 20 TOC (wt %)

Laney Member (evaporitic) Luman Tongue (deltaic) 400 Luman Tongue(vitrinite-rich) Hydrogen Index (mg HC g Hydrogen Index

200

III 0 0 40 80 120 160 200 -1 B Oxygen Index (mg CO2 g TOC)

Fig. 22. Lateral variation and kerogen character of the Laney Member and the Luman Tongue of the Eocene Green River Formation, USA. (A) Schematic E–W cross section showing lateral extent and thickness of various lacustrine units (after Bohacs et al., 2000). (B) Hydrogen and oxygen indices. (C) Pyrolysis yields of hydrocarbon-equivalents (mg g 1 rock) plotted against organic carbon percentages. (B and C) after Horsfield et al. (1994).

Cretaceous Purbeck strata of Dorset, although in Basin Setting 4 this case the underlying evaporites were marine This is an increasingly documented open-marine and the depositional setting was akin to the sea- evaporite-associated source rock setting where margin meteoric lakes of today’s Coorong region of density-stratified saline bottom brines and Australia (Schnyder et al., 2009). 380 J. K. Warren organic-enriched laminites accumulate in brine- depressions with mesohaline “famine or feast” bottomed depressions on top of and adjacent to laminites (Table 6, settings 1 and 2). These Pre- shallow and dissolving salt allochthons (Fig. 20). Quaternary evaporitic source rocks generated far With burial these laminites may act as source greater hydrocarbon volumes than all lacustrine rocks, but unlike the restricted settings of the pre- source rocks combined, yet many source rock mod- ceding three styles, deposition typically occurs in els for evaporitic mesohaline carbonates still draw open-marine waters in continental slope and rise strong comparisons to underfilled Quaternary environments. The laminites accumulate on the lacustrine settings. Such “strict” uniformitarian floor of deep brine pools that form on or near comparisons lead to the conclusion that evaporitic the margins of actively flowing and dissolving mesohaline source sources are probably not all that shallow salt allochthons (Warren, 2006). This is significant as contributors to the volume of exploi- also a significant setting for the formation of base table hydrocarbons in the world. metal-hosting laminites as in Tunisia and the It is the author’s opinion that depositional set- Red Sea (Warren, 2000). As yet it is not a widely tings in arid environments are still being consid- documented environment for hydrocarbon source ered in the same way that Lotze (1957) viewed rocks, but it may in-part explain the higher than the abundance of life in modern deserts. Organic expected source potential of many prodelta and accumulations in ancient evaporitic source rocks slope muds in the passive margin fill of evaporite- should be seen as biological responses to the “feast floored halokinetic rifts. or famine” cycles that still characterize life in arid Source rocks of settings 1a, 2 and 3 are typified depositional settings. Formation of ancient mar- by the accumulation of mm-scale layers of oil- ine-fed mesohaline depressions required varying prone organics typically in a matrix of fine carbo- combinations of greenhouse eustacy (epeiric sea- nates. Setting 1b typically contains higher levels of ways) and tectonics-climate, which are also siliciclastic fines and in many cases the host to the needed to create huge sub-sea-level depressions organics is a basinal marl or less often a laminated filling with evaporites (epeiric platform evaporites, calcareous shale. The matrix of Setting 4 laminites marine-seepage rifts, soft collision belts and far- tends to be composed of whatever detrital sedi- field intracratonic sags). These systems do not ment is accumulating above the salt allochthon. have same-scale Quaternary counterparts (Warren, In many situations, such as the Gulf of Mexico 2010). Yet, it was in salinity-layered intraplatform and the Mediterranean allochthon terranes, this epeiric depressions and restricted tectonically matrix is a siliciclastic mud/clay laid down at the induced mesohaline basin centres where the requi- distal ends of prodelta wedges. In others, such as site schizohaline water columns and stable long- the Jurassic and Cretaceous of the Arabian term brine bottoms occurred. They did so across Gulf and the Triassic of Tunisia, the matrix is time scales and across areas that not only allowed carbonate. widespread periodic halotolerant blooms in the surface waters of whole mesohaline-floored sea- ways, but also formed in settings that facilitated CONCLUSION long-term stable anoxic bottom brines. This anoxic brine-soaked bottom in-turn allowed widespread It seems that there are no same-scale “famine or mesohaline source rocks to accumulate and to be feast” analogues for modern and ancient saline preserved across the areally-extensive depressions lacustrine settings (Table 6, Setting 3). Organic- (Figs 19 and 20; Table 5). rich carbonate laminites forming in the African rift As for most ancient evaporite styles, the present valley lakes have been documented and similar- is not a suitable time for studying scales of marine scale counterparts exist in the Mesozoic source mesohaline source rock development. However, rocks found for example in the Cabinda Basin of process and texture relevant to these ancient Angola and the lacustrine basins of South America mesohaline source rocks can be seen in “famine (Table 5). Likewise, Quaternary examples of supra- or feast” cycles in small-scale Quaternary conti- allochthon brine lakes with anoxic bottoms rich nental deposits. Rather than the words of in organics are now being documented (Table 6, Lotze (1957), a more apt aphorism to describe life Setting 3). in modern and ancient saline systems is found in However, there are no modern counterparts for the words of John Morley, a 19th Century Scottish most ancient large-scale marine evaporite statesman (1838–1923), agnostic, and the First Table 6. Summary of evaporitic source rock associations

Setting Other significant Some ancient examples Quaternary Tectonic/eustatic characteristics counterparts associations

Setting 1. Basin-centre 1a. Drawndown evaporite- Cambrian Ara stringer and silicilytes, None Rifts, collision belts and vprtcsuc ok:mshln epne occe f“aieo es”i aee brines layered in feast” or “famine of cycles to responses mesohaline rocks: source Evaporitic lows in marine-fed sealed and plugged Oman; Silurian reef/Salina Salt, intracratonic sags with evaporitic drawdown mesohaline basin centre Michigan Basin, USA; Devonian complete hydrographic basins, typically with carbonates Rainbow Fm of the Black Creek/ isolation of marine- evaporite platform rim Muskeg Basin, Canada; Permian seepage basin centre Stinkdolomit Zechstein Basin, Europe; Carboniferous Gothic Shales, Paradox Basin, USA; Messinian marls, Lorca Basin, Spain 1b. Density-stratified Permian Cherry Canyon Fm, Partial Often tied to early opening restricted-marine Delaware Basin, USA: Jurassic stages of rifts in semi arid slightly-mesohaline Kimmeridge shales, North Sea; climatic settings in basin centres with no Jurassic Egret Member, Jeanne greenhouse climate immediately overlying d’Arc Basin, offshore Canada; mode. Some aspects of evaporite seal Cretaceous Sirte Shale, Sirte Basin, Red Sea/Gulf of Suez are Libya similar, but high aridity and icehouse eustacy do not allow a direct comparison Setting 2. Mesohaline 2a. Intraplatform lows Hanifa Formation in the intrashelf None Greenhouse eustacy creates intrashelf lows within with adjacent epeiric Arabian Basin, Saudi Arabia and its continuous shelf- or an epeiric evaporitic mesohaline shoals equivalents throughout the Middle ramp-edge rim, the platform East; Lower Smackover Formation dissolution of the crests of (Upper Jurassic) of the northeastern nearby active halokinetic Gulf of Mexico; Cretaceous structures may contribute Sunniland Formation of Florida brines to the seafloor lows 2b. Platform edge low with 1b: Phosphoria Fm, USA None Greenhouse eustacy creates epeiric mesohaline continuous shelf- or hinterland ramp-edge rim Setting 3. Mesohaline- Underfilled stages Permian Jingjingzigou Formation in East African Rift Enhoheic basins in rift or upper column in alternating with balanced the Junggar Basin, China: Eocene Valley lakes; continent-continent perennial saline fill stages in response to Green River Formation, USA; Lake Van, collision settings lacustrine basins. tectonic/climatic changes Cretaceous Lagoa Feia Formation, Turkey; Lake Campos Basin in Brazil; Tertiary Urmia, Iran saline lacustrine basins, China Setting 4. Closed Brine seeps that create the Possible explanation for the Poorly documented Halokinetic provinces in the mesohaline-bottomed stratified brine lakes are enhanced source potential of stratified brine deep waters of the passive deep seafloor tied to ongoing salt marine deep-water shales in lakes in suprasalt margin slope and rise of depressions in dissolution and shallow various circum-Atlantic allochthon the Gulf of Mexico and halokinetic belts subseafloor salt flows halokinetic basins provinces the Mediterranean Ridge 381 collision belt

See Fig. 20. 382 J. K. Warren

Viscount of Blackburn, who once said: “The great Cellulolytic bacteria decompose cellulose; proteo- business of life is to be, to do, to do without, and lytic bacteria breakdown proteins into simpler, to depart.” soluble substances such as peptides and amino acids; saccharolytic bacteria breakdown sugars, while homoacetogens are obligately anaerobic bac- GLOSSARY teria that make acetate from either (H2 þ CO2)or from the fermentation of sugars. Aerobes are organisms that can survive and grow in Chemoautotrophs use endogenous light-indepen- an oxygenated environment. dent reactions to obtain energy, these reactions Aliphatic hydrocarbons are any chemical com- involve inorganic molecules and an electron donor pound belonging to the organic class in which the other than water and do not release oxygen. atoms are not linked together to form a ring. They Cyanobacterial toxins. Intoxication of lesser fla- are divided into three main groups according to mingo flocks by cyanobacterial toxins, and some- the types of bonds they contain: alkanes, alkenes, times even mass fatalities have occurred in nearby and alkynes. Alkanes (n-alkanes) have only single Lake Bogoria when the birds ingest detached bonds and a continuous chain structure, alkenes cyanobacterial cells from cyanobacterial mats contain a carbon-carbon double bond, and alkynes flourishing in the vicinity of hot springs (Krienitz contain a carbon-carbon triple bond. Aromatic et al., 2003). This is because the flamingos feeding hydrocarbons are classified as either arenes, which at night on plankton blooms in a saline lakes need contain a benzene ring as a structural unit, or non- to drink fresh or brackish water after feeding, and to benzenoid aromatic hydrocarbons, which are char- wash their feathers daily. They tend to do this in acterized by stability in burial but lack a benzene waters in the vicinity of the hot springs, where ring as a structural unit. salinities are lower than in the main waterbody of Anaerobes are organisms that do not require oxy- the lake where they have been feeding. Mycosystin gen for growth and may even die in its presence. heptatoxins can characterize the benthic microbial Obligate (or strict) anaerobes are unable to live in community in those hot spring mats and waters even low oxygen concentrations. Facultative anae- can be dominated by the potentially toxic cyano- robes are able to live in low or even normal oxygen bacterial association of Phormidium terebriformis, concentration as well. All anaerobes are simple Oscillatoria willei, Spirulina subsalsa and Syne- microorganisms such as bacteria, archaea and chococcus bigranulatus. some fungi. Archaea are usually strict anaerobes. Denitrification is the microbial process by which Autotrophs (literally “self-feeders”) are organisms nitrates are removed from an aqueous liquid. capable of producing organic compounds from Dissimilatory metabolic processes drive the con- simple inorganic compounds. version of food or other nutrients into products Basinwide evaporites are one of the two major plus energy-containing compounds. styles of ancient marine-fed salt accumulations Dissimilatory sulphate reduction. Sulphate-redu- known as: (1) marine-fed basinwides and (2) mar- cing bacteria gain energy for cell synthesis and ine-fed platform evaporites. Neither setting is growth by coupling the oxidation of organic com- active anywhere on the world’s current landsur- pounds or molecular hydrogen to the reduction of face. Basinwide salt fills tend be thick (>100 m) sulphate to sulphide (H S, HS ). This process is and relatively pure with deposits accumulating 2 called “dissimilatory sulphate reduction”, to allow rapidly across time frames of less than one million clear differentiation from assimilatory sulphate years. Basinwide evaporites are most likely to reduction. Assimilatory sulphate reduction gener- accumulate on the floors of isolated sub-sea-level ates reduced sulphur for biosynthesis (e.g. of depressions at times of close proximity of drifting cysteine). It is a widespread biochemical capacity landmasses (Warren 2006, 2008, 2010). in prokaryotes and plants and does not lead to the Catabolism is the breakdown in living organisms of excretion of sulphide. Only upon decay (putrefac- more complex substances into simpler ones tion) of the biomass is the assimilated reduced together with a release of energy. sulphur released as sulphide. Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 383

Endosymbionts are organisms that live within the Hopanoids are group of compounds (triterpenoids) body or cells of another organism without deleter- produced by prokaryotic organisms, and the diage- ious effects. netic alteration products of these compounds (found in oils, rock extracts and sediment extracts). Just as Extremophiles are organisms that thrive in extreme steroids (steranes) are a useful group of biomarkers conditions including: extremely saline (halo- for identifying input from various eukaryotic organ- phile), extremely hot (thermophile), extremely dry isms (e.g. plants and animals), an analogous group of (xerophile), extremely acid (acidophile), extre- compounds, hopanoids, are a useful group of bio- mely alkaline (alkaliphile), and extremely cold markers for identifying input from various bacteria. (psychrophile) environments. Hopanoids serve the same function in bacteria as Fermentation is of a series of anaerobic transforma- sterols do in eukaryotes: they act as cell wall rigidi- tion processes whereby organic matter is broken fiers. In petroleum and their source rocks, hopanoid down into compounds of smaller size, which are biomarkers exist as a subset of a group of compounds more reduced or more oxidized and eventually called triterpanes (isoprenoids). more assimilatable by living matter. When fermen- Hypersaline encompasses all waters more saline tation leads to organic acids and a lowering of pH, it is called acidogenesis. The microorganisms than seawater (mesohaline, penesaline and supersaline). responsible for this are called acidogens. Gram-negative and Gram-positive are responses to Hypertrophication describes the presence of exces- the Gram staining technique whereby micro-organ- sive nutrients in a water body. isms are first stained with crystal violet, Isoprenoids are a major class of nonsaponifiable then treated with an iodine solution, decolourized lipids that occur in plants, animals, and bacteria with alcohol, and counterstained with safranine. and are characterized by chains of modular groups Gram-positive bacteria retain the violet stain; of five carbon atoms in which the typical pattern Gram-negative bacteria do not. has four of the carbon atoms in a linear chain and a “Halobacteria”. Prior to hybridization studies and single carbon attached at the carbon one position genome mapping, classification was based on mor- removed from the end of the chain. The term phology and staining, the evolutionary relation- isoprenoid is derived from the name of the five- ships among various members of the bacterial and carbon, doubly unsaturated branched hydrocar- archaeal domains were contradictory and poorly bon isoprene, which could in principle be the defined. Today some of these contradictions and simplest monomeric chemical precursor for this confusions remain in microbial taxonomy of the class of compounds. Isoprenoids are also known as group of microbial organisms broadly known as terpenes. Terpenes are usually grouped according halobacteria, as distinct from the archaeal group to the number of isoprene (C5H8) units in the Halobacteriales. molecule: monoterpenes (C10H16) contain two such units; sesquiterpenes (C15H24), three; diter- Halophilic organisms thrive at very high salt penes (C20H32), four; triterpenes (C30H48), six; and concentrationsandcanbe killedby lowersalinities. tetraterpenes (C40H64), eight. The carotenoid pig- Halotolerant (aka halovariant) organisms can tol- ments are the best known tetraterpenes. erate high salt concentrations but grow better at Lithotrophs are organisms that use an inorganic somewhat lower salinities. substrate (usually of mineral origin) to obtain Haloxene organisms cannot tolerate high concen- reducing equivalents for use in biosynthesis (e.g. trations of salts. carbon dioxide fixation) or energy conservation via aerobic or anaerobic respiration. Heterotrophs (literally “feeders on others”) use organic molecules synthesized outside their body Meromixis indicates partial or incomplete mixing. as a source of energy and carbon. The term meromictic is used to describe a perma- nently stratified water mass where surface layers Holomixis indicates the entire mixing of the water may mix, but the bottom layer does not. Many column. Meromixis indicates partial or incomplete modern brine lakes are meromictic, the upper mixing. water mass comes and goes. 384 J. K. Warren

Mesophiles are organisms that grow best in mod- green wavelengths, which is why chlorophyll- erate temperatures, neither too hot nor too cold, bearing cyanobacteria appear green (Fig. 2B). The typically between 15 and 40 C. carotenoids and phycobiliproteins, on the other hand, strongly absorb green wavelengths. Algae Mixolimnion. An upper water mass that periodi- and microbes with large amounts of carotenoid cally mixes is the mixolimnion, it sits atop the appear yellow to brown (such as carotene-rich monolimnion. forms of Dunaliella sp.), those microbes with large Monolimnion. A lower, permanent unmixed water amounts of phycocyanin appear blue, and those mass. with large amounts of phycoerythrin appear red. Pigment levels can indicate the stratification of Neutrophilic organisms are not stained strongly or the microbial community in any photoresponsive definitely by either acid or basic dyes, but are biomass in a brine column. Red wavelengths (long stained readily by neutral dyes. wavelengths) are absorbed in the first few metres of a brine column or the uppermost millimetre or Oligomictic or oligotrophic is used to describe two of a microbial mat (where chlorophyll utilizers stratified water masses that mix or homogenize for flourish). Blue and green wavelengths (shorter) short irregular periods every few years. reach deeper into the brine column or into the Photoautotrophs use light as a source of energy and sediment. CO as a source of carbon. Term comes from auto- 2 Saprophytes obtain nourishment by absorbing dis- trophs (literally “self-feeders”), which describes solved organic material; especially from the pro- organisms capable of producing organic com- ducts of organic breakdown and decay. pounds from simple inorganic compounds. Schizohaline describes waters subject to substan- Photophosphorylation is the production of ATP tial ongoing salinity changes and periodically pass using the energy of sunlight. from brackish to hypersaline. Platform evaporites are the other major type of Third domain of life. In the late 1970s, Professor ancient marine-fed evaporite. They formed on con- tinental margins throughout much more of Phaner- Carl Woese proposed, on the basis of ribosomal RNA affiliations (gene mapping), that life be ozoic time than basinwides. Salt fills are 10–50 m divided into three domains instead of two, thick, mostly CaSO and typically interbedded 4 namely; Eukaryota, Eubacteria, and Archaebac- with normal-restricted marine carbonates. Stacked teria (Woese, 1993). He later decided that the term platform sections characterised by this style of Archaebacteria was a misnomer, and shortened it accumulation encompass time frames of 1–10 to Archaea and Eubacteria to Bacteria. Since the Myr and are largely tied to times in earth history 1970s, DNA base-pair studies (aka genomic stu- when climate was in greenhouse mode and the associated eustacy favoured widespread epiconti- dies or gene sequencing) have shown that Archaea are as different from Bacteria as from Homo nental seaways subject to periodic restriction sapiens. This new approach to taxonomy is still (Warren, 2006, 2010). working its way through the scientific community Red waters and brines. The pink to purple colours and some books and articles still ocassionally that typify many hypersaline water bodies come refer to archaea as types of bacteria. Prior to geno- mostly from concentrations of carotenoid pig- mic studies, and based on their morphology and ments present in the cytoplasm of various haloto- staining response, the archaeal Halobacteriaceae lerant and halophilic microorganisms. Most were grouped with the bacterial Gram-negative haloarchaea are red due to a high content of C-50 rods (a gram positive or gram negative description carotenoids of the bacterioruberin series. Photo- indicates whether or not the bacterial cell wall synthetic cyanobacteria and eukaryotes (e.g. reacts with Gram’s stain). unicellular green algae of the genus Dunaliella) contribute to the pigmentation of the hypersaline REFERENCES waters thanks to the presence of chlorophylls and C-40 carotenoids (mostly all-trans- and 9-cis- Aharon, P., Kolodny, Y. and Sass, E. (1977) Recent hot brine b-carotene). Chlorophylls absorb red and blue dolomitization in the “Solar Lake”, Gulf of Elat; isotopic, wavelengths much more strongly than they absorb chemical, and mineralogical study. J. Geol., 85, 27–48. Evaporitic source rocks: mesohaline responses to cycles of “famine or feast” in layered brines 385

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